The Ecology of Marine Fishes: California and Adjacent Waters 9780520932470

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TH E E C O LO GY O F MAR I N E F I S H E S

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THE ECOLOGY OF MARINE FISHES CALI FO R N IA AN D ADJAC E NT WATE R S

Edited by

LAR RY G. ALLE N DAN I E L J. P O N D E LLA I I M I C HAE L H. H O R N

UNIVERSITY OF CALIFORNIA PRESS Berkeley

Los Angeles

London

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The editors and publisher gratefully acknowledge the generous contributions to this book provided by The David and Lucile Packard Foundation and the California–Nevada Chapter of the American Fisheries Society

University of California Press Berkeley and Los Angeles, California University of California Press, Ltd. London, England © 2006 by the Regents of the University of California Library of Congress Cataloging-in-Publication Data Ecology of marine fishes : California and adjacent waters / edited by Larry G. Allen, Daniel J. Pondella II, Michael H. Horn. p. cm. Includes bibliographical references. ISBN 0-520-24653-5 (cloth : alk. paper) 1. Marine fishes—Ecology—California. I. Allen, Larry Glenn. II. Pondella, Daniel J. III. Horn, Michael H. QL628.C2E33 2006 597.177'09794—dc22 2005010629 Manufactured in Colombia 10 09 08 07 06 05 10 9 8 7 6 5 4 3 2 1 The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-1992 (R 1997) (Permanence of Paper) ∞

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TO OUR TEACHERS

JULES M . CRANE , JR .

(1928–1995), naturalist, mentor, and friend

who published broadly on snails, amphipods, clams, fossil fishes, grunion and wiggling sticks, midshipman courtship, and truly loved all things bioluminescent. —LGA

JOHN S . STEPHENS , JR .

(1932), naturalist, systematist, ecologist,

scholar, teacher, friend—a true ichthyologist. Doc may know more about fish than all of the rest of us. This book would be much shorter if it were not for John. —DJP

CARL D . RIGGS

(1920–2002), fish biologist, station director, able

administrator, dry wit, steady mentor, and warm friend, who studied white bass, gars, and bowfin and offered his support at the right moment to help launch an ichthyological career. —MHH

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C O NTE NTS

PART I

9

Introduction 10 1

Biogeography 3 Horn, L. Allen, and Lea

2

Phylogeography 26 Dawson, Waples and Bernardi

3

Evolution 55 Hobson

4

Ecological Classification 81 L. Allen and Pondella

Rocky Reefs and Kelp Beds 227 Stephens, Larson and Pondella Deep Rock Habitats 253 Love and Yoklavich

P E L A G I C H A B I TAT S

11

Ichthyoplankton 269 Moser and Watson

12

Surface Waters 320 L. Allen and Cross

13

Deep Sea 342 Neighbors and Wilson

PART I I

PART IV

Behavioral Ecology 19

Reproduction 483 DeMartini and Sikkel

20

Movement and Activity Patterns 524 Lowe and Bray

21

Symbiotic Relationships 554 McCosker

PART V

Spatial and Temporal Change

Habitats and Associated Fishes PART I I I

S O F T S U B S T R ATA

5

Bays and Estuaries 119 L. Allen, Yoklavich, Cailliet and Horn

14

6

Surf Zone, Coastal Pelagic Zone, and Harbors 149 L. Allen and Pondella

15

Recruitment 411 Carr and Syms

16

7

Continental Shelf and Upper Slope 167 M. J. Allen

Predation 428 Steele and Anderson

17

Competition 449 Hixon

18

Disturbance 466 Stouder and McMullin

H A R D S U B S T R ATA

8

Rocky Intertidal Zone 205 Horn and Martin

22

Subsistence, Commercial, and Recreational Fisheries 567 Love

23

Pollution 595 M.J. Allen

24

Alien Fishes 611 Schroeter and Moyle

25

Climate Change and Overexploitation 621 Horn and Stephens

Population and Community Ecology Feeding Mechanisms and Trophic Interactions 387 Horn and Ferry-Graham

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LI ST O F AUTH O R S

DR . LARRY G . ALLEN Department of Biology, California State University, Northridge, Northridge, CA 91330-8303

DR . ROBERT N . LEA Department of Fish and Game, Marine

DR . M . JAMES ALLEN Southern California Coastal Water,

DR . MILTON S . LOVE , Marine Science Institute, University of

Research Project, 7171 Fenwick Lane, Westminster, CA 92683

California, Santa Barbara, CA 93106

DR . TODD W. ANDERSON Department of Biology, San Diego State University, San Diego, CA 92182-4614

DR . CHRISTOPHER G . LOWE Department of Biological Sciences, California State University Long Beach, 1250 Bellflower Blvd., Long Beach, CA 90840

DR . GIACOMO BERNARDI Department of Ecology and

Region, Monterey, CA 93940

Evolutionary Biology, University of California Santa Cruz, Santa Cruz, California 95060

DR . KAREN L . M . MARTIN Department of Biology, Pepperdine University, Malibu, CA 90263-4321

DR . RICHARD N . BRAY Department of Biological Sciences, California State University, San Marcos, CA 92096-0001

DR . JOHN E . M C COSKER , California Academy of Sciences,

DR . GREGOR M . CAILLIET, Moss Landing Marine

Laboratories, P.O. Box 450, Moss Landing, CA 95039

MICHELLE L . M C MULLIN Pacific Northwest Research Station, 3625 93rd Avenue SW, Olympia, WA 98512-9193

DR . MARK H . CARR Department of Ecology and

DR . H . GEOFFREY MOSER , National Marine Fisheries Service

Evolutionary Biology, University of California, Santa Cruz, CA 95064

(NOAA), Southwest Fisheries Science Center, La Jolla, CA 92038-0271

DR . JEFFREY N . CROSS Grand Canyon National Park,

DR . PETER B . MOYLE , Department of Wildlife, Fish, and Conservation Biology, University of California, One Shields Ave., Davis, CA 95616

P.O. Box 129, Grand Canyon, AZ 86023 DR . MICHAEL N DAWSON School of Biological, Earth, and

Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia DR . EDWARD E . DEMARTINI NOAA Fisheries Service, Pacific

San Francisco, CA 94103-3098

DR . MARGARET A . NEIGHBORS , Section of

Vertebrates/Fishes, Natural History Museum of Los Angeles County, Los Angeles, CA 90007-4000

Islands Fisheries Science Center, Honolulu, HI 96822-2396

DR . DANIEL J . PONDELLA II , Vantuna Research Group,

DR . LARA A . FERRY- GRAHAM Moss Landing Marine Labs,

8272 Moss Landing Rd., Moss Landing, CA 95039

Occidental College, 1600 Campus Road, Los Angeles, CA 90041-3314

DR . MARK A . HIXON Department of Zoology, Oregon State

DR . ROBERT E . SCHROETER Department of Wildlife, Fish,

University, Corvallis, OR 97331-2914

and Conservation Biology, University of California, One Shields Ave., Davis, CA 95616

DR . EDMUND S . HOBSON Southwest Fisheries Science

Center, Santa Cruz Laboratory, National Marine Fisheries Service, NOAA Santa Cruz, CA 95060

DR . PAUL SIKKEL Department of Biology, Murray State

DR . MICHAEL H . HORN Department of Biological Sciences,

DR . MARK A . STEELE , Marine Science Institute, University of California, Santa Barbara, CA 93106

California State University, Fullerton, Fullerton, CA 92834-6850 DR . RALPH J . LARSON Department of Biology, San Francisco

State University, San Francisco, CA 94132

University, Murray, KY 42071-0009

DR . JOHN S . STEPHENS , JR . Vantuna Research Group, Occidental College, 1600 Campus Road, Los Angeles, CA 90041-3314

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DR . DEANNA J . STOUDER American Rivers, 1025 Vermont

WILLIAM WATSON National Marine Fisheries Service

Ave. NW, Suite 720, Washington, DC 20005

(NOAA), Southwest Fisheries Science Center, La Jolla, CA 92038-0271

DR . CRAIG SYMS , Department of Ecology and Evolutionary

Biology, University of California, Santa Cruz, CA 95064

DR . RAY R . WILSON , JR ., Department of Biological Sciences,

DR . ROBIN WAPLES , Conservation Biology Division,

California State University Long Beach, 1250 Bellflower Blvd., Long Beach, CA 90840

Northwest Fisheries Science Center, 2725 Montlake Blvd. East, Seattle, WA 98112

MARY YOKLAVICH Pacific Fisheries Environmental Laboratory, National Marine Fisheries Service, Pacific Grove, CA 93950

X

LIST OF AUTHORS

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P R E FAC E

Starting with David Starr Jordan in the late 1800s, California marine fishes have been one of the most intensively studied groups of fishes in the world. Known for its sandy beaches, kelp beds and palisades, the California coastline is a mere glimpse of the beauty that lies beneath its waves. Some of the most prestigious universities and institutions of higher learning gaze down upon these shores. Thus, it is not surprising that in such an ideal setting some of the fundamental ideas in the science of marine ecology have been formulated. The volume of literature published on California marine fishes is stunning and truly daunting for someone new to this field. With, this in mind, we asked 35 experts in science, policy, and conservation to assemble this unique text. This book was designed to provide the first-ever compilation and interpretation of the large body of information on the ecology of California’s marine fishes. Each chapter brings together color illustrations to greatly enhance its accessibility to the reader. Our goal was to make this volume a valuable source of information for students and professionals, as well as the general public. This book should also be an important contribution to the study of marine fish ecology worldwide, but particularly for California’s marine fish populations. The fish populations in California are greatly impacted by coastal shelf development, commercial and recreational fishing, discharge of pollutants, and other human activities. The decline of many fisheries species has led to rather drastic management measures, the development of

the Nearshore Fishery Management Plan, the the Marine Life Management Act and the Marine Life Protection Act, which is being used to establish marine reserves. The information in this book should prove useful in these processes. In general, each chapter begins with an overview of the subject matter providing a synthesis of existing information including theory, models, and classifications where appropriate. Most examples focus upon California representatives placed in the context of information known from other temperate habitats worldwide. Finally, many chapters end with a prospectus for future research. The authors and editors of this work are greatly indebted to a large number of professionals who have contributed their knowledge and talents to the review process for each chapter. They include Jonathan Baskin, Denise Breitburg, Jennifer Caselle, Robert Cowen, Edward DeMartini, Christopher Dewees, Michael Fahay, David Greenfield, Richard Haedrich, Mark Hixon, Edmund Hobson, Sally Holbrooke, Timothy Hovey, G. David Johnson, Geoff Jones, Phillip Lobel, George Losey, William MacFarland, Alan Mearns, H. Geoffrey Moser, Tim Mulligan, Hiroyuki Munehara, John Musick, John Paxton, Theodore Pietsch, Chet Rakocinski, John E. Randall, Bruce Robison, Richard Rosenblatt, Stephen Ross, Russell Schmitt, Eric Schultz, John S. Stephens, Jr., Camm C. Swift, Russell Vetter, and Robert Warner. Illustrations by Larry G. Allen unless otherwise indicated.

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PART I

I NTR O D U CTI O N

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CHAPTER 1

Biogeography M I C HAE L H. H O R N, LAR RY G. ALLE N, AN D R O B E RT N. LEA

Introduction Environment of the Northeastern Pacific Ocean The marine environment of the northeastern Pacific is a complex and dynamic system that offers a daunting challenge for any distributional analysis of its fish fauna, either of the entire region or a portion, such as the waters along the approximately 10° of latitude (32°–42°N) that border the state of California and that form the focus of this chapter. The narrow continental shelf of northern and central California gives way to a broader continental borderland off southern California that is etched with several deep-sea basins and marked with a series of islands of varying size and distance from the mainland and each other. These borderland features add to the complexity and sheer size of the California marine environment. The region provides a wide variety of habitats for fishes and undergoes changes that lead to shifts in distribution and abundance of the coastal fish fauna. The southward-flowing California Current and inshore countercurrents transport young stages of fishes and influence the movements of larger individuals. Water masses of northern, western, and southern origin impart their own character to the offshore fish fauna and converge to create a large transition zone in waters bordering the southern half of California (fig. 1-1). Upwelling events proceed seasonally from south to north along the coast resulting in sections of nearshore waters that are periodically cooler and more productive and, thus, contain more concentrated food resources.

Biogeographic Regions and Provinces On a continental scale, two distinctive fish faunas meet and intermingle in California, a warm-temperate, southern element and a cool-temperate, northern component (Briggs, 1974; Horn and Allen, 1978). The well-known biogeographic boundary largely separating these two faunas has long been recognized to occur in the vicinity of Point Conception at about 34.5°N on the south central California coast. This boundary is perceived mainly as a temperature discontinuity, and studies of distributional patterns of fishes (Horn and

Allen, 1978), molluscs (Valentine, 1966) and macrophytes (Murray and Littler, 1981) show that these patterns are strongly related to temperature regimes governed by oceanographic processes. Hayden and Dolan (1976) recognized the value of faunal distributions and range end points as indicators of abiotic zones and discontinuities. The traditional biogeographic regions and provinces of the eastern North Pacific have been described with some minor variations in a number of publications (McGowan, 1971; SCCWRP, 1973; Briggs, 1974; Horn and Allen, 1978; Brusca and Wallerstein, 1979; Allen and Smith, 1988; Hastings 2000; fig. 1-1). The politically demarcated latitudinal expanse of California contains parts of two biogeographic regions and subordinate provinces. To the north of Point Conception, the Oregonian Province extends to the Washington–British Columbia or British Columbia–Alaska border before giving way to the Aleutian Province; both provinces are contained within the Boreal Eastern Pacific Region. To the south of Point Conception, the San Diegan Province extends to the temperate-tropical boundary at Bahia Magdalena, Baja California Sur, Mexico. This province coupled with the Cortez Province, which extends from Bahia Magdalena and includes the entire Gulf of California upper Gulf, completes the Warm-Temperate California Region. To the south, the subtropical/tropical Mexican Province extends through Central America and is replaced to the south by the Panamic Province. The Panamic Province extends to northern Peru as part of the Tropical Eastern Pacific Region. This region also includes the Galapagos Province, which is described as all of the oceanic islands from the Galapagos in the south to Islas Revillagigedo off the tip of Baja California Sur to the north. For rocky shore fishes, Hastings (2000) has described the significance of stretches of soft bottom habitat that form gaps in the rocky coastline between the Cortez and Mexican provinces and between the Mexican and Panamic provinces. These subtropical/tropical faunas are bounded to the north and south by thermal transitions. Taken together, these regions and provinces and their boundaries provide useful structure and organization for studying faunal associations and distributional changes in the northeastern Pacific. They convey, however, a certain static picture that belies the complex and shifting interrelationships of the California fish fauna (Hubbs, 1974), which are driven in large part by

3

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F I G U R E 1-1 Zoogeographical provinces of the Pacific coast of North America (after Briggs, 1974).

short- and long-term variability in climate. Consistent with this dynamic picture and with our increasingly detailed knowledge of fish distributions, the generality and validity of Point Conception as a biogeographic boundary for fishes and marine invertebrates has been challenged recently based on phylogeographic analyses (see below).

Climatic Variability The dynamic nature of the climate in the northeastern Pacific overlays an already complex marine environment in California coastal waters and strains the reliance on fixed boundaries and provinces for understanding the distributional patterns of the fish fauna. Both short- and long-term fluctuations in atmospheric and oceanographic conditions characterize the climate of the region. El Niño–Southern Oscillation (ENSO) events occur naturally as intervals of alternating warm

4

INTRODUCTION

and cool oceanographic conditions in the eastern tropical Pacific but affect regions far beyond, including the California marine environment (Kousky and Bell, 2000). El Niño events represent the warm extremes of the cycle and result in higher sea surface temperatures, weaker upwelling, and reduced nutrient levels in the water column. These events tend to occur every 4 to 5 years, last 12–15 months, and emerge strongest every 10–15 years (e.g., the powerful El Niño conditions of 1982–1983 and 1997–1998). El Niño events, detectable back to the 1700s in climate records and as a long ago as 5000 years in paleoclimatic signals, can now be predicted 9 to 12 months in advance. La Niña and more neutral conditions alternate in an irregular pattern with El Niño events in the ENSO cycle. La Niña conditions represent the cool extremes of the cycle and result in lower sea surface temperatures, stronger, deeper upwelling, increased nutrient levels, and heightened productivity in coastal waters. These events may last 1 to 3 years; for example, the recent La Niña

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event characterized by rapid onset in 1998 and persistence at least into early 2001 (Durazo et al., 2001). Although a shift to a cold-water regime has been suggested (Bograd et al., 2000) for the California Current system that may be associated with a Pacific Decadal Oscillation (Mantua et al., 1997), monitored features of the system do not yet indicate a climate regime shift (Durazo et al., 2001), although Chavez et al. (2003) present evidence that the shift has indeed occurred. Thus, the dynamics of the California marine environment create regional complexities beneath, so to speak, the recognized (e.g., Houghton, 2002) overall trend of global warming. The California Transition Zone provides an excellent ‘natural’ experiment for studying this process.

Continued Interest in Fish Distribution Patterns Since the last distributional analysis of California coastal fishes was published more than 25 years ago (Horn and Allen, 1978), several events and developments have occurred in the intervening years to sustain and increase the scientific interest in the biogeography of California marine organisms including fishes. As alluded to above, most prominent among these occurrences has been climate change, particularly the warming of ocean surface waters, especially in the Southern California Bight, from the mid-1970s up through the strong El Niño conditions of 1997–1998, followed then by a rapid change to cooler temperatures and La Niña conditions from late 1998 to early 2001 (Smith, 1995; Bograd et al., 2000; Durazo et al., 2001). The intensified focus on this warming phenomenon has revealed that the ecosystem changes can be relatively slow and pervasive as in zooplankton declines occurring over two decades of warming (Roemmich and McGowan, 1995), or rapid and dramatic as in the 1997–1999 El Niño–La Niña cycle (Lynn and Bograd, 2002), with remarkable additions of Panamic fishes to the California fish fauna occurring during this brief period (Lea and Rosenblatt, 2000; Pondella and Allen, 2001). The increased attention to climate change and its effects on biotic distributions has helped provide the impetus for long-term monitoring studies of fish abundances and distributions, which, in turn, has yielded biogeographic information on fishes at local and regional scales (e.g., see Chapter 8, Rocky Reefs and Kelp Beds; Chapter 9, Near Shore Soft Bottoms). Also important for California fish biogeography during the last quarter century has been the development of two new disciplines in biology—phylogeography and macroecology. Each of these nascent fields has had its champion, who has described the field in detail in book-length treatments. John Avise has led the emergence of phylogeography and recently synthesized the discipline (Avise, 2000). Phylogeography is about the geographic distributions of genealogical lineages particularly within and among closely related species. The discipline has grown out of the burgeoning mitochondrial DNA analyses of lineages and forms a link between microevolution, especially involving population genetics, and macroevolution, in particular the subdisciplines of historical geography and phylogenetics. This rapidly expanding field has infused new life into the analysis of traditional biogeographic boundaries because lineages of natural populations frequently show distinct geographic patterns. As a subdiscipline of biogeography, phylogeography prompts the question whether the geographic orientation of genetically structured populations matches that of well-

known biogeographic boundaries. For example, studies of two California fish species, black perch (Embiotoca jacksoni) by Bernardi (2000) and tidewater goby (Eucyclogobius newberryi) by Dawson et al. (2001), showed that, for these taxa, phylogeographic structure is not concordant with the biogeographic break at Point Conception. This unexpected finding has given rise to alternative hypotheses about the possibility of biogeographic boundaries at other locations. In a review of the literature describing the distributional patterns of coastal marine taxa in California, Dawson (2001) provided evidence that phylogeographic breaks are concordant with biogeographic patterns but that the boundaries match environmental discontinuities in the vicinity of Los Angeles (33°–34°N) and Monterey Bay (36°–37°N), not Point Conception. He points out that the range termini of fishes actually peak at 33°N in the Horn and Allen (1978) study, which was completed before phylogeographic analyses had begun. Even though Dawson (2001) acknowledges that Point Conception marks the northern limit of some San Diegan species and the southern limit of some Oregonian fishes, he asserts that Point Conception is more appropriately recognized as the center of a California Transition Zone (fig. 1-1). This zone is interpreted by Dawson as a heterogeneous region in which Oregonian and San Diegan faunas are replaced incrementally over several degrees of latitude and in which most species cross Point Conception and end their ranges elsewhere. In light of the Dawson work, we interpret our distributional analyses in this chapter with respect to the California Transition Zone concept as well as to Point Conception as the traditional biogeographic boundary. Phylogeography and the associated topics of genetic variation, population dispersal, and gene flow are discussed in detail in Chapter 2. The second relevant discipline to emerge in the last two decades is macroecology, a field devoted to identifying and understanding ecological patterns on large spatial scales although the focus is not necessarily restricted to any particular spatial scale (Blackburn and Gaston, 2002). James Brown is the co-founder of macroecology and described the discipline in a book by the same name (Brown, 1995). Macroecology involves interpreting the statistical patterns of abundance, distribution, and diversity and examining the domain where the discipline intersects with ecology, biogeography, and paleontology. The premise of the field is that finding repeated statistical patterns of ecological variables leads to testable hypotheses of underlying mechanistic processes (Brown and Lomolino, 1998). Topics of macroecological interest include the distribution of geographic range sizes and the relationship between body size and species diversity. A recent application of macroecology involved analysis of body size and depth of occurrence of 409 species of eastern North Pacific pelagic fishes occurring at 40° to 50°N latitude and within a depth gradient of 0 to 8000 m (Smith and Brown, 2002). Their analysis did not include the latitudinal ranges of species, but they argue that species richness ought to be driven more by depth than latitude because the vertical temperature gradient in the ocean is so much greater than the horizontal (latitudinal) gradient. A third recent approach to biogeographic analysis has been termed thermogeography by its proponents, Adey and Steneck (2001). This temperature/time/space model was developed by Adey and Steneck to show conditions under which assemblages of marine benthic algae evolve regional biogeographic patterns in their distribution and abundance. The model generates distribution patterns based on the part of geographic ranges where the taxa studied are most abundant rather than

BIOGEOGRAPHY

5

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on total ranges that emphasize range end points. According to Steneck and Adey, the core of most of the classic coastal biogeographic regions, including those of the northeastern Pacific, correspond to those derived by the thermogeographic model. Whether the model can be applied successfully to more mobile taxa, such as fishes, remains to be determined, but it is worthy of consideration in the future.

Purposes and Expectations of the Chapter Our analytical contribution to this chapter consists mainly of an update of the distributional analysis of California coastal fishes completed more than 25 years ago (Horn and Allen 1978). The current analysis incorporates range extensions and recent additions of species to the fauna. Given that surface water temperatures generally have warmed in the northeastern Pacific over the last 25 years, that most of the period (1976–1998) lay within a warm regime cycle, and that three strong El Niño events occurred during the interval, we expected our new analysis to reflect the known additions to the fauna and perhaps to detect some northward range shifts in the fauna as a whole. The updated analysis largely paralleled that of the earlier work in that we (1) displayed the species richness gradient for California coastal fish species over their geographic ranges as far north as 60°N and to the equator and beyond southward; (2) portrayed richness patterns of principal taxa (family or genus) across California latitudes to emphasize the northern or southern affinities of these faunal elements; (3) examined the relationship of fish distributions, sea surface temperatures, and degrees of latitude; (4) determined the effectiveness of established faunal boundaries, especially Point Conception and more recently identified breaks in part derived from phylogeographic analyses (see Dawson, 2001, and Chapter 2), for bay-occurring and non-bay occurring fish species using cluster analysis; and (5) compared the effectiveness of these same boundaries for coastal species of northern and southern affinities based on principal coordinates analysis and range end-point analysis. Given that our analysis included only the juvenile and adult stages of coastal (primarily continental shelf) fish species, the contributions on ichthyoplankton by Moser and Watson (Chapter 11) and deep-sea fishes by Neighbors and Wilson (Chapter 13) help to provide a relatively complete picture of the distributional patterns of fishes in California waters.

Methods The basic data for the analysis were derived from a list of 519 fish species known to occur in the coastal waters of California (Appendix 1). The list, with geographic ranges, was obtained from Miller and Lea (1972), with distributional information on certain species also acquired from Hart (1973). Additions to the California fauna since the Horn and Allen (1978) analysis were obtained from several published sources including Lea and Rosenblatt (2001) and are given in table 1-1. Most of the deep midwater and benthic species in the list of Miller and Lea (1972) were not used in the analysis although the distribution patterns of deepwater assemblages are examined, as mentioned, in Chapters 11 and 13 of this volume. Three sets of species and their geographic ranges were used: (1) a set of 519 species referred to as “all coastal species”; (2) a set of 225 species that occur in bays and estuaries (hereafter,

6

INTRODUCTION

“bay” used for “bay and estuary”) and correspond to the species in 13 bays used in Horn and Allen (1976) plus two additional sites, Carpinteria Marsh and Mugu Lagoon; and (3) a set of 289 species that do not occur in bays. Species distributions at 1° or 2° intervals of latitude were plotted depending upon the type of analysis performed. A species was considered to occur or end its range at a particular latitude if it had been recorded at any geographic location within that latitudinal interval (e.g., any location from 32.0° to 32.9°N was considered 32°N). A few species now recorded as occurring in California were not included in the analyses because they were added too recently or because of lack of other information. These species include white mullet (Mugil curema), Pacific golden-eyed tilefish (Caulolatilus affinis), Pacific dog snapper (Lutjanus novemfasciatus), armed grunt (Conodon serrifer), Cortez grunt (Haemulon flaviguttatum), bluestriped chub (Sectator ocyurus), Panamic sergeant major (Abudefduf troschellii), swallow damselfish (Azurina hirundo), silverstripe chromis (Chromis alta), threeline prickleback (Esselenichthys carli), twoline prickleback (Esselenichthys laurae), saddled prickleback (Lumpenopsis clitella), deepwater bass (Serranus aequidens), and Pacific stargazer (Astroscopus zephyreus). References on the distributional information for these species can be obtained from any of the authors of this chapter. To show the degree of resemblance among bays and degrees of latitude in terms of their fish faunas, cluster analysis was performed. A Pearson product-moment correlation matrix was used to produce linkage distances among the bays or latitudes scaled to a maximum linkage distance of 100%. The principal coordinates analysis used to generate the ordination two-way table of 289 non-bay species by latitude (Appendix 2) was performed according to a procedure described in Smith (1976) and used by Horn and Allen (1978). Ordination in the present study means that the species were ranked on a north-to-south latitudinal axis according to the average axis score of the species at each degree of latitude. For example, the first species in the ranking occurred only at 41° and 42°, the last species at 32°, and the intermediate species at latitudinal intervals that were progressively more southerly in character. Sea surface temperatures at 2° intervals of latitude were obtained from charts prepared by Eber et al. (1968). Minimum temperatures were derived from monthly means for the 14-year period 1949–1962. Although ocean temperatures increased slightly in the latter half of the century, our fundamental distributional information largely reflects the longterm temperature profile of the warm- to cool-temperate waters of California latitudes. This approach allowed us to emphasize the changes in recent decades in fish distributions as shown in table 1-1 and as related to changes in ocean temperatures as presented in the Discussion (see below).

Results Species Richness Patterns The species richness of California non-bay coastal fishes was highest in southern California, peaking at 32°N with 243 species (fig. 1-2). Species richness declined relatively sharply from 33° to 34° and then gradually to the north with 125 species recorded at 42°. The number of fish species was significantly correlated (r
0.92, p  .0001) with latitude (32°–42°N), and latitude was significantly correlated (r
0.94, p  .0001) with minimum sea surface temperature.

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TA B L E 1-1

Changes (in Part) in California Marine Fish Fauna Since the Publication of Horn and Allen (1978)

Common Name

Scientific Name

Family

Reference or Comment

Elopidae Fistulariidae Scorpaenidae Cottidae Kyphosidae Serranidae Apogonidae Carangidae Carangidae Carangidae Lobotidae Labridae Scaridae Blenniidae Stichaeidae Stichaeidae Gobiesocidae Callionymidae Sphyraenidae Bothidae Paralichthyidae Tetraodontidae Diodontidae

Fitch and Schultz (1978) Lea and Rosenblatt (2000) inadvertently omitted in Horn and Allen (1978) study Lea (1974) Crooke (1973) Lea and Rosenblatt (2000) Lea and Rosenblatt (2000) Lea and Walker (1995) Lea and Rosenblatt (2000) Lea and Walker (1995) Rounds and Feeney (1993) Lea and Rosenblatt (2000) Lea and Rosenblatt (2000) Lea and Rosenblatt (2000) Miller and Lea (1976, Appendix) Miller and Lea (1976, Appendix) Briggs (2002) Lea and Rosenblatt (2000) Lea and Rosenblatt (2000) Lea and Rosenblatt (2000) Allen (1976) Fitch (1973) Leis (1978)

Species added to the list in the present study

Machete Deepwater cornetfish Flag rockfish Puget Sound sculpin Striped sea chub Greater sand perch Pink cardinalfish Bigeye trevally Cocinero Mexican lookdown Pacific tripletail Blackspot wrasse Loosetooth parrotfish Sabertooth blenny Slender cockscomb Decorated warbonnet Channel Islands clingfish Blacklip dragonet Mexican barracuda Speckletail flounder Gulf sanddab Longnose puffer Balloonfish 23 species

Elops affinis Fistularia corneta Sebastes rubrivinctus Ruscarius meanyi Kyphosus analogus Diplectrum maximum Apogon pacificus Caranx sexfasciatus Caranx vinctus Selene brevoortii Lobotes pacificus Decodon melasma Nicholsina denticulata Plagiotremus azuleus Anoplarchus insignis Chirolophis decoratus Rimicola cabrilloi Synchiropus atrilabiatus Sphyraena ensis Engyophrys sanctilaurentii Citharichthys fragilis Sphoeroides lobatus Diodon holocanthus

Species deleted from the Horn and Allen (1978) list and not included in the present study

Smoothtail mobula

Mobula lucasana

Mobulidae

Orangemouth corvina Scarlet kelpfish 3 species

Cynoscion xanthulus Gibbsonia erythra

Sciaenidae Clinidae

California records not this species; only M. japanica known from state Introduced into Salton Sea; no coastal records Synonym of Gibbonsia montereyensis; see Stepien and Rosenblatt (1991)

Replacement names or name changes

Threadfin bass Pacific crevalle jack Bigscale goatfish

present study Pronotogrammus multifasciatus Caranx caninus Pseudupeneus grandisquamis

Serranidae Carangidae Mullidae

Masked prickleback Sixspot prickleback

Ernogrammus walkeri Kasatkia seigeli

Stichaeidae Stichaeidae

Horn and Allen (1978) As Hemanthias peruanus Previously as Caranx hippos As Mulloidichthys dentatus; see Lea and Rosenblatt (2000) As Askoldia sp. As Stichaeopsis sp.

Pacific scabbardfish

Lepidopus fitchi

Trichiuridae

As Lepidopus xantusi

NOTE: The net 20 species are included among the 519 species used in the overall analysis of the fauna in this chapter. Replacement names and name changes that have occurred since the 1978 study also are listed.

The numbers of species within 14 principal taxonomic groups representing 13 families and one genus (fig. 1-3) account for about 50% of the fish species occurring in California coastal waters. These are plotted at 1° latitudinal intervals in California (32°–41°) and resulted in at least three geographic patterns of richness (fig. 1-4). These three patterns are as follows: (1) six of the families (Carcharhinidae, Sciaenidae, Carangidae, Scombridae, Gobiidae, and Clinidae) showed highest richness in southern California (mainly 32°–33°), reflecting their warm temperate to tropical affinities; (2) three of the families (Zoarcidae, Pholidae, Agonidae,) displayed gradual increases in species richness northward with peak species richness at 40° and 41°, an indication of their cool-temperate affinities in the northeastern Pacific (see Miller and Lea, 1972; Eschmeyer et al., 1983); and (3) the remaining taxa showed highest richness across a broad expanse of

latitude either across southern and central California (Embiotocidae, 32°–38°, Sebastes, 33°–37°) or central and northern California (Cottidae, Stichaeidae, Pleuronectidae). Note that latitude 34°, encompassing 34.0° to 34.9°, straddles the Point. Conception area at 34.5°. This geographic detail means, for example, that the Cottidae showed relatively high richness in this area with a drop in species richness at 33° and that Sebastes exhibited relatively high species richness at both 33° and 34°. Cluster analysis produced dendrograms for three distributional groupings of coastal fishes that revealed different amounts of faunal resemblance among latitudinal components of the fauna (fig. 1-5a). The cluster of 15 bays showed the greatest distance (mean linkage distance, MLD
40.0%  24.1, n
14) among the three clusters. Linkage distance was greatest (scaled linkage distance, LD
100%) between three large northern BIOGEOGRAPHY

7

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F I G U R E 1-2 Numbers of coastal fish species at 1° intervals of latitude

encompassing the California coastline. Minimum sea surface temperatures derived from monthly means for the 14-year period 1949–1962 (after Eber et al., 1968).

California bays (Tomales-Bodega Bay, Humboldt Bay, San Francisco Bay) plus Elkhorn Slough on the central coast and the remaining 11 bays both north (Bolinas Lagoon) and south (10 central and southern California bays) of San Francisco Bay. The next largest distance (LD
60%) separated a cluster consisting of four southern California bays (Mugu Lagoon, Newport Bay, Mission Bay, and San Diego Bay) from a northern California (Bolinas Lagoon), a central California (Morro Bay), and five southern California bays (Alamitos Bay, Anaheim Bay, Carpinteria Marsh, Los Penasquitos Lagoon, and Tijuana Estuary). In turn, Bolinas Lagoon and Morro Bay were separated by an LD of 44% from the five southern California systems. These two more northerly bays were separated by a linkage distance (LD
35%) almost as great. In southern California, two clusters emerged in the analysis separating Alamitos Bay and Anaheim Bay from the remaining three bays (LD
29%). This cluster analysis of 15 bays shows that these systems were not related in a strictly linear (i.e., consecutive latitude) arrangement. For example, Elkhorn Slough on the central coast was linked with the three large northern California bays, and Morro Bay, also on the central coast, was linked most closely with Bolinas Lagoon located just north of San Francisco Bay. Moreover, Carpinteria Marsh to the north was linked most closely to Los Penasquitos Lagoon and Tijuana Estuary, two bays near Mission Bay and San Diego Bay. Mugu Lagoon, geographically nearest to Carpinteria Marsh, linked mostly closely (although at LD
36%) with the three large southern bays (Newport Bay, Mission Bay, and San Diego Bay). Alamitos Bay and Anaheim Bay, however, were closely linked (LD
17%) and are nearest one another along the southern California coast. The dendrogram for non-bay species (fig. 1-5b) was entirely linear with respect to latitude and exhibited the lowest mean within-cluster MLD (24.4%  31.6, n
9) although two large breaks occurred. Cluster distance was greatest (LD
100% scaled linkage distance) between two southern California latitudes (32° and 33°), and the eight other more northerly latitudes, including 34°, which, again, encompasses the Point Conception area. The second largest dichotomy (LD
48%) occurred between a set of three central California latitudes (34°–36°) and a set of five more northerly latitudes (37°–41°). Latitudes 38° and 39° were closely linked (LD
1%) as were latitudes 40° and 41° (LD
3%). The dendrogram for all coastal species (fig. 1-5c) was entirely linear with respect to latitude, and the cluster analy-

8

INTRODUCTION

sis produced a mean within-group MLD (27.7%  31.8, n
9) intermediate between that for the bay and the non-bay species. The cluster topology was more similar to that for the non-bay species set than to that for bay species; the greatest separation (LD
100% scaled linkage distance) was between two southern latitudes (32° and 33°) and the eight more northerly latitudes. The second largest distance (LD
59%) mirrored that for the non-bay species described above but with slightly deeper dichotomies between 38° and 39° (LD
4%) and between 40° and 41° (LD
5%). The 37° interval was distinct from the four more northerly latitudes, at an LD of 24%, and the 34° interval was distinct from the two other central latitudes at LD
21%. The distributional pattern derived from the principal coordinates analysis with ordination of the 289 non-bay species (fig. 1-6) depicts several biogeographic features of the California coastal fish fauna. The ordination showed the high degree to which latitude is associated with the distributions of this subset of the fauna. The length and position of each latitudinal line in fig. 1-6 represent the species richness and composition of species at each latitude relative to the ranked list of 289 species represented by the length of the rectangle. The magnitude of the decline in species richness and change in species composition in a south-to-north direction compared to that in a north-to-south direction is proportional to the sizes of the “open areas” in the upper left and lower right sections of the rectangle. The relatively high species richness in southern California was well illustrated, with 83% and 84% of all of the 289 species occurring at 32° and 33°N. The marked decrease in species richness reflects the importance of boundaries in southern California, or in the Point Conception area (see below), as a faunal break for southern species. A total of 95 species (18.3% of all 519 species) occurred exclusively no farther north than 33°, whereas 64 species (12.3%) occur only north of this latitude. Four large discontinuities occurred in proportions of non-bay species represented per degree of latitude. The largest break in proportions occurred between 33° and 34° (83% to 64%), the next largest between 34° and 35° (64% to 57%), then between 36° and 37° (57% to 49%), and, finally, from 37° to 38° (49% to 45%). The ordination showed an overall northward shift in the non-bay fauna compared to the 1978 ordination with each latitude showing at least a 1% increase in proportion of the total species contained and with the latitudes 32°, 33°, and 36° registering a 2% increase in proportions.

Analysis of End Points of Species Ranges Range end-point analysis (fig. 1-7) showed that California coastal fishes as a group occur over a broad latitudinal expanse but that southern and northern range end points are bimodal in frequency and therefore concentrated at relatively narrow latitudinal intervals. Southern limits of species ranges occurred most frequently off Baja California, southern California, and South America (table 1-2), whereas northern limits occurred most commonly in Alaska, southern California, and central California (table 1-3). Although the distal modes of each bimodal pattern were at latitudes remote from California, the proximal modes were adjacent or clearly overlapped in southern California (32° and 33°). The differing patterns of southern and northern range end points are expressed somewhat further by the degree of correlation between end points and sea surface temperatures (which as shown above are highly correlated with latitude) off California.

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F I G U R E 1-3 Illustrations of representative species for 13 families and one genus of fishes occurring in California coastal waters

(see fig. 1–4).

The number of southern end points at each degree of latitude in California was significantly correlated (r
0.93, p  .0001) with minimum surface temperatures, whereas the number of northern end points was less strongly though still significantly correlated with surface temperatures (r
0.62, p
.040). These differing correlation values reflect the patterns that, whereas northern end points peaked sharply at temperatures corresponding to 33°N and then declined irregularly northward, southern end points gradually increased in number southward along the California coast peaking at temperatures corresponding to 32°N (tables 1-2 and 1-3). One must keep in mind that species richness is a function of sampling effort, which is not equal across the range of these fishes.

Discussion Both similarities and differences are apparent between the distributional analyses published in Horn and Allen (1978) and the present analysis. The broad pattern of geographic ranges of the California fish fauna, as expected, remains largely unchanged. The specific changes, however, that have occurred in coastal fish distributions are notable and can be interpreted in the light of our increased knowledge of climate change, including fluctuations at different spatial and temporal scales. Moreover, the increased resolution that now can be brought to

distributional analysis through phylogeographic approaches using molecular genetic techniques has added a new dimension to the study and understanding of California fish biogeography, as can be seen in Chapter 2. The species-rich fish fauna occurring in California waters is of varied origin and complex distribution, but it is largely a mixture of warm-temperate and subtropical species dominating in southern California and blending with a cool-temperate fauna descending from northerly latitudes. Species richness is clearly greatest in southern California with a sharp decline in richness northward beyond this region and then a more gradual decline farther northward in central and into northern California. This richness pattern is highly correlated with increasing latitude and decreasing minimum surface temperature across California latitudes. To the south of California, the richness of species that occurs in California declines more rapidly than that observed to the north, as demonstrated by range end-point distributions. This marked decline reaches its lowest point in southern Baja California followed by a more gradual decrease in the occurrence of California species southward to central Chile. Overall, this southerly pattern in the distribution of California fish species most likely reflects a combination of changing oceanographic conditions, the presence of a diverse fauna occupying the tropical eastern Pacific biogeographic region (see Hastings, 2000), and less intense and consistent sampling efforts across these lower latitudes.

BIOGEOGRAPHY

9

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F I G U R E 1-4 Species richness patterns in California waters at 1° intervals of latitude for 13 families and one genus of California

coastal fishes. (see fig. 1–3).

Latitudinal Patterns of Particular Faunal Elements Richness patterns for several families and a species-rich genus (Sebastes) across California latitudes demonstrate the varied origins and complexity of the marine fauna of the state (fig. 1-4). Some families clearly illustrate the warm-temperate and tropical component of the fauna with highest richness in southern California. Other families represent the cool-water affinities of part of the fauna with highest richness in more northerly latitudes. Still other higher taxa, including the genus Sebastes, reach peak species-richness in central California or across a broad expanse of latitudes in southern and central California or

10

INTRODUCTION

central and northern California. The overall species richness patterns observed in these higher taxa in the present analysis are similar to those depicted in the earlier study.

Cluster Analysis of Bay and Non-Bay Species Like Horn and Allen (1978), we also found that the dendrogram based on bay-occurring species clustered less tightly than that based on non-bay-occurring species arranged by latitude. This difference may be explained by at least two factors. First, bay-occurring fish species, among them California killifish

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F I G U R E 1-5 Dendrograms of the clustering of 1° intervals of latitude

or bays at irregular latitudes based on presence/absence of fish species using a Pearson product-moment correlation matrix to produce linkage distances among the bays or latitudes scaled to a maximum linkage distance of 100%. (A) For 225 bay-occurring species where the recorded latitudes are those at the midpoints of the mouths of the 15 bays: HB
Humboldt Bay, TBB
Tomales-Bodega Bay; SFB
San Francisco Bay; ES
Elkhorn Slough MgL
Mugu Lagoon, NB
Newport Bay; MiB
Mission Bay; SDB
San Diego Bay; BL
Bolinas Lagoon; MoB
Morro Bay; AlB
Alamitos Bay; AnB
Anaheim Bay; CM
Carpinteria Marsh; LPL
Los Penasquitos Lagoon, TE
Tijuana Estuary. (B) For 289 non-bay-occurring species. (C) For the total of 519 coastal species.

(Fundulus parvipinnis) and certain species of goby, such as arrow goby (Clevelandia ios) and longjaw mudsucker (Gillichthys mirabilis), tend to be inshore species or even confined to bay habitats and therefore have limited powers of latitudinal dispersal. In contrast, non-bay species, as the name implies, are

more offshore taxa with greater opportunities for dispersal across latitudes. Second, the uneven distribution of bays along the California coast promotes greater dissimilarity among the faunas of the more widely separated bays. The third dendrogram, for all coastal fish species, was intermediate in similarity but more similar to the non-bay than to the bay cluster. An important difference emerged from the bay dendrogram in the present study compared to that in the 1978 publication. In the earlier investigation, the greatest dissimilarity in all three dendrograms was found between latitudes or bays north and south of Point Conception, emphasizing the distinctiveness of the southern California fish fauna compared to that of the rest of the state. These differences were sustained in the present study for the non-bay and all-species clusters but not for the bay cluster. The greatest dissimilarity in the more recent bay dendrogram emerged between three large northern bays (Humboldt Bay, Tomales-Bodega Bay, and San Francisco Bay) plus Elkhorn Slough on the central California coast versus the 11 other bays from various parts of the state (table 1-4: fig. 1-8). A further divergence in the present study was that the next largest break among the bay faunas was that uniting Morro Bay on the central coast and Bolinas Lagoon in northern California with five southern California bays more closely than the latter were to the remaining four southern California bays. At least three factors may have helped to produce this different bay dendrogram. The first two involve differences in the analysis, one about the bays included and the second concerning use of a different clustering index. Two southern California bays, Mugu Lagoon and Carpinteria Marsh, were added to the present analysis, and the Pearson productmoment correlation matrix was used in the current study instead of the Canberra-metric dissimilarity measure of the earlier work. Neither of these differences would be expected a priori to produce the differences found between the current and earlier bay dendrograms. The addition of two southern California bays predictably would enhance the distinctiveness of the southern California bay faunas. Moreover, the two different indexes ought to parallel each other in cluster pattern rather than causing the divergence observed between the two dendrograms. The third factor that may have helped to cause the greater latitudinal mixing among the bay faunas in the present study was the overall increase in coastal surface temperatures that occurred during the 25-year interval between the two distributional analyses. Hubbs (1948, 1960) observed that bays tend to be warmer than deeper, more offshore waters thus enhancing the occupation of central and northern California bays by southern species moving northward with the overall warming of coastal waters.

Ordination Analysis by Latitude The ordination of non-bay species by principal coordinates analysis shows two important differences in outcome compared to that of a similar analysis presented in the 1978 paper. The first difference is that the faunal discontinuity in southern California between 33° and 34° is the most prominent boundary in California, exceeding that between 34° and 35°, which encompasses Point Conception. The prominence of the southern California discontinuity was present in the 1978 analysis, as pointed out by Dawson (2001), but was deemphasized in favor of the more well-known break in the vicinity of Point Conception. Dawson (2001) also notes that peaks in range end points occur between 33o and 34o N

BIOGEOGRAPHY

11

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F I G U R E 1-6 Number and compositional pattern of fish species occurring at each degree of latitude in California. The data were analyzed by

principal coordinates analysis with ordination of species by latitude. The length of the rectangle (to the left of the map) represents the ordered list of 289 non-bay-occurring species (see Appendix 2). The length and position of the bar for each degree of latitude represent the number and composition, respectively, of fish species relative to the ordered list. The numbers at the left end of each bar are the number and percentage of species for that degree of latitude. (Further explanation in the text.)

F I G U R E 1-7 Frequency of northern and southern end points of geographic ranges of 519 California coastal fish species at each degree of lati-

tude over the total distributional range (0° and south to  60°N). The bars representing the numbers of northern and southern end points originate at the basal line.

12

INTRODUCTION

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TA B L E 1-2

The Top 11 Latitudes for Occurrence of Southern Range End Points

Latitude °S 28 32 23 (10) 0 equator 33 27 (30) 24 34 31

Number of Range End Points

% of Total

Geographic Area

45 43 40 40 39 30 27 26 26 24 24

8.7 8.3 7.7 7.7 7.5 5.8 5.2 5.0 5.0 4.6 4.6

Central Baja California Southern California Southern Baja California Peru Ecuador Southern California Central Baja California Central Chile Southern Baja California Point Conception (Central California) Northern Baja California

Total 70.1% NOTE:

Ranked by the number and percentage of end points at each latitude for California Marine Fish Fauna (519 species).

TA B L E 1-3

The Top 10 Latitudes for Occurrence of Northern Range End Points

Latitude °N 60 33 57 36 34 37 50 32 53 40

Number of Range End Points

% of Total

Geographic Area

91 73 40 36 33 29 26 22 14 14

17.5 14.1 7.7 6.9 6.4 5.6 5.0 4.2 2.7 2.7

Alaska Southern California Alaska Monterey Bay (central California) Point Conception (central California) Central California Southern British Columbia Southern California Central British Columbia Northern California

Total 72.8% NOTE:

Ranked by the number and percentage of end points at each latitude for California Marine Fish Fauna (519 species).

TA B L E 1-4

Comparison of Results from Horn and Allen (1978) and the Present Study for three Distributional Analyses

Analysis

Horn and Allen (1978)

Present study

Clustering of bay-occurring species

Greatest dissimilarity between southern California bays and those to the north

Greatest dissimilarity between southern California bays and those to the north

Ordination of nonbay-occurring species

82% of species at 33°N 81% of species at 34°N 55% of species at 36°N

84% at this latitude 83% at this latitude 57% at this latitude

Range end points

Number of northern end points not correlated significantly with minimum sea surface

Number significantly correlated

temperature

BIOGEOGRAPHY

13

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F I G U R E 1-8 Visual comparison of the dendrograms for (A) 224 bay-occurring species from 13 bays in the Horn and Allen (1978) analysis and

(B) 225 bay-occurring species from 15 bays in the present study. (See fig. 1-5 and the text for details.)

for both mollusks and marine algae and describes the Los Angeles region in this latitudinal interval as marked by several physical discontinuities of probable ancient origin. The second difference is that the current analysis demonstrates an overall northward shift in the fish fauna since the earlier analysis with the largest increase in proportions at two southern (32° and 33°) latitudes and one central (36°) California latitude (table 1-4); the latter is the second latitude of marked discontinuities for the California biota in Dawson’s (2001) analysis. These increases appear to reflect mainly the additions to the fish fauna since the earlier study, additions that are composed almost entirely of southern, warmer water species (see table 1-1).

be significant (r
0.62, p
.040; see Results), indicating some northward shift in the fish fauna since the earlier analysis (table 1-4). Thus, this change based on range end points represents the second part of the current distributional analysis that provides evidence for a northward shift in distributions (table 1-4). As already discussed above, the change in proportions of fish species occurring per degree of latitude in the ordination analysis also appear to reflect the addition of new species to the fauna, mainly of southern, warm-water fishes, and the expansion northward of certain elements of the fauna in a scenario of warming coastal waters.

Summary Based on a Climate Perspective Analysis of Range End Points The distribution of range end points clearly shows the mixture of southern (warm-water) and northern (cool-water) elements that characterizes the Californian fauna. The narrowly clustered and largely bimodal pattern of southern and northern range end points represents one way to illustrate this faunal mixture. Southern California, the part of the state with the highest species richness, contains about 16% of the total number of northern and southern range end points even though it covers mostly just 2° of latitude (32° and 33°). It is also the most heavily sampled area of our coastline. As Horn and Allen (1978) pointed out in the earlier analysis, numerous species with southern affinities end their ranges northward off southern California and southward off Baja California or much farther south, off South America. Furthermore, the earlier study showed that many species with northern affinities end their ranges northward off Alaska and British Columbia and southward off southern California and Baja California. A noticeable shift in distributional ranges, however, has apparently occurred within the fauna since the 1978 study because in that study, northern end points were not correlated significantly with minimum sea surface, temperature (r
0.49, p  .05). In the present study, this relationship was found to

14

INTRODUCTION

Distributional patterns are increasingly seen as dynamic entities that shift with climate change occurring at different temporal and spatial scales. Temperature has long been recognized as a major factor influencing the distributions of marine organisms. Collections from both Pleistocene fossil (Fitch, 1967) and Holocene archaeological (Gobalet, 2000) sites support the relationships between distribution and temperature for California coastal fishes as does information from historical times, e.g., the nineteenth and twentieth centuries (Hubbs and Schultz, 1929; Hubbs, 1948, 1960). The northward shifts in distribution of fishes as a result of warm-water intervals off the California coast have been known at least since the 1950s, for example, when Radovich (1961) documented the effects of the increased ocean temperatures of 1957 to 1959 on fish and invertebrate distributions. More recently, as ENSO cycles have become more thoroughly understood and recorded, their impacts on the distributions of California fishes have become increasingly appreciated. For example, the effects of the strong 1997–1998 El Niño condition have been well documented (Lea and Rosenblatt, 2000; Pondella and Allen, 2001) and included some remarkable additions of subtropical fishes to the California fish fauna, including, for example, the loosetooth parrotfish (Lea et al., 2001) and Pacific cornetfish (Curtis and Herbinson, 2001).

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Many of these added species are included in the analyses in the present study, as shown in table 1-1. The zebraperch (Hermosilla azurea) is an example of a species that temporarily extended its range northward during short-term periods of ocean warming associated with El Niño conditions but increased in abundance and established breeding populations in the Southern California Bight only after the sustained warming trend in the region over the last quarter of the twentieth century (Sturm and Horn, 2001). Periods of sustained climate conditions are better understood now because of the recognition of intervals intermediate between ENSO cycles of a few years’ duration and continued global warming trends. These intermediate-length periods of climatic conditions have been labeled Pacific Decadal Oscillations and are associated with shifts in ecosystem production regimes in cycles of about 50-year duration (Mantua et al., 1997; Zhang et al., 1997). Because these climate regime shifts seem remarkably similar to changes in biological conditions, Hare and Mantua (2000) suggested that a regime shift may best be determined by monitoring marine organisms rather than climate. In this regard, Chavez et al. (2003) labeled the alternating 20–30 year periods of cool then warm periods in the Pacific as “anchovy” and “sardine” regimes, respectively, because the abundance of northern anchovy and Pacific sardine fluctuate in association with large-scale changes in Pacific Ocean temperatures. These authors identified the period of 1976 to about 1998 as a warm or sardine regime and the previous 25-year period (1950–1975) as a cool or an anchovy regime. Thus, the temporal and spatial resolution for associating biological and oceanographic conditions has increased greatly in the last 50 years and has led to finer scale recognition and prediction of the effects of climate change on marine organisms (e.g., Fields at al., 1993; Roemmich and McGowan, 1995; McFarlane et al., 2000; Fiedler, 2002). Our analyses in the present study showing additions to the California fish fauna mainly from the south and suggesting an overall shift northward in the fauna as a whole seem consistent with climatic shifts occurring over different temporal scales but driven largely by an overarching warming trend.

Recommendation for Future Studies Several types of investigations are needed if we are to deepen our understanding of distributional patterns and to improve our powers to predict the effects of climate change on coastal fish biogeography. New approaches to biogeographic analysis strengthen the prospects for greater resolution and understanding of fish distributions. The variety of techniques and knowledge stores now focused on ocean change on different spatial and temporal scales promises to enhance our assessment and prediction of the effects of climate dynamics on marine ecosystems in general and fish populations in particular. Here are some types of studies that seem worthy of undertaking in the future: 1. Continue ongoing long-term studies of fish distributions in California coastal waters in relation to oceanographic and atmospheric conditions and institute new such studies as appropriate. Investigations could be directed toward key indicator species (e.g., highly responsive species such northern anchovy and Pacific sardine) or the composition and structure of whole communities (e.g., estuaries, kelp beds, coastal soft bottoms). The

phylogenetic perspective should be incorporated increasingly into distributional analyses of California fish species as our knowledge of phylogenetic relationships of the faunal elements continues to expand. 2. Combine traditional biogeography with phylogeography and macroecology to form a highly integrated approach to understand more deeply and to predict more accurately the factors controlling shifts in the abundance and distribution of coastal fish species. Applying the thermogeographic method also may become a reality in the future. 3. Analyze fishes in end-point areas to discover the basis for their range terminations, perhaps as related to recruitment patterns or settlement requirements. For example, what are the biotic and abiotic conditions in the Los Angeles and Monterey Bay regions that result in so many species apparently ending their distributions in those locations? 4. Compare distributional shifts of fishes with those of seaweeds and macroinvertebrates to determine the relative importance of different environmental and climatic factors on their ranges and therefore to increase the power of predicting change in entire ecosystems.

Literature Cited Adey, W.H., and R.S. Steneck. 2001. Thermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test for benthic marine algae. J. Phycol. 37:677–698. Allen, M.J. 1976. Addition of Citharichthys fragilis Gilbert to the California fauna. Calif. Fish Game 62:299–303. Allen, M.J., and G.B. Smith. 1988. Atlas and zoogeography of common fishes in the Bering Sea and northeastern Pacific. NOAA Tech. Rept. NMFS 66, Seattle, WA. Avise, J.C. 2000. Phylogeography, the history and formation of species. Harvard University Press, Cambridge, MA. Bernardi, G. 2000. Barriers to gene flow in Embiotoca jacksoni, a marine fish lacking a pelagic larval stage. Evolution 54:226–237. Blackburn, T.M., and K.J. Gaston. 2002. Scale in macroecology. Global Ecol. Biogeogr. 11:185–189. Bograd, S. J., P. M. DiGiacomo, R. Durazo, T. L. Hayward, K. D. Hyrenbach, R.L. Lynn, A.W. Mantyla, F.B. Schwing, W.J. Sydeman, T. Baumgartner, B. Lavaniegos, and C.S. Moore. 2000. The state of the California Current, 1999–2000: forward to a new regime? Calif. Coop. Ocean. Fish. Invest. Rep. 41:26–52. Briggs, J.C. 1974. Marine zoogeography. McGraw-Hill, New York. ———. 2002. New species of Rimicola from California. Copeia 2002:441–444. Brooks, A.J. 1987. Two species of Kyphosidae seen in King Harbor, Redondo Beach, California. Calif. Fish Game 73(1):49–61. Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago, IL. Brown, J.H., and M.V. Lomolino. 1988. Biogeography. 2d ed. Sinauer, Sunderland, MA. Brusca, R.C., and B.R. Wallerstein. 1979. Zoogeographic patterns of idoteid isopods in the northeast Pacific, with a review of shallow water zoogeography of the area. Bull. Biol. Soc. Wash. No. 3:67–105. Chavez, F.P., J. Ryan, S.E. Lluch-Cota, and M. Ñiquen C. 2003. From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science 299:217–221. Crooke S. J. 1973. The first occurrence of Kyphosus analogus in California. Calif. Fish Game 59:310–311. Curtis, M.D., and K.T. Herbinson. 2001. First record of the Pacific cornetfish, Fistularia corneta Gilbert and Starks 1904, a new species to the southern California fauna during the 1997–1998 El Niño. Bull. South Calif. Acad. Sci. 100:156–159. Dawson, M.N. 2001. Phylogeography in coastal marine animals: a solution for California? J. Biogeogr. 28:723–736.

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Dawson, M.N., J.L. Staton, and D.K. Jacobs. 2001. Phylogeography of the tidewater goby, Eucyclogobius newberryi (Teleostei: Gobiidae), in coastal California. Evolution 55:1167–1179. Durazo, R., T.R. Baumgartner, S.J. Bograd, C.A. Collins, S. Campa, J. Garcia, G. Gaxiola-Castro, et al. 2001. The state of the California Current, 2000–2001: a third straight La Niña year. Calif. Coop. Ocean. Fish. Invest. Rep. 42:29–60. Eber, L.E., J.F.T. Sauer, and O.E. Sette. 1968. Monthly mean charts of sea surface temperature, North Pacific Ocean 1949–62. U. S. Fish Wildlife Service Circular 258. Eschmeyer, W.N., E. S. Harold, and H. Hammann. 1983. A field guide to Pacific Coast fishes of North America from the Gulf of Alaska to Baja California. Houghton Mifflin, Boston, MA. Fiedler, P.C. 2002. Environmental change in the eastern tropical Pacific Ocean: review of ENSO and decadal variability. Mar. Ecol. Prog. Ser. 244:265–283. Fields, P.A., J.B. Graham, R.H. Rosenblatt, and G.N. Somero. 1993. Effects of expected global climate change on marine faunas. Trends Ecol. Evol. 8:361–367. Fitch, J.E. 1967. The marine fish fauna, based primarily on otoliths, of a lower Pleistocene deposit at San Pedro, California (LACMIP 332, San Pedro Sand). Los Angeles County Mus. Contrib. Sci. 128. ———. 1973. The longnose puffer, Sphoeroides lobatus (Steindachner), added to the marine fauna of California. Bull. South Calif. Calif. Acad. Sci. 72:163. Fitch, J.E., and S.A. Schultz. 1978. Some rare and unusual occurrences of fishes off California and Baja California. Calif. Fish Game 64:74–92. Gobalet, K.W. 2000. Has Point Conception been a marine zoogeographic boundary throughout the Holocene? Evidence from the archaeological record. Bull. South. Calif. Acad. Sci. 99:32–44. Hare, S.R., and N.J. Mantua. 2000. Empirical evidence for North Pacific regime shifts in 1977 and 1989. Prog. Oceanogr. 47:103–145. Hart, J.L. 1973. Pacific fishes of Canada. Bull. Fish. Res. Bd. Canada 180. Hastings, P.A. 2000. Biogeography of the Tropical Eastern Pacific: distribution and phylogeny of chaenopsid fishes. Zool. J. Linn. Soc. 128:319–335. Hayden, B.P., and R. Dolan. 1976. Coastal marine fauna and marine climates of the Americas. J. Biogeogr. 3:71–81. Horn, M.H., and L.G. Allen. 1976. Number of species and faunal resemblance of marine fishes in California bays and estuaries. Bull. South. Calif. Acad. Sci. 75:159–170. ———. 1978. A distributional analysis of California coastal marine fishes. J. Biogeogr. 5:23–42. Houghton, J. 2002. An overview of the Intergovernmental Panel on Climate Change (IPCC) and its process of science assessment, pp. 1–20. In: Issues in environmental science and technology 17, Global environmental change, R.E. Hester and R.M. Harrison (eds.). Royal Society of Chemistry, Cambridge, UK. Hubbs, C.L. 1948. Changes in the fish fauna of western North America correlated with changes in ocean temperature. J. Mar. Res. 7:459–482. ———. 1960. The marine vertebrates of the outer coast. Syst. Zool. 9:134–147. ———. 1974. Review, Marine zoogeography by J.C. Briggs. Copeia 1974:1002–1005. Hubbs, C.L., and L.P. Schultz. 1929. The northward occurrence of southern forms of marine life along the Pacific Coast in 1926. Calif. Fish Game 15:234–241. Kousky, V.E., and G.D. Bell. 2000. Causes, predictions, and outcomes of El Niño 1997–1998, pp. 28–48. In: El Niño 1997–1998. The climate event of the century, S.A. Changnon (ed.). Oxford University Press, Oxford, UK. Lea, R.N. 1974. First record of Puget Sound sculpin, Artedius meanyi, from California. J. Fish. Res. Bd. Canada 31:1242–1243. Lea, R.N., E. Erikson, K. Boyle, and R. Given. 2001. Occurrence of the loosetooth parrotfish, Nicholsina denticulata (Scaridae), from Santa Catalina Island, California. Bull. South Calif. Acad. Sci. 100: 167–169.

16

INTRODUCTION

Lea, R.N., and R.H. Rosenblatt. 2000. Observations on fishes associated with the 1997–98 El Niño off California. Calif. Coop. Ocean. Fish. Invest. Rep. 41:117–129. Lea, R.N., and H.J. Walker, Jr. 1995. Record of the bigeye trevally, Caranx sexfasciatus, and Mexican lookdown, Selene brevoorti, with notes on other carangids from California. Calif. Fish Game 81:89–95. Leis, J.M. 1978. Systematics and zoogeography of the porcupinefishes (Diodon, Diodontidae, Tetraodontiformes), with comments on egg and larval development. Fish. Bull. 76:535–567. Lynn, R.J., and S.J. Bograd. 2002. Dynamic evolution of the 1997–1999 El Niño–La Niña cycle in the southern California Current system. Prog. Oceanogr. 54:59–75. Mantua, N.J., S.R. Hare, Y. Zhang, J.M. Wallace, and R.C. Francis. 1997. A Pacific interdecadal climate oscillation with impacts on salmon production. Bull. Am. Meteorol. Soc. 78:1069–1079. McFarlane, G. A., J. R. King., and R. J. Beamish. 2000. Have there been recent changes in climate? Ask the fish. Prog. Oceanogr. 47:147–169. McGowan, J.A. 1971. Oceanic biogeography of the Pacific, pp. 3–74. In: The micropaleontology of oceans, B.M. Funnell and W.R. Riedel (eds.). Cambridge University Press, Cambridge, UK. Miller, D.J., and R.N. Lea. 1972. Guide to coastal marine fishes of California. Calif. Dep. Fish Game Fish Bull. 157. ———. 1976. Guide to coastal marine fishes of California. Calif. Dep. Fish Game Fish Bull. 157 (with addendum to 1972 edition). Murray, S.N., and M.M. Littler. 1981. Biogeographical analysis of intertidal macrophyte floras of southern California. J. Biogeogr. 8: 339–351. Pondella, D.J. II, and M.J. Allen (eds.). 2001. Proceedings of special symposium: new and rare fish and invertebrate species to California during the 1997–1998 El Niño. Bull. South Calif. Acad. Sci. 100:129–130. Pondella, Daniel J., II, and M.T. Craig. 2001. First record of the sabertooth blenny, Plagiotremus azaleus, in California with notes on its distribution along the Pacific coast of Baja California. Bull. South. Calif. Acad. Sci. 100:144–148. Radovich, J. 1961. Relationships of some marine organisms of the Northeast Pacific to water temperatures. Calif. Dep. Fish Game Fish Bull. 112. Roemmich, D., and J.A. McGowan. 1995. Climate warming and the decline of zooplankton in the California Current. Science 267:1324–1326. Rounds, J.M., and R.F. Feeney. 1993. First record of the tripletail (Lobotes surinamensis, family Lobotidae) in California waters. Calif. Fish Game 79:167–168. Smith, K.F., and J.H. Brown. 2002. Patterns of diversity, depth range and body size among pelagic fishes along a gradient of depth. Global Ecol. Biogeogr. 11:313–322. Smith, P.E. 1995. A warm decade in the Southern California Bight. Calif. Coop. Ocean. Fish. Invest. Rep. 36:120–126. Smith, R.W. 1976. Numerical analysis of ecological survey data. Unpubl. Ph.D. Diss. University of Southern California, Los Angeles. SCCWRP (Southern California Coastal Water Research Project). 1973. The ecology of the Southern California Bight: Implications for water quality management. Tech. Rep. 104, El Segundo, CA. Stepien, C.A., and R.H. Rosenblatt. 1991. Patterns of gene flow and genetic divergence in the northeastern Pacific Clinidae (Teleostei: Blennioidei), based on allozyme and morphological data. Copeia 1991:863–896. Sturm, E. A., and M. H. Horn. 2001. Increase in occurrence and abundance of zebraperch (Hermosilla azurea) in the Southern California Bight in recent decades. Bull. South. Calif. Acad. Sci. 100:170–174. Valentine, J.W. 1966. Numerical analysis of marine molluscan ranges on the extratropical northeastern Pacific shelf. Limnol. Oceanogr. 11:198–211. Zhang, Y., J.M. Wallace, and D. S. Battisti. 1997. ENSO-like interdecadal variability: 1900–93. J. Climate 10:1004–1020.

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Appendix 1-1.

California coastal fish species

This list of 519 California Coastal fish spercies used in the present study gives their southern and northern latitudinal range limits. See fig. 1-7.

Pholis laeta Agonus acipenserinus Asterotheca infraspinata Bathygonus nigripinnis Chirolophus decoratus Delolepis gigantea Lumpenus sagitta Lyconectes aleutensis Thaleichthys pacificus Pallisina barbata Sebastes reedi Anoplarchus insignis Artedius meanyi Pholis clemensi Hippoglossoides elassodon Lampetra ayresii Liparis rutteri Oncorhynchus clarkii Spirinchus thaleichthys Trichodon trichodon Occella verrucosa Ascelichthys rhodorus Liparis pulchellus Pholis ornata Ronquilus jordani Theragra chalcogramma Enophrys bison Erilepis zonifer Hemilepidotus hemilepidotus Sebastes borealis Zaprora silenus Clinocottus acuticeps Amphisticus rhodoterus Pleurogrammus monopterygius Scytalina cerdale Sebastes nigrocinctus Bothragonus swanii Liparis fucensis Pholis schultzi Blepsias cirrhosus Platichthys stellatus Allocyttus folletti Chlamydoselachus anguineus Gadus macrocephalus Hexagrammus superciliosus Isopsetta isolepis Liparis florae Lycodapus mandibularis Sebastes maliger Spirinchus starksi Xiphister mucosus Anoplarchus purpurescens Artedius harringtoni Clinocottus globiceps Sebastes nebulosus Synchirus gilli Nautichthys oculofasciatus Artedius fenestralis Microgadus proximus Jordania zonope

South Lat.

North Lat.

41 40 40 40 40 40 40 40 38 38 38 38 38 38 37 37 37 37 37 37 37 37 36 36 36 36 36 36 36 36 36 36 36 35 35 35 35 35 35 35 34 34 34 34 34 34 34 34 34 34 34 34 34 34 34 34 34 34 34 34

60 64 60 60 60 60 60 60 60 58 57 54 50 50 60 60 60 60 60 60 58 56 60 60 60 60 57 57 57 57 55 52 50 60 60 60 57 57 49 41 68 60 60 60 60 60 60 60 60 58 58 57 57 57 57 56 55 54 54 50

Zenopsis nebulosa Ernogrammus walkeri Plagiogrammus hopkinsii Radulinus vinculus Alopias superciliosus Ammodytes hexapterus Atheresthes stomias Hippoglossus stenolepis Hypomesus pretiosus Oncorhynchus nerka Phytichthys chirus Psettichthys melanostictus Rhamphocottus richardsonii Sebastes brevispints Sebastes caurinus Sebastes crameri Somniosus pacificus Apodichthys flavidus Chirolophus nugator Oligocottus maculosus Hemilepidotus spinosus Radulinus boleoides Oligocottus rimensis Sebastes melanops Allosmerus elongatus Xeneretmus leiops Euprotomicrus bispinatus Oligocottus rubellio Enophrys taurus Sebastes phillipsi Icelinus fimbriatus Rimicola cabrilloi Clupea harengus Asterotheca pentacantha Bathyraja interrupta Lamna ditropis Lepidopsetta bilineata Lycenchelus crotalinus Lycodapus fierasfer Lycodes diapterus Oncorhynchus gorbuscha Oncorhynchus keta Oncorhynchus tshawytscha Poroclinus rothrocki Raja stellulata Reinhardtius hippoglossoides Sebastes alutus Sebastes proriger Sebastes ruberrimus Sebastes flavidus Agonopsis vulsa Anarrhichthys ocellatus Icosteus aenigmaticus Radulinus asprellus Sebastes helvomaculatus Sebastes entomelas Sebastes wilsoni Icelinus burchami Hexagrammus decagrammus Plectobranchus evides

South Lat.

North Lat.

34 34 34 34 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32 32

37 36 36 34 60 60 60 60 60 60 60 60 60 60 60 60 60 57 57 57 56 54 53 51 48 48 40 39 37 37 36 34 65 60 60 60 60 60 60 60 60 60 60 60 60 60 60 60 60 59 57 57 57 57 57 57 57 56 55 55

BIOGEOGRAPHY

17

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(continued)

Careproctus melanurus Icelinus filamentosus Paricelinus hopliticus Sebastes zacentrus Melanostigma pammelas Sebastes aleutianus Lycodes cortezianus Sebastes babcocki Bothrocara brunneum Icelinus oculatus Morone saxatilus Eucyclogobius newberryi Neoclinus uninotatus Sebastes lentiginosus Acipenser medirostris Acipenser transmontanus Clinocottus embryum Oncorhynchus mykiss Sebastes mystinus Lycodes pacificus Brosmophycis marginata Pleuronichthys coenosus Xipister atropurpureus Embiotoca lateralis Sebastes pinniger Hexanchus griseus Bothrocara molle Gibbonsia montereyensis Zesticelus profundorum Rimicola muscarum Phanerodon furcatus Rathbunella hypoplecta Sebastes ovalis Hypsurus caryi Lethops connectens Ulvicola sanctaerosae Anchoa compressa Leicottus hirundo Antimora microlepis Oncorhynchus kisutch Sebastes rubrivinctus Oligocottus snyderi Cymatogaster aggregata Leptocottus armatus Artedius lateralis Xeneretmus triacanthus Apristurus brunneus Xenertmus latifrons Artedius corallinus Artedius notospilotus Sebastes jordani Seriola lalandi Lyconema barbatum Cebidichthys violaceus Gasterosteus aculeatus Stereolepis gigas Micrometrus aurora Sphyrna zygaena Sebastes gilli Cryptotrema corallinum Lampetra tridentata Coryphaenoides acrolepis Bathyraja trachura

18

INTRODUCTION

South Lat.

North Lat.

32 32 32 32 32 32 32 32 32 32 32 32 32 32 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 31 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 30 29 29 29

54 54 54 54 53 53 52 52 50 50 49 48 38 33 60 60 60 60 60 58 57 57 57 56 56 55 53 53 53 52 50 50 42 40 36 36 35 34 60 60 60 57 56 56 55 52 51 49 48 48 48 47 42 41 60 40 38 37 36 34 61 60 60

Ophiodon elongatus Sebastes paucispinis Thunnus alalunga Rhacochilus vacca Gobiesox maeandricus Oxylebius pictus Hyperprosopon ellipticum Liparis mucosus Xererpes fucorum Stellerina xyosterna Hyperprosopon anale Sebastes rufus Orthonopias triacis Sebastes hopkinsi Sebastes simulator Gobiesox eugrammus Sebastes diploproa Anoplopoma fimbria Eopsetta jordani Eptatretus deani Glyptocephalus zachirus Hydrolagus colliei Pleuronichthys decurrens Raja binoculata Raja rhina Sebastes elongatus Sebastolobus alascanus Odontopyxis trispinosa Syngnathus leptorhynchus Tetragonurus cuvieri Icelinus tenuis Torpedo californica Lyopsetta exilus Hyperprosopon argenteum Lepidogobius lepidus Seabastes miniatus Sebastes aurora Raja inornata Seabastes melanostomus Sebastes chlorosticus Atherinopsis californiensis Sebastes rastrelliger Sebastes levis Nezumia stelgidolepis Sebastes serranoides Amphisticus argenteus Micrometrus minimus Oxyjulis californica Phanerodon atripes Synodus lucioceps Neoclinus blanchardi Platyrhinoides triseriatus Sebastes ensifer Sebastes eos Sebastes rosenblatti Sebastes serriceps Ophidion scrippsae Rimicola dimorpha Xeneretmus ritteri Tenogobius sagittula Eptatretus stoutii Aulorhynchus flavidus Icichthys lockingtoni

South Lat.

North Lat.

29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 29 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 28 27 27 27

57 57 57 56 55 54 50 50 49 48 44 42 37 37 36 33 61 60 60 60 60 60 60 60 60 60 60 57 57 55 53 53 51 50 50 50 50 48 47 47 44 44 42 41 41 38 38 38 38 38 37 37 37 37 37 37 34 34 34 32 60 57 57

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Appendix 1-1.

(continued)

Sebastes saxicola Rhinogobiops nicholsii Alopias vulpinus Brachyistius frenatus Gibbonsia metzi Sbastes rosaceus Chilara taylori Zaniolepis frenata Zaniolepis latipinnis Clinocottus recalvus Sebastes carnatus Sebastes chrysomelas Clinocottus analis Rhacochilus toxotes Sebastes atrovirens Zalembius rosaceus Sebastes dallii Sebastes semicinctus Chromis punctipinnis Neoclinus stephensae Ruscarius creaseri Agonopsis sterletus Gobiesox rhessodon Alloclinus holderi Squalus acanthias Sebastes auriculatus Scorpaenichthys marmoratus Galeorhinus galeus Amphisticus koelzi Embiotoca jacksoni Sebastes umbrosus Rimicola eigenmanni Chitonotus pugetensis Bathyraja abyssicola Paralichthys californicus Peprilus simillimus Seriphus politus Hypsopsetta guttulata Pleuronichthys verticalis Pleuronichthys ritteri Typhlogobius californiensis Gymnothorax mordax Merluccius productus Squatina californica Atractoscion nobilis Trachurus symmetricus Notorhynchus cepedianus Sebastes goodei Genyonemus lineatus Paralabrax clathratus Sebastes constellatus Anisotremus davidsonii Leuresthes tenuis Paralabrax nebulifer Scorpaena guttata Syngnathus californiensis Heterodontus francisci Hypsypops rubicundus Icelinus cavifrons Sebastes macdonaldi Fundulus parvipinnis Gibbonsia elegans Cheilotrema saturnum

South Lat.

North Lat.

27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 27 26 26 26 26 26 26 26 26 25 25 25 25 25 25 25 25 25 25 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24

57 53 50 50 50 48 45 43 43 42 42 40 39 39 38 38 37 37 36 36 36 35 35 34 60 57 56 55 48 39 37 33 54 54 50 49 44 40 37 35 35 34 60 60 58 57 53 51 50 46 40 34 37 37 37 37 36 36 36 36 35 35 34

Hypsoblennius gilberti Paraclinus integripinnis Porichthys myriaster Anchoa delicatissima Odontaspis ferox Cetorhinus maximus Citharichthys sordidus Citharichthys stigmaeus Lampris guttatus Microstomus pacificus Parophrys vetulus Sardinops sagax Sebastolobus altivelis Engraulis mordax Atherinops affinis Clevelandia ios Argentina sialis Myliobatis californica Triakis semifasciata Medialuna californiensis Lepidopus fitchi Mustelus californicus Mustelus henlei Cosmocampus arctus Gillichthys mirabilis Ilypnus gilberti Rhinobatos productus Hermosilla azurea Hippoglossina stomata Hypsoblennius gentilis Lythrypnus dalli Paralabrax maculatofasciatus Parmaturus xaniurus Scomberomorus concolor Xystreurys liolepis Quietula y-cauda Gnathophis cinctus Halichoeres semicinctus Menticirrhus undulatus Roncador stearnsii Umbrina roncador Apogon guadalupensis Cynoscion parvipinnis Hyporhamphus rosae Mycteroperca jordani Porichthys notatus Sphyraena argentea Heterostichus rostratus Cheilopogon pinnatibarbatus Symphurus atricauda Icelinus quadriseriatus Girella nigricans Semicossyphus pulcher Hemianthias signifer Cololabis saira Chaenopsis alepidota Lythypnus zebra Carcharhinus obscurus Carcharhinus longimanus Hypsoblennius jenkinsi Bathyraja spinosissima Citharichthys xanthostigma Xanthichthys mento

South Lat.

North Lat.

24 24 24 24 24 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 23 22 22 22 22 22 22 22 22 22 20 20 18 18 18 16 10 10 10

34 34 34 33 33 60 60 60 60 60 60 55 55 53 50 50 44 44 43 41 40 40 40 38 38 38 37 36 36 36 36 36 36 36 36 35 34 34 34 34 34 33 33 33 32 57 57 53 46 41 38 37 37 33 60 34 36 33 32 34 44 36 34

BIOGEOGRAPHY

19

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Appendix 1-1.

(continued)

Scorpaenodes xyris Uraspis secunda Zapteryx exasperata Physiculus rastrelliger Urolobatus halleri Albula vulpes Syngnathus auliscus Gobiesox papillifer Mustelus lunulatus Oligopus diagrammus Hippocampus ingens Bellator xenisma Melichthys niger Decodon melasma Manta birostris Selene brevoortii Nicholsina denticulata Alepocephalus tenebrosus Brama japonica Mola mola Pteroplatytrygon violacea Pseudopentaceros wheeleri Lagocephalus lagocephalus Decapterus muroadsi Desmodena lorum Mugil cephalus Naucrates ductor Ruvettus pretiosus Euthynnus lineatus Pteraclis aesticola Mobula japanica Lactoria diaphana Allothunnus fallai Assurger anzac Bagre panamensis Prognathodes falcifer Chilomycterus reticulatus Citarichthys fragilis Diplectrum maximum Echeneis naucrates Euleptorhamphus longirostris Euthynnus affinis Hemiramphus saltator Macroramphosus gracilis Makaira indica Makaira mazara Myxine circifrons Phtheirichthys lineatus Plagiotremus azaleus Sphyraena ensis Synchiropus atrilabiatus Taractichthys steindachneri Zu cristatus Apogon pacificus Caranx caninus Caranx vinctus Cheilopogon heterurus Lophotus capellei Rhincodon typus Dormitator latifrons Dasyatis dipterura Mycteroperca xenarcha Cetengraulis mysticetus

20

INTRODUCTION

South Lat.

North Lat.

10 10 9 8 8 8 8 8 8 8 6 5 4 3 3 2 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 5 5 5

33 33 33 40 40 37 34 33 33 33 33 33 32 33 33 32 33 60 60 55 50 50 39 36 36 36 36 36 35 35 34 34 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 32 32 32 32 32 32 33 50 37 34

Carcharhinus leucas Scomberomorus sierra Caranx caballus Chaetodipterus zonatus Epinephelus niphobles Thunnus orientalis Caulolatilus princeps Katswonus pelamis Lepidocybium flavobrunneum Thunnus obesus Prionotus stephanophrys Ophichthus triserialis Ophichthus zophochir Kathetostoma averruncus Strongylura exilis Echinorhinus cookei Xenistius californiensis Elops affinis Epinephelus analogus Fodiator acutus Gymnura marmorata Pristigenys serrula Trachinotus rhodopus Zalieutes elater Antennarius avalonis Auxis thazard Carcharhinus brachyurus Chaetodon humeralis Chloroscrombrus orqueta Engyophrys sanctilaurentii Fistularia corneta Galeocerdo cuvier Lobotes pacificus Myrophis vafer Nematistius pectoralis Polydactylus opercularis Rhizoprionodon longurio Remora osteochir Selene peruviana Seriola rivoliana Sphyrna tiburo Trachinotus paitensis Trichiurus nitens Harengula thrissina Hyporhamphus naos Sphoeroides annulatus Eucinostomus dowii Polydactylus approximans Auxis rochei Calamus brachysomus Eucinostomus currani Kyphosus analogus Sphoeroides lobatus Carcharodon carcharias Prionace glauca Trachipterus altivelis Sarda chiliensis Scomber japonicus Remora australis Coryphaena hippurus Isurus oxyrinchus Luvarus imperialis Xiphias gladius

South Lat.

North Lat.

5 5 6 6 8 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 11 12 12 12 12 20 20 30 30 30 30 30 30 30 30 30 30

33 33 36 32 35 57 50 48 47 47 46 40 40 39 37 36 36 34 34 34 34 34 34 34 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 33 32 32 32 32 36 33 33 33 33 33 60 60 60 57 57 50 47 46 44 44

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Appendix 1-1.

(continued) South Lat.

North Lat.

30 30 30 30 30 30 30 30 30

42 41 37 37 36 36 35 35 34

Tetrapturus angustirostris Balistes polylepis Remora remora Remora albescens Cephaloscyllium ventriosum Etrumeus teres Ranzania laevis Thunnus albacares Tetrapturus audax

Appendix 1-2.

Gempylus serpens Pseudupeneus grandisquamis Regalecus glesne Trachipterus fukuzakii Caranx sexfasciatus Diodon holocanthus Diodon hystrix Istiophorus platypterus Remora brachyptera

South Lat.

North Lat.

30 30 30 30 30 30 30 30 30

33 33 33 33 32 32 32 32 32

Non-bay-occurring California fish species

This list of 289 non-bay occurring species is ordered by latitude according to principal coordinates analysis. See fig. 1.6 for pattern.

Latitude (°N)

Pholis laeta Agonus acipenserinus Bathyagonus infraspinatus Bathyagonus nigripinnis Delolepis gigantea Lyconectes aleutensis Anoplarchus insignus Oncorhynchus nerka Pholis clemensi Sebastes reedi Hippoglossoides elassodon Oncorhynchus clarkii Erilepis zonifer Pleurogrammus monopterygius Ronquilus jordani Sebastes borealis Theragra chalcogramma Zaprora silenus Pholis schultzi Sebastes nigrocinctus Allocyttus folletti Chlamydoselachus anguineus Clinocottus globiceps Gadus macrocephalus Jordania zonope Lycodapus mandibularis Sebastes maliger Synchirus gilli Alopias superciliosus Oligocottus rimensis Oncorhynchus keta Phytichthys chirus Radulinus boleoides Rhamphocottus richardsonii Sebastes brevispinis Sebastes crameri Somniosus pacificus Xeneretmus leiops Agonopsis vulsa Alepocephalus tenebrosus Antimora microlepis Apristurus brunneus

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1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1

BIOGEOGRAPHY

21

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Appendix 1-2.

(continued) Latitude (°N)

Argentina sialis Artedius corallinus Asterotheca pentacantha Bathyraja interrupta Bathyraja spinosissima Bathyraja abyssicola Bothrocara brunneum Bothrocara molle Brama japonica Carcharodon carcharias Careproctus melanurus Caulolatilus princeps Chitonotus pugetensis Coryphaena hippurus Coryphaenoides acrolepis Cheilopogon pinnatibarbatus Eptatretus deani Euthynnus pelamis Glyptocephalus zachirus Isurus oxyrinchus Lamna ditropis Lampris guttatus lcelinus oculatus lcelinus burchami lcelinus filamentosus lcelinus tenuis lcichthys lockingtoni lcosteus aenigmaticus Lepidocybium flavobrunneum Lepidopsetta bilineata Lycenchelus crotalinus Lycodapus fierasfer Lycodes diapterus Lycodes cortezianus Lyconema barbatum Melanostigma pamelas Oncorhynchus gorbuscha Paricelinus hopliticus Pseudopentaceros wheeleri Plectobranchus evides Poroclinus rothrocki Prionotus stephanophrys Radulinus asprellus Raja stellulata Reinhardtius hippoglossoides Remora australis Sebastes aleutianus Sebastes auriculatus Sebastes entomelas Sebastes chlorostictus Sebastes rosaceus Sebastes helvomaculatus Sebastes jordani Sebastes babcocki Sebastes elongatus Sebastes ruberrimus Sebastes diploproa Sebastes aurora Sebastes melanostomus Sebastes proriger Sebastes alutus Sebastes miniatus

22

INTRODUCTION

41

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1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

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Appendix 1-2.

(continued) Latitude (°N)

Sebastes saxicola Sebastes zacentrus Sebastes carnatus Sebastes rufus Sebastes levis Sebastes ovalis Sebastolobus alascanus Sebastolobus altivelis Seriola lalandi Tetragonurus cuvieri Tetrapturus angustirostris Thunnus alalunga Thunnus obesus Thunnus orientalis Trachurus symmetricus Xeneretmus triacanthus Xeneretmus latifrons Xiphias gladius Zaniolepis frenata Zaniolepis latipinnis Zesticelus profundorum Balistes polylepis Nezumia stelgidolepis Lepidopus fitchi Physiculus rastrelliger Sebastes constellatus Kathetostoma averruncus Lagocephalus lagocephalus Oligocottus rubellio lcelinus quadriseriatus Phanerodon atripes Zalembius rosaceus Cephaloscyllium ventriosum Echinorhinus cookei Etrumeus teres Mycteroperca xenarcha Orthonopias triacis Parmaturus xaniurus Remora remora Remora albescens Sebastes serriceps Sebastes hopkinsi Sebastes ensifer Sebastes eos Sebastes rosenblatti Sebastes semicinctus Semicossyphus pulcher Sebastes phillipsi Zenopsis nebulosa Ruscarius creaseri Caranx caballus Citharichthys xanthostigma Decapterus muroadsi Desmodena lorum Hippoglossina stomata Icelinus cavifrons Lethops connectens Lythrypnus dallii Lythrypnus zebra Naucrates ductor Neoclinus stephensae Polydactylus approximans

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1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1

BIOGEOGRAPHY

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

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Appendix 1-2.

(continued) Latitude (°N) 41

Ruvettus pretiosus Scomberomorus concolor Sebastes umbrosus Sebastes gilli Sebastes macdonaldi Sebastes simulator Ulvicola sanctaerosae Ernogrammus walkeri lcelinus fimbriatus Plagiogrammus hopkinsii Agonopsis sterletus Euthynnus lineatus Pteraclis aesticola Ranzania laevis Thunnus albacares Typhlogobius californiensis Alloclinus holderi Cetengraulis mysticetus Chaenopsia alepidota Cryptotrema corallinum Pteroplatytrygon violacea Epinephelus analogus Fodiator acutus Gnathophis cinctus Gymnothorax mordax Leiocottus hirundo Lophotus capellei Mobula japanica Lactoria diaphana Pristigenys serrula Rimicola dimorpha Tetrapturus audax Trachinotus rhodopus Xanthichthys mento Xeneretmus ritteri Zalieutes elater Rimicola cabrilloi Radulinus vinculus Oligoplites saurus Allothunnus fallai Antennarius avalonis Apogon guadalupensis Assurger anzac Auxis thazard Auxis rochei Bagre panamensis Bellator xenisma Calamus brachysomus Carcharhinus obscurus Carcharhinus leucas Carcharhinus remotus Prognathodes falcifer Chaetodon humeralis Chilomycterus reticulatus Chloroscrombrus orqueta Cynoscion parvipinnis Decodon melasma Diplectrum maximum Dormitator latifrons Echeneis naucrates Eucinostomus currani Euleptorhamphus longirostris

24

INTRODUCTION

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1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1

1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

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Appendix 1-2.

(continued) Latitude (°N) 41

Euthynnus affinis Fistularia corneta Galeocerdo cuvier Gempylus serpens Gobiesox papillifer Gobiesox eugrammus Hemiramphus saltator Hippocampus ingens Lobotes pacificus Macroramphosus gracilis Makaira indica Makaira mazara Manta birostris Myrophis vafer Myxine circifrons Nematistius pectoralis Nicholsina denticulata Odontaspis ferox Grammonus diagrammus Phtheirichthys lineatus Plagiotremus azaleus Polydactylus opercularis Pseudupeneus grandisquamis Regalecus glesne Rhizoprionodon longurio Rhombochirus osteochir Rimicola eigenmanni Scomberomorus sierra Scorpaenodes xyris Sebastes lentiginosus Selene peruviana Seriola rivoliana Sphoeroides lobatus Sphyraena ensis Sphyrna tiburo Synchiropus atrilabiatus Taractichthys steindachneri Trachinotus paitensis Trachipterus fukuzakii Trichiurus nitens Uraspis secunda Zu cristatus Apogon pacificus Caranx caninus Carcharhinus longimanus Chaetodipterus zonatus Cheilopogon heterurus Diodon hystrix Diodon holocanthus Engyophrys sanctilaurentii Epinephelus niphobles Eucinostomus dowii Ctenogobius sagittula Harengula thrissina Hyporhamphus naos lstiophorus platypterus

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1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

Melichthys niger Mycteroperca jordani Remora brachyptera Rhincodon typus Sphoeroides annulatus

1 1 1 1 1

BIOGEOGRAPHY

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CHAPTER 2

Phylogeography M I C HAE L N DAWS O N, R O B I N S. WAP LE S, AN D G IAC O M O B E R NAR D I

Introduction Comparative Phylogeography Phylogeography seeks to explain the geographic distribution of genetic lineages. To the extent that organisms are products of their DNA, phylogeography also seeks to explain the distribution of organisms, including variation within and, less commonly, between species. Because genetic variation may take thousands or millions of years to accrue, phylogeography has a strong historical component. Thus, phylogeography is closely allied with biogeography, particularly historical and cladistic biogeography, and can be thought of as opening a window in time through which we can observe the influence of historical factors on modern patterns of biodiversity. Since its inception (Avise et al., 1987), phylogeography has grown exponentially (Avise, 2000), reflecting its intuitive appeal and perceived success. Although the vast majority of phylogeographic studies still explore patterns within single species, greater access to larger amounts of molecular data is making comparative phylogeography, which compares the genealogies of two or more species with overlapping geographic ranges, increasingly popular and powerful (Avise, 1992, 1994; Riddle et al., 2000a, b, c). Comparative phylogeography has proven particularly useful in revealing common patterns and causes of genetic heterogeneities within species as well as suggesting links between life history and genetic structure. The goal of this chapter is to employ the comparative phylogeographic approach to elucidate the factors that have most influenced geographic patterns of genetic variation in California fishes. Phylogeographic hypotheses fall into two categories: those that focus on (intrinsic) properties of the organism and those that focus on (extrinsic) properties of the environment. They map, to an extent, onto the juxtaposed issues of dispersal and vicariance, often focusing on issues regarding (1) life-history, particularly the duration and dispersal potential of larval stages, and (2) the degree of geographic isolation, respectively. 1. Dispersal potential, gene flow, phylogeographic structure, and the case of planktonic larval duration. As formulated above, a larva may move between populations if the distance between them is shorter than the distance over which it can disperse; the closer they are together, the more likely it will move between

26

them (assuming there is not some minimum time to competence that precludes early settlement). Gene flow measures the actual dispersal and mixing that occurs between populations. Because mixing cannot occur without dispersal and more dispersal should foster more mixing, gene flow is expected to reflect dispersal potential. Hypothetically, the larger the disposal potential, the greater the gene flow, the less the phylogeographic structure (fig. 2-1). Typically, in coastal marine fishes that exhibit a benthic sedentary adult phase and a pelagic larval phase, dispersal potential has been framed in the context of planktonic larval duration (PLD). A number of studies have now examined whether PLD is a good estimator of gene flow in a wide range of fishes and areas as diverse as coastal California, the Sea of Cortez, the Caribbean, and the Great Barrier Reef (Waples, 1987; Doherty et al., 1995; Shulman and Bermingham, 1995; Riginos and Victor, 2001). Few have found conclusive evidence that the degree of population or phylogeographic structure is simply correlated with PLD. The vast majority suggests that a complex of interacting factors, including PLD but also historical geography, hydrography, ecology, chance events, extirpations, habitat, and other life-history attributes (e.g., fecundity), influence modern phylogeographic structure. In addition, many coastal marine fishes can be highly vagile as adults (Chapter 20) and this needs to be taken into account. Hypotheses based on PLD may have little relevance to fishes that are strongly nektonic throughout much of the potentially dispersive life stages, such as anadromous fishes. Thus, the relationship between dispersal potential and realized gene flow remains something of an enigma. 2. Deep phylogenetic gaps usually arise from long-term zoogeographic barriers to gene flow. Zoogeographic barriers are environmental discontinuities that demonstrably have limited the distribution of a large number of species. Such discontinuities are expected to have a similar effect within some species, leading to divergent populations on different sides of the barrier. The special value of phylogeography in this context is that phylogeny can indicate the mode of divergence (fig. 2-2). Moreover, in this context, phylogeography explicitly integrates microevolution and macroevolution, relating ecology to evolution and patterns of variation within species to patterns of variation among species. These relationships were proposed, in the phylogeographic context, in the original phylogeographic paper

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disjunct in the northern Sea of Cortez; and (5) California’s Islands which, although they lie relatively short distances from the mainland California and Baja California coastlines, are inhabited by populations that are apparently somewhat isolated from the mainland and from each other by deepwater channels. On the basis of life-history characteristics, we recognize a sixth category, anadromous fishes, that illustrates another set of processes leading to quite different evolutionary patterns. By discussing these subgroups, we hope to elucidate certain processes by describing specific local examples. This has the added benefit of further simplifying discussions that naturally cover a large region, numerous species, and complex histories. At the end of the chapter, we briefly synthesize the regional studies to provide a more holistic perspective and highlight areas that require further research.

F I G U R E 2-1 Schematic of possible relationships of genetic differentia-

tion to planktonic larval duration (PLD; red) and geographic isolation (blue). The shapes of the curves (initially drawn as straight lines) may vary depending on, for example, habitat structure (e.g. stepping stone model) and, notably, may be sigmoidal if certain levels of PLD (1) are required to establish any gene flow or (2) flood the system, or if certain levels of geographic isolation (3) do not inhibit gene flow or (4) prevent gene flow. Realized gene flow is likely to be a complex of these and possibly other functions, such as fecundity. Please note that the shapes and positions of lines (straight and curved) are extremely generalized and are likely to vary among species, places, and possibly times.

(Avise et al. 1987) and subsequently tested in coastal California (e.g. Burton and Lee, 1994; Edmands et al., 1996; Burton, 1998; Bernardi, 2000; Dawson et al., 2001). Like hypotheses relating PLD to genetic structure, the phylogeographic hypotheses were found wanting (Burton, 1998), although a solution has since been offered (Dawson, 2001). Data describing additional taxa in California and adjacent Pacific North American coastal areas are now available, so we will revisit these issues here and examine the implications for our understanding of genetic variation in coastal marine fishes. R EC O G N I Z I NG S U B R E G ION S

Coastal Pacific North America can be subdivided geographically on the basis of species distributions (e.g., Chapter 1). These biogeographic divisions are important in phylogeography because, along with environmental data, they suggest extrinsic biotic and abiotic factors that have influenced the distributions of organisms at the species level and, according to the phylogeographic hypotheses, may have had similar effects within species. The geographic relationship between intraspecific phylogenetic structure and supraspecific biotic and abiotic divisions is key in understanding modes of evolution (fig. 2-2). As such, in this chapter, we consider phylogeography in the context of five regions in which different processes probably played greater or lesser roles in structuring coastal fishes (fig. 2-3): (1) the Cordilleran, northwest North America, where the effects of glacial cycles have been most immediate and most intense; (2) California state, where debate has focused on the presence of a biogeographic break at Point Conception yet its apparent lack of influence on phylogeographic structure; (3) Pacific Baja California, which includes another proposed biogeographic and phylogeographic boundary at Punta Eugenia; (4) the Gulf of California, where populations of circa 20 species of California fishes are thought to be

Some Technical Background Comments A number of landmark papers provide historical context for this chapter. Large-scale phylogenetics, as practiced in phylogeography (although the field did not exist at the time), made a giant leap forward with the advent of PCR and sequencing. Phylogeography was conceived and christened less than 10 years later (Avise et al., 1987). A momentous paper from Allan Wilson’s laboratory at the University of California Berkeley that described “universal” vertebrate oligonucleotide PCR primers (Kocher et al., 1992) provided tools that promoted the rapid growth and diversification of the new discipline. Primers described in that paper included mitochondrial cytochrome b primers that were proven well matched to diverse fish DNAs by the ensuing deluge of data. Although cytochrome b was used more often for interspecific studies than intraspecific studies, the trend of generating vast amounts of data was set and provided the stepping stone for more involved studies on fish populations. Wide access to the rapidly evolving noncoding mitochondrial control region (mtCR; also referred to as the “D-loop”) of fishes was promoted by Lee et al. (1995) and mtCR is now the workhorse of intra-specific phylogeography. MtCR tends to evolve more rapidly than most markers accessed via DNA sequencing technology due to its noncoding nature, the lack of a mitochondrial DNA repair mechanism in fishes, very low levels of recombination, usually uniparental inheritance, and the haploid state of mtDNA (Avise, 1994). Thus, mtCR is particularly well suited for studies that require resolution of genetic variation among populations using gene trees. Throughout this period, advances in statistical phylogenetics have been central to the reconstruction of the reliable gene trees that are central to phylogeography (Avise, 2000). In recent years, critics of mitochondrial-based studies have championed the use of nuclear molecular markers such as RAPDs, “EPIC” amplification of intron sequences, microsatellites, AFLPs, and SNPs which, notably, generate types of information similar to that of allozymes—the first molecular markers widely used to quantify connectivity between populations by determining levels of genetic similarity or gene flow. One consequence has been an increase in the number of non-tree-based analyses often co-opted from the already very well developed field of population genetics. Gene flow is usually estimated using traditional F-statistics or their molecular equivalents,
ST and
CT, derived by analysis of molecular variance (AMOVA; Excoffier et al., 1992). Though there are a number of important differences in the use of these various

PHYLOGEOGRAPHY

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F I G U R E 2-2 Schematic of patterns of biogeography, phylogeography, and speciation. In each fig. (A–D), the map shows 12 coastal populations that lie in two biogeographic provinces (purple or blue; green is land). The four symbols (triangles, squares, filled circles, and open circles) represent four distinct evolutionary groups (e.g., intraspecific clades or species). The trees in panels A–C show that the same biogeographic pattern can result from at least three phylogenetic patterns representing three modes of divergence: (A) sympatry, (B) allopatry [or peripatry], (C) mixed allopatry and sympatry. An alternative biogeographic pattern, which is inconsistent with a firm barrier to gene flow is (D) parapatric speciation. However, the biogeographic pattern illustrated in panel D also could result from allopatric or sympatric speciation that subsequently was modified by postspeciation dispersal. The probability that dispersal has modified the pattern of differentiation increases with time since divergence. Extirpation also might modify phylogeographic and biogeographic patterns. For example, extirpation of the fourth or fifth populations from the bottom in D might lead one to infer that speciation was not parapatric. A fifth pattern, not shown, is no phylogeographic structure, which might result from high gene flow. Finally, it is possible that such patterns could result from chance or lineage sorting, although these are considered unlikely—particularly if phylogenies for multiple species show concordant structure. The figures show generalized patterns along an anonymous coastline; to generate patterns specific to California, simply place a mirror along the left-hand side of the figure and look at the reflection.

markers, our goal here is not to evaluate the relative advantages of one method over another. We will rarely mention allozymes in favor of focusing, for simplicity and because of their explicit historical component, on tree-based approaches, although the strongest analyses undoubtedly will use a multitude of markers and analyses and the current emphasis on mtDNA sequence data will probably diminish in the future. Using different markers raises the issue of how to reconcile analyses that indicate different results. This issue cannot be avoided because many DNA sequence-based studies have been inspired by and directly benefited from prior analyses using allozymes (e.g., Waples, 1987) or employ multiple markers (e.g. Burton, 1998; Huang and Bernardi, 2001). In some cases, differences may be random (e.g., due to genetic drift). In others, they may reflect more orderly, deterministic processes. For example, molecular markers that evolve at different rates may

28

INTRODUCTION

provide additional information on the timing of divergence using molecular clocks. Notably, if a marker does not show any phylogeographic structure, it could be for one of two reasons. There may really be no population structure due to gene flow, or the method may be too insensitive (e.g., the marker evolves too slowly). In either case, the comparative approach is key to maximizing information, for example, about a species’ life history (e.g., Dawson et al., 2002) or about the rate of evolution. Studies of evolutionary rates often employ molecular clocks. Molecular clocks have a largely chaotic mechanism (mutation) with epigenetic modifiers (e.g., drift, selection). Their rates may vary between very closely related taxa and even within lineages (Hillis et al., 1996b). Calibration is therefore essential— ideally against a series of clear-cut, well-dated geological events each of which left indisputable molecular signatures. However, calibration can be tricky because similar geological events may

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FIGURE 2-3 Summary of some factors hypothesized to influence or be related to phylogeographic structure in

coastal California fishes. Reconstructions of coastal topography during the early-to-mid Pliocene (5–3 My BP; Riddle et al., 2000; Carreño and Helenes, 2002; Hall, 2002; Murphy and Aguirre-Léon, 2002), the early Pleistocene (2–1 My BP; Riddle et al., 2000; Dawson, 2001; Carreño and Helenes, 2002), and last glacial maximum (LGM; ice cover shown in light blue; based on Jennings et al., 1977; Vedder and Howell, 1980; USGS 1991; Álvarez-Borrego, 2002; Durazo and Baumgartner, 2002; Williams et al., 2004). The numbers 1–5 (LGM) indicate the regions discussed in this chapter: 1 Cordilleran, 2 California, 3 Pacific Baja California, 4 Gulf of California, and 5 the California Islands. Schematics of major coastal currents in the northeastern Pacific Ocean during spring and summer (summer) or fall and winter (winter; Lyle et al., 2000) overlaid on 9-km weekly composite NOAA/NASA Pathfinder Advanced Very High Resolution Radiometer (AVHRR) sea-surface temperature images for August and February, 1996, respectively (gray, no data; http://coho.coas.oregonstate.edu/Pathfinder/comp/9698.html). Finally, a histogram showing the modern-day frequency distribution of northern (pink) and southern (blue) end points of the ranges of California fishes (see Chapter 1) compared with nearshore biogeography during Pleistocene glaciation (CT, cold temperate; T, temperate; WT, warm temperate “Verdean Province”; S, subtropical-to-tropical; Addicott, 1966).

have occurred multiple times in the same place, for example, glaciation, sea-level rise, opening of the Bering Strait, or take many millions of years to complete, as for the emergence of the Isthmus of Panama, and have different effects at different stages (Lyle et al., 2000). In addition, different species may not respond in the same way to the same event. For example, geminate species pairs across the Isthmus of Panama diverged between 12 million years ago (My BP) and 3 My BP depending, in large part, on whether they occupied offshore or coastal habitats (Knowlton et al., 1993; Bermingham et al., 1997; Lessios, 1998; Donaldson and Wilson, 1999). Another is raised by the results of Craig et al. (2004), who showed that transisthmian species pairs were not sister taxa. The immense value of a well-calibrated molecular clock, however, has generated a vast literature on the subject and a number of rules of thumb (e.g., Li and Graur, 1996). For example, protein-coding regions generally evolve more slowly than noncoding regions; nDNA generally evolves more slowly than mtDNA. Thus noncoding mtDNA—the mtCR of vertebrates— is among the fastest evolving regions of DNA. Within the mtCR, the region adjacent to tRNAPro generally evolves faster than the region adjacent to tRNAPhe, and there is a highly conserved region in the middle (Lee et al., 1995). The rules of thumb also extend to absolute rates of evolution. For example, the evolutionary rate of cytochrome b (cyt b), the most sequenced marker in fishes, is generally between 1.5% and 2.5% per million years (My), but in some rare cases may be as much as 8 to 20% per My (Bowen and Grant, 1997). In

extreme cases, several factors may be invoked to explain the unusual behavior of cyt b, including errors in species identification. In general, cyt b sequence data offers a better gauge of divergence times than mtCR and thus can be used to corroborate mtCR calibrations (McMillan and Palumbi, 1995). Thus, molecular clocks can provide an indication of the relative merits of different evolutionary scenarios and might then be recalibrated to causally related events.

Case Studies Anadromous Fishes A variety of native (e.g., salmonids, sturgeons) and nonnative (e.g., American shad, striped bass) anadromous fishes occur in California. Here we focus on salmonids (table 2-1), in part due to their high conservation profile and relatively rich literature. Populations of Pacific salmon and anadromous trout (Oncorhynchus spp.) are distributed in temperate to cold waters around the Pacific Rim, where they play major roles in both marine and freshwater ecosystems. The state of California represents the current and/or historical southern limit of the range of these species and presents significant ecological challenges to species with limited thermal tolerance. Although pink (O. gorbuscha), chum (O. keta), and sockeye salmon (O. nerka) are only sporadically found in California and anadromous cutthroat trout (O. clarkii) are found only in streams from the Eel River to

PHYLOGEOGRAPHY

29

Central California to Russia Southern California to Kamchatka (all California populations are in coastal subspecies)

Central California to Russia

Oncorhynchus kisutch (coho salmon)

O. mykiss (steelhead)

O. tshawytscha

(chinook salmon)

Range of Species

Species

TA B L E 2-1

Central Valley

Central California to northern British Columbia

Anadromous

10 microsatellites

33 allozymes

18 microsatellites

California range

mtCR

50 allozymes

Marker

50 allozymes

Anadromous

Anadromous

Life History

Southern California to Washington

Central California to British Columbia California

Range Sampled

Phylogeographic Structure

Isolation by distance; three regions: (1) Klamath River to the north, (2) Russian River to the south, and (3) those in between. Central Valley and Upper Klamath distinct from coastal populations and each other; coastal populations distinct south vs. north of Klamath; multiple parallel evolution of run time in coastal and upper Klamath populations Distinct winter-run populations in upper Sacramento River

Central Valley distinct from coastal populations; coastal populations distinct south vs. north of Klamath

Gualala River/Russian River, Pt. Sur/San Simeon

Populations south of Punta Gorda are most distinctive group

Phylogeographic Characteristics of Some California Salmonids

Banks et al. (2000b)

Waples et al. (2004)

Garza et al. (2004)

Busby et al. (1996)

Nielsen (1999)

Weitkamp et al. (1995)

Reference

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the north, chinook salmon (O. tshawytscha), coho salmon (O. kisutch), and steelhead (anadromous O. mykiss) all were historically abundant and well distributed geographically in California. Human interventions have strongly affected the abundance and, in some cases, the population structure of salmon and steelhead in California (Moyle, 1994). For example, a century and a half ago, hydraulic mining transformed most of the streams in the Central Valley. During the middle of the twentieth century, the construction of high dams on major tributaries of the San Joaquin and Sacramento blocked access to historic spawning areas for spring-run chinook salmon, which historically was the dominant life-history form in the Central Valley. Smaller dams and water withdrawals have restricted access by steelhead to the lower reaches of many streams in central and southern California. Large hatchery programs, particularly in the Klamath River basin and the Central Valley, have altered population structure as a result of stock transfers and, in some cases, widespread straying of hatchery fish. In spite of these anthropogenic effects, which have led to listing the majority of California’s anadromous salmonid populations under the federal Endangered Species Act, California salmon and steelhead populations are genetically diverse, and empirical data illustrate several interesting phylogenetic and biogeographic patterns. First, coho salmon and steelhead show high levels of genetic diversity among California populations compared to similar areas in the Pacific Northwest. For example, Waples et al. (2001) reviewed extensive allozyme data for Pacific salmon and steelhead from California to southern British Columbia and, using standardized criteria, identified major genetic groups of populations in each species. Just two major genetic groups of coho salmon were identified over this large geographic area; one group included only coastal populations south of Punta Gorda (see Bartley et al., 1992). Similarly, five of the seven major genetic groups of steelhead populations identified by Waples et al. (2001) occur only in California. These results are consistent with, and provide a broader geographic context for, studies of mtDNA in California steelhead (Nielsen, 1994, 1999; Nielsen et al., 1997) that have demonstrated a high level of genetic diversity among populations. Notably, both allozyme and mtDNA diversity among steelhead populations is highest in the southern half of the state (Busby et al., 1996; Nielsen, 1999). These results refute two common perceptions regarding the origin of steelhead in southern California. First, they show that steelhead are not merely the offspring of hatchery rainbow trout. Nielsen et al. (1997) and Busby et al. (1996) showed that southern steelhead are not genetically similar to any hatchery populations of rainbow trout that have been sampled. Second, they show that these populations are not part of a large, relatively homogeneous metapopulation that opportunistically invades streams with ocean access in years when environmental conditions are favorable and numbers are abundant. Genetic divergence among populations in both mtDNA and nuclear DNA is much too large to be consistent with this hypothesis. In addition to the high degree of divergence among California steelhead populations, Nielsen (1994) also reported high mtDNA haplotype diversity within populations. This was particularly true in the area south of Point Conception, where many haplotypes occur that have not been found in populations to the north. Nielsen (1999) believes this pattern is not consistent with the hypothesis that southern steelhead are a result of simple range extension by northern populations following the last glaciation; instead, she has argued that the data

support Behnke’s (1992) hypothesis for a separate Pleistocene refuge for O. mykiss, perhaps in the Gulf of California, and that the current population structure reflects secondary contact by two divergent lineages. Low genetic diversity and derived haplotypes in northern, glaciated areas relative to more southerly areas, as reported for several salmonids (Danzman et al., 1998; Turgeon and Bernatchez, 2001; Brunner et al., 2001), has been interpreted as support for this type of scenario. However, preliminary data on microsatellite variation in California steelhead (Garza et al., 2004) indicate that levels of nuclear gene diversity increase with latitude, and stronger evidence for recent bottlenecks is found in populations from the southern part of the state. Additional analyses and perhaps additional sampling will be required to disentangle the apparently complex history of anadromous O. mykiss in the southern part of the species’ range. Genetic data also provide important insights into the evolution of life-history diversity in California chinook salmon. Salmon populations are typically characterized by the time of year at which adults enter freshwater (e.g., spring-run fish enter freshwater in the spring, whereas fall-run fish remain in the ocean until later in the year). Table 2-2, which summarizes data for a gene diversity analysis of chinook salmon (Waples et al., 2004), illustrates a pattern described earlier by Utter et al. (1989) and Myers et al. (1998): in coastal areas and in the lower Columbia River, the majority of the genetic differences are explained by geography (differences among areas within geographic provinces or among samples within areas) rather than run timing. As a result, spring-run and fall-run populations from the same coastal river typically are more similar genetically to each other than either is to populations of similar run timing from other river basins. In these areas, therefore, springand fall-run populations do not form discrete, monophyletic lineages; instead, the two life-history forms appear to have evolved independently many times through a process of parallel evolution (Waples et al., 2004). In contrast, in the interior Columbia River, spring- and fall-run chinook salmon form two very divergent genetic lineages, and in these regions (mid Columbia, Upper Columbia, Snake River), run-timing differences explain most (74–94%) of the total gene diversity (GSP) within each province (table 2-2). In the interior Columbia River, therefore, run-timing differences have a much more ancient origin, perhaps predating the last episode of glaciation. A possible explanation for the contrasting coastal and interior patterns is that coastal basins are not large enough to provide strong and persistent reproductive isolation between run types, whereas the extensive Columbia-Snake basin does provide opportunities for geographic isolation of run types. For example, in the Snake River basin, the spring chinook salmon spawn and rear in high-elevation (up to 2000 m) upper tributaries, well isolated from the mainstream spawning fall-run populations. In California, joint analysis of geographic and run-time variation for chinook salmon is possible in the Klamath and Sacramento basins. Both allozyme (Myers et al. 1998; Waples et al. 2004) and nuclear DNA (Banks et al. 2000a,b) data show that chinook salmon from the Klamath River basin follow the “coastal” pattern above, and that geography is a stronger determinant of genetic differences than run timing (table 2-2; 4% of GSP is due to differences in run timing). In the California Central Valley, the pattern of genetic variation does not perfectly follow either the coastal or inland template. The overall level of genetic differentiation is modest compared to other regions (GSP  0.018 for the Central Valley compared to GSP  0.09–0.16 in the interior Columbia), but a substantial fraction (39%; table 2-2) is attributable to differences among

PHYLOGEOGRAPHY

31

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TA B L E 2-2

Hierarchical Gene Diversity Analysis of Chinook Salmon in the Western United States

Region California Central Valley Klamath Mts. Oregon/Wash. Coastal Lower Columbia Mid-Columbia Upper Columbia Snake River Georgia Basin

GSP

Run/ Province

Area/ Run

Sample/ Area

0.018 0.055 0.038 0.050 0.131 0.164 0.091 0.064

38.9 3.6 10.5 32.0 76.5 93.9 73.9 12.3

5.6 85.5 31.6 42.0 9.8 2.4 7.6 41.5

55.6 10.9 57.9 26.0 13.6 3.6 18.5 46.2

NOTE : Values in hierarchy columns are the percent of the total within-province gene diversity (GSP) that is explained by that hierarchical level. Modified from Waples et al. (2004).

populations with different run times. Furthermore, all of the fall- and late-fall run populations from both the Sacramento and San Joaquin basins form a single genetic lineage that is well differentiated from all the native spring-run populations and the single remaining winter-run population (Winans et al., 2001; Banks et al., 2000a,b; Hedgecock et al., 2001). Thus, the Central Valley is the only area in the United States outside the interior Columbia where there is evidence for the monophyletic origin of different run types. However, the absolute level of divergence among run types is small, suggesting either a relatively recent origin or incomplete isolation. A monophyletic origin of the spring-run populations is not well established. It is also possible that sampling current populations in this area does not accurately assess historical evolutionary relationships. Prior to about 1850, spring-run chinook salmon were very abundant in the upper tributaries of the San Joaquin system, but they were decimated by placer mining in the latter half of the nineteenth century. Subsequently, the construction of dams on the lower reaches of all major San Joaquin streams blocked access to historical spawning and rearing areas of spring chinook salmon. Therefore, it is possible that genetically divergent spring-run chinook salmon evolved in high-elevation tributaries of the San Joaquin system but were extirpated before modern genetic sampling commenced. It may be possible to test this hypothesis in the future if scales or other archived material that will yield DNA from these populations exists and can be analyzed. Finally, analysis of ocean harvest of tagged fish shows that California populations of coho and chinook salmon tend to remain in the productive waters south of Cape Blanco, southern Oregon, rather than migrating along the continental shelf northward to British Columbia and Alaska, as do most populations originating north of Cape Blanco (Myers et al., 1998; Weitkamp et al., 1995; Weitkamp and Neely, 2002). Not surprisingly, genetic data for most anadromous Pacific salmonids also show strong genetic differentiation across Cape Blanco (summarized by Waples et al., 2001). Thus, in addition to occupying distinctive freshwater habitats, California salmon populations also have a distinctive marine ecology. In summary, the current population structure of California salmon and steelhead reflects a balance of several forces. Whereas many areas of the Pacific Northwest became habitable only after the Wisconsin glaciation, i.e., within the last 15,000 years, salmon and steelhead have had a continuous presence over a much longer time in California habitats, thus

32

INTRODUCTION

providing ample opportunities for divergence. On the other hand, high temperatures and seasonally low and variable flow rates in California streams present extreme environmental challenges to anadromous salmonids in the southern extent of their ranges. Environmental conditions have become even more challenging in the last century as a result of human pressures. These considerations suggest two hypotheses regarding population structure of anadromous salmonids in California. (1) Genetic and demographic linkages among salmonid populations in California may be fundamentally different than in areas to the north. California populations may have evolved the ability to persist in relatively strong isolation at relatively low numbers, perhaps by developing ways to dampen natural fluctuations in abundance. (2) The current population genetic structure may not reflect historical, equilibrium conditions; instead, it may reflect a relatively recent and rapid genetic drift caused by habitat fragmentation and population bottlenecks. Under this scenario, the population structure may be in a state of decay. These hypotheses should be testable in the near future through careful design of experiments that use highly polymorphic molecular markers in conjunction with field observations.

Coastal Marine and Estuarine Fishes C OR DI LLE RAN R E G ION

Influence of Glaciations

Northern hemisphere glaciation initiated during the Pliocene, approximately 2.6 My BP (Lyle et al., 2000). The Pleistocene (1.8 My BP–10 Ky BP) was characterized by over a dozen glacial episodes (Dawson, 1992). During the last glacial maximum (LGM; fig. 2-3), the Cordilleran ice sheet extended south to Puget Sound and sea surface temperatures (SSTs) off northwestern North America were substantially cooler—estimates range from 3.3°C ( 1.5°C) to 6°C off Oregon depending on the source (Lyle et al., 2000)—than at present. In general, the impression of glacial cycles is one of unremitting cold forcing organisms further and further south during glacial advance, contrasted by uncovering of a denuded landscape ripe for colonization by species advancing northward during glacial retreat. Then the cycle repeats, erasing what went before. Such a monolithic scenario is expected to have left behind genetic signatures—derived haplotypes and low genetic diversity—that differentiate recently established northern populations from their ancestors to the south (fig. 2-3A).

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As mentioned above, some evidence of these patterns exists in several salmonids in Canada and the northern United States (Danzman et al., 1998; Turgeon and Bernatchez, 2001; Brunner et al., 2001). However, the intensity and likely effects of different glacial, interglacial, and interstadial periods varied (Dawson, 1992; Lyle et al., 2000), as did the regional effects. For example, the Younger Dryas (
11–10 Ky BP) was almost as cold as but much shorter than the LGM, the Cordilleran ice sheet displaced organisms westward as well as southward, and some places within the limits of the ice sheet remained relatively unscathed (Williams et al., 2004; fig. 2-3 LGM). The same studies of the salmonids also indicated the occurrence of glacial intrusions and refugia (Danzman et al., 1998; Turgeon and Bernatchez, 2001; Brunner et al., 2001). Studies of marine fishes (table 2-3) have revealed similarly mixed evolutionary histories consistent with a complex history in the north. For example, northern clingfish, Gobiesox maeandricus, which occur from Baja California to Alaska, occur in two distinct mitochondrial clades: one is characterized by low haplotype diversity and includes only individuals from the Strait of Georgia, the other has high haplotype diversity and representatives in all populations. These genetic patterns indicate an unglaciated refugium in the Strait of Georgia where fish survived and maintained ancient haplotypes while surrounded by areas of unsuitable habitat (Hickerson and Ross, 2001; figs. 2-4A, 5A). Two distinct mtCR clades are also evident in painted greenling, Oxylebius pictus, and occur at significantly different frequencies in populations along a north–south axis, consistent with ancient glacial vicariance (fig. 2-6). The painted greenling data set, however, also demonstrates that episodic glaciations periodically expose the population structure they generate, if any, to other influences that may maintain or erode it. The two mitochondrial clades in painted greenling, for example, are equally represented in all populations bar the most northerly and most southerly populations (in which they occur in significantly different proportions (1.0/0.0 and 0.25/0.75, respectively), indicating high levels of gene flow following secondary contact. In this case, glaciation appears to have had a long-lasting effect on molecular diversity but a somewhat transient effect on population structure. Oceanographic Influence and Pelagic Larval Duration (PLD)

Population differentiation in rosethorn rockfish, Sebastes helvomaculatus, also indicates restricted gene flow in the northeastern Pacific (Rocha-Olivares and Vetter, 1999). Given this coastal species’ deep-water habitat, the structure seems unlikely to be attributable to vicariance caused by glaciation, although this cannot be ruled out during colder climes they may have inhabited shallower water and reduced genetic diversity in Alaskan populations is consistent with postglacial northward expansion (Rocha-Olivares and Vetter, 1999). Rather, the genetic heterogeneity between populations of rosethorn rockfish from Alaska (Fairweather and Sitka,) and those from further south (Vancouver Island, Oregon, California;
CT  0.22, p  .001) has been attributed primarily to patterns of larval dispersal, particularly with reference to the divergence of the North Pacific Gyre into the northward flowing Alaskan Current and southward flowing California Current in the vicinity of the Aleutian–Oregonian provincial boundary (fig. 2-3). Similar genetic structure has been reported in algae (Lindstrom et al., 1997) and mtDNA of moon jellyfish (Dawson and Jacobs, 2001), but this is by no means a ubiquitous pattern (e.g., Debenham et al., 2000). Dover sole

(Microstomus pacificus) and shortspine thornyhead (Sebastolobus alascanus) show no population structure in the region. Although the absence of structure could indicate recent postglacial colonization, the associated high haplotype and nucleotide diversity in this case are more likely to indicate a long history of high gene flow (Stepien, 1995, 1999; Stepien et al., 2000; see also Hedgecock, 1994 for an analysis of barnacles). The extremely long, 1 year, PLD of Dover sole and shortspine thornyhead may explain why these species also do not show genetic heterogeneity across the proposed biogeographic boundary between Aleutian and Oregonian provinces (Rocha-Olivares and Vetter, 1999). Plurality of Influences and Commonality of Effects

Comparison of these studies raises several issues. First, the same geographic area has been affected by glaciation and by divergent ocean currents, probably for over 2 My. Second, both of these factors are expected to lead to population differentiation north and south of the region. Third, northward range extension, a bottleneck (in a refugium), and high PLD are all expected to result in low population structure, although the genetic signatures of each should vary. Fourth, evolutionary changes are contingent on those changes that preceded them. Thus, multiple influences can have common effects on phylogeographic structure and it may be difficult to distinguish among them. The same influence may also vary through time, such as in glacial cycles, but also in the weakening and strengthening of the North Pacific Gyre (Maruyama, 2000) and its changing latitude (on seasonal and other timescales; e.g., Lyle et al., 2000). Of course, a multiplicity of variable influences with a common effect and others that maintain or erode that effect, or even generate a different effect, probably does reflect the true evolutionary history of species in this region (Rocha-Olivares and Vetter, 1999). Thus, an evolutionary tension is established among various factors with a suite of possible outcomes, depending on the chain and intensity of events, and it is these things we are interested in deciphering. In these cases from the Cordilleran region, however, it is still difficult to distinguish among most of the probable causes.

CA LI FOR N I A

Tectonism and Its Influence on Oceanographic Patterns

“Pacific” coastlines are tectonic coastlines. Tectonism, with its many consequences including orogenesis (mountain formation), erosion, changing catchment areas, and coastal uplift, has been the single most important factor shaping California’s coastline; it has also influenced climate, ocean currents, and the distribution of habitat. The entire coast of California has been affected by tectonism with potentially important biotic consequences—for example, Tomales Bay, where the San Andreas Fault flooded, may form a warm-water refuge for some species (McCormick et al., 1994). Here, we will focus our attention on southern California where the suite of factors in which we are interested is best documented. For the last several millions of years, coastal southern California has been uplifted approximately 1 km My1 (Vedder and Howell, 1980; Sorlien, 1994). Uplift radically changed the structure of the coast (fig. 2-3). For example, the California Channel Islands probably emerged less than 5 My BP as a result of changing tectonic movements (Atwater, 1998) forming a channel off Ventura; the Palos Verdes peninsula became a

PHYLOGEOGRAPHY

33

1 to 2 months planktonic larvae, fecundity 104–105 Planktonic larvae,

Deep ocean slopes Deep ocean slopes

Microstomus pacificus (Dover sole) Sebastolobus spp. (thornyheads) Gobiesox maeandricus (northern clingfish) Shallow rock reefs

Subtidal rocky shore surface to 50 m

Estuaries and coastal lagoons (no marine phase)

Subtidal rocky shore surface to 40 m

Estuaries

Oxylebius pictus (painted greenling)

Embiotoca jacksoni (black perch)

Eucyclogobius newberryi (tidewater goby)

Embiotoca lateralis (striped seaperch)

Fundulus parvipinnis (California killifish)

Rocky intertidal

Planktonic larvae

Kelp beds and rock reefs to 50 m

Sebastes atrovirens (kelp rockfish)

Planktonic larvae

Live bearing, phylopatric, fecundity 18–92, longevity 6–10 years

Eggs brooded in burrows,
3 d planktonic larvae, later stages are benthic, fecundity 102–103, longevity 1–3 years

Live bearing, phylopatric, fecundity 8–60, longevity 4–10 yrs

Territorial, demersal eggs, 1–3 mo planktonic larvae

Planktonic larvae, fecundity 105, longevity 20 yrs

Planktonic larvae in estuaries and nearshore waters, fecundity 300– 1200, longevity 1–3 yrs

Estuaries

Clevelandia ios (arrow goby)

3 to 6 wks planktonic larvae, juveniles estuarine, coastal adults, longevity 30 yrs, fecundity 105–106

Life History*

Nearshore: to 183 m, within 6 km of shore

Habitat and Depth

Paralichthys californicus (California halibut)

Species: Fishes

TA B L E 2-3

Santa Barbara to south of Punta Eugenia

Alaska to Punta Banda

California

Fort Bragg to south of Punta Eugenia

British Columbia to Pta. San Carlos

Bering Sea to San Diego Bering Sea to San Diego Alaska to Monterey

Monterey to San Diego

mtCR

mtCR

nDNA (CK6)

mtCR, cytochrome b

Allozyme loci mtDNA (CR)

9 allozyme loci

mtCR

mtCR

mtCR

Morphology (tympanic spines)

mtCR

mtCR

Monterey to Bahia Magdalena

Central and southern California

15 allozyme loci

Marker

LA and San Diego

Range Sampled

Phylogeographic Characteristics of Some Pacific Coastal California Fishes

Pta. Eugenia

Bernardi and Talley (2000)

Bernardi (2005)

Dawson et al. (2001)

mtDNA: LAR  MB/PtB  Big Sur  SC/PtA  Seacliff; nDNA none.

LAR

Waples (1987) Bernardi (2000)

Davis et al. (1981)

Hickerson and Ross (2001)

Stepien et al. (2000)

Stepien (1999)

Love and Larson (1978)

Dawson et al. (2002)

Hedgecock and Bartley (1988) Dawson (2001)

Reference

Yes across Punta Eugenia LAR  Pta. Eugenia  BigSur/MB

Monterey Bay/Sta. Barbara

Two clades: Strait of Georgia / other pops

None

None

Sta. Barbara/San Diego

None

Weak (Punta Eugenia?)

Significant at 2 loci

Phylogeographic Structure

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Intertidal to 30 m

Rocky inter-/subtidal to 20 m

To depth 50 m larvae inshore? Shallow water to 136 m, larvae inshore-offshore Shallow water to 61 m, larvae inshore-offshore Larvae mostly inshore Larvae in/offshore; Rocky reef, kelp, intertidal to 85 m

Larvae inshore/offshore Neashore to 50 m

Anoplarchus purpurescens (high cockscomb)

Clinocottus analis (wooly sculpin)

Alloclinus holderi (island kelpfish)

Caulolatilus princeps (ocean whitefish)

Chromis punctipinnis (blacksmith)

Paralabrax clathratus (kelp bass)

Semicossyphus pulcher (California sheephead)

Medialuna californiensis (halfmoon)

Gibbonsia spp (kelpfishes)

LA Region to south of Pta. Eugenia Monterey Bay to Guadalupe Is.

2mo. larvae inshore fecundity 102–103

LA Region to south of Pta. Eugenia Pacific/Gulf

LA Region to south of Pta. Eugenia

LA Region to south of Pta. Eugenia

LA Region to south of Pta. Eugenia

LA Region to south of Pta. Eugenia

Monterey Bay to south of Pta. Eugenia

Puget Sound to San Luis Obispo

Monterey Bay to south of Pta. Eugenia

LA Region to south of Pta. Eugenia San Luis Obispo to Bahia Ascuncion

Range Sampled

(continued)

Few months in plankton? fecundity 105

4 weeks in plankton? Fecundity 105, longevity 30–34 years 37 to 78 days planktonic larvae, fecundity 3*104 to 3*105, longevity 20–29 yrs

Few months in plankton? fecundity 105

Few months in plankton? Fecundity 105, longevity 13 years

Brief larval stage, fecundity 103

Benthic eggs; nearshore, few wks planktonic larvae, fecundity 102–103

Benthic egg mass, larvae in shallow water for few days

Planktonic larvae, estuaries and nearshore waters,

Several months-long planktonic larvae, fecundity 105

Life History*

mtCR, mitochondrial control region; nDNA (CK) nuclear Creatine Kinase intron.

Estuaries, lagoons

Gillichthys mirabilis (longjaw mudsucker)

NOTE :

Nearshore, shallow reefs

Habitat and Depth

Girella nigricans (opaleye)

Species: Fishes

TA B L E 2-3

40 allozyme loci

Evidence of divergent forms on Guadalupe Is.

None

None

mtCR

26 allozyme loci

None

None

None

None

None 1 locus significant, FST  0.2

San Simeon/Pt. Conception Significant with distance

Weak break at Monterey Bay

26 allozyme loci

26 allozyme loci

26 allozyme loci

26 allozyme loci

26 allozyme loci

10 allozyme loci 26 allozyme loci

2 allozyme loci morphology

nDNA (CK7)

mtDNA: Break at or between LAR and/or Pta. Eugenia nDNA - none.

Pta. Eugenia

mtCR

cytochrome b

None

Phylogeographic Structure

26 allozyme loci

Marker

Stepien and Rosenblatt (1991)

Waples (1987)

Bernardi et al. (2003)

Waples (1987)

Waples (1987)

Waples (1987)

Waples (1987)

Waples (1987)

Swank (1979) [weak] Waples (1987)

Sassaman and Yoshiyama (1979)

Huang and Bernardi (2001)

Terry et al. (2000)

Waples (1987)

Reference

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FIGURE 2-4 Phylogenetic trees expected to result from two different evolutionary histories.

A. Vicariance, in this case involving a northern glacial refugium, although similar patterns could result from isolation of warm-water species in a refugium in, say, Tomales and Monterey Bays. Colored circles show the mitochondrial haplotypes used to reconstruct the phylogeny; note that they represent only a small portion of the evolutionary history of the species (see fig. 2-5A) and that some extant haplotypes may remain unsampled. B. Northward expansion resulting from, for example, climate warming that might result from deglaciation at high latitudes or northward movement of isotherms at lower latitudes. These patterns might also be reversed, indicating southward expansion or a cold-water refugium in the south, or occur on an east–west axis, consistent with colonization or isolation involving, for example, the Sea of Cortez.

permanent terrestrial feature only approximately 1 My BP (Nardin and Henyey, 1978; Ward and Valensise, 1994); the Los Angeles Region (LAR) remained fully or partially submerged; and Redondo Canyon did not exist until approximately 0.7 My BP (Nardin and Henyey, 1978; Vedder and Howell, 1980; Davis et al., 1989). These changes inevitably affected the distribution of habitat and local environmental conditions. For example, uplift of the California Channel Islands and numerous submerged banks reduced exchange between the Southern California Bight and surrounding oceanic and coastal waters (Owen, 1980) increasing the mean residence time (currently about 314 days; Hickey, 1992) and facilitating a warming of surface waters in the Bight (e.g., Caldeira and Marchesiello, 2002). Reduced flow along the mainland coast likely was effected largely by constriction of a narrow seaway between the Northern Channel Islands and Point Hueneme but was also contributed to by the Palos Verdes peninsula which now interrupts longshore drift, causes eddies and localized upwelling, and modifies wind and wave patterns. The emergence of LAR during the Late Pleistocene eradicated much coastal habitat such as estuaries at the feet of the hills that now surround Los Angeles (fig. 2-6 of Vedder and Howell, 1980) although, at the same time, some replacement estuaries developed along the new coastline (as indicated by the currently submerged canyons at Redondo, Santa Monica, and Point Heuneme). Uplift of LAR also probably opened shortened migratory routes or allowed secondary contact between previously isolated shallow-water coastal fish populations north and south of LAR. Tectonism also influenced weather patterns in California with effects recorded in coastal waters (Lyle et al., 2000). For example, a low deposition event, indicating low productivity, in the California Borderlands during the late Miocene to early Pliocene may be linked to the initiation of San Andreas fault motion around 6 My BP. Uplift of the Sierra Nevada mountains, from 2km elevation 3 My BP to 3 km elevation now, apparently

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INTRODUCTION

trapped additional precipitation over western California contributing to increased sediment load out of the mountain range from the Pliocene to the Holocene. Interestingly, these sediments accumulated in the Central Valley “Lake Clyde” (SarnaWojcicki, 1995) until approximately 0.5 My BP when the lake emptied, as indicated by an increase in predominant particle size and rate of sedimentation (Lyle et al., 2000). Analogous changes likely accompanied building of the Santa Ynez and other mountain ranges in southern California. Climate Change, Sea Level, and Coastal Conditions

Periods of glaciation likely exacerbated many of the effects of tectonism. Glacially lowered sea level would have rapidly increased the mass of islands in the Southern California Bight, further constricting seaways such as those between the Northern Channel Islands and Point Hueneme, inevitably altering coastal hydrography (Lindberg and Lipps, 1996) and possibly isolating some basins (e.g. Lyle et al., 2000). Lowered sea level also led to increased coastal erosion (Lyle et al., 2000). Although trends across the region are similar, signals also differ considerably between locales, indicating variation within the region, for example, in erosion and deposition (e.g., Lyle et al., 2000). As in the Cordilleran region, glacial cycles affected more southerly regions, as is evident in, for example, records of depressed SSTs. Some floral and faunal planktonic assemblages suggest that sea surface and air temperatures of southern California were considerably cooler (e.g., 6–10°C) during some Pliocene and Pleistocene glaciations than at present (Powell, 1994; Mortyn et al., 1996; Davis, 1999). Abundances of the leftcoiling foram Neogloboquadrina pachyderma have been posited to indicate SST in the California Borderlands as much as 8°C cooler than present (i.e. about 7–8°C SST at LGM, approximately the same as off Oregon now; Kennett and Venz, 1995; Thunell and Mortyn, 1995). However, these extreme temperatures have been disputed because these plankters also occur in

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FIGURE 2-5 Schematic representations of the matrilineal inheritance and sorting of mitochondrial DNA, a complicated demographic, ecological, and evolutionary process of which we see only a small fraction in reconstructed phylogenies (compare panel A with fig. 2-4A). Five hypothetical patterns are shown; large gray branches represent prior evolutionary history, faint blue shading indicates the original range, black lines represent matrilineal inheritance, and circles are haplotypes. A. Southward shift of range accompanying incomplete glaciation which also leaves a northern refugium;a change of color in inherited haplotypes indicates mutation. B. Northward range shift and expansion accompanying deglaciation. C. Vicariance of existing wide range due, for example, to tectonic uplift or sea level lowering. D. Shift of range from the tip of a peninsula northward along opposing coastlines leading to disjunct populations, possibly associated with deglaciation. E. Dispersal through a temporary seaway followed by vicariance due, for example, to tectonic uplift, leads to disjunct populations. Note that similar patterns may also result from other processes in different regions. Modified from Grant and Waples (2000) and Avise (2000).

abundance associated with SSTs of 12°C (Lyle et al., 2000 and references therein) and other reconstructions of SST concomitantly estimate less extreme conditions, only 2–3°C cooler than present (Herbert et al., 1995; Yamamoto et al. 2000; OstertagHenning and Stax, 2000). It is possible that the extreme estimates from plankton represent relatively short excursions

that influenced highly vagile organisms or extralimital observations (Muhs et al., 2002), as El Niño events influence extralimital observations today, but were not matched by redistribution of other less vagile organisms such as the vast majority of coastal invertebrates. It is also possible that changes were moderated considerably in nearshore waters, such as those

PHYLOGEOGRAPHY

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graphic conditions appear to have persisted in the area for at least the last 3.5 My BP, although conditions were not constant. (The disparity in SST between Oregon and central California, for example, suggests that the California Current flow weakens during glacial maxima, decreasing to
60% of its strongest flow compared to strong interglacials [Lyle et al., 2000]). Therefore, at least during a few of the cool Pleistocene highstands, the Oregonian-San Diegan faunal boundary occurred in the vicinity of LAR (Valentine, 1958; Addicott, 1966), and faunal distributions were also similar during some periods of warmer climate (Gobalet, 2000). Preliminary analyses of a number of California fishes reveal genetic patterns that are consistent with different aspects of these historical scenarios. For example, the phylogeographic structures of the tidewater goby, Eucyclogobius newberryi, and black perch, Embiotoca jacksoni, suggest derived haplotypes and shallower evolutionary history in the north of their ranges (fig. 2-7; Bernardi, 2000; Dawson et al., 2001; see also figs. 2-4B, 2-5B). In the next section, we focus on phylogeographic patterns associated with the climatically more stable, but physically more variable, region in southern California. Phylogeography and Biogeography

F I G U R E 2-6 Molecular phylogeny of Oxylebius pictus (Bernardi, unpubl.) based on mitochondrial control region sequences from southern (La Bufadora, Baja California, Mexico; white circles) and northern (Kelvin Grove, British Columbia, and Queen Charlotte Island; black circles) individuals. Gray squares represent individuals from intermediate locations: Bodega Bay, Monterey Bay, Anacapa Island, Palos Verdes, and Point Loma).

protected by the Borderlands within the Southern California Bight (fig. 2-3); embayments contained consistently warmer water faunas than open coastal regions during cooling trends (Jacobs et al., 2004). However, the controversy over how extreme the changes were in SSTs off California during the glaciations remains far from settled. Glaciation did lead to a cooler wetter climate in southern California, increasing the flow through coastal canyons and their impact on longshore transport and local habitat and likely increasing the frequencies of catastrophic floods (e.g. Schimmelmann et al., 1998). Conversely, during drier periods, as some in the Holocene (Stine, 1990; Davis, 1999), droughts may have had equally severe impacts on coastal lagoons and wetlands. Thus, climate change presumably shifted conditions suitable for habitation to more southerly latitudes, only for them to expand northward again during interglacials. The fossil record shows that climate change did affect the distribution of coastal organisms, generally pushing faunas southward during glaciation and allowing them to expand northward during deglaciation, and that these effects were probably less extreme at lower latitudes in the eastern Pacific Ocean (Valentine, 1958; Addicott, 1966; Valentine, 1966; Johnson, 1977; Graham and Grimm, 1990; Fields et al., 1993; Mortyn et al., 1996; Davis, 1999). However, modern oceano-

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INTRODUCTION

The long-term stability of the position of departure of the massive cold California Current from the coast at Point Conception has been posited as a major factor influencing California coastal biogeography (Briggs, 1974) and phylogeography (Burton and Lee, 1994). Environmental discontinuities (ecotones) at biogeographic ‘boundaries’ are expected to inhibit movement physically, tax the physiologies of species beyond their limits, or put them at selective disadvantages resulting in limited, or in the extreme, zero realized migration across the “boundary.” Thus, much of the early work in the region focused on determining whether the Point Conception biogeographic break and genetic discontinuities of fish populations coincided. Morphological work on kelp rockfish, Sebastes atrovirens, and midshipman, Porichthys notatus (Love and Larson, 1978; Thompson and Tsuji, 1989), and early genetic work using allozymes in painted greenling, Oxylebius pictus (Davis et al., 1981), were consistent with Point Conception as a zone of genetic transition. The other major work indicating a phylogeographic break at Point Conception is a study of the invertebrate intertidal copepod Tigriopus californicus (Burton and Lee, 1994). However, further investigations of T. californicus with additional sites and markers and a review of existing data on invertebrates indicated that, although there was a small break, Point Conception was not a major region of genetic discontinuity for populations of marine species (Burton, 1998). This result has been supported by analysis of painted greenling using mtCR (Bernardi, unpubl.). In recent years, two phylogeographic studies of fish populations have focused on this region (Bernardi, 2000; Dawson et al., 2001), providing an opportunity to compare patterns between species with overlapping ranges. The first described the black surfperch, Embiotoca jacksoni, which like other species of surfperches (Embiotocidae) broods its young and displays very little dispersal potential (Bernardi, 2000). The second focused on a small estuarine gobiid, the tidewater goby, Eucyclogobius newberryi (Dawson et al., 2001), which also displays minimal dispersal potential. The patterns found in the two species were remarkably similar to each other (fig. 2-7) and with that of T. californicus (Burton, 1998). All three species showed a major phylogeographic break in the Los Angeles

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F I G U R E 2-7 Phylogeographic structure of California fishes showing discontinuities in the Los Angeles Region. A. Relationships among populations of black perch, Embiotoca jacksoni, reconstructed by neighbor-joining analyses of pairwise population Fst values (scale bar indicates Fst of 0.1; from Bernardi, 2000). B. Phylogeographic structure in the tidewater goby, E. newberryi, as indicated by maximum likelihood analyses of combined mitochondrial cytochrome b and control region (redrawn from Dawson et al., 2001). Light gray branches were not present in all reconstructions. Numbers above branches indicate percent support calculated by quartet puzzling.

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Region (LAR). Black perch populations sampled extensively in that region indicated that Santa Monica Bay was the precise area of the genetic break (see also Edmands et al., 1996). Recent extirpation of key populations of tidewater gobies in the region prevented similarly fine-scale conclusions based on genetic data, but subsequent analysis of the sensory canal system of tidewater goby in museum specimens shows an abrupt change in morphology in the vicinity of Palos Verdes (Ahnelt et al., 2004). Thus, there is strong evidence that a relatively short stretch of coastline in the LAR is the site of processes that have severely restricted gene flow in multiple coastal marine species. A review of molecular data for over 30 species reinforced the idea that this region was an important zone of genetic transition (Dawson, 2001) and, most recently, new molecular data on the striped seaperch, Embiotoca lateralis, have again revealed a pattern almost identical to that of its sister species, the black surfperch (Bernardi, 2005). Thus, at present, three species of fishes, and an invertebrate, have geographically concordant phylogeographic gaps in the LAR. Variation in the depths of these breaks suggests somewhat different evolutionary histories in these taxa. This is perhaps related to ease of extirpation, timing of original divergence, and disposition to erode breaks by subsequent gene flow, but also reinforces the view that clustering of phylogenetic gaps in this region results from long-term processes. This has left an apparent discrepancy between the placement of the traditional biogeographic boundary (at Point Conception) and phylogeographic breaks (at LAR). Such a discrepancy might conceivably result from a number of factors, including decoupling of factors influencing biogeographic and phylogeographic patterns (Burton, 1998) and the migration of boundaries with changing climate (Addicott, 1966). However, reconsideration of biogeographic data suggests that, in this case, it most probably is a misconception (Dawson, 2001). Although Point Conception is often cited as the principal biogeographic boundary in California, none of the three related measures that are often used to estimate the position of biogeographic boundaries, (1) concentrations of range termini of many widely distributed species, (2) peaks in edge-effect species, and (3) regions of high species richness (e.g., Newell, 1948; Valentine, 1966; Seapy and Littler, 1980; Longhurst, 1998; Briggs, 1974; Hayden and Dolan, 1976; Doyle, 1985) support that assignment. Rather, LAR is indicated as the site of the predominant biogeographic boundary. The range termini of fishes peaks at 33° N (Horn and Allen, 1978; and Chapter 1, this volume), and the highest densities of range termini, of “edge-effect” species, and of the most speciesrich assemblages of marine algae and mollusks occur between 33° and 34° North (fig. 2-3; Murray et al., 1980; Newell, 1948; Valentine, 1966; Murray and Littler, 1980). The number of 1° species, species-richness, and the number of range terminations are fewer, and usually considerably fewer, between 34° and 35°N, the degree of latitude that encompasses Point Conception (Newell, 1948; Valentine, 1966; Horn and Allen, 1978; Murray and Littler, 1980). In retrospect, the implication of LAR, rather than Point Conception, as the site of long-term barriers to gene flow makes some sense. Though Point Conception has been a relatively stable coastal feature associated with the California Current and changes in dominant plankton for millions of years (Maruyama, 2000), which might reflect suitable conditions for stable long-term differences to arise, it is also associated with features that could inhibit or break down such patterns. Point Conception is part of an open coastline along which relatively quick currents flow in opposite directions at

40

INTRODUCTION

different times of year and from which eddies are frequently shed into the Santa Barbara Channel, i.e., it is a point that would seem to foster relatively high gene flow. In contrast, during the last several millions of years—the timescale we are dealing with in the evolution of structure in surfperches and tidewater goby—coastal southern California has undergone dramatic metamorphoses that likely would limit genetic exchange in coastal marine taxa. Other Areas in California

Lesser genetic heterogeneities occur elsewhere in California, most notably in the Monterey Bay Region (e.g. Bernardi, 2000; Dawson et al., 2001) consistent with distributional evidence of a secondary biogeographic discontinuity also linked to physical discontinuities attributable to tectonism, oceanography, and habitat distribution (Dawson, 2001). As such, we suggest that these lesser breaks result from a subset or suite of processes similar to those in the LAR, but perhaps less severe, and therefore do not discuss them in detail here.

B A J A CA LI F O R N I A

Geological, Geographic, and Oceanographic Setting

The eastern Pacific coastline at approximately the modern latitudes of Baja California, circa 30 My BP, had features reconcilable with the modern geography of the peninsula (Helenes and Carreño, 1999). The late Oligocene also saw the tectonic movements that presaged the formation of peninsular California which had begun to separate from mainland Mexico by the middle Miocene, as indicated by the establishment of a protogulf. The peninsula has resembled its current configuration for over 5 My (Helenes and Carreño, 1999: Carreño and Helenes, 2002; fig. 2-3). Modern eastern North Pacific oceanographic conditions were probably established by the middle Miocene and certainly by the late Miocene (Helenes and Carreño, 1999, and references therein). This is indicated by Pacific coast deposits and biogenic sediments from an inland sea east of the forming peninsula characterized by mixed temperate and tropical flora and fauna that may have entered via a central transisthmian seaway (Helenes and Carreño, 1999, and references therein). The Pacific coast of Baja California is characterized by long stretches of sandy coastline occasionally fragmented by rocky outcrops. One of the major geographic features of the region is Punta Eugenia (
28°N; fig. 2-3), approximately halfway between the peninsula’s northern and southern ends, like a large barb on an otherwise straight hook. At Punta Eugenia, the California Current from the north meets a warmer current from the south which, in association with the San Benito islands just off shore from Punta Eugenia, creates a complex oceanography in the region. A massive estuary complex (Ojo de Liebre) lies just north of Punta Eugenia, and a very long stretch of sandy shore lies to the north of Ojo de Liebre. The southern portion of the Baja California Peninsula has very large bays and estuaries, Bahía San Ignacio and Bahía Magdalena. The latter corresponds to the transition zone between the San Diegan biogeographic province and the Panamic biogeographic province (Chapter 1). Thus, we will not discuss the features of Bahía Magdalena and its southern Panamic fauna beyond noting that this probably has been the site of this boundary, approximately, on and off for quite some time.

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Climate Change

Current evidence indicates that climatic excursions associated with glacial cycles may not have been large in Baja California. The distributions of fossil fauna indicate that the warmtemperate Verdean Province probably occupied much the same range as its Holocene analog, the San Diegan Province (Addicott, 1966; Fields et al., 1993; fig. 2-3). Thus, the northern extent of the Magdalenan region—the region of overlap between San Diegan and Panamic provincial faunas—may have been relatively stable, perhaps in the vicinity of Punta Eugenia, 28°N (Addicott, 1966; fig. 2-3). Analyses of fossil molluscan assemblages, which are most strongly indicative of distributions during interglacials, show peaks in the number of end points and 1° endemics at 27–28°N (also at 30°N and 25°N; Valentine, 1966). Although there was also an accumulation of end points at 23°N, there was no concomitant peak in 1° endemics (Valentine, 1966). This fits with arguments that the southern extent of the Magdalenan region, where the Verdean Province is supercsded by the northern limit of the tropical Panamic fauna, may have migrated from its currently recognized position at Magdalena Bay southward past the tip of Baja California Sur and then north again with each glacial cycle. On the whole, however, biogeographic zones along the Pacific coast of Baja California probably changed little, at least compared to regions further north (Fields et al., 1993). Part of this stability was likely due to the reduced influence of the California Current this far south, whose weakening during the latest Miocene and Pliocene did have considerable effects on SST, recorded in diatom assemblages, north of Point Conception and evident at least as far south as 30–31°N (Maruyama, 2000). Analogous events probably also occurred more recently (Pisias, 1978). For example, the weakening of the California Current occurred during high latitude warming (Barron, 1981; Muhs et al., 2002), conditions resembling modern El Niño patterns [including reduced upwelling] (Maruyama, 2000). Consequently, an idea of the potential effects in more southerly parts of Baja California during this period can be gleaned by examining oceanographic changes from the 1980s and 1990s (Hernandez-Trujillo, 1999; Durazo and Baumgartner, 2002; see also Schwing et al., 2002).

P HYLO G EO G RAP HY

Conceptually, the area of Punta Eugenia is similar to Point Conception and the LAR. For example, it is an obvious geographic feature that strongly influences local oceanography, and adjacent regions are physiographically quite distinct. Punta Eugenia also has been proposed as the site of an important biogeographic break. The obvious question then, is whether phylogenetic gaps are concordant with a biogeographic break at Punta Eugenia. DNA sequence data pertinent to this question are available from six species of fish: the California killifish (Fundulus parvipinnis), opaleye (Girella nigricans), black perch (Embiotoca jacksoni), longjaw mudsucker (Gillichthys mirabilis), spotted sand bass (Paralabrax maculatofasciatus), and sargo (Anisotremus davidsonii). In all cases, genetic discontinuities were found across Punta Eugenia (figs. 2-8 and 2-9; but see Tranah and Allen, 1999). Due to sometimes limited geographic sampling, however, it is difficult to determine precisely where discontinuities occur (or even to exclude the alternative of isolation by distance) and, therefore, which factors may have been the dominant

influence. Though the lack of habitat in itself could contribute to the separation, as has been hypothesized for biogeographic discontinuities in other regions (Hastings, 2000; see Chapter 1), it is not yet possible to distinguish its contribution from that of ocean currents in the region, although coastal fishes show lower gene flow than offshore fishes (Waples, 1987; Waples and Rosenblatt, 1987), suggesting a role for nearshore processes. Only samples of the estuarine California killifish were obtained at Ojo de Liebre and, in this case, the genetic discontinuity was found between the Ojo de Liebre population and the one south of Punta Eugenia at La Bocana (fig. 2-8; Bernardi and Talley, 2000). Though this implicates Punta Eugenia as a potentially important factor in generating phylogeographic structure, it does not exclude other influences within that
200 km stretch of coastline. More work is obviously needed in the region.

G U LF OF CA LI FOR N I A

Evolutionary Setting

Much of the pertinent information regarding the geography, climate, and sea level of Baja California was discussed in the previous section. These include a hypothesized, relatively stable biogeographic structure on the Pacific coast of the Peninsula for the last several millions of years, with the exception of the southern limit of San Diegan taxa, which may have extended well south of Cabo San Lucas during periods of glaciation. To interpret genetic patterns in the region, a few additional details are necessary, specifically those pertaining to the opening of the Gulf of California, and possible routes of communication with the Gulf from the eastern Pacific (fig. 2-3). The rift valley that became the Gulf of California is first evident in the middle Miocene, approximately 12 My BP (Helenes and Carreño, 1999). Marine deposits with mixed tropical and temperate floras and faunas in a central protogulf sea suggest similar oceanographic conditions in the Pacific Ocean and a transisthmus seaway in the vicinity of San Ignacio by the late Miocene,
8 My BP (Carreño and Helenes, 2002). By this time, the protogulf had extended and reached depths of at least 150 m (Helenes and Carreño, 1999). A separate marine embayment also formed south of the protogulf (Helenes and Carreño, 1999). The Gulf of California in its modern configuration was probably largely established around 5–4 My BP when the protogulf and southern embayment merged, opening the mouth of the Gulf (Helenes and Carreño, 1999; Carreño and Helenes, 2002). More than 40 fish species have been described as disjunct across the Baja California peninsula, in the northern Sea of Cortez versus Pacific Baja California and/or California (Present, 1987). However, only 19 species, representing a highly variable assemblage of taxonomic and ecological groups encompassing 14 families, are unequivocally disjunct. Each of the disjunct species is absent or rare in the warmer southern waters of the Cape region (Cabo San Lucas), and the majority exhibit morphological differences between Gulf and Pacific coast populations (Walker, 1960), although differences are usually small and often limited to color variations. Questions of the origin, relationships, and divergence among the disjunct species have stimulated molecular investigations into levels of genetic isolation (Crabtree, 1983; Orton and Buth, 1984; Present, 1987; Terry et al., 2000; Huang and Bernardi, 2001) and can be framed in the context of specific dispersal/vicariance hypotheses (Avise, 2000; Grismer, 2000). The restriction of disjunct species to the northern colder waters of

PHYLOGEOGRAPHY

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F I G U R E 2-8 Mitochondrial control region (D-loop) gene tree for Fundulus parvipinnis (from Bernardi and Talley,

2000). Labels correspond to sampling localities as follows (from north to south): north of Punta Eugenia: Carpinteria Slough (CAS), Newport Bay (NEB), Mission Bay (MIS), Bahia San Quintin (BSQ), Ojo de Liebre lagoon (ODL), and south of Punta Eugenia: La Bocana (BOC). The tree is rooted using Fundulus lima as an outgroup. Bootstrap support higher than 70% is shown above the nodes (for the neighbor-joining method) and below the nodes (for the maximum parsimony method).

the Gulf of California may have resulted from two different processes: (1) dispersal during periods of oceanic cooling associated with glacial events (between 1 My BP and 10,000 BP; Brusca, 1973) or (2) vicariance with the closing of Neogene transisthmus waterways connecting the Gulf of California to the Pacific (1 My BP; Riddle et al., 2000a,b,c). Furthermore, on the basis of geological, biogeographic, and molecular analyses of terrestrial fauna (Walker, 1960; Murphy, 1983;

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INTRODUCTION

Grismer, 1994; Upton and Murphy, 1997; Carreño and Helenes, 2002; Murphy and Aguirre-Léon, 2002), three scenarios for dispersal via Neogene waterways have been posited. One, a Pliocene (
5-3 My BP) seaway connecting the northern Gulf of Mexico to the Pacific Ocean around Ensenada. Two, a Pliocene (
4-3 My BP) seaway connecting the southern Gulf of Mexico to the Pacific Ocean around La Paz. Three, a Pliocene (5 or 3 [but not 4] My BP) or middle Pleistocene

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(ca. 1 My BP) seaway connecting the central Gulf of Mexico to the Pacific Ocean south of Punta Eugenia and north of Santa Rosalia (fig. 2-3). These scenarios generate specific hypotheses regarding the evolutionary histories of fishes in this region that can be tested using the phylogeographic approach (e.g., fig. 2-5C,D). Phylogeography

Molecular analyses of 12 disjunct species (table 2-4), using allozyme, RFLP, and DNA-sequence data, revealed two distinct patterns of phylogenetic relationships. The first pattern, evident in eight species, was of distinct Gulf and Pacific clades (fig. 2-9A) between which there were many fixed differences (0.97  Fst  0.51; 0.01 Nm 0.48); sequence divergences between Gulf and Pacific populations varied from 1.06% to 11.6% in mtCR and from 1.34% to 2.21% in cytochrome b (table 2-5). The second pattern, evident in the remaining four species, was of indistinct Pacific and Gulf populations (0.00 Fst 0.02; Fig. 2-9B; table 2-5). These two major patterns between Gulf and Pacific populations may reflect, respectively, vicariant events (fig. 2-7A) or high levels of gene flow (fig.-7B). However, questions remain as to the timing of vicariant events and whether apparent gene flow reflects recent massive dispersal or ongoing dispersal at lower levels. Of the eight species showing fixed differences between the Gulf and Pacific, populations of three—blue-banded goby, spotted bass, and orangethroat pikeblenny—were separated by relatively small genetic distances. Using rule of thumb molecular clocks, genetic divergence (table 2-5) between Gulf and Pacific populations were estimated to have occurred between 120,000 and 600,000 years ago in spotted bass (Stepien et al., 2001; but see Tranah and Allen, 1999), 200,000 to 900,000 years ago in orangethroat pikeblenny, and 200,000 to 400,000 years ago in blue-banded goby. The similarity of both pattern and estimated times of divergence suggests that these three species were affected by common extrinsic mechanisms compatible with a Pleistocene separation of disjunct populations (Stepien et al., 2001). But the actual divergence time of Pacific and Gulf populations (which will be smaller than molecular estimates of divergence times [e.g. Knowles, 2004]) may postdate even the most recent transisthmian seaway, making expansion around the cape during glacial periods then separation as populations shift northward during subsequent warming the more likely cause of disjunction (Tranah and Allen, 1999). Populations of the five species that showed higher levels of sequence divergence (opaleye, grunion, sargo, mussel blenny, and longjaw mudsucker) including many fixed differences, are likely to have separated much earlier (Bernardi et al., 2003). Using molecular clocks, the times of divergence between Gulf and Pacific populations have been estimated at 0.76–2.3 My BP (longjaw mudsucker, Gillichthys mirabilis; Huang and Bernardi, 2001), 0.3–2.2 My BP (opaleye, Girella nigricans; Terry et al., 2000), 1.3–2.6 My BP for sargo, 0.3–2.0 My BP for mussel blenny, and 0.4–3 My BP for grunion (Bernardi et al., 2003). While the lower end of the potential divergence times is again consistent with Pleistocene separation of disjunct populations after dispersal around the cape, the upper limits are more compatible with vicariance due to closure of more ancient northern transpeninsular seaways 3–1 My BP (e.g., Upton and Murphy, 1997; Riddle et al., 2000a; fig. 2-3). Thus, although geological evidence may leave room for interpretation (Carreño and Helenes, 2002; Jacobs et al. 2004), biological data on terrestrial (Murphy and Aguirre-Léon, 2002) and marine faunas strongly

indicate a midpeninsular, Pliocene–Pleistocene, transpeninsular seaway and, interestingly, as has happened before (Rudwick, 1985), may prove to be the decisive evidence. The issue could be further elucidated by comparing the genetic affinities of fishes from north of Punta Eugenia, central Baja (say, between Natividad and Laguna San Ignacio), the southernmost Pacific populations, and their Gulf counterparts. A suite of alternate hypotheses can be tested, including (1) if fish dispersed around the cape, the southernmost Pacific and Gulf populations should be most similar and genetic distances small; (2) if populations were connected via a recent midpeninsular seaway, then central Pacific Baja and Gulf populations should be most similar and genetic distances intermediate; and (3) if populations were connected via an older northern (or alternatively southern) seaway, Gulf and northern (or alternatively southern) Pacific Baja populations should be most similar and genetic distances large. No species studied to date clearly distinguish among these hypotheses. For example, considering G. mirabilis, Gulf populations are more similar to populations north of Punta Eugenia (1.9%) than south of Punta Eugenia (2.3%; Huang and Bernardi, 2001), but genetic distances between central Pacific and Gulf populations are consistent with the timing of the midpeninsular seaway (see above); yet, this population south of Punta Eugenia also shares haplotypes with Gulf populations consistent with recent dispersal around the cape (fig. 2-9a); moreover, human introduction also cannot be discounted (Huang and Bernardi, 2001). Irrespective of the route, the similarity of phylogeographic patterns among opaleye, longjaw mudsucker, sargo, mussel blenny, and grunion, together with similar times of divergence among disjunct populations (1.3–2.6 My BP for sargo, 0.3–2.0 My BP for Mussel blenny, 0.4–3 My BP for grunion) suggest that broadly similar historical processes shaped the population structures of these species (Bernardi et al., 2003). CA LI FOR N IA I S LAN DS

Studies of islands have been central to the growth of ecological and evolutionary sciences for almost 150 years (Darwin, 1859; Wallace, 1880; MacArthur and Wilson, 1967; Grant, 1998). The patterns and processes of evolution by natural selection and genetic drift continue to be elucidated by seminal ecological and evolutionary studies of insular faunas inhabiting oceanic islands, freshwater lakes, headwaters and tributaries, and mountaintops and forests (e.g., Grant, 1998). The Theory of Island Biogeography (MacArthur and Wilson, 1967) contributed to and stimulated major advances in ecology, evolution, biodiversity, and conservation biology (Hubbell, 2001) and is merging with other key areas such as metapopulation dynamics (Matter et al., 2002). However, studies of marine taxa that are heavily invested in island biogeographic theory are rare (e.g. Thomson and Gilligan, 2002). In part, this may be because the recent paradigm of marine dispersal did not foster an “island” perspective. For several decades, the oceans were typically thought to be large, essentially well-mixed, interrelated units with few barriers to gene flow and few discrete islands of habitat (Palumbi, 1992, 1994). However, this perspective is changing, and reports of structure in marine organisms, particularly coastal animals, are becoming increasingly common, as in this chapter. It is therefore reasonable to ask whether studies of islands can also make large contributions to the knowledge of patterns of evolution in marine taxa. There are several series of islands off Pacific North America, including the Farallon Islands, California Channel Islands, San Benito Islands, and Guadalupe Island (plus the islands of

PHYLOGEOGRAPHY

43

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F I G U R E 2-9 Parts a and b. Phylogenetic relationships of populations of fishes disjunct across the Baja California peninsula. Phylogenetic rela-

tionships were based on a portion of the mitochondrial cytochrome b gene for Lythrypnus dalli, Gillichthys mirabilis, and Anisotremus davidsonii and on a portion of the mitochondrial control region for all remaining species. Each individual is represented by a circle, white if collected in the Sea of Cortez, black if collected on the Pacific coast north of Punta Eugenia, and gray if collected on the Pacific coast south of Punta Eugenia. Trees with large numbers of individuals were pruned to facilitate presentation but retain their principal elements (Gillichthys mirabilis, Girella nigricans, Paralabrax maculatofasciatus, and Sebastes macdonaldi). Figure modified from Bernardi et al. (2003).

Pacific/Gulf

Planktonic larvae 37 to 78 days planktonic larvae, fecundity 3*104 to 3*105, longevity 20–29 yrs

Intertidal to 70 m

Rocky reef, kelp, intertidal to 40 m Rocky reef Rocky reef, intertidal to 27 m Larvae in/offshore; Rocky reef, kelp, intertidal to 85 m

Lythrypnus dalli (bluebanded goby)

Halichoeres semicinctus (rock wrasse)

Sebastes macdonaldi (Mexican rockfish) Hermosilla azurea (zebraperch) Semicossyphus pulcher (California sheephead)

Chaenopsis alepidota (orangethroat pikeblenny) Hypsoblennius jenkinsi (mussel blenny)

Pacific/Gulf

Planktonic larvae

Eggs buried in sandy beaches; rocky reef to 18 m

Leuresthes tenuis/sardina (grunion/gulf grunion)

Planktonic larvae Planktonic larvae

Rocky reef Rocky reef

Planktonic larvae, longevity 9–14 yrs

2 to 3 months planktonic larvae, fecundity 102–103, longevity 19–24 months

30 to 40 days planktonic larvae, fecundity 1000– 3000, longevity 3–4 yrs

2–4 months planktonic larvae, longevity  10 yrs

Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

LA Region to south of Pta. Eugenia Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

allozymes mtCR

mtCR

mtCR

mtCR

mtCR

mtCR

cytochrome b

26 allozyme loci

mtCR

mtCR

cytochrome b

Pacific/Gulf

Rocky reef, intertidal to 30 m

cytochrome b

RFLP mtCR

Marker

Pacific/Gulf

Girella nigricans (opaleye)

Planktonic larvae, longevity 12–15 yrs Planktonic larvae, estuaries and nearshore waters,

Rocky reef, intertidal to 60 m Estuaries, lagoons

Pacific/Gulf

Range Sampled

Anisotremus davidsonii (sargo) Gillichthys mirabilis (longjaw mudsucker)

18 to 31 days planktonic larvae, fecundity 5*104, longevity 9–15 years

Life History*

Sand/rocky reef

Habitat and Depth

Paralabrax maculatofasciatus (spotted sand bass)

Species

TA B L E 2-4

Pacific/Gulf

Pacific/Gulf

None

None

None

None

2 of 3 polymorphic loci significant, FST 0.2 Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

Pacific/Gulf

Phylogeographic Structure

Phylogeographic Characteristics of Some Coastal Fishes Disjunct Across the Baja Peninsula

Present (1987) Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Waples (1987)

Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Bernardi et al. (2003)

Tranah and Allen (1999) Stepien et al. (2001)

Reference

GRBQ065-2067G-CO2[26-54].qxd 11/8/05 8:40 PM Page 45

Gillichthys mirabilis Anisotremus davidsonii Lythrypnus dalli

Hermosilla azurea Halichoeres semicinctus Semicossyphus pulcher Sebastes macdonaldi

Gobiidae Haemulidae Gobiidae

Kyphosidae Labridae Labridae Scorpaenidae

Zebraperch Rock wrasse California sheephead Mexican rockfish

Longjaw mudsucker Sargo Bluebanded goby

Grunion Opaleye Mussel blenny Orangethroat pikeblenny Spotted sand bass

Common Name

mtCR mtCR mtCR mtCR

CYTB CYTB ALLO/CYTB

ALLO/mtCR ALLO/mtCR ALLO/mtCR mtCR ITS, mtCR

Method

15 21 20 95

63 26 254/10

NA/11 24/119 200/7 11 180/63

n

0.003

0.28 0.99 0.04

D

0.02 0.01 0.01 0.01

0.67 0.65 0.71

0.97 0.51 0.84 0.67 0.81

Fst

28 38 115 602

0.2 0.3 0.2

0.1 0.5 0.1 0.3 0.1

Nm

(0.39) (1.70) (0.61) (0.14) (0.26)

2.30 0.79 0.84 0.64

(1.28) (0.41) (0.59) (0.25)

2.21 (0.51) 1.34 (0.17) 0.20 (0.07)

11.60 8.49 7.87 1.87 1.06

%div Pac/Gulf

(0.25) (4.58) (0.38) (0.10) (0.14)

2.33 0.68 0.76 0.55

(1.50) (0.44) (0.61) (0.29)

0.69 (0.48) 0.30 (0.31) 0.00 (0.00)

0.29 5.77 0.44 0.04 0.15

%div Pacific

(0.26) (1.43) (0.00) (0.28) (0.30)

2.32 0.89 0.91 0.53

(1.34) (0.38) (0.50) (0.26)

0.72 (0.60) 0.65 (0.48) 0.11 (0.09)

0.31 2.58 0.20 1.16 0.25

%div Gulf

NOTE : Methods are ALLO  allozymes, mtCR  mitochondrial control region sequences, ITS  ITS RFLPs, CYTB  cytochrome b sequences. n is sample number (if more than one method is used, sample number refers to each method). D is Nei’s genetic distance. Divergences are given as percentage sequence divergence; the standard deviations are in parentheses. Seven of the unequivocally disjunct taxa have not yet been studied: Hypsoblennius gentilis (Blenniidae, bay blenny), Pleuronichthys verticalis (Pleuronectidae, hornyhead turbot) Zalembius rosaceus (Embiotocidae, pink seaperch), Scorpaena guttata (Scorpaenidae, scorpionfish), Stereolepis gigas (Polyprionidae, giant seabass), Xeneretmus ritteri (Agonidae, stripefin poacher), and Hypsopsetta guttulata (Pleuronectidae, diamond turbot). Citations to studies are given in table 4.

Leuresthes tenuis, L. sardina Girella nigricans Hypsoblennius jenkinsi Chaenopsis alepidota Paralabrax maculatofasciatus

Species

Atherinopsidae Kyphosidae Blenniidae Chaenopsidae Serranidae

Family

TA B L E 2-5

Genetic Characteristics of Coastal Fishes Disjunct Across the Baja Peninsula

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the Gulf of California). The intraspecific evolution of fishes of the California Channel Islands and San Benito Islands has been investigated with genetic tools in the last two decades. In both cases, early work indicated that offshore islands harbored divergent populations. The original study of the San Benito Islands indicated that island populations were more genetically divergent from populations on the adjacent mainland, the Baja California peninsula, than were other populations along the Pacific coast of the Baja California peninsula separated by much greater geographic distances (Waples, 1987). The indication is that something about islands (biological and/or physical) can lead to isolation in coastal marine fishes, as in terrestrial and freshwater organisms, and therefore that island biogeographic theory might also be relevant. Below, we elucidate processes influencing islands as well as possible by reviewing and exploring the data set describing black perch in the California Channel Islands (Bernardi, 2000). Geologic, Geographic, and Oceanographic Context for California Channel Islands

The California Channel Islands comprise three groups of islands. The first group in the north includes four islands, San Miguel, Santa Rosa, Santa Cruz, and Anacapa, which are currently separated from each other by narrow channels generally shallower than 50 meters. The second group in the south comprises three islands, San Nicolas, San Clemente, and Santa Catalina, which are separated from each other and from the northern group by wide, deep-water channels; the shallowest point is approximately 800 meters deep. The third group comprises several small islets and rocks generically referred to as Santa Barbara Island. It is centrally located halfway between the two previous groups and is separated from them by deep water. During the last several millions of years, the California Borderlands have been uplifted approximately 1 m per millennium (Vedder and Howell, 1980; Sorlien, 1994). The California Channel Islands emerged within the last 5 My and have generally increased in area since. The islands are thus relatively new structures that have changed within the evolutionary timescale of many of the lineages discussed above. Climate change also has been considerable during this period, and lowered sea level rapidly increased island mass in the Southern California Bight with several results (see section on California) of which two are of particular interest here. First, the seaway between Anacapa Islands and the mainland was reduced to approximately one-sixth of its current (6 km) breadth (Johnson, 1977). Second, the shallow shelf between the four northern Channel Islands—Anacapa, Santa Cruz, Santa Rosa, and San Miguel—was exposed thus generating the superisland Santarosea (Johnson, 1978). These changes almost certainly influenced the hydrography of the Southern California Bight, likely reducing connectivity with the California Current to the west and diminishing northward flux in the California Counter Current. Increased island mass would also have affected mesoscale patterns within the Bight. Depending on their area, shape, elevation, and orientation to prevailing winds, currents, and swell, islands modify local circulation, including the formation of boundary layers, mesoscale eddies, and modification of vertical water-column structure (e.g. Wolanski and Hamner, 1988; Wolanski et al., 1996), which can influence local productivity (Caldeira and Marchesiello, 2002), have knock-on effects through the food web (Lasker, 1975), and might entrain larvae near discrete habitat patches in the vicinity of their natal area for up to

several weeks (e.g. Owen, 1980; Black et al., 1990; Hickey, 1992; Scheltema et al., 1996; Pinca and Huntley, 2000; Strub and James, 2000). Relationships Between Mainland and Island Populations

As a group, Channel Island black surfperch individuals cluster with samples collected north of Santa Monica Bay (fig. 2-7A). This is consistent with prevailing southward currents in the region. More specifically, however, fish from the northern Channel Islands clustered with fish from Ventura-Port Hueneme-Point Dume, i.e., the geographically closest region of the mainland. This genetic connection probably was greater during periods of lower sea level when Santarosae was separated from the mainland only by a much reduced seaway (Vedder and Howell, 1980; Junger and Johnson, 1980), thus explaining the observed high genetic similarity between northern Channel Islands and the Ventura region. These observations are consistent with island biogeographic theory regarding mainland and connectedness along island series. In contrast, in general, individuals from the southern channel islands did not cluster with individuals from the mainland closest to them (Palos Verdes-San Diego region) but, like the northern Channel Islands, with areas to the north. Only one individual from the southern islands, from Santa Catalina Island the island closest to the mainland, showed a strong affinity with fish from the adjacent “southern” mainland clade. Another single individual from Ventura showed close affinity with Catalina haplotypes. The closer genetic affinity of the southern Channel Islands with the northern Channel Islands, rather than nearest mainland, is largely consistent with prevailing currents in the region (fig. 2-3). The California Current washes over and through the northern islands, presumably picking up potential migrants as it heads toward the southern islands. In contrast, the southern California Countercurrent runs northward out of the open ocean or along the mainland coast and therefore tends not to carry potential migrants or, at least, not to the islands. Relationships among the California Channel Islands

Within the Channel Islands, mitochondrial control region sequences of fish from the northern Channel Islands (San Miguel, Santa Cruz, and Anacapa) were all very closely related (mean pairwise divergence
0.3%, haplotype diversity
0.58), even on north- and south-facing shores that show striking differences in habitat conditions, forming a monophyletic clade (figs. 2-5A and 2-8). One dominant haplotype was shared by 65% of individuals from all northern islands. Gene flow between islands within the northern group was therefore high (average Fst
0.05, Nm
39.1). In contrast, individuals collected from the more isolated southern islands (San Nicolas, Santa Catalina, and San Clemente), showed high levels of haplotype diversity (0.86) and grouped in two well-separated clades (average pairwise distance was 0.97%). Individuals from the offshore San Clemente and San Nicolas Islands grouped together, distinct from all individuals from the inshore Santa Catalina Island. No haplotypes were shared between these two clades, resulting in very low levels of gene flow (Fst = 0.59; Nm = 0.32). Although San Nicolas and San Clemente Islands were remarkably homogeneous (genetic diversity was 0.38 and 0.00, respectively), Santa Catalina Island showed the highest diversity of all island populations (0.80). The population on the smallest of the Channel

PHYLOGEOGRAPHY

47

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F I G U R E 2-10 Embiotoca jacksoni. Superimposed map of the California Channel Islands and a simplified (polymorphisms were removed) neighbor-joining phylogenetic tree of the corresponding island populations of black surfperch. Each sample is represented by a circle. Black circles represent individuals from the northern Channel Islands, open circles represent individuals from the southern islands, and gray circles represent individuals sampled in Santa Barbara Island. Samples from Santa Barbara Island were found clustered with northern Channel Islands (9 individuals) and with San Nicolas/San Clemente Island individuals (3 individuals). One individual from Santa Catalina Island clustered with mainland individuals. Santa Rosa Island was not sampled (Bernardi, 2000)

Islands, Santa Barbara Island, which lies between the northern and the southern group, did not show any unique haplotypes, it was composed of northern Channel Islands (75%) and southern Channel Islands (25%) haplotypes (fig. 2-10). Although the small sample size may have an effect on these data, the higher proportion of haplotypes that originated from the northern group is consistent with the general southward current pattern between the islands (Hickey, 1992). Moreover, because the island is very small, the local population of black perch may be prone to replacement. The absence of unique haplotypes on Santa Barbara Island may be due to high rates of extirpation and recolonization due, for example, to environmental stochasticity, consistent with island biogeographic theory (Matter et al., 2002). The dynamics of E. jacksoni may therefore be amenable to modeling using metapopulation models and population genetic expectations of island biogeographic theory (Johnson et al., 2000). Deep and Wide: Water as an Effective Barrier to Gene Flow

The high genetic similarity of all northern Channel Island individuals, their close association with haplotypes from the adjacent mainland, and their high degree of separation from southern Channel Island individuals suggests that deep water is an effective barrier to gene flow for black perches. The bimodal distribution of FST values (0.2 or 0.4) with respect to geographic distance (fig. 2-11) bears hallmarks of the sigmoidal relationship proposed between genetic differentiation and geographic isolation, assuming that dispersal over a certain distance is a particu-

48

INTRODUCTION

larly rare event (fig. 2-1; blue curve), of which fishes on Santa Barbara Island may constitute particularly recent examples (Bernardi, 2000) leading to anomalously low genetic differentiation at high geographic distances (and vice versa). Though black perch are probably able to migrate between the different northern islands, their access to the southern islands is most likely via rafting in association with floating debris or kelp patties that provides cover against predation. The frequency of rafting is very low, as indicated by fish collection efforts that failed to detect the presence of black perch in rafts of giant kelp, Macrocystis pyrifera (Mitchell and Hunter, 1970; Kingsford, 1995 [for a genetic study of kelp that shows interisland and ecological differences, see Miller et al., 2000]). That occasional dispersal events do occur, however, is indicated by the capture of one southern mainland haplotype at Catalina Island, one Catalina haplotype at Ventura, and the occurrence of only shared haplotypes at Santa Barbara Island (Bernardi, 2000). Thus, the pattern of predominantly different clades on different islands suggests that, though dispersal potential and physical environment are likely to play a role in population structure, the incumbent biota and subsequent demographic effects also influence successful establishment. The indication that deep marine water can act as a barrier to dispersal by shallow water marine fish such as the black surfperch, can be added to its list of isolating effects on organisms already including animals restricted to freshwater, such as Hawaiian gobies (Chubb et al., 1998) and many terrestrial animals, including the miniature California Islands mammoth (e.g. Johnson, 1977; Gilbert et al., 1990; Edwards, 1993; Thorpe et al., 1993; Clarke et al., 1996; Grant and Grant, 1996; Juan et al., 1998; see also Lessios et al., 1998).

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F I G U R E 2-11 Genetic differences among California Channel Island

populations of black surfperch, Embiotoca jacksoni, in relation to A, the shortest geographic distance between populations (y  0.0037x  0.1095, r 2  0.29), and B, the shortest distance in line with predominant circulation in the Southern California Bight (y  0.0038x  0.0643, r 2  0.39). The lines of best fit differ significantly in their intercepts (F  67.54, p  .001) but not slope (F  2.06, p  .218). Solid squares, comparisons between Northern Channel Islands only; hollow circles, comparisons with Santa Barbara Island; solid circles, all other comparisons.

Rare Migrations and Founder Effects—Distant Islands

The absence of shared haplotypes among the southern islands indicates very low levels of migration (Edwards, 1993). However, migration among southern islands has occurred more recently than migration between the northern and southern islands because individuals from the southern islands are phylogenetically more closely related to each other than they are to northern island individuals (figs. 2-5, 2-8). Overall, rates of migration among the islands are negatively correlated with their geographic separation, a relationship that is improved slightly by taking into account likely routes of dispersal via currents (fig. 2-11; see also Michels et al., 2001; Muñoz et al., 2004) even though such generalized currents (inset, fig.-11B) dramatically over-simplify both the complexity of modern flow and changes in flow on evolutionary timescales. Assuming a molecular clock for mtCR of 20%/MY to 8%/MY (Bowen and Grant, 1997), populations on the southern islands have been isolated for 30,000 to 110,000 years (0.6% to 0.9% sequence divergence). If such rare migratory events reflect the main mechanism for island colonization, founder effects should dominate the early genetic structure

on islands and their signal be retained subsequently. One would expect to find single or very few very closely related haplotypes on recently colonized islands, and more numerous, more divergent, haplotypes within monophyletic clades on islands colonized for longer periods of time. This expectation is consistent with patterns observed in the southern islands but, given the low heterogeneity and highly derived nature of San Nicolas and San Clemente populations (0.38 and 0.00, respectively [Bernardi, 2000]) also suggests a role for founder effects and local bottlenecks. In this case, the higher diversity of Santa Catalina populations (0.94) indicates that the island historically has had a larger more stable population allowing endemic diversification. As well as the stochastic extinction/recolonization dynamics of small islands, as indicated by Santa Barbara and San Nicolas, changes in temperature may have led to repeated, severe, selective bottlenecks in black perch populations (Holbrook et al., 1997). In some ways, the widespread occurrence of marine taxa with limited dispersal ability on isolated islands initially seems paradoxical (Johannesson, 1988) because it is not obvious how they got there. However, it is consistent with patterns seen in the terrestrial faunas and floras of oceanic and coastal islands (Wallace, 1880; Cody and Overton, 1996) and can be explained by the fact that reduced dispersal ability favors establishment of populations after rare accidental colonization events (Johannesson, 1988). Given its viviparous birth, phylopatry, and low dispersal ability, it is no surprise, therefore, that the black perch is relatively common among the California Channel Islands.

Synthesis Dispersal Genetic studies investigating the relationship between dispersal potential and gene flow in phylogenetically disparate species with variable pelagic larval durations (PLDs) have not reached definitive conclusions (Waples, 1987; Doherty et al., 1995; Shulman and Bermingham, 1995; Grosberg and Cunningham, 2001; Riginos and Victor, 2001). Comparisons of California taxa suggested relationships between phylogeographic structure and PLD, habitat structure, and fecundity (Dawson, 2001). A comparative study of sympatric sister species in California demonstrated that the species with higher dispersal also had less phylogeographic structure (Dawson et al., 2002). This suggests that, though gene flow is related to dispersal potential, phylogeographic structure is also influenced by numerous other factors. The results reported here generally support this perspective. For example, opaleye which display a strong phylogeographic break, have a pelagic larval stage of 2 to 4 months (Waples, 1987). Spotted sand bass and blue-banded goby (Lythrypnus dalli), which display a shallow phylogeographic break, have a pelagic larval stage of approximately 1 month and 2 months, respectively (Waples, 1987). Sheephead (Semicossyphus pulcher) and rock wrasse (Halichoeres semicinctus), which show no phylogeographic break, have a pelagic larval stage of 37 days and 30 days, respectively (Victor, 1986). Thus, understanding geographic structure demands a more holistic approach, which may begin by looking in more detail at deviations from hypothesized relationships between dispersal potential and gene flow (e.g., fig. 2-1).

PHYLOGEOGRAPHY

49

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Vicariance

Future Directions

Deviations from the relationship between dispersal potential and realized gene flow indicate the influence of other factors. One obvious factor is the traditionally juxtaposed phenomenon of vicariance. Sigmoid relationships (e.g. fig. 2-1; consider also fig. 2-11) would be consistent with a certain intensity of a barrier to gene flow below which structure is unlikely to form and above which structure is likely to form. The critical intensity is unlikely to be the same for different species and is probably affected by the many factors previously discussed. The idea that modifiers of gene flow are not all-or-nothing is more consistent with the idea of zootic filters (Carlquist, 1965) that inhibit the movement of individuals of different species, and therefore their genes, to different extents depending in part on the strength and nature of the filter, and in part on the attributes of the entity being filtered (see also Mayr, 1942:243). Undoubtedly, the strongest filters, which are functional barriers for marine organisms, are land bridges, isthmuses, and long peninsulas such as Baja California, but other significant filters clearly exist and are likely to operate in concert. The influence of reduced gene flow linked to vicariant events is evident in Gulf and Pacific fish population disjunctions, across the LAR, in the north due to currents and glaciation, and to a lesser extent among the California Channel Islands. Sometimes the mechanism of the filter may be difficult to identify because physical and ecological factors may often be superimposed.

We have attempted to summarize the phylogeographic patterns that have been described for California fishes and to elucidate the principal factors that influence them. In the light of the apparent complexity of factors influencing the modern genetic structure of organisms, what we find remarkable about these patterns is that they are so similar for many different species, suggesting that the comparative approach can be informative of predominant patterns and processes. However, it is also clear from this review that, for the most part, studies to date lack the necessary resolution and experimental design to distinguish among the many potential influences that often overlap geographically. Distinguishing among these factors will require more thorough geographic sampling and choices of species that will maximize information retrieval (e.g., groups of closely related species within monophyletic clades that are broadly sympatric and possess a variety of life-history traits, with replication). Such study systems may be few and far between, but they are one possible way that we may learn more about the generalities of the processes influencing evolution in coastal marine fishes. This endeavor will also depend on greater knowledge of the geological and climatic history of the region, as well as better oceanographic information and models. The theoretical and analytical foundations, often based on such information, must also continue to be developed. For example, despite advances in statistical phylogeography (see Knowles, 2004) and quantification of coastal complexity methods for statistically integrating molecular with biogeographic and environmental information are still relatively poorly developed and would be helpful in this field.

Sympatry Ecological effects are probably easiest to investigate in sympatric species or in geographically proximate but ecologically separated con-specific populations between which there is no obvious physical reason for a lack of gene flow. Since the early development of the idea (Bush, 1969), evolution in sympatry has become more widely considered as a possible component of speciation and is currently the subject of much theoretical and empirical work (Bush, 1994; Kondrashov and Kondrashov, 1999; Dieckmann and Doebeli, 1999; Schilthuizen, 2001). In this context, the most interesting species discussed in this chapter are the chinook salmon in coastal streams, the lower Columbia River, and Klamath River basin, in which spring- and fall-run populations appear to have evolved independently multiple times in close geographic proximity (Myers et al., 1998; Banks et al., 2000a,b).

Evolutionary Consequences—Speciation Recent evidence based on molecular phylogenetics and distributional data, following the arguments of Lynch (1989) and others, suggests that some species of California fishes may have evolved sympatrically, possibly in relation to microhabitat colonization, i.e., via ecological speciation (Dawson et al., 2002; Bilton et al., 2002; McKinnon et al., 2004). Though divergence in sympatry is now generally accepted as a real mode of speciation, it is likely that allopatric speciation has an essential role and is probably the most common mechanism for incipient speciation in disjunct species (Endler, 1977). However, there are still relatively few studies that have evaluated the role of population disjunctions in the speciation of marine organisms (Stepien and Rosenblatt, 1991; Palumbi, 1992, 1994; Hellberg, 1998; Burton, 1998).

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Acknowledgments This publication would have been impossible without the Editors’ vision that a synthesis of the ecology of California marine fishes was necessary and without the unusually rich history of coastal research in California indicated by the many diverse publications we were able to cite. This collaboration/ review was made possible by the organizations and people who have contributed financially, intellectually, and otherwise to our prior researches on this topic. MND was supported by a Vice-Chancellor’s Post-doctoral Research Fellowship at the University of New South Wales. GB was funded by UC Mexus, the Committee on Research at UCSC, and the David and Lucille Packard Foundation’s PISCO program. We would like to thank Pete Raimondi, Nicole Crane, David Huang, Astrid Terry, Stian Alesandrini, Karen Crow, and Marina Ramon for their contributions to this research.

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Turgeon, J., and L. Bernatchez. 2001. Clinal variation at microsatellite loci reveals historical secondary intergradation between glacial races of Coregonus artedi (Teleostei: Coregoninae). Evolution 55:2274–2286. Upton, D. E., and R. W. Murphy, 1997. Phylogeny of the side-blotched lizards (Phrynosomatidae: Uta) based on mtDNA sequences: support for a midpeninsular seaway in Baja California. Mol. Phyl. Evol. 8: 104–113. USGS. 1991. CAORWALL: Bathymetry for the California, Oregon, Washington EEZ: open-file report 91-396, United States Geological Survey, Reston, VA. http://coastalmap.marine.usgs.gov/GISdata/ regional/westcoast/bathymetry/caorwall.zip Utter, F., G. Milner, G. Stahl, and D. Teel. 1989. Genetic population structure of Chinook salmon in the Pacific Northwest. Fish. Bull. US 85:13–23. Valentine, J. W. 1958. Late Pleistocene megafauna of Cayucos, California, and its zoogeographic significance. J. Paleontol. 32:687–696. Valentine, J. W. 1966. Numerical analysis of marine molluscan ranges on the extratropical northeastern Pacific shelf. Limnol. Oceanogr. 11:198–211. Vedder, J. G., and D. G. Howell. 1980. Topographic evolution of the Southern California Borderland during Late Cenozoic time, pp. 7–31. In: The California Islands: Proceedings of a Multi-Disciplinary Symposium, D. M. Powers (ed.). Santa Barbara Museum of Natural History, Santa Barbara, USA. Victor, B. C. 1986. Duration of the planktonic larval stage of one hundred species of Pacific and Atlantic wrasses (family Labridae). Mar. Biol. 90:317–326. Walker, B. W. 1960. The distribution and affinities of the marine fish fauna of the Gulf of California: the biogeography of Baja California and adjacent seas. Syst. Zool. 9:123–133. Wallace, A. R. 1880. Island life. Macmillan, London. Waples, R. S. 1987. A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution 41:385–400. Waples, R. S., and R. H. Rosenblatt. 1987. Patterns of larval drift in southern California USA marine shore fishes inferred from allozyme data. Fish. Bull. 85:1–12. Waples, R. S., D. J. Teel, J. Myers, and A. Marshall. 2004. Life history divergence in chinook salmon: historic contingency and parallel evolution. Evolution 58:386–403. Waples, R. S., R. G. Gustafson, L. A. Weitkamp, J. M. Myers, O. W. Johnson, P. J. Busby, J. J. Hard, G. J. Bryant, F. W. Waknitz, K. Neely, D. Teel, W. S. Grant, G. A. Winans, S. Phelps, A. Marshall, and B. Baker. 2001. Characterizing diversity in Pacific salmon. J. Fish Biol. 59(Suppl. A):1–41. Ward, S. N., and G. Valensise. 1994. The Palos Verdes terraces, California: bathtub rings from a buried reverse fault. J. Geophys. Res. 99:4485–4494. Weitkamp, L., and K. Neely. 2002. Coho salmon (Oncorhynchus kisutch) ocean migration patterns: insight from marine coded-wire tag recoveries. Can. J. Fish. Aquat. Sci. 59:1100–1115. Weitkamp, L. A., T. C. Wainwright, G. J. Bryant, G. B. Milner, D. J. Teel, R. G. Kope, and R. S. Waples. 1995. Status review of coho salmon from Washington, Oregon, and California. U.S. Dept. of Commerce, NOAA Tech. Memo. NMFS-NWFSC-24. Williams, J. W., B. N. Shuman, T. Webb III, P. J. Bartlein, and P. L. Leduc. 2004. Late Quaternary vegetation dynamics in North America: scaling from taxa to biomes. Ecol. Monogr. 74:309–334. Winans, G., D. Viele, A. Grover, M. Palmer-Zwahlen, D. Teel, and D. Van Doornik. 2001. An update of genetic stock identification of chinook salmon in the Pacific Northwest: test fisheries in California. Rev. Fish. Sci. 9:213–237. Wolanski, E., and W. M. Hamner. 1988. Topographically controlled fronts in the ocean and their biological influence. Science 241. Wolanski, E., T. Asaeda, A. Tanaka, and E. Deleersnijder. 1996. Threedimensional island wakes in the field, laboratory experiments and numerical models. Continental Shelf Res. 16:1437–1452. Yamamoto, M., M. Yamamuro, and R. Tada. 2000. Late Quaternary records of organic carbon, calcium carbonate, and biomarkers from Site 1016 off Point Conception, California margin, pp. 183–194. In Proceedings of the Ocean Drilling Program, scientific results vol. 167, (M. Lyle, I. Koizumi, C. Richter, and T. C. Moore, Jr., (eds.). ODP, College Station, TX.

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CHAPTER 3

Evolution E D M U N D S. H O B S O N

Introduction Attempts to understand determinants of species composition in animal communities generally have been limited to current influences on existing communities (e.g., MacArthur, 1969; Paine, 1966; Sale, 1977, 1991). Evolutionary history is routinely ignored, often because key issues can be examined only by inference. But more than 45 years of experience with marine communities has convinced me that major determinants of species structure lie in evolutionary processes that greatly transcend the current scene. The conclusions developed in this chapter draw from my widespread studies of marine communities of California, most in collaboration with Tony Chess. Our efforts in the south were concentrated at Santa Catalina Island (e.g., Hobson and Chess, 1976, 1986, 2001; Hobson et al., 1981), whereas most in the north were along the Mendocino Coast (e.g., Hobson and Chess, 1988; Hobson et al., 2001). The chapter also incorporates a perspective gained through intensive studies of communities elsewhere, particularly in the tropical eastern Pacific (e.g., Hobson, 1968) and on tropical coral reefs of the central and western Pacific (e.g., Hobson, 1972, 1974; Hobson and Chess, 1978). Topics discussed here were the basis of two papers, Hobson (1994) and Hobson and Chess (2001). Most California coastal fishes are teleosts of the superorder Acanthopterygii (as defined by Nelson, 1994), which are characterized by skeletons of bone and fins supported by spines. This group includes the vast majority of modern fishes other than sharks and rays. Most of California’s marine teleost fishes represent a subset (series) of acanthopterygians, the Percomorpha (Nelson, 1994). More specifically, visual assessments of fish communities near the California coast invariably find more than 95% of the fishes—species as well as individuals—representing the percomorph orders Perciformes, Scorpaeniformes, or Pleuronectiformes (e.g., Ebeling et al., 1980; DeMartini and Roberts, 1990; Stephens and Zerba, 1981). According to Nelson (1994), these are three of the four most recently evolved orders of fishes. To understand the nature and basis of their dominance, one should consider certain features of teleost history. The account of teleost history that follows draws from a problematic body of knowledge, simplified here for more effective presentation. Much of the evidence comes from the

fossil record, which is notoriously incomplete and at least to some extent controversial on virtually every point. I integrate published interpretations of the data to develop a cohesive synthesis, while declining to pursue various inconsistencies and unresolved conflicts in peripheral issues that would unnecessarily cloud essential points.

Relevant Features of Teleost History Acanthopterygian teleosts represent advanced levels in the evolution of actinopterygian (“ray-finned”) fishes, which, according to Schaeffer and Rosen (1961), evolved based mainly on improvements in feeding related capabilities. They stated (p. 187), “In the main stream of actinopterygian evolution from paleoniscoid to acanthopterygian, there has been progressive improvement in a fundamentally predaceous feeding mechanism.” They also cited changes in the structure and placement of fins that improved their ability to swim and therefore to capture prey or evade predators. The history of these fishes, therefore, can be considered an evolution of feedingrelated adaptations. The main evolutionary line leading to modern acanthopterygian teleosts has been described as a succession of generalized carnivores, with each major advance producing a diverse array of specialized offshoots (Gosline, 1960). If actinopterygian evolution has been driven by trophic relations, it would follow that the “diverse array of specialized offshoots” resulted mainly from proliferation of ways to obtain food or thwart predators. The major evolutionary advances and production of specialized offshoots referred to by Gosline can be related to the global episodes of mass extinction–resurgence that have been so prominent in the history of life on the earth (Stanley, 1987).

Impact of Extinction–Resurgence Episodes The major episodes of global mass extinction–resurgence have followed a common pattern. Each has begun with a catastrophic

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event, at least some the impact of an immense asteroid or comet (e.g., Alvarez et al., 1980, McLaren and Goodfellow, 1990; O’Keefe and Aherns, 1989; Ward et al., 2001; Ellwood et al., 2003). These events created environmental conditions intolerable to significant proportions of existing species and resulted in global extinctions that led to collapse of ecosystems that had been stable for tens of millions of years. Immediately following the extinctions and loss of ecosystems have been periods of limited community development lasting some millions of years, which Fagerstrom (1987) referred to as ecological and evolutionary vacuums. Eventual resurgence from this condition has involved surviving representatives of the main evolutionary line that, though generalized in form, embodied specific highly adaptive features. These features, most involving mouth and /or fin structure, have promoted proliferation of diverse forms that filled developing niches during widespread biological resurgence toward new ecosystems. Other surviving actinopterygians failed to radiate in the new environment because they lacked the potential of mainstream species to diversify. Some of these were well adapted to specific ecological circumstances, however, and managed to persist along distinct evolutionary lines where conditions favorable for them continued to exist. We return to these later in the chapter, but for now we focus on the main line. Consider the record. It is generally recognized that there have been five major episodes of global extinction–resurgence since late in the Ordovician Period (Raup and Sepkoski, 1982), and all can be related to major advances in actinopterygian evolution, as identified by Long (1995). The extinctions that closed the Ordovician about (
) 440 million years ago (mya) may have influenced actinopterygian origins. The earliest records of these fishes—bone fragments, scales and teeth are from Silurian deposits dated
30 million years after the Ordovician extinctions. Lacking substance and precision, this evidence can only suggest a possible connection, but relations become clearer as the fossil record improves. The second period of major extinctions came late in the Devonian (
350–375 mya) and could have promoted the radiation of paleoniscoids—the dominant actinopterygians of the late Paleozoic. This dominance lasted until the end of the Permian (
245 mya), when the greatest of all global extinctions brought the Paleozoic to a close by eliminating an estimated 80 to 95% of marine species (Erwin, 1994). Resurgence from this catastrophic episode involved radiation of early neopterygians, which dominated until the fourth major episode of extinctions closed the Triassic (
208 mya). The actinopterygian radiation that followed the end-Triassic extinctions brought advanced neopterygians into prominence. Among these were teleosts, which have become the most successful of modern fishes. The fifth major episode of extinctions came at the end of the Cretaceous (
65 mya), and can be linked to the radiation of percomorph lines that now dominate among fishes in California and elsewhere. It is significant that forms involved in postextinction radiations had been established as minor elements of communities decimated by the extinctions. Paleoniscoids, for example, are known from the Silurian and were a minor presence among other more dominant forms (e.g., placoderms and acanthodians) throughout the Devonian “Age of Fishes.” They radiated only after the late Devonian extinctions eliminated all or many members of the dominant groups. Similarly, there were early neopterygians in Permian communities, but radiation came

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only after mass extinctions ended that period. And though teleosts (which are advanced neopterygians) originated midway through the Triassic (Greenwood et al., 1966), their proliferation during the Jurassic (Gosline, 1971) came after the endTriassic extinctions. The pattern has persisted to recent times; some percomorph lines that dominate among modern fishes can be traced back into the Cretaceous but did not radiate until some time after mass extinctions and collapse of ecosystems closed the Mesozoic (Gosline, 1960; Patterson, 1964). In addition to the five major episodes of global mass extinction–resurgence, there have been at least 27 lesser episodes (Sepkoski, 1986). One that decimated reef communities at the Jurassic–Cretaceous boundary (
145 mya; Scott, 1988) has been implicated in the advance of the teleost main line to the acanthopterygian level of development (Hobson, 1994). Certainly not all extinctions and originations have occurred during episodes of mass extinction and subsequent resurgence. To the contrary, extinction and origination have been continuous throughout the history of life on the earth, probably most during intervals between global episodes. Nonetheless, in making this point, Wood (1999) went on to elaborate (p. 165): “mass extinctions are disproportionately significant in that they . . . by virtue of their speed, unpredictability and magnitude—are capable of removing dominant taxa and their habitats, which can lead to the collapse of whole ecosystems.” The removal of dominant taxa and habitats would seem the key because the continuous extinctions of ordinary times are most likely to concentrate on removing misfits during comparatively minor changes in local conditions that do not represent global threats to the environment. Because ecosystems that developed after episodes of extinction have been derived from distinctive combinations of survivors, each has been unique. Consider the involvement of actinopterygian fishes. If one accepts the proposition that actinopterygian evolution has been driven mainly by trophic relations, it follows that radiation of forms during ecosystem resurgence has been largely a proliferation of diverse feeding types and defensive structures. This means that there must also have been concurrent and rapid evolution of form and behavior among the organisms that interacted with these fishes as predator or prey. In drawing this conclusion earlier (Hobson, 1994), I reasoned that (p. 63) “ . . . evolution of feeding adaptations in predators is inseparable from the evolution of defensive adaptations in prey, the two in combination representing a developing system of coevolved offenses and defenses (Hobson, 1979). The effect . . . would spread far beyond interactions between any two organisms to include, modify and expand the trophic system.” It has been concluded that the trophic system is the primary basis for community speciesstructure (Hobson and Chess, 2001), which leads to the conclusion that resurgence from collapsed ecosystems to a large extent has involved trophic interactions among developing species. One would expect, therefore, strong affinities between specific ecosystem components.

Teleost–Scleractinia Connection Teleostean fishes concurred with scleractinian coral reefs in time and place of both first record and subsequent radiation, which suggests a common history. The earliest records of both are fossils laid down during the mid-Triassic at margins of the

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Tethys Sea, and their subsequent radiation during the Jurassic was part of a biological resurgence that followed the endTriassic extinctions (Greenwood et al., 1966; Gosline, 1971; Newell, 1971; Wood, 1999). These and later concurrences led me to propose that the main teleost line has been linked to scleractinian coral reef communities from their beginnings (Hobson, 1974). The Tethys involvement had a powerful influence on teleost– scleractinia connections, as well as on other facets of teleost evolution. An earlier manifestation of this ancient sea, surrounded on three sides by the supercontinent Pangaea, had been a major feature of the Paleozoic; however, Pangaea began to break apart midway through the Triassic—at about the time teleosts and scleractinians deposited their initial traces—and Tethys became an equatorial seaway that ultimately connected the ancestral Pacific, Indian, and Atlantic oceans (Dietz and Holden, 1970; Stanley, 1989). Remaining that way through the rest of the Mesozoic, Tethys covered much of what are now southern regions of Asia and Europe, with east–west shores that would have contained the evolution of its fauna, including teleost fishes and scleractinian corals, at lower latitudes. An opposing view held that preacanthopterygian teleosts were maladapted to reef conditions and that teleosts became reef fishes only after acquiring features that advanced the actinopterygian line to the acanthopterygian level during the Cretaceous (Smith and Tyler, 1972). This position was based mainly on the absence of fishes among fossils from early Mesozoic reefs, but Newell (1971) attributed this absence (and the absences of arthropods, polychaetes, and other organisms expected on coral reefs) to their skeletal remains being (p. 6) “systematically removed by scavengers that abound in this strongly oxidizing environment.” In contending that coral reef communities have always included fishes and certain other organisms missing in the fossil record, Newell stated (p. 6), “The history of coral reef crabs and fishes and some other groups must be inferred from the evidence provided by other preserved groups and by the circumstantial evidence of inferred relationships.” Scleractinian coral reefs thrived during most of the Jurassic but suffered extinctions late during that period and into the Cretaceous (Scott, 1988). Although fishes were not part of the fossil record that marks the decline of Jurassic reefs, it can be assumed that they were among the organisms eliminated during the process. As the corals and other organisms that had structured Jurassic reefs declined, they were replaced as dominant forms in shallow water by rudistids, a diverse group of mollusks (Kauffman and Johnson, 1988). Despite these replacements, however, teleosts remained poorly represented in the fossil record until after scleractinian corals re-established dominance on the seaward margins of reefs
15 to 20 million years into the Cretaceous (Newell, 1971). The first evidence of resurgence among teleosts comes from the mid-Cretaceous,
100 mya, and involved the earliest known percomorph acanthopterygians, representatives of the order Beryciformes (Patterson, 1993). As elements of the main teleost line, preadapted to niches characteristic of coral reef communities, these were primed to diversify when conditions suitable for the expansion of coral reefs developed. Beryciforms developed in ways similar to development at previous stages of the main actinopterygian line. Apparently their early evolution was rapid because their initial appearance in the fossil record is as a diverse group representing
25% of that period’s marine fishes (Patterson, 1993).

Perpetuating a pattern established during earlier resurgences from mass extinctions, the diversity among them was based largely on enhanced abilities to capture prey, defend against predators, or increase maneuverability—all trophic-related adaptations (Patterson, 1964). The proliferation of beryciforms produced many species that resembled modern coral reef fishes, including serranids, carangids, kyphosids, chaetodontids, acanthurids, and balistids (Patterson, 1964). The similarities were strong enough to be considered by some as evidence that modern members of these families represent lines independently derived during the Cretaceous from different lines of beryciforms (e.g., Greenwood et al., 1966). Others, however, have argued that the similarities are superficial and not indicative of phyletic relations (e.g., Gosline, 1966). No matter which view is correct, it would mean Cretaceous reef communities were shaped by the same evolutionary processes that have shaped modern communities. Despite the diversity and great success of beryciforms, most perished with the global extinctions that decimated reef communities at the close of the Mesozoic (Patterson, 1964; Gosline, 1971).

Percoids at Last At some point prior to the end-Cretaceous extinctions, a combination of minor structural changes in one or more lines of generalized beryciforms resulted in the next major advance in actinopterygian evolution—the percoid level of development (Patterson, 1964; Gosline, 1971). These changes were passed on to bass-like early “percoids,” at least some of which represented basal elements of the perciform suborder Percoidei (Patterson, 1964). The evolutionary advances evident at the percoid level were refinements of those same trophic-related features that had made beryciforms better adapted than their progenitors to reef conditions. The early percoids, therefore, represented an extension of the main actinopterygian line of generalized carnivores, which had radiated as beryciforms at an earlier evolutionary stage. The actinopterygian mainstream continued into the Tertiary as elements of the percomorph order Perciformes, but apparently it was some time before the adaptive potential of the percoid condition was realized. There is little evidence of diversity among actinopterygians through the 10 million years of the Paleocene (Patterson, 1993)—a period also characterized by lack of coral reef development (Newell, 1971). The earliest evidence of increasing diversity among actinopterygians is from late in that period and early in the Eocene (
55 mya; Patterson, 1993). If perciform percoids extended an evolutionary line with adaptive potential linked especially to coral reefs, one would expect that they lacked diversity during times lacking such reefs. In assessing the diversity among actinopterygian fossils in early Cenozoic deposits, Carroll (1988) and Choat and Bellwood (1991) concluded that the perciform radiation began during the Cretaceous and made major advances throughout the Paleocene. Although it is likely that various lineages originated during the Paleocene, I question whether there could have been a major radiation of forms during a period of limited community development. In the resurgence scenario proposed above, explosive radiation of species is inseparably linked to expanding communities. Furthermore, it could have been predicted that up to 10 or more millions of years would pass after the end-Cretaceous extinctions before there would

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be such proliferation because that has been a facet of major extinction–resurgence episodes from the beginning. A gap in the fossil record could explain the apparent absence of community development and perciform radiation during the Paleocene, but terrestrial deposits from that period provide a much better record than marine deposits, and they too lack evidence of modern vertebrates (Romer, 1966). The critical unknown is the rate at which evolution proceeds during resurgence from ecosystem collapse. Considering that beryciforms, too, were diverse when they first appear in the fossil record, probably evolution proceeds rapidly under conditions that favor ecosystem resurgence. Actinopterygians regained prominence when perciforms radiated coincident with expanding coral reef communities during early to mid-Eocene (
40–50 mya), and the result was a variety of forms characterized by features that continue to define modern coral reef fishes (Choat and Bellwood, 1991; Bellwood, 1996). The expansion of reef communities at that time also produced many new scleractinian corals, and by the Period’s end, all modern scleractinian1 families had appeared (Wood, 1999). Thus, present-day coral reef communities are extensions of communities that developed during that time. Other aquatic communities must have been stabilizing then as well, because by the close of the Eocene all major families of modern fishes had come to exist (Berg, 1940). Although the highly variable Cenozoic environments that followed had profound effects on origination, extinction, and distribution at the levels of genera and species, the major variations in morphology and presumably behavior that characterize modern teleost fishes at the family level had been set. Thus, in pondering the derivation of modern species, one can focus on developments during the Eocene and on the evolution of form and behavior as expressed in present-day representatives of the various families. Although the species (and most genera) used as examples in the following synthesis did not evolve until later in the Cenozoic, they embody the features under discussion and so serve as effective stand-ins for their poorly known progenitors.

Derivation of Modern Teleost Fishes The derivation of modern teleost fishes can be examined based on circumstances involved in their divergence from the main evolutionary line. We begin by characterizing mainstream feeding relations. Mainstream species, as perceived here, are those generalized carnivores that Gosline (1960) and Schaeffer and Rosen (1961) envisioned having the essential actinopterygian features but lacking specialized adaptations to contemporary settings. Current mainstream actinopterygians are among species included in the perciform suborder Percoidei, which has been described as “ . . . the basal evolutionary group from which other perciform groups . . . have been derived” (Nelson, 1994, p. 331). The Percoidei, however, are widely recognized as an unnatural group (e.g., Lauder and Liem, 1983; Johnson, 1993) and as usually constituted (e.g., Nelson, 1994), include species considered in this chapter and elsewhere as divergent from the main line.

1 Throughout the rest of this chapter, the terms “coral reef(s)” and “reef coral(s)” refer mainly to scleractinians; they have remained the major reefbuilding corals up to the present.

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F I G U R E 3-1 Kelp bass, Paralabrax clathratus.

F I G U R E 3-2 Broomtail grouper, Mycteroperca xenarcha, surrounded by senoritas, Oxyjulis californica.

Feeding Relations in the Mainstream Although the main actinopterygian line has produced periodic radiations of specialized offshoots from its inception, the generalized carnivores at its core have remained conservative (Gosline, 1960). There have been progressive improvements in jaw and fin structure, along with other minor changes, but most basic features have remained as before. This constancy led to my suggestion that mainstream teleosts probably have attacked the same types of organisms in the same way throughout their history (Hobson, 1974, 1979). Modern representatives of the teleost mainstream include serranids of the subfamilies Serraninae and Epinephelinae; the former (which includes the California kelp bass, Paralabrax clathratus, fig. 3-1) are considered the stem of the family; the latter (which includes the broomtail grouper, Mycteroperca xenarcha, fig. 3-2) is an early derivative (Kendall, 1976). Certain key trophic features of serranine and epinepheline serranids have been identified (Hobson, 1968, 1979; Hobson and Chess, 2001; Shpigel and Fishelson, 1989): They have large, generalized mouths and use vision to target organisms in daylight (especially twilight) that are fully exposed to direct attacks. In these attacks, they ambush, run down, or stalk prey that are large enough to grasp and entrap, yet small enough to manipulate and swallow whole. Their prey also lack heavy armor, spines, and other noxious components that an unspecialized digestive system cannot process.

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Probably, these trophic features have described mainstream predators and their prey at least throughout most of actinopterygian history. Certainly during this long evolution, potential prey acquired ways to defend against offensive capabilities characteristic of such predators, and, just as certainly, predators countered with modified feeding morphologies and/or behaviors. I suggest that these interactions between predator and prey have been the basis of divergences from the teleost mainstream. F I G U R E 3-3 (a) Ling cod, Ophiodon elongatus. (b) California halibut,

Divergences From the Mainstream

Paralichthys californicus (from Hobson and Chess 1986, with permission from Springer Science and Business Media).

Although the adaptive potential of the percoid condition was most evident in the explosive radiation of perciforms as coral reef communities expanded during resurgence from the endCretaceous extinctions, there have been major divergences from the main line for which there is no evidence of comparable radiation or of coral reef involvement. The distinction can be related to whether the departures were based on adaptations that increased the effectiveness of an existing mode of feeding or on adaptations in response to specific prey defenses that enabled new modes of feeding. These two categories of divergence are considered next.

Divergences Based on Increased Effectiveness of an Existing Mode of Feeding The main feeding tactics of generalized predators—the ambush and the straightforward rush (Hobson, 1979)—probably have always been the primary means of attack by mainstream actinopterygians, and it is evident that each has keyed major divergences from the main teleost line.

F I G U R E 3-4 Grass rockfish, Sebastes rastrelliger.

AM B US H E R S

Divergences based on adaptations that improved performance as ambushers were particularly significant because they involved basal elements of the percomorph orders Scorpaeniformes and Pleuronectiformes (rockfishes and flatfishes). Distinguishing features of both—sedentary habits and highly cryptic features—make them more effective ambushers. Modern species clearly adapted to launch attacks from ambush include the ling cod (Ophiodon elongatus: family Hexagrammidae, fig. 3-3a), a scorpaeniform, and the California halibut (Paralichthys californica: family Paralichthyidae, fig. 3-3b), a pleuronectiform. It is generally agreed that scorpaeniforms and pleuronectiforms evolved from basal percoids (Hubbs, 1945; Gosline, 1971; Chapleau, 1993), some place the origin of pleuronectiforms with the earliest percoids or even prepercoids (Amaoka, 1969; Li, 1981). Furthermore, modern representatives show evidence of their ancestry in that the most primitive representative of both orders—species of the scorpaeniform family Scorpaenidae and of the pleuronectiform family Psettodidae— are characterized by serranid-like feeding mechanisms, and it is known or inferred that they attack from ambush (Norman, 1934; Harmelin-Vivien and Bouchon, 1976). Although there is no evidence of explosive radiation when scorpaeniforms and pleuronectiforms departed the teleost mainstream, both orders have since diversified greatly. Furthermore, though their origins seem unconnected to coral reef expansion and their subsequent evolution has progressed mainly in other habitats, both orders were represented among

F I G U R E 3-5 An aggregation of blue rockfish, Sebastes mystinus.

coral reef fishes of the Eocene (Blot, 1980; Bellwood, 1996) and at present include coral reef specialists (e.g., Hobson, 1974). Modern scorpaeniforms and pleuronectiforms in California coastal communities include variations from their generalized progenitors. Consider, for example, the scorpaeniform genus Sebastes (family Scorpaenidae), which includes the majority of rockfishes. Though most that have retained sedentary habits continue to attack prey mainly by ambush, for example, the grass rockfish (S. rastrelliger, fig. 3-4), there are varied modes of feeding among others that have abandoned sedentary habits for activities in the water column. Thus, the shortbelly rockfish (S. jordani) coordinates its feeding with diel vertical movements of various planktonic crustacea (Chess et al., 1988), whereas the bocaccio (S. paucispinis) feeds from an early juvenile stage on smaller fishes in the water column. The blue rockfish (S. mystinus, fig. 3-5) feeds largely on gelatinous zooplankters—

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a major departure from the standard rockfish diet of crustacea and small fishes (Hobson and Chess, 1988). That planktivorous scorpaenids have greatly reduced versions of the head spines so prominent in basal representatives of the family indicates that feeding in the water column is a derived feature. There may be at least one ambusher among those scorpaenids that forage in the water column, the kelp rockfish (S. atrovirens, fig. 3-6), a nocturnal planktivore that hovers above the bottom at night and strikes at prey that may be detected through bioluminescence in surrounding turbulence (Hobson et al., 1981). Many of the differences that distinguished early scorpaeniforms from their percoid progenitors, and upon which the divergence of the scorpaeniform line from the teleost mainstream was based, have been lost or variably suppressed by convergences that have developed among modern representatives. For example, the olive rockfish (Sebastes serranoides) was named from its similarity to the kelp bass, a serranid perciform (fig. 3-7). Other California scorpaeniforms show that in retaining the trophic features of generalized predators, it helps to be small. Smallness enables them to feed on microcrustacea, an exceptionally rich source of food. By remaining small, the snubnose sculpin (Orthonopias triacis: family Cottidae, fig 3-8), is able to feed throughout life on amphipods, which are exceedingly numerous on reefs (Chess and Hobson, 1997; Hobson and Chess, 2001). Variations among modern pleuronectiforms are less obvious, mainly because their distinctive flattened bodies overshadow other features. Nevertheless, from the primitive condition, as represented by the large mouth, long pointed teeth, and short, uncomplicated digestive tract of the psettotids (Norman, 1934), their feeding-related morphologies have diversified greatly. Differences in diet define three types of feeding: crustacean feeders, fish feeders, and polychaetemollusk feeders (DeGroot, 1971). Representatives of all three types commonly occur on sediment along the California coast. The speckled sand dab (Citharichthys stigmaeus: family Paralichthyidae, fig. 3-9) feeds mainly on crustacea throughout life, whereas the California halibut, introduced above, feeds on crustacea as a juvenile, but on fishes as an adult. And the C-O sole (Pleuronichthys coenosus: family Pleuronectidae, fig. 3-10) feeds on crustacea as a subadult, but later switches to polychaetes and mollusks (Haaker, 1975; Hobson and Chess, 1986). A number of perciform lines have developed much like scorpaeniforms and pleuronectiforms as sedentary species that ambush prey from positions at rest on specific substrata. Included are the stargazers (family Uranoscopidae), gobies (family Gobiidae), sleepers (family Eleotridae), sand stargazers (family Dactyloscopidae), triplefins (family Tripterygiidae), clinids (family Clinidae), labrisomids (family Labrisomidae), pricklebacks (family Stichaeidae), and gunnels (family Pholidae). Many are similar to scorpaeniforms; for example, the stargazers and sand stargazers resemble stonefishes (family Synanceiidae), and many of the others are like sculpins in both appearance and in being small enough to continue feeding as adults on the exceptionally abundant microcrustacea (Hobson, 1994). The habitats of these species are mostly inorganic reefs, algal turf, or sediment, and though there are both tropical and temperate forms in all suborders represented (except the zoarcoids, which are strictly temperate), few are more than peripherally associated with coral reefs (Hiatt and Strasburg, 1960; Feder et al., 1974, Thomson

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F I G U R E 3-6 A kelp rockfish, Sebastes atrovirens, hovering in midwater

at night.

F I G U R E 3-7 A group of sub-adult olive rockfish, Sebastes serranoides,

at the edge of a kelp forest. Inset: a kelp bass of about the same age and size.

F I G U R E 3-8 Snubnose sculpin, Orthonopias triacis (from Hobson

1994, with permission from Springer Science and Business Media).

et al., 1979). Prominent representatives in California reef communities include the blackeye goby (Rhinogobiops (=Coryphopterus) nicholsii: family Gobiidae, fig. 3-11), the spotted kelpfish (Gibbonsia elegans: family Clinidae, fig. 3-12) and the island kelpfish (Alloclinus holderi: family Labrisomidae, fig. 3-13).

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F I G U R E 3-9 Speckled sand dab, Citharichthys stigmaeus.

F I G U R E 3-13 Island kelpfish, Alloclinus holderi (from Hobson 1994, with

permission from Springer Science and Business Media).

F I G U R E 3-10 C-O sole, Pleuronichthys coenosus (from Hobson and Chess

2001, with permission from Springer Science and Business Media).

F I G U R E 3-14 Blue-banded goby, Lythrypnus dalli (from Hobson and

Chess 2001, with permission from Springer Science and Business Media).

F I G U R E 3-11 Blackeye goby, Rhinogobiops (=Coryphopterus) nicholsii (from Hobson and Chess 2001, with permission from Springer Science and Business Media).

Exceptional is the blue-banded goby (Lythrypnus dalli: family Gobiidae, fig. 3-14). Unlike virtually all other small sedentary fishes that prey mainly on microcrustacea on or near the seabed, this species is brightly hued and thus readily visible. It would appear there is no need to avoid being detected by prospective prey, which may be the case. The blue-banded goby feeds mainly by darting up from resting positions on the bottom to capture zooplankters at the base of the water column (Hartney, 1989), and because zooplankters have evolved in a pelagic environment, they may not recognize threats from the benthos (Hobson, 1991). STRAIG HTFORWAR D R US H

F I G U R E 3-12 Spotted kelpfish, Gibbonsia elegans.

The divergences based on improved performance in capturing prey with a straightforward rush have been based on tendencies toward streamlining, development of body musculature, and other features that promote rapid swimming and therefore an ability to run down prey. These characteristics are most adaptive in pelagic predators, which can take full advantage of speed in open water. Among modern teleosts, they are best developed in the perciform suborder Scombroidei, as defined by Nelson (1994). Representatives of this group common in California waters include tunas (family Scombridae) and billfishes (family Xiphiidae), which are strictly open-water predators. At least one scombroid, however, regularly occurs close to southern California reefs, the California barracuda (Sphyraena argentea, family Sphyraenidae). Also defined by features that

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An examination of the way predaceous fishes have responded to each of these prey defenses identifies many of the processes that have diversified modern fishes. S MALLN E S S

F I G U R E 3-15 Almaco jack, Seriola rivoliana.

improve a straightforward rush are species of the family Carangidae, which is represented off southern California by the almaco jack (Seriola rivoliana, fig. 3-15) and the yellowtail (Seriola lalandi), both common near reefs and known to consume reef fishes (Randall, 1967; Craig, 1960). Carangids have long been included among the Percoidei (for example, by Nelson, 1994), but Johnson (1993) recommended placing them in a separate suborder, the Carangoidei, which is consistent with regarding them as divergent from the main line (Hobson, 1994).

Divergences Based on New Modes of Feeding The radiation of perciforms with expanding coral reef communities early during the Tertiary demonstrated the adaptive potential of the percoid condition. I suggest that this profusion of forms was part of the resurgence from mass extinctions and ecosystem collapse that had ended the Mesozoic. The restructuring of a devastated ecosystem is a process that has been repeated a number of times during the history of life on the earth, as recounted before. Ecosystem stability depends on highly evolved complexes of established interspecific relations. It has become clear that sudden removal of a large proportion of the interacting species by an episode of mass extinction is certain to disrupt the system; the extent of disruption is related to the proportion removed. Resurgence from the end-Permian extinctions, which are estimated to have removed up to 90% of marine species (Erwin, 1994), must have involved a broad restructuring of the system! Although the end-Cretaceous crisis was less severe, the resurgence process clearly was extensive. The discussion presented above led to the conclusion that ecosystem resurgence from mass extinctions begins with trophic relations among generalized survivors. It has become evident that this process centers on the trophic characteristics of mainstream predators and proceeds as adaptive responses to these characteristics among potential prey. Four basic ways that prey defend against mainstream predators have been identified (Hobson and Chess, 2001): (1) smallness, which presents difficulties to predators with large and simply constructed feeding mechanisms; (2) dissemblance, which results in going unrecognized by diurnal visual hunters; (3) inedibility, which is attained by incorporating materials that an unspecialized digestive system cannot process, and (4) nocturnality, which results in avoiding diurnal predators altogether.

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That smallness protects organisms against mainstream predators can be inferred from changes in the diet of kelp bass as they grow. Individuals shift from a diet of zooplankton to one of benthic microcrustacea before attaining lengths of about 10 cm and from benthic microcrustacea to fishes before attaining about 30 cm. It has been widely reported that serranids shift from crustacea to fishes as they grow; the shift is based on increasing size of prey. These reports have come from the Caribbean (Randall, 1967), the Gulf of California (Hobson, 1968), the South Pacific (Randall and Brock, 1960) and the Indian Ocean (Harmelin-Vivien and Bouchon, 1976). Obviously the trait is widespread among serranids, as probably it is among at least most generalized carnivores of the teleost mainstream. There seems to have been a consensus that these shifts to larger prey are adaptive as means to meet nutritional needs of their own growth. It has long been recognized that fishes tend to consume the larger of available prey (e.g., Ivlev, 1961), and experimental studies have shown that organisms taken as prey tend to be, on average, larger among gut contents than in the environment (e.g., Brooks and Dotson, 1965; Werner and Hall, 1974). The usual conclusion is that larger prey are preferred and that predation on them is more efficient (Eggers, 1982; Zaret, 1980). It has been argued, however, that the main reason kelp bass and other generalized carnivores shift to larger prey as they grow is that it becomes increasingly difficult for them to capture the smaller ones (Hobson and Chess, 2001). It is questionable whether the shifts would occur if kelp bass were able to continue feeding effectively on the smaller prey because each shift involves turning to organisms that are less numerous and less accessible and also more difficult to capture. This is evident in that the incidence of empty stomachs increases greatly as the fish continues to grow. Furthermore, the way these predators stalk and attack individual prey would become inefficient as the increased nutritional needs of their own growth required them to consume smaller prey in greater numbers. Kelp bass were found to cease feeding on zooplankton upon attaining a size of about 10 cm and then to cease feeding on the larger but still small microcrustacea of the benthos when about 20 cm. It is significant that kelp bass usually attain this size in their third year and they can live at least 33 years (Love et al., 1996). Clearly, being small offers protection from such predators. The need to shift to larger prey as they grow deprives mature mainstream predators of exceedingly rich sources of readily available prey. Probably, it is in response to this that some of the most successful evolutionary lines diverged from the mainstream based on adaptations that provide life-long access to minute prey. The key has been relative mouth size. If increasing mouth size forces kelp bass and other mainstream predators to turn elsewhere for food, an obvious solution would be to acquire a mouth that remains small relative to the size of prey. Teleosts have solved the problem in two ways: by evolving smaller adult size or through modification of head and jaw structure that results in a mouth that is small relative to the size of their bodies. The first is the more straightforward and widespread. As noted above, many of those that attack from ambush have acquired life-long abilities to feed on microorganisms by

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evolving as smaller predators. Here we are most concerned with those that have reduced relative mouth size through changes in head and jaw structure. (Many of these have also acquired smaller adult size, thus increasing the effect.) Diurnal planktivores are prominent examples in which structural changes in head and jaws permit relatively large individuals to feed on minute prey. Virtually every major family of modern coral reef fishes includes species specialized as planktivores, and they have become major components of coral reef communities (Hobson, 1974, 1991; Davis and Birdsong, 1973). Furthermore, one planktivore, the blacksmith (Chromis punctipinnis, family Pomacentridae, fig. 3-16), may be the most numerous fish species in reef communities of southern California (Bray, 1981; Hobson and Chess, 1976). The blacksmith’s mouth is typical of reef fishes specialized for planktivory (fig. 3-17). In addition to being small, its upturned orientation results in a shortened snout and the ability to train both eyes on prey close enough to entrap, and its highly protrusible jaws can be thrust forward to add even more precision to the strike. Probably, the diurnal planktivores referred to here represent lines that diverged from the mainstream as benthivorous carnivores (Hobson, 1994). It is clear that adaptations for planktivory are highly evolved because their occurrence in species representing diverse families has resulted in a convergence that has tended to obscure family characteristics (Davis and Birdsong, 1973). The highly specialized trophic features typical of reef planktivores demonstrate the adaptive capabilities inherent in the protrusible jaw of advanced actinopterygians. This feature made its initial appearance in early acanthopterygians and has since been the primary key to success in modern teleosts (Alexander, 1967; Gosline, 1971; Motta, 1984). As Gosline (1981, p. 11) stated, “The acanthopteran (acanthopterygian) system of premaxillary protrusion . . . appears to form part of the inheritance of all higher teleosts.” According to Schaeffer and Rosen (1961, pp. 198–199), “It is largely the acanthopterygian mouth that has given rise to the enormous variety of specialized . . . feeding mechanisms for which teleosts are so well known”. Although jaw protrusion is particularly well developed among diurnal planktivores, most of the variety of feeding mechanisms referred to here are adaptive features of perciforms specialized to consume organisms characteristic of the coral reef benthos. A coral reef is a living surface of incredibly diverse organisms that, despite their great abundance and accessibility, are unavailable as food for generalized predators of the teleost mainstream. Only predators with highly specialized trophic capabilities find food on the reef’s surface, with each limited to just a narrow and distinctive selection of the organisms present. Virtually all benefit from a small adaptive mouth, but many—such as the abundant labrids—have diets that require additional capabilities and so are more appropriately considered in the next section. Here we concentrate on predators with feeding adaptations developed mainly for prey smallness. Examples include butterflyfishes, which represent the perciform family Chaetodontidae and are widely recognized as characteristic of coral reefs (e.g., Burgess, 1978). Many heavily armored organisms on coral reefs have parts vulnerable to a precise snip by a tiny, manipulative mouth—a weakness that butterflyfishes are equipped to exploit. For example, the pebbled butterflyfish (Chaetodon multicinctus) uses its small mouth and pointed snout to pluck coral polyps from their armored encasements. And the longnose butterflyfish (Forcipiger flavissimus) uses its exceptionally

F I G U R E 3-16 Feeding aggregation of blacksmith, Chromis

punctipinnis.

F I G U R E 3-17 The protrusible upper jaw of the blacksmith is a wide-

spread feature among diurnal planktivores. (Drawings by Ken Raymond, Southwest Fisheries Science Center; from Hobson 1991, with permission from Elsevier.)

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long snout and small mouth to reach among spines of echinoids to pluck podia and pedicellaria (Hobson, 1974). Perhaps more than any other group, butterflyfishes demonstrate the versatility inherent in the acanthopterygian mouth, which argues strongly against the current practice (e.g., Nelson, 1994) of including them in the basal perciform suborder Percoidei. Surely a close examination would distinguish butterflyfishes at a major taxonomic level apart from the more generalized members of that heterogeneous assemblage. The advantages gained from a small, adaptive mouth extend beyond the ability to pluck minute organisms from the benthos or water column, however. In fact, the adaptive potential of an advanced acanthopterygian mouth in exploiting the vast store of potential prey among the benthos has been the major force in diversifying modern fishes. This conclusion is implicit in the findings of Gosline (1987) and Kotrschal (1988) that advanced acanthopterygian evolution has been a progression from large mouths that take mobile prey by suction (as do serranids and other mainstream predators) to smaller mouths that take benthic organisms by biting (as do labrids and many other derivative acanthopterygians).

F I G U R E 3-18 Rock wrasse, Halichoeres semicinctus (adult male; from Hobson and Chess 2001, with permission from Springer Science and Business Media).

DI S S E M B LANCE

A visual assessment of the seabed in the clearest sunlit water is unable to detect the vast majority of the microcrustacea that rest there fully exposed. Some are visible by closer inspection, such as the abundant caprellid amphipods on bryozoans and algae, but most remain unseen even under careful scrutiny (Hobson and Chess, 2001) because they are either transparent or have hues and/or textures that match the underlying substrate. Generally, the match to substrate features defines the distribution of these organisms in the environment; the more abundant match the most widespread substrata (Chess and Hobson, 1997). Clearly, fishes must find prey far more difficult to detect on the seabed than in the water column. As important as cryptic morphology is in making benthic crustacea difficult to discern, it is clear that they must remain motionless to escape detection. This became clear with repeated observations of kelp bass about 10 to 20 cm long hovering motionless for long periods, their attention clearly fixed on a substrate directly ahead, and only infrequently darting forward to snap prey (e.g., Hobson and Chess, 2001). It was evident that this predator attacked when organisms previously unseen became visible momentarily. Based on my own experience that benthic microcrustacea generally become visible only when they move, I surmise that it was prey movement that elicited the attacks. Although such organisms cease movement when predators approach, they may relax their guard and eventually move if the predator shows no further aggression (Hobson, 1979). There must have been strong selection for increased visual acuity among predators that would habitually feed on benthic microcrustacea, so it is not surprising that species of the labroid family Labridae have acquired exceptionally sharp vision (McFarland, 1991). Prey taken by the rock wrasse (Halichoeres semicinctus: family Labridae, fig 3-18) from southern California reefs are mostly microcrustacea plucked “from a substrate after close visual scrutiny” (Hobson and Chess, 2001, p. 425). Two other California reef fishes of the labroid family Embiotocidae, the black perch (Embiotoca jacksoni; fig. 3-19) and the rubberlip perch (Rhacochilus toxotes, fig. 3-20) have solved the problem of prey dissemblance by ingesting mouthfuls of sediment/turf algae without distinguishing targets and winnowing edibles from inedibles only after ingestion (Drucker and Jensen, 1991).

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F I G U R E 3-19 A group of black perch, Embiotoca jacksoni. (Photo:

Tony Chess.)

F I G U R E 3-20 Rubberlip perch, Rhacochilus toxotes.

I N E DI B I LIT Y

Being inedible may be the best defense. A wide variety of highly visible prey are readily accessible on many reefs but are protected by armored exteriors or toxic/noxious interiors from all but certain predators equipped with specialized feeding capabilities. They include sessile forms such as sponges, hydroids, anthozoans, bryozoans, and ascidians, as well as mobile mollusks and echinoids. In addition, marine plants,

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F I G U R E 3-24 A pair of pile perch, Rhacochilus vacca (from Hobson F I G U R E 3-21 School of senoritas, Oxyjulis californica.

F I G U R E 3-22 California sheephead, Semicossyphus pulcher (adult

male).

F I G U R E 3-23 Garibaldi, Hypsypops rubicundus.

which have combinations of structural and chemical defenses, deter feeding fishes (Hay, 1991). Predators able to circumvent the defenses of such organisms to snip off vulnerable parts, such as butterflyfishes, are discussed above. Here we consider predators adapted to deal directly with these defensive structures. Especially prominent are the various benthivores of the perciform suborder

and Chess 2001, with permission from Springer Science and Business Media).

Labroidei. In addition to having relatively small mouths, labroids are characterized by highly developed pharyngeal dentition that can crush ingested shelled organisms being passed from mouth to gut. This capability has enabled labroids of the families Pomacentridae and, especially, Labridae to share dominance with butterflyfishes among benthivores in coral reef communities. Benthivorous labroids dominate the reef communities of southern California. Especially prominent are species of the family Labridae, which (in addition to the rock wrasse, introduced above) is represented by the senorita (Oxyjulis californica, fig. 3-21) and the California sheephead (Semicossyphus pulcher, fig. 3-22). The family Pomacentridae is represented among benthivores on California reefs by the garibaldi (Hypsypops rubicundus, fig. 3-23), and the family Embiotocidae by (in addition to the black perch and rubberlip perch, introduced above) the pile perch (Rhacochilus vacca, fig. 3-24). Species that have acquired features enabling herbivory represent a highly adaptive departure from the mainstream. Marine plants offer an immense trophic resource unavailable to mainstream species, but it is evident that adaptations related specifically to herbivory in coral reef herbivores developed in lines that had diverged from the mainstream as benthivorous carnivores (Hobson, 1994). In suggesting similar derivations for coral reef herbivores and diurnal planktivores, I stated (Hobson, 1994, p. 79), “Certain features that adapt fishes to feed on benthic animals are also adaptive in feeding on zooplankters and plants.” Considering these features as preadaptations, I commented in regard to herbivory (p.79), “Benthic plants are like sessile invertebrates in possessing an array of structural and chemical defenses that deter feeding fishes (Hay, 1991), so adaptations that allow benthivorous carnivores to deal with these defenses should also be adaptive in herbivory.” It was suggested that herbivory developed among benthivorous carnivores that acquired the means to access nutrients encased in cellulose, a rare substance in animal tissue but a major component of plant cell walls. The previous remarks are limited to the derivation of coral reef herbivores because the major herbivores in California’s reef communities—the opaleye (Girella nigricans, fig. 3-25) and the halfmoon (Medialuna californica, fig. 3-26)—are from a different evolutionary line. Both represent the family Kyphosidae, which has an uncertain origin. Generally, kyphosids are included among the more primitive perciforms in the suborder Percoidei (e.g., by Nelson, 1994), but certainly they are far removed from the bass-like percoids of the teleost

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F I G U R E 3-25 A group of opaleye, Girella nigricans.

F I G U R E 3-26 Aggregation of halfrnoons, Medialuna californiensis,

under the canopy of a kelp forest. (Photo: Tony Chess, from Hobson 1994, with permission from Springer Science and Business Media.)

mainstream. Patterson (1964) suggested they might have been independently derived from kyphosid-like beryciforms of the Cretaceous. In contrast, species considered here as coral reef herbivores are widely considered (e.g., by Nelson, 1994) among the more highly evolved perciforms. The relatively few kyphosids among modern fishes lack obligate ties to coral reefs, and there is no reason to suspect that such ties existed among earlier kyphosids. The family was not reported among fossils recovered from coral reef deposits of the early Tertiary (Blot, 1980; Patterson, 1993; Bellwood, 1996), so may not have been represented among perciform lines that radiated with expanding coral reef communities during the Eocene. The more typical coral reef herbivores scrape fine algae from the surface of rocks or dead coral, whereas the opaleye and halfmoon feed largely on foliose forms—often as fragments adrift in the water column (Hobson, 1994; Hobson and Chess, 2001). Furthermore, they are more omnivorous, with benthic invertebrates frequently included in their diets (Quast, 1968). The halfmoon differs further in feeding regularly on planktivore feces, which are consumed as these drift through the water column (Hobson and Chess, 2001). NO CTU R NALIT Y

An effective defense against visual predators is to be sheltered when most visible. This would explain why so many organisms vulnerable to generalized predators occur in exposed positions only at night. These are organisms “large enough to

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INTRODUCTION

grasp and entrap, yet small enough to manipulate and swallow whole” and which “lack heavy armor, spines and other noxious components that an unspecialized digestive system cannot process” (Hobson and Chess, 2001, p. 454 and above). Among them are species of amphipods, isopods, and other crustacea that kelp bass capture from the benthos during the day and that rise into the water column only at night (Hobson and Chess, 1976; Chess and Hobson, 1997). There are varied reasons why organisms that are benthonic by day become planktonic at night (Hobson and Chess, 1976, 1986; Chess and Hobson, 1997). Some disperse in the nocturnal water column to hunt prey, as do certain mysids; others are there to reproduce, as are epitokus nereids. Some, including caprellids and certain myodocopid ostracods, remain at lower levels of the water column, but most are like those isopods that range widely in open water. Some, including certain ostracods, isopods, and amphipods, rise through the water column to concentrate at the water’s surface. For whatever reasons these organisms need to enter the water column, probably they do so at night because in reduced light they are less conspicuous as visual targets. The protection that these organisms gain by limiting their excursions into the water column to periods of darkness is only relative, however, because many predators have acquired abilities to detect prey in dim light. For most, this has involved increased visual sensitivity; many that have acquired this feature have been enormously successful. Some, including species of the perciform families Lutjanidae and Haemulidae, school in large numbers at the edge of reefs while inactive during the day, and then spread out to forage on organisms that emerge from sediments in surrounding areas at night (Hobson, 1968). Others, including species of the perciform families, Apogonidae and Priacanthidae, shelter in reef caves and crevices by day and forage above the reef at night on crustacea and other prey that are in the water column there only after dark (Hobson, 1974). It is clear that abilities to function at low levels of illumination are highly adaptive. This is evident in that of the great variety of beryciforms that were so dominant during the Cretaceous, the relatively few present-day survivors are specialized for activity in dim light. These few, however, include some highly successful species. The very abundant squirrelfishes and soldierfishes of the nocturnal family Holocentridae are prominent components of reef communities throughout the present tropics (Randall, 1967; Hobson, 1974; Sano et al., 1984). The only other beryciforms in modern reef communities are small, inconspicuous flashlight fishes, family Anomalopidae, and pinecone fishes, family Monocentridae (Kotlyar, 1985; McCosker and Rosenblatt, 1987), but the order is well represented in the dimly lit deep sea. Among such beryciforms are the roughies (family Trachichthyidae; Nelson, 1994), including the orange roughy (Hoplostethus atlanticus), a major commercial food fish exported from New Zealand. There are no beryciforms near California shores, but nocturnal perciforms are prominent there, especially in the south. Like their close relatives in the tropics, the sargo (Anisotremus davidsoni, fig. 3-27) and the salema (Xenistius californica, fig. 3-28), both of the grunt family Haemulidae, school above or near southern California reefs during the day and forage on emergent crustacea and other small organisms in surrounding open areas at night (Hobson and Chess, 1976; Chess and Hobson, 1997). The same behavior describes the queenfish (Seriphus politus, family Sciaenidae, fig. 3-29) and

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F I G U R E 3-3 0 School of walleye surfperch, Hyperprosopon argenteum.

F I G U R E 3-27 Pair of sargo, Anisotremus davidsoni (from Hobson 1994,

with permission from Springer Science and Business Media).

F I G U R E 3-31 Treefish, Sebastes serriceps. F I G U R E 3-28 Salema, Xenistius californiensis.

F I G U R E 3-29 School of queenfish, Seriphus politus (from Hobson 1994, with permission from Springer Science and Business Media).

F I G U R E 3-32 Black-and-yellow rockfish, Sebastes chrysomelas.

the walleye surfperch (Hyperprosopon argenteum, family Embiotocidae, fig. 3-30), except that the latter occurs abundantly off central and northern California as well (Eschmeyer et al., 1983). Nocturnal predators that forage over sand at the base of the water column, such as the sargo, tend to have smaller eyes than predators that forage high in the water column, such as the salema and walleye surfperch, probably because ambient

light increases near the seabed by reflected moonlight and/or starlight (Hobson et al., 1981). Nocturnal foraging is widespread among species of the scorpaeniform family Scorpaenidae. Some, for example, the treefish (Sebastes serriceps, fig. 3-31) and the black-and-yellow rockfish (Sebastes chrysomelas, fig. 3-32), find their prey close to the sea bed; others, such as the kelp rockfish, feed in the water column close to columns of giant kelp (Macrocystis). Consistent

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with circumstances among the nocturnal perciforms, as noted above, kelp rockfish (fig. 3-5) have larger eyes (even though treefish typically feed among rocks, not over sand). Like smallness, dissemblance, and inedibility, therefore, nocturnality has promoted specialized feeding adaptations characteristic of certain evolutionary lines. But though the others involved osteological features, with major change in external appearance, nocturnality has elicited mainly sensory features, especially increased photic sensitivity. So while predators adapted to prey smallness, dissemblance or inedibility have acquired distinctive morphological features, predators adapted to nocturnality have remained morphologically similar to their progenitors—at least in features used to assess phylogeny. The result has been that nocturnal predators tend to occupy basal positions in phylogenetic classifications (e.g., Nelson, 1994); thus, both the salema and sargo (as haemulids) and the queenfish (as a sciaenid) generally are placed in the basal perciform suborder Percoidei, whereas treefish and kelp rockfish are placed in the basal scorpaeniform family Scorpaenidae (Gosline, 1971; Nelson, 1994). This chapter, however, considers species specialized as nocturnal predators to be classified as divergent from the mainstream, much like labroids and others generally advanced teleosts. They differ mainly in that their divergence is based on sensory and behavioral features that cannot be properly assessed by procedures ordinarily used in studies of phylogeny.

Cenozoic Influences on Distributions, Extinctions, and Originations Although basic features of modern reef ecosystems were established with resurgence from the end-Cretaceous extinctions early in the Tertiary, evolution of these systems has continued to evoke change through the present. Conditions under which teleosts diversified, as recounted above, varied in ways that greatly influenced subsequent extinctions, originations, and distributions. It has been suggested, however, that certain broad features based on trophic relations were in place at the outset (Hobson, 1994). Early Tertiary seas were warm far to the north and south of the present tropics (Newell, 1971), so the temperature barriers to poleward expansion, so prominent today, were not a feature of that period. Of the two types of divergence from the evolutionary mainstream defined above, lines based on advances in existing modes of attack—the ambush and the straightforward rush—should have had more poleward mobility. This would follow if, as suggested, lines based on new modes of feeding developed mainly as elements of expanding coral reef communities. Certainly the ambush and straightforward rush would have been more adaptive in a wider range of settings than modes of feeding associated with specific environmental features.

Distribution at Higher Latitudes Based on criteria identified above, poleward mobility should have been widespread among scorpaeniforms and pleuronectiforms, as well as among gobioid and blennioid perciforms. Furthermore, once established at higher latitudes, representatives of these groups would have been positioned to evolve as temperate species as the seas there cooled. Consistent with this scenario, coastal communities at high latitudes today, including those off northern California, are dominated by such forms (Hobson, 1994).

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Cooling developed at higher latitudes with the progressive isolation of Antarctica. When Australia and South America separated from Antarctica late in the Eocene, 40–45 mya, the southern high latitudes were opened for the Circumpolar Current. This cut off the southerly flow of warm water from tropical latitudes that had maintained relatively high sea temperatures in that region (Stanley, 1989). By mid-Miocene, the condition had progressed to the extent that an icecap covered Antarctica and seas had cooled everywhere, both north and south of the equator, except in the sun-warmed surface waters of the tropics (Newell, 1971).

Distribution at Lower Latitudes Lines that proliferated with expanding coral reef communities diversified far more than lines distributed at higher latitudes, discussed above, but they were limited in extending their distributions poleward. This limitation has been attributed to low sea temperatures at higher latitudes (e.g., Mead, 1970), but, as noted above, high-latitude seas were warm during the perciform radiation. It is more likely that exclusion of coral reef perciforms from high latitudes related to limits on the distribution of reef-building corals. According to Ziegler et al. (1984), poleward distribution of reef corals has depended more on sun angle than on water temperature. Their findings indicate that sunlight penetrating to the sea bed since Mesozoic time has been insufficient for the coral’s symbiotic algae beyond about 36° latitude, which would have made this the poleward limit for reef-building corals and also for organisms with obligatory connections to coral reef communities. Although limited in distributions poleward, coral reef fishes had great success extending their lineages west and east. It is believed this expansion originated in the region of what is now the Indo-Malay Archipelago (Ekman, 1953) and that from there reef fishes spread through all tropical seas of the world. Westward expansion would have progressed along the shores of the Tethys Sea, and eastward expansion would have progressed from island to island into the Pacific. When teleosts diversified early in the Eocene, Tethys had been narrowed by northward movement of southern continents, but nonetheless remained a pantropical seaway. Subsequent global developments, however, created major barriers to trans-Tethys distributions. Of particular significance was closing of the seaway between what is now the Indian Ocean and the Mediterranean Sea. This occurred when Africa collided with Eurasia during the Miocene (14–18 mya; Stanley, 1989), blocking passage between the region now encompassing the Indo-Malay Archipelago and what had been the western reaches of Tethys.2 Tropical reef fishes had gone this way in extending their lines to the ancestral Atlantic, Caribbean, and—as the Isthmus of Panama had not yet connected North and South America—the eastern Pacific. The Caribbean–Pacific connection closed with formation of the Isthmus of Panama during the Pliocene (3–4 mya; Stanley, 1989), and since then tropical eastern Pacific shore fishes have developed without further input from the east.

2 Fishes to the east of this barrier continued to evolve as components of what is now recognized as the Indo-Pacific fauna. Today this diverse complex of species extends from the coast of east Africa (and the Red Sea) eastward across the Indian and western Pacific Oceans to Polynesia, with some elements in the eastern Pacific.

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Although it has been over three million years since closure of the Atlantic–Pacific connection between North and South America, the vast majority of fishes near shore in the tropical eastern Pacific today have their closest relatives in the Caribbean and tropical Atlantic, which shows where their affinities lie (Ekman, 1953; Walker, 1960; Rosenblatt, 1967). Relatively few are products of eastward distribution of IndoPacific species from the west. There have been no land barriers to impede progress from that direction, but the broad expanse of open ocean that separates mid-Pacific islands from the Americas, which Ekman (1953) termed the East Pacific Barrier, is considered to have blocked passage of most coastal marine organisms (e.g., Grigg and Hey, 1992). It may be, however, that this barrier is less an obstacle to coastal fishes (and certain other organisms, including reef corals) than is generally supposed; an argument can be made that the main reason for few Indo-Pacific reef fishes (and reef corals) in the eastern Pacific at present is that habitats there generally are unfavorable for them. The marine environment near shore in the tropical eastern Pacific today is mainly one of isolated rocky reefs separated by extensive expanses of sand and/or mud. A broad assortment of tropical reef fishes inhabits the rocky areas (Allen and Robertson, 1994), but forms that inhabit the broad areas of sand and/or mud are more typical of the region. Examples include representatives of the perciform families Haemulidae and Sciaenidae—the grunts and croakers. Grunts generally favor areas of sand, including reef sand-patches (Hobson, 1968), while most croakers favor areas of sand/mud, which tends to draw many to the vicinity of river outflows, including estuaries (Allen and Robertson, 1994). The first grunt on record is represented by a fossilized otolith from a mid-Eocene coral reef (Patterson, 1993), which would connect the early history of its line with the perciform radiation and resurgence of coral reef communities early in the Tertiary. From this, it would follow that the line evolved with adaptations that enabled feeding on organisms in sediment within and adjacent to coral reefs. Croakers may have evolved in a similar way, but there is lack of evidence that would support this possibility. Although today there are grunts and croakers among eastern Pacific reef fishes that forage in reef sand-patches (Hobson, 1968; Allen and Robertson, 1994), many more of both families occur over the expanses of sediment that lie off most mainland shores (Hobson, 1968; Allen and Robertson, 1994). Coral reefs are poorly developed at present in the eastern Pacific (Darwin 1842; Durham, 1966; Glynn, 1997), but this condition developed only after final closure of the tropical Atlantic–Pacific connection. There was a greater variety and abundance of reef corals in the eastern Pacific earlier in the Cenozoic, including many with affinities eastward in the Caribbean and beyond (Durham, 1966). The eastern Pacific environment turned against coral reefs late in the Miocene, however, and became increasingly unfavorable to them as uplifting of what is now the Isthmus of Panama progressively closed the Central American Seaway (Stanley, 1989). Final closure of the tropical Atlantic–Pacific connection coincided with the onset of alternating expansion and contraction of glaciers that characterized the Pleistocene (Stanley, 1989). Seas cooled and dropped to lower levels, as water became ice in each expanding glacier, then warmed and rose to higher levels, as ice became water in each contracting glacier. Although conditions associated with expanding glaciers have been widely destructive to coral reefs, conditions associated with glacier

contraction have provided coral reefs time to recover in many regions. Not so in the eastern Pacific, however, where (as at present) contraction has been a time of frequent and powerful El Niño–Southern Oscillation (ENSO) events that have proved damaging to reef corals (Colgan, 1989; Glynn, 1997). Although the vast majority of today’s tropical eastern Pacific shore fishes have evolutionary ties to the Caribbean and tropical Atlantic, all of the region’s current reef-building corals are from the central Pacific. Reef corals present in the eastern Pacific when the tropical Atlantic–Pacific connection finally closed (including the many with links to the Caribbean) were eliminated during Pleistocene glaciation, and subsequent recruitment has been limited to Indo-Pacific migrants from the west (Dana, 1975). But as with Indo-Pacific reef fishes, relatively few IndoPacific reef corals have become established in the eastern Pacific. The generally held notion that this has resulted from difficulties in crossing the Eastern Pacific Barrier ignores the findings of many (e.g., Dana, 1975; Colgan, 1989; Glynn, 1997) that the eastern Pacific generally offers poor habitats for coral reefs. Although the tropical eastern Pacific environment is recognized as “marginal for coral reef development” (Dana, 1975, p. 355), little has been made of the great difference in coral coverage between the offshore islands and the mainland. Reef corals are of relatively few species along both island and mainland shores (Glynn, 1997), but coral coverage is much richer at the islands; Clipperton, the island farthest offshore, is a coral atoll (Glynn, 1996). Conditions are especially poor for reef corals along mainland shores, at least partly because continental runoff into coastal waters typically carries materials damaging to reef corals—notably suspended sediments and algae-nourishing nutrients (Wood, 1999). Localized concentrations of cold water at centers of coastal upwelling also contribute to conditions unfavorable for reef corals near the mainland. (Dana, 1975). Indo-Pacific reef fishes, too, are more abundant around the islands (Rosenblatt, 1967); a number that are abundant around the islands generally are rare or absent along the adjacent mainland (Rosenblatt et al., 1972, Allen and Robertson, 1994). Furthermore, the few mainland locations noted for unusual abundances of Indo-Pacific fishes—the Cape region of Baja California and the Gulf of Chiriqui in Panama (Walker, 1960; Rosenblatt et al., 1972)—are also noted for unusual abundances of reef corals (Squires, 1959; Dana, 1975). That eastern Pacific distributions of Indo-Pacific fishes and reef corals are so closely matched is consistent with the close ties that have existed between them throughout their histories, as recounted above. Finally, it is telling that though “reef fishes” can be an appropriate term in general reference to fishes around the islands (including those active over sand patches or sediment peripheral to reefs), it is rarely, if ever, appropriate as a general reference to fishes along mainland shores (despite the prominence of reef fishes at some locations). An appropriate term for general reference to fishes along the mainland is “shore fishes”. It would appear, therefore, that though fishes arriving in the eastern Pacific from the tropical Atlantic and Caribbean often found favorable habitats along western shores of tropical America, fishes from the central Pacific generally have not. The difference may relate to environments encountered as evolutionary lines progressed westward or eastward from origins in the ancestral Indo-Malayan region. With westward distribution progressing along the shores of Tethys, there would have been extensive experience with continents in the evolutionary history of lines that reached the Eastern Pacific from that direction. Certainly this experience would have

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weakened, if not eliminated, obligatory ties to coral reefs connected to their early history. (Many of today’s eastern Pacific grunts may have such a history, as noted above.) In contrast, as eastward distribution from the Indo-Malayan region progressed from island to island across the Pacific, lines that reached the Eastern Pacific from that direction would lack evolutionary experience with continental shores, and they would also have maintained contact with insular coral reefs throughout their evolution. Lines with this history may well have retained obligatory relations with coral reefs connected to their origins, which could explain why so few migrants from the west have become established in the tropical eastern Pacific. F I G U R E 3-33 Aggregation of black rockfish, Sebastes melanops.

To Be a California Marine Fish A review of the geographical affinities of taxa involved is an effective way to begin a consideration of what it has taken to be a successful California marine fish. SC OR PA E N I F O R M E S

The major California scorpaeniforms are among the scorpionfishes (family Scorpaenidae), the sculpins (family Cottidae), the greenlings (family Hexagrammidae), and to a lesser extent, the poachers (family Agonidae). Representatives of these families have affinities that are overwhelmingly temperate. Of the scorpionfishes, species of the genus Sebastes—the rockfishes—dominate reef communities across the North Pacific Rim from California to Japan, with 61 species reported from California alone (Eschmeyer et al., 1983; Allen and Smith, 1988). A prominent example is the black rockfish (Sebastes melanops, fig. 3-33), a major component of many northern California reef communities. There are no species of Sebastes in the tropics, but two other scorpaenids represent the only exceptions to strictly temperate distributions among California scorpaeniforms: the California scorpionfish (Scorpaena guttata, fig. 3-34) and the rainbow scorpionfish (Scorpaenodes xyris). The former is a warm-temperate representative of a tropical genus that occurs from southern California to the Gulf of California. The latter is widely distributed from southern California to Peru, including the Galapagos Islands (Eschmeyer et al., 1983). The sculpins (family Cottidae) are widespread in reef communities at higher latitudes, but though more numerous than other families on many reefs, generally they go unnoticed because most are so small and cryptic. An atypically large cottid on many California reefs is the cabezon (Scorpaenichthys marmoratus, fig. 3-35), which is the only member of this large family to have commercial importance (Eschmeyer et al., 1983). The greenlings (family Hexagrammidae) are limited to temperate reefs of the north Pacific (Quast, 1965; Hart, 1973), where they are represented by, in addition to the ling cod introduced above, the kelp greenling (Hexagrammos decagrammus, fig. 3-36) and the painted greenling (Oxylebius pictus; fig. 3-37) Most of the poachers (family Agonidae) are fishes of deepwater sediment, but some are numerous, though inconspicuous, on cold-temperate reefs near shore. Examples off central and northern California are the kelp poacher (Agonomalus mozinoi) and the rockhead (Bothragonus swanii). All are small, cryptic, and sedentary, so generally go unnoticed by casual observation. They are distinctive in being covered by bony plates that meet but do not overlap. Where diets are known,

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F I G U R E 3-3 4 California scorpionfish, Scorpaena guttata.

F I G U R E 3-35 Cabezon, Scorpaenichthys marmoratus.

their major foods are microcrustacea (Hart, 1973; Eschmeyer et al., 1983).

P LE U RON ECTI FOR M E S

Two pleuronectiform families (as defined by Hensley and Ahlstrom, 1984), the Pleuronectidae and the Paralichthyidae, dominate near California shores. The Pleuronectidae are strictly temperate forms. Of the 20 species that occur in California (Eschmeyer et al., 1983), 17, including the C-O turbot, range only northward to various

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F I G U R E 3-3 6 Kelp greenling (male), Hexagrammos decagrammus.

F I G U R E 3-37 Painted greenling, Oxylebius pictus (from Hobson and

F I G U R E 3-3 8 Giant kelpfish, Heterostichus rostratus.

Chess 2001, with permission from Springer Science and Business Media).

locations across the North Pacific Rim between Alaska and Japan. The other three occur off southern California and Baja California; two also have isolated populations in the northern Gulf of California. There are no pleuronectids in the tropics. Though most of the Paralichthyidae worldwide are temperate species, the family has many ties to the tropics. Of the seven species that occur off California (Eschmeyer et al., 1983, who considered them bothids), only two, including the speckled sand dab, range north to Alaska. Furthermore, though the California halibut has been reported as far north as Washington, the other four range only southward—three into the Gulf of California, the fourth to Costa Rica. That paralichthyids have many tropical connections is also evident in that they have been considered a subfamily of the Bothidae, a family with many tropical representatives (e.g., Norman, 1934).

F I G U R E 3-3 9 Group of kelp perch, Brachyistius frenatus next to stipes of giant kelp, Macrocystis.

P E RCI F O R M E S

Most perciforms on reefs of southern California represent families that occur at least incidentally on tropical reefs. They include the sea basses (family Serranidae), grunts (family Haemulidae), croakers (family Sciaenidae), sea chubs (family Kyphosidae), damselfishes (family Pomacentridae), wrasses (family Labridae), labrisomids (family Labrisomidae), and gobies (family Gobiidae). All but one of these families are prominently represented in coral reef communities throughout the tropics (Hiatt and Strasburg, 1960; Hobson, 1974; Randall, 1967; Sano et al., 1984; Vivien, 1973). Labrisomids, the one exception, are mostly inhabitants of inorganic reefs in the Western Hemisphere tropics (Thomson et al., 1979; Nelson, 1994).

Two perciform families prominent off southern California— the clinids (family Clinidae) and the surfperches (family Embiotocidae)—vary from this pattern. Both are limited to temperate waters (Nelson, 1994), and they are also represented in reef communities throughout California. Among the clinids are the spotted kelpfish (fig. 3-12) and the giant kelpfish (Heterostichus rostratus; fig. 3-38); among the ubiquitous surfperches are the kelp perch (Brachyistius frenatus, fig. 3-39) and the shiner perch (Cymatogaster aggregata, fig. 3-40); nevertheless, although both families are strictly temperate, they have tropical affinities. The clinids are closely related to tropical labrisomids (George and Springer, 1980; Stepien, 1992), and

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F I G U R E 3-4 0 School of shiner perch, Cymatogaster aggregata.

an earlier study that combined the two groups (Hubbs, 1952) concluded that their origin was in the American tropics. Similarly, although the 21 species of surfperches are temperate forms (Eschmeyer et al., 1983), their closest relatives—the cichlids (family Cichlidae) and damselfishes—are tropical, and these three families, along with the tropical wrasses and parrotfishes (Scaridae), constitute the suborder Labroidei, a group with tropical origins (Kaufman and Liem, 1982). Although the great majority of California perciforms can be linked to tropical origins, there is no evidence of tropical connections for representatives of the perciform suborder Zoarcoidei (as defined by Nelson, 1994). These include the ronquils (family Bathymasteridae), the gunnels (family Pholidae), and the pricklebacks (family Stichaeidae)—all strictly coldwater families that dominate at high latitudes in the northeastern Pacific (Hart, 1973; Allen and Smith, 1988). Examples include the stripedfin ronquil (Rathbunella hypoplecta; fig. 3-41) and the kelp gunnel (Ulvicola sanctaerosae; fig. 3-42). These two are among the few representatives of this cold-water assemblage to occur southward into southern California.

Products of Other Evolutionary Lines Earlier in this chapter, it was noted that actinopterygians surviving each episode of global extinctions included evolutionary lines apart from the mainstream. Although lacking mainstream potential to diversify in new environments, these persisted— even dominated—under specific ecological circumstances. Following are examples of some now prominent off California. LOW E R TE LEOSTS

Evolutionary lines believed to have developed with the first major teleost radiation were classified by Gosline (1971) as “lower teleosts”, an assessment that would connect their early history with ecosystem resurgence from end-Triassic extinctions. These lines departed the mainstream with primitive features that proved adaptive in Mesozoic habitats and also enabled some to not only survive the end-Jurassic and end-Cretaceous extinctions, but also to persist with prominence into the present. Lower teleosts among modern marine fishes of California include clupeiforms (herrings, sardines, and anchovies), osmeriforms (smelts), and salmoniforms (salmon and anadromous trout). Clupeiforms are mostly small, silvery fishes that occur in midwater schools and feed on plankton. Modern representatives

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F I G U R E 3-41 Stripedfin ronquil, Rathbunella hypoplecta (from

Hobson 1994, with permission from Springer Science and Business Media).

F I G U R E 3-42 Kelp gunnel, Ulvicola sanctaerosae (from Hobson 1994,

with permission from Springer Science and Business Media).

include two species of the family Clupeidae—the Pacific herring (Clupea pallasi) and the California sardine (Sardinops sagax). Both occur in coastal waters of California and across the North Pacific Rim from Mexico to Asia. Another is the northern anchovy (Engraulis mordax, family Engraulidae), which is a major species from Baja California north to Canada (Eschmeyer et al., 1983). Osmeriforms have persisted based partly on features adaptive in the deep sea, but some modern species occur in coastal habitats (others in fresh water) at higher latitudes (Nelson, 1994). The order is represented off California by the smelts, family Osmeridae, which, like clupeiforms, are small silvery fishes that occur in schools and feed on zooplankton. Some marine osmerids spawn in shoreline turbulence, others enter rivers or streams to spawn in fresh water. Two of the former, the surf smelt (Hypomesus pretiosus) and the night smelt (Spirinchus starksi), enter the surf zone from Alaska to California (particularly off northern California) to spawn and lay eggs in coarse sand on an incoming tide. Both may spawn in the same areas, but the surf smelt does so by day, whereas the night smelt, as its name implies, does so at night (Eschmeyer et al., 1983). Among north-coast osmerids that ascend rivers to spawn in fresh water is the longfin smelt (Spirinchus thaleichthys; Eschmeyer et al., 1983). Salmoniforms in California marine habitats—the various salmon and anadromous trout of the family Salmonidae—are like certain osmeriforms in entering freshwater streams to

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(Cypselurus californicus, family Exocoetidae) generally occurs offshore at the surface (Eschmeyer et al., 1983). B AS I S OF TH E I R EVO LUTIONARY P E R S I STE NCE

F I G U R E 3-43 Topsmelt, Atherinops affinins.

spawn; salmonids have developed this habit far more than osmeriforms or any other group. Salmon of the genus Oncorhynchus and trout of the genus Salmo are particularly abundant in the northeast Pacific, where many coastal streams lead to appropriate spawning grounds. I NTE R M E DIATE TE LEOSTS

Evolutionary lines thought to have gained prominence with the resurgence from end-Jurassic extinctions are among those that Gosline (1971) identified as “intermediate teleosts.” Most had attained the acanthopterygian level of teleost development, with mainstream elements represent the series Percomorpha (as defined by Nelson, 1994). The first percomorphs were beryciforms, which, as recounted above, perpetuated the main line and subsequently gave rise to modern forms (the “higher teleosts” of Gosline, 1971). Concurrent with the evolution of percomorphs has been that of another set of acanthopterygian orders, grouped by Nelson (1994) as the series Atherinomorpha. These departed the mainstream based on features adapted to a pelagic setting and, unlike percomorphs, without evidence of reef involvement. Among atherinomorphs that have persisted to the present, atheriniforms (silversides) and beloniforms (needlefishes, halfbeaks, and flyingfishes) are prominently represented in California marine communities, whereas cyprinodontiforms are exceptionally abundant (and diverse) in tropical fresh waters and as aquarium fishes. California atheriniforms include species of the family Atherinidae: the topsmelt (Atherinops affinis), the jacksmelt (Atherinopsis californica), and the grunion (Leuresthes tenuis). These are elongate, silvery fishes that generally occur in schools and feed on zooplankton in the upper regions of the water column, but though topsmelt often dominate the canopy region of southern California’s kelp forests (fig. 3-43; Hobson et al., 1981), jacksmelt and grunion generally occur away from reefs. Grunion are distinctive in that they spawn by coming up onto beaches during spring and summer with a nocturnal rising tide to deposit eggs in the sand, mainly in southern California (Walker, 1952). Beloniforms are mostly fishes of warm seas, but several are abundant off southern California. Although a few species of the needlefish family Belonidae are large (a meter or more long) and piscivorous, most are like atherinids in being small and elongate silvery fishes that feed on zooplankton close to the surface. Two of the more common—the California needlefish (Strongylura exilis, family Belonidae) and the California halfbeak (Hyporhamphus rosae, family Hemiramphidae)—usually are close to shore, often in bays, whereas the California flyingfish

The continued success of these diverse evolutionary lines can be attributed to some combination of a few highly adaptive features. Foremost are the small size and pelagic habits that have enabled so many to feed on zooplankton, which probably represent the richest source of prey in the sea. In positioning themselves to feed on zooplankton in the water column, they become fully exposed to predators. I suggest that it was largely an adaptive response to this threat that virtually all have evolved as silvery fishes that occur in schools. Schools are to their advantage because predators are likely to have difficulty distinguishing targets from among flashing silver sides of schooling individuals (Hobson 1968, 1978). That these attributes have evolved independently in a variety of lineages is strong evidence that they are highly adaptive. Among lower teleosts, they characterize most clupeiforms and many osmeriforms; among intermediate teleosts, they characterize most atheriniforms and many beloniforms. Those that have evolved as piscivorous predators may gain another benefit from their silvery sides. According to Denton and Nicol (1962, 1965), light reflected from the sides of silvery fishes can project a mirror-like effect that renders the fish virtually invisible. This effect, however, requires that the fish be rigid and vertical, which questions its effectiveness as a defense for small fishes that occur in large schools—like clupeids and atherinids. The reason is that at any given time various individuals in such schools deviate from the vertical to produce highly visible flashes of reflected light. It is different, however, with large, silvery predators like needlefishes that hover in the water, as these tend to be rigidly vertical when stalking prey. So even though California needlefish may grow to a meter in length and are fully exposed while approaching prey in open water, they may go unseen by their quarry before the attack. Certain of these lines probably owe their persistence to highly distinctive means of reproduction that allow vulnerable early life-history stages to avoid the marine environment near shore. That grunion leave the sea to deposit eggs under beach sand is a clear indication that eggs are at particularly high risk in coastal waters. Similar though less extreme habits define many of the osmerids; for example, eggs of surf smelt and night smelt are deposited in sand under turbulence of waves breaking on shore. Even more telling are the habits of anadromous salmonids and osmerids that leave the marine environment to spawn in fresh water—presumably finding there more secure settings during vulnerable periods of early life, from eggs through early juveniles. The highly refined behavior that leads salmon and certain trout from the sea to specific streams certainly indicates exceptionally strong selection for means to escape problems with spawning in coastal marine waters. Problems associated with reproducing near shore in the sea have profoundly influenced behavior, morphology, and distribution among a wide variety of California’s marine fishes, as discussed further in sections that follow.

Determinants of Species Composition in California Marine Communities Based on the evolutionary history of the mainstream, recounted above, it is evident that virtually all acanthopterygian

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lines can be traced to tropical origins; nevertheless, the distribution of California fishes shows that some developed more readily than others at higher latitudes. That generalized carnivores with trophic features widely adaptive in nearshore habitats have more poleward mobility than species with feeding adaptations developed on coral reefs explains the dominance of scorpaeniforms, pleuronectiforms, and zoarcoid perciforms in California’s cold-temperate habitats. But what about species composition of communities in warm-temperate habitats south of Point Conception? It is well known that species in California’s warm-temperate communities represent a mix of temperate and tropical lineages (Ebeling and Bray, 1976; Hobson et al., 1981), but less appreciated is the extent that tropical lineages dominate. Of 34 teleost species recorded on transects at Santa Catalina Island during all seasons over three years (9/72–9/75: Hobson and Chess, 1986, 2001), all 24 perciforms and one scorpaeniform (California scorpionfish) are of tropical stock. Clearly their tropical connections did not prevent adapting to warmtemperate conditions; in fact their dominance in communities off southern California might be taken as a contradiction to the notion that advanced perciforms have been limited in poleward distributions by early ties to coral reefs. That there is greater poleward mobility in evolutionary lines unrestricted by coral reef connections does not mean that coral reef fishes are inherently incapable of acquiring tolerance for temperate conditions or evolving as temperate species; to the contrary, it is clear that many have done so. Although earlier in the chapter it was proposed that evolutionary lines originating with expanding coral reef communities early in the Tertiary were likely to have started with obligate ties to these communities, it was later pointed out that many of these ties were weakened or eliminated by subsequent evolutionary processes—particularly in the highly variable environments off continental shores. Consider the species of tropical lineages now dominant in the warmtemperate habitats of southern California. Presumably many evolved from progenitors of coral reef stock that had previously lost whatever obligatory connections their early ancestors may have had to coral reefs. The grunt family Haemulidae was cited as representing numerous examples, and, two grunts—the sargo (Anisotremus davidsoni) and salema (Xenistius californiensis)—range northward from the Gulf of California to prominence through southern California. But tropical species of coral reef stock would not have expanded their lines to temperate latitudes without both an incentive and a mechanism. The incentive could well have been the great store of food resources readily available at higher latitudes. Organisms of types consumed by tropical reef fishes are (and presumably were) more accessible at higher latitudes. Sessile invertebrates are less cryptic and noxious in temperate regions than in the tropics (e.g., Bakus and Green, 1974; Jackson et al., 1971), and zooplankton of types taken by diurnal planktivores are more numerous near kelp forests of southern California than above coral reefs of the tropical Pacific (Hobson and Chess, 1976, 1978). Macrovegetation, too, generally is more abundant and accessible at temperate latitudes than in the tropics. Fishes that feed on such forms in the tropics would gain great trophic benefit by extending their distributions poleward. The mechanism that enabled certain lines of tropical fishes to become established at temperate latitudes was likely to have involved the latitudinal shifts in isotherms that have periodically extended tropical conditions toward the poles since

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Miocene time. It has been suggested that certain families and genera of tropical invertebrates produced temperate representatives this way (Smith, 1919; Durham, 1950), and similar histories can be inferred for certain fishes. Representatives of the perciform suborder Labroidei have been particularly successful as temperate derivatives of tropical stock. These include the blacksmith and garibaldi (family Pomacentridae); the rock wrasse, senorita, and sheephead (family Labridae); and many of the surfperches (family Embiotocidae), including the kelp perch, shiner perch, black perch, and pile perch (Hobson and Chess, 1976, 1986, 2001). Although relatively few in species compared to tropical labroids, the great numbers of individuals involved is the main reason that tropical derivatives dominate in the warmtemperate communities of southern California. The great success that labroids have had in warm-temperate habitats is based largely on feeding capabilities inherited from tropical progenitors. Of particular benefit are the relatively small, adaptable mouths and highly evolved pharyngeal dentition that characterize the group. These features, used together, enable feeding on the minute shelled organisms that are so abundant and exposed on California reefs. Among such prey are bryozoans, ascidians, and ophiuroids (Quast, 1968; Bray and Ebeling, 1975; Hobson and Chess, 2001). Although tropical representatives of these invertebrate groups are important prey of labroids on coral reefs (Randall, 1967; Hobson, 1974; Sano et al., 1984), temperate representatives constitute a larger proportion of labroid diets on warmtemperate reefs (e.g., Hobson and Chess, 2001), probably because their defenses are less developed there. It has been suggested that benthic invertebrates are more cryptic and noxious in the tropics than in temperate regions because threats from predatory fishes increase toward the equator (e.g., Bakus, 1969, 1981; Bakus and Green, 1974; Jackson et al., 1971). This suggestion has been criticized because supporting evidence is perceived as lacking (e.g., by Jones et al., 1991), but I accept it as a valid—and important— generalization based on finding that though many fishes of tropical stock are equipped to feed on these organisms, fishes of temperate stock typically are not. Despite the great abundance, variety, and ready availability of algae in temperate habitats, there are no herbivores of the more advanced perciform lines there. Two herbivores of tropical stock—the opaleye and halfmoon—are prominent in warm-temperate communities, but both are kyphosids and so considered among the more primitive perciforms (Nelson, 1994); the label “herbivore” is applied to them somewhat loosely because their diets also include invertebrates (Quast, 1968; Hobson and Chess, 2001). There has been much speculation why there are so few herbivorous fishes at higher latitudes, considering the widespread abundances of benthic algae there (Horn, 1989). Reports have implicated problems with vegetation as food in temperate habitats. One suggested that fishes are ineffective in digesting plant tissues at low water temperatures (Gaines and Lubchenko, 1982), and another that fishes have difficulty processing the coarse tissues of temperate algae (Bakus, 1969). And still another proposed that production rates of turf algae at temperate latitudes are too low to meet the needs of herbivorous fishes (Choat, 1991). These suggestions identify forces of natural selection likely to be at work on temperate herbivores, but the primary reasons that there are so few fishes among them probably transcend factors related specifically to herbivory. This follows from the fact that carnivorous groups closely related to

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tropical herbivores are similarly limited in occurrences at higher latitudes (Hobson, 1994; Hobson and Chess, 2001). Most perciforms of tropical stock that dominate the reef communities of southern California are sharply limited in their distributions farther north. The boundary between warm-temperate and cold-temperate regions of the northeastern Pacific generally is considered at Point Conception (Briggs, 1974; Horn and Allen, 1978), which is essentially the northern limit of perciforms of coral reef stock. Although habitats northward from there to Monterey represent a zone of transition irregularly frequented by southern forms, reef communities north of the Point tend to be dominated by perciforms of temperate heritage, such as the ronquils, pricklebacks, and gunnels. The obvious question is, why have perciforms with tropical affinities apparently been excluded from north-coast habitats, especially considering their dominance in habitats to the south? If the incentive for labroids to become established in warm-temperate communities was the wealth of foods available to them there, as I have suggested, then why have they not responded similarly to the even greater wealth of the same foods farther north? Consider the labroids that Hobson and Chess (2001) found dominant as benthivorous carnivores in south-coast habitats—the garibaldi, rock wrasse, senorita, sheephead, pile perch, black perch, and rubberlip perch. Of these, only the last three, which are embiotocids, ordinarily range into northern California. And of the labroids that Hobson and Chess (1976) found highly successful diurnal planktivores—the blacksmith, kelp perch, and shiner perch— only the last two, which are embiotocids, regularly occur along the north coast. In addition, neither of the two warm-temperate herbivores—the opaleye and the halfmoon—normally occurs in north-coast communities. Clearly the surfperch family Embiotocidae is exceptional. This group originated in California (Tarp, 1952), so it is not surprising that representatives are broadly adapted to conditions throughout the region. Embiotocids inhabiting the north coast are able to use the highly adaptive labroid trophic capabilities to access feeding opportunities generally unavailable to species of temperate stock. The result has been what may be the most trophically diverse family of marine fishes. For example, the kelp perch is a diurnal planktivore, with features similar to certain highly evolved tropical perciforms specialized for this habit, whereas the walleye surfperch schools by day and feeds on the larger crustacea that enter the water column only at night, just like certain basal percoids (Hobson and Chess, 1976, 1986; Ebeling and Bray, 1976). The white seaperch (Phanerodon furcatus) and the sharpnose seaperch (Phanerodon atripes) are benthivorous carnivores that pluck tiny organisms from a substrate, the latter often taking ectoparasites from the bodies of other fishes (Hobson, 1971; Ebeling and Bray, 1976). The shiner perch has exceptionally broad feeding habits that include both planktivory and benthivory, day and night, at different periods of adult life (Hobson et al. 1981). The black perch and the rubberlip perch have exceptionally broad diets based on their specialized abilities to winnow edible material from mouthfuls of the benthos (Laur and Ebeling, 1983; Hobson and Chess, 1986), and the pile perch has massive (for a surfperch) pharyngeal teeth that are used to crush shells of mollusks and brittlestars (Laur and Ebeling, 1983). The list goes on to include all 18 species of surfperches that occur off California shores, each with features suited to a distinctive diet. It is a radiation that demonstrates the adaptive potential of the group (DeMartini, 1969) and also the

F I G U R E 3-4 4 Wolf eel, Anarrhichthys ocellatus. (Photo: Tony Chess,

from Hobson 1994, with permission from Springer Science and Business Media.)

availability, in temperate habitats, of feeding opportunities generally unavailable to fishes of temperate stock. Although fishes of temperate stock generally lack the trophic capabilities needed to feed on sessile invertebrates, zooplankton, and benthic plants so abundantly accessible in north-coast habitats, there are striking exceptions. Among these are a number of zoarcoid and trachinoid perciforms that have acquired trophic capabilities more characteristic of tropical species. For example, the wolf eel (Anarrhichthys ocellatus, family Anarhichadidae, fig. 3-44), a zoarcoid perciform, uses highly specialized teeth to feed on heavily shelled invertebrates (Hart, 1973). The Pacific sand lance (Ammodytes hexapterus, family Ammodytidae), a trachinoid perciform, is a highly successful diurnal planktivore (Hart, 1973; Hobson, 1986). Other exceptions include the monkeyface prickleback (Cebidichthys violaceus) and the rock prickleback (Xiphister mucosus), which are blennioid perciforms (family Stichaeidae) that have acquired abilities to feed on vegetation (Montgomery, 1977; Horn et al., 1982). Although these species have feeding abilities that are highly adaptive in temperate habitats, they are atypical of their families and represent trophic types that generally are poorly developed among fishes of temperate stock. Fishes of temperate affinities have fewer limitations in southern occurrences. This assessment agrees with Horn and Allen (1978), who concluded, based on an analysis of published range limits, that Point Conception is less of a boundary for northern species than for southern ones. Northern dominants occur more widely in the south than southern dominants do to the north, although the southern occurrences for some northern forms are in deeper water or at points of coastal upwelling (Hubbs, 1948); for example, the dominant embiotocid in the reef communities of northern California—the striped seaperch (Embiotoca lateralis)—is sparsely distributed through southern California but abundant in the vicinity of upwelling near Punta Banda in northern Baja California, Mexico. Even more telling are the many species of temperate stock most abundant or even limited to southern habitats. Included are at least two rockfishes (genus Sebastes)—the treefish and the kelp rockfish—along with a number of the sculpins, such as the lavender sculpin (Leiocottus hirundo, fig. 3-45) and the roughcheek sculpin, Artedius creaseri (Eschmeyer et al., 1983). These distributions are exceptions to the general pattern, however. More

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F I G U R E 3-45 Lavender sculpin, Leiocottus hirundo (from Hobson and

Chess 2001, with permission from Springer Science and Business Media).

F I G U R E 3-4 6 China rockfish, Sebastes nebulosus.

typical of those with temperate affinities is the china rockfish (Sebastes nebulosus, fig. 3-46), which ranges southward from Alaska to southern California—but is abundant only through northern California (Love et al., 2002). So it is evident that fish communities in the region of Point Conception are affected by a northward decline in species of tropical stock and by a southward decline in species of temperate stock. It was to demonstrate resulting effects on these communities that for many years Professor Boyd Walker of UCLA led his students, me among them, to sites near Morro Bay, 90 miles north of the Point. There, collections of the fishes near shore included many ronquils, pricklebacks, gunnels, and poachers—species with northern affinities that were sparsely represented in collections from south of the Point (records of the UCLA Fish Collection now at the Los Angeles County Museum of Natural History). Direct observations of communities north and south of the Point show a sharper faunal break than indicated by published range limits of the species (e.g., Horn and Allen, 1978), which too often represent individuals that have strayed (or were carried) beyond limits of conditions favorable for their species. The differences in species composition of communities north and south of Point Conception (as well as at other locations along the coast) have been attributed to differences in sea temperatures (e.g., by Horn and Allen), and certainly temperatures are important. That occurrences of various northern species in the south tend to be in deeper water or at centers of upwelling presumably is related to temperature (Hubbs, 1948).

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Temperatures alone, however, cannot account for this break in the fauna. Certainly temperatures are important in setting immediate limits to the distribution of species, but evolutionary processes can modify these limits when there are adaptive advantages in doing so. The complex physiological adjustments involved in shifting tolerance limits for temperature have been made many times, as in those tropical lineages that range widely over latitude. An example is the tropical gobiid genus Coryphopterus, which has representatives throughout the tropical eastern Pacific (Thomson et al.,1979). One species of this genus that is abundant off southern California, the blackeye goby, has a published poleward limit of northern British Columbia (Eschmeyer et al., 1983), and I have seen it in southeastern Alaska. So although responses to temperature may be the means by which existing species maintain spatial relations with the Point, the advantage of doing so must lie elsewhere. Certainly any such advantage must be great because it would be shared by a diverse assortments of species highly varied in their evolutionary histories. A likely basis for the faunal break at Point Conception is the prevailing pattern of surface currents (Hobson, 1994). To the north, surface currents associated with coastal upwelling flow seaward during most of the year (Bakun et al., 1974), while to the south, the usual condition is a closed cyclonic eddy (Reid et al.,1958). These two systems are vastly different in ways that must influence the eggs, embryos, and larvae of fishes that expose their early life-history stages to the environment. In developing a case for the importance of hydrographic features to the distribution of these fishes, Cowen (1985) concluded that warm-temperate species are prevented from ranging northward into the cold-temperate region by currents that carry their larvae southward. Species of tropical stock may be able to exercise their trophic capabilities in warm temperate habitats of southern California only because they experience favorable surface currents in that region. Most release their eggs into the water column (Breder and Rosen, 1966), which is a highly adaptive feature of reproduction under conditions in which their coral reef progenitors developed, as noted above. This mode of egg development is unsuited to coastal waters of the northeast Pacific, however, because offshore currents associated with coastal upwelling would carry them to unfavorable environments. Among families with this limitation are the serranids (e.g., kelp bass), haemulids (salema and sargo), sciaenids (e.g., croakers and queenfish), labrids (senorita, rock wrasse, and sheephead), and kyphosids (halfmoon and opaleye). The eggs and larvae produced by species of these families are pelagic (Breder and Rosen, 1966), and therefore are poorly suited to north-coast conditions. Some families of tropical derivation produce benthic eggs, and these have had mixed success in extending their distributions northward. The pomacentrids (blacksmith, garibaldi) deposit adhesive eggs in nests on reefs but have failed to populate the north coast, perhaps because their lunar hatching schedule ( Johannes, 1978) is inappropriate in a strong upwelling system. Others do well in cold-temperate habitats, however, including certain clinids (e.g., kelpfishes of the genus Gibbonsia) and gobiids (e.g., blackeye goby). The fishes of cold-temperate communities north of Point Conception typically show major adaptations to counter the possibility that their eggs, embryos, and larvae may be carried in surface currents to unfavorable settings. As Parrish et al. (1981) pointed out (p. 175), “The fishes spawning in this region have a wide range of reproductive strategies that reduce

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the planktonic phase of early life history.” Some species avoid these problems with adaptive behavior as adults. For example, many species with pelagic habits off central and northern California, such as the jack mackerel, Trachurus symmetricus (family Carangidae), migrate southward to reproduce off southern California, and certain pleuronectiforms migrate into deeper water beyond reach of surface currents (Parrish et al., 1981). But most species that inhabit California’s coldtemperate marine habitats lack the capacity for such migrations and so have acquired modes of reproduction adapted to north-coast conditions. The pelagic egg represents the point in early life history most vulnerable to unfavorable surface currents, and virtually all north-coast fishes have acquired ways to keep their eggs out of the water column. The scorpaeniform rockfishes have an especially effective mechanism wherein fertilization is internal and the female retains the eggs throughout their development—a practice that probably contributes to the group’s extraordinary success in the northeast Pacific. Most of the other reef fishes in this region produce benthic eggs, including such scorpaeniforms as sculpins and greenlings, as well as such perciforms as clinids, gobies, ronquils, gunnels, and pricklebacks (Breder and Rosen, 1966). Moreover, though tropical reef fishes that produce benthic eggs coordinate spawning with lunar phases and therefore tidal currents (Johannes, 1978), fishes that do so in temperate communities of the northeastern Pacific coordinate with seasonal patterns of coastal upwelling (Parrish et al., 1981). The coastal osmeriforms have other ways of protecting their eggs, as noted above. That the surf smelt and night smelt find it adaptive to enter the north-coast surf zone and deposit their eggs in course sand under breaking waves—a highly rigorous setting—represents strong evidence that eggs are at risk in the nearshore water column there. Such measures effectively protect the eggs, but the eggs of most hatch as planktonic larvae, which are similarly vulnerable to unfavorable transport. To limit this problem, a majority of these species put their larvae into the environment during winter, when shoreward surface transport is most likely. And the larvae of many, including various sculpins, pricklebacks, and gunnels, resist being carried offshore (into the southward flowing California Current) by schooling close to rocks and other benthic structures (Marliave, 1986). At least some that cannot escape unfavorable surface currents descend to more favorable transport in deeper currents (Parrish et al., 1981). These adaptations limiting unfavorable transport of larvae would seem less effective than the adaptations that limit unfavorable transport of eggs, but larvae have less need for them because they have at least some control over their movements. Probably it is mainly to remove early life stages from problems they would experience near shore in the sea that marine salmonids and some osmerids spawn in fresh water. If so, the complexity of behavior and physiological adjustments that have evolved shows that these problems are profound. Furthermore, it is clear that the problems are particularly acute in the northeast Pacific because that is where the species involved are concentrated. The most effective means of keeping early life-history stages out of the nearshore water column, however, has developed in the embiotocids. The surfperches avoid unfavorable transport of eggs and larvae by retaining these in the pregnant female throughout their development and delivering the young as small adults (Baltz, 1984). The males of Micrometrus spp. are

sexually mature at birth (Hubbs, 1921; Schultz, 1993). Clearly, this has been the key to their widespread success in the coastal waters of the northeast Pacific. It has been largely through their viviparity that members of this family have gained access to exceedingly rich trophic resources largely unavailable to other species of tropical heritage (Hobson, 1994). As a result, Point Conception has been less of a barrier to species of this family than to species of the other major nearshore families— both temperate and tropical.

Perspectives on the California Condition S PATIAL

Many of the determinants of species composition in California’s reef communities have global relevance, but others are limited to the western shore of North America. Differing oceanic conditions account for much of the variation between regions. The coastal upwelling system off California and Oregon, for example, creates conditions intolerable to most fishes of tropical stock poleward of about 35°N, the latitude of Point Conception. Different circumstances, however, exist on the eastern side of the continent. There, a wide variety of tropical fishes routinely occur in high-latitude communities influenced by the Gulf Stream, and tropical derivatives such as the cunner (Tautogolabrus adspersus; family Labridae) are established above 45°N (Scott and Scott, 1988). Other differences are evident in temperate communities of the southwest Pacific, where species of the order Tetraodontiforms are prominent components of coastal marine communities (Ayling and Cox, 1982). This order is now represented in California marine communities only by rare occurrences in the southernmost of puffers (family Tetraodontidae) and porcupine fish (family Diodontidae). At the outset of this chapter, it was noted that the Perciformes, Scorpaeniformes, and Pleuronectiformes—the dominant orders represented among California fishes—are three of the four most recently evolved orders of fishes. In making this assessment, Nelson (1994) identified the fourth as the Tetraodontiformes; he regarded the tetraodontiforms as the most recently evolved of all. Only one tetraodontiform is common in coastal waters off California, however. This is the ocean sunfish (Mola mola; family Molidae), which has pelagic habits but often occurs close to shore. TE M P ORAL

The species composition of teleost fishes in California marine communities, therefore, is the product of a continuum of interactions among species and their environment over evolutionary time. There is a natural tendency to consider the current condition as an end point, and certainly it represents a culmination of all that has gone before. But, just as the condition today is forever different from that of yesterday, tomorrow’s condition will be forever different from that of today. Constant change is the norm, but it is change constrained within limits set by features of ecosystems that have been stable for tens of millions of years. The history of life on the earth, however, has shown that this stability is finite.

Acknowledgments For inspiration, guidance, and friendship, I am thankful for having known Boyd Walker, Al Tester, and Bill Gosline.

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Horn, M. H., S. N. Murray, and T. W. Edwards. 1982. Dietary selectivity in the field and food preferences in the laboratory for two herbivorous fishes (Cebidichthys violaceous and Xiphister mucosus) from a temperate intertidal zone. Mar. Biol. 67:237–246. Hubbs, C.L. 1921. The ecology and life-history of Amphigonopterus aurora and of other viviparous perches of California. Biol. Bull. 40:181–209. ———. 1945. Phylogenetic position of the Citharidae, a family of flatfishes. Univ. Mich. Mus. Zool., Misc. Publ. 63:1–38. ———. 1948. Changes in the fish fauna of western North America correlated with changes in ocean temperature. J. Mar. Res. 7:459–482. ———. 1952. A contribution to the classification of the blennioid fishes of the family Clinidae, with a partial revision of the eastern Pacific forms. Stanford Ichthyol. Bull. 4:41–165. Ivlev, V. S. 1961. Experimental ecology of the feeding of fishes. Yale University Press, New Haven. Jackson, J.B.C., T.F. Goreau, and W.D. Hartman. 1971. Recent brachiopod-coralline sponge communities and their paleontological significance. Science 173:623–625. Johnson, G.D. 1993. Percomorph phylogeny: progress and problems. Bull. Mar Sci. 52(1):3–28. Johannes, R.E. 1978. Reproductive strategies of coastal marine fishes in the tropics. Environ. Biol. Fish. 3:65–84. Jones, G.P., D. J. Ferrell, and P.F. Sale. 1991. Fish predation and its impact on the invertebrates of coral reefs and adjacent sediment. In P. F. Sale (ed.), The ecology of fishes on coral reefs. Academic Press, San Diego, pp. 156–179. Kauffman, E.C., and C.C. Johnson. 1988. The morphological and ecological evolution of middle and upper Cretaceous reef-building rudistids. Palaios 3:194–216. Kaufman, L.S., and K.F. Liem. 1982. Fishes of the suborder Labroidei (Pisces: Perciformes): phylogeny, ecology, and evolutionary relationships. Breviora 472:1–19. Kendall, A.W. 1976. Predorsal and associated bones in serranid and grammistid fishes. Bull. Mar. Sci 26:585–592. Kotlyar, A.N. 1985. Taxonomy and distribution of Monocentridae (Beryciformes). J. Ichthyol. 25(4):91–104. Kotrschal, K. 1988. Evolutionary patterns in tropical marine reef fish feeding. Z. Zool. Syst. Evolut. Forsch. 26:51–64. Lauder, G.V., and K.F. Liem. 1983. The evolution and interrelationships of the actinopterygian fishes. Bull. Mus. Comp. Zool. 150:95–197. Laur, D.R., and A.W. Ebeling. 1983. Predator-prey relationships in surf perches. Environ. Biol. Fish. 8:217–229. Li, S.Z. 1981. On the origin, phylogeny and geographical distribution of the flatfishes (Pleuronectiformes). Trans. Chin. Ichthyol. Soc. 1981:11–20. Long, J.A. 1995. The rise of fishes. John Hopkins University Press. Love, M.S., A. Brooks, D. Busatto, P. Gregory, and J. Stephens. 1996. Aspects of the life histories of the kelp bass, Paralabrax clathratus, and the barred sand bass, P. nebulifer, from the southern California bight. U. S. Fish. Bull. 94:472–481. Love, M.S., M. Yoklavich, and L. Thorsteinson. 2002. The rockfishes of the Northeast Pacific. University of California Press, Berkeley. MacArthur, R.H. 1969. Patterns of communities in the tropics. Biol. J. Linn. Soc. 1:19–30. Marliave, J.B. 1986. Lack of planktonic dispersal of rocky intertidal fish larvae. Trans. Am. Fish. Soc. 115:149–154. McCosker, J.E., and R.H. Rosenblatt. 1987. Notes on the biology taxonomy and distribution of the flashlights fishes (Beryciformes: Anomalopidae). Jpn. J. Ichthyol. 34:157–164. McFarland, W.N. 1991. The visual world of coral reef fishes. In P. F. Sale (ed.), The ecology of fishes on coral reefs. Academic Press, San Diego, pp.16–38. McLaren, D. J., and W.D. Goodfellow. 1990. Geological and biological consequences of giant impacts. Ann. Rev. Earth Planet. Sci. 18: 123–171. Mead, G.M. 1970. A history of South Pacific fishes. In W. W. Wooster (ed.), Scientific Exploration of the South Pacific. National Academy of Science, Washington, DC, pp. 236–251. Montgomery, W.L. 1977. Diet and gut morphology in fishes, with special reference to the monkeyface prickleback, Cebidichthys violaceus (Stichaeidae: Blennioidei). Copeia 1977:178–182. Motta, P. J. 1984. Functional morphology of the head of Hawaiian and mid-Pacific butterfly fishes (Perciformes, Chaetodontidae). Environ. Biol. Fish. 13:253–276. Nelson, J.S. 1994. Fishes of the world, 3rd ed. John Wiley, New York.

EVOLUTION

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Newell, N.D. 1971. An outline history of tropical organic reefs. Am. Mus. Novitates 2465:1–37. Norman, J.R. 1934. A systematic monograph of the flatfishes (Heterosomata) 1. British Museum of National History, London. O’Keefe, J.D., and T. J. Aherns. 1989. Impact production of CO2 by the bolide and the resultant heating of the earth. Nature 338:247–249. Paine, R.T. 1966. Food web complexity and species diversity. Am. Nat. 100:65–75. Parrish, R.H., C.S. Nelson, and A. Bakun. 1981. Transport mechanisms and reproductive success of fishes in the California Current. Biol. Oceanogr. 1:175–202. Patterson, C. 1964. A review of Mesozoic acanthopterygian fishes, with special reference to those of the English Chalk. Philos. Trans. R. Soc. London. Ser. B. Biol. Sci. 247:213–482. Patterson, C. 1993. An overview of the early fossil record of acanthomorphs. Bull. Mar. Sci. 52:29–59. Quast, J.C. 1965. Osteological characteristics and affinities of the hexagrammid fishes, with a synopsis. Proc. Calif. Acad. Sci. Ser. 4, 31:563–600. Quast, J.C. 1968. Observations on the food of the kelp-bed fishes. pp. 109– 142. In W. J. North and C.L. Hubbs (ed.), Utilization of Kelp-Bed Resources in Southern California. Calif. Dep. Fish Game, Fish Bull. 139. Randall, J.E. 1967. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanogr. 5:665–847. Randall, J.E., and V.E. Brock. 1960. Observations on the ecology of epinepheline and lutjanid fishes of the Society Islands, with emphasis on food habits. Trans. Am. Fish. Soc. 89:9–16. Raup D.M., and J.J. Sepkowski. 1982. Mass extinctions in the marine fossil record. Science 215:1501–1503. Reid, J.L., G.I. Roden, and J.G. Wyllie. 1958. Studies of the California Current system. CalCOFI Prog. Rep., 1 July 1956 to 1 Jan. 1958:27–90. Romer, A.S. 1966. Vertebrate paleontology. University of Chicago Press, Chicago. Rosenblatt, R.H. 1967. The zoogeographic relationships of the marine shore fishes of tropical America. Studies Trop. Oceanogr. Miami 5:579–592. Rosenblatt, R. H., J. E. McCosker, and I Rubinoff. 1972. Indo-West Pacific fishes from the Gulf of Chiriqui, Panama. Nat. Hist. Mus. Los Angeles Cty. Contrib. Sci. 234:1–18. Sale, P.H. 1977. Maintenance of diversity in coral reef fish communities. Am. Nat. 111:337–359. ———. 1991. Reef fish communities: open nonequilibrium systems. In P. F. Sale (ed.), The ecology of fishes on coral reefs. Academic Press, San Diego, pp. 564–598. Sano, M., M. Shimizu, and Y. Nose. 1984. Food habits of teleostean reef fishes in Okinawa Island, southern Japan. Univ. Mus. Univ. Tokyo Bull. 25. Schaeffer, B., and D.E. Rosen. 1961. Major adaptive levels in the evolution of the actinopterygian feeding mechanism. Am. Zool.1: 187–204. Schpigel, M., and L. Fishelson. 1989. Food habits and prey selection of three species of groupers from the genus Cephalopholis (Serranidae: Teleostei). Environ. Biol. Fish. 24:67–73.

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Schultz, E.T. 1993. Sexual size dimorphism at birth in Micrometrus minimus (Embiotocidae): a prenatal cost of reproduction. Copeia 1993: 456–463. Scott, R.W. 1988. Evolution of late Jurassic and early Cretaceous reef biotas. Palaios 3:184–193. Schaeffer, B., and D.E. Rosen. 1961. Major adaptive levels in the evolution of the actinopterygian feeding mechanism. Am. Zool. 1:187–204. Sepkoski, J. J., Jr. 1986. Phanerozoic overview of mass extinctions. In D.M. Raup and D. Jablonski (eds.), Patterns and processes in the history of life. Springer-Verlag, Berlin, pp. 277–295. Smith, C.L., and J.C. Tyler. 1972. Space resource sharing in a coral reef fish community, In B.B. Collette and S.A. Earle (eds.), Results of the Tektite Program: ecology of coral reef fishes, Nat. Hist. Mus. Los Angeles Cty. Sci. Bull. 14, pp. 125–178. Smith, J.P. 1919. Climatic relations of the Tertiary and Quaternary faunas of the California region. Proc. Calif. Acad. Sci. 9:123–173. Squires, D.F. 1959. Results of the Puritan-American Museum of Natural History expedition to Western Mexico, 7. Corals and coral reefs in the Gulf of California. Bull. Am. Mus. Nat. Hist. 118:371–431. Stanley, S.M. 1987. Extinction. Scientific American Books, New York. ———. 1989. Earth and life through time. W. H. Freeman, New York. Stephens, J.S., and K.E. Zerba. 1981. Factors affecting fish diversity on a temperate reef. Environ. Biol. Fish. 6:111–121. Stepien, C.A. 1992. Evolution and biogeography of the Clinidae (Teleostei: Blennioidei). Copeia 1992:375–392. Tarp, F.H. 1952. A revision of the family Embiotocidae (the surfperches). Calif. Dep. Fish Game, Fish Bull. 88. Thomson, D.A., L.T. Findley, and A.N. Kerstitch. 1979. Reef fishes of the Sea of Cortez. Wiley-Interscience, New York. Vivien, M.L. 1973. Contribution a la connaissance de la l’ethologie alimentaire de l’ichthyofauna du platier interne des recifs coralliens de Tulear (Madagascar). Tethys Suppl. 5:221–308. Walker, B.W. 1952. A guide to the grunion. Calif. Fish Game 38:409–420. ———. 1960. The distribution and affinities of the marine fish fauna of the Gulf of California. Symposium: the biogeography of Baja California and adjacent seas. Syst. Zool. 9(3–4):123–133. ———. 1966. The origins and affinities of the Galapagos shore fishes. In R.I. Bowman (ed.), The Galapagos. University of California Press, Berkeley, pp. 172–174. Ward, P.D, J.W. Haggart, E.S. Carter, D. Wilbur, H.W. Tipper, and T. Evans. 2001. Sudden productivity collapse associated with the Triassic-Jurassic boundary mass extinction. Science 292:1148–1151. Werner, W.E., and D. J. Hall. 1974. Optimal foraging and the size selection of prey by the blue gill sunfish (Lepomis macrochirus). Ecology 55:1042-1052. Wood, R. 1999. Reef evolution. Oxford University Press. Zaret, T. M. 1980. Predation and freshwater communities. Yale University Press, New Haven. Ziegler, A. M., M. L. Hulver, A. L. Lottes, and W. F. Schmachtenberg. 1984. Uniformatarianism and paeleoclimates: inferences from the distribution of carbonate rocks. In P. J. Brenchley (ed.), Fossils and climate. Wiley-Interscience, New York, pp. 3–26.

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CHAPTER 4

Ecological Classification LAR RY G. ALLE N AN D DAN I E L J. P O N D E LLA I I

Introduction The marine environment off the California coastline supports a diverse ichthyofauna consisting of northern, cold water (Oregonian) and southern, warm water (San Diegan) fish species as well as Panamic species primarily from Cortez Province (Horn and Allen, 1978). To a large extent, this high faunal diversity reflects the great variety of marine habitats that are available to fishes within the expansive latitudinal range covered by California proper and Baja California (e.g., bays and estuaries, nearshore soft bottom, shelf, slope, rocky intertidal, kelp beds, shallow and deep rocky reefs, as well as pelagic habitats) (Horn, 1980). Fortunately, the fishes of these various California habitats have been the subject of numerous ichthyofaunal studies (see table 4-1) during the past 40 years. These studies allow us to ask and begin to answer one of the most fundamental questions of all, “Which fishes occur where in California’s marine waters?” In the Californias, marine fishes are readily quantifiable by various techniques and, in terms of taxonomy, are relatively well understood compared to other groups of organisms. Data from these ecological and fishery surveys can be applied easily to models of numerical ecology. For these reasons, the descriptions of marine habitats and inferences about them can be made using data obtained from the study of these fishes. In fact, the major biogeographical provinces in the tropical eastern Pacific have been described using information from fish surveys (Hastings, 2000). More specifically, this chapter will seek to answer the following questions: 1. What are the basic types of marine fish habitats that occur off California? 2. Which types of fishes tend to occur in these habitats? 3. Which types of fishes are most abundant or otherwise distinctive to the different habitats? 4. Which physical attributes define these habitats and how might these influence the fishes there? 5. Are all species linked to particular habitats or are there habitat generalists? 6. Which families and orders of fishes are best represented overall in the various habitats and the fish fauna?

7. How many different species occur in the various habitats and in what relative abundance? 8. Why are there more species in some habitats than in others? The analysis presented here represents the first attempt at a coastwide synthesis of information about all California marine fish species and their habitats. To address these general questions, this chapter will (1) present a quantitative classification of marine habitats off California, based on the affinities of their fish assemblages; (2) present a quantitative classification of fish species according to habitat affinity; and (3) describe the general patterns of diversity within the various habitat types and attempt to explain them.

The Approach This analysis is an extension of that reported in Allen (1985) for the fishes and habitats of southern California nearshore waters. However, the present analysis greatly extends the latitudinal, depth, and offshore range of the previous study. Data on species composition and relative abundances of fishes from 168 locales from 77 ichthyofaunal studies (table 4-1) of all marine habitats except those of the meso- and bathypelagic zones were compiled for analysis. These quantitative studies ranged in latitude from Eureka in northern California south to Isla Asuncion on the mid-Pacific coast of Baja California (fig. 4-1). Relative abundances of species in each study were expressed as the percentage that the species represented in the total number of individuals (juveniles and adults could not be distinguished). For a species to be included in the analysis, it must have had a relative abundance of
0.1% in the study. The species abundances were, therefore, standardized to 100% in each study for subsequent numerical classification. This approach to quantifying species within habitats carried two major, but not unreasonable, assumptions. First, we assumed that the

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TA B L E 4-1

Study Localities Used in the Present Synthesis

Habitat Bay/estuary

Region

Locality

NOCAL CENCAL

San Pablo Bay Elkhorn Slough Morro Bay Upper Anaheim Bay Carpenteria Slough Colorado Lagoon Mugu Lagoon South San Diego Bay (2 regions) Upper Newport Bay Upper Newport Bay Bahia de Ojo Liebre Estero de Punta Banda

SOCAL

BAJA

Coastal pelagic Deep bank

SOCAL SOCAL

Deep reef

CENCAL SOCAL

Harbor

Kelp bed rock reef

SOCAL

CENCAL

SOCAL

SOCAL/BAJA

Inner shelf

CENCAL SOCAL

Pelagic

CALIF

Rocky intertidal

NOCAL

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INTRODUCTION

Bahia de San Quintin San Onofre-Oceanside San Pedro Channel (2 regions) Soquel Canyon, Monterey Bay Southern California (9 regions, 3 depths) Tanner - Cortez Bank Cabrillo Beach Outer Los Angeles–Long Beach Harbor Lower Newport Bay Outer Anaheim Bay Port of Los Angeles North San Diego Bay Diablo Cove, California

Sampling Methods

Source(s)

MT, OT OT, BS, SS BS BS, GN, OT BS, TR BS BS OT, PS, BS, SS

Ganssle (1966) Yoklavich et al. (1991) Horn (1980) Lane and Hill (1975) Brooks (1999) Allen and Horn (1975) Onuf and Quammen (1983) Allen et al. (2002)

BS, GN, OT BS, GN, OT OT OT, GN, BT

Horn and Allen (1981) Allen (1988) Galvan et al. (2000) Beltran-Felix et al. (1986); Rosales-Casian (1997) Rosales-Casian (1996) Allen and DeMartini (1983) Cross (1987)

BT, OT, BS, GN LP LL, OT SM SM SM BS GN OT OT

Yoklavich et al. (2000) Love and Yoklavich (unpubl. data) Love and Yoklavich (unpubl. data) Allen et al. (1983) Stephens et al. (1974)

BS GN OT BS, OT OT, LP, BS OT, PS, BS, SS DT

Allen (1976) Lane and Hill (1975) MEC (1988) Allen et al. (2002) Burge and Schultz (1973)

Monterey Bay Diablo Cove, California Big Fisherman’s Cove, Catalina Island King Harbor Redondo Beach Naples Reef near Santa Barbara Santa Cruz Island Palos Verdes Peninsula San Mateo Kelp Bed San Onofre Kelp Bed Hermosa Beach King Harbor Redondo Beach Malibu Beach Mission Bay Breakwater

DT DT DT, P

Miller and Geibel (1973) Burge and Schultz (1973) Allen et al. (1992)

DT, P DT DT DT DT DT DC DT DC DT

La Jolla–Pt. Loma Santa Monica Beach Del Mar, La Jolla, and Papalote Bay (Baja Calif.) Santa Barbara to Isla Asuncion, Baja (23 sta) Elkhorn Slough Morro Bay Southern California Coast, Islands and Bays Southern California Bays (3 regions) Pelagic (4 regions)

DT DC DC, P

Stephens et al. (1986) Ebeling et al. (1980) Ebeling et al. (1980) Stephens et al. (1984) DeMartini (unpubl. data) DeMartini (unpubl. data) Turner et al. (1969) Stephens and Zerba (1981) Turner et al. (1969) DeMartini and Roberts (1981) DeMartini (1981) Turner et al. (1969) Quast (1968)

Arena Cove Dillion Beach

DT

Love et al. (1999)

OT OT GN

L.G. Allen (unpubl. data) “ Pondella and Allen (2000)

OT LL, AR, MT P P

“ Hanan et al. (1993), Squire (1983), Mais (1974) Yoshiyama et al. (1987) Grossman (1982)

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TA B L E 4-1

Habitat

Rocky subtidal

Shelf

Slope

Surf zone

Region

(continued)

Sampling Methods

Locality

CENCAL

Diablo Cove San Simeon, California

DT, P B, P

SOCAL

Corona del Mar Pin Rock Catalina Island Resort Point, Palos Verdes Peninsula Punta Clara Arena Cove Diablo Cove, California Palos Verdes Peninsula Fort Ord, Monterey Bay (3 depths) Palos Verdes Peninsula (3 depths) Newport Beach (3 depths) Southern California Shelf (3 regions; 3 Depths) San Onofre–Oceanside Eureka Region (2 depths) Monterey Region (2 depths) Pt. Conception Region (2 depths) Southern California Region (2 depths) Monterey Bay Coast Morro Bay Coast Carpinteria–Coronado Southern California Coast (3 regions) Southern California Islands (3 regions) Aliso Canyon Beach Enlisted Man’s Beach San Onofre Beach Bahia de San Quintin Coast Bahia de Todos Santos

P P B P DT, P DT, P P OT OT OT OT

BAJA NOCAL CENCAL SOCAL CENCAL SOCAL

NOCAL CENCAL SOCAL CENCAL SOCAL

BAJA

OT OT OT OT OT BT BT BS BT BT BS BS BS BT BT

Source(s) Burge and Schultz (1973) Allen and Horn (unpubl. data) Cross (unpubl. data) Allen (1985) Crase (1990) Stepien et al. (1991) Yoshiyama et al. (1987) Burge and Schultz (1973) Walker (unpubl. data) Burton et al. (1995) LAUSD (unpubl. data) Allen (1976) M.J. Allen et al. (1999) DeMartini and Allen (1984) NOAA (unpubl. data) “ “ “ Allen (unpubl. data) “ Carlisle et al. (1960) Allen (unpubl. data) “ Tetra Tech (1977) Tetra Tech (1977) Tetra Tech (1977) Rosales-Casian (1997) Rosales-Casian (1997)

NOTE: Habitat designations are post facto. (AR = Aerial survey; B = Bail tidepool; BS = Beach Seine; BT = Beam Trawl; DC = Diver Census; DT = Diver Transect; GN = Gill Net; LL = Long Line; LP = Lampara seine; MT = Midwater Trawl; OT = Otter Trawl; P = Poison quadrats; PS = Purse Seine; SM = Submersible transects; SS = Small Seine; TR = Traps).

methods employed were those most effective for sampling fishes in that particular habitat. Second, the methods sampled the most abundant and common species in the habitat in proportion to their actual abundances. A synthesis such as that presented here is wrought with problems, which must be considered before formulating conclusions. These inherent problems (see table 4-1) include, but are not limited to the following: (1) the major habitats were physically different; (2) the methods employed differed between habitats; (3) the durations of the studies were variable; (4) sample sizes (unit of effort and total effort) were variable; (5) some studies employed multiple methods, whereas others used only one method; and (6) the expanses of the sampling areas were different. The first two problems (1 and 2 above) were addressed by the two major assumptions stated previously. The general importance of items 3–6 to the estimation of habitat diversity was minimized by using Shannon Wiener H’ as a diversity index and by taking the mean species proportions of all the samples within a particular habitat in a latitudinal region (essentially collapsing the “replicates”). Both species and habitats were classified by computer-aided cluster analysis using Statistica (Statsoft, Inc). Clustering was carried out using the Pearson correlation coefficient (r) as the similarity measure. Relative abundance data were log-transformed to minimize the impact of highly abundant species. Only those species having a minimum occurrence at two sites

or a minimum summed percentage of 0.1% were clustered. These minimum inclusion values resulted in a data matrix that included 244 species of fish within the 168 habitat sites. Complete sorting was used to maximize the separation between groups. Clustering of species based on correlation coefficients emphasized species co-occurrence, thus producing distinct and interpretable groupings. Because of the large size of the data matrix, the determination of site groupings was a two-stage process. First, the 168 original sites were reduced to 38 site groups based on species associations using cluster analysis. The mean relative abundances of the 244 species within these site groups were then used to cluster the 38 site groups, which formed 15 major types of marine fish habitats found in California waters (table 4-2). Species groups were also determined from the mean relative abundances within the 38 site groups to minimize variation introduced by individual site samples. The numerical dominance of young-of-year (YOY) rockfishes (genus Sebastes) consistently led to habitat groups, particularly in the north, based solely on their presence regardless of other associated species. For high YOY rockfish abundance, the relative abundances were adjusted by reducing them by two orders of magnitude (relative abundance/100) to minimize their impact on species groupings. This adjustment also emphasized the adult associations of the particular species in question.

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F I G U R E 4-1 Locations of the ichthyofaunal studies used in the quantitative assessments of California fish habitats and species groups.

Designations of major habitat are from the subsequent analysis. Not all studies in southern California are depicted due to their high concentration. Diagonal lines separate the five major latitudinal regions.

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TA B L E 4-2

Thirty-Eight Site Groups

Major Habitat Pelagic Rocky intertidal Rocky subtidal Kelp bed rocky reef

Designation

Site Group

Description

PEL RIT

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38

PELAGIC ALL RIT SOCAL NOBAJA RIT NOCAL CENCAL RST CENCAL SOCAL KBRF CENBAJA KBRF SOCAL BAJA KBRF SOCAL KBRF SOCAL NOBAJA KBRF SOCAL CRRF SOCAL KBRF SOCAL KBRF SOCAL KBRF BAJA KBRF CENCAL NOBAJA RRF SOCAL SZ SOCAL SZ NSB NOBAJA BE SOCAL BE SOCAL BE BAJA BE CENCAL BE NSB SOCAL CP SOCAL IS SOCAL IS SOCAL IS SOCAL IS CENCAL SOCAL IS CENCAL SOCAL MS DSB SOCAL OS CENCAL SOCAL MDRF SOCAL MDRF SOCAL DDRF SOCAL DDRF SOCAL DCYN CENCAL SOCAL SSLP NOCAL CENCAL SOCAL DSLP NOCAL CENCAL SOCAL DBNK SOCAL

RST KBRF

Surf zone

SZ

Bay/estuary

BE

Coastal pelagic Inner shelf

CP IS

Middle shelf Outer shelf Mid-depth rocky reef

MS OS MDRF

Deep rocky reef

DDRF

Shallow slope Deep slope Deep bank

SSLP DSLP DBNK

NOTE: Derived by primary cluster analysis grouped into major habitats derived by secondary clustering of the original 38 based on mean relative abundances of co-occurring species.Legend: Habitats: BE  bay/estuary; CP  coastal pelagic; CRRF  cryptic reef fish; DBNK  deep bank; DCYN  deep canyon; DDRF  deep rocky reef; DSLP  deep slope; IS  inner shelf; KBRF  kelp bed rocky reef; MDRF  mid-depth deep rocky reef; MS  middle shelf; OS  outer shelf; PEL  pelagic; RRF  rocky reef (no kelp); RIT  rocky intertidal; RST  rocky subtidal; SLP  slope; SSLP  shallow slope; SZ  surf zone; Locations: NOCAL  Northern California; CENCAL  central California; SOCAL  southern California; NOBAJA  northern Baja California; CENBAJA  central Baja California.

Patterns of diversity within the habitat groups defined by cluster analysis were examined in two ways. First, the Shannon-Weiner (H’) information function (Shannon and Weaver, 1949) was calculated using all species with
0.1 % of the abundance at each sample site. Second, species richness (S) was calculated for each of the 168 sampling sites where S equaled the number of species contributing 0.1% of the individuals “sampled.” Because species richness by individual sampling site was so highly variable, a second measure of richness was calculated. This richness value was the total number of species recorded within major habitats within the five latitudinal regions (northern California, central California, southern California, northern Baja California, and central Baja California). Species that composed
0.1% of the mean

relative abundance within the habitat/region were summarized and compared among regions and by major habitat.

Habitat and Species Associations Biological Basis of Groups W HAT AR E TH E BAS IC T Y P E S OF MAR I N E F I S H HAB ITATS THAT O C CU R OF F CA LI FOR N I A?

Quantitative clustering of sites based on species composition yielded 15 major habitats that clustered into three main groups: shallow, deep, and pelagic (fig. 4-2). The major shallow habitats were designated as bay/estuary (BE), surf zone (SZ), nearshore soft

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FIGURE 4-2 Dendrogram depicting the relationships among the 15 major habitats derived through cluster analysis of the relative abundances of species within the original 38 defined habitats. Groups and relationships were defined using correlation coefficients and complete linkeage.

bottom (NSB), coastal pelagic (CP), rocky intertidal (RIT), rocky subtidal (RST), and kelp bed rock reef (KBRF). The deeper habitats fell into the following categories: inner shelf (IS), outer shelf (OS), mid-depth rock reef (MDRF), deep rock reef (DRF), deep slope (DSLP), deep bank (DBNK), and continental slope (SLP) (fig. 4-3). These habitats are discussed in detail in the chapters of Unit II. The seven shallow habitats fell into two major types based on their respective fish assemblages, those associated with soft substrata and those with rock substrata. Of the three major habitats with soft substrata, the bay and estuary (BE) and coastal pelagic (CP) habitats showed the closest affinity. The surf zone (SZ) was next in similarity to the BE-CP group followed by nearshore soft bottom (NSB). The kelp bed (KBRF) habitat had a higher similarity (lower distance) to the shallow, soft-bottom habitat than it did to the other two, shallow rock substratum habitats, the rocky intertidal (RIT) and rocky subtidal (RST). This unanticipated finding resulted from the large number of nearshore, softbottom species that are associated with the margins of rocky reefs. Physically, the KBRF sites were segregated according to latitude, substratum (cobble or bench rock), and whether or not they supported kelp beds at the time of sampling. The RIT habitat was restricted to the rocky intertidal zone and adjacent shallow subtidal areas (
2m depth). The RST habitat was located close to shore at depths from (approximately) 2–10 m and contained many cryptic species. KBRF habitats were generally found further offshore at depths between about 8 and 30 m. These depth limits apply only to the sites used in this analysis

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INTRODUCTION

and should not be interpreted as definite boundaries between all such habitats in California. Harbor breakwaters and jetties were classified as RST habitats with close KBRF affinities. W H ICH T Y P E S OF F I S H E S TE N D TO O C CU R I N T H E S E HAB ITATS?

The 244 species used in the analysis clustered into 42 species groups (table 4-3). The species within these groupings represent the most common or, otherwise conspicuous (i.e., large predators with relatively low abundance) members of the fish assemblages within the major types of habitats. The species groups in numerical order vary from pelagic (species groups 1–2) to primarily rock associated groups (3–14), to groups with more widespread occurrence across the major shallow habitats (15, 18, 19), and to groups (with few exceptions) whose species were primarily restricted to soft substratum habitats (16–17 and 20–33). Species groups 33–42 are associated primarily with deep water, benthic habitats. W H ICH T Y P E S OF F I S H E S AR E MOST AB U N DANT OR OTH E RW I S E DI STI NCTIVE TO TH E DI F F E R E NT HAB ITATS?

In the following characterizations, species groups with widespread distributions among major habitats are referred to as generalized and those with restricted distributions are specialized. Species Group 1 contained 16 species of pelagic fishes,

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F I G U R E 4-3 Diagrammatic representation of the relative positioning of the major habitats derived through cluster analysis.

which only rarely enter the waters over the continental shelf. According to the data analyzed, yellowtail and Pacific bonito (Species Group 2) were allied to both the open ocean species, coastal pelagic, and reef systems. These two species migrate along the coast of the Californias annually moving north in the spring–summer months and south in the late fall and winter (fig. 4-4). Yellowtail are also found in association with kelp patties drifting in pelagic environments. Species Groups 3–5 included fishes almost exclusively from rocky intertidal and adjacent subtidal areas (RIT). Group 3 contained four species that occur in greatest abundance in the southern rocky intertidal habitat. Group 4 included two species, which were common to the intertidal and shallow subtidal habitats in both northern and southern locations, and Group 5 was made up of 15 distinct species found on the rocky shoreline of central and northern California (fig. 4-5). Species Group 6 was composed of five species of primarily northern fishes that occurred both in the rocky intertidal (as juveniles) and rocky subtidal habitats (fig. 4-6). Cabezon regularly occur on southern California reefs. Species Groups 7–9 consisted of rock-associated species with northern affinities (fig. 4-6). Group 7 included four species common to northern subtidal and kelp bed habitats, which also occur commonly in the cooler portions of southern California and in the northern Baja upwelling area. Group 8 also contained four species with widespread occurrence in kelp beds and rocky reefs of the north and the northern part of southern California. Species Group 9 was composed of the most abundant, cryptic reef fishes in the northern rocky subtidal and reef habitats.

Species Groups 10–15 contained kelp bed and rocky reef species from a wide latitudinal distribution. Group 10 and 11 were made up of species from rocky reefs and kelp beds of southern California and Baja California (fig. 4-7). Nine cryptic species, which inhabit mainly the cobble substratum and crevices of rocky subtidal and reef areas, formed Species Group 10. Four of these cryptic species also occur in the intertidal zone as adults. Group 11 contained seven abundant or otherwise distinctive southern kelp bed species. One of them, the blacksmith, is often the most abundant fish found in southern kelp beds, and, another, the giant sea bass, is the top carnivore in this system. Group 12 included seven species, which were found primarily in the southernmost reefs of central Baja California, although three of these, rock wrasse, ocean whitefish, and zebraperch, are often abundant as far north as the reefs systems in the southern half of the southern California Bight. Group 13 consisted of five, widespread kelp bed and rocky reef species and included the señorita, which is common to most kelp beds from central California south into northern Baja California. The last group, 14, consisted of two species of rocky subtidal and reef fishes with more northern affinities. Species Group 15 contained six generalist species, which occur over a wide range of substrata and shallow water habitats (fig. 4-7). Four of these were surfperches, which inhabit both rocky and soft bottom substrata from the shoreline out to depths of about 30 m throughout central, southern, and northern Baja California. The remaining two species were serranids (kelp bass and barred sand bass) that inhabit a variety of shallow water habitats south of Point Conception.

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TA B L E 4-3

Mean Abundance of Members within Species Groups in Major Habitats

DSLP

DBNK

SSLP

DRF

MDRF

OS

MS

1.2 0.5 0.1

0.3 0.9 0.3

0.6 0.4 0.4 0.3 0.3 0.2

0.1 0.1

0.1 0.3 0.1 0.2 0.1 0.4

0.1 0.1 0.3

0.1

0.1

0.1

0.8 0.1 0.1 0.1 0.6 0.1

0.2 0.3 0.2 1.0 0.1 0.3 0.1

0.1 0.1 0.8 0.2 0.1

0.1 0.4

0.1

0.2 0.4

0.2 0.1 0.2 0.3 0.1 0.1 0.1 0.1 0.1 0.1 0.3 0.1 0.3 0.1

0.1

0.3

0.2

0.2 0.3 0.5 0.6

0.3 0.5 0.2 0.6 0.1

0.1 0.1 0.1

NOTE:

0.1 0.1 0.1

0.1 0.1 0.3 0.5 0.1 0.1 0.1

0.1 0.1 0.5 0.3 0.1 0.3 0.1 0.1 0.2

0.1 0.4 0.4 0.9

Only mean abundances
0.1% are shown to emphasize the most important components of the major habitats.

Species Groups 16 and 17 are made up of species common to the bays and estuaries of California (fig. 4-8). Group 16 contained seven species that are indigenous to the BE habitats in Southern and Baja California. Five of them, the longjaw mudsucker, California killifish, shadow goby, barred pipefish, and California halfbeak, are commonly associated with the salt marsh portions of these habitats. The second group, 17, consisted of estuarine and nearshore species of central and northern California. At least three of them, coho salmon, American shad, and striped bass, are anadromous species that pass through estuaries on spawning migrations

88

IS

Deep Habitats

CP

0.1 0.1

BE

KBRF

0.2 0.6 0.1 0.3

SZ

RST

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42

RIT

PEL

SPP GRP

Shallow Habitats

INTRODUCTION

and use them as nursery areas. The latter two were introduced to California from the eastern seaboard (see chapter 25). The remaining members of Group 17 (Pacific herring, surf smelt, staghorn sculpin, and starry flounder) are euryhaline, marine species that spend all or part of their lives in northern estuaries. The members of Species Groups 18 and 19 can be characterized as nearshore generalist species (fig. 4-9). Species in both groups are commonly encountered in a wide range of shallow, nearshore habitats. Topsmelt and shiner perch (Group 18) are often very abundant in all nearshore soft bot-

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F I G U R E 4-4 Pelagic members of Species Groups 1 and 2 derived by cluster analysis based on relative abundances and co-occurrence of species

within habitats.

tom habitats and are also sometimes associated with reefs. Jacksmelt and sargo (Group 19) are schooling species that move among various nearshore habitats. Further, sargo occur in numbers only south of Point Conception, whereas the others occur throughout California coastal waters.

Species Group 20 contained three abundant coastal pelagic species (Fig. 4-9). The northern anchovy has been the most abundant nearshore marine fish off California for most of the last 50 years and can occur up to 1000 km offshore (see chapter 12). The second member, the Pacific sardine, is also an

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F I G U R E 4-5 Benthic members of Species Groups 3, 4 and 5 derived by cluster analysis based on relative abundances and co-occurrence of

species within habitats.

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F I G U R E 4-6 Members of Species Groups 6–9 derived by cluster analysis based on relative abundances and co-occurrence of species within

habitats.

abundant species that has cyclically replaced the northern anchovy as the most abundant species during the last few centuries (see chapters 12 and 17). Pacific sardine was also one of the most important commercial species in the state (see chapter 23). The third species, the Pacific pompano, is also an abundant and largely underappreciated pelagic fish of coastal waters. Members of Species Groups 21–24 can be characterized as southern nearshore generalists, although individually the

groups exhibit affinities to particular habitats (fig. 4-10). The five members of Group 21 are commonly found in the shallow nearshore waters of the inner shelf, harbors, and deeper parts of bays and estuaries in southern and Baja California. One member, the queenfish, is possibly the second most abundant fish in the nearshore waters off southern California (Allen and DeMartini, 1983). Group 22 contained species that are also found throughout the shallow, nearshore zone of southern

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FIGURE 4-7 Reef associated members of Species Groups 10–15 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats.

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F I G U R E 4-8 Bay and estuary associated members of Species Groups 16 and 17 derived by cluster analysis based on relative abundances and

co-occurrence of species within habitats. Groups are arranged north to south.

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F I G U R E 4-9 Widespread members of Species Groups 18–20 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats.

California and Baja California and include species that are typical of the surf zone environment. Group 23 represented a collection of large, mobile species that are active mainly at night and are often from the rock/sand margins of rocky reef and kelp bed complexes. They may be present in both soft-

94

INTRODUCTION

bottom and rocky nearshore habitats. Six of these 11 species are elasmobranches that contribute a great deal of biomass to nearshore fish assemblages. The nocturnal behavior of these species, in the past, has rendered them inconspicuous to most diver surveys of reef areas. A recent assessment of these habitats

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F I G U R E 4-10 Nearshore members of Species Groups 21–24 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats.

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F I G U R E 4-11 Southern coastal pelagic members of Species Groups 25 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats.

by gill net sampling in southern California was solely responsible for the identification of this ecologically important group (Pondella and Allen, 2000). Group 24 included eight species that are commonly from southern bays and estuaries but are also variously found in nearshore, soft-bottom areas of the southern coastline. One of them, the bullseye puffer, was found only in the bays and on the shoreline of central Baja California. Species Group 25 (fig. 4-11) consisted of four coastal pelagic species, including three (white seabass, California barracuda, and jack mackerel) that are found around kelp beds and reefs in the southern regions of California and in Baja California. They can be found in the same types of habitats as members of Species Group 23. Species Groups 26–29 contained nearshore soft-bottom species, which are usually encountered along sandy beaches (fig. 4-12). Group 26 included three species found commonly on the shallow inner shelf off southern California and northern Baja California. Group 27 contained four species from similar environments off central California. The four species in Group 28 were found mainly in southern, shallow, soft-bottom habitats, particularly those close to shallow reefs.The giant kelpfish of Group 28 is commonly found in all shallow habitats with algae (live or drift), surf grass, or eelgrass. Group 29 included three widespread members found in the surf zone and shallow inner shelf. The two pipefishes are associated with the drift algae of the surf zone, whereas the speckled sanddab is an abundant species throughout the nearshore soft-bottom environment. Species Groups 30–32 contained soft-bottom, inner to midshelf generalists (fig. 4-13). White croaker and basketweave cusk-eel of Group 30 are abundant, nocturnal species of the nearshore soft-bottom and inner shelf. Groups 31 and 32 consisted of nine inner shelf and seven midshelf species, respectively.

96

INTRODUCTION

In Species Group 33, we encounter the first of the truly deep dwelling species, especially in southern waters (fig. 4-13). In general, fishes occur in deeper water in the southern regions of the distribution because of temperature stratification, a phenomenon referred to as submergence (see Chapter 1). The six members of Group 33 are typical of the mid- to outer shelf of the California coastline. Species Groups 34–39 are composed of deeper reef species (50–250 m) and are dominated by rockfish species (genus Sebastes) (figs. 4-14 and 4-15). Group 34 included four species (three rockfishes) common to mid-depth rocky reefs and surrounding soft-bottom areas. Groups 35 and 36 included 11 rockfish species that are widespread over mid to deep rocky reefs. Members of groups 37–39 are typical of deep rocky reefs and deep canyons of central and southern California. Members of Group 38, however, also live in shallower kelp bed and rocky reefs and recruit to subtidal areas north of Point Conception (Burge and Schultz, 1973; Miller and Geibel, 1973; Yoshiyama et al., 1987). Species Group 40 contained six deep shelf and continental slope species indicative of the soft-bottom areas of the deep waters off California (fig. 4-16). This group included one of the most abundant flatfishes of the deep shelf and slope, the Dover sole, as well as the common rockfish relative, the longspine thornyhead. Also, the two rattails (macrourids) and the slickhead (alepocephalid) of this group are typical of the deep, benthopelagic realm. Finally, Species Groups 41 and 42 contained species that were widespread over deep shelf, slope, and deep bank habitats, usually in excess of 200 m depth (fig. 4-16). Each major habitat and associated species identified by this analysis and earlier works will be covered in greater detail in Unit II of this volume. Soft substratum habitats are the subjects of chapter 5 (BE-bays and estuaries), chapter 6 (NSB-nearshore soft-bottom, SZ-surf zone, and harbors), chapter 7 (IS-inner shelf and OS-outer shelf), chapter 13 (SLP including SSLP and

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F I G U R E 4-12 Nearshore members of Species Groups 26–29 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats.

DSLP-shallow and deep continental slope) and chapter 12 (CP and PEL-surface waters). The rocky intertidal (RIT) habitat will be discussed in chapter 8, and the rocky subtidal (RST) and kelp bed/rocky reefs (KBRF) are the subjects of chapter 9. Fishes of the deep rocky reefs and banks (MDRF, DRF, and DBNK) are the subjects of chapter 10 in this volume.

Physical Basis for Groups W H ICH P HYS ICAL AT T R I B UTE S DE F I N E TH E S E HAB ITATS AN D HOW M I G HT TH E S E I N F LU E NCE TH E F I S H E S TH E R E?

The site and species groups covered above were determined strictly by fish species associations. To begin to address the

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F I G U R E 4-13 Shelf associated members of Species Groups 30–33 derived by cluster analysis based on relative abundances and co-occurrence of

species within habitats.

question, information on the substratum type, mean depth, and latitude for each of the original 168 sites was assembled from the literature. Substratum type was represented by an index derived from available information and ranged from 0 (mud) to 5 (bench rock). Cobble and mixed rock/sand or rock/mud substrata fell in the middle of the index range. Depths were recorded as the mean depth (m) of the habitat in question, and latitude (°N) was determined from charts if not otherwise available from the source publication. These data were then used to discriminate among the 15 major types of

98

INTRODUCTION

habitats identified through cluster analysis. In this multivariate analysis, these three physical variables discriminated extremely well among major habitats in a highly significant manner. These three physical variables accounted for as much as 90% (R2
0.90) of the variance within the site group model. The differences among the major habitats relative to these physical attributes can be visualized by plotting the mean canonical scores (centroids) of the sites within the major habitats by the three significant discriminant roots (fig. 4-17). Root 1 represented mainly substratum type and ranged from rocky substrata

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F I G U R E 4-14 Shelf and deeper reef associated members of Species Groups 34, 35, and 38 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats.

on the left and muddy substrata on the right of the axis. Root 2 was loaded heavily on depth and is represented in the graph as shallow (top) to deep (bottom) on this axis. Latitude was the primary influence in root 3 and ranges from north to south on the axis. Therefore, shallow, rocky habitats fall into

the upper left, back portion of the three-dimensional space. Conversely, deep, muddy habitats fall into the lower right portion of the space. The deep bank (DBNK) habitat falls in the center of root 1 reflecting the rock/mud mix character of this deep-sea habitat.

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F I G U R E 4-15 Deep reef and shelf associated members of Species Groups 36, 37, and 39 derived by cluster analysis based on relative abundances

and co-occurrence of species within habitats.

Based on the significant discrimination of site groups by physical attributes, the 42 species groups were also discriminated based on individual species correlations with the same three physical factors, substratum, depth, and latitude. This discrimannt analysis was carried out to link the species group-

100

INTRODUCTION

ings directly to the physical attributes of their habitats. Not surprisingly, substratum, depth, and latitude significantly discriminated among the groups of fishes at a level equivalent to that of the major habitat types. The three physical variables, once again, accounted for as much as 90% (R2
0.90) of the

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F I G U R E 4-16 Deep shelf, bank, and slope associated members of Species Groups 40–42 derived by cluster analysis based on relative abundances and co-occurrence of species within habitats. Groups are arranged by relative depth (top to bottom).

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F I G U R E 4-17 Plot of mean canonical

scores of 15 major habitats derived from discriminate function analysis using substrate, depth, and latitude.

variance within the site group model. This implies that fish species associations are closely allied to the characteristics of their habitat. Again, this is not surprising considering the millions of years in which marine fishes have had to adapt to such conditions (see chapter 2). What it means, in a practical sense, is that we can closely predict which fish assemblages should normally occur at specific latitudes, depths, and substrata off California. As with the site groups, plotting the species groups according to the mean canonical scores on the three significant roots allows us to determine the general habitat of a particular species group directly from its position in the three-dimensional space (fig. 4-18). For example, in Fig. 4-18, species group 5 falls in the back of the upper left quadrant of the plot. Its position indicates (and predicts) that the species in this group occupy shallow, rocky habitats in higher latitudes relative to other species groups in the plot. Similarly, species group 40 is positioned in the middle of the lower right portion of the space indicating that this species group occupies a deep, soft-bottom habitat (slope) throughout California (root 3 score of zero). The cluster of habitats in the upper, right middle of the space represent the 21 species groups that occupy the shallow, nearshore, soft-bottom areas off California. Likewise, the cluster including “rockfish” species groups 34–39 falls in the space representing mid-depth to deep rocky reefs. Therefore, the value of this three-dimensional plot lies mainly in the fact that it represents a heuristic, predictive model of species occurrence in the multivariate space depicting habitat substratum, depth, and latitude. One drawback to this approach at this time is that a number of holes remain in the space. Potential habitat, depth, and latitude

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INTRODUCTION

combinations (e.g., surf zone in central California) remain unstudied at this time (table 4-4).

Habitat Generalists A R E A LL S P E C I E S LI N K E D TO PA R T I C U L A R HAB ITATS OR AR E TH E R E HAB ITAT G E N E R A LI STS?

The species groups represent a collection of both widespread (generalized) and restricted (specialized) distributions among major habitats. A number of the more common species found off California occur over a wide range of habitats either in shallow water (30 m) or in deep water (table 4-5). Among the species of shallow water habitats, the black perch was reported from the broadest range of habitats, 24 of the 29 shallow site groups. Kelp bass, pile perch, white seaperch, and barred sand bass also occurred in a large percentage of shallow habitats with both rocky and soft substrata. These species were members of the same nearshore generalist species group (15). Shiner perch and topsmelt were recorded from a large portion of the shallow water site groups as were opaleye, California halibut, and northern anchovy. Blackeye goby, white croaker, and California scorpionfish were also found in a wide variety of habitats and should be considered shallow generalists as well. Deep-water generalist species were best represented by shortspine thornyhead that occurred in seven of the nine possible deep-water site groups, followed by the spotted ratfish, bank rockfish, shortspine combfish, and Pacific hake. Six other species of rockfish—swordspine, greenstriped, greenblotched,

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F I G U R E 4-1 8 Plot of mean canoni-

cal scores of 42 species groups derived from discriminate function analysis of correlations with substrate, depth, and latitude.

stripetail, splitnose, and boccacio—plus the lingcod were all reported from most deep-water habitats. These deep-water generalists tended to be equally represented in habitats with both rocky and soft substrata. At the level of species group occurrence within the major habitats, members of species groups 15, 18, 20, 28, and 29 were recorded in more than two-thirds of the shallow major habitats (see table 4-3). Topsmelt and shiner perch (Species Group 18) were reported from all of the major shallow habitats, save the rocky subtidal, as were the members of group 28 although in much lower abundance. The broad occurrence of species group 28 was largely the result of the widespread distribution of one member, giant kelpfish, that was associated with macrophyte (kelp, drift algae, eelgrass, and surfgrass) substratum in many shallow water habitats. Group 15 was represented in all shallow habitats south of Point Conception except for the rocky intertidal. Four members of this group, black perch, pile perch, kelp bass, and barred sand bass, are ubiquitous in most nearshore habitats in southern California and northern Baja California. White seaperch is common to the nearshore areas throughout California, and the last member, rubberlip seaperch, was more closely associated with reefs over a wide latitudinal range. Large schools containing the members of Species Group 20 were reported from the water column of five major shallow habitats as well as the pelagic habitat offshore. Northern anchovy, Pacific sardine, and Pacific pompano may represent three of the most abundant coastal pelagic species in California waters (Allen and DeMartini, 1983; Cailliet et al.,

1979) and range throughout the nearshore waters as both adults and juveniles. Finally, the speckled sanddab, barcheek pipefish, and kelp pipefish (Group 29) occurred in a wide latitudinal range along the coast of the Californias, primarily in the surf zone, nearshore soft-bottom, and inner shelf. The two pipefishes associated mainly with the drift algal beds just outside the surf. Deep-water generalist species were clustered largely into Species Groups 39 and 42. The species in Group 39 were reported from both mid to deep rocky reefs and deep shelf locations. Lingcod and cowcod occurred over soft substrata mainly as juveniles, and the remaining rockfish species (shortbelly, stripetail, and to some extent rosy) were reported widely from both substrata as adults. Members of Group 42, particularly Pacific hagfish, Pacific hake, spotted ratfish, spiny dogfish, and splitnose rockfish, were reported throughout the deep shelf, shallow slope, deep reef, and deep bank habitats. One member, rex sole, along with Dover sole (Group 40), were the two most abundant and widespread flatfishes of the deep, softbottom habitats.

Taxonomic Composition of Assemblages W H ICH FAM I LI E S AN D OR DE R S OF F I S H E S AR E B E ST R E P R E S E NTE D OVE R A LL I N TH E VA R IOUS HAB ITATS AN D F I S H FAU NA?

Certain families exhibited great flexibility in habitat requirements and occurred across a wide range of habitats over a

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103

Allen (unpubl. data) No data Allen (unpubl. data)

Burton et al. (1995) Burton et al. (1995) NOAA (unpubl. data) NOAA (unpubl. data)

No data

No data No data

No data

No data

NOAA (unpubl. data) NOAA (unpubl. data)

SZ

CP IS

MS

OS

SSLP DSLP

NOTE:

Past studies stratified by habitat and latitude.

Yoklavich et al. (2000) Yoklavich et al. (2000) No data Yoklavich et al. (1991); Horn (1980)

No data No data No data Ganssle (1966)

MDRF DRF DBNK BE

RIT

PEL

RST KBRF

Central California Hanan et al. (1993), Squire (1983), Mais (1974) Burge and Schultz (1973); Allen and Horn (unpubl. data) Burge and Schultz (1973) Burge and Schultz (1973); Miller and Geibel (1973)

Northern California

Hanan et al. (1993), Squire (1983), Mais (1974) Grossman (1982); Yoshiyama et al. (1987) Yoshiyama et al. (1987) No data

Major Habitat

TA B L E 4-4

Walker (unpubl. data) Allen et al. (1992); DeMartini (1981); DeMartini (unpubl. data); DeMartini and Roberts (1981); Ebeling et al. (1980); Love et al. (1999); Stephens and Zerba (1981); Stephens et al. (1986); Stephens et al. (1984); Turner et al. (1969) Love and Yoklavich (unpubl. data) Love and Yoklavich (unpubl. data) Cross (1987) Allen (1988); Allen and Horn (1975); Allen et al. (2002); Brooks (1999); Horn and Allen (1981); Lane and Hill (1975); Onuf and Quammen (1983) Allen (unpubl. data); Carlisle et al. (1960); Tetra Tech (1977) Allen and DeMartini (1983) Allen (1976); Allen et al. (1983); Allen et al. (2002); Lane and Hill (1975); MEC (1988); Pondella and Allen (2000); Stephens et al. (1974) Allen, L.G. (1976); Allen, M.J. et al. (1999); DeMartini and Allen (1984); LAUSD (unpubl. data) Allen, L.G. (1976); Allen, M.J. et al. (1999); DeMartini and Allen (1984); LAUSD (unpubl. data) NOAA (unpubl. data) NOAA (unpubl. data)

Allen (1985); Crase (1990); Cross (unpubl. data)

Hanan et al. (1993), Squire (1983), Mais (1974)

Southern California

Habitat Analysis Summary Table

No data Love et al. (1999)

No data No data No data Galvan et al. (2000)

No data No data No data

No data No data No data No data

No data No data No data Beltran-Felix et al (1986), Rosales-Casian (1996,1997) No data No data Rosales-Casian (1997)

No data No data No data No data

Hanan et al. (1993), Squire (1983), Mais (1974) No data

Central Baja California

No data Love et al. (1999); Quast (1968)

Hanan et al. (1993), Squire (1983), Mais (1974) Stepien et al. (1991)

Northern Baja California

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TA B L E 4-5

Top 15 Shallow and Deep Water Generalist Species

Shallow Generalists SPP Group 15 15 15 15 28 13 15 11 20 18 21 18 7 30 38

Species Embiotoca jacksoni Paralabrax clathratus Rhacochilus vacca Paralabrax nebulifer Heterostichus rostratus Oxyjulis californica Phanerodon furcatus Girella nigricans Engraulis mordax Cymatogaster aggregata Paralichthys californicus Atherinops affinis Rhinogobiops nicholsii Genyonemus lineatus Scorpaena guttata

Common Name

#Occur Shallow (29)

#Occur All (38)

#Occur Rocky Bottom (20)

#Occur Soft Bottom (16)

Black perch Kelp bass Pile perch Barred sand bass Giant kelpfish Senorita White seaperch Opaleye Northern anchovy Shiner perch California halibut Topsmelt Blackeye goby White croaker California scorpionfish

24 21 20 18 18 16 16 16 15 14 14 14 13 13 12

24 21 20 18 18 17 17 16 16 16 16 14 15 15 15

13 11 11 9 9 14 7 11 3 4 1 6 11 2 7

9 8 7 8 7 2 8 3 11 10 13 6 4 11 7

Common Name

#Occur Deep (9)

#Occur All (38)

#Occur Rocky Bottom (20)

#Occur Soft Bottom (16)

Shortspine thornyhead Ratfish Bank rockfish Shortspine combfish Pacific hake Swordspine rockfish Boccacio Greenstriped rockfish Greenblotched rockfish Lingcod Stripetail rockfish Dover sole Splitnose rockfish English sole Pink seaperch

7 7 6 6 6 5 5 5 5 5 5 5 5 4 4

7 8 6 7 7 5 12 6 6 11 7 8 5 11 8

4 6 5 5 3 5 10 4 4 8 3 2 3 2 3

3 2 1 2 4 0 2 2 2 3 4 6 2 8 5

Deep Generalists SPP Group 41 42 36 37 42 35 36 37 37 39 39 40 42 32 32

Species Sebastolobus alascanus Hydrolagus colliei Sebastes rufus Zaniolepis frenata Merluccius productus Sebastes ensifer Sebastes paucispinis Sebastes elongatus Sebastes rosenblatti Ophiodon elongatus Sebastes saxicola Microstomus pacificus Sebastes diploproa Pleuronectes vetulus Zalembius rosaceus

NOTE:

Ranked by number of occurrences in 38 shallow and deep site groups.

wide latitudinal range. Overall, rockfishes and close relatives (family Scorpaenidae) represented the most commonly occurring family of fishes off California, they were recorded from 78% of California habitats when they are stratified by region (table 4-6). Surfperches (Embiotocidae) were also widespread, occurring in 70% of the habitats. Other prominent families occurring in over 50% of the regional habitats included the right-eyed flatfishes (Pleuronectidae), sculpins (Cottidae), and kelpfishes (Clinidae). Sculpins and rockfishes dominated the shallow water habitats north of Point Conception; surfperches and greenlings were also common (table 4-7). The rockfishes also dominated both the deep northern and southern habitats along with pleuronectids. On the other hand, although rockfishes are present in reduced numbers, the shallow, southern habitats tend to be dominated by a different set of families. Species of

surfperches, sculpins, kelpfishes, and pleuronectids remain important and are joined by croakers (Sciaenidae), sea chubs (Kyphosidae), silversides (Atherinopsidae), gobies (Gobiidae), and sea basses (Serranidae). The vast majority of fish species encountered in the coastal marine habitats off California belonged to the superorder Acanthopterygii, including the orders Pleuronectiformes, Scorpaeniformes, and, especially, the Perciformes. Perciform fishes were dominant or well represented in every major habitat attesting to the adaptability of these highly derived bony fishes. Perciform fishes ranged in body form and habits from dorso-ventrally flattened, benthic, hole dwelling forms such as blennies and gobies to laterally compressed, demersally oriented forms such as surfperches (Embiotocidae), croakers (Sciaenidae), and sea basses (Serranidae), to fusiform, midwater swimmers such as bonita, mackerel (Scombridae), and

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TA B L E 4-6

Top 20 Fish Families

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Scorpaenidae Embiotocidae Pleuronectidae Cottidae Clinidae Gobiidae Hexagrammidae Paralichthyidae Sciaenidae Engraulidae Atherinopsidae Batrachoididae Pomacentridae Clupeidae Syngnathidae Gobiesocidae Kyphosidae Labridae Ophidiidae Serranidae

Family

% Occur

Scorpionfishes Surfperches Righteye flounders Sculpins Clinids Gobies Greenlings Lefteye flounders Croakers Anchovies Silversides Toadfishes Damselfishes Herrings Pipefishes Clingfishes Sea chubs Wrasses Cusk-eels Sea basses

78 70 68 62 51 49 46 43 43 41 38 35 35 32 32 30 30 30 30 30

NOTE: Ranked by percent occurrence within habitats stratified by latitudinal region.

jacks (Carangidae). In general, perciform and scorpaeniform fishes dominated in habitats with rock substrata. Members of these orders possess the derived acanthopterygian characteristics of fin spines, ctenoid scales (unless secondarily lost), protrusible jaws and, in basal members, deepened, laterally compressed bodies (Helfman et al., 1997). Fin spines and ctenoid scales may offer protection from predators as well as from abrasion by rocks. The deepened body with thoracic pelvic fins and pectorals high on the sides of the fish (particularly in basal perciform fishes) represent adaptations for efficient maneuverability in close quarters. Protrusible jaws were prerequisite for the diversification of feeding strategies seen among these species (see chapter 13). Pleuronectiform fishes dominated the soft substratum habitats (particularly the nearshore soft-bottom, inner shelf, and outer shelf). These fishes are highly specialized for a benthic existence by having both eyes on one side, lying on the other side, and having extensive color and pattern change capabilities. Cryptically colored, scorpaeniform, carcharhiniform, and rajiform fishes were also well represented in habitats with soft substrata. The pelagic habitats (PEL and CP) and the open water within the other habitats were occupied principally by atheriniform, clupeiforrn, and perciform (particularly scombroid) fishes. The pelagic realm also contained an impressive number of carcharhiniform and lamniform sharks. Major adaptations of these water column fishes included elongate, streamlined, or fusiform body shapes. All are relatively fast swimmers that exhibit marked countershading (see Chapter 12).

TA B L E 4-7

Top 10 Fish Families

Family Cottidae Scorpaenidae Embiotocidae Hexagrammidae Clinidae Paralichthyidae Pleuronectidae Gobiidae Engraulidae Batrachoididae

Sculpins Scorpionfishes Surfperches Greenlings Clinids Righteye flounders Lefteye flounders Gobies Anchovies Toad fishes

Family Embiotocidae Clinidae Cottidae Sciaenidae Atherinopsidae Kyphosidae Serranidae Scorpaenidae Pleuronectidae Gobiidae NOTE:

106

Surfperches Clinids Sculpins Croakers Silversides Sea chubs Sea basses Scorpionfishes Lefteye flounders Gobies

% Occur North Shallow 100 82 82 73 64 64 55 55 55 45

Scorpaenidae Pleuronectidae Merlucciidae Anoplopomatidae Rajidae Chimaeridae Macrouridae Squalidae Alepocephalidae Embiotocidae

% Occur South Shallow 93 86 79 71 71 71 71 64 64 64

Scorpionfishes Lefteye flounders Hakes Sablefishes Skates Chimaeras Grenadiers Dogfish sharks Slickheads Surfperches

Scorpaenidae Pleuronectidae Merlucciidae Anoplopomatidae Chimaeridae Myxinidae Embiotocidae Hexagrammidae Macrouridae Argentinidae

100 100 100 80 80 60 60 40 40 20

% Occur South Deep

Family

Ranked by percent occurrence within habitats stratified by region and depth.

INTRODUCTION

% Occur North Deep

Family

Scorpionfishes Lefteye flounders Hakes Sablefishes Chimaeras Hagfishes Surfperches Greenlings Grenadiers Argentines

100 83 67 67 67 67 50 50 50 50

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F I G U R E 4-19 H’ Diversity from habitats by latitude (top) and major habitats overall (bottom). Habitats are ranked (low to high) and stratified by substrate and depth.

Patterns of Diversity HOW MANY DI F F E R E NT S P ECI E S O C CU R I N TH E VA R IOUS HAB ITATS AN D I N W HAT R E L ATIVE AB U N DANCE?

No clear patterns of H’ diversity nor species richness (S) among the 168 habitat sites were evident. Neither measure was significantly related to the three major physical factors, which were shown to influence species composition so closely. Neither H’ (canonical correlation, X2  2.16, p  .54, R2  0.01) nor S (X2  4.22, p  .24, R2  0.03) varied significantly

according to substratum index, depth, or latitude. Individual H’ and S values were highly variable among habitat types and the physical variables, particularly depth and latitude. The H’ diversity index combines measures of richness and evenness; it is, in practice, largely a measure of the equity of species abundance (evenness). Ranking habitats by latitude and major habitats based on mean value of H’ (fig. 4-19) also failed to yield clear patterns of diversity. H’ ranged from 0.62 for the inner shelf off of Monterey to a high of 3.24 for the nearshore soft-bottom in southern California. Values for the

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F I G U R E 4-20 Number of species recorded from habitats by latitutude (top) and by major habitats overall (bottom). Habitats are ranked (low to high) and stratified by substrate and depth.

majority of habitats ranged between 2.0 and 3.0, and habitats with rocky substrata occurred throughout the ranking. Softbottom habitats were well represented at both ends of the H’ diversity spectrum. H’ diversity did not differ significantly over the 14 major types of habitats listed (ANOVA, F[12,22]  1.22, p  .33). The major habitats fell into two groups relative to H’ diversity. The first group included relatively low diversity habitats (CP, DSLP, and possibly DBNK) where assemblages are dominated numerically by one or two species. The second group includes all the remaining major habitats with relatively high diversity ranging only between 2.0 and 2.6 in mean H’. This

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INTRODUCTION

group includes a very wide range of habitats from shallow to deep and rocky to soft-bottom. An inescapable and rather surprising conclusion is that most of the major habitats displayed equivalent levels of evenness independent of substratum, depth, and latitude. Some, but not all of those habitats with generally low H’ diversity, particularly the CP south, BE north, and RIT south are highly variable environments with unpredictable rates of disturbance resulting from storm surge, rainfall, patchy resources, shifting water masses, and unpredictable bouts of upwelling (see Chapter 18). A high rate of disturbance may be responsible for the high dominance in their fish assemblages. Important

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F I G U R E 4-21 A diagrammatic representation of the three major components of a kelp bed rocky reef complex. Conspicuous forms are joined by a rich fauna of cryptic and nearshore forms that associate with reefs to varying degrees when present. Historically, most studies have concentrated only on conspicuous forms within habitats.

questions, however, remain. Why do the various California marine fish habitats possess similar H’ diversity? Are most of these habitats, saturated with common species? What other physical (e.g. disturbance) and biological factors (e.g. recruitment to nursery areas) may explain the differences or similarities in diversity? The ranking of species richness within habitats by latitude and major habitats (fig. 4-20) created a pattern similar in some ways to that of H’ but different in others. Species richness ranged from a low of 9 species from the deep slope off central California to a high of 101, again, for the nearshore soft bottom in southern California. In general, soft, deep habitats ranked low in richness, whereas shallow and deep rocky and shallow soft habitats tended to rank higher. Values for the majority of habitats ranged between 20 and 50 species. Of the five habitats that recorded more than 50 species, four are found in the south (NSB Baja, OS south, IS south, and NSB south). The kelp bed rocky reefs of southern California ranked highest among the habitats with rocky substrata where 79 species were recorded. When the major habitats are ranked, the total number of species recorded (Fig. 4-20) and the same general pattern of low richness in deep soft and high in shallow rocky and soft substratum habitats remained. The coastal pelagic (CP) habitat again ranked lowest among the major habitats, although it should be pointed out that this habitat was sampled only in southern California and therefore, had no corresponding sites in other regions. The deep and shallow slope (soft) and deep

bank (rock/mud) habitats were also ranked low in species richness. In this view, three shallow, well-studied habitats (BE, KBRF, and NSB) clearly stand out from the others; more than 100 species were recorded from each. W HY AR E TH E R E MOR E S P E C I E S I N SOM E HAB ITATS THAN I N OTH E R S?

Rocky reefs that support kelp beds are widely recognized as highly diverse habitats. Allen (1985) concluded that these important habitats ranked among the most diverse of all fish habitats within the Southern California Bight, despite the fact that cryptic fish assemblages associated with rocky reefs were not assessed in that study. Interestingly, in the previous analysis, the shelf, soft-bottom habitat ranked as high as the rocky reefs in diversity (Allen, 1985). The problem with that result, as was pointed out at the time, was that the soft-bottom samples represented collections summed over a wide depth range and therefore did not take depth replacement of fish assemblages into account. The current analysis summarized data from the shelf stratified by depth (inner, mid-, and outer shelf), which ultimately clustered into the major habitats designated as inner shelf (IS), middle shelf (MS), and outer shelf (OS). The species richness of the IS habitat was high, but the MS and OS soft-bottom habitats, though on the higher end of the range, were substantially lower than that of the KBRF habitat. The KBRF habitats represented in the current analysis

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F I G U R E 4-22. Number of species associated with macrophytes, reefs, or soft-bottom as adults recorded from habitats by latitutude (top) and by major habitats overall (bottom). Habitats are ranked (low to high) and stratified by substrate and depth.

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F I G U R E 4-23 Species recorded that associate with macrophytes in soft-bottom habitats that greatly enhance species richness. Many species of macrophyte associated fishes recruit to and occur wherever there is a macrophyte structure, regardless of substrate. In addition many species of reef associated fishes recruit to these beds and remain with them for some time, using them as nursery areas.

actually represent complexes of three subhabitats (fig. 4-21). The conspicuous species that are normally recognized as kelp bed or reef species are only one component of the complex. The cobble and rock substratum with its turf algae assemblages provides habitat for a diverse assemblage of cryptic species. The third important component of the reef complex is made up of the primarily soft-bottom species that are associated with the rock/sand margins of the reefs. These include coastal pelagic species as well as many nocturnal species (e.g., members of Species Group 23), which feed on or near the reef at night. How can shallow, soft-bottom habitats have as many or more species recorded than the highly diverse rocky reef systems with kelp beds? The answer lies partially in the fact that bays and estuaries and nearshore soft-bottom areas are more complex environments than previously thought (fig. 4-22). These habitats represent shallow, productive areas that possess macrophyte structure over sand or mud bottom. In bays, eelgrass beds (Zostera marinus) provide structure to an otherwise homogenous substratum. Attached and drift algae provide the same for the nearshore soft-bottom habitat. Protected areas along the coast and in harbors often support beds of filamentous red algal (e.g., Gracillaria spp). Open coast sandy beaches provide nearly continuous drift algal

bed habitat just outside the surf line over much of California’s coastline. If a variable describing the presence or absence of macrophyte substratum is added to the multivariate analysis involving substratum, depth, and latitude, the number of species recorded from the habitat sites stratified by latitudinal region becomes significantly explained (X2  9.88, p  .04, R2  0.06) by the four-factor model (results for H’ diversity remained unchanged). Therefore, at least part of the variability in species richness may be explained by a combination of the four physical factors of substratum, presence of macrophytes, depth, and latitude. The model accounts for only 6% of the variance, however, and generalizations must be tempered by this fact. Nevertheless, there was a tendency for shallow habitats with rocky substrata, combinations of substrata (e.g., rock/sand, rock/mud, cobble/sand, etc.), and/or macrophyte substratum to support more species. The addition of macrophytes to soft-bottom habitats is important for the enhancement of species richness for two main reasons. First, many species recruit to and occur wherever there is macrophyte structure, regardless of substratum (fig. 4-23). Second, and perhaps more important, many species of reef associated fishes recruit to these beds and remain with them for some time, using them as nursery areas. In the northern regions, juvenile rockfishes and surfperches use eelgrass

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and drift algal beds extensively. In the south, juvenile surfperches join juvenile croakers, sea basses, sea chubs, and wrasses in using macrophyte beds in bays and along the open coast. The addition of the macrophyte associated species and the juveniles of reef fishes largely accounts for the high species richness in the BE and NSB habitats (fig. 4-23). The significant, multivariate relationship between the number of species at each of the original 168 sites and a combination of substratum, the presence of macrophytes, and depth strongly attests to the overall importance of macrophyte structure to the enhancement of species richness in shallow water habitats.

Recommendations for Future studies Clearly, several large holes remain in our knowledge of California’s fish habitats. Major habitats within latitudinal regions remain unstudied. Thorough quantitative studies have not been carried out or are not published for most of the major habitats in northern California, northern Baja California, and central Baja California. The surf zone, coastal pelagic, deep reef, and deep bank habitats of central California also need further study. It is important that future ichthyofaunal investigations target each major component of the fish assemblage of the habitat sampled. This will require multiple-gear strategies aimed at the quantitative assessment of species inhabiting both the water column (conspicuous species) and the benthos (cryptic species) of the habitat. Because nocturnal assemblages are sometimes quite different from those that occupy the habitat during the day, future studies may also need to involve nighttime sampling. A thorough explanation of the factors regulating species diversity within habitats awaits these future studies. Such studies should, wherever possible, employ stratified, saturation sampling of the habitat within some restricted time period. Saturation sampling involves the collection of fishes at least until species accumulation curves level off. Also, such future investigations should preferably be accompanied by assessments of the physical and chemical environment so that objective models may replace subject indexes and ranking strategies. Such undertakings will require considerable effort but need not require large funding sources as long as care is taken to assess the abundance of the fishes accurately within each of the subhabitats of the system.

Literature Cited Allen, L.G. 1976. Abundance, diversity, seasonality and community structure of fish populatikons in Newport Bay, California. M.A. Thesis. Calif. State Univ., Fullerton. ———. 1983. Seasonal abundance, composition, and productivity of the littoral fish assemblage in upper Newport Bay, California. U.S. Fish. Bull. 80(4):769–790. ———. 1985. A habitat analysis of the nearshore marine fishes from Southern California. Bull. South. Calif. Acad. Sci. 84(3):233–155. ———. 1988. Recruitment, distribution, and feeding habits of youngof-the-year California halibut (Paralichthys californicus) in the vicinity of Alamitos Bay, California, 1983–1985. Bull. South. Calif. Acad. Sci. 87:19–30. Allen, L.G., and M.H. Horn. 1975. Abundance, diversity, and seasonality of fishes in Colorado Lagoon, Alamitos Bay, California. Estuarine Coastal Mar. Sci. 3(2):371–380. Allen, L.G., and E.E. DeMartini. 1983. Temporal and spatial patterns of nearshore distribution and abundance of the pelagic fishes off San Onofre-Oceanside, California. U.S. Fish.Bull. 81(3):569–586.

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Allen, L.G., M.H. Horn, F. A. Edmands, and C. A. Usui. 1983. Structure and seasonal dynamics of the fish assemblage in the Cabrillo Beach area of Los Angeles harbor, California. Bull. South. Cal. Acad. Sci. 82(2):47–70. Allen, L.G., L.S. Bouvier, and R.E. Jensen. 1992. Abundance, diversity and seasonality of cryptic fishes and their contribution to a temperate reef fish assemblage off Santa Catalina Island, California. Bull. South. Calif. Acad. Sci. 91(2):55–69. Allen, L.G., A.M. Findlay, and C.M. Phalen. 2002. Structure and standing stock of the fish assemblages of San Diego Bay, California from 1994 to 1999. Bull. South. Cal. Acad. Sci. 101(2):49–85. Allen, M. J., S.L. Moore, K.C. Schiff, S.B. Weisberg, D. Diener, J.K. Stull, A. Groce, J. Mubarak, C.L. Tang, and R. Gartman. 1998. Southern California Bight 1994 Pilot Project: V. Demersal fishes and megabenthic invertebrates. Southern California Coastal Water Research Project, Westminster, CA. Beltran-Felix, J.L., M.G. Hammann, A. Chagoya-Guzman, and S. Alvarez-Borrego. 1986. Ichthyofauna of Estero de Punta Banda, Ensenada, Baja California, Mexico, before a major dredging operation. Ciencias Marinas 12(1):79–92. Brooks, A. J. 1999. Factors influencing the structure of an estuarine fish assemblage: the role of interspecific competition. Ph.D. Dissertation. University of California, Santa Barbara. Burge, R.T., and S. A. Schultz. 1973. The marine environment in the vicinity of Diablo Cove with special reference to abalones and bony fishes. Cal. Fish Game, Tech. Rep. 19. Burton, E. J., J. Neer, and T. Sozanski. 1995. Diversity and abundance of soft-bottom fishes in southern Monterey Bay, California. Report for Ford Ord Survey. Moss Landing Marine Laboratories, Moss Landing, CA. Cailliet, G.M., K. A. Karpov, and D.A. Ambrose. 1979. Pelagic assemblages as determined from purse seine and large midwater trawl catches in Monterey Bay and their affinities with the market squid, Loligo opalescens. California Cooperative Oceanic Fisheries Investigations Reports 20:21–30. Carlisle, J.S., J.W. Schott, and N.J. Abramson. 1960. The barred surfperch (Amphisticus argenteus Agassiz) in Southern California. Calif. Fish Game Fish. Bull. 109. Clifford, H.T., and W. Stephenson. 1975. An introduction to numerical classification. Academic Press, New York. Crase, M.S. 1992. A survey of the intertidal ichthyofauna of Resort Pt., Palos Verdes, California. M.S. Thesis, California State University, Northridge. Cross, J. N. 1987. Demersal fishes of the upper continental slope off southern California. CalCOFI Rep. 28:155–167. DeMartini, E.E. 1981. The spring-summer ichthyofauna of surfgrass (Phyllospadix) meadows near San Diego, California. Bull. South. Calif. Acad. Sci. 80(2):81–90. DeMartini, E.E., and D. Roberts. 1981. An empirical test of biases in the rapid visual technique for species time censuses of reef fish assemblages. Mar. Biol. 70:129–134. DeMartini, E.E., and L.G. Allen. 1984. Diel influences on the species and size composition, numbers and diversity of fishes caught by a 7.6 in otter trawl in Southern California coastal waters. CalCOFI Reports, Vol. 25. Ebeling, A.W., R. J. Larson, and W. S. Alevizon. 1980a. Habitat groups and island-mainland distributions of kelp-bed fishes off Santa Barbara, California. In D.M. Power (ed.), Multidisciplinary Symposium on the California Islands. Santa Barbara Museum of Natural History. pp. 403–431. Ebeling, A.W., R. J. Larson, W. S. Alevizon, and R.N. Bray. 1980b. Annual variability of reef-fish assemblages in kelp forests off Santa Barbara, California. U.S. Fish. Bull. 78(2):361–377. Forey, P.L., C.J. Humphries, I.L. Kitching, R.W. Scotland, D.J. Siebert, and D.M. Williams. 1992. Cladistics. Oxford University Press, New York. Galván, M.F, F.J. Gutierrez, S., L. A. Abitia, C., and J. Rodríguez, R. 2000. The distribution and affinities of the shore fishes of Baja California Sur lagoons. In M. Munawar, S. Lawrence, I. F. Munawar, and D. Malley (eds.), Aquatic ecosystems of Mexico: status and scope. Ecovision World Monograph series. Backhuys, P, Leiden, The Netherlands, pp. 383–398. Ganssle, D. 1966. Fishes and decapods of San Pablo and Suisun Bays. Calif. Fish Game Fish Bull. 133:64–94. Grossman, G.D. 1982. Dynamics and organization of a rocky intertidal fish assemblage: the persistence and resilience of taxocene structure. Am. Nat. 119(5):611–637.

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Hanan, D. A., D. B. Holts, and A.L. Coan, Jr. 1993. The California drift gill net fishery for sharks and swordfish, 1981–82 through 1990–91. Calif. Fish Game Fish Bull. 175. Hastings, P. A. 2000. Biogeography of the tropical eastern Pacific: distribution and phylogeny of chaenopsid fishes. Zool. J. Linn. Soc. 128:319–335. Helfman, G.S., B.B. Collette, and D.E. Facey, 1997. The diversity of fishes, Blackwell Science, Malden, MA. Horn, M.H. 1970. Systematics and biology of the stromateid fishes of the genus Peprilus. Bull. Mus. Comp. Zool. 140:165–261. ———. 1980. Diversity and ecological roles of noncommercial fishes in California marine habitats. CalCOF1 21:37–47. ———., and L.G. Allen. 1978. A distributional analysis of California coastal marine fishes. J. Biogeogr. 5:23–42. Horn, M.H., and L.G. Allen. 1981. Ecology of fishes in upper Newport Bay, California: seasonal dynamics and community structure. Cal. Fish Game, Tech. Rep. 45. Kluge, A. G., and J. S. Farris. 1969. Quantitative phyletics and the evolution of anurans. Systematic Zool. 18:1–32. Lane, E. D., and C. W. Hill (eds.). 1975. Marine resources of Anaheim Bay. Calif. Dept. Fish Game, U. S. Fish. Bull. 65. Love, M.S., M. Nishimoto, D. Schroeder, and J. Caselle. 1999. The ecological role of natural reefs and oil and gas production platforms on rocky reef fishes in southern California: final interim report. U.S. Dept. Interior, U.S. Geological Survey/Biological Resources Division. USGS/BRD/CR-1999-007. Mais, K. F. 1974. Pelagic fish surveys in the California Current. Calif Dept. Fish Game, Fish Bull. 162. MEC Analytical Systems, Inc. 1988. Biological baseline and an ecological evaluation of exisiting habitats in Los Angeles Harbor and adjacent waters, Vol I, final report. Exec. Sum., MEC05088001, Port of Los Angeles, San Pedro, CA. Miller, D. J., and J. J. Geibel. 1973. Summary of blue rockfish and lingcod life histories; a reef ecology study; and giant kelp, Macrocystis pyrifera, experiments in Monterey Bay, California. Calif. Fish Game Fish. Bull. No. 158. Onuf, C.P., and M.L. Quammen. 1983. Fishes in a California coastal lagoon: effects of major storms on distribution and abundance. Mar. Ecol. Prog. Ser. 12:1–14. Pondella, D. J. II, and L.G. Allen. 2000. The nearshore fish assemblage of Santa Catalina Island. In Proc. Fifth California Islands Symp., D. R. Browne, K. L. Mitchell, and H. W. Chaney (eds.) U.S. Department of the Interior, Mineral Management Service, Pacific OCS Region, MMS 99-0038, pp.394–400. Quast, J. C. 1968. Fish fauna of the rocky inshore zone. In W. J. North and C.L. Hubbs (eds.), Utilization of kelp-bed resources in Southern California. Calif. Fish Game Fish Bull. 139:109–142.

Rosales-Casian, J.A. 1996. Ichthyofauna of Bahia de San Quintin, Baja California, Mexico, and its adjacent coast. Ciencias Mar. 22(4): 443–458. ———. 1997. Inshore soft-bottom fishes of two coastal lagoons on the northern Pacific coast of Baja California. CalCOFI Rep. 38:180–192. Shannon, C. E., and W. Weaver. 1949. The mathematical theory of communication. University of Illinois Press, Urbana, IL. Squire, J. L., Jr. 1983. Abundance of pelagic resources off California, 1963–78, as measured by an airborne fish monitoring program. NOAA Tech. Rep NMFS SSRF-762. Stephens, J. S., Jr., C. Terry, S. Subber, and M. J. Allen. 1974. Abundance, distribution, seasonality and productivity of the fish populations in Los Angeles Harbor, 1972–73. In Marine Studies of San Pedro Bay, Part IV, Environ. Field Invest., (D. Soule and M. Oguri eds.), Allan Hancock Found. Pub. USC-SG-6-72, pp. 1–42. Stephens, J. S., Jr., and K. E. Zerba. 1981. Factors affecting fish diversity on a temperate reef. Environ. Biol. Fish. 6:111–121. Stephens, J. S., Jr., G. A. Jordan, P. A. Morris, M. M. Singer, and G. E. McGowan. 1986. Can we relate larval fish abundance to recruitment or population stability? A preliminary analysis of recruitment to a temperate rocky reef. Calif. Coop. Oceanic Fish. Invest. Rep. 27:65–83. Stephens, J. S., Jr., P. A. Morris, K. Zerba, and M. Love. 1984. Factors affecting fish diversity on a temperate reef: the fish assemblage of Palos Verdes Point, 1974–1981. Environ. Biol. Fish. 11:259–275. Stepien, C. L., H. Phillips, J. A. Adler, and P. J. Mangold. 1991. Biogeographic relationships of a rocky intertidal fish assemblage in an area of cold water upwelling off Baja California, Mexico. Pac. Sci. 45(1):63–71. Swofford, D. L. 1998. Phylogenetic analyses using parsimony (PAUP* 4.0b8). Sinauer Associates, Sunderland, MA. Tetra Tech, Inc. 1977. MRC Fish Program: Final Report, Appendices, December 1977. Report submitted to the Marine Review Committee of the California Coastal Commission. Turner, C. H., E. E. Ebert, and R. R. Given. 1969. Man-made reef ecology. Cal. Fish Game Fish Bull. 146. Yoklavich, M. M., H. G. Green, G. M. Cailliet, D. E. Sullivan, R. N. Lea, and M. S. Love. 2000. Habitat associations of deep-water rockfishes in a submarine canyon: an example of a natural refuge. U. S. Fish. Bull. 98:625–641. Yoklavich, M. M., G. M. Cailliet, J. P. Barry, D. A. Ambrose, and B. S. Antrim. 1991. Temporal and spatial patterns in abundance and diversity of fish assemblages in Elkhorn Slough, California. Estuaries 14(4):465–480. Yoshiyama, R. M., C. Sassaman, and R. N. Lea. 1987. Species composition of rocky intertidal and subtidal fish assemblages in central and northern California, British Columbia-Southeast Alaska. Bull. South. Calif. Acad. Sci. 86(3):136–144.

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PART I I

HAB ITATS AN D AS S O C IATE D F I S H E S

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SOFT SUBSTRATA

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CHAPTER 5

Bays and Estuaries LAR RY G. ALLE N, MARY M. YO K LAVI C H, G R E G O R M. CAI LLI ET, AN D M I C HAE L H. H O R N

Introduction to Estuarine Systems Few habitats offer a more challenging environment to marine fishes than bays and estuaries. These interfaces between land and sea at river mouths present highly variable physical and chemical conditions for marine fishes most of which usually have narrow tolerances to these environmental gradations. Virtually all of the prominent physical and chemical characteristics of water, such as temperature, salinity, dissolved oxygen, and pH, change dramatically over space and time in these relatively shallow habitats. Tidal exchange, especially over the sometimes extensive mudflats and salt marshes, creates additional variability associated with strong currents, possible aerial exposure, and isolation in pools. Despite these dramatic environmental fluctuations, bays and estuaries throughout the world are recognized as important fish habitats, serving especially as spawning and nursery sites, migration routes, and areas naturally supporting large populations of certain coastal fish species (e.g., McHugh, 1967; Haedrich, 1983; Elliott, 2002). The complex and dynamic qualities of estuaries have fostered continuing discussion in the literature as to their definition and classification and to their role as nursery grounds. Elliott and McLusky (2002) point out that the basic challenge of defining and classifying estuaries stems from their prominence as habitats that represent spatial and temporal continua, for example, in the environmental variable of salinity and the biological variable of community structure. These authors argue for an “expert judgment checklist” that involves assessment of physical, chemical, and biological characteristics to help define, delimit, and classify estuaries for both scientific and managerial needs while still recognizing the inherent variability of these systems. The nursery role of different habitats within and among estuaries has continued to be a topic of research, and Beck et al. (2001) have proposed a nursery-role hypothesis for marine and estuarine habitats that, if tested adequately, would result in a more rigorous assessment of the nursery value of nearshore areas. Estuaries are among the most productive areas on earth, and fish biomass in these habitats ranks with that of the marine regions of upwelling, coral reefs, and kelp beds (table 5-1). Based on energy fixed by plants and algae, estuaries and associated salt marshes may offer the greatest availability of food

of any habitat types in the world (see Whittaker and Likens, 1973). These unique environments are sinks for nutrients that flow from the land or are tidally transported from the sea. The concentrations of nutrient levels coupled with the shallow, well-mixed, and well-lit nature of these areas are primarily responsible for the high seasonal productivity that characterizes estuaries. The same turbid conditions and reduced water flows that result in deposition of nutrient-containing sediment in estuaries also trap contaminants, thus creating one of the chronic environmental problems of these habitats (see Marchand et al., 2002). Various taxonomic groups of marine fishes, many of commercial importance, are represented in estuarine systems throughout the world. In the northeastern Atlantic and Mediterranean estuaries, the main species are anguillifoms (eels), mugiliforms (mullets), perciforms (especially temperate basses), and pleuronectiforms (flatfishes) (Costa et al., 2002). In South Africa, the prominent species are clupeiforms (anchovies and herrings), mugiliforms , atheriniforms (silversides), perciforms (especially sparids and gobies), and pleuronectiforms (Day et al., 1981). In New England, estuarine fish assemblages are dominated by salmoniforms (salmon and smelts), atheriniforms (silversides and killifishes), and gasterosteiformes (sticklebacks) (Haedrich and Hall, 1976). These groups include eurythermal and euryhaline species that are adapted for estuarine existence; however, major marine groups such as gadiforms (cods), clupeiforms (herrings), anguilliforms, and perciforms are represented by relatively few species that have adapted to thrive in estuarine systems of New England (Haedrich and Hall, 1976). Along the southern Atlantic and Gulf coasts of the United States, perciforms (especially croakers, porgies, and mojarras), clupeiforms (anchovies and menhaden), and mugiliforms become more important in estuaries (Peterson and Ross, 1991; Houde and Rutherford, 1993). Although fishes can move from one area to another within an estuarine system, some degree of temperature tolerance (Hubbs, 1965) and osmoregulatory ability (Carpelan, 1961; Haedrich 1983) is required for success in these variable habitats. As implied above, predominantly estuarine species typically belong to groups that have evolved broad tolerance to changes

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TA B L E 5-1

Fish Biomass Density in Various Aquatic Ecosystems

Ecosystem

Biomass Density g m
2

Unpolluted rivers Georges Bank Matamek River, Quebec Narragansett Bay Gulf of Mexico Flax Pond (Long Island) Estuary California kelp bed Bermuda coral reef in summer Narragansett Bay salt marsh embayment

Peruvian upwelling in autumn NOTE:

1–5 1.6–7.4 2.1–17.8 3.2 5.6–31.6 24.0 33.2–37.6 59.3 69.2

216.7

After Haedrich and Hall 1976.

in temperature and salinity. Salmon, true smelts (osmerids), killifishes, and sticklebacks can adjust rapidly to abrupt changes in salinity by having (1) low permeability of body surfaces, (2) marked activity of the kidneys, and (3) highly functional salt glands in their gills (Haedrich and Hall, 1976). Quantitative sampling of estuarine fish populations presents several difficulties and has been the topic of much discussion (e.g., Haedrich and Hall, 1976; Kjelson and Colby, 1976, Smith et al., 1984; Horn and Allen, 1985; Moyle et al., 1986; Rozas and Minello, 1997; Hemingway and Elliott, 2002). The fish assemblages of estuaries and other nearshore habitats, unlike the benthos or plankton, comprise many different groups representing different niches and thus requiring diverse but complementary collecting methods (Hemingway and Elliott, 2002),. Each of the several subhabitats of estuaries, e.g., tidal channels, mudflats, eelgrass beds, and marsh pools, support their own suite of associated fish species in various life stages (Allen, 1982; Yoklavich et al, 1991; Valle et al., 1999; Allen et al., 2002). Some types of gear are much more effective at sampling these various subhabitats and particular life stages than others (Allen et al., 2002; see review by Hemingway and Elliott, 2002). For instance, purse seines are superior for sampling and estimating densities of midwater, schooling species and large, mobile taxa. Square enclosures, seines, and channel nets are most useful for estimating intertidal densities of cryptic, demersal, and schooling juvenile fishes. Beam trawls and drop nets more effectively assess the abundance of eelgrass-associated species and some larger demersal species. Otter trawls are needed to collect large, demersal fishes in the deeper channels. Therefore, programs using several types of gear are required to sample all species and subhabitats effectively. Unfortunately, many studies of estuarine fish assemblages completed to date have not employed multiple gear strategies, thus limiting our ability to compare species assemblages that are represented in different systems.

California Bays and Estuaries and Their Fish Assemblages Background and Organization of the Chapter Embayments come in many forms along the nearly 2600 km expanse of the California and Baja California coastline. Depending on size, general characteristics, and local custom, they are variously referred to as bay (bahia), estuary (estero),

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slough, lagoon (laguna), and marsh (fig. 5-1). Most qualify as estuaries in the broadest sense because they are diluted with freshwater during a portion of the year, but, because of the limited freshwater input into some of the systems, we use the collective name of “bays and estuaries” in this chapter. The arid climate of much of the California coast, especially from the central region southward into Baja California, can give the impression that such estuarine habitats are few in number and small along this coastline. These habitat types are scarcer and smaller than those on the Atlantic and Gulf coasts of the United States. Nevertheless, bays and estuaries as broadly defined above are diverse in size and type in California and Baja California and present an array of different environmental conditions for coastal fishes. Large embayments, such as San Francisco Bay and San Diego Bay, generally represent the broadest range of habitats including deep to shallow channels, mudflats, eelgrass beds, and salt marshes. The deep portions of these large systems are peninsular extensions of the shallow continental shelf and therefore offer habitat to many species of nearshore fishes. The smallest bays and estuaries predictably contain some reduced combination of shallow channels, mudflats, eelgrass beds, and salt marshes and are inhabited by a smaller number of typical bay-estuarine fish species. The wide variety of bay and estuaries in California is largely a result of the diverse geology, climate, and topography of the state, and these systems have been described and classified by Ferren (1996a,b,c). In northern California, the relatively high annual rainfall results primarily in river-dominated estuaries. These systems usually receive frequent freshwater influx and develop classic estuarine salt-wedge characteristics, sharp gradients of salinity with depth that move upstream or downstream depending on variations in the input of fresh water over the annual hydrologic cycle (fig. 5-2). Southward along the California coast, these relatively large bays and estuaries give way to smaller embayments where freshwater input is largely restricted to the winter months when rainfall is most prevalent (fig. 5-3). These types of embayments have sometimes been referred to as “intermittent estuaries,” and those of central and southern California generally fall into this category. Ferren et al. (1996a,b,c) classified the wetlands of central and southern California into five types, including estuarine systems, and, in turn, recognized seven kinds of estuaries for these two sections of the state’s coastline, a reflection of the remarkable geomorphological and climatic diversity of California. The very small bay-estuarine systems at the creek mouths of canyons and structural basins in the classification of Ferren and co-workers have rather distinctive fish assemblages because of the relatively consistent freshwater inflow into a limited space. In the bays and estuaries on the Pacific coast of Baja California, where annual rainfall is especially low, evaporation may exceed precipitation, resulting in hypersaline conditions during much of the year; these systems are sometimes referred to as “negative estuaries.” The upper portions of most of the bay-estuarine systems in California and northern Baja California are fringed by salt marshes, which are characterized by shallow channels, mudflats, and islands that support salt-tolerant plants. California bays and estuaries have received a great deal of study during the last 40 years (table 5-2). This heightened attention has been prompted mainly by the alarming and ever-increasing rate of human modification and destruction of these unique habitats and the continuing accumulation

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F I G U R E 5-1 Map of the coastline of California and Baja California with locations of 19 bay-estuarine systems.

of pollutants in them. Estimates of the degree of loss of coastal wetlands, including bays, estuaries, and salt marshes range as high as 90% in southern California (Zedler et al., 2001). Types of pollution in California bay-estuarine systems range from nutrient loading (e.g., Kamer et al., 2001) to organochlorine and heavy metal contamination (e.g., Davis et al., 2002). Habitat loss and environmental pollution are discussed in a broader context of California marine fish habitats in Chapter 23. Recognition of the biological importance and the diminished number and quality of these habitats in California has resulted in a growing number of restoration projects in estuaries and salt marshes in recent years (Zedler, 2001).

We characterize California bay-estuarine fish assemblages below from two broad perspectives, each with links to other chapters in this book: (1) latitudinal distribution patterns, and (2) major ecological features. The coastline from Humboldt Bay in northern California to Laguna de Ojo Liebre in central Baja California spans about 11° of latitude (fig. 5-1) and crosses biogeographic boundaries and environmental gradients, especially of temperature and rainfall. As such, the latitudinal perspective treated here is related to the larger scale distributional analyses in chapters 1 and 2. This perspective can be divided into two components: (a) speciesarea relationships, and (b) classification based on salt tolerance and life-history pattern, which relate generally to the

B AY S A N D E S T U A R I E S

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F I G U R E 5-2 Large-scale variation in depth-averaged salin-

ity (parts per thousand) in San Francisco Bay before and after the freshwater pulses of November to December 1981 and February to March 1982 (after Armor and Herrgesell, 1985).

ecological classification of the entire California marine fish fauna (chapter 4). The overarching ecological features of diversity, productivity, seasonality, interannual variability, and nursery function are important in portraying and understanding bay-estuarine fish ecology, and they link to varying degrees to the conceptual topics discussed in Unit III on Population and Community Ecology, especially feeding and trophic interactions (chapter 14) and recruitment (chapter 15).

Latitudinal Distribution Patterns S P ECI E S-AR EA R E L ATION S H I P S

In an earlier analysis of the relationships among California bays and estuaries based on presence/absence of fish species, the seven sites studied in southern California formed a distinctive unit (Horn and Allen, 1976). The six bays and estuaries studied in central and northern California (i.e., north of Point Conception) also grouped together in the analysis; however, the group of large bays and estuaries in the north (Humboldt Bay, Tomales-Bodega Bay, and San Francisco Bay) and the smaller, intermittent estuaries of Northern and central California (Bolinas Bay, Elkhorn Slough, and Morro Bay) clustered as separate subunits. We have updated the Horn and Allen (1976) analysis here by (1) adding two sites, Carpenteria Estuary (Brooks, 2001) and Mugu Lagoon (Onuf and Quammen, 1983), and (2) using the species lists from Elkhorn Slough (Yoklavich et al., 1991) and San Diego Bay (Allen et al., 2002). From this revised analysis, a group of 38

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species was identified that occur widely in California bays and estuaries, a group of 60 species that inhabits bays and estuaries primarily in southern California, and a group of 133 species that occurs mainly in bay-estuarine habitats north of Point Conception. These three geographic categories are listed adjacent to an updated dendrogram (fig. 5-4) and permit recognition of the faunal composition of each bay and estuary in the cluster according to these categories. As was found for the 13 bays and estuaries in the original Horn-Allen analysis, variation in the number of species among the 15 sites in the new analysis was driven largely by the size (surface area) of the habitat. Multiple regression analysis was used to determine the relative contributions of six independent environmental variables (surface area, latitude, mean annual sea surface temperature, diurnal tidal range, distance to nearest neighboring site, and mean annual rainfall) to explain the variation in the number of species recorded from each bay-estuarine site. Surface area was the only significant independent variable and accounted for 81% (R2  0.81) of the variation in species richness. As in the previous paper, our new analysis yielded a statistically significant relationship between the number of species and the area of the bay-estuarine habitat. This species-area relationship (fig. 5-5) is best described by the power function S  1.31 A0.33 (where S  the number of species and A  the surface area of the bay-estuarine system) for log-transformed data (r  0.92; p  0.001) and S  12.44 A0.24 for nontransformed data (r  0.96; p  0.001). The latter equation is a more easily accessible model to predict the species richness of any bayestuarine system in California. The width of the mouth of

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TA B L E 5-2

References to Works on Fish Assemblages in 18 Bays and Estuaries in California and Baja California

Bay-estuarine System

References

Humboldt Bay Tomales-Bodega Bay

Bahia de San Quintin

Monroe, 1973; Barnhart et al., 1992 Bane and Bane, 1971; Hardwick, 1973 Giguere, 1970 Ganssle, 1966; Aplin, 1967; Green, 1975; Armor and Herrgesell, 1985; Matern et al., 2002 Browning, 1972; Cailliet et al., 1977; Yoklavich et al., 1991; Yoklavich et al., 1992; Barry et al. 1996 Fierstine et al., 1973; Gerdes et al., 1974; Horn, 1980 Brooks, 2001 Onuf and Quammen, 1983 Allen and Horn, 1975; Valle et al., 1999 Lane and Hill, 1975 Allen, 1982, 1988; Horn and Allen, 1985 Mudie et al., 1974; Williams et al., 2001; Desmond et al., 2002 Chapman, 1963 Peeling, 1974; Allen et al., 2002 White and Wunderlich, 1976; Williams et al., 2001; Desmond et al., 2002 Beltran-Felix et al., 1986; Rosales-Casian, 1997 Rosales-Casian, 1996, 1997

Laguna de Ojo Liebre

Galvan et al., 2000

Bolinas Lagoon San Francisco Bay

Elkhorn Slough

Morro Bay Carpinteria Lagoon Mugu Lagoon Alamitos Bay Anaheim Bay Newport Bay Los Penasquitos Lagoon

FIGURE 5-3 Monthly variation in temperature and salinity within three

California bay/estuaries from northern to southern California: Humboldt Bay (1960), Elkhorn Slough (2000), and Upper Newport Bay (1978).

each habitat also was significant when included in the speciesarea analysis. Mouth width and surface area, however, were highly intercorrelated variables thus adding undesirable redundancy to the analysis. Recognition of three broad distributional categories (widespread, southern, and northern) of bay-estuarine fish assemblages illustrates the complex and dynamic character of the California coastal fauna that Hubbs (1974) emphasized. Many species cross faunal boundaries, some as a result of local or seasonal fluctuations in environmental variables, especially temperature. Hubbs (1948, 1960) noted the general tendency for primarily southern species to occur in bays and estuaries in central and northern parts of California and for primarily northern species to occur in deeper (hence, cooler) waters in southern California and in cool, upwelling areas off northern Baja California. As a result, Horn and Allen (1976) hypothesized that of the 224 species in California’s bays and estuaries, southern ones would be more likely in systems north of Point Conception than would northern species in this type of habitat south of Point Conception. The results of their study supported this view because of 55 primarily southern species, 25% occurred in one to three northern bays and estuaries, whereas of 128 northern species, only 9% variously occurred in no more than one of the southern systems. A comparison of the remaining, generally deeper dwelling, coastal fishes (Horn and Allen 1978) showed the opposite trend, i.e., Point Conception is less of a boundary to northern species than to southern ones. Our update of the Horn and Allen (1976) database and the new analysis did not change these general conclusions.

Mission Bay San Diego Bay Tijuana Estuary

Estero de Punta Banda

NOTE:

Arranged in order from north to south; see Fig. 1 for locations.

Ecological Classification Based on Salt Tolerance and Life History Pattern DE SCR I PTION OF TH E MODE L AD OPTE D

Several attempts have been made to classify the bay-estuarine fishes of California based on their life histories as well as on temporal and spatial distributions. These efforts have resulted in a number of different ecological classifications specific to particular habitats. The fish species of Newport Bay and San Diego Bay in southern California have been grouped into residents, spring–summer seasonals (periodics), and visitors (Allen, 1982; Allen et al., 2002). Similarly, Yoklavich et al. (1991) categorized the fishes in Elkhorn Slough in central California as either marine species, marine immigrants, slough residents, partial residents, or freshwater species. Using salinity tolerance more explicitly, Armor and Herrgesell (1985) classified fish species in San Francisco Bay as freshwater (occurrence at salinities 1 ppt ), anadromous, estuarine (occurrence at 1–20 ppt), marine estuarine (9–30 ppt), or marine (only 20 ppt). These several, overlapping classification strategies emphasize the need for a composite model applicable to California bay-estuarine systems in general. Therefore, we have adopted here a scheme based on the general classification proposed by Moyle and Cech (2000), with modifications derived from Armor and Herrgesell (1985) and Yoklavich et al. (1991).

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FIGURE 5-4 Dendrogram of the clustering of 15 California bays and estuaries based on the presence/absence of fish species using correlation coef-

ficients (r) and complete linkage. The species of each bay-estuarine system are grouped into three broad distributional categories (widespread, northern, and southern) based on a two-way table (bay vs. species) generated in the cluster analysis (after Horn and Allen, 1976).

Our classification, shown in table 5.3, recognizes the fish species of California bay-estuarine systems as either freshwater taxa, diadromous (anadromus or catadromous) taxa, estuarine residents, marine migrants, or marine species that seasonally or occasionally enter the system. These five categories are defined as follows: (1) Freshwater taxa are those forms that occur only in upstream (sometimes brackish) areas where salinities are generally less than 1 ppt. (2) Diadromous taxa are those that migrate between marine and freshwater (or brackish) environments for spawning purposes. Most common among these species are anadromous fishes, which mature in the ocean and enter freshwater to spawn. Catadromous fishes are much rarer in California, but one species, striped mullet, may qualify in southern California bays and estuaries because small juveniles recruit to brackish and freshwaters from the open sea during the winter months (Horn and Allen, 1985). (3) Estuarine residents are those euryhaline and eurythermal species that complete their entire life cycle in bays and estuaries. This category contains species that are widespread in the state and also those that mainly inhabit the salt marsh areas of southern California bays and estuaries. (4) Marine migrants include both species that migrate into bays and estuaries to spawn or give birth (sharks, rays, herrings, and surfperches) and species that are spawned offshore, recruit into bays and estuaries, and then use these habitats as nurseries during their juvenile stage (e.g., some flatfishes). (5) Marine species are those that occur broadly in all life-history stages in the nearshore environment and enter bays and estuaries at certain times of the year or at varying intervals. This scheme has the advantage of combining salt tolerance, life-history pattern, and latitudinal occurrence for each fish species. Latitudinal change in species composition occurs in part because thermal and biogeographic boundaries are crossed, as discussed in the

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previous section, and in part because freshwater input decreases from north to south in California and into Baja California. Given these considerations, the bay-estuarine habitats and their associated fish assemblages in this coastal expanse are portrayed in four segments and discussed in turn below. NORTH E R N CA LI FOR N I A

This part of the coast contains the two largest bay-estuarine environments in California: San Francisco Bay and Humboldt Bay. More than 100 species of fishes have been reported from each of these systems (Armor and Herrgesell, 1985; Barnhart et al., 1992). Even though the fishes in the two systems represent the entire spectrum of salinity tolerance, the consistent inflow of freshwater greatly influences the composition of both fish assemblages. As a result, they are dominated seasonally by a relatively small number of anadromous and otherwise euryhaline species of mainly northern affinities, including salmon and trout, true smelts, cods, and herrings (table 5-3; fig. 5-6). Among the most prevalent freshwater brackish species in northern bays and estuaries are threespine stickleback and prickly sculpin. Diadromous (anadromous) species in California are largely confined to northern bays and estuaries and include white sturgeon, American shad, chinook salmon, and striped bass. A relatively small number of species of estuarine residents occur in these systems and are represented mainly by longfin smelt, bay pipefish, Pacific staghorn sculpin, and several species of goby. Dominant marine migrants include pelagic species, especially Pacific herring, silversides (jacksmelt and topsmelt), and shiner perch, as well as benthic (demersal) forms such as starry flounder and English sole. The most

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FIGURE 5-5 Relationship of number of species (S) and surface area (A) of 15 California bays and estuaries, plus the continental shelf (CCS) and

Chesapeake Bay (CB) for comparison. The equation is based on California bays and estuaries and the continental shelf. AL = Alamitos Bay; AnB = Anaheim Bay; BL = Bolinas Lagoon; CM= Carpenteria Marsh; ES = Elkhorn Slough; HB = Humboldt Bay; LPL = Los Penasquitos Lagoon; MB = Morro Bay; MgL = Mugu Lagoon; MiB = Mission Bay; NB = Newport Bay; SDB = San Diego Bay; SFB = San Francisco Bay; TBB = Tomales-Bodega Bay; TE = Tijuana Estuary (after Horn and Allen, 1976).

abundant marine species in these northern systems appears to be northern anchovy. Finally, freshwater brackish and diadromous species such as three-spine stickleback, starry flounder, tidewater goby, steelhead, and juvenile salmon are well represented in the low-salinity regions of these larger bays and estuaries, and have been the prevalent species in smaller, river-mouth systems throughout the region (fig. 5-7). Many of the species in northern bays and estuaries, including starry flounder (Orcutt, 1950), striped bass (Raney, 1952), threespine stickleback (Snyder, 1991), and jacksmelt (Clark, 1929), have been the subject of life-history investigations. The life histories of Chinook salmon, coho salmon, steelhead, English sole, and other species are well summarized in Emmett et al. (1991), Leet et al. (2001), and Moyle (2002). Species in Jeopardy

Those bay-estuarine species in decline and threatened with extinction in California are discussed in this northern section because of the relatively high diversity of such fish taxa in this region. The bay-estuarine fish assemblages of northern California are a remarkable mixture of species in terms of origins, life history, and status and include icons of rarity, decline, and success. Anadromous fishes, in particular sturgeon and salmon, are more diverse and abundant in

northern compared to central and southern parts of the state. Habitat loss and alteration involving dams, water diversions, and pollution have played major roles in reducing fish populations, especially of anadromous species. These and other impacts on California’s native bay-estuarine fish faunas are described in Leet et al. (2001) and by Moyle (2002). Such perturbations have resulted in several species and populations being recognized as endangered, threatened, or in some lesser state of jeopardy by the federal or state government (table 5-4). Although most species of sturgeon worldwide are listed as in trouble, one of the two species in California, at least, appears to be faring better in recent years than in earlier decades as a result of improved fisheries management. White sturgeon, the largest fish species that enters fresh waters in North America (apparently reaching 6 m and 630 kg), spends most of its life in estuaries of large rivers. Recognition that this species requires at least 10 years to mature at a size of about 1 m or more led to closure of the commercial fishery in 1917. Effective management of the sport fishery in the state has resulted in white sturgeon being one of the few species in San Francisco Bay to sustain its population. In contrast, green sturgeon is a rarer species that spends most of its life in the ocean, spawns at an even older age (15–20 years), and is less well studied. Thus, it has not fared as well as white sturgeon and is currently listed as a species of special concern in California. Green sturgeon

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CATADROMOUS ESTUARINE RESIDENTS

DIADROMOUS ANADROMOUS

FRESHWATER (BRACKISH)

Species Category

Oncorhynchus kisutsch # Oncorhynchus tshawytscha # Oncorhynchus mykiss # Alosa sapidissima * Acipenser transmontanus Acipenser medirostrus Morone saxatilis * Mugil cephalus Spirinchus thaleichthys Hypomesus transpacificus # Lepidogobius lepidus Leptocottus armatus Syngnathus leptorhynchus Clevelandia ios Gillichthys mirabilis Ilypnus gilberti Quietula ycauda Acanthogobius flavimanus * Fundulus parvipinnis Anchoa delicatissima Anchoa compressa Paralabrax maculatofasciatus Syngnathus auliscus Hypsoblennius gentilis

Longfin smelt Delta smelt Bay goby Pacific staghorn sculpin Bay pipefish Arrow goby Longjaw mudsucker Cheekspot goby Shadow goby Yellowfin goby California killifish Slough anchovy Deepbody anchovy Spotted sand bass Barred pipefish Bay blenny

Gasterosteus aculeatus Eucyclogobius newberryi # Gambusia affinis * Cottus asper

Scientific Name

Coho salmon Chinook salmon Steelhead American shad White sturgeon Green sturgeon Striped bass Striped mullet

Threespine stickleback Tidewater goby Western mosquitofish Prickly sculpin

Common Name

TA B L E 5-3

Klamath River X

X

X X X X X X

X

X

X X

X X X X

X

X

X

X X X X

X X X

X

X

Humboldt Bay

X

Eel River

X

Tomales Bay X X X X

X

X

X

X

San Francisco Bay X

X X X X X X X X

X X X X X X

X

X

Elkhorn Slough X X X X X

X X X X

Morro Bay X

X

X X X X X

X X

X X X X

X X X X X X

X

Alamitos Bay

Ecological Classification of Some Principal Fishes in 13 Bays and Estuaries in California and Baja California

Newport Bay X X X X X X X X X X X X

X

Mission Bay X X X X X X

X X X X X X

X

San Diego Bay X X X X X X X X X X X X X

X

Estero de Punta Banda X X X X

X

X X X X X

X

Bahia de San Quintin X

X X X

X X X X X

X

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NOTE:

Mustelus henlei Engraulis mordax Citharichthys stigmaeus Phanerodon furcatus Mustelus californicus Urolophus halleri

Paralabrax nebulifer

Barred sand bass

Clupea pallasi Platichthys stellatus Pleuronectes vetulus Triakis semifasciata Myliobatis californicus Atherinopsis californiensis Cymatogaster aggregata Atherinops affinis Paralichthys californicus Hypsopsetta guttulata Embiotoca jacksoni Pleuronichthys ritteri Umbrina roncador Hypomesus pretiosus

Brown smoothhound Northern anchovy Speckled sanddab White seaperch Gray smoothhound Round stingray

Pacific herring Starry flounder English sole Leopard shark Bat ray Jacksmelt Shiner perch Topsmelt California halibut Diamond turbot Black perch Spotted turbot Yellowfin croaker Surf smelt X

X

X X

X X X

X X X

X

X X

X X X X X

X

X

X X

X X X

X X X

X

X X X X X X X X X

X X X X

X

X X X X X X X X X X

X X X X X

X

X X X X X X X X X X X

X X X X

X X X X X X

X X X X

X

X

X X

X X X X X

X

X

X

X X X X X X X X

X

X X X X X X X

X X X X X X X X

X

X X

X

X X X X X X X X X

X

X X

X

X X X X X X X X X

X

X

X

X X X X X X X X X

Based on salt tolerance and life- history pattern. X  species present; #  species is endangered, threatened, or contains one or more populations with this status; *  alien species. Modified from Moyle and Cech, 2000.

MARINE

MARINE MIGRANTS

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F I G U R E 5-6 Profiles of fishes in northern California bays and estuaries representing five ecological categories based on salt tolerance and life-

history pattern: freshwater taxa, anadromous taxa, estuarine residents, marine migrants, and marine species that seasonally or occasionally enter these habitats. (See Table 5-3.)

apparently spawn only in the Sacramento, Klamath, and Trinity rivers in California although there are recent signs of stable populations and increased spawning activity (Kohlhorst, 2001). In 2005, the federal government proposed to list the distinct population segment of green sturgeon in the Sacramento River as a threatened species under the Endangered Species Act. Salmon are much better publicized as anadromous species in jeopardy, and there is much to justify this notoriety (see Moyle, 2002). Of the six species that historically occurred in and transcended estuaries in California, pink salmon have been extirpated from the state and certain populations of other species are extinct as well. The remaining five, coho, chinook, chum, steelhead, and cutthroat, have at least some populations threatened with extinction (table 5-4). As with sturgeon, the losses and declines can be linked mainly to large dams and water diversions that deny access of adult fish to spawning streams and disrupt the life cycle of these anadromous species. Other causes of decline include overfishing and additional sources of environmental damage such as loss of riparian habitat, siltation, pollution, effects of alien species, and competition from hatcheryreared juveniles for food and adults for spawning areas. The enormous reduction in salmon numbers and the concomitant loss of energy and nutrients that these fishes transport from the ocean to estuaries and inland streams undoubtedly have had

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profound effects on these aquatic ecosystems (Gende et al., 2002). Recovery of salmon populations in California presents a tremendous challenge requiring major long-term investments in habitat restoration and improved management of hatcheries, fisheries, and spawning streams. True smelts (Osmeridae) are part of the mix of native fishes in northern bays and estuaries, and they, too, have suffered large population declines (Moyle, 2002). Marked reduction in these small planktivorous fishes capable of occurring in great numbers seems unlikely and perhaps is even more alarming than that of the much larger and late-reproducing salmon and sturgeon. The status of three species, delta smelt, longfin smelt, and eulachon, is important to mention in this context. Delta smelt is a euryhaline species endemic to the upper San Francisco Bay estuary, mainly in Suisun Bay and the Delta. Although its population size has fluctuated greatly in the past, delta smelt was historically one of the most abundant species in the upper estuary. Beginning in the early 1980s, numbers declined precipitously, and the species was listed as threatened by both federal and state governments in 1993 with critical habitat (Suisun Bay and Suisun Marsh) defined in 1996. The causes of decline in delta smelt appear to be varied and include water diversion, fluctuating water flows, and invasive species that represent alternative, less preferred prey organisms or that

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F I G U R E 5-7 Profiles of principal fish species in three small canyon- or river-mouth estuaries. Navarro River estuary is located in Northern California south of Humboldt Bay, Pescadero Creek lagoon in Central California near Monterey Bay, and Malibu Creek lagoon in Southern California in the city of Malibu just northwest of Los Angeles.

hybridize with the species (see below). Longfin smelt is more widely distributed in northern bays and estuaries and once was one of the most abundant species in San Francisco Bay and Humboldt Bay and an important element of the food webs. Populations have declined in most locations, and the species is now listed by the state as a species of special concern. Like those of delta smelt, longfin smelt numbers declined abruptly in the early 1980s in San Francisco Bay and have remained low. Causes of the long-term decline there appear to be similar to those for delta smelt, and recovery probably depends on restoration of more natural cycles of water flow in estuaries. A

third smelt species in decline in California and also a state species of special concern is the eulachon, a fish famous for its high oil content and use by native people of the Pacific Northwest for food and candles. It spends most of its life in the ocean, returning to spawn in the lower reaches of coastal streams usually no farther south than the Klamath River and tributaries of Humboldt Bay. Numbers have been low for most of the last 30 years in the Klamath River, and, although the causes of the decline are unknown, ocean conditions, including El Niño–Southern Oscillation (ENSO) events as well as the quality of spawning habitat, may be important factors.

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TA B L E 5-4

Bay-Estuarine Fish Taxa in California That Are in Some State of Jeopardy

Common Name

Scientific Name

Status in California

Pacific lamprey Green sturgeon Delta smelt Longfin smelt Eulachon Coho salmon

Petromyzon tridentata Acipenser medirostris Hypomesus transpacificus Spirinchus thaleichthys Thaleichthys pacificus Oncorhynchus kisutch

Chinook salmon Pink salmon Chum salmon Steelhead

Oncorhynchus Oncorhynchus Oncorhynchus Oncorhynchus

Coastal cutthroat trout

Oncorhynchus clarki clarki

Watch list State special concern Federally threatened State special concern State special concern Northern ESU: federally threatened Central ESU: federally threatened and state endangered Seventeen runs: ranging from extirpated to stable or increasing Extirpated Near extirpation At least eight ESUs; ranging from watch list to candidate for federally threatened to federally threatened to federally endangered State special concern

Tidewater goby

Eucyclogobius newberryi

Federally endangered; state fully protected

tshawytscha gorbuscha keta mykiss

NOTE: Based on information in Moyle, 2002. ESU  Evolutionary Significant Unit, a geographic group of populations that share common genetic, lifehistory, ecological, and other traits and that seem to be on a common evolutionary trajectory (Waples, 1991).

TA B L E 5-5

Alien Fishes Established in Bay-Estuarine Habitats in California

Common Name

Year of Introduction

American shad Striped bass Rainwater killifish

1871 1879 1950s

Eastern USA Eastern USA Eastern USA

Food Sport/food Hitchhiker

Wakasagi Yellowfin goby

1959 Early 1960s

Japan Eastern Asia

Forage Ballast water

Chameleon goby Shimofuri goby

1962


1980

Japan Japan

Ballast water Ballast water

Shokihaze goby


1995

Japan

Ballast water

NOTE:

Origin

Current Distribution in California Mainly north Mainly San Francisco Bay Mainly San Francisco Bay, also Newport Bay Mainly San Francisco Bay Tomales Bay, San Francisco Bay, and south Mainly San Francisco Bay Mainly San Francisco Bay and reservoirs

Mainly San Francisco Bay

Based on information in Dill and Cordone, 1997; and Moyle, 2002.

Another species in jeopardy is the tidewater goby, a species listed as federally endangered since 1994 and fully protected by the state since 1987 (Moyle, 2002). This small, annual fish originally occurred in coastal lagoons in northern California and also all along the coast from Del Norte County in the north to San Diego County in the south. The species has been extirpated from San Francisco Bay and numerous other localities, especially south of Point Conception. Tidewater gobies prefer shallow, well-oxygenated lagoons with salinities 10 ppt, but they can live over a much broader range. Populations rarely intermingle, and therefore sites of extirpation are unlikely to be recolonized. Causes of decline and extirpation of tidewater goby populations include farming, logging, and urbanization upstream, draining of wetlands, opening of coastal lagoons to tidal flushing, and encountering nonnative species that either prey upon or compete with them. This species, however, seems to be a sensitive indicator of environmental conditions and responds quickly to improved health of coastal lagoons and adjoining watersheds.

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Main Reason for Introduction

S O F T S U B S T R A TA A N D A S S O C I A T E D F I S H E S

Alien Species

References were made to the impacts of alien species (also referred to as introduced or exotic species) in the above discussion of species in jeopardy. Other than in freshwater habitats, alien fish species in California are most common and diverse in bay-estuarine systems (see chapter 24). Several exotic species occur in both freshwater and bay-estuarine habitats, in part a reflection of their tolerance of a wide range of salinity conditions. Alien species in bays and estuaries in California are listed in table 5-5, and detailed accounts are provided in Dill and Cordone (1997) and Moyle (2002). Some of these nonnative species have been members of northern bay-estuarine ecosystems for such a long time that they are undoubtedly considered native species by some people. Prominent among these alien forms are two anadromous species, American shad and striped bass. Shad were introduced from Atlantic coastal waters to the Sacramento River in 1871, and since that time they have been a highly successful

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transplant, becoming first an important commercial species and then a popular sport fish. Although now distributed from Alaska to northern Baja California, American shad spawn mainly in larger rivers from the Sacramento drainage northward with lesser runs in smaller streams in northern California. No negative impacts of this planktivorous species on native fishes have been documented. Shad populations have declined in recent decades, probably as a result of water diversions from spawning tributaries and, in turn, reduced attraction of potential spawners to these diminished flows. The striped bass, even though also in decline in California, presents a different picture of an alien species and its impacts (Moyle, 2002). Introduced first from a New Jersey river to San Francisco Bay in 1879, the population of this piscivorous fish increased dramatically in the early decades and may have been responsible for changes in the estuarine food web and in part for declines in some native species, including Central Valley chinook salmon populations. The striped bass is still one of the most abundant fish species in San Francisco Bay, which is home to the main breeding population even though this euryhaline species has been widely planted in reservoirs in California and other states. The decline in striped bass numbers may be the result mainly of water diversion, as is the case for numerous other species, but also of several other interacting factors including climatic fluctuations, pollution, reduced estuarine productivity, invasions of alien species, and harvesting, especially of large females. The impacts of new alien species on this established alien species are fascinating to contemplate. A recent invader in particular, the overbite clam, has reduced plankton populations in San Francisco Bay thus decreasing the food available to larval and juvenile striped bass. Juvenile bass, in turn, are the principal prey of adult striped bass. Importantly, management of the San Francisco Bay ecosystem has focused heavily on striped bass with the thought that the measures that benefit this species also help other species. As Moyle (2002) points out, however, striped bass is a unique species and, among other differences, mostly spawns later than native species, so that the management practices of timing increased outflows for this species will not necessarily enhance the reproduction of native fishes. Some of the more recent fish introductions appear to have the potential for serious detrimental effects on native fishes. We refer here to small Asian species, in particular a smelt and several species of goby that have become established in California estuarine waters in the last 50 years, also as reviewed by Moyle (2002). Wakasagi is a planktivorous smelt intentionally introduced from Japan into California reservoirs in 1959 to provide forage for rainbow trout and other salmonids. By the 1990s, it had spread through water diversions into the San Francisco Bay estuary where it has already hybridized with delta smelt and shows the potential to compete with this endangered species for food and spawning sites. Interestingly, however, even though wakasagi has broader salinity and temperature tolerances than delta smelt, it had not become abundant in San Francisco Bay as of 2001, perhaps because of its vulnerability as a schooling species to predation by striped bass. In contrast to wakasagi, the exotic estuarine gobies in California were not the result of deliberate introductions but accidental transplants presumably arriving in ballast water of ships from Japan or other parts of Asia (Moyle, 2002). The earliest of these arrivals was yellowfin goby, a relatively large species, which appeared in San Francisco Bay in the early 1960s and subsequently colonized other bay-estuarine

habitats, especially Elkhorn Slough in central California and Newport Bay and San Diego Bay in southern California. This species is broadly tolerant of fluctuating temperatures, salinities, and oxygen levels. It can survive in freshwater but requires some salt content for breeding and can complete its life cycle entirely in the ocean. Although the yellowfin goby has become one of the most abundant species in San Francisco Bay and Newport Bay and is still increasing its range, its effect on native species remains unknown. Other alien gobies established in California include shimofuri goby, chameleon goby, and shokihaze goby, all of which belong to the genus Tridentiger. Shimofuri goby has expanded rapidly, and, as is characteristic of many successful introduced species, exhibits high dispersal ability, broad tolerance to changing environmental conditions, high reproductive output, aggressive behavior, and a flexible diet that includes exotic invertebrates. Although its impact on native species in San Francisco Bay is largely unknown, its expected invasion of smaller lagoons in southern California may spell trouble for the tidewater goby because, as Matern (1999) has shown in laboratory experiments, shimofuri gobies win out in interactions with this endangered species. Moyle (2002) has cautioned that tidewater goby habitats should be protected from invasion by this alien species wherever possible. Rainwater killifish is another small alien species that has become established in San Francisco Bay and a few freshwater habitats, and apparently in Newport Bay in southern California (table 5-5). This species is native to coastal waters of the Atlantic and Gulf coasts as well as some rivers in Texas and New Mexico and may have been introduced from the Atlantic coast into San Francisco Bay and Yaquina Bay in Oregon as embryos attached to live oysters (Moyle, 2002). The rainwater killifish obviously tolerates a range of salinities and feeds opportunistically on a variety of invertebrates. Like the western mosquitofish, which it resembles superficially, the fish is known to consume mosquito larvae, and its spread may be aided by attempts to use it for mosquito control (Moyle, 2002). CE NTRAL CA LI FOR N I A

Elkhorn Slough and Morro Bay (fig. 5-1) are the largest bayestuarine systems on the central California coast. Smaller wetlands also form seasonally at the mouths of the numerous creeks along the central coast (Ferren et al., 1996a,b,c). The fish assemblages of Elkhorn Slough have been well studied, those of Morro Bay less so, and those occurring in the smaller systems have been surveyed in only a few cases. Each of the two large systems supports a fish assemblage with varying numbers of year-round estuarine residents, freshwater occupants, and marine species from nearshore waters that enter the estuary to feed, mate, and spawn (table 5-3; fig. 5-8). In contrast to northern California bays and estuaries, both Elkhorn Slough and Morro Bay are characterized by fewer diadromous species, given that sturgeon, shad, salmon, and striped bass are absent or rare in these systems. Elkhorn Slough, a part of the National Estuarine Research Reserve System, is a shallow, tidal embayment and seasonal estuary at the head of the Monterey submarine canyon in Monterey Bay. The slough system comprises several distinct fish habitats, including the Moss Landing harbor, adjacent Bennett Slough, the main channel extending inland about 10 kilometers and fringed by extensive mudflats, a network of tidal creeks that meander through pickleweed marshes, and salt-evaporation ponds. All of these habitats are connected by the exchange of

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F I G U R E 5-8 Profiles of fishes in central California bays and estuaries representing five ecological categories based on salt tolerance and life-

history pattern: freshwater taxa, anadromous taxa, estuarine residents, marine migrants, and marine species that seasonally or occasionally enter these habitats. (See Table 5-3.)

tidal water, but differ in water depth, tidal influence (primarily salinity and current flow), and biological components such as plants that provide spawning sites and refuge for their particular assemblages of invertebrates and juvenile fishes. As in most bays and estuaries, fish distribution patterns vary with distance from the mouth of Elkhorn Slough. For example, marine species typically reside in the lower slough and harbor, where waters are strongly influenced by ocean and bay hydrographic properties such as higher salinity, lower water temperature, and variable turbulence compared with upper reaches of the slough. Resident fishes are distributed widely but most are abundant in the upper slough. Freshwater species occupy middle and upper slough habitats, including tidal creeks, ponds, and salt marshes. Dominant species of the upper slough and tidal creeks are best characterized as euryhaline with affinities toward higher temperature. At least 102 fish species from 43 families have been identified in Elkhorn Slough, and most (82 species) of them are marine fishes from Monterey Bay (Yoklavich et al., 1991). The most prevalent freshwater species are threespine stickleback, western mosquitofish, and prickly sculpin. Numerically dominant estuarine residents are bay pipefish, Pacific staghorn sculpin, and several species of goby. Principal species of marine

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migrants are topsmelt, jacksmelt, shiner perch and white seaperch, leopard shark, and bat ray. Some of the most abundant marine migrant species that visit the slough seasonally (e.g., Pacific herring, topsmelt, and shiner perch) are important forage species for coastal birds, fishes, and mammals. Other marine migrants, including economically valuable species such as English sole and California halibut, use Elkhorn Slough as a nursery ground and inhabit the relatively warm, calm slough waters as juveniles before moving offshore to continue development as adults. Gray smoothhound, northern anchovy, and speckled sanddab are marine species that also commonly occur in the Slough. Notably, only four alien species, American shad, western mosquitofish, striped bass, and yellowfin goby, occur in the Elkhorn Slough system. Compared to San Francisco Bay, Elkhorn Slough seems to have offered little opportunity for the introduction of exotic fish species. The Slough’s narrow opening may isolate it from tanker traffic and mariculture operations, two activities usually implicated in the introduction of nonnative fishes (Yoklavich et al., 1991). Various aspects of the fish assemblages in Elkhorn Slough have been studied in recent decades, including temporal and spatial patterns in abundance and diversity of juvenile and adult fishes (Talent, 1985; Yoklavich et al., 1991; Yoklavich et al., 2002), species

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composition and seasonality of larval fishes (Yoklavich et al., 1992), feeding ecology and energetics (Talent 1976, 1982; Yoklavich 1982a,b; Barry et al., 1996), and growth and reproduction of elasmobranchs (Martin and Cailliet, 1988a,b; Yudin and Cailliet, 1990; Kusher et al., 1992). The fish assemblages of Morro Bay, a designated National Marine Estuary, have been investigated in only two surveys. Fierstine et al. (1973) used small otter trawls to characterize the fish species in five zones during a 1-year period, and Horn (1980) sampled fishes with a beach seine at one location for 24-hour periods each quarter for a year. These two studies are complementary in that they used different sampling gear and, in part because of this difference, overlapped only slightly in habitats sampled. Whereas Fierstine et al. (1973) sampled the main channels and collected 66 species, Horn (1980) collected over the large mudflats of the Baywood Park area, along with some of the main channel west of these shallow areas, and captured 21 species, most of which had been taken in the earlier study. The combined list of species from the two studies is dominated by topsmelt, shiner perch, Pacific staghorn sculpin, and northern anchovy. Depending upon habitat and time of year sampled, the next species of numerical importance were California killifish, bay pipefish, shadow goby, bay goby, and tidewater goby, in addition to several species of surfperch and shark. The importance of habitat heterogeneity and environmental gradients in supporting fish species diversity is clearly demonstrated in Morro Bay, as it is in Elkhorn Slough, despite the limited number of studies of Morro Bay fishes. These relationships hold whether the focus is on the distinctiveness of fish assemblages in different habitats or on the classification of species based on salinity tolerance and life-history pattern. Fierstine et al. (1973) showed that zonation patterns occur in Morro Bay similar to those reported by Yoklavich et al. (1991) for Elkhorn Slough. For example, the sandy habitat near the entrance of Morro Bay was dominated by walleye surfperch, diamond turbot, sand sole, and speckled sanddab. In contrast, the area just inside the bay near the power plant was populated mainly by pelagic species, including northern anchovy, jack mackerel, and Pacific pompano, and by more inshore species such as topsmelt. Based on Fierstine’s (1973) trawl samples, silty areas containing eelgrass in the channels and mudflats of the southern part of Morro Bay were dominated by surfperches, including shiner perch and black perch plus walleye surfperch and white seaperch, flatfishes such as English sole, starry flounder, and diamond turbot, and two silversides, topsmelt and jacksmelt. Pacific staghorn sculpin was also relatively abundant as were juveniles of lingcod and several species of rockfishes. Six species of elasmobranchs—bat ray, round stingray, horn shark, shovelnose guitarfish, gray smoothhound, leopard shark, and thornback—were collected in the spring and summer months. Horn’s (1980) beach seine hauls in shallower areas of the southern part of the bay were more heavily dominated by topsmelt, contained more gobies, and, uniquely, captured bay pipefish and California killifish. Unfortunately, fishes occupying tidal creeks or habitats other than mudflats and channels in Morro Bay have not been sampled. Both Yoklavich et al. (1991) and Barry et al. (1996) noted that tidal creeks are most likely to be the main nursery habitats in Elkhorn Slough and that this function could be diminished by human-induced physical processes such as erosion. Similar studies and predictions need to be conducted in Morro Bay so that human influences on the habitats and their fish assemblages can be understood and minimized.

In terms of salt tolerance and life-history pattern, Morro Bay fish assemblages are similar to those of Elkhorn Slough with a few differences based largely on latitudinal distinctions (table 5-3; fig. 5-8). The principal freshwater species in Morro Bay is threespine stickleback. As mentioned above, diadromous fishes are uncommon in both Morro Bay and Elkhorn Slough. Dominant estuarine residents are similar to those in Elkhorn Slough, except that two species of southern affinity, California killifish and shadow goby, reach the northern extent of their ranges in Morro Bay. Marine migrants that commonly enter Morro Bay include forage species such as Pacific herring, topsmelt, and shiner perch and commercially important species such as English sole and California halibut. Another marine migrant, spotted turbot, extends northward only to Morro Bay and thus further distinguishes the fish assemblages of this system from those in Elkhorn Slough. Principal marine species that enter Morro Bay at least occasionally include gray smoothhound, northern anchovy, and speckled sanddab, as in Elkhorn Slough, but two other marine species, brown smoothhound and surf smelt, occur more commonly in the latter system. No alien species appears to have established itself in Morro Bay. The reasons proposed for the limited number of exotic species in Elkhorn Slough, isolation from tanker traffic and mariculture operations, also may be largely responsible for the absence of such species in Morro Bay. SOUTH E R N CA LI FOR N I A

Bays and estuaries in southern California are nestled within an arid region of Mediterranean climate and are fed by small, seasonal rivers and streams. As a result, these systems are mostly small and mainly marine in character, with fish assemblages that are largely devoid of freshwater and anadromous species and are dominated by estuarine residents and marine migrants (table 5-3 and fig. 5-9). Nevertheless, bays and estuaries in the region vary greatly in size from numerous small, canyon-mouth estuaries such as Malibu Lagoon to a few large systems, especially Anaheim Bay, Newport Bay, and San Diego Bay. The larger bays and estuaries display considerable habitat diversity and develop environmental gradients, especially during the winter months when the most rainfall occurs. These seasonal variations in habitat conditions combined with the warm-temperate geographic setting result in dynamic and distinctive fish assemblages occupying southern California bays and estuaries. These bay-estuarine assemblages (table 5-3, fig. 5-9) are distinguished, as mentioned, by lack of a freshwater component, except during occasional wintertime floods (see Horn and Allen, 1985), and also by lack of anadromous species, other than small runs of Pacific lamprey and mostly historic runs of the now endangered southern steelhead population (see table 5-4). Further distinction is achieved by the presence of striped mullet, the only catadromous species in the state. Principal estuarine residents in the larger bays and estuaries in southern California include Pacific staghorn sculpin, bay pipefish, and arrow goby, all virtually ubiquitous in these habitats in the state. Other common estuarine species are California killifish, slough anchovy, deepbody anchovy, spotted sand bass, and several other species of goby. Marine migrants are dominated by topsmelt, shiner perch, black perch, diamond turbot, juvenile California halibut, spotted turbot, and yellowfin croaker. Marine species that move into bays and estuaries in spring and summer include northern anchovy, gray smoothhound, round stingray, and barred sand bass. The most abundant alien

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F I G U R E 5-9 Profiles of fishes in Southern California and Northern Baja California bays and estuaries representing four ecological cate-

gories based on salt tolerance and life-history pattern: catadromous taxa, estuarine residents, marine migrants, and marine species that seasonally or occasionally enter these habitats. (See Table 5-3.)

species in southern California bay-estuarine systems is probably yellowfin goby. A few other alien species, such as rainwater killifish, which has been collected in upper Newport Bay, chameleon goby, now known from Los Angeles Harbor, and shimofuri goby have the potential to expand broadly into southern California bays and estuaries (Moyle, 2002). Attempts by the California Department of Fish and Game to introduce striped bass into Newport Bay in the 1970s eventually failed even though, for several years, the species was a reasonably abundant member of the top carnivore guild in that system (Horn and Allen, 1985). Reproductive failure occurred apparently because of insufficient amounts of low-salinity water required by the species for spawning (Horn et al., 1984). Differential habitat use characterizes the bay-estuarine fish assemblages in southern California just as in the other parts of the state (see Horn and Allen, 1985; Valle et al., 1999; Allen et al., 2002). The tidal channels of salt marshes are occupied primarily by California killifish and longjaw mudsucker. Shallow benthic areas of mudflats are inhabited most abundantly by four other species of goby, whereas the adjacent water column of both the shoreline and main channels are occupied by several common species, especially topsmelt, striped mullet, deepbody anchovy, and slough anchovy.

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Deeper areas of bay-estuarine habitats are populated mainly by marine migrants, including black perch, spotted sand bass, diamond turbot, and juvenile California halibut, and by marine species such as round stingray and barred sand bass. Eelgrass beds provide important habitat for several bay-estuarine fish species, including bay pipefish, barred pipefish, shiner perch, and giant kelpfish (Allen et al., 2002). Recent eelgrass transplants on mitigation sites in San Diego Bay indicate that successful restoration of eelgrass habitat can be achieved with fish densities quickly reaching those of a natural, reference eelgrass bed in the bay (Pondella et al., 2003). The fish assemblages of several small to large bay-estuarine systems in southern California have been studied intensively in recent decades. The major findings of studies in Malibu Lagoon, Anaheim Bay, Newport Bay, San Diego Bay, Sweetwater Marsh, and Tijuana Estuary are highlighted here. Malibu Lagoon is one of the small, canyon-mouth estuaries that occur throughout coastal southern California and contain relatively diminished fish assemblages, including endangered steelhead and tidewater goby (Lafferty et al., 1999; Dawson et al., 2001) and small populations of common estuarine residents. This small lagoon has a continuous freshwater inflow, but this flow varies seasonally in magnitude (Swift et al., 1989,

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TA B L E 5-6

Tropical/Subtropical Fishes Captured During a 1994 to 1999 Study of Fish Assemblages in San Diego Bay

Common Name California halfbeak Bonefish California needlefish Shortfin corvina Pacific seahorse California butterfly ray Banded guitarfish Red goatfish

Scientific Name

Total Number Collected

Hyporhamphus rosae Albula vulpes Strongylura exilis Cynoscion parvipinnis Hippocampus ingens Gymnura marmorata Zapteryx exasperata Pseudoupeneus grandisquamosus Total

Percent of grand total of fishes collected NOTE:

410 175 42 30 13 4 2 1 677

0.14%

After Allen et al., 2002.

1993). A study by Ambrose and Meffert (1999) showed that this system contains typical salt marshes species, such as topsmelt, California killifish, arrow goby, and longjaw mudsucker, near its mouth plus steelhead, tidewater goby, and various freshwater species in the upstream areas (fig. 5-7). Anaheim Bay (fig. 5-1), a part of the National Wildlife Refuge system since 1972, consists mainly of a relatively undisturbed salt marsh within the United States Naval Weapons Station near Seal Beach, California. Dredging of the mouth and adjacent harbor has allowed uninterrupted tidal flow into the marsh over the years. The main habitats within this bayestuarine system include salt marsh, tidal mud flats, and subtidal channels. About the time that Anaheim Bay became a refuge, its fish assemblage and other marine resources were examined in a multifaceted study that was published as an edited volume by Lane and Hill (1975). This work included an annotated checklist of 45 fish species in Anaheim Bay and 42 in the outer harbor and detailed life-history accounts of six of the most common species: California killifish, shiner perch, arrow goby, Pacific staghorn sculpin, California halibut, and diamond turbot. Overall, these studies indicated that the Anaheim Bay salt marsh is highly productive and supports rapid growth rates of the resident fish populations. Upper Newport Bay (fig. 5-1) was purchased by the state of California in 1975 and since then has been managed as an ecological reserve by the California Department of Fish and Game. The upper portion represents one of the largest, least altered salt marsh systems in the state south of Morro Bay. Shortly after Upper Newport Bay was established as a reserve, comprehensive 1-year (1978–1979) studies of the fish assemblages were conducted (Allen, 1982; Horn and Allen, 1985) and were followed by a 2-year monitoring survey in 1986–1987 to assess the effects of additional estuarine habitat on fishery-related species (Allen, 1988). In these investigations, topsmelt made up the majority of individuals in seine hauls, and this species along with striped mullet accounted for most of the fish biomass in the samples. Typically, topsmelt was followed in numerical abundance in these studies by California killifish, arrow goby, western mosquitofish, deepbody anchovy, and slough anchovy. Heavy rainfall in the first few months of the 1978–1979 study was responsible for the relatively high abundance of western mosquitofish during that period in this normally marine-dominated estuary. San Diego Bay (fig. 5-1), the third largest California bayestuarine system in California after San Francisco Bay and

Humboldt Bay, provides expansive and diverse habitats for fishes, including deep channels, marinas, and extensive shallows largely covered with eelgrass. The southern half of the bay is relatively unaltered and represents more natural condition of the system. In a 5-year (1994–1999) study of the bay’s fish assemblages by Allen et al. (2002) using a variety of sampling gear, just three of the 78 species collected, northern anchovy, topsmelt, and slough anchovy, accounted for most of the total numbers, whereas five species, round stingray, spotted sand bass, northern anchovy, bat ray, and topsmelt, made up two-thirds of the total biomass. In terms of an Index of Community Importance incorporating numbers, biomass, and frequency of occurrence, topsmelt, round stingray, and northern anchovy were the top-ranked species. One of the striking outcomes of the 5-year study by Allen and co-workers (2002) was the variety of tropical/subtropical species that were captured in San Diego Bay (table 5-6). Six of these species ranked in the top 50 in the Index of Community Importance: California halfbeak, shortfin corbina, California needlefish, California butterfly ray, bonefish, and Pacific seahorse (in descending index value). All warm-water species listed in Table 5-6 occur mainly farther south in the Mexican and Panamic biogeographic provinces (see Hastings, 2000), and each reaches the northern limit of its range in Southern California (Allen and Robertson, 1994). The shallow portions of San Diego Bay, as well as other bays and estuaries in the southern part of southern California, seem to act as refuges for these species. The frequent occurrence of El Niño events starting in 1982–1983 and culminating in the 1997–1998 event, along with the sustained warming trend in the region during the same time period (Smith, 1995), appears to have promoted the establishment of these otherwise tropical and subtropical fishes in Southern California. Studies of the fish assemblages in Sweetwater Marsh and Tijuana Estuary by Joy Zedler and associates are important contributions to bay-estuarine fish ecology in the region. Sweetwater Marsh, the largest remaining wetland on San Diego Bay and a part of the National Wildlife Refuge system, is continuously open to tidal action and comprises a mosaic of salt marsh vegetation and channels along with dredged channels and elevated roadways (Zedler, 2001). Tijuana Estuary (fig. 5-1), one of the most nearly intact salt marshes in southern California and a National Estuarine Research Reserve since 1981, also has retained its connection to the ocean almost continuously and persisted as an important bay-estuarine habitat

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TA B L E 5-7

20 Most Abundant Species Captured in Beam Trawl Sampling Estero de Punta Banda

Common Name Kelp bass Bay blenny Bay pipefish California halibut Barred sand bass Spotted turbot Spotted sand bass Diamond turbot Shiner perch Salema Giant kelpfish Sargo California tonguefish Senorita Queenfish Deepbody anchovy Mussel blenny Opaleye California halfbeak California corbina

NOTE:

Scientific Name

Bahia de San Quintin

Number

% of Total

Paralabrax clathratus Hypsoblennius gentilis Syngnathus leptorhynchus Paralichthys californicus Paralabrax nebulifer Pleuronichthys ritteri Paralabrax maculatofasciatus Hypsopsetta guttulata Cymatogaster aggregata Xenistius californiensis Heterostichus rostratus Anisotremus davidsoni Symphurus atricauda Oxyjulis californica Seriphus politus Anchoa compressa Hypsoblennius jenkinsi Girella nigricans Hyporhamphus rosae Menticirrhus undulatus

353 119 107 105 58 56 32

38.1 12.9 11.6 11.3 6.3 6.0 3.5

23 22 13 11 6 4 4 2 2 1 1 1 1

2.5 2.4 1.4 1.2 0.6 0.4 0.4 0.2 0.2 0.1 0.1 0.1 0.1

Totals

926

Common Name

Scientific Name

Number

% of Total

Bay pipefish Shiner perch Cheekspot goby California tonguefish California halibut Black perch Bay blenny

Syngnathus leptorhynchus Cymatogaster aggregata Ilypnus gilberti Symphurus atricauda Paralichthys californicus Embiotoca jacksoni Hypsoblennius gentilis

790 205 183 162 137 127 87

41.0 10.6 9.5 8.4 7.1 6.6 4.5

Diamond turbot Mussel blenny Specklefin midshipman Giant kelpfish Reef finspot Arrow goby Round stingray Spotted turbot Spiny dogfish Longjaw mudsucker Spotted scorpionfish Plainfin midshipman Kelp bass

Hypsopsetta guttulata Hypsoblennius jenkinsi Porichthys myriaster Heterostichus rostratus Paraclinus integripinnis Clevelandia ios Urolophus halleri Pleuronichthys ritteri Squalus acanthias Gillichthys mirabilis Scorpaena guttata Porichthys notatus Paralabrax clathratus

55 40 33 28 19 15 8 7 5 5 4 3 3

2.9 2.1 1.7 1.5 1.0 0.8 0.4 0.4 0.3 0.3 0.2 0.2 0.2

Totals

1929

Sampling occurred at 5 m depth in two northern Baja California bays and estuaries, Estero de Punta Banda and Bahia de San Quintin. After Rosales-Casian

1997.

despite problems of water quality and sedimentation (Zedler, 2001). The experimental and modeling approaches taken by Zedler and co-workers have demonstrated the importance of salt marsh vegetation and tidal creeks for fish inhabitants. Dominant species at both the Sweetwater and Tijuana sites are the longjaw mudsucker, California killifish, and arrow goby (Desmond et al., 2000). California killifish with access to the rich foraging areas of marsh surfaces consume much more food than killifish confined to creek habitats (West and Zedler, 2000). Applying a bioenergetics model to California killifish growth, Madon et al. (2001) showed that members of this species grow faster if they can feed on the marsh surface than if they are restricted to subtidal channels. These and other findings by the Zedler team make a strong case for including salt marshes and interconnecting tidal creeks in mitigation and restoration projects involving bay-estuarine fish habitats in southern California. NORTH E R N BA J A CA LI F O R N IA

The bays and estuaries of northern Baja California (fig. 5-1) support fish assemblages generally similar to those of southern California (table 5-3; fig. 5-9). Comparisons are limited, however, because the two Baja California systems, Estero Punta Banda and Bahia de San Quintin, have been sampled using mainly benthic trawls with lesser use of beach seines and gill nets (Hammann and Rosales-Casian, 1990; Rosales-Casian, 1996, 1997) rather than with several types of sampling gear used in the more comprehensive studies in southern California. In particular, the differences in the types of gear employed pre-

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cludes comparison of schooling and midwater fishes from the southern California and northern Baja California systems. Beam trawl samples taken in the two Northern Baja California systems were dominated by species commonly collected in trawls in bays and estuaries in southern California (table 5-7). The most abundant species sampled in Estero Punta Banda in 1992–1993 were kelp bass (juveniles), bay blenny, bay pipefish, California halibut, barred sand bass, and spotted turbot. Together, these six species accounted for 86% of the total catch. In Bahia de San Quintin in 1994, the most common species in the trawls were bay pipefish, shiner perch, cheekspot goby, California tonguefish, California halibut, and black perch, which, together, made up 83% of the total numbers of fish collected. Both Estero Punta Banda and Bahia de San Quintin have been characterized as highly productive bay-estuarine systems that are nursery areas for a number of marine fish species (Rosales-Casian, 1997). Three of these species, California halibut, kelp bass, and barred sand bass, are of major economic importance in both Mexico and the United States (see chapter 22). Baja de San Quintin, which is similar in size to San Diego Bay, may be the more important of the two systems because it is one of the largest, most nearly pristine such habitats on the Pacific coast of Baja California (Zedler, 2001); it also contains extensive eelgrass beds and features an almost permanent upwelling zone near its mouth (Rosales-Casian, 1997). This complex and heterogeneous embayment serves as a reference ecosystem for coastal wetland restoration efforts in southern California, but its pristine status is threatened by several potential development projects (Zedler, 2001).

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F I G U R E 5-10 Profiles of fishes in Central Baja California bays and estuaries representing three ecological categories based on salt tolerance

and life-history pattern: estuarine residents, marine migrants, and marine species that seasonally or occasionally enter these habitats. (See Table 5-3.)

CE NTR A L BA J A CA LI F O R N IA

Based on benthic trawl samples, Laguna de Ojo Liebre (fig. 5-1), also known as Scammon’s Lagoon, supports a fish assemblage with distinct southern affinities and therefore is substantially different from those in the bays and estuaries of northern Baja California and southern California (fig. 5-10). These trawl samples, containing a mixture of estuarine residents, marine migrants, and marine species, were dominated numerically by spotted sand bass, smooth puffer (Sphoeroides lispus), stingrays (Urolophus halleri and U. maculates), sargassum blenny (Exerpes asper), bay pipefish, and diamond turbot (Galván et al., 2000). Only three of these eight species are represented in the bays and estuaries of southern California. Overall, the Ojo Liebre fish assemblage shows a greater affinity with the assemblage in Bahia de Magdalena on the coast of southern Baja California.

Major Ecological Features of Bay-Estuarine Fish Assemblages in California The fish assemblages inhabiting bays and estuaries in California share several major ecological characteristics, at least some of which are common to bay-estuarine assemblages

in other parts of the world. Most of these features have been mentioned in the foregoing sections but are summarized explicitly in this section. LOW S P ECI E S DIVE R S IT Y

Bay-estuarine fish assemblages in California and elsewhere in the temperate zone tend to be dominated in abundance by a few (usually 5) species (table 5-8) and therefore have relatively low diversity even though many other, but much less common, species are typically encountered (Allen and Horn, 1975; Horn, 1980; Haedrich, 1983; Able and Fahay, 1998). This observation is supported by recent studies in New Zealand (Morrison et al., 2002), Germany (Thiel and Potter, 2001), the northeastern United States (Able and Fahay, 1998; Hughes et al., 2002; Hagan and Able, 2003; Lazzari et al., 2003) and California (Allen et al., 2002; Desmond et al., 2002; Matern et al., 2002). The five or fewer most abundant species in these systems are low in the trophic structure as would be expected from general patterns of relative abundance at different trophic levels. Thus, Allen and Horn (1975) observed that these species are usually planktivores (e.g., anchovies and herrings), omnivores (e.g., silversides, mullets, killifishes), or low-level

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TA B L E 5-8

Relative Proportions of the Five Most Abundant Fishes Sampled in Eight California Bays and Estuaries

San Pablo Bay (Ganssle, 1966)

Elkhorn Slough (Yoklavich et al., 1991)

Morro Bay (Horn, 1980)

Topsmelt Arrow goby Shiner perch Northern anchovy Slough anchovy Pacific staghorn sculpin California killifish Pacific herring Starry flounder California halibut Longfin smelt Longjaw mudsucker Striped bass Deepbody anchovy Jacksmelt

— — — 57.7 — — — 29.3 — — 4.7 — 3.1 — 1.9 —

22.3 15.5 10.8 — — 15.6 — — 8.5 — — — — — — —

Totals for top 5 species

96.6

72.6

Species

NOTE:

Carpinteria Marsh (Brooks, 2001)

Mugu Lagoon (Onuf and Quammen, 1983)

Upper Newport Bay (Allen, 1982, 1988)

South San Diego Bay (Allen et al., 2002)

Tijuana Estuary, (Williams et al., 2001)

31.1 — 26.6 11.2 — 23.9 2.2 — — — — — — — — —

30.6 50.3 — — — 3.2 9.8 — — — 2.5 — — — —

10.7 — 54.7 — — 11.4 5.4 — — 4.8 — — — — — —

66.3 13.9 — — 1.2 — 6.1 — — — — — — 2.6 — —

18.3 3.2 5.5 4.2 60.5 — — — — — — — — — — —

36.0 46.2 — — — 2.8 12.6 — — — — 1.1 — — — —

95.1

96.4

87.0

90.1

96.1

98.7

Percentage of total. Sites arranged left to right to portray their north to south latitudinal positions.

carnivores (e.g., gobies and flatfishes). In a 5-year study of San Diego Bay fishes by Allen et al. (2002) in which 78 species were collected, northern anchovy, topsmelt, and slough anchovy were the most abundant species, together accounting for 86% of the total catch. Similarly, in an 11-year survey of the fish assemblages in three Southern California estuaries by Desmond et al. (2002) in which 37 species were collected, arrow goby, topsmelt, and California killifish made up 70–95% of the cumulative abundance over all sites and years. In those studies that have determined biomass as well as numerical abundance, the results also show that only a few species, most of which are omnivores or planktivores, dominate the system. For example, in Upper Newport Bay, two species (striped mullet and topsmelt) accounted for almost 60% of the biomass, and three other species (yellowfin croaker, deepbody anchovy, and shiner perch) represented 14% of the total (Horn and Allen, 1985). In San Diego Bay, five species (round stingray, spotted sand bass, northern anchovy, bat ray, and topsmelt) accounted for 66% of the biomass (Allen et al., 2002). The preponderance of lower trophic-level species affects the overall trophic structure of bay-estuarine fish assemblages resulting in a shorter, “telescoped” (Odum, 1970) food chain. H IG H P RODUCTIVIT Y AN D B IOMAS S

Bays, estuaries, and salt marshes are among the most productive habitats in the world. They rank with tropical rain forests and coral reefs in net annual primary productivity (Whittaker and Likens, 1973). Swamps and marshes, including salt marshes that form at the edges of estuaries, emerge at the highest level in such a ranking. Given their extraordinarily high primary productivity and disproportionate abundance of low trophic-level fishes, bay-estuarine systems should be expected to support high secondary productivity. Though still sparse, the data that have been obtained so far bear out this prediction.

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The scarcity of studies on fish production in bays and estuaries is understandable because of the difficulties in obtaining meaningful information (Costa et al., 2002). Attempts to obtain productivity estimates based on biomass increase of a cohort of fish through the year must contend with an environment that is constantly changing because of tidal and stream inflow and with species that grow rapidly, migrate according to age and hydrologic condition, and recruit in several temporal pulses or perhaps in continuous immigration. Such a project requires that the collecting gear be chosen to sample all juvenile stages effectively; otherwise, the results may represent an artifact of sampling. In addition, other factors that must be considered include variability in local climate, food availability, and cohort mortality resulting from disease, predation, and fishing. These challenges help to explain why, to our knowledge, only one estimate of fish production exists for a bay-estuarine assemblage in California, and only a few have been completed for assemblages or individual species occurring in Atlantic coast systems of the United States and Europe. The single production estimate for a California assemblage of 9.4 g dry weight m
2 yr
1 was obtained in 1978 by Allen (1982) for the littoral portion of the fish assemblage in Upper Newport Bay (table 5-9). Young-of-the-year topsmelt accounted for
85% of the total production followed by deepbody anchovy (
5%), and California killifish (
4%). Productivity was highly seasonal, the main peak occurred in August and a much smaller peak in October. The annual value obtained must be considered an underestimate because adult striped mullet, even though the major contributor to fish biomass in a concurrent study (Horn and Allen, 1985), were inadequately sampled and therefore excluded from the calculations. Despite this underestimate, the annual productivity for the Upper Newport Bay littoral fish assemblage may be the highest yet recorded for any aquatic system using comparable methods of determination

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TA B L E 5-9

Annual Fish Production Estimates for Marine and Bay-Estuarine Systems with Comparable Production Determinations

Annual Production gDW m
2 yr
1

Source

Estuary, Upper Newport Bay, California Coastal lagoon, Mexico Restored salt marsh, New Jersey Salt marsh creek, Delaware Freshwater lagoons, Cuba Eelgrass beds, North Carolina Coral reef, Bermuda Coastal lagoon, Laguna Madre, Texas Kiel Bay, Sweden Salt marsh, Massachusetts Forth estuary, Scotland English Channel

9.4 8.6 8.4 8.1* 6.2 4.6 4.3 3.8 1.9 1.6* 1.1 1.0

Allen (1982) Warburton (1979) Teo and Able (2003) Meredith and Lotrich (1979) Holcik (1970) Adams (1976) Bardach (1959) Hellier (1962) Pihl and Rosenberg (1982) Valiela et al. (1977) Elliott and Taylor (1989) Harvey (1950)

Georges Bank (commercial fishes)

0.4

Clarke (1946)

System

*Recalculated value by Teo and Able (2003) from the original published value. NOTE: Wet weights converted to dry weights using a conversion factor of 0.25.

(table 5-9). The estimate of 10.2 g dry weight m
2 yr
1 reported for mummichog (Fundulus heteroclitus) inhabiting a tidal creek in Delaware (Meredith and Lotrich, 1979) was considered earlier (Allen, 1982) the highest fish productivity determination available. This value, however, has been recalculated down to 8.14 g dry weight m
2 yr
1 by Teo and Able (2003), who themselves obtained a productivity estimate of 8.37 g dry weight m
2 yr
1 for mummichog in a restored salt marsh in New Jersey (table 5-9). Other fish productivity estimates for European estuaries and a variety of marine systems are considerably lower than the above values (table 5-9). Although no estimates of annual productivity have been reported for other bay-estuarine fish assemblages in California, standing stock estimates (biomass densities, g m
2) are available for a few systems in the state and in Northern Baja California. Generally, similar values have been obtained for Morro Bay (3.1 g m
2) by Horn (1980), Upper Newport Bay (4.1 g m
2) by Allen (1982), and San Diego Bay (7.1 g m
2) by Allen et al. (2002), all using a beach seine in shallow-water areas of these three bayestuarine systems. The similarity of the Morro Bay and San Diego Bay densities to the Upper Newport Bay estimate, which was associated with high productivity estimates for that system, suggests that these two bays also contain highly productive fish assemblages. In contrast, biomass densities estimated for the fish assemblages in Estero de Punta Banda and Bahia de San Quintin in northern Baja California by Rosales-Casian (1997) from beam trawl catches were about 100 times lower (0.05–0.07 g m
2) than those for the three California systems. This discrepancy may have resulted from the absence of midwater, schooling fishes in the Baja California samples and also from the use of a beam trawl, which is less effective than a beach seine in capturing certain bottom species. MAR K E D S EASONALIT Y

California spans latitudes characterized by temperate conditions, cooler in the north and warmer in the south. Thus all shallow-water habitats in California experience some degree of seasonal temperature change. Moreover, precipitation varies dramatically during the year at most latitudes of the state because a large portion of the coast is under the influence

of a Mediterranean-type climate with warm, dry summers and cool, wet winters. In an earlier section, the higher rainfall of the northern part of California was contrasted with the lower rainfall conditions of the central and especially the southern parts of the state. Therefore, both a seasonal and a latitudinal component contribute to variations in temperature and rainfall (and freshwater inflow) experienced by the bay-estuarine systems of the state. Not surprisingly, the fish assemblages in the bays and estuaries of California undergo marked seasonal fluctuations in abundance, diversity, and composition that are correlated with variations in temperature and salinity during the year. Virtually all studies of these fish assemblages carried out for at least 1 year show a seasonal pattern of change, whether in the northern, central, or southern part of the state, in northern Baja California, or in expansive embayments such as San Diego Bay or small canyon-mouth estuaries such as Mugu Lagoon. The basic seasonal pattern in California bay-estuarine systems involves a few common species (e.g., gobies, Pacific staghorn sculpin) that reside year-round in the system and are joined in the spring and summer months by several abundant species entering as juveniles (e.g., northern anchovy, California halibut) or reproductively active adults (e.g., topsmelt, shiner perch). Studies in Elkhorn Slough (Yoklavich et al., 1991), Morro Bay (Horn, 1980), Colorado Lagoon in Alamitos Bay (Allen and Horn, 1975), Upper Newport Bay (Horn and Allen, 1985), and San Diego Bay (Allen et al., 2002), among others, provide evidence to support this general pattern of abundance and diversity on monthly (fig. 8-11), seasonal (fig. 8-12), and interannual scales (fig. 8-13). Salinity and especially temperature are identified most commonly as the environmental factors associated with these patterns in fish assemblages. The relationship between the biotic and abiotic variables, however, is often more complicated than may be appreciated at first, and we highlight several examples here. For instance, Desmond et al. (2002) concluded that variation in the fish assemblages of three southern California estuaries resulted from seasonal differences driven by changes in temperature but in the same study found that the invertebrate assemblages showed little seasonal variation. The variations that were

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F I G U R E 5-11 Monthly variation in number of species, abundance, and biomass of the littoral fishes from Upper Newport Bay, California in 1978 (after Allen 1982).

shown by the invertebrates were more related to stream flow and dissolved oxygen levels than to temperature. For the Upper Newport Bay fish assemblage, Horn and Allen (1985) emphasized that temperature was the main factor influencing the annual cycle of abundance and diversity but recognized the importance of salinity especially because their study was conducted during a year (1978) marked by heavy rainfall during the first few months. Increased sedimentation accompanying the elevated freshwater inflow was a complicating factor in attempts to account for the seasonal pattern of upper bay fishes. Major storms and associated flooding impacted the fish populations in Mugu Lagoon, as documented during a 5year study conducted in the late 1970s by Onuf and Quammen (1983). Water-column fishes, especially topsmelt and shiner perch, were more severely affected than bottomdwelling species because the additional sediment inflow reduced the low tide volume of the lagoon and destroyed the eelgrass beds. El Niño events, which raise water temperatures and affect other habitat conditions as well, also create a set of complicating factors that can influence fish assemblages within an annual cycle. Allen et al. (2002) provided evidence

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F I G U R E 5-12 Seasonal pie diagrams depicting the annual cycle of (A) numbers and (B) biomass of four of the most common fish species and the remaining species collected by beach seine in the Baywood Park section of Morro Bay. Total diversity (H’) is given in the center of each cycle; the area of each circle is proportional to sample size, the number to the lower left of each circle is quarterly diversity H’, and the number on the connecting arrow is percentage similarity between months (after Horn, 1980).

that the 1997–1998 El Niño measurably reduced fish abundance in San Diego Bay in 1997, especially of schooling, planktivorous species. One of these species, northern anchovy, the most abundant fish overall in the 5-year study, was virtually absent during 1997, apparently in response to the increased temperatures associated with the El Niño. A final example of the influence of complicating factors is provided by Matern et al. (2002) in their long-term (21-year) study of fishes in Suisun Marsh, a part of the San Francisco Bay estuary. Although these investigators acknowledged that temperature and salinity were factors correlated with variations in abundance in some fish species, they concluded that the lack of predictable assemblage structure in the system was also significantly affected by human-caused disturbances (e.g., changes in freshwater input) and frequent invasions by alien species. STRONG I NTE RAN N UAL VA R IAB I LIT Y

Only a small number of long-term investigations, of 5 years or longer, have been conducted on bay-estuarine fish assemblages in California or, for that matter, in other temperate regions of the world. Yet, bays and estuaries are widely recognized as highly variable systems inhabited by fluctuating populations of fishes

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F I G U R E 5-13 Seasonal variation in fish abundance (number) and biomass (kg) during a 5-year period in San Diego Bay (1994–1999) (after Allen et al., 2002).

and other organisms that are not likely to remain the same year after year because of natural changes in the environment. Bayestuarine systems, however, have been subjected to more than natural forces, i.e., to degradation by human activities and invasion by alien species. Their recognized importance as fish habitats and growing efforts to restore them create the need for longterm surveys of their fish and invertebrate assemblages to assess the variability of these assemblages over space and time and to attempt to understand the causes of the variations. Here we review some of the long-term studies of bayestuarine fish assemblages in California in part to justify our use of the word “strong” in the subheading for this section of the chapter, remembering that the overall purpose of the section is to summarize five general ecological features of bay-estuarine fish assemblages and their habitats. We have used a minimum of 5 years to define a long-term survey in part because the recruitment dynamics of short-lived species such as silversides, killifish, and gobies ought to be observable in this length of time. Another reason stems from the value derived from two 5year studies that were mentioned in the previous subsection. In the first of these investigations, Onuf and Quammen (1983) evaluated the impact of major storms and flooding on the fish assemblage in Mugu Lagoon, a small, canyon-mouth estuary in southern California. Occurring at the start of the second and fourth years of the 5-year study, these disturbances were substantial enough to account for most of the annual changes seen in the fish populations inhabiting the lagoon. Accumulation of sediment resulting from the storms reduced the available habitat for water-column fishes such as topsmelt and shiner perch and destroyed the eelgrass beds, which were used for feeding

and refuge sites by several fish species. Onuf and Quammen (1983) reasoned that major disturbances that sharply and somewhat irreversibly reduce fish abundance are to be expected in small embayments along steep coastlines in regions of Mediterranean-type climate in southern California where winter storms are common and occasionally severe in magnitude. In the second 5-year study, which spanned 1994–1999, Allen et al. (2002) detected the apparent impacts of the 1997–1998 El Niño on the fish assemblage in San Diego Bay. Schooling, planktivorous fishes were most heavily affected. Among these species, northern anchovy, which ranked first in overall abundance in the study, almost disappeared in 1997. None was recorded in the samples taken in July 1997 in contrast to nearly 150,000 captured in July of the previous year. Simply stated, these two studies were long enough to have included infrequent but powerful environmental events and to have allowed evaluation of their impacts on fish assemblages. A few longer term surveys of bay-estuarine fish assemblages in California have been conducted, and three recently completed such works are summarized here with an emphasis on the value of an extended investigation in highly variable systems. Matern et al. (2002) documented the changing and unpredictable composition of the fish assemblages of Suisun Marsh in the San Francisco Bay estuary in a 21-year otter trawl and beach seine survey. The fauna of 53 total species comprised a mixture of native and alien species and a combination of freshwater, estuarine, and marine representatives in this brackish tidal marsh. Not only was the assemblage structure unpredictable over time, but overall abundance declined, particularly among native

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F I G U R E 5-14 Average yearly catch per minute of (A) alien fishes excluding yellowfin goby and shimofuri goby, (B) yellowfin goby

plus shimofuri goby, (C) native fish species excluding threespine stickleback, and (D) threespine stickleback in Suisun Marsh, San Francisco Bay estuary, 1979–1999. The timing of some major events is indicated (after Matern et al., 2002).

resident and seasonal species but not among alien species (fig. 5-14). The investigators attributed the lack of assemblage structure to naturally fluctuating conditions of the estuary, to species declines probably related to anthropogenic disturbances, and to the frequent invasions of alien species of both fishes and invertebrates. According to Matern and co-workers, some degree of predictable assemblage structure and stabilized abundances of native species will not be achieved until human disturbances and alien invasions are reduced. High year-to-year variability in abundance of resident species was also supported by long-term data from Tijuana Estuary, a relatively small embayment in southern California adjacent to the U.S.-Mexican border (Williams et al., 2001) (fig. 5-15). The annual abundance of the top five species (arrow goby, topsmelt, California killifish, staghorn sculpin, and longjaw mudsucker) recorded from Tijuana Estuary varied dramatically from 1986 to 1999 with coefficients of variation ranging from 350% to 195% of the mean for each species. In a third, related survey, Desmond et al. (2002) sampled both fish and invertebrate assemblages in three southern California estuaries (Los Penasaquitos Lagoon, Sweetwater Marsh, and Tijuana Estuary) during an 11-year period. For fishes, which were sampled using a bag seine and blocking nets, the study focused on resident rather than transient species because sampling was conducted only at low tide.

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Perhaps as expected given the fluctuating character of estuaries, the investigators found high variation in fish (fig. 5-16) and invertebrate species, within and among the three estuaries. Less expected, however, were results showing that the fish assemblage varied seasonally in abundance and species richness, whereas the invertebrate assemblage varied little over the seasons but exhibited a much higher degree of interannual variation than the fishes. Variation in the fish assemblage was driven primarily by seasonal changes in temperature, as has been shown for other bayestuarine fish assemblages in southern California (e.g., Allen and Horn, 1975; Horn and Allen, 1985; Allen et al., 2002). In contrast, the invertebrate assemblage responded more predictably to interannual changes in stream flow and dissolved oxygen levels, indicating that irregular disturbances such as flooding have a more profound effect on these inhabitants than predictable, seasonal changes in temperature. Clearly, a value of this long-term study was the discovery that the fish and invertebrate assemblages vary differently in space and time. These results can be applied to the design of monitoring programs for wetland restoration or mitigation. P ROM I N E NT N U R S E RY F U NCTION

The role as nursery area for juveniles of coastal fish species is probably the most widely recognized and accepted func-

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F I G U R E 5-15 Annual variation in abundance of the most common bay and estuarine species captured in Tijuana Estuary from 1986 through 1999 (after Williams et al., 2001).

tion of bays and estuaries in their overall status as important fish habitats. Pihl et al. (2002) defined a nursery as a concentration of juvenile stages that are feeding and growing and listed nursery area as one of the four main habitat functions of estuaries along with spawning ground, feeding ground, and pathway for spawning migrations of diadromous species. In their survey of 26 European estuaries, Pihl and co-workers found that more than 60% of the fish species recorded in these habitats were using them as nurseries. Numerous recent publications on bay-estuarine, salt marsh, and other near shore coastal fishes contain “nursery” in the title, an indication of the continued importance of evaluating this function in shallow-water habitats (e.g., Forrester and Swearer, 2002; Gillanders et al., 2003; Lazzari et al., 2003; Minello et al., 2003). In California, most of the sampling studies of bay-estuarine fish assemblages mention the importance of the nursery function and often that a large proportion of the catch were juveniles (e.g., Yoklavich et al., 1991; Matern et al., 2002). Length-frequency analyses further show the predominance of juveniles among the most abundant species (Horn, 1980; Horn and Allen, 1985; Valle et al., 1999), as well as differential habitat use in tidal creek habitats by juveniles and adults (Desmond et al., 2000). The only bay-estuarine study to date in California to report the actual percentages of juveniles for a large portion of the total number of species captured is that by Allen et al. (2002) in their 5-year survey of fish assemblages in San Diego Bay. Nearly 70% of all fishes captured were juveniles, and for 27 of the 34 most abundant fish species, more than half of the

individuals sampled were juveniles (table 5-10). Collections of four species, northern anchovy, spotted kelpfish, giant kelpfish, and kelp bass, consisted entirely of juveniles, and more than 90% of the individuals of six other species were juveniles. Despite the wide acceptance of a nursery function for bays and estuaries and associated salt marshes, concern has been raised about the rigor that been applied in ascribing a nursery function to bays and estuaries and other coastal habitats. In a seminal paper authored by 13 estuarine fish ecologists, Beck et al. (2001) criticize the ambiguity that they claim surrounds the nursery-role concept and interferes with its use as a tool in conservation and management. To strengthen the concept, they propose a hypothesis built on the prevailing notion that some inshore juvenile habitats contribute disproportionately to the production of juveniles that recruit to adult populations. Their hypothesis states that “a habitat is a nursery for juveniles of a particular species if its contribution per unit area to the production of individuals that recruit to adult populations is greater, on average, than production from other habitats in which juveniles occur.” A nursery habitat in the terms of Beck et al. (2001) supports a greater than average combination of higher density, growth, and survival of juveniles and movement to adult habitats. This demanding but testable hypothesis holds promise for increasing the rigor of research in estuarine fish ecology. Papers already are being published that address components of the nursery-role hypothesis (e.g., Gillanders et al., 2003; Heck et al., 2003; Minello et al., 2003), and it is important to test the hypothesis in California bay-estuarine systems.

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FIGURE 5-16 Biplots of non-

metric multidimensional scaling (NMDS) analysis of fish assemblage data collected in three southern California bays and estuaries from 1987 to 1998. LPL  Los Penasquitos Lagoon, SM  Sweetwater Marsh, and TE  Tijuana Estuary. NMDS axis 1 was significantly affected by estuary, station, and season but not year; NMDS axis 2 was significantly affected by station, year, and season but not estuary. Values are means  standard errors for all samples (after Desmond et al., 2002).

Recommendations for Future Studies Several types of studies are needed if we are to deepen our understanding of the structure and function of bay-estuarine fish assemblages in California and Baja California and to enhance our abilities to conserve and manage these impacted species and their diminished habitats more effectively. Here are some of the types of projects and problems that are worthy of attention in future research. 1. Conduct comprehensive surveys in understudied bays and estuaries to establish baseline information on their fish assemblages and undertake new surveys of systems studied decades ago to detect any changes, both using an array of the most effective types of sampling gear. 2. Revive ichthyoplankton surveys after a few decades of reduced activity for the same purposes as stated in 1 above. Excellent baseline studies exist from previous works, and an outstanding atlas of egg and larval types for California marine fishes (Moser, 1996) is available to facilitate the renewed efforts. Relevant here is the impression gained by Matern et al. (2002) that environmental variables act mainly on very young life stages rather than on the larger juveniles and adults usually captured in trawls and seines. 3. Initiate or continue long-term surveys (of 5 or more years) for both juvenile-adult and ichthyoplankton assemblages. Such studies yield expected and

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unexpected results of value especially with regard to understanding interannual variability and the effects of pulsed disturbances such as flooding or ENSO events on these assemblages. The several studies summarized in this chapter produced both types of results. 4. Determine food origins and trophic positions using stable isotopes and lipid biomarkers. A variety of carbon and energy sources are potentially available in bay-estuarine habitats, especially for abundant species such as topsmelt ands striped mullet that feed on a wide range of food sources including detritus, which may have multiple origins. The comprehensive food web analysis of two bay-estuarine systems in southern California by Kwak and Zedler (1997) using multiple stable isotopes provides a solid basis for further research. 5. Estimate production for fish populations in a variety of bay-estuarine systems. To our knowledge, only one such estimate of fish production exists for a California system, and that study yielded what may be the highest value yet determined for an aquatic habitat. For European estuaries, Costa et al. (2002) emphasized the need to assess fish production in areas with contrasting features, to quantify the loss of production in degraded habitats, to determine what production is exported to marine areas, and to estimate the relative proportions of production of migrating marine species that have some production in both estuarine and marine habitats. These needs seem even greater

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TA B L E 5-10

Estimated Percent of Juveniles Among the 34 Most Abundant Fishes in a 1994–1999 Study in San Diego Bay

Common Name Northern anchovy Spotted kelpfish Giant kelpfish Kelp bass California halibut Bonefish Barred sand bass Pacific sardine Striped mullet Salema Arrow goby Barred pipefish Bay pipefish Topsmelt Queenfish California killifish Shadow goby Jacksmelt Specklefin midshipman Cheekspot goby Black perch California grunion Yellowfin croaker Dwarf perch Fantail sole Round stingray Shiner perch Slough anchovy Bay blenny Black croaker Spotted turbot Deepbody anchovy Spotted sand bass Diamond turbot

NOTE:

Scientific Name

% Juveniles

Engraulis mordax Gibbonsia elegans Heterostichus rostratus Paralabrax clathratus Paralichthys californicus Albula vulpes Paralabrax nebulifer Sardinops sagax Mugil cephalus Xenistius californiensis Clevelandia ios Syngnathus auliscus Syngnathus leptorhynchus Atherinops affinis Seriphus politus Fundulus parvipinnis Quietula y-cauda Atherinopsis californiensis Porichthys myriaster

100 100 100 100 99 99 97 96 95 94 79 78 76 73 73 72 71 69 67

Ilypnus gilberti Embiotoca jacksoni Leuresthes tenuis Umbrina roncador Micrometrus minimus Xystreurys liolepis Urolophus halleri Cymatogaster aggregata Anchoa delicatissima Hypsoblennius gentilis Cheilotrema saturnum Pleuronichthys ritteri Anchoa compressa Paralabrax maculatofasciatus Hypsopsetta guttulata

67 66 66 66 63 61 53 51 43 37 36 35 23 22

Average % juveniles/ species

69

18

After Allen et al., 2002.

populations. Continued monitoring is required to detect the occurrence and spread of alien species, and manipulative field and laboratory experiments similar to those conducted by Matern (1999) on shimofuri goby are needed to assess the impact and predict the spread of such invaders. Alien species, especially gobies, continue to appear and establish breeding populations and to spread from their site of introduction. 9. Determine the impacts of nutrient pollution (eutrophication) on bay-estuarine fish assemblages in California. A recent study on an Atlantic coast bay-estuarine system shows that, as the nitrogen load increases, macroalgal biomass increases, eelgrass density and biomass diminish, and fish abundance, diversity, and growth decline (Deegan et al., 2002). Such studies are rare in California systems (see Minello et al., 2003), but nutrient loading is a widespread phenomenon in temperate bays and estuaries, including many in California such as Upper Newport Bay (Kamer et al., 2001). 10. Assess and predict the impacts of climate change from long-term monitoring of fish assemblages in California’s bays and estuaries. Climate change is likely to exacerbate the effects of eutrophication and other stresses through higher water temperatures and alterations in sea level, freshwater input, and ocean exchange (Scavia et al., 2002). Restoration projects and water management plans involving bays and estuaries should take into account longer term changes anticipated as a result of climate change.

Acknowledgments We thank the many students and colleagues who have helped us in our own studies of bay-estuarine fish assemblages over the years. The Monterey Bay National Marine Sanctuary, Elkhorn Slough Foundation, California Department of Fish and Game, National Marine Fisheries Service, Department of the Navy, and the Port of San Diego provided funds and administrative support for the studies summarized in this chapter. Peter Moyle provided data on the fish assemblage of the Navarro River Estuary. Elkhorn Slough National Estuarine Research Reserve provided temperature data for 2000.

in California given the near absence of fish production studies in the state’s bays and estuaries. 6. Investigate estuarine–coastal coupling using up-todate tagging procedures, molecular genetic techniques, and stable isotope and lipid biomarkers as in 5 above. Research is still needed to determine whether certain especially abundant species move from estuaries into coastal waters and transport outward the high secondary production characteristic of bay-estuarine systems. 7. Test the nursery-role hypothesis of Beck et al. (2001) for different habitats within and among bay-estuarine systems in California. If tested as proposed, this challenging hypothesis ought to increase the effectiveness of conserving and managing bay-estuarine habitats and their fish assemblages. 8. Design and implement studies to test the impacts of alien fish and invertebrate species on native fish

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CHAPTER 6

Surf Zone, Coastal Pelagic Zone, and Harbors LAR RY G. ALLE N AN D DAN I E L J. P O N D E LLA I I

Introduction The nearshore zone off the Californias includes a number of other unique, primarily soft-bottom habitats. This expansive area spans the exposed, sandy beaches to the water column above the inner shelf along the entire coastline of California and south into Baja California. The fishes common to this area typically occur over the shallower portions of the shelf (see chapter 7) and the soft bottom surrounding rock reef and kelp bed environments (see chapter 8). The fish assemblages of this area tie all of the shallow water habitats closely together (Allen, 1985). In this chapter, three of the more distinctive fish assemblages within this general area will be discussed: (1) fishes of the surf zone and adjacent drift algal habitat, (2) the coastal pelagic fishes that occupy the water column above the shallow soft bottom and shelf, and (3) fishes of the numerous harbors that have been formed by breakwater construction within this general zone.

Surf Zone and Adjacent Drift Algal Beds The fishes living in the surf zone must contend with one of the most turbulent environments in the sea. Wave action, tidal exchange, and long-shore currents produce a high energy environment, which should require correspondingly high energy expenditure by the fishes just to maintain position (Romer, 1990; Clark, 1997). On the other hand, the surf zone is an interface between the sea and land and receives nutrient and detrital input from both (Robertson and Lenanton, 1984). The productivity from this flux supports large populations of small invertebrates, which are repeatedly uncovered by the shifting sands of the surf. Thus the surf zone can support surprisingly large populations of relatively few species on both a diel and seasonal basis (McFarland, 1963; Naughton and Saloman, 1978; Modde and Ross, 1981, Ross et al. 1987, Santos and Nash, 1995) and provides nursery habitat for a number of coastal fish species throughout the world (Modde, 1980; Lenanton et al, 1982; Ruple, 1984; Lasiak, 1986; Senta and Kinoshita, 1985, Harris and Cyrus, 1996; Beyst et al., 1999; Suda et al., 2002).

Worldwide, exposed beaches are occupied by the following types of fishes: (1) small, active planktivores; (2) roving substratum feeders; (3) benthic flatfishes; (4) migratory species; (5) beach spawners; and (6) piscivores (Moyle and Cech, 2000). Most species in the surf also occur in other coastal habitats, and a few species occur primarily in the surf. Small, silvery, streamlined planktivores, including silversides (Atherinidae and Atherinopsidae), anchovies (Engraulidae), and herrings (Clupeidae) are often the most abundant fishes that occupy surf zones. Croakers (Sciaenidae) represent roving substratum feeders, particularly those of the genus Menticirrhus known as kingfish (Atlantic and Gulf of Mexico) or corbina (Pacific). Many species of croakers, including members of the genus Menticirrhus, possess sensitive chin barbels for detecting prey in the substratum. Fishes of this genus lack swimbladders as adults as an adaptation for living in these turbulent environments (Eschmeyer et al, 1983). Flataegs can also minimize the effect of turbulence. Both flatfishes (pleuronectiforms) and rays (rajiforms) are suited for living in the surf and are well represented in this habitat in many parts of the world (McFarland, 1963; Robertson and Lenanton, 1984; Ross et al., 1987; Romer, 1990; Santos and Nash, 1995; Clark, 1997; Beyst et al., 1999). Many migratory species are found in the surf zone seasonally. Mullets (Mugilidae) whose large schools are often observed from shore throughout the warmer waters of the world are probably the best documented among the migratory species (Thomson, 1955; Chubb et al., 1981; Cech and Wohlschlag, 1982; Funicelli et al., 1989). Beach spawners are not common, but various species of silversides (Atherinopsidae), smelts (Osmeridae; Schaefer, 1936; Hart and McHugh. 1944), and some puffers (Tetraodontidae; Yamahira, 1997) deposit eggs either on or in the sand at or above the water line. The best known examples of beach spawners are the California and gulf grunion (Leuresthes tenuis and L. sardina) of the northeastern Pacific Ocean (Walker, 1952; Thomson and Muench, 1976). Finally, the large numbers of small forage fishes that occupy the surf zone throughout the world attract many piscivorous fishes. The best known examples of large piscivores entering the surf to feed as evidenced by surf fisheries are bluefish (Pomatomus saltatrix; Buckel et al., 1999), striped bass (Morone

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TA B L E 6-1

Relative Abundance of Fishes Collected by Beach Seine Along Orange and San Diego County Coasts

Common Name

Scientific Name

Walleye surfperch California grunion Topsmelt Barred surfperch California corbina Spotfin croaker Queenfish Yellowfin croaker Dwarf perch Jacksmelt Northern anchovy Round stingray Deepbody anchovy Kelp pipefish White seaperch Pacific sardine White croaker Giant kelpfish Opaleye Bat ray Rock wrasse Leopard shark Calico surfperch Gray smoothhound Black perch

Hyperprosopon argenteum Leuresthes tenuis Atherinops affinis Amphisticus argenteus Menticirrhus undulatus Roncador stearnsii Seriphus politus Umbrina roncador Micrometrus minimus Atherinopsis californiensis Engraulis mordax Urolophus halleri Anchoa compressa Syngnathus californiensis Phanerodon furcatus Sardinops sagax Genyonemus lineatus Heterostichus rostratus Girella nigricans Myliobatis californica Halichoeres semicinctus Triakis semifasciata Amphisticus koelzi Mustelus californicus Embiotoca jacksoni

California barracuda

Sphyraena argentea

Aliso Beach 33.7 14.6 6.7 18.1 16.9 0.7 2 2.1 0.3 1.7 1.3 0.3

Enlisted Man’s Beach

San Onofre Beach

11.6 39.2 10.5 6.1 3.1 9 4.4 3.5 3.9 1.6 1.6 1.5 0.8 0.9 0.5

37.2 13.8 19.7 10.1 4.2 3.7 4.3 2 1.5 0.1 0.1 0.2 0.3 0.2 0.4

0.9 0.7 0.4 0.1 0.4 0.1 0.2 0.1

0.3 0.4 0.3 0.2 0.2 0.3

0.2

NOTE : Ranked by mean abundance. Collected at three stations along the open coast of southern Orange County and northern San Diego County between approx. 33° 21’ N; 117° 33’ W and 33 ° 12’ N; 117° 24’ (after Tetra Tech 1977).

saxatilus; Settler et al., 1980; Carmichael et al., 1998), sea trout (Cynoscion spp.; Moflett, 1961; Ditty et al., 1991), red drum (Sciaenops ocellatus; Mercer, 1984), and jacks (Carangidae; Thompson and Munro, 1974; Saloman, and Naughton, 1984) on the Atlantic and Gulf coasts of North America. In California, the surf zone along sandy beaches is a major habitat. Sandy beaches make up approximately 57% of the coastline north of Pacific Transition Conception and almost 82% of the mainland coastline from Pacific Transition Conception south to the Mexican border (see chapter 1, this volume). Despite this, the fish assemblages of the surf zone have not received a great deal of attention in California mainly because it is a very difficult place to sample effectively. The turbulent environment of the surf zone presents problems to the fish, and it also makes seining difficult to impossible at times. The most consistent, and comprehensive study of this environment in California waters was carried out by Carlisle et al. (1960) during a 44-month period (February 1953 to September 1956) in conjunction with lifehistory studies on barred surfperch for the California Department of Fish and Game. This study included data from 451 beach seine hauls of various lengths at 11 locations from Carpinteria near Santa Barbara south to San Diego. Unfortunately, the original catch records from this monumental sampling effort were discarded; thus, a detailed analysis of the data is no longer possible. Nevertheless, Carlisle et al. (1960) reported more than 70 species of fish from the seine hauls. The top 10 species in order of abundance were

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northern anchovy (Engraulis mordax), queenfish (Seriphus politus), barred surfperch (Amphisticus argenteus), walleye surfperch (Hyperprosopon argenteum), shiner perch (Cymatogaster aggregata), topsmelt (Atherinops affinis), staghorn sculpin (Leptocottus armatus), white croaker (Genyonemus lineatus), California corbina (Menticirrhus undulatus), and deepbody anchovy (Anchoa compressa). However, Carlisle’s summary table pooled the catch from beach seine hauls from the exposed coast with some from bays and estuaries which overemphasized the relative abundance of some species (e.g., Pacific staghorn sculpin) in the surf zone. Allen (1985) incorporated Carlisle’s data along with more recent seine data from surf zone habitat in Orange and San Diego counties (table 6-1) and identified a distinct group of fishes that characterized the open coast environment. This group included barred surfperch, walleye surfperch, California grunion (Leuresthes tenuis), and three species of croakers, California corbina, spotfin croaker (Roncador stearnsi), and yellowfin croaker (Umbrina roncador) (fig. 6-1). The surf zone is the primary habitat for only two of these species, barred surfperch and California corbina. Not surprisingly, both have long been the primary target of surf anglers in Southern California for many years (Joseph, 1962). Based on existing studies, the surf zone of southern California can be characterized as numerically dominated by silversides (topsmelt and jacksmelt, Atherinopsis californiensis), anchovies (northern anchovy), juvenile queenfish (a croaker), and walleye surfperch that represent small planktivores.

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F I G U R E 6-1 Common fish species of the surf zone in Southern California (see figure 6-3 for an enlargement of drift algal associates).

Queenfish and walleye surfperch are nocturnal planktivores that inhabit the surf zone during the day (Hobson and Chess, 1976). The three species of croaker, including the California representative of the genus Menticirrhus, the California corbina, qualify as roving substrate feeders along with barred surfperch, leopard shark (Triakis semifasciata), and gray smoothhound (Mustelus californicus)(Carlisle et al., 1960; Joseph, 1962; Russo, 1975, Talent, 1982; Haeseker and Cech, 1993, Webber and Cech. 1998). Round stingrays (Urobatis halleri) are the most common “flatfish” in the southern California surf zone, although spotted turbot (Pleuronichthys ritteri) also frequent this area. California grunion represents the surf spawner group. The piscivorous species that frequent the surf zone in California waters are not well documented but undoubtedly include two species of commercially important fishes, white seabass (Atractoscion nobilis—actually a croaker) and California halibut (Paralichthys californicus). Both are large, mobile, predatory fishes that frequent the surf zone in southern California seasonally (Pondella and Allen 1999) and have, historically been targeted there by both commercial and recreational fishers (Thomas, 1968; M. J. Allen 1990). Recently, Mulligan and Mulligan (in prep) found that the surf zone of northern California is numerically dominated by true smelts (e.g., surf smelt, Hypomesus pretiosus and night smelt, Spirinchus starksi), silversides (topsmelt), and surfperches (shiner perch and calico surfperch, Amphisticus koelzi) (fig. 6-2). Furthermore, the overwhelming majority (92%) of all individuals captured in the surf zone at two sites in Trinidad Bay were juveniles (table 6-2). This investigation

also identified a number of species that were closely associated with the mixed algal and debris mats that are common in this northern surf zone. These algal-associated species included a number of cryptically colored fishes that occur more frequently in shallow rocky habitats, including striped seaperch (Embiotoca lateralis), black rockfish (Sebastes melanops), slimy snailfish (Liparis mucosus), pricklebreast poacher (Stellerina xyosterna), bay pipefish (Syngnathus leptorhynchus), cabezon (Scorpaenichthys marmoratus), silverspotted sculpin (Blepsias cirrhosus), and penpoint gunnel (Apodichthys flavidus). Drift algae has been recognized as an important component of the surf zone in other parts of the world (Robertson and Lenanton, 1984; Romer, 1990) but was largely overlooked in California for many years. This important nursery area was largely unstudied until the 1980s when the search for the nursery grounds for the two commercially important species, the white seabass and California halibut was undertaken within the southern California Bight (Allen, 1988; Allen and Franklin, 1988; 1992; Allen and Herbinson, 1990). Beam trawl studies identified the beds of drift algae adjacent to the surf line as the primary settlement areas for white seabass during the summer months. The cryptic coloration of settling juveniles is particularly well suited for this habitat by providing necessary camouflage (fig. 6-3). These surveys (Allen et al, 1990) and those conducted by Kramer (1990, 1991) and Allen and Herbinson (1990) in the southern portion of the Bight also concluded that in certain, protected areas (e.g., Malaga Cove north of the Palos Verdes Peninsula), this subhabitat consti-

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F I G U R E 6-2 Common fish species of the surf zone in Trinidad Bay, northern California (after Mulligan and Mulligan, in prep).

tuted an important secondary settlement area along the open coast for California halibut, which settle primarily in bays and estuaries (see chapter 5). Similarly, the juveniles of an important recreational species, kelp bass (Paralabrax clathratus), also recruit to these southern drift beds (Cordes and Allen, 1997) during the summer months. Although kelp bass settle out primarily in kelp beds, drift beds probably attract a significant proportion of recruiting kelp bass because these beds occur over extensive stretches of the exposed coastline. Furthermore, an assessment of the other fishes captured in these beam trawl surveys indicated that algal beds also are nursery areas for many species of coastal marine fishes. Most species captured in these surveys were represented solely by juveniles (table 6-3). In central California, juveniles of seven species of surfperches (barred, spotfin (Hyperprosopon anale), black (Embiotoca jacksoni), shiner, white (Phanerodon furcatus), rainbow (Hypsurus caryi), and dwarf (Micrometrus minimus); Embiotocidae), four species of rockfishes (copper, Sebastes caurinus; brown, S. auriculatus; black, and grass, S. rastrelliger; Scorpaenidae), giant kelpfish (Heterostichus rostratus), English sole (Pleuronectes vetulus), and cabezon were also commonly encountered in drift algal beds. Southern California drift algal beds harbored the juveniles of six species of surfperches (barred and walleye surfperch, white and rainbow seaperch, and dwarf and black perch). These southern beds and surrounding areas, however, were numerically dominated by the juveniles of northern anchovy and two croakers (queenfish and white croaker) that are three of the most abundant species farther offshore

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(Allen and DeMartini, 1983). The drift algal beds off the beaches of central and southern California appear to be the primary habitat for a single species, the barred pipefish (Syngnathus exilis) (See chapter 4 and Allen and Herbinson, 1991). This species is rarely encountered anywhere outside this specialized habitat. No information on seasonality and other forms of temporal variability, spatial variation, or productivity of the fishes in the surf zone is available at this time. A great deal of information does exist, however, on the life histories and basic ecology of several species occupying this habitat primarily because they are important sport fishes. Information on growth rates, reproduction, movements, and food habits exists for barred surfperch (Carlisle et al., 1960), spotfin croaker, and California corbina (Joseph, 1962). The reproductive and growth dynamics of walleye surfperch from waters near San Diego were studied by DeMartini et al. (1983). The tide-related reproductive biology of California grunion has been well known for many years and was summarized by Walker (1952). Large, mobile fishes of the surf zone and shallow soft bottom, such as sharks and large croakers, have always presented major problems for quantitative assessment. Abundances of these species are routinely underestimated because they are adept at avoiding most types of sampling gear. These species can easily outswim and escape most seines and trawls. Passive samplers such as gill nets, trammel nets, and traps capture these fishes effectively but provide poor quantification. In recent years, gill nets have been used to assess populations of large, mobile fishes in the Gulf of Mexico (summarized in

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TA B L E 6-2

Fishes Collected at Two Sites in Trinidad Bay, California, April 1993 to March 1994

Common Name Surf smelt Shiner perch Topsmelt Night smelt Calico surfperch Speckled sanddab Striped seaperch Black rockfish Sand sole Slimy snailfish Spotfin surfperch Walleye surfperch Pricklebreast poacher Bay pipefish Cabezon Pacific herring Silver surfperch Silverspotted sculpin Pacific sardine Penpoint gunnel English sole California halibut Tubenose poacher Grass rockfish Pacific sand lance Pacific tomcod Jacksmelt Bonehead sculpin Threespine stickleback Pacific staghorn sculpin Chinook salmon Saddleback gunnel

Scientific Name

Number

Hypomesus pretiosus Cymatogaster aggregata Atherinops affinis Spirinchus starksi Amphistichus koelzi Citharichthys stigmaeus Embiotoca lateralis Sebastes melanops Psettichthys melanostictus Liparis mucosus Hyperprosopon anale Hyperprosopon argenteum Stellerina xyosterna Syngnathus leptorhynchus Scorpaenichthys marmoratus Clupea pallasi Hyperprosopon ellipticum Blepsias cirrhosus Sardinops sagax Apodichthys flavidus Pleuronectes vetulus Paralichthys californicus Pallasina barbata Sebastes rastrelliger Ammodytes hexapterus Microgadus proximus Atherinops californiensis Artedius notospilotus Gasterosteus aculeatus Leptocottus armatus Oncorhynchus tshawytscha Pholis ornata

3878 1511 771 458 321 96 63 61 48 46 40 35 30 27 25 24 19 11 10 9 7 6 5 4 3 3 2 1 1 1 1 1

51.6 20.1 10.3 6.1 4.3 1.3 0.8 0.8 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.3 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0 0 0 0 0 0 0 0

100 95 100 44.1 76.3 84.4 50.8 100 100 0 30 97.1 36.7 48.1 100 91.7 100 81.8 100 100 100 100 0 100 100 33.3 100 100 100 100 100 100

0 5 0 55.9 23.7 15.6 49.2 0 0 100 70 2.9 63.3 51.9 0 8.3 0 18.2 0 0 0 0 100 0 0 66.7 0 0 0 0 0 0

7518

100

92.4

7.6

TOTALS

%Total

%Juveniles

%Adults

NOTE : Number of individuals, percent of the total fish sampled, and percent juveniles and adults are given for each species. After Mulligan and Mulligan, in prep.

Hueter, 1994) and along the Pacific coast of Mexico (GodinezDominguez et al., 2000). A recent sampling survey for juvenile white seabass along the southern California coast has provided the first, long-term assessment of large, mobile fish species in California waters. This nighttime, gill-net survey has been conducted at 19 stations from throughout the Southern California Bight from April through October since 1996. The total catch of all species during the first two years (1996–97) was reported in Pondella and Allen (1999). Overall, the collections contained a “cross section” of fish species that frequent nearshore, soft-bottom areas, including bay and estuary, surf zone, coastal pelagic, and inner shelf habitats, as well as the rock/sand interfaces of rocky reefs and kelp beds. Characteristic assemblages were dominated numerically by various species of croakers including yellowfin croaker, white croaker, queenfish, black croaker (Cheilotrema saturnum), white seabass, and California corbina (fig. 6-4), probably as a result of their nocturnal activities (see chapter 20). On the other hand, several species of elasmobranchs heavily dominated the catch in biomass (Pondella and Allen, 1999).

The most numerous of the elasmobranchs were the horn shark (Heterodontus francisci), brown smoothhound (Mustelus henlei), gray smoothhound, leopard shark, swell shark (Cephaloscyllium ventriosum), angel shark (Squatina californicas), and bat ray (Myliobatis californica) (table 6-4). Further, the average weight of the individuals of these species ranged from 1.2 kg up to 6.2 kg making them easily the largest among the species encountered (table 6-5). Although these species are also often recorded in other nearshore habitats, they are usually listed as rare and periodic. This appears to reflect a sampling bias; clearly, elasmobranchs are much more abundant in the nearshore environment than previously recorded. Pondella and Allen (1999) concluded that the assemblage of large, mobile fishes in the nearshore area around the channel island of Santa Catalina differed from those of the mainland in diversity, abundance, richness, and biomass mainly because of habitat differences. The nearshore environment of the mainland is dominated by sand that separates the widely spaced rocky reefs. In contrast, the nearshore habitats at Santa Catalina Island are primarily reefs with relatively small expanses of sand.

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F I G U R E 6-3 Common fish species of the drift algal beds of the surf zone throughout the Southern California Bight (see text for explanation).

Coastal Pelagic Zone The coastal pelagic zone technically encompasses open water environment extending out from the surf zone to the continental shelf break. Many of the coastal pelagic species usually occur within a few kilometers of the shore. The fish assemblages of this zone are largely unstudied in California waters, except for the results reported by Cailliet et al. (1979) from Monterey Bay and by Allen and DeMartini (1983) off northern San Diego County between San Onofre and Oceanside. Cailliet et al. (1979) reported that commercial purse-seine hauls made at night in the surface waters of Monterey Bay contained 99.9% northern anchovies, which were the target species. In addition to anchovies, Pacific herring (Clupea pallasi) were captured in low abundance along with night smelt (Spirinchus starksi) and Pacific sauries (Cololabis saira). Largely benthic species, such as plainfin midshipman (Porichthys notatus) and Pacific electric ray (Torpedo californica), composed a surprisingly large portion of the remaining catch in these night hauls; this supports the hypothesis that they probably rise into the water column at night to feed. Allen and DeMartini (1983) summarized the results of a 19-month study involving 643 lampara net hauls partitioned among three depth blocks and day/night periods from 1979 to 1981. As in Monterey Bay, the hauls off San Onofre-Oceanside were overwhelmingly dominated by silvery, schooling fishes (fig. 6-5). Northern anchovy, queenfish, white croaker, Pacific pompano (Peprilus simillimus), and a species complex of silversides accounted for
98% of the individuals sampled

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(table 6-6). Northern anchovy, the dominant offshore pelagic species in California waters at the time of sampling (Mais 1974), was also numerically dominant nearshore. Queenfish and white croaker, the two most abundant croakers in this assemblage, are best characterized as demersal (bottom) fishes that rise into the water column at night. Both of these species are well represented in bottom trawls in the area (DeMartini and Allen, 1984). White croakers are generally more abundant in trawls, indicating that they are more closely associated with the bottom than queenfish. The silverside complex consisted of three species (jacksmelt, California grunion and topsmelt) that were not readily distinguishable in the field. Subsamples of the “atherinopsid spp.” taxon in field lampara catches contained about 48% jacksmelt, 42% grunion, and 10% topsmelt (Allen and DeMartini, 1983). Two groups of species were identified as seasonal components within the assemblage. Pacific bonito (Sarda chiliensis), Pacific mackerel (Scomber japonicus), and jack mackerel (Trachurus symmetricus) composed a group of pelagic carnivores that generally occurred in the offshore portion of the study area during the warmer months (spring-summer). On the other hand, four species (California barracuda, Sphyraena argentea; deepbody anchovy; salema, Xenistius californiensis; and yellowfin croaker) were more abundant at shallow depths during the colder water months (fall-winter). Two of these species, the deepbody anchovy and the yellowfin croaker, occur in bay-estuarine habitats such as Newport Bay during the summer months (Horn and Allen, 1981; Allen et al., 2002) and belong primarily to tropical families. The presence of

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TA B L E 6-3

Relative Abundance of Fishes Collected by Beam Trawl Sampling along the Coast of Central and Southern California from 1988 to 1993

Common Name

Scientific Name

Mean %

Central California Speckled sanddab English sole Barcheek pipefish Barred surfperch Bay goby Giant kelpfish Staghorn sculpin Spotfin surfperch Black perch California tonguefish Copper rockfish Cabezon Shiner perch Sand sole California lizardfish White seaperch Brown rockfish Spotted kelpfish Kelp clingfish Black rockfish California halibut Striped kelpfish Rainbow seaperch Dwarf perch Grass rockfish

Citharichthys stigmaeus Pleuronectes vetulus Syngnathus exilis Amphisticus argenteus Lepidogobius lepidus Heterostichus rostratus Leptocottus armatus Hyperprosopon anale Embiotoca jacksoni Symphurus atricauda Sebastes caurinus Scorpaenichthys marmoratus Cymatogaster aggregata Psettichthys melanostictus Synodus lucioceps Phanerodon furcatus Sebastes auriculatus Gibbonsia elegans Rimicola muscarum Sebastes melanops Paralichthys californicus Gibbonsia metzi Hypsurus caryi Micrometrus minimus Sebastes rastrelliger

66.7 9.3 4.1 2.2 2.1 1.5 1.3 1.3 1.0 0.9 0.8 0.7 0.5 0.5 0.5 0.4 0.4 0.3 0.3 0.3 0.2 0.2 0.2 0.2 0.2

Southern California Queenfish Speckled sanddab White croaker Northern anchovy Barcheek pipefish Giant kelpfish California halibut White seabass Fantail sole Spotted turbot Kelp pipefish California lizardfish Spotted kelpfish English sole Dwarf perch Walleye surfperch White seaperch California barracuda Staghorn sculpin Kelp bass Black croaker Cheekspot goby Barred surfperch

Seriphus politus Citharichthys stigmaeus Genyonemus lineatus Engraulis mordax Syngnathus exilis Heterostichus rostratus Paralichthys californicus Atractoscion nobilis Xystreurys liolepis Pleuronichthys ritteri Syngnathus californiensis Synodus lucioceps Gibbonsia elegans Pleuronectes vetulus Micrometrus minimus Hyperprosopon argenteum Phanerodon furcatus Sphyraena argentea Leptocottus armatus Paralabrax clathratus Cheilotrema saturnum Ilypnus gilberti Amphisticus argenteus

44.6 20.0 10.2 5.2 2.6 2.3 2.0 1.2 0.8 0.6 0.6 0.5 0.5 0.4 0.4 0.4 0.3 0.2 0.2 0.2 0.1 0.1 0.1

Black perch NOTE :

Embiotoca jacksoni

0.1


90% Juv.

* * * * * * * *

* *

*

* * * * * * * * * * *

* * * * * * * *

*

L. Allen, unpublished data.

these two species in the study area during fall and winter suggested that they seasonally migrate out of embayments and into shallow coastal waters in response to cooler water temperatures. Many demersal fishes were also captured because the nets extended from the surface to the bottom. Most of these benthic fishes were relatively rare in catches except for

the bat ray. Spatially, California barracuda, salema, jack mackerel, and atherinopsids were more abundant in the proximity of the San Onofre kelp bed during the study. All of these species associate with kelp beds or rocky reefs at some time during the year (Feder et al. 1974; Hobson and Chess 1976; Mais 1974).

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F I G U R E 6-4 Large mobile, nocturnally active fishes of the inner shelf in southern California (after Pondella and Allen, 1999).

The coastal pelagic fish assemblage off San OnofreOceanside varied greatly over time. Some of the notable differences were attributed to spatial patchiness and sampling error, but others undoubtedly reflected short-term, temporal changes in the environment. Upwelling was probably a major factor that contributed to short-term variation in the abundance and distribution of these fishes. The waters within the Southern California Bight are often subjected to bouts of upwelling anytime during the year, although upwelling is most likely from March to July (Parrish et al. 1981). Both short-term temperature variations due to upwelling and longterm seasonal warming and cooling of coastal waters probably exerted strong influences on the abundance of individual taxa in this assemblage. Abundances of only two of the top five taxa, however, were significantly correlated with sea surface temperature (northern anchovy were positively correlated, whereas atherinopsids were negatively correlated). Although the fourth most abundant species captured, Pacific pompano, varied significantly among samples, it showed no significant relationship to temperature. Extremely patchy distributions and high vagility might account for the observed short-term variation in the abundance of this species. Neither queenfish nor white croaker varied greatly in seasonal abundance, although queenfish did show significant variation that was apparently unrelated to temperature. The only major change in catches of queenfish and white croaker occurred during the fall and early winter, when adults of both species presumably migrated out of the sampling area into deeper water. Observed temporal differences in the abundances of the major higher

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carnivores of the assemblage (Pacific bonito, Pacific mackerel, and California barracuda) probably reflected differences in general long-shore migratory patterns and residence times of juveniles within the study area. Adults of these species were generally more abundant in the summer and fall, whereas juveniles could occur year-round (Allen and DeMartini, 1983). Although location differences and temporal changes were evident for some species within this Southern California assemblage, the dominant pattern was a general dispersal offshore at night from nearshore diurnal schools. Significant day/night interactions with depth were found for the total number of individuals, total individuals minus northern anchovy, species counts, numbers of northern anchovy, and numbers of queenfish (Allen and DeMartini, 1983). Further, adult queenfish of both sexes made diel, onshore, and offshore migrations, but juveniles did not (DeMartini et al. 1985). Both juvenile and adult queenfish occurred in demersal, resting schools in shallow water during the day. At night, adult queenfish dispersed up to 3.5 km offshore. A greater fraction of adult male queenfish migrated offshore at night than did mature females. The majority of immature fish stayed inshore of the 10-m depth contour. Various diel and/or depth effects were also found for other taxa, including Pacific pompano, white croaker, silversides, and Pacific mackerel. These results plus the significant correlations between species abundances and time of collection and depth underscored the general importance of diel and depth factors to the abundance and distributions of fishes in this assemblage (Allen and DeMartini, 1983).

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TA B L E 6-4

Large, Mobile Nearshore Soft-bottom Fishes Captured by Gill Net from 1996 to 1998 in Southern California Ranked by Number and Biomass

Common Name Yellowfin croaker * California hornshark Queenfish * Brown smoothhound White croaker California corbina * Bat ray Black croaker Walleye surfperch Kelp bass Opaleye Sargo Pacific sardine White seaperch Pacific mackerel White seabass Salema * Swell shark Spotted scorpionfish * Thornback Black perch Jacksmelt Rock wrasse * Gray smoothhound California halibut * Leopard shark Barred sand bass Halfmoon * Round stingray California barracuda Blacksmith Rubberlip seaperch * Angel shark * Spiny dogfish Pile perch Jack mackerel Garibaldi Specklefin midshipman California sheephead Kelp rockfish Zebraperch * Shovelnose guitarfish Kelp perch Spotted turbot American shad Staghorn sculpin Grass rockfish Pacific bonito

Pacific sanddab NOTE :

Scientific Name

% Number

Umbrina roncador Heterodontus francisi Seriphus politus Mustelus henlei Genyonemus lineatus Menticirrhus undulatus Myliobatis californica Cheilotrema saturnum Hyperprosopon argenteum Paralabrax clathratus Girella nigricans Anisotremus davidsoni Sardinops sagax Phanerodon furcatus Scomber japonicus Atractoscion nobilis Xenistius californiensis Cephaloscyllium ventriosum Scorpaena guttata Platyrhinoides triseriatus Embiotoca jacksoni Atherinopsis californiensis Halichoeres semicinctus Mustelus californicus Paralichthys californicus Triakis semifasciata Paralabrax nebulifer Medialuna californica Urolophus halleri Sphyraena argentea Chromis punctipinnis Rhacochilus toxotes Squatina californica Squalus acanthias Rhacochilus vacca Trachurus symmetricus Hypsypops rubicundus Porichthys myriaster Semicossyphus pulcher Sebastes atrovirens Hermosilla azurea Rhinobatis productus Brachyistius frenatus Pleuronichthys ritteri Alosa sapidissima Leptocottus armatus Sebastes rastrelliger Sarda chiliensis

9.7 8.9 6.1 5.3 5.0 4.9 3.8 3.7 3.6 3.5 3.3 2.9 2.8 2.6 2.5 2.5 2.1 2.1 2.0 1.9 1.8 1.6 1.6 1.4 1.3 1.3 1.1 1.1 0.9 0.8 0.7 0.7 0.7 0.6 0.6 0.6 0.6 0.5 0.4 0.4 0.3 0.3 0.3 0.3 0.2 0.2 0.2 0.1

Citharichthys sordidus

0.1

Common Name * * * * * * *

*

* *

*

California hornshark Brown smoothhound Bat ray Angel shark Swell shark Leopard shark Gray smoothhound California corbina Yellowfin croaker Opaleye Spiny dogfish Sargo White seabass Kelp bass Black croaker Pacific mackerel California halibut Thornback Shovelnose guitarfish Queenfish California barracuda White croaker Spotted scorpionfish Round stingray Halfmoon Black perch Jacksmelt Barred sand bass Rubberlip seaperch White seaperch Rock wrasse Pacific sardine Specklefin midshipman Pile perch Salema Zebraperch Walleye surfperch Garibaldi California sheephead Jack mackerel Kelp rockfish Blacksmith California moray Striped mullet American shad Pacific bonito Grass rockfish Spotted turbot

Scientific Name

% Biomass

Heterodontus francisi Mustelus henlei Myliobatis californica Squatina californica Cephaloscyllium ventriosum Triakis semifasciata Mustelus californicus Menticirrhus undulatus Umbrina roncador Girella nigricans Squalus acanthias Anisotremus davidsoni Atractoscion nobilis Paralabrax clathratus Cheilotrema saturnum Scomber japonicus Paralichthys californicus Platyrhinoides triseriatus Rhinobatis productus Seriphus politus Sphyraena argentea Genyonemus lineatus Scorpaena guttata Urolophus halleri Medialuna californica Embiotoca jacksoni Atherinopsis californiensis Paralabrax nebulifer Rhacochilus toxotes Phanerodon furcatus Halichoeres semicinctus Sardinops sagax Porichthys myriaster Rhacochilus vacca Xenistius californiensis Hermosilla azurea Hyperprosopon argenteum Hypsypops rubicundus Semicossyphus pulcher Trachurus symmetricus Sebastes atrovirens Chromis punctipinnis Gymnothorax mordax Mugil cephalus Alosa sapidissima Sarda chiliensis Sebastes rastrelliger Pleuronichthys ritteri

16.3 13.6 12.4 6.4 6.0 4.9 4.1 3.6 3.4 2.9 2.8 2.3 2.2 1.6 1.5 1.5 1.4 1.3 1.2 0.9 0.9 0.9 0.7 0.6 0.6 0.5 0.5 0.5 0.4 0.4 0.4 0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1

After Pondella and Allen, 2000.*  elasmobranchs.

Harbors Artificial harbors have been placed at the mouths of many of the natural bay and estuarine habitats within California in the last century. As of 1970, more than 60% of the original estuarine areas had either been highly modified into harbors or destroyed (Frey et al., 1970). Despite this, systematic studies of

these altered habitats are largely limited to those in the Southern California Bight. The ichthyofauna of several southern California harbors have been the subject of past studies including those in Newport Harbor (Allen, 1976), King Harbor, Redondo Beach (Stephens, 1978), Marina del Rey (Stephens et al., 1992), and especially the Los Angeles–Long Beach Harbor complex (Stephens et al., 1974; Horn and Allen,

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TA B L E 6-5

Large, Mobile Nearshore Soft-Bottom Fishes Captured by Gill Net from 1996 to 1998 in Southern California Ranked by Biomass Per Individual

Common Name * * * * * * * * *

* *

Number of Individuals

Scientific Name

Angel shark Spiny dogfish Leopard shark Shovelnose guitarfish California moray Bat ray Gray smoothhound Swell shark Brown smoothhound Striped mullet Horn shark California barracuda California halibut Zebraperch Opaleye White seabass Pacific bonito Sargo Fantail sole California corbina Round stingray Thornback Rubberlip seaperch California sheephead

Squatina californica Squalus acanthias Triakis semifasciata Rhinobatis productus Gymnothorax mordax Myliobatis californica Mustelus californicus Cephaloscyllium ventriosum Mustelus henlei Mugil cephalus Heterodontus francisi Sphyraena argentea Paralichthys californicus Hermosilla azurea Girella nigricans Atractoscion nobilis Sarda chiliensis Anisotremus davidsoni Xystreurys liolepis Menticirrhus undulatus Urolophus halleri Platyrhinoides triseriatus Rhacochilus toxotes Semicossyphus pulcher

Specklefin midshipman

Porichthys myriaster

128 119 245 62 5 754 271 416 1035 7 1744 155 248 63 641 492 15 576 5 954 169 372 139 88

104

Biomass (kg) 799 352 608 148 12 1555 507 756 1709 10 2045 110 171 38 361 273 8 291 3 455 73 161 55 34

39.6

Kg/ind 6.2 3.0 2.5 2.4 2.3 2.1 1.9 1.8 1.7 1.4 1.2 0.7 0.7 0.6 0.6 0.6 0.5 0.5 0.5 0.5 0.4 0.4 0.4 0.4

0.4

Note: After Pondella and Allen, 2000: *  elasmobranchs.

1981b; Allen et al., 1983; MBC, 1984; and MEC, 1988). These studies have found that harbor habitats generally contain relatively diverse and abundant fish assemblages compared to equivalent, undeveloped, nearshore habitats. The richness of these areas can probably be attributed to their protected nature, high nutrient loads from runoff and upwelling, presumed high productivity and abundant food supply, adequate circulation and, most importantly, variety of substrata (Stephens, 1978). Adequate circulation and good water quality are unquestionably important to the health of harbor fish populations. Poor water quality apparently contributed to the very “poor condition” of many fishes trawled (Young 1964) from Los Angeles–Long Beach Harbor before pollution abatement was begun in 1968 (Reish et al., 1980). The bottom fishes of harbors include most of the common species of the inner shelf as represented by the inclusion of harbors and nearshore soft bottom into one type of habitat by Allen (1985). Harbors, however, also include various rock substrates, most notably, the rocky shoreline, jetties, bulkheads, floats and pilings, and, in some cases, sandy beaches with sea grass or algal beds. Fish assemblages of the rocky shorelines and jetties of harbors were indistinguishable from those and other shallow rock reefs in southern California and were, therefore, classified as shallow rock reef fishes (SRRF) by Allen (1985). The Los Angeles–Long Beach Harbor complex is the most intensively studied harbor in California. This complex now sits on what was once the site of the largest bay and estuarine system between San Francisco Bay and San Diego Bay

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(fig. 6-6). Most of the studies of the fish populations have been unpublished surveys and environmental impact analyses. Comprehensive studies of both Long Beach Harbor (MBC, 1984) and Los Angeles Harbor (MEC, 1988) have been completed; however, most of the information remains unpublished except for Allen et al. (1983). The fish assemblages of Los Angeles-Long Beach Harbor are diverse. Chamberlain (1974) listed 132 species of fish that had been reported from Los Angeles–Long Beach Harbor. Horn and Allen (1981b) reported that 113 species had been collected in the harbor in studies conducted between 1971 and 1979. Otter trawl and gill-net collections (table 6-7) of the fish populations of harbors in the Bight in general and of Los Angeles–Long Beach Harbor in particular are numerically dominated by two species of croaker, white croaker and queenfish and juveniles of northern anchovy. Other common species included white seaperch, California tonguefish (Symphurus atricauda), speckled sanddab (Citharichthys stigmaeus), shiner perch, specklefin midshipman (Porichthys myriaster), black perch, walleye surfperch, and bay goby (Lepidogobius lepidus) (Horn and Allen, 1981b). More recently, as suggested by Horn and Allen (1981b), investigations have also used beach seines and purse seines (table 6-7) in addition to otter trawls (MBC, 1984) and gill nets (MEC, 1988) to characterize the harbor fish fauna more thoroughly. Beach seine catches along sandy beaches within the harbor have reported shoreline fish assemblages that are distinctive within the harbor, yet very similar in many respects to those

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F I G U R E 6-5 Common fish species of the coastal pelagic zone in southern California (After Allen and DeMartini, 1983).

from bay and estuarine and exposed coast surf zone habitats. Numerically abundant species taken in beach seines include topsmelt, arrow goby (Clevelania ios), cheekspot goby (Ilypnus gilberti), northern anchovy, queenfish, white croaker, and grunion (Allen et al., 1983; MBC, 1984). The Cabrillo Beach area of the harbor contained a unique group of fishes, which were associated with algal beds (Gracillaria sp.) along the sandy shoreline. This group included dwarf perch, spotted kelpfish (Gibbonsia elegans), giant kelpfish, and barcheek pipefish (Allen et al., 1983). Purse-seine hauls (MBC, 1984) captured mainly fishes from the water column within the harbor. The ten most abundant species captured in Los Angeles– Long Beach Harbor in order of abundance were northern anchovy (45%), queenfish (19%), Pacific sardine (Sardinops sagax) (12%), white croaker (4%), Pacific pompano (2%), jack mackerel (1%), California barracuda (1%), jacksmelt (0.5%), grunion (0.4%), and Pacific mackerel (0.2%). This list and the relative abundances of fishes from Long Beach Harbor was virtually indistinguishable from that reported by Allen and DeMartini (1983) from the coastal pelagic zone off San Onofre-Oceanside, California. The similarities among the fishes of harbors and the surf zone, inner shelf, coastal pelagic, and bay/estuarine habitats noted above are largely responsible for the close association among these four types of habitats reported in Allen (1985) and Allen and Pondella, (chapter 4, this volume). The species abundances reported in four studies from various parts of the

Los Angeles–Long Beach Harbor complex occur across three major nearshore habitats (fig. 6-7). The fishes reported from trawls by Stephens et al. (1974) were those common on the inner shelf of southern California. The relative abundances of species reported in both Allen et al. (1983) and MEC, 1988 were more closely allied to those of the coastal pelagic zone off southern California, due largely to the high abundance of northern anchovies in seine hauls in these studies. Finally, the fish assemblages from the Los Angeles Federal Breakwater (table 6-8) are indistinguishable from those of natural rocky reef habitats within Southern California. They are dominated numerically by blacksmith (Chromis punctipinnis), black perch (Embiotoca jacksoni), pile perch (Rhacochilus vacca), kelp bass (Paralabrax clathratus), and senorita (Oxyjulis californica) (Froeschke et al., in press). Therefore, the fish assemblage within the Los Angeles–Long Beach Harbor complex is a composite of those from various nearshore habitats (fig. 6-8). This harbor sits at the mouth of the Los Angeles and San Gabriel Rivers. The interior of this facility was created in part by the filling of an expansive wetland that historically met the Ballona Wetlands to the north. Bay and estuarine fishes are distributed along the interior portions of the harbor in what is the remnant of the estuary habitat. A few areas in the harbor support marcrophytes (algae and eelgrass) and associated fishes. Rocky groins, breakwaters, and jetties that have been used to construct most of the harbor bracket this habitat and include a diverse assemblage of reef

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TA B L E 6-6

Frequency of Occurrence of the Top 23 Fishes in 643 Lampara Net Samples from September 1979 to March 1981

Scientific Name

Number

% Number

Frequency

% Frequency

Northern anchovy Queenfish White croaker Pacific pompano Atherinopsidae Pacific mackerel Jack mackerel Deepbody anchovy Pacific bonito California barracuda Walleye surfperch White seaperch Bat ray California corbina Yellowfin croaker Barred surfperch Salema California halibut Pacific sardine Barred sand bass Shiner perch Spiny dogfish

Engraulis mordax Seriphus politus Genyonemus lineatus Scomber japonicus silversides Scomber japonicus Trachurus symmetricus Anchoa compressa Sarda chiliensis Sphyraena argentea Hyperprosopon argenteum Atractoscion nobilis Myliobatis californica Menticirrhus undulatus Umbrina roncador Amphisticus argenteus Xenistius californiensis Paralichthys californicus Sardinops sagax Paralabrax nebulifer Cymatogaster aggregata Squalus acanthias

819,872 80,513 53,994 26,003 16,811 7,386 2,750 1,915 1,394 1,066 936 665 455 412 269 211 182 139 130 108 86 66

80.79 7.93 5.32 2.56 1.56 0.73 0.27 0.19 0.14 0.11 0.09 0.07 0.04 0.04 0.03 0.02 0.02 0.01 0.01 0.01 0.01 0.01

440 413 335 238 326 194 92 85 115 99 106 101 212 117 38 51 25 79 15 56 34 23

68.4 64.2 52.1 37.0 50.7 30.2 14.3 13.2 17.9 15.4 16.5 15.7 33.0 18.2 5.9 7.9 39.0 12.3 23.0 8.7 5.3 3.6

Spotted scorpionfish

Scorpaena guttata

57

0.01

28

4.3

Common Name

NOTE :

Species (and one family) are ranked by total number of individuals. After Allen and DeMartini, 1983.

F I G U R E 6-6 Reproduction of an 1895 chart of San Pedro Bay, California. The superimposed outline

traces the current 2005 shoreline and associated structures of the present Los Angeles–Long Beach Harbor complex.

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TA B L E 6-7

Relative Abundance of Fishes in Four Sampling Gears in the Los Angeles–Long Beach Harbor Complex

Common Name

Scientific Name

Northern anchovy White croaker Queenfish Topsmelt White seaperch Arrow goby Pacific sardine Shiner perch Walleye surfperch Cheekspot goby California tonguefish Jacksmelt Pacific pompano Black perch Speckled sanddab Bay goby California grunion California halibut Threadfin shad Pile perch California barracuda Jack mackerel California corbina

Engraulis mordax Genyonemus lineatus Seriphus politus Atherinops affinis Phanerodon furcatus Clevelandia ios Sardinops sagax Cymatogaster aggregata Hyperprosopon argenteum Ilypnus gilberti Symphurus atricauda Atherinopsis californiensis Peprilus simillimus Embiotoca jacksoni Citharichthys stigmaeus Lepidogobius lepidus Leuresthes tenuis Paralichthys californicus Dorosoma petenense Rhacochilus vacca Sphyraena argentea Trachurus symmetricus Menticirrhus undulatus

Dwarf perch

Micrometrus minimus

NOTE :

Otter Trawl

Gill Net

Purse Seine

Beach Seine

15 41 9

45 4 19 1

8

7 25 13 1 16

24 1 4 41 1 14

1 7 5

12

3 1

4 3 4

1 2

1 1 7

7 1

1

5 3 1 1

1 2 1 1 1

1

1 2 1 2

1 1

1

Percentage of total. After Horn and Allen, 1981b; Allen et al.; 1983; and Marine Biological Consultants, 1984.

F I G U R E 6-7 Specific placement of four site samples from within the Los Angeles–Long Beach Harbor complex based on

species composition among 41 nearshore fish assemblage studies from the Southern California Bight. Five studies from the pelagic realm were also included for comparison (to “root” the tree). The species composition reported in Stephens et al. (1974) is grouped with inner shelf samples. The assemblages reported in Allen et al. (1983) and MEC (1988) were closely associated with coastal pelagic and surf zone samples. Fishes reported from the Los Angeles Federal Breakwater (Froeschke et al., in press) were indistinguishable from samples from other kelp bed and rocky reef habitats.

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TA B L E 6-8

Relative Abundance of Conspicuous Fishes in Dive Surveys of the Los Angeles Federal Breakwater from October 2002 to November 2003 (after Froeschke and Allen, in Press)

Scientific Name

Percent Abundance

Blacksmith Black perch Pile perch Kelp bass Senorita Kelp perch Zebraperch California sheephead Painted greenling Opaleye Barred sand bass Garibaldi Halfmoon Olive rockfish Rock wrasse Rubberlip seaperch Kelp rockfish Blackeye goby Rainbow seaperch Giant kelpfish Sargo Island kelpfish White seaperch Spotted scorpionfish Cabezon Black-and-yellow rockfish California hornshark

Chromis punctipinis Embiotoca jacksoni Rhacochilus vacca Paralabrax clathratus Oxyjulis californica Brachyistius frenatus Hermosilla azurea Semicossyphus pulcher Oxylebius pictus Girella nigricans Paralabrax nebulifer Hypsopops rubicundus Medialuna californiensis Sebastes serranoides Halichoeres semicinctus Rhacochilus toxotes Sebastes atrovirens Rhinogobiops nicholsi Hypsurus caryi Heterostichus rostratus Anisotremus davidsoni Alloclinus holderi Phanerodon furcatus Scorpaena guttata Scorpaenichthys marmoratus Sebastes chrysomelas Heterodontus francisci

56.60% 11.95% 5.51% 3.48% 3.26% 3.05% 2.44% 1.59% 1.55% 1.46% 1.46% 1.17% 1.08% 0.93% 0.87% 0.83% 0.81% 0.53% 0.49% 0.38% 0.15% 0.13% 0.11% 0.04% 0.04% 0.04% 0.02%

Tree rockfish

Sebastes serriceps

Common Name

fishes. There is also one long stretch of sandy beach and associated fishes along the Long Beach portion of the harbor. This heterogeneous collection of habitats has been artificially placed within the inner shelf and coastal pelagic (CP) zones creating a very dynamic ecosystem. Harbor fish populations, like those of other nearshore habitats, are markedly seasonal (Stephens et al., 1974; Allen et al., 1983). The greatest number of species, individuals, and biomass usually occur in the summer and early fall (fig. 6-9). This pattern is mainly the result of (1) the high abundance of juvenile resident fishes, including northern anchovy, white croaker, queenfish, and various species of surfperches in the inshore areas during the summer months; and (2) the presence of warm-water, seasonal species, such as Pacific bonito, California barracuda, gray smoothhound, and leopard shark (Allen et al., 1983). The seasonal patterns in abundance and biomass at Cabrillo Beach differ chronologically from those observed in Upper Newport Bay (Horn and Allen, 1981a; Allen, 1982). Peak abundance in Newport Bay occurred in the spring and early summer followed by biomass peaking in mid summer and early fall (fig. 6-8). The abundance and biomass peaks of the harbor fishes were delayed compared to those in Newport Bay of southern California and were greatest in midsummer and fall, respectively. Diel variability in the Cabrillo Beach fish assemblages was also evident when day and night catches were compared (Allen et al., 1983). The great majority (88%) of fishes were collected

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0.02%

during the day, whereas a slightly greater proportion (56%) of the biomass was captured at night. The predominance of young-of-the-year northern anchovy in daytime beach seine hauls and the large nighttime catches of white croakers in both otter trawls and gill nets contributed greatly to these diel differences. Four of the five most abundant species, northern anchovy, queenfish, California grunion, and white seaperch, which comprised 85% of the total number of individuals, were caught in greater numbers during the day. Only white croakers were more numerous at night. All five species, however, had greater mean weights in nighttime collections. In most cases, no significant differences in number of species, number of individuals, or biomass were detected between day and night samples taken with the three types of gear. The two exceptions were that nighttime otter trawl samples captured significantly greater numbers of individuals and biomass than day samples. Despite the apparent lack of statistical differences, individual species varied greatly in their day versus night occurrences in samples. Variability was probably the result of diel activity patterns, patchy distributions, and visually mediated gear avoidance. Behavior patterns undoubtedly contribute to differences in day-night catches. Juvenile northern anchovy formed dense schools nearshore during the day where they were susceptible to capture by beach seines. At night, these schools dispersed from the shoreline and were no longer accessible to beach seines. White croakers appeared to be more active and more widely dispersed at night, presumably in search of food.

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F I G U R E 6-8 A representation of the distributions of

the diverse fish assemblages of the Los Angeles–Long Beach Harbor complex. The relatively high diversity in harbors results from of the combination of multiple habitats suited for nearshore soft-bottom, coastal pelagic, kelp bed and rocky reef, surf zone, bay-estuary, and macrophyte associated species.

Similar activity patterns have been reported for these species in the nearshore coastal waters (Allen and DeMartini, 1983). The increased numbers of other nocturnally active species such as basketweave cusk-eel (Ophidion scrippsae) and spotted cusk-eel (Chilara taylori), specklefin midshipman, and California tonguefish in the night catches also made an important contribution to the day-night differences (Greenfield, 1968; DeMartini and Allen, 1984). The high abundance of low trophic level fishes (e.g., northern anchovy, queenfish, and juvenile white croaker) in the Los Angeles–Long Beach Harbor complex results in a relatively high standing stock and production potential. Total annual productivity of trawl-captured species in Long Beach Harbor from March 1983 to April 1984 was estimated at 1.7 to 1.9 g DW/m2 based on a realistic capture efficiency of 10% (MBC, 1984). These values were substantially less than the earlier production estimate of 4.0 g DW/m2 by Stephens et al. (1974). The causes of this relatively large discrepancy are not clear. Nevertheless, these estimates are approximately one-fourth to one-half of that (9.4 g DW/m2) estimated for the littoral fishes of Upper Newport Bay (Allen, 1982). Overall, the annual production estimates for Long Beach Harbor are low compared to those of various marine and estuarine studies summarized by Allen (1982). However, the harbor productivity estimate was

for trawl-captured fishes only and excludes a major component of the harbor ichthyofauna, the water column fishes. The inclusion of this important component would undoubtedly increase production estimates substantially. Given this caveat, the assertion that harbors are productive fish habitats in southern California is still reasonable. In summary, southern California harbors, particularly the Los Angeles–Long Beach Harbor complex, are productive and heterogeneous environments that can support abundant, diverse fish assemblages if good water quality is maintained. Harbors combine the attributes of extensive, nearshore softbottom habitat with those of coastal pelagic, sandy and rocky shores, and shallow rock reefs. Not surprisingly, California harbors represent composite habitats with fish assemblages sharing close affinities to those of bay and estuarine, exposed coast surf zone, inner shelf, and coastal pelagic habitats. In addition, hard substrates provided by harbor development add a variety of reef species to the mix. Last, note that most of what we know about the fish assemblages of harbor environments is restricted to southern California sites. Quantitative studies of harbors and marinas in northern and central California are virtually nonexistent in the literature and would be excellent subjects for future investigations and publications.

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habitats discussed in this chapter. Such studies yield an understanding of interannual variability and the effects of pulsed disturbances such as flooding or ENSO events on these assemblages. 3. Estimate production for fish populations in a variety of nearshore systems, particularly in harbors. Such information is critical to our understanding of ecosystem function and is also important in the estimation of “habitat value” for mitigating of habitat loss from human activities. 4. Determine the sources of nutrient enrichment (e.g., runoff, upwelling, pollution) in harbor environments and their impacts on harbor fish assemblages in California.

Literature Cited

F I G U R E 6-9 Seasonal trends in species richness, abundance, biomass

of fishes at Cabrillo Beach, Los Angeles Harbor and Upper Newport Bay (after Allen et al., 1983 and Horn and Allen, 1981).

Recommendations for Future Studies As with most other California marine fish habitats, many studies are needed if we are to deepen our understanding of the structure and function of nearshore fish assemblages in California and Baja California. Future investigations worthy of attention include, but are certainly not limited to the following: 1. Conduct comprehensive surveys in the surf zone and adjacent drift algal beds, coastal pelagic zone and harbors in selected areas representing central, southern, and Baja California to establish baseline information on their fish assemblages using an array of the most effective types of sampling gear. We believe that it is particularly critical that new surveys of surf zones in Southern California are undertaken to update that reported, incompletely, decades ago in Carlisle et al. (1960). 2. Initiate long-term surveys (of 5 or more years) for juvenile-adult assemblages in all of the nearshore

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Allen, L.G. 1976. Abundance, diversity, seasonality and community structure of the fish populations in Newport Bay, California. M.A. Thesis. California State University, Fullerton. . 1985. A habitat analysis of the near- shore marine fishes from southern California. Bull. South Calif. Acad. Sci. 84:133–155. . 1988. Recruitment, distribution, and feeding habits of youngof-the-year California halibut (Paralichthys califomicus) in the vicinity of Alamitos Bay-Long Beach Harbor, California, 1983–1985. Bull. South Calif. Acad. Sci. 87:19–30. Allen, L.G., and E. E. DeMartini. 1983. Temporal and spatial patterns of nearshore distribution and abundance of the pelagic fishes off San Onofre, Oceanside, California. U.S. Fish. Bull. 81(3):569–586. Allen, L.G., and M.P. Franklin. 1988. Distribution and abundance of young-of-the-year white seabass, Atractoscion nobilis, in the vicinity of Long Beach Harbor, California, in 1984–1987. Calif. Fish Game 74:245–248. . 1992. Abundance, distribution, and settlement of young-ofthe-year white seabass, Atractoscion nobilis, in the Southern California Bight, 1988–1989. U.S. Fish. Bull. 90:633–641. Allen, L.G., A. M. Findlay, and C. M. Phalen. 2002. The fish assemblages of San Diego Bay in the five-year period of July 1994 to April 1999. Bull. South Calif. Acad. Sci. 101(2):49–85. Allen, L.G., M.H. Horn, F. A. Edmands II, and C.A. Usui. 1983. Structure and seasonal dynamics of the fish assemblage in the Cabrillo Beach area of Los Angeles Harbor, California Bull. South Calif. Acad. Sci. 82:47–70. Allen, L.G., R.N. Jensen, and J. Sears. 1990. Open coast settlement and distribution of young-of-the-year California halibut (Paralichthys californicus) along the southern California shoreline between Pt. Conception and San Mateo Pt., June–October, 1988. In The California halibut, Paralichthys californicus, resource and fisheries. Calif. Dept. Fish Game Fish. Bull.174, pp.145–152. Allen, M. J. 1982. Functional structure of soft-bottom fish communities of the southern California shelf. Ph.D. Dissertation. University of California, San Diego. . 1990. The biological environment of the California halibut (Paralichthys californicus). In Haugen, C.W. (ed). The California halibut, Paralichthys californicus, resource and fisheries. Calif. Fish Game Fish Bull. 174:7–29. Allen, M. J., and K.T. Herbinson. 1991. Beam-trawl survey of bay and nearshore fishes of the soft-bottom habitat of southern California in 1989. Calif. Coop. Oceanic Fish. Invest. Rep. 32:112–127. . 1990. Settlement of juvenile California halibut, Paralichthys californicus, along the coasts of Los Angeles, Orange, and San Diego counties in 1989. Calif. Coop. Ocenaic Fish. Invest. Rep. 31:84–96. Beyst, B.,A. Cattrijsse, and J. Mees. 1999. Feeding ecology of juvenile flatfishes of the surf zone of a sandy beach. J. Fish Biol. 55:1171–1186. Buckel, J.A., M.J. Fogarty, and D.A. Conover. 1999. Foraging habits of bluefish, Pomatomus saltatrix, on the U.S. east coast continental shelf. U.S. Fish. Bull. 97:758–775. Cailliet, G. M., K. A. Karpov, and D. A. Ambrose. 1979. Pelagic assemblages as determined from purse seine and large midwater trawl catches in Monterey Bay and their affinities with the market

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squid, Loligo opalescens. Calif. Coop. Oceanic Fish. Invest. Rep. 24:57–69. Carlisle, J.G., Jr., J.W. Schott, and N.J. Abramson. 1960. The barred surfperch (Amphisticus argenteus Agassiz) in southern California. California Dept. Fish Game, Fish Bulletin No. 109. Carmichael, J.T., S.L. Haeseker, and J.E. Hightower. 1998. Spawning migration of telemetered striped bass in the Roanoke River, North Carolina. Trans. Am. Fish. Soc. 127:286–297. Cech, J. J., Jr., and D.E. Wohlschlag. 1982. Seasonal patterns of respiration, gill ventilation, and hematological characteristics in the striped mullet, Mugil cephalus L. Bull. Mar. Sci. 32:130–138. Chamberlain, D.W. 1974. A checklist of fishes from Los Angeles-Long Beach Harbors. In D. Soule, and M. Oguri (eds.), Marine studies of San Pedro Bay. Part III: Environmental field investigations. Allan Hancock Found. Publ. USC-SG-1-74, pp. 43–78. Chubb, C.F., I.C. Potter, C. J. Grant, R.C. J. Lenanton, and J. Wallace. 1981 Age structure, growth rates and movements of sea mullet, Mugil cephalus L. and yellow-eye mullet, Aldrichetta forsteri (Valenciennes), in the Swan-Avon River System, Western Australia. Aust. J. Mar. Freshwater Res. 32(4):605–628. Clark, B.M. 1997. Variation in surf-zone fish community structure across a wave-exposure gradient. Estuar. Coast. Shelf Sci. 44: 659–674. Cordes, J.F., and L.G. Allen. 1997. Estimates of age, growth, and settlement from ototliths of young-of-the-year kelp bass (Paralabrax clathratus). Bull. South Calif. Acad. Sci. 96(2):43–60. DeMartini, E.E., and L.G. Allen. 1984. Diel variation in catch parameters for fishes sampled by a 7.6-m otter trawl in southern California coastal waters. Calif. Coop. Oceanic Fish. Invest. Rep. 25:119–134. DeMartini, E.E., L.G. Allen, R.K. Fountain, and D. Roberts. 1985. Diel and depth variations in the sex-specific abundance, size composition, and food habits of queenfish, Seriphus politus (Sciaenidae). U.S. Fish. Bull. 83:171–185. DeMartini, E.E., T.O. Moore, and K.M. Plummer. 1983. Reproductive and growth dynamics of Hyperprosopon argenteum (Embiotocidae) near San Diego, California. Environ Biol. Fishes 8:29–38. Ditty, J.G.,M. Bourgeois, R. Kasprzak, and M. Konikoff. 1991. Life history and ecology of sand seatrout (Cynoscion arenarius Ginsburg) in the northern Gulf of Mexico: A review. Northeast Gulf Sci. 12:35–47. Eschmeyer, W.N., E.S. Herald, and H. Hammann. 1983. A field guide to Pacific coast fishes of North America. Houghton Mifflin Company, Boston. Froeschke, J.T., L.G. Allen, and D.J. Pondella II. In press. The reef fish assemblage of the outer Los Angeles Federal Breakwater. Bull. South Cal. Acad. Sci. Feder, H.M., C.H. Turner, and C. Limbaugh. 1974. Observations on fishes associated with kelp beds in southern California. California Dep. Fishery Game Fishery Bulletin 160. Funicelli, N.A., D.A. Meineke, H.E. Bryant, M.R. Dewey, G.M. Ludwig, and L.S. Mengel. 1989. Movements of striped mullet, Mugil cephalus, tagged in Everglades National Park, Florida. Bull. Mar. Sci. 44:171–178. Godinez-Dominguez, E., J. Rojo-Vazquez, V. Galvan-Pina, and B. Aguilar-Palomino. 2000. Changes in the structure of a coastal fish assemblage exploited by a small scale gillnet fishery during an El Nino-La Nina event. Estuar. Coast. Shelf Sci. 51(2):773–787. Greenfield, D.W. 1968. Observations on the behavior of the basketweave cusk-eel, Otophidium scrippsi Hubbs. Calif. Fish Game 54:108–114. Haeseker, S.L., and J. J. Cech, Jr. 1993. Food habits of the brown smoothhound shark (Mustelus henlei) from two sites in Tomales Bay. Calif. Fish Game 79:89–95. Harris, S.A., and D.P. Cyrus. 1996. Larval and juvenile fishes in the surf zone adjacent to the St. Lucia Estuary mouth, KwaZulu-Natal, South Africa. Mar. Freshwater Res. 47:465–482. Hart, J.L., and J.L. McHugh. 1944. The smelts (Osmeridae) of British Columbia. J. Fish. Res. Board Can. Bull. 64. Hobson, E.S., and J.R. Chess. 1976. Trophic interactions among fishes and zooplankters near shore at Santa Catalina Island, California. U.S. Fish. Bull. 71:777–786. Horn, M.H., and L.G. Allen. 1981b. A review and synthesis of ichthyofaunal studies in the vicinity of Los Angeles and Long Beach Harbors, Los Angeles County, California. Final Rep. to U.S. Fish Wildl. Serv., Ecological. Serv., Laguna Niguel, CA. . 1981a. Ecology of fishes in upper Newport Bay, California: seasonal dynamics and community structure. California. Dep. Fish and Game, Mar. Res. Tech. Rep. 45.

Hueter, R.E. 1994. Early life history and relative abundance of blacktip and other coastal sharks in eastern Gulf of Mexico nursery areas, including bycatch mortality of sharks and associated fishes. MARFIN NA57FF0034-01. Mote Marine Lab, Sarasota, FL. Joseph, D.C. 1962. Growth characteristics of two southern California surf fishes, the California corbina and spotfin croaker, family Sciaenidae. California. Dep. Fish Game Fishery Bulletin 119. Kramer, S.H. 1990. Distribution and abundance of juvenile California halibut, Paralichthys californicus, in shallow waters of San Diego County. Calif. Dept. Fish Game Fishery Bulletin 174:99–126. . 1991. Growth, mortality, and movements of juvenile California halibut, Paralichthys californicus, in shallow coastal and bay habitats of San Diego County, California. U.S. Fish. Bull. 89(2):195–207. Lasiak, T. A. 1986. Juveniles, food and the surf zone habitat: Implications for teleost nursery areas. South Afr. J. Sci. 21:51–56. Lenanton, R.C.J., A.I. Robertson, and J.A. Hansen. 1982. Nearshore accumulations of detached macrophytes as nursery areas for fish. Mar. Ecol. Prog. Ser. 9:51–57. Love, M.L. 1996. Propbably more than you want to know about the fishes of the Pacific coast. Really Big Press, Santa Barbara, CA. Mais, K. F. 1974. Pelagic fish surveys in the California Current. California. Dep. Fish Game Fishery Bulletin 162. Marine Biological Consultants (MBC). 1984. Outer Long Beach HarborQueensway Bay biological baseline survey. Prepared for the Port of Long Beach, Division of Port Planning. Marine Ecological Consultants (MEC). 1988. Biological baseline study of outer Los Angeles Harbor. Biological baseline survey prepares for the Port of Los Angeles, Division of Port Planning. McFarland, W.N. 1963. Seasonal change in the number and the biomass of fishes from the surf at Mustang Island, Texas. Publ. Inst. Mar. Sci. Univ. of TX. 9:91–105. Mercer, L.P. 1984. A biological and fisheries profile of red drum, Sciaenops ocellatus. U.S. Fish and Wildlife Service, Biological Report 41. Modde, T.C. 1980. Growth and residency of juvenile fishes within a surf zone habitat in the Gulf of Mexico. Gulf Res. Rep. 6:377–385. Modde, T.C., and S.T. Ross. 1981. Seasonality of fishes occupying a surf zone habitat in the northern Gulf of Mexico. U.S. Fish. Bull. 78:911–922. Moflett, A. 1961. Movements and growth of spotted sea trout, Cynoscion nebulosus, Cuvier, in West Florida. Fla. St. Bd. Conserv. Tech. Ser. (36):1–35. Moyle, P.B., and J.J. Cech. 2000. Fishes: an introduction to ichthyology. 4th ed. Prentice-Hall, Upper Saddle River, NJ. Mulligan T.J., and H.L. Mulligan. In prep. Fishes associated with drift macroalgae: exposed surf zones of northern California. Naughton, S.P., and C.H. Saloman. 1978. Fishes of the nearshore zone of St. Andrews Bay, Florida, and adjacent coast. Northeast Gulf Sci. 2:43–55. Parrish, R.H., C.S. Nelson, and A. Bakun. 1981. Transport mechanisms and reproductive success of fishes in the California Current. Biol. Oceanogr. 1:175–203. Pondella, D. J. II, and L.G. Allen. 1999. The nearshore fish assemblage of Santa Catalina Island. Proc. 5th Calif. Islands Symp. Mineral Management Service and Santa Barbara Museum of Natural History, pp. 394–400. Reish, D.J., D.F. Soule, and J.D. Soule. 1980. The benthic biological conditions of Los Angeles-Long Beach harbors: results of 28 years of investigations and monitoring. Helgolander Meers-unter. 34:193–205. Robertson, A.I., and R. C.J. Lenanton. 1984. Fish community structure and food chain dynamics in the surf-zone of sandy beaches: The role of detached macrophyte detritus. J. Exp. Mar. Biol. Ecol. 84:265–283. Romer, G.S. 1990. Surf zone fish community and species response to a wave energy gradient. J. Fish Biol. 36:279–287. Ross, S.T., R.H. McMichael, Jr., and D.L. Ruple. 1987. Seasonal and diel variation in the standing crop of fishes and macroinvertebrates from a Gulf of Mexico surf zone. Estuar. Coast. Shelf Sci. 25:391–412. Ruple, D. 1984. Occurrence of larval fishes in the surf zone of a northern Gulf of Mexico barrier island. Estuar. Coast. Shelf Sci. 18:191–208. Russo, R.A. 1975. Observations on the food habits of leopard sharks (Triakis semifasciata) and brown smoothhounds (Mustelus henlei). Calif. Fish Game 61:95–103. Saloman, C.H., and S.P. Naughton. 1984. Food of the crevalle jack, Caranx hippos, from Florida, Louisiana, and Texas. NOAA Tech. Memo. NMFS-SEFSC-134.

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Santos, R.S., and R.D.M. Nash. 1995. Seasonal changes in a sandy beach fish assemblage at Port Pim, Faial, Azores. Estuar. Coast. Shelf Sci. 41:579–591. Schaefer, M.B. 1936. Contribution of the life history of the surf smelt, Hypomesus pretiosus, in Puget Sound, WA. Dep. Fish. Biol. Rep. 35B:1–45. Senta, T., and I. Kinoshita. 1985. Larval and juvenile fishes occurring in surf zones of western Japan. Trans. Am. Fish. Soc. 114:609–618. Setler, E.M., W.R. Boynton, K.V. Wood, H.H. Zion, L. Lubbers, N.K., Mountford, P. Frere, L. Tucker, and J. A. Mihursky. 1980. Synopsis of biological data on striped bass, Morone saxatilis (Walbaum). NOAA Tech. Rep. NMFS Circ. 433, FAO Synopsis No. 121. Stephens, J.S., Jr. 1978. Breakwaters and harbors as productive habitats for fish populations: Why are fishes attracted to urban complexes? In M.D. Dailey, S.N Murray, and E. Segal, (eds.), Proc. 1st South. Calif. Ocean Stud. Consortium Symp. The Urban Harbor Environment. Tech. Pap. No.1. South. Calif. Ocean Studies Consortium, California State University, Long Beach, CA. 49–60. Stephens, J. S., Jr., C. Terry, S. Subber, and M. J. Allen. 1974. Abundance, distribution, seasonality and productivity of the fish populations in Los Angeles Harbor, 1972–73. In D. Soule, and M. Oguri, (eds.), Marine studies of San Pedro Bay. Part IV. Environmental field investigations. No. USC-SG-72. Allan Hancock Foundation, University of Southern California, Los Angeles, CA, pp. 1–42. Stephens, J.S., Jr., D. J. Pondella II, P. A. Morris, and D. Soule. 1992. Marina del Rey as a fish habitat: studies of the fish fauna since 1977. In P. M. Grifman and S. E. Yoder (eds.), Perspectives on the marine environment. Proc. Symp. Mar. Environ. South. Calif. May 10, 1991, Sea Grant, pp. 28–48.

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Suda, Y., T. Inoue, and H. Uchida. 2002. Fish communities in the surf zone of a protected sandy beach at Doigahama, Yamaguchi Prefecture, Japan. Estuar. Coast. Shelf Sci. 55:81–96. Talent, L.G. 1982. Food habits of the gray smoothhound, Mustelus californicus, the brown-smoothhound, Mustelus henlei, the shovelnose guitarfish, Rhinobatos productus, and the bat ray, Myliobatus californica, in Elkhorn Slough, California. Calif. Fish Game 68:224–234. Tetra Tech, Inc. 1977. MRC Fish Program: Final Report, Appendices, December 1977. Report submitted to the Marine Review Committee of the California Coastal Commission. Thomas, J.C. 1968. Management of the white seabass (Cynoscion nobilis) in California waters. Calif. Fish Game Fish. Bull. 142. Thompson, R., and J. C. Munro. 1974. The biology, ecology and exploitation and management of the Carribean reef fishes. Part V. Carangidae (jacks). Res. Rep. Zool. Dep. Univ. West Indies 3:1–43. Thomson, D.A., and K.A. Muench. 1976. Influence of tides and waves on the spawning behavior of the Gulf of California grunion, Leuresthes sardina (Jenkins and Evermann). Bull. South. Calif. Acad. Sci. 74(2):198–203. Thomson, J.M. 1955. The movements and migrations of mullet (Mugil cephalus L.). Aust. J. Mar. Freshwater Res. 6:328–347. Walker, B.W. 1952. A guide to the grunion. Calif. Fish Game 38:409–420. Webber, J.D., and J.J. Cech. 1998. Nondestructive diet analysis of the leopard shark from two sites in Tomales Bay, California. Calif. Fish Game 84:18–24. Yamahira, K. 1997. Proximate factors influencing spawning site specificity of the puffer fish, Takifugu niphobles. Mar. Ecol. Prog. Ser. 147:11–19. Young, P.H. 1964. Some effects of sewer effluent on marine life. Calif. Fish Game 50:33–41.

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CHAPTER 7

Continental Shelf and Upper Slope M. JAM E S ALLE N

Introduction Historically, the continental shelf (conventionally defined from shore to 200 m) and the upper slope (depths of 200–500 m) have been the focus of much of the world’s marine fishing. The predominant habitat of the shelf and upper slope consists of sandy and muddy sediments. Many species of fish characteristically occur in this habitat, and some of these show unique adaptations to life on a relatively flat and featureless benthic habitat. This soft-bottom habitat is easily fished using bottom trawls, and hence the soft-bottom fish fauna is often the source of important fisheries in much of the world. More recently, because of the ease of sampling and the discharge of wastewater onto this habitat, this fauna has become the focus of environmental assessments of human activities on the shelf. Because of the importance of the soft-bottom fish fauna to fisheries and to environmental assessments, the biology and ecology of the fauna have been relatively well studied. However, although the fauna has been relatively well studied off California and Pacific Baja California, there is no overall summary of the soft-bottom fish fauna and its ecology for the entire region. This chapter provides a first recent attempt to summarize what is known about the ecology of the soft-bottom fish fauna of the continental shelf and upper slope of the California and the Pacific coast of the Baja California Peninsula (the deeper slope is discussed in Neighbors and Wilson in chapter 12 of this book). The chapter begins with an overview of the physical conditions of the habitat, followed by overviews of scientific study, sampling methods, the soft-bottom fish fauna of the Californias (e.g., taxonomic composition, biogeography, morphology, lifehistory traits, assemblages, and community organization), a brief comparison of this fauna to similar faunas elsewhere in the world, and ends with a prospectus for future research.

Physical and Biological Conditions on the Shelf and Upper Slope

continental slope. Conventionally, the continental shelf is considered to extend seaward to the 200 m isobath (Emery, 1969), although the geological shelf is somewhat shallower (Curray, 1966). The geological shelf extends seaward to the shelf break (a sharp change of slope), occurring at a depth of 130 m, in most places, worldwide (Curray, 1966). Although the shelf break is also at this depth off northern and central California (Jane A. Reid, United States Geological Survey Pacific Science Center [USGS, PSC], University of California, Santa Cruz, CA; pers. comm.), it ranges from 80 to 145 m in southern California (Emery, 1960). Along California and the Pacific Coast of Baja California, the continental shelf occurs continuously along the mainland, with shelf areas also at coastal islands and some banks (Fig. 7-1). The shelf (shore to 200 m) is moderately wide off northern and central California (
1–50 km), very narrow along mainland southern California (0.06–13 km), moderate to narrow along northern Baja California (3–22 km), and very broad in Bahia Sebastian Vizcaino and along the west coast of Baja California Sur (85–135 km). The area of the California shelf is estimated at about 28,000 km2 (25,000–30,000 km2) (Jane A. Reid, USGS, PSC, pers. comm.). Although there are no similar estimates for the shelf off the Pacific coast of the Baja California Peninsula, most of the shelf area clearly lies off Baja California Sur. The upper slope (between the 200 and 500 m isobaths) is generally much narrower than the shelf because of its steeper slope. It typically ranges from about 1 to 10 km wide but is relatively wide (75 km) west of southernmost Baja California Sur. A branch of the upper slope extends as a large submarine peninsula off southern California, extending 160 km south from Point Conception as the Santa Rosa–Cortez Ridge to San Nicolas Island. From Santa Rosa to San Nicolas Island, the upper slope extends 45 km in continuous length with additional large upper slope bank areas south to Cortez Bank.

Topography

Soft-Bottom Habitat

The continental shelf is the gently sloping submerged continental margin that extends seaward to the steeply sloping

The soft-bottom habitat is the dominant habitat of the shelf and upper slope. This habitat comprises more than 50% (and

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500 m (Emery, 1960). Oxygen decreases from 6 mL/L at the surface to 1.5 to 2 mL/L at 200 m and to about 0.6 mL/L at 500 m. Pressure changes from 2.1 kg/cm2 (2 atmospheres) at 10 m to 21.7 kg/cm2 (21 atm) at 200 m and 52.7 kg/cm2 (51 atm) at 500 m. Light penetration decreases with depth more rapidly in coastal waters than in the clear open ocean; sufficient ambient light exists for vertebrate sight during the day to a depth of about 200 m (coastal turbidity further decreases light penetration) (Clarke and Denton, 1962). In contrast, similar light levels occur in clear open ocean water at depths of 1000 m in daylight and 600 m in moonlight. Bioluminescence becomes more important than ambient light at night or in deep water (Clarke and Denton, 1962).

Overview of Scientific Studies of Soft-Bottom Fishes of the Californias Types of Studies by Focus

F I G U R E 7-1 Shelf (shore to 200 m isobath) and upper slope (200–500 m) of California and Pacific Coast of Baja California, with analytical regions discussed in text.

probably from 70 to 90%) of the California shelf area (J. A. Reid, USGS, PSC, pers. comm.) and is probably the dominant habitat off the Pacific Coast of Baja California, particularly on broad shelf areas off Baja California Sur. Hard bottoms are most common inshore near rocky headlands, along steep narrow shelf areas (e.g., islands, central California), and the shelf break or submarine canyons. Some low-relief, hard-bottom areas are transitional between hard- and soft-bottom areas. Sandy sediments are more common in nearshore areas, along the shelf break, and on the island and bank shelf; silt, clay, and mud sediments are common between the shelf break and inshore sand zone and below the shelf break (Emery, 1960; Curray, 1966). Although the soft-bottom habitat is relatively flat, there is some microrelief resulting from water movement (waves, currents) or biological activity (e.g., excavations, burrows, protruding tubes).

Changes in Physical Conditions with Depth Temperatures off southern California decrease from 14.5 to 19.5°C at the surface to 8 to 9°C at 200 m, and to 6°C at

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Information on soft-bottom fishes off the Californias has been gathered for more than 150 years. Most of this information is from three types of studies, each with a different focus: (1) taxonomic, (2) fisheries, and (3) pollution assessment (table 7-1). Taxonomic studies (conducted by museums) focused on species descriptions and have been conducted from the early 1850s to the present along the entire coast of the Californias. Fisheries studies that have been conducted since the early 1900s consist primarily of stock assessments and gathering of fisheries-relevant life-history information. These studies were done by the California Department of Fish and Game (CDFG) in state waters (less than 4.8 km from shore) and by the National Marine Fisheries Service (NMFS) in federal waters (more than 4.8 km from shore). Environmental studies in California since the late 1950s generally focus on assessment of pollution effects. These are usually monitoring studies that are required by the State Water Resources Control Board (SWRCB) or United States Environmental Protection Agency (USEPA), although research oriented studies are also conducted, particularly by the Southern California Coastal Water Research Project (SCCWRP).

Early Studies (1850–1950) The earliest scientific studies of the soft-bottom fish fauna of the Californias focused on species descriptions because almost the entire fauna was unknown to science. The first scientific collections of soft-bottom species began in the 1850s with the U.S. Pacific Railway surveys (table 7-1). Many fish species were collected from fish markets at this time and sent to the Smithsonian Institution for description by ichthyologists (e.g., C.F. Girard, W.O. Ayres, W.N. Lockington) (Hubbs 1964). The first scientific ocean surveys of this fauna were U.S. Fisheries Commission Steamer Albatross surveys, which were conducted from northern California to southern Baja California, and particularly off southern California during 1889–1916 (Hedgpeth, 1945; Moring, 1999). These surveys sampled stations at depths from 15 to 4100 m using beam trawls (USBF, 1906), and fishes were distributed to museum ichthyologists (e.g., Charles Henry Gilbert) for description. The next major scientific survey was the Allan Hancock Foundation Anton Dohrn survey conducted on the shelf in

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TA B L E 7-1

Historical Summary of Soft-Bottom Fish Studies on the Continental Shelf and Upper Slope off California and Baja California I. Types of studies by focus A. Taxonomic studies (museum surveys), 1850s to present, used beam trawls early, otter trawls later B. Fisheries studies (stock assessments, fisheries-relevant life-history studies), early 1900s to present 1. CDFG—State waters (
4.8 km from shore)—12.2-m wide otter trawls, 20–30 min tows 2. NMFS—Federal waters (4.8 km from shore)—22–32 m wide otter trawls, 20–30 min tows C. Environmental studies—late 1950s to present, water quality agencies, 7.6-m wide otter trawls, 10-min tows 1. SWRCB—regulatory, by CDFG, POTWs, and consulting firms—5.3–12.2 m wide otter trawls, 5–20 min tows 2. SCCWRP—research and assessment surveys—7.6-m wide otter trawls, 10-min tows II. Early studies (1850–1950)—unknown fauna, focus on species descriptions A. U. S. Pacific Railway surveys of California, sampled fish markets (Hubbs, 1964) B. U. S. Fisheries Commission Steamer Albatross surveys (California and Baja California), sampled depths of 15–4100 m with 2.2–4.9 m wide beam trawls towed for 20–25 min; species described by C. H. Gilbert (USBF, 1906) C. USC, AHF Southern California surveys, 10–200 m, 1.5-m wide beam trawl, 20-min tow (Ulrey and Greeley, 1928) III. Studies since 1950 by region A. Northern and Central California 1. Environmental assessments of inner shelf (
30 m) a. 1960s—Morro Bay (Heimann and Miller, 1960); Monterey Bay (Heimann, 1963); San Francisco Bay (Alpin, 1967) b. 1970s—SWRCB predischarge surveys (Humboldt Bay, San Francisco Bay, Watsonville, central Monterey Bay, San Luis Obispo, Morro Bay) c. 1980s to present—San Francisco Bay (CDFG; Baxter et al., 1999), San Francisco Coast (City of San Francisco) 2. NMFS groundfish stock assessment surveys of shelf and slope (50–1280 m), 32 m wide nets, 30-min tows a. Shelf and upper slope (50–366 m) (Gunderson and Sample, 1980; Weinberg et al., 1984; 1994; Coleman, 1986, 1988; Dark and Wilkins, 1994; Jay, 1996; Zimmerman et al., 1994; Wilkins et al., 1998; Shaw et al., 2000) b. Slope (183–1280 m) Lauth (1997, 1999, 2000, 2001), Lauth et al. 1997) B. Southern California 1. Fishery surveys—CDFG (Jow, 1969); NMFS in 1977 (Gunderson and Sample, 1980) and 2002–2003 2. Environmental surveys (SWRCB, USEPA, and SCCWRP)—7.6 m wide trawls, 10-min tows a. CDFG—Santa Monica Bay, 1957–1963, 10–200 m (Carlisle 1969) b. POTW Monitoring Surveys (USEPA-SWRCB NPDES and 301h Waiver)—POTW quarterly reports 1. County Sanitation Districts of Los Angeles, Orange County Sanitation Districts (1970s to present) 2. City of Los Angeles, City of San Diego (1980s to present) c. SCCWRP research and assessement surveys (1970s to present)—SCCWRP (1973) and Annual Reports; M. J. Allen (1982a); Thompson et al. (1987, 1993); M. J. Allen et al. (1998, 2002) 3. Educational surveys (1970s to present) a. Occidental College (Stephens et al., 1973, 1974; Love et al., 1986); UCLA (Mearns and M. J. Allen, 1973); b. Ocean Institute ( = Orange County Department of Education; Orange County Marine Institute) C. Baja California—Hubbs (1960) provides some information on soft-bottom fishes of Pacific Coast 1. Scripps Instititution of Oceanography (SIO) surveys, 1950–1984, 200 sites, 2–622 m (SIO Fish Collection) 2. CalCOFI surveys—1970–1971, 27–95 m, incidental to plankton surveys, (R. N. Lea, CDFG, pers. comm.) 3. Baja California University surveys a. CICESE—Baja California,
30 m depth (Hamman and Rosales Casian, 1990) b. CICIMAR—Baja California Sur, 1990, 38–218 m, 21 m wide otter trawl (Murillo et al., 1998) NOTE : CalCOFI  California Cooperative Oceanic Fisheries Investigations; CDFG  California Department of Fish and Game; CICESE  Centro de Investigación Científica y de Educación Superior de Ensenada; CICIMAR  Centro Interdisciplinario de Ciencias Marinas; NMFS  National Marine Fisheries Service; POTW  publicly owned treatment works; SCCWRP  Southern California Coastal Water Research Project; SWRCB  State Water Resources Control Board; UCLA  University of California, Los Angeles; USEPA  United States Environmental Protection Agency; USC, AHF  University of Southern California, Allan Hancock Foundation.

southern California at depths of 10–200 m from 1912 to 1922 using beam trawls (Ulrey and Greeley, 1928). This was the first survey where all species collected at a site were reported. Other scientific studies of these fishes made after 1922 were conducted by CDFG and a focused on life-history information on important fisheries species.

Studies Since 1950 by Region Since 1950, information on the soft-bottom fish fauna of the Californias has increased dramatically with routine fisheries and environmental monitoring surveys. The types and intensity of the surveys, as well as the sampling methods vary in

each of three regions: (1) northern and central California, (2) southern California, and (3) Baja California (table 7-1). Northern and central California surveys consist primarily of environmental assessments using small otter trawls on the inner shelf at depths less than 30 m and NMFS groundfish stock assessment surveys using large otter trawls on the deeper shelf and slope (50–1280 m) (table 7-1). The former have been conducted irregularly from the early 1960s to the present from Humboldt Bay to Morro Bay, usually in response to SWRCB regulatory requirements. The latter in some form have been conducted regularly since 1977. Data from the former studies are found in reports submitted to the SWRCB and in CDFG reports. Good and extensive data summaries from the NMFS studies are found in numerous technical reports (e.g.,

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Coleman, 1986; Zimmerman et al., 1994; Lauth et al., 1997; Wilkins et al., 1998; Shaw et al., 2000), journals (e.g., Heimann and Miller, 1960; Heimann, 1963; Gabriel and Tyler, 1980; Gunderson and Sample, 1980; M.J. Allen and Smith, 1988; Wakefield and Smith, 1990; Dark and Wilkins, 1994; Weinberg, 1994; Jay, 1996; Williams and Ralston, 2002), and dissertations (Gabriel, 1980; Wakefield, 1990). Southern California surveys consist primarily of environmental assessments using small otter trawls at depths mostly less than 200 m, but some to 1000 m (table 7-1). These have been conducted since the late 1950s by CDFG and publicly owned treatment works (POTWs) in response to USEPA or SWRCB requirements but also by SCCWRP. Educational surveys have been regularly conducted since the early 1970s. Most fisheries surveys have focused on single species collections, but recent NMFS surveys (2002–2003) are providing stock assessment information on more species. Although studied extensively, most information from this region is found in monitoring reports submitted by large POTWs to State Regional Water Quality Control Boards or USEPA, technical and annual reports produced by SCCWRP, CDFG internal reports, and reports submitted to California Sea Grant. Some studies in this region have been published in journals or books (e.g., Carlisle, 1969; Mearns, 1974; M. J. Allen, 1977; Mearns, 1979; Gunderson and Sample, 1980; M. J. Allen, 1982b; Love et al., 1986; Cross, 1987; Stull, 1995; Stull and Tang 1996) and dissertations (e.g., M. J. Allen, 1982a). The most extensive regionwide studies of this fauna in the Southern California Bight are M. J. Allen (1982a) and M. J. Allen et al. (1998, 2002). Baja California surveys have been largely exploratory. Museum collections by Scripps Institution of Oceanography are the most extensive (more than 200 sites at depths of 2–622 m from 1950 to 1984) (table 7-1). Trawl samples were also conducted incidentally in 1970–1971 California Cooperative Oceanic Fisheries Investigation surveys. Baja California universities (Centro de Investigación Científica y de Educación Superior de Ensenada [CICESE] and Centro Interdisciplinario de Ciencias Marinas [CICIMAR]) have conducted more recent surveys along this coast (e.g., Hammann and Rosales Casián, 1990; Murillo et al., 1998). Hubbs (1960) described in general the fish fauna on the Pacific Coast of Baja California but provided little information on the soft-bottom fauna of the shelf and slope.

Sampling Methods Soft-bottom fishes live on a relatively flat, featureless bottom of sediment and hence can be effectively caught by dragging a net along the bottom. Beam trawl samples were used in the earliest scientific studies of this fauna (USBF, 1906; Ulrey and Greely, 1928); otter trawls were more commonly used after 1950. Beam trawls have metal rectangular mouth frames and hence a mouth opening with fixed dimensions. Otter trawls use otter boards attached to the wings of the net. As the net is towed, water force on the boards causes the net to spread open. In contrast to the fixed-opening beam trawls, otter trawls have mouths with more variably sized openings. However, the size and weight of the frame makes large beam trawls impractical, limiting beam trawls to small mouth openings (e.g., 1.0–1.6 m). Small beam trawls capture smaller and less mobile fishes than are caught by small otter trawls and are less useful for assessing soft-bottom assemblages.

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Nevertheless, they are valuable tools (with very fine net mesh) for capturing very small juveniles (L. G. Allen et al., 1990; M.J. Allen and Herbinson, 1990; Kramer and SWFSC, 1990; M.J. Allen and Herbinson, 1991; L. G. Allen and Franklin, 1992). Otter trawl nets used in surveys range in width from 4.9–32.0 m (headrope). Small nets (4.9–12.2 m wide) are used on the inner shelf of central and northern California and across the southern California shelf and upper slope. Large nets (22–32 m) are used by CDFG and NMFS assessment surveys of the deeper shelf and upper slope (predominantly off central and northern California). However, the width of the net opening during a tow (board or net spread) is less than the actual headrope length; the actual board spread of small nets is 3.4 m for 4.9-m nets, 4.9 m for 7.6-m nets, and 7.9 m for 12.2-m nets (Mearns and Stubbs, 1974). This is likely to vary, depending on vessel speed, bottom type, and weight of catch in the bag. The actual horizontal sweep (net spread) of a 27-m headrope Nor’Eastern trawl is 13.4 m with a headrope height of 8.8 m (Gunderson and Sample, 1980). In 1972, sampling gear and protocol for environmental trawl surveys in southern California were standardized to 7.6-m wide (headrope) semiballoon otter trawls with 1.3-cm cod-end mesh towed along isobaths for 10 minutes (Mearns and M. J. Allen, 1978). NMFS trawl surveys of the shelf and slope off California have used commercial nets (22–32 m headropes with roller gear) towed for 30 minutes to provide catches similar to those obtained by commercial fishermen (Gunderson and Sample, 1980; Dark and Wilkins, 1994). Compared to other sampling methods, otter trawls provide the most information for assemblage studies and for assessment of population status and fish health (M. J. Allen, 1975, 1976). Relative to hook-and-line and observational techniques, otter trawls yield the most species and allow accurate identification of species; counts of individuals; measurement of biomass and lengths; examination of diseases; and collection of specimens for stomach analysis, age and growth studies, and tissue chemistry analysis. However, they provide little information on the behavior of the fishes in their natural environment. Depending on the net size, they underestimate the abundance of large individuals and fast swimming species (for small trawls) or small individuals and species (for large trawls). Jow (1969), using 22 and 32-m wide (headrope) otter trawls, caught larger individuals and missed many small species that are typically taken in smaller (7.6-m wide headrope) otter trawls (e.g., M. J. Allen et al., 1998). Large species are caught more efficiently with larger otter trawls or hook-and-line techniques. Soft-bottom trawl (7.6-m headrope) stations have been sampled with hook-and-line methods on the shelf (M. J. Allen et al., 1975) and upper slope (Cross, 1987) to compare methods. Benthic set lines effectively sampled wide-ranging, benthic foraging species that may escape the net, whereas fishing by rod-and-reel in sonar-located schools near the bottom was a more effective way to catch highly clumped fishes likely missed by chance in a trawl (M.J. Allen et al., 1975; M.J. Allen 1976). Although most individuals caught were equivalent to large-sized trawl-caught individuals, fewer small individuals were taken by hook-and-line. Cross (1987) caught more species by longline than trawl on the upper slope but attributed this to more fishing on banks, with more vertical relief, than strictly on a softbottom. Observational sampling (diver observation—M. J. Allen et al., 1976; remote photographs or videos—SCCWRP, 1974; Moore and Mearns, 1980; Wakefield, 1990) gives more information on fish behavior in the natural environment, but

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identifications are less accurate and fewer measurements can be taken. SCCWRP (1974) used a cine camera left on the bottom for a 24-hour period and timed to take a 15-second film every half hour to document diel changes in fish activity. A combination of methods would yield the most behavioral and ecological information (M. J. Allen, 1976).

Trawl Survey Assessments of Soft-Bottom Fauna Comparability of Surveys Although sampling of the soft-bottom fish fauna has been extensive (particularly in California), differences in sampling gear and protocol and differences in types of data gathered in the fisheries surveys of northern and central California and the environmental surveys of the southern California shelf make coastwide comparisons difficult. NMFS surveys use commercialsized nets (e.g., 27-m headrope, with an actual net spread of 13.4 m), often with roller gear, and towed for 30 minutes at 1.5 m/second (Gunderson and Sample, 1980), whereas environmental surveys use small shrimp trawls (7.6-m headrope, and actual net spread of 4.9 m) towed for 10 min along isobaths at 1 m/second (Mearns and M. J. Allen, 1978). Thus a NMFS trawl sample using a 27-m net collects fish from an area of about 16,800 m2, whereas an environmental trawl survey using a 7.6-m net collects fish from about 2900 m2. Further, the NMFS trawls have larger net mesh (e.g., 8.9-cm body mesh and 3.2-cm cod-end mesh; Dark and Wilkins, 1994) than trawls used in southern California (3.8–5.0-cm body mesh and 1.3-cm cod-end mesh; Mearns and M. J. Allen, 1978). The use of roller gear, which allows trawling on a hard bottom results in an increased proportion of hard-bottom species (e.g., some rockfish species) in the catches, which blurs the distinction between the soft- and hard-bottom fauna. The difference in horizontal sweep and height of net opening, as well as differences in tow duration, body and cod-end mesh size, and presence or absence of roller gear, all but preclude comparisons between northern/central California and southern California trawl surveys of the shelf, except in a very gross manner (e.g., presence/absence of species, relative abundance of species). These two types of surveys also gather slightly different attributes of the fishes. The NMFS surveys focus on type of species, biomass by species, with information on numbers of individuals for some species, as well as length measurements and otoliths (for aging) of important fisheries species. The environmental surveys in southern California collect information on type of species, numbers and lengths of individuals, biomass by species and assesses anomalies and diseases (e.g., Mearns and M. J. Allen, 1978; M. J. Allen et al., 1998, 2002). Environmental surveys of the inner shelf of northern and central California are comparable with those of southern California, because they used similar gear and protocol.

Population Characteristics A number of measures are used to summarize trawl catches across all species sampled, including numbers of individuals (abundance), biomass, species richness (numbers of species), and species diversity (e.g., Shannon-Wiener diversity;

Shannon and Weaver, 1949). Abundance and biomass, frequently expressed as catch per unit effort (CPUE), describe the number or biomass of fish per some sampling unit (e.g., unit area; standard tow) (Dark and Wilkins, 1994). In addition to these, length or age frequency distributions are sometimes used to provide information on the population structure of individual species (Dark and Wilkins, 1994; M. J. Allen et al., 1998, 2002). Based on 2237 otter trawl samples collected in southern California from 1957 to 1975, an average standard 7.6-m headrope otter trawl towed for 10 minutes captured 173 fish representing 11 species, weighing 7 kg, and with a ShannonWiener diversity of 1.36 (M. J. Allen and Voglin, 1976). In this area, CPUE is expressed in terms of catch per standard trawl sample, which samples an area of about 2900 m2. In regional surveys of the southern California shelf in 1994 and 1998, an average trawl sample (same dimensions and protocol) collected 156–157 fish representing 10–12 species, weighing 5–6 kg, and with a diversity of 1.57–1.59 (M. J. Allen et al., 1998, 2002). Variation of fish population attributes (abundance, biomass, species richness or number of species, and diversity) have been examined by region and depth in southern California (M. J. Allen and Voglin, 1976; M. J. Allen and Mearns, 1977; M. J. Allen, 1982a; Cross, 1987; Thompson et al., 1987, 1993; M. J. Allen et al., 1998, 2002). In this region, the best assessment of this variation over a large scale was based on regional surveys of the southern California shelf in July–September 1994 and 1998 using a stratified random survey design for assessing spatial differences (M. J. Allen et al., 1998, 2002). Population attributes vary more significantly by depth than by region within southern California (M. J. Allen and Moore, 1996; M. J. Allen et al., 1998, 2002). Fish abundance, biomass, species richness, and diversity were lowest on the inner shelf; abundance and biomass increased from the middle to the outer shelf. The low population attributes on the inner shelf may be related to a more variable environment (e.g., of temperature, salinity, turbulence, and food availability) (M. J. Allen et al., 1998). High daytime light levels on the inner shelf may make active benthic fishes more susceptible to predation than in deeper water, resulting in less diurnal benthic activity and increased selection for schooling in watercolumn species. High light levels may also facilitate net avoidance by fishes. Southern California trawl catches were larger and more diverse on the coastal shelf than on the upper slope (M. J. Allen and Mearns, 1977). Biomass per individual increased on the outer shelf and upper slope (100 to 450 m) due largely to a decrease in the abundance of juveniles. Along the upper slope, significantly more species were taken at 290 m than at deeper stations (Cross, 1987). Although NMFS surveys provide extensive information on populations of individual fisheries species, they provide less information on the catch as a whole; they lack information on distributions of mean densities, diversity, and species richness per sample (all measures commonly used in environmental analyses). In northern and central California, mean CPUE (kg/km trawled) of all species decreased from the shelf (55–183 m) to upper slope (184–366 m) in the Eureka INPFC area from 1977 to 1986 (Dark and Wilkins, 1994). However, in the Monterey region, this relationship varied by survey year (decreased with depth in 1980 and 1986 and increased with depth in 1977 and 1983).

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Taxonomic Composition of Catches California trawl surveys collect a large number of species and these represent a diversity of taxa. Three surveys (M. J. Allen, 1982a; M. J. Allen et al., 1998, 2002) in southern California provide information on the general taxonomic composition of southern California regional trawl surveys across depths of 10–200 m. In these surveys, 87–142 species were collected, representing 34–57 families, 12–19 orders, and 3–4 classes. Trawl surveys were overwhelmingly dominated by Actinopterygii (ray-finned fishes), followed by Chondrichthyes (cartilaginous fishes), and Myxini (hagfishes). For example, actinopterygiian fishes comprised 88.1% of the species and 99.8% of total individuals in 1972–1973 (M. J. Allen, 1982a). Scorpaeniform (scorpionfish-like fishes), perciform (perch-like fishes), and pleuronectiform (flatfishes) species comprised 75.4% of the species and 93.5% of total individuals in 1972–1973. Scorpaenidae (scorpionfishes and rockfishes), Pleuronectidae (right-eyed flounders), Cottidae (sculpins), and Paralichthyidae (sand flounders) were the most diverse families (M. J. Allen, 1982a). Typically, 17–24 species occurred in 20% or more of the survey area, 23–26 species comprised 95% of the total catch, and 28–44 species comprised 95% of the total biomass (M. J. Allen, 1982a; M. J. Allen et al., 1998, 2002). The most frequently occurring species were Dover sole (Microstomus pacificus) in 1972–1973 and Pacific sanddab (Citharichthys sordidus) in 1994 and 1998. The most abundant species was stripetail rockfish (Sebastes saxicola) in 1972–1973, Pacific sanddab in 1994, and white croaker (Genyonemus lineatus) in 1998 (which included harbors as well as the shelf). The biomass dominant was California halibut (Paralichthys californicus) in 1994 and white croaker in 1998. The dominance of white croaker in the latter study was due to inclusion of Los Angeles-Long Beach Harbors (a preferred habitat for this species) in the survey. Pacific sanddab was biomass dominant in 1998 when harbors were excluded from the analysis. NMFS surveys of the shelf (55–183 m) of central and northern California in 1995 and 1998 (Wilkins, 1998; Wilkins and Shaw, 2000) collected the same four classes as in southern California. Scorpaenidae was the most diverse family with 33 species, followed by Pleuronectidae with 13, and Cottidae with 7. Dominant species by biomass CPUE varied by INPFC areas (Wilkins et al., 1998; Shaw et al., 2000); Pacific hake (Merluccius productus) was dominant in the Eureka and Monterey INPFC areas and either spotted ratfish (Hydrolagus colliei) or shortbelly rockfish (Sebastes jordani) in the Conception INPFC area. Pacific sanddab was generally the dominant obligate soft-bottom species in these trawls in all areas, usually ranking second or third to the dominant species. Other species ranking among the top three in these regions were epipelagic species: Pacific herring (Clupea pallasii) (Eureka and Conception) and jack mackerel (Trachurus symmetricus; (Monterey and Conception). Important demersal species were English sole (Parophrys vetulus), chilipepper (Sebastes goodei), and spiny dogfish (Squalus acanthias) in the Eureka, Monterey, and Conception areas, respectively. On the upper slope (200–500 m), the four classes mentioned above occurred with similar abundance and diversity relationships as on the shelf (M. J. Allen and Mearns, 1977; Cross, 1987; SCCWRP, unpublished data). As on the shelf, Scorpaenidae and Pleuronectidae are the most diverse families, but Zoarcidae (eelpouts) ranked third. Although sablefish (Anoplopoma fimbria), Dover sole, shortspine thornyhead (Sebastolobus alascanus), and splitnose rockfish (Sebastes diplo-

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proa) were the four most frequent species in both periods, sablefish occurrence decreased by nearly half between the 1970s and 1980s. Similarly, in NMFS surveys of the central and northern California upper slope (183–500 m) in 1995 and 1998, Scorpaenidae, Pleuronectidae, and Zoarcidae were the most diverse families, with 30, 10, and 7 species, respectively (Wilkins, 1998; Wilkins and Shaw, 2000). Dominant species differ somewhat between the shallower (183–366 m) and deeper (367–500 m) parts of the this depth zone as well as by region. Pacific hake was typically the dominant species in the shallower region and Dover sole in the deeper region. In the Eureka area, three species have the highest biomass CPUE in both years and depths: Pacific hake, Dover sole, and sablefish; Pacific hake dominated the shallower region. In the Monterey Area, Pacific hake and splitnose rockfish dominated the shallow region (with stripetail rockfish or chilipepper third), whereas Dover sole dominated the deeper region (Pacific hake or rex sole, Glyptocephalus zachirus, were second or third). In the Conception area, the shallow region was dominated by splitnose rockfish, stripetail rockfish, and Pacific hake, respectively, whereas the deeper region was dominated by Dover sole or Pacific hake (rex sole or splitnose rockfish also was important).

Assemblages Soft-bottom fish assemblages have been described on the shelf and upper slope of California, but descriptions are done by different methods, based on different population attributes of the species and for only part of the area. Assemblages described on the shelf and upper slope of northern and central California have used NMFS survey data, species biomass, and cluster analysis (Gabriel, 1980; Jay, 1996). In southern California, statistical assemblage analysis has used environmental and academic survey data. Two types of analyses have been used there. Recurrent group analysis with presence/absence data (SCCWRP, 1973; Mearns, 1974; M.J. Allen, 1982a; M.J. Allen and Moore, 1997; M.J. Allen et al., 1998, 2002) and cluster analysis using species abundance data (L.G. Allen, 1985; M.J. Allen et al., 1998, 2002). Rockfish assemblages in NMFS West Coast trawl surveys were defined by ordination and cluster analysis (Williams and Ralston, 2002). Recurrent group analysis describes groups of species that occur together frequently (Fager, 1957, 1963) and is based on binary (presence–absence) data. Recurrent group analyses in southern California have generally shown distinct recurrent groups associated with different shelf depth zones (e.g., inner shelf, middle shelf, outer shelf), but some groups with overlapping distributions did occur (e.g., inner shelf–middle shelf; middle shelf–outer shelf) (SCCWRP, 1973; Stephens et al., 1973; Mearns, 1974; M. J. Allen, 1982a; M. J. Allen and Moore, 1997; M. J. Allen et al., 1998, 2002). In the 1998 survey (which included bays, harbors, and islands), bay and harbor groups were identified, but there was no major island recurrent group (M. J. Allen et al., 2002). At the 0.50 affinity level, these studies described 9–11 recurrent groups with 2–7 species per group. Generally, 33–34 species comprised the recurrent groups, and these represented 23–39% of the species taken in a survey. Comparison of recurrent groups from a cold-regime period (1972–1973; M. J. Allen, 1982a), warm-regime period (1994; M. J. Allen et al., 1998), and El Niño period (1998; modified by M. J. Allen et al., 2002) identified core groups of species that occurred together in all three oceanic periods. These included

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the following: (1) an inner shelf–middle shelf group— California tonguefish (Symphurus atricaudus) and hornyhead turbot (Pleuronichthys verticalis); (2) a middle shelf–outer shelf group—Pacific sanddab, Dover sole, plainfin midshipman (Porichthys notatus), and stripetail rockfish; (3) an outer shelf group associated with fragile sea urchin (Allocentrotus fragilis)— slender sole (Lyopsetta exilis) and shortspine combfish (Zaniolepis frenata); and (4) an outer shelf group associated with northern heart urchin (Brisaster latifrons)—rex sole and blacktip poacher (Xeneretmus latifrons) (M. J. Allen et al., 2002). Other species co-occurred variably with other species during the three periods. Site and species assemblages on the shelf and slope of central and northern California have been described in fish biomass data from NMFS surveys (Gabriel, 1980; Jay, 1996). Gabriel (1980) identified three major site groups, with two extending into southern California: (1) an upper slope group extending from Juan de Fuca Canyon, Washington, to Port Hueneme, California at depths of 183–467 m; and (2) a southern midshelf break [southern outer shelf–upper slope] group, extending from Cape Flattery, Washington, to Port Hueneme at depths of 91–267 m. These were divided into subregions along isobaths. Eight species groups were also identified, and two are important in California: a deepwater group of ubiquitous species largely found in the upper slope group and a shallow group concentrated in the southern outer shelf–upper slope site group. Jay (1996) described 23 site assemblages based on the biomass of the 33 dominant species in the NMFS continental shelf and upper slope surveys from the CanadaWashington border to Monterey, California, from 1977 to 1992. Most of the assemblages were dominated by Pacific hake. Of the 23 assemblages, 20 extended into California, with 13 occurring commonly. Of these, three were largely middle shelf assemblages and one was an upper slope assemblage; the remaining nine were predominantly outer shelf assemblages (with some overlapping into the mesobenthal slope). Williams and Ralston (2002) defined four major rockfish assemblages based on NMFS trawl surveys off California and Oregon: (1) a nearshore assemblage at depths less than 150 m; (2) a northern shelf group, from about 150 to 200 m and extending south to Monterey Canyon; (3) a southern shelf group, extending north to Cape Mendocino; and (4) a deepwater slope group, occurring below 200 m. Although site and species clusters have been described in local assessments of pollution effects in southern California (e.g., CSDOC 1996), regionwide descriptions of fish site and species assemblages for this area were not done until 1994 and 1998 (M. J. Allen et al., 1998, 2002). These identified depth-related assemblages in both years and also identified bay and harbor assemblages in 1998 (when these areas were included in the surveys). Five site assemblages and four species assemblages were described for the mainland shelf in 1994 (M. J. Allen et al., 1998). Site assemblages included inner shelf, inner shelf–middle shelf, middle shelf (two), and outer shelf assemblages. Species clusters included the following dominant species: (1) inner shelf—white croaker, (2) middle shelf—yellowchin sculpin (Icelinus quadriseriatus), (3) middle–outer shelf—Pacific sanddab, and (4) outer shelf— slender sole. In 1998, eight site clusters and seven species clusters were defined (M. J. Allen et al., 2002). Although the same five depth-related site clusters of 1994 were defined in 1998, a northern inner shelf- harbor group, a central inner shelf harbor group, and a southern bays group were also defined. Species groups were dominated by the following

species: (1) southern bays—round stingray (Urobatis halleri), (2) southern inner shelf/harbors—deepbody anchovy (Anchoa compressa), (3) central inner shelf/harbor—white croaker, (4) middle shelf–inner shelf—California lizardfish (Synodus lucioceps), (5) middle shelf–outer shelf (soft bottom)—Pacific sanddab, (6) middle shelf–outer shelf (island sand-rock)—spotfin sculpin (Icelinus tenuis), and (7) outer shelf—slender sole.

General Characteristics of the Fauna What Is a Soft-Bottom Fish? Although many fish species are caught on the soft-bottom habitat by trawls, only some are characteristic of the habitat. Soft-bottom fishes live on sandy, silty, or muddy bottoms of the sea floor. The true soft-bottom fish fauna of the California and Baja California shelf and slope is regarded here as those species that occur commonly on the soft bottom in at least one of the different life zones and play important ecological roles (generally with regard to feeding) in the community. Frequent occurrence is more important than abundance in this regard because this generally identifies species that are adapted to the soft-bottom habitat. Some taxonomic groups (e.g. Pleuronectiformes, Rajiformes, Ophidiidae [cusk-eels]) have morphologies specifically adapted to the soft-bottom habitat. Others (e.g., Cottidae, Scorpaenidae, Embiotocidae [surfperches]) commonly show fewer morphological adaptations (although some may show color adaptations) for this habitat. Also included here in this study are some nearbottom neritic species which occur frequently across the soft-bottom habitat. Although a large number of species are taken in trawl surveys in any area, only about half or less are characteristic softbottom species. A high proportion of the species on the softbottom habitat of the mainland shelf of southern California are either incidental to the habitat or region or are inadequately sampled by trawl. For instance, of 126 fish species collected in the early 1970s at depths of 10 to 200 m on the southern California shelf, 33 (26%) formed recurrent groups, occurred commonly in different life zones of the shelf, and were considered to represent the most characteristic softbottom fishes of the region (M. J. Allen, 1982a). These species accounted for 95% of the total fish abundance in this habitat. The remaining 93 species (68% of the total) were considered incidental (i.e., strays from other habitats, biogeographic provinces, or life zones). Similarly, 33 species (including most but not all of the recurrent group species) played important ecological roles as dominant members of different foraging guilds in life zones (M. J. Allen, 1982a). A soft-bottom fish then, is a fish that uses the soft-bottom habitat as its primary or one of its primary habitats and is a foraging guild dominant for this habitat in some part of its range.

Biotic Zones Z O O G E O G R A P H I C P R OVI N C E S

The distribution of marine organisms varies with latitude along the west coast of North America, usually from regional changes in water temperature (see chapter 1). This results in different regions having fish faunas with different species.

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Similar faunas are often found over a large part of the coast, but these faunas may change abruptly at certain locations along the coast (Briggs, 1975; Horn and L G. Allen, 1978; M. J. Allen and Smith, 1988; Briggs, 1995). Along the coasts of California and Baja California are two major zoogeographic provinces: Oregonian and San Diegan (Briggs, 1974, 1995). The cold temperate Oregonian Province extends from Vancouver Island south along the oceanic edge of the Southern California Bight into the nearshore upwelling areas of Northern Baja California. The warm temperate San Diego Province extends from southern California (inside of the California Current) down the Baja California coast to about Bahía Magdalena. In cold periods (e.g., 1950 to 1980) and particularly in the shallowest areas, Point Conception represents the northern limit of this fauna. However, in the past two decades of warm ocean conditions (Smith, 1995), many species in this zone have expanded their ranges farther north to Monterey or beyond. Off Baja California Sur, the San Diego fauna mixes with fishes from the warm temperate Cortez Province of the Gulf of California and the tropical Mexican and Panamanian Provinces (Briggs, 1974, 1995). Most of the Oceanic Region offshore of the Californias lies within the Transition Zone. During the past two warm decades, many of these species have extended their ranges northward; some reached southern California during the 1997–1998 El Niño (Lea and Rosenblatt, 2000; M. J. Allen and Groce, 2001a,b; Groce et al., 2001a,b). Although some species have ranges typical of the provinces described, others are temperate species, whose distributions of frequent occurrence extend across both Oregonian and San Diego Provinces (e.g., Pacific electric ray, Torpedo californica; Pacific hake; M. J. Allen and Smith, 1988). In addition, some are Californian warm-temperate species (found in both San Diego and Cortez Provinces) (e.g., Gulf sanddab, Citharichthys fragilis) or warm temperate-tropical, found in San Diego Province as well as in Mexican and Panamanian Provinces (e.g. longfin sanddab, Citharichthys xanthostigma). M. J. Allen and Smith (1988) examined distributions of softbottom species in 25,000 trawl samples collected in 30 years from the Arctic Ocean to the U. S.-Mexico border from a zoogeographic perspective. None of the 125 most common species had distributions restricted to a single biogeographic province of Briggs (1974). Because this study focused on the temperate Northeast Pacific, the greatest number of species were Eastern Boreal Pacific (i.e., Aleutian-Oregonian) species. Many of these boreal species extend in abundance into California to about the Mendocino Escarpment, with notable reduction in occurrence and abundance south of there. Examples of these species include Pacific tomcod (Microgadus proximus) and butter sole (Isopsetta isolepis). Others extend further south to Point Conception with reduced abundance to the south (e.g., big skate, Raja binoculata). A number of soft-bottom species typically have a San Diego Province distribution pattern (Point Conception to Bahía Magdalena) (Eschmeyer et al., 1983). These include thornback (Platyrhinoidis triseriata), California skate (Raja inornata), California lizardfish (Synodus lucioceps), specklefin midshipman (Porichthys myriaster), basketweave cusk-eel (Ophidion scrippsae), barred sand bass (Paralabrax nebulifer), bigmouth sole (Hippoglossina stomata), and California tonguefish. A number of species have San Diego-Cortez distributions and are found in both southern California and the Pacific Coast of Baja California and in the Gulf of California (usually the upper

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F I G U R E 7- 2 Pelagic and benthic life zones on the continental shelf

and slope of California and Pacific Baja California (modified from M. J. Allen and Smith, 1988).

Gulf). These include California scorpionfish (Scorpaena guttata), stripefin poacher (Xeneretmus ritteri), California halibut, fantail sole (Xystreurys liolepis), diamond turbot (Pleuronichthys guttulatus), and hornyhead turbot. LI F E ZON E S

Adaptive zones on or over the shelf and upper slope include pelagic and benthic habitats, with subregions of these, and depth-related life zones (Hedgpeth, 1957; M. J. Allen and Smith, 1988) (fig. 7-2). The pelagic region is divided into Oceanic and Neritic Subregions. The Neritic Subregion is that portion of the water column lying over the continental shelf (from the shore to a depth of 200 m), with the Oceanic Region over the slope and basins. Over the study area of this chapter (5 to 500 m), there are two Oceanic Zones: Epipelagic at depths of 0–200 m, and Mesopelagic from 200–1000 m. Hedgpeth (1957) partitioned the benthic region relevant to this chapter into a Sublittoral Zone from shore to depths of 200 m (the continental shelf), a Mesobenthal Zone from 200 to 500 m (the upper slope), and a Bathybenthal Zone from 500 to 1000 m. The Sublittoral Zone was then subdivided into an Inner Sublittoral Zone from 0–100 m and an Outer Sublittoral Zone from 100–200 m. M. J. Allen (1982a) described three major life zones (inner shelf—0–20 m; outer shelf—20–80 m, and upper slope— 80–170 m) for soft-bottom fishes on the continental shelf of southern California, based on shifts in the occurrence of 18 foraging guilds and changes in the dominance of depthdisplacing guild species comprising these guilds. Based on recognition that the continental shelf has conventionally been defined as extending to 200 m, regardless of the actual depth of the shelf break, I suggest that the outer shelf zone of M.J. Allen (1982a) be called the middle shelf zone, and the upper slope of that study be the outer shelf. Guild-related depth breaks change somewhat between different oceanic regimes; the inner shelf ranges from 0 to 20–30 m, the middle shelf from 20–30 m to 80–120 m, and the outer shelf from there to 170–200 m (M.J. Allen, 1982a; M.J. Allen et al., 1998, 2002). M.J. Allen and Smith (1988) used three shelf zones in an atlas of trawl-caught fishes from the Arctic Ocean to the United States-Mexico Border: inner shelf (0–50 m), middle shelf (50–100 m), and outer shelf (100–200 m), with the mesobenthal (upper) slope (200–500 m) and bathybenthal

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slope (500–1000 m). The greater depth of the inner shelf zone was based on a hydrographic region in the Bering Sea and on inshore limits of most National Marine Fisheries Service (NMFS) surveys along the West Coast. Hecker (1990) defined an upper slope zone from 200–500 m and an upper middle slope zone from 500–1,000 m (the same as Hedgpeth’s Mesobenthal and Bathybenthal Zones). In this chapter, the following definitions are used for these zones: inner shelf (5–30 m); middle shelf (31–100 m); outer shelf (101–200 m); and mesobenthal slope (201–500 m) (fig 7-2). In southern California the inner shelf, middle shelf, and outer shelf comprise about 22%, 54%, and 24% of the mainland shelf, respectively (M. J. Allen, 1982a). Although conditions vary along the coast, the inner shelf zone has relatively high temperature, oxygen, light, and turbulence with strong seasonal variability; low water pressure; and generally coarser sediments (except in protected areas). The deeper zones have decreasing temperatures, oxygen, and light, with less seasonal variability; low turbulence; and increasing water pressure. Offshore of the inner shelf, benefits from neritic and epipelagic productivity are highest on the middle shelf (which is the broadest shelf zone), decreases on the steeper outer shelf, and is least on the mesobenthal slope.

Regional Distribution of Families DI STR I B UTIONAL DATA SOU RCE S

Important species of soft-bottom fishes were identified based on information on the frequency of occurrence and abundance from the following sources: northern and central California— inner shelf (California State Water Resources Control Board data, 1973–1977) and middle and outer shelf and mesobenthal slope (Wilkins, 1998; Wilkins and Shaw, 2000); southern California—inner shelf, middle, outer shelf, and mesobenthal slope (M. J. Allen, 1982a; Cross, 1987; SCCWRP historical trawl database from 1969 to 2000 [about 6200 samples]); and Baja California (Scripps Institution of Oceanography, Fish Collection data, 1950–1998; California Department of Fish and Game, CalCOFI cruise data, 1970–1971). These surveys provide widespread information on fish occurrence but differ widely in the size of trawl used; much larger trawls (27-m headrope) were used on the northern and central California middle and outer shelf and Mesobenthal slope; smaller trawls (e.g., 7.6-m) used on the northern and central California inner shelf and southern California shelf and Mesobenthal slope; and 3- to 15-m headrope trawls off the Baja California shelf and Mesobenthal slope. Because of this, small species were not well represented in the northern and central California middle and outer shelf and mesobenthal slope, and large species were poorly represented on the inner shelf of northern and central California, southern California, and Baja California. Nevertheless, these surveys provide relatively comparable information on moderatesized species across all areas. Few samples were collected on the mesobenthal slope of Baja California, and hence it is is not well characterized in this study. In comparing the fauna across the California/Baja California shelf and slope, regions are defined as follows: northern California (Oregon-California border to Cape Mendocino); north-central California (Cape Mendocino to San Simeon); south-central California (San Simeon to Point Conception); southern California (Point Conception to the U.S.–Mexico Border); northern Baja California (U.S.–Mexico

border to the Baja California–Baja California Sur border); Northern Baja California Sur (Baja California–Baja California Sur border to Magdalena Bay); and southern Baja California Sur (Magdalena Bay to Cabo San Lucas, Baja California Sur) (fig. 7-1). A large number of species were collected in these surveys, and it is not possible to list all in this chapter. Those listed and considered important in this study (table 7-2) are those that occur frequently within a life zone and a region (based on the distributional information sources listed above) and are likely to be important representatives of a foraging guild there. DI STR I B UTION OF I M P ORTANT FAM I LI E S

About 40 families have members that are good representatives of the soft-bottom habitat of the shelf and slope of the Californias (tables 7-2, 7-3). Based on the frequency of occurrence in the above trawl surveys, the most widespread families on the soft-bottom habitat of the Californias were the Paralichthyidae, Pleuronectidae, Batrachoididae (midshipmen), and Ophidiidae, in all regions from northern California through Southern Baja California Sur (table 7-3). Pleuronectidae and Ophidiidae were generally important across the shelf and mesobenthal slope, Paralichthyidae and Batrachoididae on the shelf. Merlucciidae was important in all regions except northern Baja California, predominantly on the middle shelf, outer shelf, and mesobenthal slope. Of the remaining families, there is a gradual shift in distribution from the north to the south (table 7-3). Of families with northern affinities, Gadidae (cods) are important only in northern California and across the shelf. Osmeridae (smelts) and Squalidae (dogfish sharks) were important from Northern through south-central California on the inner shelf and middle shelf–outer shelf, respectively. Torpedinidae (torpedo electric rays), Anoplomatidae (sablefish), Scyliorhinidae (cat sharks), Liparidae (snailfishes), and Macrouridae (grenadiers) were important from northern California through southern California. Torpedinidae is most important on the outer shelf and the others on the mesobenthal slope. Hexagrammidae (greenlings), Chimaeridae (chimaeras), and Zoarcidae were important from northern California through northern Baja California, the first on the shelf and the last two on the outer shelf–mesobenthal slope. Cottidae, Embiotocidae, Rajidae (skates), Scorpaenidae, and Agonidae, also widespread, were important from northern California through northern Baja California Sur. Cottidae and Embiotocidae were imporant on the shelf, Rajidae and Scorpaenidae on the shelf and mesobenthal slope, and Agonidae on the outer shelf. Of families with southern affinities, Sciaenidae (drums and croakers) were important from north-central California through northern Baja California on the inner shelf and middle shelf. Cynoglossidae (tonguefishes) were important from northcentral California to southern Baja California Sur on the shelf, shifting to deeper zones going south. Platyrhinidae (thornbacks) were important on the inner shelf in southern California and Argentinidae (argentines) on the middle shelf of southern California and northern Baja California. Serranidae (sea basses) and Synodontidae (lizardfishes) were important from southern California to southern Baja California Sur on the shelf; the former are restricted to the inner shelf to the north. Uranoscopidae (stargazers) and Moridae (codlings) were important on the mesobenthal slope in northern Baja California. Balistidae (triggerfishes), Congridae (conger eels), Urolophidae (round stingrays), Achiridae (American soles), Gerreidae (mojarras), Haemulidae

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(grunts), and Triglidae (searobins) were important on the shelf from northern to southern Baja California Sur, Balistidae and Achiridae are restricted to the inner shelf. Bothidae (lefteye flounders), Rhinobatidae (guitarfishes), Labridae (wrasses), and Callionymidae (dragonets) were important in these trawl data primarily on the outer shelf off southern Baja California Sur.

DI STR I B UTION OF I M P ORTANT FAM I LI E S AN D S P ECI E S BY R EG ION W ITH I N TH E LI F E ZON E

Inner Shelf

The inner shelf (5–30 m) is the shallowest part of the shelf (fig. 7-2). It is the zone most subject to environmental variability, with seasonally variable changes in water temperature, salinity, productivity, and turbulence; diel variability in light levels; and coastwise variability in sediment type (sandy along exposed coasts and silty along protected coasts). Important soft-bottom fish families and species in this zone vary regionally from northern California to southern Baja California Sur (table 7-2, fig. 7-3). Note that additional species of some families are important shallower than 10 m (see chapter 6), and some species that occur infrequently in this zone were not considered important. The most widespread families (seven regions from northern California to southern Baja California Sur) are Pleuronectidae and Paralichthyidae. Batrachoididae was imporant in six regions from north-central California to southern Baja California Sur. The next most widespread families (five regions) were Embiotocidae (northern California through northern Baja California) and Ophidiidae (important from northern California through northern Baja California Sur, except in south-central California). Other families that were important both north and south of Point Conception included Rajidae, Sciaenidae, and Cynoglossidae (all occur in four regions). Other families were important over more restricted ranges. Families important only in the north included Gadidae and Liparidae (northern California) and Osmeridae, Hexagrammidae, and Cottidae (northern California to south-central California). Families important only in the south include Platyrhinidae (southern California); Synodontidae and Serranidae (southern California through southern Baja California Sur); and Urolophidae, Gerreidae, Haemulidae, Triglidae, Achiridae, and Balistidae (northern and southern Baja California Sur). The most widespread species are the shiner perch (Cymatogaster aggregata), white seaperch (Phanerodon furcatus), speckled sanddab (Citharichthys stigmaeus), and English sole that occur commonly from northern California through northern Baja California (five regions) (table 7-2; fig. 7-3). Different patterns are found among species continuously common in four regions. White croaker and California tonguefish are important from north-central California through northern Baja California. Specklefin midshipman and California halibut are important from the southern California Bight to southern Baja California Sur. Other species (table 7-2) are important over more restricted ranges. Middle Shelf

The middle shelf (30–100 m) is typically the broadest part of the shelf (figs. 7-1 and 7-2). It is less subject to environmental variability than the inner shelf zone and generally lies below the thermocline (except during El Niño events). Compared with the inner shelf, there is less seasonal vari-

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ability in water temperature and salinity, although seasonality in productivity in epipelagic waters affects this zone. Also, there is little turbulence, sediments are generally finer, pressure is greater, oxygen and light levels are lower, and diel variability in light levels is less. Important soft-bottom fish families and species in this zone vary regionally from northern California to southern Baja California Sur (tables 7-2, 7-3; fig. 7-4). The most widespread families (seven regions) were Ophidiidae, Batrachoididae, and Paralichthyidae. Nearly as widespread (six regions) were Rajidae, Scorpaenidae, Cottidae, and Pleuronectidae (northern California through northern Baja California Sur). Families important in five regions were Merlucciidae (northern California through south-central California and northern Baja California Sur), Hexagrammidae (northern California through northern Baja California), and Cynoglossidae (south-central California through southern Baja California Sur). Other families found north and south of Point Conception include Sciaenidae and Embiotocidae (four regions, north-central California through northern Baja California). Families important only in the north include Gadidae (northern California) and Squalidae (three regions; northern through south-central California). Families important only in the south included Argentinidae and Agonidae (two regions; southern California through northern Baja California); Synodontidae (four regions; southern California through southern Baja California Sur); Gerreidae, Haemulidae, and Triglidae (two regions; northern through southern Baja California Sur); and Urolophidae, Congridae, and Bothidae (Baja California Sur). The restricted importance of some families with small species (e.g., Agonidae) from other areas is likely to be a gear-related artifact. The most widespread species on the middle shelf were stripetail rockfish and English sole, occurring in six regions from northern California through northern Baja California Sur (table 7-2; fig. 7-4). Plainfin midshipman, spotted cuskeel (Chilara taylori), longspine combfish (Zaniolepis latipinnis), and roughback sculpin (Chitonotus pugetensis) were important in five regions (northern California through northern Baja California). Species important in four regions included Pacific sanddab (northern California through southern California), white croaker, and pink seaperch (Zalembius rosaceus) (north-central California through northern Baja California). Other species (table 7–2) are important over more restricted ranges. Outer Shelf

The outer shelf (100–200 m) is typically at least partly below the shelf break and hence usually has a steeper slope than the middle shelf (fig. 7-2). In most areas along the coast of the Californias, the outer shelf is narrower than the middle shelf. The water directly over the outer shelf is typically part of the California Counter Current that flows northward. Compared with the outer shelf, sediments are typically finer, and water temperature, oxygen levels, and light levels are lower with virtually no diel variation in ambient light. However, pressure and salinity are higher. Although topographically part of the upper slope where this is below the shelf break, this zone is still strongly influenced by epipelagic productivity. Important soft-bottom fish families and species in the outer shelf zone vary regionally from northern California through southern Baja California Sur (tables 7-2, 7-3; fig. 7-5). Ophidiidae were important in all seven regions. Rajidae,

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TA B L E 7-2

Ecologically Important Soft-Bottom Fishes of the Shelf and Mesobenthal Slope of California and Baja California

California Species

Common Name

Baja California

North

N-Cen

S-Cen

South

NBC

NBCS

SBCS

Shortnose Chimaeras Spotted ratfish

OU

OU

OU

OU

O

—



Dogfish Sharks Spiny dogfish

MO

MO

MO







—

Cat Sharks Brown cat shark

U

U

U

U



—

—

Torpedo Electric Rays Pacific electric ray

O

O

O

O





—

—

—

—







O

—





I







I-MO  U

I-MO  U

I-MO  U

 MO U

 I-MO U

 MO 

—  —











I

I-M

Conger Eels Thicklip conger

—

—

—

—

—

O

M

Argentines Pacific argentine







M

M





Smelts Night smelt

I

I

I

—

—

—

—

Lizardfishes Spotted lizardfish California lizardfish Lance lizardfish

— — —

—  —

—  —

— I-MO —

— I-MO —

— I-MO —

MO  I

Cusk-Eels Black brotula Spotted cusk-eel Finescale cusk-eel Mexican cusk-eel Basketweave cusk-eel

— I-MOU — — —

— I-MOU — — —

— MOU — — 

— MOU — — I

— MO — — I

— O   I-M

U — O M 

U

U

U

U





—









U





— MOU

— MOU

— MOU

 OU

 

 MOU

U 

I-M





—

—

—

—

Chondrichthyes Chimaeriformes Chimaeridae Hydrolagus colliei Squaliformes Squalidae Squalus acanthias Carcharhiniformes Scyliorhinidae Apristurus brunneus Torpediniformes Torpedinidae Torpedo californica Rajiformes Rhinobatidae Zapteryx exasperata Platyrhinidae Platyrhinoidis triseriata Rajidae Raja binoculata Raja inornata Raja rhina Myliobatiformes Urolophidae Urobatis halleri

Cartilaginous Fishes

Actinopterygii Anguilliformes Congridae Chiloconger dentatus Argentiniformes Argentinidae Argentina sialis Salmoniformes Osmeridae Spirinchus starksi Aulopiformes Synodontidae Synodus evermanni Synodus lucioceps Synodus scituliceps Ophidiiformes Ophidiidae Cherublemma emmelas Chilara taylori Lepophidium microlepis Lepophidium stigmatisium Ophidion scrippsae Gadiformes Macrouridae Nezumia stelgidolepis Moridae Physiculus rastrelliger Merlucciidae Merluccius angustimanus Merluccius productus Gadidae Microgadus proximus

Ray-finned Fishes

Guitarfishes Banded guitarfish Thornbacks Thornback Skates Big skate California skate Longnose skate Round Stingrays Round stingray

Grenadiers California grenadier Codlings Hundred-fathom codling Merlucciid Hakes Panama hake Pacific hake Cods Pacific tomcod

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TA B L E 7-2

(continued)

California Species Batrachoidiformes Batrachoididae Porichthys analis Porichthys myriaster Porichthys notatus Scorpaeniformes Scorpaenidae Scorpaena guttata Sebastes caurinus Sebastes chlorostictus Sebastes diploproa Sebastes jordani Sebastes rosenblatti Sebastes saxicola Sebastes semicinctus Sebastolobus alascanus Triglidae Bellator gymnostethus Prionotus ruscarius Prionotus stephanophrys Anoplomatidae Anoplopoma fimbria Hexagrammidae Ophiodon elongatus Zaniolepis frenata Zaniolepis latipinnis Cottidae Chitonotus pugetensis Icelinus filamentosus Icelinus quadriseriatus Leptocottus armatus Radulinus asprellus Agonidae Agonopsis sterletus Bathyagonus pentacanthus Odontopyxis trispinosa Xeneretmus latifrons Xeneretmus ritteri Liparidae Careproctus melanurus Liparis pulchellus Perciformes Serranidae Diplectrum labarum Diplectrum pacificum Paralabrax maculatofasciatus Paralabrax nebulifer Pronotogrammus multifasciatus Serranus aequidens Gerreidae Eucinostomus argenteus Haemulidae Haemulopsis axillaris Orthopristis reddingi Xenistius californiensis Sciaenidae Genyonemus lineatus Seriphus politus Embiotocidae Cymatogaster aggregata Phanerodon furcatus Zalembius rosaceus

Common Name

Toadfishes Darkedge midshipman Specklefin midshipman Plainfin midshipman

North

N-Cen

S-Cen

South

NBC

NBCS

SBCS

— — MO

— — I-MO

— — I-MO

— I MO

— I MO

— I-M O

M I 

 M O U   MO  U

 M O U   MO  U

M   U O O MO  U

M   U  O MO  

 —    O M O 

— — — —  — — — —

— — 

— — 

— — 

— — 

— — I-M

O I-O MO

U

U

U





—

I-MO  M

I-MO O M

 O M

 O M

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Scorpionfishes California scorpionfish — Copper rockfish  Greenspotted rockfish  Splitnose rockfish U Shortbelly rockfish  Greenblotched rockfish — Stripetail rockfish MO Halfbanded rockfish  Shortspine thornyhead U Searobins Nakedbelly searobin — Rough searobin — Lumptail searobin  Sablefishes Sablefish U Greenlings Lingcod I-MO Shortspine combfish  Longspine combfish M Sculpins Roughback sculpin M Threadfin sculpin  Yellowchin sculpin — Pacific staghorn sculpin I Slim sculpin M Poachers Southern spearnose poacher — Bigeye poacher  Pygmy poacher  Blacktip poacher O Stripefin poacher — Snailfishes Blacktail snailfish U Showy snailfish I Sea Basses and Groupers Highfin sand perch Pacific sand perch Spotted sand bass Barred sand bass Threadfin bass Deepwater serrano Mojarras Spotfin mojarra Grunts Yellowstripe grunt Bronzestriped grunt Salema Drums and Croakers White croaker Queenfish Surfperches Shiner perch White seaperch Pink seaperch

Baja California

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TA B L E 7-2

(continued)

California Species Labridae Polylepium cruentum Zoarcidae Lycodes cortezianus Lycodes pacificus Lyconema barbatum Uranoscopidae Kathetostoma averruncus Callionymidae Synchiropus atrilabiatus Pleuronectiformes Bothidae Engyophrys sanctilaurentii Perissias taeniopterus Paralichthyidae Citharichthys gordae Citharichthys sordidus Citharichthys stigmaeus Citharichthys xanthostigma Hippoglossina bollmani Hippoglossina stomata Paralichthys californicus Syacium ovale Xystreurys liolepis Pleuronectidae Atheresthes stomias Eopsetta jordani Glyptocephalus zachirus Isopsetta isolepis Lyopsetta exilis Microstomus pacificus Parophrys vetulus Pleuronichthys decurrens Pleuronichthys ritteri Pleuronichthys verticalis Psettichthys melanostictus Achiridae Achirus mazatlanus Cynoglossidae Symphurus atramentatus Symphurus atricaudus Symphurus oligomerus Tetraodontiformes Balistidae Balistes polylepis

Common Name Wrasses Bleeding wrasse Eelpouts Bigfin eelpout Blackbelly eelpout Bearded eelpout Stargazers Smooth stargazer Dragonets Blacklip dragonet Lefteye Flounders Speckledtail flounder Flag flounder Sand Flounders Mimic sanddab Pacific sanddab Speckled sanddab Longfin sanddab Spotted flounder Bigmouth sole California halibut Oval flounder Fantail sole Righteye Flounders Arrowtooth flounder Petrale sole Rex sole Butter sole Slender sole Dover sole English sole Curlfin sole Spotted turbot Hornyhead turbot Sand sole American Soles Pacific lined sole Tonguefishes Halfspotted tonguefish California tonguefish Whitetail tonguefish Triggerfishes Finescale triggerfish

Baja California

North

N-Cen

S-Cen

South

NBC

NBCS

SBCS

—

—

—

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NOTE: “Ecologically important” species listed here are species that occur frequently on the soft-bottom habitat in a region and which are likely to be the dominant representative of a foraging guild in the region and life zone. Those reported but less important () may occur incidentally in trawl catches beyond the area of most importance. In addition, differences in sampling gear between regions (Northern to south-central California, southern California, northern Baja California to Baja California Sur) may affect the occurrence of species in this table. Also note that a typical trawl survey captures many species from adjoining habitats and hence would include many more species.   not reported;   reported but less important; North  northern California; N-Cen  north-central California; S-Cen  south-central California; South  southern California; NBC  northern Baja California; NBCS  northern Baja California Sur; SBCS  southern Baja California Sur; I  inner shelf; M  middle shelf; O  outer shelf; U  mesobenthal (upper) slope.

Data from California State Water Resources Control Board data (northern and central California); Southern California Coastal Water Research Project data (southern California); Scripps Institution of Oceanography, fiish collection data; and California Cooperative Oceanic Fisheries Investigations data (Baja California). Taxonomic classifiication, scientifiic names, and common names from Nelson et al. (2004

Batrachoididae, Scorpaenidae, Agonidae, and Pleuronectidae were important in six regions, ranging from northern California through northern Baja California Sur. Chimaeridae, Hexagrammidae, Zoarcidae, Merlucciidae, and Embiotocidae were important in five regions. The first three ranged from

northern California through northern Baja California, Merlucciidae from northern California through southern California and in northern Baja California Sur, and Embiotocidae from north-central California through northern Baja California Sur. Families important only in the north C O N T I N E N TA L S H E L F A N D U P P E R S L O P E

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TA B L E 7-3

Ecologically Important Soft-Bottom Fish Families of the Shelf and Mesobenthal Slope of California and Baja California

California

Baja California

Family

North

N-Cen

S-Cen

South

NBC

NBCS

SBCS

Gadidae Osmeridae Squalidae Torpedinidae Liparidae Anoplomatidae Scyliorhinidae Macrouridae Hexagrammidae Chimaeridae Zoarcidae Cottidae Embiotocidae Rajidae Scorpaenidae Agonidae Paralichthyidae Batrachoididae Pleuronectidae Ophidiidae Merlucciidae Sciaenidae Cynoglossidae Platyrhinidae Argentinidae Serranidae Synodontidae Uranoscopidae Moridae Balistidae Achiridae Urolophidae Gerreidae Haemulidae Triglidae Congridae Bothidae Rhinobatidae Labridae Callionymidae

I-M I MO O I-U U U U I-MO OU OU I-M I I-MOU MOU O I-M MO I-MOU I-MOU MOU  

 I MO O U U U U I-MO OU OU I-MO I-MO I-MOU MOU O I-M I-MO I-MOU MOU MOU I-M I-M       

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         M O MO MO O I-MO I-MO I-MO I-MO MOU  MO   I-MO I-MO   I I I I-M I-M I-M O    

   

 

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 I-MO I-M I MOU U  MO   I-MO I-MO   I I I-M I-M I-M I-MO M MO O O O

NOTE : North  northern California; N-Cen  north-central California; S-Cen  south-central California; South  southern California; NBC  northern Baja California; NBCS  northern Baja California Sur; SBCS  southern Baja California Sur. Based on California State Water Resources Control Board data (Northern and Central California); Southern California Coastal Water Research Project data (southern California); Scripps Institution of Oceanography, fiis collection data; and California Cooperative Oceanic Fisheries Investigations data (Baja California).I  inner shelf; M  middle shelf; O  outer shelf; U  mesobenthal slope;   family reported from region;   not reported.

included Squalidae (three regions, northern through southcentral California), Torpedinidae (four regions, northern through southern California), and Cottidae (two regions, north-central and south-central California). Those important only in the south included Paralichthyidae and Synodontidae (four regions, southern California through southern Baja California Sur), Serranidae and Cynoglossidae (two regions, northern and southern Baja California Sur); Congridae (northern Baja California Sur); and Rhinobatidae, Labridae, Callionymidae, and Bothidae (all southern Baja California Sur).

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The most widespread species on the outer shelf (six regions) were spotted cusk-eel, plainfin midshipman, and Dover sole, ranging from northern California to northern Baja California Sur (table 7-2). Species important in five regions include spotted ratfish, stripetail rockfish, slender sole, blacktip poacher, and blackbelly eelpout (Lycodes pacificus) from northern California to northern Baja California; Pacific hake from northern California through southern California and northern Baja California Sur; and pink seaperch from north-central California through northern Baja California Sur. Species important in four regions were Pacific electric ray (northern California through

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F I G U R E 7-3 Soft-bottom fishes representative of the inner shelf in four latitudinal regions off the Californias.

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F I G U R E 7-4 Soft-bottom fishes representative of the middle shelf in four latitudinal regions off the Californias.

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F I G U R E 7-5 Soft-bottom fishes representative of the outer shelf in four latitudinal regions off the Californias.

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southern California) and bigmouth sole (southern California through southern Baja California Sur). Mesobenthal Slope

The mesobenthal slope (200–500 m) typically has a steep slope with fine sediments (fig. 7-2). In most areas along the coast of the Californias, the mesobenthal slope is narrower, but in southern California, it extends as an elongate peninsula from Point Conception to Cortez Bank (with a small gap north of Tanner Bank) as the Santa Rosa-Cortez Ridge. Another broad area of the mesobenthal slope occurs off Baja California Sur. As with the outer shelf, the water over the mesobenthal slope is exposed to the California Counter Current that flows northward. Compared with the outer shelf, pressure is higher, water temperature is lower, oxygen levels approach the oxygen minimum for this area, and ambient light is virtually nonexistent. In contrast to the outer shelf, this zone is less strongly influenced by epipelagic productivity and has fewer small juvenile fish. The distribution of families and species in this zone is less well defined in this study because few data are available from the mesobenthal slope of Baja California (table 7-2, 7-3; fig. 7-6). Merlucciidae was the most widespread family (six regions), important from northern California to southern Baja California Sur, except in northern Baja California. Rajidae, Scorpaenidae, and Pleuronectidae were important in five regions from northern California through northern Baja California. Ophidiidae was also important in five regions but from northern California through southern California and off southern Baja California Sur. Chimaeridae, Scyliorhinidae, Macrouridae, Anoplopomatidae, Liparidae, and Zoarcidae range from northern California through at least southern California. In this limited data set, Pacific hake was important from northern California through southern California and off northern Baja California Sur. Longnose skate (Raja rhina), splitnose rockfish, and slender sole were important from northern California through northern Baja California. Species that were important from northern California through at least southern California included brown cat shark (Apristurus brunneus), spotted ratfish, California grenadier (Nezumia stelgidolepis), spotted cusk-eel, shortspine thornyhead, sablefish, blacktail snailfish (Careproctus melanurus), bigfin eelpout (Lycodes cortezianus), rex sole, and Dover sole. Other species (table 7-2, fig. 7-6) are important over more restricted ranges.

Natural History Traits Soft-bottom fishes are diverse; some species have adaptations specific to the soft-bottom habitat, whereas others have traits that are also found among fishes in other habitats. Some traits are characteristic of taxonomic affiliation rather than specifically of habitat. Examination of the variety of natural history traits found in soft-bottom fishes provides insight into the diversity of lifestyles found in the fauna and their relevance to life in this habitat. Many of these traits are described for individual taxa in taxonomic works (e.g., Jordan and Evermann, 1896–1900, Norman, 1934), life-history compilations (e.g., Hart, 1973; Fitch and Lavenberg, 1968, 1971; Leet et al., 1992, 2001; Love, 1996), and studies on specific species (e.g., Hagerman, 1952; Ford, 1965) or ecological groups of species (e.g., Hobson and Chess, 1976). M. J. Allen (1982a) provides a description of many of these traits of soft-bottom fish com-

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munities on the southern California shelf and their relation to community organization. The following sections describe the variation of natural history traits found in soft-bottom fishes of the Californias. MOR P HOLO G ICAL AT TR I B UTE S

The soft-bottom habitat is generally flat and relatively featureless. Although vast areas are flat with no relief, relief occurs in some areas in the form sand ripples, flat rock outcroppings, excavations made by rays, burrows of infaunal or epifaunal invertebrates, protruding tubes of polychaete or tube anemones, protruding sea pens, and large, well-protected echinoderms (sea urchins, sea cucumbers, sand dollars, sea stars), crustaceans (e.g., crabs), gastropods (e.g., sea slugs, snails), and brachiopods. Benthic fish species adapted for living on this soft-bottom generally can hide in this relatively featureless bottom either by being flat and presenting a profile similar to the bottom or by reducing their visibility (generally during the day) by burrowing in the sediments or living in preexisting fixed burrows. Fishes with flattened bodies are morphologically most specialized for these habitats. There are two basic flattened body morphologies: (1) compressed, laterally asymmetrical species and (2) depressed, laterally symmetrical species. The compressed, laterally asymmetric morphology occurs entirely within the flatfishes, Pleuronectiformes. Although flatfishes are bilaterally symmetrical as larvae, they are asymmetrical after settling to the bottom as juveniles. The body is laterally compressed and the fish lie on their sides with both eyes on the side of the body away from the sediment. Typically, the eyed side has a color typical of the substrate; some species can change colors to match the substrate. The blind side is typically white. Some species also have other asymmetries (e.g., no lateral line on blind side, smaller or no teeth on the eyed side). This morphology is most specialized for the soft-bottom habitat because none (at least on the coast of the Californias) is found predominantly in either hardbottom or water-column habitats. With their flat bodies and cryptic coloration, pleuronectiform fishes are hardly noticeable on the bottom and most bury themselves slightly in the sediments with only the eyes (and perhaps mouth, and gill opening) visible when inactive. Paralichthyidae and Pleuronectidae are found along almost the entire coast of California and Pacific Baja California, whereas Cynoglossidae occur largely from central California south, and Bothidae and Achiridae predominantly south of Bahia Magdalena, Baja California Sur, with stragglers to southern California. Depressed, laterally symmetrical species are dorsoventrally flattened; lateral features are symmetrical in color and form. On the shelf and slope of the Californias, the most extreme forms include Pacific angel shark (Squatina californica), rays (Batoidea: Torpediniformes, Rajiformes, and Myliobatiformes), and lophiiform (e.g., Lophiidae [goosefishes]; Ogcocephalidae [batfishes], found predominantly off southern Baja California). Batoid fishes are depressed (flattened dorsoventrally), with flattened heads and bodies; eyes are on the dorsal body, the mouth on the ventral side, and small gill openings (spiracles) on the dorsal side behind the eyes. Some roundfish species that bury in sediments have flattened dorsal surfaces to match the profile of the soft bottom (Uranoscopidae, Batrachoididae, some Cottidae). These morphologies are found primarily on soft bottoms. Other morphologies found on soft-bottoms (e.g., eel-like and tadpole-shaped species) are also found in hard-bottom habi-

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F I G U R E 7-6 Soft-bottom fishes representative of the upper (mesobenthal) slope in two latitudinal regions off the Californias.

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tats. White body coloration is typical of inner shelf watercolumn species that live on soft bottoms (e.g., white croaker; queenfish, Seriphus politus; shiner perch; and white seaperch. Benthic soft-bottom species typically have rather plain brownish bodies with some spotting. R E F UG E

Unlike the hard bottom, the soft bottom provides little cover for fishes during their periods of inactivity (at night for diurnal species or during the day for nocturnal species). Major soft-bottom community members on the southern California shelf find refuge in four ways: (1) by burial or burrowing in sediments, (2) exposed on the bottom, (3) in schools, and (4) in crevices where such cover occurs (M. J. Allen, 1982a). Of 40 major species comprising the soft-bottom fish community of the Southern California shelf, 42% burrow into sediments, 38% are exposed on the bottom, 10% are in schools, and 10% are in crevices (M. J. Allen, 1982a). Burial or Burrowing

Generalizing beyond M. J. Allen (1982a), which focused on individual species, soft-bottom fishes that bury themselves in the sediments have distinct body shapes adapted to hiding in the sediments. They typically bury themselves by wiggling their bodies until they gradually sink into the sediment. The body shapes of these fishes are often characteristic of families and orders. This group includes (1) flattened fishes, (2) benthic roundfishes with subcircular or triangular cross sections (with dorsal, ventral, or both sides depressed), and (3) eel-like fishes. Flattened fishes include those that are depressed (dorsoventrally flattened) such as Rajiformes, Pacific angel shark, and lophiids, as well as those that are laterally compressed and lie on their sides (Pleuronectiformes). Some benthic roundfishes, such as uranoscopids and batrachoidids are dorsally depressed. Others, such as most synodonitids and triglids have partly depressed cross sections. Some small cylindrical fishes hide in fixed burrows of infaunal invertebrates (e.g., bay goby, Lepidogobius lepidus; Grossman, 1979) or protruding polychaete tubes (e.g., orangethroat pikeblenny, Chaenopsis alepidota; Thomson et al., 2000). Eel-like fishes found on soft bottoms typically burrow backward into the sediment using their pointed tails (usually the dorsal, caudal, and anal fins are confluent). This group includes Myxinidae (hagfishes), Congridae, Ophichthidae (snake eels), Ophidiidae, and Zoarcidae. Exposed in Open

Many species stay in the open when inactive, either relying on spines or armor for protection or are difficult to find at night. Species with spines include the spotted ratfish, combfishes (Zaniolepis), nonschooling rockfishes (Sebastes), thornyheads (Sebastolobus), and scorpionfishes (Scorpaena). Some of these taxa, and in particular, the scorpionfishes, have venomous spines. Agonids may get some protection from their armored bodies. Other species, such as soft-bottom embiotocids (e.g., shiner perch, white seaperch, pink seaperch), lie on the bottom in the open at night, although individuals are solitary at this time (Bray and Ebeling, 1975; Ebeling and Bray, 1976; M. J. Allen, 1982a). Shiner perch school during the day when feeding but lie exposed on the bottom at night (Stephens and Zerba, 1981).

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S O F T S U B S T R A TA A N D A S S O C I A T E D F I S H E S

Schooling

Schooling species include those that school as a lifestyle and those that school during part of the day. Many of the coastal pelagic species that occur over soft bottoms of the shelf and slope probably school when feeding or inactive. These include neritic-mesopelagic species such as Pacific hake and neritic-epipelagic species such as northern anchovy (Engraulis mordax), as well as neritic species such as shortbelly rockfish. Pacific hake schools can extend continuously for up to 19 km (Quirollo et al., 2001). Some nocturnal species (e.g., white croaker; queenfish; and walleye surfperch, Hyperprosopon argenteum) in nearshore soft-bottom areas form standing schools during the day and presumably break up into smaller groups or schools at night (M. J. Allen, 1982a). Crevices

Some species caught on soft bottoms may typically find refuge in crevices on hard bottoms. Some of these species may leave the soft bottom at night or may find crevices in a low relief hard bottom or under shells or other objects on a soft bottom. These species are mostly incidental to the soft-bottom habitat but make up a large number of the species taken in trawl surveys. These include many species of Scorpaenidae and Cottidae, as well as occasional Bathymasteridae (ronquils) or Stichaeidae (pricklebacks).

R E P RODUCTIVE MODE S, LI F E H I STO RY STRATEG I E S, AN D R ECR U ITM E NT

Reproductive Modes

The reproductive mode of a species often determines its habitat needs, dispersal abilities, conditions affecting early survival, and recruitment strength (M. J. Allen, 1982a). Differences in reproductive mode are generally associated with differences in higher taxa (Breder and Rosen, 1966; Balon, 1975); species of different families or genera generally have similar strategies. Of particular importance here, are the locations of the zygote and the developing embryo or larva. Zygotes can be either internal or as pelagic or demersal eggs. Developing embryos are maintained internally in some species or are released or hatched as larvae (pelagic, sometimes benthopelagic or benthic). Where maintained internally, the young are released as juveniles. On the southern California shelf, M. J. Allen (1982a) found that 45% of the 40 major community members had pelagic eggs and larvae, 18% (all rockfishes) were ovoviviparous with pelagic larvae, 15% (e.g., combfishes, Cottidae, Agonidae) had demersal eggs and pelagic larvae, 12% (all Embiotocidae) were viviparous (livebearers), and 10% (e.g., Batrachoididae, Zoarcidae) had demersal eggs and larvae. Spotted ratfish and some elasmobranchs (e.g., Scyliorhinidae; Heterodontidae [bullhead sharks]; Rajidae) lay eggs with keratinous shells, which hatch small juveniles. Other sharks and rays are viviparous. Bythitidae (viviparous brotulids), such as red brotula (Brosmophycis marginata) and rubynose brotula (Cataetyx rubrirostris), are ovoviviparous. Species with pelagic larvae and/or eggs generally have the best dispersal abilities at this stage, whereas those with demersal eggs and larvae or juveniles have the least, and subadults and adults have the best ability to disperse.

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Life-History Strategies

Species differ in their natural life spans and lifetime reproductive output. For a species to survive, its life span and reproductive output must be such that, on average, each individual replaces itself during its lifetime (or a female replaces two individuals). If this rate is maintained, populations remain stable. If more individuals than this survive, the population grows; if fewer, it declines. Thus, it is reasonable to assume that a shortlived species has fewer years to replace itself than a long-lived species, and hence, must have better short-term repopulation capabilities than a long-lived species. For instance, a speckled sanddab that lives for 3 or 4 years has to do this within this time frame, whereas a rockfish, which lives up to 80 years and produces thousands of larvae each year after reaching maturity, is very poor at doing this and needs a long life to get a successful replacement. Given a narrow shelf off the coast of the Californias and strong upwelling along the central and northern California Coast with offshore transport of surface water, pelagic larvae are likely to be carried offshore and away from a suitable habitat for settlement. Species that settle in relatively shallow water (e.g., California halibut, fantail sole, hornyhead turbot) spend less time in the water column (29 days for California halibut; L. G. Allen, 1988) and settle out at very small sizes (e.g., 10 mm for California halibut) (Kramer, 1990). This strategy reduces the likelihood of drifting offshore of shallow settlement habitat. In contrast, long-lived pelagic larvae which settle more deeply are found among many species common on the outer shelf (e.g., Dover sole, slender sole, rex sole, and some rockfishes; Pearcy et al., 1977; Richardson and Pearcy, 1977; Charter and Moser, 1996b). Dover sole can remain in the water column for up to 2 years before settling (Markle et al., 1992). Some species characteristic of the inner and middle shelf (e.g., speckled sanddab, Pacific sanddab, California tonguefish) tend to settle at intermediate sizes (Kramer, 1990; Moser and Charter, 1996; Charter and Moser, 1996a).

Recruitment

Species on the edge of their geographic ranges recruit more sporadically than those near the middle of the ranges (Andrewartha and Birch, 1954). Southern California is at the edge of the range of many cool- and warm-water species. Recruitment of small juveniles (young of the year) of southern California demersal fishes is episodic, strong in some years and weak in others, and is species-specific (Mearns, 1979; Mearns et al., 1980). From 1969 to 1978, recruitment was particularly high in 1975 (comprising 50% of the total catch) and represented 20 species; it was particularly low in 1972, 1974, and 1976 (Mearns, 1979). Variability in recruitment of stripetail rockfish and calico rockfish (Sebastes dallii) was the main source of variability in rockfish abundance in southern California trawl catches (Mearns et al., 1980). Sherwood and Mearns (1981) found that 15% of the fishes caught by trawl on the soft bottom of the southern California shelf from 1972 to 1977 were less than 60 mm SL. Of these, juveniles of speckled sanddab and stripetail rockfish were most abundant. In contrast, during the warm years of the 1990s, juveniles of both species occurred only in low abundance on the southern California shelf (M. J. Allen et al., 1998, 2002). During the 1997–1998 El Niño, four species of soft-bottom fishes previously not reported north of Baja California Sur were collected in southern California or just south of the border (M. J. Allen and Groce, 2001a,b; Groce et al., 2001a,b).

Most recent studies of settlement and early recruitment have been conducted on the inner part of the inner shelf (
15 m depth). In the late 1980s, a number of studies assessed settlement of juvenile California halibut in this zone and in enclosed embayments of Southern California using small nets (beam trawls or otter trawls) with fine mesh (L. G. Allen, 1988; L. G. Allen et al., 1990; M. J. Allen and Herbinson, 1990, 1991; Kramer, 1990, 1991; Kramer and SWFSC, 1990; L. G. Allen and Franklin, 1992). M. J. Allen and Kramer (1991) provide a review of the factors influencing the settlement of California halibut. Coastal settlement is more variable than that in bays; interannual variation probably is largely due to oceanic conditions (advection, upwelling) that affect transport and survival of larvae, along with successful spawning and availability of suitable benthic conditions for settling juveniles. M. J. Allen and Herbinson (1991) compared settlement of all fish species collected by fine-mesh (2.5 mm) beam trawls on the inner shelf and embayments in southern California in 1989. In 288 samples, 72 species representing 31 families were collected; these were dominated by newly transformed (10–15 mm) fish. Fish densities were higher in the bays than on the coast, decreased with increasing depth on the coast, and were highest in May. On the inner shelf, speckled sanddab was the most frequent species, but queenfish was most abundant.

MOB I LIT Y, MOVE M E NTS, AN D M IG RATION S

Mobility

Fish mobility is generally related to size, morphology, and habitat. Larger fishes are more likely to move further than small fishes; those with more fusiform bodies with swimbladders are more likely to move further than those with short depressed bodies without swimbladders. Pelagic species without fixed habitat sites are more likely to move great distances than rocky bottom species which use crevices for refuge. Among soft-bottom fishes, flatfishes and cusk-eels that bury in sediments wherever they need to find refuge are likely to move more than species (e.g., bay goby) that find refuge in fixed burrows. Soft-bottom fishes vary in mobility, ranging from species that conduct large-scale coastwise migrations, cross-shelf bathymetric migrations, and vertical migrations in the water column to sedentary species that do not move large distances during their postlarval lives. Migrations can be coastwise, bathymetric (along the bottom), or vertical (in the water column). Movements have been most studied for fisheries species; little information on movements exist for most nonfisheries species. Coastwise Migrations and Movements

Pelagic or neritic schooling species, as well as large benthopelagic and benthic species, move great distances. Pacific hake, a neritic-mesopelagic species (M. J. Allen and Smith, 1988) migrates up to 1800 km from pelagic spawning areas off southern California to British Columbia during spring and summer, moving along the upper slope and continental shelf of central and northern California (Bailey et al., 1982; Quirollo et al., 2001). Mature fish return to spawning grounds offshore of southern California and Baja California, moving at a rate of 5–11 km per day (Bailey et al., 1982). Sablefish, a benthopelagic species of the shelf and slope, generally moves less than 50 km, but some individuals have moved as far as 4400 km during 6 years from the Bering Sea to San Francisco (Sasaki, 1985).

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Dover sole can move up to 680 km (Westerheim and Morgan, 1963). Bathymetric Migrations and Movements

Bathymetric movements across the shelf and/or slope occur seasonally in some species and ontogenetically in other species. Seasonal migrations from shelf to slope depths occur in middle and outer shelf species. For example, Dover sole moves inshore to depths of 55 m for feeding during the summer and offshore to depths of 550 m during the winter for spawning (Garrison and Miller, 1982; Hirschberger and Smith, 1983). Ontogenetic movements from shallow to deep water occur for many species; juveniles occur in shallow water and adults in deeper water (e.g., California halibut; sablefish; bocaccio, Sebastes paucispinis; English sole). Splitnose rockfish make a distinct ontogenetic migration from surface waters near kelp patties as small juveniles to the outer shelf and mesobenthal slope depths as subadults and adults (Boehlert, 1977). California scorpionfish undertake spawning migrations of up to 42 km to traditional deepwater spawning sites during May through August (Love et al., 1987). Some species (e.g., Pacific hake; Quirollo et al., 2001) undertake diel vertical migrations, moving higher in the water column at night and lower in the water column during the day. These migrations are usually associated with feeding and are related to similar migrations of prey organisms such as euphausiids. The plainfin midshipman undertakes a similar migration. However, it is buried in the mud during the day (swimbladder deflated), rises into the water column at night after inflating the swimbladder at dusk, and returns to the bottom again, deflating the swimbladder at dawn (Ibara, 1970). Local Movements

California halibut, a large benthic species, general moves less than 13 km but can move up to 365 km (Domeier and Chun, 1995). Smaller species are more localized, moving from
100 m to several kilometers in their lives. Very small benthic species (e.g., cottids, agonids, zoarcids, and Gobiidae [gobies]) are likely to be more sedentary due to their size and/or lack of swimbladders, but the mobility of these species is generally not studied because they lack importance to fisheries. DI E L B E HAVIOR

As with fishes on other shelf habitats, the diel activity of softbottom fishes falls into one of four general types: diurnal, nocturnal, crepuscular (dawn and dusk), or no clear diel behavior (Hobson, 1965, 1968; Hobson and Chess, 1976; Hobson et al., 1981). Diel activity patterns are likely to be better developed at shallow depths, where there is a greater difference in ambient light levels between day and night. With increasing depth, diel differences in ambient light levels decrease to very little by 200 m in coastal waters (Clarke and Denton, 1962), and hence diel behavior may be less well-defined. I have observed spotted cusk-eel, commonly nocturnal in shallow water, actively foraging during the day in deeper waters of the shelf. Further, nocturnally active fishes may be more active in shallow water during the day when conditions are turbid. Bioluminescence in nocturnal, vertically migrating, mesopelagic organisms that move over the shelf at night may nevertheless result in deepwater species that focus on one time period or another.

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Nocturnal species often have larger eyes and/or obvious nonvisual sense organs (e.g., barbels, enlarged olfactory organs, more elaborate lateral line systems, electroreceptive organs) than diurnal species at the same depth. Hobson and Chess (1976) note that nocturnal planktivores have larger eyes and mouths than diurnal planktivores. Some direct observation of nocturnal activities of pelagic fishes occurring over soft bottoms have also been made (L. G. Allen and DeMartini, 1983) (see chapter 6). Of 40 major species in soft-bottom fish communities on the Southern California shelf at depths of 10–200m, M. J. Allen (1982a) surmised (based on literature, sensory morphology, diet, and/or some direct observation) that 32% were predominantly or probably diurnal, 25% were predominantly or probably nocturnal, and 42% had no discernible or predictable diel pattern. Species comprising shallow recurrent groups had distinct differences in diel behavior, but those comprising deeper groups generally had some species with no obvious patterns. However, diel differences in behavior extended at least as deep as the outer shelf. Some families of soft-bottom fishes in this study were characteristically of one type or another. Ophidiidae, Batrachoididae, Sciaenidae, and Cynoglossidae were nocturnally active; Hexagrammidae were diurnally active; Cottidae and Agonidae had no obvious pattern; and Embiotocidae, Scorpaenidae, Paralichthyidae, and Pleuronectidae had species representing more than one pattern.

F E E DI NG AN D FORAG I NG

Diet

Species with commercial or recreational importance often have had extensive studies of stomach analysis sometimes from California waters and sometimes from areas to the north (e.g., Conway, 1967; Jones and Geen, 1977; Kravitz et al., 1977; Pearcy and Hancock, 1978; Gabriel and Pearcy, 1981), but feeding studies of less important species are more limited (e.g., Luckinbill, 1969; Ware, 1979; Murillo et al., 1998). A difficulty in comparing diet studies results from inconsistencies in the way data were analyzed (e.g., number of prey individuals, volume or biomass, frequency of occurrence, index of relative importance). The same set of stomachs of a species can give very different assessments of diet if number of prey, prey volume, or frequency of occurrence are examined alone. The Index of Relative Importance (IRI) (Pinkas et al., 1971) combines the three variables into a single index. Percent IRI provides a useful means of comparing diets of different species (M. J. Allen, 1982a). Few studies have focused on feeding habits of the softbottom fish community as a whole. M. J. Allen (1982a) examined 1018 stomachs of the 40 most common soft-bottom species on the southern California shelf; these contained 461 prey species, representing 218 families, and 31 classes. Crustacea were the most important class of prey and were found in all species. These were followed by Polychaeta and Actinopterygii (ray-finned fishes), both occurring in 65% of the fish species. Of the crustacea, gammaridean amphipods were consumed by all species, calanoid copepods and reptantian decapods (crabs) each occurred in 68% of the species. Noteworthy was the near absence of gastropods and isopods in the diets of these fishes. Most of the prey were species that were active on or just above the sediments but could be found in either location.

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Many fishes undergo ontogenetic diet changes. Coastal pelagic and neritic fishes over the soft bottom typically feed on calanoid copepods when small, shift to euphausiids (over the middle shelf to mesobenthal bottom) or mysids (on the inner shelf) at moderate sizes, and to fish and squid when large. Some species never get beyond one of these stages: shiner perch feed primarily on calanoid copepods on the shelf, never growing larger. Stripetail rockfish and shortbelly rockfish (residents of the middle and outer shelf) feed on euphausiids when larger than the calanoid-feeding stage, whereas queenfish feed primarily on mysids at night over the inner shelf. Larger species (e.g., bocaccio, Pacific hake, California halibut) can grow beyond the euphausiid/mysid stage to feed on fish and sometimes squid. Similarly, among larger species feeding on benthopelagic prey (e.g., greenblotched rockfish, Sebastes rosenblatti; California scorpionfish), the sequence is typically gammaridean amphipods when small; amphipods and decapod crustaceans (shrimp, crabs) at moderate sizes; and decapods, fish, and octopus when large. This sequence of dietary change also occurs in Rajidae (Orlov, 1998). Small species (e.g., yellowchin sculpin) or small-mouthed species (e.g., pink seaperch, white seaperch) remain at the gammaridean amphipod level. Moderate sized species (white croaker) or small species with moderate sized mouths (e.g., roughback sculpin) feed primarily on amphipods and decapods. Some species (e.g., white croaker, Ware, 1979; benthopelagic rockfishes) feed on calanoid copepods in the water column before making a transition to feeding on gammarideans on the bottom. Infaunal feeders show less of a change in diet to higher taxonomic levels as they grow. Smaller individuals feed on smaller polychaetes, larger individuals on larger polychaetes and small clam siphons, and larger species include larger clam siphons. The size transitions discussed above were noted in fish collected with the small (7.6-m headrope) otter trawls used in southern California. Some species with adaptations for crushing hard shells (e.g., bat ray, Myliobatis californica) feed on whole clams. Because small species and smaller individuals of larger species are not so well represented in catches of larger trawls used in NMFS surveys, the general diet patterns are euphausiids to fish and squid for pelagic feeders; decapods, fish, and octopus for benthopelagic feeders; and polychaetes and clams for some infaunal feeders. Foraging Behavior

Foraging behavior generally determines what a species eats. Foraging behavior is often reflected in the morphology of a fish because the morphology creates constraints on behavior. M. J. Allen (1982a) examined the morphology and diet of 40 soft-bottom species on the southern California shelf and using additional information from underwater videos or photographs and the literature, described inferred foraging behavior of these species. Fishes were first classified into roundfishes and flatfishes (M. J. Allen, 1982a). Roundfishes were further divided into those with swimbladders and without, and then further classed by mouth type (superior, terminal, and inferior). Flatfishes were sorted into those with symmetrical mouths (same size and tooth development on eyed and blind side of head) and those with asymmetrical mouths (larger mouth and better tooth development on blind side). Roundfishes with swimbladders could forage either in the water column or more widely over the bottom than fishes without swimbladders. The latter, however, were likely to be able to forage more thor-

oughly in small areas of the bottom or were ambushers of nektonic prey. Roundfishes with superior mouths fed on pelagic prey (calanoid copepods, euphausiids, mysids) or nektonic benthopelagic prey, presumably capturing them in the water column. Some benthic species with superior mouths (e.g., smooth stargazer, Kathetostoma averruncus) ambush nektonic prey swimming near the bottom. Those with terminal mouths generally ate nektonic and benthic prey, whereas those with inferior mouths generally ate benthic prey. Among flatfishes with symmetrical mouths, those with large mouths feed predominantly on nektonic prey and those with medium-sized mouths were generalists, feeding on both nektonic and benthic prey. Flatfishes with asymmetrical mouths feed primarily on infaunal prey (polychaetes and clam siphons). Sense organ development also provides information on the way a fish forages. Large eyes relative to confamilial species (e.g., among surfperches) indicate nocturnal feeding, whereas small eyes indicate diurnal feeding (M. J. Allen, 1982a). Among the pelagic planktivores of the inner shelf, nocturnal feeders have large eyes and small mouths, whereas diurnal feeders have small eyes and small mouths (Hobson and Chess, 1976). Within the depth range of the shelf and mesobenthal slope, eye size sometimes increases in confamilial species occupying different bathymetric zones. For instance, eye size is small in the pygmy poacher (Odontopyxis trispinosa), a resident of the middle shelf, but large in the blacktip poacher, a resident of the outer shelf (M. J. Allen, 1982a), and larger in the bigeye poacher (Bathyagonus pentacanthus) of the mesobenthal slope. Increased development of other sense organs often indicates feeding in low light levels (at night or in deepwater). Midshipmen (Porichthys spp.) have well-developed lateral line systems and small eyes; they are nocturnally active and feed on euphausiids or mysids in the water column, which they locate with the lateral line system (Ibara, 1967, 1970; M. J. Allen, 1982a). Rex sole has an enlarged cephalic lateral line system on the blind side of the head, covered by skin and with no lateral line pores. M. J. Allen (1982a) surmised that this may function like a stethoscope for detecting vibrations of burrowing infauna. Interestingly, this species is closely associated with the northern heart urchin (Brisaster latifrons), which burrows beneath sediments (M. J. Allen et al., 2002). Ampullae of Lorenzini (electroreceptive organs) allow Rajidae and Rhinobatidae to detect infaunal prey and benthic fishes on the bottom at night. Barbels (fleshy appendages on the snout or lower head) found in some sciaenids, agonids, and zoarcids (e.g., bearded eelpout, Lyconema barbatum) and modified fin rays (pelvic in Ophidiidae, pectoral in Triglidae) are used tactilely to locate prey on the bottom at night or, as with Triglidae, buried in the sand during the day. Sometimes, these or other parts of the body likely to be used in foraging on the bottom are covered with taste buds or chemosensory spindle cells. Tonguefishes (Cynoglossidae) have very small eyes but have enlarged olfactory organs, as well as taste buds on the blind side of the head for locating prey on the bottom at night (M. J. Allen, 1982a). Other aspects of foraging behavior are also related to the morphology of a species. Of species of similar body morphology and size, those with larger mouths generally eat larger prey than those with small mouths. For instance, roughback sculpin often co-occurs with yellowchin sculpin on the soft-bottom middle shelf of Southern California. Although it grows larger than the yellowchin sculpin, it has a larger mouth when the two are the same size, and eats larger prey (M. J. Allen, 1982a).

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Four general types of foraging behavior are common among soft-bottom fishes in southern California: (1) ambushers, (2) searchers, (3) pursuers, and (4) stalkers (M. J. Allen, 1982a). Ambushers expend relatively little energy searching for prey, relying on prey passing by their location. Searchers typically expend much effort locating prey, which once found are not likely to escape. Pursuers typically chase prey that enters their field of vision. Stalkers combine searching and ambushing or pursuing behaviors, expending energy searching for prey that once located, is likely to escape. Soft-bottom fishes have four major behaviors with regard to the degree to which they forage in the water column or on the bottom (M. J. Allen, 1982a). Different species feed (1) entirely in the water-column, (2) mostly in the water column with some benthic foraging, (3) mostly on the bottom with some water column foraging, and (4) entirely on the bottom. The behavior of these species can be inferred from morphological characters and diet. Both water-column species with swim bladders and benthic species without swimbladders have species representing all four of these categories. Species that live in the water column and feed on prey in the water column typically have superior mouths, whereas those doing this from the bottom typically have large symmetrical mouths. Water-column species that feed on the bottom typically have inferior or terminal mouths; benthic species doing this have inferior mouths (roundfishes) or asymmetrical mouths (flatfishes). Species that feed in both areas tend to have generalized terminal mouths. Prey behavior can also provide insight into the foraging zone of a fish species (M. J. Allen, 1982a). Prey can be classified by its potential for being captured in the water column (e.g., calanoid copepods), on the bottom (crabs), and whether it is sessile (tubicolous polychaetes) or buried (clams). Though some prey, such as those mentioned, are good indicators of the location of prey capture, most crustaceans (e.g., gammaridean amphipods, shrimp, etc.) are not because they can be taken in a variety of locations (e.g., in the water column, on the bottom, buried, or sometimes in tubes). The use of indicator prey along with the morphology of a fish provides good insight into the probable foraging zone of the fish.

Ecological Segregation As with other organisms, fish communities can be viewed from a large-scale perspective and a small-scale perspective (M. J. Allen, 1982a,b). The large-scale perspective (biogeographic community) consists of species that live together over a large geographic area and probably represent historical associations. A small-scale perspective (local assemblage) consists of whatever species live together and interact with each other at a given location. It includes some or all of the biogeographic community members plus a number of incidental species with centers of distribution in other biogeographic communities in different biogeographic provinces, life zones, or habitats. Ecological segregation among biogeographic community members is more likely to be the result of coevolution because these species have lived together and have interacted with each other over a large area and a long time. Ecological segregation among species in the local assemblage may in part reflect this among its biogeographic community members; however, differences or lack of difference of many species in the local assemblage may be due to the chance occurrence of species at a given time or location that have evolved in differ-

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ent biogeographic communities in different places. The following discussion of the functional organization of species is based on this biogeographic community concept (i.e., that ecological segregation among species in a biogeographic community is due to coevolution of the species in the community rather than due to chance). F U NCTIONAL ORGAN I ZATION OF C OM M U N ITI E S ON TH E SOUTH E R N CA LI FOR N I A S H E LF

M. J. Allen (1982a) used a synthetic approach, beginning with recurrent group analysis and using information on depth distributions, relative abundance, diet and morphological data collected in the study, as well as behavioral information from the literature, to describe the functional organization of the soft-bottom fish communities of the southern California shelf (10–200 m) based on data from 1972–1973. Recurrent groups were generally associated with different depth zones (a major group is in each of the three shelf life zones). Species that were most similar occurred in different recurrent groups at different depths. Recurrent groups contained species that were dissimilar in morphology. Morphological differences were associated with feeding and foraging. The basic difference among species that occurred together most frequently over a large area was orientation to the bottom. Based on this as a point of organization, the 40 most common species were classified into 18 foraging guilds (15 major guilds with one guild divided into four size classes) (fig. 7-7). Fish were classified into water-column and benthic lifestyles, and within these categories, species were classed according to whether they foraged in the water column (pelagivores) or on the bottom (benthivores), with two intermediate foraging zones (mostly water column, some on bottom—pelagobenthivores; mostly bottom, with some in water column—benthopelagivores). All four orientations occurred among both water-column and benthic fishes found near the seafloor on the soft bottom. Some of these orientations were further broken down by refuge mode (e.g., schooling, bottom refuge), sensory differences (e.g., visual, nonvisual), and behavior (e.g., pursuing, ambushing, extracting, excavating). In one guild (benthic ambushing benthopelagivores), ecological segregation appeared to be related to mouth size; up to four different species with nonoverlapping mouth sizes forage similarly on the soft bottom within a given life zone. Species within the same guild were sometimes morphologically similar because they are congeners (e.g., specklefin midshipman, plainfin midshipman), but some were similar due to convergence (e.g., queenfish and shortbelly rockfish or Pacific sanddab and slender sole). Some guilds, however, included species that were not morphologically similar (e.g., bigmouth sole and California lizardfish). Species comprising a guild were generally segregated by depth; two to four species (depending on the guild) form a depth-displacement series across the shelf (M. J. Allen, 1982a). Depth displacement was best identified by shifts in the relative abundance of guild members with depth. Overlap zones existed where displacing species coexisted. A set of depth-displacing patterns for each guild was arranged to describe the functional structure and species composition of the communities (fig. 7-8). The functional structure was described in terms of the number and type of feeding guilds at a given depth and the species composition in terms of the dominant species of each guild at a given depth. Dominant species in each guild in 1972–1973 were as follows: (1) schooling (neritic) pelagivores—queenfish (inner shelf)

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F I G U R E 7-7 Foraging guilds of soft-bottom fishes on the southern California shelf (from M. J. Allen, 1982a).

and shortbelly rockfish (middle and outer shelf); (2) bottomrefuge visual pelagivores—stripetail rockfish (middle and outer shelf); (3) bottom-refuge nonvisual pelagivores—specklefin midshipman (inner shelf) and plainfin midshipman (middle and outer shelf); (4) midwater pelagobenthivores—shiner perch (inner and middle shelf); (5) cruising pelagobenthivores—sablefish (outer shelf); (6) cruising diurnal benthopelagivores—white seaperch (inner shelf) and pink seaperch (middle and outer shelf); (7) cruising nocturnal benthopelagivores—white croaker (inner and middle shelf); (8) cruising nonvisual benthivore— spotted cusk-eel (middle and outer shelf) [Note that basketweave cusk-eel should be the inner shelf dominant of this guild, but because of daytime trawling, this nocturnal species was not common in the catches.]; (9) benthic pelagivores— California lizardfish (inner shelf) and bigmouth sole (middle and outer shelf); (10) benthic pelagobenthivores—speckled sanddab (inner shelf), Pacific sanddab (middle shelf), and slender sole (outer shelf); (11) benthic pursuing benthopelagivores—longspine combfish (middle shelf) and shortspine combfish (outer shelf); (12) tiny benthic sedentary benthopelagivores—pygmy poacher (middle shelf) and juvenile blacktip poacher (outer shelf); (13) small benthic sedentary benthopelagivores—yellowchin sculpin (inner and middle shelf) and adult blacktip poacher (outer shelf); (14) medium benthic sedentary benthopelagivores—fantail sole (inner shelf), roughback sculpin (middle shelf), and juvenile greenblotched rockfish (outer shelf); (15) large benthic ambushing benthopelagivores—California scorpionfish (inner and middle shelf) and adult greenblotched rockfish (outer shelf); (16) benthic extracting benthivores—hornyhead turbot (inner shelf), curlfin sole (Pleuronichthys decurrens) (northern inner shelf), and Dover sole (middle and outer shelf); (17) benthic excavating benthivores— English sole (inner and middle shelf) and blackbelly eelpout (outer shelf); and (18) benthic nonvisual benthivores — California tonguefish (inner and middle shelf) and rex sole

(outer shelf). Depth-displacing members of these guilds are considered ecological counterparts; each performs a similar role within its community relative to other community members. Examination of the pattern of shifts in dominant guild members and overall occurrence of guilds identified three major faunal breaks within the shelf (M.J. Allen, 1982a). The primary break was at 80 m (roughly the depth of the shelf break along the central shelf of southern California), and 50% of the guilds showed changes there. The next most important break was at 170 m (44% of the guilds showed changes), followed by 20 m (39% showed changes). These breaks separated the shelf into three zones: inner shelf; middle shelf; and outer shelf (the latter two zones were called outer shelf and upper slope in M.J. Allen, 1982a, but as noted above, the terms inner shelf, middle shelf, and outer shelf are more appropriate). In terms of relative abundance, generalists (pelagobenthivores) dominated the community on the inner and middle shelf, and specialists (pelagivores and benthivores) were more important on the outer shelf. This model of the organization of soft-bottom fish communities of the southern California shelf was examined again in two recent surveys of the southern California shelf (10–200 m): the mainland shelf in 1994 (M. J. Allen et al., 1998) and the mainland shelf and islands in 1998 (M. J. Allen et al., 2002). This provided a perspective on the functional organization of the community in three time periods: (1) cold regime (1972–1973), (2) warm regime (1994), and (3) El Niño (1997–1998) (M.J. Allen et al., 2002). The overall pattern of the guilds and their dominant species were similar, and in particular, the sequence of depth-displacing species within a guild. However, different guilds showed different responses to the warming conditions in later years, particularly in 1998. Minor guilds (e.g., water-column pelagivores) were less widespread. Among dominant members of a guild, some shallow dominant species expanded their depth range into deeper water, but others retreated from shallow water. Some middle shelf species expanded onto the outer

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F I G U R E 7-8 Functional structure of soft-bottom fish communities of the southern California shelf in 1972–1973 (modified from M. J. Allen, 1982a).

shelf in 1998, and some outer shelf species retreated deeper on the outer shelf to the mesobenthal slope. In some cases, a southerly guild member (not normally a dominant) intruded into the expected depth-displacing series. For example, the bottom-living pelagivore guild typically consisted of the speckled sanddab (inner shelf), Pacific sanddab (middle shelf), and slender sole (outer shelf). In 1998, the longfin sanddab became a dominant in the inner part of the middle shelf between the speckled sanddab and the Pacific sanddab. The Pacific sanddab expanded its zone of dominance to the inner part of the outer shelf. Also, since the 1970s, some cold-water species were replaced by warm-water species across the shelf; however, some guild dominants virtually disappeared during this period but were not replaced, suggesting an open niche. Bottom-living pelagobenthivores (sanddab guild), bottomliving extracting benthivores (turbot guild), and bottom-living pelagivores (lizardfish/halibut guild) were the most widespread guilds on the mainland shelf in both 1994 and 1998

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(M. J. Allen et al., 1998, 2002). In 1994, the sanddab guild occurred in 96% of the samples, the turbot guild in 92%, and the lizardfish/halibut guild in 75%. In 1998, the lizardfish/halibut guild was most widespread (75%) when islands and mainland were combined but was second (87%), following the sanddab guild (93%), but above the turbot guild (80%). Others showed decreasing levels of occurrence, and nonvisual benthivores (tonguefish guild) were next in occurrence. Water column pelagobenthivores and water-column benthivores had the lowest frequency of occurrence in these surveys. S PATIAL S E G R EGATION OF D OM I NANT S P ECI E S W ITH I N S E LECTE D FORAG I NG G U I LDS ALONG TH E S H E LF AN D M E SOB E NTHAL S LOP E OF TH E CA LI FOR N IAS

In addition to forming depth-displacement series, guild members can also form biogeographic displacement series. M.J. Allen (1986) examined biogeographic displacement in fusiform

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gadoids around the coasts of the Americas and Europe. Similarly, M.J. Allen (1990) provided a preliminary depiction of biogeographic displacement series of ecological counterparts of the California halibut along the coasts of the Californias. No description of foraging guilds of soft-bottom fishes exists along the shelf and slope of the Californias, except the depthdisplacement model for southern California (M. J. Allen, 1982a). Because of major differences in trawl net size, mesh size, and trawl duration between NMFS surveys on the middle shelf to the mesobenthal slope and small otter trawls used for environmental assessments and museum collections along the inner shelf of the same area and on the shelf and slope of southern California and Baja California, it may seem unreasonable to attempt such an assessment. However, general attributes, such as morphological attributes of the species, information from the literature on feeding and foraging, frequency of occurrence of guilds, and relative abundance of guild members by life zone (using NMFS, SWRCB, SCCWRP, and SIO data, mentioned above) provide the basis for a preliminary description of the spatial segregation of guild dominants along the Californias (figs. 7-9–12). In attempting this description, it became obvious that the NMFS trawls collected larger species, including more elasmobranchs than in the small trawls used from Southern California south. Thus, I have added three guilds (IA2b2, IC2a, and IID2b) to provide some description of the distribution of soft-bottom elasmobranchs. The first is represented by the Pacific electric ray; the second by small benthopelagivore sharks (e.g., brown cat shark); and the last by skates, rays, and guitarfishes. Their generally larger size and use of electroreception are likely to contribute to segregating them ecologically from bony fishes with similar foraging orientation. I have also separated benthic pelagivores into flatfishes (e.g., California halibut, bigmouth sole; IIA1) and roundfishes (e.g., lizardfishes, lingcod; IIA2) because both types occur commonly in the same areas, although they forage similarly. Many of the guilds form intuitively good geographic displacement series, with ecological counterparts in different regions, as well as across life zones. Bottom-living pelagobenthivores (sanddab guild) represent the most widespread guild on the southern California mainland shelf (M. J. Allen et al., 1998, 2002). Members of this guild are small flatfishes with medium-sized, symmetrical mouths, and they are generalists that feed on nektonic prey near the bottom and on benthic prey. In southern California, this guild consists of a depthdisplacement series of speckled sanddab, Pacific sanddab, and slender sole (M. J. Allen, 1982a). Along the coasts of the Californias, speckled sanddab is the dominant member of this guild on the inner shelf from northern California through northern Baja California but is replaced by longfin sanddab from there at least to Magdalena Bay (fig. 7-9). Similarly, Pacific sanddab is the guild dominant on the middle shelf from northern California through southern California but is replaced by longfin sanddab from northern Baja California Sur south to Cabo San Lucas (fig. 7-10). Note that longfin sanddab became a dominant in this guild on the southern and inner part of the middle shelf of southern California during the 1998 El Niño (M. J. Allen et al., 2002). On the outer shelf, slender sole is the dominant from northern California through southern California but is replaced by longfin sanddab and, along the coast of northern Baja California Sur and mimic sanddab (Citharichthys gordae) at the southern tip of Baja California on the outer shelf (fig. 7-11). Along the mesobenthal slope, slender sole is the dominant member of this guild from northern California through northern Baja California (fig. 7-12).

The next most widespread foraging guild is the bottomliving extracting benthivores (turbot guild), which consists of flatfishes with small asymmetrical mouths and large eyes, that extract polychaetes from tubes and clip off clam siphons protruding from the sediments. Along the inner shelf of the Californias, the dominant species of this guild off northern California is the butter sole, followed by the curlfin sole in central California (or into southern California during cold periods; M. J Allen, 1982a), the hornyhead turbot in southern California and northern Baja California, and the spotted turbot (Pleuronichthys ritteri) along the coasts of Baja California Sur (fig. 7-9). On the middle shelf, Dover sole is the guild dominant from northern California through southern California. Hornyhead turbot is dominant off northern Baja California, spotted turbot off northern Baja California Sur, and speckledtailed flounder (Engyophrys sanctilaurentii) off southern Baja California Sur (fig. 7-10). On the outer shelf, Dover sole is dominant from northern California through northern Baja California Sur. Flag flounder (Perissias taeniopterus) is a possible replacement in southern Baja California Sur (fig. 7-11). Dover sole is the dominant species along the mesobenthal slope at least from northern California through southern California, and presumably from there through northern Baja California Sur (fig. 7-12). However, there are few trawl samples from this zone off Baja California, and this can be inferred only from its distribution on the outer shelf and its range (M. J. Allen and Smith, 1988). Interesting patterns also occur among other guilds. Among the cruising nonvisual benthopelagivores on the inner and middle shelf, Pacific tomcod is dominant in northern California, white croaker (also called ‘tomcod’ by some anglers) from central California to northern Baja California, and other species, such as bronzestriped grunt (Orthopristis reddingi) and yellowstripe grunt (Haemulopsis axillaris), are possible replacements to the South (figs. 7-9 and 7-10). Among bottom-living pelagivore (ambushing) flatfishes, sand sole (Psettichthys melanostictus) is dominant among the inner shelf species in northern and central California but is replaced by California halibut in southern California and off Baja California (fig. 7-9) (M. J. Allen, 1990). On the middle and outer shelf, petrale sole is dominant in northern and central California, and bigmouth sole in southern California and Baja California (figs. 7-10 and 7-11); however, petrale sole grows larger than the bigmouth sole and becomes more piscivorous. Similarly, among elongate roundfishes of this guild, lingcod is dominant in northern and central California, and California lizardfish in southern California and Baja California on the inner, middle, and outer shelves (figs. 7-9– 7-11). Among large nonvisual benthivores, big skate is dominant on the inner, middle, and outer shelves of northern and central California, whereas California skate is typically dominant in these zones off southern California and Baja California (although thornback, a platyrhinid, is dominant on the inner shelf in southern California) (figs. 7-9–7-11). Round stingray, typical of shallow bays in southern California, is common on the inner and middle shelves off Baja California Sur (figs. 7-9 and 7-10). Examination of these patterns (figs. 7-9–7-12) also elucidates biogeographic changes in fauna. Cold temperate Oregonian species are dominant in all life zones off northern and central California, but this fauna is almost exclusively dominant on the mesobenthal slope of California (although there is insufficient data to know how far south off Baja California this is true) (fig. 7-12). Warm-temperate species representing San Diegan fauna

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F I G U R E 7-9 Generalized functional organization of soft-bottom fish communities on the inner shelf (5–30 m) of California and the Pacific Coast of Baja California.

are distinct in most life zones off southern California and northern Baja California. Along Baja California, there are relatively distinct faunas in northern Baja California (San Diegan fauna), northern Baja California Sur, and southern Baja California Sur (apparently, Mexican and Cortez faunal provinces contribute to different faunas of the Baja California Sur coast). In addition, there are cases of submergence, a shift in species dominance to deeper depths when its range extends into warmer regions. For instance, rex sole is common on the middle shelf in northern and central California but only on the outer shelf and mesobenthal slope in southern California (figs. 7-10–7-12). California tonguefish is the dominant of this guild on the middle shelf of southern California and Baja California. Similarly, spotted cusk-eel is dominant on the inner shelf of northern and central California and on the middle and outer shelves of California and Baja California but is replaced on the inner

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shelf of southern California and Baja California by the basketweave cusk-eel (figs. 7-9–7-11). The same pattern also occurs with plainfin midshipman and specklefin midshipman. Many species typical of bays of southern California (e.g., spotted sand bass, Paralabrax maculatofasciatus; round stingray; banded guitarfish, Zapteryx exasperata) are guild dominants on the inner shelf or deeper off southern Baja California (figs. 7-9–7-11). The patterns described here give some preliminary insight into the ecological organization of the soft-bottom fish fauna of the Californias. EVOLUTION OF C OM M U N ITI E S

M. J. Allen (1982a,b) examined the geologic age of taxa of soft-bottom fishes in southern California fish communities. Most of the species that co-occurred in communities were

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FIGURE 7-10 Generalized functional organization of soft-bottom fish communities on the middle shelf (31–100 m) of California and the Pacific Coast of Baja California.

phylogenetically different; the body form was developed over millions of years of evolution. Of 44 families represented in trawl catches in southern California, 91% were found in the worldwide fossil record (Romer, 1966). Chimaeridae (the earliest) appeared in the Lower Jurassic. About 30% of the families first appeared in the Eocene, and 82% had appeared by the Miocene. All 32 species of demersal species in a Pliocene deposit in southern California exist today. Ecological segregation among phylogenetically different species in the existing fauna is likely to be related to many millions of years of interaction among precursors of existing species and other extinct species and more recently among currently existing species (Allen,

1982a,b). Glacial/interglacial changes in sea level (140 m lower during the maximum of the last ice age) and shifts in isotherms equatorward and poleward, along with isolation of portions of coastal populations in the upper Gulf of California, may have contributed to the recent evolution of the soft-bottom fauna of the Californias (M. J. Allen, 1982a).

Interactions with Other Organisms Soft-bottom fishes interact with other organisms in a variety of ways. They prey upon other species (discussed above in the

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F I G U R E 7-11 Generalized functional organization of soft-bottom fish communities on the outer shelf (101–200 m) of California

and the Pacific Coast of Baja California.

section on Feeding), compete for food or space (often with species of the same or related guilds), associate with them for refuge, are eaten by predators, or are parasitized. Soft-bottom fishes eat a wide variety of pelagic and benthic invertebrates and also other soft-bottom fishes, including young of their own species. Bay gobies find refuge in burrows made by invertebrates (Grossman, 1979). I have observed small splitnose rockfish moving along under California king crabs (Paralithodes californiensis) within the basket formed by their legs in movies made by divers in submersibles in Santa Monica Bay. Some soft-bottom fishes may associate with worm tubes, sea pens, urchins, and sea cucumbers. Predators of soft-bottom fishes often include larger members of the fauna (e.g., Pacific halibut, skates, Pacific angel sharks, benthic feeding sharks) as well as seals and sea lions, dolphins, and some diving seabirds (e.g., cormorants). Sixgill sharks (Hexanchus griseus) and northern elephant seals (Mirounga angustirostris) may be predators of larger members of the fauna. Soft-bottom fishes are parasitized

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by a variety of external and internal parasites. External parasites include parasitic copepods, cymothoid isopods, and leeches (Mearns and Sherwood, 1977; Perkins and Gartman, 1997; Kalman, 2001). Among the most obvious external parasites is the eye copepod (Phrixocephalus cincinnatus—a pennellid copepod), which attaches to the eye of Pacific sanddab and some other soft-bottom species (Mearns and Sherwood, 1977; Perkins and Gartman, 1997). Internal parasites include (among others) nematodes, digenetic trematodes, and cestodes.

Comparison of California Fauna to Other Regions The soft-bottom fish fauna (groundfish) is an important food resource worldwide and hence the focus of extensive surveys by fisheries agencies of many countries. Trawl surveys outside of the Californias to assess North American fisheries stocks

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F I G U R E 7-12 Generalized functional organization of soft-bottom fish communities on the mesobenthal (upper) slope (201–500 m)

of California and the Pacific Coast of Baja California.

extend from Oregon to the Bering Sea on the West Coast and from northeastern Canada south along the Atlantic and Gulf Coasts of the United States. The results of these surveys as well as studies on the biology of commercially important soft-bottom species in these surveys are published extensively in Fishery Bulletin and NOAA Technical Report and many additional studies are described in the Technical Memoranda series of the NMFS fishery science centers. Beyond the Californias, soft-bottom fish communities have been described statistically off Oregon (Day and Pearcy, 1968), the Pacific Northwest (Gabriel, 1980; Gabriel and Tyler, 1980; Weinberg, 1994; Jay, 1996), the Caribbean and Pacific Coasts of Central America (Bayer et al., 1970), and from the Atlantic Coast of Africa (Fager and Longhurst, 1968). M. J. Allen and Smith (1988) examined the geographic and depth distribution of the 125 most common trawl-caught species along the U. S. West Coast from the Arctic Ocean to the U.S.-Mexico international border based on 24,881 trawl samples collected during a 30-year period. The species were classified zoogeographically and by life zone. Most of the

species were wide-ranging and hence occurred over more than one zoogeographic province and more than one life zone. The study updates geographic ranges of the species and provides good information on depths of greatest occurrence. Garrison and Link (2000) examined the diet of 40 species of soft-bottom fishes on the Northeast U. S. continental shelf and identified 14 significant trophic guilds, comprising divisions of six major predator groups. The predator groups included the following: (1) crab eaters, (2) planktivores, (3) amphipod/shrimp eaters, (4) shrimp/small fish eaters, (5) benthivores, and (6) piscivores. This study did not combine dietary information with morphological and distributional information as in M. J. Allen (1982a). M. J. Allen (1986) described ecological segregation in fusiform gadoid fishes from the Arctic Ocean, along the Eastern Pacific, along the Western Atlantic to the Arctic, and along the Eastern Atlantic, and New Zealand. Pelagivores (including Gadidae and Merlucciidae) formed a geographical displacement series of 25 species. Benthopelagivores (12 species, all Gadidae) were restricted to the North Pacific, Arctic Ocean, and

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North Atlantic. Haddock (Melanogrammus aeglefinus) was the only benthivore. Comparison of major gadid foraging types in the North Pacific and North Atlantic showed ecological counterparts of two of three guilds in both regions: (1) pelagivores— walleye pollock (Theragra chalcogramma) in the Pacific and pollock (Pollachias virens) in the Atlantic, (2) benthopelagivores— Pacific cod (Gadus macrocephalus) and Atlantic cod (Gadus morhua), and (3) benthivores—none in the Pacific and haddock in the Atlantic. Examination of all trawl-caught species in the North Pacific did not reveal a likely ecological counterpart of haddock, suggesting an “open niche” in the North Pacific. Other examples of assemblages of ecological counterparts among gadids were also presented.

Summary Soft-bottom fishes occupy the largest benthic habitat of the shelf and upper slope of the Californias and have been important to commercial and recreational fisheries in these areas. They have been extensively surveyed off most of California but only sparsely sampled off the Pacific Coast of Baja California. However, the extensive NMFS surveys in northern and central California and environmental surveys in southern California provide a wealth of information about soft-bottom species in this habitat. Though the shelf and slope habitat is rather narrow along most of the coast of the Californias, except along the southern Baja California Peninsula, the physical and biological characteristics of the habitat vary greatly with depth, and to a lesser extent geographically. With depth, there are at least four life zones from about 5 to 500 m: inner shelf (5–30 m), middle shelf (31–100 m), outer shelf (101–200 m), and mesobenthal slope (201–500 m). Physical variables, such as temperature, ambient light levels, oxygen levels, and pressure, change dramatically over this depth range, and many species are specifically adapted to one zone or another. Two or three major coastal biogeographic provinces occur along this coast, with major changes in the fauna at Point Conception, California, and Magdalena Bay, Baja California Sur. Scientific study of this fauna began about 1850 and initially (and largely to this day) was focused on fisheries species, in particular stock assessment and basic biology of species that might affect their abundance and availability. Most scientific fisheries surveys of these fish used commercial trawl gear. These surveys have produced good information on the population status and distribution of fisheries species, with some description of assemblages. In the late 1950s and in particular since 1969, environmental surveys of this fauna have been made to assess pollution effects in southern California and on the inner shelf of northern and central California. These surveys used small otter trawls and focused on all species caught because many of the species were not part of fisheries. These studies have produced good information on fish populations and assemblages, distribution of contaminants in fishes, and distribution of fish diseases. The soft-bottom fish fauna of the shelf and slope of Baja California has largely been sampled intermittently for museum specimens, with little attention to assessment of populations, and for some scientific studies off northern Baja California and Baja California Sur. Trawl surveys are conducted on soft bottom and typically collect a large number of species. However, only about 30% of these are typical of the soft-bottom habitat in any particular area; many are found primarily in other habitats and only inci-

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dentally over the soft bottom. The true soft-bottom fish fauna of the California and Baja California shelf and slope is regarded here as those species that occur commonly on the soft bottom in at least one of the different life zones and play important ecological roles (generally with regard to feeding) in the community. Frequent occurrence is more important than abundance in determining their importance, and this generally identifies species adapted to the habitat. Because the soft-bottom is relatively flat with little relief, the species best adapted are those with flat bodies (e.g., skates, rays, flatfishes) or those that burrow (e.g., cusk-eels). Nevertheless, some species of families apparently best adapted to hard bottoms (e.g., sculpins, rockfishes, and surfperches) live primarily in this habitat. At least 40 families of fishes have species that are soft-bottom species. The most widespread families are Paralichthyidae, Pleuronectidae, Batrachoididae, and Ophidiidae, which occur in all regions from northern California to southern Baja California Sur on or over the soft bottom. Other families have either a northern or southern occurrence to different degrees. The most widespread species in the shelf life zones occurred commonly from northern California through northern Baja California. The most widespread species by life zone were the following: inner shelf—shiner perch, white seaperch, speckled sanddab, and English sole; middle shelf—stripetail rockfish and English sole; and outer shelf—plainfin midshipman, spotted cusk-eel, and Dover sole. The most widespread species on the mesobenthal slope was Pacific hake; it occurs from northern California through southern California and in northern Baja California Sur. The mesobenthal slope was not well sampled off Baja California. Soft-bottom fishes have a variety of life-history traits that allow them to live on the soft bottom. Species that live on soft bottoms find refuge by burrowing or burial, being exposed in the open, schooling over the bottom, or occasionally finding crevices in low relief rocky bottoms or objects on the bottom (these latter are likely to be hard-bottom species). In southern California, most of the species were oviparous with pelagic eggs and larvae, the remaining species are divided among three additional categories. Soft-bottom fish vary in their lifehistory strategies; some are long-lived with poor replacement capabilities and some short-lived with good replacement. For species with pelagic larvae, the narrow shelf and offshore drift in upwelling areas may result in loss of many larvae. Inner shelf species often have larvae that spend little time in the plankton and outer shelf, and mesobenthal species may have larvae that spend several months in the plankton. Recruitment varies as a result of oceanic factors (currents, productivity), as well as spawning success. Some species, such as Pacific hake, undertake long coastwise migrations, whereas others show only local movements. Bathymetric migrations include seasonal migrations, ontogenetic movements of many species from shallow to deep water, and diel vertical migrations. Diel differences among species within a life zone are greater on the inner shelf than in deeper water, largely due to greater diel differences in ambient light on the inner shelf than on the outer shelf. Bioluminescence becomes an important light source on the outer shelf and upper slope. In southern California, soft-bottom fishes caught by small otter trawls feed largely on crustaceans, followed by polychaetes and ray-finned fishes. Of the crustacea, gammaridean amphipods were consumed by all 40 species examined, followed by calanoid copepods and crabs. The diet of species (neritic or benthic) that feed on nektonic prey changes with growth from

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copepods, to euphausiids and mysids, to nektonic fish or squid. Benthopelagic feeders shift from gammaridean amphipods, to shrimp, to fish and octopus with growth. Small species of these two groups stop before reaching one of the next levels. Polychaete-feeders focus on polychaetes and clam siphons. The foraging behavior of soft-bottom fishes differs in orientation with respect to the bottom; foraging zone (watercolumn, benthic, or both); and depending on the species, diel activities, strategy, and specialized behavior. Some watercolumn and some benthic species feed in the water column, on the bottom, or both. Foraging guilds, groups of species that forage in the same way, consist of a series of two to four species that displace each other with depth in Southern California (and presumably elsewhere). A set of the depthdisplacement patterns of 18 foraging guilds was arranged to describe the functional organization of soft-bottom fish communities in southern California (M. J. Allen, 1982a). Foraging guilds also show biogeographic displacement series, indicating that similar patterns with different species occur along the entire coast. Soft-bottom fishes are affected by a variety of other organisms (including predators and parasites, as well as prey abundance) and anthropogenic activities, including commercial and recreational fishing, habitat alteration, and pollution.

Prospectus for Research Although the soft-bottom fish fauna of the California shelf has been extensively surveyed in most areas, with many survey reports and studies on biological information on important fisheries species, there are still plenty of opportunities to do significant work on the soft-bottom fish fauna off California and Baja California. The following are some suggestions for future research on this fauna: 1. Conduct comparable trawl surveys in different areas. 2. Conduct baseline surveys off Pacific Baja California. 3. Assess small individuals and species on the middle and outer shelves of Northern and Central California shelf and slope. 4. Conduct comparative studies of catches from small and large trawl gear used in different areas. 5. Make better use of fish caught in scientific trawl surveys to enhance our understanding of soft-bottom fishes. 6. Make better use of life-history information to assess potentially threatened species. 7. Maintain time series surveys, where possible, to understand natural and anthropogenic factors that affect fish populations. 8. Collect more information on the behavior of softbottom species on the shelf and slope using basic and innovative techniques.

Acknowledgments I thank the following people for their assistance with this study: Valerie Raco-Rands and Erica T. Jarvis (both of the Southern California Coastal Water Research Project) for assistance with data analysis and figures for this study; Cindy

Klepadlo (Scripps Institution of Oceanography) for trawl fish collection data from the shelf and upper slope of Baja California; Waldo Wakefield (National Marine Fisheries Service [NMFS], Northwest Fisheries Science Center) and Robert Lauth and Mark Wilkins (NMFS, Alaska Fisheries Science Center) for data and survey reports on NMFS West Coast Shelf and Slope Surveys; and Jane A. Reid (United States Geological Survey, Pacific Science Center) for information on shelf width and sediment composition off California. I thank Larry G. Allen (California State University, Northridge) for initiatating this book, for illustrations of fishes from different regions, and for suggestions. I thank John A. Musick (Virginia Institute of Marine Science), Alan J. Mearns (National Oceanic and Atmospheric Administration, National Ocean Service, Office of Response and Restoration), and John S. Stephens (retired, formerly Occidental College) for suggestions regarding this manuscript.

Literature Cited Allen, L.G. 1985. A habitat analysis of the nearshore marine fishes from Southern California. Bull. South. Calif. Acad. Sci. 84(3): 133–155. ———. 1988. Recruitment, distribution, and feeding habits of young-ofthe-year California halibut (Paralichthys californicus) in the vicinity of Alamitos Bay-Long Beach Harbor, California, in 1984–1987. Calif. Fish Game 74(4):245–248. Allen, L.G., and E. E. DeMartini. 1983. Temporal and spatial patterns of nearshore distribution and abundance of the pelagic fishes off San Onofre-Oceanside, California. U. S. Fish. Bull. 81:569–586. Allen, L.G., and M. Franklin. 1992. Abundance, distribution, and settlement of young-of-the-year white seabass Atractoscion nobilis in the Southern California Bight, 1988–89. U. S. Fish. Bull. 90: 633–641. Allen, L.G., R.E. Jensen, and J.R. Sears. 1990. Open coast settlement and distribution of young-of-the-year California halibut (Paralichthys californicus) along the southern California coast between Point Conception and San Mateo Point, June—October, 1988. In C.W. Haugen (ed.), The California halibut, Paralichthys californicus, resource and fisheries. California Fish Game, Fish Bulletin. 1974, pp. 145–165. Allen, M.J. 1975. Alternative methods for assessing fish populations. Annual Report for the year ended 30 June 1975. SCCWRP, El Segundo, CA, pp. 95–98. ———. 1976. Field methods for sampling demersal fish populations and observing their behavior. In C. A. Simenstad and S. J. Lipovsky (eds.), Fish food habits studies. Washington Sea Grant, University of Washington, Seattle, WA, pp. 56–62. ———. 1977. Pollution-related alterations of demersal fish communities. Cal-Neva Wildlife Trans. 1977:103–107. ———. 1982a. Functional structure of soft-bottom fish communities of the Southern California shelf. Ph.D. Dissertation. University of California, San Diego, La Jolla, CA. ———. 1982b. Large-scale considerations in studies of resource partitioning. In G.M. Cailliet and C.A. Simenstad (eds.), Gutshop ‘81, Fish food habits studies. Washington Sea Grant, University of Washington, Seattle, WA, pp. 185–189. ———. 1986. Ecological segregation of fusiform gadoid fishes. In M. Alton (compiler), A workshop on comparative biology, assessment, and management of gadoids from the North Pacific and Atlantic Oceans. NOAA, NMFS, Northwest Alaska Fisheries Center, Seattle, WA, pp. 185–211. ———. 1990. The biological environment of the California halibut, Paralichthys californicus. In C.W. Haugen (ed.), The California halibut, Paralichthys californicus, resource and fisheries. California Fish Game, Fish Bulletin 174, pp. 7–29. Allen, M.J., and A.K. Groce. 2001a. First occurrence of blackspot wrasse, Decodon melasma Gomon 1974 (Pisces: Labridae) in California. Bull. South. Calif. Acad. Sci. 100(3):131–136. ———. 2001b. First occurrence of speckletail flounder, Engyophrys sanctilaurentii Jordan & Bollman 1890 (Pisces: Bothidae), in California. Bull. South. Calif. Acad. Sci. 100(3):137–143. Allen, M.J., A.K. Groce, D. Diener, J. Brown, S.A. Steinert, G. Deets, J.A. Noblet, et al. 2002. Southern California Bight 1998 Regional

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CHAPTER 8

Rocky Intertidal Zone M I C HAE L H. H O R N AN D KAR E N L. M. MARTI N

Introduction Rocky intertidal habitats are small living spaces occupied by a variety of fishes either year-round as residents or temporarily as visitors. These species live at the very margin of the ocean and thus must contend with the fluctuating conditions of both marine and terrestrial environments. The rocky intertidal zone represents in part a shoreward extension of subtidal rocky reefs, and the intertidal fish fauna comprises those inshore species that to varying degrees have colonized this extreme, partially terrestrial habitat. As a result, some species occur in both subtidal and intertidal habitats although, as is discussed below, intertidal fishes represent largely distinct assemblages. In this chapter, the main features of rocky shores as habitats for fishes are described followed first by the vertical and horizontal distribution patterns of the associated fauna then by the behavioral, physiological, and reproductive traits of the fishes, with an emphasis on resident species; and, finally, by an account of the structure and dynamics of intertidal fish communities. Californian intertidal fishes are relatively well known in certain ways and are referenced in several other places in this book including chapter 3 (teleost evolution), chapter 4 (ecological classification), chapter 14 (feeding and trophic interactions), and chapter 19 (reproduction).

Rocky Intertidal Zone as a Fish Habitat The narrow strip of coastline between the tidemarks on rocky shores represents a unique and demanding habitat for marine fishes (see chapter 4, this volume; Horn et al., 1999). Although often highly productive and rich in seaweed and invertebrate species, the rocky intertidal zone is a wave-swept and turbulent environment with both temporal and spatial variations. On the California coast, the mixed semidiurnal tide regime cuts off the intertidal zone from the open ocean twice a day to varying degrees. The extent of the exposure depends on the time of day and period in the lunar cycle. At low tide, the water that remains in the habitat is confined to isolated pools and under-rock spaces. Thus, any resident fish must be able to withstand some time either completely out of

water or at least partly exposed to air although usually in a moist location. The daily fluctuations in water level combined with time of day can result in rapid and large changes in physical and chemical features of tidepools. During an afternoon low tide on a spring tide series, an isolated pool has ample time, especially under full sun, to increase dramatically in temperature and salinity compared to the conditions that would prevail during a nighttime or an early morning low tide. Intertidal animals and seaweeds are exposed to rapid and sometimes extreme changes in temperature (fig. 8-1), one of the most important factors determining the distribution and physiological performance of these organisms (Helmuth and Hofman, 2001). Oxygen levels also increase during the daytime as photosynthesis proceeds but fall at night when only respiration occurs. Carbon dioxide accumulates, and pH may decline as respiration continues in isolated pools (Davenport and Woolmingon, 1981). Seasonal changes in climate add another temporal component to the fluctuating conditions within a given rocky intertidal habitat (e.g., Horn et al., 1983; Murray and Horn, 1989; Helmuth and Hofman, 2001). For example, marked differences occur in environmental conditions between winter and summer months on central California shores (fig. 8-2), reflecting the Mediterranean climate that characterizes much of the California coast. The winter months are characterized by short, cool days with long periods of aerial exposure and occasional rainfall frequently accompanied by storms of varying intensity. In contrast, summers days are long and warm with little rainfall and minimum daytime exposure in the intertidal zone. Seasonal differences in water temperature, however, are reduced because of pronounced upwelling during the summer months, which lowers temperatures toward the more uniformly cool sea temperatures of winter. Rainfall and the resulting flow of water into intertidal habitats during the winter reduce salinities that can create osmotic stress for fishes. Not surprisingly, members of intertidal fish communities exhibit mechanisms found in their more completely aquatic predecessors for maintaining internal osmotic, pH, and nitrogen balance even though many physiological questions remain to be answered for fishes in this habitat (Evans et al., 1999). Spatial variation on several scales adds further complexity to rocky shores as fish habitats. Within a single location,

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F I G U R E 8-1 Monthly temperature variation in a small tidepool

on the rocky shore adjacent to Hopkins Marine Station in Pacific Grove on the central California coast (after Helmuth and Hofman, 2001).

habitat heterogeneity is derived from a variety of substratum and microhabitat types. Gravel expanses and boulder fields interspersed with shallow pools are unstable areas and frequently are rearranged by storms and wave action, yet provide many hiding places for small fishes. On the other hand, crevice-type rockpools and fixed rock outcrops often topped with turf or foliose macroalgae exhibit greater permanence, although all microhabitats are subject to the longer term forces of erosion and tectonic activity. Differences in aspect and slope increase the heterogeneity of environmental conditions on rocky shores. For example, Helmuth and Hofman (2001) recorded temperatures consistently higher by several degrees at horizontal microsites than on a north-facing vertical site with intermediate temperatures taken in a nearby tidepool on a rocky shore in Pacific Grove on the central California coast. On a larger spatial scale, rocky intertidal habitats themselves are not continuous but are separated by sandy beaches, steep bluffs, river mouths, or some combination of these coastal features. On a latitudinal scale, temperature and other climatic conditions differ along the expanse of the California coastline and help determine the composition of the intertidal fish fauna at any given location. That two biogeographic provinces are represented in California coastal waters (chapters 1 and 2, this volume) reflects the substantial changes in the environment that occur over the 10° of latitude of the state. Given the great temporal and spatial variations typical of rocky intertidal habitats, year-round fishes may be expected to show broad tolerance to fluctuating conditions or to possess traits that allow them to survive and even reproduce in the intertidal zone. In contrast, fishes that occur only temporarily in the habitat may be less specialized for intertidal life but are often larger and more mobile and thus better able to avoid or escape the rigors of the intertidal zone as the tide ebbs. The following section of the chapter addresses these

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F I G U R E 8-2 Seasonal patterns of environmental conditions on the

central California coast (after from Horn et al., 1983).

expectations and summarizes and evaluates the existing information relevant to them.

Distribution Patterns Vertical Zonation in Intertidal Fish Assemblages We are accustomed to thinking of vertical zonation in the rocky intertidal zone as shown by bands of sessile invertebrates

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and algae (i.e., Stevenson and Stevenson, 1972; Benson, 2002). Intertidal fishes also segregate at different tidal heights as seen among pricklebacks and gunnels on California rocky shores (Horn and Riegle, 1981; Jones, 1981). Physical factors such as tidal height, type of cover, wave exposure, and substratum influence habitat choice in fishes. During low tides, intertidal fishes face potential exposure to aerial or aquatic changes that increase in duration and effect with height on the shore. In addition, habitat use by fish in the intertidal zone is strongly influenced by biotic interactions (Benson, 2002). For certain fish species, abundance of different size classes varies across the intertidal zone. Larval fish tend to settle on substrata preferred by conspecific adults (Marliave, 1977), but smaller individuals of clingfishes (Stepien, 1990), sculpins, (Nakamura, 1976; Freeman et al., 1985; Wells, 1986), and pricklebacks (Horn and Riegle, 1981) are more abundant higher in the intertidal zone perhaps because larger fish tend to win intraspecific contests (Richkus, 1981). Five species of pricklebacks in the rocky intertidal zone of central California have overlapping, yet distinguishable, vertical distributions (Horn and Riegle, 1981; Barton, 1982). Early juveniles of the rock prickleback (Xiphister mucosus) consistently occur higher in the intertidal zone than those of the monkeyface prickleback (Cebidichthys violaceus) (Setran and Behrens, 1993). Increased body size results in relatively smaller body surface area and contributes to tolerance of water loss during low tides. Even among amphibious fishes, however, the smaller, more vulnerable juveniles are found higher in the intertidal zone than larger conspecifics (Horn and Riegle, 1981). Juveniles of some shallow subtidal fishes can be found in tidepools (Williams, 1957; Martin, 1993; DeMartini and Sikkel, chapter 19 this volume). Although this occurrence may help juvenile fish avoid large aquatic predators, they face increased exposure to piscivorous birds, which are known to capture fish in the rocky intertidal zone (MHH, pers. obs.). Some kelpfish in California show sexual differences in vertical distribution. Williams (1954) reported that approximately 90% of spotted kelpfish (Gibbonsia elegans) in lower intertidal pools are female but that males and females are present in equal abundance in subtidal habitats. Sex differences in vertical distribution are seen in in other species of tidepool kelpfish; mostly females and juveniles are found intertidally, whereas males are seen only subtidally (Stepien, 1987; Stepien and Rosenblatt, 1991). The explanation is that females migrate to subtidal depths only to mate and lay eggs, whereas the males guard the eggs there until they hatch. Differences in color or morphology among members of the same species collected at different vertical heights may be related to diet. Limited evidence exists, however, to show that vertical distribution among intertidal fishes may be affected by dietary habits. For example, herbivorous species such as the monkeyface prickleback feed on algae during high tides (Horn et al., 1986; Ralston and Horn, 1986). Some algae-eating fishes show a distinct preference for the upper intertidal zone (Horn, 1989; Horn and Ojeda, 1999), even though in higher pools the fish have less time for foraging, unless they leave the home pool during a low tide. On a larger temporal scale, seaweed abundance is greatest in summer and lowest in winter on the central California coast (Horn et al., 1983) and may influence the vertical abundance of herbivorous fishes. As described above, many species of sculpins occur in the intertidal zone. This intertidal diversity probably is associated

with niche specialization and with differences in vertical distribution. Among the three to six cottid species that coexist in midintertidal pools (Pfister, 1992), the tidepool sculpin (Oligocottus maculosus) prefers high tidepools, whereas the fluffy sculpin (O. snyderi) is found in lower pools, in both Canada (Green, 1971; Nakamura, 1976) and on the central California coast (Yoshiyama, 1981). Not surprisingly, Nakano and Iwama (2002) found that the tidepool sculpin has a higher temperature tolerance and higher heat shock protein (hsp 70) levels than the fluffy sculpin. The mosshead sculpin (Clinocottus globiceps) prefers the lower intertidal zone in Canada (Mgaya, 1992), but it is found in high pools with tidepool sculpins on central California rocky shores. Even within the high zone, the mosshead sculpin is most abundant in pools farther from shore, and the tidepool sculpin occurs in the higher pools where wave exposure is reduced (Yoshiyama, 1981; Yoshiyama et al., 1986).

Temporal Variations in Vertical Distribution DI U R NAL CHANG E S

The vertical distribution of some intertidal fishes may be subject to diurnal changes, but California species are not well studied in this regard. Changes in fish distribution with tidal level are more often seen in transient species that leave during low tides than in resident intertidal fishes (Gibson, 1999). For example, kelpfishes are typically absent from tidepools during nocturnal low tides, when the danger of hypoxia is great (Congleton, 1980). Tidepools high on the shore may increase in temperature during daytime low tides, resulting in fewer woolly sculpin and opaleye (Girella nigricans) in these pools during daytime compared to nighttime lows (Davis, 2001). S EASONAL CHANG E S

Some species of intertidal fishes show declines in abundance during the winter in California (Burgess, 1978; Chandler and Lindquist, 1981; Davis, 2000b), perhaps because some species, especially the more mobile, transient forms, migrate to deeper waters. Wave turbulence increases during the winter (Horn et al., 1983), and stronger waves generally correlate with fewer intertidal fishes (Grossman, 1982). The tidepool sculpin as well as the monkeyface prickleback and the rock prickleback decline during winter on California shores, probably because of the pounding by heavy waves (Green, 1971; Setran and Behrens, 1993). Intertidal fishes resist being swept away by strong waves in part because they are relatively small and have a reduced or no swimbladder. Some sculpins and clingfishes possess dermal calcifications that help the fish remain attached to the substratum (Zander et al., 1999), and gobies and clingfishes have modified pelvic fins that act at least in some species as ventral suckers to help the fish maintain position during wave wash (Horn and Gibson, 1988). In summer, increased species richness results from the influx of transient species, both adults and juveniles, as the rocky intertidal zone undergoes its seasonal role as a nursery (Moring, 1986; see below). This greater species richness and increase in the proportion of juveniles usually skew the peak of abundance to pools higher in the intertidal zone. Seasonal temperature fluctuations also may have important effects on

ROCKY INTERTIDAL ZONE

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vertical zonation. For example, the rockweed gunnel (Apodichthys fucorum) occurs higher on the shore in summer than in winter in central California (Burgess, 1978), probably because of temperature changes. Conversely, in a rocky intertidal area of winter upwelling off Baja California, both the number of species and the number of individuals increase during this season (Stepien et al., 1991), perhaps because the cooler waters attract cool-temperate fishes otherwise found at higher latitudes in California. Davis (2000b), however, found relatively stable species distributions for five species of tidepool fishes in southern California, even though temperatures and fish abundances changed seasonally.

Horizontal Zonation in Intertidal Fishes Microhabitats: Aquatic During High Tide When the rocky shore habitat is inundated at high tide, it takes on important characteristics of the surrounding ocean. These features include relatively uniform temperatures and salinity and oxygen saturation or even supersaturation, a well-buffered pH, and relatively low dissolved carbon dioxide levels (Bridges, 1993). In the rocky intertidal zone, productivity is high (Leigh et al., 1987), and large predators are rare. Oxygen tensions in the ocean are elevated, generally in equilibrium with air, and may even supersaturate with pounding surf or tidepool photosynthesis (Graham et al., 1978). At high tide, wave action mixes and rapidly dispels any short-term changes from weather or biological activities at the transition from subtidal to rocky intertidal habitats. Thus, with the exception that fewer predators may exist in this still relatively small habitat, the intertidal zone when inundated is more or less continuous with and similar to waters beyond the low tidemark.

1993). On exposed substrata, wind and sun cause desiccation and create temperature fluctuations that are much greater than those in water. Out of water and without its buoyant effects, intertidal fish must adjust to the increased pull of gravity. Although the speed of diffusion of respiratory oxygen increases in air, exposure to air causes desiccation and the collapse of gills (Randall et al., 1981). Dependent upon gills and skin for respiration, most intertidal fishes must remain in moist, sheltered microhabitats under boulders or seaweeds or return frequently to pools to moisten respiratory surfaces (Horn and Riegle, 1981; Martin, 1995). Even though some amphibious species of gobies and blennies in tropical and subtropical regions live above the waterline and are consistently out of water (Graham, 1997), no known temperate-zone fish species, including those in California rocky intertidal habitats, has evolved the specializations necessary for surviving the extreme environment of the supralittoral zone (see below).

Behavioral and Physiological Traits Tolerance to Emersion All fishes make behavioral choices in their habitats, and intertidal fishes, routinely experiencing ebb tides, may be expected to choose to avoid either a degraded aquatic habitat or accidental stranding in air (Sayer and Davenport, 1991). A number of intertidal fishes on California shores are amphibious to some extent and, under certain stressful conditions, leave the water deliberately (Yoshiyama and Cech, 1994; Martin, 1995; Watters and Cech, 2003). Adults of some species, however, emerge occasionally during low tides as they guard their eggs (Coleman, 1999; DeMartini and Sikkel, chapter 19, this volume). Thus, rocky intertidal fishes may leave the water under stress or as part of the natural life cycle as in parental care.

Microhabitats: Aquatic During Low Tides—Tidepools

Emergence Behaviors

Aside from the fluctuating conditions already described in the introduction, oxygen solubility is an important environmental factor in tidepools. Oxygen solubility is lower in seawater than freshwater (Dejours, 1994) and declines with increasing temperature and salinity, worsening the hypoxia that can occur in pools during low tide. Because transient fish species may become concentrated in these aquatic refuges during low tide, respiration can be a challenge for these active swimmers. At night, in the absence of photosynthesis, hypoxic conditions may become severe (Congleton, 1980; Bridges, 1993). Carbon dioxide released by respiring animals and seaweeds also affects the tidepool habitat. In the open ocean, respiratory carbon dioxide is buffered by bicarbonates and consumed by algae carrying out photosynthesis. In the small volume of a tidepool, however, and particularly at night in the absence of photosynthesis, bicarbonate buffering may be overwhelmed and the pH may decline by several units during the course of a few hours (Truchot and Duhamel-Jouve, 1980; Bridges, 1993).

A variety of intertidal fish species occasionally can be found out of water on California rocky shores. Resident intertidal fishes are small, negatively buoyant, and typically lack a swimbladder. The large pectoral fins of sculpins or sinusoidal body of pricklebacks allow them to perch upright on the substratum during terrestrial emergence (Martin, 1991; Horn, 1999). Some degree of desiccation is likely for fish out of water (Horn and Riegle, 1981; Martin, 1996; Luck and Martin, 1999) because the entire body of the fish emerges, including the head and gills, for the duration of the low tide. Some amphibious fish species, even while emerged under boulders, periodically roll to one side into shallow pools (Daxboeck and Heming, 1982; Graham et al., 1985; Brown et al., 1992; pers. obs.), apparently to maintain moisture on the skin surface. This behavior may have the dual effects of resisting desiccation and maintaining the integrity of the skin, and perhaps the gills, as a respiratory surface while the fish is exposed to air. Three groups of amphibious fishes have been recognized based on the type of emergence behavior they exhibit: (1) skippers, (2) tidepool emergers, and (3) remainers. The latter two types are represented in California (table 8-1). All three types emerge fully from the water and exchange both oxygen and carbon dioxide in air (Martin, 1995). Skippers, known only from tropical latitudes, include the mudskipper gobies (Clayton, 1993) and the rockskipper blennies (Zander, 1972;

Microhabitats: Aerial Habitats During Low Tide Vertical zonation is more pronounced in animals and seaweeds on rock substrata exposed to air at low tide than in those species that are confined to tidepools (Metaxas and Scheibling,

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Remainer Emerger Remainer Remainer Remainer Remainer

Gobiesox maeandricus Girella nigricans Apodichthys flavidus Pholis laeta Xererpes fucorum Anoplarchus purpurescens

Remainer Remainer

Yes Yes

Yes

Yes

No No Yes

Yes

Yes

Yes Yes Yes No Yes

No Yes Yes

No Yes

Yes

Yes

Air Breather

W, LF W, LF

W, LF

W, LF

W W W, LF

LF

W, LF

W, LV, LF LF W, LV, LF W W, LV, LF

W W, LV, LF W, LV, LF

W W, LV, LF

LF

W, LF

Emergence

Cross, 1981; Horn and Riegle, 1981; Martin, 1996; Yoshiyama and Cech, 1994; Lamb and Edgell, 1986 Riegle, 1976; Horn and Riegle, 1981; Edwards and Cech, 1990; Martin, 1993 Daxboeck and Heming, 1982; Lamb and Edgell, 1986; Martin, 1993 Horn and Riegle, 1981; Lamb and Edgell, 1986; Martin, 1993

Cross, 1981; Lamb and Edgell, 1986 Lamb and Edgell, 1986 Horn and Riegle, 1981; Lamb and Edgell, 1986; Martin, 1993

Martin, 1993; R. Orton (pers. comm.)

Cross, 1981; Martin, 1993

Lamb and Edgell, 1986 Cross, 1981; Martin, 1996; Yoshiyama and Cech, 1994; Yoshiyama et al., 1995 Yoshiyama and Cech, 1994 Martin, 1991; Watters and Cech, 2003 Martin, 1993; Yoshiyama and Cech, 1994; Lamb and Edgell, 1986; Yoshiyama et al., 1995; Watters and Cech, 2003 Wright and Raymond, 1978; Martin, 1993 Martin, 1993 Martin, 1993; Yoshiyama and Cech, 1994; Yoshiyama et al., 1995 Yoshiyama and Cech, 1994 Martin, 1993; Yoshiyama and Cech, 1994; Yoshiyama et al., 1995

Luck and Martin, 1999

Crane, 1981; Martin, 1993

Reference

NOTE: Classified as either tidepool emergers, remainers, or other, as air breathers (yes) or not (no), and as to whether emergence behavior was observed in the wild (W), forced in the laboratory (LF), or voluntary in the laboratory (LV). “Yes” for air breather means that gas exchange in air has been confirmed by laboratory experiments. All intertidal fishes that are found consistently emerged in the wild probably have the ability to breathe air, but this ability needs to be verified experimentally.

Xiphister atropurpureus Xiphister mucosus

Emerger Emerger Emerger Emerger Emerger

Clinocottus recalvus Leptocottus armatus Oligocottus maculosus Oligocottus rimensis Oligocottus snyderi

Bald sculpin Pacific staghorn sculpin Tidepool sculpin Saddleback sculpin Fluffy sculpin Gobiesocidae Northern clingfish Kyphosidae (Girellidae) Opaleye Pholidae Penpoint gunnel Crescent gunnel Rockweed gunnel Stichaeidae High cockscomb

Black prickleback Rock prickleback

Emerger Emerger Emerger

Clinocottus acuticeps Clinocottus analis Clinocottus globiceps

Sharpnose sculpin Woolly sculpin Mosshead sculpin

Remainer

Remainer Remainer

Artedius lateralis Ascelichthys rhodorus

Cebidichthys violaceus

Other

Hypsoblennius gilberti

Monkeyface prickleback

Remainer

Classification

Porichthys notatus

Scientific Name

Batrachoididae Plainfin midshipman Blenniidae Rockpool blenny Cottidae Smoothhead sculpin Rosylip sculpin

Family Common Name

TA B L E 8-1

California Rocky Intertidal Fishes

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Graham et al., 1985; Martin and Lighton, 1989). These fishes can forage, feed, defend territories, and mate while out of water on tropical shores. Tidepool emergers move out of the water when aquatic conditions, such as low oxygen tension (hypoxia), become inhospitable. Sculpins have been shown to display this type of emergence behavior in numerous studies (Wright and Raymond, 1978; Davenport and Woolmington, 1981; Martin, 1991; Yoshiyama et al., 1995). Tidepool emergers may use a tail flip or a crawling locomotion involving the pectoral fins to exit from a tidepool. They move about rarely when emerged, but can locomote well enough to escape from predators or move between pools, at least when pursued by scientific investigators (pers. obs.). Tidepool emergers have been seen emerged from pools in caves (Wright and Raymond, 1978) and during the night (Martin, 1993). In addition to conditions of hypoxia, unsuitable levels of temperature, salinity, pH, or carbon dioxide may be important factors, but they have not yet been shown to elicit emergence in marine fishes (Davenport and Woolmington, 1981; Sayer and Davenport, 1991). Tidepool emergers frequently are collected from tidepools but are rarely found emerged under boulders during low tide. Some of these species may opt to breathe at the surface rather than emerging when they perceive the threat of predators (Watters and Cech, 2003). In contrast to tidepool emergers, which move actively out of pools, remainers emerge passively from water simply by staying in a location that is slowly exposed to air by a low tide (Horn and Riegle, 1981, Martin, 1995). These fishes are found under boulders or in crevices, sometimes in pools only a few millimeters deep. Fishes classified as remainers are not very active on land although they can thrash about, presumably to escape predators (Horn and Gibson, 1988). Species of fish found emerged under these conditions can occur in pools during low tide, but they sometimes are more numerous out of water. Remainers are found among several taxa of California intertidal fishes, including pricklebacks (Horn and Riegle, 1981, Daxboeck and Heming, 1982; Edwards and Cech, 1990), gunnels (Martin, 1993), sculpins (Cross, 1981; Martin, 1996), clingfishes (Eger, 1971; Martin, 1993), and toadfishes (Crane, 1981). Remainers variously can tolerate several hours out of water and considerable desiccation (Horn and Riegle, 1981). Some intertidal fishes act as remainers in the intertidal zone when they guard eggs. If the nest emerges during low tide, the parental fish remain with the eggs, as in the high cockscomb, Anoplarchus purpurescens (Coleman, 1992), and some species of sculpins (Marliave and DeMartini, 1977) in the Pacific Northwest and the plainfin midshipman (Porichthys notatus) in California (Crane, 1981; Coleman, 1999). As long as they do not suffer excessive desiccation, egg masses benefit from accelerated development as a result of the increased oxygen levels and higher temperatures afforded by occasional aerial exposure (Strathmann and Hess, 1999; Smyder and Martin, 2002). A few intertidal fish species, even though they have not been observed out of water in nature and cannot be induced to emerge from hypoxic water in the laboratory, nevertheless, can breathe air when removed from water and can tolerate prolonged emergence of several hours with no apparent ill effects. California species exhibiting these capabilities include juvenile opaleye (Martin, 1993) and adult rockpool blenny, Hypsoblennius gilberti (Luck and Martin, 1999). Both of these species can breathe air and survive hours of emergence during a low tide although how frequently these abilities are actually used is unknown.

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By contrast, some intertidal fishes and most subtidal species, of course, do not emerge and if taken out of water, will not survive for the duration of a low tide (Davenport and Woolmington, 1981). Tidepool fishes that can neither emerge nor breathe air include kelpfish (Congleton, 1980; Martin, 1996) and, most likely, juvenile rockfishes and surfperches found in tide-pools. Such fishes are not found in tidepools during nocturnal low tides, when hypoxia is most likely to occur; rather, they avoid hypoxia, probably by migrating to subtidal habitats (Congleton, 1980).

Aerial and Aquatic Respiration Many of the intertidal fish species in California can breathe air (Riegle, 1976; Martin, 1993, 1995; Yoshiyama and Cech, 1994; Martin and Bridges, 1999), exchanging both oxygen and carbon dioxide at rates similar to their aquatic rates, and at the same rate as they are metabolized (Bridges, 1988; Martin, 1993). Table 1 lists the species of California rocky intertidal fishes that have shown evidence of air-breathing ability. Respiratory gas exchange in these fishes variously can occur across the gills, the skin, and possibly the linings of the opercular and buccal cavities in both water and air. Intertidal fishes often emerge fully from the water when breathing air although occasionally they lift just the head and opercula out of the water, poised at the water’s edge, rather than emerging. Some species, such as the pricklebacks, are capable of a wriggling escape behavior and limited locomotion out of water, but mostly they remain calm and move little. Ventilation in air typically includes “gulping,” and the rate of ventilation decreases dramatically in air. The gap between the opercula and the body wall may be sealed shut by mucus, changing the gill ventilation from flow-through in water to tidal flow in air. Oxygen is plentiful in air, and diffusion occurs quickly, so boundary layers are not a problem for respiratory surfaces (Feder and Burggren, 1985). Fish gills, however, typically function in water, and they collapse when fish are out of water, causing a reduction in respiratory surface area. Air-breathing marine fishes cope with this effect in several ways, first by emerging into a moist microhabitat with high humidity. Some amphibious fishes show morphological specializations to strengthen and support the gills for use in air (fig. 8-3; Brown et al., 1992). Also, fish use the skin as an alternative respiratory surface, one that is not subject to collapse (see below). Cutaneous surfaces are in direct contact with the air and need only be kept moist and well supplied with blood to be used in respiration (Feder and Burggren, 1985). The partitioning of gas exchange between the gills and the skin varies with the taxon (Martin, 1991, 1995; Martin and Bridges, 1999). Long, eel-like fishes tend to rely more heavily on cutaneous respiration than shorter, thicker fishes. Some blennies show increased reddening of certain cutaneous surfaces on emergence (Zander, 1972; Luck and Martin, 1999), suggesting that skin respiration may be more important in air than it is in water. The gills and other respiratory structures have not been examined in most remainer and tidepool emerger species; however, the black prickleback (Xiphister atropurpureus), a remainer, has cartilaginous rods within its primary gill lamellae (Sanders and Martin unpublished; fig. 8-3) that may stiffen and support the primary lamellae. Some skipper fishes have thickened gill epithelia, reduced surface area of the secondary lamellae, and cartilaginous rods to stiffen and support the

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F I G U R E 8-3 Photomicrographs of the primary and secondary lamellae of the gills of the black prickleback (Xiphister atropurpureus): A. 100x;

B. 400x (Sanders and Martin, unpubl.).

primary lamellae (Low et al., 1990; Brown et al., 1992; Graham, 1997). Reduced gill surface area with thicker epithelia, however, could inhibit respiration in water (Graham, 1997), a trade-off that might force fish to emerge during a hypoxic low tide. Specialized air-breathing organs, such as respiratory trees in the pharyngeal region or vascularized stomachs, are rarely present in marine fishes and more typically are found in freshwater fishes that remain aquatic while breathing air at the surface (Graham, 1976). Among the very few marine fishes that remain submerged while breathing air is the longjaw mudsucker (Gillichthys mirabilis). This California estuarine goby uses its highly vascularized buccopharyngeal epithelium as an accessory air-breathing organ (Todd and Ebeling, 1966). Little evidence exists to demonstrate that rocky intertidal fishes when out of water show a reverse “diving response” although the following observations can be made. Some blennies, including the high intertidal rockpool blenny, have a decreased metabolic rate in air (Luck and Martin, 1999). The monkeyface prickleback does not show bradycardia when placed in air; instead its heart rate increases, then gradually decreases during the time of emergence (Riegle, 1976). A transient drop in heart rate has been observed in California grunion (Leuresthes tenuis) on emergence (Garey, 1962), but this fish emerges onto sandy beaches after high tides to spawn (Walker, 1952; Martin and Swiderski, 2001), and it remains emerged only a few minutes, unlike emerging fishes in the rocky intertidal zone. The Mexican goby, Bathygobius ramosus, decreases its metabolic rate at high tides and decreased daily temperatures and may also have a diel component in its metabolism (Alcaraz et al., 2002). No intertidal fish species appears to require anaerobic metabolism while quietly and calmly emerged in air (Riegle, 1976; Martin, 1991, 1995, 1996; Martin and Bridges, 1999). Aquatic oxygen consumption rates are equal before and after long periods of emergence in both the woolly sculpin, Clinocottus analis (Martin, 1991) and the rockpool blenny (Luck and Martin, 1999), indicating that no oxygen debt has been incurred. Whole body lactate concentrations did not change in the monkeyface prickleback after four hours of emersion, also indicating no lactate buildup (Riegle, 1976). On the other hand, subtidal sculpins, such as the longfin sculpin (Jordania zonope), significantly increase production of lactate when forced to emerge (Martin, 1996).

Few studies have been carried out on marine fishes while they are active out of water partly because most species remain largely inactive when they emerge (Ralston and Horn, 1986; Horn and Gibson, 1988; Martin, 1993). Nevertheless, the relatively inactive black prickleback, a remainer, can double its aerial oxygen consumption over its resting aquatic rate if forced to move about (Daxboeck and Heming, 1982; Martin, 1993). Anaerobiosis also may be involved during some kinds of terrestrial activity (Martin and Lighton, 1989), for example, when remainers thrash about rapidly to escape predators, possibly incurring an oxygen debt. Under asphyxic conditions, the blind goby (Typhlogobius californiensis) increases lactate concentrations (Congleton, 1974). Skipper fishes, such as the rockskipper blennies that are highly active out of water on tropical shores, increase aerial oxygen consumption during this activity (Hillman and Withers, 1987; Martin and Lighton, 1989). For intertidal fishes, carbon dioxide release in air matches their rate of production (Martin, 1993; Martin and Bridges, 1999). In contrast, freshwater air-breathing fishes use lungs and enclosed air-breathing organs that are ventilated tidally and infrequently (Randall et al., 1981; Graham, 1997). Thus, carbon dioxide accumulates within the respiratory organ, causing changes in blood pH. Intertidal fishes use the skin and gills for breathing, where blood capillaries flow in constant, direct contact with the air rather than within an enclosed organ. As a result, carbon dioxide is constantly diffused away, and no carbon dioxide accumulation occurs in the circulatory system of intertidal species (Feder and Burggren, 1985). Aquatic hypoxia normally causes greater ventilatory responses than hyperoxia in intertidal fishes (Martin and Bridges, 1999), but these responses have not been carefully studied in any California intertidal species. Below a critical aquatic oxygen tension (Pc), intertidal fishes cannot continue to maintain resting metabolic rates, and oxygen consumption falls. The oxygen tension where this happens varies for different species, but the Pc values for intertidal fishes are low compared to those for other teleosts (Hughes et al., 1983). The woolly sculpin, a tidepool emerger, has a lower Pc than that of two remainers, the reef finspot (Paraclinus integripinnis) and the spotted kelpfish (Congleton, 1980). The blind goby, with an even lower Pc (Congleton, 1974), can colonize mud burrows of ghost shrimps, and, at what must be very low oxygen tensions, anaerobic metabolism may become

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important. Further studies are needed on the effects of low oxygen tension on intertidal fishes.

Osmoregulation and Resistance to Desiccation Despite the immediate risks of desiccation, no clear evidence exists for physiological or anatomical adaptations to desiccation among California intertidal fishes; instead, they face this challenge with behavioral responses. Some fish emerge only at night (Wright and Raymond, 1978; Congleton, 1980; Martin, 1993), when hypoxic stress is highest but desiccation risk is low in tidepools. During the daytime, when desiccation stresses are greatest, fish may emerge under cover (Cross, 1981; Horn and Riegle, 1981; Martin, 1995, 1996) or remain semisubmerged in very shallow pools (Daxboeck and Heming, 1982). Some California intertidal fishes can survive emergence for many hours, but mass decreases over time, most likely from evaporative water loss (Horn and Riegle, 1981; Martin, 1991; Luck and Martin, 1999). For five California intertidal species that occur across a vertical tidal gradient but commonly beneath boulders and not in tidepools, Horn and Riegle (1981) found that the monkeyface prickleback, the fish living highest on the shore, had the greatest initial water content and tolerance to desiccation. In contrast, two midintertidal species, the black prickleback and the rockweed gunnel, lost water in air and went on to lose even more water after reimmersion, showing the importance of avoiding desiccation in the first place. On the other hand, five species of sculpins from a vertical tidal gradient in Puget Sound, but more confined to tidepools than the pricklebacks above, showed no difference in the rate of water loss that could not be explained by differences in body size (Martin, 1996). To recover lost fluids, intertidal fishes drink seawater (Dall and Milward, 1969; Evans et al., 1999). The black prickleback also can osmoregulate in dilute media, maintaining plasma osmolarity when immersed in 20% sea water. Thus, tolerance to alterations in the external medium allows this euryhaline fish to survive ephemeral changes in tidepool salinity, an ability that also may exist in other intertidal pricklebacks. No California intertidal fishes have been studied with regard to the storage or excretion of nitrogenous waste products in air, although the monkeyface prickleback excretes nitrogen in the form of urea in water (Horn et al., 1995), so this species also may exhibit terrestrial ureotelism. Ip et al. (2002) have identified a number of strategies for amphibious fishes to cope with ammonia production and pH changes while out of water. The physiological mechanisms that allow California intertidal fishes to survive out of water for long periods of time are of particular interest for future studies.

Movements and Homing Resident intertidal fishes recognize features of their complex environment well enough to choose specific microhabitats. After swimming out of their home pools, presumably to forage, several species of sculpins excel at finding their way back to these pools (Yoshiyama et al., 1992; Pfister, 1992). The tidepool sculpin can find its home pool from as far way as 100 meters, and woolly sculpins return to the same pools every day (Williams, 1957; Richkus, 1978). Juvenile opaleye normally inhabit low pools during an ebb tide, but they move higher in the intertidal zone during high tides (Williams, 1957).

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Some intertidal fishes move between pools but rarely travel more than a few meters, as indicated by mark and recapture studies or telemetry (Stephens et al., 1970; Richkus, 1978), The monkeyface prickleback, one of the larger resident intertidal fishes and a species more abundant in boulder fields than in tidepools (pers. obs.), moves less than 1 m2 per day based on ultrasonic tracking (Ralston and Horn, 1986). When resident fish are removed experimentally from tidepools, member of the same species occupy the vacated habitat (Grossman, 1982). This process, however, may take many weeks (Matson et al., 1986), even in a broad expanse of rocky intertidal habitat with numerous intact pools nearby as sources of newly occupying fish. Out of water, fish obviously move about differently than when swimming. Sculpins on land generally use their pectoral fins as levers while balanced on the body and tail in a tripod stance. Members of the sculpin family actively emerge from hypoxic water by pushing off the substratum with their tails (Martin, 1991, 1996; Yoshiyama et al., 1995). Elongate intertidal fishes, such as pricklebacks, can slip into crevices between rocks, a behavior probably most often used to avoid predators. Although capable of thrashing and directional sinusoidal locomotion, pricklebacks probably move little during low tides (Ralston and Horn, 1986; Horn and Gibson, 1988). The rockweed gunnel, another elongate remainer, weaves its body between fronds of intertidal seaweeds such as the fucoid brown alga Sylvetia compressa, where it emerges, until the tide returns as high as 0.5 m above the substratum if the seaweed is attached atop a large boulder (Burgess, 1978; Martin, 1993).

Agonistic Behavior, Interference Competition, and Territoriality Interspecific interactions among fishes of intertidal habitats in temperate latitudes are not well studied. Nevertheless, such interactions ought to be expected especially among resident species, given the numerous co-occurring species and limited space of the habitat. As Gibson and Yoshiyama (1999) point out, major limitations to testing these expectations involve the turbulence of the rocky shore environment and the evasive and cryptic nature of the fishes. Of the relatively few studies that have been completed on interspecific interactions among intertidal fishes in California or the Pacific Northwest, most were focused on sculpins. Several of these investigations have failed to detect aggressive behavior or territoriality among species (Green, 1971; Nakamura, 1976; Cross, 1981; Grossman, 1986a; Pfister, 1995), and both Cross and Grossman concluded that any competition among the fishes they studied is of the exploitative, not of the interference, type. Nevertheless, various observations and qualitative studies of the woolly sculpin, one of the most abundant resident intertidal species in California, suggest that this species through its aggressive behavior may have a negative influence on the distribution and abundance of other intertidal fishes (see Gibson and Yoshiyama, 1999). Field experiments are needed to test for this possibility. Part of the reason for the seeming lack of interspecific aggression among intertidal fishes may lie in their limited contact with each other, based on studies by Davis (2000b) in southern California on a guild of five co-occurring species—woolly sculpin, opaleye, rockpool blenny, California clingfish (Gobiesox rhessodon), and spotted kelpfish. She found that these species partitioned

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tidepool habitats spatially and seasonally and reasoned therefore that contact was limited and that interference and exploitative competition were reduced, at least during low tide. Even though the four species of pricklebacks that commonly co-occur in rocky intertidal habitats on the central California coast often shelter beneath the same individual boulder at low tide (pers. obs.), laboratory experiments carried out by Jones (1981) suggest that aggressive interactions and competitive exclusion occur among them. Jones first established that the high cockscomb is found associated significantly more often with sandy substrata in the habitat at low tide than the monkeyface prickleback, black prickleback, or rock prickleback, all three of which are associated more frequently with rocky substrata. In isolation in the laboratory, the high cockscomb preferred rocky substrata. Jones then set up one-on-one species experiments with one high cockscomb and one individual of one of the three other prickleback species and with substratum type (sandy or rocky) as the treatment to test the hypotheses that a sandy substratum is suboptimal for all four species and that the high cockscomb is relegated to this substratum type by interference competition from each of the three other species. The findings supported his hypotheses: all four species preferred rocky substrata, and the high cockcomb occurred more frequently on sandy substrata in the presence of individuals, especially larger ones, of any of the three other species. The experiments, however, were conducted under simulated high tide conditions and were designed to represent what is rarely seen in the intertidal zone, that is, the behavior of fishes during high tide.

Sensory Systems When intertidal fishes are out of the water, they encounter light rays with a different refractive index in air than in water, sound waves that travel slower in air than in water, and a lateral line system that cannot function in air. Fishes have eyes with round lenses, not elliptical lenses as do terrestrial vertebrates, and accommodate for near vision by moving the lens (Graham, 1971). Mudskippers, however, which are among the most terrestrial of fishes, have a flattened lens adapted to aerial vision (Graham, 1971), and rockskippers, another highly amphibious group, have a flattened cornea (Graham and Rosenblatt, 1970). The eyes of California intertidal fishes, including remainer or tidepool emerger species that generally emerge only during low tides, have not been studied. These species, however, clearly respond when on land to visual stimuli by evasion (pers. obs.), perhaps as a survival mechanism to avoid potential predators. Sound is probably not used for communication by most intertidal fishes because of the consistent background noise from the surf and their lack of a swimbladder that could serve as a resonating organ. One exception is the plainfin midshipman, which has a swimbladder modified for sound production. Male midshipman congregate in the intertidal zone during the spawning season and form mating choruses that are loud enough to be heard by nearby humans (Brantley and Bass, 1994; pers. obs.). Lateral lines sense near-body movement and water displacement with hair cells that can function only under water. All aquatic vertebrates, including larval amphibians, possess lateral lines, but no terrestrial animals do, including most adult amphibians. Some highly amphibious skippers have a greatly reduced lateral line system (Zander, 1972). On the other hand, a comparison of 12 species of Mediterranean

blennies shows no clear correlation of vertical zonation with lateral-line development, but a trend toward shortened lateral lines and fewer pores occurs among intertidal species (Zander, 1972). Anatomical features of the lateral line have not been studied in California intertidal fishes. Chemosensory structures also are unstudied among California shore fishes, but, given the known homing abilities of a number of the species, such structures may be important in a variety of taxa.

Reproduction Spawning and Parental Care Resident intertidal fishes live and reproduce in the rocky shore habitat and exhibit different ways of protecting their offspring (Coleman, 1999; DeMartini and Sikkel, chapter 19, this volume). Typically, resident species lay demersal rather than planktonic eggs. The eggs are sometimes attached to a rocky substratum, to seaweeds or seagrasses, or only to one another. Pricklebacks, a group that contains resident intertidal species, have external fertilization and lay eggs that adhere to one another but not to the substratum. In these fishes, a parent guards the egg mass and keeps the eggs from being washed away or consumed by predators, remaining with them even when low tides expose them to air (Marliave and DeMartini, 1977). As an indication of the importance of turbulence to fishes that spawn in the intertidal zone, the black prickleback spawns in protected locations on rocky shores during the storms of late winter but in more exposed locations during the calmer conditions of spring (Marliave and DeMartini, 1977). The plainfin midshipman exhibits another variation on parental care of eggs in the intertidal zone. Territorial males establish under-boulder nest sites and mate with multiple females (Crane, 1981). These males then guard the eggs that are attached as a single layer on the underside of a boulder until the well-formed young fish break free and swim on their own. In this case, the eggs adhere to the substratum, not to each other as in the coherent, but unattached mass formed by pricklebacks. At least two live-bearers, reef perch (Micrometrus aurora) and dwarf perch (M. minimus), are associated with rocky intertidal habitats as transient species and occasionally may bear their young there (Hubbs, 1921; Warner and Harlan, 1982). Not surprisingly, sculpins, the most species-rich group of fishes in the California rocky intertidal zone, show highly diverse forms of reproduction, including the rocky shore habitat. Resident species such as the fluffy sculpin and bald sculpin spawn demersal eggs in tidepools (Morris, 1952, 1956). The cabezon (Scorpaenichthys marmoratus) migrates to the intertidal zone to spawn, and its conspicuous eggs are highly toxic to vertebrates (DeMartini and Sikkel, chapter 19, this volume). The buffalo sculpin (Enophrys bison) spawns in the low intertidal zone, and the male guards the eggs and fans them with his pectoral fins (DeMartini, 1978). Sharpnose sculpin (Clinocottus acuticeps) spawn beneath fucoid brown algae (Fucus sp. or Sylvetia sp.) in the high intertidal zone to prevent desiccation while increasing the exposure of eggs to oxygen (Marliave, 1981). Males of scalyhead sculpin (Artedius harringtoni) guard eggs in the intertidal zone (Ragland and Ficher, 1987). To add to the diversity of reproductive behavior in cottoid fishes, the female grunt sculpin (Rhamphocottus richardsonii) have been observed in aquaria to chase the male into caverns and to trap him there until she lays her eggs (Eschmeyer et al., 1983).

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Eggs laid in the intertidal zone may be exposed to air for extended periods during extreme low tides. These exposed eggs may accrue certain advantages as long as desiccation is prevented (Strathmann and Hess, 1999). For example, increased oxygen availability and higher temperatures may speed development and thus reduce the chances of egg mortality from hypoxia or from aquatic predation. Eggs of Pacific herring (Clupea pallasi), which are spawned on seagrasses in the low intertidal zone, survive better than eggs laid in subtidal habitats, presumably because of reduced predation in the intertidal zone (Jones, 1972; Blaxter and Hunter, 1982).

Recruitment The larvae of most intertidal fishes that have been examined spend about 1 to 2 months in the plankton (Stephens et al., 1970; Marliave, 1986; Stepien et al., 1991), a range of times influenced by temperature fluctuations, spawning dates, and current patterns. Despite a period of planktonic existence, the larvae of rocky intertidal fishes dipserse only short distances and tend to stay within the area in which they were hatched (Marliave, 1986). These results were corroborated by Setran and Behrens (1993) who found that larvae of black prickleback, rock prickleback, and monkeyface prickleback declined in density offshore and somehow avoided offshore and perhaps longshore drift. For sculpins, kelpfishes, and other tidepool-oriented fishes, the larvae are likely to settle on the same substratum as the adult fish prefer although higher on the shore (Marliave, 1977; Pfister, 1995). High intertidal pools may act as refuges for small intertidal fishes because lower pools hold larger individuals (see above). Pfister (1995) found little evidence for competitive interactions in recruitment of three species of intertidal sculpins to tidepools and no effect of the presence of an adult on the distribution of species among recruits to a particular pool. In addition, the number of recruits do not necessarily correlate well with the number of adult females or with the number of adults in subsequent years (Pfister, 1999). For pricklebacks, which associate more closely with the gravel and cobble of boulder fields, the preferred substratum does change as the fish grow in size after settlement. This statement is based on the work of Setran and Behrens (1993), who found in laboratory experiments that, soon after settlement (17–22 mm total length, TL), both rock prickleback and monkeyface prickleback prefer gravel and cobble; then at 30–36 mm TL they preferred cobble over gravel, apparently because the latter provided insufficient interstitial space for larger juveniles. These experiments corroborated the field collections made by Setran and Behrens and supported the view that the physical characteristics of the substratum are important for microhabitat selection by the two prickleback species. Substratum preference and microhabitat selection by the different types of rocky intertidal fishes are complex but important subjects that deserve further study and probably will require long-term data sets to unravel.

Community Structure and Function The concept of community faces special scrutiny when applied to intertidal fish assemblages. Given the dynamic nature and relatively small size of the rocky intertidal zone, questions arise as to whether such a habitat supports groups of

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populations that are predictable in space and time or whether the species at a particular locality are merely stranded there at low tide and thus participate minimally in the intertidal ecosystem. The results of numerous studies show that the former is the case and that intertidal fish faunas clearly offer examples of the community, if it is defined as a group of populations living in the same place (Fauth et al., 1996; Ricklefs and Miller, 2000). This definition works particularly well for rocky intertidal fish communities in the sense that they are demarcated sharply by the land on one side and separated abruptly along the shore by stretches of sandy beach or muddy river mouths. The distinction, however, is blurred to the seaward at the intertidal/subtidal boundary, as revealed in the ecological classification described in chapter 4 (this volume). In full, the intertidal fish community consists of both resident species that live year-round in the habitat and transient species that enter the intertidal zone from adjacent waters only at high tide. This mixed composition demonstrates the complex and dynamic nature of intertidal fish communities and, again, challenges the concept of community. As observed by Gibson and Yoshiyama (1999), resident species have received greater attention because they are more interesting to study as a result of their presumed adaptations to an extreme habitat and are easier to study because they can be sampled at low tide. Despite the changing species composition of intertidal fishes on a diel basis and the unbalanced treatment of resident versus transient species, this section of the chapter attempts to describe the intertidal fish community as a whole. Focus is placed on certain interrelated components of community structure and function (Ricklefs and Miller, 2000), species diversity and relative abundance, age composition, trophic relationships, and resilience to perturbation. The overall goal of the section is to identify the members of the community and the interactions that tie them together into an intricate web.

Taxonomic Composition Intertidal fish communities on California and northern Baja California shores are dominated by advanced acanthopterygian (spiny-rayed) fishes, primarily in two orders— Scorpaeniformes and Perciformes, as would be expected from Hobson’s analysis of reef fish evolution in the northeastern Pacific (chapter 3, this volume). This dominance is seen in the family and species compilations for three geographic regions of California as well as northern Baja California (table 8-2; fig. 8-4). Among the scorpaeniforms, the Cottidae (sculpins) are represented in all regional rocky intertidal habitats, and the Scorpaenidae (rockfishes), Hexagrammidae (greenlings), and Liparidae (snailfishes) are frequently represented by one or more species. Among the perciforms, the families Stichaeidae (pricklebacks), Pholidae (gunnels), and Clinidae (kelpfishes) are relatively diverse and common, and one or another species of clingfish (Gobiesocidae) is consistently present in these habitats (fig. 8-5A). In the regional compilations shown in Table 2 and fig. 4, greenlings occurred only at northern California localities; graveldivers (Scytalinidae) only in central California habitats; and blennies (Blenniidae), nibblers (Girellidae), and labrisomids (Labrisomidae) only in southern California or northern Baja California. Pricklebacks were absent from both of these latter sites, and gunnels were not recorded in the rocky intertidal zone in southern California.

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TA B L E 8-2

Most Common Fishes Collected from the Rocky Intertidal Zone

% of Total

Common Name

Scientific Name

Black rockfish Grass rockfish Black-and-yellow rockfish Blue rockfish Kelp greenling Fluffy sculpin Tidepool sculpin Mosshead sculpin Woolly sculpin Bald sculpin Smoothhead sculpin Saddleback sculpin Cabezon Rosy sculpin Tidepool snailfish Opaleye Reef perch High cockscomb Monkeyface prickleback Black prickleback Rock prickleback Penpoint gunnel Rockweed gunnel Graveldiver Reef finspot Striped kelpfish Crevice kelpfish Spotted kelpfish Rockpool blenny Northern clingfish

Sebastes melanops Sebastes rastrelliger Sebastes chrysomelas Sebastes mystinus Hexagrammos decagrammus Oligocottus snyderi Oligocottus maculosus Clinocottus globiceps Clinocottus analis Clinocottus recalvus Artedius lateralis Oligocottus rimensis Scorpaenichthys marmoratus Oligocottus rubellio Liparis florae Girella nigricans Micrometrus aurora Anoplarchus purpurescens Cebidichthys violaceus Xiphister atropurpureus Xiphister mucosus Apodichthys flavidus Xererpes fucorum Scytalina cerdale Paraclinus integripinnis Gibbonsia metzi Gibbonsia montereyensis Gibbonsia elegans Hypsoblennius gilberti Gobiesox maeandricus

California clingfish

Gobiesox rhessodon

Northern California

Central California

Southern California

Northern Baja California

6% 4% — — 2% 28% 7% 2% 1% 1% — — 6% — 2% — — 2% — 11% 8% 7% 2% — — 2% — — — 2%

— — 1% 1% — 2% — — 2% — 3% 2% 1% — — — — 2% 4% 25% 12% 1% 18% 1% — 2% 5% — — 11%

— — — — — — — — 50% 1% — — — — — 24% — — — — — — — — 5% — — 7% 4% —

— — — — — 3% — — 20% — 4% — — 10% 1% 8% 2% — — — — — 4% — — 8% 12% 22% — —

—

—

7%

1%

NOTE: Includes species
1% identified by cluster analysis (see Chapter 4) for four latitudinal regions of California and northern Baja California. Occurrences and abundances derived from all sources used in the analysis. See Fig. 4 for a pictorial representation of most species in the four regions.

With few exceptions, the intertidal fish communities of California and northern Baja California comprise species of cold-water affinities (chapter 1, this volume). Both the sculpins and the rockfishes of the genus Sebastes occur only in the Northern Hemisphere as do the other scorpaeniforms represented (greenlings and snailfishes). Pricklebacks, gunnels, kelpfishes, and the graveldiver among the perciforms also have cold-temperate distributions. In contrast, nibblers, labrisomids, and blennies occur primarily in warm-temperate or tropical waters. Surfperches (Embiotocidae) are distributed broadly in warm- and cold-temperate latitudes of the northeastern Pacific, and clingfishes are represented worldwide in temperate and tropical habitats.

Species Richness and Relative Abundance Taxonomic compilations for four California and northern Baja California localities show that fish species richness is highest in Northern and central California (table 8-2, fig. 8-4). Eighteen species are listed for northern California, 17

for central California, 12 for northern Baja California, and only seven for southern California. At the family level, the Cottidae are represented by the most species in all four regions. Although differences in sampling effort must be taken into account, the regional differences in species richness may reflect the prevalence of cold-temperate fishes, especially sculpins, in the northeastern Pacific and their increased presence at higher latitudes and in areas of strong upwelling as in northern Baja California. A similar picture of dominance prevails in the numbers of individuals apportioned among families and species. Summaries of relative abundance based on the compilations from all sources (table 8-2) show that sculpins account for the largest proportion of individuals in northern California (46%) and southern California (51%) and the second largest proportion in northern Baja California (37%). Particularly abundant sculpins are the fluffy sculpin in northern California and the woolly sculpin in southern California and northern Baja California. The general abundance of these two sculpins at several northern and central California collection sites is illustrated in fig. 8-5b. In central California, sculpins are

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F I G U R E 8-4 Pictorial representations of common fish species from rocky intertidal habitats in northern California, central California,

southern California, and northern Baja California.

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F I G U R E 8-5 Proportional abundances of rocky inter-

tidal fish families (A) and species of Cottidae (B) at six localities on the California coast. The names, latitudes, and references for each locality are given between the graphs. In (B) the genera represented by the major species are Clinocottus, Oligocottus, Artedius (A. lateralis), Ascelichthys (A. rhodorus), and Scorpaenichthys. Common names are C. analis (woolly sculpin), C. globiceps (mosshead sculpin), O. maculates (tidepool sculpin), O. rubellio (saddleback sculpin), O. snyderi (fluffy sculpin), A. rhodorus (rosylip sculpin), and S. marmoratus (cabezon) (after fig. 8-2 in Gibson and Yoshiyama, 1999).

replaced as the most abundant intertidal species. Here, collection summaries reveal that members of the Stichaeidae (43%) and Pholidae (19%) are the predominant species, in particular, black prickleback and rockweed gunnel. In northern Baja California, the Clinidae (42%) are the best represented family, especially by spotted kelpfish.

Residents and Visitors Part of the complexity and dynamics of intertidal fish communities results from the differing periods of time that various species spend in the rocky shore habitat. As already mentioned, some species spend virtually their entire lives between the tidemarks, whereas others visit only briefly at high tide. A continuum of types exists between these extremes and has led to several attempts to classify intertidal fish faunas accordingly. Gibson and Yoshiyama (1999) point out, however, that all such attempts reach the same basic distinction that the community consists of residents, species that live permanently in the intertidal zone, and transients, which are species that visit the habitat for differing lengths of time during their lives. Nevertheless, these variations in occupancy of the habitat lead to some further, potentially useful distinctions along the continuum of intertidal species (Gibson and Yoshiyama, 1999). Primary residents are those small, cryptic species that are the typical (Breder, 1948) inhabitants, and to show various specializations for intertidal life. They settle out of the plankton as larvae and transform into juveniles, then grow to adults, reproduce, and

live out their lives in the intertidal zone. In contrast, secondary residents (Thomson and Lehner, 1976) are mainly larger, subtidal species that reside as juveniles in the intertidal zone for varying lengths of time and then as adults enter the habitat for breeding or foraging at high tide, daily or seasonally. Still other species occur as casual visitors that feed over the intertidal zone at high tide then occasionally become trapped in pools at low tide. Unlike both resident and transient species, casual visitors probably play only minor roles in the ecology of rocky intertidal communities. On California shores, the proportions of primary and secondary residents and transient species vary widely in both species and individual fish (table 8-3). For a series of northern and central California rocky intertidal sites, the proportions of primary residents range from less than a third to more than 80% of the total species, whereas secondary residents comprise less than half and transients a third or less of the species, depending on the location. In proportions of individuals, primary residents rise to greater prominence and account for more than 90% of the total fish at most of the sites sampled. These high proportions of year-round species are not surprising, given that the collections were made at low tide when the smaller, bottom-associated fishes commonly thought of as residents would be captured with greater likelihood than the more mobile and often pelagic secondary residents or transients. Comparisons between widely separated geographic regions in the world are difficult because equivalent categories are seldom used. Despite this difficulty, a broad range of proportions

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TA B L E 8-3

Proportions of Primary Residents, Secondary Residents, and Transients in Rocky Intertidal Assemblages at Five Northern and Central California Localities

Primary Residents Locality (N Latitude)

Secondary Residents

Transients

Totals Numbers

Sp

Ind

Sp

Ind

Sp

Ind

Sp

Ind

Reference

42% 31% 83% 73%

? 77% 94% 92%

45% 35% 17% 27%

? 19% 6% 8%

13% 35% — —

? 3% — —

31 29 12 11

1599 2857 62 64

Moring, 1986 Grossman, 1982 Boyle, 2004 Boyle, 2004

Trinidad Bay (41° 31’) Dillon Beach (38° 15’) Dillon Beach (38° 15’) Pescadero Point (37° 14’) Pescadero Point, Bean Hollow, and Pigeon Point (37° 14’)

54%

90%

33%

9%

13%

1%

24

3703

Yoshiyama, 1981

San Simeon (35° 39’)

40%

91%

33%

8%

27%

1%

30

3265

Boyle, 2004

NOTE:

Sp  % of species; Ind  individuals. After Table 1 in Gibson and Yoshiyama, 1999.

of residents and transients is seen in intertidal fish communities around the world (Gibson and Yoshiyama, 1999; Table 1). The extremes of proportions are illustrated in Gibson’s and Yoshiyama’s tabulation because the range extends from the absence of transients on certain South African shores (Prochazka, 1996) to the lack of residents in Maine tidepools where fish are absent in winter (Moring, 1990). These variations emphasize the fact that both resident and transient species play important roles in the structure of intertidal fish communities, but the degree depends greatly on season and geographic location.

Age Composition Most resident species of rocky intertidal fishes are relatively short-lived, mostly  5–6 years (Gibson, 1969; Stepien, 1990; Gibson and Yoshiyama, 1999), perhaps reflecting the small body size attained by most of these fishes. For example, the four species in the cottid genus Oligocottus occur commonly in tidepools in California and farther north and attain maximum sizes of only about 60–100 mm TL (Eschmeyer et al., 1983). Populations of O. maculosus in northern California are made up mostly of 0- and 1-year age classes and a smaller proportion of somewhat older fish (Moring, 1979). Another member of the genus, O. snyderi, can be represented in tidepools by as many as five age groups beyond the young of the year (Chadwick, 1976), but still within the small size reached by the species. Longer lived exceptions include some species of stichaeids, in particular, the monkeyface prickleback, estimated to reach 18 years of age (Marshall and Echeverria, 1992) and cabezon, reported to attain 13 years (O’Connell, 1953; Grebel, 2003). The monkeyface prickleback also is an exception in size as it is one of the largest resident intertidal fish, attaining a length of 760 mm SL (Marshall and Echeverria, 1992). In fact, however, the larger monkeyface pricklebacks live lower on the shore or, like the cabezon, which reaches nearly 1 m in length (Eschmeyer et al., 1983), become associated with subtidal reefs (pers. obs.; chapter 9, this volume). These examples of increasing depth of occurrence with age indicate spatial differences in age structure within fish species that occur mainly during the early part of their lives in the intertidal zone. Information showing that some marine fish species are represented mainly by young fish in the intertidal zone leads to

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the supposition that rocky intertidal habitats are nursery areas for subtidal species. The examples above involving cabezon and monkeyface prickleback lend support to this suggestion, but too few studies of intertidal fish communities in California have provided detailed age structure data on community members to make a strong case for a nursery function of the habitat. Nevertheless, our compilation of the proportion of juveniles for 12 species of fishes collected in 18 quarterly samplings from a tidepool near Piedras Blancas on the central California coast shows that, with one exception, the majority or all individuals collected were juveniles (table 8-4). Although other species were captured in the tidepool, the list of species here is limited to those for which age at maturity information is available. The data in Table 4 provide evidence for a nursery role for this central California intertidal habitat, but further studies and support are required to establish unequivocally that rocky intertidal habitats serve a nursery function. This challenge is heightened with the proposal (Beck et al., 2001) that to qualify as a nursery ground, an inshore habitat must contribute to a greater production per unit area of individuals that recruit to adult populations than that of other habitats in which juveniles occur (see chapter 5, this volume). Clearly, further research is needed in this area of intertidal fish ecology.

Trophic Interactions The majority of intertidal fish species are either carnivores or omnivores (table 8-5). Most fishes that feed in rocky intertidal habitats in California and other temperate regions consume benthic invertebrates, especially copepod, amphipod, and decapod crustaceans; other invertebrates, such as mollusks and polychaetes, are less important dietary items as are larger crustaceans, fishes, and algae (fig. 8-6; Grossman, 1986a; Gibson and Yoshiyama, 1999; Horn and Ojeda, 1999; Norton and Cook, 1999). The rarity of herbivores parallels that found in other temperate-zone marine habitats and continues to inspire speculation as to cause (e.g., Gaines and Lubchenco, 1982; Horn, 1989; Horn and Ojeda, 1999). The two California intertidal fishes that rely most heavily on macroalgae as an energy source are the monkeyface prickleback and the rock prickleback. Feeding and digestion in these two species have been the subject of several studies in recent decades (e.g., Montgomery, 1977; Barton, 1982; Horn et al. 1982, 1986, 1995; Fris and

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TA B L E 8-4

Proportions of Juveniles in 18 Samples Collected from a Tidepool on the Central California Coast Near San Simeon from 1979 to 1983

Family

Total No. Collected

% Juveniles

Plainfin midshipman Gopher rockfish Black-and-yellow rockfish Grass rockfish Black rockfish Olive rockfish Cabezon High cockscomb Monkeyface prickleback Black prickleback

Batrachoididae Scorpaenidae Scorpaenidae Scorpaenidae Scorpaenidae Scorpaenidae Cottidae Stichaeidae Stichaeidae Stichaeidae

20 17 3 3 1 1 5 70 135 673

0 94 67 100 100 100 100 93 98 64

Rock prickleback

Stichaeidae

144

85

Common Name

TA B L E 8-5

Relative Abundance of Species 4 by Trophic Category in Four Rocky Intertidal Fish Assemblages on the California Coast

Carnivore

Omnivore

Herbivore

Total No. Species in Sample

Dillon Beach (38° 15’) Dillon Beach (38° 15’) Pescadero Point (37° 14’)

86% 40% 56%

7% 40% 33%

7% 20% 11%

15 10 9

% food mass Average % food mass Average % food mass

Grossman, 1986a Boyle, 2004 Boyle, 2004

San Simeon (35° 39’)

50%

36%

14%

14

Average % food mass

Boyle, 2004

Locality (N Latitude)

Basis of Assessment

Reference

N OTE : Carnivores arbitrarily classified as species with 5% plant material in diet, omnivores as those with 5–69%, and herbivores as those with diets of 70% plant material. After Table 2 in Gibson and Yoshiyama, 1999.

Horn, 1993, Chan et al., 2004; German et al., 2004). Omnivorous fishes, which consume a mixture of seaweed and animal material (table 8-5), are more common than strict herbivores in California intertidal habitats and include woolly sculpin, mosshead sculpin, and reef perch (fig. 8-4; Grossman, 1986a). Perhaps the availability of a diverse and abundant standing crop of algae on California rocky shores has led to its use as part of the diet in some species, as intertidal fish communities have evolved under a scenario of food resource partitioning proposed by Grossman (1986a). The food webs involving intertidal fishes and the fish assemblages in other California marine habitats are analyzed in chapter 14 (this volume). Ontogenetic shifts in diet appear to be a common feature in the life history of intertidal fishes. As pointed out by Norton and Cook (1999), intertidal fishes commonly increase twofold to fourfold, but as much as 15-fold, in length from metamorphosis to adulthood. With this growth, they change their diets, either qualitatively by adding or dropping items from the diet or quantitatively by changing the relative importance of prey types or the size of given prey items. One of the most dramatic qualitative shifts among California intertidal fishes is that documented for the monkeyface prickleback and the rock prickleback. Both species begin to shift from carnivory to herbivory at about 45 mm standard length (SL) (Horn et al., 1982; Setran and Behrens, 1993), a size of only 6–8% of the maximum size recorded for these two species. Recent feeding experiments and digestive enzyme studies support the hypothesis that the shift is genetically fixed, because as these

two fishes increase in size the relative activities of their proteases and carbohydrases change even when the fishes are fed a high-protein diet (German et al., 2004). These two pricklebacks also exhibit quantitative shifts once they become herbivores because certain algae that are too tough for small fish to bite become increasingly important foods for larger fish (e.g., Miller and Marshall, 1987). Another qualitative ontogenetic shift in diet is seen in the woolly sculpin in which harpacticoid copepods and gammarid amphipods were commonly found in the diets of the smallest fish (34 mm SL) studied but dropped out of the diets of larger fish (
40 mm SL) to be replaced by crabs, limpets, chitons, and algae (Norton and Cook, 1999). These changes in diet observed in the woolly sculpin as it grows larger are typical of a common pattern in intertidal fishes: harpacticoid copepods and gammarid amphipods dominate the diets of the smallest fish to be replaced in ontogeny most often by crabs, fishes, and algae (see Norton and Cook, 1999; Table 2). Mouth size and biting strength increase with size in fishes and, therefore, allow fish to expand their diets and to consume variously larger, more abundant, or mobile prey (Norton and Cook, 1999). In simplest terms, small fish are limited to items that fit within their gape (mouth) because they cannot generate enough force to bite pieces from larger prey. Adding to the complexity of the ontogenetic change in diet is the fact that fish may change their attack strategy with an increase in body size. For example, the woolly sculpin appears to use ram feeding when young (Cook, 1996) and suction feeding as an adult

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F I G U R E 8-6 Diet spectrum of 14 fish species

(n  7–25) collected from three central California rocky intertidal habitats based on the average contribution of each prey type to the total food biomass for each fish (from unpubl. data in Boyle, 2004)

(Norton, 1991). Dietary shifts that involve different combinations of ram, suction, and biting attacks are likely to occur as well and deserve further study in California intertidal fishes. A prevailing notion is that herbivory and predation in the broader sense by fishes have little effect on the structure of temperate intertidal communities (e.g., Gibson, 1982; Horn, 1989; Raffaelli and Hawkins, 1996). Nevertheless, the question still seems open because too few studies have been conducted to test the impact hypothesis adequately. Norton and Cook (1999) list three kinds of information that can be used to assess the impacts of fish feeding on intertidal communities: (1) elaborate antipredator traits of potential prey organisms, (2) fish consumption estimates compared to prey production estimates, and (3) experimental manipulations of fish consumers and potential intertidal prey species. The evidence that Norton and Cook assemble on these three sources of evidence is drawn from a wide array of inshore habitats but is sparse for temperate, rocky intertidal communities. Three intriguing examples of potential impacts of fishes on intertidal organisms in California can be mentioned in the context of the Norton–Cook framework. The first example is of an antipredator trait. The chemical defenses found in the foot of the limpet, Collisella limatula, is effective against intertidal fishes and crabs but not against sea stars, octopi, or gulls (Pawlik et al., 1986). The implication is that the evolution of this trait was driven at least in part by fish predation. A second case is that of grazing by the high cockscomb on the distasteful polychaete worm, Cirriformia luxuriosa, interpreted by Yoshiyama and Darling (1982) as an example of circumventing an antipredator mechanism possibly in a coevolved rela-

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tionship. Apparently, the high cockscomb is the only intertidal fish that feeds on this worm and thus may gain access to an otherwise little-used food resource. A third example is that of the selective feeding by the mosshead sculpin on sea anemones, as shown in dietary studies by Grossman (1986a) and confirmed in laboratory experiments by Yoshiyama et al. (1996a,b). Grossman proposed that sustained feeding by the fish on sea anemones could have a significant impact on biomass production and relative abundance of anemones in rocky intertidal habitats. In all three of the foregoing examples, manipulative experiments are needed to provide further insights into the relationships described. A marked example of a grazing impact on algae by an intertidal fish has been documented in experimental field manipulations not in California but in Chile showing that an herbivorous blenniid fish (Scartichthys viridis) exerts a strong effect on macroalgal abundance and diversity in the intertidal zone of the central Chilean coast (Ojeda and Muñoz, 1999). We are not aware of a similar type of experimental study on fish–algae grazing relationships in the intertidal zone of California. Assessing the potential impacts of fishes on rocky intertidal communities in California is clearly open for investigation.

Stability, Resilience, and Persistence One of the enduring questions about communities is whether their structure, basically species composition and relative abundance, changes over time or whether the structure persists for years and decades. Long-term studies obviously are required

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to test for community persistence and, therefore, are likely to be few in number for most systems. The increased interest in environmental monitoring and assessment, however, promises to lead to increasing numbers of long-term studies that will allow more tests of community persistence. According to Gibson and Yoshiyama (1999), the most comprehensive studies on the persistence of intertidal fish communities have been conducted on the west coast of North America. A tidepool on the central California coast near Piedras Blancas, defaunated quarterly over a 5-year period (1979–1983) followed by another year of quarterly fish removals about 20 years later (2000–2001), revealed a high degree of persistence in the assemblage (Horn, Allen, and Boyle, unpubl. data). For example, two species, black prickleback and northern clingfish (Gobiesox maeandricus), ranked first or second in all 23 sampling periods; the former species ranked first 19 times and second four times. Together, these species accounted for 35–70% of the total individuals collected in each sampling period. Of the total list of 30 species captured during the entire study period, five species made up 67–78% of the individuals collected. In addition to the two species mentioned before, the top five species usually included the rock prickleback, monkeyface prickleback, and penpoint gunnel (Apodichthys flavidus). Other studies conducted in California rocky intertidal habitats also have shown some degree of persistence. An intertidal fish community sampled at Dillon Beach on the north-central coast during a 42-month period was interpreted as deterministically structured based on the persistence of relative abundances of species (Grossman, 1982, 1986b). Although the top three species fluctuated from year to year and the relative abundances of species changed somewhat, the overall structure remained unchanged statistically. At Pescadero Point, another central California site, the intertidal fish community exhibited some degree of constancy, but the fluffy sculpin, one of the primary resident species, had declined noticeably in abundance after 7 years (Yoshiyama, 1981; Yoshiyama et al., 1986). As Gibson and Yoshiyama (1999) observe, species abundances are bound to change somewhat from year to year as a result of variations in spawning and recruitment under differing environmental conditions. Repeated defaunations of tidepools during varying time periods have been conducted in California affording a test of whether intertidal fish communities are stable and resilient, two other temporal measures of community structure related to persistence. These two features refer to the ability of a community to maintain its structure in the face of environmental perturbations and to recover from intermittent disruptions of that structure. Grossman (1982) showed that a resident fish assemblage at Dillon Beach subjected to repeated defaunation over a 29-month period recovered and therefore showed resilience to this type of disturbance. Polivka and Chotkowski (1998) removed the fishes from tidepools near Piedras Blancas during a 90-day period and found that after one or two removals the recolonization involved the same dominant species but that the less common species in the assemblage were more variable in composition and abundance. Species diversity was restored after 60–90 days, but some species were depleted in the area during this period. These results suggest that the rarer or patchily distributed species may not recover from external disturbances as well as the more common and uniformly distributed species. In addition, the restricted movements of many intertidal fishes (Moring, 1976; Gibson, 1999) may limit their capacity to

recover from local depletion of their populations. The rate and amount of recovery appears to depend on the severity of the disturbance and the magnitude of repeated removals. For example, Alaskan intertidal fishes required two or more years to recover from the Exxon Valdez oil spill (Barber et al., 1995), and intertidal organisms including fishes may require years to recover from continuous, heavy collecting (Moring, 1983).

Influence of Climate Change As evidence has mounted in recent decades for accelerated global climate change, especially warming on different temporal scales (e.g., Pittock, 2002), increased attention has been focused on the potential impacts of this change on marine organisms (e.g., Fields et al., 1993; Scavia et al., 2002). In the northeastern Pacific, the increase in sea surface temperature that has already been documented (Smith, 1995; Sagarin et al., 1999; Bograd and Lynn, 2003) may be expected to cause a northward shift in the ranges of at least some species as it did during warming after the Pleistocene glaciations (Hubbs, 1948). Of course, not all species will shift their ranges in response. If their rate of northward migration is too slow to keep pace with the changes, they will either adapt genetically, live under suboptimal conditions, or perhaps go locally extinct. If climate change is not too extreme, some species may adjust phenotypically and thus tolerate climate change in place (Fields et al., 1993). Intertidal organisms might be expected to exhibit broad tolerances given the temporally dynamic environment in which they live (see Tomanek and Somero, 1999). Some northward shifts in abundance in response to climate change have already has been documented for intertidal organisms in California. Barry et al. (1995) and Sagarin et al. (1999) provided data to show that during a 60-year period (1931–1933 to 1993–1996) at Hopkins Marine Station on the central California coast, macroinvertebrates changed in abundance as related to geographic ranges of species. Ten of 11 southern species increased in abundance, five of seven northern species decreased, and widespread species showed no clear pattern with 12 increasing and 16 decreasing. Shoreline temperatures for the 60-year period increased by 0.79°C, whereas average summer temperatures increased by 1.94°C. This climatic warming explained the changes in abundance better than the alternative hypotheses of habitat changes, anthropogenic effects, indirect biological interactions, ENSO events, or upwelling episodes. In another study, focused on mussel (Mytilus californianus) populations, Helmuth et al. (2002) showed that climatic warming and timing of low tides in the northeastern Pacific produce more thermally stressful conditions at northern sites compared to southern sites and proposed that “hot spots” of extinction rather than poleward shifts of intertidal organisms may occur at northern sites. Intertidal fishes exhibit limited powers of dispersal (Marliave, 1986), and rocky intertidal habitats are separated by stretches of sandy or muddy shores (Horn and Ojeda, 1999), so that northward migration in response to ocean warming may not be an option for some species. Little attention has been focused on the responses of intertidal fishes to climate change although the removal study near Piedras Blancas, described above, that spanned the 1982–1983 El Niño and a 20-year period overall, showed little response by the fish assemblage to the El Niño or to the two-decade time frame

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F I G U R E 8-7 Abundance of (A) Clinocottus analis (woolly sculpin), a member of the cool-temperate family Cottidae and (B) Paraclinus integripinnis (reef finspot), a member of the tropical/warm temperate family Labrisomidae, in tidepools at two sites near San Diego, California, before, during, and after the 1997–1998 El Niño (after Davis, 2000a).

(Horn, Allen, and Boyle, unpubl. data). In a shorter term study, Davis (2000a) monitored the changes in assemblage structure and habitat use of a guild of intertidal fishes in response to ENSO conditions at two sites near San Diego, California, during the 1996–2000 time period. Although habitat use of the fishes was only slightly affected by the El Niño, two of the six species responded measurably to the fluctuating climate (fig. 8-7). The woolly sculpin, a member of the cooltemperate family Cottidae, decreased in abundance during the El Niño because of lack of recruitment but increased during the La Niña that immediately followed. In contrast, reef finspot, a member of the tropical/warm temperate family Labrisomidae, was more abundant during the El Niño. As climate change continues, further studies are warranted to document and predict changes in rocky intertidal fish assemblages in California.

Recommendations for Future Studies Several types of investigations are needed if we are to deepen our understanding of the way intertidal fishes, especially the resident species, survive and flourish in rocky intertidal habitats in California, and by extension, elsewhere. Comparative studies of intertidal fishes and their subtidal relatives seem particularly important to appreciate how resident species have been shaped, presumably through some combination of adaptive traits and phenotypic plasticity. Of critical interest is to advance our knowledge so we can protect and manage fishes that live in such small, vulnerable, and widely separated habitats at the interface of the land and sea. Here are

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some of the types of studies that seem worthy of attention in future research: 1. Compare air-breathing abilities in rocky intertidal fishes and their subtidal relatives from a phylogenetic perspective. Air breathing associated with emergence is complex and variable, occurring in numerous taxa and correlated to some extent with the vertical distribution of these species on the shore. The families Cottidae and Stichaeidae are well suited for comparative analysis. These two families are species-rich in both rocky intertidal and subtidal habitats in California. 2. Determine the contributions of the gills, skin, and other organs to respiratory gas exchange when the fish is in water and out of water. Histological examination, microsphere perfusion, and enzymatic assays for carbonic anhydrase will aid the elucidation of these structures and their functions. Biochemical assays of the hemoglobins in fish blood could illuminate the affinities to oxygen, the sensitivity to acid–base disturbances, and possibly the ontogenetic changes in the expression of different forms of hemoglobin, particularly for species in which the juveniles inhabit tidepools and the adults occur in deeper waters. 3. Compare the contributions of aerobic and anaerobic metabolism to the activity of intertidal fishes during aquatic and terrestrial locomotion. Especially intriguing would be to examine the possibility that metabolic acidosis caused by anaerobic terrestrial activity could be reversed by respiratory release of carbon dioxide

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from the gills. The potential accumulation of lactate under hypoxic aquatic conditions needs to be investigated as do the excretion of nitrogenous wastes and the excretory acid–base balance. These physiological studies need to be coupled with detailed field observations of the natural history and ecology of air-breathing fishes on California rocky shores. 4. Compare sensory structures, especially the eyes, lateral line, and chemosensory organs in rocky intertidal fishes with their subtidal relatives from a phylogenetic perspective. These organs are little studied among species in the rich California fauna, especially with research designed to test for adaptations to intertidal life. Again, the families Cottidae and Stichaeidae offer excellent opportunities for comparative analysis. 5. Investigate substratum preferences and microhabitat selection in larval fishes as they settle out of the plankton into the rocky intertidal habitat. Following how these preferences and selection processes change with age in tidepool versus boulder field species could be rewarding and might help explain patchy distributions on different spatial scales and even the limits of geographic ranges. The work by Setran and Behrens (1993) offers a good model for further studies. 6. Test the nursery-role hypothesis of Beck et al. (2001) for rocky intertidal and adjacent habitats in California. This role is often assumed for rocky intertidal habitats, but data are lacking. If tested as proposed, this demanding hypothesis could increase the appreciation of rocky intertidal habitats as nurseries and enhance the effectiveness of conserving and managing these habitats and their fish assemblages. 7. Design and implement field experiments to test for interspecific aggression among co-occurring fishes in the rocky intertidal zone of California. Most studies to date have failed to detect aggressive behavior or territoriality, but more research needs to be conducted during high tide or simulated high tide rather than only at low tide. The works by Jones (1981) and Pfister (1995) provide useful models for further investigation. 8. Design and implement field experiments to test for the impacts of herbivory and predation by fishes on the structure of rocky intertidal communities. The kinds of information that Norton and Cook (1999) recommend to assess the impacts of fish feeding on these communities are still sparse, especially in temperate waters including California. 9. Assess and predict the impacts of climate change from long-term monitoring of fish assemblages in rocky intertidal habitats of California. Climate change is likely to accelerate the effects of pollution or other stresses on rocky shore fishes through higher water temperatures and alterations in salinity, precipitation, and sea level. Marine reserves designed to protect intertidal communities should be planned with recognition of long-term changes anticipated as a result of climate change.

Acknowledgments We thank the many students and colleagues who have helped us in our own studies of rocky intertidal fishes over the years. Kelly

Boyle was particularly helpful to us in compiling data and constructing tables and figures for the chapter.

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CHAPTER 9

Rocky Reefs and Kelp Beds J O H N S. STE P H E N S, J R., RALP H J. LAR S O N, AN D DAN I E L J. P O N D E LLA, I I

Introduction

Historical Review

California’s kelp bed and rock-reef habitats are among the most spectacular marine habitats in the world, due in part to the assemblage of fishes that occupy these areas. In Chapter 3, two shallow subtidal reef assemblages associated with kelp beds and rocky reefs were discussed. These assemblages are discussed together in this chapter for several reasons. Kelp beds are largely restricted to rocky reefs because they depend on hard substrate for the attachment of holdfasts. The composition of fishes within these two habitat groups overlaps almost entirely because there are very few obligate kelp species. Kelp may be limited in its abundance and distribution by various factors, but most of the fishes associated with it are not susceptible to the same limitations. In fact, the abundance and distribution of kelp along California’s coastline fluctuates appreciably because of seasonal and annual variability and episodic events. Although the variability in the abundance and distribution of reef fishes responds to the presence and absence of kelp, it is only one of many factors that affect the distribution of these species. Thus, all of these nearshore reef fishes are treated together. Due to their accessibility, their ecological and commercial importance, the high diversity and abundance of fishes, and their sheer beauty, rocky reefs and kelp beds have been studied intensively for more than five decades. The diversity and abundance of the fish assemblage is higher than those in most other California marine habitats. Recent estimates suggest that this habitat supports between 6 and 15 times the density of fishes compared to a similar area of soft substrate (Bond et al., 1999). Rocky reefs and kelp beds are an important resource for the neritic fishes of California and are economically important (chapter 22). These, plus the aesthetic appeal of conducting research in such picturesque settings, are some of the major reasons that such a large body of research has been conducted on these fishes. In addition, much of what we know about the community organization (Unit III), behavioral ecology (Unit IV), and spatial and temporal changes (Unit V) of California marine fishes has been based on studies of rocky reef fishes. The major goals of this chapter are to describe that body of work, provide readers a feeling of where the field is today, and discuss avenues for research in the future.

Initial surveys in the nineteenth century, which were based largely on fishery landings, provided the first taxonomic descriptions and data on distributions for California fishes. By the late nineteenth century and early twentieth century, several guides to identification and distribution had appeared (e.g., Jordan and Gilbert 1881; Starks and Morris, 1907; Barnhart, 1936). Investigation of the biology of some groups (such as viviparity in embiotocids; see the review in Tarp, 1952) began in the nineteenth century and continued into the early twentieth century. By the postwar years, natural history information on a range of species was part of the fisheries lore (e.g., Cannon, 1953; Schenck, 1955), although not all of this was information was available in the scientific literature. Concern over increased levels of sport fishing after World War II, plus the general expansion of marine research, led to more focused studies of life history in a number of exploited species (e.g., O’Connell, 1953; Young, 1963). The advent of the scientific use of scuba, however, allowed the greatest expansion of research on fishes of rock reefs and kelp forests. Concern over the effects of kelp harvesting on sportfish abundance led to a long-term research program on kelp-forest ecology that was carried out largely with scuba. This produced Limbaugh’s (1955) pioneering descriptions of distribution and habitat preferences of kelp-forest fishes and Quast’s quantitative studies of the distribution, abundance, habitat utilization, and diet of kelp-forest fishes (North and Hubbs, 1968). Pequegnat (1964) published one of the first scuba-based descriptions of subtidal faunas. Department of Fish and Game biologists provided additional information on the habits and habitats of reef and kelp-forest fishes (Carlisle et al., 1964; Turner et al. 1968, 1969). The observations of Conrad Limbaugh and Charles Turner were published posthumously in Feder et al. (1974). These works are all important contributions to the body of knowledge on fishes of rocky reefs and kelp forests off California. Papers by Clarke (1970), Stephens et al. (1970), and Hobson (1971) were among the first observational/experimental studies on kelp-forest fishes that evaluated broader themes in ecology and led the way for many of the works discussed in this volume.

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Overview of Reef Structure

Overview of Kelps and Their Characteristics

The distribution of nearshore reefs varies throughout California. Along the mainland coast of the Southern California Bight and Baja California, rocky reefs are distributed patchily, separated by long stretches of sandy beaches, although this has varied over the glacial–interglacial cycles (Graham et al., 2003). Approximately 10–15% of the mainland of the southern California coast is rock, and this rock is primarily associated with headlands. The Southern California islands consist largely of rocky shorelines and constitute a substantial fraction of the rocky reef and kelp habitat off southern California. Because of these islands, there is as much coastline in the Southern California Bight as in the rest of the state of California. Rocky shorelines are predominant from Point Conception to the north, interrupted mainly by embayments such as Morro Bay, Monterey Bay, and San Francisco Bay, and by river mouths in the north. However, though it is possible to characterize the shoreline in many areas, the relief and extent of rocky bottom has not been determined for many portions of the California coast, making it nearly impossible to assess the extent of habitat for nearshore reef and kelp fishes and to assess their overall abundances. Shallow coastal reefs share their geological composition with the adjacent terrestrial shoreline. Both emergent and submergent shorelines occur in California, the result of eustatic changes from intrusions and crustal deformation as well as sea level changes from glacial modifications. The resultant rock formations can then be subject to burial by sedimentation (Graham et al., 2003). Rocky substrates can consist of boulders, sedimentary formations (sandstone, mudstone, shale), igneous formations (basalts, andesites), or metamorphic formations (schists, gneisses, and quartzites). Emery (1960) suggested that the latter three types of rock occur in a ratio of 90:7:3 in southern California, but this varies geographically. For example, the substrate between San Francisco and Monterey Bay is largely shale, whereas the substrate around the Monterey Peninsula and south past Pt. Lobos is composed largely of granite. The composition of rock reefs can affect reef ecology in at least three ways: the hardness of the reef matrix, the pattern of bottom relief, and the clarity of water over the reefs. Very hard rock resists modification by boring and scraping organisms and on a scale of centimeters, presents a smooth and uncomplicated surface. Softer rock allows burrowing by mollusks, such as piddocks and date mussels, and erosion by gastropods, echinoderms, etc., which provides small-scale habitat complexity and sites of protection for small benthic fishes. The composition of rock reefs may also affect habitat on a scale of meters. Sedimentary rocks often form relatively flat surfaces but do provide vertical relief and areas of broken rock (with attendant cavities used by fish and their prey) when tilted strata emerge and break off. Depending on the circumstances, igneous and metamorphic rock may form more continuous areas of boulders and rubble and higher vertical relief. The type of rock (along with many other factors) can also affect water clarity. Most sedimentary rocks produce finer particles when eroded than igneous or metamorphic rocks, and these particles reduce water clarity when suspended. In addition to rock reefs, extensive biogenic reefs are present in some areas. The colonial sand tubeworm, Phragmatopoma californica, can create extensive reef habitat that is used by fishes and as an attachment substrate for giant kelp.

The two major canopy-forming kelps off California are Macrocystis pyrifera and Nereocystis luetkeana (Abbott and Hollenberg, 1976; Foster and Schiel, 1985). Macrocystis pyrifera, or giant kelp, occurs along the Pacific coast from central Baja California to approximately Año Nuevo Island, between Santa Cruz and San Francisco. Occurring between depths of about 5 and 20 m (Foster and Schiel, 1985), M. pyrifera forms the bulk of the offshore kelp forests off southern California and much of central California. Young plants begin with a single stipe, but produce additional stipes as they mature (Tegner et al., 1996), and these stipe bundles may act as points of orientation or as shelter for fish in the midwater region (Quast, 1968b; Larson and DeMartini, 1984; Nelson, 2001). At the surface, stipes and fronds spread to form a canopy, which also serves as a point of orientation for fish and as shelter for some fish and invertebrates. Macrocystis is a perennial, although beds are thinned by wave action during the winter, especially in central California. Nereocystis luetkeana, or bull kelp, occurs primarily north of Pt. Conception and is common in waveexposed sites (Foster and Schiel, 1985). It may occur intermixed with giant kelp, or it may occur in monospecific stands. It is the only offshore canopy-forming kelp north of Año Nuevo. It grows as a single stipe with one float, from which large fronds hang. As a result, bull kelp may serve as a point of orientation in the water column for fishes, but it does not provide the same complexity of cover as giant kelp. In addition, bull kelp is an annual. Inshore of Macrocystis pyrifera and Nereocystis kelp beds, Macrocystis integrifolia and Egregia menziesii may occur in dense stands that also form canopies. Macrocystis integrifolia occurs primarily north of Point Conception. Together with surf grass, Phyllospadix sp., these organisms provide cover for fish and invertebrates in the shallow nearshore region. Offshore of giant kelp beds in southern California, Pelagophycus porra (elk kelp) extends into the water column and occasionally to the surface. It is not common, but it can form extensive beds. Cystoseira osmundacea sometimes co-occurs with M. pyrifera and forms dense masses of reproductive tissues in the summer that can serve as shelter for juvenile fishes. Likewise, Sargassum sp. can form canopies in winter–spring in southern California, especially in shallow water, and attracts some fishes normally associated with Macrocystis, such as kelp perch, Brachyistius frenatus. Several species of brown algae (Pterygophora californica, Laminaria farlowii and L. setchellii, Eisenia arborea, and Desmarestia ligulata) form understory canopies in some areas.

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Assessing Reef Fish Abundance Various techniques have been used to study the abundance of reef fishes. Some types of mobile fisheries gear (such as trawls and seines) are ineffective in kelp forests and rock reefs because the gear cannot be deployed. Stationary fishing gear (gill nets, traps, hook and line) can be deployed successfully in kelp forests, providing at least estimates of relative density. However, in the three-dimensional structure of a kelp forest, scuba gear has proved the most widespread method for assessing the abundance of kelp-forest fishes. Scuba-based techniques can provide estimates of relative density, or of absolute density, if the area sampled can be estimated. Increasingly quantitative methods for sampling have been applied to kelp forests, and quantitative habitat assessment techniques that

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are currently under development will prove valuable in assessing abundance. The distribution and abundance of rock-reef and kelp-forest fishes have been assessed with differing degrees of quantification and precision, and these different techniques have often been used to different ends. Range limits, or the presence/ absence of species in different regions, can be useful in the analysis of biogeography and evolution (Quast, 1968b; Horn and Allen, 1978; Hobson, 1994; chapters 1 and 2), and in the effect of climate change on distribution (Lea and Rosenblatt, 2000; Richards and Engle, 2001). Nonquantitative observations have been very useful in formulating the initial descriptions of habitat use and behavior in kelp-forest fishes (Limbaugh, 1955; Feder et al., 1974) and are always useful in formulating questions and hypotheses. Because they are not based on replicable measurements, however, the results of such studies cannot be evaluated or repeated. For example, without any indication of the effort expended in observation, it is difficult to evaluate comparisons of presence and absence, and nonquantitative notes on observations can be biased in a number of ways. Semiquantitative indices of distribution and abundance can provide greater information and can be replicated if the criteria for sampling and scoring are clear. For example, Engle (1993) used a consensus of observers to develop ordinal scores for abundance of fishes, which he then used to evaluate the geographical distribution of fishes on the southern California islands (see figure 9-10). Pequegnat (1964) included a somewhat greater degree of quantitative replicability in his assessments of 22 species of reef fish by basing counts on the total number of fishes counted by two observers throughout a dive (twin 2500 psi tanks). His index is a rough measure of catch per unit effort (CPUE), based on fish counted per unit of time. Systematic sampling surveys based on consistent levels of sampling effort can produce estimates of relative abundance (or CPUE) when the sampling area is unknown, estimates of density when the sampling area is known, and estimates of total abundance when the estimates of density can be extrapolated to the area of habitat that is to be represented. A number of techniques are available for assessing abundance; each has its own biases, advantages, and disadvantages. Traps, hook and line, spears, and gill nets can provide estimates of relative abundance (CPUE) of reef fishes. These techniques also provide the ability to obtain precise measurements of fish length, biomass, and maturity stage. They are also the techniques preferred by commercial and recreational fisheries (see chapter 23), allowing data to be obtained in cooperative endeavors. Fish traps are presently used extensively to capture rockfishes and sheephead for the live finfish fishery (Stephens, 1992; Love et al., 2002). Gill nets had been used for commercial fisheries in southern California kelp beds; they were outlawed within state waters in southern California (within 3 miles of the mainland and 1 mile of the islands) in 1992. They have been used in scientific monitoring programs (Pondella and Allen, 2000). Data from both gill nets and traps can be standardized as CPUE by dividing the catch by each net or trap set by soak time. In these studies, each fish is identified by species, measured, and weighed, allowing precise biomass and taxonomic information. Specimens can also be vouchered for museum collections. One drawback of these techniques is that they are invasive, potentially damage the substrate, and remove fishes from the environment when they cannot be returned alive. These techniques can also be biased toward more mobile fishes, those attracted to the bait used in traps, and those sizes of fish best captured or retained by the sampling device.

Hook and line has been used extensively to capture individuals for life-history and tagging studies (Young, 1963; Love et al., 1987). In these studies, relatively shallow water fishes, kelp bass and California scorpionfish, were caught, tagged, and released. Hook and line data can be standardized as CPUE. On a small scale, this technique is extremely variable because of the complex behavior of fishes. However, on a large scale, this data can be extremely valuable in describing regional and temporal trends (Love et al., 1998). These CPUE techniques afford the opportunity for tagging fishes prior to release. Recapture data has been used extensively to estimate stock size in other habitats and other parts of the world (Ricker, 1975). Mark and recapture/resighting techniques can provide direct estimates of abundance, and, unlike visual census techniques, are not biased against cryptic species and do not depend on accurate estimates of the amount of area sampled. However, they usually require marking a substantial portion of the population and that marked individuals mix randomly with the remainder of the population (Krebs, 1998). Martell et al. (2000) used mark and resighting techniques based on diver-applied dart tags and diver surveys to estimate the abundance of lingcod at sites in British Columbia. They used a Bayesian estimation technique to analyze the results of the mark/recapture survey, which allowed marking a smaller proportion of the population. In California, Davis and Anderson (1989) conducted a modified Schnabel (Ricker, 1975) mark and resighting experiment by capturing kelp-bed fishes with a subtidal electroshocker, tagging, releasing, and resighting them. In this study, they compared the estimates of fish abundance in belt transects, video transects, and baited stations to the density estimates from the modified Schnabel density estimates. Although they acknowledged the limitations of the mark and resighting technique, they concluded that all three techniques underestimated the density of kelp-bed fishes. They found that visual band transects gave the most accurate and precise density estimates. Electroshocking and the tag and resighting technique were noted to be labor-intensive and obviously dangerous. In a similar comparative approach, the rapid visual technique (RVT), which has been used in coral reef systems, was evaluated for this temperate system and found inaccurate (DeMartini and Roberts, 1982). Certainly, more comparative studies would be pertinent to this science. Probably the most daring attempt to quantify a reef fish assemblage was conducted by Quast and colleagues in the late 1950s when they used a wall net (similar to a purse seine) and rotenone to poison all fishes within a set area of a reef (Quast, 1968c). If practical, this technique would be the best for obtaining one-time estimates of absolute density and biomass. This technique was tried only three times, and Quast switched to “belt” transects (also referred to as band transects), originally developed by Brock (1954), which have become the standard technique used today. Belt transects and their variants are the most commonly applied sampling technique for kelp-forest fishes. In belt transects, divers swim a predetermined distance, usually along a measuring tape, and record on a handheld slate the number of all fishes seen within a certain distance of the tape. The slate may also contain a thermometer, depth meter, and a compass. If conducted consistently, belt transects can provide comparable estimates of relative abundance, and if the volume or area covered can be estimated accurately, belt transects can provide estimates of density. Belt transects were originally carried out near the bottom but have also been employed in the water

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FIGURE 9-1 Orientation of diver transects in kelp beds.

column and kelp canopy (fig. 9-1; Ebeling et al., 1980a,b; Stephens et al., 1984; Larson and DeMartini, 1984). If the belttransect sampling program is stratified over water-column position and on-offshore gradients, estimates of total abundance or water-column density can be obtained (Stephens et al., 1984; Larson and DeMartini, 1984). However, the accuracy of density estimates obtained from belt transects depends on the how accurately the volume or area sampled has been estimated. Variation in the volume or area sampled can also influence the degree to which estimates of relative abundance can be compared. A number of variations on the basic belt-transect method have been employed in California. First, the basic method of obtaining counts has been refined. Terry and Stephens (1976) and the Channel Islands National Park (Davis et al., 1999) used replicate counts from a pair of divers swimming along the transect line. Terry and Stephens (1976) used the highest counts for small schools and individuals and an average of estimates for large schools. This technique takes into account that single observers inevitably miss fish on transects, such as when they look at their slates, and in general provides the obvious advantage of replicated observation and averaging of potential observer biases. It has also been used as a training tool by the Channel Islands National Park (Davis et al., 1999). Logistically, this method may be easiest to implement on permanent transects or when a transect course is clearly determined. Another variation has been the use of film or videotape to record fishes (“cinetransects” of Ebeling et al., 1980a, b; Larson and DeMartini, 1984; DeMartini and Roberts, 1990). In the method of Ebeling et al., the camera is essentially used as the slate for recording fishes. Divers search for fishes along the course of the transect as if they were conducting a visual transect, but pan the camera over fishes as they are encountered instead of recording them manually. This method provides a permanent record, does not require the diver to divert attention to the slate while recording, and may allow counting large schools of fish frame by frame. However, the resolution of both film and videotape is less acute than the human eye, making some fish identifications difficult. In addition, this method requires considerable time in the laboratory for counting fish (a 5:1 ratio of laboratory observation to transect time according to Ebeling, 1982). Another variation in the conduct of belt transects is the means for determining their lengths. Permanent transect lines

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F I G U R E 9-2 Orientation of diver transects on breakwaters.

can be established for long-term monitoring (Davis et al., 1999), automatically fixing the length of a transect. Playing out a measuring tape or reel of line can also fix the length of a transect, but usually requires time to rewind before beginning another transect. However, Ugoretz et al. (1997) developed the use of retractable dog leashes for measuring the distance of underwater transects, avoiding the problem of rewinding the transect tape. Transect length has also been standardized by time. Timed transects, when swum at a constant rate, can allow time for a greater number of transects because the measuring tape need not be retrieved. The ability to conduct more replicates per dive allows greater precision per effort and is especially useful for deeper dives. In addition, deployment of a measuring tape can be difficult in the water column, over very rugose substrates, and on vertical walls. Terry and Stephens (1976) employed timed transects at King Harbor; these are swum along isobaths at fixed sections of the breakwater (fig. 9-2). The National Marine Fisheries Service used timed transects for juvenile rockfish off Northern

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California (Ralston and Howard, 1995; Adams and Howard, 1996), and the cinetransects of Ebeling et al. (1980a,b) were essentially timed (by the duration of a film cassette). If timed transects consistently cover the same distance, they can provide comparable estimates of relative abundance, and if the distance covered in timed transects can be determined, the transects can provide estimates of density (Ebeling et al., 1980b; Stephens et al., 1984; Larson and DeMartini, 1984). Larson and DeMartini (1984) found a standard deviation of about 5.2 m in the length of 12 simulated cinetransects in the kelp canopy, which was 6.9% of the average length of 75.6 m. The width of belt transects has also been determined in different ways. Quast (1968c) used the limits of visibility for his density estimates. However, later researchers have often used a fixed distance, usually 1–2 meters, for their density estimates. This reduces the variance in counts associated with changes in visibility and increases the accuracy of counts because the likelihood of fish detection decreases at greater distances. Using devices to fix the distance from the transect line is not practical because of the rugosity and unevenness of the rocky reefs and the presence of kelp, and because of the loss of survey time. As a result, even in belt transects that are supposed to be of fixed width, the width is still estimated. Larson and DeMartini (1984) found an asymptotic relationship between the distance at which fish could be distinguished on film and the limits of underwater visibility as determined by eye. This set an upper limit to the width of cinetransects. They also developed a method for estimating the volume of a cinetransect, given the relationship between camera range and horizontal visibility and assumptions about the cross-sectional shape of a cinetransect. We feel that though it is possible to estimate fish density from both visual belt transects and cinetransects, additional cross-referencing evaluations of these estimates should be undertaken. Another variation in the use of belt transects is the incorporation of information on fish size and age classes. Terry and Stephens (1976) distinguished age classes of fish (adults, subadults, and juveniles) at King Harbor. The age classes are based on size classes for a particular species. For instance, many species of surfperch can be categorized into three size classes: adults (
150 mm SL), subadults (100–150 mm SL), and juveniles (100 mm SL) (Ebeling and Laur, 1985). Depending on the experimental design, more size classes can be used. However, the accurate estimation of fish sizes can be difficult for various reasons. Underwater objects are magnified and it takes extensive training for divers to adjust for this visually. One technique that is commonly used to overcome this problem is the use of parallel lasers that are a fixed distance apart with video (Gingras et al., 1998). The video is reviewed and fish length is estimated as a ratio of the distance between the lasers and the total length of the fish. This technique is labor-intensive and can have other significant problems. The fish need to be perpendicular to the field of view to be accurately measured, and there can be considerable error in these estimates if not done correctly (Yoshihara, 1997; Gingras et al., 1998). Some other important issues in the use of belt transects still need to addressed. We have already discussed the difficulties in determining the length and width of belt transects. In addition, whether filming or counting fishes, scuba divers repel and attract certain species of fish. It is not uncommon for schools of various species of fish to follow divers along transects. For example, wrasses (California sheephead and señorita) are notorious for being attracted to divers. Thus, it is critical for

accurate density estimates that divers not count fish that pass them from behind. The divers must be aware of this when starting a transect because the attracted fish will generally be circling the divers at this time. Scuba divers may also repel many fishes. For instance, white sea bass typically avoid divers, and many elasmobranchs that frequent kelp beds are also rarely observed by divers (Pondella and Allen, 2000). Larger individuals of species that are hunted in certain areas will tend to be wary of divers (California sheephead and kelp bass). An excellent summary of the utility of diver observations can be found in Ebeling (1982). Finally, divers must be trained adequately to conduct visual belt transects. Observers must be physically fit and experienced and comfortable with scuba, so that they devote attention to the technical aspects of data collection. Even fit and experienced divers typically have steep learning curves. Identifying fishes underwater is difficult because of variable lighting and visibility constraints. The loss of colors with depth also adds to the difficulty. Typically problematic taxonomic groups are the rockfishes and the surfperches. Most temperate conspicuous reef fishes (fig. 9-3) are mobile, requiring that they be identified at all angles and at various speeds. Taxonomic identifications must be made instantly while the counts are being taken, often at the same moment size class estimations are being made. Many programs train divers in pools with models to learn to estimate sizes. Repeated dives with an experienced fish counter and continued discussion of the techniques and results are essential. Generally a complete season of diving is necessary to train a diver in this technique because the amount of training required can vary substantially among individuals. However, after this training period, data can be collected efficiently and effectively. At this point, belt transects are very cost-effective and reliable and allow relatively precise density estimates. This is a major reason that belt transects are used today. Cryptic species (fig. 9-3) are not surveyed adequately by visual techniques. Cryptic species are four times as dense as conspicuous fishes and may double the ichthyofaunal diversity on a reef, although their biomass may not be large (Allen et al., 1992). From an ecological standpoint, the influence of these taxa must be significant, but this subset of the reef community has been included in studies only a few times (Stephens and Zerba, 1981; Stephens et al., 1984, 1986; Allen et al., 1992). Surveys of cryptic reef fishes are often conducted with an ichthyocide (usually quinaldine or rotenone) in a standardized fashion. A typical quadrat is 1 meter square, and all of the fishes within the quadrat are either anesthetized or poisoned. Rotenone is more difficult to use subtidally because it clouds the water and works best when constrained within a particular area. Thus, the best method for working with rotenone is to tarp off the meter-square (Allen et al., 1992). Quinaldine mixed with isopropyl alcohol (1:9 ratio) and administered directly to the reef with a standard laboratory squeeze bottle is cloudy upon release, enabling the divers to see the release point, but it becomes clear within a few seconds. Because it does not cloud the reef, fishes can easily be captured when they lose consciousness and float off the reef. Divers can capture fish in small 333-m mesh bags (commercial paint bags work well) or use an airlift on complex reefs or reefs with high densities of cryptic fishes (Stephens et al., 1984). The airlift was modified from Roach et al. (1964) in which a standard inflater hose was fitted to a rigid intake pipe attached to 1.5-m flexible hose (
5 cm in diameter) with a 333-m mesh bag attached to the other

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F I G U R E 9-3 Comparison of life zones (Zones 1,2,3, and 4) defined by Quast (1968b) and the categories of conspicuous, cryptic, and transient

(associated) species referred to in this chapter.

side. As the air flows up the hose, it creates a vacuum that delivers fish into a mesh bag. Using quinaldine, fish are anesthetized and not necessarily sacrificed, so fish can be returned to the reef if desired. Meter-square quadrats have been typically made of PVC, but they can be cumbersome. Lead line works better and can be easily transported by divers. The airlift and anesthetic captures close to 100% of the small cryptic fishes, but larger camouflaged species (rockfishes, scorpionfishes, black croaker, moray eels) are not as susceptible to the anesthetic in open environments, and their presence needs to be noted by divers. Predatory fishes are also a problem in cryptic collections and need to be deterred from entering the study area. There are other anesthetics and poisons on the market, but their use subtidally has not been widely studied in California. Cyanide poisoning is the most commonly used collection technique for aquarium fishes in the tropics; however, its use is not recommended. In addition, larger but hidden fishes can be counted in belt transects using techniques that are specifically designed for maximizing detection of these fishes. For example, Larson (1980) counted black-and-yellow rockfish along fixed transects by peering to the extent possible into crevices and into cavities using a dive light. Settlement and recruitment of larval fishes to reefs was and continues to be of interest to reef ecologists (chapter 15). Assessment of this critical life-history stage has been conducted using both diver surveys and ichthyoplankton tows (chapters 11 and 15).

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Major Taxa of Reef and Kelp Fish The fishes found in and near rock reefs and kelp forests represent a variety of taxa (table 9-1). The more than 150 species listed in Table 1 show differing degrees of association with rock reefs and kelp forests per se, but they do interact with the reef and kelp community. Taxa contributing the greatest biomass, numerical abundance, or species richness to the rock-reef and kelp-forest community are Acanthopterygians (Hobson, 1994), including Serranidae, Pomacentridae, Labridae, Kyphosidae, Embiotocidae, Scorpaenidae (especially Sebastes), Hexagrammidae, Gobiidae, and Cottidae. Transient, pelagic species from the Clupeidae, Engraulidae, Scombridae, Carangidae, and Sciaenidae may play a significant role in the energetics of reef and kelp communities. The taxonomic composition of both conspicuous and cryptic fishes in kelp-rock habitats varies considerably with latitude (figs. 9-4 and 9-5) and with a number of features of the habitat (see next section).

Factors Affecting Species Composition and Abundance of Fishes There is no such thing as a unitary assemblage of fishes inhabiting reef and kelp habitats off California, even within biogeographic regions. Although areas of reef and kelp habitat within a biogeographic region may harbor a familiar assemblage of species, most of these species appear to respond differently to

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TA B L E 9-1

Californian Rocky-Reef Fishes by Range, Position, Habitat, and Behavioral Characteristics

Scientific Name Hexanchiformes Hexanchidae Notorynchus cepedianus (Peron, 1807) Squatinaformes Squatinidae-angel sharks Squatina californica (Ayres, 1859) Heterodontiformes Heterodontidae-bullhead sharks Heterodontus francisci (Girard, 1855) Lamniformes Alopiidae-thresher sharks Alopias vulpinus (Bonnaterre, 1788) Carcharhiniformes Scyliorhinidae-cat sharks Cephaloscylium ventriosum (Garman, 1880) Triakidae-hound sharks Mustelus californicus (Gill, 1864) Mustelus henlei (Gill, 1863) Galeorhinus galeus (Linnaeus, 1758) Triakis semifasciata (Girard, 1855) Torpediniformes Torpedinidae-torpedo electric rays Torpedo californica (Ayres, 1855) Rajiformes Rhinobatidae-guitarfishes Rhinobatis productus (Ayres, 1854) Zapteryx exasperata (Jordan & Gilbert 1880) Platyrhynidae-thornbacks Platyrhinoides triseriata (Jordan & Gilbert, 1880) Myliobatiformes Urolophidae-round stingrays Urobatis halleri (Cooper, 1863) Myliobatidae-eagle rays Myliobatis californica (Gill, 1865) Anguilliformes Muraenidae-morays Gymnothorax mordax (Ayres, 1859) Clupeiformes Engraulidae-anchovies Engraulis mordax (Girard, 1854) Clupeidae-herrings Sardinops sagax (Jenyns, 1842) Salmoniformes Salmonidae-trouts and salmons Onchorynchus keta (Walbaum, 1792) Onchorynchus kisutch (Walbaum, 1792) Onchorynchus tshawytscha (Walbaum, 1792) Ophidiiformes Bythitidae-viviparous brotulas Brosmophycis marginata (Ayres, 1854) Batrachoidiformes Batrachoididae-toadfishes Porichthys myriaster (Hubbs & Schultz, 1939) Porichthys notatus (Girard, 1854) Atheriniformes Atherinopsidae-New World silversides Atherinops affinis (Ayres, 1860) Atherinopsis californiensis (Girard, 1854) Leuresthes tenuis (Ayres, 1860) Gasterosteiformes Aulorhynchidae-tubesnouts Aulorhynchus flavidus (Gill, 1861)

Common Name

Range

Position

Habitat and Behavioral

Cow sharks Sevengill shark

W

Angel shark

C

Bt

Horn shark

S

Bt

n

Thresher shark

W

WC

p

Swell shark

S

Bt

n

Gray smoothhound Brown smoothhound Soupfin Leopard shark

S N,S (C?) W C

Bt Bt WC Bt

ab,n ab,n ab ab

California electric ray

C

Bt

n

Shovelnose guitarfish Banded guitarfish

S,B S,B

Bt Bt

Thornback

S

Bt

Round stingray

C

Bt

Bat ray

C

Bt

California moray

S

Bt

h

Northern anchovy

C

WC

p,sc

Pacific sardine

C

WC

p,sc

N

Bt

S C,N

Bt/WC Bt/WC

Topsmelt Jacksmelt Grunion

C C S

WC WC WC

p,sc p,sc p,sc

Tubesnout

C

WC/Bt

c,sc

Chum salmon Coho (silver) salmon Chinook (king) salmon

Red brotula

Specklefin midshipman Plainfin midshipman

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Scientific Name

Common Name

Syngnathidae-pipefishes Cosmocampus arctus (Jenkins & Evermann, 1889) Syngnathus californiensis (Storer, 1845) Scorpaeniformes Scorpaenidae-scorpionfishes Scorpaena guttata (Girard, 1854) Scorpaena histrio (Jenyns 1840) Scorpaenodes xyris (Jordan & Gilbert, 1882) Sebastes atrovirens (Jordan & Gilbert, 1880) Sebastes auriculatus (Girard, 1854) Sebastes carnatus (Jordan & Gilbert, 1880) Sebastes caurinus (Richardson, 1844) Sebastes chrysomelas (Jordan & Gilbert, 1881) Sebastes constellatus (Jordan & Gilbert, 1880) Sebastes dallii (Eigenmann & Beeson, 1894) Sebastes flavidus (Ayres, 1862) Sebastes hopkinsi (Cramer, 1895) Sebastes melanops (Girard, 1856) Sebastes miniatus (Jordan & Gilbert, 1880) Sebastes mystinus (Jordan & Gilbert, 1881) Sebastes nebulosus (Ayres, 1854) Sebastes paucispinis (Ayres, 1854) Sebastes rastrelliger (Jordan & Gilbert, 1880) Sebastes serranoides (Eigenmann & Eigenmann, 1890) Sebastes serriceps (Jordan & Gilbert, 1880) Hexagrammidae-greenlings Hexagrammos decagrammus (Pallas, 1810) Hexagrammos lagocephalus (Pallas, 1810) Ophiodon elongatus (Girard, 1854) Oxylebius pictus (Gill, 1862) Cottidae-sculpins Artedius corallinus (Hubbs, 1926) Artedius harringtoni (Starks, 1896) Enophrys bison (Girard, 1854) Hemilepidotus spinosus (Ayres, 1854) Jordania zonope (Starks, 1895) Leiocottus hirundo (Girard, 1856) Oligocottus rubellio (Greeley, 1899) Orthonopias triacis (Starks & Mann, 1911) Ruscarius creaseri (Hubbs, 1926) Scorpaenichthys marmoratus (Ayres, 1854) Hemitripteridae-sea sravens Nautichthys oculofasciatus (Girard, 1858) Perciformes Polyprionidae-wreckfishes Stereolepis gigas (Ayres, 1859) Serranidae-sea basses and groupers Epinephelus analogus (Gill, 1865) Epinephelus labriformis (Jenyns, 1840) Mycteroperca jordani (Jenkins & Evermann, 1889) Mycteroperca xenarcha (Jordan, 1888) Paralabrax auroguttatus (Walford, 1936) Paralabrax clathratus (Girard, 1854) Paralabrax nebulifer (Girard, 1854) Paranthias colonus (Valenciennes, 1846) Serranus psittacinus (Valenciennes, 1846) Apogonidae-cardinalfishes Apogon guadalupensis (Osborn & Nichols, 1916) Apogon pacificus (Herre, 1935) Malacanthidae-tilefishes Caulolatilus princeps (Jenyns, 1840) Carangidae-jacks Seriola lalandi (Valenciennes, 1833)

234

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Snubnose pipefish Kelp pipefish

Range

Position

Habitat and Behavioral

S

WC

c/st

California scorpionfish S Player scorpionfish B Rainbow scorpionfish B,S Kelp rockfish S, N Brown rockfish C Gopher rockfish C Copper rockfish C Black-and-yellow rockfish C Starry rockfish S Calico rockfish S Yellowtail rockfish N Squarespot rockfish S Black rockfish N Vermilion rockfish C Blue rockfish C China rockfish N Bocaccio C Grass rockfish C Olive rockfish C

Bt

WC/Bt Bt Bt Bt Bt

st,h,sc

Bt

ab,sr

WC/Bt WC Bt WC Bt Bt Bt WC/Bt

st,ab ab ab st,sc,n h ab,sc h st,ab

h ab,sr h

Treefish

S

Bt

h

Kelp greenling Rock greenling Lingcod Painted greenling

N N C C

Bt Bt Bt Bt

cr

Coralline sculpin Scalyhead sculpin Buffalo sculpin Brown irish lord Longfin sculpin Lavender sculpin Rosy sculpin Snubnose sculpin Roughcheek sculpin Cabezon

C C N N

Bt Bt Bt Bt

al

S

Bt

rs

S S C

Bt Bt Bt

al al

Giant sea bass

S,B

Bt

ab

Spotted cabrilla Flag cabrilla Gulf grouper Broomtail grouper Golden spotted rock bass Kelp bass Barred sand bass Pacific creolefish Banded serrano

B B B S,B B S S B B

Bt Bt Bt Bt Bt WC/Bt Bt WC/Bt Bt

Guadalupe cardinalfish Pink cardinalfish

B B

Bt Bt

Ocean whitefish

C

Bt

ab,p

Yellowtail

C

WC

p,sc

Sailfin sculpin

st fs,rs

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TA B L E 9-1

Scientific Name Trachurus symmetricus (Ayres, 1855) Haemulidae-grunts Anisotremus davidsonii (Steindachner, 1876) Anisotremus interruptus (Gill, 1862) Xenistius californiensis (Steindachner, 1876) Sparidae-porgies Calamus brachysomus (Lockington, 1880) Scieanidae-croakers Atractoscion nobilis (Ayers, 1860) Cheilotrema saturnum (Girard, 1858) Parques viola (Gilbert, 1898) Seriphus politus (Ayres, 1860) Mullidae-goatfishes Mulloidichthys dentatus (Gill, 1862) Chaetodontidae-butteryflyfishes Chaetodon humeralis (Gunther, 1860) Johnrandallia nigrirostris (Gill, 1862) Prognathodes falcifer (Hubbs & Rechnitzer, 1958) Pomacanthidae-angelfishes Pomacanthus zonipectus (Gill, 1862) Kyphosidae-sea chubs Girella nigricans (Ayres, 1860) Hermosilla azurae (Jenkins & Evermann, 1889) Medialuna californiensis (Steindachner, 1876) Embiotocidae-surfperches Brachyistius frenatus (Gill, 1862) Cymatogaster aggregata (Gibbons, 1854) Embiotoca jacksoni (Agassiz, 1853) Embiotoca lateralis (Agassiz, 1854) Hyperprosopon argenteum Gibbons, 1854 Hyperprosopon ellipticum (Gibbons, 1854) Hypsurus caryi (Agassiz, 1853) Micrometrus aurora (Jordan & Gilbert, 1880) Micrometrus minimus (Gibbons, 1854) Phanerodon atripes (Jordan & Gilbert, 1880) Phanerodon furcatus (Girard, 1854) Rhacochilus toxotes (Agassiz, 1854) Rhacochilus vacca (Girard, 1855) Pomacentridae-damselfishes Abudefduf troschelli (Gill, 1862) Azurina hirundo (Jordan & McGregor, 1898) Chromis alta (Greenfield & Woods, 1980) Chromis atrilobata (Gill, 1862) Chromis punctipinnis (Cooper, 1863) Hypsypops rubicundus (Girard, 1854) Stegastes rectifraenum (Gill, 1862) Labridae-wrasses Bodianus diplotaenia (Gill, 1862) Halichoeres dispilus (Gunther, 1864) Halichoeres melanotis (Gilbert, 1890) Halichoeres semicinctus (Ayres, 1859) Oxyjulis californica (Gunther, 1861) Semicossyphus pulcher (Ayres, 1854) Thalassoma lucasunum (Gill, 1862) Scaridae-parrotfishes Nicholsina denticulata (Evermann & Radcliffe, 1917) Bathymasteridae-ronquils Rathbunella alleni (Gilbert, 1904) Rathbunella jordani (Gilbert, 1889) Stichaeidae-pricklebacks Anoplarchus insignis (Gilbert & Burke 1912)

(continued)

Common Name

Range

Position

Habitat and Behavioral

Jack mackerel

C

WC

p,sc

Sargo Burrito grunt Salema

S B S

WC/Bt

st,sc

WQ

c,n,sc

Pacific porgy

B

Bt

White sea bass Black croaker Rock croaker Queenfish

C S B C

WC Bt Bt WC

Mexican goatfish

B

Bt

Threebanded butterflyfish Barberfish Scythe butterflyfish

B B B

Bt Bt Bt

Cortez angelfish

B

Bt

Opaleye Zebraperch Halfmoon

S S S

WC WC WC

st/c,sc st/c,sc st/c.sc

Kelp perch Shiner perch Black perch Striped seaperch Walleye surfperch Silver surfperch Rainbow seaperch Reef perch Dwarf perch Sharpnose seaperch White seaperch Rubberlip seaperch Pile perch

C C S C C C C N S C C C C

WC WC Bt Bt WC WC Bt Bt Bt WC B/WC WC/Bt Bt

c/st st,sc ab,sl ab,ca st,i,n,sc st,i,n,sc ab,sr,sc ab,i ab,i c c,ab,sc st,ab ab,sr

Panamic sergeant major Swallowtail damsel Silverstripe chromis Scissortail chromis Blacksmith Garibaldi Cortez damselfish

B B B B S S B

Bt Bt WC/Bt WC/Bt Bt Bt

Mexican hogfish Chameleon wrasse Golden wrasse Rock wrasse Senorita California sheephead Cortez rainbow wrasse

B B B S C S B

Bt Bt Bt Bt WC/Bt Bt Bt

Loosetooth parrotfish

B

Bt

Stripedfin ronquil Northern ronquil

C N

Bt Bt

st,o,sc ab,h,n st,p,n,sc

h,ab,u,sc cr,ab

ab,sc st.sc ab

h h

Slender cockscomb

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TA B L E 9-1

Scientific Name

(continued)

Common Name

Cebidichthys violaceus (Girard, 1854) Chirolophis decoratus (Jordan & Snyder, 1902) Chirolophis nugator (Jordan & Williams, 1895) Plagiogrammus hopkinsii Bean, 1894 Xiphister mucosus (Girard, 1858) Pholidae-gunnels Ulvicola sanctaerosae (Gilbert & Starks, 1897) Anarhichadidae-wolffishes Anarrhichthys ocellatus (Ayres, 1855) Tripterygiidae-triplefins Enneanectes reticulatus (Allen & Robertson, 1991) Labrisomidae-labrsomid blennies Alloclinus holderi (Lauderbach, 1907) Labrisomus xanti (Gill, 1860) Paraclinus integripinnis (Smith, 1880) Clinidae-clinids Gibbonsia elegans (Cooper, 1864) Gibbonsia metzi (Hubbs, 1927) Gibbonsia montereyensis (Hubbs, 1927) Heterostichus rostratus (Girard, 1854) Chaenopsidae-pikeblennies Neoclinus stephensae (Hubbs, 1953) Blenniidae-combtooth blennies Hypsoblennius gentilis (Girard, 1854) Hypsoblennius gilberti (Jordan, 1882) Hypsoblennius jenkinsi (Jordan & Evermann, 1896) Ophioblennius steindachneri (Jordan & Evermann, 1898) Plagiotremus azaleus (Jordan & Bollman, 1890) Gobiesocidae-clingfishes Gobiesox meandricus (Girard, 1858) Rimicola muscarum (Meek & Pierson, 1895) Rimicola eigenmanni (Gilbert, 1890) Gobiidae-gobies Lythrypnus dalli (Gilbert, 1890) Lythrypnus zebra (Gilbert, 1890) Rhinogobiops nicholsii (Bean, 1882) Sphyraenidae-barracudas Sphyraena argentea (Girard, 1854) Sphyraena ensis (Jordan & Gilbert, 1882) Scombridae-mackerels Sarda chiliensis (Cuvier, 1832) Scomber japonicus (Houttuyn, 1782) Pleuronectiformes Paralichthyidae-sand flounders Citharichthys stigmaeus (Jordan & Gilbert, 1882) Hippoglossina stomata (Eigenmann & Eigenmann, 1890) Paralichthys californicus (Ayres, 1859) Pleuronectidae-righteye flounders Pleuronichthys coenosus (Girard, 1854) Tetraodontiformes Balistidae-leatherjackets Balistes polylepis (Steindachner, 1876) Suflamen verrres (Gilbert & Starks, 1904) Tetraodontidae-puffers Sphoeroides annulatus (Jenyns, 1842) Diodontidae-porcupinefishes Diodon hystrix (Linnaeus, 1758)

Range

Position

Habitat and Behavioral

Monkeyface prickleback Decorated warbonnet Mosshead warbonnet Crisscross prickleback Rock prickleback

N

Bt

h

N

Bt

h

N

Bt

h

Kelp gunnel

S

WC

c

Wolf-eel

N

Bt

h

Flag triplefin

B

Bt

Island kelpfish Largemouth blenny Reef finspot

S B S

Bt Bt Bt

h,al

Spotted kelpfish Striped kelpfish Crevice kelpfish Giant kelpfish

S C N C

Bt Bt Bt WC/Bt

al al al st

Yellowfin fringehead

S

Bt

h

Bay blenny Rockpool blenny Mussel blenny Panamic fanged blenny

S S S B

Bt Bt Bt Bt

Sabertooth blenny

B

Bt

Northern clingfish Kelp clingfish Slender clingfish

C C

WC/Bt WC

c.al c

Bluebanded goby Zebra goby Blackeye goby

S S C

Bt Bt Bt

sl h fs,sr,h

Pacific barracuda Mexican barracuda

S B

WC WC

p,s

Pacific bonito Pacific chub mackerel

C W

WC WC

p,sc p,o,sc

Speckled sanddab Bigmouth sole

C S

Bt Bt

fs fs

California halibut

C

Bt

fs

C-O sole

C

Bt

rs,fs

S,B B

Bt Bt

Bullseye puffer

B

Bt

Porcupinefish

B

Bt

Finescale triggerfish Orange-side triggerfish

cr

h

NOTE: S  southern; N  northern; C  through out coastal California, generally temperate north Pacific; B  southern Baja California, W  worldwide. Bt  bottom; WC  water column; C  water column-canopy; st  stipes; O  outer kelp margin; I  inner kelp margin; U  upcurrent margin; P  pelagic; FS  bottom-fringing sand; SR  sand/rock interface; SL  slope; CR  crest; H  in substrate; AL  algae; AB  above substrate; SC  often in schools; N  primarily nocturnally active.

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F I G U R E 9-4 North, south, and Baja latitudinal distribution of conspicuous reef fishes.

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F I G U R E 9-5 North and south latitudinal distribution of representative cryptic reef fishes (list compiled from Quast, 1968c; Yoshiyama et al.,

1987; Stephens et al., 1986; and Allen et al., 1992).

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F I G U R E 9-6 A representative southern reef fish scene.

variation in environmental factors. Some of the more important environmental factors are latitude (or exposure to different oceanographic conditions), bottom depth, bottom composition (presence or absence of rock or other hard substrates and the relief and rugosity of reefs), and vegetation (the presence, species composition, and density of kelp and other forms of vegetation, including drift). One of the major issues in the ecology of reef and kelp fishes off California has been the role of kelp in determining the species composition and abundance of fishes.

Latitude The species composition of fishes changes rapidly at some major biogeographic boundaries off California, such as Point Conception and Punta Eugenia (Garth, 1955; Hubbs, 1960; Quast, 1968b; Horn and Allen, 1978; chapter 1). These changes in species composition have a profound influence on the nature of the assemblages. Three faunal provinces are found off the coast of the Californias: Oregonian, San Diegan, and Cortez. In the San Diegan Province, the reef fish assemblage includes three faunal elements. One element consists of species from families that are distributed primarily in the tropics and subtropics, including chubs (Kyphosidae), grunts (Haemulidae), croakers (Sciaenidae), damselfishes (Pomacentridae), wrasses (Labridae), gobies (Gobiidae), blennies (Blenniidae), and basses

(Serranidae) (fig. 9-6). The warm-temperate California representatives of these families exhibit historically derived tropical characteristics (chapter 2), and they are relatively unimportant elements in the Oregonian Province north of Pt. Conception. A second element consists of Oregonian species that dominate north of Pt. Conception, particularly members of the rockfishes (Sebastes), surfperches (Embiotocidae), greenlings (Hexagrammidae), and sculpins (Cottidae), which may occur at least in some areas in Southern California. A final element consists of species that can be called San Diegan, which are generally derived from cool-temperate taxa, but whose distributions are centered in the San Diegan Province. Examples of such fishes are kelp rockfish and black perch. In addition to these primary faunal elements, more tropical members of some families expand into the Southern California Bight during warming periods, as has been observed during the last 25 years (Mearns, 1988; Pondella and Allen, 2001). The Southern California Bight is a transitional zone between the San Diegan and Oregonian faunas and may be dominated by either fauna, depending on oceanographic conditions (Horn and Allen, 1978; Holbrook et al., 1997). In central California, the Oregonian fauna (fig. 9-7) dominates with incursions from the south during warming events. northern California is overwhelmingly Oregonian and is dominated by taxa such as rockfish, greenlings, and cottids. Fish assemblages in rock reef and kelp habitats off southern Baja California (fig. 9-8) are generally similar to those from

ROCKY REEFS AND KELP BEDS

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F I G U R E 9-7 A representative northern reef fish scene.

southern California but differ primarily by the occurrence of four tropical species (sergeant major, chameleon wrasse, bullseye puffer, and scissortail chromis). All of these species have been reported in southern California in recent years. The coastline from just north of Punta Eugenia to around the international border complicates the fish fauna off Baja California. This section of coastline is primarily Oregonian (figs. 9-4 and 9-9) due to continual coastal upwelling (Hubbs, 1948; Horn and Allen, 1978). Finally, Cortez Province, which lies below the San Diegan, is basically unstudied. Although the species composition of reef and kelp fishes does vary geographically and changes most strongly at some important places, not all species are affected in the same fashion by biogeographic boundaries. Even within a biogeographic region, there may be incremental changes in species composition that are related to biogeographical factors. For example, though some species of fish reach their geographical limits at or near Pt. Conception, other species that are characteristic of one geographic region occur beyond this typical range. Garibaldi and California scorpionfish are now extremely rare north of Pt. Conception, but several other species of fish from tropical families occur north of Pt. Conception (such as señorita, blacksmith, opaleye, kelp bass, California sheephead, and halfmoon). Furthermore, even within this group, some species seem better adapted to conditions in central California. The señorita appears to have recruited nearly every year in Monterey during the 1990s, whereas blacksmith and California sheephead recruited only during El Niño years and blue-banded

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gobies recruited only during the El Niño of 1983 (Lenarz et al., 1995; Walters, 2002). Señoritas are an example of a wrasse that is clearly not a subtropical species. Furthermore, although some species that are characteristic of central and northern California are very uncommon south of Pt. Conception (such as kelp greenling and China rockfish), others have been common in the southern California Bight (such as black-and-yellow, blue, and olive rockfish), at least before 1977. The distribution and abundance of central California expatriates off southern California also indicate an incremental response to biogeographical factors. For example, the kelp rockfish seem to have been common throughout the southern California Bight, but the olive rockfish, black-and-yellow rockfish, and blue rockfish have been progressively less common (Limbaugh, 1955; Quast, 1968b,c; Hobson and Chess, 1976). Fish surveys on the California Channel Islands (fig. 9-10) further illustrate this phenomenon. The biogeographical differences among the islands are clear, but different species appear to respond differently to the biogeographical gradient (fig. 9-10). Patton et al. (1985) demonstrated that the abundance of a number of reef and kelp fishes changed along the mainland coast of southern California. Their analyses indicated that geographic position within the Southern California Bight influenced the species composition of fishes on rock bottoms as much as bottom relief and kelp density. In addition, some northern species may be able to survive off southern California by submergence (Hubbs, 1948, 1952), as they seek cooler, isothermal conditions beneath the warmer surface waters.

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F I G U R E 9-8 A representative Baja reef fish scene.

Incremental differences in latitudinal distribution also seem to be correlated with differences in recruitment. For example, recruitment of olive rockfish in the Southern California Bight, as indicated by entrainment in power plants, seems to have persisted since 1977, whereas recruitment of blue rockfish ceased during the period covered in the study (Stephens et al., 1994; Love et al., 1998). Cowen and Bodkin (1993) found that some southerly species occurred at San Nicolas Island from 1981 to 1986 and documented the irregular recruitment of some species (such as California sheephead, rock wrasse, and garibaldi) but regular recruitment of others (such as blacksmith and señorita). Finally, distributions of nearshore fishes have changed in response to changes in ocean climate (Hubbs, 1948; Stephens et al., 1994). These observations show that, though major biogeographic features do strongly influence the species composition of nearshore fishes, the species composition of fishes in kelp and rock assemblages still exhibit incremental variation within regions.

Bottom Depth The composition of fish assemblages in rock and kelp habitats also changes with bottom depth. Some of this change seems to be related to depth or depth-related abiotic factors per se, but some of this change may be related to habitat and vegetation. Temperature is the abiotic factor with the greatest direct effect on fishes. Even though the reefs with which we are concerned are relatively shallow (30m), water temperature gradients can

be seasonally stable and persistent, and reef fishes often distribute themselves with regard to these gradients (Terry and Stephens, 1976). Stephens and Zerba (1981) showed that species composition changed with depth-related changes in water temperature at King Harbor and suggested that the overall diversity of fishes at this site was enhanced by the heterogeneity of temperature conditions produced by the conjunction of entrained upwelling from a nearby submarine canyon and the discharge of power plant thermal effluent. Temperature-related depth distributions of mobile fish should change with daily, seasonal, or annual changes in these gradients. For less mobile species, temperature changes are sometimes reflected in changes in activity (Ebeling and Hixon, 1991). The depth distributions in several species of fish appear to be related to the occurrence of vegetation. Ebeling et al. (1980a) and DeMartini (1981) found that shallow habitats with surf grass (and sometimes Egregia and other brown algae) supported some species that are also found on deeper reefs in Macrocystis forests (such as subadults and adults of black perch, rainbow seaperch, opaleye, señorita, garibaldi, and kelp bass) and others that are limited to those habitats, at least during the daytime (dwarf perch, walleye surfperch). Related to bottom depth, but not dependent on bottom depth per se, is the relationship between fish abundance and the margins of the kelp forest. Both in southern California (Ebeling et al., 1980a; Bray, 1981; Larson and DeMartini, 1984) and in central California (Stallings, 2002), several species of fish (especially plankton feeders such as blacksmith and blue rockfish,

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F I G U R E 9-9 Mean July isotherms (°C at 10 m depth) off California and Baja California recorded during CalCOFI cruises from 1950 to 1978.

but also other species such as olive rockfish) tend to concentrate at the upcurrent and outer margin of the kelp forest. Here, kelp provides a point of visual orientation. It is not clear what the effects of lack of kelp might be on the overall abundance of these species. Blacksmith appeared to form water-column aggregations closer to shore off Santa Cruz Island in 1996, when kelp was less abundant than in the 1970s (Larson, personal observation), and orient to pinnacle reefs lacking kelp as well as to seamounts without kelp (Pondella, personal observation). Blue rockfish orient toward rock outcrops when kelp is absent. The tendency for many species to concentrate along the kelp-bed margins results in an unequal distribution of densities across a bed.

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Within the depth range of kelp forests, a number of species show limited depth distributions (such as grass rockfish, blackand-yellow and gopher rockfish and striped and black perch). Several species that occur in kelp forests also occur much more deeply (such as California sheephead, many species of rockfish, and blackeye goby) or may migrate seasonally between deeper and shallower waters (such as lingcod). Some of the information on deeper dwelling fishes is available from fisheries, but the preponderance of research on fishes from rock and kelp habitats has been based on observations by scuba divers and may therefore underrepresent the significance of those portions of populations living below typical scuba depths. The use of surveys by submersibles (chapter 9) will

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FIGURE 9-10 Relative abundance scores for selected species

of fish with southerly distributions (upper panel) and northerly distributions (lower panel) from 105 sites on eight southern California islands (Santa Catalina, SCA; San Clemente, SCL; Anacapa, ANA; Santa Barbara, SBA; Santa Cruz, SCR; San Nicolas, SNI; Santa Rosa, SRO; and San Miguel, SMI), 1978–1986. Adapted from Engle (1993).

help to determine the true bathymetric extent of some species of fish from rock and kelp habitats.

Macroalgae and Bottom Characteristics The effects of macroalgae and bottom characteristics on fish assemblages are closely intertwined. Much of the initial research on kelp-forest fishes concerned the effects of kelp and kelp harvesting on fishes (Limbaugh, 1955; Quast, 1968a–f; Davies, 1968; North, 1968, 1971), and further research (see below) has continued to address this issue. The confounding factor in all of this research is the relatively strong dependence of kelp and other types of macroalgae upon the rock bottom for attachment. This makes it difficult to distinguish the effects of kelp from the effects of rock bottom on fishes. Because of this, we will initially address the relative effects of kelp (primarily Macrocystis pyrifera, and secondarily Nereocystis luetkeana) and bottom type on fishes together.

Limbaugh (1955), in addressing the effects of kelp harvesting on fishes, provided the first comprehensive description of the natural history of kelp-forest fishes. As in later studies, he compared areas with different combinations of habitat, including rocky and sandy areas with and without kelp. He described suites of species associated with the kelp canopy, bottom (kelpbed rock bottom and kelp-bed sand bottom), and midkelp region and discussed his conclusions regarding habits and habitat requirements of many species. In his qualitative analysis, he concluded that most species of fish that occur in kelp forests are bottom species that are “completely independent of kelp” but allowed that some species seek shelter in the kelp canopy as adults, that a few species deposit eggs on kelp (and on other substrates), and that juveniles of some species occur in kelp. Quast (1968b,c) used quantitative sampling as well as the presence and absence of species from areas of differing habitat to evaluate further the effects of bottom type and kelp on the species composition and abundance of fishes. He concluded (Quast, 1968b, p. 43) that “Substrate character seems of primary

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importance to the rocky inshore fishes, while the presence or absence of kelp is secondary.” He noted that several species (such as California sheephead and blacksmith) are abundant in areas of high-relief rocky bottom, whether or not kelp is present, and that areas of kelp with low-relief rock or sandy bottom lack many species and have a lower total standing crop than areas of high-relief rocky bottom (Quast, 1968b,c). However, he also noted that areas of low to moderate bottom relief with kelp supported larger standing crops of fishes than those without kelp (Quast, 1968b,c,f). Envisioning the kelp forest as a “giant filter” for coastal zooplankton, Quast (1968b,f) thought that kelp served inshore fishes primarily though the collection of plankton by attached invertebrates and through its effect as a point of visual orientation, allowing several species of fish to extend their range into the water column. Ebeling et al. (1980a) surveyed fishes in bottom and kelpcanopy habitats differing in bottom depth, bottom type, and kelp density off Santa Barbara and Santa Cruz Island. Because the south-facing coast off Santa Barbara is somewhat protected from oceanic swells, kelp forests there sometimes grow on sand or low-relief rocky bottom, facilitating the comparison of kelpforest fish assemblages over high-relief and low-relief substrates. However, kelp was present in most samples from high-relief rocky bottoms. Their analysis distinguished five “habitat groups” of fishes: a “kelp-rock” group of species from high-relief rocky bottoms in kelp forests; a “canopy” group that was associated with the kelp canopy, relatively independently of bottom type; an “inner marginal” group associated with shallow water and surfgrass inshore of kelp forests; a “commuter” group of species that showed no strong habitat association, but which moved throughout the water column and a “bottom” group associated with the rock bottom on the outer edges of kelp forests. Species from the “kelp-rock,” “commuter,” and “bottom” groups often occurred together, forming the core of the benthic, epibenthic, and midwater column species typically seen over rocky bottoms in kelp forests. The species composition in any location was seen as responding continuously to several habitat variables. They concluded that areas of kelp over lowrelief rocky bottom supported kelp-canopy species and generalist species but that higher relief was required for a number of species. Like Quast (1968b,c,f), they found that the presence of kelp over low-relief substrate did enhance density and diversity of species. They also found that in bottom transects, fish density and species diversity increased with both bottom depth and bottom relief. The relationships of density and diversity with bottom relief did not reach asymptotes; instead, they reached their highest values at the greatest values of bottom relief. In this study, bottom relief was scored on a subjective 1–5 scale that reflected both reef height and bottom rugosity, but neither of these parameters was measured directly. Because kelp was present in essentially all samples over moderate to high-relief rocky bottoms, it was impossible to determine whether kelp enhanced the rock-reef habitat for members of the “kelp-rock” group. Stephens and Zerba (1981) reported on surveys of the breakwater at King Harbor, a high-relief rock reef without kelp, located in Southern California. Although their discussion did not focus primarily on fish–habitat relationships (other than the effect of temperature stratification), their results describe a diverse and abundant fish fauna containing a large number of species that are common in kelp forests. These include species that one might expect to find on a rock reef, including benthic and epibenthic species (such as various surfperches, garibaldi, painted greenling, and opaleye) typically associated with rocky bottoms in kelp forests and water-column species (such as blue

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rockfish and blacksmith) that also use rock bottoms for shelter. The fish fauna also included other species that are often associated with kelp even in the absence of a high-relief rocky bottom (such as kelp bass, señorita, and halfmoon), and even species that are frequently associated strongly with kelp (such as kelp perch and giant kelpfish). Their data indicate that many members of the “kelp-rock” and “commuter” groups of Ebeling et al. (1980b) can be found on rock bottoms that lack kelp, as can some members of the “canopy” group. Larson and DeMartini (1984) surveyed fishes in a cobblebottom kelp forest and an adjacent kelp-free site of similar bottom type near San Onofre, California. The cobble bottom here offered little variation in bottom height and little fishsized bottom shelter. It was periodically inundated or scoured by sand, so there was little growth of attached algae and invertebrates on the rocks. Several species that depend on a rocky bottom for shelter or food were absent or uncommon at this site (such as blacksmith, opaleye, garibaldi, painted greenling, benthic rockfishes, and some surfperches). The species present in the kelp forest were kelp-canopy species (such as kelp perch, halfmoon, and giant kelpfish), bottom and/or water-column species that were less reliant on a highrelief rocky bottom (such as kelp bass, señorita, and perhaps California sheephead), and species that seem to prefer lowrelief bottom habitats (such as barred sand bass and white seaperch). The abundance and biomass of nearly all of the species except barred sand bass were substantially greater in the kelp forest than in the kelpless cobble site. It appears that the presence of kelp had a great influence on the fishes at San Onofre and provided habitat for a large number and biomass of species, particularly those inhabiting the water column. Stephens et al. (1984) reported on surveys of fishes of Palos Verdes during the recovery of the kelp forest there and during a major shift in oceanic climate. They found that the reef-kelp habitat at Palos Verdes supported a less diverse and less abundant fish fauna than the kelp-free but high-relief breakwater at King Harbor. Only a few species seemed to increase in abundance in concert with the regrowth of the kelp bed at Palos Verdes. Benthic counts of kelp bass increased, but so did counts at King Harbor. From the added counts of kelp bass above the bottom at Palos Verdes, they concluded that kelp bass might have increased in abundance in response to the growth of the kelp forest. Kelp perch increased at Palos Verdes but also increased at King Harbor. Other species, including kelp rockfish and various surfperches, did not increase in abundance with the development of the kelp bed at Palos Verdes. The effects of altered ocean climate (regime shift) may have obscured the relationship of these species with kelp after 1977. Patton et al. (1985) carried out an extensive survey of sites within the Southern California Bight that included different combinations of bottom relief and kelp abundance. They found a saturating (asymptotic) effect of reef height on the abundance of “oxyphilic” (rock-loving) species and on species density. Kelp density seemed to have no effect on fish density or species density over high-relief rock bottoms and had a saturating effect on fish density and species density over low-relief bottoms, especially when sites with sand bottom and kelp were included. In a cluster analysis, the effects of kelp on species composition could be distinguished regionally for high-relief rocky bottoms, but substrate composition and geography accounted for deeper levels of clustering. Bodkin (1988) examined the effects of Macrocystis on the density and species composition of fishes near Pt. Piedras Blancas in central California by clearing kelp from a 1-ha area.

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TA B L E 9-2

Pearson Correlation Coefficients Between Fish Counts and Kelp Abundance on Santa Cruz Island, 1996

Bottom Transects

Canopy Transects

0.338  0.572 0.031  0.272  0.438  0.649 0.229 0.119 0.391  0.279 0.509  0.455 0.922* 0.609 0.352  0.216  0.462

0.820?

Kelp bass California sheephead Señorita Blacksmith Garibaldi Halfmoon Opaleye Black perch Striped seaperch Pile perch Rubberlip seaperch Kelp perch Kelp rockfish Olive rockfish Black-and-yellow rockfish Treefish Painted greenling

Rock wrasse

0.706  0.384  0.565 0.624

0.551 0.871? 0.732

0.033

NOTE: Mean kelp scores were made subjectively on a scale of 1 to 5. Fish were counted at five sites on the north shore of Santa Cruz Island, in 2.5 minute video transects conducted as in Ebeling et al. (1980a,b) near the bottom and in the kelp canopy (or at the depth the kelp canopy would have been). Significance levels: * (p .05); ? (.05  p  0.1). From Larson, Alevizon, Niesen, and Clark (unpublished data).

The effect of kelp removal was substantial in the midwater zone, where kelp provided the only substrate and point of orientation, but was small in the benthic/epibenthic zone. Juveniles of rockfish and adults and subadults of blue rockfish, olive rockfish, kelp rockfish, and señorita decreased in abundance relative to controls in midwater transects. Overall, the biomass declined substantially after kelp was removed in the experimental area. This study was carried out over a high-relief rocky bottom. DeMartini and Roberts (1990) compared fish density in areas of differing kelp density at San Onofre, an area of lowrelief cobble bottom. Fish density showed a significant, positive relationship with kelp density for at least one life stage in 11 of 14 species evaluated. Total fish density and biomass increased significantly with kelp density. The latter relationship was nonsaturating; it applied, even if the samples with very low kelp density were excluded from the analysis. Like others, they concluded that the presence of kelp might have a stronger effect on fish abundance over a low-relief bottom than over a high-relief bottom because kelp is the primary feature providing structural heterogeneity in such habitats. Holbrook et al. (1990) compared the abundance of selected species of fish in areas of differing Macrocystis density at Santa Cruz and Santa Catalina Islands. Like DeMartini and Roberts (1990), they specifically addressed the effects of Macrocystis on different life stages, but in addition they addressed indirect effects of Macrocystis on fishes through its effect on understory algae. Some species and life stages (such as kelp perch, giant kelpfish, kelp rockfish, and young-of-year of kelp bass) showed strong positive relationships with kelp density; some seemed to require a threshold density of kelp to be present. The density of adult kelp bass was unrelated to kelp density. Different species of benthic surfperch appeared to respond either positively (black perch, pile perch) or negatively (striped seaperch) to kelp density, as apparently influenced by their dependence on features of bottom cover. Kelp appeared to inhibit foliose understory algae, which is used as a substrate for foraging by

striped seaperch, but cover of benthic “turf,” which is used by black perch and pile perch for foraging, increases in the absence of foliose understory algae. Larson and colleagues (unpublished data) repeated the surveys of Ebeling et al. (1980b) at Santa Cruz Island, investigating the effects of climate change and other factors on fishes there. They found a substantial decline in the abundance of kelp, which in 1996 was restricted to only a few sites on the north side of Santa Cruz Island. They sampled five sites, two with essentially no kelp, one with sparse kelp but a continuous kelp canopy, and two with relatively dense stands of kelp. All sites had the high-relief rocky bottom typical of Santa Cruz Island (Ebeling et al., 1980a). In bottom transects, the mean abundance of most species at a site was weakly correlated (positively or negatively) with the mean kelp-density score at a site (table 9-2). Kelp rockfish showed a strong, significant positive correlation with kelp density over sites. In canopy transects, most species showed large (though not significant) positive correlations with kelp-density score (table 9-2). The aggregate of these correlations indicates that in the water column, species composition and abundance responded strongly to the presence of kelp. For these species, total abundance at a site (integrated from the surface to bottom) may be greater in areas of kelp even if their abundance on the bottom is independent of kelp density. Although the kelp forests of southern California are dominated by Macrocystis, Nereocystis beds occur in more exposed sites in central California and are the only types of offshore kelp beds in northern California. In general, far less has been published to date on the fishes of central and northern California rock reefs and kelp forests than on those of southern California. Burge and Schultz (1973) provided descriptions of the fish fauna of Diablo Cove but did not specifically evaluate the effects of habitat on the fish assemblage there. Miller et al. (1967; summarized also in Miller and Geibel, 1973) contrasted the sportfish catches on exposed reefs in clear water with those at more sheltered reefs in turbid water. Miller and Geibel (1973) reported on scuba-based surveys of fishes in rock-reef and kelp-forest

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habitats near Monterey. They described the assemblage and the habitat associations of several species. In a relatively small-scale (0.5-ha) kelp-canopy removal experiment, they found no significant changes in adult density but did find a displacement of juvenile rockfish from the kelp canopy to the bottom. Bodkin’s (1988) Macrocystis removal experiments near Pt. Piedras Blancas were described before. Bodkin (1986) has also provided the best comparison to date of fish assemblages in Macrocystis and Nereocystis forests. In surveys near Pt. Piedras Blancas and Big Creek, he found that species composition and species diversity differed very little between the two types of kelp forests but that several species were more abundant, often markedly so, in Macrocystis. These included blue, olive, kelp, and black rockfishes in the midwater and gopher rockfish, kelp rockfish, striped seaperch, and painted greenling on the bottom. He concluded that the following factors may contribute to the differences in fish abundance in the two types of kelp forests: (1) increased food availability for blue rockfish during seasons when they consume algae; (2) the perennial nature of Macrocystis forests; (3) differences in abiotic conditions such as wave surge and sand scour, which affect the occurrence of Macrocystis versus Nereocystis and may also affect fishes directly; and (4) the differing physical structure of Macrocystis and Nereocystis in the midwater and canopy regions. The effects of other brown algae that provide vertical structure such as Egregia menziesii, Cystoseira osmundacea, Pelagophycus porra, and understory brown algae species such as Pterygophora californica, Laminaria farlowii and L. setchelli, Eisenia arborea, and Desmarestia ligulata have not been investigated extensively. Ebeling and Laur (1985) found that juvenile surfperch decreased in abundance when the understory of Pterygophora californica and Laminaria farlowii was reduced either naturally or experimentally. Stephens et al. (1984), however, found that fish density was low in the midbed region of the kelp forest at Palos Verdes, where Pterygophora californica was abundant. Likewise, the “kelpless cobble” site of Larson and DeMartini (1984), where the abundance of benthic and epibenthic species was lower than at the site with a Macrocystis canopy (see above), was dominated by Pterygophora. Rather than serving as a point of visual orientation, like Macrocystis and other brown algae with vertical structure, dense stands of Pterygophora may inhibit visibility within a meter of the bottom for benthic and epibenthic fishes. In addition, Pterygophora may inhibit the growth of foliose algae and “turf” (Foster and Schiel, 1985), upon which benthic species of fishes may depend for foraging. We have observed that juvenile rockfish settle in Cystoseira in Monterey Bay, and in general, small fishes may orient toward any large structure. Benthic drift algae, which are ultimately temporary but may persist for at least weeks, form an extension of the rock-reef and kelp habitat for some species of fishes (Vetter, 1998; Vetter and Dayton, 1999). Vetter (1998) found a number of fishes typically associated with rock reefs and kelp forests, including kelp bass, sheephead, blacksmith, señorita, pile perch, and black perch, near mats of drifting macrophytes near Scripps Canyon. These fishes often occurred in very high densities. We have also observed juvenile fishes, such as rockfish and white sea bass, associated with macrophyte detritus (Allen and Franklin, 1992; chapter 5). In summary, the effects of bottom characteristics and macroalgae on fishes off California are complex and perhaps not completely resolved. Bottom characteristics clearly influence the species composition and abundance of fishes. Species may associate with rocky bottoms in a variety of ways, such as for shel-

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ter, for nesting sites, for prey that lives in or on rocks, for points of visual orientation, or for the attached algae or “turf” that provides shelter for fish or for fish prey. Because of this, different aspects of bottom characteristics may best describe the habitat needs of different species. Some may require shelter holes of particular size, some may require high vertical relief, some even associate with the rock–sand interface, and some may be quite generalized in their requirements. Improvements in the measurement of bottom characteristics may help to resolve questions such as whether fish abundance and diversity are saturating functions (Patton et al., 1985) or accelerating functions (Ebeling et al., 1980a) of bottom relief. Recent advances in remote sensing have facilitated new ways of describing habitat (Greene et al., 1999), and these methods have, in turn, been applied to characterizing of species–habitat relationships and to estimating of fish abundance (Yoklavich et al., 2000). Although most work conducted in California shows that a high-relief rocky bottom is essential for a number of species of fish, the effect of Macrocystis on fishes is more complex. Over a sandy or low-relief rocky bottom, it seems clear that the presence of Macrocystis substantially enhances the diversity and abundance of fishes. As noted by DeMartini and Roberts (1990), a number of species with generalized habitat requirements will occupy an area of low-relief bottom if kelp is present. They suggest that kelp provides a point of visual orientation for a number of water-column species and that epibenthic, bottom-feeding species may benefit from prey produced in drifting kelp. The effect of kelp on fishes over high-relief rocky bottoms has been more difficult to determine. Clearly, a high-relief rocky bottom supports diverse and abundant assemblages of fishes. Nevertheless, some species depend to a great degree on kelp, even when a high-relief rocky bottom is present and even though they may occur in other habitats. These species include kelp perch, giant kelpfish, kelp clingfish, and perhaps kelp rockfish. In addition, young stages of several species associate strongly with kelp. On or near the bottom, abundances of many species are uncorrelated or only loosely correlated with kelp density. However, the abundances of some species increase in the water column over a high-relief rocky bottom when kelp is present, so the density of species measured over the entire water column may increase when kelp is present. We might tentatively conclude that some species depend strongly (although not completely) on kelp, even over a high-relief rocky bottom, and that other species may be more abundant when kelp is present, but that much of the fish assemblage over a high-relief rocky bottom is not dependent upon kelp. It would be good to resolve the nature of the relationship between kelp density and the species composition and abundance of fishes. Is fish density a saturating function of kelp density? Is there a lower threshold of kelp abundance for some species? What are the effects on fish assemblages of temporal variation in kelp density on various temporal scales? What happens seasonally, interannually, and perhaps interdecadally to fishes when kelp density fluctuates? DeMartini and Roberts (1990) found that with a decline in the area of the kelp forest at San Onofre, fish became denser in the remaining kelp forest. Similarly, there have been indications of shifts from cleared to uncleared areas in kelpremoval experiments (Miller and Geibel, 1973, Bodkin, 1988). What do such shifts mean relative to the carrying capacity of kelp forests for fishes and to the nature of the relationship between kelp density and fish abundance? Some of these questions may be difficult to resolve, in part because of matters of spatial scale. For example, kelp-removal experiments, or

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comparisons of fish abundance or recruitment in areas with or without kelp, may depend on the choices available for fish within the ranges of their movements and perception. Finding that fish disappear from a small area that is cleared of kelp does not necessarily mean that those fish would never use an area without kelp because they may simply have chosen between available alternatives. Levin and Hay (2002) examined the effect of the spatial scale of study on the relationship between fishes and Sargassum filipendula in the South Atlantic Bight. Similar studies of California could be useful. In any case, these are important questions in assessing populations of fishes in nearshore areas off California.

Overview of Habitat Functions for Fish Assemblages The structure of the reef/kelp habitat serves a number of functions for fishes, and the heterogeneity of this structure provides opportunities for niche diversification. Together, these factors account for the high density and diversity of fishes associated with this habitat (Bond et al., 1999). Some of the more important functions provided by the reef/kelp habitat to the fish assemblage are shelter, orientation, food availability, and nesting sites for the fish assemblage. Shelter is one of the most important functions provided by the reef/kelp habitat. Shelter is especially important to small species and to the young-of-year of many larger species but is also important to larger species that associate with the substrate. The notion of “shelter” is actually complex and can work in a number of ways. Most obviously, hard structures can provide physical protection from predators. Here, crevices, burrows, and caves in rock and other solid structures can prevent a predator from gaining access to potential prey. Second, an immobile substrate can provide physical shelter from wave surge. For example, black-and-yellow and gopher rockfish are found in more protected positions as wave surge increases (Larson, 1980a). Third, both hard and soft substrates can serve as objects behind which fish can hide, escaping visual detection by potential predators or prey. For example, newly settled kelp rockfish hide among the stipes and blades of Macrocystis in the kelp canopy and dart for shelter when approached by potential predators (Nelson, 2001). Closely related to the role of substrate in hiding fish, the substrate may provide a cryptic background that conceals a fish, even if it is not hidden behind an object. This function is important in both concealing potential prey from their predators, like kelp perch that are concealed by kelp from potential predators (Anderson, 1994, 2001), and in concealing ambush predators, such as giant kelpfish, from potential prey. Steele (1996, 1997, 1998, 1999) conducted one of the more thorough experimental analyses of the influence of predators and shelter abundance on mortality, using two species, bluebanded and blackeye goby. Behrents (1987) previously suggested that the recruitment success and survivorship of bluebanded gobies depend on shelter availability. Steele (1997) showed that predation halved survivorship in bluebanded gobies, but survivorship increased with shelter availability, with or without predator pressure (Steele, 1999). In contrast, shelter increased the survivorship of blackeye gobies only in the presence of predators. Survivorship on small patch reefs also increased in both species with distance from larger reefs (Steele, 1996). This suggests a predatory effect, which was confirmed for a variety of blennies in recent King Harbor recruit-

ment studies (Stephens and Pondella, unpubl. data). Recruitment of bluebanded gobies was strongly positive to the presence of conspecifics (Steele, 1997) but not blackeye gobies (Steele et al., 1998). Both species showed asymptotic survivorship based on species specific density characteristics, and bluebanded gobies showed reduced growth in the presence of predators. These data suggest that the effect of shelter is important to settlement survivorship and is species specific. In this case, the bluebanded goby is a very small brightly colored, territorial species that displays on open reefs but retreats to protective shelters for survival. By contrast, the blackeye goby is larger and protectively colored for its sand reef habitat, and numerous adults may occupy the same shelter. In tube dwelling species, such as the mussel blenny, Hypsoblennius jenkensi, and the yellowfin fringehead, Neoclinus stephensae, the presence of adults depends on available burrows (Stephens et al., 1970). Recruitment (settlement) may occur in burrow-free habitat, but postrecruitment mortality or migration occurs subsequently. The ability of competent reef fish larvae to select specific habitats (shelter sites, etc.) has not been demonstrated in these species. The absence of young-ofyear in inappropriate habitat sites could result from either habitat selection or postsettlement mortality. Shelter is required as a resting site for the adults of some species. For example, the blacksmith, an important diurnal planktivore, is missing from reefs without available nocturnal shelter sites. Some labrids (rock wrasse and señorita) shelter at night by burying in soft substrate adjacent to the reef. Shelter sites are the basis of territorial behavior in many small, shelterusing species (blennies, gobies, clinids, etc.). Shelter or nesting sites also anchor the territories of a number of larger species as well, such as garibaldi (Clarke, 1970), black-and-yellow and gopher rockfish (Larson, 1980b,c; Hoelzer, 1987), black perch (Hixon, 1981), giant kelpfish (Coyer, 1982), painted greenling (DeMartini, 1985, 1987), and possibly treefish (Haaker, 1978). Reefs and kelp provide relatively stable visual cues that allow fishes to orient to positions in and above the substrate. This feature is not found in pelagic or soft substrate (sand, mud) habitats. Much of the diversity of the reef fish assemblage is due to the differing features in the reef habitat: sand fringe, rock–sand interface, reef slope, reef crest, algal layering, and canopy. Each of these areas includes morphological or biotic features that further subdivide it. Many species are restricted to specific areas (sites). Orientation to such sites may involve species-specific habitat preference, competition, or fortuitous timing and history. The reef/kelp habitat affects food availability in many ways. Most algae growing on a reef require attachment to a hard substrate, and a limited number of reef fish use this resource directly (Horn, 1989). Invertebrate organisms feed or shelter in the algae, and they represent the greatest food resource for most reef fishes (see chapter 13). Many epibenthic species that do not directly seek shelter in the reef are pickers or winnowers of this resource (Laur and Ebeling, 1983), and nocturnal planktovores feed on zooplankton that emerges from the substrate at night (Ebeling and Bray, 1976; Hobson and Chess, 1976). Reef structure also affects water currents, concentrating planktonic organisms and making them more available to midwater feeders (Bray, 1981). Other species that reside on the reef may feed on adjacent soft substrate (DeMartini et al., 1994). The reduction in prey density in fringing areas may force longer feeding migrations by these residents. Finally, the presence of abundant and diverse reef fishes allows their exploitation by meso- (primarily Paralabrax and species of Sebastes) and macrocarnivores

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(largely elasmobranchs, white sea bass, lingcod, giant sea bass, and groupers). The importance of macrocarnivores to this system is poorly understood (Pondella and Allen, 2000) and may be highly modified due to fishing pressure. The nesting site is most often identical to the shelter site, especially for small cryptic or territorial species (gobies, blennies, kelpfishes, ronquils, pricklebacks, gunnels, clingfishes, and sculpins). Of the larger reef species, most are watercolumn spawners (basses and groupers, chubs, croakers, grunts, etc.) or viviparous (surfperches and rockfishes) (see chapter 24). Some larger species also have demersal eggs and usually parental care, i.e, damselfishes, toadfishes, wolffish, sculpin (Scorpaenichthys), and greenlings, many of which nest at their shelter sites like the smaller species.

with and without kelp (within the range of perception and choice for settling fish) and the subsequent survival of those that settle in alternative conditions. Settled juveniles of many other species show restricted habitat distributions. Rockfish show a number of specializations in habitat (Carr, 1991; Love et al., 1991). Many young-of-year fishes occupy warm shallow tidepools at settlement (opaleye, black perch, pile perch, and zebraperch) and subsequently develop preferences similar to those of adults, leaving the pools for their subtidal habitat and exhibiting ontogenetic shifts in temperature selection (Norris, 1963; Schrode et al., 1982; Ehrlich et al, 1978). A more in-depth discussion of these processes is presented in chapter 15.

Activities of Fishes in Reef Habitats Roles of Reef and Kelp in Recruitment and Survival of Young-of-Year Fishes

Residency, Seasonality, and Movement of Kelp/Reef Fishes

Recruitment of fishes to rock reefs and associated kelp beds may occur in a number of ways, although the mechanisms are not clearly understood for most species. Most commonly, passive drift may carry late larval stages to the reef vicinity, where settlement takes place (Cowen, 1985). In other species (perhaps chubs, giant kelpfish, or rockfishes), actively swimming late larvae or pelagic juveniles may follow gradients in perceptual cues or internal waves to the reefs. In still other species, larvae produced on the reef may have behavioral mechanisms to retard the drift process, keeping them in the general area for subsequent settlement (Marliave, 1986; Stevens et al., 1987). In the case of livebearers such as embiotocids, the relatively mature young-of-year are born on the reef occupied by the adult. In other species, individuals migrate to the reef from other places where they settled or were born. Shiner perch, Cymatogaster aggregata, exhibit this behavior. Once young-of-year individuals have established residence on the reef, survival depends on their behavioral abilities and the protection supplied by the reef, kelp, and epibenthic cover. Two interesting differences have been noted in settlement: some species settle primarily to sites occupied by conspecifics (bluebanded goby; Steele, 1997), whereas others settle in habitats in the reef/kelp region that are not occupied by adults of that species and then migrate later to adult habitats. The distributions of postlarval, settled fishes is likely to be a combination of habitat selection by the fish and postsettlement mortality. Habitat selection seems clear in some species. Kelp seems to play a role in settlement of some species associated with a reef/kelp habitat. Carr (1989) reported selective settlement of late larval kelp bass to kelp fronds at Santa Catalina Island in the Southern California Bight, followed by movement of settled young-of-year to the rock reef. Several species of rockfish (kelp, black-and-yellow, gopher, and copper) also seem to settle preferentially in the kelp canopy, at least when a canopy is available (Hoelzer, 1988; Carr, 1991; Nelson, 2001). However, although species such as kelp bass and these rockfishes do seem to use kelp when it is present, the consequences of a large-scale lack of kelp are still not clear. For example, in the absence of kelp at King Harbor, Redondo Beach, young-of-year kelp bass recruit to the intertidal portion of the breakwater and subsequently move to the breakwater base where they associate with patches of foliose algae. These territorial young-of-year may hold position for many months, later forming aggregations of subadults, which may emigrate. In cases such as this, it would be interesting to compare the number of larvae that initially settle in areas

Temperate reefs have a greater seasonal component of productivity than tropical reefs, which affects the structure and continuity of the fish assemblage. Additionally, whereas coral reefs are generally isolated habitats, sublittoral rocky reefs may extend for miles with little habitat break. These two factors should affect the way species occupy temperate reef habitats (Ebeling and Hixon, 1991). Unfortunately, these aspects of reef fishes are not well described for California fishes because most communitywide studies are carried out once a year. An alternative concept would describe reef assemblages as temporary assemblages with many key species moving between reefs and along the coastline searching for food and shelter and remaining at a site only as long as habitat quality is sustained. In such a model, the genetic structure of such populations should not reflect local specializations, and the assemblage should be bounded by regional physical gradients and the physiological limits of its component species within the limits of their ecological flexibility. Movements by adults may supplement larval drift, producing panmictic California fish populations. The limited population genetic work on California reef fishes may support this premise (Halderson, 1980; Beckwitt, 1983; Tranah and Allen, 1999; Bernardi, 2000). Much of our knowledge of reef fish biology is based on information from coral reef fishes (reviews by Ehrlich, 1975; Sale, 1991). Our early (1950–60s) ideas of assemblage interactions, territoriality, recruitment, and stability are centered on these data because little work in temperate communities was available. Temperate rocky reefs or kelp beds are known primarily from summer–fall studies (Ebeling and Hixon, 1991). But as “seasonality increases from the tropics . . . through the cold temperate zones, the stronger seasonal variation in the higher latitudes elicits greater, albeit predictable, responses in the reef fish assemblages” (Ebeling and Hixon, 1991). What can we infer is occurring in these fish assemblages during the colder, less productive months? The major question regarding temperate assemblages is, “What response does the assemblage have to seasonal changes in productivity and climate?” Do assemblage members modify their behavior to cope with these regular occurrences (e.g., change their diets; Love and Ebeling, 1978), or do they search for more favorable sites? To illustrate the difficulty and magnitude of this problem, consider sportfishing data from isolated reefs such as Naples Reef (off the Santa Barbara coast) and power plant entrapment data from the well-studied system of King Harbor, Redondo Beach. In both systems, hundreds to thousands of fishes are

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removed annually. Yet these reefs maintain high standing stocks and easily outperform other reefs in fish abundance. To attempt to address this problem, from 1975 through 1977, we (Stephens et al., unpublished data) tagged more than 2000 fish of 34 species captured in fyke nets set along the King Harbor breakwater. Tagged fish were released adjacent to the capture site. We recorded sightings of tagged fish along the breakwater as well as returns and losses to intake entrainment. Diver sightings of tagged fishes diminished rapidly; few fishes were sighted after 4 months and only one fish at 7 months. Loss to entrainment occurred rapidly (usually within a few days of tagging), whereas fishers recaptured fish up to 14 months later (Stephens, unpublished data). No significant movements were recorded in these data, but the absence of tagged fish suggested movement off the breakwater site or tag loss. Similarly, DeMartini et al. (1994) tagged fish on an isolated artificial reef off Del Mar to follow growth patterns in an 8-month study (April–November 1989). The observed median period at liberty for tagged fish was 6 months. Certainly some fishes are residents on reefs (Clarke, 1970; Larson, 1980; Hixon, 1981; Lea et al., 1999; Lowe et al., 2003). However, if studied at all, the residence of most fishes has not been tracked for long periods of time and certainly not for their entire life spans or over large spatial areas, leaving this as an important aspect of future studies (chapter 20). One possible explanation for these processes is that fishes move based on “ideal free distribution” (MacCall, 1990). As resources in an “ideal free distribution” decrease, fish should search for increased “habitat quality.” Similarly, as fish are removed from a system with high resource value, one might expect movement onto the reef from less valuable habitats. This theory may explain why loss of fishes at relatively high rates from Naples Reef and King Harbor does not elicit drastic decreases in abundance. Perhaps these fishes are quite mobile, and these observations indicate linkage along the lines of metapopulation theory. Seasonal changes in fish assemblages have rarely been studied in temperate regions due to poor scuba study conditions in winter and spring (Ebeling and Hixon, 1991). Thus we have limited knowledge of the seasonal movements of rocky reef fishes, and this is summarized in chapter 21. In addition to seasonal movements, fishes have daily activity cycles that are genetically encoded. These cycles are entrained by light intensity and/or tides (Wooton, 1990; Thorpe, 1978). On subtidal reefs, most species are either diurnal or nocturnal, although activities such as feeding may be enhanced during crepuscular periods. Temperate species show less specialization than tropical assemblages for activity periods, though tropically derived taxa such as wrasses and damselfish show remnants of these specializations. There are fewer nocturnal teleosts on our temperate reefs and many elasmobranchs are nocturnal. Daily activity cycles are largely associated with feeding strategies (see chapter 13). The reef is a dynamic place as we move through nocturnal, diurnal, and crepuscular periods; chapter 21 discusses these processes.

Interannual Variability of Reef Fish Assemblages Few long-term studies of interannual variability in reef/kelp fish assemblages have been carried out. The longest such study is that of Hobson at Catalina Island, which began in 1973 as an annual survey and still continues. Unfortunately, however, an analysis of this long-term data set has not been published. The surveys at King Harbor and Palos Verdes Point by Stephens and colleagues began in 1974 and include a continuous series of

quarterly transects by depth as well as monthly larval samples, recruitment and young-of-year surveys, and cryptic fish samples. This continuing 28-year study is the baseline for assemblage variability in southern California (Stephens and Zerba, 1981; Stephens et al, 1984, 1994; Holbrook et al., 1994, 1997; Holbrook and Schmitt, 1996; Pondella et al., 2002; Stephens and Pondella, 2002). Although fish recruitment and mortality are critical factors for understanding the population dynamics of reef fishes, temperature and productivity appear to be important driving factors in these processes. The King Harbor and Palos Verdes studies began near the end of the cool cycle of the Pacific decadal oscillation (PDO) (Hare and Francis, 1995; Mantua et al., 1997) which began in 1946 and ended in 1976 to 1977, in concert with the small ENSO event in 1977 to 1978. A warm phase of the PDO occurred subsequently, although it may have ended in the mid to late 1990s (Chavez et al., 2003). As of 2004, King Harbor data had not yet shown a faunal shift associated with the return of cooler temperatures. However, the fish assemblage did undergo a major faunal shift correlating with the shift from a cool to a warm regime in 1977 (Stephens and Zerba, 1981; Stephens et al., 1994). Two dominant planktivores, Sebastes mystinus and Cymatogaster aggregata, disappeared or became rare with this temperature shift, and species of the largely tropical wrasses (Labridae), damselfishes (Pomacentridae), and sea basses (Serranidae) became more important members of the assemblage. During the early 1980s, the increase in warm temperate fishes reached a maximum, and the great El Niño of 1982 to 1984 affected the densities of many species. Since the mid 1980s, there has been a general decline in reef fishes (Stephens et al., 1994). This decline is observed in larval abundance (Stephens and Pondella, 2002) as well as in adults (Holbrook et al., 1997; Brooks et al., 2002). Although the density of many species changed significantly in the last three decades, the overall density and species richness of the assemblage has shown no long-term trends. The assemblage at King Harbor had a significantly higher number of species and species per transect in five fully sampled years prior to 1980, during the cold-water period and transition, than after 1980, but the decline was a stepwise change with the advent of the warm cycle (Holbrook et al., 1997). After 1980, no trend was apparent. At Palos Verdes, no trend is apparent from the onset of the studies. This suggests that there was some overall consistency in the “community” even with major changes in the densities of individual species, and this might suggest that the assemblage was operating at close to its biotic potential. One problem with many “long-term” data sets is that they rarely include more than a few species of interest. In that case, decreases in species densities, which may represent normal decadal variability, may be interpreted as a decremental trend. Data on “core teleosts” from King Harbor and Santa Cruz Island (Holbrook and Schmitt, 1996) show such a decrease from 1985 to 1992. That same data set prior to 1985 would have shown an increasing or stable assemblage, and since 1992 to 2001, would also appear relatively stable, whereas data for the whole period appear stable after about 1980 (20 years). Brooks et al. (2002) analyzed the above data sets as well as impingement data from southern California Edison’s coastal electric generating plants to see if fish declines noted between 1977 and 1993 were consistent across trophic levels, modes of reproduction, extent of geographic range, benthic versus pelagic food webs, and habitat. They found strong concurrence in these data and relate the declines to a productivity shift that began in 1977. Productivity would also explain the decline in larval abundance during the same period (Stephens and Pondella,

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2002) and a decline in juvenile survivorship of surfperches (Pondella et al., 2002). Brooks et al. (2002) suggest that only a regime-change reversal would be expected to change this pattern. Such a change is apparently occurring as young-of-year surfperch are increasing at their study site as well as in King Harbor (A. Brooks personal communication; D. Pondella unpublished data). This hypothesis will be tested with the continued progress of these research programs. The changes reported here underscore the necessity of continued long-term monitoring.

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Norris, K.S. 1963. Function of temperature in the ecology of the percoid fish Girella nigricans (Ayres). Ecol. Monogr. 33:23–62. O’Connell, C.P. 1953. The life history of the cabezon, Scorpaenichthys marmoratus (Ayres). California Department of Fish and Game, Fish Bulletin 93. Patton, M.L., R.S. Grove, and R.F. Harman. 1985. What do natural reefs tell us about designing artificial reefs in Southern California? Bull. Mar. Sci. 37:279–298. Pequegnat, W.E. 1964 The epifauna of a California siltstone reef. Ecology 45:272–283. Pondella, D. J. II, and L. G. Allen. 2000. The nearshore fish assemblage of Santa Catalina Island. In the Proceedings of the Fifth California Islands Symp., D. R. Browne, K. L. Mitchell, and H. W. Chaney (eds.). Santa Barbara Museum of Natural History, Santa Barbara, CA, 394–400. Pondella, D.J., and M.J. Allen (eds.) 2001. Proceedings Spec. Symp.: New and rare fish and invertebrate species to California during the 1997–98 El Niño, sponsored by The Southern California Academy of Sciences, May 20, 2000. 2001. Daniel J. Pondella, II and M. James Allen (eds.). Bull. South. Calif. Acad. Sci. 100(3):129–251. Pondella, D.J., II, J.S. Stephens, Jr., and M.T. Craig. 2002. Fish production of a temperate artificial reef based upon the density of embiotocids (Teleostei: Perciformes). ICES J. Mar. Sci. 59:S88–93. Quast, J.C. 1968a. Some physical aspects of the inshore environment, particularly as it affects kelp-bed fishes. In W. J. North and C.L. Hubbs (eds.), Utilization of kelp-bed resources in southern California. California Department of Fish and Game, Fish Bulletin 139, pp. 25–34. ———. 1968b. Fish fauna of the rocky inshore zone. In W.J. North and C.L. Hubbs (eds.), Utilization of kelp-bed resources in Southern California. California Department of Fish and Game, Fish Bulletin 139, pp. 35–55. ———. 1968c. Estimates of the populations and the standing crop of fishes. In W.J. North and C.L. Hubbs (eds.), Utilization of kelp-bed resources in Southern California. California Department of Fish and Game, Fish Bulletin 139, pp. 57–79. ———. 1968d. Observations on the food and biology of the kelp bass, Paralabrax clathratus with notes on its sportfishery at San Diego, California. In W.J. North and C.L. Hubbs (eds.), Utilization of kelpbed resources in Southern California. California Department of Fish and Game, Fish Bulletin 139, pp. 81–108. ———. 1968e. Observations on the food of the kelp-bed fishes. In W.J. North and C.L. Hubbs (eds.), Utilization of kelp-bed resources in southern California. California Department of Fish and Game, Fish Bulletin 139, pp. 109–142. ———. 1968f. Effects of kelp harvesting on the fishes of the kelp beds. In W. J. North and C. L. Hubbs (eds.), Utilization of kelp-bed resources in southern California. California Department of Fish and Game, Fish Bulletin 139, pp. 143–149. Ralston, S., and D.F. Howard. 1995. On the development of year-class strength and cohort variability in two northern California rockfishes. U.S. Fish. Bull. 93:710–720. Richards, D.V., and J.M. Engle. 2001. New and unusual reef fish discovered at the California Channel Islands during the 1997–1998 El Niño. Bull. South. Calif. Acad. Sci. 100(3):175–185. Ricker, W.E. 1975. Computation and interpretation of biological statistics of fish populations. Fish. Res. Bd. Can. Bull. 191:1–382. Roach, S.W., F.G. Claggett, and J.S.M. Harrison. 1964. An air lift pump for elevating salmon, herring, and other fish of similar size. J.Fish. Res. Bd. Can. 21(4):845–849. Sale, P.F. (ed.). 1991. The ecology of fishes on coral reefs. Academic Press. Schenck, H., Jr. 1955. Skin diver’s and spearfisherman’s guide to American waters. Cornell Maritime Press, Cambridge, MD. Schrode, J.B., K. Zerba, and J.S. Stephens, Jr. 1982. Ecological significance of temperature tolerance and preference of some inshore California fishes. Trans. Am. Fish. Soc. 111:45–51. Starks, E.C., and E.L. Morris. 1907. The marine fishes of southern California. Univ. Calif. Publ. Zool. 8:9–19. Stallings, C.D. 2002. The influence of habitat at several spatial scales on kelp forest fishes. M.S. Thesis, San Francisco State University. Steele, M.A. 1996. Effects of predators on reef fishes: separating cage artifacts from effects of predation. J. Exp. Mar. Biol. Ecol. 198: 249–267. ———. 1997. The relative importance of processes affecting recruitment of two temperate reef fishes. Ecology 78:129–145. ———. 1998. The relative importance of predation and competition in two reef fishes. Oecologia 115:222–232.

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———. 1999. Effects of shelter and predators on reef fishes. J. Exp. Mar. Biol. Ecol. 233:65–79. Steele, M.A., G.E. Forrester, G.R. Almany. 1998. Influences of predators and conspecifics on recruitment of a tropical and a temperate reef fish. Mar. Ecol. Prog. Ser. 172:115–125. Stephens, J.S., Jr. 1992. California sheephead. In California’s living marine resources and their utilization, W.S. Leet, C.M. Dewees and C.W. Haugen (eds.). Sea Grant Extension Publication UCSGEP 9212, pp. 176–177. Stephens, J.S., Jr., R.K. Johnson, G.S. Key, and J.E. McCosker. 1970. The comparative ecology of three sympatric species of California blennies of the genus Hypsoblennius Gill (Teleostomi, Blenniidae). Ecol. Monogr. 40:213–232. Stephens, J.S., Jr., and K.E. Zerba. 1981. Factors affecting fish diversity on a temperate reef. Environ. Biol. Fishes. 6:111–121. Stephens, J.S., Jr., P.A. Morris, K. Zerba, and M. Love. 1984. Factors affecting fish diversity on a temperate reef: the fish assemblage of Palos Verdes Point, 1974–1981. Environ. Biol. Fishes. 11:259–275. Stephens, J.S., Jr., G.A. Jordan, P.A. Morris, M.M. Singer, and G.E. McGowan. 1986. Can we relate larval fish abundance to recruitment or population stability? A preliminary analysis of recruitment to a temperate rocky reef. CalCOFI Rep. 27:65–83. Stephens, J.S., Jr., P.A. Morris, D.J. Pondella, T.A. Koonce, and G.A. Jordan. 1994. Overview of the dynamics of an urban artificial reef fish assemblage at King Harbor, California, USA, 1974–1991: A recruitment driven system. Bull. Mar. Sci. 55:1224–1239. Stephens, J.S., Jr. and D.J. Pondella, II. 2002. Larval productivity of a mature artificial reef: the ichthyoplankton of King Harbor, California, 1974–1997. ICES J. Mar. Sci. 59:S51–58. Stevens, E.G., W.Watson, and H.G. Moser. 1987. Development and distribution of larvae and pelagic juveniles of three kyphosid fishes (Girella nigricans, Medialuna californiensis, and Hermosilla azurea) off California and Baja California. U. S. Fish. Bull. 87:745–768. Tarp, F.H. 1952. A revision of the family Embiotocidae (the surfperches). California Department of Fish and Game, Fish Bulletin 88. Tegner, M.J., P.K. Dayton, P.B. Edwards, and K.L. Riser. 1996. Is there evidence for long-term climatic change in southern California kelp forests? CalCOFI Rep. 37:111–126. Terry, C. and J.S. Stephens, Jr. 1976. A study of the orientation of selected embiotocid fishes to depth and shifting vertical temperature gradients. Bull. South. Calif. Acad. Sci. 75:170–183. Thorpe, J.E. (ed). 1978. Rhythmic activity of fishes. Academic Press. Tranah, G.J., and L.G. Allen. 1999. Morphologic and genetic variation among six populations of the spotted sand bass, Paralabrax maculatofasciatus, from southern California to the Upper Sea of Cortez. Bull. South. Calif. Acad. Sci. 98 (3):103–118. Turner, C.H., E.E. Ebert, and R.R. Given. 1968. The marine environment offshore from Point Loma, San Diego County. California Department of Fish and Game, Fish Bulletin 140. Turner, C.H., E.E. Ebert, and R.R. Given. 1969. Man-made reef ecology. California Department of Fish and Game, Fish Bulletin 146. Ugoretz, J., D.A. VenTresca, C.A. Pattison, S.E. Blair, R.S. Hornady, J.N. Plant, and A.A. Voss. 1997. New equipment for performing measured-distance diving surveys. Calif. Fish Game 84:168–170. Vetter, E.W. 1998. Population dynamics of a dense assemblage of marine detritivores. J. Exp. Mar. Biol. Ecol. 226:131–161. Vetter, E.W., and P.K. Dayton. 1999. Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Mar. Ecol. Prog. Ser. 186:137–148. Walters, K. 2002. A comparison of life histories in two species of fish. M.A. Thesis, San Francisco State University, San Francisco, CA. Wooton, R.J. 1990. Ecology of teleost fishes. Chapman and Hall, Fish and Fisheries Series. Yoklavich, M.M., H.G. Greene, G. Cailliet, D. Sullivan, R. Lea, and M. Love. 2000. Habitat associations of deep-water rockfishes in a submarine canyon: an example of a natural refuge. U.S. Fish. Bull. 98:625–641. Yoshihara, K. 1997. A fish body length measuring method using an underwater video camera in combination with laser discharge equipment. Fish. Sci. 63(5):676–680. Yoshiyama, R.M., C. Sassaman, and R.N. Lea. 1987. Species composition of rocky intertidal and subtidal fish assemblages in central and northern California, British Columbia-southeast Alaska. Bull. South. Calif. Acad. Sci. 86(3):136–144. Young, P.H. 1963. The kelp bass (Paralabrax clathratus) and its fishery, 1947–1958. California Fish and Game, Fish Bulletin 122.

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CHAPTER 10

Deep Rock Habitats M I LTO N S. LOVE AN D MARY M. YO K LAVI C H

Introduction In this chapter, we discuss those fishes characteristically found on or over complex seafloor habitats comprising various amounts of cobble, boulders, and rock outcrops in water depths ranging from 30 to 500 m. This depth range encompasses the continental shelf and upper continental slope of California (Greene et al., 1999). We also discuss those fishes associated with such artificial structures as oil platforms off Southern California at similar depths. Because very little is known of fish assemblages associated with deep rock habitats off Baja California, we limit our discussion to California waters. See fig. 10-1 for a general depiction of bathymetry and place names of areas referenced in this chapter. Fishes that associate with complex benthic habitats below scuba depths (i.e., greater than 30 m) are difficult and expensive to survey. Historically, fishing nets of various types, particularly trawl nets, have been used to make almost all assessments of deep-water fish communities. However, the rugged nature of many of these habitats renders trawl surveys less effective over low-relief structures, such as cobblestone and boulder fields, and virtually useless to assess fish assemblages accurately over high-relief rock outcrops. In addition, surveys conducted remotely from the sea surface using all types of fishing gear yield little or no information on the association among benthic habitats and fish assemblages. Early California biologists, such as William Ayres, Carl and Rosa Eigenmann, and David Starr Jordan, rarely conducted their own field surveys. Almost all of their information on fishes associated with rock habitats came from specimens purchased in fish markets and from interviews with fishermen regarding their catches. Unfortunately, most of these fishermen spoke little or no English, which often led to only a vague understanding of the substratum type and depth from which the fishes were collected. As an example, Jordan (1884) described the greenspotted rockfish (Sebastes chlorostictus) as “Occurring about the rocks in considerable depths of water.” In the same publication, he erroneously stated that the nearshore treefish (Sebastes serriceps) inhabited “rather deep water.”

In contrast to the fine-mesh trawl nets that caught most species occurring on soft substrata, the hook-and-line fisheries operating over rocky outcrops were more selective and did not in any way accurately sample the diverse species assemblages. Even when researchers collected their own specimens from deep waters, as did Carl and Rosa Eigenmann from Cortes Bank in 1889, precise depths of capture rarely were provided (Eigenmann and Eigenmann, 1889). Thus, although this early sampling was useful in establishing the occurrence of a species in a region and something of its general habitat association, it was not possible to characterize complete species assemblages accurately on complex structures. The first summary of fish assemblages on deep-water rock outcrops off California resulted from collections made aboard commercial passenger fishing vessels (CPFVs) in central and northern California (Miller and Gotshall, 1965). Fishes were measured and identified, and estimates of seafloor depth were recorded. Characterizing this assemblage, Miller and Gotshall noted that most of the fishes taken in water between about 40 and 100 m were rockfishes, although lingcod (Ophiodon elongatus), sablefish (Anoplopoma fimbria), petrale sole (Eopsetta jordani), and cabezon (Scorpaenichthys marmoratus) were caught occasionally. Over the entire depth range, yellowtail rockfish (Sebastes flavidus) followed by bocaccio (S. paucispinis), chilipepper (S. goodei), widow (S. entomelas), greenspotted, and starry (S. constellatus) rockfishes, dominated the catch. More recently, information regarding fish assemblages off California has come from recreational creel censuses (Reilly et al., 1993; Karpov et al., 1995; Mason, 1995, 1998), commercial fishery data (Pearson and Ralston, 1990), and fisheryindependent government surveys (Gunderson and Sample, 1980; Dark and Wilkins, 1994; Shaw et al., 2000; Williams and Ralston, 2002). However, all of these surveys suffered from a lack of habitat specificity because it is not possible to assess fish communities accurately over complex, high-relief seafloor substrata with any of these techniques. A more comprehensive understanding of fish assemblages associated with deep rock habitats has been the result of quantitative surveys conducted from an occupied research submersible during the past decade at several sites off central and southern California. Such surveys have described

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F I G U R E 10-1 Locations of place names, including islands, canyons, natural rock outcrops, and oil and gas platforms, referenced in this chapter. Also depicted is general bathymetry (in meters).

the importance of small-scale refugia to deepwater fishes in a submarine canyon in Monterey Bay (Yoklavich et al., 2000), assessed habitats and associated fishes in and out of marine protected areas off central and southern California (Lissner and Dorsey, 1986; Yoklavich et al., 1997, 2002; Love and

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Yoklavich, unpublished data), and characterized the fish assemblages around offshore oil platforms off southern California (Love et al., 1999; 2000; 2003). These studies form the foundation of our chapter on fish assemblages associated with deep rock habitats.

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Natural Outcrops Overview of Habitats The distribution of fishes off California is influenced by depth, substratum type, temperature, and ocean currents, which when integrated produce fish habitat. We have divided deep rock habitats into two categories based on water depth: (1) shelf (30–200 m) and (2) upper slope (201–500 m). The extent of the continental shelf ranges from about 0.5 km (off the Big Sur coast) to 180 km (around Cortes Bank) offshore of California. The offshore continental slope extends to more than 1000 m water depth. There are a variety of deep rock habitat types off California. The shelf habitats comprise bedrock outcrops, isolated pinnacles and large rock banks, boulder fields, mixtures of low-relief sand or mud and cobble fields, and a few offshore islands. Examples include extensive rock and boulder fields off headlands such as Point Sur; isolated bedrock that can be several meters high and surrounded by a flat, sandy seafloor of Monterey Bay; Cordell Bank off central California, and Tanner and Cortes Banks in the offshore water of the Southern California Bight. The offshore upper slope habitats are largely composed of expansive mud fields interspersed with rock outcrop and scattered boulders. Several submarine canyons containing slumps of rock talus piles, scarps, and ledges are part of the shelf and slope systems. A prominent example is the Monterey Bay Canyon system, which cuts into the shelf less than 1 km from shore and extends down the continental slope to depths greater than 1000 m off central California. Megafaunal invertebrates, such as sea anemones, sponges, black coral, crinoids, and basket stars, provide substantial structure on deep rock habitats. In broad terms, the ocean off California can be divided into two water masses (see fig. 10-2 for reference). Waters to the north and west of Point Conception typically are cool because (1) the California Current flows equatorward from high latitudes year-round and (2) frequent upwelling of cold deep water occurs at several headlands along this stretch of coast during spring and summer. On the other hand, year-round cyclonic circulation in the Southern California Bight entraps water, which results in warm water flowing poleward along the coast to the south and east of Point Conception as far as the Santa Barbara Channel. Reflecting these temperature regimes, fishes in central and northern California generally are more tolerant of cold water than those in southern California, which are more temperate or subtropical. Interestingly, San Miguel Island and part of Santa Rosa Island are located farthest north and west of all the Channel Islands and are therefore bathed in California Current water; fish assemblages of these two islands more closely resemble those off central California than those around other of the Channel Islands (Hubbs, 1974; Love et al., 1985).

Overview of Fish Assemblages Rockfishes dominate the fish assemblages on deep rock habitats off California. Half of the 52 species and 77% of the total number of fishes identified in a submarine canyon in Monterey Bay at 94–305 m water depth were rockfishes (Yoklavich et al., 2000). At least 36 species of the 82 species of fishes identified in one study off the central California coast were rockfishes; 95% of all fishes surveyed at water depths of

35–100 m were rockfishes, and 64% of fishes at depths of 100–250 m were rockfishes (Yoklavich et al., 2002). Similarly, 42 rockfish species comprised 92.5% of all fishes surveyed at depths of 35–300 m off southern California (Love et al., 2003). In general, species diversity (that is, the number of rockfish species) is greatest off southern California and diminishes to the north and south (fig. 10-3). Rockfish diversity also increased in mixed habitats of complex rock and mud (Yoklavich et al., 2000) and generally with water depth (Yoklavich et al., 2002). Reflecting differences in water masses, a number of more temperate or subtropical species, particularly freckled (Sebastes lentiginosus), honeycomb (S. umbrosus), pinkrose (S. simulator), and whitespeckled (S. moseri) rockfishes, treefish, California scorpionfish (Scorpaena guttata), and threadfin bass (Pronotogrammus multifasciatus) are either absent or less common north of Point Conception. Flag (Sebastes rubrivinctus), greenblotched (S. rosenblatti), rosy (S. rosaceus), speckled (S. ovalis), squarespot (S. hopkinsi), and starry rockfishes, chilipepper and cowcod (S. levis) are common on mid- and deep-shelf rock habitats off southern and central California but become less abundant or are absent altogether off northern California. A number of species, including black (Sebastes melanops), China (S. nebulosus), quillback (S. maliger), rosethorn (S. helvomaculatus), redbanded (S. babcocki), yelloweye (S. ruberrimus), and yellowtail rockfishes, and wolf-eel (Anarrhichthys ocellatus) are relatively abundant in northern and even central California but rare in much of southern California (Reilly et al., 1993; Love et al., 2002; Love, unpubl. data; Yoklavich unpubl. data; Yoklavich et al., 2000). Some of these species, such as yelloweye rockfish, have a center of distribution to the north and occur in southern California only in deep water (i.e., about 200 m) around those offshore banks (e.g., Tanner and Cortes Banks) that are influenced by the California Current (Eigenmann and Eigenmann, 1889; MacGregor, 1970). In addition, adults of some species, such as copper (Sebastes caurinus) and vermilion (S. miniatus) rockfishes and lingcod, live in shallower water (e.g., 10 m) north of Point Conception than they do off southern California (Burge and Schultz, 1973; Love et al., 2002). Fishes living on rock outcrops can be placed into one of three behavioral categories: (1) midwater aggregators, (2) demersal aggregators, and (3) demersal nonaggregators or solitary individuals. Midwater aggregators, though loosely associated with rock structure, spend time as many as 30 m or more above the seafloor in large schools. Many, if not most, of these species descend to the seafloor during part of the day, most often at dusk, but sometimes at dawn. Black, blue (Sebastes mystinus), canary (S. pinniger), chilipepper, shortbelly (S. jordani), widow, and yellowtail rockfishes, juvenile and young-adult bocaccio, and blacksmith (Chromis punctipinnis) are examples of species in this category. Demersal aggregators rarely ascend more than a few meters from the bottom; these include squarespot, halfbanded (S. semicinctus), pygmy (S. wilsoni), young vermilion, and copper rockfishes. Demersal nonaggregators usually occur on the seafloor, often sheltering in or near complex habitat such as caves, crevices, and overhangs. These species are either solitary or found in small groups and include adult brown (S. auriculatus), copper, flag, greenspotted (S. chlorostictus), greenstriped (S. elongatus), pinkrose, rosethorn, rosy, swordspine (S. ensifer), and yelloweye rockfishes, as well as cowcod, large adult bocaccio, blackeye goby (Rhinogobiops nicholsii), combfishes (Zaniolepis spp.), lingcod, wolf-eel, and cabezon. A few species are not so easily categorized. Individual splitnose

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F I G U R E 10-2 A schematic of the primary ocean currents off California, modified from PFMC (2003).

rockfish, for instance, often rest in shallow depressions in soft mud or next to rock on the seafloor; each fish is well separated from one another. However, occasionally they form large schools tens of meters above the seafloor. In addition, some species change behavior as they mature. Young bocaccio are midwater aggregators whereas older individuals become

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reclusive, solitary individuals residing in caves and crevices (Love et al., 2002; Yoklavich et al., 2000). In this chapter, we attempt to portray representative fish assemblages as they exist today, covering a relatively broad depth and geographic range (table 10-1). These characterizations do not dwell on the rare fish visitor or the unusual unfished

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F I G U R E 10-3 Distribution of the number of species of rockfishes along the west coast of North America (from Love et al., 2002).

outcrop. In addition, some species occupy more than one community. As an example, juveniles of several species often occur in waters shallower than that of the adults, and therefore these species will be included in several depth categories. These should be considered only as generalized divisions because fish assemblages vary considerably on multiple scales of time and space. For instance, the long-term ocean warming of the 1980s and 1990s has drastically altered the midshelf rockfish communities off southern California. Juvenile and adult blue and olive (Sebastes serranoides) rockfishes and juvenile copper rockfish and bocaccio, once important members of the midshelf community, were absent for most of that period (Stephens et al., 1984).

In addition and almost without exception, these are impacted fish assemblages. Decades of overfishing, together with over 20 years of warm ocean conditions since the mid1970s, has in many cases significantly changed these communities. Many of the previously dominant species, such as canary, darkblotched (Sebastes crameri), and widow rockfishes, bocaccio, cowcod, and lingcod, are now classified as overfished and in some instances are almost absent from important habitats (Love et al., 1998, 2002; M. Love and M. Yoklavich, unpubl. data; Yoklavich et al., 2000). Today, the fishes that dominate most rock outcrops in deep water are dwarf species such as pinkrose (southern California only), halfbanded, pygmy, squarespot, and swordspine rockfishes. These fishes

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TA B L E 10-1

Typical Adult Fish Assemblages over Rock Substrata off California Southern California Midshelf Scorpaenidae: Blue, bocaccio, California scorpionfish, canary, calico, chilipepper, copper, cowcod, flag, freckled, greenblotched, greenspotted, halfbanded, honeycomb, olive, pygmy, rosy, speckled, squarespot, starry, vermilion, widow, whitespeckled Gobiidae: Blackeye goby Labridae: Senorita, sheephead Pomacentridae: Blacksmith Serranidae: Threadfin bass Embiotocidae: Pile perch, sharpnose seaperch, white seaperch (Phanerodon furcatus) Hexagrammidae: Lingcod, painted greenling Deep Shelf Scorpaenidae: Bocaccio, bank, canary, chameleon (Sebastes phillipsi), chilipepper, cowcod, dwarf-red (S. rufinanus), flag, halfbanded, greenblotched, greenspotted, Mexican (S. macdonaldi), pink (S. eos), pygmy, pinkrose, semaphore (S. melanosema), shortbelly, speckled, swordspine, vermilion, whitespeckled, widow, yellowtail Hexagrammidae: Lingcod Slope Scorpaenidae: Aurora (Sebastes aurora), bank, blackgill, bocaccio, bronzespotted (S. gilli), chameleon, chilipepper, cowcod, greenblotched, pink, pinkrose, shortbelly, splitnose Cottidae: Threadfin sculpin (Icelinus filamentosus) Hexagrammidae: Lingcod Central California and Northern California Midshelf Scorpaenidae: Black, blue, bocaccio, canary, chilipepper, china, copper, cowcod, flag, halfbanded, olive, pygmy, quillback, rosy, squarespot, starry, vermilion, widow, yellowtail, yelloweye Hexagrammidae: Lingcod, kelp greenling, painted greenling Cottidae Cabezon Gobiidae: Blackeye goby Embiotocidae: Pile perch, sharpnose seaperch, white seaperch Anarhichadidae: Wolf-eel Deep Shelf Scorpaenidae: Bocaccio, bank, canary, chilipepper, cowcod, darkblotched, halfbanded, greenblotched, greenspotted, pygmy, redbanded, rosethorn, sharpchin, swordspine, splitnose, vermilion, widow, yelloweye, yellowtail Hexagrammidae: Lingcod Slope Scorpaenidae: Aurora, bank, blackgill, bocaccio, chilipepper, cowcod, darkblotched, greenblotched, greenspotted, Pacific Ocean perch (Sebastes alutus), rosethorn, sharpchin, splitnose (S. diploproa)

Hexagrammidae: Lingcod NOTE : Midshelf-30–100 m, deep shelf-101–200 m, and upper slope-201–500 m. From Miller and Geibel (1973); Gotshall et al. (1974); Gabriel and Tyler (1980); Gunderson and Sample (1980); Allen and Smith (1988); Dark and Wilkins (1994); Mason (1995); Love et al. (2002); Williams and Ralston (2002); Yoklavich et al. (2000, 2002).

either are too small to take a hook or are small enough to pass through a net. Release from competition and from predation by the larger, overfished species likely has resulted in the dominance of these weed-like species on deep rock habitats. Many fish species associated with deep-water habitats are distributed on a macroscale (up to tens of meters) in response to specific types of seafloor sediments and water depth (Pearcy et al., 1989; Stein et al., 1992). From an example of benthic fish and habitat surveys conducted off the Big Sur coast, four distinct fish assemblages or guilds were separated primarily by depth (ranging from 30 to 250 m) and secondarily by a combination of sediment type and slope of the seafloor (fig. 10-4; Yoklavich et al., 2002). The two midshelf groups were associated primarily either with sand waves, ripples, and shell hash (dominated by speckled, Citharichthys stigmaeus, and Pacific sanddabs, C. sordidus) or with high-relief boulders and rock outcrops sometimes overlaid with kelp and understory algae (members of this group included blue, gopher (Sebastes carnatus), olive, rosy, and vermilion rockfishes, painted greenling

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(Oxylebius pictus), lingcod, and sharpnose seaperch (Phanerodon atripes). Fish assemblages associated with various types of rock habitats on the midshelf are dominated by similar species off southern and central California (table 10-1; fig. 10-5; Yoklavich et al., 2002; Love et al., 2003). Juvenile greenstriped and stripetail (Sebastes saxicola) rockfishes, young-of-the-year cowcod, longspine (Zaniolepis latipinnis) and shortspine (Z. frenata) combfishes, pink seaperch (Zalembius rosaceus), and blackeye gobies position themselves on the sand and mud surrounding rock outcrops. Blackeye gobies also commonly rest on boulders and rocks of all sizes. Schools of young halfbanded and pygmy rockfishes swarm over cobblestones and low-lying broken rock; the halfbandeds often are distributed as much as 10 m into the water column, whereas the pygmies are much closer to the bottom. Young-of-the-year widow, squarespot, and other rockfish species also school with each other over rocks, usually in areas devoid of larger fishes. Larger juvenile and subadult greenspotted and swordspine rockfishes

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F I G U R E 10-4 Fish assemblages characterized primarily by depth and secondarily by sediment and slope of the seafloor off Big Creek Marine Ecological Reserve, central California (from Yoklavich et al., 2002).

and cowcod hide in cracks and between stones or hover just over the seafloor. As the relief in habitat increases and becomes more complex, adult flag, greenspotted, pygmy, rosy, starry, and swordspine rockfishes, kelp (Hexagrammos decagrammus) and painted greenlings, senorita (Oxyjulis californica), and sheephead (Semicossyphus pulcher) and blacksmith (both southern California) are relatively abundant on or very near the seafloor, often alone but occasionally in small groups. At the same time, schools of late juvenile or young adult bocaccio, blue, speckled, squarespot, pygmy, vermilion, and whitespeckled (southern California only) rockfishes and sharpnose seaperch swim from near the seafloor to several meters above it. These species can occur together or in segregated aggregations. A few large cowcod (southern California), vermilion, and yelloweye rockfishes reside deep within caves and crevices in this depth category. Juvenile and adult lingcod are found from the edge of the rock outcrop to its crest. With a few exceptions, little has been published on the habitat associations of fishes on deep-shelf (101–200 m) and upper slope (201–500 m) rock habitats. The two deep water (100–250 m) groups that were delineated from fish and habitat surveys off the Big Creek Marine Ecological Reserve (central California; Yoklavich et al., 2002) were associated either with smooth, fine sediment (members included rex [Glyptocephalus zachirus], slender [Lyopsetta exilis], and Dover [Microstomus pacificus] soles, Pacific hake [Merluccius productus], poachers [Family Agonidae], and sculpins [Family Cottidae]) or with steeply sloping bedrock

and some cobbles (primarily bank [Sebastes rufus], greenspotted, darkblotched, rosethorn, squarespot, and yelloweye rockfishes; fig. 10-4). Five of the six guilds of benthic fishes that were described based on their associations with sediment types in deep water (75–305 m) of Soquel submarine canyon in Monterey Bay, comprised various combinations of high relief rock outcrop and boulders, low-relief cobble and pebbles, and fine muds (fig. 10-6; Yoklavich et al., 2000). Assemblages in the two guilds that were defined by low-lying habitats of cobble, pebble, and mud were diverse and included either relatively small species (greenstriped, halfbanded, rosethorn, stripetail, and, to a lesser degree, pygmy rockfishes) or small individuals of a large species (greenspotted rockfish). Two other guilds were defined by high-relief structures of large boulders and rock outcrops interspersed with fine mud on the canyon’s steep walls. Some of the largest species (e.g., cowcod and yelloweye rockfishes up to 1 meter long, greenblotched and redbanded rockfishes, and bocaccio) were closely associated with rock ledges, caves, and overhangs in the canyon’s rock walls. One isolated rock outcrop surrounded by a field of soft mud served as a natural refuge to the highest densities and largest members of these species that have been documented off California. The fifth guild, defined by rock and boulder habitat of moderate relief at 75–175 m depth, was dominated by pygmy rockfish; this type of habitat is typical for this species elsewhere off Southern (Love et al. et al., 2003) and central California (Yoklavich et al., 2002; Yoklavich, unpublished data) (fig. 10-7).

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F I G U R E 10-5 Representative fishes on midshelf rock habitats off southern and central California.

Anthropogenic Structures: Oil and Gas Platforms, Shell Mounds, and Pipelines There are two types of artificial structures in the ocean off California. The first of these, artificial reefs, was created under the direction of the California Department of Fish and Game to enhance recreational fishing by providing marine habitat (Wilson et al., 1990). Because almost all of these artificial reefs are in water less than 30 m deep, these structures are not discussed in this chapter. A second group of artificial structures include offshore oil and gas platforms and various pipelines. These were created for other obvious purposes but also provide habitat for fishes. Almost all of the research on these structures has been directed toward offshore platforms (Carlisle et al., 1964; Allen and Moore, 1976; Bascom et al., 1976; Simpson, 1977; Love and Westphal, 1990; Love et al., 1999, 2000, 2003; Love, 2001). There are 23 platforms off California in greater than 40 m water depth. Of these, 19 are located in the Santa Barbara Channel and Santa Maria Basin (fig. 10-1). Almost no research has been conducted on the three platforms to the south of the Santa Barbara Channel. Seven platforms, located 3 to 12 miles from shore and based in 65 to 224 m water depth, have been most extensively surveyed (fig. 10-1). In general, there are three distinct fish assemblages around these deep-water platforms: (1) those in the midwater around the platform (defined as between the surface and

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about 10 m above the seafloor); (2) those on the bottom, adjacent to and within the platforms; and (3) those on the shell mound surrounding the platform. Rockfishes, including about 36 species, dominate all of these assemblages in both density and biomass (Love et al., 1999, 2000, 2003; Love, 2001).

Midwater Assemblage Young-of-the-year (YOY) and 1-year-old rockfishes dominated surveys conducted during a 6-year period from July to November in midwater, particularly at platforms north of Point Conception. YOY rockfishes are virtually the only fishes seen around many platforms. Most of these are midwater or epibenthic species, primarily blue, olive, pygmy, squarespot, widow, and yellowtail rockfishes and bocaccio. These species form large schools that rarely leave the cover of the platform. Young-of-the-year copper and flag rockfishes and painted and kelp greenlings also may be common, but they are closely associated with the crossbeams and vertical framework of the platforms. Typical shallow-water outcrop species, such as blacksmith, kelp bass (Paralabrax clathratus), pile perch (Rhachochilus vacca) and sheephead, are found in the midwater around platforms close to shore. The midwater around platforms also hosts a number of transient pelagic visitors, such as northern anchovy (Engraulis mordax), Pacific sardine

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F I G U R E 10-6 Cluster analysis of nonschooling benthic fish species in Soquel Canyon, Monterey Bay, based on associated type of seafloor sediments (from Yoklavich et al., 2000).

(Sardinops sagax), Pacific chub mackerel (Scomber japonicus), and mola (Mola mola). On offshore platforms, only a few species, such as blue and widow rockfishes, remain in the midwater after their first year. After about 1 year, many species, such as copper, flag, and yellowtail rockfishes, bocaccio, and kelp and painted greenlings, either move down to the platform bottom or off the platform all together. Because oceanographic conditions strongly affect fish recruitment success, the density of YOY rockfishes may vary interannually by a factor of 10 or more (fig. 10-8a). Similarly, densities may vary by that much between adjacent platforms within a year. During the mid-to-late 1990s, platforms north of Point Conception (Irene, Hidalgo, Harvest, and Hermosa) had higher densities of YOYs than those in the Santa Barbara Channel (figure 10-8a). This is most clearly seen between 1995 and 1998, when there was little fish recruitment at Santa Barbara Channel platforms. However, the fortuitously timed upwelling of 1999 brought with it an exceptionally good year for rockfish recruitment, reflected at all of the platforms, including those within the Santa Barbara Channel. Rockfishes even recruited to Platform Gail, which had not supported YOY rockfish during the previous 4 years. Bocaccio most clearly exemplifies extremes in annual and geographic variability in rockfish recruitment (fig. 10-8b). Between 1995 and 1998, YOY bocaccio were uncommon or absent from the platforms. In 1999, high densities of bocaccio were observed at Platforms Irene and Grace, and at least a few individuals occurred at other platforms. Platform Grace, in particular, provides a striking example of interannual variability; almost no YOY bocaccio were observed prior to 1999. On average, the midwater platform habitat harbors higher densities of juvenile rockfishes than nearby natural rock piles. Between 1996 and 1999, fishes were surveyed at Platform Hidalgo and at five nearby rock piles in about the same water depth (112–140 m). In all 4 years, there were higher densities of YOY rockfishes around the platform midwater than on the rocks (fig. 10-9). The occurrence of con-

sistently high densities of YOY rockfish at Platform Hidalgo depends partially on the depth of these habitats. Four rock piles (North, B, C, and D) are in water shallower than 120 m, whereas the platform and A Reef are located in somewhat deeper water. However, because Platform Hidalgo covers the entire water column, it is much more likely to be encountered and colonized by shallow-dwelling pelagic juvenile rockfishes than the relatively low-lying rocks that have a vertical dimension of only a few meters.

Bottom Assemblage Bottom habitat is the area where the seafloor meets the platform framework. At every platform, there is a crossbeam that rests either on or close to the seafloor. However, some or all of the crossbeams may be buried by sediment. Subadult and adult rockfishes and lingcod dominate bottom assemblages that are either very close to or within the crossbeams, pilings, and wellheads of the platforms. An exception is the mobile, schooling halfbanded rockfish, which is found near the bottom and some distance outside the platform structure, perhaps avoiding large predators. Common hiding or resting spaces for many individuals are the crevices formed by near-bottom currents that erode sediments from beneath the crossbeams. The bottom depth of the platforms strongly influences the species composition of associated fish assemblages (Love, 2001). Relatively shallow-water platforms (i.e., 50–130 m depth) are often habitat to halfbanded, copper, vermilion, flag, brown, and calico (Sebastes dalli) rockfishes and adult and juvenile lingcod. Painted and kelp greenlings and some seaperches also are common. Only rarely are YOY rockfishes abundant on the bottoms of these structures. Pinkrose, greenspotted, greenblotched, greenstriped, and stripetail rockfishes, bocaccio, cowcod, and combfishes commonly occur on platform bottom habitats in deep water.

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F I G U R E 10-7 Representative fishes on deep-shelf and upper slope rock habitats off central and southern California

F I G U R E 10-8 (a) Densities of young-of-the-year rockfishes by year and platform and (b) densities of young-of-the-year bocaccio by year

and platform.

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TA B L E 10-2

Densities of All Species Found in Bottom and Midwater Habitats Around Platform Hidalgo and on North Reef

Family

Common Name

Scorpaenidae

Bocaccio Canary rockfish Cowcod Flag rockfish Greenblotched rockfish Greenspotted rockfish Greenstriped rockfish Halfbanded rockfish Pygmy rockfish Rockfish YOY Rosy rockfish Sebastomus sp. Sharpchin rockfish Squarespot rockfish Starry rockfish Swordspine rockfish Vermilion rockfish Widow rockfish Yelloweye rockfish Yellowtail rockfish Kelp greenling Lingcod Painted greenling Shortspine combfish Longspine combfish Unid. combfish Pink seaperch Blackeye goby Poachers

Hexagrammidae

Embiotocidae Gobiidae Agonidae

Platform Midwater

206.2

North Reef

1.8 3.3

0.7

10.7 0.4 37.2 6.6 284.7 1.1 2.2 1.5 1.8

308.6

2.6 2.2 1.1 1.1

0.4 32.2 12.3 52.8 0.4 14.3 0.4 10.6

Platform Midwater

0.5

2622.6

0.7 0.4 0.4 0.4

1999 Platform Bottom

North Reef

3.9 0.4 15 2.8 41.5 1.9 574.7 0.4 81.3 1.2 1.2

1.6 7.2 1.7 0.5 2.6 10.9 0.8 10.6 52.9 333.4 5.8 13.7

4.7 0.8 0.4 13.8 0.8

0.4

0.6 1 3.9 276.7 0.6 3.8

3.8 9.3

Unidentified fishes NOTE :

1998 Platform Bottom

3.3 4.4

1.1

4.3 19.4

2.8 1.2

7.4 0.4 2.1 5.3 5.4

7.5

0.6 0.3 4.6

2.3 2.8 0.3

1.6

Density
fish/100 m2. From Love 2001

Because the species assemblages around the platform bottom include primarily subadult and adult fishes, their densities are less reflective of annual recruitment processes and perhaps more stable than densities of midwater assemblages. The extent to which individual fish move on and off the platform is unknown. However, it is likely that relatively sedentary species, such as greenspotted and greenblotched rockfishes, rarely leave the platform environment. More mobile species, such as halfbanded rockfish and young widow rockfish and bocaccio, may move extensively. Some platforms serve as de facto reserves because there is little fishing pressure in their vicinity. For instance, there are higher densities of adult bocaccio and cowcod (both species declared “overfished” by the National Marine Fisheries Service) at Platform Gail, located in the eastern end of the Santa Barbara Channel, than at any of the 50 natural rock habitats surveyed throughout southern California (Love, 2001; Love, unpubl. data). Love (2001) compared the species compositions of fish assemblages surveyed in midwater and bottom habitats at Platform Hidalgo and at the nearby North Reef in 1998 and 1999 (see fig. 10-1 for locations). Although there was almost complete overlap in species composition, the densities of the dominant species varied between the two sites (table 10-2). Higher densities of

young-of-the-year rockfishes (YOY) and adult halfbanded and flag rockfishes, painted greenling, and lingcod occurred at Platform Hidalgo, whereas pygmy, rosy, and yellowtail rockfishes and cowcod were more abundant at North Reef. As previously noted, the higher densities of YOY rockfish in Platform Hidalgo’s midwater habitat compared to those associated with North Reef are likely to reflect the greater vertical relief of the platform. The high densities of flag rockfish at Platform Hidalgo also may be linked to increased facilitation of juvenile recruitment at the platform. On natural outcrops, flag rockfish usually are found as solitary animals. However, 10 or more individuals were found crowded together under the bottom crossbeam at Platform Hidalgo. Pelagic juvenile flag rockfishes are abundant in surface waters (Love et al., 2002) and therefore are more likely to encounter platforms than natural outcrops. During years of good recruitment, large numbers of YOY flag rockfish occupy the midwater habitat of some platforms. From surveys of fishes at Platform Grace between 1999 and 2002, flag rockfish that had recruited to the midwater in 1999 remained at the platform through the succeeding 3 years. By 2002, large numbers of flag rockfish, with densities similar to those at Platform Hidalgo, were observed in the bottom habitat of Platform Grace (Love et al., 2003).

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F I G U R E 10-9 Mean annual densities of young-of-theyear rockfishes at Platform Hidalgo and at five natural rock outcrops, 1996–1999.

Shell Mound Assemblage The seafloor surrounding platforms is covered by living and dead mussel shells that have fallen from the platforms during storms or cleaning operations. These shell mounds harbor a rich invertebrate fauna, including large numbers of anemones, seastars, brittlestars, crabs, and shrimps. They also are home to YOY rockfishes (primarily benthic species such as cowcod, copper, brown, stripetail, blackgill [Sebastes melanostomus], greenspotted), other small rockfishes (e.g., halfbanded, pinkrose, greenblotched, rosy), juvenile and occasionally adult lingcod, both longspine and shortspine combfishes, Pacific sanddab, and poachers. The rugose substratum formed by mussels and other invertebrates provides refuge from predation for these small fishes. In general, the fish assemblage on shell mounds is an extension of the bottom assemblage adjacent to the platform (Love et al., 2003).

Pipeline Assemblage Most of the pipelines in deep water off California release treated sewage or are associated with oil and gas platforms. These pipes range from 0.3–3.7 m in diameter. Only two studies have examined the fish assemblages on these structures: a sewer line in Santa Monica Bay (Allen et al., 1976) and a gas line located between Platforms Gail and Grace in the Santa Barbara Channel (M. Love, unpubl. obs). In both surveys, pipelines harbored relatively high numbers of fishes of those species (particularly rockfishes, as well as painted greenling, sculpins, and poachers) common to rock habitats, along with high densities of large invertebrates such as anemones and sea stars. The relatively shallow (60–100 m) Santa Monica Bay pipe was home to high densities of blue, olive, flag, shortbelly, and vermilion rockfishes, as well as young bocaccio and cowcod. Some of these species were noted on a section of the oil and gas pipeline at about 100 m water depth. The deep sections (to 220 m) of this pipeline were occupied by juvenile cowcod, stripetail, pinkrose, splitnose, and blackgill rockfishes and poachers. Fishes were particularly abundant where there was dense invertebrate cover on the pipe.

A Final Comment It is important to reiterate that the fish communities we have discussed are not “natural.” As noted in Jackson (2001) and

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Jackson et al. (2001), coastal ecosystems worldwide have been dramatically altered by human activity. It is clear that the fish assemblages on deep rock habitats off California have been substantially changed. This alteration has occurred both from intense, continuous recreational and commercial fishing at least as far back as the 1940s and, beginning in the mid1970s, from more than two decades of a warm and planktondepleted oceanographic regime, which was at least partially responsible for the poor reproductive success of many fish species. This has led to fish assemblages dominated by dwarf species that perhaps are more productive and able to avoid capture. We have almost no data on prefishery fish assemblages on deep rock habitat, and we can only speculate on the structure of unfished communities and on the significance and magnitude of subsequent impacts. However, based on observations by Yoklavich et al. (2000) of an unfished outcrop on a canyon wall in Monterey Bay, it is likely that the optimal high-relief habitat was occupied by high densities of the adults of larger species, such as greenspotted, greenblotched, and yelloweye rockfishes, boccacio, cowcod, and lingcod. In the past, the young of these species and the dwarf species that now dominate these outcrops were probably relegated to suboptimal habitats, such as cobble. On the Pacific Coast, mapping and subsequent characterization of deep rock habitats and their faunal assemblages are only just beginning and are critical when trying to understand and protect essential fish habitats. In addition, those surveys of deep rock habitats that evaluate the role of oil platforms as fish habitat or of submarine canyons as marine refuges have been narrowly focused. With additional seafloor mapping and broadly based community studies, it will be possible to fill in the gaps in our knowledge. However, it is unfortunate that we will not be able to reconstruct these vanished ecosystems completely.

Acknowledgments We appreciate the assistance of G. Cailliet, J. Field, R. Lea, J. DeMarignac, G. Moreno, M. Nishimoto, R. Starr, D. Schroeder, and L. Snook in conducting underwater surveys of fishes and habitats; Delta Oceanographics personnel and the

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crews of the many support vessels; J. Harvey and C. Syms for statistical consultation; L. Allen, M. Amend, and R. Bloom for their graphic expertise. This research was partially supported by NOAA National Undersea Research Program, West Coast and Polar Regions Undersea Research Center, University of Alaska Fairbanks (nos. UAF-92-0063, UAF-930036, and UAF-CA-02-09); David and Lucile Packard Foundation (no. 2001-18125); California Sea Grant (no. R/BC1) under sponsorship of the California Department of Fish and Game, Marine Resources Protection Act, Marine Ecological Reserves Research Program; NOAA Fisheries Office of Habitat Conservation and Office of Protected Resources; Biological Resources Division, U. S. Geological Survey (National Offshore Environmental Studies Program 1445-CA0995-0386); Minerals Management Service; and California Artificial Reef Enhancement Program.

Literature Cited Allen, M.J., H. Pecorelli, and J. Word. 1976. Marine organisms around outfall pipes in Santa Monica Bay. J. Water Pollut. Control Fed. 48:1881–1893. Allen, M. J., and M.D. Moore. 1976. Fauna of offshore structures. SCCWRP, Annual Report 1976. Allen, M. J., and G.B. Smith. 1988. Atlas and zoogeography of common fishes in the Bering Sea and northeastern Pacific. NOAA Tech. Rep. NMFS 66, Seattle. Bascom, W., A.J. Mearns, and M.D. Moore. 1976. A biological survey of oil platforms in the Santa Barbara Channel. J. Pet. Technol. 28: 1280–1284. Burge, R.T., and S.A. Schultz. 1973. The marine environment in the vicinity of Diablo Cove with special reference to abalones and bony fishes. California Fish Game, Marine Research Technical Report No. 19. Carlisle, J.G., Jr., C.H. Turner, and E.E. Ebert. 1964. Artificial habitat in the marine environment. California Fish Game, Fish Bulletin 124. Dark, T.A., and M.E. Wilkins. 1994. Distribution, abundance, and biological characteristics of groundfish off the coast of Washington, Oregon, and California, 1977–1986. NOAA Technical Report NMFS 117, Seattle. Eigenmann, C.H., and R.S. Eigenmann. 1889. Notes from the San Diego Biological Laboratory. West Am. Sci. 6:123–132. Gabriel, W.L., and A.V. Tyler. 1980. Preliminary analysis of Pacific Coast demersal fish assemblages. Mar. Fish. Rev. 43(3–4):83–88. Gotshall, D.W., R.N. Lea, L.L. Laurent, T.L. Hoban, and G.D. Farrens. 1974. Mendocino power plant site, ecological study, final report. California Fish and Game, Marine Research Division Administrative Report. No. 74-7. Greene, H.G., M.M. Yoklavich, R.M. Starr, V.M. O’Connell, W.W. Wakefield, D.E. Sullivan, J.E. McRea Jr., and G.M. Cailliet. 1999. A classification scheme for deep seafloor habitats. Oceanologica Acta 22:663–677. Gunderson, D.R., and T.M. Sample. 1980. Distribution and abundance of rockfish off Washington, Oregon, and California during 1977. Mar. Fish. Rev. 42(3-4):2–16. Hubbs, C.L. 1974. Review and comments. Marine Zoography. Copeia 1974(4):1002–1005. Jackson, J.B.C. 2001. What was natural in the coastal oceans? Proc. Nat. Acad. Sci. USA 98:5411–5418. Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Bjorndal, L.W. Botsford, B.J. Bourque, R.H. Bradbury, et al. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637. Jordan, D.S. 1884. The rock cods of the Pacific. In G.B. Goode (ed.), The fisheries and fishery industries of the United States. United States Commission of Fish and Fisheries, Section 1, pp. 262–267. Karpov, K. A., D. P. Albin, and W. H. VanBuskirk. 1995. The marine recreational finfishery in northern and central California: a historical comparison (1958–1986), status of stocks (1980–1986), and effects of changes in the California Current. Calif. Fish Game Bull. 176:1–192.

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Stephens, J.S. Jr., P.A. Morris, K. Zerba, and M. Love. 1984. Factors affecting fish diversity on a temperate reef: the fish assemblage of Palos Verdes Point, 1974–1981. Environ. Biol. Fishes 11:259–275. Williams, E.H., and S. Ralston. 2002. Distribution and co-occurrence of rockfishes (family: Sebastidae) over trawlable shelf and slope habitats of California and southern Oregon. U. S. Fish. Bull. 100:836–855. Wilson, K.C., R.D. Lewis, and H.A. Togstad. 1990. Artificial reef plan for sport fish enhancement. California Fish Game, Administrative Report No. 90-15. Yoklavich, M., R. Starr, J. Steger, H.G. Greene, F. Schwing, and C. Malzone. 1997. Mapping benthic habitats and ocean currents in

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the vicinity of central California’s Big Creek Ecological Reserve. U.S. Dept. Commerce NOAA Technical Memorandum NMFSSWFC-245. Yoklavich, M.M., G.H. Greene, G. Cailliet, D. Sullivan, R.N. Lea, and M. S. Love. 2000. Habitat associations of deepwater rockfishes in a submarine canyon: An example of a natural refuge. U.S. Fish. Bull. 98:625–641. Yoklavich, M.M., G. Cailliet, R.N. Lea, H.G. Greene, R. Starr, J. deMarignac, and J. Field. 2002. Deepwater habitat and fish resources associated with the Big Creek Marine Ecological Reserve. 2002. CalCOFI Reports 43:120–140.

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PELAGIC HABITATS

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CHAPTER 11

Ichthyoplankton H. G. M O S E R AN D W. WATS O N

Historic Overview The term ichthyoplankton is applied to fish eggs and larvae that are found among the other planktonic organisms drifting with the currents in the upper part of the water column. Fish eggs are immotile, whereas larvae swim feebly after hatching and become more motile as they develop toward the juvenile stage. Ichthyoplankters are further classified as meroplankton (temporary plankton), the early, planktonic ontogenetic stages of aquatic organisms that develop into juveniles and adults and ultimately occupy a variety of pelagic and demersal habitats. Plankton research began in the nineteenth century when British and German scientists, experimenting with fine-mesh nets of various designs, began to describe the vast array of small organisms captured in the sea. In 1865, the Norwegian scientist, G.O. Sars discovered that the eggs of cod and other species in Norwegian seas are pelagic; this marked the beginning of ichthyoplankton research, which accelerated at the turn of the twentieth century with the realization that quantitative ichthyoplankton sampling could be a means of estimating the size and extent of commercial fish stocks (Hempel, 1979; Ahlstrom and Moser, 1981; Kendall, 2000). As in the North Atlantic, fisheries concerns generated the first ichthyoplankton studies off California. The Pacific sardine (Sardinops sagax) fishery expanded rapidly in the 1920s and by the mid-1930s had become one of the largest world fisheries, with annual landings exceeding 700 thousand tons. During the rapid expansion of the fishery, California Department of Fish and Game (CDFG) biologists realized that catch and life-history information essential to rational management of the fishery were lacking (Clark, 1982). A system for monitoring landings was established and research on sardine early life history began with a series of plankton-oceanographic surveys during 1920 to 1932. These surveys, conducted by scientists from CDFG and the Hydrobiological Survey of the Hopkins Marine Station, provided the first information on sardine eggs and larvae in an area extending from northern California to Cabo San Lucas, Mexico, and marked the beginning of ichthyoplankton research in the California Current region (Scofield and Lindner, 1930; Scofield, 1934).

By the 1930s, the sardine population had expanded northward to British Columbia, its management had become international in scope, and scientists of the U.S. Fish and Wildlife Service Bureau of Commercial Fisheries (BCF) joined the group of fishery biologists and managers dealing with the sardine fishery. This consortium included two scientists who were especially important to the development of ichthyoplankton research in the California Current region: Oscar E. Sette and Elbert H. Ahlstrom. Sette (1943) was the principal designer of a cooperative research plan for sardine that emphasized the importance of ichthyoplankton surveys in attacking the problems of recruitment, trophic dynamics, and biomass estimation. Sette, along with Ahlstrom, oceanographers from Scripps Institution of Oceanography (SIO), and scientists from CDFG, developed a plan to monitor the early life stages of sardine, associated planktonic organisms, and the ocean environment. A series of 24 cruises was conducted during 1937 to 1941 to establish the boundaries, station placement, and sampling frequency needed to meet key requirements of Sette’s research plan, principally to collect sardine eggs and larvae over the entire areal and seasonal spawning range of the species. In 1949, under the sponsorship of the Marine Research Committee of the State of California, the consortium of BCF, SIO, and CDFG scientists that would eventually be known as the California Cooperative Oceanic Fisheries Investigations (CalCOFI) began the annual biological-oceanographic surveys. At this time, the sardine population had declined to a small fraction of its former size during the mid-1920s (Ahlstrom, 1966; Hewitt, 1988; Kawasaki, 1991; Moser et al., 1993, 1994a, 2001a; Smith and Moser, 2003). During the past half-century, these surveys have produced a wealth of data on the biology, chemistry, and physics of the California Current, in addition to the information on sardine early life history originally sought by the CalCOFI founders. Ahlstrom was in charge of CalCOFI ichthyoplankton investigations from the beginning of the program and, although the focus was on sardine, he attempted to identify all fish larvae captured in each CalCOFI tow. His “faunal” approach formed the basis for advances in our knowledge of ichthyoplankton ecology in the CalCOFI survey area (Ahlstrom, 1959, 1960, 1965, 1966, 1969, 1972; Orton 1953a,b, 1955a,b, 1962, 1963; Orton and Limbaugh, 1953; Kramer, 1970; Moser et al., 1974, 1984, 1987,

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1993, 1994a, 2001a, 2002; Ahlstrom and Moser, 1975; Ahlstrom and Stevens, 1976; Ahlstrom et al., 1976, 1978; Sumida and Moser, 1980, 1984; Gruber et al., 1982; Loeb et al., 1983a,b,c; MacCall and Prager, 1988; Smith and Moser, 1988, 2003; Moser and Watson, 1990; Moser and Boehlert, 1991; Moser and Smith, 1993; Moser, 1996; Moser and Pommeranz, 1999). The southern region of the California Current off Mexico was an integral part of the CalCOFI surveys until 1985 when coverage was limited to the Southern California Bight region (SCB: a region between the major upwelling centers off central California and the central Baja California peninsula, approximately Point Conception, California, to Point Baja, Baja California, Mexico; Bakun, 1996). Centro Interdisciplinario de Ciencias Marinas (CICIMAR), Instituto Politecnico Nacional’s marine laboratory in La Paz, Baja California Sur, continued limited ichthyoplankton surveys in the Magdalena Bay region during the 1980s and early 1990s (Funes-Rodriguez et al., 2001), and in 1997, a collaboration of CICIMAR and Centro de Investigacion Cientifica de Educacion Superior de Ensenada (CICESE) reinstituted biological-oceanographic surveys off Baja California, following CalCOFI station placement and standard protocols (Baumgartner et al., 2000). The CalCOFI survey design has an offshore emphasis because, at the inception of the program, sardines spawned over a broad expanse of the California Current region (fig. 11-1); however, with the decline of the population, spawning contracted to a narrow coastal band by the 1960s. Since the mid 1980s, sardine spawning has expanded rapidly to reoccupy a large portion of the California Current region, as far north as British Columbia (McFarlane et al., 2000). During this period, human impact on coastal fish communities stimulated numerous nearshore ichthyoplankton programs along the California coast. A primary concern has been the use of seawater to cool reactors at nuclear power plants and the effect this may have on nearshore fish populations and other marine life. This resulted in a number of monitoring programs that have greatly advanced our knowledge of the taxonomy, distribution, and abundance of nearshore ichthyoplankton in the SCB region (Brewer et al., 1981, 1984; Brewer and Smith, 1982; Schlotterbeck and Connally, 1982; Watson, 1982, 1992; Allen et al., 1983; Barnett et al., 1984; Brewer and Kleppel, 1986; Jahn and Lavenberg, 1986; Lavenberg et al., 1986; Walker et al., 1987; Jahn et al., 1988; Watson and Davis, 1989; McGowen, 1993). Ichthyoplankton studies at San Onofre Nuclear Generating Station ended in 1986; however, ichthyoplankton sampling and analysis at the Diablo Canyon nuclear power plant in central California continued through 1999 (Ehrler et al., 2002). Other ichthyoplankton studies off central and northern California have focused largely on the declining populations of nearshore fishes, especially the rockfishes (Eldridge and Bryan, 1972; Misitano, 1976; Eldridge, 1977; Icanberry et al., 1978; Laidig et al., 1991; Laidig and Sakuma, 1998; Lenarz et al., 1991; Ralston and Howard, 1995; Sakuma and Laidig, 1995; Sakuma and Ralston, 1995; Laidig et al., 1996; Ralston et al., 1996; Yoklavich et al., 1992, 1996; Sakuma et al., 1999; Ralston et al., 2003). In recent years, the growing popularity of the livefish restaurant trade has generated an intense nearshore fishery that targets shallow water rockfishes (Sebastes), e.g., copper (S. caurinus), grass (S. rastrelliger), gopher (S. carnatus), brown (S. auriculatus), and kelp (S. atrovirens) rockfishes, and other associated reef fishes such as cabezon (Scorpaenichthys marmoratus), greenlings (family Hexagrammidae), lingcod (Ophiodon elongatus), and California sheephead (Semicossyphus pulcher) (Pattison and Vejar, 2000; Moser et al., 2001b; Walters, 2001).

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Ichthyoplankton surveys in Pacific northwest waters were conducted by CalCOFI and its precursors in 1939, 1949, 1950, 1955, 1972, and 1989 (Hewitt, 1988; Moser et al., 1994a). LaBrasseur (1970) published a checklist of fish larvae collected in
3000 zooplankton samples from the northeast Pacific from 1956 to 1959. Although most of these samples were taken in the Gulf of Alaska, a substantial number also were taken in the California Current region as far south as northern California. In the 1970s, ichthyoplankton studies were initiated at Oregon State University (OSU) and at the Alaska Fisheries Science Center. At OSU, the collaboration of William G. Pearcy and Sally L. Richardson and their students generated an ichthyoplankton program that ranged from Yaquina Bay to offshore waters of the Oregon and Washington coasts and included studies on seasonal and interannual distribution and abundance, recruitment, and larval taxonomy and systematics (Richardson, 1973, 1977, 1980, 1981a,b; Pearcy and Meyers, 1974; Pearcy et al., 1977; Richardson and Pearcy, 1977; Richardson and Stephenson, 1978; Laroche and Richardson, 1979, 1980, 1981; Richardson and Laroche, 1979; Richardson and Washington, 1980; Richardson et al., 1980a,b; Stein, 1980; Brodeur et al., 1985; Shenker, 1988). After the departure of Dr. Richardson from OSU, ichthyoplankton research at the Hatfield Marine Science Center in Newport, Oregon, continued with George W. Boehlert and his students and research group and included physiological as well as field studies (Boehlert and Yoklavich, 1984, 1985; Boehlert et al., 1985; Boehlert and Mundy, 1987, 1988). Another center of ichthyoplankon research in the region is the Resource Assessment and Conservation Engineering Division (RACE) of the Alaska Fisheries Science Center, National Marine Fisheries Service, in Seattle, Washington. Although their field surveys and research are focused on the Gulf of Alaska and Bering Sea, they have made extensive contributions to our knowledge of the northern California Current region. An early survey sampled a station grid extending from Vancouver Island to northern California, from the coast to several hundred miles offshore (Waldron, 1972). Comprehensive ichthyoplankton investigations began under the direction of Arthur W. Kendall, Jr., who conducted a series of 10 biological/oceanographic surveys off the coasts of Washington, Oregon, and northern California from 1980 to 1987 (Doyle, 1992a). These collections provided information on the distribution and abundance of Pacific northwest fish eggs and larvae (Doyle, 1992a,b; Doyle et al., 1993) and formed the basis for an ichthyoplankton laboratory guide (Matarese et al., 1989) and numerous other contributions (e.g., Matarese et al., 1981; Kendall and Vinter, 1984; Kendall and Matarese, 1987, 1994; Kendall, 1993; Busby, 1998; Busby et al., 2000; Orr and Matarese, 2000).

Ichthyoplankton Sampling A primary reason for conducting ichthyoplankton surveys is to determine the distribution and abundance of the eggs and/or larvae of fishes in a region of the ocean, usually to detect interannual changes in the size and scope of one or more populations. Indexes of relative abundance derived from these surveys often are the only fishery-independent information available to scientists who have the task of estimating the biomass of a stock from catch-at-age fishery data. In addition to indexes of larval abundance, ichthyoplankton surveys can provide valuable information on spawning seasons and temperatures, larval dispersion and mortality, and a great many other aspects

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F I G U R E 11-1 The CalCOFI survey pattern extending from the California-Oregon border (line 40) to the south of Cabo San Lucas, Baja California Sur, Mexico (line 157). Numbers at the ends of the onshore-offshore lines indicate survey lines; station numbers are shown along line 40; present (since 1985) survey area outlined.

of fish life history and ecology. Ichthyoplankton surveys designed to estimate spawning biomass must encompass the geographic limits of target spawning stock(s). For species such as the Pacific sardine, this may involve thousands of square kilometers and require multiship surveys (Ahlstrom, 1966), whereas shorefish species may require a sampling area that extends only to the edge of the continental shelf or to the mouth of a bay in the case of some estuarine species. Another requirement for a quantitative survey is the need to encompass the vertical extent of the ichthyoplankton target species. Most ichthyoplankters live in the upper water column and are adequately sampled by a plankton tow to 212 m depth, the target depth for the standard CalCOFI oblique plankton tow (Ahlstrom, 1959; Moser and Smith, 1993; Moser and Pommeranz, 1999). For stations over the shelf, the target depth of the tow is determined by bottom depth, usually as close to the bottom as possible without endangering the sampling gear. Quantitative plankton sampling began with Hensen’s (1895) “egg net,” a conical net with a three-lead bridle that became the archetype for ichthyoplankton samplers until the development of the bongo net (McGowan and Brown, 1966). The bongo net has the advantage of being able to take two adjacent simultaneous samples during a single tow with a bridleless frame that presents fewer avoidance signals to organisms in front of the net. In the standard CalCOFI 1-m diameter ring net used from 1949 to 1977, a cylindrical section preceded the conical section to improve filtration efficiency

(Ahlstrom, 1954; Smith et al., 1968). Nylon mesh (0.505 mm) replaced the original silk mesh (0.55 mm) in 1969, and the 71-cm bongo net frame came into use in 1977 (Smith and Richardson, 1977; Moser et al., 1993; Ohman and Smith, 1995). The bongo net, with mouth diameters of either 60 or 71 cm, has gained international acceptance as the preferred sampler for ichthyoplankton surveys. Usually, double oblique tows are employed on ichthyoplankton surveys. During a CalCOFI tow, for example, 300 m of wire are paid out at a constant rate of 50 m/minute (35 m of depth/minute) to reach the target depth of 212 m; then, after fishing at depth for 30 seconds, the net is retrieved at a constant rate of 20 m/minute (14 m of depth/minute), with the wire held at a constant angle of 45° by adjusting the ship speed and course (see Kramer et al., 1972 and Smith and Richardson, 1977 for detailed descriptions of gear and methods). If the tow is quantitative, i.e., the vertical range of the target species has been encompassed and the net has filtered an equal amount of water in each stratum of the water column, the numbers of specimens of any species captured in the tow can be converted to the number of organisms under a unit surface area (subsequently denoted as number/unit area) by multiplying the number per unit volume of water filtered during the tow (measured by the flowmeter at the mouth of each net) by the depth of the tow. The abundance at each station in a grid can be expanded to the area represented by each station and then summed to obtain the abundance for the entire area encompassed by the grid.

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Oblique tows taken with the research vessel underway, usually at a speed of
1.5 knots, have a better chance of capturing fish larvae compared to vertical tows taken with the ship stopped on station; however, vertical tows employing a bongo or ring net are appropriate for sampling fish eggs which drift passively and lack the ability to avoid the approaching net. Surveys designed to measure the daily egg production of large spawning stocks use vertical tows with a small-mouth net (e.g., 0.25 m diameter) that is cast and retrieved rapidly (
70 m/minute retrieval speed), thus allowing high station density and improved sampling precision (Lasker, 1985). This net also has been used successfully in shallow coastal waters (Lavenberg et al., 1987), and vertical tows with bongo nets, primarily for sampling fish eggs, have proved useful in shallow waters as well (Watson et al., 1999). Although oblique net tows are designed to sample the entire vertical distribution of target taxa, they are relatively poor samplers for species whose eggs and larvae are concentrated exclusively in the near-surface zone, which, during a typical oblique tow, is sampled for only a few seconds (Zaitsev, 1970; Hempel and Weikert, 1972; Doyle, 1992b; Moser et al., 2002). Some of these are valuable fisheries species and/or are important ecologically. Specialized “neuston” samplers such as the Manta net (Brown and Cheng, 1981) and the Sameoto neuston net (Sameoto and Jaroszynski, 1969) that can take a quantitative sample from the surface stratum have become part of the standard protocol for ichthyoplankton surveys where target species have obligate neustonic larvae (Doyle, 1992b; Moser et al., 2002). Another important feature of neuston nets is their tendency to capture specimens at the upper ends of larval size distributions; such specimens are relatively rare in catches from oblique nets (Ahlstrom and Stevens, 1976; Doyle, 1992a,b; Moser et al., 2002). Ichthyoplankton studies in shelf and bay waters have shown that larvae of some species descend from the water column to the epibenthos as early as the yolk-sac stage (e.g., some sciaenids) and are inadequately sampled with standard oblique tows (Schlotterbeck and Connally, 1982; Barnett et al., 1984; Jahn and Lavenberg, 1986). Epibenthic sled plankton samplers have been used effectively for these larvae (Eldridge and Bryan, 1972; Walker et al., 1987), and the Auriga net, a specialized, wheelmounted epibenthic sampler, also has been used successfully in coastal waters (Schlotterbeck and Connally, 1982; Barnett et al., 1984). Another coastal zone sampler, a bongo net mounted between wheels and used to make oblique tows that include the epibenthos, has been used as well (Lavenberg et al., 1986). The need for information on the vertical distribution of ichthyoplankton and micronekton has stimulated the invention of numerous devices for sampling discrete depth strata, beginning with simple messenger-actuated devices that constrict and close the net immediately behind the mouth (Nansen, 1915; Leavitt, 1935; Motoda, 1962) and pressureactuated devices at the cod end of the net that divert the sample from one collecting bucket to another (Foxton, 1963). Multiple-net samplers include the Tucker net, and modified versions of it, which consists of one or more nets attached to bars, forming a rectangular mouth, that can be opened and closed mechanically or acoustically (Tucker, 1951; Davies and Barham, 1969; Baker et al., 1973; Hodell et al., 2000). Another sampler, the MOCNESS (Multiple Opening-Closing Nets/ Environmental Sampling System), consists of a rectangular frame with sequentially opening/closing nets attached to horizontal bars that are released electronically via signals from a shipboard computer (Weibe et al., 1985). The MOCNESS can be

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configured as paired 0.5-m2 nets, or in 1-m2, 10-m2, or 20-m2 versions. A conductivity-temperature-depth sensor attached to the frame relays environmental data to the deck unit throughout each tow, and other sensors (e.g., pH, O2) can be added. Sampler avoidance can be reduced by increasing towing speed; however, water pressure increases rapidly with towing speed which can result in increased extrusion of eggs and larvae through the mesh, specimen damage, and damage to the net itself. Many approaches have been used to overcome this problem, usually by reducing the mouth diameter of the net and encasing the net in a streamlined housing (Aron et al., 1965; Fraser, 1968). One series of high-speed nets, the “Gulf” samplers, has appeared in numerous versions (Gehringer, 1952; Bridger, 1958; Nellen and Hempel, 1969), including a model capable of taking discrete depth samples (Moser and Pommeranz, 1999). Shipboard pumps have been used extensively to sample zooplankton (Lasker, 1975; Mullin and Brooks, 1970; Jahn and Lavenberg, 1986); however, their utility in capturing ichthyoplankton is limited to eggs and weakly swimming newly hatched larvae, although in some applications pumps may be superior to plankton nets (Leitheiser et al., 1979). Until recently, most shipboard pumps have been used with the research vessel drifting or at anchor (Mullin et al., 1985), but the invention of a system (CUFES: Continuous Underway Fish Egg Sampler) that can be operated while the research vessel is underway has provided new opportunities for measuring egg production over a large area (Checkley et al., 1997, 2000; Van der Lingen et al., 1998; Lo et al., 2001). Anchored and buoyed net arrays (Graham and Venno, 1968; Graham and Davis, 1971; Graham, 1972) and other fixed nets (Eldridge, 1977; Boehlert and Mundy, 1987; Witting et al., 1999) have been used effectively in estuaries to sample ichthyoplankton during tidal flows. Another collecting technique is to dip-net fish larvae that are attracted to lights either aboard ship or from piers (Busby et al., 2000). Although highly selective, dip-netting is a relatively inexpensive means of developing a time series of larval fish that may not be attainable by other means. In shallow estuarine and bay waters, dropbox enclosures have been used, and small-mesh beach seines have been used to collect late larval and juvenile stages of fishes (Allen et al., 1983; Kramer, 1991). Diver-operated samplers consisting of a small plankton net attached to a diver propulsion vehicle (Ennis, 1972) or a small diver-steered, towed plankton net (Marliave, 1986), have been used to sample very close to substrates (e.g., rocks, kelp). A wide variety of other plankton samplers has been used elsewhere, but little or not at all in Californian waters. Examples of some of these are the push-net surface sampler (Miller, 1973; Miller et al., 1973); the plankton purse seine (Murphy and Clutter, 1972); the multiple openingclosing net sampler related to the MOCNESS, the BIONESS (Bedford Institute of Oceanography Net and Environmental Sampling System: Sameoto et al., 1980; Sameoto, 1983); an automated high-speed sampler, the Hardy Plankton Recorder (Hardy, 1936) and a variant, the Longhurst-Hardy Plankton Recorder (Longhurst et al., 1966); and light traps, which are highly selective and difficult to quantify, but are effective in capturing larger fish larvae that are taken rarely by plankton nets (Thorrold, 1992, 1993; Choat et al., 1993; Brogan, 1994).

Ontogenetic Stages During ontogeny, an animal proceeds from the fertilized egg stage through a series of developmental processes that lead to the formation of a reproducing adult. In a large proportion of

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F I G U R E 11-2 Major events (in capitals) and stages (lower case) in the ontogeny of fishes.

F I G U R E 11-4 Developmental stages of northern anchovy (Engraulis mordax) larvae. A: yolk-sac stage, 2.5 mm; B: preflexion stage, 5.0 mm; C: early flexion stage, 9.6 mm; D: late flexion stage, 11.5 mm; E: postflexion stage, 18.4 mm; F: transformation stage, 31.0 mm. Illustrations from Kramer and Ahlstrom (1968).

F I G U R E 11-3 Developmental stages of northern anchovy (Engraulis

mordax) eggs (modified from Moser and Ahlstrom, 1985). A: Stage I; B: early Stage II; C: Stage II; D: Stage III; E: Stage IV; F: Stage V; G: Stage VI; H: Stage VII; I: Stage VIII; J: Stage IX; K: Stage X; L: Stage XI. A–D are “early stage”; E–F are “middle stage”; G–L are “late stage.”

marine fishes, the eggs are free-floating after spawning and develop into planktonic larvae that inhabit the productive upper region of the water column. Although developmental processes are continuous, it is helpful to subdivide the ontogenetic process from egg to juvenile into a series of stages or periods that are punctuated by critical life-history events (fig. 11-2). The “events” in fig. 11-2 are emphasized to suggest their critical place in the dynamics of fish populations. Kendall et al. (1984) presented terminology that generally is used in ichthyoplank-

ton research and compared it with alternate terminologies; ontogenetic stages have been described and discussed further by a number of authors, for example, Fahay (1983), Matarese et al. (1989), Moser (1996), and Leis and Carson-Ewart (2000). Here we present illustrations of developmental stages of northern anchovy, Engraulis mordax (fig. 11-3 and 11-4). Typical teleost egg development may be subdivided into three stages as follows: early stage, from extrusion and fertilization to the formation of an advanced blastodisc (fig. 11-3A–D); middle stage, from the beginning to the end of epiboly, essentially the gastrulation process (fig. 11-3E,F); and late stage, from the end of epiboly and “blastopore” closure to hatching (fig. 11-3G–L). Early-stage eggs of many teleosts are similar in size and morphology and are difficult to identify; however, the state of development and the appearance of organs, structures, and pigmentation in middle and late-stage eggs provide a suite of taxonomic characters that are helpful in identifying species (Ahlstrom and Moser, 1980; Matarese and Sandknop, 1984). Further subdivision of egg development is needed when samples of eggs are staged for biomass estimation using the daily egg production method (DEPM) (Lasker, 1985; Lo et al., 2001). The set of 11 stages for northern anchovy was based on structural criteria chosen from the sequence of morphological changes that occur during embryogenesis (Moser and Ahlstrom, 1985). Once stage criteria are established, temperature-specific stage-to-age keys can be obtained by laboratory studies from which mortality curves can be derived for egg samples from field surveys. They form the basis for estimating daily egg production (Lasker, 1985; Lo et al., 2001). The stages of egg development described for northern

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F I G U R E 11-5 Developmental processes and events in northern anchovy, Engraulis mordax, from Hunter and Coyne (1982).

anchovy have been used with slight modification for other species (e.g., Pacific sardine, Pacific hake, Dover sole, croakers) and are applicable to a wide variety of teleosts. In the majority of fish species with planktonic eggs, the larvae hatch at a non-feeding yolk-sac stage of development typically characterized by a large yolk sac, unpigmented or only partially pigmented eyes, nonfunctional mouth, and no fin rays or bony fin supports (fig. 11-4A). Larvae that hatch from larger planktonic eggs (
2–3 mm diameter) may be more developed at hatching, and larvae that hatch from demersal eggs typically are more developed, with little or no yolk remaining and with pigmented eyes, a functional mouth, and commonly with fin rays forming in one or more fins. Exhaustion of the yolk reserve and acquisition of functional eyes, mouth, and digestive tract in preparation for the commencement of feeding marks the end of the yolk-sac stage. Subdivision of the post yolk-sac larval period into three stages based on the state of notochord flexion during caudal-fin development (preflexion-fig. 11-4B; flexion-fig. 11-4C,D; postflexion-fig. 11-4E) effectively defines the early, middle, and late stages of larval development. Organogenesis and behavioral development in fish larvae involves a complicated orchestration of processes and events that lead to transformation (fig. 11-4F) into the juvenile stage. In the well-studied northern anchovy, for example, the process of notochord flexion that takes place at a body length of
10–13 mm coincides with the appearance of rods in the retina, the formation of multiple red muscle layers, the proliferation of red blood cells,

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initial swim bladder development and diel vertical movement, the threshold for schooling, and the transition from viscous to inertial hydrodynamic regimes (fig. 11-5) (Hunter and Coyne, 1982). Also, in anchovy and typically in other teleosts, the formation of dorsal and anal fin rays begins during caudal fin formation (Moser, 1996). Margulies (1989) found that notochord flexion in white sea bass (Atractoscion nobilis) larvae coincided with an improvement in their ability to escape juvenile white sea bass predators; this was related, in part, to major developmental events during this stage (e.g., rapid improvement in visual acuity, visual accommodation to distant objects, growth and stratification of the optic tectum, and large increases in the number of free neuromasts on the head and body) (fig. 11-6). Although other information on the coordination of developmental events in teleosts is scanty, where this has been studied (O’Connell, 1981; Blaxter, 1984; Fuiman, 1997; Fuiman et al., 1998), notochord flexion typically coincides with the development of an array of structures and functional capabilities critical to larval survival and serves as a meaningful and practical milestone with which to divide the larval period. At the end of this period, larvae undergo a transformation process during which larval characters are lost and juvenile/adult characters are acquired (Moser, 1996). This process may be abrupt and involve morphological changes that require rapid differentiation and allometric growth (e.g., changes in shape and general morphology, development of a stomach, and formation of a thick, solidly pigmented integument invested with scales and, in some, a silvery guanine layer,

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F I G U R E 11-6 Developmental processes and events in white sea bass, Atractoscion nobilis, modified from Margulies (1989). I.O.  infraorbital; H.M.  hyomandibular; L.L.  lateral line; ONL  outer nuclear layer of retina; S.O.  supraorbital; T.L.  torus longitudinalis. Values for acuity refer to minutes of arc.

photophores, or other luminous tissue). Full complements of fin rays are present and specialized larval structures (see below) are lost. At the end of this process, epipelagic species may remain in the same habitat or move to inshore nursery areas, midwater species descend to juvenile depths, and demersal species settle in appropriate juvenile habitats. Some demersal species have specialized pelagic juvenile stages that may remain in the pelagic environment for a protracted period (Kendall et al., 1984; Moser, 1996; Leis and Carson-Ewart, 2000).

CalCOFI Larval Fish Assemblages About 26 orders and 160 families of fishes are represented in the ichthyofauna of the California Current region. Among the families that produce planktonic larvae, the region has about 800 species. A guide to the ichthyoplankton of the region (Moser, 1996) included 25 orders, 158 families, and 586 species. Species whose larvae remain unidentified are primarily nearshore fishes (e.g., cottids, sticheoids, gobioids, blennioids) that are relatively poorly sampled by CalCOFI or other research programs. In CalCOFI oblique plankton tows, coastal pelagic fish larvae are the dominant category; about 70% of the total larvae is contributed by only 4% of the total taxa (Moser et al., 2001b). Midwater fish larvae have the most taxa (38%) and are second in abundance with 20% of the total

larvae. Rocky-shore fishes contribute about one-fourth of the taxa but represent only 7% of the total larval abundance. In the Natural History Museum of Los Angeles County (LACM) nearshore larval surveys, bottom fish taxa constitute
80% of the total taxa; about half belong to rocky-shore taxa (Moser et al., 2001b). Larvae of midwater species represent only 11% of the total taxa and
1% of the total larval abundance. As in the CalCOFI surveys, larvae of coastal pelagic fishes dominate the LACM surveys; more than 70% of the total abundance is contributed by 8.5% of the taxa. In the LACM surveys, larvae of soft substrate fishes are 10 times more abundant than in CalCOFI surveys. Larval northern anchovy are dominant in CalCOFI and in LACM surveys. In CalCOFI oblique plankton samples northern anchovy are 3.5 times more abundant than the second ranking species, Pacific hake, Merluccius productus (table 11-1). California smoothtongue Leuroglossus stilbius, a bathylagid, ranks third in total abundance, and the importance of midwater fishes in the ecology of the California Current system is apparent from the fact that midwater fishes (e.g., bathylagids, phosichthyids, gonostomatids, myctophids) represent more than half of the 30 most abundant taxa taken in CalCOFI samples (table 11-1). The overall CalCOFI survey pattern extends from the California-Oregon border to the southern tip of Baja California, Mexico, and offshore to the outer edge of the California Current (fig. 11-1); however, most annual surveys covered a

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TA B L E 11-1

Thirty Most Abundant Larval Fish in CalCOFI Surveys (Present Pattern) 1951–2000

Number Taxon

Common Name

Family

Occurrences

Rank

Total

Rank

Total

Engraulis mordax Merluccius productus Leuroglossus stilbius Sebastes spp. Vinciguerria lucetia Stenobrachius leucopsarus Sardinops sagax Trachurus symmetricus Sebastes jordani Bathylagus ochotensis Sciaenidae Triphoturus mexicanus Bathylagus wesethi Protomyctophum crockeri Ceratoscopelus townsendi Citharichthys stigmaeus Nannobrachium ritteri Tarletonbeania crenularis Diogenichthys atlanticus Citharichthys spp. Scomber japonicus Sebastes paucispinis Symbolophorus californiensis Cyclothone signata Nannobrachium spp. Genyonemus lineatus Citharichthys sordidus Diaphus spp. Cyclothone spp.

Northern anchovy Pacific hake California smoothtongue Rockfishes Panama lightfish Northern lampfish Pacific sardine Jack mackerel Shortbelly rockfish Popeye blacksmelt Croakers Mexican lampfish Snubnose blacksmelt California flashlightfish Dogtooth lampfish Spotted sanddab Broadfin lampfish Blue lanternfish Longfin lanternfish Sanddabs Chub mackerel Bocaccio California lanternfish Showy bristlemouth Lampfishes White croaker Pacific sanddab Headlightfishes Bristlemouths

Engraulidae Merlucciidae Bathylagidae Scorpaenidae Phosichthyidae Myctophidae Clupeidae Carangidae Scorpaenidae Bathylagidae Sciaenidae Myctophidae Bathylagidae Myctophidae Myctophidae Paralichthyidae Myctophidae Myctophidae Myctophidae Paralichthyidae Scombridae Scorpaenidae Myctophidae Gonostomatidae Myctophidae Sciaenidae Paralichthyidae Myctophidae Gonostomatidae

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29

2999304 850302 371276 317355 247015 234471 146602 82668 70374 53112 37904 37822 35442 32067 24678 23655 21988 21649 19941 18755 18006 17692 17455 16268 16126 14299 13544 12945 11690

1 6 4 2 11 3 25 14 19 7 36 8 13 5 21 12 9 10 15 18 42 22 16 27 17 63 30 24 23

6064 3464 4579 5563 1975 4882 1009 1810 1500 2831 668 2390 1862 3686 1212 1951 2134 1978 1799 1591 438 1161 1790 945 1725 212 864 1025 1040

Vinciguerria poweriae

Highseas lightfish

Phosichthyidae

30

9612

70

168

NOTE:

“Number” is a standardized value adjusted for standard haul factor and fraction of the plankton sample sorted.

smaller area from San Francisco, California, to Bahia Magdalena, Baja California Sur, and seaward to include the California Current. Spatial and temporal coverage was most complete during the early years of the surveys (1951–1960) when multivessel cruises occupied much of the survey pattern at monthly intervals (Moser et al., 1993). A recurrent group analysis (Fager, 1957) of the CalCOFI larval fish assemblages for 1954 to 1960 (Moser et al., 1987) revealed nine recurrent groups with numerous associated taxa (fig. 11-7). These formed Northern and Southern Complexes, each containing four groups and their associated taxa, and a Southern Coastal Complex that included one group and its associated taxa. The major recurrent group in the Northern Complex, Leuroglossus, is formed by three midwater species, popeye blacksmelt (Bathylagus ochotensis), California smoothtongue, and northern lampfish (Stenobrachius leucopsarus), and two demersal taxa, Pacific hake and the speciose rockfish genus (fig. 11-8A). Tarletonbeania is composed of blue lanternfish (Tarletonbeania crenularis), a myctophid that migrates to surface waters at night, and the medusafish (Icichthys lockingtoni), an epipelagic species of the family Centrolophidae (fig. 11-8B). The other two groups in the Northern Complex, Sardinops and Citharichthys, are composed of coastal pelagic and demersal species. Sardinops includes Pacific sardine and chub mackerel (Scomber japonicus) (fig. 11-8C). Citharichthys is

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formed by northern anchovy, longfin sanddab (Citharichthys xanthostigma), and Gulf sanddab (C. fragilis) (fig. 11-8D). Speckled sanddab (C. stigmaeus), though not a member of a recurrent group, has significant affinities with members of the Leuroglossus and the Citharichthys groups (fig. 11–7). In the Southern Complex the largest group, Symbolophorus, is formed by five midwater species: snubnose blacksmelt (Bathylagus wesethi), bristlemouths (genus Cyclothone in the family Gonostomatidae), and three myctophids, California lanternfish (Symbolophorus californiensis), longfin lanternfish (Diogenichthys atlanticus), and broadfin lampfish (Nannobrachium ritteri) (fig. 11-9A). Snubnose blacksmelt and broadfin lampfish are endemic to the California Current region, whereas longfin lanternfish and two of the bristlemouth species, benttooth bristlemouth (C. acclinidens) and slender bristlemouth (C. pseudopallida), have worldwide distributions that include equatorial and central water masses. Showy bristlemouth (Cyclothone signata), the most common bristlemouth species in CalCOFI collections, is endemic to the eastern central Pacific. California lanternfish may range westward from the California Current to the Kuroshio. The three-member Triphoturus group includes two myctophids, Mexican lampfish (Triphoturus mexicanus) and California flashlightfish (Protomyctophum crockeri), and jack mackerel (Trachurus symmetricus) (fig. 11-9B). California flashlightfish is endemic to the

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F I G U R E 11-7 Recurrent groups and their

associates in the CalCOFI survey area, 1954–1960. A line between two groups indicates that there are intergroup pairs with significant affinity indexes ( 0.3). The number associated with each line is the fraction of significant affinity pairs divided by the number of possible pairs. Northern, Southern, and Southern Coastal Complexes are separated by dashed lines (modified from Moser et al., 1987).

California Current region, and Mexican lampfish, the most abundant myctophid in the southern part of the California Current region, extends into the Gulf of California, and is replaced by a similar species, T. oculeus, southward along the mainland coast of Mexico and by highseas lampfish (T. nigrescens) westward of the California Current. Jack mackerel is a prominent pelagic species of the California and Baja California coasts. Two myctophids, dogtooth lampfish (Ceratoscopelus townsendi) and sunbeam lampfish (Lampadena urophaos), comprise Ceratoscopelus (fig. 11-9C). Sunbeam lampfish is a warmwater cosmopolite, whereas dogtooth lampfish is a California Current endemic (John Paxton, Australian Museum, pers. commun.). The Vinciguerria group (fig. 11-9D) is composed of four eastern tropical Pacific species whose ranges extend northward to the waters off southern California. Of the four species, the phosichthyid, Pacific lightfish (Vinciguerria lucetia ), the most abundant off California, ranks fifth in total larval abundance, and its abundance increased sharply during the recent warm climate regime. Larvae of the other species, the myctophids Diogenes lanternfish (Diogenichthys laternatus), thickhead lanternfish (Hygophum atratum), and slendertail lanternfish (Gonichthys tenuiculus), are abundant off Baja California and occur rarely off southern California, typically during El Niño conditions when they are advected poleward by the strong coastal countercurrent (Moser et al., 2001a,b). The midwater genus Melamphaes, primarily highsnout bigscale (M. lugubris) and little bigscale (M. parvus), and the midwater predator family Paralepididae, primarily slender barracudina (Lestidiops ringens), are associates of Symbolophorus; Melamphaes also is an associate of Triphoturus. Blackbelly dragonfish

(Stomias atriventer), a midwater predator in the family Stomiidae, is an associate of the Vinciguerria group. The Southern Coastal Complex, Synodus, is composed of basketweave cusk-eel (Ophidion scrippsae) and three temperatetropical genera, Synodus, Prionotus, and Symphurus, that inhabit soft-bottom shelf habitats (fig. 11-10). Each of these genera contains a species (California lizardfish, S. lucioceps; lumptail sea robin, P. stephanophrys; and California tonguefish, S. atricaudus), whose distribution extends northward into southern California waters and accounts for the largest proportion of the larvae of that genus in CalCOFI samples. The round herring (Etrumeus teres) is an associate of Synodus. The highest abundances of all of these species are in Bahia Sebastian Viscaino (the bay formed by the Punta Eugenia peninsula) and the region between Punta Eugenia and Bahia Magdalena (fig. 11-1). Together, these two regions have
39,000 km2 of shelf habitat (20,008 and 18,897 km2, respectively), approximately 70% of the shelf habitat for the entire Baja California coast and
4.6 times the amount of shelf habitat off southern California.

Geographic and Seasonal Distribution The California Current region, including the coastal waters of California and Baja California, south to Cabo San Lucas, encompasses an area
1 million km2 and includes three coastal zoogeographic provinces (the Oregonian, San Diegan, and Panamic), a coastal upwelling zone, and three oceanic water masses (Subarctic-Transitional, Central, and Eastern Tropical Pacific—the more or less distinct segment of Pacific equatorial

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F I G U R E 11-8 Members of the four recurrent groups of fish larvae of the Northern Complex in the CalCOFI survey area, 1954–1960. (A) Leuroglossus; (B) Tarletonbeania; (C) Sardinops; (D) Citharichthys. Citharichthys stigmaeus is an associate of Leuroglossus and Citharichthys; Citharichthys spp. is an associate of Citharichthys. All illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained.

water east of about 140°W) (fig. 11-11). Two of the three midwater members of Leuroglossus, northern lampfish (fig. 11-12A) and popeye blacksmelt (see Moser et al., 1993: CalCOFI Atlas 31, p.18), inhabit California Current waters south to northern Baja California and westward in the transition zone (Willis et al., 1988). The third midwater species, California smoothtongue, is a more southerly and coastal species with a center of distribution off southern California (CalCOFI Atlas 31, p.14). Larval abundance of the three species peaks in winter, and substantial numbers of larvae are present in spring. Pacific hake spawns off California and Baja California; the juveniles migrate north as they grow, reach maturity in the waters of the Pacific northwest and the Gulf of Alaska, and then migrate south to their spawning grounds. Spawning is concentrated

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during winter; off southern California, half the total larvae are produced in February and
90% during January-March. The larval peak off southern Baja California (CalCOFI Atlas 31, p.8) is believed to represent a subpopulation distinct from the main population (Bailey et al., 1982). About sixty species of viviparous rockfishes occur off California and Baja California. Although rockfish larvae in aggregate rank fourth among all larvae captured on CalCOFI surveys (table 11-1), only seven species can be distinguished in CalCOFI samples. Most species release their larvae in winter, although parturition tends to shift to spring or summer at higher latitudes (CalCOFI Atlas 31, p.12). Some species have extended parturition seasons; for example, off southern California, aurora rockfish (S. aurora) releases larvae from November to August with a peak in June,

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F I G U R E 11-9 Members of four recurrent groups of fish larvae of the Southern Complex in the CalCOFI survey area, 1954–1960. (A) Symbolophorus; (B) Triphoturus; (C) Ceratoscopelus; (D) Vinciguerria. Melamphaes spp. is an associate of Symbolophorus and Triphoturus. Paralepididae is an associate of Symbolophorus; Stomias atriventer and Nannobrachium spp. are associates of Vinciguerria. All illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained.

and splitnose rockfish (S. diploproa) produces larvae year-round with a summer-fall peak (Moser and Boehlert, 1991; Moser et al., 2000). Slender sole (Lyopsetta exilis), a pleuronectid flatfish, is not a Leuroglossus group member but is the most abundant affiliate of the group (Moser et al., 1987). Slender sole larvae occur year-round off California and Baja California with a spring peak (CalCOFI Atlas 31, p. 86). The higher spring abundance of slender sole larvae off central California and in the Sebastian Viscaino Bay region, compared to regions between the two, probably reflects the amount of suitable habitat and relatively large spawning populations in the two regions. The two Tarletonbeania species, blue lanternfish and medusafish, have a subarctic-transitional distribution ranging across the North Pacific and southward in the California

Current to northern Baja California. Larvae are present yearround in the northern sector of the CalCOFI survey area with peak abundance of blue lanternfish during fall-winter (CalCOFI Atlas 31, p.38) and medusafish in spring–summer (CalCOFI Atlas 31, p.70). The two Sardinops group species, Pacific sardine (fig. 11-12B) and chub mackerel (CalCOFI Atlas 31, p.48), have broad spawning distributions that can extend from the Gulf of Alaska to the Gulf of California, depending on ocean conditions. During 1951 to 1984 their larvae were primarily south of Point Conception and most abundant off central and southern Baja California. Both species produce larvae year-round with winter and summer peaks off Baja California. Off southern California, chub mackerel larval abundance peaks during spring–summer (CalCOFI Atlas 31, p. 48).

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F I G U R E 11-10 Members of the Synodus recurrent group of fish larvae that form the core of the Southern Coastal Complex in the CalCOFI survey area, 1954–1960. Etrumeus teres is an associate of Synodus. Most illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained. Synodus spp. from Okiyama (1984); Prionotus spp. from Richards (1996).

The Citharichthys group member, northern anchovy, was the most abundant species in the CalCOFI time series during 1951 to 1984 and accounted for almost half of the total fish larvae (Moser et al., 1993). Larval anchovy were ubiquitous seasonally, with a winter peak off southern California and northern Baja California (fig. 11-12C). The other two species in the group, longfin and Gulf sanddabs, also spawn yearround, but peak larval abundance is shifted to summer months in the Sebastian Viscaino Bay region (CalCOFI Atlas 31, pp. 60 and 50). Speckled sanddab, a Citharichthys associate species shared with the Leuroglossus group, spawns yearround with a fall peak off California and the Sebastian Viscaino Bay region (CalCOFI Atlas 31, p. 52). The Sebastian Viscaino Bay region provides optimum habitat for temperate–subtropical sanddabs; all three species had their highest average larval abundance there. In Symbolophorus, larvae of California lanternfish (fig. 1112D), snubnose blacksmelt (CalCOFI Atlas 31, p. 28), and broadfin lampfish (CalCOFI Atlas 31, p. 44) occur year-round with highest average larval abundances in the core of the central region of the California Current during spring–summer. Although a species similar to, and perhaps conspecific with,

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California lanternfish occurs in the western Pacific (Wisner, 1976; Willis et al., 1988), the rarity of larvae in the northern region of the California Current (Doyle, 1992a) suggests that the populations are disjunct. Showy bristlemouth accounts for
90% of bristlemouth larvae in CalCOFI samples, benttooth and slender bristlemouths contribute most of the remaining larvae,
4 and 2%, respectively (Moser et al., 2001a). Larvae are present year-round with highest abundance in the core region of the California Current in summer and fall (CalCOFI Atlas 31, p. 34). The pattern of larval distribution for longfin lanternfish clearly demonstrates the protrusion of the population from the central water mass into the midregion of the California Current (fig. 11-12E). Slender barracudina, a Symbolophorus associate, is a California Current region endemic, replaced to the south by L. neles and to the west by L. pacificum. It spawns year-round with highest abundance in the California Current core (CalCOFI Atlas 31, p.112). In Triphoturus, Mexican lampfish spawns year-round with peak larval abundance in summer off Northern and Central Baja California (CalCOFI Atlas 31, p.16). California flashlightfish spawns year-round in the core of the California Current with highest larval abundance in winter at the northern part of the CalCOFI survey pattern (CalCOFI Atlas 31, p. 36). Jack mackerel exhibits a seasonal south-to-north spawning progression, beginning in winter–spring and peaking off southern California in early summer (CalCOFI Atlas 31, p.24). An offshore segment of the population ranges to the western margin of the California Current and spawning progresses northward into the transition zone in summer and autumn. The Triphoturus associate genus, Melamphaes, spawns yearround with highest larval abundance from the core to the outer margins of the California Current (CalCOFI Atlas 31, p. 62). In Ceratoscopelus, dogtooth lampfish spawns year-round with highest larval abundance in the core and outer margin of the California Current (CalCOFI Atlas 31, p. 40). The high summer abundance in the outermost CalCOFI region probably represents larvae of the warm-water cosmopolite, C. warmingii (a species morphologically similar to dogtooth lampfish), an inhabitant of equatorial and central water masses. Larval abundance of the warm-water cosmopolite, sunbeam lampfish, is more seasonal, with a progression toward a summer–fall peak in the southern core of the California Current (CalCOFI Atlas 31, p. 134). Larvae of the four Vinciguerria species are present yearround; only Pacific lightfish show high abundance as far north as southern California; in the CalCOFI time series for 1951 to 1984 the larval abundance of the Pacific lightfish peaked off northern Baja California in summer (fig. 11-12F). The abundance of Diogenes lanternfish larvae was consistently highest off southern Baja California without a seasonal peak (CalCOFI Atlas 31, p. 26). Larvae of the other two Vinciguerria members occurred primarily off southern Baja California; slendertail lanternfish larval abundance was highest in winter–spring (CalCOFI Atlas 31, p.108), whereas thickhead lanternfish showed little seasonality (CalCOFI Atlas 31, p.88). Larvae of the Vinciguerria associate, blackbelly dragonfish, are widespread off California and Baja California and present yearround, with highest abundance off California (CalCOFI Atlas 31, p.130). Spawning of Ophidion scrippsae (fig. 11-27E) and the other Synodus members, Synodus spp. (CalCOFI Atlas 31, p. 54), Prionotus spp. (CalCOFI Atlas 31, p. 68), and Symphurus spp. (CalCOFI Atlas 31, p.72), are distinctly seasonal with peak abundance during summer–fall in the extensive shelf habitats off central and southern Baja California.

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F I G U R E 11-11 Water masses and zoogeographic Provinces of the northeast Pacific in relation to the CalCOFI survey area. The Eastern Tropical Pacific water mass referred to in the text is the wedge-shaped eastern limb of the equatorial water mass. From Brinton (1962), Allen and Smith (1988), and Moser (1996).

Interannual and Decadal Changes Ichthyoplankton samples are dominated by eggs and early larval stages that reflect the reproductive output of adult stocks, thus providing useful indexes of relative population abundance. Consequently, the changes undergone by many fish populations off California and Baja California during the past half-century are evident in the CalCOFI ichthyoplankton time series. The most dramatic of these are the waxing and waning of the Pacific sardine and northern anchovy populations. CalCOFI surveys in 1954 showed that sardine and anchovy larvae extended from central California to Cabo San Lucas and offshore to the margin of the survey pattern occupied that year (
250 n. mi.); anchovy larvae were more concentrated coastally than sardine (fig. 11-13A). Eight years later, larval sardine abundance had plummeted and their distribution had contracted to semi-isolated patches along the shelf regions from southern California to central Baja California (Ahlstrom, 1966) (fig. 11-13B). In contrast, anchovy larval abundance increased markedly (Ahlstrom, 1966; Smith, 1972); areas of high concentration extended offshore to the margin of the survey pattern occupied in 1954 (fig. 11-13B). Average abundance of sardine larvae in the SCB region, the area covered by CalCOFI surveys since 1984, declined from
10/10 m2 of surface area in 1954 to 1/10 m2 for a 20-year period from 1961 to 1981 (fig. 11-13C). Abundance increased sporadically from 1984 to 1995 and then abruptly to
90/10 m2 in 1997. Larval anchovy, however,

showed a distinctly different trend, increasing from
20/10 m2 in 1951 to a maximum of
800 larvae/10 m2 in 1981, and declining to 100/10 m2 in recent surveys (fig. 11-13C). A fishing moratorium for Pacific sardine was in force during the years when the population was depressed and had retracted to bays and nearshore areas along the southern California and Baja California coast (Wolf and Smith, 1985; Wolf et al., 1987). An increase in larval sardine abundance was detected in nearshore habitats as early as 1981 (Watson, 1992), and subsequent ichthyoplankton surveys have shown extensive spawning offshore to the California Current and northward to central California, whereas anchovy spawning has contracted to nearshore areas of the SCB (fig. 11-14) (Checkley et al., 2000; Smith and Moser, 2003). The role that fisheries management has played in the resurgence of the Pacific sardine should be considered in the light of natural fluctuations in sardine and anchovy populations over a period of centuries. Deposition rates of sardine and anchovy scales in anaerobic sediments from the Santa Barbara Basin indicate that populations of both species varied cyclically over periods of about 60 years and that northern anchovy also varied over a 100-year period (fig. 1113D; Baumgartner et al., 1992). Moreover, Pacific sardine has experienced nine major population collapses and recoveries during the past 1700 years with an average recovery time of about 30 years (Baumgartner et al., 1992). The importance of ocean climate in the regulation of Pacific sardine populations is highlighted by the fact that stocks underwent near-synchronous

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F I G U R E 11-12 Quarterly maps showing mean larval abundance (number per 10 m2) from 1951 to 1984 in each of 22 CalCOFI regions (Moser et

al., 1993) for Stenobrachius leucopsarus (Leuroglossus recurrent group of the CalCOFI survey area), Sardinops sagax (Sardinops), Engraulis mordax (Citharichthys), Symbolophorus californiensis (Symbolophorus), Diogenichthys atlanticus (Symbolophorus), and Vinciguerria lucetia (Vinciguerria).

cycles of collapse and recovery in three separate regions of the Pacific (U.S. west coast, Japan, Chile-Peru) during the past century (Kawasaki, 1991) and that these cycles coincided with shifts in decadal-scale ocean climate regimes. Extensive records of population changes, such as those available for sardine and anchovy, are not available for other species in the California Current region; however, decadal-scale fluctuations in larval

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abundance are apparent in the CalCOFI time series for most of the teleost fishes of the region. CalCOFI oceanographic measurements made at each station provide the opportunity to examine the variation in larval distribution and abundance in the context of interannual and decadal environmental changes. The cyclic warming and cooling of equatorial waters, known as the El Niño/Southern Oscillation (ENSO), produced

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F I G U R E 11-13 Interannual changes in abundances and distributions of Pacific sardine and northern anchovy. A: larval distributions in the CalCOFI survey area, 1954, from Ahlstrom (1966); B: larval distributions in the CalCOFI survey area, 1962, from Ahlstrom (1966); C: mean annual larval abundance (number per 10 m2) in the Southern California Bight from 1951 to 2000; D: 1700-year series of estimated adult biomasses off California and Baja California based on scale deposition rates in ocean sediments, from Baumgartner et al. (1992).

a series of warm (1957–1958, 1963, 1982–1983, 1993, and 1997–1998) and cold (1954–1956, 1988–1989, 1998–1999) episodes in the California Current region during the past 50 years. Prolonged cold ocean conditions in the CalCOFI region during 1970 to 1976, produced by three closely spaced La Niñas, were followed abruptly by a shift to a warm ocean regime late in 1976. Ocean regimes in the North Pacific are generated by a 20–30 year oscillation (Pacific Decadal Oscillation or PDO) that is related to basin-scale changes in atmospheric pressure, particularly the intensification and position of the Aleutian low pressure system, and possibly to low latitude atmospheric teleconnections (Miller et al., 1994; Mantua et al., 1997; Hollowed et al., 1998; Schwing et al.,

2002). The PDO produced two cool ocean regimes (1900 to 1924 and 1947 to 1976) and two warm regimes (1925 to 1946 and 1977 to at least 1998) during the past century. Primary and secondary production in the California Current region decreased dramatically after the regime shift of 1976 to 1977 (Brodeur and Ware, 1992; Roemmich and McGowan, 1995a,b; Ware, 1995; Hayward, 1997; McGowan et al., 1998). Major shifts occurred in the distributions of larval fishes in response to ENSO events and the PDO, as the boundaries between subarctic and equatorial water masses shifted latitudinally and intrusion of central water into the SCB region waxed and waned (Moser et al., 1987, 2001a; Smith and Moser, 1988, 2003).

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F I G U R E 11-14 Mean abundance of Pacific sardine larvae at CalCOFI stations (present survey pattern) during cool (A) and warm (B) ocean regimes compared with mean abundance of northern anchovy larvae during cool (C) and warm (D) regimes, from Moser (2001a).

Northern lampfish, a subarctic-transitional species in the Leuroglossus recurrent group, demonstrates the effect that ENSO and the PDO have on larval fish distribution and abundance (fig. 11-15). The shoreward and northward contraction of the larval distribution in response to long-term offshore warming is apparent (fig. 11-15A,B); equally apparent are the abrupt decline in larval abundance associated with the El Niño episode in 1957 to 1959 and the trend of increasing relative abundance from 1960 to 1972. One would expect that the relative abundance would have declined during the three El Niño events after the regime shift and would have been relatively low, generally, during the warm regime; however, there was no obvious trend in relative abundance associated with the transition from cool to warm ocean regimes nor with ENSO

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events during the warm regime. A possible explanation may be found in the compression of spawning toward the continental borderland (fig. 11-15A,B) where generally higher production (Hayward and Venrick, 1998) could have compensated for reduced primary and secondary production during the warm regime. Also, reproduction in this species is essentially limited to the cold months of the year in the CalCOFI survey area, when the effect of warm ocean conditions might have been minimized (fig. 11-15D). The medusafish, a subarctictransitional species in the Tarletonbeania group, showed a 4-fold decline in larval abundance between the two regimes (fig. 11-16A,B), relatively high abundance during the cold ocean episodes in the cool regime, and abrupt declines during El Niño episodes (fig. 11-16C). Larval production peaked during

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F I G U R E 11-15 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Stenobrachius leucopsarus in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

March and June and declined sharply during summer months (fig. 11-16D). Shortbelly rockfish (Sebastes jordani), an associate of the Leuroglossus group, showed little change in distribution pattern between the two regimes (fig. 11-17A,B); however, the generally elevated abundance during cold episodes and the abrupt declines in response to El Niños are apparent (fig. 11-17C). The marked peak in larval abundance (1988 to 1991) during the warm regime may be related to the appearance of an anomalously large year class in the late 1980s (Moser et al., 2000); rockfishes are well known for sporadic and unexplained production of large year classes. Like other species associated with the Leuroglossus group, shortbelly rockfish release their larvae during cold months (fig. 11-17D). In contrast to shortbelly rockfish, a noncommercial species, the cowcod (S. levis) is a heavily exploited species whose larvae declined precipitously

at the regime shift and were nearly absent from CalCOFI samples during the warm regime, when their distribution receded to a few stations in the Santa Barbara Channel area (fig. 11-18). A recent population analysis of cowcod (Butler et al. 1999, 2003) used fishery data in combination with the CalCOFI larval time series to estimate changes in biomass during the past century. This study showed that the cowcod stock has declined to 7% of its biomass prior to 1940 and recommended a rebuilding program to include a Cowcod Conservation Area, where fishing is prohibited. Although the data are sparse, a continuance of the apparent trend of increasing larval abundance in 1999 and 2000 may indicate a reversal of the population decline (fig. 11-18C). The larval distribution pattern of snubnose blacksmelt, a California Current endemic in the Symbolophorus group, changed little during the two regimes; however, the trend of

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F I G U R E 11-16 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Icichthys lockingtoni in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

increasing larval abundance during the 1980s and 1990s is apparent (fig. 11-19A–C). Consonant with this is the peak of larval production centered on the warm months (fig. 11-19D). The precipitous decline in larval abundance following the 1997 to 1998 El Niño (fig. 11-19C) may be indicative of a shift to a cool ocean regime. A positive reaction to warm conditions was even more apparent in longfin lanternfish, a warm-water cosmopolite in the Symbolophorus group. Larval abundance increased steadily throughout the time series with increased intrusion into the California Current from the central water mass (fig. 11-20A–C). As for snubnose blacksmelt, larval abundance declined sharply following the 1997 to 1998 El Niño. There was no apparent seasonality in larval production, as is typical of warm-water cosmopolites (fig. 11-20D). In the Triphoturus group, Mexican lampfish, an endemic species of the southern region of the California Current and Gulf of

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California, showed a northward shift in larval distribution during the warm regime, increases in larval abundance just before or during El Niño episodes, decreases during La Niña events (especially after the 1998 to 1999 La Niña), and peak spawning during the warmest ocean period in the SCB (fig. 1121A–D). Members of the eastern tropical Pacific recurrent group Vinciguerria show the largest response to ocean changes. The larval distribution of Panama lightfish shifted northward and coastward from the cool to warm regime, abundance increased markedly during the warm regime and episodically in response to El Niño conditions during both regimes (fig. 11-22A–C). As evident in the time series for Symbolophorus members, larval abundance declined precipitously following the 1998 to 1999 La Niña, possibly a trend signaling a shift to a cool ocean regime. Like Mexican lampfish, larval production in the SCB

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F I G U R E 11-17 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Sebastes jordani in the Southern California

Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

was highest during the months when the ocean was warmest (fig. 11-22D). Diogenes lanternfish larvae, in the Vinciguerria group, were rare in the SCB until 1997 when an unusually strong coastal countercurrent associated with the 1997 to 1998 El Niño advected relatively large numbers of them into the SCB from waters off Baja California (fig. 11-23A–D). After 1998, Diogenes lanternfish larvae were not taken on CalCOFI surveys, demonstrating the value of larval fish distributions as indicators of dynamic oceanographic events (Moser et al., 2001b; Smith and Moser, 2003). The increased presence of early-stage larvae of midwater species from eastern tropical Pacific and central Pacific water masses during warm regimes in the California Current reflects shifts in the boundaries of these populations. This could result from intrusion of these water masses into the California

Current, carrying these populations, or could be a result of modifications of the subarctic-transitional water of the California Current that are conducive to survival and reproduction of these populations in a region adjacent to their typical range. Perhaps these population boundary shifts are caused by a combination of both scenarios. One of the most fascinating questions in marine zoogeography is how oceanic midwater fish species are segregated by water mass boundaries (Ebeling, 1962; Johnson and Barnett, 1975, Miya and Nishida, 1996, 1997). The CalCOFI ichthyoplankton time series, spanning two ocean regimes and numerous ENSO episodes, offers an excellent opportunity to study the dynamics of fish populations and habitat variables at these water mass boundaries and could provide insight into the mechanisms underlying this fundamental zoogeographic question.

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F I G U R E 11-18 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Sebastes levis in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

CalCOFI Assemblages—Summary Fisheries landings and ichthyoplankton surveys show that the epipelagic habitat of the California Current region is dominated by large coastal pelagic fish stocks (northern anchovy, Pacific sardine, jack mackerel, chub mackerel) and a demersal species, Pacific hake. Similar species of the same genera dominate the other major eastern boundary currents: the Peru, Canary, and Benguela Currents (Bakun, 1985, 1996). Relatively large interannual and interdecadal oscillations of stock sizes of these species present a challenging suite of scientific and social problems. Ichthyoplankton surveys designed to encompass the spawning distributions of these populations have become indispensable to scientists who study their dynamics and to fisheries managers given the task of conserving them. Additional benefits of these surveys are the vast amounts of

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information obtained on the physics and chemistry of the habitat, on the invertebrate zooplankton, and on the larvae of the other species that make up the ichthyofaunas of these regions. The larval fish assemblages in the California Current reflect the water masses of this complex region. The Northern Complex contains subarctic-transitional species that spawn primarily in the cold months. The Southern Complex consists of a relatively large group of California Current endemics and warm-water cosmopolites and another group of eastern tropical Pacific species. The Southern Coastal Complex consists of larvae of shorefishes that inhabit the large shelf areas of central and southern Baja California. Spawning in both southern complexes occurs primarily during warm months. The larval abundance of species in the Southern Complex increased during El Niño events and during the warm regime when their geographic distributions expanded northward and shoreward.

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F I G U R E 11-19 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Bathylagus wesethi in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

Continuing CalCOFI surveys will reveal whether or not the precipitous declines in larval abundances of Southern Complex species following the 1998 La Niña are harbingers of a shift from a warm to a cool ocean regime. Studies of the CalCOFI ichthyoplankton time series show the importance of midwater fishes to the ecology of the California Current region and suggest that they use a large proportion of the annual production of this system.

Nearshore Assemblages The coastal fishes of California, species whose distributions are centered over the continental shelf (shoreward of 200 m depth), comprise more than 400 species representing well over

100 families (e.g., Miller and Lea, 1972). Somewhat more than 200 marine species of somewhat fewer than 100 families have been recorded from California’s bays and estuaries (e.g., Horn and Allen, 1976). The coastal larval fish assemblage is dominated by Pacific sardine and herring (Family Clupeidae) and northern anchovy (Engraulidae); some other abundant coastal taxa are silversides (Atherinidae), croakers (Sciaenidae), and various flatfishes (Paralichthyidae and Pleuronectidae). Marine larval fish assemblages of the bays and estuaries are dominated by gobies (Gobiidae); examples of other common bay/estuarine taxa are herrings, several species of anchovies, silversides, sculpins (Cottidae), and blennies (Blenniidae, Chaenopsidae, and Labrisomidae). The oceanic, coastal, and bay/estuarine zones do not exist in isolation from one another and although each is characterized

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F I G U R E 11-20 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Diogenichthys atlanticus in the Southern

California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

by a distinct ichthyoplankton assemblage, many taxa that are most abundant in one zone also occur in adjacent zone(s). For example, larvae of some oceanic taxa such as Mexican lampfish and several bristlemouth species, which are most abundant
200 km and more than 400 km from shore, respectively (Moser et al., 1993), also occur relatively commonly in coastal waters (Walker et al., 1987; McGowen, 1993; Moser et al., 1993) and occasionally are taken in bays (Eldridge and Bryan, 1972). Eggs and larvae of northern anchovy are most abundant over the shelf but also occur in smaller numbers more than 400 km from shore (Moser et al., 1993) and may be moderately abundant in bays and estuaries as well (Eldridge, 1977; Allen et al., 1983; McGowen, 1993). Goby larvae such as the arrow goby, Clevelandia ios, among the most abundant of the bay/estuarine taxa (e.g., Eldridge, 1977; Leithiser, 1981;

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Allen et al., 1983), are relatively common along the open coast (Walker et al., 1987) but do not occur in the oceanic zone.

Coastal Assemblages Most of the studies that have focused on the Californian coastal ichthyoplankton as a whole have been conducted since the mid-1970s (most in the 1970s and 1980s) in the SCB (e.g., Barnett et al., 1984; Lavenberg et al., 1986; Walker et al., 1987; McGowen, 1993; Watson et al., 1999); thus, the following description of coastal ichthyoplankton assemblages, based on McGowen (1993), has a southern bias. Using cluster analyses (Sokal and Michener, 1958; Boesch, 1977) of ichthyoplankton collections between the 6–75 m isobaths along four

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F I G U R E 11-21 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Triphoturus mexicanus in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

widely spaced transects in the Bight, McGowen (1993) identified six assemblages of fish eggs and larvae (fig. 11-24, 11-25). Abundance patterns in the cross-shelf direction clearly were present, but indications of alongshore patterns within the SCB were weak or absent. The Genyonemus assemblage, consisting of white croaker (Genyonemus lineatus) larvae, northern anchovy eggs, and eggs and/or larvae of four flatfishes, sanddabs, California halibut (Paralichthys californicus), diamond turbot (Hypsopsetta guttulata), and hornyhead turbot (Pleuronichthys verticalis) (fig. 11-24A), was characterized as most abundant between about the 15–36 m isobaths throughout the Bight. Eggs of white croaker and California halibut were not included in McGowen’s analysis, but Watson et al. (1999), working in the northern SCB, showed that both occurred primarily shoreward of about the 60-m isobath, with peak abun-

dance between about the 20–30 m isobaths for white croaker and the 40–60 m isobaths for California halibut. Gruber et al. (1982), working in the southern Bight, used recurrent group analysis (Fager, 1957) to identify a small, nearshore (54 m bottom depth) group containing the larvae of white croaker and California halibut, with one affiliate, hornyhead turbot. Larval sanddabs were classified as affiliates of a cosmopolitan group, and diamond turbot was identified as an inshore taxon but was not included as a member or affiliate of a recurrent group. Sanddab larvae also are members and associates of a broadly distributed coastal recurrent group in the California Current system (fig. 11-7; Moser et al., 1987). Most of the members of Genyonemus do occur in small numbers seaward of the inner shelf region, and they are collected during CalCOFI ichthyoplankton surveys, where their abundances

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F I G U R E 11-22 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Vinciguerria lucetia in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

seem to track trends in the nearshore zone reasonably well (e.g., Moser and Watson, 1990; Moser et al., 2001b). McGowen’s (1993) coastal Stenobrachius assemblage included larval northern anchovy, northern lampfish, rockfishes, and bay goby (Lepidogobius lepidus), together with the eggs of California smoothtongue (fig. 11-24B). Members of this assemblage were characterized as most abundant seaward from the 36-m isobath, with no apparent alongshore pattern in the Bight. Gruber et al. (1982) placed northern anchovy, northern lampfish, and rockfish larvae in an offshore/cosmopolitan recurrent group, and larval northern lampfish and rockfish (as well as larval California smoothtongue) also are members of a California Current recurrent group of subarctictransitional species more likely to be found nearer the shore south of Point Conception than farther north (fig. 11-7; Moser

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et al., 1987). Larval northern anchovy also are members of a different California Current group (Citharichthys) but have reasonably strong affinities with the subarctic-transitional group (Moser et al., 1987). McGowen’s Sardinops egg assemblage contained Pacific sardine eggs and spotted turbot (Pleuronichthys ritteri) larvae (fig. 11-24C), and the Sardinops larvae assemblage contained Pacific sardine larvae and spotted turbot eggs (fig. 11-24E). Both assemblages were most abundant between the 22–36 m isobaths in the central Bight (McGowen’s study was conducted during the period when sardine spawning was largely restricted to the nearshore zone) and both extended farther seaward where they were collected during CalCOFI surveys. Larval Pacific sardine also are members of a broadly distributed coastal recurrent group in the California Current system

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F I G U R E 11-23 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Diogenichthys laternatus in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

(Moser et al., 1987). Gruber et al. (1982) classified the larvae of both Pacific sardine and spotted turbot as nearshore but included neither as a member or associate of a recurrent group. Paralabrax included the eggs and larvae of 14 taxa (fig. 11-25) of temperate–subtropical affinity, five subsets of two to six taxa each reflected primarily cross-shelf, and in one case alongshore, location. The largest subset, including larvae of kelp and sand basses (Paralabrax), blennies of the genus Hypsoblennius, California barracuda (Sphyraena argentea) eggs, bigmouth sole (Hippoglossina stomata) eggs and larvae, fantail sole (Xystreurys liolepis) larvae, and California tonguefish eggs, was most abundant between the 22–36 m isobaths; an alongshore pattern was not apparent in the Bight. California corbina (Menticirrhus undulatus) and California barracuda larvae were most abundant

in the same depth zone, primarily in the central Bight. Five species in two of the subsets, California lizardfish eggs, and basketweave cusk-eel, señorita (Oxyjulis californica), California sheephead, and California tonguefish larvae, were most abundant over a broad depth range between the 22–75 m isobaths. Larval blacksmith (Chromis punctipinnis) and Mexican lampfish were most abundant at the most seaward stations (75 m depth); there was no alongshore pattern in the Bight. Watson et al. (1999) found similar cross-shelf spawning locations for señorita and California sheephead but suggested a broader depth range, perhaps extending seaward to the vicinity of the 100-m isobath, for California barracuda. Gruber et al. (1982) included kelp and sand bass and Hypsoblennius larvae in a nearshore (shoreward of the 54-m isobath) recurrent group; Mexican lampfish was considered an offshore taxon but not

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FIGURE 11-24 Members of the

Genyonemus (A), Stenobrachius (B), Sardinops Egg (C), Goby (D), and Sardinops larvae (E) coastal ichthyoplankton assemblages of the Southern California Bight (McGowen, 1993). All illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained.

included as an associate or member of a recurrent group. Larval Mexican lampfish do belong to a broadly distributed temperate–subtropical recurrent group in the California Current. McGowen’s Synodus subset of Paralabrax was nearly the same as the California Current recurrent group Synodus, a group of temperate–tropical coastal taxa (Moser et al., 1987). The sixth SCB coastal assemblage (Goby) contained two types of undentified goby larvae (fig. 11-24D), probably mostly arrow goby and early stages of bay goby. Both were abundant shoreward of the 36-m isobath, primarily shoreward of the 22-m isobath. In the SCB, larval bay goby occur in small numbers at the most shoreward CalCOFI stations (e.g., Moser et al., 2001a), but larval arrow goby rarely occur as far seaward as the most inshore CalCOFI stations.

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Icanberry et al. (1978) conducted a 15-month ichthyoplankton survey at two stations (20-m and 60-m isobaths) off Diablo Canyon, central California. With one exception, the coastal ichthyoplankton assemblages described by McGowen (1993) from the SCB were not present off Diablo Canyon. Major elements of McGowen’s coastal Stenobrachius assemblage were present off Diablo Canyon, including larval northern lampfish, northern anchovy, and rockfish. Larval bay goby, another Stenobrachius member, were not identified in the Icanberry et al. study, but the species is present in the area and an unidentified gobiid larval type had a seasonal pattern similar to that of other members of the group. In addition, croakers (probably white croaker) and cabezon also had similar seasonal occurrence. Larval northern lampfish were most abundant at the offshore

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F I G U R E 11-25 Members of the Paralabrax coastal ichthyoplankton assemblage of the Southern California Bight (McGowen, 1993). All illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained.

station; abundances of northern anchovy, rockfishes, and croakers did not differ between the two stations. A group of larvae more or less analogous to McGowen’s Genyonemus assemblage included the hexagrammids, painted greenling (Oxylebius pictus), lingcod, and kelp/rock greenlings (Hexagrammos spp.), and three unidentified “Blennioidei” types (the category “Blennioidei” of Icanberry et al. probably included Zoarcoidei). This group had seasonal occurrence similar to Genyonemus, but unlike Genyonemus, its members may not have been concentrated at shallow depths in the coastal zone: the abundance of “Blennioidei” did not differ between the 20-m and 60-m stations. There were no obvious analogs to McGowen’s Sardinops or Paralabrax assemblages, and the Goby analog consisted of two sculpin taxa (Artedius

spp. and an unidentified type). Artedius larvae were most abundant at the inshore station. Little information is available concerning open coastal ichthyoplankton assemblages of northern California, but a study by Richardson and Pearcy (1977) off central Oregon that included coastal stations may serve as a proxy. They identified a coastal assemblage of 53 taxa that occurred over the shelf at stations 2–28 km from shore (primarily 2–18 km from shore, 20–85 m bottom depth). Thirteen taxa (fig. 11-26) accounted for 92% of the total larvae in the coastal assemblage; these tended to be most abundant 6–9 km from shore (46–59 m bottom depth). Richardson and Stephenson (1978) used cluster analysis of a summer subset of the same data to identify a smaller coastal assemblage that contained the larvae of nine

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F I G U R E 11-26 The 13 most abundant members of the central Oregon coastal ichthyoplankton assemblage (Richardson and Pearcy, 1977). Microgadus proximus from Matarese et al. (1981); Sebastes from Kendall (1989); Artedius sp. 1 ( A. harringtoni) and sp. 2 ( A. fenestralis), Cottus asper and Hemilepidotus spinosus from Richardson and Washington (1980); Isopsetta isolepis from Richardson et al. (1980a); Platichthys stellatus from Matarese et al. (1989); other illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained.

taxa including smelts (Osmeridae), Pacific tomcod (Microgadus proximus), butter sole (Isopsetta isolepis), sand sole (Psettichthys melanostictus), three unidentified sculpins (two Artedius and one Icelinus species), pricklebreast poacher (Stellerina xyosterna), and unidentified snailfish (Cyclopteridae) larvae. A separate analysis (Richardson and Stephenson, 1978) of a larger subset of coastal stations (2–18 km from shore) in all seasons, that included most of Richardson and Pearcy’s (1977) coastal assemblage, yielded two seasonal assemblages, one of 16 primarily (94%) coastal, spring–summer taxa that included all

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nine taxa of Richardson and Stephenson’s coastal assemblage, and a mixed coastal and offshore group (66% coastal) of 12 taxa that were most abundant in winter and spring. The remaining 20 taxa were not classified.

Coastal Assemblages—Geographic and Seasonal Distribution Seasonal spawning patterns are at least as important as cross-shelf location in structuring coastal ichthyoplankton

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F I G U R E 11-27 Quarterly maps showing mean larval abundance (number per 10 m2) from 1951 to 1984 in each of 22 CalCOFI regions (Moser et

al., 1993) for Genyonemus lineatus (Genyonemus assemblage of the coastal Southern California Bight; McGowen, 1993), Paralichthys californicus (Genyonemus), Sphyraena argentea (Paralabrax), Semicossyphus pulcher (Paralabrax), Ophidion scrippsae (Paralabrax), and Ophiodon elongatus (central California analog to Genyonemus assemblage of the coastal Southern California Bight).

assemblages. McGowen’s (1993) Southern California Bight Genyonemus assemblage was characterized as a winter–spring group. Based on a study near McGowen’s southernmost transect, Walker et al. (1987) also identified a winter–spring group that included larval white croaker (fig. 11-27A) but placed the other Genyonemus taxa in another group characterized as

being present year-round with highest abundance in winter and spring. The nearshore group of Gruber et al. (1982), which contained larval white croaker and California halibut, was identified as an autumn through spring group, and another Genyonemus member, larval sanddabs, was classified as an affiliate of a winter through summer group. Watson et al.

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(1999) collected white croaker eggs during late winter/spring and reported highest abundance during that period for eggs of three Genyonemus group flatfish species (speckled sanddab, California halibut, and diamond turbot) but noted that speckled sanddab and California halibut continued to spawn at lower levels during summer. Moser and Watson (1990) showed that California halibut spawns year-round, with a peak in late winter/spring and smaller increases in midsummer and autumn (fig. 11-27B). A principal spawning peak during late winter/spring in the northern part of its range is somewhat unexpected, given the warm-water affinity of California halibut; it may reflect an adaptation to the microzooplankton production cycle along the California coast (Moser and Watson, 1990). The members of Genyonemus are coastal, warm-water taxa broadly distributed from central California to the central or southern Baja California Peninsula, essentially the San Diegan faunal Province (e.g., Hubbs, 1960), but extending into the Oregonian Province to the north. In most cases, abundance is centered in the warmer waters south of Point Conception (figs. 11-27A,B; also see CalCOFI Atlas 31, pp. 6, 118, and Moser et al., 1994a: CalCOFI Atlas 32, p. 80). Like Genyonemus, the Stenobrachius coastal assemblage was characterized as a primarily winter–spring group but with broader seasonal occurrence. Walker et al. (1987) placed larval northern lampfish in a winter–spring group, but classified the remaining Stenobrachius larvae (together with most of the Genyonemus larvae) in a separate group described as present year-round with highest abundance in winter and spring. Gruber et al. (1982) placed larval northern anchovy, northern lampfish, and rockfishes in a winter through summer recurrent group, and Moser et al. (1987) described the last two as primarily autumn through spring taxa. Geographic distributions of most of the Stenobrachius larvae are described above under CalCOFI Assemblages. The Sardinops egg and larvae assemblages were present throughout the year in the coastal zone with highest abundance in spring and autumn, suggesting a bimodal spawning season. Walker et al. (1987) described the larvae of both species as belonging to a group of year-round spawners with winter–spring peak abundance, and Gruber et al. (1982) characterized the larvae of both as most abundant in autumn. Seasonal and geographic distributions of larval Pacific sardine in the larger CalCOFI study area are described above under CalCOFI assemblages; sardine eggs, not surprisingly, are distributed seasonally and geographically much like the larvae (CalCOFI Atlas 31, p. 22; fig. 11-12B), except that the eggs are relatively more abundant in spring. Larval spotted turbot in CalCOFI collections typically are most abundant from midsummer to autumn along the central Baja California Peninsula, especially in the vicinity of Sebastian Viscaino Bay, reflecting the extensive adult habitat available there (CalCOFI Atlas 31, p. 226). McGowen (1993) characterized the Paralabrax assemblage taxa as summer–autumn spawners; larval kelp/sand bass, Hypsoblennius spp., and bigmouth sole were most abundant in summer, and the others were abundant in both summer and autumn. Walker et al. (1987) included larvae of eight of the Paralabrax taxa in their analysis, classifying six as summer spawners and two, Hypsoblennius spp. and Mexican lampfish, as spring–summer spawners. On the other hand, Gruber et al. (1982) described larval Mexican lampfish, kelp/sand bass, and Hypsoblennius spp. as most abundant in summer and autumn. Seasonal and geographic distributions of some Paralabrax group taxa are described above under CalCOFI Assemblages:

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Mexican lampfish (CalCOFI Atlas 31, p.16), lizardfishes (CalCOFI Atlas 31, p. 54), basketweave cusk-eel (fig. 11-27E), and tonguefishes (CalCOFI Atlas 31, p. 72). Larvae of several of the Paralabrax shorefish taxa occur in small numbers farther offshore into the CalCOFI sampling area; all of these occurred primarily from Point Conception southward to central or southern Baja California Sur with peak abundance in summer or autumn, usually off the Baja California Peninsula (figs. 11-27C, D; CalCOFI Atlas 31, pp. 66, 102, 110, 124, 140, 210). The Goby coastal assemblage of two undentified larval types occurred year-round with no dominant seasonal pattern, although it did display some tendency toward higher larval abundance in winter and spring (McGowen, 1993). Walker et al. (1987) included both arrow and bay gobies, the species most likely represented by the Goby assemblage, in a group of year-round spawners with peak larval abundance in winter and spring, and in the SCB, larval bay gobies are collected year-round with highest abundance from autumn through spring, at inshore CalCOFI stations (Moser et al., 2001a). In central California, the group of larvae analogous to McGowen’s Stenobrachius assemblage (northern anchovy, northern lampfish, rockfishes, unidentified croaker, and goby larvae that may have been white croaker and bay goby) were collected through much or all of the year with highest abundances in winter and spring (Icanberry et al., 1978). Larvae more or less analogous to McGowen’s Genyonemus assemblage (painted greenling, lingcod, kelp/rock greenlings, “Blennioidei”) were collected mostly or entirely during winter in central California (Icanberry et al., 1978). Small numbers of larvae of all four taxa have been collected during CalCOFI surveys; within the larger survey area, all were most abundant in the coastal zone off central or northern California in winter (fig. 11-27F; CalCOFI Atlas 32, pp. 46, 48, 84), reflecting their subarctic–warm temperate affinities. The central California Goby analog consisted of two sculpin taxa that were collected year-round with no clear seasonal pattern. Larvae of most sculpin species occur relatively infrequently and in low abundance in CalCOFI collections; larvae of the family as a whole occur year-round in the CalCOFI survey area but are most abundant from late winter through late spring with highest abundance in the coastal zone of northern California (Moser et al., 1993), reflecting their cool-water (Oregonian) affinity. Larvae of nine of Richardson and Pearcy’s 13 most abundant central Oregon coastal taxa have been identified from CalCOFI surveys in sufficient numbers to map their larger scale distributions (CalCOFI Atlas 31, pp. 12, 84, 86; CalCOFI Atlas 32, pp. 6, 20, 42, 70, 118, 128). Within the CalCOFI area, all nine were most abundant in the coastal zone off central or northern California, with winter or spring abundance peaks.

Coastal Assemblages—Interannual and Decadal Changes Responses to ENSO events and the 1976 to 1977 regime shift varied among taxa of the Genyonemus assemblage of SCB coastal taxa. California halibut showed no change in distribution, relatively little difference in abundance between the cool and warm regimes, and no consistent response to ENSO episodes (fig. 11-28A–C). The somewhat higher overall average larval abundance apparent during the warm regime was largely attributable to very high abundance in 1981; apart

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F I G U R E 11-28 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Paralichthys californicus in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

from that year, annual mean abundances differed little between the cool and warm regimes (fig. 11-28C). The interannual differences in larval abundance are well correlated with commercial landings of California halibut through most of the CalCOFI time series, suggesting that larval abundance reflects adult abundance and that larval surveys could be used as a fishery-independent tool in managing the California halibut fishery (Moser and Watson, 1990). Among the other Genyonemus members, white croaker displayed fluctuating larval abundance with a general declining trend since at least the late 1980s and a tendency for larval abundance to decline more during El Niño events. Larval Pacific and speckled sanddabs, and hornyhead turbot were more abundant, on average, during the warm regime than during the cool regime.

Both sanddab species tended to decline in larval abundance during El Niño events and, from the late 1980s to the late 1990s, larval speckled sanddab and hornyhead turbot declined to abundance levels comparable to those of the cool regime. Abundance increased rapidly after 1999 for both sanddab species but changed little for hornyhead turbot. Larval diamond turbot, like California halibut, showed little evidence of ENSO- or PDO-related change in abundance or distribution (Moser et al., 2001a) but gradually declined in abundance in CalCOFI collections and reached zero by 1998. Among the Stenobrachius group of coastal SCB larvae, interannual and decadal-scale changes are described under CalCOFI assemblages for northern anchovy (figs. 11-13, 11-14), northern lampfish (fig. 11-15), and two of the rockfish species

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F I G U R E 11-29 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Sphyraena argentea in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

(figs. 11-17, 11-18); the remaining species, bay goby, showed variable but generally declining larval abundance in CalCOFI collections since 1985 but no relationship between ENSO events and abundance. Larval spotted turbot of the coastal Sardinops egg assemblage were more abundant, on average, and were more or less evenly distributed inshore throughout the entire SCB during the warm regime, in contrast to the cool regime when they were largely concentrated in the southern part of the Bight (Moser et al., 2001a). This is consistent with their summer–autumn abundance peak and the warm-water affinity of the adults. However, larval abundance trends within the SCB apparently are unrelated to ENSO events. Larval California barracuda of the Paralabrax assemblage provide an example of ENSO and PDO effects on warm-water,

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summer spawners of coastal SCB. Larval California barracuda increased in abundance through the warm regime, and their distribution along the coast shifted northward, from highest abundance in the south with no occurrences from Point Conception northward during the cool regime, to highest abundance in the central and northern Bight with some occurrences north of the Bight in the warm regime (fig. 1129A,B). Larvae tended to be more abundant during El Niño events, although a direct relationship is far from clear, and at least during the warm regime, abundance tended to peak at about 4-year intervals (fig. 11-29C). Fantail sole showed essentially the same trends (fig. 11-30), increased abundance and larval distribution spreading northward during the warm regime (fig. 11-30A,B), increased abundance during El Niño

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F I G U R E 11-3 0 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Xystreurys liolepis in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

events, and decreased abundance during La Niña events (fig. 11-30C). Spawning is primarily in late summer and autumn (fig. 11-30D), when the water is warmest. This pattern contrasts sharply with that of California halibut (fig. 11-28), another paralichthyid flatfish, and reflects the more tropical affinity of fantail sole. A final example of PDO and ENSO effects on larval abundance and distribution of a shorefish species with tropical–subtropical affinity is provided by California lizardfish. Again, larval abundance increased, and the alongshore distribution extended northward during the warm regime (fig. 11-31A,B), but in this case, larval abundance and ENSO events were not closely coupled (fig. 11-31C). Larval abundance peaked in the early 1990s and subsequently declined to levels not much higher than those of the cool

regime. The remaining coastal Paralabrax taxa also increased in larval abundance during the warm regime, except for blacksmith and California tonguefish which changed little. In contrast to the examples above, most of the other Paralabrax taxa displayed only small changes in alongshore distributions, with slight increases in abundance in the northern SCB and/or to the north of the SCB during the warm regime (Moser et al., 2001a). The California tonguefish was unusual in that its larval distribution contracted southward during the warm regime—opposite what one would expect based on its warm-water affinity. Four Paralabrax taxa in addition to California lizardfish, (kelp/sand bass, blacksmith, señorita, bigmouth sole) declined in abundance beginning in the mid1980s to early 1990s and reached levels comparable to those

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F I G U R E 11-31 Interannual and decadal scale changes in larval abundance (number per 10 m2) of Synodus lucioceps in the Southern California Bight (Moser et al., 2001a). A: map of mean abundance at CalCOFI stations during the cool regime; B: map of mean abundance at CalCOFI stations during the warm regime; C: mean annual abundance relative to PDO and ENSO events (El Niño: shaded; La Niña: hatched; the wide, hatched bar from 1970 to 1976 represents three closely spaced La Niña events); D: mean monthly abundance.

of the cool regime by the late 1990s (Moser et al., 2001a). In addition to California barracuda and fantail sole, three other Paralabrax species (blacksmith, California sheephead, bigmouth sole) displayed some tendency for larval abundance to peak during or just after El Niño events, although in all three cases there also were mismatches between abundance peaks and warming events (Moser et al., 2001a).

Coastal Assemblages—Summary The results of the various coastal ichthyoplankton studies in the SCB agreed generally with regard to patterns of seasonal and spatial distributions of the ichthyoplankters but differed to some degree in the details of the temporal and spatial patterns

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of individual taxa. They also differed in the allocation of some taxa to the various coastal ichthyoplankton assemblages. These interstudy differences resulted primarily from differences in sampling and analytical methodologies. In general, seasonal abundance patterns that have been recognized in all SCB studies reflect spawning primarily during winter–spring (cool water), summer–fall (warm water), or more or less evenly throughout the year with interannual variation of up to a few weeks in initiation and termination of spawning. About twothirds of the coastal fishes in the SCB are planktonic spawners and most have distinct seasonal patterns of highest larval abundance; evidence for more even year-round spawning among the coastal taxa appears to be largely limited to some of the inner shelf demersal spawners. Horizontal spatial patterns within the Bight are primarily cross-shelf rather than along-

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shore, probably reflecting the relative magnitudes of cross-shelf and alongshore flow in the SCB: coastal currents are primarily alongshore and cross-shelf transport is relatively weak. The central California coastal larval fish assemblage reflects a higher proportion of demersally spawning taxa (about 60% of the oviparous species) but as in the SCB, more or less even spawning throughout the year may be largely limited to some of the inshore demersal spawners. Larvae that hatch from demersal eggs typically are larger, more developed, and more competent in the first days after hatching than larvae that hatch from small planktonic eggs. The much higher proportion of demersally spawning coastal taxa may reflect more vigorous coastal circulation off central California, especially stronger upwelling (Parrish et al., 1981), compared with the SCB. The majority of central Californian coastal fishes apparently spawn principally during winter and spring, before or during the principal upwelling period. The majority of coastal larvae appear to be broadly distributed across the shelf, perhaps reflecting upwelling during some part of their period of high abundance. Off Oregon, 87% of the coastal assemblage fish larvae are of demersal spawners. Here, most coastal fish larvae occur between late winter and early summer, typically primarily before and/or after the spring upwelling period. The majority apparently tend to be most abundant in the inner to midshelf zones. Larval abundances and distributions of coastal taxa in the SCB, where the most complete time series is available, tended to respond to ENSO and PDO events as would be predicted based on adult zoogeographic affinities. Larvae of warm-water taxa tended to be more abundant, higher abundance extended farther north during the warm regime, and they tended to become more abundant during ENSO warm events and/or less abundant during cool events. Cool-water taxa tended to display the opposite patterns. These were most apparent for taxa with the strongest warm- and cool-water affinities; taxa whose ranges are centered in or near the SCB had less apparent responses (or none at all) to ENSO and PDO events.

Bay and Estuarine Assemblages Bay and estuarine habitats are quite limited on the Pacific coast. They account for only about one-fifth of the total coastline (Emery, 1967), and their ichthyoplankton assemblages typically are small compared with those of the more extensive bay and estuarine systems of the Atlantic and Gulf coasts. Larval fish assemblages of Californian bays and estuaries typically are composed predominantly of resident species (fig. 11-32), often with relatively small contributions from open coastal species. In southern California, the larval fish assemblages (fig. 11-32A) typically are dominated by gobies (Leithiser, 1981; Snyder, 1965; McGowen, 1977; White, 1977; Nordby, 1982; and Edmands, 1983, all cited in McGowen, 1993);
60–90% of the total larvae is some combination of longjaw mudsucker (Gillichthys mirabilis), arrow goby, cheekspot goby (Ilypnus gilberti), and shadow goby (Quietula y-cauda) (reliable diagnostic characters were unavailable during most of the studies cited above and thus larvae of the last three species commonly were incompletely distinguished or were not distinguished in those studies). Silversides typically contribute another
5–10% of the total larvae, topsmelt (Atherinops affinis) is probably the most common species. Anchovies commonly account for
1–5% of the total larvae but can be the dominant taxon, contributing more than half the total (e.g., Allen et al., 1983). Any or all of the nonresident

northern anchovy and two resident Anchoa species may be present. Blenniids (Hypsoblennius spp.) typically contribute another 1–3% of the total. These four families typically account for 85% (often
95%) of the fish larvae collected in the bays and estuaries of southern California. All except the anchovies are demersal spawners. The blennies and gobies spawn year-round, usually with higher larval abundance in the spring to autumn period. Topsmelt spawns from spring through early autumn (larvae of the spring–summer spawning California grunion, Leuresthes tenuis, and especially the winter–spring spawning jacksmelt, Atherinopsis californiensis, also may occur in bays and estuaries), and the Anchoa species are summer spawners. Apart from northern anchovy and Hypsoblennius spp., these taxa are uncommon to rare as far from shore as the inshore CalCOFI stations (e.g., Moser et al., 1993, 1994a). As in southern California, goby larvae are an important component of the central and northern Californian bay and estuarine ichthyoplankton (fig. 11-32B,C). They occur yearround with higher abundance in summer and autumn and contribute somewhat less than half to more than 90% of the total larvae (Eldridge and Bryan, 1972; Eldridge, 1977; Yoklavich et al., 1992; G. M. Cailliet and E. Grannis, pers. commun., October 2002). Longjaw mudsucker and arrow goby are important components of the central California larval goby assemblage, and bay goby becomes an important member of the assemblage in northern California and Oregon (Eldridge and Bryan, 1972; Pearcy and Myers, 1974) where cheekspot and shadow gobies drop out. Pacific herring (Clupea harengus) is an important seasonal component of the central and northern Californian and Oregonian bay/estuarine larval fish assemblages, where it can account for half or more of the total larvae in winter and spring. In central California, northern anchovy may contribute up to about a quarter of the total bay/estuarine fish larvae, but in northern California and Oregon, it becomes only a very minor component of the bay/ estuarine ichthyoplankton (Pearcy and Myers, 1974; Eldridge, 1977; Misitano, 1977; Yoklavich et al., 1992). Sculpins usually are minor components of southern Californian bay and estuarine ichthyoplankton but can contribute on the order of 5% of the total in central California during winter and spring and can become important contributors to total larval abundance during winter and spring in northern California and Oregon. Osmerid smelts may account for up to
5–10% of total fish larvae during winter and spring in central and northern California. Both families spawn demersally. In the estuaries and bays generally, ichthyoplankton species richness typically is highest and the proportion of the eggs and larvae that are of coastal species typically is greatest toward the mouth. In the interiors of the bays and estuaries, ichthyoplankton typically is composed predominantly of resident species. Some coastal fishes, primarily flatfishes, use estuaries as nursery areas (e.g., Pearcy and Myers, 1974; Misitano, 1976, 1977; Krygier and Pearcy, 1986; Boehlert and Mundy, 1987, 1988; Gunderson et al., 1990; Kramer, 1991; Yoklavich et al., 1992), and juveniles may be found far into the interior, although spawning and most or all of larval development is in open coastal waters.

Bay and Estuarine Assemblages—Summary The most abundant bay and estuarine fish larvae are predominantly of demersally spawning species. Because typically they are larger and more competent early in larval life than

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F I G U R E 11-32 Characteristic taxa of bay and estuarine larval fish assemblages of (A) southern California, (B) central California, and (C) north-

ern California. Most illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained; Anchoa spp. from Caddell (1988), Atherinops affinis and Clupea pallasi from Matarese et al. (1989), and Cottidae from Richardson and Washington (1980).

the larvae of planktonic spawners, they may be better able to resist or avoid transport out of the bay/estuarine environment during the early larval period than larvae hatched from planktonic eggs. In addition, the larvae of resident demersal spawners especially tend to be dominant in the bay and estuarine interiors, where less dynamic tidal water exchange may further facilitate larval retention. In southern California the most abundant larvae are gobies, anchovies, silversides, and blennies. To the north, goby larvae may be somewhat reduced in relative abundance, but they remain an important compo-

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nent of the ichthyoplankton and may be dominant in some cases. Anchovies also may be reduced in relative abundance in central California, and they are a minor component of the northern ichthyoplankton. Silversides and blennies become minor components of the bay/estuarine ichthyoplankton in central California and are absent to the north. Clupeids are added as a seasonally important component of both the central and northern assemblages, sculpins increase in relative abundance in central and northern California, and smelts are an important winter–spring taxon in central and northern

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California. Resident species typically contribute the largest fraction of total ichthyoplankton in the interiors of bays and estuaries; coastal taxa typically occur primarily nearer the estuary and bay mouths.

Vertical Distribution Ahlstrom (1959) analyzed 22 discrete depth samples taken on nine cruises during a 14-year period off southern California and Baja California and found that most planktonic fish eggs and larvae occurred in the upper part of the water column that includes the upper mixed layer and thermocline. Further, he determined that species occupied different strata within the upper water column and that the limits of these strata varied in relation to the upper mixed layer depth. The highly productive coastal pelagic species have shallow distributions generally limited to the upper 50 m of the water column. Ahlstrom (1959) found that
80% of Pacific sardine larvae occurred in the upper 48 m, and in an earlier study (Ahlstrom, 1954) he found 93% of their larvae in the 0–42 m stratum. Sardine eggs were similarly distributed. Vertical distributions of eggs and larvae of northern anchovy and associated species were analyzed from 104 discrete depth tows taken at two sites off southern California in March 1980 (Moser and Pommeranz, 1999). Northern anchovy eggs were slightly shallower than larvae (
95% vs. 90% in the upper 30 m); peak egg concentration occurred at the surface and peak larval occurrence was in the 10–20 m stratum. Boehlert et al. (1985) found northern anchovy larvae at even shallower depths at a midshelf site off Newport, Oregon. Larvae were restricted to the upper 10 m with about equal concentrations in the 0–5 and 5–10 m strata. Hunter and Sanchez (1976), examining Ahlstrom’s (1959) data on northern anchovy distribution, found that larvae

12 mm occurred at the surface only at night and proposed that postflexion larvae migrate to the surface at night to fill their air bladders and float with little energy expenditure during nonfeeding hours. This hypothesis was supported by Brewer and Kleppel (1986) who found anchovy larvae
12 mm at the surface exclusively at night in Santa Monica Bay, California. Two other coastal pelagic species, chub and jack mackerel, also have shallow distributions. Ahlstrom (1959) found 80% of jack mackerel larvae above 80 m and 80% of chub mackerel larvae above 23 m; eggs of the two species have similar distributions. Moser and Smith (1993) found somewhat broader depth distributions for these species in a series of MOCNESS samples taken at the Ensenada Front at the southwest corner of the SCB, although peak concentrations of both species were in the 25–50 m stratum. Shallow distributions typically are found for shorefish eggs and larvae. For example, Ahlstrom (1959) found that
80% of labrid larvae and all of the California barracuda and blacksmith larvae occurred in the upper 10 m. At CalCOFI station 90.26, over the continental slope, Moser and Pommeranz (1999) found that larvae of white croaker, California pompano (Peprilus simillimus), queenfish (Seriphus politus), and California halibut occurred primarily in the upper 30 m with peak concentrations for the first two species in the 10–20 m stratum and in the 0-10 m stratum for the last two. On the shelf, white croaker, queenfish, and other croakers become epibenthic soon after hatching, some while still in the yolk-sac stage (Schlotterbeck and Connally, 1982; Barnett et al., 1984; Brewer and Kleppel, 1986; Jahn and Lavenberg, 1986). Late-stage and transforming California halibut larvae migrate to the neuston

where they may be carried shoreward for settlement by onshore winds and by surface slicks generated by tidally forced internal waves (Shanks, 1983, 1986; Moser and Watson, 1990). Larvae of other abundant demersal fishes such as
60 species of rockfishes are found somewhat deeper in the water column, although still within the zone that includes the mixed layer and thermocline. In Ahlstrom’s (1959) samples, 97% of the rockfish larvae occurred at depths shallower than 80 m and 75% of the larvae were between 25 and 80 m (Moser and Boehlert, 1991). In the Moser and Pommeranz (1999) study, 90% of the rockfish larvae were in strata shallower than 80 m; however, at their slope station, highest densities were in the 20–30 m stratum and in the neuston, whereas their offshore station had no larvae in neuston samples and the highest larval concentrations were in the 40–80 m stratum. Boehlert et al. (1985) found an even shallower distribution over the shelf at Newport, Oregon, apparently related to a shallow thermocline (30 m); 95% of the rockfish larvae occurred above 40 m and 70% were within the 5–30 m depth range (Moser and Boehlert, 1991). Off central California, Sakuma et al. (1999) found highest catches of postflexion rockfish larvae in the 0–40 m stratum during the day and in the 20–60 m stratum at night, with peak catches in the 20–40 m stratum. Larvae of postflexion shortbelly rockfish, S. jordani, were more evenly distributed with slightly elevated catches in the 20–40 m and 60–90 m strata during the day and fairly uniformly elevated catches in strata from 20–90 m during the night. Sakuma et al. provided evidence of vertical diel movement and confirmed the finding of previous investigators that the rockfish larvae do not occur below the thermocline. Pacific hake is an abundant demersal species whose larvae occur within or below the thermocline. Ahlstrom (1959) found that only 5% of hake larvae occurred between the surface and 48 m and that the average center of abundance was at 72 m. Similarly, Mullin and Cass-Calay (1997) found the largest fraction of hake larvae at 50–75 m, with slightly lower concentrations in the 75–100 m stratum; Moser and Pommeranz (1999) found highest concentrations in the 40–80 m stratum. Hake eggs occurred in relatively high concentrations in strata from 50–150 m, with peak concentrations at 75–100 m (Moser et al., 1997). Larvae of four species of sanddabs occur commonly in the California Current region and have wide vertical distributions that can extend below the thermocline (Ahlstrom, 1959; Moser and Pommeranz, 1999). Sakuma et al. (1999) found that postflexion larvae of Pacific sanddab were most abundant at 60–90 m during the day and 40–60 m during the night, whereas larval speckled sanddab were most abundant at 60–90 m during the day but at 20–40 m at night, providing evidence for diel migration through the pycnocline. Larvae of midwater fishes occupy a wide range of vertical habitats in the California Current region. Larvae of Pacific lightfish are found at relatively shallow depths, primarily from the surface to
125 m, with a maximum concentration at 50–75 m depth (Moser and Smith, 1993). Larvae of species in the two major subfamilies of myctophids have contrasting vertical distributions; lampanyctine larvae occupy relatively shallower strata than larvae of myctophines (Moser and Smith, 1993). Within the lampanyctines, northern lampfish larvae range from near surface to 200 m with peak abundance in the 20–40 m stratum (Ahlstrom, 1959; Moser and Pommeranz, 1999). Dogtooth, broadfin, and Mexican lampfish, and California headlightfish (Diaphus theta) have similar overall distributions with peak concentrations at 25–50 m, 25–50 m, 50–75 m, and 50–75 m, respectively (Moser and

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Smith, 1993). Among the myctophines, larvae of California, longfin, and blue lanternfish were captured as deep as
300 m, with upper ranges of 25 m, 50 m, and 75 m and peak concentrations at 100–125 m, 75–100 m, and 125–150 m, respectively. California flashlightfish larvae were deeper in the water column, ranging from 175–500 m with a peak at 200–225 m. The vertical distributions of the larvae of the two myctophid subfamilies are in sharp contrast to the distributions of the adults: adult myctophines generally have shallower distributions compared to adult lampanyctines and are stronger vertical migrators, often coming to the surface at night. The fact that the larvae and adults of each subfamily are effectively separated vertically may be an adaptation that results in reduced mortality from cannibalism (Moser and Smith, 1993). The deepest known larval vertical distributions in the California Current region are found in argentinoids and sternoptychids. Larvae of the bathylagids, California smoothtongue and popeye and snubnose blacksmelt, are found mainly within and below the thermocline, to 300 m, with highest abundance in strata between 50 m and 200 m (Ahlstrom, 1959; Moser and Smith, 1993; Moser and Pommerz, 1999). Eggs of California smoothtongue have a somewhat wider vertical distribution than larvae, from the surface to
300 m, with highest concentrations in the same depth zone or slightly shallower, between 50–100 m (Ahlstrom, 1959). Larvae of an argentinoid, dusky pencilfish (Microstoma spp.), range from 150–850 m with highest concentrations from 200–400 m, below depths sampled quantitatively by CalCOFI bongo tows (Moser and Smith, 1993). Larvae of the hatchetfish genus Argyropelecus occur even deeper in the water column. They were the dominant taxon in closing net tows taken at 131–262 m on the NORPAC Expedition (Ahlstrom, 1959). Moser and Smith (1993) found Argyropelecus larvae in strata from 300–1000 m, at the Ensenada Front in July; another sternoptychid, bottlelight (Danaphos oculatus), had a similar distribution in those samples. The surface zone, or neuston, is inhabited by the early life stages and adults of a large array of fish species; eggs and larvae of some occur throughout the upper water column, whereas those of others are found exclusively in surface waters and have evolved special adaptations for life in that zone (Moser, 1981; Moser et al., 2001b,c). Use of the term “neuston” for surface-living marine organisms is controversial because it was applied originally by Naumann (1917) to organisms associated with the surface film in freshwater habitats. Banse (1975) reviewed the evolution of the term, which is now used by most workers in referring to the uppermost (upper
10–20 cm) layer of the sea and to the assemblage of organisms that lives in that zone, either permanently or facultatively (Moser et al., 2001b,c, 2002). Obligate neustonic larvae have evolved independently in a variety of phylogenetic lineages of marine fishes. Most prominent are the beloniforms (flyingfishes, halfbeaks, needlefishes, sauries) where juveniles and adults also occupy the surface zone. In the California Current region, neustonic larvae have evolved within the atheriniforms (e.g., topsmelt, grunion), scorpaeniforms (e.g., sablefish, lingcod, greenlings, cabezon and some other sculpins), within a variety of perciform families, such as the carangids (e.g., yellowtail, pompanos), coryphaenids (dolphinfish), and istiophorids (billfishes), and the pleuronectiforms (turbots of the genus Pleuronichthys). Sablefish (Anoplopoma fimbria), a demersal species of the continental slope, has a complex ontogeny that includes neustonic larvae and deeply distributed planktonic

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eggs. Off central California, egg distributions ranged from 160–800 m depth with highest concentration between 240–400 m (Moser et al., 1994b). McFarlane and Beamish (1992) hypothesized from laboratory experiments that newly hatched yolk-sac larvae sink to
1000 m and then ascend gradually to the surface during about a 40-day period. Larvae are 8–9 mm when they reach the surface and rapidly accrue the heavy melanistic pigment characteristic of the neustonic stage (Kobayashi, 1957; Ahlstrom and Stevens, 1976; Kendall and Matarese, 1987; Doyle, 1992b; Moser et al., 1994b). Growth is rapid, up to 2 mm/day (Boehlert and Yoklavich, 1985), supporting the general notion that the neuston is a favorable habitat for growth and survival for species that have adapted to its special requirements.

Life History Ichthyoplankton Specializations Marine ichthyoplankters have evolved a large array of specializations in morphology, pigmentation, behavior, and physiology that contribute to their survival in the demanding epipelagic environment. Fascination with these life stages began when the early researchers first observed them under the microscope and continues today as our knowledge of their remarkable characteristics grows. For some of these (e.g., general transparency of eggs and larvae, heavy melanistic pigmentation and firm body structure in neustonic larvae, superficial neuromasts present in newly hatched marine larvae) their adaptive value is obvious; for others, adaptive significance is suggested by their frequency of appearance in disparate phylogenetic lineages (Moser, 1981; Govoni et al., 1984; Webb, 1999). Knowledge of the possible functions of these morphological specializations has been limited to the realm of speculation, owing to the difficulty in culturing marine fish larvae, particularly highly specialized ones, and the lack of opportunities to study them in experimental aquaria. Nonetheless, the specialized features of fish eggs and larvae provide a useful suite of taxonomic characters for workers in the growing fields of ichthyoplankton ecology and population monitoring, who have established a large fund of basic knowledge for the investigators who eventually will observe these larvae in laboratory cultures or directly in the sea. In this section, we discuss a few of the more interesting examples of morphological specialization in ichthyoplankton. For detailed information on ichthyoplankton taxonomy of the California Current region, see Matarese et al. (1989) and CalCOFI Atlas 33 (Moser, 1996). The Ahlstrom Symposium (Moser et al., 1984) summarized worldwide knowledge of teleost ontogeny and focused on its potential contribution to systematic investigations. Kendall and Matarese (1994) summarized the status of the descriptions of marine teleost life histories, including the many identification guides that had been published up to that time. An identification guide to ichthyoplankton of the western central North Atlantic is being prepared (Richards, in press). Recent guides to the fish larvae of the Indo-Pacific regions also are available (Neira et al., 1998; Leis and Carson-Ewart, 2000). Relevant information is presented in Webb’s (1999) chapter on developmental and evolutionary aspects of fish larvae and in other chapters in Hall and Wake (1999). The maximum size of most marine fish larvae ranges from
10–20 mm; however, larvae of some species attain considerably larger sizes and, in some species, transformation occurs at

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sizes 10 mm. The largest larvae are found in eels; the notacanthiform Leptocephalus giganteus attains a length of almost 2 m (Nielsen and Larsen, 1970), and the larva of the anguilliform Thalassenchelys coheni attains a length of 30 cm (Smith, 1979) and a weight of
20 gm (Moser, 1981). Large size in marine fish larvae is associated with extended planktonic life, best illustrated by the European eel (Anguilla anguilla). The work of Schmidt (1932) showed that adult eels migrate from European rivers to the Sargasso Sea where they reproduce; then, the developing larvae are carried back to Europe by the North Atlantic Current, a journey that lasts 2–3 years, and the larvae attain a length of
75 mm. The range of sizes among flatfishes is greater than in any other group of marine teleosts (Moser, 1981). Larvae of Mazatlan sole (Achirus mazatlanus) hatch at 1.3–1.6 mm and transform within a size range of 2.8–4.7 mm (Ortiz-Galindo et al., 1990). California halibut transform at 7.5–9.4 mm (Oda, 1991). In contrast, larvae of some flatfishes attain large sizes; for example, Dover sole (Microstomus pacificus) may reach
60 mm and remain planktonic for 1–3 years (Toole et al., 1993; Butler et al., 1996), and rex sole (Glyptocephalus zachirus) larvae up to
70 mm long have been reported (Pearcy et al., 1977). Small size and short larval life in shallow-living shelf species such as California halibut or the estuarine Mazatlan sole reduce the dispersal of their planktonic larvae away from bottom habitat appropriate for settlement (Moser, 1981). Extension of the planktonic phase through sustained growth in deep-living species such as Dover sole permits maximum dispersal of the population and increases the probability of successful settlement following shoreward and bottomward drift or migration (Moser, 1981). Also, the existence of overlapping multiple year-classes of pelagic larvae may be a causal factor in the relatively small interannual recruitment variability characteristic of this species. A recurring theme in larval fish morphology is the enlargement or elongation and proliferation of anatomical structures (e.g., finfold, gut, eyes, head spines, fin spines, and soft tissue) (figs. 11-33–11-36). Enlarged or voluminous finfolds are characteristic of several groups (e.g., anglerfishes, snailfishes, tetraodontiforms) (e.g., figs. 11-33D, 11-34B). Moderate extension of the gut, where it is trailing free from the body, occurs, for example, in some congrid leptocephali (Castle, 1984), in some stomiiforms (e.g., Ichthyococcus), and in the golden lanternfish (Myctophum aurolaternatum) (fig. 11-35D; Moser, 1981). In other stomiiforms (e.g., Eustomias, some astronesthines and malacosteines), the trailing gut may exceed the body length and develop a prominent pigment pattern and/or elaborate ornamentation (fig. 11-35A, E, G; Moser, 1981, 1996; Kawaguchi and Moser, 1984). Usually, the trailing gut is broken off in net-caught specimens but in a hand-caught, unidentified malacosteine larva, the intact gut was five times the length of the body (fig. 11-35G; Moser, 1981). In some neobythitine ophidiiform “exterilium” larvae, the gut is extended as a loop and may be ornamented with pigmented finger-like extensions and an arborescent appendage, reminiscent of siphonophore structures (fig. 11-35J; Fraser and Smith, 1974; Moser, 1981). A looped gut extension occurs also in some cynoglossid flatfishes (fig. 11-35I; Ahlstrom et al., 1984). Elongate fin rays are found commonly in marine fish larvae. In some taxa, most of the soft or spinous rays in the median or paired fins are elongate (e.g., Bathysaurus, Physiculus, Nannobrachium hawaiiensis, Sebastes paucispinis, gempylids; fig. 11-34). In other taxa, one or more rays of the median or paired fins are elongate and, in the case of spinous rays, may bear secondary spinules (e.g., epinephalines, acanthurids, balistids) or,

where the elongations are composed of soft tissue, have ornamentation usually in the form of serial pigmented spatulate swellings (e.g., in the myctophid genera Loweina and Tarletonbeania, among carapids, lophiiforms, lampridiforms, liopropomine serranids, the carangid genera Alectis and Selene, many paralichthyid genera, and the bothid flatfish genus Arnoglossus; fig. 11-33). In notacanthiforms (e.g., Leptocephalus giganteus), an elaborate appendage emerges from the caudal region and exceeds the body in length (fig. 11-35F). The potential for strong, elongate fin spines to deter predators is obvious (Moser, 1981; Govoni et al., 1984; Baldwin et al., 1991; Webb, 1999); however, a role for the trailing ornamented extensions found in many phylogenetic lineages is enigmatic. Their resemblance to structures on siphonophores suggests their potential for predator deterrence through siphonophore mimicry (Kendall et al., 1984; Govoni et al., 1984). Baldwin et al. (1991) suggested an even more fascinating possibility, “. . . siphonophore mimicry may be an adaptation to attract food items. Tim Targett (pers. commun.) observed behavior of a living larva of Liopropoma in a bucket aboard a research vessel and noted that zooplankton appeared to be attracted to the elongate filaments, which the larva kept suspended above its head. Harbison et al. (1977) found that species of five families of hyperiid amphipods associate with gelatinous zooplankton in relationships ranging from commensalism to obligate parasitism. Attracting prey by luring this fauna away from siphonophores could be a primary function of elongate filaments. . . .” Head spination is rare in larvae of “primitive” teleosts but becomes highly developed in many acanthopterygiian orders (e.g., in beryciforms, zeiforms, scorpaeniforms, perciforms, pleuronectiforms; fig. 11-36). Among these groups, larval head spines have developed on almost every superficial head bone; however, they are most often encountered in association with bones of the opercular-preopercular series, and with the posttemporal, supracleithral, parietal, frontal, and circumorbital bones. Like the elongate spinous fin rays, their role in predator deterrence seems obvious, although alternative possibilities have been suggested (Moser, 1981; Webb, 1999). Vision is the most important sensory modality for larval fish feeding, and it is not surprising that marine teleosts have evolved a variety of specializations in eye morphology. A recurrent theme is the presence of elliptical eyes in larvae of many lineages. For example, in myctophids, larvae of the two major subfamilies differ in eye shape, with narrow elliptical eyes in myctophines and round, or nearly round, eyes in lampanyctines (Moser and Ahlstrom, 1970). In some groups, the eyes protrude from the head to various degrees or are distinctly stalked (e.g., notacanthiforms, bathylagids, myctophids, stomiiforms; fig. 11-35A–D). Elliptical eyes can be more fully rotated compared to round eyes, and the subsequent enlargement of the visual field could be advantageous for feeding and predator avoidance (Weihs and Moser, 1981). The visual field would be further enlarged in larvae with stalked eyes; in blackdragon (Idiacanthus) larvae, the stalks reach 30% of the body length and may increase the visual field by an order of magnitude (Weihs and Moser, 1981).

Trophic Relationships In an attempt to explain large interannual abundance changes observed in cod and herring stocks, Hjort (1914) hypothesized that the number of recruits each year is determined during a

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F I G U R E 11-33 Examples of fish larvae with elongate, ornamented spinous, or segmented fin-rays. Except where noted, illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained. A: Trachipteridae, Zu cristatus, 5.8 mm; B: Carapidae, Carapus acus, 3.8 mm (Padoa, 1956); C: Melamphaidae, Melamphaes lugubris, 4.8 mm; D: Lophiidae, Lophiodes spilurus, 8.1 mm; E: Myctophidae, Loweina rara, 17.6 mm; F: Serranidae, Liopropoma sp., 11.0 mm (Kendall et al., 1984); G: Paralichthyidae, Cyclopsetta panamensis, 17.8 mm; H: Carangidae, Selene brevoortii, 6.4 mm; I: Bothidae, Arnoglossus japonicus, 30.5 mm (Amaoka, 1973).

critical period early in larval life. His critical period concept was that the strength of a year class is determined primarily by the availability of suitable food to the first-feeding larvae, although survival could be reduced if currents were to transport the larvae to an area unsuitable for continued development. Cushing (1974, 1975, 1982) extended Hjort’s concept in the match/mismatch hypothesis, based on the observations that fish in temperate North Atlantic waters tend to spawn at

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a relatively fixed time each year corresponding more or less with the spring and/or autumn plankton production peaks, and that plankton production tends to be more variable in time than fish spawning. Cushing suggested that the match or mismatch of fish spawning and plankton production is crucial in determining larval survival and explains, at least in part, the variability in year-class strength. Later, Cushing (1990) added a second part to the hypothesis, suggesting that at

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F I G U R E 11-3 4 Examples of fish larvae with enlarged or elaborate fins. Except where noted, illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained. A: Bathysauridae, unidentified, 33 mm (Marshall, 1961); B: Caulophrynidae, Caulophryne sp., 9.5 mm (Bertelsen, 1951); C: Moridae, Physiculus rastrelliger, 12.7 mm; D: Serranidae, Paranthias colonus, 5.9 mm; E: Myctophidae, Nannobrachium hawaiiensis, 9.4 mm; F: Scorpaenidae, Sebastes paucispinis, 14.0 mm; G: Balistidae, Balistes polylepis, 4.0 mm; H: Lutjanidae, Lutjanus peru, 10.7 mm; I: Gempylidae, Diplospinus multistriatus, 5.3 mm (Voss, 1954).

lower latitudes, fish spawning may be more closely attuned to local plankton production in oceanic upwelling and divergence zones through the mechanisms of adult feeding and multiple batch spawning, thus minimizing the mismatch between larval fish and plankton production cycles. Lasker (1975, 1978, 1981) also extended Hjort’s hypothesis, as the stable ocean concept, based on work with the northern anchovy off the California coast; he suggested that a stable environment facilitates the development and maintenance of

patches of suitable organisms at densities that promote larval survival and growth and conversely, that strong turbulence results in poor feeding conditions with attendant reduced larval growth and survival, leading to poor recruitment. However, “stable” does not necessarily mean “static,” and low level turbulence may be beneficial (e.g., Cushing, 1990). Rothschild and Osborn (1988) demonstrated that contact rates between planktonic predators and their prey depend on the concentrations of both and also on their velocities and

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F I G U R E 11-35 Examples of fish larvae with elongate soft tissue structures. Except where noted, illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained.A: Idiacanthidae, Idiacanthus antrostomus, 55.0 mm; B: Bathylagidae, Bathylagus pacificus, 7.1 mm; C: Bathylagidae, Bathylagus bericoides, 17.7 mm; D: Myctophidae, Myctophum aurolaternatum, 25.8 mm; E: Astronesthidae, unidentified, 33.0 mm (Kawaguchi and Moser, 1984); F: Notocanthidae, Leptocephalus giganteus, 314.0 mm; G: Malacosteidae, unidentified, 34.5 mm (Moser, 1981); H: Mirapinnidae, Eutaeniophorus festivus, 35 mm (105 mm TL) (Bertelsen and Marshall, 1956); I: Cynoglossidae, Symphurus atricaudus, 23.0 mm; J: Neobythitinae, unidentified, 64.0 mm (Moser, 1981).

that small-scale turbulence can increase the predator–prey encounter rate. Lasker (1975) provided direct observational evidence that strong turbulence can reduce larval feeding, and several studies have provided indirect evidence in the form of correlations of food availability and/or turbulence with larval survival or recruitment (e.g., Arthur, 1976; Smith and Lasker, 1978; O’Connell, 1980; Bailey, 1981; Methot, 1983; Grover

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and Olla, 1986; Peterman and Bradford, 1987; Cass-Calay, 1997) that could be interpreted as showing that larval feeding conditions are important in determining larval survival and subsequent recruitment. However, correlations do not demonstrate causality and other interpretations are possible. Some studies have shown that other factors (e.g., temperature, currents) strongly influence larval survival and/or recruitment

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F I G U R E 11-3 6 Examples of fish larvae with enlarged spines on the head and/or pectoral girdle. Except where noted, illustrations are from publications by personnel at SWFSC and are reproduced from Moser (1996), where original attributions can be obtained. A: Diretmidae, Diretmus argenteus, 6.2 mm; B: Paralepididae, Sudis atrox, 21.5 mm; C: Anoplogastridae, Anoplogaster cornuta, 4.3 mm; D: Scorpaenidae, Pontinus sierra, 5.0 mm; E: Malacanthidae, Caulolatilus princeps, 6.0 mm; F: Scorpaenidae, Sebastolobus altivelis, 11.2 mm; G: Holocentridae, Sargocentron suborbitalis, 4.2 mm; H: Paralichthyidae, Syacium ovale, 6.5 mm; I: Priacanthidae, Pristigenys serrula, 4.0 mm; J: Serranidae, Hemanthias signifer, 6.6 mm; K: Molidae, Ranzania laevis, 2.8 mm (Tortonese, 1956).

(e.g., Cowen, 1985; Houde, 1989; Houde and Zastrow, 1993), and some have shown poor correlations, at least in some years, between food availability or larval abundance and recruitment (e.g., Anderson, 1988; Peterman et al., 1988; Butler, 1989; Kendall et al., 1996; Bradford and Cabana, 1997; Kendall, 2000). This suggests that larval survival may not always be the critical factor in determining recruitment success. Nevertheless, since Hjort’s (1914) work, feeding has been

a major focus in studies of larval survival and recruitment in marine fishes, although in recent years, the emphasis has begun to shift to other areas of investigation (e.g., physical processes, predation, dynamics of the juvenile stage). The majority of marine fishes in California waters are oviparous, and have planktonic eggs. The larvae that hatch from these eggs typically are relatively poorly developed at hatching, but by the end of the yolk-sac stage, little yolk

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remains and the larvae have developed to the point that feeding can commence. Larvae that hatch from demersal eggs and larger planktonic eggs typically are larger and more vagile and have greater internal nutrient reserves that may confer greater initial resistance to starvation, compared with larvae from small planktonic eggs (e.g., Chambers, 1997). Most planktonic fish eggs in the California Current region fall within the range of about 0.5–3.0 mm in diameter; “typical” planktonic eggs are about 1 mm. Larvae that hatch from those eggs complete yolk absorption in about 3–7 days and reach the point of irreversible starvation if they are unsuccessful in obtaining a sufficient number of prey of sufficient quality within another 1–8 days (e.g., Lasker et al., 1970; Hunter and Kimbrell, 1980a; Bailey, 1982). Resistance to starvation subsequently increases (e.g., Hunter, 1976a; Theilacker, 1986). Larval fish consume a wide variety of plankters; copepods, especially their naupliar and copepodite stages, typically are a major component of larval fish diets in the California Current region (e.g., Arthur, 1976, 1977; Hunter and Kimbrell, 1980a; Sumida and Moser, 1980, 1984; Mullin et al., 1985; Brewer and Kleppel, 1986; Grover and Olla, 1987; Watson and Davis, 1989). Other common prey taxa include diatoms, dinoflagellates, tintinnids, rotifers, appendicularians, mollusk veliger larvae, and cladocerans (e.g., Gadomski and Boehlert, 1984; Sumida and Moser, 1984; Mullin et al., 1985; Brewer and Kleppel, 1986; Jahn et al., 1988; Watson and Davis, 1989). Fish larvae may become important in the diets of older larvae of some species such as California barracuda and chub mackerel (Hunter, 1981). The largest size prey that can be eaten is determined by larval fish mouth size and the critical prey dimension is width rather than length. Small larvae consume small prey, typically in about the 30–100 m width range. The maximum prey size selected increases more or less rapidly as the larvae grow, but the minimum size consumed increases much more slowly; thus larger larvae can select from among a larger range of prey sizes, presumably subsisting on smaller prey when the larger, more energetically valuable, but rarer (e.g., Vlymen, 1977) prey are unavailable (e.g., Sumida and Moser, 1980, 1984; Hunter, 1981; Watson and Davis, 1989). Marine fish larvae are visual predators that feed during daylight hours (e.g., Arthur, 1976; Hunter, 1981; Sumida and Moser, 1984; Watson and Davis, 1989; Margulies, 1997), although some feeding at lower light levels also has been suggested for some species (e.g., Watson and Davis, 1989; Mullin and Cass-Calay, 1997). First-feeding larvae have limited visual range. Prey is perceived only within distances less than about 0.5–1.0 body lengths; perceptual range increases with larval growth (e.g., Hunter, 1972, 1981; Margulies, 1997). Water viscosity is an important factor in determining swimming behavior and speed in small fish larvae. The lack of fin rays and supporting structures and the relatively poorly developed musculature of typical first-feeding marine teleosts results in swimming speeds somewhat less than about a body length per second. As larvae grow, viscosity becomes relatively unimportant, leading to a change in swimming behavior from intermittent burst swimming to a beat and glide mode (e.g., Weihs, 1980), and average swimming speed increases as a function of larval length (e.g., Hunter, 1981). Owing to their limited swimming ability and small visual range, first-feeding larvae are capable of searching only a small volume of water for prey, probably not much more than about 100 mL, per hour, but they have the ability to remain in a patch of food if one is encountered (e.g., Hunter and Thomas, 1974). Searchable volume increases rapidly as swimming speed and

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perceptual range increase with larval growth (e.g., Hunter, 1972, 1981). Laboratory rearing studies have shown that to survive, firstfeeding larvae must find enough food to grow on the order of 15–20% per day (e.g., Houde and Schekter, 1980); high food densities on the order of 1000 or more microcopepods per liter are required for high survival rates (e.g., O’Connell and Raymond, 1970; May, 1974; Hunter, 1981). However, these high food concentration requirements generally were based on larval rearing in static systems and did not take into account possible increased encounter rates in the sea resulting from microscale turbulence (Rothschild and Osborn, 1988). Average densities of copepod nauplii and microcopepods in the sea are two or three orders of magnitude lower (e.g., Beers and Stewart, 1969; Arthur, 1977) than those indicated as necessary by the laboratory studies. Even given the potential benefit of microscale turbulence, it seems likely that fish larvae must depend on plankton patches, where concentrations of prey are higher than average. Plankton patchiness on scales of kilometers to centimeters has been demonstrated in the California Current region (Lasker, 1975; Haury, 1976; Mullin, 1979; Owen, 1981, 1989), although the highest concentrations of fish larvae and their potential prey do not always coincide (e.g., Jahn et al., 1988; Frank, 1988; Watson and Davis, 1989). O’Connell (1980) found patches of starving and well-fed northern anchovy larvae off southern California, and Lasker (1978) demonstrated that northern anchovy larvae fed successfully at high natural prey densities in water collected from the chlorophyll maximum zone, but not at the low densities available in surface water or in water from either stratum after a storm dispersed the chlorophyll maximum. On the other hand, Butler (1989) and Owen et al. (1989) found little difference in survival and the condition of larval northern anchovy under eutrophic and relatively oligotrophic conditions off southern California. Predation may have as large an effect on recruitment as larval feeding, but it has been the subject of far fewer directed studies than feeding. Predation probably is the major source of mortality during the egg and yolk-sac larval stages (e.g., Hunter and Kimbrell, 1980b; Hunter, 1981; Hewitt et al., 1985). Many kinds of invertebrates, such as cnidarian medusae, ctenophores, chaetognaths, copepods, amphipods, and euphausids, are known larval fish predators (e.g., Lillilund and Lasker, 1971; Theilacker and Lasker, 1974; Alvariño, 1980; Brewer et al., 1984). Most of these are effective predators only on the nonmotile and weakly swimming early stages through yolk absorption (e.g., Feigenbaum and Reeve, 1977; Landry, 1978; Hunter, 1981); predation may become a less important source of mortality than starvation during early feeding-stage larval life (e.g., Hewitt et al., 1985), although starving larvae probably are more vulnerable to predation (e.g., Hunter, 1976b; Cushing, 1990), so that predation may be the immediate cause of death of a starving larva. As the larvae grow and increase in competence, their susceptibility to starvation and to most planktonic predators diminishes, although they may actually become more vulnerable to some (e.g., Houde, 1997) and they remain very susceptible to mobile predators such as juvenile and adult planktivorous fishes (e.g., Hunter and Kimbrell, 1980b; Hunter, 1981; Pepin et al., 1987) through at least mid- to late larval life when escape responses improve or schooling behavior begins (e.g., Hunter, 1981; Webb, 1981; Margulies, 1989). Predators, as well as food, are patchily distributed in the sea, and as has been suggested in larval fish feeding studies, patchiness may be critical in determining

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larval mortality due to predation (Hunter, 1981). Whatever the cause(s) of mortality may be, it seems probable that the growth rate during early life (through larval or juvenile stage) is a critical determinant in survival and subsequent recruitment (e.g., Anderson, 1988; Lo et al., 1995).

Acknowledgments This review was based largely on information derived from CalCOFI and we are indebted to all those who have contributed to it. The quality and scope of the ichthyoplankton data used in this chapter derive from Elbert “Ahlie” Ahlstrom’s guidance over the first decades of CalCOFI and from the great efforts of those who conducted the CalCOFI research program. Richard Charter’s contributions as field survey coordinator, plankton laboratory supervisor, and data manager continue to be vital to all aspects of CalCOFI ichthyoplankon research. The work of his staff, Dimitry Abramenkoff, Ronald Dotson, David Griffith, Amy Hays, Susan Jacobson, Cynthia Meyer, and Susan Manion, has been essential to the production of the CalCOFI ichthyoplankton data base and associated publications. Lucy Dunn and the many other plankton sorters played a central role in processing the CalCOFI ichthyoplankton samples. Special recognition is due the talented and dedicated people who identified the eggs and larvae from the plankton samples and documented the life histories of the several hundred species of fish larvae in CalCOFI samples: David Ambrose, Sharon Charter, Barbara MacCall, Elaine Sandknop, and Elizabeth Stevens. Their work is the basis for the CalCOFI ichthyoplankton data base, reports, atlases, and other publications. Roy Allen and Henry Orr helped with much of the graphical material used in this chapter. We thank Timothy Baumgartner, John Hunter, and Daniel Margulies, for permission to use figures from their publications and gratefully acknowledge the authors of published larval fish illustrations used in the composite plates; their papers are cited in the captions to those plates. We thank Larry Allen, William Richards, Joanne Lyczkowski-Shultz, Bruce Mundy, and anonymous reviewers for improvements to the manuscript.

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Ralston, S., E.W. Brothers, D.A. Roberts, and K.M. Sakuma. 1996. Accuracy of age estimates for larval Sebastes jordani. U.S. Fish. Bull. 94:89–97. Ralston, S., J.R. Bence, M.B. Eldridge, and W.H. Lenarz. 2003. An approach to estimating rockfish biomass based on larval production with application to Sebastes jordani. U. S. Fish. Bull. 101:129–146. Richards, W.J. 1996. Triglidae. In H.G. Moser (ed.), The early life stages of fishes in the California Current region. CalCOFI Atlas 33., pp. 979–805. ———. (in press). Early stages of Atlantic Fishes: An identification guide for the western central North Atlantic. Taylor and Francis CRE Press, Boca Raton, FL. Richardson, S.L. 1973. Abundance and distribution of larval fishes in waters off Oregon, May–October 1969, with special emphasis on the northern anchovy, Engraulis mordax. U. S. Fish. Bull. 71: 697–711. ———. 1977. Larval fishes in ocean waters off Yaquina Bay, Oregon: abundance, distribution, and seasonality, January 1971 to August 1972. Oregon State University Sea Grant College Program Publication No. ORESU-T-77-003. ———. 1980. Spawning biomass and early life of northern anchovy, Engraulis mordax, in the northern subpopulation off Oregon and Washington. U. S. Fish. Bull. 78:855–876. ———. 1981a. Current knowledge of larvae of sculpins (Pisces: Cottidae and allies) in northeast Pacific genera with notes on intergeneric relationships. U. S. Fish. Bull. 79:103–121. ———. 1981b. Pelagic eggs and larvae of the deepsea sole, Embassichthys bathybius (Pisces: Pleuronectidae), with comments on generic affinities. U. S. Fish. Bull. 79:163–170. Richardson, S.L., and W.A. Laroche. 1979. Development and occurrence of larvae and juveniles of the rockfishes Sebastes crameri, Sebastes pinniger, and Sebastes helvomaculatus (family Scorpaenidae) off Oregon. U. S. Fish. Bull. 77:1–46. Richardson, S.L., and W.G. Pearcy. 1977. Coastal and oceanic fish larvae in an area of upwelling off Yaquina Bay, Oregon. U. S. Fish. Bull. 75:125–145. Richardson, S.L., and W. Stephenson. 1978. Larval fish data a new approach to analysis. Oregon State University Sea Grant College Program Publication No. ORESU-T-78-002. Richardson, S.L., and B.B. Washington. 1980. Guide to identification of some sculpin (Cottidae) larvae from marine and brackish waters off Oregon and adjacent areas in the northeast Pacific. U.S. Department of Commerce, NOAA Technical Report. NMFS Circular. 430. Richardson, S.L., J.R. Dunn, and N.A. Naplin. 1980a. Eggs and larvae of butter sole, Isopsetta isolepis (Pleuronectidae), off Oregon and Washington. U. S. Fish. Bull. 78:401–417. Richardson, S.L., J.L. Laroche, and M. D. Richardson. 1980b. Larval fish assemblages in the north-east Pacific Ocean along the Oregon coast, winter–spring 1972–1975. Estuarine Coastal Mar. Sci. 11:671–699. Roemmich, D., and J. McGowan. 1995a. Climatic warming and decline of zooplankton in the California Current. Science 267:1324–1326. Roemmich, D., and J. McGowan. 1995b. Sampling zooplankton: Correction. Science 268:352–353. Rothschild, B.J., and T.R. Osborn. 1988. Small-scale turbulence and plankton contact rates. J. Plankton Res. 10:465–474. Sakuma, K.M., and T.E. Laidig. 1995. Description of larval and pelagic juvenile chilipepper, Sebastes goodei (family Scorpaenidae), with an examination of larval growth. U. S. Fish. Bull. 93:721–731. Sakuma, K.M., and S. Ralston. 1995. Distributional patterns of late larval groundfish off central California in relation to hydrographic features during 1992 and 1993. CalCOFI Rep. 36:179–192. Sakuma, K.M., S. Ralston, and D.A. Roberts. 1999. Diel vertical distribution of postflexion Citharichthys spp. and Sebastes spp. off central California. Fish. Oceanogr. 8:68–76. Sameoto, D.D. 1983. Micronekton sampling using a new multiple-net sampler, the BIONESS, in conjunction with a 120 kHz sounder. Biol. Oceanogr. 2:179–198. Sameoto, D.D., and L.O. Jaroszynski. 1969. Otter surface trawl: a new neuston net. J. Fish. Res. Bd. Can. 26:2240–2244. Sameoto, D.D., L.O. Jaroszynski, and W.B. Fraser. 1980. BIONESS, a new design in multiple net zooplankton samplers. Can. J. Fish. Aquat. Sci. 37:722–724. Schlotterbeck, R.E., and D.W. Connally. 1982. Vertical distribution of three nearshore Southern California larval fishes (Engraulis mordax, Genyonemus lineatus, and Seriphus politus). U. S. Fish. Bull. 80:895–902. Schmidt, J. 1932. Danish eel investigations during 25 years (1905–1930). Carlsberg Foundation. Copenhagen.

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Schwing, F.B., T. Murphree, and P.M. Green. 2002. The Northern Oscillation Index: a new climate index for the northeast Pacific. Prog. Oceanogr. 53:115–139. Scofield, E. C. 1934. Early life history of the California sardine (Sardinops caerulea) with special reference to distribution of eggs and larvae. California Fish and Game, Fish Bulletin. 41. Scofield, E.C., and M.J. Lindner. 1930. Preliminary report of the early life history of the California sardine. Calif. Fish Game. 16:120–124. Sette, O.E. 1943. Studies on the Pacific pilchard or sardine (Sardinops caerulea) I. Structure of a research program to determine how fishing affects the resources. U.S. Fish and Wildlife Special Scientific Report 19. Shanks, A.L. 1983. Surface slicks associated with tidally forced internal waves may transport pelagic larvae of benthic invertebrates and fishes shoreward. Mar. Ecol. Prog. Ser. 13:311–315. ———. 1986. Vertical migration and cross-shelf dispersal of larval Cancer spp. and Randallia ornata (Crustacea: Brachyura) off the coast of southern California. Mar. Biol. 92:189–199. Shenker, J.M. 1988. Oceanographic associations of neustonic larvae and juvenile fishes and Dungeness crab megalopae off Oregon. U. S. Fish. Bull. 86:299–317. Smith, D. G. 1979. Guide to the leptocephali: (Elopiformes, Anguilliformes, and Notacanthiformes). U.S. Department of Commerce, NOAA Technical Report NMFS Circular 424. Smith, P.E. 1972. The increase in spawning biomass of northern anchovy, Engraulis mordax. U. S. Fish. Bull. 70:849–874. Smith, P.E., and R. Lasker. 1978. Position of larval fish in an ecosystem. Rapp. P.-v. Réun. Cons. Int. Explor. Mer, 173:77–84. Smith, P.E., and H.G. Moser. 1988. CalCOFI time series: an overview of fishes. CalCOFI Rep. 29:66–78. ———. 2003. Long-term trends and variability in the larvae of Pacific sardine and associated species in the California Current region. Deep-Sea Res. Pt. II. 50:2519–2536. Smith, P.E., and S.L. Richardson. 1977. Standard techniques for pelagic fish egg and larva surveys. FAO Fish. Tech. Pap. 175. Smith, P.E., R.C. Counts, and R.I. Clutter. 1968. Changes in filtration efficiency of plankton nets due to clogging under tow. J. Cons. Perm. Int. Explor. Mer 32:232– 248. Sokal, R. R., and C. D. Michener. 1958. A statistical method for evaluating systematic relationships. Univ. Kans. Sci. Bull. 38:1409–1438. Stein, D.L. 1980. Description and occurrence of macrourid larvae in the northeast Pacific off Oregon, U.S.A. Deep-Sea Res. 27A:889–900. Sumida, B.Y., and H.G. Moser. 1980. Food and feeding of Pacific hake (Merluccius productus) larvae off southern California and northern Baja California. CalCOFI Rep. 21:161–166. Sumida, B.Y., and H.G. Moser. 1984. Food and feeding of bocaccio (Sebastes paucispinis) and comparison with Pacific hake (Merluccius productus) larvae in the California Current. CalCOFI Rep. 25:112–118. Theilacker, G.H. 1986. Starvation-induced mortality of young seacaught jack mackerel, Trachurus symmetricus, determined with histological and morphological methods. U. S. Fish. Bull. 84:1–17. Theilacker, G.H., and R. Lasker. 1974. Laboratory studies of predation by euphausid shrimps on fish larvae. in J. H. S. Blaxter (ed.), The early life history of fish. Springer-Verlag, New York, pp. 287–299. Thorrold, S.R. 1992. Evaluating the performance of light traps for sampling small fish and squid in open waters of the central Great Barrier Reef lagoon. Mar. Ecol. Prog. Ser. 89:277–285. ———. 1993. Post-larval and juvenile scombrids captured in light traps: preliminary results from the Central Great Barrier Reef lagoon. Bull. Mar. Sci. 52:631–641. Toole, C.L., D.F. Markle, and P.M. Harris. 1993. Relationships between otolith microstructure, microchemistry, and early life history events in Dover sole, Microstomus pacificus. U.S. Fish. Bull. 91:732–753. Tortonese, E. 1956. Plecognathi. In Uova, larva e stadi giovanili di Teleostei. Fauna e Flora del Golfi di Napoli Monogr. 38:960–977. Tucker, G.H. 1951. Relation of fishes and other organisms to the scattering of underwater sound. J. Mar. Res. 10:215–238. Van der Lingen, C.D., D. Checkley, Jr., M. Barange, L. Hutchings, and K. Osgood. 1998. Assessing the abundance and distribution of eggs of sardine, Sardinops sagax, and round herring, Etrumeus whiteheadi, on the western Agulhas Bank, South Africa, using a continuous, underway fish egg sampler. Fish. Oceanogr. 7:35–47. Vlymen, W.J. 1977. A mathematical model for the relation between larval anchovy (Engraulis mordax) growth, prey microdistribution, and larval behavior. Environ. Biol. Fishes.2:211–233.

Voss, N.A. 1954. The postlarval development of the fishes of the family Gempylidae from the Florida Current. I. Nesiarchus and Gempylus Cuv. and Val. Bull. Mar. Sci. 4:120–159. Waldron, K.D. 1972. Fish larvae collected from the northeastern Pacific Ocean and Puget Sound during April and May 1967. U.S. Department of Commerce, NOAA Technical Report. NMFS SSRF–663. Walker, H.J., Jr., W. Watson, and A.M. Barnett. 1987. Seasonal occurrence of larval fishes in the nearshore Southern California Bight off San Onofre, California. Estuarine Coastal Shelf Sci. 25:91–109. Walters, K. 2001. Nearshore live-fish. In L. Rogers-Bennett (ed.), Review of some California fisheries for 2000: Market squid, Dungeness crab, sea urchin, prawn, white abalone, groundfish, ocean salmon, Pacific sardine, Pacific herring, Pacific mackerel, nearshore live-fish, halibut, yellowfin tuna, white seabass, and kelp. CalCOFI Rep. 42:12–28. Ware, D.M. 1995. A century and a half of change in the climate of the NE Pacific. Fish. Oceanogr. 4: 267–277. Watson, W. 1982. Development of eggs and larvae of the white croaker, Genyonemus lineatus Ayres (Pisces: Sciaenidae), off the southern California coast. U. S. Fish. Bull. 80:403–417. ———. 1992. Distribution of larval Pacific sardine, Sardinops sagax, in shallow coastal waters between Oceanside and San Onofre, California:1978–1986. CalCOFI Rep. 33:89–99. Watson, W., and R.L. Davis, Jr. 1989. Larval fish diets in shallow coastal waters off San Onofre, California. U. S. Fish. Bull. 87:569–591. Watson, W., R.L. Charter, H.G. Moser, R.D. Vetter, D.A. Ambrose, S.R. Charter, L.L. Robertson, E.M. Sandknop, E.A. Lynn, and J. Stannard. 1999. Fine-scale distributions of planktonic fish eggs in the vicinities of Big Sycamore Canyon and Vandenberg Ecological Reserves, and Anacapa and San Miguel Islands, California. CalCOFI Rep. 40: 128–153. Webb, J.F. 1999. Larvae in fish development and evolution. In B.K. Hall and M.H. Wake (eds.), The origin and evolution of larval forms. Academic Press, San Diego, pp. 109–158. Webb, P.W. 1981. Responses of northern anchovy, Engraulis mordax, larvae to predation by a biting planktivore, Amphiprion percula. U. S. Fish. Bull. 79:727–735. Weibe, P.H., A.W. Morton, A.M. Bradley, R.H. Backus, J.E. Craddock, V. Barber, and G.R. Flierl. 1985. New developments in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Mar. Biol. 87:313–323. Weihs, D. 1980. Energetic significance of changes in swimming modes during growth of larval anchovy, Engraulis mordax. U. S. Fish. Bull. 77:597–604. ———. and H.G. Moser. 1981. Stalked eyes as an adaptation for more efficient foraging in marine fish larvae. Bull. Mar. Sci. 31: 31–36. Willis, J.M., W.G. Pearcy, and N.V. Parin. 1988. Zoogeography of midwater fishes in the Subarctic Pacific. In T. Nemoto and W.G. Pearcy (eds.), The biology of the Subarctic Pacific—Proceedings of the Japan-United States of America Seminar on the biology of micronekton of the Subarctic Pacific. Bull. Univ. Tokyo Ocean Res. Inst. 26, Part II, pp 79–142. Wisner, R.L. 1976. The taxonomy and distribution of lanternfishes (family Myctophidae) of the eastern Pacific Ocean. U.S. Government Printing Office, Washington, DC. Witting, D.A., K.W. Able, and M.P. Fahay. 1999. Larval fishes of a Middle Atlantic Bight estuary: assemblage structure and temporal stability. Can. J. Fish. Aquat. Sci. 56:222–230. Wolf, P., and P.E. Smith. 1985. An inverse egg production method for determining the relative magnitude of Pacific sardine spawning biomass off California. CalCOFI Rep. 26:130–138. Wolf, P., P.E. Smith, and C.L. Scannell. 1987. The relative magnitude of the 1986 Pacific sardine spawning biomass off California. CalCOFI Rep. 28:21–29. Yoklavich, M.M., M. Stevenson, and G.M. Cailliet. 1992. Seasonal and spatial patterns of ichthyoplankton abundance in Elkhorn Slough, California. Estuarine Coastal Shelf Sci. 34:109–126. Yoklavich, M. M., V. J. Loeb, M. Nishimoto, and B. Daly. 1996. Nearshore assemblages of larval rockfishes and their physical environment off central California during an extended El Niño event, 1991–1993. U. S. Fish. Bull. 94:766–782. Zaitsev, Y.P. 1970. Marine neustonology. Naukova Dumka. Kiev. 264 pp. [In Russian]. [English transl.: 1971. Israel Progr. Sci. Transl. No. 5976.

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CHAPTER 12

Surface Waters LAR RY G. ALLE N AN D J E F F R EY N. C R O S S

The Pelagic Zone The epipelagic realm technically encompasses the upper 200 m of the ocean beyond the continental shelf, world-wide (Parin, 1968; Helfman et al., 1997). It is easily the largest habitat off California and the home of 40% of the species and 50% of the families of fishes. The water column that overlies the continental shelf comprises what we will call the coastal pelagic (neritic) realm (fig. 12-1). Because the continental shelf off most of California and Baja California is narrow, the fish assemblages of the epipelagic zone and those of the coastal pelagic realm overlap and interact on a seasonal basis (see Chapter 5). In fact, unlike most coastal areas, the highly productive waters of the major upwelling region off California are dominated by coastal pelagic species that spread into the open ocean environment well offshore (up to 300–400 km). The waters below the epipelagic zone include the Mesopelagic (approximately 200–800 m) and the bathypelagic zones (
800–1000 m). These deep sea habitats are the main subjects of chapter 13 of this volume. About 200 species (70 families) have been collected in the California Current (Berry and Perkins, 1966), 79 species (30 families) have been collected in the coastal waters (Horn, 1974), and 124 species have been collected in the mesopelagic and bathypelagic zones (Lavenberg and Ebeling, 1967). Epipelagic fishes are relatively large, active, fast-growing, and long-lived fishes that reproduce early and repeatedly (Childress et al., 1980). Mesopelagic fishes are relatively small, slow-growing, and long-lived fishes that reproduce early and repeatedly. Bathypelagic fishes are relatively large, sluggish, rapid-growing, and slightly short-lived fishes that reproduce late and maybe only once (Childress et al., 1980). Light penetration, water temperature, and water mass structure define vertical zonation. The epipelagic zone is euphotic, and temperatures fluctuate diurnally and seasonally. It is approximately 50m deep in turbid nearshore waters and expands offshore in clear oceanic waters. The mesopelagic zone is characterized by steep environmental gradients. This zone extends from the permanent thermocline, below the compensation depth, to the 6°C isotherm between 500–1000 m depending on location. The bathypelagic zone is characterized by uniformity and extends nearly to the bottom. It is absent or

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restricted in the nearshore basins off of southern California and expands offshore (Lavenberg and Ebeling, 1967). Physical and biological variability in the epipelagic zone are closely linked to oceanographic processes. Wind-driven, coastal upwelling is a prominent feature of the California Current system. Movement of water from nearshore to offshore as driven by Ekman transport causes intense, periodic upwelling, particularly off northern and central California. Such upwelling brings cold, nutrient-rich water to the surface, which promotes the bloom of phytoplankton. These blooms then set up a trophic cascade upon which pelagic fishes depend. Cold, upwelled water adjacent to the coast is swept far offshore in large eddies and plume-like structures of up to several hundred kilometers wide (fig. 12-2). Temperature fronts where cold surface water is adjacent to relatively warm surface are produced and maintained over large distances. These fronts concentrate large numbers of fishes in this otherwise featureless world. Upwelling is not only responsible for high primary productivity, but is also produces an unpredictable distribution and availability of food in the habitat (Parrish et al., 1981). The California Current is one of only four major eastern boundary currents of the world. These boundary currents occur over narrow continental shelves in temperate areas and are characterized by surface flow toward the equator, coastal upwelling, and high primary productivity. The other boundary currents are the Peru Current off the west coast of South America, the Canary Current off the west coast of southern Europe and northern Africa, and the Benguela Current off the west coast of southern Africa. All four boundary currents are physically similar and are dominated by a small number of closely related, temperate pelagic fishes that can reach large population sizes including anchovy (Engraulis), sardine (Sardinops or Sardina), jack mackerel (Trachurus), hake (Merluccius), mackerel (Scomber), and bonito (Sarda) (Parrish et al., 1983).

Prominent Epipelagic Fish Groups World-Wide Elasmobranch and acanthomorph (spiny-finned) fishes dominate the epipelagic zone throughout the world’s oceans. Prominent elasmobranch groups include the carcharhinid and lamnid sharks (e.g., blue shark, pelagic white tip, shortfin

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F I G U R E 12-1 A classification of pelagic habitats or “life zones”. The top 100–200 m constitutes the epipelagic zone covered in the present chapter. The meso-, bathy-, benthopelagic and deep benthic realms are covered in Chapter 13.

mako, and salmon shark). The Atherinomorpha, an important acanthomorph group, includes halfbeaks, needlefish, flying fishes, and sauries, which are typically the smaller, low-level carnivores of the open ocean. Another acanthomorphan superorder, the Percomorpha, is also well-represented, especially among the active swimmers of the surface waters. Large, active fishes belong mainly to the perciform suborders: Scombroidei (mackerels, tunas, and billfishes), Stromateioidei (driftfishes and medusafishes), and Percoidei (jacks and dolphinfishes). Finally, the Lampridiomorpha is well-represented, particularly in the lower portions of the epipelagic zone, by the highly specialized ribbonfishes, oarfishes and opahs (Parin, 1968). In nearshore and boundary current areas, the surface waters are dominated by Clupeomorph fishes, such as anchovies, herrings, sardines, menhadens, and pilchards (Smith et al., 1983; Helfman et al., 1997).

Adaptations to Epipelagic Existence Epipelagic fishes live in a three-dimensional world that is virtually devoid of physical structure to use as visual reference points. The fishes that inhabit this unique realm range widely in size from the two largest fishes in the world, the whale shark and the basking shark, to the various small species of halfbeaks, sauries and stromateioids. In general, pelagic fishes are counter-shaded and silvery, round or slightly compressed laterally, and streamlined with forked or lunate caudal fins. They typically: 1) posses large eyes for visual predation, 2) have efficient respiration and food conversion capabilities, 3) have a high percentage of red muscle tissue and lipids. 4) form

schools, and 5) undertake long migrations. Finally, all known examples of fish endothermy occur in this habitat (Carey et al., 1971; Helfman et al., 1997). Species that are associated with rare substrata, such as floating kelps including Sargassum, are often cryptically colored and not counter-shaded (Parin, 1968).

Locomotory Adaptations Foremost among the adaptations to the epipelagic zone are the notable locomotory adaptations in many of the fishes that inhabit it. Locomotion among epipelagic fishes evolved along two main paths. The first and most evident path involves active, continuous swimming using caudal propulsion, which is often associated with long distance migrations. A number of less active species have evolved or retained locomotory modes that enable them to hover and move with a lower expenditure of energy. This second, less evident path often involves either the retention of anguilliform locomotory patterns using undulation of the entire body or elongate fins (snake mackerels, and ribbon and oarfishes) (fig. 12-3) or by oscillation of various fins (Parin, 1968; Webb, 1993). Oscillation of fins is best represented by the pelagic members of the Tetraodontiformes (ocean sunfish and oceanic puffers) that use modified dorsal and anal fins, but also includes the opah, a lampridiform fish, that primarily uses its pectoral fins in a labriform-type of locomotory pattern. Many disparate groups of fishes have converged on the active, continuous swimming mode using caudal propulsion. Most of these undergo long distance feeding and reproductive migrations during their life cycles. Various species of large, oceanic sharks, salmon, tunas, and billfishes migrate thousands

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F I G U R E 12-2 This infrared satellite image shows summer upwelling along the California coast. Surface water temperatures are color coded with red indicating warm water and blue-violet cold (after Castro and Huber, 2000).

of kilometers each year. Even smaller, coastal pelagic species such as herrings, sardines, and jacks migrate 100s to 1000s of kilometers annually in some parts of the world. Continuous swimming during long-distance migrations requires that these species have very large proportions of red muscle, which operates aerobically and does not fatigue easily. In most fishes, red muscle is superficial to the deeper white muscle masses and occurs in a lateral band along the body. In the highly derived tunas (Thunnus), however, the red muscle mass is more extensive and occurs deeper in the body musculature and is kept warm by counter-current heat exchangers promoting endothermy. Similar structures have evolved by convergence in the epipelagic mackerel sharks (Lamnidae) (see chapter 20, Fish Movements and Activity Patterns). Besides red muscle, highly derived epipelagic fishes, such as tunas, have evolved a number of other important adaptations that promote rapid swimming, including: fusiform (streamlined) bodies, stiff fins that fit into grooves in the body, scale corselets, finlets, keels, lunate caudal fins, and ram gill ventilation (Marshall 1971; Magnuson 1973, 1978). Fusiform body shapes, which greatly minimize drag, have the maximum circumference of the body two-fifths of the way back from the head. Smaller, stiff fins aid in maneuvering, but create drag when swimming straight ahead. At such times, tunas and their relatives depress these fins into depressions or grooves in the body, greatly reducing drag. Tunas have added a corselet of large, bony scales around the area of maximum girth, which also serves to reduce drag and promote laminar water

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FIGURE 12-3 Epipelagic fishes that move by means of undulating or

oscillating fins: a) king-of-the-salmon (anguilliform and/or amiiform); b) opah (labriform); c) ocean sunfish (tetraodontiformd); d) and oceanic puffer (tetraodontiform) (after Parin, 1968).

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flow over the posterior half of the body. Many high-speed fishes, such as mackerels and tunas, possess small finlets that occur between the dorsal and anal fins and the caudal fin. These structures have long been thought to prevent eddies from forming, allowing the stiff, lunate caudal to thrust against less turbulence (Helfman et al., 1997). Recent evidence from studies of mackerel indicate that finlets vary greatly in flexure during a caudal fin stroke and that the most posterior finlet is oriented to redirect flow into the developing tail vortex. This action may increase thrust produced by the tail of the swimming mackerel (Nauen and Lauder, 2001). The small second dorsal and anal fins of mackerel sharks, billfishes, and swordfishes are thought to have similar functions to those of finlets. Two kinds of keels have evolved in rapidly swimming fishes, caudal and peduncular keels. Sharks, many jacks, mackerels, tunas, billfishes, and swordfishes all have single or multiple keels near their tails. Tunas have both a singular keel on the caudal peduncle and a pair of caudal keels that angle toward one another front to back. Single peduncular keels reduce drag and act as cut-waters as the narrow peduncle rapidly oscillates through the water with the caudal fin as well as providing hydrodynamic lift to the posterior portion of the fish (Magnuson, 1973, 1978; Pelster, 1997). Paired caudal keels are believed to act as nozzle that accelerates water moving across the tail fin (Collette, 1978). Lunate caudal fins represent a great advantage because they possess very high aspect ratios and produce maximum thrust with a minimum of drag (Magnuson, 1978). Finally, the high level of activity in pelagic fishes comes with a high oxygen demand that requires a very efficient respiratory system. Continuous swimming provides a means of gill ventilation that does not require the substantial energy expenditure necessary for buccal pumping of water over the gills (estimated at 15% of total energy expenditure by fish). Continuous swimmers need only to open their mouths while swimming to have water flow over their gills. This mode is termed ram gill ventilation and requires fusion of gill lamellae in some fishes to prevent damage. The downside of ram gill ventilation is that many fishes relying on it, such as pelagic sharks, tunas, and billfishes, have lost the ability to pump water over the gills and must swim continuously to breathe (Roberts, 1978). Two striking adaptations related to locomotion and predatory behavior are well represented in epipelagic fishes. The first is the “flying” behavior of flyingfishes and their relatives. The other is the use of bills as spears in billfishes for prey capture. Evading the pursuit of a predator in surface waters requires maneuverability. Small fishes are at a distinct speed disadvantage because larger predatory fishes are faster. One way to outmaneuver and out-distance predators is to become airborne. This tactic is seen in many members of the Atheriniformes (e.g., sauries, halfbeaks, needlefishes, and flyingfishes) that are common in the surface waters of the world’s temperate and tropical seas. By leaping out of the water, a flyingfish can double its speed (36 km/hr to 72 km/hr) as a result of the significant reduction in drag (Davenport, 1994). In part, because of the speed and maneuverability of most epipelagic prey, the large predatory billfishes have evolved spears for impaling prey. Bills are elongated extensions of the upper jaws of two groups of billfishes, the marlins, sailfishes, and spearfishes (Istiophoridae), and the swordfish (Xiphiidae). Marlins and relatives possess rough bills that are round in cross-section while swordfish bills are flattened and smooth (broadbills in the vernacular).

Recent direct and indirect evidence points to the inescapable fact that both of these bills are indeed used in foraging. A fortuitous, albeit hair-raising observation, made by two spearfisherman off Durbin, South Africa offered convincing confirmation of this fact (van der Elst and Roxburgh, 1981). One of the free-divers speared an amberjack (Seriola lalandi) weighing about 15 kg. The following observations were then made: The fish pulled off the spear and dashed straight for Roxburgh (at the surface) who simultaneously observed a 3–4 m marlin (probably a black marlin, Makaira indica) making a direct charge for the amberjack which was now hiding behind him. At the last moment the marlin halted and Roxburgh was able to push the bill aside after which the marlin circled (the) diver and amberjack several times. Seconds later the amberjack dashed off at great speed to the bottom, closely followed by the highly agitated marlin. Within an estimated 5 sec the marlin had reached its prey and impaled it on its bill. The marlin then shook the amberjack free and swallowed it. Duration of the entire incident was an estimated 30–50 sec (van der Elst and Roxburgh, 1981, p. 215).

Swordfish appear to use their broadbill like a broad sword. They use it to decapitate cephalopod prey and slash them into swallowable pieces. Like marlins, swordfish are also known to slash schooling prey with their bills and return to pick up maimed fish on subsequent passes (Wisner, 1958; Ellis, 1989).

Schooling Schooling is major characteristic of fishes inhabiting the epipelagic zone world-wide (Smith, 1981) and this is certainly true for pelagic fishes off California. School structure and behavior of several of the common species off California (northern anchovy, in particular) have received a great deal of attention in the past. Within a species, schooling can vary from well-defined, compact aggregations to widespread, scattering layers (Mais, 1974). Commercial fishermen recognize more than a dozen different school types among eastern Pacific tunas (Scott, 1969; Scott and Flittner, 1972). The formation of schools among clupeioids depends largely on vision, but the maintenance of school structure depends on vision and lateral line stimuli (Blaxter and Hunter, 1982; Partridge, 1982; Parrish, 1989a,b). The formation and maintenance of schools is also affected by light level. Schooling fish are randomly distributed in darkness; they join groups that form and disperse as light levels rise, then form compact schools as light levels rise still further (Hunter, 1968; Hunter and Nicholl, 1985). Schooling increases intraspecific competition for food, but the disadvantages must be outweighed by reduction in predation and by facilitation of reproduction (Smith, 1978a; Blaxter and Hunter, 1982). Smith (1978a) defined four spatial scales for pelagic schooling fishes: behavioral (scale of aggregation caused by individual behavior, that is, the fish school); hydrographic (scale that attracts and keeps fish in a small geographic area, e.g., upwelling and zooplankton blooms); physiological (distribution of a species determined by its physiological limits); and external (scale at which food or predators enter the environment of a species from outside its area of distribution). Individual epipelagic fish schools aggregate into school groups that occupy areas on the order of 10 km (Smith, 1978a, b). The distribution of school groups is often patchy and nonrandom (Mais, 1974, 1977). There may be 3,500 schools in an area

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10 km in diameter; for anchovies, this represents about 1% of the biomass of the total stock. The school group comprises a wider range of anchovy sizes and ages than an individual school. The hydrographic features that control this scale of aggregation have not been strictly identified (Smith, 1978a), but the importance of biological factors such as vision (Hunter and Coyne, 1982; Hunter and Nicholl, 1985), predation (Butler and Pickett, 1988), prey acquisition (Nonacs et al., 1994), and distribution of prerecruits (Smith et al., 2001) have received attention. Finally, school distribution and formation often change over the course of a day. During the day, northern anchovy occur in small, low-density schools near the surface and in large, loosely compacted schools in deep water (110–220 m). Schools rise to the surface at night and disperse into thin scattering layers. Between midnight and dawn, the fish condense into schools and return to deep water (Messersmith et al., 1969; Mais, 1974, 1977). Schools of jack mackerel remain near the bottom or under kelp canopies in shallow rocky areas during the day, then venture into deeper surrounding areas at night (Mais, 1974). Laboratory experiments suggest that light is sufficient for jack mackerel to maintain schools near the surface on clear, moonless nights and to feed effectively near the surface on full, moonlight nights (Hunter, 1968).

Global Classification of Epipelagic Fishes A surprisingly heterogeneous assemblage of fishes inhabits the epipelagic zone on a global scale. Joining the fishes that normally occupy this seemingly featureless, three-dimensional habitat are species that associate with various rare substrata, those that spend only a portion of their life history in the open ocean, and those that sporadically penetrate into the surface layers beyond the shelf. Parin (1968) provided a thorough classification of the world’s epipelagic fish fauna based on the degree of association with the epipelagic realm. He recognized three main types of epipelagic fishes, holoepipelagic, meroepipelagic and xenoepipelagic (table 12-1; fig. 12-4), as described in the following paragraphs.

Holoepipelagic Fishes This group of fishes includes those that are normally associated with the oceanic epipelagic zone worldwide. These holoepipelagic (holos—all, entire) species are the permanent inhabitants of the oceanic epipelagic and occur there in all life history stages. Holoepipelagic fishes can be divided into two main groups, those that are active swimmers and those that are associated with various animate and inanimate substrata. The active swimmers of the water column include many pelagic sharks, such as oceanic whitetips, porbeagles, makos, basking sharks, and blue sharks. Prominent among the active swimming bony fishes include flyingfishes, sauries, tunas, marlins, swordfish, opah, pomfrets, and ocean sunfishes (fig. 12-5). Parin (1968) stated that most of these holoepipelagic fishes are limited to the isothermic, surface layer and are mainly encountered in tropical waters where a permanent thermocline exists. These species penetrate into temperate and higher latitudes mainly during the summer when seasonal thermoclines develop. The holoepipelagic species noted above normally inhabit only the uppermost layer of the epipelagic to depths of 20–30 m. Other active species occur mainly in the deep layers of the

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oceanic epipelagic zone, adjacent to the mesopelagic zone, and rarely appear near the surface. This lower epipelagic group includes megamouth sharks, lancetfishes, oarfishes, ribbonfishes, crestfishes, opahs, and pomfrets, as well as several species of cutlassfishes and snake mackerels ( fig. 12-6). Finally, some large, predatory fishes such as tunas, marlins, and swordfish feed throughout the epipelagic and may even penetrate into the upper horizons of the main thermocline (Parin, 1968). Species that associate with substrata compose a special group of holoepipelagic fishes. The most specialized and geographically localized of these species include the forms that have evolved to live in association with the floating Sargassum algae of the western portion of the North Atlantic Ocean (Sargasso Sea) (Parin, 1968). The sargassum fish (which is actually an anglerfish, Histrio histrio) and the sargassum pipefish (Syngnathus pelagicus) are the most recognized among these cryptic taxa, although the juveniles of dolphinfish, flyingfish, and many coastal species (halfbeaks, jacks, blennies, triggerfishes, and filefishes) associate with floating Sargassum beds (Parin, 1968). The other, more widespread group of substrate-associated fishes usually lives in symbiosis with other pelagic animals. Members of the bony fish suborder Stromateioidei commonly associate with either inanimate drift or large gelatinous zooplankton including scyphomedusae (sea jellies), siphonophores, and salps (fig. 12-7). In primarily tropical waters, juveniles of the Man-O-War fish (Nomeus gronovii) have an obligatory commensal relationship with the highly venomous siphonphore, Portuguese Man-O-War (Physalia spp.). Juveniles of the centrolophid genera of Centrolophus, Icichthys, and Schedophilus are often found in association with medusae or siphonophores while those of squaretails (Tetragonurus) are sometimes found within the cylindrical colonies of the salp, Pyrosoma (Parin, 1968; Haedrich, 1965; Horn, 1975). Another interesting association occurs between the pilotfish (Naucrates ductor) and a number of large pelagic sharks including the oceanic whitetip and the blue shark (fig. 12-7). Pilotfish are jacks that swim with large, mobile pelagic animals apparently to facilitate locomotion. Several authors (c.f. Parin, 1968) have noted that a small species such as the pilotfish may minimize energy expenditure by swimming in the friction layer encompassing the body of the host. This idea is supported by the observation of other pelagic species such as dolphinfish (Coryphaena hippurus) and rainbow runners (Elegatis bipinnulatus) practicing the same behavior with oceanic whitetip sharks (Parin, 1968). Lastly, a most interesting symbiotic relationship exists between remoras (Echeneidae) and various species of marine vertebrates including sharks (fig. 12-8). This association relies on contact attachment between the remora, also known as suckerfish, and its host by way of a highly evolved sucker disk. This disk is actually a modified, spinous dorsal fin that allows the suckerfish to be carried along with the host with no net expenditure of energy. This contact attachment behavior may have evolved from piloting behavior similar to that seen in Naucrates spp. The various genera and species of suckerfishes exhibit preferences for certain hosts. The slender sucker (Phtheirichthys lineatus) is either free-living or found on sharks. The sharksucker (Echeneis naucrates) is usually found on sharks, but also has been found on sea turtles. The whalesucker (Remilegia australis) is found only on whales and dolphins while remora (Remora remora) is usually found on sharks

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TA B L E 12-1

A Classification of Epipelagic Fishes of the World I. Holoepipelagic (Grk—entire) fishes inhabiting the isothermic surface layer of the ocean at all stages of life history. A. Actively swimming fishes of the upper epipelagic; B. Actively swimming fishes of the lower epipelagic; C. Actively swimming fishes populating all depths of the epipelagic; D. Fishes associated with substrate. 1. Fishes of permanent floating Sargassum beds; 2. Fishes associated with gelatinous zooplankton 3. Fishes associated with large marine vertebrates II. Meroepipelagic (Grk—part) fishes, occurring in the epipelagic at certain stages in life history. A. Epheboepipelagic (Grk—adult) fishes inhabiting the upper layers of the ocean pelagic in the adult stage but spawn nearshore or in freshwater; B. Brephoepipelagic (Grk—babe) fishes, going through the early stages of their life history in the upper layers of the open ocean but inhabiting coastal pelagic or benthic areas as adults; C. Nyctoepipelagic (Grk—nocturnal) fishes, in the adult stage undergoing regular vertical migrations between the epipelagic and mesopelagics, occupying the surface layers at night. III. Xenoepipelagic (Grk—foreign) fishes, permanently occurring in coastal waters but sporadically penetrating into the epipelagic. A. Coastal pelagic fishes B. Coastal benthic fishes

C. Algophilic fishes associating with floating algae (kelp paddies). NOTE:

After Parin, 1968.

F I G U R E 12-4 Parin’s classification of the main groups of epipelagic fishes (after Parin 1968) (BE  rephoepipelagic, EE  epheboepipelagic, and NE  nyctoepipelagic, see text for explanation).

and sea turtles. Gray (Remora brachyptera) and hardfin (Rhombochirus osteochir) marlinsuckers are found on marlins, sailfishes, and swordfish. Lastly, the white suckerfish (Remorina albescens) occurs mainly in the gill cavity of manta rays (Parin, 1968; Miller and Lea, 1972).

the upper layers of the epipelagic and their adult stages in coastal waters are categorized as Brephoepipelagic fishes (brephicos—babe). Finally, Parin viewed those fishes that inhabit deeper, mesopelagic waters during the day and migrate vertically into the surface waters at night to constitute a special type of epipelagic fish group, termed Nyctoepipelagic (nyctios—nocturnal).

Meroepipelagic Fishes E P H E B O E P I P E L AG I C G R O U P

The second major group of epipelagic fishes includes those species that occur in the epipelagic zone only during a portion of their life history. Parin (1968) referred to these as meroepipelagic fishes because they spend part (mero-) of their lives as epipelagic forms. Meroepipelagic forms are biologically diverse and have been classified into three types (Parin, 1968). First, those species that spend their adult lives in the epipelagic, but migrate into coastal waters or freshwater to spawn are termed Epheboepipelagic (ephebos—adult). Second, those species that spend the early stages of their life history in

The most familiar forms of epheboepipelagic fishes are the salmons of the genera Salmo and Oncorhynchus that originally inhabited the cold temperate and boreal waters of the north Atlantic and Pacific oceans. The spawning migrations of salmons into their natal streams are well known and equally well documented (cf. Quinn and Dittman, 1990). Oceanic herring (Clupea harengus) belong to the group and exhibit northern distributions much like salmon. The lower latitude forms in this group include the whale shark (Rhincodon typus), dolphinfish

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F I G U R E 12-5 California representatives of actively-swimming, surface-dwelling holoepipelagic fishes.

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F I G U R E 12-6 California representatives of actively-swimming, deep-dwelling holoepipelagic fishes.

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F I G U R E 12-7 Examples of holoepipelagic substrate symbionts. A. Man-O-War fish (Nomeus gronovii) and host

siphonophore (Physalia sp., does not occur off California); B. California medusafish (Icichthys lockingtoni) and Purple striped sea jelly (Pelagia sp.); C. Juvenile smalleye squaretail (Tetragonurus cuvieri) in lumen of colonial salp (Pyrosoma sp.); D. Driftfish (Psenes pellucidus) under the scyphomedusa (Cyanea sp.); and E. Pilotfish (Naucrates doctor) and remora (Remora remora) accompanying an oceanic whitetip shark (Carcharhinus longimanus). Examples B–E are known to occur off California.

(Coryphaena hippurus), and several species of flyingfishes and halfbeaks. Most of the species above lay eggs in nearshore waters. Whale sharks are ovoviviparious, giving birth in shallow waters. Dolphinfish spawn pelagic eggs where as herrings, halfbeaks, and flyingfishes lay their eggs in floating or attached algae. Typically, the juvenile stages of epheboepipelagic species inhabit the productive, coastal waters and move offshore as they reach maturity.

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B R E P HOE P I P E L AG I C G ROU P

These fishes display a life history strategy that is the opposite of epheboepipelagic species (Parin, 1968). Brephoepipelagic species spend the main part of the life history in coastal waters, but produce larval, post-larval, and juvenile forms that spend a significant amount of time in the oceanic surface waters. Worldwide, certain families of fishes tend to

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F I G U R E 12-8 Examples of two members of the sharksucker family (Echeneidae)

show this strategy, which undoubtedly leads to long distance dispersal in most cases. Parin (1968) noted that greenlings (Hexagrammidae), goatfishes (Mullidae), and soldierfishes (Holocentridae) have extended epipelagic stages. He also included in this group members of the 1) primarily coastal pelagic families, Atherinidae (old world silversides), Scombridae (mackerels), and Carangidae (jacks); 2) coastal benthic families: Synodontidae (lizardfishes), Stichaeidae (pricklebacks), Scorpaenidae (scorpionfishes and rockfishes), Cottidae (sculpins), Acanthuridae (surgeonfishes), Bothidae (left-eye flounders); Cynoglossidae (tonguefishes), and Pleuronectidae (right-eye flounders; and even 3) brackish and freshwater families: Anguillidae (Freshwater eels) and Mugillidae (mullets).

NYCTOE P I P E LAG IC

These vertical migrators are best represented by members of the families: Myctophidae (lanternfishes), Gonostomatidae (bristlemouths), Dalatiidae (dwarf sharks), Stomiidae (dragonfishes), and Gempylidae (snake mackerels). Although Parin (1968) considered this group of fishes to be nocturnal epipelagics, the vast majority of classification schemes of marine fishes consider these to be mesopelagic forms (see Chapter 13 for detailed discussion).

Xenoepipelagic Fishes The third and last major group of epipelagic fishes in Parin’s (1968) scheme includes those species that sporadically pene-

trate into the epipelagic realm from another habitat. Such fishes are termed xenoepipelagic (xenos—foreign). Parin recognized two main groups of xenoepipelagic fishes: 1) coastal pelagic species, that migrate offshore into pelagic waters on an irregular basis and 2) algophilic species, which associate with floating algae (kelp paddies). Coastal pelagic species that often occur very far offshore, particularly in upwelling areas, include anchovies (Engraulidae), sardines, herrings (Clupeidae), jacks (Carangidae), and some species of flyingfishes (Exocoetidae). Algophilic species from coastal waters often become associated with floating algae either through displacement with the algae from shallow water or by recruiting from the plankton to the floating paddy. Such species include pipefishes (Syngnathidae), triggerfishes (Balistidae), porcupinefishes (Diodontidae), and juveniles of many nearshore species (e.g., Kyphosidae, Carangidae, and Scorpaenidae).

Epipelagic Fishes of the Californias The holoepipelagic fish fauna off the coast of the Californias reflects the diverse nature of the water masses converging on this vast area of the northeastern Pacific Ocean (see fig. 12-11, chapter 11). The California Current dominates the northern portion of the region, transporting cold surface water south over much of this range. This transport results in an epipelagic fauna dominated by boreal and temperate forms over much of the year. The warm water species are normally restricted to the southernmost portion of this region (central to southern Baja California). Each summer, however, tropical forms move northward with the warming surface waters to

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TA B L E 12-2

Characteristic Species of Epipelagic Fishes in the Main Biogeographical Regions of the Eastern North Pacific

Characteristic Species Eastern North Pacific

Holoepipelagic

Meroepipelagic

Xenoepipelagic

Boreal

Salmon shark, daggertooth, longnose lancetfish, ragfish

chinook salmon, coho salmon, Pacific herring

Temperate

Basking shark, blue shark, Pacific saury, opah, bigscale pomfret, escolar, bluefin tuna, albacore, swordfish, medusafish, smalleye squaretail, ocean sunfish

California flyingfish

Northern anchovy, Pacific sardine, Pacific butterfish, chub mackerel, Pacific bonito, jack mackerel, California barracuda, Yellowtail

Tropical

Shortfin mako, oceanic whitetip,

Whale shark, dolphinfish,

Manta ray, sailfish, black marlin,

pygmy shark, pelagic stingray, Pacific saury, darkwing flyingfish, opah, oarfish, snake mackerel, oilfish, skipjack, yellowfin tuna, bigeye tuna, striped marlin, blue marlin, swordfish, louvar, cigarfish, Pacific squaretail, man-o-war fish, oceanic puffer, ocean sunfish, slender mola NOTE:

wahoo

After Parin, 1968.

feed or reproduce. This northward migration intensifies during ENSO events resulting in tropical forms penetrating into much higher latitudes than is seen in more neutral years (see chapter 1).

Boreal Region The holoepipelagic ichthyofauna of the boreal region of the northeastern Pacific is fairly depauperate commonly including only four species (table 12-2). The salmon shark (Lamna ditropis) is joined by three, predatory species that are normally associated with the deep epipelagic realm in more southerly latitudes. These three species, daggertooth (Anotopterus pharao), longnose lancetfish (Alepisaurus ferox), and ragfish (Icosteus aenigmaticus), normally occur with the salmon shark off northern California, but can extend farther south during cold water years. The meroepipelagic group dominates the fish fauna of the boreal region off California and northward and includes chinook (Oncorhynchus tyshawytscha) and coho (O. kisutch) salmon and Pacific herring (fig. 12-9).

Temperate Region The epipelagic ichthyofauna off California has been characterized historically as temperate in character (table 12-2). Furthermore, it is numerically dominated by several low trophic-level species that are common to the coastal pelagic (xenoepipelagic) realm. Because the waters off central and northern California represent a major upwelling area, many of these coastal pelagic species may occur far offshore (see chapters 3 and 4, and California Current section at end of

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the current chapter). Chief among these species are northern anchovy (Engraulis mordax) and Pacific sardine (Sardinops sagax), which have alternated as the most abundant fishes of the coastal pelagic zone off California throughout recent history and are among the best studied of all California species because of their commercial importance (Mais, 1974; Squire, 1983) (fig. 12-10). In addition, Pacific pompano (Peprilus simillimus), chub mackerel (Scomber japonicus) and jack mackerel (Trachurus symmetricus) are abundant, low-level carnivores that often occur in open ocean waters far from shore. This group also includes three piscivorous species, California barracuda (Sphyraena argentea), Pacific bonito (Sarda chiliensis), and yellowtail (Seriola lalandi) which are common in waters off of Baja California and enter southern California during the spring and summer months of most years (fig. 12-11). True holoepipelagic species (fig. 12-5) of the uppermost portions of the offshore water column include blue shark (Prionace glauca), basking shark (Cetorhinus maximus), and Pacific saury (Cololabis saira). Active swimmers of the deeper regions of the temperate epipelagic include opah (Lampris regius), bigscale pomfret (Taractes longipinnis), and escolar (Lepidocybium flavobrunneum). Large, active swimmers of depths throughout the epipelagic zone include albacore (Thunnus alalunga), bluefin tuna (T. thynnus), and swordfish (Xiphias gladius). Research on the daily activities of ocean sunfish (Mola mola) indicate that this species makes regular vertical migrations between the surface and lowest portions of the epipelagic zone, and is best placed in the same ecological group as the tunas and swordfish (Cartamil and Lowe, 2004). The medusa fish (Icichthys lockington), blackrag (Psenes pellucidus), smalleye squaretail (Tetragonurus cuvieri) are all cooler water, stromateioid fishes that associate with

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F I G U R E 12-9 California representatives of epheboepipelagic fishes (epipelagic adults that breed nearshore or in freshwater) arranged from north to south in occurrence.

medusa and salps as juveniles and become holoepipelagic as adults.

Tropical Region Parin (1968) noted that the majority of truly holoepipelagic forms are restricted to the isothermic surface layer that occurs mainly in the tropics because of the permanent thermocline that exists there. This restriction is certainly true for the tropical waters of the northeastern Pacific, where the greatest diversity of holoepipelagic forms has been recorded. This

fauna normally exists in the waters to the south of the Californias, but regularly enters the southern region off Baja and southern California in the summer months (Bedford and Hagerman, 1983; Cailliet and Bedford, 1983; Cross and Allen, 1993). This tropical fauna includes shortfin mako (Isurus oxyrhynchus), oceanic whitetip (Carcharhinus longimanus), pelagic stingray (Dasyatis violacea) and the small, deeper dwelling, pygmy shark (Euprotomicrus bispinatus). Representative bony fishes of the surface layers include Pacific saury, several species of flyingfishes, including darkwing flyingfish (Hirundichthys rondeletii), and skipjack tuna (Katsuwonus pelamis). Several other

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F I G U R E 12-10 California representatives of xenoepipelagic fishes (coastal pelagic).

relatively rare, tropical species have been recorded in small numbers off California including: slender snipefish (Macrorhamphosus gracilis), oceanic puffer (Lagocephalus lagocephalus), and slender mola (Ranzania laevis). Dolphinfish (Coryphaena hippurus) is also an abundant meroepipelagic fish in the surface layers, particularly around floating objects (Mitchell and Hunter, 1970; Kingsford and Defries, 1999). Tropical waters also support a diverse group of deep epipelagic forms that penetrate into the upper regions of the mesopelagic zone and are rarely seen at the surface. These species are sometimes found in the temperate zone and include: opah, escolar, and other rare, specialized forms such

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as ribbon-like lampridiform fishes (oarfish, Regalaceus glesne; highbrow crestfish, Lophotus cristatus; and king-of-the-salmon, Trachipterus altivelis), gempylids (snake mackerel, Gempylus serpens and oilfish, Ruvettus pretiosus), cutlassfish (Pacific cutlassfish, Trichiurus nitens), and louvar (Louvaris imperalis), an oceanic acanthuroid (surgeonfish) (Fig. 12-5 and 12-6). Large tropical tunas, (yellowfin, Thunnus albacares; and bigeye, T. obesus), marlins (striped, Tetrapterus audax; and blue, Makaira nigricans), swordfish, and ocean sunfish inhabit a broad depth range within epipelagic zone. These large, holoepipelagic fishes are encountered at all depths within the epipelagic zone and often make feeding excursions into the main thermocline.

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F I G U R E 12-11 Commercial Passenger Fishing Vessel (CPFV) monthly catches of four species of tunas (top) and three species of coastal pelagic fishes in California from 1974 to 1978.

Greenlings, most notably lingcod (Ophiodon elongates) and kelp greenling (Hexagrammus decagrammus), have pelagic juvenile stages and recruit to shallow, benthic nursery areas at relatively large sizes. Cabezon (Scorpaenichthys marmoratus), the largest cottid, and many scorpaenids (including genera, Scorpaena, Sebastes, and Sebastolobus) also produce pelagic juveniles that remain in the epipelagic zone for extended periods and attain lengths between 30–50 mm SL (O’Connell, 1953; Ambrose, 1996a, Ambrose, 1996b; Moser, 1996; Love et al., 2002). These scorpaenids are loosely aggregating, benthic fishes that live on mud from 60–600 m depth (M. J. Allen, 1982; Cross, 1987). In the south, prejuveniles (10–14 mm SL) of splitnose rockfish (Sebastes diploproa) congregate in surface waters under drifting objects, such as kelp patties (Mitchell and Hunter, 1970) from August through December. Juveniles at 40–50 mm SL emigrate from the surface waters in April and May (Boehlert, 1977), descend to 200–250 m depth, and migrate horizontally until they contact the bottom (Moser and Ahlstrom, 1978). The two scorpaenid genera, Sebastes and Sebastolobus, are represented in fig. 12-12 by the boccacio and longspine thornyhead. Pleuronectids (right-eyed flatfish), such as the Dover sole (Microstomus pacificus) (fig. 12-12) and rex sole (Erres zachirus) have large, leaf-like larval/juvenile phases that are transparent and can remain pelagic for up to a year (Charter and Moser, 1996). Off southern and Baja California, striped mullet (Mugil cephalus) and several species of blennies (Hypsoblennius spp.) are brephoepipelagic with the latter having an extended neustonic phase (Sandknop and Watson, 1996; Watson, 1996). The productive California Current system is actually dominated by coastal pelagic fishes that are more properly considered xenoepipelagic forms in Parin’s classification and are discussed in the following section.

The California Current System Stromateioid fishes are also well represented in the tropical epipelagic realm and are usually associated with floating objects, including medusae, siphonophores, and salps. Various species of cigarfish (Cubiceps spp.), squaretails (Tetragonurus spp), driftfishes (Psenes spp.) all associate with flotsam or gelatinous zooplankton on the high seas and have been variously recorded off the Californias (Miller and Lea, 1976; Fitch and Lavenberg, 1968). The Man-O-War fish, Nomeus gronovii, inhabits the surface layers of the tropical regions of the eastern north Pacific in association with the siphonophore Physalia sp. (Allen and Robertson, 1994). The occurrence of Nomeus off southern Baja California is probably associated only with ENSO events. Prominent meroepipelagic (epheboepipelgic) fishes of the tropical province of the eastern north Pacific that have been recorded off California include the aforementioned dolphinfish, whale shark (Rhincodon typus), the largest living fish, and ribbon halfbeak (Euleptorhamphus viridis). Manta (Manta birostris), sailfish (Istiophorus platypterus), black marlin (Makaira indica), and wahoo (Acanthocybium solandri) are probably better classified as xenoepipelagic because they sporadically occur far from shore in the epipelagic realm (table 12-2). The surface waters off the Californias also support an important group of fishes that occupy the epipelagic zone only during their early life history stages (see also chapter 10— Ichthyoplankton). This brephoepipelagic group (Parin, 1968) includes a diverse array of species that have extended pelagic juvenile stages (fig. 12-12). In higher latitudes, many scorpaenifiorm fishes qualify as brephoepipelagic species.

Species Composition and Abundance The fish fauna of the California Current system is dominated by small, planktivorous schooling fishes such as: northern anchovy, Pacific sardine, jack mackerel and chub mackerel (Mais, 1974, 1977; Parrish et al., 1981; Squire, 1983b). The population ecology and biology of the pelagic planktivores is well known (table 12-3) because they have supported important commercial fisheries in the past; far less is known about the large predatory fishes, such as albacore, bluefin tuna, and opah. Parrish et al. (1981) emphasized that pelagic fishes that spawn throughout the California Current region during the more productive upwelling periods usually suffer a great loss of larvae via offshore surface transport. Northern anchovy, Pacific sardine, jack mackerel, chub mackerel, and Pacific hake are residents of this system, and their reproductive strategies are adapted to its flow characteristics (Parrish et al., 1981; Cross and Allen, 1993). Parrish et al. (1981) separated the California Current system into four distinct units based on fisheries data, surface transport characteristics, and reproductive characteristics of fish populations: 1) the Pacific Northwest region from Vancouver Island south to Cape Blanco, 2) the region of maximum upwelling between Cape Blanco and Point Conception, 3) the Southern California Bight from Pt. Conception south to Pt. Eugenia, and 4) the southern Baja California Region. Coastal fishes with pelagic larvae in the Pacific Northwest region tend

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F I G U R E 12-12 California representatives of brephoepipelagic fishes (coastal adults that have pelagic juvenile

stages).

to spawn in the winter when the wind drift of surface waters is directed toward the coast. The region of vigorous upwelling between Cape Blanco and Pt. Conception (northern and central California), where offshore transport occurs year-round, has few locally spawning fishes. Instead, the region is dominated by large stocks of migratory planktivorous fishes (e.g., northern anchovy, Pacific sardine, jack mackerel, and chub mackerel) that spawn in the more favorable wind drift conditions found farther south in the Southern California Bight and off southern Baja. The closed gyral circulations that characterize these regions foster favorable conditions for spawning that have lead to more-or-less distinct subpopulations of these

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coastal pelagic species. The reliance of spawning success upon surface drift conditions in the California Current is probably responsible for the wide, year-to-year fluctuations in population size that is characteristic of these important fisheries species. Anomalies in the surface transport caused by ENSO and other climatic events have dramatic impacts on such populations. Large-scale, fisheries-independent assessments of California pelagic fish populations where juvenile and adult fishes were physically captured are largely limited to two midwater trawl studies conducted from 1950 to 1951 (Radovich, 1952) and from 1966 to 1971 (Mais, 1974) (table 12-4). In the earlier

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TA B L E 12.3

Research Conducted on the Biology of Economically Important Pelagic Species Off California

Pelagic Species

References

Northern anchovy (Engraulis mordax)

Bagarinao and Hunter (1983), Booman et al. (1991), Butler (1990), Butler and Pickett (1988), Checkley et al. (2000), Coyer and Hall (1993), Folkvord and Hunter (1986), Hunter (1972), Hunter (1976), Hunter (1977), Hunter (1985), Hunter and Coyne (1982), Hunter and Dorr (1982), Hunter and Goldberg (1980), Hunter and Kimbrell (1980), Hunter and Leong (1981), Hunter and Macewicz (1980), Hunter and Macewicz (1985a), Hunter and Macewicz (1985b), Hunter and Nicholl (1985), Hunter and Sanchez (1977), Hunter and Thomas (1974), Hunter et al. (1981), Hunter et al. (1979), Hunter et al. (1985), Jacobson et al. (1994), Kaupp and Hunter (1981), Moser and Pommeranz (1999), Nonacs et al. (1994), Nonacs et al. (1998), Nonacs et al. (1998), Owen et al. (1990), Santander et al. (1984), Smith (1972), Smith (1980), Smith et al. (1983), Smith et al. (1985), Smith et al. (1989), Vetter et al. (1999), Vlymen (1977), Vrooman and Smith (1971) Arenas et al. (1996), Alvarez and Butler (1992), Arenas et al. (1996), Brewer and Smith (1982), Butler (1991), Butler and Pickett (1988), Butler and de Mendiola (1985), Butler et al. (1993), Butler et al. (1996), Castillo et al. (1985), Checkley et al. (2000), de la Campa et al. (1976), Jacobson and MacCall (1995), Kramer and Smith (1971), Lasker (1970), Lo et al. (1995), Lo et al. (2001), Logerwell (2001), Logerwell and Smith (2001), MacCall (1979), Macewicz et al. (1996), Mallicoate and Parrish (1981), Schwartzlose and Smith (1989), Silliman (1943), Smith (1973), Smith (1990), Smith et al. (2001), Smith et al. (1983), Smith et al. (1989), Smith et al. (1992), Wada and Jacobson (1998), Wolf and Smith (1985), Wolf and Smith (1986), Wolf et al. (1987) Hunter (1968), Hunter (1969), Hunter (1971), Hunter and Zweifel (1971), Kramer and Smith (1970), Macewicz and Hunter (1993), Mallicoate and Parrish (1981), Mason (1991), Pritchard et al. (1971) Dickerson et al. (1992), Hunter and Kimbrell (1980), Knaggs and Parrish (1973), MacCall et al. (1985), Mallicoate and Parrish (1981), Parrish and MacCall (1978) Bertignac et al. (1999), Bayliff (2001), Dotson and Graves (1984), Dotson et al. (1984), Dotson et al. (1989), Dotson (1976), Dotson (1978), Dotson (1980), Finneran et al. (2000), Hunter et al. (1986), Laurs and Dotson (1983), Laurs and Lynn (1991), Laurs et al. (1981), Laurs et al. (1982), Laurs (1989), Pinkas et al. (1971), Schaefer and Oliver (2000), Sharp and Dotson (1977) Barrett et al. (1998), Hinton (2001), Hinton et al. (2002)

Pacific sardine (Sardinops sagax)

Jack mackerel (Trachurus symmetricus) Pacific chub mackerel (Scomber japonicus) Tunas (Thunnus, Katsuwonus)

Billfishes

(Makaira, Xiphias)

study, which occurred prior to the collapse of the California sardine fishery, the catch was dominated nearly equally by northern anchovy (35.8%) and Pacific sardine (35.2%), followed by jack mackerel (22.2%) and chub mackerel (6.7%). By the 1960s, the northern anchovy (68.1%) dominated the catch in midwater trawls. Jack mackerel ranked second (18.3%) and Pacific hake (10.5%) ranked third (Mais, 1974). Another fisheries-independent study involved an aerial monitoring program from 1962 to 1978, covering much of California and Baja California coastline (Squirre, 1983). This study reported sightings and estimated abundances of schools of small planktivorous and larger predatory fish species that were observed near the surface from low flying aircraft (table 12-5). Over the 16 years of aerial observations, northern anchovy and jack mackerel were the most abundant species spotted off central California and a number of basking sharks were also observed. Northern anchovy and jack mackerel dominated sightings off southern California, followed by bluefin tuna and chub mackerel. Pacific bonito and albacore tuna constituted a lesser, but important portion of the estimated abundance. Off northern Baja, aerial sightings were dominated by tunas and their relatives, including bluefin, Pacific bonito, and albacore followed by northern anchovy and chub mackerel. In the decades of the 1970s and 1980s, northern anchovy dominated the catch of all smaller-scale sampling programs

that use round-haul nets. Commercial purse seine hauls made at night in the surface waters of Monterey Bay contained 99.9% northern anchovies, which is not surprising because anchovies were the targeted species (Cailliet et al., 1979). In addition to anchovies, seine hauls collected a mixed group of both coastal pelagic and benthic species. Pacific herring were captured in lower abundance along with night smelt (Spirinchus starksi) and Pacific sauries. Largely benthic species, such as plainfin midshipman (Porichthys notatus) and Pacific electric ray (Torpedo californica), composed a surprisingly large portion of the remaining catch in these night-time hauls supporting the hypothesis that they rise into the water column at night to feed. Another type of round-haul net, a lampara net, was used to assess the populations of coastal pelagic fishes off of San Onofre (Allen and DeMartini, 1982—see chapter 6). Again, northern anchovies dominated the catches, particularly in the offshore sets. In addition to anchovies, southern, coastal pelagic species, including chub mackerel, jack mackerel, Pacific bonito, and California barracuda, were all well represented in the catches. Beginning in the late 1970s through to the present time, most fisheries-independent, population assessments of California Current fishes (primarily northern anchovy and Pacific sardine) have been indirect in nature. Fisheries-related studies have focused on distribution and biomass estimation

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TA B L E 12-4

TA B L E 12-5

Relative Abundance of Epipelagic Fishes by Region off California Determined by Midwater Trawl Survey

Mean Abundance of Epipelagic Fishes by Region off California Determined by Air Born Fish Monitoring

Midwater Trawls

Species Northern anchovy Jack mackerel Pacific sardine Pacific hake Chub mackerel

Pacific saury

Radovich (1952) 1950–51

Mais (1974) 1966–71

35.8 22.2 35.3

68.1 18.3 1.7 10.5 0.9

6.7

0.5

NOTE: Surveys from 1950 to 1952 (Radovich 1952) and 1966 to 1971 (Mais, 1973).

1962–1978 Species

Cencal

Region Socal

Nobaja

Northern anchovy Bluefin tuna Jack mackerel Pacific bonito Albacore tuna Basking shark Chub mackerel White seabass Pacific sardine Yellowtail

39.1 0.0 30.3 2.3 0.00 17.2 0.6 6.4 3.8 0.1

31.4 20.2 25.2 5.5 2.2 1.4 10.5 1.4 1.7 0.2

9.3 45.1 1.3 21.1 17.8 0.0 4.8 0.0 0.3 0.1

0.1

0.1

0.1

California barracuda NOTE:

based on: 1) egg and larval densities (Smith et al., 1985; Wolf and Smith, 1985; Wolf and Smith, 1986; Wolf et al., 1987; Butler, 1991; Arenas et al., 1996; Moser and Pommeranz, 1999; Checkley et al., 2000; Lo et al., 2001; Smith et al., 2001) and 2) hydroacoustic (sonar) surveys (Mais, 1977; Smith, 1978; Hewitt and Smith, 1979; Holiday and Larson, 1979); 3), lidar (airborne laser) surveys (Churnside and Hunter, 1996; Lo et al., 1999); and 4) computer modeling (Jacobson et al., 1994; Jacobson and MacCall, 1995; Lo et al. 1995). Published assessments of the populations of large predatory fishes of the epipelagic realm off the Californias are rare. Hanan et al. (1993) compiled the catch data (landings) from the commercial drift net fishery operating offshore from northern to southern California from 1981 to 1991. This fishery used large mesh nets and targeted swordfish, thresher sharks, and shortfin makos, that constituted the bulk of the catch, but captured a wide variety of other epipelagic fishes (table 12-6). All five major tuna species (bluefin, albacore, yellowfin, bigeye, and skipjack) were well-represented in the catch along with ten species of shark (common thresher, shortfin mako, bigeye thresher, soupfin, hammerhead, blue, pelagic thresher, salmon, white, and dusky) and two oceanic bony fishes (opah and louvar). The remainder of the catch was composed largely of coastal pelagic species (e.g. white seabass (Atractoscion nobilis), Pacific bonito, California barracuda, and chub mackerel). More recently, catch data from the Oregon-California drift net fleet from 1990 to 2002 has become available (table 12-7). These data were collected by onboard observers of the National Marine Fisheries Service and included several, non-fisheries species that are captured, but not normally brought back to landings. One such species, the ocean sunfish ranked first in the catch over the 13-year period. Obviously, ocean sunfish are much more common in the surface waters off California than had been reported from previous, fishery-dependent data. Fisheries-dependent assessments continue to dominate as indicators of population status for fisheries management purposes. Commercial landings over the past 70 years document large fluctuations in northern anchovy, Pacific sardine, and chub mackerel biomass that are attributable largely to fluctuations in recruitment. Anchovy biomass was high in the early 1970s because of favorable environmental conditions, low adult mortality, and above average recruitment (Methot,

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Program from 1963 to 1978 (Squire, 1983).

1982). The subsequent decline in northern anchovy abundance was attributed to a return to more normal environmental conditions, increased fishing pressure, predation by an expanding chub mackerel population (Mais, 1981; MacCall et al., 1985), and possible interspecific competition with an expanding Pacific sardine population (Wolf et al., 1987; Butler, 1991; Smith et al., 2001; Jacobson et al., 1994). After almost four decades of depressed population levels, the Pacific sardine had once again returned to prominence in the California Current with commercial catches exceeding those of northern anchovies by an order of magnitude by 1999 (Wolf and Smith, 2001). Long-term changes in the fisheries of these two, numerically dominate species are discussed in detail in chapter 25. Recruitment success in chub mackerel has also been roughly cyclical since the 1930s (MacCall et al., 1985). The total biomass of chub mackerel, one of the most thoroughly studied and variable fisheries in the world, exploded threetimes in the last 70 years (MacCall et al., 1985; Prager and MacCall, 1988; Konno and Wolf, 2001) and at least once in the 1800s (Soutar and lsaacs, 1974). Reproductive success of chub mackerel in 1976 at the beginning of the most recent population increase was about 750 times reproductive success in 1983 (Parrish and MacCall, 1978).

Future Research We hesitate before recommending future directions of research because studies of this expansive habitat and its fishes will undoubtedly require large-scale efforts from commercial and research vessels and equally large budgets. At present, the limited funding for oceanographic and fisheries research off California does not bode well for such endeavors. Never-theless, we believe the following avenues of study would yield valuable information. 1. Fisheries independent quantitative studies should be undertaken to estimate the standing stocks of epipelagic organisms including fishes at the various trophic levels. If the formidable logistic hurdles can be overcome, such an investigation would yield critical

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TA B L E 12-6

TA B L E 12-7

Total Catch of Large Epipelagic Fishes off of California Taken by Commercial Drift Nets from 1981 to 1991

Summary of All Fish Observed Caught in the California/Oregon Drift Gillnet Fishery from 1990 to 2002

Species

Catch (kg)

% Wt

Species

Swordfish Common thresher Shortfin mako Opah Albacore Bigeye thresher White seabass Yellowfin tuna Pacific bonita Soupfin shark Louvar Bigeye tuna Bluefin tuna Skipjack tuna Hammerhead shark Yellowtail Blue shark California barracuda Pelagic thresher Chub mackerel Jack mackerel Salmon shark Dolphinfish White shark Pacific butterfish Pacific sardine Dusky shark Wahoo

9,334,408 4,687,869 1,190,495 524,990 452,789 178,089 54,444 53,729 49,635 36,795 30,608 28,473 23,251 22,851 21,976 19,565 19,340 19,001 12,757 7,849 2,043 1,714 581 554 198 143 79 64

55.6 27.9 7.1 3.1 2.7 1.1 0.3 0.3 0.3 0.3 0.3 0.3 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1

Common Mola Blue Shark Albacore Swordfish Skipjack Tuna Shortfin Mako Shark Pacific Mackerel Common Thresher Shark Opah Bluefin Tuna Bullet Mackerel Louvar Yellowfin Tuna Pacific Pomfret Bigeye Thresher Shark Pacific Bonito Striped Marlin Pacific Hake Pelagic Stingray Jack Mackerel Remora Salmon Shark Pelagic Thresher Shark Yellowtail Blue Marlin Smooth Hammerhead Shark Pacific Sardine Pacific Electric Ray California Barracuda Bigeye Tuna Manta Bat Ray Oarfish Northern Anchovy White Seabass plus 21 species 0.01 including black marlin, soupfin shark, white shark, megamouth shark, dolphinfish, basking shark, king of the salmon, dolphinfish and sailfish

TOTAL NOTE:

16,774,291

Hanan et al., 1993.

information on energy flow and dynamics of the pelagic realm. These studies could utilize hydroacoustic and/or LIDAR technologies in conjunction with ground-truth sampling with large midwater trawls and purse seines to enhance resolution at the species-level. 2. Population abundance assessments may still be made via large-scale tag-and-recapture studies. Satellite and other types of radio-tagging studies should continue to examine horizontal and vertical movements of large pelagic fishes (see chapter 20—Fish Movement & Activity Patterns). 3. Many ecomorphological and ecophysiological studies of the adaptations to pelagic realm by oceanic and coastal pelagic fishes remain to be undertaken. The learned works of Alexander (1990), Bone (1972), Bone and Roberts (1969), Magnuson (1973, 1978), and Marshall (1960, 1972), as described in Pelster (1977) have only scratched the surface. 4. Time series analyses of data from fisheries-dependent assessments of all pelagic fishes, large and small, must be continued and extended in order to track the effects of both exploitation and large-scale oceanographic variation.

TOTAL

Total

% Total

34,704 19,978 15,564 13,205 7,270 5,170 4,834 4,688 3,406 3,255 2,962 607 463 453 413 357 322 255 253 141 101 99 77 51 49 42 40 33 29 20 14 9 8 7 7

29.18 16.80 13.09 11.10 6.11 4.35 4.06 3.94 2.86 2.74 2.49 0.51 0.39 0.38 0.35 0.30 0.27 0.21 0.21 0.12 0.08 0.08 0.06 0.04 0.04 0.04 0.03 0.03 0.02 0.02 0.01 0.01 0.01 0.01 0.01

118,886

NOTE: Data were collected at sea by NMFS observers and represents a total of 6,346 sets. See: http://swr.nmfs.noaa.gov/psd/codgftac.htm.

Literature Cited Alexander, R.M. 1990. Size, speed and buoyancy adaptations in aquatic animals. Am. Zool. 30:189–196. Allen, G.R., and D.R. Robertson. 1994. Fishes of the tropical eastern Pacific University Hawaii Press, Honolulu. Allen, L.G., and E.E. DeMartini. 1983. Temporal and spatial patterns of nearshore distribution and abundance of the pelagic fishes off San Onofre, Oceanside, California. U.S. Fish. Bull. 81(3):569–586. Alvarez, F. and J.L. Butler. 1992. First attempt to determine birthdates and environmental relationship of juvenile sardine, Sardina pilchardus (Walb.), in the region of Vigo (NW Spain) during 1988. Biol. Inst. Exp. Oceanogr. 8:115–121. Ambrose, D.A. 1996a. Hexagrammidae. In Moser, H.G. (ed), The early stages of the fishes in the California current region. CalCOFI Atlas No. 33, p. 811–820.

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Ambrose, D.A. 1996b. Cottidae. In Moser, H.G. (ed), The early stages of the fishes in the California current region. CalCOFI Atlas No. 33, p. 821–840. Arenas, P.R., J.R. Hunter, and L.D. Jacobson. 1996. The 1994 MexicoU.S. spawning biomass survey for Pacific sardine (Sardinops sagax) and the 1995 CalCOFI Sardine Symposium. CalCOFI Rep. 37:129–133. Bagarinao, T. and J.R. Hunter. 1983. The visual feeding threshold and action spectrum of northern anchovy (Engraulis mordax) larvae. CalCOFI Rep. 24:245–254. Bakun, A. 1986. Definition of environmental variability affecting biological processes in large marine ecosystems. In: K. Sherman, and L.M. Alexander, eds. Variability and Management of Large Marine Ecosystems. Am. Assoc. Adv. Sci., Selected Symp. 99. Westview Press, Boulder, CO. pp. 80–108. Barrett, Izadore, Oscar Sosa-Nishikawa, and Norman Bartoo (eds.) 1998. Biology and fisheries of swordfish, Xiphias gladius. NOAA Tech. Rep. NMFS 142. Baxter, J.L. 1960. A study of the yellowtail, Seriola dorsalis (Gill). Calif Dept. Fish Game Fish Bull. No. 110. Bayliff, William H. 2001. Status of bluefin tuna in the Pacific Ocean. Inter-Amer. Trop. Tuna Comm., Stock Assess. Rep., 1: 211–254. Bedford. D.W., and F.B. Hagerman. 1983. The billfish fishery resource of the California Current. CalCOFI Rep. 24: 70–78. Bernal, P.A. 1981. A review of the low-frequency response of the pelagic ecosystem in the California Current. CalCOFI Rep. 22:49–62. Berry, F.H., and H.C. Perkins. 1966. Survey of pelagic fishes of the California Current area. U.S. Fish. Bull. 65: 625–682. Bertignac, M., J. Hampton, and A. Coan. 1999. Estimates of exploitation rates for north Pacific albacore, Thunnus alalunga, from tagging data. Fish. Bull. 97 (3):421–433. Blaxter, J.H.S., and J.R. Hunter. 1982. The biology of the clupeoid fishes. In: J.H.S. Blaxter, F.S. Russell, and M. Younge, eds. Advances in Marine Biology. Vol. 20. Academic Press, London. Boehlert, G.W. 1977. Timing of the surface-to-benthic migration in juvenile rockfish, Sebastes diploproa, off southern California. U.S. Natl. Mar. Fish. Serv. U.S. Fish. Bull. 75:887–890. Bone, Q. 1972. Buoyancy and hydrodynamic functions in integument in the castor oil fish, Ruvettus pretiosus (Pisces: Gempylidae). Copeia, 72: 78–87. Bone, Q., and B.L. Roberts. 1969. The density of elasmobranches. J. Mar. Biol. Assoc. U.K. 49:913–937. Booman, C., A. Folkvord, and J.R. Hunter. 1991. Responsiveness of starved northern anchovy Engraulis mordax larvae to predatory attacks by adult anchovy. U.S. Fish. Bull., U.S. 89(4):707–711. Brewer, G.D., and P.E. Smith. 1982. Northern anchovy and Pacific sardine spawning off Southern California during 1978–1980: Preliminary observations on the importance of the nearshore coastal region. CalCOFI Rep. 23:160–171. Butler, J.L. 1990. Growth during the larval and juvenile stages of the northern anchovy, Engraulis mordax, in the California Current during 1980–84. U.S. Fish. Bull. 87:645–652. Butler, J.L. 1991. Mortality and recruitment of Pacific sardine, Sardinops sagax caerulea, larvae in the California Current. Can. J. Fish. Aquat. Sci. 48: 1713–1723. Butler, J.L., and B. Rojas de Mendiola. 1985. Growth of larval sardines off Peru. CalCOFI Rep., Vol. XXVI. 113–117. Butler, J.L., and D. Pickett. 1988. Age specific vulnerability of Pacific sardine (Sardinops sagax) to predation by northern anchovy (Engraulis mordax). U.S. Fish. Bull. 86: 163–167. Butler, J.L., M.L. Granados G., J.T. Barnes, M. Yaremko, and B. J. Macewicz. 1996. Age composition, growth and maturation of the Pacific sardine, Sardinops sagax, during 1994. CalCOFI Rep. 37:152–159. Butler, J.L., P.E. Smith, N.C.H. Lo. 1993. The effect of natural variability of life-history parameters on anchovy and sardine population growth. CalCOFI Rep. 34:104–111. Cailliet, G.M., and D.W. Bedford. 1983. The biology of three pelagic sharks from California waters, and their emerging fisheries: A review. CalCOFI Rep. 24:57–69. Cailliet, G.M., K.A. Karpov and D.A. Ambrose. 1979. Pelagic assemblages as determined from purse seine and large midwater trawl catches in Monterey Bay and their affinities with the market squid, Loligo opalescens. CalCOFI Rep. 24:57–69. Carey, F.G., J.M. Teal, J.W. Kanwisher, K. D. Lawson, and J.S. Beckett. 1971. Warm-bodied fish. Amer. Zool. 11:137–145.

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Radovich, J. 1952. Report on the young sardine, Sardinops caerulea, survey in California and Mexican waters, 1950 and 1951. Calif. Fish Game, Fish. Bull. 57: 31–63. Roberts, J.L. 1978. Ram gill ventilation in fish. In: The physiological ecology of tunas, G.D. Sharp and A.E.Dizon (eds), Academic Press, NY., p. 83–88. Rothschild, B. J. 1986. Dynamics of Fish Populations. Harvard Univ. Press, Cambridge, MA. 277 pp. Sandknop, E.M., and W. Watson. 1996. Mugilidae. In: Moser, H.G. (ed). The early stages of the fishes in the California current region. CalCOFI Atlas No. 33, p. 1078–1081. Santander, H., J. Alheit, and P.E. Smith. 1984. Estimacion de la biomasa de la poblacion desovante de anchoveta Peruana Engraulis ringens en 1981 por aplicacion del “metodo de produccion de huevos” Bol. Inst. Mar. Peru Callao 8:213–250. Schaefer, K.M. and C.W. Oliver. 2000. Shape, volume, and resonance frequency of the swimbladder of yellowfin tuna (Thunnus albacares). U.S. Fish. Bull. 98(2): 364–374. Schaefer, K.M., and J. Childers. 1999. Northernmost occurrence of the slender tuna, Allothunnus fallai, in the Pacific Ocean. Cal. Fish & Game 85(3):121–123. Schwartzlose, and P.E. Smith. 1989. World-wide fluctuations of sardine and anchovy stocks: the regime problem. S. Afr. J. Mar. Sci. 8:195–205. Scott, J.M. 1969. Tuna schooling terminology. Calif Fish Game. 55: 136–140. Scott, J.M., and G.A. Flittner. 1972. Behavior of bluefin tuna schools in the Eastern North Pacific Ocean as inferred from fishermen’s logbooks, 1960–67. U.S. Fish. Bull. 70: 915–927. Sharp, G.D., and R.C. Dotson. 1977. Energy for migration in albacore (Thunnus alalunga). Fish. Bull., U.S. 75(2):447–450. Shepherd, J.G., J.G. Pope, and R.D. Cousens. 1984. Variations in fish stocks and hypotheses concerning their links with climate. Rapp.-v: Reun. Cons. Int. Explor. Mer. 185:255–267. Skud, B.E. 1982. Dominance in fishes: The relationship between environment and abundance. Science. 216:144–149. ———. 1983. Interactions of pelagic fishes and the relation between environmental factors and abundance. In: J. Csirke, and G.D. Sharp, (eds.). Reports of the Expert Consultation to Examine Changes in Abundance and Species Composition of Neritic Fish Resources. FAO Fish. Rep./ FAO Inf. Pesca, 291(2): 1133–1140. Smith, P.E., J.K. Horne, and D.C. Schneider. 2001. Spatial dynamics of anchovy, sardine, and hake pre-recruit stages in the California Current. ICES J. Mar. Sci. 58:1063–1071. Smith, P.E. 1972. The increase in spawning biomass of Northern anchovy, Engraulis mordax. Fish. Bull., U.S., 70:849–874. ———. 1973. The mortality and dispersal of sardine eggs and larvae. Rapp. P.-v Reun. Cons. Explor. Mer.164:282–292. ———. 1980. A time series of age composition and apparent abundance of the northern anchovy, Engraulis mordax, with inferences about the strength of recruitment. SWFC-LJ-80-07. ———. 1981. Fisheries of coastal pelagic schooling fish. In: R. Lasker, (ed) Marine Fish Larvae. Washington Sea Grant Program, Seattle, WA. pp. 1–31. ———. 1990. Monitoring interannual changes in spawning area of Pacific sardine (Sardinops sagax). CalCOFI Rep. 31:145–151. Smith, P.E., and H.G. Moser. 1988. CalCOFI time series: An overview of fishes. CalCOFI Rep. 29:66–77. Smith, P.E., and R.W. Eppley. 1982. Primary production and the anchovy population in the Southern California Bight: Comparison of timeseries. Limno. Oceanogr. 27:1–17. Smith, P.E. 1978a. Biological effects of ocean variability: Time and space scales of biological response. Rapp. P.- V. Reun. Cons. Int. Explor. Mer. 173:117–127. Smith, P.E. 1978b. Precision sonar mapping for pelagic fish assessment in the California Current. J. Cons. Int. Explor. Mer. 38:33–40.

Smith, P.E., H. Santander, and J. Alheit. 1983. Comparison of egg sample probability distributions of the anchovy (Engraulis ringens) and sardine (Sardinops sagax) off Peru and the anchovy (Engraulis mordax) and the sardine (Sardinops caerulea) off California. In: Proceedings of the expert consultation to examine changes in abundance and species composition of neritic fish resources Gary D. Sharp and Jorge Csirke, (eds.) FAO Fish. Rep. 291, Vol. 3:1027–1038. ———. 1989. Comparison of the mortality rates of sardine (Sardinops sagax) and anchovy (Engraulis ringens) eggs off Peru. Fish. Bull., U.S. 87(3):497–513. Smith, P.E., N.C.H. Lo, and J.L. Butler. 1992. Life-stage duration and survival parameters as related to interdecadal population variability in Pacific sardine. CalCOFI Rep. 33: 41–49. Smith, P.E., W.C. Flerx, and R.P. Hewitt. 1985. The CalCOFI Vertical Egg Tow (CalVET) net. In: An egg production method for estimating spawning biomass of pelagic fish: Application to the northern anchovy, Engraulis mordax Reuben Lasker. (ed.) NOAA Technical Report NMFS 36:27–33. Soutar, A., and J.D. Isaacs. 1969. History of fish populations inferred from fish scales in anaerobic sediments off California. CalCOFI Rep. 13:63–70. Soutar, A., and J.D. Isaacs. 1974. Abundance of pelagic fish during the 19th and 20th centuries as recorded in anaerobic sediment off the Californias. U.S. Fish. Bull. 72(2):257–273. Squire, J.L., Jr. 1983b. Abundance of pelagic resources off California, 1963–78, as measured by an airborne fish monitoring program. NOAA Tech. Rep NMFS SSRF-762, 75 p. ———. 1983a. Warm water and southern California recreational fishing: A brief review and prospects for 1983. Mar. Fish Rev. 45(4–6): 27–34. Stauffer, G., and K. Parker. 1980. Estimate of the spawning biomass of the northern anchovy central subpopulation for the 1978–79 fishing season. CalCOFI Rep. 21:12–16. Tanaka, S. 1983. Variation of pelagic fish stocks in waters around Japan. In: J. Csirke, and G.D. Sharp, eds. Reports of the Expert Consultation to Examine Changes in Abundance and Species Composition of Neritic Fish Resources. FAO Fish Rep./FAO Inf. Pesca, 291(2): 17–36. Van der Elst, R.P., and M. Roxburgh. 1981. Use of bill during feeding in the black marlin (Makaira indica). Copeia 1981: 215. Vetter, R.D., A. Kurtzman, and T. Mori. 1999. Diel cycles of DNA damage and repair in eggs and larvae of northern anchovy, Engraulis mordax, exposed to solar ultraviolet radiation. Photochem. Photobiol. 69:27–33. Vlymen, W. J. 1977. A mathematical model of the relationship between larval anchovy (Engraulis mordax) growth, prey microdistribution, and larval behavior. Env. Biol. Fish. 2:211–233. Vrooman, A.M., and P.E. Smith. 1971. Biomass of the subpopulations of northern anchovy, Engraulis mordax Girard. CalCOFI Rep. 15:49–51. Watson, W. 1996. Blennidae. In: Moser, H.G. (ed.), The early stages of the fishes in the California current region. CalCOFI Atlas No. 33, p. 1182–1200. Wisner, R.L. 1858. Is the spear of istiophorid fishes used in feeding? Pac. Sci. 12:60–70. Wolf, P., and P.E. Smith. 1985. An inverse egg production method for determining the relative magnitude of Pacific sardine spawning biomass off California. CalCOFI Rep. 26:130–138. ———. 1986. The relative magnitude of the 1985 Pacific sardine biomass off Southern California. CalCOFI Rep. 27:25–31. ———. 2001. Pacific sardine. In: Leet, W.S., C.M. Dewees, R. Klingbeil, E.J. Larson (eds). California’s Living Marine Resources: A Status Report. Calif. Dept Fish Game, U.C. Agri. Nat. Res. Pub. SG01-11, 592 pp. Wolf, P., and C.L. Scannell. 1987. The relative magnitude of the 1986 Pacific sardine spawning biomass off California. CalCOFI Rep. 28:21–26.

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CHAPTER 13

Deep Sea MAR GAR ET A. N E I G H B O R S AN D RAYM O N D R. W I LS O N, J R.

Introduction Below the euphotic epipelagic zone is the realm of deep-sea fishes. The depth zones of this major portion of the earth’s oceans have been characterized by the physical features and types of organisms present (Hedgpeth, 1957; Angel, 1997). The upper limit of the mesopelagic zone (the interface with the epipelagic) occurs at approximately 100 m or even as deep as 200 to 250 m. The mesopelagic may be further subdivided into shallow and deep portions, often at about 600 to 700 m, based on the inhabitants (Angel, 1997). In the shallower portion, fish are silvery, and decapod crustaceans are a combination of red and transparent. Both groups may migrate upward through the thermocline at night. Nonreflective fishes and totally red decapod crustaceans inhabit the deeper zone. The vertically migrating micronekton from these greater depths usually do not cross the seasonal thermocline, and the majority of the macroplankton do not migrate vertically. The bathypelagic zone, where daylight ceases to affect the distributions and behavior of the inhabitants, is found below approximately 1,000 m. At temperate latitudes, the mesopelagic-bathypelagic interface may be in the region of the permanent thermocline and the oxygen minimum layer (Angel, 1997). Accounting for 75% of the ocean, this dark, cold, sparsely populated region of increasing ambient pressure is the largest habitat type on earth (Helfman et al., 1997). Midwater assemblages may again change below 2,500 to 2,700 m in the abyssopelagic zone (Angel, 1997). This, then extends to near the ocean floor, where the benthopelagic inhabitants swim just above the bottom, in the so-called nepheloid layer. The physical features of ocean waters change with increasing water depth. Pressure increases by one atmosphere (14.7 psi) per 10 m of depth. Temperature, which decreases in the upper 1,000 m, but then remains at fairly constant lows down to the bottom of the ocean (Marshall, 1971a), must influence the vertical ranges of organisms as it does the horizontal ranges of inhabitants of the epipelagic (Bruun, 1955). Light, however, is the feature most readily related to the vertical distributions of oceanic organisms. Phytoplankton are restricted to the epipelagial, where the solar energy is sufficient for their photosynthetic requirements. As a result of absorption and scattering, daylight intensity decreases to 1/10 for approximately every

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75 m increase in depth, and the wavelengths that penetrate the deepest (about 430—530 nm, centered around 475 nm) are those of blue light (Denton, 1990). The sun is not the only source of light in the ocean. Even in the epipelagic zone, organisms capable of producing light (bioluminescence) abound. At greater depths, any light present increasingly becomes due to bioluminescence, which generally is blue or blue-green. Daylight dominates the upper 200 m of the water column and diminishes to virtually absent at around 900 m; between 200 and 900 m, light from both sources is found (Denton, 1990), and in deeper regions, the only light present is produced by the inhabitants. Most deepsea fishes, as well as many deep-sea invertebrates, produce their light with chemical reactions within specialized organs such as photophores; however, some species employ luminous symbiotic bacteria for this function. The appearances of open water fishes living at different depths are related to the amount, directionality, and wavelengths of the light in their environment. These species lack structural features in their habitat where they can hide and, as a result have developed ways to blend into their open water backgrounds. Fishes of well-lit waters may be very brightly colored. Coral reef fishes are obvious in aquaria; in their natural habitats their frequently blue and yellow coloration may function in camouflage when viewed from afar against a reef or open blue water (Marshall, 2000). Larval fishes inhabiting the epipelagic are often transparent. Many juvenile and adult fishes of the upper waters, particularly schooling species, are silvery with a dark dorsal surface (McFall-Ngai, 1990). This countershading is cryptic when viewed either from above against darker deeper waters or from below against downwardly directed sunlight. Additionally, the orientations of their silvery reflecting scales on laterally flattened bodies that may taper ventrally (e.g., herring) further aid in hiding in the light filled environment of the epipelagic (Denton, 1970). In the upper mesopelagial, numerous fishes are also largely transparent or silvery with dark dorsal surfaces. Many have broad vertical ranges, as they make regular upward movements (diel vertical migrations) to the epipelagic zone at night to feed. Light in their environment will change from that of their daytime depth regime as they swim upward in the late afternoon, perhaps encounter night-time down-

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welling light from a full moon, and then return to their daytime depths. Predators of the epipelagial, which largely rely on vision for prey detection and are not as active at night when migrators reach the upper portions of their ranges, may be the driving force behind these vertical movements (Robison, 2003). Some transparent mesopelagic fishes can darken their coloration at night by varying the distribution of the dark melanin pigment within their melanophores (Badcock, 1969). The fish inhabitants found at increasing depths are less likely to migrate into well-lit waters. Lower mesopelagic and bathypelagic fishes often lack silvery scales and have black, brown, or reddish colorations. Pigments that do not reflect the blue light of bioluminescence will appear black and thus provide camouflage in this dark environment (Clarke and Denton, 1962). Many deep-sea fishes are bioluminescent (Herring and Morin, 1978), even though light production would seem to make them stand out in their dark world. Indeed, this might be so for those species that utilize bioluminescence either to attract prey or conspecifics or to escape predation. The photophores of many mesopelagic and bathypelagic fishes are, however, arranged in rows along the ventral surface of the animal. These are thought to provide counterillumination by producing light that is similar to the ambient light in color, intensity, and angular dispersion (e.g., Denton et al., 1972; Case et al., 1977; Young and Roper, 1977; Denton et al., 1985), which, like countershading, renders the fish less visible when viewed from below against a background of downwelling light. Photophores near the eyes may enable some species to fine tune the match of their bioluminescence with the ambient light (Lawry, 1974; Herring, 1977). Photosensitive cells in the pineal complex of deep-living fishes (McNulty, 1976; McNulty and Nafpaktitis, 1976; McNulty and Nafpaktitis, 1977) occur under a window in the skull between the eyes and may also monitor the intensity of the downwelling light (Young et al., 1979). The ability to counterilluminate effectively may influence the upper daytime depth limits of mesopelagic organisms (Young et al., 1980). The visual systems of the inhabitants must also be considered when discussing roles of bioluminescence in a region. The eyes of deep-sea fishes are quite varied and have been the subject of many studies (see Douglas et al., 1998; Wagner et al., 1998; and Herring, 2002 for recent reviews). The relatively large eyes of epipelagic fishes afford them high visual acuity. The retinas of these laterally-directed eyes contain two types of receptors: cones and rods, the latter assuming importance during periods of reduced light. The presence of different types of receptor cells containing visual pigments reactive to different wavelengths of light gives these fishes sensitivity to the many colors present in their well-lit environment (Herring, 2002). The eyes of many deep-sea fishes are also large but exhibit much variation related to differences in their visual environment. The retinas of the vast majority of these species contain only rods with one photopigment maximally sensitive to wavelengths in the range of bioluminescence rather than the blue of downwelling sunlight (Herring, 2002). The requirement of sensitivity outweighs that of acuity, and many deep-sea fish eyes collect as much light as possible from their dim environment. Often an aphakic space is present between the lens and the iris in the front of the eye (Nicol, 1978; Herring, 2002). Such cases of the pupil being larger than the lens allows light to strike the retina without passing through the lens and thus increases the chances of detection

of light from obliquely placed sources (Denton, 1990). Additionally, the visual fields of a pair of aphakic eyes may overlap, resulting in binocular vision (Herring, 2002). Binocular vision is also possible with tubular eyes (Herring, 2002), which may be directed either upward or forward. This type of eye permits enlargement of the lens, which gathers the minimal light available and focuses it on a small area of retina. An upwardly directed eye might see prey silhouetted against the downwelling sunlight. Those fishes with forwardly directed tubular eyes may hang vertically in the water column (Herring, 2002). Eye size tends to decrease in the fishes of the lower mesopelagic and bathypelagic zones. Warrant (2000), however, argues against the commonly held notions that the eyes of bathypelagic fishes are degenerate or regressed compared to those of the shallower deep-sea fishes. Instead, he notes that their eyes, although small, have relatively large pupils and other adaptations that are “quite adequate for seeing bioluminescent flashes up to several tens of metres away.” Because these fishes are not well-muscled swimmers, such visual limits allow detection and localization of bioluminescence flashes within ranges they could cross for capture of prey or encountering a mate. The acoustico-lateralis system of fish functions in electroreception (in sharks and their relatives), mechanoreception, and proprioception. Sound production is scarce in the midwaters, but is thought to be relatively common among benthopelagic fishes (Marshall, 1979). Midwater fishes show variation in their lateral line systems, the neuromasts of which may be free-standing and, thus, fully exposed or housed in mucus-filled canals (Marshall, 1980; Herring, 2002). Free neuromasts, which may be mounted on stalks or even at the end of filaments, occur on the heads, bodies, or tails of some species and are more a feature of slow moving bathypelagic fishes. Mesopelagic fishes are more likely to have neuromasts on their heads or along their lengths in a series of canals, which dampen the sensations caused by their own body movements. The main function of the lateral line as a whole is likely detection of near by movements (e.g., other fish in a school or potential predators or prey (Herring, 2002)). Greater differences in signal along the length of the lateral line may be related to the elongate shapes of many deep-sea fishes (Herring, 2002). The semicircular canals of the system are quite large in some bathypelagic fishes, which lack light cues for orientation (Montgomery and Pankhurst, 1997). Although some midwater fishes are either synchronous or sequential hermaphrodites, in many species the sexes are separate (Herring, 2002). Olfaction is believed important in mate location in the dioecious species. A difference in the degree of development of the olfactory lamellae, as well as the olfactory nerves, bulbs, and forebrain, between males and females occurs in many bathypelagic fishes (Marshall, 1967; Herring, 2002). Olfactory receptors of these males increase in size and complexity (become macrosmatic), whereas in the females the receptors may regress (become microsmatic). Thus, in sexually dimorphic species pheromones might be important for mate location (Marshall, 1980). If pheromones are present, the search time for a male to find a female may be reduced to hours rather than days in the well-dispersed fishes of the midwaters (Jumper and Baird, 1991). In some species, both the males and females become microsmatic, leaving vision as the most likely means of locating a mate (Baird and Jumper, 1993). Herring (2000) suggested that for many deep-sea fishes bioluminescence

DEEP SEA

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and vision become important after detection of a long-range chemical cue and before close-range mechanosensory identification. Food density decreases with depth; abundances of fishes and invertebrates diminish with increasing depth. The ability to consume any potential food item encountered is more important as encounters become scarcer. Many deeper living species have larger mouths relative to their body size with large entrapping teeth in addition to well-developed pharyngeal baskets for capture of small items (Ebeling and Cailliet, 1974; Herring, 2002). At an extreme, the black swallower, Chiasmodon niger, is capable of consuming fishes larger than itself (Marshall, 1980). The body compositions of deeper living midwater fishes change. Species of the upper mesopelagic tend to have better developed bones and musculature and reduced body densities due to the presence of either gas-filled swimbladders or high lipid contents (Denton and Marshall, 1958; Marshall, 1960; Butler and Pearcy, 1972; Bone, 1973; Childress and Nygaard, 1973). Their neutral lipids consist largely of either triacylglycerols, the usual form of stored lipids in vertebrates, or lower density wax esters (Nevenzel et al., 1969; Kayama and Ikeda, 1975; Sargent et al., 1976; Sargent, 1978; Nevenzel and Menon, 1980; Neighbors and Nafpaktitis, 1982; Reinhardt and Van Vleet, 1986; Neighbors, 1988). Many of these fishes make diel vertical migrations of over hundreds of meters distance. Deeper-living species without functional swimbladders generally have less well developed skeletal, muscular, and circulatory systems in their flabby, watery bodies (Blaxter et al., 1971; Childress and Nygaard, 1973; Yancey et al., 1989; Yancey et al., 1992). Inconsistencies in the decrease of lipid and protein contents in species living at greater depths have been attributed to regional differences in constancy of food availability or visual predation (Bailey and Robison, 1986; Stickney and Torres, 1989; Childress et al., 1990; Donnelly et al., 1990). Near the seafloor of even the world’s deepest oceans, one finds that the fishes are typically much larger, more substantial, and usually more active than those of the overlying midwaters. Because the fish need not hang in midwaters, their tissues are generally not as watery or as flaccid, and their skeletal bones are more strongly developed. Although some species apparently do maintain their neutral buoyancy via some tissue reduction or have oily livers, most have functional physoclistous swimbladders. These bottom (benthic) and near-bottom (demersal or benthopelagic) fishes also generally lack photophores and are rarely bioluminescent, and, yet have well-developed eyes. They collectively feed on a diversity of prey, and the various Atlantic Ocean species have been classified into ten guilds (Gartner et al. 1997). By the definitions of those guilds, the abundant benthic and demersal species off California would be classified mostly as piscivores, macronekton foragers, micronekton/epibenthic predators, or specialist necrophages. Many deep-sea benthopelagic fishes share the peculiar, apparently convergent, body form of a relatively long tail with a continuous anal fin of many rays that tapers to a fine tip. Marshall (1971a) dubbed them “rat-tailed” fishes and suggested that one function of the tail might be accentuation of the acoustico-lateralis system for prey and predator detection. If present, the caudal fin is indistinct or confluent with the anal and dorsal fins at the end of the tail, producing a rounded tip. The tapered tail of some benthic species is likely useful for burrowing into the sediment to lay eggs or to hide from predators.

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P E L A G I C H A B I TA T S A N D A S S O C I A T E D F I S H E S

General differences in the characteristics of fishes from the epipelagic through the benthopelagic regions of the open ocean are summarized in table 13-1.

Physical Features of the Deep Sea Off the Californias Geologic Features Geologic features determine water depth and thus influence the distribution of deep-sea fishes near the edges of continents as well as along the seafloor. The continental shelf, the edge of the continent under 200 m or less of water (Duxbury, 1971), north of Point Arguello, California (34° 35’ N), and south of Cedros Island, Mexico (28° 20’ N), is relatively broad and flat like other continental shelves (Uchupi and Emery, 1963). In the Southern California Bight, the continental borderland, a region with islands and deep basins, lies seaward of the shelf (fig. 13-1, Uchupi and Emery, 1963). The shelves of the mainland and around the islands of the borderland are narrow (Uchupi and Emery, 1963). Over 20 basins pit the borderland (Emery, 1960; Krause, 1965). Sills, the submerged elevations that separate basins (Sverdrup et al., 1942), and floors of the 13 northern basins (fig. 13-2) range from about 475 to 1,900 m and 625 to 2,570 m in depth, respectively (Emery, 1960). Areas of these basins at sill depth range from approximately 135 to 1,175 km2 (Emery, 1960). The basin floors are typically silty-clay sediments, containing organic material and many infaunal species, chiefly polychaetes. In the Santa Catalina Basin, sediment organic carbon is near 55 mg C g
1 sediment with total macrofaunal abundance near 10,000 individuals m
2 (Smith et al., 1983). Tidally caused near-bottom currents generally travel at less than 5 cm sec
1 (Wilson, unpub.), and a zone of suspended particulates, the nepheloid layer, rises to about 50 m above the bottom. Seaward of the continental shelf or borderland, the continental slope descends to the deep-sea rise, which joins the ocean basin floor. North of Point Conception, the continental slope at first descends gently from the continental shelf to a depth of about 600 m, forming a plateau. Three deep-sea fans constituting the deep-sea rise at the base of this slope join the abyssal floor at about 4,000 m. Seaward of the borderland, the slope, as the Patton Escarpment, descends steeply to a depth of about 3,400 m. Off Cedros Island, the slope descends from the shelf to the Cedros Trench, which is up to 1,000 m deeper than the adjoining 3,600 m deep abyssal floor (Uchupi and Emery, 1963). Rolling abyssal hills appear at the base of the Patton Escarpment, approximately 325 km west of San Diego. The seafloor there remains layered with sediments of silty clay, but organic content falls to about 10 mg C g
1 sediment (Smith et al., 1983); macrofaunal abundance drops 20% from that of the Santa Catalina Basin. Near-bottom currents are once again tidal at 5 cm sec
1 (Wilson and Smith, 1984). Proceeding west into the Pacific Basin, manganese nodules become prevalent features of the seafloor, but the sediments remain silty clay. Sediment organic carbon continues to drop slightly, but by 4,400 m depth, ca. 720 km west of San Diego, total macrofaunal abundance is only 1,000 individuals m
2, one-tenth of that in the Santa Catalina Basin (Smith et al., 1983). Submarine canyons, deep cuts in the continental slope that may extend into or cross the adjoining shelves (Emery, 1960), of various sizes occur along the length of California and Baja

NOTE:

Wide size range, from small to large

Small

Small

Small

Relatively large

Mesopelagic (vertical migrators) Mesopelagic (non-migrators)

Bathypelagic

Benthopelagic

Size

Epipelagic

Pelagic Zone

After Castro and Huber, 1997.

Appearance

TA B L E 13-1

Very elongated

Relatively elongate and/ or laterally compressed Elongate, often globular in shape

Varied, mainly fusiform, some elongate and laterally compressed Relatively elongate and/or laterally compressed

Shape

Strong muscles

Weak, flabby muscles

Weak, flabby muscles

Moderately strong muscles

Strong dense muscles, fast swimming

Musculature

Eye

large

Eyes varied, small to relatively

Very large, sensitive eyes, sometimes tubular eyes Eyes small or absent

Very large, sensitive eyes

Large eyes

Characteristics

General Characteristics of Pelagic Oceanic Fishes by Vertical Zone

Dark brown or black

Black, occasionally red

Black or black with silver sides and belly

Black or black with silver sides and belly

Countershading, dark back and white or silver belly

Coloration

Bioluminescence common, often used for counterillumination Bioluminescence common, often used for counterillumination Bioluminescence common, often used to attract prey Only a few groups bioluminescent

Bioluminescence uncommon

Bioluminescence

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F I G U R E 13-1 The seafloor off California (after Uchupi and Emery, 1963).

California (Uchupi and Emery, 1963). Four of these (Monterey, Arguello, Scripps, and Coronados canyons) are considered to be among the major submarine canyons of the world (Duxbury, 1971). Monterey and Scripps canyons in particular bring midwater species closer to shore. Water depth limits the inshore occurrence of pelagic deepsea fishes. Mesopelagic fishes may require water deeper than 200 or 300 m (Pearcy, 1964; Hulley, 1992). Depths over 183 m (100 fm contour on charts) occur within 20 km of the coast between Cape Mendocino, California (40° 30’ N), and Pt. Colnett, Baja California (30° 50’ N). Areas deeper than 914 m (500 fm contour) may be within 40 km of shore. In the Southern California Bight, the shallower inshore Santa Barbara,

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Santa Monica, and San Pedro basins have bottom depths of 627, 938, and 912 m, respectively (Emery, 1960), and thus provide habitats for lanternfishes and other deep-sea families relatively near shore.

Water Types and Currents The complex of water types found off the coasts of California and Baja California influences the diversity of deep-sea fishes in midwaters. From the north Pacific Ocean, the Subarctic water mass adds water of relatively low temperature, low salinity, high dissolved oxygen, and high phosphate content (Reid

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F I G U R E 13-2 Thirteen northern

basins of the Southern California Bight (after Hickey, 1993).

et al., 1958). To the south is found the Pacific Equatorial water mass (“southern” water, Hickey, 1993), whose water is characterized by relatively high temperature and salinity and, as it moves up the coast of Baja California, low dissolved oxygen and high phosphate content (Sverdrup et al., 1942; Reid et al., 1958). A region of transition exists below 300 m between 22° N and 45° N where waters from these two masses mix (Sverdrup et al., 1942). To the west lies the eastern north Pacific central water mass, whose water is characterized by relatively warm temperatures, high salinity, low dissolved oxygen, and low surface-layer nutrients (Reid et al., 1958). Currents off the west coast of North America change seasonally in their transport of water to both the south and the north. The California Current is a wide, slow-moving southeastward flow between 48° N and a southern limit of 23° N (Sverdrup et al., 1942). The western limit of the California Current is the boundary region between subarctic water and eastern north Pacific central water, which at 32° N is about 700 km from the coast (Sverdrup et al., 1942). Where a dividing front is less well-defined, the western edge is often set at 1,000 km offshore (Longhurst, 1998). Horizontal surface mixing with central water occurs on this westward edge as the California Current flows southward. The majority of the water movement to the south occurs between 200 and 500 km offshore, and maximum water speeds are shallower than 200 m (Hickey, 1993). Therefore, the upper waters of the transition area are more influenced by subarctic water than are waters below 100 m (Reid et al., 1958). The California Current consists of multiple regions of flow at most latitudes. South of

Cape Blanco, Oregon (42° 50’ N), nearshore flow is most fully developed during spring and early summer, and the offshore region is strongest in the late summer or fall (Hickey, 1979). Near the coast, various counterflows replace or displace the nearshore southward current. North of Point Conception, counterflow occurs during fall and winter. The Southern California Countercurrent exists in the upper half of the Southern California Bight all year except during April and in the lower half of the bight from April to December (Hickey, 1979). This countercurrent may be continuous with the Davidson Current (see below), particularly during winter (Hickey, 1979). The California Undercurrent carries equatorial water northward along Baja California and California over the slope and borderland (Hickey, 1979, 1993). North of Point Conception in late fall and winter, its core rises from 200–300 m to the surface and becomes known as the Davidson Current (Hickey, 1979). Further south, maximum flow occurs in summer and early fall (Hickey, 1979). The waters trapped in the borderland basins below the sill depths are nearly isothermal, isohaline, and typically low in dissolved oxygen (i.e., 1 ml O2 l
1, Emery, 1954; Smith et al., 1983). The northwest gradient of increasingly higher temperatures of the bottom water in the basins indicates movement of this deep water from the southeast (Emery, 1954). In the outermost basins, bottom water comes from the open sea to the west. Thus, northward flowing Equatorial water predominates in the deeper water of the borderland basins. Shallower Subarctic water is carried into the region from the north by

DEEP SEA

347

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the California Current, and central water is more likely to be found in the outer basins. Within the basins, the lower boundary of the mesopelagic zone is marked by the presence of 50% Southern water, resulting in the interface between this zone and the bathypelagic being a band of mixed northern and southern waters. The bathypelagial is predominantly Southern water. Shallow Santa Barbara Basin contains no Southern water and, therefore, no true bathypelagic zone (Lavenberg and Ebeling, 1967). Where offshore of the Californias are the boundaries of the deep sea that in turn define which species are the deep-sea fishes? The shallow boundary of the demersal deep sea is typically regarded as 1,000 m; below this depth no sunlight penetrates, resulting in permanent darkness. Weitzman (1997), however, included many fishes occurring as shallow as 500 to 600 m in his systematic review of deep-sea fishes, chiefly to include highly specialized mesopelagic species not typically caught below 1,000 m. Yet the mesopelagic zone is shallower than even 500 m. The bathypelagic zone is also considered to begin in the darkness near 1,000 m (Hedgpeth, 1957; Angel, 1997). In the borderland basins of southern California the thermocline marks the lower limit of the epipelagic zone (Lavenberg and Ebeling, 1967). The mesopelagic zone ranges from the thermocline at 50 m or deeper to the 6° C isotherm near 500 to 600 m, and the bathypelagic zone extends from there to near the sea bottom (Lavenberg and Ebeling, 1967). Fitch and Lavenberg (1968) included 259 species from 71 families in their list of deep-sea teleosts, both pelagic and benthic, from off California. The 70 species collected in more than one pelagic trawl survey off the Californias listed in table 13-2 represent 18 common midwater families. Not all fishes occurring in the deep waters of the Californias were collected in these studies. Some are too large or too quick to be captured by relatively small pelagic trawls; others (e.g., the umbrellamouth gulper, Eurypharynx pelacanoides) must be so rare or widely distributed that they are not collected with limited sampling. Assigning the shallow boundary of the deep sea to between 500 and 600 m for benthic fishes results in about 41 species typically encountered as deep or deeper in surveys of the California slope, continental rise, and abyss (table 13-3). However, some fishes that occur below those depths, such as the Pacific electric ray Torpedo californica, also range much shallower off California. In addition, a few species display high-latitude emergence (i.e., ranging into cold, relatively shallow, waters at high latitudes). A fish occurring below 500 to 600 m off California might be found in less than 100 m in the Bering Sea. Thus, the more precise definition of a deep-sea benthic fish would be a species that is virtually never taken shallower than about 500 to 600 m over its full geographic range. Applying that definition here, however, would omit discussion of some important species of the California slope that display high-latitude emergence. Nevertheless, we adopt Weitzman’s (1997) view of benthic deep-sea fishes as those mostly inhabiting depths of 500 to 600 m and deeper, but generally not shallower, with the caveat that the shallow boundary applies to benthic fishes off California (i.e., between about 32° and 42° North latitude).

Midwater Fishes Knowledge about the midwater fishes from off the Californias has largely been gained by collecting with midwater trawls,

348

P E L A G I C H A B I TA T S A N D A S S O C I A T E D F I S H E S

often of 3 m or less width. Initially trawling was done with a net that was always open. Improved ecological information was obtained when trawls were fitted with opening-closing devices. Since fishes become scarcer and trawling takes longer with increasing depth, most hauls have been made within the upper 1,000 m of the water column. Many types of investigations (e.g., systematics, distributions, feeding, reproduction, morphology, chemical composition, enzymic activities) have utilized fishes collected by trawls. Another approach to learning about the biology of these fishes is the collecting of living animals with trawls. Thermally protected cod ends (Childress et al., 1978) facilitate the capture of living specimens, and systems for maintaining caught animals in the laboratory (Robison, 1973a; McCosker and Anderson, 1976) have been considered. Laboratory investigations (Childress and Meek, 1973; Belman and Anderson, 1979; Belman and Gordon, 1979) have been successfully completed with two particularly hardy deep-sea fishes that often live after capture, the midwater eelpout, Melanostigma pammelas, and fangtooth, Anoplogaster cornuta. Observations from manned submersibles (e.g., Barham, 1971) or via video cameras in ROVs (remotely operated vehicles, e.g., Robison, 1992; Newman and Robison, 1992; Robison, 1999, 2004) have allowed viewing of the midwater inhabitants and their behaviors at the depths where they live. Direct observations enhance rather than replace collections by nets, as Smith-Beasley (1992) concluded that trawls are suitable for systematic, medium-scale studies and submersibles are more effective for microscale studies, especially of gelatinous organisms. In situ experiments have been conducted from submersibles (e.g., Smith and Laver, 1981). Another approach to the study of these fishes within their habitat has utilized the reflection of sound waves of certain frequencies by these organisms, particularly if they possess gas filled organs such as swimbladders in fishes and floats in siphonophores. Usual features of the world’s oceans are aggregations of organisms, deep scattering layers (DSLs), in the midwaters that produce layers of sound scattering on echosounders, and much study has centered upon the organisms causing and the vertical migrations of DSLs (e.g., Farquhar, 1971; Andersen and Zahuranec, 1977). Acoustic measurements have been used in conjunction with trawl collections to study midwater assemblages and their behaviors (e.g., Kalish et al. 1986; Pieper and Bargo, 1980). Acoustics are now able to be used for study of both community (Benoit-Bird and Au, 2001) and individual fish (Torgersen and Kaartvedt, 2001) movements.

Representative Families and Species The epipelagic zone, as well as the continental shelf region, is populated by numerous species of fishes, many of which belong to families in the order Perciformes and other more derived orders. Weitzman (1997) lists 22 orders of fishes that include some members of the deep-sea fauna and notes that the bony fishes that exhibit evolutionary adaptations to deep regions are generally derived from the relatively primitive groups of teleosts rather than the more derived orders. Some of the many teleost orders commonly occurring in deep ocean midwaters include the Anguilliformes, Argentiniformes, Stomiiformes, Myctophiformes, Lophiiformes, and Beryciformes. The order Anguilliformes contains families of midwater eels whose larvae are transparent leaf-shaped leptocephali. Within the Serrivomeridae, the sawtooth eel, Serrivomer sector (fig. 13-3),

Argentiniformes

Anguilliformes

Order

Alepocephalidae

Opisthoproctidae

Bathylagidae

Serrivomeridae

Nemichthyidae

Family

Bajacalifornia burragei Townsend and Nichols, 1925 Talismania bifurcata (Parr, 1951)

Bathylychnops exilis Cohen, 1958 Dolichopteryx longipes (Vaillant, 1888) Macropinna microstoma Chapman, 1939

Bathylagus pacificus Gilbert, 1890 Leuroglossus stilbius Gilbert, 1890 [Bathylagus stilbius, L. stilbius stilbius] Lipolagus ochotensis (Schmidt, 1938) [Bathylagus ochotensis] Pseudobathylagus milleri (Jordan & Gilbert, 1898) [Bathylagus milleri]

Bathylagoides nigrigenys (Parr, 1931) [Bathylagus nigrigenys] Bathylagoides wesethi (Bolin, 1938) [Bathylagus wesethi]

Serrivomer sector Garman, 1899

Avocettina bowersii (Garman, 1899) Nemichthys scolopaceus Richardson, 1848 [N. avocetta ]

Species [synonym]

BAJA CALIF.

&

X

d

X

e

X

X

X

f

X

X

X

g

X

X

X

h

30–19

X

X

i

California smoothtongue Popeye blacksmelt, eared blacksmelt Robust blacksmelt, stout blacksmelt Barreleyes or spookfishes Javelin spookfish Brownsnout spookfish Barreleye Slickheads Sharpchin slickhead Threadfin slickhead

X

X X

X

X

X

X

X

X

X

X

X

X

X

X

X

X

X X

X

X

X

X

X X X

X

X

X

X X

X

X

X

X

X

c

SANTA BARBARA AREA

Snubnose blacksmelt Pacific blacksmelt, slender blacksmelt

X

b

SAN PEDRO BASIN

X X

X

X

X

a

CALIF.

35–33

SANTA CATALINA BASIN

Blackchin blacksmelt

Deep-sea smelts

Slender snipe eel Sawtooth eels Sawtooth eel

Snipe eels

Common Name

MONTEREY BAY

37–36

MONTEREY BAY

38–23

SANTA BARBARA AREA

Latitude ( North)

SANTA BARBARA AREA

TA B L E 13-2

BAJA CALIFORNIA

Family Representatives Collected by More Than One Midwater Trawl Survey Off California and Baja California

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Stomiiformes

Order

Stomiidae

Phosichthyidae

Sternoptychidae

Gonostomatidae

Platytroctidae

Family

Aristostomias scintillans (Gilbert, 1915)

Ichthyococcus irregularis Rechnitzer and Böhlke, 1958 Vinciguerria lucetia (Garman, 1899)

Argyropelecus affinis Garman, 1899 [A. pacificus] Argyropelecus hemigymnus Cocco, 1829 [A. heathi, A. intermedius ] Argyropelecus lychnus Garman, 1899 [A. lychnus lychnus] Argyropelecus sladeni Regan, 1908 [A. hawaiensis] Danaphos oculatus (Garman, 1899) Sternoptyx diaphana Hermann, 1781 Sternoptyx obscura Garman, 1899

Cyclothone acclinidens Garman, 1899 Cyclothone pallida Brauer, 1902 [C. canina] Cyclothone signata Garman, 1899

Holtbyrnia macrops Maul, 1957 Holtbyrnia melanocephala (Vaillant, 1888) Mentodus facilis (Parr, 1951) [Pellisolus facilis] Sagamichthys abei Parr, 1953

Species [synonym]

TA B L E 13-2

BAJA CALIF.

& Shining loosejaw

Bulldog lightfish Panama lightfish Barbeled dragonfishes

Lightfishes

Tropical hatchetfish Lowcrest hatchetfish, Sladen’s hatchetfish Bottlelight Diaphanous hatchetfish

X

X

X

X X X X

X X X

X X

X

X

X X X

X X

b

MONTEREY BAY

X

X

X

X X X

X X

Shining tubeshoulder Bristlemouths Benttooth bristlemouth Tan bristlemouth Showy bristlemouth Hatchetfishes Slender hatchetfish, Pacific hatchetfish Spurred hatchetfish, half-naked hatchetfish

?

a

CALIF.

Tubeshoulders Bigeye searsid

Common Name

X X

X

X

X

X

X

X

X

X

X

X

e

X X

d

SANTA BARBARA AREA

X

c

MONTEREY BAY

37–36

35–33

X

X X

X X X

X

X

X

X X X

X X X X

f

SANTA BARBARA AREA

38–23

SANTA BARBARA AREA

Latitude ( North)

SAN PEDRO BASIN

X

X

X X

X

X

X

X

X

X X X X

g

SANTA CATALINA BASIN

X

X

X

X

X

X

X

X

X

X

X

i

X X

X

X

X

X X X

X

h

30–19

BAJA CALIFORNIA

(continued)

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Myctophiformes

Aulopiformes

Myctophidae

Neoscopelidae

Paralepididae

Scopelarchidae

Ceratoscopelus townsendi (Eigenmann and Eigenmann, 1889) Diaphus anderseni Tåning, 1932 Diaphus theta Eigenmann and Eigenmann, 1890 [D. protoculus] Diogenichthys atlanticus (Tåning, 1928) Diogenichthys laternatus (Garman, 1899) Lampadena urophaos Paxton, 1963 Lobianchia gemellarii (Cocco, 1838) [Diaphus nipponensis] Nannobrachium regale (Gilbert, 1892) [Lampanyctus regalis] Nannobrachium ritteri (Gilbert, 1915) [Lampanyctus ritteri] Notolychnus valdiviae (Brauer, 1904) Parvilux ingens Hubbs and Wisner, 1964 Protomyctophum crockeri (Bolin, 1939) [Hierops crockeri] Stenobrachius leucopsarus (Eigenmann and Eigenmann, 1890) [Lampanyctus leucopsarus] Symbolophorus californiensis (Eigenmann and Eigenmann, 1889) Taaningichthys bathyphilus (Tåning, 1928) Tarletonbeania crenularis (Jordan and Gilbert, 1880) Triphoturus mexicanus (Gilbert, 1890) [Lampanyctus mexicanus]

Scopelengys tristis Alcock, 1890

Lestidiops ringens (Jordan and Gilbert, 1880) [Lestidium ringens]

Benthalbella dentata (Chapman, 1939) Benthalbella linguidens (Meade and Böhlke, 1953)

Bathophilus flemingi Aron and McCrery, 1958 Borostomias panamensis Regan and Trewavas, 1929 Chauliodus macouni Bean, 1890 Idiacanthus antrostomus Gilbert, 1890 Photonectes margarita (Goode and Beane, 1896) Stomias atriventer Garman, 1899 Tactostoma macropus Bolin, 1939

X X X

Northern lampfish California lanternfish, bigfin lanternfish

X

X

California flashlightfish

Mexican lampfish

X X X

Broadfin lampfish Topside lampfish Giant lampfish

X

X

X

Pinpoint lampfish

Blue lanternfish

X

X

Cocco’s lanternfish

X

X

X

X

X X X X

California headlightfish Longfin lanternfish Diogenes lanternfish Sunbeam lampfish

X

X

X ?

X

X

Dogtooth lampfish Andersen’s lantern fish

Blackchins Pacific blackchin Lanternfishes

Slender barracudina

Longfin pearleye Barracudinas

X

X

X X X

Blackbelly dragonfish Longfin dragonfish Pearleyes Northern pearleye

X X

X X X

Panama snaggletooth Pacific viperfish Pacific blackdragon

X

X

Highfin dragonfish

X

X

X

X

X

X X

X

X

X X

X

X

X

X

X

X

X

X X

X

X

X

X

X

X X

X

X X X

X X

X

X

X

X

X

X

X

X

X

X X

X

X

X

X X

X

X

X X X X

X

X

X

X

X

X X

X X

X

X

X

X X

X

X

X

X

X X

X X

X

X

X

X

X

X

X

X

X

X X

X

X

X

X X X

X

X

X

X X

X X

X

X

X

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Family

Zoarcidae

Anoplogastridae

Melamphaidae

Oneirodidae

Eelpouts Pallid eelpout

Midwater eelpout

Melanostigma pammelas Gilbert, 1896

Twospine bigscale Fangtooths Fangtooth

Bigscales Slender bigscale Highsnout bigscale or melamphid Little bigscale Crested bigscale Longjaw bigscale

Dreamers Spiny dreamer Bulbous dreamer

Common Name

Lycodapus mandibularis Gilbert, 1915

Anoplogaster cornuta (Valenciennes, 1833)

Melamphaes parvus Ebeling, 1962 Poromitra crassiceps (Günther, 1878) Scopeloberyx robustus (Günther, 1887) Scopelogadus mizolepis bispinosus (Gilbert, 1915) [Melamphaes bispinosus]

Melamphaes acanthomus Ebeling, 1962 Melamphaes lugubris Gilbert, 1891

Oneirodes acanthias (Gilbert, 1915) Oneirodes eschrichtii Lütken, 1871

Species [synonym]

BAJA CALIF.

& CALIF.

X

e

X

f

X

X

X

X

X

X

X

X

X

X

X

X

d

X X X X

X

c

35–33

X

X

b

SANTA BARBARA AREA

X

? X

a

MONTEREY BAY

37–36

MONTEREY BAY

38–23

SANTA BARBARA AREA

Latitude ( North)

SANTA BARBARA AREA

(continued)

SAN PEDRO BASIN

X

X

X

X

X

X

X X

g

SANTA CATALINA BASIN

X

X

X

X X

X

X

X

h

30–19

X

X

X

i

BAJA CALIFORNIA

c

b

a

Berry and Perkins (1966): 3 m IKMT, 3 m  4.3 m collapsible midwater beam trawl, 1.5 m  1.5 m nekton net, 21m  24m, Cobb Mark II pelagic trawl Anderson et al. (1979): 1.8 m modified opening-closing Tucker Trawl Smith-Beasley (1992): modified 1.8 m.opening-closing RMT d Best and Smith (1965): intermediate-sized midwater trawl with 3.3 m2 mouth e Pieper (1967): instrumented 1.8 m IKMT with 4 chamber cod end. Trawls 36–45 in modified Subarctic region. f Brown (1974): instrumented 1.8 m IKMT with 4 chamber cod end g Lavenberg and Ebeling (1967) and Paxton (1967a): 3 m IKMT h Rainwater (1975): 1.8 m opening-closing modified Tucker trawl i Wisner (1962): 3 m IKMT NOTE: Species synonyms used in cited literature are in brackets (Eschmeyer 1998, on-line version May 10, 2004, www.calacademy.org/research/ichthyology). Common names from Moser (1996a) and Froese and Pauly (2003).

Sources and collecting gear:

Perciformes

Beryciformes

Lophiiformes

Order

TA B L E 13-2

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TA B L E 13-3

Common Benthic and Benthopelagic Fishes Below 500 to 600 m on the California Slope and in the Eastern North Pacific Ocean Basin

Order

Family

Species

Common Name

Principal Depth Range off California (m)

Myxiniformes Myxinidae Eptatretus deani

Black hagfish

107–2,743

Apristurus kampae Parmaturus xaniurus

Longnose cat shark Filetail cat shark

367–1,888 327–936

Centroscyllium nigrum Somniosus pacificus*

Combtooth dogfish Pacific sleeper shark

Bathyraja abyssicola Bathyraja trachura

Deep-sea skate Black skate

644–2,910 565–1,993

Alepocephalus tenebrosus* Talismania birfurcata

California slickhead Threadfin slickhead

327–1,253 584–2,000

Bathysaurus mollis

Highfin lizard fish

Carcarhiniformes Scyliorhinidae

Squaliformes Dalatiidae 400–1,143 1,044–2,000

Rajiformes Rajidae

Argentiformes Alepocephalidae

Aulopiformes Synodontidae 1,680–4,900

Ophidiiformes Aphyonidae Barathronus pacificus

3,334–3,860

Ophidiidae Lamprogrammus niger Spectrunculus grandis

Paperbone cuskeel Pudgy cuskeel

797–2,000 800–4,255

Merluccius productus*

Pacific whiting

181–1,205

Antimora microlepis

Pacific flatnose

335–3,048

Coryphaenoides acrolepis Coryphaenoides armatus Coryphaenoides filifer Coryphaenoides leptolepis Coryphaenoides pectoralis Coryphaenoides yaquinae Echinomacrurus occidentalis Nezumia kensmithi Nezumia liolepis Nezumia stelgidolepis

Pacific grenadier Abyssal grenadier Threadfin grenadier Ghostly grenadier Giant grenadier Rough abyssal grenadier

Psychrolutes phrictus

Blob sculpin

800–2,800

Anoplopoma fimbria*

Sablefish

181–2,740

Careproctus cypselurus Careproctus gilberti* Careproctus melanurus* Paraliparis cephalus Rhinoliparis barbulifer

Blackfinned snailfish Smalldisk snailfish Blacktail snailfish Swellhead snailfish

378–1,608 187–1,181 200–2,286 604–1,384 775–1,128

Sebastolobus alascanus* Sebastolobus altivelis*

Shortspine thornyhead Longspine thornyhead

181–1,524 409–1,757

Gadiformes Merlucciidae Moridae Macrouridae

Bluntnose grenadier Smooth grenadier California grenadier

600–2,500 2,000–4,300 2,065–2,904 2,000–3,860 565–2,170 3,600–6,400 ???–4,000 500–??? 681–2,825 285–800

Scorpaeniformes Psychrolutidae Anoplopomatidae Liparidae

Scorpaenidae (Sebastidae)

DEEP SEA

353

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TA B L E 13-3

Order

Family

(continued)

Species

Common Name

Principal Depth Range off California (m)

Perciformes Zoarcidae Bothrocara brunneum Lycenchelys crotalinus Lycodapus endemoscotus Lycodes diapterus Lycodapus fierasfer

Two-line eelpout Snakehead eelpout Deepwater eelpout Black eelpout Black mouth eelpout

Microstomus pacificus*

Dover sole

Embassichthys bathybius

Deep-sea sole

432–1,253 392–1,236 555–2,122 242–1,007 416–1,046

Pleuronectidae 367–1,253

416–1,433

*Shows high-latitude emergence NOTE:

Principal depth ranges determined from data in Lauth (1999), museum collection records, and various published accounts.

a silvery fish with elongate jaws and a saw-edged vomerine plate in the midline of the roof of its mouth, feeds primarily on crustaceans and occasionally small cephalopods and fishes (Fitch and Lavenberg, 1968). The blackline snipe eel, Avocettina infans (fig. 13-3), and its relatives in the Nemichthyidae have elongate bodies and long recurved jaws lined with many minute, posteriorly directed teeth, which Mead and Earle (1970) suggested ensnare the long antennae of the shrimp-like crustaceans, sergestids and their relatives, upon which they feed while hanging vertically in the water column. However, Gartner et al. (1997) reported snipe eels to be active predators. Males of the slender snipe eel, Nemichthys scolopaceous, were originally assigned to a different genus until Smith and Nielsen (1976) determined that nemichthyid males undergo a second metamorphosis at maturity, after which they have short jaws, no teeth, and tubular anterior nostrils, which presumably detect pheromones produced by the females. Three deep-sea families within the Argentiniformes are the Bathylagidae, Alepocephalidae, and Platytroctidae. Bathylagids, or deep-sea smelts, are common mesopelagic fishes throughout the world’s oceans. Three species regularly occurring in the waters off California are illustrated in fig. 13-4. The shallower, smaller members of this family (e.g., California smoothtongue, Leuroglossus stilbius, and snubnose blacksmelt, Bathylagoides wesethi) have a silvery countershaded pigmentation and large eyes, whereas deeper living species (e.g., Pacific blacksmelt, Bathylagus pacificus) still have large eyes but are darker, with larger and flabbier bodies. Slickheads (Alepocephalidae), which lack scales on their heads, are deep living, darkly pigmented species that may be mesopelagic to benthopelagic or abyssal. Their close relatives the midwater tubeshoulders (Platytroctidae), represented by the shining tubeshoulder, Sagamichthys abei, in fig. 13-4, are similar in appearance but able to bioluminesce with two types of light organs. In addition to their ventrally placed photophores, near their pectoral girdle and lateral line they have a shoulder organ or sac with an external tube through which luminous cells or particles can be expelled. This cloud of flickering light left behind a fish moving forward could aid in escape from a potential predator (Herring, 1972). The order Stomiiformes includes four common oceanic families of mesopelagic or occasionally bathypelagic fishes; representatives of many of the genera are found worldwide.

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The arrangements of the photophores on the bodies of the various stomiiforms characterize the many subgroups (Weitzman, 1997), and typically consist of two rows on the ventral portion of the head and trunk regions and one row at the same level along the tail per side (Marshall, 1980). Some of the strangest looking fishes in this order belong to the family Sternoptychidae, the hatchetfishes, of which five representatives are illustrated in fig. 13-5. The bottlelight, Danaphos oculatus, is a small largely transparent mesopelagic species. The slender hatchetfish, Argyropelecus affinis, and the lowcrest hatchetfish, A. sladeni, are small silvery fishes that are laterally compressed and deep bodied anterior to the caudal peduncle, giving them the hatchet shape from which they derive their common names. Their narrow ventral surfaces are lined with photophores and their backs are darkly pigmented. These hatchetfishes have upwardly directed mouths and tubular eyes with yellow lenses (McFall-Ngai et al., 1986), which have been hypothesized to allow distinction of the bioluminescence of their counterilluminated invertebrate prey from background ambient light (Muntz, 1976; Somiya, 1976; Douglas et al., 1998). Argyropelecus spp. have been observed to swim downward diagonally, thus maintaining their horizontal body posture and the vertical orientation of their ventral photophores and tubular eyes (Janssen et al., 1986). The diaphanous hatchetfish, Sternoptyx diaphana, like its congeners, has an abdominal flap of transparent tissue, laterally directed eyes, and ventrally directed photophores. Photophores in the mouths of Sternoptyx species may improve counterillumination by enabling comparison of the ambient light and an animal’s luminescence (Herring, 1977). The family Gonostomatidae (bristlemouths) contains some of the most abundant marine fishes in the genus Cyclothone. These small, bioluminescent fishes may be mesopelagic (e.g., the transparent showy bristlemouth, C. signata, fig. 13-5) or bathypelagic (e.g., the darker benttooth bristlemouth, C. acclinidens, fig. 13-5). Their elongate mouths are lined with needlelike teeth. Females grow larger than the males, and the males become macrosmatic, which presumably allows them to locate pheromones produced by the females in the wide open, dark waters of their habitat (Marshall, 1967, 1980). The fishes thus far discussed prey on invertebrates, largely crustaceans although some specialize on gelatinous species. In contrast, the family Stomiidae consists of many larger species

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FIGURE 13-3. Representative midwater fishes:

eel-like fishes.

F I G U R E 13-4. Representative midwater fishes: barracudina, deep-sea smelts, and tubeshoulder.

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F I G U R E 13-5. Representative midwater fishes: bristlemouths and hatchetfishes.

living in the mesopelagic zone (Marshall, 1980) that prey on other midwater fishes. Stomiids have ventral rows of photophores, large photophores below and behind the eyes, large elongate mouths with needle-like teeth, and often chin barbels that are tipped with a light organ lure. Viperfishes (e.g., Pacific viperfish, Chauliodus macouni, fig. 13-6), lack a chin barbel, but have an elongated dorsal fin ray with a luminous tip that could lure in prey for capture by teeth that are so long they do not fit within their mouths. In addition to their ventral and venterolateral rows of photophores, the elongate bodies of viperfishes and dragonfishes (e.g., the blackbelly dragonfish, Stomias atriventer, fig. 13-6) are enveloped in a gelatinous sheath that contains many small round red luminescent organs along the dorsal and ventral margins and on the fins of the fish. When lit, these cause the whole body outline to glow (O’Day, 1973). The Pacific blackdragon (Idiacanthus antrostomus, fig. 13-6) has a row of luminous tissue in chevron shaped patches along its back and rows of small patches of luminous tissue along its ventral surface and fin rays with which it can also outline its body with light (O’Day, 1973). Large blackdragons with chin barbels and teeth are females, as these features are absent in the much smaller pale-colored males, who lack a functional digestive tract (Marshall, 1954; Fitch and Lavenberg, 1968). The proportionately larger cheek photophore of the males may attract the females for mating (Marshall, 1954). In contrast to the dominant colors of bioluminescence in deep waters, the suborbital light organs of three stomiid genera produce far-red bioluminescence (Widder et al., 1984). Thus far the eyes of these species

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alone have been found to be sensitive to bioluminescence of this color (e.g., O’Day and Fernandez, 1974; Crescitelli, 1989; Douglas et al., 1998). These fishes, one of which is the shining loosejaw, Aristostomias scintillans (fig. 13-6), may be able to avoid detection while illuminating within a range of about 2 m (Partridge and Douglas, 1995) red crustaceans and other midwater fishes that have retinal pigments sensitive only to the predominantly blue and blue green wavelengths of ambient and most bioluminescent light. The Myctophiformes contains the Myctophidae (lanternfishes), the most speciose family of midwater fishes. These fishes are common in the deep waters of all oceans. Fitch and Lavenberg (1968) list 33 species as occurring in the waters off California. Seven of these lanternfishes are shown in fig. 13-7. Like all but one lanternfish species, these have photophores arranged in species-specific patterns. The majority of the photophores are found along the fish’s ventral surface, as are those of many other midwater fishes. Additionally, lanternfishes have photophores elevated on their sides to the level of or even above the lateral line. Well-developed photophores on the snout of Diaphus theta give it the common name of California headlightfish. Often species have luminescent organs on the caudal peduncle whose development probably coincides with sexual maturity (Paxton, 1972). In some species, (e.g., the northern lampfish, Stenobrachius leucopsarus, and the broadfin lampfish, Nannobrachium ritteri), these occur on both the dorsal and ventral surface with no differences between the sexes. In others, the caudal organs are sexually dimorphic; those of males are on the dorsal surface and those of females

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F I G U R E 13-6. Representative midwater fishes: barbeled dragonfishes.

F I G U R E 13-7. Representative midwater fishes: lanternfishes and blackchin.

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F I G U R E 13-8. Representative midwater fishes: bigscales, fangtooth, and dreamer.

either on the ventral surface (e.g., the California lanternfish, Symbolophorus californiensis) or absent (e.g., the blue lanternfish, Tarletonbeania crenularis). Other patches of luminescent tissue may be found in species-specific regions such as over the eyes, near the origin of the pectoral fin, and on the dorsal and ventral margins of the body of the dogtooth lampfish, Ceratoscopelus townsendi. Even though lanternfishes typically have large eyes, their ability to distinguish the species-specific photophore and other luminescent tissue patterns that allow us to tell the species apart has been questioned. Mensinger and Case (1997) suggested that species specific flash patterns of the caudal organs may better serve this purpose in addition to possibly aiding in the avoidance of predators. Deeper living members of the family (e.g., the pinpoint lampfish, Nannobrachium regale) are often darker, grow larger but have flabbier bodies, and may have smaller photophores and eyes. Species of a second myctophiform family, the blackchins (family Neoscopelidae), are far less numerous then myctophids and are represented off California by only one species, the Pacific blackchin (Scopelengys tristis, fig. 13-7), which lacks photophores. In members of the order Lophiiformes, the anterior dorsal fin spine is modified to form the flexible illicium tipped with a fleshy esca that together are used as a fishing pole with a lure. In most genera of the midwater dwelling anglerfishes (suborder Ceratioidei), the females have esca containing luminescent bacteria (O’Day, 1974; Herring and Morin, 1978) that presumably allow these animals to fish for prey even in their

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dark midwater environment. Unexpectedly, whip nose anglerfish (Gigantactis sp.) observed drifting and swimming upsidedown with their escas close to the ocean bottom might be seeking benthic prey (Moore, 2002). The much-smaller males of most species become macrosmatic; free-living males with small olfactory organs have well developed eyes (Marshall, 1980). Pheromones may direct the males to the females, and eyesight allow species identification by species-specific differences in the esca (Marshall, 1971a; 1980). The normal jaw teeth of the males are lost during metamorphosis and replaced by pincher-like denticles at the anterior tips of the jaws that allow attachment to a female (Pietsch, 1976). Some species form only a temporary attachment during spawning and fertilization, whereas in others attachment by the male is followed by fusion of epidermal tissues and joining of the circulatory systems, resulting in the male becoming a parasite of the female. The males of some species appear to be obligate parasites, whereas those of others may be facultative sexual parasites (Pietsch, 1976). The spiny dreamer, Oneirodes acanthias (fig. 13-8), is a California representative of the Oneirodidae, the most speciose family of the anglerfishes. Two beryciform families of midwater fishes that occur worldwide have representatives that are caught off California. The fangtooth, Anoplogaster cornuta, of the family Anoplogastridae, is a stout bodied, flabby black fish that has a large sculptured head and mouth bearing the impressive teeth (fig. 13-8) from which it gets its common name. Unlike most of the midwater fishes, this species is often still alive after being collected

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from hundreds of meters depth with a midwater trawl. Bigscales (family Melamphaidae) are short bodied, brown fishes with round snouts, large midset dorsal fins, and bands of minute teeth in their jaws (Marshall, 1980). These mesopelagic and bathypelagic fishes lack photophores. As in some other mesopelagic species (e.g., lanternfishes and tubeshoulders), bigscales have well developed portions of the lateral line on their heads consisting of both free neuromasts and large neuromasts set in wide canals covered with membranes pierced with pores (Herring, 2002). The neuromasts in the body canal are relatively small (Marshall, 1980). Species found off California include the crested bigscale, Poromitra crassiceps, and the highsnout melamphaid, Melamphaes lugubris (fig. 13-8).

Geographic Variations in Diversity and Abundance Variation in sampling protocols and equipment, as well as differences in regional abundances and diversities, complicates comparison of areas that have been surveyed and permits only general conclusions. Clearly, however, the diversity and abundance of midwater fishes changes with latitude and longitude off the west coast of North America, mostly in relation to differing proportions of water types present. Off Oregon, with subarctic water to the north and transitional water to the south, the number of mesopelagic species increases to the south (Pearcy, 1964). Mesopelagic fishes dominated the list of about 50 species captured in trawls to depths of 1,000 m, both in number and variety. Three lanternfishes, northern lampfish (45% of the catch), California headlightfish (21%), and blue lanternfish (10%), were taken in over 80% of the tows and absent only from shallow daytime tows and tows in shallow water. The longfin dragonfish, Tactostoma macropus (8%), was next in abundance. Offshore of California in the central Pacific, midwater fish diversity increases and abundance decreases. Between Hawaii and Santa Barbara, organisms were 100 times less abundant in hauls to depths of 550 m in the Central Pacific than in the cooler modified Subarctic water near California (Pieper, 1967); this decrease in numbers held for lanternfishes, bristlemouths, and invertebrates. Whereas lanternfish and bristlemouth biomass increased shoreward, their diversity was greatest in the warmer central water. Of the fish and invertebrate species collected, 85% were associated with either central or subarctic water, and species characteristic of either region were found in the area of mixing. Thus, rich coastal subarctic water supports fewer but more abundant species than central water, which supports a higher diversity of species that are less abundant (Pieper, 1967). Bailey (1984) compared the midwater fish faunas of three different regions of increasing depth and distance from San Diego: a California Current station above the Patton Escarpment 300 km west of San Diego, a transition station 672 km west, and a gyre station 1,536 km west (tables 13-2 and 13-4). Temperature-salinity profiles showed characteristics of subarctic water at the transition station and Pacific central water at the gyre station. The catch at the gyre station had the greatest diversity and lowest overall numbers and biomass. Diversity again decreased shoreward, with highest faunal abundance at the transition station. Average fish size was greatest at the California Current station. Bristlemouths, Cyclothone spp., were the most abundant fishes at all three stations (table 13-4). Lanternfishes were approximately 66% less abundant at the outermost station, and the mean weight per fish increased

shoreward. The rate of decrease in biomass with increasing depth was significantly higher at the gyre station than at the other two. Bailey (1984) concluded that the total micronekton biomass appears to be directly related to the level of primary production of an area. In a study conducted within a region influenced by the California Current, Brown (1974) compared the abundance (relates to productivity), diversity (indicates complexity), composition (reflects adaptations of its species), and distribution (indicates heterogeneity in space and time) of midwater faunas at increasingly seaward locations with differing water depths (Santa Barbara Basin, 600 m deep; Santa Cruz Basin, 2,000 m deep; the continental slope east of Rodriquez Dome seamount, 1,000–2,500 m deep). Santa Barbara Basin had a relatively large standing crop of fishes composed of relatively few species and lacked a bathypelagic fauna due to its shallow depth. A smaller standing crop of characteristically oceanic species, as well as an obvious bathypelagic fauna, exists at the locales farther offshore. The two offshore locations exhibited much greater faunal overlap than either did with the fauna of the Santa Barbara Basin; 61% of the total 81 species occurred only offshore. The number of species making up 90% of the fish fauna increased from three to seven to 15 at increasingly seaward locales (table 13-4). Santa Cruz Basin, at the northern portion of the chain of basins in the borderland, receives deep southern water flowing northward. Its deep-water species are derived more from the south than from central water to the west. Central and northern species have more direct access to the continental slope (Brown, 1974). Lavenberg and Ebeling (1967) concluded that the complexity of the water types present influences the diversity of the midwater fishes of an area. In the borderland, the northern faunal component of 32 species associated with the Pacific subarctic water mass generally occupies the mesopelagic region where northern water predominates. The southern faunal component of 76 species occurs mostly deeper in the lower-mesopelagic and bathypelagic regions of Southern water. The central faunal component of 16 species is most abundant offshore where central water occurs in the mesopelagic zone. Within the basins, deeper-living, seasonally abundant, northern fishes generally co-occur with southern species. Many of the mesopelagic species make diurnal vertical migrations, but few of the southern species are strong migrators. Great differences in species abundances became clear from the survey of pelagic fishes from off central California to central Baja California conducted by Berry and Perkins (1966). Over 189 fish species were collected up to 970 km seaward of the coast from between the surface and 2,234 m over bottom depths of 5,124 m or less. Forty-four species were each represented by a single specimen. Among the deep-sea fishes, lanternfishes were taken at more stations than any other fish family. Mexican lampfish were collected at more stations (76) than any other species and were the most abundant fish in a single tow, with a haul of around 3,000 individuals. Other commonly collected myctophids were California flashlightfish (66 stations), dogtooth lampfish (66 stations), broadfin lampfish (63 stations), California headlightfish (61 stations), California lanternfish (55 stations), and northern lampfish (54 stations). Commonly collected species from four other deep-sea families were the gonostomatids showy bristlemouth (64 stations) and benttooth bristlemouth (49 stations); the sternoptychids tropical hatchetfish (54 stations), slender hatchetfish (49 stations), bottlelight (47 stations), and spurred

DEEP SEA

359

Percentage of catch.

Emery (1960).

DeWitt (1972).

b

a

NOTE:

Not reported

Trawl (mouth or sampling area) Sampling protocol Number of trawls Deepest trawl (m) Bottom depth (m) Bristlemouths Cyclothone spp. Benttooth bristlemouth Showy bristlemouth Deep-sea smelts California smoothtongue Snubnose blacksmelt Lanternfishes Blue lanternfish Broadfin lampfish California headlightfish California flashlightfish Mexican lampfish Northern lampfish Larvae Hatchetfishes Bottlelight Slender hatchetfish Tropical hatchetfish Dragonfish predators Anguilliformes Big scales Other fishes 2.1

10.6

4.0

1.1 0.6 1.6 0.7

0.1

8.1

1.1

2.0 0.0 1.0 0.3

15 >2500 ? 87.1 83.7

Transition 32o 38’ N 124o 09.3’ W

Bailey (1984) Current 32o 34’ N 120o 22.5’ W

3.9 0.2 3.5 0.9

6.9

18.4

3.0

opening-closing RMT-8 (8m2) horizontal tows at depth 13 11 2000 1250 ? ? 79.2 63.2 77.5 62.4

Gyre 33o 08’ N 133o 03.4’ W

TA B L E 13-4

Santa Cruz Basin

Santa Barbara Basin

9

3

1 1 1

1 6 6 2 2 15 2

2 2

19 28

8

5

14.5

0.6 24.1

17 11

2.0

41.5 12.9

4.4

33

58

4

2 4

16

27 15

15.5

21.1 7.6

10.7

1.8

32.9 10.4

10.3

9.8 15.3

4.0

10.1

41.0 9.5

open 3 m IKMT (7.8 m2) oblique tows 5 8 650 m 650 m 912b

8.7

7.6 24.2

2.0

7.4

43.1 7.0

6 650 m

San Pedro Basin Day Night

Atsatt and Seapy (1974)

Santa Catalina Basin Day Night

1.8 m IKMT, 4 chambered cod end (2.9 m2) horizontal and oblique tows 91 267 210 9 1000a 1000a 500? 650 m 1000-2500 2000 600 1357b

Rodriguez Dome area

Brown (1974)

Composition of Midwater Fish Collections from Off Southern California

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hatchetfish (Argyropelecus hemigymnus, 45 stations); the melamphaid the twospine bigscale (Scopelogadus mizolepis bispinosus, 50 stations); and the stomiid Pacific blackdragon (50 stations).

Four Abundant Species The surveys of Berry and Perkins (1966) and others provided information regarding the distributions of the many midwater fishes off California and Baja California, but the biology of only a few abundant species of the California Current region has been studied in any detail. Among these are the myctophids northern lampfish and Mexican lampfish and the gonostomatids showy bristlemouth and benttooth bristlemouth. Although not representative of the life histories and ecologies of many other important midwater fishes (particularly their own predators) these species constitute a huge proportion of the assemblages of midwater fishes off the Californias and thus in an indirect way represent a “typical” midwater fish. ST E NOB R AC H I US L E UCO P S A R US

The northern lampfish is likely the most ecologically important myctophid in the subarctic Pacific, where its biomass may approach 21  106 tons (Beamish et al., 1999). This lanternfish ranges from Japan and the Bering Sea to northern Baja California (Miller and Lea, 1972). It has numerically dominated catches of mesopelagic fishes from the subarctic region of the north Pacific to the coastal waters off San Luis Obispo Bay and in Santa Barbara Channel (Aron, 1962; Pearcy, 1964; Best and Smith, 1965; Pieper, 1967; Frost and McCrone, 1979; Willis, 1984; Balanov and Il’inskii, 1992; Lapko, 1995; Sinclair et al., 1999). Northern lampfish are also common in catches from borderland basins (Paxton, 1967a; Brown, 1974; Rainwater, 1975). Fast (1960) suggested that because the range of northern lampfish covers a large portion of the north Pacific, its total standing population comprises billions of individuals; the young must therefore number in the hundreds of billions to support the adult population. The larva of this species was the seventh most common fish larva collected during California Cooperative Oceanic Fisheries Investigations (CalCOFI) survey cruises between 1951 and 1984, and its abundance was calculated to be over 326,000 individuals 10 m
2 of sea surface (Moser et al., 1994). Local populations of northern lampfish vary seasonally in abundance. Adults were almost twice as common in collections off Oregon during summer as during winter (Pearcy et al., 1977). In Monterey Bay, northern lampfish abundance was maximal at the time of the Davidson Current in winter and minimal during the upwelling period from March to June (Fast, 1960). Comparison of the Monterey Bay catch data with that from collections offshore (Ahlstrom, 1959) showed that the Monterey Bay population peaked in December, whereas the offshore population peaked in June and October (Fast, 1960). In San Pedro Basin, population size was greatest from November through March (Paxton, 1967a). Northern lampfish occur in horizontal patches (Pearcy and Mesecar, 1971; Willis and Pearcy, 1980) and display diel vertical migration (Pearcy and Laurs, 1966). Individual fish may not migrate every night into the surface waters (Pearcy et al., 1977). Depth distribution of northern lampfish off southern California varies slightly with location. Maximum abundances

are near 250 m in Santa Barbara Basin, above 400 m offshore near Rodriquez Dome, and somewhat deeper in Santa Cruz Basin (Brown, 1974). In Santa Catalina Basin, northern lampfish occurred with other relatively shallow-living midwater species that had their maximum abundance at about 350 m during the day (Rainwater, 1975). The San Pedro Basin population is centered above 650 m and makes nightly migrations to below 50 m. (Paxton, 1967a). Vertical distributions and migratory patterns of northern lampfish change with age (Fast, 1960; Willis and Pearcy, 1980). Larvae up to 10 mm SL are found in the surface waters, and metamorphosing larvae move deeper to 400–500 m. Juveniles return to the upper levels of the adult range at 200–300 m and begin making diel vertical migrations to within 30 m of the surface. With age, fish move deeper in the water column to depths of between 300 and 600 m and continue to migrate vertically, although not to as shallow waters (75–95 m). The largest fish (70–80 mm SL) off Oregon were not usually caught above 200 m at night (Willis and Pearcy, 1980). Watanabe et al. (1999) also found northern lampfish off Japan to have a bimodal vertical distribution at night. Fast (1960) concluded that the primary factors influencing the vertical distribution of northern lampfish are levels of light penetration and fish age. Time and place of northern lampfish feeding may vary with location. Off Oregon, Pearcy et al. (1979) collected the highest percentage of fish with very full stomachs in the morning and the lowest in the afternoon, whereas the percentage of fish with empty stomachs was highest in the afternoon and lowest at night. The rank order of the common prey of fish from the upper 100 m at night differed from that of fish that had remained between 300 and 500 m. Comparison of stomach fullness and content digestion further indicated that fish captured in deep water at night probably had fed at deeper depths as well as in shallow water on the previous night. Gorbatenko and Il’inskii (1992) suggested that on the average only 11% of the Bering Sea population migrates to the epipelagic zone (0–200 m) during a night, and that more prey is consumed in the mesopelagic zone (200–500 m) during either day or night than in the epipelagic at night. In contrast, Moku et al. (2000) found that nonmigratory northern lampfish in the western north Pacific had significantly higher proportions of empty stomachs than did migrators and probably did not actively feed at night. Crustaceans make up the bulk of the diet of northern lampfish. Stomachs of Oregon fish contained primarily euphausiids and secondarily copepods, but typically only one type of food was present in a single stomach (Tyler and Pearcy, 1975). Of 95 specimens with distended abdomens taken from San Pedro Basin, 73% had eaten euphausiids, 11% copepods, 8% sergestids, and 8% fishes (Paxton, 1967b). Fish collected in Santa Barbara, Santa Cruz, and Santa Catalina basins had also foraged predominately on euphausiids and copepods (Collard, 1970). Variability in the frequency of occurrence of these and other crustaceans was related to both season and location. The greatest seasonal difference was seen between spring, when copepods were eaten twice as often as euphausiids, and summer, when euphausiids were eaten 10 times as often as copepods. Other prey made up a larger portion of the diet during fall and winter (Collard, 1970). Gorbatenko and Il’inskii (1992) estimated that 1.8  106 tons of this small fish consume 1.9  104 tons of food per day in the Bering Sea alone. In turn, northern lampfish are the prey of squid, fishes, birds, and mammals (Beamish et al., 1999).

DEEP SEA

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Growth rates are similar between populations of northern lampfish off California and Oregon, and fish attain an average 59–68 mm SL in three years (Bolin, 1956; Fast, 1960; Smoker and Pearcy, 1970). Maximum life expectancy has been estimated as four (Bolin, 1956) or five (Fast, 1960) years. Smoker and Pearcy (1970) suggested some individuals may live eight years but were confident of assigned ages based on otolith analysis only to five years or less. In Oregon waters, northern lampfish mature at about 65 mm SL (approximately four years old) and spawning occurs from December to March; 20 to 25 mm SL individuals appear in largest proportions in trawl samples in winter, presumably about eight months after spawning (Smoker and Pearcy, 1970). In Monterey Bay, only northern lampfish over 50 mm SL had large eggs (Fast, 1960). Fast suggested that spawning occurred once in a season and possibly only once in a lifetime. Larvae of 3 mm total length (TL) were first found in the Monterey Bay plankton during early November, and larvae of less than 6 mm were present until August, indicating an approximately nine month spawning season. Gravid females occurred in San Pedro Basin samples from October through April, and individuals termed “postlarvae” were captured during five months of the year (Paxton, 1967b). The larvae were most common in CalCOFI collections along the California coastline between January and March (Moser et al., 1993). T R I PHOT U R US M E X ICAN US

The Mexican lampfish is a more important myctophid species in the southern portion of the region influenced by the California Current. This smaller fish ranges between northern Chile and San Francisco but is seldom caught north of Point Conception (Miller and Lea, 1972). Populations can be quite concentrated in areas with transitional or Equatorial water. In the CalCOFI region, Mexican lampfish were collected at more stations than any other species and were also among the most abundant species in a single tow (Berry and Perkins, 1966). This fish was also a commonly collected species in surveys of the Gulf of California (Lavenberg and Fitch, 1966; Robison, 1972; Brewer, 1973). Brewer noted that as over 23,000 specimens were caught at a single Gulf of California station, the Gulf population must be enormous. Imsand (1982) calculated the total population sizes of Mexican lampfish in the California Current and the Gulf of California to be approximately 2  1012 individuals each. However, densities of the two populations are quite different, as their areas of distribution have the ratio 5 (California Current): 1 (Gulf), where each unit of area equals approximately 106 km2. The abundance of Mexican lampfish in the California borderland varies by location and depth. It is more common in Santa Cruz Basin than offshore over the slope or in shallow Santa Barbara Basin and localized near the surface at night and at 500 m by day (Brown, 1974). It is the third most abundant fish in Santa Catalina Basin and occurred with fishes characterized by maximum daytime concentrations at around 450 m (Rainwater, 1975). In San Pedro Basin, Mexican lampfish have a diurnal center of distribution above 650 m and are seldom found shallower than 50 m at night (Paxton, 1967a). Captures there were greatest in November and December. Mexican lampfish forage on crustaceans, particularly euphausiids and copepods. Imsand (1981) compared the food of Mexican lampfish from the California Current region and Gulf of California with that of its congener the highseas lampfish, Triphoturus nigrescens, and found no significant difference

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in their feeding habits. The diet biomass of each was at least 88% euphausiids, less than 5% copepods, and less than 8% “other.” During a single diel-feeding period, both species prey on a variety of copepods but generally only a single species of the available euphausiids, apparently gorging on these when they are found (Imsand, 1981). The stomach contents of Mexican lampfish collected in the southern portion of the Gulf of California included ostracods, copepods, small shrimp, and, rarely, fish larvae (Holton, 1969). Information about Mexican lampfish growth and reproduction is limited. It attains a maximum size of about 70 mm SL (Wisner, 1976) at around four years of age (Childress et al., 1980). Their larvae were the sixth most common fish larva collected by CalCOFI survey cruises between 1951 and 1984, with an estimated abundance of over 404,000 individuals 10 m
2 of sea surface (Moser et al., 1994), and were most commonly collected July to September off Baja California (Moser et al., 1993). CYC LOT HON E S IG NATA AN D C. AC C L I N I DE NS

Species of the gonostomatid genus Cyclothone are among the most common oceanic pelagic fishes (Kashkin, 1995). Cyclothone “spp.” was the fifteenth most abundant larval taxon collected in CalCOFI survey cruises between 1951 and 1984 with over 68,000 individuals 10 m
2 sea surface (Moser et al., 1994). The larvae were plentiful throughout the year off the coasts of both California and Baja California (Moser et al., 1993). Several Cyclothone species have been collected off California and Baja California, but only the showy and benttooth bristlemouths are abundant (Berry and Perkins, 1966). The showy bristlemouth is largely an eastern Pacific species, although it has been collected at low latitudes of the central Pacific east of about 160° E (Kobayashi, 1973). The benttooth bristlemouth, probably the most abundant species of the genus, occurs in the Atlantic, Indian, and Pacific oceans (Kobayashi, 1973). In the eastern Pacific, it ranges from Oregon to the Peru-Chile Trench (Miller and Lea, 1972) and extends westward in equatorial waters to the Indo-Malayan archipelago and off Japan (Kashkin, 1995). Showy bristlemouth adults reach a maximum size of about 40 mm SL and usually live at depths between 200 and 800 m with maximum abundance at about 400 to 500 m (Kobayashi, 1973). Benttooth bristlemouth adults attain a length of approximately 65 mm SL and are collected mainly between 300 and 1,700 m deep with peak abundance at 600–700 m (Kobayashi, 1973). The vertical size distribution pattern of benttooth bristlemouths is similar to that of other Cyclothone species. Relatively small specimens occur within the upper portion of the range (300–500 m). Size then increases with depth to or deeper than the region of maximum abundance. No clear size trend is seen among individuals collected deeper than 1,100 m, and occasionally a larger specimen is found shallower than the usual range (Kobayashi, 1973). Distributions of these two species of bristlemouths vary in the borderland. Off Santa Barbara, the less pigmented showy bristlemouth is mesopelagic, with adult distribution maxima at both the surface to 100 m and 400 to 500 m, whereas seaward of the Channel Islands the darker benttooth bristlemouth lives between 300 and 1,200 m with a maximum abundance at 700 to 800 m (DeWitt, 1972). Young fish occupy shallow waters (DeWitt, 1972; Talbot, 1973). In Santa Catalina Basin, adult benttooth bristlemouth abundance was significantly correlated with depth down to 1,000 m (Talbot, 1973). Neither species appears to migrate vertically (DeWitt, 1972; Talbot, 1973).

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Benttooth bristlemouths live in zones of the eastern Pacific with low oxygen concentration (Kashkin, 1995); long gill filaments may allow them to thrive in these regions (DeWitt, 1972). Gill lamellae on the first branchial arch of benttooth bristlemouths vary depending on where the fish are collected. Those from areas with low dissolved oxygen concentrations have gill lamellae that are greatly expanded, heavily branched, and unfused, whereas gill lamellae of specimens from waters with high oxygen concentrations are either fused or otherwise greatly reduced in surface area (Kobayashi, 1973). Both Cyclothone species prey mainly on crustaceans. Stomachs of 277 showy bristlemouths from Santa Cruz Basin and the slope contained copepods (35%), and less often unrecognizable material and ostracods (DeWitt and Cailliet, 1972). Most of the observed prey organisms live in the upper 200 m, and, therefore, stomach contents suggest some vertical migration. More than 50% of the stomachs were empty, and deeper caught fish had empty stomachs more often than those caught shallower. “Unrecognizable material” was the most common food category in the stomachs of 225 benttooth bristlemouths from the same area, followed by copepods, chaetognaths, ostracods, and amphipods. The copepods eaten are found predominantly below 200 m (DeWitt and Cailliet, 1972). Bristlemouth males are smaller than the females and become macrosmatic when mature (Marshall 1967; 1980). Showy bristlemouths may be single spawners, with most females reaching sexual maturity at age 3 (Aughtry, 1953 cited in Miya and Nemoto, 1991). The larger benttooth bristlemouths may spawn multiple times and have a higher fecundity (Miya and Nemoto, 1991). More information about the life histories of these two species would allow comparisons with those of other bristlemouths such as the study by Miya and Nemoto (1991) of three species from off Japan.

Vertical Distributions The vertical distributions of the myctophids and neoscopelid in San Pedro Basin do not necessarily follow groupings of the species based on their horizontal distributions, which largely coincide with the presence of the waters from three water masses or mixtures thereof (Paxton, 1967a). Paxton divided these species into five geographic groups: 1) SubarcticTransitional (blue lanternfish, California headlightfish, northern lampfish, broadfin lampfish); 2) Transitional (California lanternfish, sunbeam lampfish Lampadena urophaos, giant lampfish Parvilux ingens); 3) Subarctic-Central Pacific (California flashlightfish, pinpoint lampfish); 4) Eastern Equatorial (Diogenes lanternfish Diogenichthys laternatus, Mexican lampfish, Pacific blackchin); and 5) Cosmopolitan (longfin lanternfish Diogenichthys atlanticus, Taaningichthys bathyphilus, dogtooth lampfish). Included in his five observed vertical distribution patterns were: two deep species that do not migrate and have an apparent upper nocturnal limit of 650 m (T. bathyphilus, Pacific blackchin); three deep species with diurnal centers below 650 m that migrate to 50 m (sunbeam lampfish, pinpoint lampfish, giant lampfish); nine shallow species with a diurnal distribution above 650 m, four of which migrate into the upper 10 m (longfin lanternfish, California lanternfish, California headlightfish, dogtooth lampfish) and five of which migrate to between 10 and 50 m (Diogenes lanternfish, blue lanternfish, northern lampfish, Mexican lampfish, broadfin lampfish); and one shallow species (California flashlightfish) found below 350 m during daytime and 150 m at night.

Paxton (1967a) hypothesized that the broad ranges of dogtooth lampfish and longfin lanternfish are probably the result of a wide tolerance of conditions. Yet, other species lacking horizontal ranges that extend over all three water masses may encounter all three water types over their vertical ranges. Depths of occurrence are possibly related to the thermocline at 50 m and the year round halocline at 150 m, but apparently not to dissolved oxygen. Paxton (1967a) concluded that temperature and light strongly influence both vertical and horizontal limits of lanternfishes. Vertical distributions of midwater species may change in locales differing in water depth and distance from shore. Offshore of Santa Barbara, Brown (1974) found California smoothtongue to be most abundant between 150–450 m in Santa Barbara Basin, but seaward in Santa Cruz Basin the population of mostly young fish lived deeper. Northern lampfish concentrations varied from around 250 m in Santa Barbara Basin to above 400 m over the slope and deeper in Santa Cruz Basin. California headlightfish had a relatively shallow distribution maximum at above 200 m in Santa Cruz Basin, but over the slope were most commonly caught at about 400 m. Showy bristlemouths were caught at each of the three areas; they occurred at 300–500 m in open water and had less defined concentrations in the basins. Benttooth bristlemouth were most abundant in Santa Cruz Basin between 700 to 900 m and scarce in shallow Santa Barbara Basin.

Ecological Groupings and Community Compositions Several studies have searched for ecological groupings of the midwater fauna of the southern California borderland. Ebeling et al. (1970) tested for groupings of fishes and some invertebrates collected in open 3 m Isaacs-Kidd midwater trawl (IKMT) collections from the San Pedro (36 samples) and Santa Catalina (55 samples) basins and the continental slope between Guadalupe Island and San Juan Seamount (11 samples). Species distributions were clumped, especially those of vertically migrating mesopelagic species living at intermediate depths during daytime; bathypelagic species were less clumped. Common species segregated into three general groups (upper mesopelagic, mesopelagic, and bathypelagic), with some rare species as outliers. As in an earlier study by Lavenberg and Ebeling (1967), species of subarctic, transitional and central waters dominated mesopelagic groups, whereas bathypelagic groups contained largely equatorial water, pantropic, and cosmopolitan species. Even though the fauna of deeper Santa Catalina Basin is more diverse and oceanic than that of the shallower inshore San Pedro Basin, 60% of the San Pedro groupings clustered in a manner similar to those produced by analysis of the total data set. Ebeling et al. (1970) did not find evidence of taxonomically similar species competitively excluding one another from similar ecological niches. Taxonomic diversity varied in the ecological groups formed, some of which contained closely related species. Many rare species may be transients that contribute little to the structure of the communities specifically adapted to the borderland and surrounding regions. However, rare species in this region are not necessarily rare species elsewhere and might be ecologically more important in other areas. Groups differed in the depth, locality, season, and vertical migration patterns of their members. Bathypelagic groups were better defined than mesopelagic groups, and more of their variance could be related to physical parameters. Thus,

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Ebeling et al. (1970) determined that deep-sea animals do assemble into ecological groups, but these groupings are less obvious in the mesopelagic region because of interactions and overlapping vertical ranges. The middle mesopelagic transition groups contain the most abundant species, followed by the bathypelagic and upper mesopelagic groups. The mesopelagic zone constitutes approximately 33% of the environment sampled in this study, yet supports 75% of the groups containing 60% of the species; its faunal complexity is greater than that of the vast bathypelagic zone, which is comparatively uniform and sparsely populated. Ebeling et al. (1971) used factor analysis to produce 10–14 groups of intercorrelated species and environmental measures based on data from monthly collections in Santa Barbara and Santa Cruz basins with a 1.8 m IKMT equipped with a fourchambered cod end. Four groupings of fishes and invertebrates were termed “resident communities”, which overlap in space and time and interact with the remaining transitory groups of offshore species, larvae, and environmental factors. Resident communities remained intact no matter how many factors were analyzed and were predicted to be more stable in composition, abundance, and function than were transitory groups, members of which may have seasonal abundances that do not always vary synchronously. Members of transitory groups may be almost equally abundant or replace each other in abundance seasonally or year-to-year. The Ebeling et al. (1971) model indicates that midwater animals live in associations with varying degrees of structure. The parameters depth, location, and time have direct effects on species associations and behavior. Within the basins, abundances of animals are related to features such as time of day, location, bottom depth, trawl depth, and temperature. However, as species abundances were not correlated with the group of bathythermograph temperatures and seasonal parameters, water mass characteristics such as temperature-depth profiles influence the animals either indirectly or not at all. Ebeling et al. (1971) hypothesized that the resident communities of this region are not greatly affected by localized variations in the water resulting from upwelling or currents bringing in different water mass types. The resident communities overlap in space and time but are distinguishable by the relatively stable concordant abundances of their members. Transitory species, in contrast, move in and out of the area and often segregate into relatively unstable groups by their different daily and seasonal movements. Based on a year’s data from monthly water samples and discrete-depth collections taken with a 1.8 m modified Tucker trawl, Rainwater (1975) examined the species associations of fishes living between 200 and 800 m in Santa Catalina Basin to determine if the midwaters could be partitioned as habitat regimes that relate to environmental factors and these associations. A subset of 27 frequently-caught species with significantly distinct bathymetric distributions clustered into seven species groups of two to five species with differing depth distributions and vertical migration patterns. Daytime and nighttime associations each contributed to the formation of two species groups; species of three groups co-occur both day and night. Based on the same species, 151 sites (trawls) clustered into five shallow-depth (upper mesopelagic, 55 sites) regime groups, four middle-depth (lower mesopelagic, 48 sites) regime groups, and two deep-water (bathypelagic, 48 sites) regime groups. Only four relatively rare species were randomly distributed among the site groups. The upper mesopelagic regime

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contained significant portions of the abundances of members of four species groups. The lower mesopelagic was inhabited largely by members of two species groups. The two bathypelagic regime site groups had the lowest total abundances of fishes. One of the species groups was well represented in the bathypelagic collections from 550–800 m, as was the benttooth bristlemouth from another. Of temperature, salinity, oxygen, depth, and month of year, only month of year was found not to be significant in explaining the separation of the site groups with the exception of one pair. Thus season appears to have little or no effect on the groupings of trawls because of changing species abundances and composition. Members of each of Rainwater’s (1975) seven species associations frequently co-occurred in trawls and displayed similar abundance trends in those trawls. The members of each association appear to be adapted to a set of environmental conditions and co-occur wherever those conditions are found. Two of her species groups contain a mixture of the six fish species in two resident communities of Ebeling et al. (1971). Unfortunately, Rainwater (1975) collected only in the mesopelagic zone between 200 and 800 m, so many vertically migrating species were not sampled in the upper portions of their ranges above these depths at night. Information about shallower nighttime abundance peaks could change the composition of the species associations as well as the trawl groupings. Detailed reports of the abundances and distributions of at least the important members of the midwater community for major portions of their vertical ranges, such as have been completed in the eastern Gulf of Mexico (e.g., Hopkins and Lancraft, 1984; Gartner et al., 1987; Sutton and Hopkins, 1996a), are lacking for the waters off the Californias. Thus, comparisons of community composition within a basin over time, between basins, or with other geographic areas are difficult. Bailey (1984) included some information on the proportions of fishes in his catches at three stations increasingly seaward of San Diego (table 13-4). Bristlemouths were the most common fishes at all three locations. Two species of bristlemouths also dominated the Rodriguez Dome and Santa Cruz Basin catches of Brown (1974) and the San Pedro and Santa Catalina Basin catches of Atsatt and Seapy (1974, table 13-4). Because the objective of this latter study was analysis of sampling variability in replicated midwater trawls, only the upper 650 m were sampled.

Feeding Many midwater fishes are hard-bodied (crustacean) zooplanktivores (Gartner et al., 1997). Not surprisingly, the great majority of the midwater fishes in the California Current region feed on small crustaceans (Paxton, 1967b; Collard, 1970; DeWitt and Cailliet, 1972; Tyler and Pearcy, 1975; Pearcy et al., 1979; Imsand, 1981). Two northern species that are common in inshore basins of the borderland exhibit very different feeding habits (Cailliet and Ebeling, 1990). The northern lampfish is abundant in both near and offshore basins of the borderland, but the California smoothtongue occurs in large numbers only inshore. The lanternfish eats larger, faster, more elusive prey and feeds mainly on crustaceans, whereas the deep-sea smelt eats smaller, less active prey and feeds mostly on larvaceans and salps, which are less dense and only seasonally available offshore. Cailliet and Ebeling (1990) concluded that feeding differences might account for the offshore density differences of these two species.

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Basic information on the food web of the midwater fishes off California exists (See fig. 14-11, chapter 14). The midwater fish assemblage consists of vertically migrating zooplanktivores (e.g., lanternfishes), nonmigrating zooplanktivores (e.g., hatchetfishes), ambush predators (e.g., anglerfishes, most barbeled dragonfishes), and active foragers (e.g., barracudinas, Robison and Bailey, 1982; Gartner et al., 1997). More thorough food web investigations, such as those completed in the eastern Gulf of Mexico (e.g., Hopkins and Baird, 1985; Hopkins and Gartner, 1992; Sutton et al., 1995; Sutton and Hopkins, 1996b; Hopkins et al., 1996; Hopkins and Sutton, 1998), are still needed for these midwater fishes and invertebrates. Little is known about the impact of feeding on prey populations, resource partitioning, or the role of this community in the energy budget of the area. Clarke (1972) concluded that myctophids and other vertically migrating micronekton probably account for most of the zooplankton consumption in the tropical open ocean. The very large populations of some midwater fishes off the Californias must be supported by large quantities of localized prey, and their feces must represent a great source of energy to deeper waters, particularly the benthos (Robison and Bailey, 1981). Also transported either to the benthos (Robison and Bailey, 1981) or to predators (e. g., Thompson et al., 1998) will be metals, pesticides, or any other contaminants (e.g., Cox, 1970; Robison, 1973b; MacGregor, 1974; Baird et al., 1975; Zdanowicz et al., 1996; Takahashi et al., 2000) present in the population of midwater fishes.

Chemical Compositions, Swimbladders, and Buoyancy Prey availability is reflected in fish tissue densities and thus may affect whether or not a species is neutrally buoyant. Pelagic fishes utilize several means of maintaining their position in the water column (Gee, 1983). If their bodies are denser than seawater, they must swim to avoid sinking. Hydrodynamic lift provided by outstretched pectoral fins while moving forward aids in the maintenance of vertical position. Pelagic teleosts commonly have a swimbladder filled with gases. Usually a swimbladder volume of about 5% of the fish’s body volume is necessary for neutral buoyancy (Taylor, 1922). The density of the body tissues may be decreased either by increased water contents often accompanied by decreased skeletal density (Denton and Marshall, 1958) or increased lipid stores, usually as triacylglycerols but sometimes as lower density wax esters (Hølmer, 1989; Lee and Patton, 1989; Morris and Culkin, 1989). In some cases, the juveniles of a species have inflated swimbladders, and then the buoyancy mechanism changes with growth. Examples of each of these means of achieving buoyancy are found in the midwater fishes from off California (table 13-5). Species that have decreased densities due to higher water contents (83% wet weight, WW) tend to live at deeper depths, lack inflated swimbladders, not make extensive diurnal vertical migrations, and have low protein (8% WW), skeletal ash (1.3% WW), and lipid (7% WW) contents (Childress and Nygaard, 1973). Examples of California fishes with higher water contents are the Pacific blacksmelt, shining tubeshoulder, fangtooth, Pacific blackchin, and pinpoint lampfish, as well as the stomiids the shining loosejaw, Pacific viperfish, and blackbelly dragonfish (Childress and Nygaard, 1973; Neighbors and Nafpaktitis, 1982; Neighbors, 1988). Pinpoint lampfish from the northern subarctic Pacific off

Japan had lipid contents averaging over 14% WW. These, like those from off California, accumulated wax esters (Seo et al., 1996; Saito and Murata, 1998). Pacific blacksmelt and Pacific viperfish were two of the four species in which Yancey et al. (1989) found gelatinous material containing glycosaminoglycans. These polysaccharides, which are major components of animal gelatinous tissue in general, are highly hydroscopic and thus hold some of the water that aids in the buoyancy of these species. This gelatinous material is particularly evident as a subcutaneous layer in Pacific blacksmelt. The deep-sea smelts off California fall into two ecological groupings (Childress and Nygaard, 1973). Like the already mentioned Pacific blacksmelt, the robust blacksmelt, Pseudobathylagus milleri, a fish with a high water and low lipid content (Childress and Nygaard, 1973; Neighbors, 1988), lives deep in the water column and does not make extensive vertical migrations. Other species, such as the snubnose blacksmelt, popeye blacksmelt (Lipolagus ochotensis), and California smoothtongue, make at least diffuse migrations to shallower waters. None of these bathylagids have inflated swimbladders as adults. Increased lipid contents, in the form of triacylglycerols, may be important in the buoyancy of at least the larger individuals of these migrators, particularly in the latter two species (Neighbors, 1988). Inflated swimbladders are found in the adults of many mesopelagic fishes, including representatives of the hatchetfishes, lightfishes, bigscales and lanternfishes (Marshall, 1960, 1971b, 1972). Fishes collected by trawls brought rapidly to the surface are subjected to rapid pressure decreases of one atmosphere per 10 m depth decrease. The state of inflation of the swimbladders at the time of capture in fishes hauled up over many meters is difficult to determine. Despite this pressure change, burst swimbladders or ruptured body walls are rarely seen (Marshall, 1960) or seen only in some species (Kleckner and Gibbs, 1972). Hatchetfishes often float at the surface of a catch with greatly expanded swimbladders forcing the viscera out of their mouths. Hatchetfishes do not migrate into shallow waters at night, but rather remain at similar depths both day and night. These fishes appear to maintain inflated swimbladders (Marshall, 1960; Capen, 1967; Neighbors, 1988). Hatchetfishes from off California are high in protein and skeletal ash contents and low in lipid and water contents, although deeper living Sternoptyx species may have higher water contents (Childress and Nygaard, 1973). Buoyancy strategies in the big scales from off California vary. The highsnout melamphaid has a low water content and inflated swimbladder (Childress and Nygaard, 1973); information about its lipid content is lacking. A longjaw bigscale, Scopeloberyx robustus, with an inflated swimbladder had a high lipid content (22% WW) consisting largely of triacylglycerols (Neighbors, 1988). Crested and twospine, Scopelogadus mizolepis bispinosus, bigscales have high water contents and lack inflated swimbladders (Childress and Nygaard, 1973; Neighbors, 1988). Bristlemouths also differ in their buoyancy mechanisms. Some, such as Diplophos taenia from off Baja California, have inflated swimbladders and low lipid contents with triacylglycerols used for energy storage (Neighbors, 1988). The shallower living showy bristlemouth has an inflated swimbladder (DeWitt, 1972) and a lipid content of around 4% or less, consisting largely of both wax esters and triacylglycerols (Nevenzel and Menon, 1980; Bailey and Robison, 1986; Neighbors, 1988). Many species of Cyclothone, including the deeper living benttooth bristlemouth (Marshall, 1960; DeWitt, 1972), develop fat-invested swimbladders (Marshall, 1960). In these

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Mexican lampfish Northern lampfish Broadfin lampfish Pinpoint lampfish (Japan)

Lower water content (80%) Higher lipid content ( 11%)

Pacific viperfish** Benttooth bristlemouth

WE & Tag

Nonfunctional Swimbladders

Snubnose blacksmelt California smoothtongue Blackbelly dragonfish Pacific blackdragon Crested bigscale Two spine bigscale Panama snaggletooth Shining loosejaw Fangtooth Pacific blackchin Giant lampfish Pacific blacksmelt** Popeye blacksmelt

Triacylglycerols

Showy bristlemouth

WE & Tag

Taaningichthys bathyphilus

Lowcrest hatchetfish Tropical hatchetfish Bottlelight California flashlightfish

Longjaw bigscale

Slender hatchetfish Sternoptyx spp.

Triacylglycerols

Functional Swimbladders

Blue lanternfish*

California lanternfish* California headlightfish Dogtooth lampfish

Sometimes Inflated? Triacylglycerols

NOTE: Compositions of specimens from the California Current region off southern California unless otherwise noted. As chemical composition may change with age, composition classification based on highest values reported in the literature. Nonfunctional swimbladders may be absent, regressed, or fat invested. Functional swimbladders may or may not be inflated. Neutral lipids stored classified as mixture if both wax esters and triacylglycerols account for over 10% of the lipid content. From Nevenzel et al., 1969; Butler and Pearcy, 1972; Childress and Nygaard, 1973; Torres et al, 1979; Nevenzel and Menon, 1980; Bailey and Robison, 1986; Neighbors and Nafpaktitis, 1982; Neighbors, 1988; Seo et al., 1996; Saito and Murata, 1998.

* Species with large pectorals and therefore possibly utilizing hydrodynamic lift (Gee, 1983). ** Species with buoyant glycosaminoglycan layers present (Yancey et al., 1989).

Lower water content ( 80%) Lower lipid content ( 6%)

Pinpoint lampfish

Wax Esters

Higher water content ( 81%) Lower lipid content ( 8%)

Chemical composition (% wwt)

Type of Neutral Lipid Present

TA B L E 13-5

Chemical Compositions and Swimbladder States of Selected Midwater Fishes

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fishes, lipids are deposited between the peritoneum and the outer wall of the swimbladder. Lipid deposition, which begins in the larva, continues as the fish grows and ultimately surrounds the regressing swimbladder. Marshall (1960) noted that in a number of midwater fishes “the swimbladder regresses after metamorphosis and becomes a convenient site for the deposition of fat, but this plays a relatively small part on the ‘credit side’ of the ‘buoyancy balance sheet.’ The benttooth bristlemouth has a lipid content of 4–6% WW consisting largely of wax esters and triacylglycerols (Childress and Nygaard, 1973; Nevenzel and Menon, 1980; Bailey and Robison, 1986). DeWitt (1972) observed oily globules both around the swimbladder and along the vertical septum between the muscle masses along the back in this species. Lanternfishes, a speciose family found in all oceans at various depths, exhibit the range of buoyancy mechanisms (Bone, 1973). Much of the variation is related to the state of the swimbladder present. Some species do not have a swimbladder. If their bodies are denser than seawater, these species must constantly swim to maintain their position in the water column. Many juvenile lanternfishes have functional swimbladders. A swimbladder that ceases to grow as the fish grows has been termed “regressed.” Such a swimbladder is seen in the deep-living pinpoint lampfish (Butler and Pearcy, 1972; Neighbors and Nafpaktitis, 1982), a species already noted to have a higher water content. Some regressed swimbladders become fat invested (Capen, 1967; Zahuranec and Pugh, 1971). Species that deposit large stores of lipids do so throughout their bodies, e.g., around the viscera and in the musculature, subcutaneous sacs, and bones (Nevenzel et al., 1969; FalkPetersen et al., 1986; Reinhardt and Van Vleet, 1986; Phleger et al., 1997, 1999). Some lanternfishes have inflated swimbladders both as juveniles and adults. Species that remain within a relatively narrow depth range both day and night may have constantly inflated swimbladders. Lanternfishes commonly undergo extensive diel vertical migrations and may even reach the upper 50 m or the surface at night. Whether lanternfishes with functional swimbladders maintain either constant volumes (gas volume maintained at approximately 5% of the fish’s body volume as required for neutral buoyancy throughout the vertical range) or constant masses (amount of gas remains the same and thus swimbladder volume is sufficient for neutral buoyancy only in the decreased pressure of the upper portion of the vertical range) of gas throughout their vertical ranges has been discussed by many (e.g., Kanwisher and Ebeling, 1957; Marshall, 1960; Alexander, 1971, 1972; D’Aoust, 1971; Ross, 1976; Vent and Pickwell, 1977; Blaxter and Tytler, 1978; Kalish et al., 1986). Additionally, the swimbladders of some species may not always be inflated with gas. Specimens have been collected with well developed but uninflated swimbladders (Marshall, 1960; Butler and Pearcy, 1972; Kleckner and Gibbs, 1972; Neighbors, 1992). Such swimbladders are different from regressed or fat invested swimbladders and have the appearance of still being functional and able to be inflated at some time. Lanternfishes from off California exhibit inflated, noninflated, and fat invested swimbladders. The California flashlightfish, which lives at depths similar to those of some hatchetfish (Argyropelecus) species, does not make extensive vertical migrations into surface waters and maintains an inflated swimbladder (Butler and Pearcy, 1972; Neighbors and Nafpaktitis; 1982). Although adults of both blue and California lanternfishes may be collected with inflated swimbladders, those of

some specimens contain no obvious gas (Butler and Pearcy, 1972; Neighbors, 1992). These two species migrate to shallow depths and can be collected at the surface with a neuston net at night. Neighbors (1992) found that fish collected at the surface at night more often had inflated swimbladders than fish collected at daytime depths and hypothesized that these species maintain neither a constant mass nor constant volume of gas but rather inflate their swimbladders on the way to the surface and remove gas as they descend. The northern and Mexican lampfish have fat invested swimbladders as adults (Capen, 1967; Butler and Pearcy, 1972). That of the broadfin lampfish is regressed and not observed to contain gas in adults (Butler and Pearcy, 1972; Neighbors and Nafpaktitis, 1982). Variations in lipid contents as well as swimbladder states complicate a discussion of buoyancy mechanisms in the common lanternfishes. The blue lanternfish, with high protein and skeletal ash and low lipid and water contents (Childress and Nygaard, 1973), must swim to maintain its position if its swimbladder is not inflated to a size sufficient to result in neutral buoyancy. Its large pectoral fins add hydrodynamic lift (Gee, 1983). Lipids, largely in the form of triacylglycerols, remain below 4% WW even in larger individuals (Neighbors and Nafpaktitis, 1982). The density of California lanternfish must be more variable. Not only are these fish found with and without inflated swimbladders, but some larger fish have lipid contents of over 10% WW, or even over 20% WW off Japan (Seo et al., 1996; Saito and Murata, 1998), consisting largely of triacylglycerols, whereas others do not. Differences in lipid content may be seasonal (Neighbors and Nafpaktitis, 1982) and represent usage of stored lipids for metabolism. The northern, Mexican, and broadfin lampfishes all accumulate large stores of lipids (11% WW), predominantly as wax esters (Nevenzel et al., 1969; Neighbors and Nafpaktitis, 1982). Lipid levels as percentages of body weight increase as the swimbladder becomes less important in buoyancy and then appear to remain relatively constant (Capen, 1967; Butler and Pearcy, 1972; Neighbors and Nafpaktitis, 1982). In addition to providing buoyancy, these lipids consisting largely of wax esters and only small amounts of triacylglycerols must also function as energy stores. The question of why some fishes store wax esters while others deposit the more usual triacylglycerols remains intriguing. The waxes are not simply transferred to the fishes from waxester rich crustaceans (Lee at al., 1971; Lee and Hirota, 1973; Saito and Murata, 1998) in their diet, but rather are synthesized by the fishes (Kayama and Nevenzel, 1974, Seo et al., 2001). The lower specific gravities of wax esters as compared to triacylglycerols (Lewis, 1970) makes them better buoyancy agents, but Phleger (1991, 1998) notes that fish lipid densities at the pressures and temperatures encountered by deep-sea fishes need to be examined. When present in substantial quantities, both types of lipids will increase buoyancy. As species with high lipid contents tend to accumulate either wax esters or triacylglycerols, both types of lipid must serve as energy reserves (Sargent, 1976; Falk-Petersen et al., 1986). Hypotheses concerning wax ester deposition, some based on studies of deep living herbivorous crustaceans that also deposit wax esters, are generally ecologically based. One leading hypothesis states that the ability of deep-sea fishes to deposit lipids rapidly (Sargent et al., 1976) when seasonal or scarce resources are available would offer a great advantage. Rapid deposititon of lipids would be particularly advantageous in the case of temperate, polar or deeper living species (Lee et al., 1971; Lee and Hirota, 1973). Seo et al. (1996) found 17

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tropical western Pacific lanternfishes generally to lack large stores of lipids and contain only trace amounts or no wax esters, whereas subarctic species had larger stores of either triacylglycerols or wax esters. Wax ester containing species exhibited limited or no diel vertical migration (Seo et al., 1996; Saito and Murata, 1998.) Midwater species living in the same region, both geographic and vertical, often vary in the type of lipid deposited, as noted for California fishes. Even midwater fishes in highly seasonal polar regions differ in their storage lipids, as shown by studies near Antarctica (Reinhardt and Van Vleet, 1986; Phleger et al., 1997; Phleger et al., 1999). For whatever reason, some very abundant midwater fish species, including members of the genus Cyclothone and the lanternfishes Electrona antarctica off Antarctica, glacier lanternfish, Benthosema glaciale, off Norway (Falk-Petersen et al., 1986), northern lampfish in the Subarctic Pacific, and the Mexican lampfish in the eastern Pacific, deposit large stores of wax esters. Information about whether or not California midwater fishes are neutrally buoyant comes from observations made at middepths by Barham (1971) from deep submersible vehicles off San Diego, California. Hatchetfishes were sometimes motionless and always oriented horizontally. Active snipe eels were vertically oriented with their heads uppermost and their elongate bodies in sinusoidal curves. Benttooth bristlemouths, California smoothtongues, and northern and Mexican lampfishes were seen hanging vertically in the water column. The two lanternfishes appeared to drift in loose aggregations during daytime. Most myctophids were hanging in the water column with their heads upward in the late afternoon and downward in the morning. Respiratory water currents may push them up or down, depending on their orientation. Barham (1971) proposed that lanternfishes fall into two groups: Those that are active, which may have functional swimbladders, large eyes, and firm silvery bodies with thin caudal peduncles, and those that are lethargic, which lack functional swimbladders, have small or medium-sized eyes, and soft dark bodies with thick caudal peduncles. Active myctophids migrate to the surface at night, whereas lethargic species only rarely reach the surface during their vertical migrations. Bone (1973) suggested that emphasis for characteristics of active and inactive species should be placed on the lipids present and fish densities. The active blue and California lanternfishes may or may not have inflated swimbladders and, in some members of the latter species, large stores of triacylglycerols. Thus many, if not all, of these fishes may need to swim to maintain their position in the water column. The lethargic northern and Mexican lampfishes, with their fat-invested swimbladders and large, relatively constant stores of wax esters, are apparently at least close to neutrally buoyant.

Growth and Reproduction Childress et al. (1980) compared growth rates of four mesopelagic (California smoothtongue, northern lampfish, Mexican lampfish, and broadfin lampfish) and five bathypelagic (crested bigscale, Panama snaggletooth Borostomias panamensis, pinpoint lampfish, robust blacksmelt, and sharpchin slickhead Bajacalifornia burragei) species with values from the literature for two epipelagic fishes (Pacific sardine and northern anchovy). The epipelagic species appeared to have the highest and mesopelagic species the lowest growth rates, but standard methods for comparing growth rates (e.g.,

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von Bertalanffy’s K parameter) were not used. Supposed faster growth rates of bathypelagic fishes compared to mesopelagic ones were attributed to higher relative growth efficiencies achieved by having low metabolic rates. Longevities, determined by counting otolith rings that were assumed to be annual, ranged from 4 to 8 years for epipelagic and bathypelagic species, and 5 to 8 years for mesopelagic species. Egg diameter data suggested that California smoothtongue, northern lampfish and broadfin lampfish first reproduce in their third year, whereas the five bathypelagic species do so only in their last year. Childress et al. (1980) characterized the epipelagic species as generally being large and having rapid growth, long life, and early and repeated reproduction. Small size, slow growth, long life, and early and repeated reproduction were thought to typify mesopelagic species. Bathypelagic species were characterized as generally having large size, rapid growth, somewhat shorter lives, and late, possibly singular, reproduction. The longevities that Childress et al. (1980) determined for the lanternfishes are greater than those of myctophid growth studies based on validated growth increments (e.g., Gartner, 1991a). Gartner (1991b) found that three mesopelagic myctophids from the eastern Gulf of Mexico grew rapidly, reaching their largest observed sizes in about one year. Moreover, these fast myctophid growth rates matched those of epipelagic fishes from the western North Atlantic. Gartner (1991b) suggested that because lanternfishes generally feed, reproduce, and develop in the epipelagial, their life history patterns are strongly influenced by that habitat. Greely et al. (1999) reached conclusions similar to those of Gartner (1991b) in their study of the age and growth of a mesopelagic myctophid of the Southern Ocean. Further study of mesopelagic and bathypelagic fishes from off California, particularly multiple species in common families, would improve our knowledge of growth rates, longevities, and reproduction of these fishes and help support or refute the above hypotheses. Information about the spawning of mesopelagic fishes in the California Current is limited to very general knowledge, even for abundant families such as the myctophids. Lanternfishes are oviparous; their larvae commonly occur in collections of larval fishes. Presumably, these fishes all have planktonic eggs, but myctophid eggs are infrequently collected (Robertson, 1977; Moser and Ahlstrom, 1996). Unlike other types of fish eggs that are collected by nets, myctophid eggs may be so fragile that they disintegrate during capture (Moser and Ahlstrom, 1996). In the eastern Gulf of Mexico, myctophid spawning occurs in the epipelagic zone and peaks after midnight (Gartner, 1993). In contrast, the lanternfish Benthosema pterotum spawns early in the night at depths of 100 to 300 m in the Gulf of Oman, and Gjøsæter and Tilseth (1988) proposed that these eggs hatch before they reach surface waters. Myctophid larvae may occur deep in the water column but generally are found in the upper mixed layer (Moser and Ahlstrom, 1996). These and other deep-sea fish larvae might be transported by surface currents during their time in shallower waters. Moser et al. (1994) listed the ranked abundances of the larval fish taxa from CalCOFI collections between 1951 and 1984. Deep-sea fishes that ranked above 20 in the list of the 245 most commonly collected larvae were Panama lightfish Vinciguerria lucetia (3), California smoothtongue (5), Mexican lampfish (6), northern lampfish (7), Diogenes lanternfish (11), snubnose blacksmelt (12), popeye blacksmelt (13), Cyclothone spp. (15), California flashlightfish (16), blue lanternfish (17),

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dogtooth lampfish (18), and Lampanyctus spp. (includes Nannobrachium spp.) (19). Moser and Watson (see chapter 11) summarize the distributions, abundances, and seasonalities of common midwater fish larvae present in the ichthyoplankton off California and Baja California. Distributions in the waters off the coasts of the Californias for adults and larvae of midwater fishes with known larval ranges (Moser et al., 1993, 1994) are shown in fig. 13-9. This limited portion of the ranges of these species and their larvae largely overlap. Larvae of many other fishes living in the CalCOFI region are collected there but less commonly (see chapter 11; Moser, 1996a). Larvae of the stomiid the Panama snaggletooth (Moser, 1996b), the platytrochtids shining tubeshoulder and streaklight tubeshoulder Holtbyrnia latifrons (Ambrose, 1996), and fangtooth (Watson, 1996) have not been taken in CalCOFI collections. Thus, a few species might be transported by currents from other areas to the region of the Californias during some portion of their life cycle.

Benthic and Benthopelagic Fishes Clearly, as with midwater fishes, the extent of our knowledge of deep-sea benthic fishes is ultimately a function of our ability to sample the deep-sea habitat efficiently. The fishes of the California deep slope and adjacent eastern Pacific Ocean basin have been thoroughly studied with benthic otter trawls (e.g., Stein, 1985; Wakefield and Smith, 1990; Lauth, 1999), freevehicle baited traps (Wilson, 1984; Wilson and Smith, 1985; Drazen et al., 2001), free-vehicle hook lines (Phleger and Soutar, 1971; Smith et al., 1979; Wilson, 1982, 1984), in situ observations from submersibles (Smith and Hamilton, 1983), towed camera sleds (Wakefield and Genin, 1987; Wakefield and Smith, 1990), and baited camera/video arrays (Isaacs and Schwartzlose, 1975; Wilson and Smith, 1984; Priede et al., 1990). Repeated deployments of such sampling devices by dozens of investigators over at least the past 50 years have led to our present knowledge of deep benthic and benthopelagic fishes of California. The California slope and rise between about 550 and 2,000 m is dominated by benthic and benthopelagic fishes of the following families (table 13-3): cuskeels (Ophidiidae), cat sharks (Scyliorhinidae), codlings (Moridae), dogfishes (Squalidae), eelpouts (Zoarcidae), flatfishes (Pleuronectidae), grenadiers (Macrouridae), hake (Merlucciidae), hagfishes (Myxinidae), lumpfishes (Cyclopteridae), rockfishes (Scorpaenidae), sablefish (Anoplopomatidae), skates (Rajiidae), sleeper sharks (Dalatiidae), slickheads (Alepocephalidae), and snailfishes (Liparidae) (Lauth, 1999; Wilson pers. obser. & various capture records). Between about 2,000 and 4,400 m off California, only about 20 species from the above families are likely present. Chiefly, these are grenadiers, followed by comparatively sparse occurrences of the highfin lizard fish, Bathysaurus mollis (Synodontidae), aphyonids, and cuskeels such as Bassozetus sp. (Stein, 1985) and Spectrunculus grandis. Deeper than about 4,400 m, and extending into the central Pacific basin to ca. 5,900 m depth and deeper, probably fewer than five or so abundant species exist, first among them the relatively abundant rough abyssal grenadier, Coryphaenoides (Nematonurus) yaquinae, likely followed by the cuskeel S. grandis. The few important benthic and benthopelagic species inhabiting depths greater than about 2,000 m off California, chiefly grenadier species, are relatively well studied ecologically. The same is not as true for many of the species living

between 550 and 2,000 m, save the most abundant and commercially important ones: the shortspine thornyhead (Sebastolobus alascanus), longspine thornyhead (S. altivelis), Dover sole (Microstomus pacificus), and sablefish (Anoplopoma fimbria), each of which has recognized fishery importance. Along the slope off Pt. Conception between about 550 and 732 m, the most abundant species by biomass from trawling (Lauth, 1999) is Dover sole (ca. 3.4 mt km
2), followed by the longspine (ca. 2.7 mt km
2) and shortspine (ca. 1.1 mt km
2) thornyheads, and sablefish (ca. 0.9 mt km
2). The 16 next most abundant species together make up less biomass than either Dover sole or longspine thornyhead alone. These four aforementioned species dominate the fish biomass to about 1,100 m depth. Below this depth, and to about 1,280 m, the Pacific grenadier, Coryphaenoides acrolepis, is significantly more abundant than any other slope species. This basic pattern of dominance persists between southern California (e.g., 34°N, 118°W) and the California slope off Eureka (e.g., 41.5°N, 125°W), except that shortspine thornyheads become less abundant, and Pacific hake (Merluccius productus) more abundant, between 550 and 1,100 m depth. Sablefish and the giant grenadier (Coryphaenoides pectoralis) become increasing more abundant between 1,100 and 1,280 m. As the longspine thornyhead is probably the most successful benthic species of the lower mid-portion of the California slope, maintaining significant abundance below 1,100 m where Dover sole and shortspine thornyhead do not, it could be regarded as a paradigm benthic species of the slope. Among the truly deep-sea fishes, the grenadiers (Macrouridae) form the richest depth replacement series down the California slope in terms of both numbers of species as well as collective extent of bathymetric range. The shallowest reported species (200 to 300 m) are the shoulderspot (Caelorinchus scaphopsis) and softhead (Malacocephalus laevis) grenadiers. The latter is known from very few records and reports from the California slope, but is abundant (Wilson, 2001) on an offshore guyot of 500-m crest depth (Fieberling Guyot; 32°27.82’N 127°47.00’W). Wilson (1985) summarized the depth replacement order off California for the grenadiers he studied as follows: California (Nezumia stelgidolepis), smooth (Nezumia liolepis), Pacific (Coryphaenoides acrolepis), ghostly (Coryphaenoides leptolepis), abyssal (Coryphaenoides armatus variabilis), and rough abyssal (Coryphaenoides yaquinae) grenadiers. The two additional California species are the giant grenadier, close in depth distribution to the Pacific grenadier (Iwamoto and Stein, 1974), and the threadfin grenadier (Coryphaenoides filifer), overlapping the depth distributions of the Pacific and ghostly grenadiers (Iwamoto and Stein, 1974; Stein and Pearcy, 1982) but with a more extensive bathypelagic habitat (Stein, 1985). Thus, there exist an upper-slope group of grenadiers abundant between about 200 and 600 m consisting of the shoulderspot, softhead, and California, a mid- to lower slope group abundant between about 600 and 2,000 m consisting of the smooth, Pacific, and giant, an upper continental rise group abundant between about 2,000 and 4,300 m consisting of the filamented, ghostly, and abyssal, and one truly Pacific basin species abundant below about 4,300 m—the rough abyssal grenadier (Wilson and Waples, 1983).

Life in the Deep-Slope and Basin Habitats Off southern California, the abundant deep-sea benthic and benthopelagic fishes inhabiting the borderland basins are

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F I G U R E 13-9. Distributions off the coasts of California and Baja California of the larvae and adults of selected midwater fishes. (Data sources:

Miller and Lea, 1972; Hart, 1973; Wisner, 1976; Moser et al., 1993; Moser et al., 1994; Fish Base Froese and Pauly, 2003).

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among the best studied ecologically. These include black hagfish, Pacific grenadier, smooth grenadier, longspine thornyhead, and sablefish. The most studied borderland basin where the above assemblage plus several other species (table 13-3) can be found is the Santa Catalina Basin (SCB) lying at about 1,340 m (fig. 13-2). The benthic community of this deep-sea basin has been thoroughly studied as a unit with all of the sampling devices listed above. In addition, the various fish species have been separately studied elsewhere in their respective ranges; our focus here is the best-known species. The longspine thornyhead (fig. 13-10) is the most abundant benthic fish in the SCB at a density of ca. 2 individuals 100 m
2 and is uniformly distributed (Smith and Hamilton, 1983). Black hagfish and smooth grenadier are likely next in abundance there. Elsewhere along the central and northern California slope between Point Conception and Eureka, longspine thornyhead is in greatest abundance between about 700 and 900 m where it numerically dominates the mid- to deep-slope assemblage by a huge degree (Lauth, 1999). Wakefield and Smith (1990) estimated its average density on the California slope off Big Sur at as high as 8 individuals 100 m
2 near 1,000 m depth, decreasing to ca. 2 individuals 100 m
2 near 1,200 m (as in the SCB). In the deep waters of Monterey Bay, the estimate was ca. 4 individuals 100 m
2 at 800 m, and 1.3 individuals 100 m
2 near 1,200 m (Vetter and Lynn, 1997). Wakefield and Smith (1990) suggested that 83% of the population (biomass) was contained between 600 and 1,000 m depth on the slope. Along the entire extent of the slope between Pt. Conception and Vancouver Island, Canada, approximately 81% of the total biomass reported for this species was between 550 and 1,100 m (Lauth, 1999). The catch per unit effort (CPUE) in the above depth interval ranged between ca. 3.3 mt km
2 off Point Conception to ca. 3.6 mt km
2 off Eureka, California, where it is the most abundant fish in that depth interval. Longspine thornyhead is a determinate spawner that spawns annually (but with multiple iterations per female over several years) during February and March off California (Wakefield and Smith, 1990, plus authors cited therein). Newly hatched larvae occur in the near-surface plankton into late spring, but the pelagic development phase can last for 18 to 20 months (Moser, 1974) before juveniles settle at ca. 55 mm SL (Wakefield and Smith, 1990). Within the first year after settlement, fish probably reach 80 mm SL, and adults evidently spawn by about 150 mm SL. Based on the growth rings of sagittae, a fish that size would be between 5 and 8 years old (Kline, 1996). Daytime observations from the deep submersible Alvin of pelagic juveniles of longspine thornyhead in midwater over the SCB indicated greatest abundance near 600 m (Smith and Brown, 1983). That pelagic juveniles concentrate near that depth in midwater over a deep (1,300 m) basin is notable because it coincides with the shallowest depth of occurrence of newly-settled juveniles on the slope (Wakefield and Smith, 1990). Juveniles near settlement size and impinging the slope would settle frequently near this depth. In-situ respirometry performed on two pelagic juveniles of 41.3 and 37.7 mm SL indicated diel activity, with the fish becoming most active at night, possibly to forage on their principal prey, the krill Euphausia pacifica (Smith and Brown, 1983). Similar respirometry measurements on four benthic adults did not show the same diel fluctuations as the juveniles (Smith and Brown, 1983). Comparison of direct metabolic rate measurements from in situ respirometry (Smith and Brown, 1983) and metabolic

rates inferred from an analysis of enzymatic activities suggested that the population oxygen consumption rate of longspine thornyhead at maintenance metabolism in the depth zone of its greatest abundance could be as high as 285 l O2 m
2 d
1 (Vetter and Lynn, 1997). To service its resting metabolism by these estimates a 200 g individual would have to consume an average of a 10-g meal only 3 or 4 times a year! An individual of 200 g biomass would likely be in the upper third of the size distribution, reproductively mature, and probably near 15 y old. Its resting in-situ oxygen consumption rate would be ca. 2.3 l O2 g
1 wet wt hr
1 (Smith and Brown, 1983). Relative to this maintenance requirement, the evident principal prey of adult longspine thornyhead, the brittle star, Ophiopthalmus normani, would represent a tremendously abundant food resource in the SCB (Smith and Hamiltion, 1983), even if the fish required substantial multiples over the maintenance requirement for its ultimate growth and reproduction. Such minimal food requirement might explain why longspine thornyhead are not as readily or as easily attracted to bait as other species of the SCB community mentioned above. Many deployments of vertical baited hook lines and experimental bait drops in the SCB and in the San Diego Trough (SDT) observed with time lapse and video cameras attracted very little interest from them (Wilson, pers. obser.) in comparison to sablefish, black hagfish, grenadiers (SDT), and the Pacific flatnose (SDT). Regarding longspine thornyhead on the slope of California or in the borderland basins as a paradigm of a food-limited, deep-sea fish population is difficult. One should perhaps consider predation, possibly from deepdiving pinnipeds or benthic/benthopelagic sharks, as a factor limiting its population size. One need barely handle freshly trawled specimens to appreciate the defensive nature of the thorny spines about the head that surely exist to deter predators. Kline (1996) and Cailliet et al. (2001) studied growth rates and longevities of longspine thornyheads in the size range of 104 to 307 mm TL from specimens trawled on the California slope between 100 and 1,400 m depth. Ages estimated from growth-ring (increment) counts of the sagittal otoliths reached 40 y for fish near 300 mm TL. Validation of the growth increments as annual marks was accomplished by radiometric ageing of pooled cores of otoliths of similar mass (size), over a range of sizes. Cores were pooled from otoliths composing one of the native pair of an individual whose other pair member had increment counts similar to others in the pool. Longevities estimated from increment counts plus radiometric ageing of cores largely agreed, suggesting ages of near 40 y for 300 mm TL fish. Although the radiometric technique does not permit direct ageing of individuals, because of the requirement that cores be combined from few to several individuals, the technique appears at least to support growth-ring (increment) periodicities as annual. The von Bertalanffy parameter was estimated at 0.072, inside the range (0.05 to 0.15) biologists generally consider low. The 18 to 20 months that longspine thornyhead spend in the pelagial evidently allow dispersal widely along the coast of western North America, and even colonization of seamounts in the depth range near 500–600 m 500 nautical miles offshore of California (Wilson, 2001) as well in the Gulf of Alaska (Kaufmann and Wilson, 1991). Population genetic studies (Siebenaller, 1978; Stepien et al., 2000) have found but scant evidence of genetic population structure, evidence that could disappear entirely with additional population sampling.

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F I G U R E 13-10. Representative benthic and benthopelagic fishes of the bathyal (deep slope) and abyss.

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Average allozyme heterozygosity (0.047) and its mtDNA equivalent, haplotype diversity (0.96), were not low in this species, indicating a sufficient level of genetic diversity exists to detect population genetic structure if indeed present. Partially sharing the deep-slope with the benthic longspine thornyhead are the grenadiers. These benthopelagic fishes, which have a gas-filled swimbladder conferring neutral buoyancy even under tremendous hydrostatic pressure, are able to “swim freely and habitually near the ocean floor” (Marshall, 1965). Thus, benthopelagic fishes typically have a diet that is a mixture of both benthic and pelagic prey items (Marshall and Merrett, 1977). The Pacific grenadier (fig. 13-10) is likely the most abundant grenadier inhabiting the deep slope below about 900 m off California, particularly off southern California. Nearly 97% of its population biomass caught between 550 and 1,280 m on the California slope occurs below 915 m (Lauth, 1999), averaging about 1.8 mt km
2 of biomass between Pt. Conception and Oregon’s Columbia River region (CPUE data of Lauth, 1999). Its full geographic range extends from off Baja California along the Pacific Rim to northern Japan, where it ranges to ca. 2,500 m (Iwamoto and Stein, 1974). Pacific grenadier is apparently surpassed in abundance deeper than about 1,000 m off Eureka and points north by the giant grenadier, its closest phylogenetic relative in the eastern Pacific Ocean (Morita, 1999; Wilson and Attia, 2003). The deepest capture known to us is from about 3,680 m off the Patton Escarpment (32°29.6’N, 120°26.8’W; SIO82-2), where two individuals were caught on a free-vehicle hook line where the hooks were at ca. 20 m above the bottom. Although other captures of Pacific grenadier over deep bottoms with trawls have been attributed to capture in midwaters (Iwamoto and Stein, 1974), such would not be the case here. The Pacific grenadier also inhabits the borderland basins of southern California (fig. 13-2). Large adults are uncommon in the SCB where chiefly only benthic juveniles, in combination with adults of the smaller smooth grenadier, are seen with submersibles and camera sleds, or captured in trawls. Smooth grenadiers there are roughly three times more abundant than juveniles of Pacific grenadier and together they average about 1–2 individuals 1,000 m
2 (Wilson, pers. obser.), which is less than one-tenth the density of longspine thornyhead. Thus, the abundance of Pacific grenadier at sizes common in SCB (i.e., 200 to 300 mm) appears lower than the average density of similar-sized individuals on the California slope, which is near 2 individuals 1,000 m
2 (Drazen, 2002). In the adjacent SDT and San Clemente Basin large adult grenadiers are frequently caught on vertical hook lines along with sablefish and Pacific flatnose (Wilson, pers. obser.) The earliest developmental stages of the Pacific grenadier are known from but a few specimens collected off Oregon (Stein, 1980). The larvae probably develop rapidly in the water column and then settle to as shallow as 600 m (Drazen et al., 2001) as alevins (Merrett, 1989) at about 80 mm TL (Stein and Pearcy, 1982); planktonic duration is not known. Benthic juveniles forage on the bottom, consuming polychaetes and epibenthic crustaceans (Drazen et al., 2001; Drazen, 2002). With increasing size fish migrate to greater slope depths below 1,000 m (Stein and Pearcy, 1982) and consume progressively larger and more pelagic prey, including fishes (hake), squids, and larger crustaceans, although forging on epibenthic organisms continues. Scavenging is evident among the large adults. Drazen (2002) determined that the slope population of Pacific grenadier likely consumes about 2.7 kg km
2 d
1 of prey,

chiefly as squid, fish, and scavenged materials. Unlike the benthic thornyheads, Pacific grenadier becomes benthopelagic in habitat with increasing size. Also, unlike the thornyheads, Pacific grenadier is readily attracted to bait—a fact exploited in studies of this species. Smith and Hessler (1974) baited it to an in-situ respirometer in the SDT and obtained the first metabolic rate measurement for any deep-sea benthopelagic fish. At 2.4 l O2 g
1 wet wt hr
1 the resting metabolism of the 1.8 kg fish was 1/25 that of a codfish measured at the same temperature. Wilson and Smith (1985) similarly baited Pacific grenadiers to a hyperbaric trap/aquarium system and brought a fish successfully to the surface under hydrostatic pressure near what it had experienced at depth. That fish was subsequently maintained for 41 h in a laboratory cold room on shore and was clearly able to maintain neutral hydrostatic buoyancy under high pressures. Wilson (1982), Matsui et al. (1990), and Andrews et al. (1999) studied the age and growth of Pacific grenadier. Wilson (1982) published data from vertebrae stained with alizarin red, but also studied sagittal otoliths sectioned in the sagittal plane. Matsui et al. (1990) used the break and burn technique to count otolith grow rings, and Andrews et al. (1999) used radiometric ageing of the sagittae in conjunction with counting sagittal growth rings in transverse sections. Even small, seemingly young individuals of 251 mm TL have relatively large sagittae (e.g., 5.5 mm) with as many as 8–10 growth rings (Wilson, pers. obser.). The radiometric ages of Andrews et al. (1999) fall between about 48 and 67 years for the largest fish (ca. 800 mm TL); the von Bertalanffy parameter was 0.041. Radiometric ages essentially agreed with ages estimated from ring counts in the sagittae, although the rings indicated slightly younger ages overall (ca. 38 to 62 y). Unpublished counts (Wilson) from sectioned sagittae agreed with Andrews et al. (1999) for fish up to about 400 mm TL, the lumped average length of fish with 15, 16, or 17 sagittal growth zones, but were lower for the larger fish. Pacific grenadier mature by ca. 580–600 mm TL and are spawning by this size, if not earlier. Based on Andrews et al. (1999), fish this size would be near 30–32 y of age. In the San Diego Trough, females dominate the sex ratio and are larger on average than the males, reaching over 800 mm TL versus approximately 700 mm for males. Ripe and spent ovaries have been seen among fish taken from the San Diego Trough in October, December, and February (Wilson, pers. obser.). Off Oregon, females with ripe ovaries occur in April and September, and those with ripe or spent ovaries in October (Stein and Pearcy, 1982). The giant grenadier (fig. 13-10) is likely the most abundant deep-slope grenadier off California after the Pacific grenadier, especially off northern California. They share a coincident Pacific Rim distribution in approximately the same depth zone, and giant grenadier has been captured in the SCB on vertical hook lines (Wilson, pers. obser. SIO80-3, SIO80-4). However, the species generally ranges shallower on the California slope than the Pacific grenadier as only 77% (compared to 97%) of the population biomass sampled between 550 and 1,280 m occurs deeper than about 915 m. This species greatly dominates trawl catches of grenadiers in northern California and further north into the Bering Sea and along Kamchatka (Novikov, 1970; Lauth, 1999). Albatrossia pectoralis is the binomen often used for the giant grenadier, but the species has variously been referred to the genera (or subgenera) Coryphaenoides, Nematonurus, and Chalinura (Iwamoto and Stein, 1974; Iwamoto and Sazonov, 1988). Adults reach the unusual size of over a meter in length

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and can weigh 7.5 kg (Novikov, 1970; Iwamoto and Stein, 1974); the muscle tissue is flaccid, and the small scales highly deciduous, rendering the fish ungainly in appearance upon capture by trawls. Despite its unusual appearance and probably derived morphological features (Iwamoto and Stein, 1974), phylogenetic studies (Wilson, 1994; Morita, 1999; Wilson and Attia, 2003) have repeatedly shown it to be a species of Coryphaenoides, probably closest to Coryphaenoides acrolepis among the eastern north Pacific species that have been studied. Its derived features, pointed out by Iwamoto and Stein (1974), include the flaccid tissue, poorly ossified skull bones, and a reduced swimbladder. The features are possibly a result of a protracted life history stage in midwater (Novikov, 1970; Iwamoto and Stein, 1974). Drazen et al. (2001) found that giant grenadier over a range of sizes forage in midwater on squids and fishes. Chief among the food items were the bathypelagic squids Octopoteuthis deletron and Vampyroteuthis infernalis, plus assorted stomiids (e.g., Pacific viperfish), bathylagids, alepocephalids, and myctophids. The largest adults appear to adopt a more benthopelagic, scavenging habit. Other authors have reported similar findings (Novikov, 1970). Little is known about its early life history except that spawning/fertilization probably occurs deep, and the larvae are planktonic at relatively shallow depths (e.g.,  200 m). Yolk-sac larvae persist until about 7.1 mm TL. The anal fin is formed on specimens larger than 22.1 mm TL, and by 38.9 mm the alevin stage (Endo et al., 1993) is reached. Recruitment to the benthic habitat might be delayed until individuals reach about 500 mm TL (Novikov, 1970). Off California the smallest giant grenadier obtained with benthic trawls (Lauth, 1999) were 130 mm preanal length (Drazen et al., 2001). By comparison, the smallest Pacific grenadier caught in the same survey were near 20 mm preanal length (175 mm TL), much larger than the estimated settling size on the Oregon slope of about 80 mm TL (Stein and Pearcy, 1982). The age and growth of the giant grenadier were described in a radiometric age validation study, as was the case with the Pacific grenadier (Andrews et al., 1999), where longevity was described as approaching or exceeding 56 years (Burton, 1999). Estimates of age from otoith sections were difficult to determine because of irregular growth and shape of the sagittal otolith. The eastern north Pacific populations of Pacific and giant grenadiers are also not lacking in genetic diversity (i.e., average heterozygosity). Siebenaller (1978) reported an average observed heterozygosity for Pacific grenadier of 0.033 over 25 presumptive loci. Wilson’s (1994) data produced a value of 0.052 over 24 loci for Pacific and 0.034 over 24 loci for giant grenadier, values highly comparable to those determined for 90 species of deep-sea fishes (Creasey and Rogers, 1999).

Life in the Abyssal Habitat The few abyssal fishes inhabiting the eastern north Pacific Ocean tend to bias perceptions of abyssal ecology to that reflected by the well-studied grenadiers. Considering the somewhat richer abyssal ichthyofauna of the north Atlantic Ocean might broaden perceptions, but in the deepest parts of both ocean basins grenadiers dominate the ichthyofauna and consequently are the best-studied fishes. Among the few abyssal (non-grenadier) fishes of the north Atlantic Ocean that are also known in the eastern north Pacific Ocean, two have received study, the flatnose, Antimora rostrata (Antimora

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microlepis is the north Pacific form, fig. 13-10) and the highfin lizard fish (Bathysaurus mollis) (fig. 13-10), the latter inhabiting much deeper regions. In the eastern north Pacific, highfin lizard fish has been taken off Oregon, northern and southern California, and Baja California (Stein and Butler, 1972; Stein, 1985; Sulak et al., 1985; Wilson, pers. obser., SIO85-132) and is generally found between about 1,680 and 4,900 m (Sulak et al., 1985). Off northern California, at least, it occurs with grenadiers, cuskeels, and snailfishes (e.g., Stein, 1985). It is possibly an ecological depth replacement in the Atlantic Ocean for its close congener, Bathysaurus ferox (ca. 860 to 3,460 m). Adults reach between 400 and 600 mm TL, but an individual of 835 mm is reported (Sulak et al., 1985). Lizard fishes are ambush apex predators. The large size of highfin, coupled with its burst-swimming ability (Sulak et al., 1985), indicates its capacity to ambush even large fishes drifting or swimming near the ocean bottom, such as the abyssal grenadier (Coryphaenoides armatus), a known prey (Sulak et al., 1985). For example, in the Charlie-Gibbs Fracture Zone of the north Atlantic Ocean many relatively small (150 to 250 mm TL) abyssal grenadiers were recently observed “hanging” horizontally in the water near the bottom of 4,300 m depth, appearing simply to drift (Wilson, pers. obser.). Highfin lizard fish lie perfectly still, seemingly rigid, on the seafloor in total darkness with pectoral and pelvic fins extended. They can be approached in a submersible with lights on to within two meters without the fish flinching or moving noticeably. The dorso-ventrally flattened head is triangular with the mouth well positioned to open and snatch prey such as abyssal grenadier from the overlying water. A close view of the living fish in its native realm revealed its lateral line to be a very prominent feature, one that must alert the predator to the presence of prey such as abyssal grenadier or nektonic shrimp. As an apparent synchronous hermaphrodite, the highfin lizard fish is monoecious, a possible reproductive adaptation for thinly distributed populations (Sulak et al., 1985). Gonadal maturation appears to be seasonal in Atlantic Bathysaurus ferox, but the pattern of gonadal maturation is not known for the highfin. Relatively large (38–83 mm TL) post-larvae occur in the mesopelagial, suggesting protracted planktonic development as in longspine thornyhead, although highfin might grow rapidly once becoming demersal (Sulak et al., 1985). Sharing the Pacific abyssal habitat with the highfin lizard fish but in far greater abundances are the benthopelagic abyssal grenadier and the more benthic ghostly grenadier, Coryphaenoides leptolepis. Of the two, the abyssal grenadier is the more widespread and possibly the most abundant grenadier in the world’s oceans. If not, it is likely second only to its congener, the rough abyssal grenadier Coryphaenoides yaquinae. Although the earliest capture records of abyssal grenadier are from the Pacific Ocean (H.M.S. Challenger), it has been most studied in the north Atlantic Ocean where it is the most abundant and widespread grenadier of the abyss, especially in the northeastern portion (Merrett, 1992). The abyssal grenadier has long been viewed as different from the other species of Coryphaenoides having first been assigned (Günther, 1887) to a new subgenus Nematonurus that was subsequently recognized as a full genus (Koefoed, 1927). Iwamoto and Stein (1974) returned Nematonurus to subgeneric status within Coryphaenoides although the subgenus is still used in the name as in C. (Nematonurus) armatus. Wilson’s (1994) phylogenetic study suggested that C. armatus was derived from the slope-dwelling Coryphaenoides species as also seemed true for

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the co-occurring abyssal C. leptolepis—the apparent sister species to C. armatus among the species he studied. Morita’s (1999) phylogenetic study of North Pacific species conversely suggested that Coryphaenoides armatus ( Coryphaenoides yaquinae) was the sister group to the other Coryphaenoides species that inhabit the slope, sharing a common ancestor with them. Wilson and Attia (2003) in a further study that included C. leptolepis confirmed that a clade containing the abyssal-dwelling species (C. leptolepis (C. armatus C. yaquinae)) was sister to the slope-dwelling species of Coryphaenoides. Thus, the three abyssal-dwelling grenadier species represent a radiation into the deep sea that parallels that of the other Coryphaenoides species inhabiting the slope. Wilson and Waples (1984) studied the population genetics of the abyssal grenadier between the western north Atlantic and eastern north Pacific oceans. The two populations differed significantly in allele frequencies at two variable loci, LDH-A and PGDH-A, in a suite of morphometric and meristic characters (Wilson and Waples, 1984; Iwamoto and Sazonov, 1988), and in otolith morphology (Wilson, 1985). (A similar difference in otolith morphology was noted between Atlantic and Pacific specimens of the ghostly grenadier.) The evidence suggested that the abyssal grenadier of the north Pacific Ocean comprised a geographic subspecies, Coryphaenoides armatus variabilis Günther (fig. 13-10), apparently confined to a rim distribution at deep-slope and rise depths along the western North American and eastern Asia continents. The rough abyssal grenadier dominates the basin of the north Pacific Ocean where there are no abyssal or ghostly grenadiers present deeper than about 4,300 m (Wilson and Waples, 1983; Endo and Okamura, 1992). In the other ocean basins, the abyssal grenadier occurs at the greatest basin depths, persisting much deeper than the ghostly. Abyssal grenadiers of the Pacific Ocean reach at least 100 cm TL, but neither the average growth rate nor average longevity is known. Sagittal otoliths have what appear to be periodic growth zones similar to those observed in the otoliths of shallow-dwelling fishes (Wilson, 1988). The zones have also been reported for abyssal grenadiers of the Atlantic as well as for many other grenadier species (Swan and Gordon, 2001). Although the zones were countable, there was no assurance that they represented the full growth record. The number of growth zones was low even among large individuals, thus not suggesting great longevities. Marginal increment analysis of the sagittae (Swan and Gordon, 2001) suggested seasonal periodicity in the formation of tertiary (Wilson, 1988) growth zones, but their analysis pertained to relatively small (young) fish and might not hold for full-sized adults (Campana, 2001). Even though there are apparent annual growth zones, counting them would probably remain a problem among large fish. Sagittae of large specimens are dome-shaped and appear to grow allometrically by accretion at the lateral surface with little along the antero-posterior axis (Wilson, 1985). Radiometric ageing might establish longevities for abyssal grenadier, but the small size and low mass of the sagittae, particularly in the Pacific form, would hinder the core method of recent use (Cailliet et al., 2001). The abyssal grenadier appears to be an active fish at its largest sizes both in the Atlantic and in the Pacific oceans where the largest individuals in the eastern North Pacific are females (Stein and Pearcy, 1982; Wilson, 1984). The fish are well-known to scavenge bait and other organic materials that fall to the seafloor (Pearcy and Ambler, 1974; Wilson and Smith, 1984), arriving at experimental bait falls in as few as

8 min after baits hit bottom (Wilson and Smith, 1984). Analyses of arrival times of first individuals at experimental bait falls (Priede and Bagley, 2000) suggested that its average standing abundance in the eastern north Atlantic Ocean (exclusive of the Maderia Abyssal Plain) was about 342 fish km
2. The average density in the eastern north Pacific Ocean is about 463 fish km
2 representing ca. 0.15 mt km
2 (Priede and Bagley, 2000), about one-tenth that of the Pacific grenadier on the slope. Acoustic tagging and tracking studies have shown that after feeding at an experimental bait drop fish depart the area somewhat irrespective of current direction but with a slight bias toward a cross-current track (Priede and Bagley, 2000). Thus, abyssal grenadiers would appear to be active searchers given the reasonable assumption that a fish with an ingested acoustic tag, but not necessarily satiated, will more-or-less resume its before-feeding behavior after tagging. Departing fish eventually swim much farther from the bait than the distance from which they probably had come, as estimated from arrival times, in obvious response to current-borne bait odors. The large ones, at least, apparently do not return to waiting positions (Wilson and Smith, 1984) near where they had been prior to responding to bait odors (Priede et al., 1990). Recent submersible observations at 4,400 m in the Charlie-Gibbs Fracture Zone (north Atlantic Ocean) support the notion that unlike small individuals, large fish do actively swim about (Wilson, pers. obser.). Stomach-content analyses (Pearcy and Ambler, 1974) agreed with reports for other species such as the Pacific grenadier (Pearcy and Ambler, 1974; Drazen et al., 2001) in that as a fish grows, pelagic prey items increase in importance. Fish larger than 500 mm TL fed almost entirely on scavenged pelagic prey, but this appeared to be less so for the ghostly grenadier where only about half the prey items were pelagic (Pearcy and Ambler, 1974). Priede et al. (1990) suggested that the amount of time grenadiers remain near an experimental bait fall after the bait has been consumed (i.e., the staying time) is possibly an inverse indicator of the commonness of naturally-occurring food falls to that bottom habitat, essentially an inverse indicator of the relative amount of overlying oceanic productivity. Video recordings of behavior at experimental bait drops (Wilson and Smith, 1985; Wilson, unpubl. data) set near 3,800 m off the Patton Escarpment show large abyssal grenadiers arriving very quickly, consuming the bait, and then dispersing quickly—all in less than an hour. Thus, relatively few fish accumulate at the bait, producing the shortest staying times observed of ca. 30 min (Wilson, unpubl. data). Near 4,400 m in the eastern north Pacific Ocean, large individuals of both the abyssal and the rough abyssal grenadier are present. The average staying time there is about is 60 min (Priede et al., 1991). In the central north Pacific basin near 5,900 m where only the rough abyssal occurs (Wilson and Waples, 1983), the staying time of 261 min is the greatest seen among the three sites studied in the north Pacific (Priede et al., 1991). The much longer staying time allows for the accumulation of many fish at the bait drop. Thus, beneath the moderate-productivity waters of the eastern north Pacific Ocean where the most food potentially available for scavenging is produced the staying time is the least, so the least number of fish are seen at once. Beneath the low-productivity waters of the central gyre the staying time is the greatest, and many more fish are seen at once. This same pattern of staying time with respect to productive versus unproductive regions of the Atlantic Ocean has been seen for

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abyssal grenadier there (Priede et al., 1991; Priede and Merrett, 1998), as well for other species in the other oceans of the world (Isaacs and Schwartzlose, 1975). Priede et al. (1990) suggested that the behavior of these grenadiers with respect to staying time is governed by optimal foraging pressure, influenced by the amount of food striking the seafloor. In low productivity regions where food striking the seafloor is a relatively rare and unpredictable event, fish remain longer at a site where food previously was found, rather than resume searching anew with the comparatively low chance of an encounter; fish therefore accumulate. Where food striking the seafloor is a relatively frequent, comparatively predictable event, the chance of finding additional food anew from a random search would be greater. Remaining at the present site would have less potential benefit, so the fish disperse quickly after the bait has been consumed and do not accumulate. Bailey and Priede (2002) modeled expected fish arrival and accumulation rates at bait for three alternative foraging strategies—cross-current searching, sit and wait, and passive drifting. Modeled (i.e., predicted) rates were based on empirical estimates of fish densities and were assumed to be in response to odor plumes emanating and spreading out from bait sources (food falls) on the seafloor. None of the models completely described foraging behavior of abyssal grenadiers at bait falls. Observed arrival rates agreed best with those predicted from the cross-current foraging model, and that model accurately described accumulation around large carcasses. Although the sit-and-wait model more accurately predicted peak numbers of fish, numbers that were much lower than predicted from the cross-current model, its predictions did not agree with arrival rates. The passive-drifting model was the least predictive. No in situ estimates of basal metabolism exist for the abyssal grenadier of the Pacific Ocean, but Smith (1978) measured the O2 consumption rate for three specimens in the Atlantic Ocean. The rate for the largest fish (1.2 kg) was 2.7 l O2 g
1 wt wet hr
1, close to that determined for the slope-dwelling Pacific grenadier (2.4 l O2 g
1 wt wet hr
1) of similar size. Analysis of stores of neutral lipids and glycogen indicated that abyssal grenadier in the Atlantic might survive 186 d without feeding. If the average basal metabolism of the Atlantic and Pacific abyssal grenadiers proved nearly the same, there would be little metabolic difference between abyssal and Pacific grenadiers in the Pacific. Thus, invasion of the deeper habitat by the abyssal grenadier (i.e., 3,800 to 4,400 m versus 1,100 m for Pacific grenadier) has not caused a reduction in basal metabolism. Therefore, the decreased food resources in the deeper habitat of the abyssal grenadier must be met by a reduced population biomass (i.e., approximately 1/10 that of Pacific grenadier on the slope). Population biomass of the abyssal grenadier in the eastern north Pacific is clearly food limited, and the same is as likely true for the rough abyssal grenadier at even greater depths, facts supporting Priede et al.’s (1990) hypothesis. Practically nothing is known of the reproductive biology and early life history of abyssal grenadier from any of the world’s oceans. Females with ripe ovaries are rarely seen (Stein and Pearcy, 1982; Stein, 1985) despite extensive collections. No early developmental stages or alevins have been reported for the abyssal grenadier but have been for the ghostly grenadier in which development is pelagic and transformation to the alevin occurs by 15.2 mm head length (HL) (Stein, 1980). Catches from bottom trawls suggest that the youngest juveniles, as in other deep slope fishes, “settle” near the shallow

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end of the depth range (ca. 2,000 m) near 80 mm TL (50 mm TL for ghostly), moving to greater depths with growth (Stein and Pearcy, 1982; Merrett, 1992). However, recent submersible observations made between 2,000 and 3,700 m depth in the Charlie-Gibbs Fracture Zone revealed that such small C. armatus overwhelmingly reside 1 to 2 m above the sediment, rather than directly on it, and were indeed abundant near 2,000 m. That layer of the water column has probably not been well sampled with trawls, accounting for the relatively few fish of that size in collections (e.g., Stein and Pearcy, 1982). The rough abyssal grenadier is the ecological (depth) replacement of the abyssal grenadier deeper than about 4,300 m in the basin of the north Pacific Ocean (Wilson and Waples, 1983; Endo and Okamura, 1992). It ranges across the North Pacific from the continental rise of western North America (Wilson and Waples, 1983) to the rim of the Japan Trench (Endo and Okamura, 1992) and is probably the deepestdwelling grenadier in the world’s oceans with records to 6,450 m along the Japan Trench (Endo and Okamura, 1992). It possibly ranges beyond the Pacific Ocean basin, but no published record of occurrence outside the North Pacific exists except for an H.M.S. Challenger record barely south of the central Pacific equator (Wilson and Waples, 1983). The species is not reported from either the north or south Atlantic, or Indian, ocean basins where the Atlantic form of the abyssal grenadier dominates trawl catches below 2,000 m at temperate latitudes (Wilson, 1984; Middelton and Musick, 1986; Merrett, 1992). Somewhere in the abyssal basin of the western south Pacific Ocean, the rough abyssal grenadier most likely yields the basin habitat to the Atlantic form of abyssal grenadier. Thus, over much of the world, the North Atlantic form occupies the entire depth range that uniquely in the north Pacific is shared between two grenadiers. Perhaps the rough abyssal grenadier will prove to be a species with a Pacific plate distribution (Springer, 1982). If so, one would not expect to find this species in its depth range (ca. 3,800 to  6,000 m) on the Nazca Plate between the east Pacific Rise and the PeruChile Trench. Only the abyssal grenadier has been collected from there (Wilson and Waples, 1983; Iwamoto and Sazonov, 1988), but sampling has apparently been shallower than 4,000 m. Rough abyssal and abyssal grenadiers are closely related genetically (I  0.74, Wilson and Waples, 1983), are very similar morphologically (Iwamoto and Stein, 1974; Endo and Okamura, 1992), and are probably true sister taxa among macrourids (Morita, 1999, Wilson and Attia, 2003). Compared to specimens from the eastern Pacific, rough abyssal grenadier of the central Pacific show significant allelic frequency differences at one genetic locus, significant morphometric differences in interorbital width and upper jaw length, a slightly lower average heterozygosity from 27 loci (0.028 vs. 0.033), and slightly smaller sagittae (Wilson and Waples, 1983; Wilson, 1985). This vast basin-wide population of rough abyssal grenadier might prove not to be genetically homogeneous over its range (e.g., Creasy and Rogers, 1999). As with abyssal grenadier, virtually nothing is known of reproduction and early life history of the rough abyssal grenadier. Between about 3,600 and 3,800 m in the eastern Pacific Ocean off southern California individuals are mostly between about 270 and 460 mm TL. At greater depths (e.g., 4,800 m) but still relatively near the continent, individuals are mostly  700 mm TL. In the central north Pacific basin near 5,900 m, this size segregation is less evident with both small and large individuals occurring together (Wilson, pers. obser.).

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Thus, the ontogeny and early life history of the rough abyssal grenadier differ from that of its slope-dwelling congeners and perhaps even the abyssal grenadier as settlement within a narrow inshore-offshore interval of distance over the slope or rise would no longer be necessary. A different set of life conditions for the central basin population might explain the apparent genetic and morphological differences. Wilson (1988) studied thin-sectioned otoliths of rough abyssal grenadier in the sagittal plane and found ostensible growth zones including evident daily growth increments. As the deepest dwelling grenadier in the Pacific Ocean, it has the smallest otoliths (Wilson, 1985). The finest-scale growth increments, interpreted as daily, were much more closely spaced (2 µm or less) in otoliths of specimens from the central basin than in otoliths of specimens from the eastern north Pacific, where increment spacing was nearly the same as that seen for the abyssal grenadier (Wilson, 1988). Confirmation by others that such growth zones are in fact deposited periodically, even annually, in deep-sea fishes (Andrews et al., 1999; Cailliet et al., 2001; Swan and Gordon, 2001) implies that the central basin fishes are growing more slowly than conspecifics inhabiting shallower depths near the continent—perhaps only half as fast. This disparity in growth would be consistent with Priede et al.’s (1990) observation and explanation of long staying times at bait drops among the rough abyssal grenadiers of the central basin. The relative scarcity of food in the central Pacific basin is reflected both in an evident slowing of growth as seen in otolith increments and in foraging behavior conforming to predictions from optimal foraging theory.

The Future Many aspects of the ecology of deep-sea fishes of the eastern Pacific Ocean remain of general interest. For example, how might species composition vary in numbers or biomass within and between years? Are bathymetric distributions generally stratified by size, sex, and degree of gonadal maturity? What drives ontogenetic changes in diet and feeding times and places? How might competition and predation structure communities or function as limiting factors for population size and species diversity? Where and when does spawning occur among the species of most interest; what are the cues? How much population and genetic exchange takes place among populations in different areas such as among the various borderland basins, latitudinally along the slope, or across the Pacific abyss? Are there seasonal or other types of periodic long migrations? Answering the above questions and probably many others must continue to include development and application of new and advanced technologies. Ultimately, progress and discovery in science, all science, is technology dependent, be it from the advent of SONAR, multiple opening and closing nets (e.g., MOCNESS), thermally-protected cod-ends and pressureinsulated traps, ROVs and AUVs (autonomous underwater vehicles), manned submersibles and accessories, in situ respirometry, in situ acoustic tracking and telemetry, radiometric ageing, molecular genetics (and systematics), or advanced computational methods. Each stand-alone technology eventually reaches a point where little more that is truly new is produced, and much more of the same inevitably results. Integration of advanced technologies raises the chances for progress. For example, increased sampling with MOCNESS, large benthic trawls, sub-

mersibles, and ROVs/AUVs might answer questions regarding bathymetric distribution and vertical stratification by size or sex, but probably not about population or genetic exchange among areas, or periodic migration, unless joined with molecular genetics or acoustic tracking. In the future, sampling and in situ observation in the deep sea should be even more thoughtfully integrated with other methods with the aim of hypothesis testing through experimentation.

Acknowledgments The first author would like to thank the Natural History Museum of Los Angeles County and Christine E. Thacker for access to the resources of the Section of Fishes, as well as Richard F. Feeney, Michael H. Horn, and Jeffrey A. Seigel for comments on a draft of the chapter. Larry G. Allen’s development and final execution of the figures are also appreciated.

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PART I I I

P O P U L ATI O N AN D C O M M U N ITY E C O LO GY

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CHAPTER 14

Feeding Mechanisms and Trophic Interactions M I C HAE L H. H O R N AN D LARA A. F E R RY-G RAHAM

Introduction

Feeding Mechanisms

The composition of the present-day California marine fish fauna is largely a reflection of trophic interactions, as stated by Hobson (see chapter 2). The diversity and complexity of the fauna are at least in part a response to these interactions over evolutionary time scales. As such, many of the feeding behaviors and associated morphologies of fishes in California waters have been shaped and honed in response to selective pressures specifically related to feeding performance. Whatever paths of evolution have resulted in this rich and varied fish fauna, the array of extant species represents much of the amazing dietary diversity seen among ocean-dwelling species in general. Fishes encounter prey that varies enormously in degree of mobility, habitat location, and in size, structure, digestibility, and nutritional content. Not surprisingly, fishes including those living in the sea off California are generally opportunistic and exhibit a wide variety of ways to capture and process food to meet their energy and nutritional requirements. In this chapter, we first organize the subject of food and feeding in fishes into three parts and variously draw our examples from members of the California marine fish fauna. In the first part, we discuss factors that determine diet including body shape and feeding behavior, identify types of food capture, and describe several kinds of feeding mechanisms. Second, we recognize some of the major types of food items consumed by representative taxa of the California fauna and associate these taxa with standard trophic level designations (i.e., herbivores, carnivores, and omnivores). Third, we use generalized profiles of trophic relationships to portray the main feeding interactions among fishes occupying: 1) bay-estuarine, 2) inner and outer shelf, 3) rocky intertidal, 4) rocky reef and kelp bed, 5) epipelagic, and 6) deep midwater habitats. The chapter broadly integrates with the treatments of predation (see chapter 16) and competition (see chapter 17) in this unit on population and community ecology and variously with all chapters (see chapters 5–13) in the unit on habitats and associated fishes.

Overview Body shape is clearly an important part of the mechanism for bringing the predator close enough to the prey or food item for it to then be consumed. Fishes have evolved streamlined shapes that facilitate sustained swimming for chasing down prey, robust shapes for burst behaviors that take prey by surprise, and cryptic shapes for evading detection by the prey until it is too late. Once the prey is within range, specific morphologies for capturing or otherwise obtaining and processing the item come into play. These structures might include features of the jaws (such as the number, size, and shape of teeth, and jaw length and width), neurocranium and suspensorium (to facilitate rotation and expansion of the head), and gill arches (such as the addition of teeth, epibranchial organs, or pharyngeal mills). These morphologies should combine with physiological features that enhance food capture abilities, such as highly developed systems for taking advantage of visual, olfactory, electrical, and auditory signals, as well as other cues related to the detection of a pressure wave propagated through water. The specific behaviors that a fish uses to locate, capture, and process a food item make up another category of traits that have been shaped over evolutionary time in much the same way as the physical features of the fish. Behavior and morphology, then, can be thought of together as creating the feeding mechanism. The mechanism, or suite of mechanisms, that any given individual possesses will set the boundaries on what food items can be taken from the environment. The types of interactions that shaped the system in the past continue to occur in the present. An individual fish is constantly responding in real time to an onslaught of interference that prevents it from simply eating all of the items of which it is capable. These interactions can occur between individuals and the environment and may include such processes as weather, currents, and tides, as well as physical features such as substratum type and topography, salinity, and temperature. Any or all of these processes or features may restrict where an individual finds itself on short (minutes) or long (days to months) time scales.

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F I G U R E 14-1 Possible scenario for how diet is determined. Implied in the Community Ecology Box are abiotic effects that impact interactions among species (after Ferry-Graham et al. (2004)).

FIGURE 14-2 Schematic representing the set of factors that ultimately determine what an organism can eat and where they act in the process of foraging: encounter with prey, detection of the prey of the predator, recognition of the prey as something to eat, the decision to attack the prey, and, ultimately, the ability then to capture the prey successfully. Note that after each filter fewer types of prey remain available to the predator as a result of the exclusion of certain prey types. Prey types might be excluded because they are not encountered as a result of the part of the habitat used by the predator or the ecological interactions that restrict where the predator forages. Prey may not be detected or recognized because of sensory ability. Prey also may not be recognized as a result of behavioral learning (or a lack of it). The predator may decide not to attack the prey because of ecological interactions external to the prey item, such as predation risk, or because of behavioral cues that cause the predator to choose not to attack, such as they prey is too far away to be captured successfully. The ability to capture the prey successfully depends upon morphological, physiological, or behavioral capabilities. (After Ferry-Graham et al. (2004), and A. Cook, unpublished).

Interactions also will occur with other individuals of the same or different species in the form of predatory encounters and competition for food resources. These limitations force the fish to make choices about when and where to forage, what to try to eat and what to avoid, and, therefore, will restrict the diet to a subset of the available items.

Factors that Determine Diet As ecologists, we tend to think of resource use, and feeding in general, as being shaped by the interactions of a species or an individual with both the environment and other community members. Clearly, such extrinsic interactions will partially determine which available prey items will ultimately become part of the diet. Nevertheless, the inherent abilities of the organism to capture and process prey also will affect diet and are determined by intrinsic factors such as organismal morphology or behavior. These extrinsic and intrinsic factors will act and interact to shape the diet of any given individual within an ecosystem (fig. 14-1). Some species have broad or generalized diets, containing a wide

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variety of prey items. Others have narrow diets composed of one or a few kinds of items, and are often said to be specialized. Species with broad diets may be composed of many generalized individuals each with broad diets, or of many specialized individuals each consuming different prey resources from the environment. Although each individual may consume a narrow range of prey, the population as a whole may appear to have a broad diet. The factors that determine diet in an individual or a species may be viewed as a series of filters that eliminates many potential prey and ultimately determines what an organism can and will eat (fig. 14-2). Organisms must first encounter a potential prey item (fig. 14-2). Although this action ostensibly involves being in the right place at the right time, that place is determined in part by the extrinsic interactions experienced by the fish. For example, dispersal and recruitment will determine the environment in which a fish lives and forages and, therefore, will ultimately affect what items are available as potential prey for an individual or species. Both dispersal and recruitment will be shaped in part by environmental factors, such as currents and tides (see chapter 15). Similarly, avoiding competition

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(see chapter 17) will affect which prey are taken from those that are available. Dietary overlap between species or individuals is one mechanism thought to lead to competition, particularly when resources are limiting (Hardin, 1960; Alevizon, 1975; Hixon, 1980; Schmitt and Coyer, 1983; Schmitt and Holbrook, 1986; Holbrook and Schmitt, 1992). Competition may be reduced by the active avoidance of a particular prey by a species. The above extrinsic forces acting on the fish, however, operate together with the intrinsic abilities of the fish. For example, a fish’s swimming ability will determine whether it forages near shore or in open water. The foraging range of the fish will, in turn, affect which prey are encountered and can potentially be included in the diet. Similarly, the abilities of the fish to swim quickly may allow it to exclude other potential predators from a prey item (see chapter 17). These intrinsic features are further shaped by interactions with both the environment and other individuals and species over evolutionary time (Abrams, 1983; Robinson and Wilson, 1994); thus, extrinsic forces continue to play a large role in shaping diet. The intrinsic abilities of the fish ultimately, however, will determine where it can forage successfully, which will differ among individuals and species. The range of these intrinsic features, of course, is enormous among fishes, and extremes of body shape and travel distance can illustrate this point. For example, the streamlined and muscular bluefin tuna (Thunnus thynnus) swims continuously and migrates along coastlines of the northeastern Pacific and across the north Pacific basin participating in various food chains along the way (Bayliff, 2001). In contrast, the blunt and elongate monkeyface prickleback (Cebidichthys violaceus) swims only a few minutes per day, in a series of short forays, and even then within an area of only a few square meters of the rocky intertidal habitat (Ralston and Horn, 1986). The second filter affecting diet is the fish’s ability to detect the prey using visual, auditory, olfactory, or other sensory abilities (fig. 14-2). This filter, in large part, is determined by the intrinsic abilities of the fish. Prey detection, for example, in the blue shark (Prionace glauca) and albacore (Thunnus alalunga), two epipelagic fishes occurring in the northeastern Pacific with overlapping diets (see epipelagic trophic relationships, below), differs because the shark relies more on olfaction and electroreception than the tuna, which primarily uses vision (see Helfman et al., 1997). The predator must then recognize the prey as something good to eat, which may depend upon acquired knowledge or learning. Herbivorous fishes, for example, avoid eating unpalatable seaweeds, which probably involves a combination of evolved recognition and proximal learning, the latter especially if the seaweed community changes seasonally, or if a fish species such as the zebraperch (Hermosilla azurea) expands its range and encounters a different mix of potential algal dietary items (Sturm and Horn, 1998, 2001). This recognition must be followed by a decision to attack the prey, which may be based upon an assessment of the prey’s energy value or handling costs. The decision to attack also may be mediated by extrinsic factors such as risk to the predator of being attacked by a larger predator (the focus of chapter 16). Those who have studied and tried to observe the cryptic fishes of rocky intertidal habitats such as sculpins (Cottidae) and kelpfishes (Clinidae) know that they seldom appear or venture far from their protective base. Ultimately, the predator then must possess the ability to capture the prey successfully. This ability will depend on the type of capture method employed, the suite of morphological

features on hand for performing that type of prey capture, and the behavioral traits necessary to perform the action (discussed below). If a foraging fish is able to perform more than one type of prey capture behavior, then the fish must choose which behavior to employ in any given situation and in such a situation risks choosing inappropriately and missing its meal. Appropriate examples here are generalized feeders such as the topsmelt (Atherinops affinis), a silverside that feeds either on zooplankton or benthic prey in kelp beds or primarily on macroalgae and detritus in bays and estuaries (see Trophic Interactions below) or senorita (Oxyjulis californica), a wrasse that either picks moving prey from the water column or removes attached or encrusting animals from surfaces (see rocky reef and kelp bed trophic relationships, below) The filters described in fig. 14-2, however, are not simply passive sieves; rather, they act and interact with one another creating a probability distribution at each juncture that determines which prey will remain at the next decision-making step (Ferry-Graham et al., 2004). The probability that a predator routinely encounters a certain prey item can affect the probability, for example, that the same predator will then recognize that prey item as something good to eat. Working in the opposite direction in fig. 14-2, the probability of a successful capture given the morphology of the predator may influence the likelihood that the predator decides to capture the prey item. Thus, fig. 14-2 represents a simplified series of steps that lie between a predator and its prey. Such filters, nevertheless, represent criteria that distinguish among species and separate their diets. Potential prey may be the same for all species, but the prey that an assemblage or a guild of species encounters, however, will differ if the search behaviors of assemblage members are different. Prey detection may then depend, for example, upon the differing neurological abilities of the associated species, as might prey recognition. The decision to attack will depend at least in part upon the predator’s ability to assess features of the prey and then to evaluate those features, effectively weighing them against some scale established in its evolutionary history or learned in its own lifetime. The decisions that are made and the ability to make those decisions can further separate species and their diets (Ferry-Graham et al., 2004). Ultimately, successful capturing and processing of any given item depend upon a suite of interacting factors that determine the abilities of the organism as distinct from its external influences (Ferry-Graham et al., 2004).

Types of Prey Capture Several kinds of prey capture are employed routinely by fishes. These foraging modes include suspension and filter feeding, grazing and picking, active predation, and scavenging. Suspension and filter feeding encompasses an array of actions whereby small particles or organisms are strained or otherwise separated from the surrounding water using a porous structure, usually the gills and associated elements (fig. 14-3; Rubenstein and Koehl, 1977). Water may enter the fish’s mouth and pass over the gills via one or both of two processes (Sanderson and Wassersug, 1993): 1) ram, where the fish moves through the water using forward locomotion thereby allowing large portions of water to enter the mouth, or 2) suction, where the water is drawn into the mouth through the expansive actions of the fish’s head. Fish species that use suspension or filter feeding tend to obtain their energy near the base of the food

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FIGURE 14-3 A head-on view of a generalized suspension feeding fish with the gill arches evident. The approximate locations of the bones that compose the branchial arches that are visible in this view are indicated: the glossohyal, the basibranchial, and hypobranchial 1, ceratobranchial 1, and epibranchial 1 on arch 1. See also figure 14-5. Drawing modified after Sanderson and Wassersug (1990) and Sanderson and Cheer (1993), with permission of S. L. Sanderson.

web and to reach either large population sizes, as in Pacific herring (Clupea pallasi), or large body sizes, as in the basking shark, Cetorhinus maximus (Sanderson and Wassersug, 1993). Pickers and grazers tend to forage on attached prey items, although technically speaking, grazing may include any mode of feeding that facilitates herbivory, or general planktivory. Thus, open-water filter-feeders, such as northern anchovy (Engraulis mordax), that capture phytoplankton and (mainly) zooplankton may be considered grazers. Blacksmith (Chromis punctipinnis), which pick zooplankton from the water column (Bray and Ebeling, 1975), also could qualify as grazers in this broad sense. Grazers, however, are more often thought of as those species that bite, clip, or scrape from larger plant or algal material although herbivores are sometimes divided into species that graze, if sediment is ingested in the scraping or sucking process, or browse, if they bite or tear relatively upright macroalgae and rarely ingest any inorganic material (Horn, 1989). Based on this distinction for herbivores in California waters, striped mullet (Mugil cephalus) would be classified as a grazer, monkeyface prickleback as a browser, and zebraperch as a combination grazer/browser (Horn, 1989; Sturm and Horn, 1998). The senorita picks bryozoans off the surface of giant kelp (Bray and Ebeling, 1975) with behaviors similar to that of a grazing herbivore and thus can included in the picker and grazer category. Picking also may be used to describe the behaviors used by fish to take small items that rest on but are not attached to the substratum. These small prey items remain largely stationary relative to the movements of the predator. Fish species that winnow prey also may be included in this category in the sense that they are selecting small prey by extracting them from a larger collection of items. The black perch (Embiotoca jacksoni), for example, scoops up large amounts of algal turf in its mouth and then uses repeated cyclic actions of the oral and pharyngeal jaws to separate nutritive from non-nutritive items, the latter of which are ejected from the mouth (Drucker and Jensen, 1991). Like suspension and filter feeders, pickers and grazers tend to feed low in the trophic structure, either as herbivores or primary carnivores.

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Active predation typically encompasses the behaviors used to capture mobile prey items ranging from shelled invertebrates to other fishes. Predatory fishes tend to use one of several modes to locate prey and approach close enough to initiate prey capture. These modes (with examples) include: pursuit/ chase (shortfin mako, Isurus oxyrinchus), group hunting (bluefin tuna), lurking (Pacific barracuda, Sphyraena argentea ), lie-in-wait (angel shark, Squatina californica), disruptive coloration with slow approach (striped bass, Morone saxatilis), and luring prey (Pacific dreamer, Oneirodes acanthias). Once prey is selected, the remainder of the predatory event can be divided into two components (Cook, 1996): 1) the attack (which begins when the predator accelerates toward the prey and is linked intimately to the locomotor abilities of the predator) and 2) the strike (which is the part of the event that begins with the opening of the mouth and ends when the mouth closes) this part is tied more closely to the features of the head and jaws as related to prey capture. The strike typically consists of one of three methods of prey capture or a combination of these methods (Liem, 1980): 1) ram, where the predator swims to overtake the prey; 2) suction, as described above; and 3) manipulation, such as biting large pieces of flesh from a prey item. Predatory fishes that use these behaviors range from the small, intertidal mosshead sculpin, Clinocottus globiceps (Yoshiyama et al., 1996a,b) to the large, epipelagic white shark, Carcharodon carcharias (Tricas and McCosker, 1984) and occupy virtually all habitats including the deep sea (Gartner et al., 1997). As predators, these fishes tend to occupy the higher trophic levels in a food web. Similarly, even though their prey is no longer mobile, scavengers may use the same modes of prey capture (i.e., combinations of ram, suction, and manipulation). Scavengers occur at almost all ocean depths, from white croaker (Genyonemus lineatus) in the surf-zone (Stephens et al., 1957) to rattails (Macrouridae) on the deep-sea floor (Pearcy and Ambler, 1974; Gartner et al., 1997; chapter 13).

Feeding Mechanics Years of study have led to the general categories of prey capture and processing behavior briefly summarized in the previous section. These invaluable findings result from the careful description of how species capture prey; the quantification of literally dozens of variables has told us how features of the head and jaw move relative to one another on the predator and how the predator moves relative to the prey (e.g., Alexander, 1967; Alexander, 1970; Anker, 1978a,b; Liem, 1978; Liem, 1979). The modes of feeding by fishes as defined by their mechanics can be divided roughly into two categories: 1) those that rely on the activity of the oral jaws, such as suction feeding, ram feeding, and biting, and 2) those that rely on features of the pharyngeal jaws and other organs derived from the gill arches, such as suspension feeding and prey processing with these jaws. B ITI NG

Although any given fish generally can use ram, suction, or biting for prey capture to some extent, species that rely primarily on biting as a means of capturing prey are thought to possess functional morphological features that enhance that mode. Biting is best achieved with forceful closure of the jaw elements that facilitates removal of an item from a larger part or

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F I G U R E 14-4 A highly generalized teleost skull with many of the superficial elements eliminated for clarity, such as details of

the neurocranium and the orbital bones. Aspects of the upper (premaxilla and maxilla) and lower jaw (dentary and articular), suspensorium, and opercular series (opercle, sub-, pre-, and interopercle) are indicated. In A, generalized fish lower jaw with the opening (top) and closing (bottom) lever arms indicated. The jaw rotates about the fulcrum in response to an input force provided by the muscular actions drawn (force may be transferred by ligamentous connections). The direction of rotation is indicated by the arrow. The output force, used by the organism to obtain the prey, will be proportional to the ratio of the in-lever length to the out-lever length. Thus, as seen in B, a shorter out-lever, and relatively longer in-lever, will be better for producing the higher jaw closing forces useful for biting (top). A longer out-lever will be better for faster movements (bottom). Skull modified after Gregory (1933). Lower jaw drawings modified after Richard and Wainwright (1995), with permission of P. C. Wainwright.

from the surface to which it is attached. A number of seemingly reliable morphological correlates have been observed in biting predators. Biting and other manipulative modes of prey capture are often seen in predators possessing enlarged or hypertrophied jaw bones and musculature, which have been shown to enhance force production (Turingan and Wainwright, 1993; Turingan et al., 1995; De Visser and Barel, 1996). Several studies, however, suggest that there is a trade-off in performance of feeding by suction when taxa are modified to enhance biting. For example, the structure of vertebrate musculoskleletal systems generally is thought to be constrained such that force production and speed of contraction cannot be maximized simultaneously. Architectural changes that provide for increased mechanical advantage during jaw closure come at the cost of jaw closing speed (Barel, 1983; Westneat, 1994). Also, morphological arrangements that facilitate biting may even decrease the capacity for head expansion and subsequent suction feeding ability (De Visser and Barel, 1996; Bouton et al., 1999). The traits associated with biting or suction feeding have been well studied, and, because these traits tend to be mutually exclusive, reasonable success has been

achieved in predicting the primary mode of prey capture that will be used by a particular species and in a given situation. We know, for example, that more force is produced by a muscle with a larger cross-sectional area relative to a muscle with a smaller cross-sectional area. A large muscle mass, however, is difficult to move quickly, and long, slender muscles are better for producing rapid movements (Wainwright et al., 1976). A long muscle also can move the element to which it is attached over a larger angle than can a short muscle, thus producing larger movements (Wainwright et al., 1976). By the same token, longer bony elements also tend to be more often associated with speed rather than force (fig. 14-4). Thus, it follows that short, robust jaws are useful for producing force and eating hard prey. S UCTION AN D RAM F E E DI NG

Fish that are feeding on unattached prey also have to contend with the aquatic medium itself, which is dense and viscous relative to air. These characteristics of water pose a problem for aquatic predators whether they feed on tiny suspended

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particles or large active prey although the magnitude of the problem will vary with the size of the prey and the drag forces acting on the prey. As a fish moves through the water to capture prey, it will generate a bow wake that pushes the prey away unless the pursuing fish somehow compensates for its own forward locomotion. A feeding fish can either expand both the oral and opercular cavities, effectively creating a tube with openings at both ends that moves through the water with little resistance (a pure ram behavior), or some suction must be generated. Suction may be generated to draw the prey into the mouth, referred to as inertial suction, or may be used only to compensate for the bow wake, called compensatory suction (van Damme and Aerts, 1997). Suction is a common solution to the problem of dealing with the dense and viscous medium; in fact, nearly all fish species are thought to produce some suction. This reliance on suction is regarded as a major evolutionary constraint on the mechanics of fish feeding, and may well have led to the similarities in prey capture behavior that are seen across widely divergent aquatic taxa (Lauder and Pendergast, 1992). Effective suction feeding depends primarily upon the ability to expand the head and draw water in from the surrounding area. The head is first compressed, forcing out any water inside of the oral cavity. The cavity is then rapidly expanded, creating a region of reduced pressure inside the mouth relative to the ambient pressure in the surrounding medium. Water flows into the region of reduced pressure through the open mouth. In the case of inertial suction, the prey item is trapped in this flow of water and therefore drawn into the predator’s mouth. More rapid or larger expansion of the oral cavity helps to produce relatively more suction for prey capture (Liem, 1980). Then, of course, the mouth must close on or around the prey item in a timely manner to prevent the prey’s escape. Researchers have focused on only a few variables as predictors of whether a fish will rely primarily upon ram or suction to capture active prey. These predictors include morphological variables, such as oral cavity volume and mouth size, and behavioral variables, such as strike distance and velocity. Efficient suction feeders hypothetically should have smaller mouths, as this trait will tend to increase the velocity of water rushing into the mouth (Norton, 1991). Suction, however, is quickly dissipated and is not effective over large distances, so that suction-feeding fish are thought to strike very close to their intended prey (Cook, 1996). Arguably, then, suction feeding may be more useful in capturing stationary or less mobile prey (Norton, 1991; Norton, 1995). Correlations between mouth size and predator-prey distance seem to hold in the sculpin species in which such relationships have been tested. For example, small-mouthed species such as mosshead sculpin (Clinocottus globiceps) tend to have small predator-prey distances and lower attack velocities (Norton, 1991; Cook, 1996) and reduced success on elusive prey (prey that can escape via locomotion) as compared to larger-mouthed species such as smoothhead sculpin, Artedius lateralis (Norton, 1991). The smaller-mouthed species are assumed to produce more suction than the larger-mouthed species to capture the same prey, but this assumption has not been demonstrated. When offered multiple prey types, however, another scorpaeniform fish, the kelp greenling (Hexagrammos decagrammus), increases attack velocities and predator-prey distance in response to more elusive prey, behavioral changes thought to be associated with ram feeding (Nemeth, 1997a). More elusive prey also elicit greater sub-ambient pressure peaks in the oral cavity, indicating greater expansion of the head and presumably increased

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water velocity entering the oral cavity (i.e., greater suction produced in response to elusive prey (Nemeth, 1997b)). Larger intra-oral pressure changes were observed only in response to clinging prey that could grasp the substratum. In contrast, truly non-elusive prey elicited much smaller changes in intraoral pressure (Nemeth, 1997b), suggesting that the use of suction is not reserved categorically for less mobile prey. In terms of predicting whether predators are primarily ram or suction feeders, the accuracy of morphological indicators such as mouth size remains uncertain. Strictly speaking, if all other factors are held constant (e.g., rate of head expansion, amount of expansion behind the mouth), flow velocities should be higher through a smaller rather than a larger mouth opening. Making such a comparison, however, is challenging because of the difficulty of finding two fish species in which all other factors are the same and only mouth size changes. Recent findings clearly show that individual behavior will affect how the prey are captured, and species that appear to be better suction feeders may not actually use more suction than their counterparts when capturing the same prey (Wainwright et al., 2001). Thus, predicting whether predators will use ram or suction without actually measuring the amount of suction produced (i.e., through intra-oral pressure measurements) has become a difficult task. S US P E N S ION F E E DI NG

In the case of filter or suspension feeding, the structures within the fish head, such as the gill arches (fig. 14-3), frequently are assumed to be used to sieve items from the water (Rubenstein and Koehl, 1977). In fishes, sieving is typically facilitated by one or two rows of gill rakers that are present on each of the five gill arches (Sanderson and Wassersug, 1993). Particles that cannot pass through the pores of the sieve are trapped and ingested. Some fish may even be able to adjust the position of the arches to alter the pore size of the sieve (Hoogenboezem et al., 1990; Hoogenboezem et al., 1991). Sieving, however, is only one mechanism of particle extraction. Particles also may be trapped on the gill elements through direct interception, inertial impaction, or gravitational deposition (Rubenstein and Koehl, 1977). The distinction between these three methods depends primarily on the size of the particles and secondarily on the velocity of the flow around the gill elements. Very small particles that are essentially without mass will be captured by a raker by direct interception if the particle passes close enough to that raker (less than one particle radius). If the particle is farther away from the raker, it will continue past the raker and not be captured. The paths of larger particles tend to follow the flow streamlines entering the mouth. If the particles are restricted to these streamlines, they will miss the rakers entirely. When fluid passes a raker, however, it tends to be diverted and accelerated. Because of their own inertia, larger particles will deviate from the streamlines in this region of accelerated flow and also will impact a raker if they pass within one particle radius. The intensity of inertial impaction will increase with increasing velocity, as well as with increasing raker diameter. Relatively large particles tend to sink as a result of gravity. If these large particles fall within one radius of a raker, they will be deposited. Gravitational deposition will increase with increasing particle size but reduced with increasing flow velocity. The gill arches, however, may not be the only feature important for prey-trapping techniques. Several microphagous fishes possess epibranchial organs, a pair of diverticula that

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F I G U R E 14-5 Generalized teleostean

gill arches with details of the pharyngeal jaws indicated. Like some filter-feeding mechanisms, the pharyngeal jaws represent a series of modifications to the gill arches. The lower pharyngeal jaw is actually the fifth, or most posterior, ceratobranchial. The upper pharyngeal jaw comprises several pharyngobranchials. The size and shape of the tooth plates on these elements vary and are presumed to correlate with the types of prey processed by the jaws. A represents the dorsal surface of the lower pharyngeal jaw of a species that eats primarily hard prey, and always uses its pharyngeal jaws in a crushing pattern regardless of prey type in the lab (see Lauder, 1983). B represents that of a species that uses a crushing behavior only when hard prey are consumed. C represents that of a species that cannot crush hard prey. Details of the toothed surfaces of the lower pharyngeal jaws are shown on the right side of the jaw only. Gill apparatus modified after Collette and Russo (1985) and Cailliet et al. (1986). Lower pharyngeal jaw drawings modified after Lauder (1983) with permission of G. V. Lauder.

project from the pharynx above the esophagus. The gill rakers direct water flow towards these organs where food is trapped and formed into a bolus that then can be swallowed. Epibranchial organs are found in the Clupeiformes, Cypriniformes, Salmoniformes, Gonorynchiformes, and Osteoglossiformes (Sanderson and Wassersug, 1993). This list means that, in California marine waters, northern anchovy, Pacific sardine (Sardinops sagax) , Pacific herring, and the species of Pacific salmon (Oncorhynchus spp.) possess an epibranchial organ. Stromateoid fishes, including Pacific pompano (Peprilus simillimus), which occurs in California waters, also are characterized by a type of epibranchial organ, which appears to be a specialization associated with macerating the jellyfishes and other gelatinous zooplankton that form a major part of the diet of many of the species (Haedrich, 1967; Horn, 1984). Sanderson et al. (1991) used endoscopy and flow velocity probes to visualize the flow patterns inside the head of feeding Sacramento blackfish (Orthodon microlepidotus), a freshwater species, and revealed that water does not flow between the gill arch structures. Rather, water is directed to the mucus-covered roof of the oral cavity. Only through the quantification of the flow regime inside the actively feeding blackfish head was this novel technique for suspension feeding detected. In the Nile tilapia (Oreochromis niloticus), another freshwater species, strands of mucus hanging from oral structures are used to trap tiny particles such as bacteria in a technique called aerosol filtration (Sanderson et al., 1996). Whether any California marine fishes use this mechanism is unknown.

P R EY P R O C E S S I NG BY P HARYNG EAL AN D ORAL JAWS

Soft prey may be swallowed as soon as they are captured; however, hard prey, such as shelled invertebrates, often require additional physical processing. This further breakdown is achieved in many species of bony fishes by sequences of repeated crushing and shearing actions performed by the pharyngeal jaws (fig. 14-5). In truly durophagous species, the pharyngeal jaws and their associated musculature are extremely hypertrophied to enhance force generation or crushing ability, much like the biting predators described earlier in this section. Two California marine species, the pile perch (Racochilus vacca), which feeds on molluscs, crabs, and sand dollars (Limbaugh, 1955; Quast, 1968), and the California sheephead (Semicossyphus pulcher), which feeds on sea urchins, other echinoderms, and other hard-shelled invertebrates (Limbaugh, 1955; Cowan, 1986), both use their massive pharyngeal jaws to crush the shells of their prey (Brett, 1979; Hobson and Chess, 2001). The hypertrophy of these jaws and their associated musculature is evolutionarily convergent across many families of fishes worldwide. Representative species can be found within the wrasses (Labridae, Wainwright, 1988), grunts (Haemulidae, Wainwright, 1989), croakers and drums (Sciaenidae, Grubich, 2000), jacks (Carangidae), and freshwater sunfishes (Centrarchidae, Wainwright et al., 1991). Extreme morphological modifications such as hypertrophied pharyngeal jaws are thought to have led to dietary specialization on particular prey types that cannot be eaten by unmodified fishes in the

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same habitat (Wainwright, 1988; Meyer, 1989; Wainwright, 1991). This limitation may be explain why such changes have evolved repeatedly in different fish families and in a myriad of habitats; such specialization may pose a distinct advantage when selection pressures lead to partitioning of resources within a community (Lauder, 1983). Some species of fishes have well-developed oral jaws that also are used for crushing their prey. Oral jaw processing is most well-studied in the tropical pufferfishes (Tetraodontidae, Turingan and Wainwright, 1993; Ralston and Wainwright, 1997), butterflyfishes (Chaetodontidae, Harmelin-Vivien and Bouchon-Navarro, 1983; Motta, 1989; Sano, 1989; Cox, 1994), and parrotfishes (Scaridae, Gobalet, 1989; Bellwood and Choat, 1990; Alfaro and Westneat, 1999). These species take prey from coral reefs, often taking the coral itself, and thus require the ability to break down the food mechanically before it is transported into the gut. The California sheephead, among fish species in California waters, possesses well-developed oral jaws that are involved along with the pharyngeal jaws in crushing hard-shelled prey such as sea urchins (L. Ferry-Graham, pers. obs.). A number of chondrichthyans, such as the spotted ratfish, Hydrolagus colliei (Allen, 1982), bat ray Myliobatis californica (Karl and Obrebski, 1976), and horn shark Heterodontus francisci (Edmonds, 1999) consume hard-shelled invertebrates and possess either tooth plates or molariform teeth for processing such prey. The same performance trade-offs exist for oral jaw processors as for pharyngeal jaw processors and biting predators, and potentially the same advantages are offered in the form of dietary specialization relative to other community members.

Trophic Categories The foregoing discussion of feeding mechanisms in fishes with frequent examples drawn from the California marine fauna provides the background for the second and third parts of this chapter. The diversification of ways in which fishes acquire and process food provides insight concerning the trophic levels that different fish species are expected to occupy in California waters. In turn, these two kinds of information lead to the general formulations of trophic relationships found among fish species in different marine habitats in California.

Herbivores Fish species that consume phytoplankton, macroalgae (seaweeds), or seagrasses as a major part of the diet are rare in California waters as they are in all temperate zones in the world’s oceans (Quast, 1968; Choat, 1982; Gaines and Lubchenco, 1982; Horn, 1989; Horn and Ojeda, 1999). As seen in the trophic relationships depicted in the next section, fish species with a majority of the diet comprising primary producers are found only in bay-estuarine, rocky intertidal, and rocky reef/kelp bed habitats. Fewer than 10% of the species in the assemblages occupying these habitats qualify as herbivores (Horn, 1989). In bays and estuaries, striped mullet and topsmelt can be considered as herbivores (Horn and Allen, 1985). Rocky intertidal habitats contain two herbivorous fish species in the monkeyface prickleback and rock prickleback, Xiphister mucosus (Barton, 1982; Horn et al., 1982; Horn and Ojeda, 1999), but other species including bald sculpin (Clinocottus recalvus), smoothhead sculpin, and reef perch (Micrometrus

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aurora) eat considerable amounts of algae (see chapter 8). In rocky reef and kelp bed habitats, the three most prominent consumers of macroalgae are halfmoon (Medialuna californiensis), opaleye (Girella nigricans), and zebraperch (Quast, 1968; chapter 9), with blue rockfish (Sebastes mystinus) also eating some macroalgae on a seasonal basis (Hallacher and Roberts, 1985). The reasons for the rarity of herbivorous fishes in temperate waters despite the often high standing stocks of macroalgae remain poorly known, but possible causes have been proposed (Choat, 1982; Gaines and Lubchenco, 1982; Horn, 1989; Harmelin-Vivien, 2002; Ferreira et al., 2004). Most likely among these possible explanations is that foodprocessing rates are more limited at the relatively low temperatures of the temperate and polar zones, which may impart the need for more energy-rich (i.e., animal) food sources in these higher latitudinal zones than in tropical waters (Harmelin-Vivien, 2002). Filter-feeding of phytoplankton and grazing and browsing on macroalgae represent the main feeding modes of herbivorous fishes in California marine habitats.

Detritivores The degree that detritus contributes significantly to the sources of carbon remains poorly understood for most food webs involving fishes in California waters. Detritus perhaps plays its most prominent role as a carbon source in bay-estuarine habitats with their diverse array of primary producers, either in the water in the form of seagrass, phytoplankton, and macroalgae, or in the adjacent salt marshes in the form of marsh grass or other wetland vegetation. Striped mullet and topsmelt (Horn and Allen, 1985; Kwak and Zedler, 1997) probably are two of the most important detritivores in California bays and estuaries, but both species also consume microalgae and macroalgae, which confounds their role as consumers of detritus. The main feeding mode used by these two species for consuming detritus likely is suction feeding on the surface of soft-bottom bay-estuarine habitats. Detritus also contributes to the carbon source of fishes of inner and outer shelf and rocky intertidal habitats but indirectly through invertebrate detritivores.

Carnivores The great majority of fish species in California marine habitats primarily consume animals, as they do in other marine habitats worldwide even on tropical reefs where herbivory is at its peak (e.g., Horn, 1989; Choat and Clements, 1998; HarmelinVivien, 2002). Crustaceans are the most abundant and frequently occurring items in the diets of fishes in all marine systems in California. This dominance as a food resource for fishes probably reflects the great abundance, wide size range but especially small size, and ubiquitous occurrence of crustaceans in marine habitats. Carnivorous fishes can be divided into three groups: 1) those that feed in the water column on zooplankton, 2) those that feed on the bottom or other surfaces, and 3) those that feed mainly on other fishes or larger invertebrates. ZO OP LAN KTON F E E DE R S

The most well-known planktivorous fishes in California are the clupeoids in general, but, in particular, northern anchovy, Pacific sardine, and Pacific herring. Planktivory also occurs

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among a few species of rocky reef and kelp-bed fishes, among most species of vertically migrating midwater fish species, and in a few pelagic species of large body size, such as the basking shark in California waters. Zooplankton, not phytoplankton, makes up the bulk of the diets of planktivorous fishes, and crustaceans are the dominant members of the zooplankton community in all of these habitats. Filter-feeding and picking (by biting) are the principal feeding modes used by planktonfeeding fishes. B E NTH IC I NVE RTE B RATE F E E DE R S

Species that eat bottom-dwelling invertebrates are the most diverse group of fishes associated with both soft substrata, as in bay-estuarine and inner and outer shelf habitats, and hard substrata, especially rocky intertidal and rocky reef and kelpbed habitats. As in other marine systems, crustaceans are the most abundant and diverse members of the invertebrate assemblages in these bottom-oriented habitats. The range of structural and behavioral specializations for exploiting this diverse prey resource probably exceeds that of any other feeding group. Pickers such as kelp perch (Brachyistius frenatus) take individual invertebrates from surfaces, including kelp and other macroalgal surfaces, not just rock or sand substrata. Grazers include species such as black perch that feed on turf algae but select small invertebrate prey by winnowing from the larger collection of material. Essentially all types of feeding mechanisms, from biting to suction and ram feeding are represented among fishes that feed on bottom-associated invertebrates (see Norton, 1995). Fishes in which hard-shelled invertebrates are a major part of the diet usually possess welldeveloped oral or pharyngeal jaws to process these prey with shearing or crushing actions, as described in the previous section.

Omnivores Some fish species in every California marine habitat consume a wide variety of prey, and these prey items often belong to different trophic levels. Thus, omnivory is common among these fishes, if, as is usual in ecology, omnivory is defined as feeding on more than one trophic level. The trophic relationships depicted in the next section (figs. 14-6–11) show that in many cases fishes are feeding on more than one trophic level even without portraying any ontogenetic changes in diet and trophic level that some species are known to undergo during their lives. Omnivory adds complexity to trophic interactions and tends to compromise the distinctiveness of trophic levels vertically (Persson et al., 1996). Sometimes omnivory is used in the more restrictive sense of referring to animals that ingest both plant and animal material, that is, feeding as a primary consumer or herbivore and on at least one higher trophic level. The prevalence of such fishes is apparent in both rocky intertidal and rocky reef/kelp bed habitats. A compilation of fishes by trophic category from three different California rocky intertidal habitats shows that omnivores accounted for 7–40% of the species based on having diets containing 5–69% algal material for inclusion (chapter 8). In a wider geographic survey, Gibson and Yoshiyama (1999) tallied 0–76% omnivores using the same criteria for inclusion. And, for kelp beds, Quast (1968) found that algae had the third highest utilization among species in his study even though only three of the 45 species examined were considered to be herbivores. As Horn and Ojeda (1999) stated, the frequent ingestion of algal material by a wide variety of presumably non-herbivorous species raises questions about the digestive specializations, if any, required for assimilating algal material and its role in the energetics of these fishes.

Trophic Interactions F I S H F E E DE R S

Conceptual Background and Limitation Fish species that prey on other fishes are represented in all California marine habitats (see Trophic interactions below) and are surprisingly abundant and diverse in some habitats considering that they feed at the third or fourth and sometimes even the fifth trophic level (Horn, 1998). Among the piscivores are generalized predators such as the three California species in the genus Paralabrax, kelp bass, P. clathratus, barred sand bass, P. nebulifer, and spotted sand bass, P. maculatofasciatus (see chapter 3), which use a burst of speed and suction feeding mainly to engulf their prey. More specialized fish predators engage a variety of behaviors and structures in capturing prey. For example, the California lizardfish (Synodus lucioceps), California scorpionfish (Scorpaena guttata), and California halibut (Paralichthys californicus) all ambush their prey from stations of camouflage on the bottom (Allen, 1982). Pacific viperfish (Chauliodus macouni), blackbelly dragonfish (Stomias atriventer), and Pacific dreamer ambush their prey in deep midwaters after luring the prey to within striking distance with luminescent devices (Gartner et al., 1997). In marked contrast, the billfishes, including swordfish (Xiphias gladius) and striped marlin (Tetrapterus audax), combine high speed with a slashing or spearing bill to overtake and disorient or disable their prey (Helfman et al., 1997). In terms of feeding mechanisms, piscivorous fishes, many of which also include large invertebrates (e.g. squid, shrimp) in their diets, use biting, ram or suction feeding or a combination of these mechanisms as described in the previous section.

In this section, we present in broad and qualitative fashion some of the main trophic relationships involving the fish assemblages of six different habitat systems in California marine waters. These feeding interactions are not portrayed as food webs, even though they broadly resemble topological food webs. Food webs represent the variety of interconnected feeding or trophic interactions that occur in communities and the various ways in which energy passes through the populations composing the communities. Topological food webs focus on trophic relationships among organisms portrayed as links in the web. Such food webs are sometimes referred to as static food webs (Winemiller and Polis, 1996; Ricklefs and Miller, 2000) because only the presence or absence, not the strength, of the interactions is depicted, and no change in trophic relationships with growth of the individual participants nor change in age structure of the resources or consumers is portrayed. Even with these qualifications, our depictions do not qualify as topological food webs because we have not attempted to tabulate all the links within the community, and the fishes but none of the other organisms are identified to species. Moreover, no attempt was made to recognize guilds of consumers either of fishes or the other organisms shown. In a sense, our depictions resemble functional or interaction food webs, which identify the trophic relationships important to community structure (Ricklefs and Miller, 2000). The importance of each population in maintaining the integrity of the community by its influence on the

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F I G U R E 14-6 Trophic relationships of bay-estuarine fishes (after Cross and Allen, 1993).

growth of other populations is exhibited in such a food web and requires experimental manipulation to reveal such a role. Our illustrations do not qualify here either, but, even with these limitations, we maintain that the trophic relationships we show provide a broad consumer picture of some of the more common fish species in each system.

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Bay-Estuarine Trophic Relationships Bay-estuarine fish assemblages are recognized as being low in diversity but high in abundance and productivity with a small number of species showing numerical dominance (e.g., Allen and Horn, 1975; Haedrich, 1983; chapter 5). Feeding relation-

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F I G U R E 14-7A Trophic relationships of inner shelf fishes (after Cross and Allen, 1993).

ships, therefore, ought to be relatively simple with a food chain comprising few trophic levels. A variety of primary producers inhabit bay-estuarine systems and includes flowering plants (e.g., cordgrass, Spartina foliosa) from adjacent salt marshes, and submerged flowering plants (especially eelgrass, Zostera marina), macroalgae (e.g., Ulva spp.), benthic microalgae

(diatoms), and phytoplankton from within the bay-estuarine system proper. Detritus derived from these and other sources provides another, more amorphous source of organic matter for higher trophic levels in the system. Based on stable isotope analysis in San Dieguito Lagoon and Tijuana Estuary, two southern California bay-estuarine systems, Kwak and Zedler

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F I G U R E 14-7B Trophic relationships of outer shelf fishes (after Cross and Allen, 1993).

(1997) found that intertidal macroalgae, marsh microalgae, and cordgrass provide the organic matter that supports fishes. Trophic spectrum analysis for common fish species in the upper Newport Bay system in southern California (Horn and Allen, 1985) reveals trophic relationships composing approximately four trophic levels as shown in Cross and Allen (1993)

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and in fig. 14-6. Topsmelt and striped mullet, two of the most abundant fish species in the system (Allen, 1982; Horn and Allen, 1985), represent the herbivore and detritivore level and the broad base of the food web. The bulk of the diet of both species comprises macroalgae, plant detritus, and pennate diatoms in upper Newport Bay, and the proportion of plant

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F I G U R E 14-8 Trophic relationships of rocky intertidal fishes (central California coast).

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F I G U R E 14-9 Trophic relationships of rocky reef and kelp bed fishes (after Cross and Allen, 1993).

material in the diet of each species increases with age (Horn and Allen, 1985). Similarly, topsmelt were placed in a trophic guild of macroalgal and zooplankton consumers in Elkhorn Slough in central California (Barry et al., 1996; chapter 5). Somewhat in contrast, topsmelt in Tijuana Estuary were positioned at a higher, secondary consumer level based on stable

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isotope analysis (Kwak and Zedler, 1997) and an associated gut content analysis (West et al., 2003). Moreover, Smith (2002) found that topsmelt in three southern California bays and estuaries including upper Newport Bay, where the fish consumed mainly detritus, macroalgae and zooplankton, occupied a higher trophic position than in three kelp-bed habitats

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F I G U R E 14-10 Trophic relationships of epipelagic fishes (after Cross and Allen, 1993).

where the fish primarily ate zooplankton. These results suggest that the topsmelt is an opportunistic omnivore involved in multiple trophic pathways in bays and estuaries and deserves further study in this regard. The other common fish species shown in fig. 14-6 variously occupy three higher trophic levels. Primary carnivores in the

upper Newport Bay system include two main groups of fishes. California killifish (Fundulus parvipinnis), arrow goby (Clevelandia ios), cheekspot goby (Ilypnus gilberti), and shadow goby (Quietula y-cauda) are benthic feeders consuming microinvertebrates, mainly crustaceans and polychaetes, whereas a second set of species, deepbody anchovy (Anchoa compressa), slough anchovy

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F I G U R E 14-11 Trophic relationships of deep midwater fishes (after Cross and Allen, 1993).

(A. delicatissima), and bay pipefish (Syngnathus leptorhynchus) feed in the water column on zooplankton or, in the case of shiner perch (Cymatogaster aggregata), either on zooplankton or benthic macroinvertebrates. Secondary carnivores feed mainly on benthic macroinvertebrates and less often on fishes and include yellowfin croaker (Umbrina roncador), Pacific staghorn sculpin (Leptocottus armatus), longjaw mudsucker (Gillichthys mirabilis), and diamond turbot (Hypsopsetta guttulata). The fish species rep-

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resenting the tertiary carnivores, spotted sand bass, striped bass, and California halibut, are mainly piscivores and feed variously on fishes that occupy the lower trophic levels.

Inner Shelf and Outer Shelf Trophic Relationships The fish assemblages considered here comprise those species occupying soft-bottom habitats in coastal waters extending

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from shallow depths out to the edge of the continental shelf at about 200 m depth (see chapter 7). Feeding patterns of these fishes predictably should reflect food webs supported by phytoplankton, detritus, and, to a lesser degree, by macroalgae. In turn, the organic matter produced is consumed either by benthic or planktonic invertebrates, mainly crustaceans. Soft-bottom fish assemblages contain no herbivorous and probably no detritivorous species; thus, the fishes occupy approximately three carnivore trophic levels as shown by Cross and Allen (1993) and fig. 14-7. Crustaceans are the most important prey type of soft-bottom fishes, as they are found in the digestive tracts of all species (Allen, 1982; chapter 7). This widespread use of crustaceans as food by fishes means that members of successively higher trophic levels feed on one to a few trophic levels below them (figs. 14-7a,14-7b). Less frequently occurring prey items in Allen’s (1982) analysis included ray-finned fishes and polychaetes, but almost no gastropods or isopods were present in the diets. Hidden in the trophic relationships portrayed in figs. 14-7a and 14-7b are the ontogenetic shifts in diet that occur in numerous soft-bottom fish species. In general, neritic and benthic fishes, such as Pacific hake (Merluccius productus) and California halibut, feed on copepods early in life then, with growth, undergo shifts to diets of euphausiids and mysids, then to nektonic fishes or squids. Smaller neritic species that do not undergo this complete series of ontogenetic changes in diet include shiner perch and stripetail rockfish (Sebastes saxicola). Similarly, benthopelagic fishes, such as California scorpionfish (Scorpaena guttata), first consume gammaridean amphipods then change to shrimp and then to fishes and octopus as they increase in size. Smaller benthopelagic species undergo fewer ontogenetic shifts in diet and include yellowchin sculpin (Icelinus quadriseriatus) and white seaperch (Phanerodon furcatus), which continue to feed on gammaridean amphipods. Eighteen foraging guilds are recognized by Allen (1982; chapter 7) for soft-bottom fish assemblages in southern California. These guilds consist of sets of species that displace one another with depth in southern California waters, each, according to Allen, performing a similar ecological role in its particular depth range. Several of these depth displacements can be discerned in the profiles of trophic relationships depicted in this chapter for the inner shelf and outer shelf assemblages (figs. 14-7a, 7b). As a first example, specklefin midshipman, Porichthys myriaster (fig. 14-7a) is replaced in deeper waters by plainfin midshipman, P. notatus (fig. 14-7b). These species are categorized in their foraging behavior as bottom-refuge nonvisual pelagivores. A second example illustrated is that of white seaperch (fig. 14-7a) and the deeperdwelling pink seaperch, Zalembius rosaceus (fig. 14-7b),which are classified as cruising diurnal benthopelagivores. A third example is that of speckled sanddab, Citharichthys stigmaeus (fig. 14-7a) replaced in deeper waters by Pacific sanddab, C. sordidus (fig. 14-7b). These two species, along with the still deeper-living slender sole, Eopsetta exilis (not illustrated), are recognized by Allen (1982) as benthic pelagobenthivores. Aside from these depth displacements of ecological counterparts, the fishes representing different trophic levels of the softbottom assemblages of the inner shelf and outer shelf (or inner, middle, and outer shelf regions—see chapter 7) mostly belong to the same, relatively few taxonomic groups (figs. 14-7a, 7b). Primary carnivores in both shelf zones are mainly schooling, plankton-feeding clupeoids, especially northern anchovy and, in recent decades, Pacific sardine (not illustrated). Secondary carnivores in both zones are dominated by cuskeels (Ophidiidae), croakers (Sciaenidae), surfperches (Embiotocidae),

and flatfishes (Paralichthyidae, Pleuronectidae), whereas the tertiary or top-level carnivores in the two zones are mainly lizardfish (Synodontidae), sea basses (Paralabrax spp.), and flatfishes.

Rocky Intertidal Trophic Relationships The feeding relationships of rocky intertidal fish assemblages are similar to those of both bay-estuarine and soft-bottom assemblages in that crustaceans are the dominant prey items for the majority of fish species (see chapter 8, fig. 14-8). Two striking, but not surprising differences, however, are that rocky intertidal assemblages are supported to a great degree by macroalgal production and contain herbivorous or omnivorous species. As is mentioned in chapter 8, the availability of an abundant and a diverse standing stock of macroalgae on rocky shores in California, especially in the central and northern regions, may have led to its use by a few fish species and several invertebrates as the assemblages evolved under competitive pressures resulting in resource partitioning and niche diversification. Four trophic levels above the primary producers can be recognized among the feeding relationships of rocky intertidal fish assemblages, as depicted for the central California coast in fig. 14-8. The herbivore/omnivore level is represented by the monkeyface prickleback, rock prickleback, and reef perch. On northern California shores, the mosshead sculpin occurs on this level as do juvenile opaleye and bald sculpin on southern California rocky shores. Bald sculpin also occurs on the central coast, but in the compilation for fig. 14-8, this species was not sufficiently abundant for inclusion. On the primary carnivore level, gammaridean amphipods are major food items for several species of sculpin in addition to a prickleback (high cockscomb, Anoplarchus purpurescens), rockweed gunnel (Xererpes fucorum), graveldiver (Scytalina cerdale), and northern clingfish (Gobiesox maeandricus). The range of species is similar for northern California rocky shores, but in southern California the prickleback, the clingfish, and the sculpins are replaced by another species of clingfish (G. rhessodon), as well as the tidepool blenny (Hypsoblennius gilberti) and reef finspot (Paraclinus integripinnis). The tertiary carnivore level is represented by various subtidal predators that visit the intertidal zone during high tide periods; these species include cabezon (Scorpaenichthys marmoratus) and several species of rockfishes, e.g., grass rockfish (Sebastes rastrelliger) and black-and-yellow rockfish (S. chrysomelas). At low tide, wading birds (e.g., Great Blue Heron) and, during high tide, diving birds (e.g., Common Loon) also prey on intertidal fishes (pers. obs.). In a recent quantitative analysis of feeding guilds, Boyle (2004) recognized four such guilds distributed among 14 species of rocky intertidal fish species that were collected in sufficient numbers for analysis on the central California coast. An omnivore, a microcarnivore, a carnivore, and a polychaete-feeder guild were distinguished. The omnivore guild contained the same three species as shown for the herbivore/omnivore trophic level in fig. 14-8; in addition, black prickleback (Xiphister atropurpureus) was determined to be a member of this guild. The microcarnivore guild consisted of northern clingfish, graveldiver, and rock prickleback, all members of the primary consumer trophic level depicted in fig. 14-8. The carnivore guild contained woolly sculpin (Clinocottus analis) and striped kelpfish (Gibbonsia metzi), the same as that of the secondary carnivore trophic level of fig. 14-8, but smoothhead sculpin was excluded from the guild because it did not meet the 71% diet similarity required for inclusion by the analysis. Boyle (2004) did not sample either of the larger predators labeled as tertiary carnivores in fig. 14-8.

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Rocky Reef and Kelp Bed Trophic Relationships The fishes associated with hard substrata and kelp in shallow subtidal waters form a diverse and abundant assemblage with densities several times greater than those estimated for softbottom habitats (see chapter 9). Rocky reef and kelp bed food webs appear to be largely phytoplankton-based although detrital carbon from kelps in other regions has been shown to enter near shore food webs (Duggins et al., 1989; Dunton, 2001) and to be assimilated by epibenthic consumers including fishes (Dunton, 2001). In a study of the trophic position of the topsmelt in southern California kelp beds, Smith (2002) showed from gut content analysis that the fish was feeding on zooplankton and from stable isotope analysis that the
13C signature of the fish matched those of zooplankton and, in turn, those of phytoplankton. In truth, however, the
13C signature of the kelp Macrocystis pyrifera overlaps that of kelp-bed topsmelt leaving open the possibility that this kelp also is a carbon source for the fish. Overall, the carbon sources for kelpassociated fishes probably are best seen as a combination of phytoplankton, kelp, and smaller macroalgae. The potential carbon sources for bay-estuarine fishes are more diverse than those for rocky reefs and kelp beds because of land-based contributions of primary production to bays and estuaries (see above). Smith (2002) found that bay-estuarine topsmelt have more possible carbon sources and occupy a higher trophic position than kelp-bed topsmelt even though the former eat more macroalgae and the latter consume more zooplankton. Identifying the sources of organic matter (carbon) for fishes associated with kelp-beds and rocky-reefs remains a worthwhile endeavor for future research, especially given the wide variety of pelagic and benthic prey consumed (see below) and the intermingling of the water-column environment with a structured and stationary kelp-rock environment. Food resources available to rocky reef and kelp bed fishes are varied and abundant, reflecting the structural complexity of these habitats and the closeness of water-column habitat. As a result, both pelagic and benthic organisms are variously consumed. Pelagic prey include zooplankton, micronekton, and some larger nektonic animals, whereas potential benthic dietary items include the kelps themselves, smaller macroalgae, and invertebrates variously occupying substrata such as kelp holdfasts and blades, algal turf, rock outcrops, and sandy stretches. Quast (1968) compiled a food utilization index from an extensive dietary analysis of kelp-bed fishes. In this index, gammaridean amphipods ranked first in importance followed in order by crabs, algae, certain species of shrimps, polychaetes, and perciform fishes among 38 items assessed. Thus, crustaceans emerge in still another major habitat as the most important dietary items for fishes, as they have in bay-estuarine, coastal soft-bottom, and rocky intertidal habitats (see above). Quast’s (1968) analysis led him to conclude that, among kelp-bed fishes, 46% are carnivores, 46% are omnivores, and 8% are herbivores. Trophic relationships involving rocky reef and kelp-bed fishes are complex, and four levels above the primary producer can be identified (Cross and Allen, 1993; fig. 14-9). As mentioned, these assemblages are supported fundamentally by phytoplankton and macroalgae, perhaps mostly kelps. As in the rocky intertidal zone, rock-kelp fish assemblages include species that consume macroalgae as part or almost all of their diet, enough to be classified as herbivores (e.g., Quast, 1968; Horn, 1989). Opaleye, halfmoon, and zebraperch are shown on the herbivore/detritivore trophic level in fig. 14-9.

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As it grows, the opaleye shifts from being an omnivorous plankton feeder to an algal browser/grazer (Mitchell, 1953; Williams and Williams, 1955), and its diet becomes a combination of red, green, and brown macroalgae and benthic invertebrates (Quast, 1968; Hobson and Chess, 2001). The diet of halfmoon is similar to that of opaleye (Quast, 1968; Hobson and Chess, 2001), and both species, often in mixed aggregations, have consumed green (Leighton, 1971), red (Foster, 1975), and brown algae, especially kelp transplants (Harris et al., 1984), in manipulated field situations directed at other purposes. The zebraperch, often treated as a species in the same family (Kyphosidae) as opaleye and halfmoon (see chapter 9), may be the most herbivorous of the three species. A species that has become increasingly abundant in southern California as ocean temperatures have warmed in recent decades (Sturm and Horn, 2001), zebraperch eat macroalgae almost exclusively, mainly red algae with much smaller amounts of brown and green algae (Sturm and Horn, 1998). Interestingly, in the same 1998 study, the fish in laboratory feeding trials assimilated constituents from nondietary brown algae as efficiently as from dietary algae, indicating that, like its tropical and subtropical relatives (Kyphosus spp.), it can digest a variety of macroalgae including brown algae containing defensive secondary compounds. Although the garibaldi (Hypsypops rubicundus) is known to consume turf algae on a defended grazing site, this territorial species appears to be pursuing bryozoans and other encrusting animals when taking bites of these algae (Quast, 1968; Clarke, 1970; Hobson and Chess, 2001). The ingested algae shows little sign of being digested (Hobson and Chess, 2001). No studies of which we are aware have been completed on whether the garibaldi can digest and assimilate algal material. The blue rockfish is another algae-consuming fish associated with rocky reefs and kelp beds, especially in central California kelp beds where it is one of the most abundant species (Miller and Geibel, 1973; Hallacher and Roberts, 1985). This schooling rockfish consumes macroalgae including kelp during warm, non-upwelling periods when zooplankton, its other main food, is low in abundance. The blue rockfish is the only species within the species-rich genus Sebastes that consumes appreciable amounts of macroalgae, and it shows herbivorous tendencies by having a somewhat longer gut than other rockfishes (Hallacher and Roberts, 1985). At the primary carnivore level, rocky reef and kelp bed fishes consume either benthic and kelp microinvertebrates, as in black perch, rock wrasse (Halichoeres semicinctus), and painted greenling (Oxylebius pictus), or zooplankton, as in kelp perch, senorita, and blacksmith, although kelp perch and senorita feed on different types of prey (Cross and Allen, 1993; fig. 14-9). Black perch are known to browse and winnow algal turf for small invertebrates (Drucker and Jensen, 1991) and to compete for these food resources with its congener, striped seaperch (Embiotoca lateralis), based on extensive manipulative field studies (Hixon, 1980; chapter 17). As its name implies, the kelp perch lives in close association with Macrocystis, preying mainly on micro-crustaceans on the kelp’s surface (Quast, 1968; Hobson and Chess, 2001) but also feeding on zooplankton before reaching 100 mm SL (Bray and Ebeling, 1975). Senorita also pluck zooplankton from the water column at sizes mainly 100 mm SL before switching to feeding from various surfaces, whether it is kelp, rock, or the bodies of animals, a habit that renders it the major cleaner fish in California kelp beds (Hobson and Chess, 2001). Predation by senorita on the isopod Idothea resecata apparently keeps in

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check the impact of this herbivore on the Macrocystis canopy (Bernstein and Jung, 1979). At the secondary carnivore level, the fishes feed on benthic or kelp macroinvertebrates, as in California sheephead, pile perch, and rubberlip seaperch (Racochilus toxotes), or on fishes from the lower trophic levels, as in kelp bass, olive rockfish, Sebastes serranoides, treefish, S. serriceps, and giant kelpfish, Heterostichus rostratus (Cross and Allen, 1993; fig. 14-9). The California sheephead feeds on fixed or slow-moving bottom invertebrates such as sea urchins, mussels, crabs, and sea cucumbers (Limbaugh, 1955; Quast, 1968; Cowen, 1986), and, like labrids in general, crushes prey with well-developed pharyngeal teeth. Echinoids are major prey of this large reef fish, and the feeding activities of the sheephead have been shown to reduce sea urchin numbers and to drive them to cover on the reef (Cowan, 1983). The pile perch also crushes prey with strong pharyngeal jaws and feeds on heavy-shelled invertebrates, including molluscs, crabs, and sand dollars (Limbaugh, 1955; Quast, 1968; Brett, 1979; Hobson and Chess, 2001). Among the piscivores at this trophic level is the olive rockfish. Although this fish feeds on zooplankton as small juveniles, as they grow they shift to fishes such as juvenile rockfishes and to macroinvertebrates including squids and octopuses and smaller prey such as isopods and krill (Love et al., 2002). The treefish is another partly piscivorous rockfish that feeds on bottom-dwelling fishes and macroinvertebrates such as shrimp and crabs (Love et al., 2002). Giant kelpfish feed near kelp or on the bottom on invertebrates such as mysids, amphipods and isopods and, with increasing size, they consume more fishes including kelp clingfish (Rimicola muscarum), small senorita, and juvenile kelp perch (Quast, 1968). The kelp bass is a major fish predator around rocky reefs and kelp beds, with young bass feeding on small crabs, copepods, and plankton before assuming a generalized carnivore diet of small fishes, including anchovies, sardines, surfperches, and queenfish (Seriphus politus), and a variety of macroinvertebrates (Quast, 1968; Allen and Hovey, 2001). At the tertiary carnivore level, the giant sea bass (Stereolepis gigas) is depicted in fig. 14-9 and represents the predatory species at the top of the rocky reef/kelp bed food chain. This extremely large (2m and 250 kg), slow-growing, and latematuring polyprionid fish has protected status in California, but its biology remains poorly known and its populations severely depressed (Domeier, 2001). The giant sea bass prefers rocky reef habitat and feeds by suction with its huge mouth to take a variety of bottom-dwelling fishes including sting rays, skates, small sharks, various flatfishes, and other species as well as macroinvertebrates such as lobsters, crabs, octopuses, and squids (Domeier, 2001). Other large predatory fishes, including Pacific electric ray, Torpedo californica (Bray and Hixon, 1978; Horn, 1980), at least occasionally, prey on rocky reef and kelp bed fishes, but their impact on the assemblage remains poorly known (Pondella and Allen, 2000).

Epipelagic Trophic Relationships The feeding relationships of open ocean, surface-dwelling fishes are phytoplankton-based and are devoid of strictly herbivorous species although anchovy and sardine feed to varying small degrees on phytoplankton depending on fish age and seasonal condition. One of the greatest challenges of studying epipelagic systems is not determining the sources of carbon as it is in some other systems such as bays and estuar-

ies, but rather it is the lack of strict spatial boundaries. Bays and estuaries end as the salinity gradient flattens out on either end, soft-bottom habitats are interrupted by rocky reefs and kelp beds and vice versa, and the rocky intertidal zone meets the land, sandy or muddy stretches of shoreline, and subtidal depths. In contrast, the epipelagic zone extends to the limits of an ocean basin or even the world ocean in the extreme sense. Only deeper, darker and colder waters provide a boundary for this system, and even this limit varies with water transparency, current patterns, and other dynamic oceanographic conditions. Moreover, vertically-migrating midwater fishes regularly penetrate the lower limits from below to feed in the warmer, richer surface waters (see chapters 11 and 13), and large, powerful, epipelagic fishes such as swordfish and some tunas visit deeper waters on feeding excursions. The fluid and changing boundaries of this large zone (see chapters 11, 12 and 13) thus create an extraordinary challenge to attempts to define the trophic relationships in a system that grades from offshore to near shore and from surface to deep waters and that includes fishes moving actively or passively in vertical and horizontal directions. In a word, it is a problem of “who” to include in any analysis or description. The trophic relationships described here for the epipelagic fish assemblage emphasize the feeding interactions of juvenile and adult fishes, whereas Moser and Watson (see chapter 11) discuss the trophic relationships of larval fishes. The trophic network depicted in this chapter comprises five levels beyond the primary producers, resulting in this system having the longest food chain among the six portrayed and described in this chapter (fig. 14-10; see Cross and Allen, 1993). Such an outcome seems consistent with the recognition that oceanic food chains tend to be longer than those in coastal and upwelling zones (Fenchel, 1988). As shown in fig. 14-10, fishes enter the system at the primary carnivore level. These species include northern anchovy and Pacific sardine, probably the most abundant fishes in shallow coastal and offshore waters. These two filter-feeding (and biting) clupeoids primarily consume zooplankton, mainly copepods, but, as mentioned above, also take phytoplankton depending upon the size of the fishes and the size and composition of the plankton (Murphy, 1966; Loukashkin, 1970; O’Connell, 1972). These two icons of the California pelagic zone are now known to cycle out of phase in abundance with each other according to alternating warm (sardine) and cold (anchovy) climatic regimes of 25-30 years each in the northeastern Pacific (Chavez et al., 2003; chapters 12 and 25). Both species are preyed upon extensively by larger fishes of all three higher trophic levels as shown in fig. 14-10 and also by a variety of marine mammals such as sea lions, seals, porpoises, and whales, and by seabirds including pelicans, gulls, terns, and cormorants (Bergen and Jacobson, 2001; Wolf et al., 2001). Some shifts in diet by predators that feed on northern anchovy and Pacific sardine occur as these two major forage species cycle in abundance (e.g., Horn et al., 2005). Two other species, Pacific saury (Cololabis saira) and California flyingfish (Cheilopogon pinnatibarbatus), shown as primary carnivores in fig. 14-10, generally inhabit surface waters farther offshore than anchovies and sardines. The saury is the more abundant and better known of the two species and, like anchovies and sardines, forms a trophic link between zooplankton and higher level carnivores including economically important fish species (Horn, 1980). At the secondary carnivore level, fishes of intermediate size as well as squids are important members (fig. 14-10), and these

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species feed on combinations of smaller fishes and planktonic crustaceans. Jack mackerel (Trachurus symmetricus) feeds on increasingly larger zooplankton as it grows, and squid and anchovies may form large parts of the juvenile diet, but the food habits of offshore adults are poorly known (MacGregor, 1966; Mason and Bishop, 2001). The Pacific chub mackerel (Scomber japonicus) shows a similar ontogenetic pattern with adult fish eating various small fish, squid, and pelagic crustaceans, and they, in turn, are consumed by an array of larger fishes, marine mammals, and seabirds (Konno et al., 2001). The Pacific bonito (Sarda chiliensis) is a powerful, continuous swimming, and fast-growing small scombrid that commonly eats northern anchovy, Pacific sardine, and squid (Magnuson and Prescott, 1966; Smiley et al., 2001). California market squid (Loligo opalescens) belongs on this trophic level because it is considered to occupy a central position in coastal food webs given that it feeds on a variety of zooplankton and other invertebrates as well as small fishes and smaller squid, and, in turn, is preyed upon by a variety of fishes, seabirds, and marine mammals (Fields, 1965; Yaremko, 2001). At the tertiary carnivore level, tunas, billfishes, yellowtail (Seriola lalandi), and sharks are members of group that consumes fishes, crustaceans, and squids occupying lower trophic positions (Cross and Allen, 1993; fig. 14-10). In California, all of these species have broadly similar diets that include anchovies, sardines, and squid, and they also consume pelagic red crab (Pleuroncodes planipes) mostly in more southerly waters except when El Niño conditions bring this crustacean into the Southern California Bight (Pinkas et al., 1971; Tricas, 1979; Horn, 1980; Bayliff, 2001; Crone, 2001). This trophic level includes powerful swimmers, especially the tunas, that migrate over long horizontal distances and participate in different food chains along the way (e.g., Blackburn, 1969). Swordfish and striped marlin, the two billfishes depicted in fig. 14-10, also are highly migratory across ocean expanses (Holts, 2001a, b). The swordfish, however, is less limited by cool waters and occurs not only in tropical waters but temperate waters as well and dives to feed at depths 500 m in the open ocean (Holts, 2001a), thus expanding its vertical foraging range well beyond the epipelagic zone. A quaternary carnivore level is represented by the shortfin mako in fig. 14-10. This large (to 500 kg) and fast-swimming lamnid shark is at or near the top of the oceanic food chain in warm seas around the world, and the Southern California Bight may be an important birthing and nursery area for the species (Taylor and Bedford, 2001). Its diet consists of numerous fishes, several of which are shown in fig. 14-10, but, according to Taylor and Bedford, shortfin mako also may consume several species of marine mammals.

Deep Midwater Trophic Relationships Like other fish assemblages concentrated farther from coastal influences, deep midwater fishes are supported by a phytoplankton-based food chain (fig. 14-11; Cross and Allen, 1993). According to Neighbors and Wilson (see chapter 13), the fundamental trophic structure of fishes inhabiting California’s deep-sea basins is recognized, but further investigations are needed to sort out the details of energy budgets, predatoryprey relationships, and competitive impacts. The trophic relationships depicted in fig. 14-11 are divided into four feeding levels beyond the phytoplankton producers. The trophic structure is devoid of herbivorous fishes, and thus, the fishes, as in the epipelagic zone, enter the picture as primary carni-

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vores. Crustaceans, especially copepods and euphausiids, provide the main food source for midwater fishes although the California smoothtongue (Leuroglossus stilbius) feeds on salps and larvaceans during the more productive time of the year (Cailliet, 1972). Lanternfishes (Myctophidae) tend to be vertical migrators, whereas hatchetfishes (Sternoptychidae) are more likely to be nonmigrators, but both groups of species are zooplanktivores ( Robison and Bailey, 1982). Other midwater fishes function as secondary and tertiary carnivores, and these include stalking and ambushing predators, such as blackbelly dragonfish (Stomias atriventer) and Pacific viperfish (Chauliodus macouni), and ambush predators, such as anglerfishes (Robison and Bailey, 1982; see fig. 14-11). Vertically migrating fishes and plankton, not only transport organic material into deeper waters from the epipelagic zone, but they also are preyed upon by epipelagic fishes and other predators in the surface layers and thus are part of a vertical transport system of energy in the open ocean (see Gartner et al., 1997). Bathypelagic and deeper-living mesopelagic fish species have larger mouths and often larger bodies and tend to have broader diets than their shallow-living relatives (Ebeling and Cailliet, 1974). These size patterns and diets reflect the energy allocation model proposed for pelagic fishes in general (Childress et al., 1980). In this model, fishes from three depth zones are characterized based on the deeper-dwelling species being increasingly removed from the surface waters and the source of primary production and thus living in waters with a sparser food supply. Epipelagic species are portrayed as fishes of large size, firm muscles, high activity and energy density, fast growth, long life, and early, repeated reproduction. Mesopelagic species are characterized as fishes of small size, firm muscles, also high activity and energy density, slow growth, long life, and also early, repeated reproduction. For these midwater species, energy storage and high activity as shown in vertical migration leave little of the energy available for growth. Bathypelagic species are depicted in the model as fishes of large size, soft muscles, low activity and energy density, but fast growth, and late, one-time reproduction. For these deep-dwelling fishes living in a food-sparse environment, growth in body mass is favored at the expense of activity and energy storage. Growth to a large size may be of selective value to escape the large-mouthed predators at greater depths, and the associated large mouth size may to enable these fishes to capture a wide size range of prey. Although the Childress et al. (1980) model clearly is of heuristic value, some of its limitations regarding growth rates, longevity, and reproduction are pointed out by Neighbors and Wilson (see chapter 13). Further tests of the model are needed, especially among related species from different depth zones. Fishes living in association with the deep-sea floor complete the bathymetric profile in the open ocean in terms of trophic relationships in that they participate in the vertical transfer of energy between the productive surface waters and the depth zones increasingly distant from the surface. The food supply for these species, in part, arrives from the waters above as sinking particles ranging from detritus to fecal pellets and carcasses, or as vertically migrating midwater animals occurring near the bottom, or from bottom-associated fishes undertaking upward migrations to feed in the deep pelagic realm. In addition, infaunal and epifaunal invertebrates contribute to the diet of these bottom-associated fishes. The feeding ecology of both pelagic and bottom-associated fishes has been reviewed by Gartner et al. (1997) and is discussed in detail by Neighbors and Wilson (see chapter 13).

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Recommendations for Future Studies Several types of investigations are needed if we are to broaden and deepen our understanding of feeding mechanisms and trophic relationships among the fish assemblages inhabiting California’s coastal waters. Studies in both areas have been concentrated in relatively few species and habitats. Although a daunting task given the diversity and complexity of the marine fish fauna, comparative studies seem particularly important if we are to learn more about the evolution of feeding behavior and mechanics and if we are to identify the origins of carbon and track the flow of energy, and other constituents including pollutants, in the food webs of California marine ecosystems. Here are some of the types of studies that seem worthy of undertaking in the future: 1. Conduct comparative studies within related groups of species to determine the circumstances under which ram or suction feeding is used. The works by Norton (1995) and Cook (1996) on sculpins provide useful models for further investigation. Many taxonomic groups in the diverse California fish fauna are wellsuited for comparative analysis including the families Cottidae (still further work), Scorpaenidae, Stichaeidae, Embiotocidae, Atherinopsidae, Paralichthyidae, Pleuronectidae, Myctophidae, and Macrouridae, the last two with the logistic challenges notwithstanding. 2. Investigate the use of the gill rakers and epibranchial organs in particle-trapping mechanisms and suspension feeding. The innovative work by Sanderson et al. (1991, 1996) on freshwater fish species offers excellent models for undertaking such studies. Appropriate candidates are fishes possessing epibranchial organs including members of the families Clupeidae, Engraulidae, Salmonidae, and Stromateidae. 3. Determine the role of detritus, compared to other carbon sources, and develop topological, energy flow, and functional food webs to track the course of carbon through the principal interactors in the near shore systems (bays and estuaries, coastal soft-bottoms, rocky intertidal zone, and rocky reefs and kelp beds) in which detritus is apparently important. Stable isotope analysis is an important technique to employ here and is widely used in such studies. 4. Develop topological, energy flow, and interaction food webs for deep-sea midwater communities so that predator-prey impacts, resource partitioning, and energy budgets can be assessed in the present state and predicted in the light of environmental change. All such research on deep-sea animals is challenging, but the studies by T. L. Hopkins and co-workers in the Gulf of Mexico (e.g., Hopkins and Sutton, 1998) serve as model approaches. 5. Investigate omnivory, including that produced by ontogenetic change in diet, as a widespread but complicating factor in understanding the trophic interactions and digestive physiology of fishes in several California marine food webs including that of the rocky intertidal zone and rocky reef and kelp bed habitat. 6. Develop and use topological and interactive food webs in altered ecosystems to assess and predict the impacts

of disturbance. Humans greatly influence the structure and dynamics of food webs by removing top predators, overexploiting dominant or key species, introducing alien taxa, and contributing to global climate change. Detailed food web analyses could serve as powerful tools in assessing and predicting the magnitude of these influences. A series of papers on food webs and applied problems in Polis and Winemiller (1996) and the recent work by N. D. Martinez and coworkers (e.g., Williams and Martinez, 2000) provide stimulating background material.

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CHAPTER 15

Recruitment MAR K CAR R AN D C RAI G SYM S

Introduction: The Ecological Consequences of a Bipartite Life History The vast majority of demersal1 marine fishes have a bipartite life history, in which benthic adults produce pelagic offspring capable of dispersing great distances from their parental population (Sale, 1980; Leis, 1991; Booth and Brosnan, 1995; Caley et al., 1996). Consequences of this life history for the population and community ecology of marine fishes are striking. In marked contrast with the life history of terrestrial vertebrates, whose young disperse short distances and contribute directly to the replenishment of their parental populations, the great dispersal potential of many marine fish larvae can decouple the local production and recruitment of young to that adult population (see recent arguments to this widespread perception for coral reef fishes by Cowen et al., 2000; Cowen, 2002; Leis and McCormick, 2002; Planes, 2002; Swearer et al., 2002). Thus, at the scale of local populations, recruitment of young fish from the pelagic larval phase to benthic adult populations is the marine equivalent of births, but can be largely dependent upon the production and dispersal of larvae from parental populations elsewhere (fig. 15-1). By extension, events that influence larval production and dispersal from one population can have strong influences on the dynamics and structure of populations elsewhere. This connectivity among local populations through the dispersal and recruitment of pelagic larvae sets the spatial scale of ecological interactions among fish populations. Together, spatial and temporal variation in recruitment can have profound effects on the distribution, dynamics and spatial, size, age and genetic structure of reef fish populations. It is not surprising, therefore, that the concept and study of recruitment has long been central to our understanding of demersal fish population and community dynamics and fisheries science. The purpose of this chapter is to explain what fish recruitment is, why it is important, what we know about it for nearshore fishes of California, what we do not know but 1 Demersal refers to fishes that live in close association with the bottom regardless of substratum type. The scope of this chapter is limited to demersal species, excluding the many more highly mobile pelagic species that inhabit the coastal waters of California.

need to know, and how this information is important with respect to management and conservation.

What Is Recruitment and Why Is It Important? Recruitment, broadly speaking, is any addition of new individuals to a population. As an ecological concept however, the term has a range of different meanings. For ecologists, interested in the overall structure and dynamics of local populations, recruitment is conceptually equivalent to the addition of new individuals as they enter a local population of demersal juvenile and adult fishes. Recruitment of young to a local population occurs at birth for most viviparous (i.e., live bearing) species such as some sharks, rays and the surfperches (family Embiotocidae), or at the transition from the pelagic to the benthic environment (i.e., settlement) for some primitively viviparous (e.g., rockfishes of the genus Sebastes) and most oviparous and ovoviviparous species (fig. 15-2, settlement). Because of the difficulty of accurately quantifying rates of births and settlement (both of which often occur at night and usually involve very small, transparent organisms), ecologists often define recruitment operationally as the number of individuals recorded at some predefined stage subsequent to birth or settlement, thereby incorporating post-settlement mortality and movement in that estimate (Keough and Downes, 1982; Levin, 1994a). One common application of this measure of recruitment is to describe interannual variation in the number of individuals that have settled and persisted to accumulate at the end of each annual recruitment season (fig. 15-2, Post-settlement). Moreover, the young of many fishes settle from the pelagic habitat to spend time in “nursery” habitats (sensu Beck et al., 2001) such as estuaries and coastal seagrass and kelp beds (Baskin et al., 2003), before migrating to adult populations, thereby recruiting first to nursery habitats, and adult populations several months later (Love et al., 1991; Gillanders et al., 2003). However, because the period soon after settlement to the bottom is typically a time of high mortality, the magnitude of recruitment under this definition is strongly influenced by the time interval between settlement and measurement of recruitment (Booth, 1991; Caley et al., 1996; Hixon and Carr, 1997; Steele and Forrester, 2002). Fisheries

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F I G U R E 15-1 Consequences of offspring dispersal distances for the spatial structure of demersal fish populations. For species that produce eggs or larvae capable of being transported long distances by ocean currents (e.g., the kelp bass, Paralabrax clathratus), replenishment of local populations is determined by the survival, transport, delivery and settlement of young produced elsewhere. Such populations are referred to as open populations. In contrast, for those species that produce young that disperse little and remain within the parental population (e.g., the black perch, Embiotoca jacksoni), replenishment is determined by local offspring production. Such populations are referred to as closed populations. The two examples illustrate extremes in the continuum of openness of populations, which is also determined by the spatial scale at which populations are defined. The greater the spatial scale at which a population is defined, and encompasses the scale of larval dispersal, populations become more closed (i.e., self-replenishing). By defining populations (stocks) at these broader spatial scales, fisheries biologists manage large-scale, self-replenishing populations.

F I G U R E 15-2 Recruitment can have a range of definitions. A typical demersal reef fish produces planktonic larvae by releasing eggs into the water column, hatching demersal eggs, or extruding larvae (top panel). Because of the great dispersal potential of planktonic propagules, these offspring often disperse from parental populations to replenish populations elsewhere. The transition from the pelagic existence to a benthic existence often corresponds with metamorphosis of form in a phase known as settlement. Ecologists have generally examined recruitment at some time subsequent to settlement (i.e., when the juveniles can be sampled). Recruitment can also be considered as the stage at which an individual matures and joins the breeding population, whereas fishery biologists typically consider the attainment of harvestable size as recruitment to a fishery. In advanced viviparous live-bearers such as surfperches (lower panel), the young are extruded and immediately commence a demersal existence within the same parental population (depicted by the continuous bar representing benthic habitat). For such species, recruitment is equivalent to the terrestrial ecologists concept of births.

scientists often consider recruitment to be the stage at which a fish reaches a harvestable size, both because their interest is focused on the number of individuals entering a fishery as it relates to forecasting future catch rates and because their estimates are often reliant on fishery-dependent sampling.

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In contrast with all of the above, population modelers interested in long-term dynamics might consider recruitment to be the stage at which a fish reaches reproductive age and size and begins to contribute to subsequent generations (fig. 15-2, Reproductive maturity). Thus, recruitment, including births

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within a population as well as immigration of larvae or older stages, is the addition of individuals to a population and is countered by losses from mortality or emigration. It is critical, therefore, that any discussion of recruitment clarify these definitions.

Local Population Structure, Dynamics and Distribution At the most basic level, recruitment of larvae or juveniles is important because it is the principal source of population replenishment, and without replenishment any population will ultimately become extinct (excepting immigration at small spatial scales). The importance of this recruitment to the structure and dynamics of fish populations depends on a complex combination of its magnitude and variability, the size and variability of the benthic population, and the extent to which postrecruitment processes dampen or modify recruitment variation. Both the magnitude of and variability in recruitment will have strong effects on adult population size and persistence (see articles cited in reviews by Doherty and Williams, 1988; Doherty, 1991, 2002, Olafsson et al., 1994; Caley et al., 1996; Armsworth, 2002; Forrester et al., 2002; Hixon and Webster, 2002; Osenberg et al., 2002). If low and variable (relative to resource availability), recruitment can limit and determine population size below levels at which resources are limiting (i.e., recruitment limitation, sensu Doherty, 1981; Victor, 1986a). However, if high (relative to resource availability), recruitment can saturate resources and density-dependent post-recruitment processes contribute more to spatial and temporal variability in population size. Thus, to understand the role of recruitment in determining or contributing to the spatial structure and temporal dynamics of fish populations requires a full understanding of recruitment (pre- and post-settlement) and post-recruitment processes. Recognition of this is reflected in the growing number of conceptual and analytical models that explore the relationships among these processes (Armsworth, 2002; Doherty, 2002; Forrester et al., 2002; Hixon and Webster, 2002; Osenberg et al., 2002, and articles cited therein). The recruitment of demersal fishes fluctuates at many scales of space and time. Within a single breeding season, births, settlement, or recruitment to the reef can occur in a single pulse, a range of pulses or as an apparently chaotic or stochastic process (Pfister, 1996; Dixon et al., 1999; Findlay and Allen, 2002; Davis and Levin, 2002; Steele et al., 2002). Recruitment can also vary between seasons, even when the spawning stock does not vary appreciably. The many examples of interannual and decadal variation in recruitment of California fishes (e.g., Cowen, 1985; Stephens et al., 1986; Schmitt and Holbrook, 1990; Anderson, 1994; Carr, 1994a; Ralston and Howard, 1995; Pfister, 1996; Holbrook et al., 1997; Love et al.,1998a; Hobson et al., 2001), reflect the great temporal variability in recruitment of marine fishes in general (Rothschild, 1986; Houde, 1987; Doherty and Williams, 1988; Sinclair, 1988; Doherty, 1991; see contributions in Chambers and Trippel, 1997). Likewise, the variety of species for which recruitment has been shown to vary markedly over scales of 10s of meters (Larson, 1980a; Ebeling and Laur, 1985; Behrents, 1987; Carr, 1989, 1991; Steele, 1997a,b; Steele and Forrester, 2002; Hartney and Grorud, 2002; Findlay and Allen, 2002) to 100s of meters (Larson, 1980a; Carr, 1994a; Anderson, 1994; Pfister, 1996) are representative of the diverse fish fauna of California. This fine scale variability in combination with larger dispersal scales is likely to decouple local production from the number of juve-

F I G U R E 15-3 Larval durations of temperate rocky reef and tropical coral reef fishes from the northeastern Pacific and indo-Pacific, respectively. Differences in sample size reflect differences in larval duration estimates between the two regions. With the exception of the viviparous surfperches, larval duration in temperate fishes is longer, implying greater dispersal potential. Larval duration estimates were compiled from Brothers et al. 1983, Brothers and Thresher 1985, Victor 1986b, Thresher et al. 1989, Wellington and Victor 1989, Cailliet et al. 2000, and Krigsman 2000.

niles entering a local population. Consequently, stock-recruitment relationships are unlikely to exist or be detectable at scales less than typical larval dispersal distances. These points emphasize the importance of broadening the spatial scale at which ecologists typically study the relationships between recruitment and other demographic processes.

Regional Population Structure, Distribution and Persistence At larger spatial scales (10s–100s of km), regional populations of benthic juveniles and adults are comprised of multiple local populations, more or less connected with one another by the dispersal and recruitment of larvae. Some evidence suggests that larval dispersal is sufficient to exchange recruits among local populations over a broad regional population. To the extent that larval duration reflects realized dispersal distances, the pronounced larval duration of many California marine fishes suggests substantial connectivity (i.e., dispersal and recruitment between local populations). Existing reviews of larval duration suggest that, as a whole, larval durations for California rocky reef fishes are shifted more toward longer durations than coral reef fishes (fig. 15-3). Three lines of evidence

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suggest that longer larval duration results in greater dispersal distance. First, there is a general positive relationship between estimates of larval duration and dispersal distance (Shanks et al., 2003). Second, recruitment patterns are often correlated with large-scale oceanographic features that have the potential to transport larvae great distances from source populations. For example, Cowen (1985) found that recruitment to local populations of California sheephead (Semicossyphus pulcher) in the northern portion of the Southern California Bight corresponded with El Niño events. He suggested that northerly shifts in currents during these events transported larvae from populations along Mexico to the northern portion of the Bight. Finally, studies of the genetic structure of populations designed specifically to estimate dispersal distances suggest long distance dispersal distances for many species, particularly for fishes (Kinlan and Gaines, 2003; Palumbi, 2003). Nonetheless, a growing number of studies suggest that dispersal distances may be substantially shorter than predicted by larval duration (Swearer et al., 2002) and tools to better estimate the extent of realized dispersal distances are developing rapidly, as are interdisciplinary approaches for determining the physical and behavioral processes that determine dispersal (Thorrold et al., 2002). With the advent of such tools and approaches, the ecology of larval dispersal is clearly one of the most exciting fields in marine fish ecology. In combination, the heterogeneous spatial structure of regional fish populations and larval connectivity among local populations has important implications for how recruitment and local population dynamics might scale-up to influence the dynamics and persistence of regional populations (Chesson, 1981, 1996, 1998; Armsworth, 2002; Carr et al., 2002; Cowen, 2002; Forrester et al., 2002). This interest in the potential influence of local-scale population processes on regional population dynamics stems from the growing theory on metapopulations and other spatially-structured populations. Much of this theory indicates that the extent to, and manner by, which local population dynamics influences regional population dynamics and regulation2 is determined by the rates and distribution of larval connectivity among populations, temporal asynchrony in dispersal, recruitment and mortality among populations, and the strength of local density-dependence in larval production and recruitment (Hanski and Gilpin, 1997; Armsworth, 2002). Because larval production and recruitment of at least some California fishes, like many coral reef fishes, are spatially variable and density-dependent (see Post-settlement Processes section) and dispersal distances of many species appear to span the spatial scales of regional populations, the persistence of regional fish populations may be strongly influenced by local production, dispersal and recruitment.

Community Structure and Dynamics The interactions between spatial and temporal variability in larval fish recruitment is central to several models hypothesized to explain the structure, dynamics and persistence of fish communities. Several of these models are direct extensions of models of population dynamics. For example, if population sizes of species constituting a local community are each lim2 Regulation refers to the maintenance of a population over time, within limits set by demographic rates such as births and deaths that change in magnitude as a function of population density. This relationship is referred to as density-dependence.

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ited by larval recruitment (and early post-settlement mortality is density-independent), such that their combined abundance remains below that which saturates resources and induces interspecific competition, then their combined and separate population sizes will largely reflect temporal variation in larval recruitment. This competition-free coexistence of a fish assemblage can reflect limited larval supply, primary recruitment limitation (Doherty, 1981), or early and rapid declines in recruit density caused by post-settlement predation, secondary recruitment limitation (Victor, 1986a). Two related lines of evidence that settlement can be limited by larval supply are provided by studies of the recruitment of kelp bass, Paralabrax clathratus, and opaleye, Girella nigricans, at the Palos Verdes Peninsula in southern California. In 1987, kelp bass recruitment was strongly and positively correlated with giant kelp density at Santa Catalina Island, but recruitment of kelp bass to kelp beds off Palos Verdes Peninsula was almost nil (Carr, 1994a). Similarly, recruitment of pelagic juvenile opaleye occurred in rocky tidal pools along the coast south of Palos Verdes but was not observed at the Peninsula (Norris, 1963). Norris hypothesized that internal waves transported larval and post-larval opaleye onshore and speculated that recruitment of opaleye at Palos Verdes was preempted by offshore advection and the destruction of internal waves caused by the persistent coastal upwelling characteristic of that area. Not until 20 years later did Shanks (1983, 1988) cleverly examine and support Norris’ hypothesis that internal waves transport fish larvae onshore, providing some support for this mechanism of limited recruitment of opaleye at Palos Verdes. In addition, at least one study suggests that population densities of an assemblage of subtidal sculpins in the San Juan Islands exist below levels at which resources (food or space) are limiting (Norton, 1991). However it is unclear if these population densities are limited by larval recruitment or postsettlement mortality. Recruitment need not be limiting to structure fish assemblages. If recruitment rates are sufficient to saturate free space, but free space is limiting and becomes available unpredictably, and if there is little difference in competitive ability between species, then community structure may appear to be an unpredictable lottery. This lottery hypothesis (Sale, 1991) predicts a cap on total number of individuals in a community, but the relative abundance of species will vary unpredictably over time, and is contingent on recruits being readily available. Few studies have tested both the required assumptions and predictions of this hypothesis for temperate fish assemblages, but those that have looked at the relative effects of variable recruitment, or the resilience or predictability of assemblages have suggested a more deterministic assemblage structure (e.g., Pfister, 1996; Steele, 1997a, 1997b; Steele et al., 1998; see studies reviewed in chapter 17, and Stephens and Zerba, 1981). The lottery model (vs. lottery hypothesis) and storage effect are extensions of the original lottery hypothesis (Warner and Chesson, 1985). With similar assumptions regarding limiting resources, this model posits that changing environmental conditions favoring recruitment of each species relative to others maintains coexistence despite their competitive equality. The model is similar to Hutchinson’s gradual change hypothesis, but focuses on the changing relative strengths of larval recruitment over time to keep each species from becoming competitively excluded. Assuming that favorable recruitment conditions occur sometime during the lifespan of adults and that larvae can be produced to take advantage of favorable

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recruitment conditions (i.e., the potential for larval recruitment is stored from one favorable recruitment event to the next over the lifespan of adults), species persist in that assemblage between bouts of larval replenishment. One possible scenario by which this mechanism contributes to coexistence of kelp forest fishes is the ever-changing composition of macroalgal assemblages on rocky reefs (in time and space) and observed differences in recruitment strength of these species in response to different states of these algal assemblages (Carr, 1994a). Some species recruit to dense canopies of giant kelp, others to sparse stands, and others to the algal understory that flourishes in the absence of giant kelp (Carr, 1989; Anderson, 1994). If not excluded by interspecific competition, these species persist between replenishment events associated with changes in algal composition caused by storms and other disturbances. In contrast with these non-equilibrial hypotheses, in which species composition varies unpredictably over time in response to temporally stochastic recruitment events, are hypotheses that predict stable assemblage structure reflecting predictable relative magnitudes of recruitment. The niche diversification hypothesis assumes that each species is competitively superior in specific niches (particular combinations of environmental conditions and resource states). In the context of recruitment, this hypothesis predicts that recruits of a species will exhibit competitive advantages (or at least differential survival) over recruits of other species under certain environmental conditions, resulting in a partitioning of limited resources (and differences in recruitment) within the assemblage. Tests of this hypothesis are few because of the requirements of demonstrating interspecific competition and resource partitioning (see chapter 17) among recruits. In some cases, where recruitment directly reflects adult distributions (e.g., the young of live bearing surfperches), putative patterns of partitioning may reflect resource partitioning of adults. The depth-related zonation of adult striped seaperch, Embiotoca lateralis, and black perch, E. jacksoni, where these two species co-occur in sympatry results in similar zonation of their newborn young (S. Holbrook, pers. comm.). In contrast, where the two common gobiids, Rhinogobiops nicholsii and Lythrypnus dalli, cooccur experimental manipulations indicate no substantive effects on the recruitment of one another (Steele, 1997a). Differences in the timing of recruitment, largely driven by the timing of reproduction, might reflect temporal partitioning of limited nursery resources among species. Year-to-year constancy in the seasonal order of parturition and recruitment of juvenile rockfishes to kelp canopy habitats, in which copper, Sebastes caurinus, gopher and black and yellow (S. carnatus and chrysomelas, respectively), and kelp (S. atrovirens) rockfish exhibit lagged peaks in recruitment over the duration of the recruitment season may reflect temporal partitioning of the canopy habitat (Anderson, 1983; Carr, 1991), although such temporal patterns may reflect other ecological processes as well. Our understanding of the role of recruitment in structuring temperate fish assemblages lags far behind that of coral reef fish ecologists, where the role of recruitment has been a central focus (Sale, 1991, 2002). Further tests of these alternative hypotheses and how their applicability varies across varying environmental conditions in time and space is an enormously fertile direction of study in temperate fish assemblages. Determining the sources of variability in recruitment and how their contributions vary and interact in time and space is fundamental to understanding population persistence and community structure and dynamics.

Processes that Contribute to Spatial and Temporal Variation in Recruitment Variability in recruitment has been demonstrated to be important in both theoretical and empirical studies. Spatial and temporal variation in the distribution and rate of replenishment of demersal populations will reflect environmental and ecological processes that act prior to the delivery of potential recruits to a population (the pre-settlement phase), during the transition from pelagic to benthic existence (the settlement phase) or at any point subsequent to settlement (the postsettlement phase; Richards and Lindeman, 1987). Moreover, processes occurring in one phase of the recruitment process can interact synergistically with those operating during other phases to generate patterns that might be difficult or impossible to explain by studying each phase in isolation. The difficulty in understanding recruitment dynamics reflects not only the complexity of the life history of demersal fishes, but also the diversity of factors that cause variation in recruitment and the multitude of spatial and temporal scales over which these processes act (fig. 15-4). To understand the absolute and relative effects of the many biotic and abiotic processes that influence larval production, pelagic dispersal and survival, settlement and post-settlement survival requires research programs that examine these processes at spatial scales from meters to 100s of kilometers and temporal scales from hours to centuries.

Pre-settlement Phase: Sources of Variation in the Dispersal and Delivery of Potential Recruits Prior to settlement to the adult population, processes that contribute to spatial and temporal variability in the distribution and magnitude of recruitment include larval production, dispersal, mortality and condition of eggs and larvae in the pelagic environment (fig. 15-1). S PATIAL AN D TE M P ORAL VAR IATION I N LARVAL P RODUCTION

As a source of recruitment variation, larval production has received little attention. One reason for this has been the perceived decoupling of local production and recruitment, particularly given the disparate scales of local variation in adult fecundity, and the scale at which the larval pool is thought to replenish local populations. Another reason is that estimated relationships between stock and recruitment in the fisheries literature are frequently weak, suggesting that the high and variable mortality of pelagic eggs and larvae obscure any relationship between production and recruitment. Additionally, the relative magnitude of year-to-year variability in larval production is thought to be much less than that of recruitment, suggesting that other sources of variation are more influential. Recent studies, however, indicate that production might in fact be more important than previously thought. The perception that variability in local larval production does not scale to or reflect variation in the size of the larval pool from which local recruitment is received, is contingent on the spatial scale of processes that influence larval production and recruitment. If larval production is in fact either autocorrelated or forced by large-scale processes, then estimates of production at the local scale can reflect larger scale variation in production. Although very few studies of temperate fishes have explored this approach, one example of its

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F I G U R E 15-4 The multitude of biotic and abiotic processes that influence larval production, pelagic dispersal and survival, settlement and postsettlement survival of demersal fishes act across a daunting array of spatial and temporal scales. Physical oceanographic and geomorphological features, along with species interactions, influence both the productivity and resources available across benthic habitats, which in turn influence larval production and the settlement and post-settlement survival of recruits. Likewise, physical-biological coupling in the pelagic environment causes variation in the transport and survival of eggs, larvae and pelagic-juveniles.

potential merit has been demonstrated for coral reef fishes (Robertson et al., 1988). Evidence that larval production is influenced greatly by regional scale climatic events comes from responses of both local and regional production to episodic and longer-term large-scale environmental variability. For example, during episodes of low productivity corresponding with the El Niño events of 1982–1983 and 1992–1993, both fecundity and recruitment of some rockfishes in central California were greatly depressed (Lenarz and Echeverria, 1986; Lenarz et al., 1995; VenTresca et al., 1995). Likewise, both fecundity and recruitment of an intertidal sculpin, Clinocottus analis, in southern California were depressed during the 1997–1998 El Niño (Davis and Levin, 2002). Long-term (one or more decades) effects of climatic change and corresponding responses of both biological productivity and larval production may also explain decade-long periods of poor recruitment. For example, long-term declines (from the late 1970s to the early 1990s) in recruitment of many reef fish species throughout the southern California Bight are thought to reflect negative trend¡s in coastal productivity, resulting in declines in larval production and survival (Holbrook et al., 1997; Love et al., 1998a,b; Brooks et al., 2002). Concurrent with these environmental sources of decline in larval production were declines in some spawning stocks that have been attributed to fishing (Love et al., 1998b). Because species with more northern distributions (e.g., rockfishes) responded more strongly to these causes of decline than those with more southern distributions, the structure (i.e., relative abundance) of fish assemblages changed over this period. For

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example, on a rocky reef in the Santa Barbara Channel, recruitment of species with cooler water affinities such as blue rockfish, Sebastes mystinus, gradually declined over a period of warming from 1977 through 1982, while recruitment of a warmer water species, the blue chromis, Chromis punctipinnis, increased (Ebeling and Hixon, 1991). Similarly, long-term (8-year) patterns of recruitment of two species of rockfish to soft bottom habitats in southern California were inversely related to one another, leading investigators to conclude that years of cooler water temperatures favored recruitment of one species, Sebastes saxicola, while warmer years favored recruitment of the other, S. dalli (Mearns et al., 1980). Although these large-scale patterns of recruitment confound larval production and dispersal processes, that they may reflect regionwide temporal patterns in larval production is suggested by persistent large-scale (e.g., latitudinal) differences in larval production (Eldridge and Jarvis, 1995), which likely explain persistent regional patterns of larval abundance along the California coast (Moser and Boehlert, 1991). In contrast with region-wide coherence in environmental conditions and larval production, smaller scale variation in environmental conditions contributing to differences in production and quality of offspring between local populations can be substantial. One example is the strong differences in production of young among local populations of both striped seaperch and black perch along the coast of Santa Cruz Island (Schmitt and Holbrook, 1990). These differences were thought to reflect responses of adult fecundity of each species to variation in local prey availability, related to differences in the local

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macroalgal assemblages at each site. Similarly, variation in the nutritional components (e.g., protein, lipids, esters) of yellowtail and shortbelly rockfish eggs and larvae at birth varied 2–3 fold between populations inhabiting three submarine canyons off northern California (MacFarlane and Norton, 1999). Thus, while episodic or long-term variation in recruitment at the regional scale may reflect region-wide coherence in responses to changes in productivity and larval production at that scale, differences in environmental conditions and larval productivity between local populations may result in marked differences in their relative contributions to the regional larval pool within and between years. Our understanding of the extent, causes and potential consequences of this variation has been hampered both by the paucity of studies that have examined it, and by the difficulty of decoupling larval production and mortality in the plankton to determine the relative effects of these temporally co-varying processes on the magnitude and variability of recruitment. S PATIAL AN D TE M P ORAL VA R I ATION I N LARVAL DI S P E R SAL,

F I G U R E 15-5 Relative abundance of midwater complex rockfish recruits (light gray bars above the line) relative to benthic complex rockfish recruits (black bars below line). El Niño conditions favor recruitment of the benthic complex, whereas La Nina favors recruitment of the midwater complex. During normal years, abundances are more equitable.

MORTALIT Y AN D C ON DITION

Most temperate demersal fishes produce vast numbers of larvae (see chapter 19), and the disparity between this tremendous production of larvae with the few number of young actually delivered to adult populations implies very high pre-settlement mortality (Hjort, 1926; Doherty, 1991; Doherty and Williams, 1988; Leggett and DeBlois, 1994). Small changes in mortality rate over the period that fish larvae spend in the pelagic environment can cause huge changes in the number of young available to replenish local or regional populations (Houde, 1987). Therefore, processes that influence larval loss have been a central focus of fisheries science (Sinclair, 1988; Heath, 1992; and contributions in Chambers and Trippel, 1997). One approach to understanding the importance of variable survival in the plankton is to compare the relationship between successive stages of the recruitment process. For example, Ralston and Howard (1995) compared year-to-year variation in the number of late-stage, pelagic juvenile, rockfish collected in mid-water trawls offshore with that of young recruits observed on shallow rocky reefs along the north coast of California. The strong positive relationship between these two stages suggest that interannual variation in recruitment of young-of-year to populations inhabiting inshore reefs is established early in the larval stage, prior to stages collected by the offshore pelagic juvenile trawls. How this variation in recruitment to reef-associated populations is ultimately manifested in the size and structure of demersal populations and numbers of adults are pressing directions of study (see Post-settlement processes that can modify or diminish settlement patterns section). The dispersal of fish eggs and larvae influences recruitment dynamics in two fundamental ways; as a source of mortality and as a source of spatial and temporal variation in delivery to adult populations. Physical processes that advect larvae far off shore, precluding their return to adult populations, are thought to be a major source of larval mortality. These processes are especially important along coastlines at the western edge of continents, like California, where coastal upwelling can be strong and persistent (Parrish et al., 1981) and where the influences of the California and Davidson Currents and coastal longshore currents shift on and offshore from year-to-year (Hickey, 1979). Large-scale changes in currents coincident with climatic events (e.g., El Niño and La Niña) are also important determinants of larval delivery. For example, Cowen

(1985) used otoliths (ear bones) to age and back-calculate the year of larval recruitment of California sheephead (Semicossyphus pulcher) at sites throughout northern Baja California and the Southern California Bight. From these recruitment estimates, he ascertained that rates of recruitment shifted among sites in accordance with changes in the California Current. Populations in the northern portion of the species range appear to be replenished during El Niño episodes when northward flowing currents transport larvae produced by parental populations along the coast of Mexico. Rockfish recruitment along central and northern California is also strongly affected by climatic events, and different responses of species to these events can lead to strong differences in relative rates of species replenishment, and the structure of local assemblages. For example, during the 1992–1993 El Niño event, the relative magnitude of recruitment of two rockfish complexes (genus Sebastes) varied markedly (Lenarz et al., 1995). The complex of more solitary benthic species, including kelp, gopher, black and yellow, copper, China, grass and quillback rockfish, are characterized by 1–2 month pelagic durations, whereas the mid-water aggregating complex, including widow, yellowtail, olive, black and blue rockfish have pelagic durations of 3–4 months. Preceding the 1992–1993 El Niño, recruitment was predominated (70–90%) by the mid-water aggregating complex. In sharp contrast, during the 1992–1993 El Niño, the solitary benthic complex recruitment was predominant (60–80%). This pattern was repeated during the more recent 1998 El Niño (fig. 15-5). We monitored recruitment of these two species complexes using diver surveys during the one-year El Niño event, the following La Niña event (1999) and a more typical La Nada condition the following year (2000). As observed during the previous event (1992–1993), the benthic complex dominated recruitment during the El Niño, the midwater aggregators dominated the La Niña event, and both complexes recruited in more equitable numbers during the more typical La Nada year (fig. 15-5). Knowledge of what life history (e.g., timing of spawning, larval duration) and behavioral attributes (e.g., vertical stratification, thermal preference) contribute to how species respond to differing oceanographic events is key to understanding and predicting recruitment dynamics (e.g., Sakuma and Larson, 1995; Sakuma and Ralston, 1995, 1997; Sakuma et al., 1999; Bjorkstedt et al., 2002).

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Smaller scale features (1–10s of kilometers), including wind stress, localized upwelling and relaxation events, offshore jets, eddies, internal waves, tides, tidal bores and others, all may contribute to spatial and temporal variation in larval delivery. Moreover, some of these features (e.g., coastal upwelling, offshore jets, eddies) can be spatially consistent, associated with particular coastal geomorphological features (e.g., angle of the coastline to prevailing wind patterns, headlands, underwater topographic features and bathymetry) and as such, establish persistent spatial patterns of larval delivery (Boehlert and Mundy, 1988; Cowen, 2002). One excellent example of the effect of persistent features is the coast-wide pattern of recruitment of purple sea urchins associated with offshore jets and eddies up current and down current of headlands, respectively along the northern coast of California (Ebert and Russell, 1998). Behavioral (e.g., differential responses to environmental cues) and mechanical (e.g., relative volume and density) responses of pelagic stages and how these responses change with ontogeny influence greatly the relative effects of physical processes on dispersal and onshore transport (Boehlert and Mundy, 1988; Moser and Boehlert, 1991; Larson et al., 1994; Sakuma and Ralston, 1995, 1997; Cowen, 2002). Of particular importance is the vertical stratification of larvae at different stages of development and how position in the water column influences exposure to transport mechanisms (Boehlert and Mundy, 1988; Cowen, 2002; Findlay and Allen, 2002). Moreover, differences in vertical stratification may determine the depth stratification of settlement and recruitment of different species (Love et al., 1991). Another example of the interaction between behavior and environmental cues is the well-documented association of late-stage pelagic juveniles of several species with biotic structures (e.g., drift macroalgae) associated with physical features (e.g., fronts, slicks, internal waves; Boehlert, 1977; Kingsford, 1993, 1995; Bjorkstedt et al., 2002). Furthermore, behavior independent of environmental features can influence patterns of dispersion (i.e., aggregation) of pre-settlement larvae prior to settlement. Although best documented for a temperate goby in Chesapeake Bay (Breitburg, 1989, 1991), some California reef fishes are known to aggregate prior to settlement to the bottom including gobies (Lethops connectens), clinids (Heterostichus rostratus, Gibbonsia spp.) and sculpins (Marliave, 1986; Carr, 1989, pers. obs.). All of these mechanisms of physical and biological coupling contribute to variation in the delivery of potential recruits to demersal populations. More recently, efforts to understand both the spatial and temporal patterns of larval supply and the physical processes that determine delivery of potential recruits to a demersal population have focused on sampling delivery at or adjacent to adult populations. An important attribute of this approach is that patterns of delivery of potential recruits to collectors positioned up current of demersal populations and standardized by their size and location sample delivery and settlement independent of benthic habitat features that vary spatially (among reefs) or temporally (among years). In contrast, estimates of delivery and settlement to benthic habitats (e.g., macroalgae), confound patterns of delivery with patterns of habitat quality and availability. An increasingly common approach employed for coral reef fishes has been light traps. These devices exploit the behavioral response of competent pelagic larvae or juveniles for light and entrap individuals attracted to the light. Although this method continues to be explored for sampling temperate reef fishes, it has met with mixed success, presumably because of the lower visibility and ability of larvae to detect the light (Steele et al., 2002).

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Alternatively, collectors designed to exploit the thigmotaxic (i.e., attraction to physical structure) behavior of fishes has proven to be very useful (Carr, 1991; Ammann, 2001; Findlay and Allen, 2002; Steele et al., 2002). This approach involves suspending structurally complex structures in the water column, and enveloping the structures (and recruits) in fine mesh nets when they are collected for sampling. A third approach has been to construct isolated benthic habitats (typically, these are small artificial structures or reefs constructed of rocky substrate) that are enclosed in cages that exclude predators to prevent post-settlement predation from altering patterns of settlement. All three approaches (light traps, suspended or benthic structures) require frequent sampling both to minimize post-settlement processes from altering settlement patterns and in order to relate patterns of delivery with physical features (e.g., internal waves and tidal flux). Frequent sampling is particularly important for the structural collectors to minimize the possibility of post-settlement emigration of recruits from the structures. Two examples of this approach for determining physical processes that contribute to larval delivery and the importance of delivery in determining patterns of recruitment have been applied to kelp bass, Paralabrax clathratus, at Santa Catalina Island off southern California (Findlay and Allen, 2002 and Steele et al., 2002, respectively). Delivery of kelp bass larvae onshore was found to be associated with tidal bores but patterns of larval supply were not reflected in subsequent patterns of recruitment in the reef environment. In addition to physical forcing, prey availability and predation are thought to be major sources of temporal variability in recruitment (Lasker, 1981; Bailey and Houde, 1989; Sinclair, 1988; Cushing, 1990, 1995; Mullin, 1993). The literature on this subject is too vast to summarize comprehensively here. In addition to determining rates of loss in the plankton, prey availability can affect the size and physiological condition of larvae at settlement, influencing their susceptibility to predation and post-settlement performance and mortality (Searcy and Sponaugle, 2001). Positive interannual relationships between larval mortality and the abundance and distribution of pelagic predators, both invertebrate and fishes, including cannibalism, attest to the potential importance of predation prior to recruitment (e.g., Butler, 1991). These critical biotic interactions are not independent of the many physical processes mentioned in this section and one of the most exciting directions of fisheries ecology is identifying how the spatial and temporal patterns of biotic interactions are coupled with physical features that influence the strength of and variation in these interactions.

Settlement Phase: Transition from the Pelagic to the Demersal Existence Having survived the vagaries of mortality and dispersal in the pelagic realm, larvae and pelagic juveniles must next survive the transition into an entirely new environment to recruit to nursery or transition habitats or directly to adult populations. Not surprisingly, settlement is one of the least understood phases in the process of recruitment. Because the transition from the pelagic to the demersal existence is brief, often occurs at night and involves small and cryptic individuals, study and knowledge of this process has been extremely limited. Factors likely to influence settlement include 1) hydrodynamic processes, 2) probabilities of encountering suitable

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habitat or environmental cues 3) behavioral responses to environmental cues, and 4) interactions with resident organisms, including predators. Small-scale hydrodynamic features (1–10s of m) are likely to influence the distribution of fish settlement. The susceptibility of larvae delivered onshore by hydrodynamic features (e.g., winds, tides, tidal bores) suggests that larvae will continue to be influenced by nearshore hydrodynamic features during settlement. Strong tidal currents capable of pushing entire kelp stands well below the surface could clearly influence the ability of fish to maintain position above the bottom. Strong swell and wave action are also likely to influence the ability of shallow species (especially intertidal fishes) to settle to the bottom. Such small-scale effects are manifested by the accumulation of recently delivered or settled individuals in eddies of physical structures, including rocky outcrops, kelp stands, even individual plants (Breitburg, 1989, 1991). One of the least explored aspects of settlement is how the spatial distribution of larval delivery and settlement habitat (including cues) influence encounter rates of larvae and their settlement habitat to determine spatial patterns and the overall magnitude of recruitment. Two important aspects of this are the combined effects of patterns of dispersion of larvae and settlement habitat, and temporal variability in availability of settlement habitat. Many of the physical processes described in the Physical-biological processes that determine dispersal and larval delivery section create highly aggregated patterns of larval dispersion as they are delivered to the benthic habitat. Varying patch sizes of larval aggregations have been well documented, but how patch size interacts with the number, distribution and size of individual settlement habitats to determine overall settlement rates has been mostly neglected. One example is Levin’s (1993, 1994a) experimental assessment of the effect of dispersion patterns (random versus clumped) of algal patches on settlement and recruitment of cunner, Tautogolabrus adspersus, an east coast temperate reef fish. Cunner settlement was initially greater in randomly distributed patches, but subsequent recruitment was similar across the two patterns of dispersion. More locally, the presence of giant kelp is known to increase local settlement of several California reef fishes (Carr, 1989, 1991, 1994a,b). This effect is most pronounced for species whose larvae occur in the midto-upper portions of the water column, where kelp is a major structure that larvae might encounter as they move along shore. The shape of a kelp bed and density of plants may have strong effects on whether larvae moving alongshore or onshore encounter a kelp stand or individual plants. Similar conditions exist for species that recruit to any benthic habitat that is distributed non-uniformly. The effects of dispersion of seagrass habitat, as well as other plant characteristics (e.g., plant height and density), have received much attention in temperate estuarine habitats. Several studies provide evidence that attributes of seagrass habitats influence the relative density of recruits within a bed (see references in Valle et al., 1999). However, while these attributes appear to influence the local density of recruits (i.e., for a given level of larval supply), at broader spatial scales patterns of distribution of seagrass beds, such as their proximity to open coast, are better predictors of relative levels of recruitment (Bell and Westoby, 1986; Bell et al., 1987, 1988; Valle et al., 1999). Similarly, the size, density and species composition of macroalgal assemblages and seagrass beds vary greatly in response to climatic condition, storm disturbance, sediment

movement, grazing and disease. For example, the highly dynamic and spatially variable stands of kelps can influence variation in settlement and recruitment within and among reefs, both for species whose larvae settle from the plankton as well as live bearing species whose young are born directly into kelp habitats (Larson and DeMartini, 1984; Ebeling and Laur, 1985; Holbrook et al., 1990a; Bodkin, 1988; Carr, 1989, 1991, 1994a,b; DeMartini and Roberts, 1990; Anderson, 1994; Nelson, 2001). Similar effects have been documented for reef fishes recruiting to non-kelp macroalgal habitats in temperate reefs around the world (Jones, 1984; Choat and Ayling, 1987; Carr, 1989; Levin, 1991, 1993; Levin and Hay, 1996) as well as fishes that recruit to seagrass stands in embayments (Orth and Heck, 1980; Orth et al., 1984; Sogard et al., 1987; Heck et al., 1989; Ferrell and Bell, 1991; Levin et al., 1997; Valle et al., 1999). Those studies that have examined the influence of such settlement habitats both at local (1–100s of meters) and more regional (1–100s of kilometers) spatial scales (Carr, 1994a; Levin et al., 1997; Steele et al., 2002) suggest that large-scale patterns of larval supply become more influential in determining recruitment patterns at larger spatial scales. Of the many potential environmental cues that have attracted attention of ecologists, two physical cues have been considered; water temperature and physical structure. Using a clever combination of both field surveys and laboratory tests of thermal preference, Norris (1963) demonstrated a positive relationship between density of opaleye, Girella nigricans, recruits and increased water temperature in rocky tidepools, and that recently settled opaleye moved to the warmest water temperature available when exposed to a thermal gradient. To determine if settling kelp bass, Paralabrax clathratus, preferred particular macroalgae, Carr (1991) conducted both field and laboratory experiments. He suspended replicate clumps of four common species of macroalgae of comparable volume and at similar depths in the water column and recorded the number of recruits that had settled to each algal species. He found significantly greater densities of settlers on the most structurally complex alga (Sargassum palmeri), but because the frequency of censuses was at intervals of several days, observed patterns confounded settlement with post-settlement survival. In the laboratory, recently settled kelp bass (9–14 mm TL) were released into large tanks (3 m3) with discrete clumps of four species of macroalgae and the initial choice and percent of time spent among algal species were recorded. He did not detect preferences (initial choice or percent time) among the different algae, but all four algae were structurally complex, and all individuals associated immediately and consistently with algal structure rather than open portions of the tank. Recruitment of bluebanded gobies (Lythrypnus dalli) increased with experimentally manipulated densities of shelter holes (Berhents, 1987; Steele, 1999) and sea urchins (Hartney and Grorud, 2002). Because this relationship existed even when predators were excluded from reefs, Steele suggested that this response might reflect behavioral preferences for shelter at or soon after settlement. The ability of structural collectors and drift macroalgae to accumulate larvae and pelagic juveniles attests to the strong affinity settling fishes have for physical structure (Kingsford, 1993). The behavioral response of competent (i.e., ready to settle) larvae and pelagic juveniles at settlement, either in the form of attraction to or avoidance of conspecifics, or avoidance of potential competitors and predators, has received increasing attention from coral reef fish ecologists (e.g., Sweatman, 1983; Booth, 1992; Almany, 2002), but tests of this behavior for

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temperate reef fishes are rare. This is surprising, given the increasing evidence from coral reef systems of both strong positive and negative effects of conspecifics, and the large number of temperate species whose recent settlers form dense aggregations (e.g., Chromis punctipinnis, Heterostichus rostratus, many species of Sebastes). Steele (1997a) found that recruitment of bluebanded gobies (Lythrypnus dalli) was greater in the presence of adults compared to similar habitats from which he had removed adults. This difference may reflect settlement facilitated by larvae responding to adult cues. In contrast, similar comparisons of recruitment of blackeye gobies (Rhinogobiops nicholsii) were equivocal, and suggested that resident adults were more likely to have a negative effect on recruitment (Steele, 1997a). For both species, no effect of the density of adults on recruitment of the other species was detected. The exclusion of predators also increased the density of L. dalli recruits (but not R. nicholsii) but because post-settlement mortality occurs quickly and is density-dependent (Steele, 1997b), it is difficult to decouple any of these potential settlement effects from post-settlement losses attributable to predation. Responses to cues provided by prey have not been examined either. Such cues may be directly associated with prey species themselves, or indirectly, associated with habitat attributes that are correlated with prey availability (e.g., water flow for planktivores, macroalgal or other substrate types for epibenthic prey). Although the effects of predators both as settlement cues (to avoid) and especially as sources of post-settlement mortality have received increasing attention, their role in inflicting mortality during settlement has received less attention. The great potential of planktivorous fishes and some invertebrates (e.g., anemones) to prevent successful settlement is clear from the diversity and abundance of temperate planktivorous fishes (Ebeling and Bray, 1976; Hobson and Chess, 1976, 1986, 2001). The few studies that have compared zooplankton density up current and down current of planktivores (Bray, 1981; Gaines and Roughgarden, 1987; Kingsford and McDiarmid, 1988) suggest that they can strongly alter plankton density. Such studies have mostly examined diurnal planktivores whose effects on larvae that arrive to reefs at night, especially ichthyoplankton, are less clear. Only one study, conducted on coral reefs, has begun to look at rates of predation during settlement at night and concluded that it can be high (Holbrook and Schmitt, 1997). This rapid effect of predators on settlement patterns is suggested by studies documenting very early (i.e., within 24 hr.) post-settlement mortality (Steele and Forester, 2002).

Post-settlement Phase: Benthic Processes that Contribute to Patterns of Recruitment Ecological processes that occur subsequent to settlement to the benthic environment can act to reinforce, alter, or entirely mask patterns of recruitment created in the pre-settlement and settlement phases. Thus, understanding how and under what conditions post-settlement processes have such effects is critical to understanding the relative importance of each phase of the recruitment process. Three ecological processes that occur subsequent to settlement can have pronounced effects alter patterns of larval settlement—movement, growth and mortality. P OST-S ET TLE M E NT MOVE M E NT

The extent to which fish move subsequent to settling to a benthic habitat varies greatly among species. Extremes vary from

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those species that appear to establish life-long territories on the order of meters at settlement, to the many species that settle into coastal or estuarine nursery habitats and migrate 10s to 100s of kilometers to adult populations offshore (Love et al., 1991; Gillanders et al., 2003). For example, recruitment (very likely reflecting patterns of settlement) of many rockfishes (genus Sebastes) occurs at depths shallower than those typically occupied by their adults (Boehlert, 1977; Love et al., 1991). For those species that move substantial distances between nursery and adult habitats, individuals essentially recruit to populations associated with each habitat type and the duration that individuals inhabit nursery or transition habitats or migrate between habitats varies on the order of days to years (Gillanders et al., 2003). For such species that recruit to a variety of habitats between initial settlement and recruitment to the adult population, understanding the consequences of habitat use and the relative contribution of different juvenile habitats to individual growth and survival are fundamental to understanding the overall structure and dynamics of a population (Beck et al., 2001). For example, although recently settled California halibut, Paralichthys californicus, in southern California occur in shallow sand bottom habitats along the open coast, the vast majority appear to occur within estuarine and lagoonal embayments, and those that settle on the open coast migrate to embayments (Plummer et al., 1983; Allen, 1988; Allen and Herbinson, 1990; Kramer, 1991). Although recently settled individuals exhibit little difference in growth rates between the open coast and embayments, mortality from predation appears to be lower for those that recruit to estuarine habitat and older juveniles may grow faster there (Kramer, 1991). The higher productivity and water temperature in embayments may enhance juvenile growth, while vegetation and lower predator densities may enhance survival, both bearing on the eventual contribution to recruitment to offshore adult populations. Temperature related sizespecific differences in growth efficiency can explain not only the advantages to smaller fish of inhabiting warmer embayments, but also why older fish move to cooler water as they grow (Boehlert and Yoklavich, 1983). For species that tend to remain in the habitat to which they settle, the presence of conspecifics and other species may influence post-settlement movement. One example of interspecific effects is the greater rate of post-settlement emigration of recruits of one tide pool sculpin, Clinocottus embryum, in the presence of recruits of another, C. globiceps (Pfister, 1995). Moreover, for both of these species the per capita rate of emigration from tide pools was related to the density of conspecifics (Pfister, 1996). Although territorial gopher (Sebastes carnatus) and black and yellow (S. chrysomelas) rockfishes appear to tolerate the presence of recently settled juveniles of either species, with increasing size and competitive interaction recruits eventually emigrate from established territories (Larson, 1980a,b). The greater larval recruitment of painted greenling, Oxylebius pictus, in areas where territorial adults were experimental reduced relative to unmanipulated controls may reflect post-settlement movement in response to adults (DeMartini, 1976). For species whose young recruit in greater density in the presence of algal structure, affinity for this structure declines with fish size and is manifested by more equitable densities of older size classes among algal habitats, presumably reflecting post-settlement movement (Ebeling and Laur, 1985; Holbrook and Schmitt, 1984; Holbrook et al., 1990a; Carr, 1989, 1991, 1994a; Anderson, 1994). Thus, local patterns of settlement can be modified by post-settlement

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emigration in response to a variety of environmental features, including interspecific interactions with competitors and predators.

factors that influence growth also influence survivorship, including seasonal variation in settlement (Pfister, 1997). DE N S IT Y-DE P E N DE NCE

P OST-S ET TLE M E NT G R OW TH

Variation in growth subsequent to settlement is ultimately manifested as an individual’s longevity or cohort’s rate of mortality and/or future reproductive contribution, including susceptibility to disease. Post-settlement growth rates are influenced directly by such variables as quality (i.e., species composition, size and condition), quantity (i.e. density and abundance) and availability (distribution and susceptibility) of prey, temperature, and water flow (the energetic cost of searching or maintaining position to feed) as well as indirect effects of intra- and interspecific competitors and predators (e.g., interference or risk). Because these variables vary temporally, timing of recruitment can also influence post-settlement growth, survivorship and rate of maturity (Pfister, 1997). Moreover, there is some suggestion that condition of larvae at the time of settlement may influence their post-settlement growth performance. Early juvenile growth can vary markedly and in response to food limitation, even for temperate planktivorous fishes (e.g., Schmitt and Holbrook, 1990; Love et al., 1991; Woodbury and Ralston, 1991; Sogard, 1992; Anderson and Sabado, 1995; Levin, 1994b; Levin et al., 1997). The few studies of temperate fishes that have examined effects of recruit density (Davis and Levin, 2002) and older residents (Steele, 1997a, 1998; Szabo, 2002) on early post-settlement growth or competition for food have found negative effects of conspecific density. Ultimately, these effects on growth can prolong the period that young fish are susceptible to predation and influence the size of a cohort’s contribution to the structure and growth of a population (Pfister, 1997; Sogard, 1997; Davis and Levin, 2002). P OST-S ET TLE M E NT MORTALIT Y

The importance of post-settlement mortality either as a source of recruitment variation or density-dependent amelioration of such variation, has become a topic of intense interest. Post-settlement modification or dampening of variable larval supply can have strong effects on subsequent population structure and dynamics (Shulman and Ogden, 1987; Sissenwine, 1984; Rothschild, 1986; Holm, 1990; Levin, 1998; Warner and Hughes, 1988; Caley et al., 1996; Forrester et al., 2002; Hixon and Webster, 2002). Post-settlement mortality of temperate fishes can be high and most observational studies documenting this mortality have suggested predation as the cause (Lockwood, 1980; Hallacher and Roberts, 1985; Myers and Cadigan, 1993b; Bailey, 1994; Adams and Howard, 1996; Hobson et al., 2001). Based on a rapid growth in experimental studies over the past decade, there now exists many examples of the substantive causal effects of predators on the survival of early post-settlement juvenile coral reef fishes (reviewed by Hixon and Webster, 2002), as well as a variety of temperate marine species (DeMartini, 1976; Carr, 1991; Steele, 1997a, 1997b; Berhents, 1987; Levin et al., 1997; Steele et al., 1998; Anderson, 2001; Steele and Forrester, 2002; see chapter 16). Environmental disturbance, such as storms and episodes of hypoxia, can also induce substantial post-settlement mortality (Hobson and Howard, 1989; Breitburg, 1992, respectively) and these environmental factors can interact with rates of predation (Breitburg et al., 1994). Because susceptibility is strongly size-dependent,

The extent to which per-capita rates of movement, growth or mortality are dependent on the density of recruits or resident conspecifics can vary substantially in space and time. If such post-settlement or post-recruitment processes are sufficiently strong and density-dependent, much of the effect of variation in larval supply and settlement on population size, growth rate and reproductive potential can be greatly dampened. Because this topic is treated in greater depth by Steele and Anderson (chapter 16), we mention it briefly as it relates to the greater recruitment process. A growing number of studies examining post-settlement mortality provide increasing evidence that the per capita rate of mortality of demersal fishes can be strongly density-dependent (see recent reviews by Hixon and Webster, 2002; Osenberg et al., 2002; Steele and Anderson, chapter 16). Evidence of this density-dependent post-settlement mortality for temperate fishes comes from three sources: 1) observations of strong positive spatial or temporal relationships between the magnitude of recruitment and limiting resources (especially refuge from predation), 2) observational tests of the relationship between the size of recruiting cohorts and their per-capita rate of mortality, and 3) experimental tests of the effect of density on per-capita mortality of recruiting cohorts. One example of the first case is the strong relationship between recruitment of recently settled kelp bass, Paralabrax clathratus, and plots of manipulated densities of the giant kelp, Macrocystis pyrifera (Carr, 1994a). The positive relationship generated across interspersed replicate kelp density plots suggest that under comparable levels of larval supply, settlers or recruits experienced density-dependent mortality, limiting their eventual numbers to the availability of refuge from predation. Thus, the many examples of positive relationships between recruitment and recruitment habitat such as shelter holes (Berhents, 1987; Steele, 1999) may reflect density-dependent mortality set by the availability of limiting resources. However, as in the case of the kelp bass-giant kelp example, this indirect evidence does not distinguish postsettlement mortality from differential settlement related to encounter rates of larvae with increasing density of plants. Hence, observations of actual rates of per-capita mortality provide stronger evidence for density-dependent mortality. With few exceptions (Tupper and Boutilier, 1995; Sano, 1997; Pfister, 1996; Davis and Levin, 2002), the majority of observational studies of post-settlement density dependence come from the fisheries literature (e.g., Lockwood, 1980; Myers and Cadigan, 1993b; Adams and Howard, 1996). These studies document the occurrence of early post-settlement densitydependent mortality at broader spatial and temporal scales than can be examined experimentally. Only a handful of these observational studies have been conducted for California fishes. Adams and Howard (1996) detected significant positive interannual relationships between the strength of recruitment of blue rockfish, Sebastes mystinus, to kelp forests along northern California and rates of cohort mortality. In contrast, a 4-year study of recruitment and population dynamics of an intertidal sculpin along the coast of southern California found that early post-settlement mortality rates were density-independent (Davis and Levin, 2002). Similarly, Pfister (1996) found that early post-settlement survival of three species of intertidal sculpins at sites along the coast of Washington State was largely

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density-independent, resulting in positive relationships between the total number of recruits in the summer and number of adults the following winter for two of the three species. Recruitment events could be detected in adult populations for short periods of time. Post-recruitment survivorship, however, dampened seasonal recruitment pulses and adult population growth rates were more sensitive to post-recruitment processes. Such observational studies have motivated experimental assessments of post-settlement density-dependent mortality. In a series of experiments examining the relative contributions of larval supply and post-settlement predation and competition for two species of gobies at Santa Catalina Island, Steele (1997a,b, 1999) Steele et al. (1998), and Steele and Forrester (2002) concluded that variable post-settlement mortality of Lythrypnus dalli and Rhinogobiops nicholsii caused by predation was very strong and occurred very quickly (e.g., 92% mortality within 24 hr of settlement for C. nicholsii) and was sufficiently density-dependent to greatly obscure patterns of larval supply and settlement. However when these effects, detected at spatial scales of tens of meters, were examined at larger spatial scales (100s–1000s of meters) patterns of recruitment were still related to larger-scale variation in larval supply and settlement. This observation underscores the importance of examining the relative roles of pre- and post-settlement processes with a combination of observational studies at broader spatial and temporal scales and experimental tests at smaller spatial scales to elucidate the actual mechanisms and sources of variation in density dependence. Another elegant example of experimental evaluation of density dependence is Anderson’s (2001) manipulations of the density of young kelp perch, Brachyistius frenatus, in the presence and absence of predators. This work demonstrated that the post-parturition density-dependent mortality experienced by young kelp perch was a result of combined functional and aggregative responses of its primary predator, the kelp bass. To determine if the presence and strength of density-dependence varied as a function of habitat complexity, recruit density was manipulated across a range of habitat complexity. This experiment demonstrated that the direction (positive or negative), presence and magnitude of density dependence are strongly influenced by structural complexity of the habitat (e.g., kelp). Surveys of per-capita mortality of kelp perch occurring at a range of densities across reefs at Santa Catalina Island demonstrated patterns concordant with the density-dependent mortality detected in the experiments. This work demonstrates the broader implications of variation in habitat attributes as they influence postsettlement processes that contribute to density-dependence (e.g., predator and refuge abundance), and more generally as sources of variation in recruitment. Intra- and interspecific interactions (competition, predation, facilitation) interact with habitat features (e.g., shelter availability) to increase the complexity and variability in how either habitat or species interactions influence recruitment. For example, Behrents (1987) sampled recruitment of bluebanded gobies, Lythrypnus dalli, to artificial habitats on which she orthogonally manipulated the presence/absence of conspecific adults and small shelter holes for recruits. In the absence of small shelter holes, the presence of adults reduced larval recruitment, while in the presence of small shelter holes, there was no effect of adults on recruitment. Moreover, this effect of adult conspecifics was opposite to the effect of enhanced recruitment that Steele (1997a,b) detected (see Settlement phase section above). The different effects do not seem to be attributable to differences in the presence of predators (Steele,

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1997a,b) and exemplify the complexity of these interactions. Another source of complexity is the role of macroalgae and other biogenic sources of habitat structure in moderating species interactions in temperate systems. These sources of habitat structure provide young fish with refuge from predation as well as modify the abundance and availability of their prey. Macroalgal assemblages are highly variable in space and time and these changes create a variable environment within which species interactions take place. Understanding how post-settlement interactions vary in response to these changing conditions is critical to understanding spatial and temporal patterns of recruitment (Holbrook et al, 1990b; Schmitt and Holbrook, 1990; Levin, 1993; Carr, 1994a,b; Anderson, 2001).

Implications of Recruitment for the Management and Conservation of Marine Fishes Our understanding of the causes and consequences of the variable replenishment of fish populations underpins all past and current approaches to managing and conserving these species as well as the ecosystems that support them. The importance of variable recruitment to the dynamics and management of marine fisheries has been recognized since the dawn of fisheries science. It has been both the Holy Grail that fisheries scientists have endeavored to understand or predict, as well as a bane of their ability to accurately forecast population dynamics. As a fundamental source of uncertainty, it has often impeded traditional management approaches based upon stock-recruitment relationships. While this uncertainty has compelled scientists and managers to consider additional approaches to complement traditional management (e.g., hatcheries, marine reserves), recruitment remains a critical consideration for the potential contribution and uncertainty of these schemes as well. The temporally variable, often episodic, recruitment of marine fishes influences the frequency at which populations are replenished. The availability of adults to produce potential recruits during such windows of favorable recruitment conditions is critical to the persistence of a population. This storage effect (sensu Warner and Chesson, 1985) implies that reducing the longevity of adults to durations less than intervals between successful recruitment events can jeopardize the persistence of a population. Similarly, if some level of larval production and recruitment is necessary to maintain populations through periods detrimental to their maintenance (e.g., detrimental climatic regimes), additional fishing mortality during such periods may incapacitate buffers in population size critical to larval production. Thus, identifying the temporal patterns of recruitment and the environmental processes that explain those patterns is critical to understanding and predicting the temporally variable effects of reducing the age and number of adults incurred from fishing mortality. Temporal patterns of recruitment also inform mangers of the relative consequences of fishing mortality during periods of differing rates of replenishment. Reducing rates of fishing mortality during prolonged periods of reduced rates of recruitment may be necessary to maintain stocks at levels capable of rebounding with the return of environmental conditions favorable for recruitment. The spatial scale of larval dispersal and recruitment sets the scale of influence of a population and, by extension, can determine the spatial scope of human impacts. Local extirpation of adults can act both to preempt recruitment to populations elsewhere, and, to the extent that local recruitment is influenced by the presence of adults, prevent replenishment

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of that local population where adult density has been altered (Raimondi and Reed, 1996). Similarly, localized human activities that alter the dispersal patterns or survival of fish larvae as they encounter altered environments can have regional impacts well down current of such activities (Kingsford and Gray, 1996; Nisbet et al., 1996). Examples include the potential entrainment of larvae by power plants, or discharge plumes of altered salinity, temperature, turbidity, or toxicants. Thus, knowledge of the processes that determine dispersal and the relationships between larval production, survival and recruitment are critical to understanding and predicting the scale and magnitude of human impacts on these three processes. The spatial scale of dispersal and recruitment also sets the spatial scale at which populations interact with one another. As such, dispersal and recruitment are fundamental to the purpose, design and evaluation of spatially explicit management approaches such as marine reserves. Several studies have discussed the implications of larval dispersal for the potential role of marine reserves as sources of replenishment of exploited populations and the importance of dispersal distance for the design (size, spacing and location) of reserve networks (Plan Development Team, 1990; Carr and Reed, 1993; Roberts, 1997; Planes et al., 2000; NRC, 2001, contributions in volume S13 of Ecological Applications, 2003). The extent to which larval retention enhances local recruitment determines the extent to which populations within reserves are self-replenishing. Alternatively, the apparent reliance of local populations on larval transmission among populations (i.e., connectivity) is the basis for the necessity of reserve networks. With better understanding of dispersal processes, we are more likely to design true networks of reserves whose replenishment and sustainability are independent of less protected populations outside reserves. Spatial patterns of larval production, dispersal and population connectivity also determine the relative contribution of local populations to the replenishment and persistence of broader regional populations that constitute metapopulations or exploited stocks. Knowledge of such contributions, measured as per-capita survival, larval production, dispersal and realized recruitment to the regional population, identifies potential source and sink populations. Identification of such populations can be useful for targeting populations for protection in reserves or for predicting or assessing the potential or realized benefit of artificial reefs for augmenting regional fish populations or mitigating for habitat loss (Carr and Hixon, 1997; Grossman et al., 1997; Holbrook et al., 2000). The degree to which density-dependent post-settlement processes (e.g., competition, predation) and resource limitation determine recruitment to a fishery or an adult population will greatly influence the potential value of propagation (e.g., hatcheries) and habitat enhancement (e.g., restoration and artificial reefs) for augmenting populations. Thus, knowledge of the relative contributions (and constraints) of each phase of the recruitment process (production, pelagic survival and dispersal, settlement and post-settlement performance), will inform decisions of alternative or complementary management approaches.

recognition of the necessity to conduct comprehensive studies that examine the entire recruitment process from larval production, supply, through the post-settlement phase to recruitment to the adult population. To date, there are many wellstudied pieces of the puzzle, but they provide an incomplete understanding of the overall recruitment process. Without a more complete picture for a subset of model species representative of key life history traits (e.g., reproductive mode, fecundity, larval duration), our understanding of the relative importance of each phase of the recruitment process and how this varies among oceanographic and other environmental conditions, will continue to impair our ability to predict both recruitment dynamics and its consequence to the structure and dynamics of demersal fish populations and the communities they constitute. Second is the shift from the current focus on single, local populations to multiple regional-scale populations. Included with this broader perspective are explorations of larval dispersal and connectivity among populations. Only through a greater understanding of the spatial scale of dispersal and population interaction and how this varies among species and oceanographic conditions can our science begin to understand how processes acting at the scale of local populations scale-up to regional, metapopulation, scales. Only with this larger scale understanding will we understand processes that contribute to the persistence of both local and regional populations and develop the capacity to inform spatially explicit management and conservation efforts. In order to do this effectively will require the third direction of research; a more interdisciplinary effort that brings to bear the tools and insights of genetic, physiological, oceanographic and other disciplines to address these complex questions. Genetic and chemical signatures and analytical approaches will be required to determine patterns of dispersal and these are being developed rapidly. Concomitant oceanographic studies will be required to interpret dispersal and recruitment patterns generated from the use of such signatures. Multidisciplinary efforts examining processes of dispersal and recruitment in coastal oceans are critical to our understanding of how larger scale processes (e.g., the California Current) interact with coastal processes (e.g., tidal bores, upwelling and its relaxation) to influence recruitment dynamics and population connectivity along the west coast of North America and upwellingdominated ecosystems throughout the world. Finally, there is a need to formally integrate these different levels of inquiry into explanatory and predictive frameworks that relate local scale processes, such as post-settlement density dependence, to regional scale dynamics such as metapopulation structure and persistence. These frameworks need to provide a means by which scientists can both understand the dynamics of fish populations and communities, and provide resource managers with predictions and forecasts about outcome of conservation and management actions. The tremendous research capacity along the West Coast has long been poised to provide models for this type of effort, and recent assessments of fish populations indicate that the need for these kinds of programs is greater now than ever. These are very exciting and important times to pursue such endeavors.

Future Directions

Acknowledgments

Four future research areas, each essentially complementary to the others, emerge from this review of our understanding of fish recruitment and population ecology. First is the growing

We thank Amy Ritter, Margaret McManus and Patrick Drake for thoughtful discussions and for Amy’s assistance in literature searches. Jennifer Caselle, Steve Ralston and one anonymous

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reviewer provided us with helpful input. Jeff Jones created fig. 15-1. Support for both M. Carr and C. Syms for preparation of the chapter was provided in part by the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO), funded by the David and Lucile Packard Foundation. This is PISCO contribution number 127.

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CHAPTER 16

Predation MAR K A. STE E LE AN D TO D D W. AN D E R S O N

Introduction Common sense suggests that predation must play some, probably important, role in the ecology of marine fishes. Many fishes are piscivorous, and virtually all fishes are vulnerable to predation at some point in their lives. Until recently, however, the effects of predation on the ecology of populations and communities of marine fishes were poorly known, although the subject of widespread speculation (Hixon, 1991). A recent spat of experimental work, reviewed in this chapter, has advanced considerably our understanding of the role of predators in the ecology of marine fishes, yet much remains to be done before we have a better sense of the general importance of predation. Coincidentally, much of the recent work on fish predation has been done on California’s temperate reef fishes. To provide context and evaluate the generality of studies from California, we compare this body of work to similar studies conducted elsewhere, mainly on tropical coral reefs. We conclude by highlighting several aspects of predation in particular that are in need of more detailed study. Predation is just one of the many processes (see other chapters in this book) that affects individuals, populations, and communities of marine fishes. Ideally, one would like to know how important these processes are relative to one another (Welden and Slauson, 1986). Are some of them trivial in nature, and therefore better ignored to instead focus our energies and resources on the more important ones? Frankly, there are too few data available to definitively judge the relative importance of predation. Nevertheless, a number of studies tell us that predation should be studied concurrently with other processes (e.g., competition) because of potential interactions, which cause the importance of one process to depend upon the level of another. In this chapter, we focus on field studies to explore the role that predators play in nature. As practicing field ecologists, we believe that such studies, although logistically more challenging, provide the best tools available for exploring the workings of nature. We also discuss laboratory studies that we believe are particularly enlightening and provide insight not available from field studies. There are a number of topics related to predation that we do not discuss in detail, either because they do not provide much insight into the effects of predators or they

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lack a strong empirical basis. For example, we do not cover gut contents studies in detail, certainly the most prevalent form of the study of predation in fishes. These studies, although essential for determining who eats whom and for questions of prey selectivity, often offer little insight into the ecological effects of predators.

Evolutionary Influence of Predation: The Arms Race Anti-predatory Adaptations Being eaten by a predator obviously reduces future reproductive value to zero, hence reducing lifetime fitness. So, it is no surprise that marine fishes have evolved a variety of color patterns, morphological features, and behaviors that reduce their risk of being eaten. These adaptations provide compelling evidence that predation is an important process driving evolutionary change, and they imply that predation is important ecologically to fishes. C OLORATION AN D MOR P HOLO GY

Marine fishes have evolved a wide range of color patterns and morphological specializations that are thought to reduce the risk of predation. Although we are aware of no work that demonstrates the efficacy of these adaptations in fishes of California, we expect that the general effects of anti-predator adaptations of fishes from other regions should be similar to those of fishes in California. Here, we briefly discuss some of the adaptations that reduce the risk of predation in fishes. One of the most widespread anti-predatory adaptations is crypsis—the use of camouflage—which reduces detection by predators and thus the risk of being eaten. Crypsis in fish can be achieved by color pattern alone or, often, by combining coloration with morphology and behavior. A very common cryptic color pattern in aquatic animals is countershading, in which the upper surface of the body is dark and the lower surface is light. In well-lit surface waters, such coloration blends in with the dark background when viewed from above and the light background when viewed from below. Further, when viewed from the side the well lit but darkly colored dorsum

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and poorly lit but lightly colored ventrum creates the impression of uniform shading that blends in with the background. Most open-water fishes such as the Pacific chub mackerel (Scomber japonicus) are counter-shaded. The California sardine (Sardinops sagax), the northern anchovy (Engraulis mordax), and a number of other species combine counter-shading with highly reflective, mirror-like scales that reflect back ambient light, enhancing their ability to blend with their environment when viewed from the side. Flatfishes match the color of the surrounding substrate and use their unique morphology to conform to or bury within the sea floor, rendering them nearly invisible to both prey and predators. The bay pipefish (Syngnathus leptorhynchus) matches both its shape and color (green to brown) to the eelgrass that it normally inhabits in California’s embayments. That most fishes employ some form of crypsis indicates that it has been a particularly effective evolutionary tactic for evading detection by both predators and prey. The selective pressure of predation also appears to have driven the evolution of physical defenses. For example, many of California’s marine fishes have spines, which are thought to deter predators. The sharp spines (modified fin rays) that are common in the dorsal, pelvic, and anal fins of many teleosts certainly would be unpleasant to swallow; they also increase the effective size of the fish when flared, thus causing gape limitation of predators at smaller prey body sizes. The California scorpionfish (Scorpaena guttata) and many rockfishes (Sebastes spp.) take matters a step further by possessing venomous spines. In addition to fin spines, these scorpaenids also have spiny projections on their heads and opercula. Cartilaginous fishes also make use of spines, as seen in the horn shark (Heterodontus francisci), spiny dogfish (Squalus acanthias), bat ray (Myliobatis californica), and round stingray (Urobatis halleri). The spines of both bat rays and round stingrays are venomous. G ROU P LIVI NG

In addition to morphological defenses and crypsis, many fishes live in groups, which can reduce the risk of predation (Pitcher and Parrish, 1993). There are a variety of benefits that may be accrued from group living (and a number of costs), but foremost among the benefits is reduced risk of predation. The likelihood of being eaten may be reduced in a variety of ways, some of which are particularly effective in a certain type of group: a school. The terms school and shoal are sometimes used interchangeably, but we will follow the strict definitions given for them by Pitcher: A shoal is any group of fish, whereas a school is a special sort of shoal, one in which the orientation of individuals within the group is polarized. That is, they are oriented in the same general direction, maintain relatively uniform spacing, move at the same speed on average, and are of similar size. A number of studies have demonstrated that the presence of predators, or even just their cues (e.g., sounds; Wilson and Dill, 2002), induces schooling in prey fishes (Pitcher and Parrish, 1993). In schools and shoals, the risk of predation may be reduced by three different mechanisms: the dilution effect, enhanced vigilance, and predator confusion. In the case of the dilution effect, the risk of predation that an individual faces is reduced by the presence of other prey (the schoolmates). In the simplest case, if there is one predator that will only capture and eat one prey item, then the risk of predation for a school member is reduced to 1/x, where x is the number of individuals in the school, relative to a solitary prey fish.

Whether the dilution effect actually works in nature depends on the responses of predators to prey density. If predators exhibit density-dependent behavioral responses (functional or aggregative responses, described later in the chapter), then the dilution effect may produce no reduction in risk of predation. For example, if many predators aggregate to large schools of prey and feed on them until the entire school is devoured, a dilution effect is nonexistent. Some predators show a preference for large schools, whereas others prefer small schools. For example, Axelsen et al. (2001) found that Atlantic puffins focused their efforts on large schools of herrings (Clupea harengus) instead of small schools, whereas Nottestad and Axelsen (1999) found that killer whales focused their efforts on small schools of herrings, ignoring larger ones. The difference between the two predator species was likely a result of their very different hunting styles (Axelsen et al., 2001). The implication is that the benefit of associating with a school of a particular size will depend upon the foraging tactics of the predators encountered. Enhanced vigilance and predator confusion are more likely to consistently benefit schooling fishes. Schools are more vigilant than individuals because there are more sensory systems (eyes, inner ears, lateral lines, etc.) available to detect predators. Thus, larger groups of fish detect predators at greater distances than smaller groups or individuals (Pitcher and Parrish, 1993). This early detection capability allows individuals within schools to initiate anti-predator behaviors earlier than solitary individuals. The predator-confusion effect occurs because it is very difficult to focus on an individual within a school, and this is usually necessary to capture prey. A variety of studies have shown that with an increase in school size, capture rate per strike declines (Pitcher and Parrish, 1993), presumably because of the confusion effect. Moreover, a common response of schooling fishes is to reduce the inter-individual spacing within the school when faced by predators (e.g., Nottestad and Axelsen, 1999), making a very compact school in which it is even more difficult to single out individuals. Some predators have altered their hunting tactics in ways that overcome the predatorconfusion tactic. For example, killer whales slap their flukes, which stun schooled prey, billfishes slash their bills as they pass through schools of prey, which injures or kills the prey, and some predatory species switch to ram feeding and simply swim through dense schools at high speeds with their mouths open. There are potential costs to group living (schooling and shoaling), including increased risk of detection by predators, increased rates of disease transmission, and competition for resources. Little evidence of increased rates of disease transmission has been found in groups of reef fishes. There is some evidence that large groups attract more predators than do small groups (see Webster, 2003 for an example involving a coral-reef fish). There is widespread suggestive evidence that competition for food occurs in dense groups of both temperate (reviewed in chapter 17) and tropical reef fishes (Jones, 1991), but definitive tests showing that density dependence is eliminated by enhancing food abundance have not been made to our knowledge. Two recent studies on coral-reef fishes, however, have clearly shown that large groups suffer higher mortality than small groups when shelter space is limited. Holbrook and Schmitt (2002) found that dense populations of an anemonefish (Pomacentridae) suffered greater rates of mortality than sparse ones because of interference competition, in which dominant, aggressive individuals forced less aggressive

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individuals from the safe central zone of the anemone into the dangerous periphery or away from the anemone. The displaced individuals were then eaten, mainly by a suite of nocturnal predators. Studying a coral-reef goby, Forrester and Steele (2004) found that individuals in large groups died (due to predation) at higher rates than individuals in small groups in areas lacking abundant shelter, but in areas with abundant shelter, group size (density) did not affect mortality rate. B E HAVI O R A L R E S P ON S E S

Many fishes alter their behavior when predators are near, thereby reducing their risk of being eaten. These behavioral changes typically reduce the risk of being detected by predators, reduce the probability of encountering a predator, or reduce the probability of capture once detected. Although schooling behavior can be induced or enhanced by the presence of predators, the most common behavioral responses of prey to predators are to reduce the rate of movement or move to a safer microhabitat. Typically, these behavioral changes come at the cost of reduced foraging success for the prey, and the trade-off between foraging success and risk of predation has been studied in detail, often in the context of optimal foraging theory and usually in the laboratory (Lima and Dill, 1990). Schmitt and Holbrook (Schmitt and Holbrook, 1985; Holbrook and Schmitt, 1988a,b) explored the combined effects of predators and food availability on the behavior of juvenile black perch (Embiotoca jacksoni; Embiotocidae) (fig. 16-1) in a series of lab and field studies done at Santa Catalina Island. In a field experiment conducted in a large (50 m2 ) enclosure, they (Schmitt and Holbrook, 1985; Holbrook and Schmitt, 1988a) manipulated the presence of the primary piscivorous predator at Catalina Island, the kelp bass, Paralabrax clathratus (Serranidae) (fig. 16-1). Kelp bass were either present or absent, and when present they were kept from eating young-of-year black perch by placing them in plastic mesh tubes. Within the enclosures, a natural array of microhabitats that differed in both prey (crustacean) abundance and suitability as shelter from predators was present. Prey abundance and shelter quality did not covary. The rate of foraging, duration of foraging bouts, number of visits, and time spent in each microhabitat were recorded during replicate trials. The general effect of the predator on microhabitat choice was to weaken the strength of the preference of black perch for microhabitats that contained high densities of crustacean prey. The details of the changes in microhabitat use in this study are informative. Phyllospadix torreyi, a vascular plant, provided the highest quality shelter, but harbored very few crustacean prey. This microhabitat was seldom used in the absence of predators and the presence of predators did not cause any increase in its use. Apparently, a high rate of food intake, which could not be obtained in this prey-poor microhabitat, was valued too highly to make use of it. Instead, black perch switched from using the alga Zonaria farlowii as the favored microhabitat when predators were absent to using the algae Cystoseira sp. and Sargassum palmeri when predators were present. All three algae contained similar densities of crustacean prey, but Zonaria is shorter and has less finely divided blades than the other two species. This structural difference likely makes Zonaria an easier substrate from which to harvest prey, but also makes it less suitable as shelter from predators. The amount of time spent in the Sargassum/Cystoseira microhabitats increased when predators were present because the black perch would visit them more often and spend more time per

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visit there, consequently taking more bites per visit. Also, black perch would move among microhabitat patches less frequently when predators were present than absent, presumably reducing their risk of detection by predators. Further, the effect of predators on microhabitat choice was greatest at dusk, when risk of predation by many piscivores, including kelp bass, is thought to be highest (e.g., Hobson, 1965, 1972). These findings were further supported by supplemental laboratory experiments in mesocosms, which also evaluated whether black perch could distinguish a predatory species from a non-predatory species and between two different species of predators (Schmitt and Holbrook, 1985; Holbrook and Schmitt, 1988a). The young black perch easily distinguished the nonpredatory species, the giant kelp fish, Heterostichus rostratus (Clinidae) (fig. 16-1), which is somewhat similar in size, shape, and color pattern to the predatory kelp bass but does not prey upon black perch (Schmitt and Holbrook, 1985). The general reaction of black perch to predators was to move slowly away while continuing to forage. There was no difference between the reaction to another predatory species, the grass rockfish (Sebastes rastrelliger; Scorpaenidae), and the kelp bass (Holbrook and Schmitt, 1988a). This result is somewhat surprising because grass rockfish are encountered by black perch much less frequently than kelp bass because they are much less abundant, cryptic, and nocturnal, whereas kelp bass are abundant and active during diurnal and crepuscular periods, when black perch are active. In these studies, food abundance (crustacean density) was allowed to vary naturally. In a later study done in laboratory mesocosms, Holbrook and Schmitt (1988b) manipulated food abundance and predator presence while holding habitat structure constant by using only one species of alga. Predators (kelp bass) were again placed in plastic mesh tubes to keep them from consuming the young black perch. When predators were present at all food patches, the preference of black perch for high-food-density patches was reduced relative to when predators were absent at all patches. In other words, black perch were less selective in foraging. The black perch were most selective when predator presence and food availability were manipulated concurrently so that choices could now be made between low-food-density patches with predators and highfood-density patches without predators. Not surprisingly, the majority of black perch were found in patches with abundant food and no predators. Interestingly, black perch did not respond to predators by reducing their rate of foraging when predators were present: in all treatments, the rate of foraging was the same. In the field, however, the presence of predators did reduce the rate of foraging by black perch by about 28% (Schmitt and Holbrook, 1985; Holbrook and Schmitt, 1988a), so it appears that the laboratory finding of no effect of predators on foraging rate cannot be extrapolated to the field. Overall, Holbrook and Schmitt (1988b) suggested that the flexible responses of black perch (e.g., more selective in some situations and less selective in others) have evolved to allow the latitude necessary to minimize the lethal and nonlethal effects of predators under the highly variable conditions typically found in nature. The only other studies on the effects of predators on the behavior of California marine fishes were also done at Santa Catalina Island. Steele (1998) explored the effects of predators on the behavior of two small gobies (Gobiidae), the bluebanded goby, Lythrypnus dalli, and the blackeye goby, Rhinogobiops nicholsii (formerly Coryphopterus nicholsii) (fig. 16-1). The study was done on an array of small (1
1 m) artificial reefs built of

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F I G U R E 16-1 Seven California reef fishes for which experimental studies of predation have been conducted: a) black perch, Embiotoca

jacksoni, b) kelp perch, Brachyistius frenatus, c) senorita, Oxyjulis californica, d) giant kelpfish, Heterostichus rostratus, e) blackeye goby, Rhinogobiops nicholsii, f) bluebanded goby, Lythrypnus dalli, and g) kelp bass, Paralabrax clathratus.

rock rubble on a sandy plain, with kelp bass again the most common predator. Smaller numbers of its congener, the barred sand bass (Paralabrax nebulifer), were also present. Observations of prey (goby) behavior were made as time budgets on haphazardly chosen focal individuals and they were divided into two categories: observations made while predators were present or absent. During the observations, divers recorded the number of foraging attempts (bites) and the time spent moving, perching on top of rocks, clinging to the sides of rocks, sitting beside rocks, hiding under rocks, or sitting on the sand away (5 cm) from rocks.

Predators had dramatic effects on the behavior of the two small gobies. The general response of both species to predators was to stop feeding, move less, hide under rocks, and remain motionless (fig. 16-2). The rate of foraging was reduced by 86% in the bluebanded goby and 90% in the blackeye goby in response to predators. These behavioral responses to predators also had effects on the growth rates of the gobies, described later in the chapter. A comparison between the responses of the black perch studied by Holbrook and Schmitt and the gobies studied by Steele offers some insight into the potential causes of differences in

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F I G U R E 16-2 The effects of predators on the behavior of blue-

banded and blackeye gobies. Data are from time budgets of focal individuals. Shown are means and standard errors. Significant differences (based on t-tests) are denoted by asterisks (from Steele 1998 with kind permission of Springer Science and Business Media).

behavioral responses to predators among prey species. In the field, all three species responded to predators by decreasing their foraging rates. The two gobies, however, reduced their rates of foraging much more dramatically than the black perch, essentially ceasing foraging, whereas the black perch continued to forage, albeit at about 72% of the rate when predators were absent. Moreover, the gobies generally ceased moving and hid under rocks when predators were present, whereas the black perch continued to move about and forage. We suspect these differences stem from differences in the risk of predation faced by the three species. Black perch grow much larger than either of the goby species, and even the young-of-year black perch used in Holbrook and Schmitt’s studies were larger than all of the bluebanded gobies and most of the blackeye gobies studied by Steele. Since piscivores are generally gape limited, it seems likely that the two gobies, by virtue of their smaller size, faced greater risk of predation, and therefore exhibited more extreme behavioral responses to predators. Like the study by Steele (1998), a study by Hastings (1991) in the Gulf of California revealed that signal blennies (Emblemaria hypacanthus) at a site where predators were abundant spent more of their time in shelters and reduced their movement relative to blennies at a site with fewer predators. This study also showed than male blennies courted females less vigorously and with less intense courtship coloration at the site with more predators.

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F I G U R E 16-3 A diagrammatic representation of the cooperative forag-

ing sequence of yellowtail hunting jack mackerel at Santa Catalina Island. The emergent cliff face is on the top left. a) Yellowtail aligned along the seaward flank of the prey school. Leading predators have begun to turn into the prey. b) After splitting a small group of jack mackerel from the main school, yellowtail have fanned into a crescent formation to herd the prey shoreward. c) The prey, pressed against the shore in shallow water, form a dense aggregation. Yellowtail surround the prey and orient toward the group. d) A single yellowtail rushes through the tight prey aggregation, scattering the jack mackerel in a radiating fashion (after Schmitt and Strand, 1982).

Adaptations of Predators Just as natural selection should favor prey that are better at avoiding predation, predators that are better at catching their prey should also have a selective advantage. Many of the adaptations that are used by prey in avoiding detection by predators should be equally effective at allowing predators to avoid detection by their prey. For example, the counter-shading and silvery scales of white seabass (Atractoscion nobilis; Sciaenidae) likely render them more difficult for their piscine and cephalopod prey to detect. Similarly, the California halibut (Paralichthys californicus; Paralichthyidae), an ambush predator, surely benefits from the crypsis provided by matching the color of and burying into the substrate, remaining motionless until small prey fish swim in close proximity. Other adaptations that increase success of predators have been noted in fishes found in California waters. Schmitt and Strand (1982) observed yellowtail (Seriola lalandi; Carangidae) using an organized, cooperative hunting behavior when attacking schools of smaller fish, which allowed them to overwhelm the defenses of their prey (fig. 16-3). The billfishes

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F I G U R E 16-4 Prey capture at night by the Pacific electric ray. a) A female ray presented a reef fish while swimming above the reef.

b) Posture of an electric ray after lunging on a prey fish. c) A ray near the completion of a forward somersault. The prey has been positioned near the mouth by peristalsis-like foldings of the disk. d) Prey being swallowed headfirst, while the disk is still folded. e) A stunned jack mackerel partially enveloped in the disk of an upside-down electric ray. f) The same ray as in (e) at the completion of the somersault. The prey is now near the mouth while fully enveloped by the disk. These rays are about 750 mm long (from Bray and Hixon 1978, with permission from the American Association for the Advancement of Science).

(in California waters, mainly the striped marlin, Tetrapturus audax [Istiophoridae] and the swordfish, Xiphias gladius [Xiphiidae]) stun or kill their prey with their bills before returning and consuming them. Bray and Hixon (1978) described the predatory behavior of the Pacific electric ray (Torpedo californica), which generates a shock with electric organs. After stunning its prey, this nocturnal predator envelops it by folding its disk and maneuvering it towards its mouth (fig. 16-4). Bray

and Hixon suggested that the Pacific electric ray might be a major nocturnal predator of temperate reef fishes. As similarly concluded by Hixon (1991) for coral-reef fishes, the ubiquity of adaptations in prey that reduce predation and in predators that enhance prey capture provides compelling circumstantial evidence that predation has been a key force driving the evolution (see chapter 3) and ecology of marine fishes of California.

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Effects of Predators on Prey Demography and Population Dynamics Fluctuations in demographic rates cause populations to vary in size. Since Hjort’s (1914) early observations that age-classes of fishes vary tremendously in abundance, fisheries biologists and fish ecologists have sought to understand what causes populations of marine fishes to vary in abundance over time. Predators may play an important role in generating dynamics in populations of their prey because they can affect prey demographic rates in a variety of ways. Moreover, predatory effects on prey populations may ultimately alter community and ecosystem structure. Interest in predation, particularly in the fisheries literature, has been focused mainly on predators as consumers, and hence, has examined effects of predators on rates of mortality. Predators, however, can also influence other demographic rates such as growth and fecundity via effects on prey behavior or population density, which can dramatically impact prey populations (e.g., Werner and Gilliam, 1994). Exposure to predators can even modify the morphology of their prey (e.g., Bronmark and Miner, 1992) and alter competitive interactions among prey (e.g., Paine, 1966). In this section, we first discuss the effects of predators on growth, a demographic rate that can strongly influence population dynamics, but one that has received disproportionately little study in marine fishes. We then discuss the impacts of predators on settlement and recruitment of fishes, followed by the effects of predators on fish mortality.

Growth Typically researchers study the lethal effects of predators on their prey. Predators, however, also have important nonlethal (“sublethal”) effects. In the previous section, we discussed behavioral responses of prey to predators, one type of nonlethal effect of predators. By altering prey behavior, predators can influence their rate of food intake, thus affecting growth rates (e.g., Steele, 1998). Predators can also alter competitive interactions by reducing the density of their prey (prey thinning), thus alleviating competition for limited resources and enhancing growth rates of the remaining prey. Hence, predators can have both negative and positive effects on the growth rates of their prey, depending upon the mechanism involved: suppression of foraging or thinning of populations, respectively. Nonlethal effects of predators on the growth of their prey matter primarily because body size strongly influences many demographic rates and biological processes (Werner and Gilliam, 1984). The importance of growth is exaggerated in fish relative to many other organisms because it is extremely labile and continues throughout life. Maturity in fishes typically is more closely related to size than to age, and once mature, body size has a dramatic influence on reproductive output (Bagenal, 1978; Wootton, 1979; Werner and Gilliam, 1984). Additionally, because the risk of mortality in fishes may decline with size (Sogard, 1997), any factor that influences growth rates may indirectly influence mortality. Moreover, many fishes change gender during their lifetime and the timing of sex change is often influenced by relative or absolute size. Consequently, factors that influence growth rates may affect the sex ratios of populations and thus their reproductive output (Sadovy, 1996). Overall, effects of predators on the

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growth of their prey may have important consequences for prey population dynamics. Few studies, however, have examined nonlethal effects of predators, especially in marine systems (for rare examples see Connell, 1998; Steele, 1998; Nakaoka, 2000; Steele and Forrester, 2002a). Some of these studies, however, focused on marine fishes in California. Steele (1998) and Steele and Forrester (2002a) examined the effects of predators on the growth of bluebanded and blackeye gobies at Santa Catalina Island, where the main predator of these two species is the kelp bass. In the 1998 study, Steele explored the effects of predators on the growth of the two gobies on an array of 1
1 m artificial patch reefs built of rock rubble. Half of the reefs were enclosed in cages that excluded predators, and the other half were enclosed in partial cages that gave predators access to the reefs. Densities of the gobies were also concurrently manipulated. Predators had different effects on the growth of the two gobies during this experiment. Bluebanded gobies grew more slowly on reefs exposed to predators than on reefs free of predators (fig. 16-5), but exposure to predators had little effect on blackeye gobies. Both species foraged at lower rates on reefs exposed to predators, so one might predict that they both would grow at slower rates on reefs with predator access. The proximate explanation for the difference between the two gobies is that the rate of growth in bluebanded gobies was related to their rate of foraging, but there was no such relationship in blackeye gobies. Why there was no relationship between foraging rate and growth rate in blackeye gobies is unknown. In the later study, Steele and Forrester (2002a) found that predators caused blackeye gobies to grow more slowly during some periods but not others (fig. 16-5). This work was done at the same site and also used cages to manipulate the presence of predators. In two of three months studied, blackeye gobies on reefs exposed to predators (uncaged reefs) grew more slowly than those protected from predators. Population density also had a negative effect on goby growth rate, but this effect was independent of the predatory effect (i.e., the two processes did not interact statistically). The effects of predators on growth of the gobies declined from summer to winter, from relatively large effects to no effects, and this pattern mirrored a typical seasonal decline in predator abundance from summer to fall as kelp bass moved to deeper areas away from the reefs that the gobies inhabited. The authors speculated that nonlethal effects of predators on growth of their prey might normally be seasonal. If predators suppress foraging and thus growth of their prey, and concurrently thin dense populations of competing individuals by eating them, they will have both positive and negative effects on prey growth. It is possible that these opposing effects of predators may balance so that there is no net effect of predators on the growth of their prey, but it is unlikely that these effects will exactly balance one another. Which effect will dominate can be determined graphically (fig. 16-5). For both species, the negative effect of predators on growth outweighed their positive effect mediated via thinning of the prey populations during the studies. During other studies, however, predators consumed more than enough of the two gobies to offset their suppression of growth (Steele et al., 1998; Forrester and Steele, 2000; Steele and Forrester, 2002b). Comparing studies of Californian fishes with studies conducted elsewhere is problematic due to the global rarity of such investigations. In the only other study on the effects of predators on growth of a marine fish of which we are aware, Connell (1998) manipulated the presence of predators with

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Settlement and Recruitment

F I G U R E 16-5 A graphical method for determining

the magnitude of predation necessary to offset the negative nonlethal effects of predators on growth of intraspecifically competing prey. Shown are data for two prey species, a) blackeye goby and b) bluebanded goby. In both species, intraspecific competition caused growth to decline as prey population density increased, both in the presence and absence of predators. Predators, by eating prey, reduce population densities and thereby alleviate competition, enhancing prey growth. Shown by broken the broken lines are the average numbers of fish that must be eaten by predators in order for the prey-thinning effect of predators to balance the negative effect that their presence has on growth. Shown by solid lines in b) is the actual average number of bluebanded gobies thinned by predators, which is insufficient to make up for their negative effect on the growth of this species. For blackeye gobies, during the study shown, predators had no effect on the density of their prey, but in other studies they have greatly reduced blackeye goby density. Data for the blackeye goby come from Steele and Forrester 2002a. The slopes and elevations of the line in b) are derived from data presented in Steele, 1998.

cages and found that predators suppressed the growth of a small, coral-reef damselfish on the Great Barrier Reef, Australia. This one non-Californian study and its similar results, combined with the ubiquity of nonlethal effects in freshwater systems (e.g., Werner et al., 1983; Semlitsch, 1987; Skelly and Werner, 1990; Fraser and Gilliam, 1992; Peckarsky et al., 1993; Scrimgeour and Culp, 1994) lead us to suspect that such effects of predators will likely play an important role in the demography of other marine fishes.

Input into local populations of most demersal marine fishes occurs when pelagic larvae or juveniles settle from the plankton and associate with benthic habitat. This transition from the pelagic to the benthic environment, defined as settlement, is very difficult to measure directly, and typically a proxy for it, recruitment, is measured. Recruitment is the number recent settlers left after some unknown amount of post-settlement mortality has occurred. (Note that this ecological definition of recruitment differs from the definition used in fisheries biology, which refers to the addition of individuals to the harvestable stock—normally large juveniles or adults). Depending on the magnitude and pattern of early post-settlement mortality, recruitment may or may not be an appropriate proxy for settlement. Studies on the effects of predators on input into populations of marine fishes have all measured recruitment, not settlement. Consequently, the exact causes of predatory effects on recruitment are not known with absolute certainty. When predators have negative effects on recruitment, these effects can arise by two different mechanisms: predators may eat settling and recently settled fishes (the typical interpretation), or settling fishes may detect predators and avoid settling in areas where predators are abundant. To our knowledge, the possibility that settling fishes detect and avoid predators has been tested only once in marine fishes, and not in California. On small coral reefs in the Bahamas, Almany (2003) confined predators in cages, which kept them from eating settling fish, but still provided cues of their presence. He measured recruitment (every other day) to reefs with caged predators (with cues) and without predators (without cues). Although an earlier experiment had revealed effects of predators on reef fish recruitment, there was no difference in the rate of recruitment between reefs with and without caged predators. Thus, he found no evidence that settling fishes avoided reefs with predators. To our knowledge, no such study has ever been done in California or any temperate system but this phenomenon deserves examination because settling fishes certainly have the sensory capabilities and swimming abilities necessary to detect and avoid predators. Sweatman (1988) showed that a highly social coral-reef fish may detect chemicals emitted by conspecifics and use them as settlement cues, so it is plausible that settling fishes could detect, either through chemosensory, visual, or other means, the presence of predators and avoid areas where they are abundant. Even relatively weak swimmers like barnacle larvae are able to detect chemical cues from their predators and respond by altering their settlement choices (Raimondi, 1988). Piscivorous fishes, however, tend to be much more mobile than invertebrate predators, and this characteristic may make cueing on them less likely to occur in settling fishes than invertebrates. Even though it has yet to be shown that predators directly influence settlement of marine fishes, it has been clearly demonstrated that predators often reduce their recruitment. The usual interpretation of this finding is that predators reduce recruitment by eating settling and recently settled fishes, but further studies on settlement choice are necessary before it can be accepted with certainty. Examples of predator-caused reductions in recruitment of marine fishes in California all come from Santa Catalina Island. In the first study of a marine fish in California to directly manipulate the presence of predators, Behrents (1987) found that bluebanded gobies recruited to artificial habitats at higher rates if they were protected from predators. Unfortunately, she

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F I G U R E 16-6 The experimental design a and b subse-

quent recruitment of kelp bass to reefs with the understory alga, Sargassum palmeri, on which predator access was manipulated. The data are means ± 1 standard error for each of three treatments (predator exclusion, predator access [no cage], and a cage control [halfcage]) over two experimental trials (after Carr, 1991).

could not rule out caging artifacts as the cause of the enhanced recruitment in caged areas. Later work by Steele (1997a, 1999), shown to be without substantial experimental artifacts, demonstrated a negative effect of predators on recruitment of this species, substantiating the results of Behrents’ study. Steele (1997a) also evaluated the importance of the effect of predators on recruitment relative to those of resident conspecifics (potential competitors or cues for settlement), potential interspecific competitors, and reef location (which can influence settlement rates). The presence of predators halved recruitment of bluebanded gobies but had little effect, on average, on the recruitment of blackeye gobies. For both species, however, the magnitude of the predatory effect varied with reef location. This pattern caused a statistical interaction between the effects of predators and reef location and made it impossible to quantify, in any meaningful way, the importance of predatory effects relative to other effects. Qualitatively, however, the effects of predators were much more important that those of any other process. In the absence of predators, reef location had strong effects on recruitment. Predators, however, completely eliminated this underlying spatial pattern of recruitment. This result implies that predators consumed the two gobies in a density-dependent manner. Notably, Steele and colleagues (Steele 1997a, 1999; Steele et al., 1998; Steele and Forrester, 2002b) have found the effects of predators on recruitment of blackeye gobies to be highly variable. Their studies have found predatory reductions in recruitment of this species as small as 14% over 21 days (Steele, 1997a) to as large as 90% within 24 hours of settlement (Steele and Forrester, 2002b). The cause of such variability in predatory effects has yet to be determined, but it is suggestive of temporally density-

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dependent predation given that per capita mortality rates generally increased with prey density (Steele and Forrester, 2002b). Carr (1991) studied the effects of cannibalism on recruitment of kelp bass. He used replicate 1m2 plots of rocks with attached algae (primarily Sargassum palmeri) in three treatments: predator exclusion (full cage that allowed access only by new recruits), predator access (open plot), and a cage control (half-cage) (fig. 16-6). In two separate 2-wk trials, Carr allowed young kelp bass to settle and accumulate on the reefs and then recorded the number of recruits (fish 10-15 mm SL) in each plot at the end of a trial. He found greater recruitment to the predator exclusion treatment than to open plots, and there was no difference in recruitment between the open plots and cage controls, suggesting that the cages did not confound the experiment by either inhibiting or enhancing settlement (fig. 16-6). In laboratory mesocosm experiments, Carr (1991) also found that risk of cannibalism did not differ among algal habitats, suggesting that the experiments using Sargassum provided a general model of predator-mediated recruitment success in other algal habitats (e.g., giant kelp, Macrocystis pyrifera). In recent work using an experimental design similar to Carr (1991), Anderson and Davenport (unpublished data) quantified recruitment of three kelp-associated fishes, the kelp bass, the senorita (Oxyjulis californica), and the giant kelpfish (Heterostichus rostratus) (fig. 16-1) to giant kelp. Despite variation in the magnitude of recruitment and the relative abundance of recruits over a two-year period, recruitment of all species was much higher in the absence of piscivorous kelp bass (there were no observed artifacts based on comparisons with cage controls). Moreover, there was evidence of size-dependent

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F I G U R E 16-7 The direct and indirect effects of predators on recruitment of the bluebanded goby. This species experiences recruitment facilitation, and therefore, predation on resident individuals reduces the cue for recruitment of juveniles. The direct effect of predators is the difference between points – P (no predators) and – FP (no facilitation, predators present) on the y-axis. The total effect of predators is the difference between points – P and FP (facilitation present, predators present). The indirect effect of predators caused by their consumption of residents (the difference between – preds and + preds on the x-axis) and the concomitant reduction of the cue for recruitment is the difference between points – FP and FP (the natural condition) on the y-axis (from Steele 1997a with permission from the Ecological Society of America).

predation. Recruited kelp bass (the only species with enough recruitment for this analysis) were much larger in predatorexclusion plots than in plots that allowed access to predators. This finding is contrary to the bigger-is-better hypothesis, widely believed to apply to marine fishes (Sogard, 1997). As noted earlier, some highly social fish use the presence and density of conspecifics as a cue for settlement (e.g., Sweatman, 1985; Booth, 1992; Schmitt and Holbrook, 1996). In species with such recruitment facilitation, the potential for an indirect effect of predators on settlement exists, mediated via the effect of predators on already settled individuals. If predators reduce the density of the conspecifics providing the cue for settlement, then settlement will be reduced. This indirect effect was found in bluebanded gobies at Catalina Island (Steele, 1997a). Using two separate approaches, one graphical and one statistical, Steele determined that the indirect reduction in recruitment was relatively small, only about 7% of the direct effect of predators on recruitment (fig. 16-7). However, in cases where recruitment facilitation is particularly strong and predatory effects on population density large, this indirect pathway for predator effects on the rate of settlement could be quite important. Studies on the effects of predators on recruitment of marine fishes of California have generally found that predators reduce recruitment of their prey, though some studies failed to detect any effect. This range of effects, from negative to none, is typical of marine fishes in other areas. For example, Levin et al.

(1997) and Petrik et al. (1999) studied the effects of predators on recruitment of two species of estuarine fish in Texas. They found a negative effect of predators on recruitment of one species, but not the other. The system in which the effects of predators on marine fish recruitment have been studied in the most detail is coral reefs, and the findings have generally been similar, though with a couple of interesting twists. Like the studies in California, the most common finding on coral reefs is that predators reduce recruitment of their prey (e.g., Shulman et al., 1983; Doherty and Sale, 1985; Carr and Hixon, 1995; Beets 1997; Steele and Forrester, 2002b; Webster, 2002; Almany, 2003). An interesting effect that has occasionally been found in coral-reef fishes, however, is a positive effect of predators on recruitment (Steele et al., 1998; Almany, 2003). In the case of a tropical goby, Steele and colleagues (1998) suggested that the predators manipulated were not the key predators of the target species, and that, in fact, the large predators manipulated actually reduced the abundance of the primary, small predators of the goby, indirectly enhancing its recruitment. Almany (2003) suggested that the positive effect of predators that he found on recruitment of a small wrasse was due to two factors: first, the wrasse is a cleaner fish and therefore is subject to little predation and, second, reefs with large predators provided a better source of food for the wrasse (greater numbers of ectoparasites) than was present on reefs without predators. In summary, studies on the effects of predators on California’s fishes have found results that are generally consistent with those from other systems, usually finding negative effects of predators on recruitment.

Mortality Predation has been implicated as a significant, if not the primary, source of mortality in populations of marine fishes (Bailey and Houde, 1989; Hixon, 1991; Sogard, 1997), despite a conspicuous lack of direct evidence in most systems. Explicit observations and experiments to determine the impact of predation on fish populations have been restricted mainly to nearshore fishes, especially those that occupy temperate and tropical reefs and have small home ranges. This situation is understandable considering the logistical difficulties in observing predation events in nature, in measuring the ecological impact of these events, and in manipulating mobile piscivores and their prey. Predation has long been implicated as an important process in the near shore habitats of California by the strong relationships between fish abundance and the abundance of shelterproviding habitats (Limbaugh, 1955; Quast, 1968; Miller and Geibel, 1973; Feder et al., 1974; Ebeling and Bray, 1976; Coyer, 1979; Hobson et al., 1981; Hobson and Chess, 1986). These relationships, however, do not conclusively demonstrate that predation is an important ecological process because they can be generated by behavioral choices (habitat preferences) of the prey in the absence of predation (Steele, 1999). An example of the importance of shelter-providing habitat is provided by Ebeling and Laur (1985). They used an experimental and observational approach to demonstrate the importance of understory kelp (Pterygophora californica and Laminaria farlowii) to young-of-year of surfperches (Embiotocidae) of five species. In the observational portion of their study, they found that the abundance of young surfperch tracked the percentage cover of the macroalgae. To demonstrate the causal nature of the relationship, they conducted an experiment in which blades

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of P. californica were removed along a 5-m band while another similar area of P. californica was left as an unmanipulated control. The abundance of young surfperches declined significantly in the area where blades were removed but not in the control, whereas the abundance of adult surfperches did not differ between treatments. Ebeling and Laur attributed the decrease in abundance of young surfperches mainly to predation by the kelp bass. Direct tests of the impact of predation on California’s marine fishes were not made until the 1980’s. As noted earlier, Behrents (1987) conducted one of the first field experiments to directly manipulate the presence of predators to test their effects on the rates of mortality and recruitment of the bluebanded goby. She manipulated both the presence of predators (mainly kelp bass) with cages and the abundance of shelter holes on artificial habitats. In addition to effects on recruitment, Behrents found that mortality was higher in the presence of predators. The strength of the effect of predators (which unfortunately could not be distinguished from a cage artifact) depended upon the size of the gobies and the abundance of shelter. Steele (1996) later tested for cage artifacts on bluebanded and blackeye gobies by placing small reefs with 3 treatments (complete cages, partial cages, and no cages) inside a large enclosure that kept all predators away from them. With this design, potential artifacts of cages were tested directly without being confounded with effects of predators. The unfortunate finding of this study was that bluebanded goby survival (though not recruitment: Steele, 1997a, 1999) was affected by cage artifacts. Hence, it is difficult to interpret the results of Behrents’ study. Further investigation led Steele to design partial cages, which allowed predators access to gobies, but that did not differ from complete cages in their effects. Comparing partially caged and fully caged treatments allowed the effects of predators to be measured unambiguously. With this technique, Steele measured the impact of predation on bluebanded and blackeye gobies, and he assessed the relative importance of predation vs. intra- and interspecific competition. Predation on bluebanded gobies was severe (about twice as many gobies died on reefs exposed to predators as on reefs free of predators) and the intensity of predation varied spatially (Steele, 1998). Moreover, the relative importance of predation was very high for bluebanded gobies, which suffered little, if at all, from intra- and interspecific competition. By contrast, blackeye gobies were not affected significantly by predation, and intraspecific competition had relatively more important effects.

Density-dependent Predation and Population Regulation Density dependence has been a major focus of recent research on marine fishes (reviewed by Hixon and Webster, 2002). In reef fishes, this recent interest was largely motivated by a desire to test the recruitment limitation hypothesis (Doherty, 1981; Victor, 1983), which specifically excludes the possibility of post-settlement density-dependent mortality (Doherty, 1983; Doherty and Fowler, 1994), and instead posits that patterns of abundance in demersal fish populations are set primarily by variable settlement. A more refined viewpoint seeks to determine the relative influence of density-independent versus density-dependent processes (since they are not mutually exclusive) (e.g., Schmitt and Holbrook, 1999). Despite the recent interest in density dependence by reef fish biologists, the study of density dependence has a long and rich history in

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general ecology (reviewed in Hixon et al., 2002) and fisheries biology (e.g., Ricker, 1954; Beverton and Holt, 1957). This is no surprise, because population regulation, essential for the persistence of populations, can only occur if one or more demographic rate is density-dependent (Murdoch, 1994). By a variety of mechanisms (discussed below), predators can cause the density dependence necessary for population regulation. Nevertheless, field experimental tests for predator-induced density dependence in marine fishes are only now becoming common (Hixon and Carr, 1997; Steele, 1997a; Forrester and Steele, 2000; Anderson, 2001; Carr et al., 2002; Webster, 2002; Holbrook and Schmitt, 2002). Tests for density-dependent predation have been made with three species of California’s marine fishes. We discuss these studies after a brief description of the mechanisms by which predators can cause density-dependent mortality of their prey. Predators can cause density-dependent mortality of their prey via four general responses to prey density: the functional response, the aggregative response, the developmental response, and the numerical response (Holling, 1959; Murdoch, 1970, 1971, 1994; Murdoch and Oaten, 1975). These four types of responses are not mutually exclusive. Briefly, the functional response is a behavioral response of individual predators to prey density, and it is measured as the number of prey killed per predator as a function of prey density (Solomon, 1949; Holling, 1959). Three basic forms of the functional response have been described, Types I, II, and III, but only the Type III response can cause density-dependent prey mortality, and it does this only over a limited range of relatively low prey densities (Holling, 1959). The aggregative response is also driven by predator behavior, and it relates the number (or time spent by) predators in an area to the density of prey there (Hassell, 1966; Hassell and May, 1974). If a strong positive relationship exists between the two variables, prey mortality may be densitydependent. The developmental response relates the somatic growth rate of predators to the density of their prey (Murdoch, 1971). If better-fed predators (ones that live in areas with dense prey populations) grow more, and as a consequence of their increased size require and eat more prey, then this too can cause density-dependent predation. Finally, the numerical response, like the aggregative response, relates the density of predators to the density of their prey, with strong positive relationships potentially causing density-dependent predation. The numerical response, however, differs from the aggregative response in the mechanism that causes predator numbers to increase with prey density: greater predator densities at high prey densities are generated by increased predator survival and/or reproductive output, not by attraction to dense prey patches. Very few field studies on marine fishes have evaluated any of these four classes of predator responses to prey densities. Anderson (2001) is the only published study of which we are aware that both tested for predator-induced density-dependent mortality with a field experiment and evaluated the mechanisms (predator responses) responsible for any densitydependent mortality. He studied the kelp perch, Brachyistius frenatus, and tested whether predatory kelp bass exhibited density-dependent functional and/or aggregative responses to prey fish density. First, in laboratory mesocosms, he evaluated the functional response of kelp bass by manipulating the density of juvenile kelp perch and quantifying the rates of predation at each density. He also concurrently manipulated the amount of shelter-providing habitat (giant kelp, Macrocystis pyrifera). The availability of shelter influenced the shape of the functional response, causing it to range from density-independent

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F I G U R E 16-8 Relationship between the density of kelp perch (no. individuals per pool) and the functional response (number of prey eaten

per predator over 15 hours) under conditions of (1) none, (b) low, (c) medium, and (d) high levels of habitat structure (giant kelp, Macrocystis pyrifera) (from Anderson 2001 with permission from the Ecological Society of America).

to inversely density-dependent, indicating a Type I or Type II functional response, respectively, depending upon the quantity of kelp (fig. 16-8). Subsequently, in a field experiment manipulating the number of juvenile kelp perch on plots of giant kelp, Anderson quantified the strike rate (number of capture attempts) of kelp bass as a proxy for the functional response. During two-hour trials conducted at dusk, when kelp bass forage actively, he also recorded the average number of kelp bass present on each plot to assess whether kelp bass exhibited an aggregative response to areas of higher prey concentration. In contrast to the laboratory experiments, mortality during the field experiment was density-dependent (fig. 16-9). Such predator-induced density dependence could have occurred either if there was a different functional response in the field than in the lab (a Type III response instead of Types I or II found in the lab), or if there was a Type II functional response combined with an aggregative response (Hassell, 1978). Anderson found that there was a strong aggregative response by kelp bass, and suggested that this behavior combined with a Type II functional response was the most likely cause of the observed density-dependent predation. He recommended that both the functional and aggregative responses be evaluated to gain a sound mechanistic understanding of patterns of predator-induced mortality over short time scales. Without focusing on the mechanisms, Steele and colleagues evaluated the possibility of density-dependent predation in the

bluebanded goby and the blackeye goby (Steele, 1997a, 1997b, 1998; Forrester and Steele, 2000). As noted earlier, Steele’s (1997a) study suggested that predation on recently settled recruits of both species was density-dependent because predatory reductions in recruit density were greatest in areas that received the highest natural recruitment of gobies and lowest in areas that received the fewest recruits. This suggestion was supported for bluebanded gobies by Steele’s (1998) study, which found that high-density populations tended to suffer higher mortality than low-density populations if they were exposed to predators, but not if predators were kept away. In this study, there was no evidence of an aggregative response by predators to bluebanded goby density, indicating that a Type III functional response was most likely the cause of density-dependent predation. The finding of density-independent mortality in the absence of predators in both bluebanded and blackeye gobies (Steele, 1998), coupled with the finding of strong density-dependent mortality of both species when exposed to predators (Steele, 1997b), gave strong, but not irrefutable, support for the notion that predators were causing density-dependent mortality in both species. These findings motivated an explicit test for predator-induced density-dependent mortality in bluebanded and blackeye gobies (Forrester and Steele, 2000). In this study, prey (goby) densities were manipulated across the natural range (using 8 different densities) and crossed with the absence or presence of predators, by excluding (by cages) or allowing predators (mainly kelp

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F I G U R E 16-9 Relationship

between the density of kelp perch and (a) the total number of strikes by kelp bass at kelp perch, standardized to a 10-min interval, (b) the mean number of kelp bass recorded on field plots, and (c) the calculated perpredator strike rate (from Anderson, 2001 with permission from the Ecological Society of America).

bass) access to the small artificial reefs inhabited by the gobies. This experiment revealed that predators were indeed the cause of density-dependent mortality in bluebanded gobies, i.e., mortality of this species was density-dependent in the presence of predators but density-independent on predator-free patch reefs. By contrast, mortality of blackeye gobies was independent of density regardless of whether predators were present or not, contrary to earlier results (Steele1997b). Forrester and Steele concluded that these inconsistent results for blackeye gobies indicate that the conditions that cause population regulation must vary temporally or ontogenetically. Density-dependence can occur in two different forms: temporal or spatial. Temporal density dependence occurs when a single population experiences higher mortality rates when it is

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dense than when it is sparse. Spatial density dependence occurs when mortality rates of populations distributed across space are greater in dense populations than in sparse populations. The two forms of density dependence are not mutually exclusive, but also, the presence of one does not ensure the presence of the other (Stewart-Oaten and Murdoch, 1990). The work of Anderson, Steele, and colleagues dealt with spatial density dependence (although comparison among some of their studies suggests that temporal density dependence may occur). We are aware of only one field study in California that addresses temporal density dependence. Hobson and colleagues (2001) conducted an 11-yr study in Mendocino County that explored temporal (interannual) variation in predation on young young-of-year (YOY) rockfishes (Sebastes spp.). The

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authors found that YOY rockfishes were more prevalent in the guts of three predators (black rockfish, Sebastes melanops; blue rockfish, Sebastes mystinus; kelp greenling, Hexagrammos decagrammus) during years when YOY were abundant. This finding implies that predation on YOY rockfishes was temporally density-dependent, and Hobson et al. suggested that this form of predation dampens interannual variation in year-class size of young, nearshore rockfishes. Overall, studies on density-dependent predation in California’s marine fishes have found results that are generally consistent with the findings of studies on coral-reef fishes (reviewed by Hixon and Webster, 2002). Predation appears to be a common cause of density-dependent mortality and we speculate that shelter limitation may be a common cause of density-dependent predation (Anderson, 2001; Holbrook and Schmitt, 2002; Forrester and Steele, 2004).

Beukers and Jones’ study, the densities of both prey and predators were positively correlated with the same habitat attribute (coral cover), and this may have driven the positive predatorprey correlation, whereas in Hixon and Beets’ studies, habitat quality was standardized on artificial reefs. Hence, it appears that similar habitat needs of predators and prey may drive positive correlations between prey and predator densities. Predators and prey may have similar habitat needs if the predators are prey of even larger species and they use structurally complex habitats in the same way their prey do, as refugia. Alternatively, predators may use such areas as ambush sites for hunting their prey. In any event, structurally complex habitats play very important roles in mediating the predator-prey interaction, and these are discussed next.

Interactive Effects of Predators and Habitat Structure

Distributional Patterns of Prey and Predators: Importance of Habitat Structural Complexity Patterns of Covariation Between Predators and Prey A number of conflicting factors influence the distributional patterns of prey and their predators. Successful predators will be located near their prey, at least when they are actively hunting, and this should generate a positive correlation between predator and prey densities. Depletion of prey by their predators, however, should generate a negative correlation between predators and prey. Moreover, to maximize their fitness, prey should avoid their predators, and this too should generate a negative correlation between prey and predator densities. The patterns generated in nature will depend on (1) the relative mobility of predators and prey, (2) the relative rates of consumption by predators vs. recruitment of prey, and (3) the scale at which the pattern is measured. Because relative mobility and rates of consumption vs. recruitment will vary from system to system, it is difficult to predict how predators and prey should be distributed relative to one another. Anderson (1994), Carr (1994), and Steele (unpublished) have explored the relationship between reef-fish prey and predators (kelp bass) at Santa Catalina Island. In Carr’s study, young-of-year kelp bass, which are extremely susceptible to being eaten by older cannibals, were the prey. Carr (1994) found no consistent relationship between the densities of predators and prey, in some years finding positive relationships, in others negative relationships, and in yet others, no relationship. Anderson (1994) found that both juvenile and adult densities of kelp perch were negatively related to kelp bass density. Steele found that bluebanded goby densities were not significantly correlated with the density of their predators (r  0.16, P  0.50, n  21), but blackeye goby densities were positively correlated with predator density (r  0.68, P  0.0007, n  21). So, perhaps not surprisingly, no consistent relationship between predator and prey densities emerges from the few studies to examine this relationship in California’s fishes. Variable relationships between predator and prey density are not unique to California’s marine fishes. Work on coralreef fishes has documented similar variability. For example, Hixon and Beets (1989, 1993) found either a negative or no relation between prey and predator density, depending on which way they measured prey density. In contrast, both Beukers and Jones (1997) and Stewart and Jones (2001) found a positive relationship between prey and predator density. In

Structurally complex habitats can provide both food and shelter from predators, although decoupling the relative value of each of these resources is no simple task (Jones, 1984, DeMartini and Roberts, 1990). On the temperate reefs that provide much of the habitat for nearshore fishes in California and other temperate areas, structurally complex habitats are typically comprised of stands of macroalgae and rocky reefs, which provide a variety of interstices, crevices, caves, and undercuts. Several researchers have documented positive relationships between the recruitment and abundance of reef fishes and the abundance of macroalgae (Larson and DeMartini, 1984; Moreno and Jara, 1984; Ebeling and Laur, 1985; Choat and Ayling, 1987; Carr, 1989, 1991, 1994; DeMartini and Roberts, 1990; Holbrook et al., 1990; Levin, 1991, 1993; Anderson, 1994; Levin and Hay, 1996, 2002), and, as noted earlier, predation is often implicated as a cause of these relationships because these structurally complex habitats are believed to provide suitable refuges from predation. Despite the prevalent notion that predators drive these habitat-abundance relationships, relatively few field experiments have tested the importance of structurally complex habitats in generating patterns of recruitment and fish abundance. Behrents (1987) manipulated the density and size of shelters for the bluebanded goby by inserting different numbers and sizes of test tubes into foam buoys that were anchored near the seafloor. All of her artificial goby habitats were exposed to predators. She found that habitats providing many shelter holes received higher recruitment than those with few holes did. She attributed enhanced recruitment on habitats with extra holes to the provision of extra shelter from predators. More recently, Hartney (formerly Behrents) and Grorud (2002) examined the importance sea urchins (Centrostephanus coronatus) as shelter for bluebanded gobies. Adult gobies are strongly associated with these urchins and field manipulations indicated that the abundance of bluebanded gobies was causally linked to the presence of urchins. Moreover, urchin presence strongly enhanced recruitment and survival of gobies. Hartney and Grorud also used artificial urchin models to mimic the physical structure provided by live urchins, but they found that these models afforded only about half the protection of live urchins. Either the models did not adequately represent the structural complexity of live urchins or other attributes (e.g., behavior) of urchins enhance goby survival. Without concurrently manipulating the presence of predators, however, one cannot be certain that the increased recruitment and survival that Hartney (Behrents) and Grorud found in habitats

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F I G U R E 16-10 Conceptual model of differential patterns of mortality for local populations of kelp perch based on the degree of habitat structure (amount of habitat) or structural complexity (habitat attributes) at lower densities of kelp perch and the strength of an aggregative response by kelp bass at higher densities of kelp perch: a) density-dependent mortality with high habitat structure or complexity and a strong aggregative response, b) inverse density-dependent mortality with low habitat structure or complexity and a weak aggregative response, and c) density-independent mortality (hatched region) caused by medium to high levels of habitat structure or complexity and a relatively weak aggregative response (from Anderson 2001 with permission of the Ecological Society of America).

with abundant shelter was caused by predation. The positive effect of shelter could instead be generated by (1) settlement preferences, (2) post-settlement migration to areas with abundant helter, or (3) positive effects of shelter-providing habitat on post-settlement survival that are unrelated to predation (e.g., protection from abiotic disturbances). To evaluate the hypothesis that abundance-shelter relationships are driven solely by predation, Steele (1999) manipulated both the abundance of shelter (the density of rocks, which provide shelter) and the presence of predators for bluebanded and blackeye gobies to assess effects on abundance via recruitment and survival of these species. In the presence of predators, both species exhibited the expected pattern of enhanced recruitment and survival on artificial reefs with abundant shelter relative to those with sparse shelter. In blackeye gobies, as expected if the shelter-related patterns of recruitment and survival were driven by predation, there was no effect of shelter abundance on recruitment and survival when predators were absent, but there was a positive effect of shelter in presence of predators. In bluebanded gobies, however, even in the absence of predators, recruitment and survival increased with increasing abundance of shelter. This result demonstrated that shelter-related patterns of abundance were not driven solely by predation, although it did play an important role, even for bluebanded gobies, in which exposure to predators exaggerated the effects of shelter abundance. Overall, shelter availability did modify the impact of predation, but Steele suggested that other factors such as settlement preferences or use of purported shelter for purposes other than escaping predation might contribute to the positive relationships between fish abundance and habitat availability. In his studies on density-dependent predation in kelp perch, Anderson (2001) manipulated both the density of juvenile kelp perch and the biomass of giant kelp, which provided shelter from predatory kelp bass. Large laboratory mesocosms were employed in which the amount of giant kelp was varied across a range of biomass. Anderson found that the pattern of mortality changed from inversely density-dependent (greater proportional mortality at lower densities) under conditions of

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no or low amounts of kelp, to density-independent at medium and high amounts of kelp. He suggested that the amount of kelp (four adult plants per plot) used in his field experiments caused increased survival at lower densities because there was necessarily greater per capita refuge availability at lower perch densities. Anderson further suggested that the pattern of predator-induced mortality (inversely density-dependent, density-independent, or density-dependent) experienced by kelp perch at varying densities would depend upon the amount of habitat or its structural complexity at low densities of kelp perch and upon the strength of an aggregative response by predators (fig. 16-10).

Community Structure Predation has been shown to influence community or assemblage structure in a variety of ways (reviewed in Sih et al., 1985; Hixon, 1986), but how it affects the structure of temperature reef fish communities remains virtually unexplored. Perhaps the most influential model of how predators affect community structure is Paine’s (1966) keystone predation hypothesis, which was developed from work on intertidal invertebrates. In this model, predation serves to maintain species diversity by disproportionately reducing the density of the competitively dominant prey species, to levels below those that would otherwise lead to competitive exclusion of inferior competitors. Nonselective predators may also help maintain species diversity if their predation causes intermediate levels of disturbance, which keep communities in a nonequilibrial state in which competitive exclusion is not possible. This situation is a special case of the more general intermediate disturbance hypothesis proposed by Connell (1978). Rather than maintain or promote species diversity, predators may cause species diversity to decline if they are 1) opportunistic and do not focus their attention on the dominant competitors (Hixon, 1986; Hixon and Beets, 1989, 1993) or 2) prefer prey species that are poor competitors (Lubchenco, 1978). In case 1, rare species may be lost from communities when they are

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consumed, leading to lower overall diversity (Hixon, 1991) and this has been found in studies of coral-reef fishes (Hixon and Beets, 1989, 1993; Caley, 1993; Eggleston et al., 1997). It is difficult to predict what sort of effect predators may have on the community diversity of California’s reef fishes because the answer will depend on the preferences of the predators and the nature of competitive interactions between prey fishes. We suspect that predation on marine fishes of California has the same effect on diversity as seen in studies on coral reefs: it will reduce species diversity. In part, this is because piscivorous predators tend to be generalists regardless of whether they are found in temperate or tropical systems, and hence, they are unlikely to disproportionately affect competitively dominant prey species. Moreover, while there are many important exceptions (e.g., Hixon, 1980; Larson, 1980; Schmitt and Holbrook, 1990), the notion of competitive dominants may have little meaning for marine fishes since interspecific competition among prey fish species is generally not strong (reviewed in Jones, 1991). Therefore competition may be unlikely to lead to competitive exclusion, which leaves little potential role for predators as mediators of competition. The notion that predation in California will serve to decrease fish community diversity is supported by the observation that generally the greatest diversity of fishes is found where structural refuge is abundant (Ebeling et al., 1980a, 1980b; Larson and DeMartini, 1984; Bodkin, 1986, 1988; Ebeling and Laur, 1988; Carr, 1989; DeMartini and Roberts, 1990; Holbrook et al., 1990), although exceptions have been found (Stephens et al., 1984;, Patton et al., 1985). Of course, these relationships between structural refuge and fish diversity may not be driven by predation (as noted earlier in this chapter), but it is likely that predation plays some role in generating these patterns and it should be weakest in areas with abundant refuge. In addition to affecting fish assemblage structure by altering diversity, predators may play an important role in generating predictable patterns of relative abundance and distribution. This role of predators also has been little explored. Recent work on coral-reef-fish assemblages by Almany (2003) has shown that that reefs with predators have predictably different patterns of relative abundance of prey species due to differential susceptibility to predation. Other work in the tropics (e.g., Carr and Hixon, 1995; Webster, 2002) has shown differential risk of predation for different prey species. As mentioned earlier, at Santa Catalina Island, Steele (1996, 1997a, 1998) found that bluebanded and blackeye gobies differed substantially in their risk of predation, with bluebanded gobies suffering greater rates of predation than blackeye gobies. Field and lab studies demonstrated that relative risk of predation varied as a function of habitat type: in sandy areas with sparse rocky cover, bluebanded gobies suffered greater mortality than blackeye gobies, but in areas with abundant rocky cover, blackeye gobies suffered greater predation (Fig. 16-11a). These habitat-related changes in the relative risk of predation may help explain the distributions of the two species in the field: blackeye gobies were most abundant and bluebanded gobies least abundant at the reef-sand interface, where rocky cover was relatively sparse, but the reverse pattern was true in predominantly rocky sections of the reef where there was high cover (Fig. 11b). Presumably, the differences in risk of predation faced by the two species are related to their coloration and behavior. The light, sand-colored blackeye goby moves little and is very cryptic when resting on sand, but when resting on dark-colored rocky background is quite obvious. The brilliantly colored, crimson and electric-blue-striped bluebanded

F I G U R E 16-11 The potential influence of predation on patterns of distribution of two reef fishes. a) The survival of the bluebanded goby relative to that of the blackeye goby increases as shelter (rock rubble) becomes more abundant. b) Bluebanded gobies are relatively rare at the rock/sand interface of reefs where shelter is sparse, but are abundant relative to blackeye gobies in the mid-reef zone where rocky cover is abundant. Absolute abundance in each zone was divided by the overall mean for each species and then these standardized species abundances were used to calculate the ratio shown. (Unpublished data from Steele.)

goby, which moves more frequently, is very easily detected where sand is abundant and rocks are sparse, but is more difficult to detect on a dark-colored rock background, where it rapidly retreats to abundant small crevices when predators are near. Because of natural differences in color patterns, morphology, and behaviors of prey species, it is likely that different species will suffer different rates of predation, which are habitat specific. Hence, it is likely that predators play a major role in creating and maintaining the habitat-specific patterns of relative abundance of fish in nature. This role of predators and their other effects on fish community structure are poorly known, especially in temperate systems, and merit greater attention in the future.

Regional and Geographic Comparisons: Generalities in the Effects of Predators? Given that relatively few studies have explored the ecological effects of predation on marine fishes, it is difficult to determine

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whether there are generalities to be found. But, overall, regardless of the system, predators seem to play some important role in the local ecology. Although there are cases in nearly every system in which research has failed to detect significant effects of predators for some prey species, there are almost always counter-examples in the same community. Hence, at the community or assemblage level, it seems likely in that in virtually every system predators will have some important impacts. Although most findings of studies on predation in temperate and tropical systems are similar, one aspect of tropical systems seems likely to cause the effects of predators to differ somewhat from temperate systems. Tropical systems, particularly coral reefs, harbor much more diverse assemblages of fishes than do temperate reefs. This extra diversity generates a greater variety of possible interactions, particularly indirect interactions, mediated through intermediary species. For example, in temperate systems, there tends to be one or a few dominant predator species, e.g., the kelp bass in southern California, whereas in tropical systems there are many more species, e.g., many different species of groupers, snappers, jacks, lizardfish, moray eels, etc. This sets up the possibility of complex interactions among predators, which may be synergistic (Hixon and Carr, 1997), additive, or inhibitory. When they are inhibitory, enhancing the abundance of one predator species may actually enhance survival of the prey species (Steele et al., 1998). Moreover, if the many different species in tropical systems have different responses to prey density (functional, aggregative, developmental, or numerical), then fluctuations in the relative abundance of the different members of the predator assemblage may cause the combined effect of the assemblage to vary substantially over time or in space. Furthermore, greater diversity of prey species in tropical systems than temperate systems may also generate more complexity in the effects of predators and interactions among prey species. For example, Webster and Almany (2002) recently demonstrated an indirectly mutualistic relationship between different prey species on the Great Barrier Reef. A number of species benefited (increased recruitment and survival) from enhanced abundance of one prey taxa, cardinalfishes. The authors argue that cardinalfishes were the preferred prey and, hence, were targeted by predators where abundant, to the extent that other prey species were ignored. In such complex systems, there may be greater opportunities prey switching, which may generate a density-dependent, Type III functional response. Regardless of the potential differences between temperate and tropical systems, the available evidence suggests that predators will play important roles in the ecology of many marine fishes.

Topics for Future Research Research on the ecological effects of predators on marine fishes is still in its early phases. Consequently, there is a wide variety of topics that beg for study. Here we outline some of the topics that we think are most worthy of attention, but note that just about any field study that explores the effects of predators on some aspect of prey behavior or demography will make a meaningful contribution to the still sparse literature on the effects of predators on marine fishes. Much of the recent research on predation in marine fishes has focused on whether predation causes density-dependent mortality and, hence, may be capable of causing or contribut-

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ing to population regulation (Hixon and Carr, 1997; Steele, 1997a; Forrester and Steele, 2000; Anderson, 2001; Holbrook and Schmitt, 2002; Steele and Forrester, 2002b; Webster, 2002; reviewed by Hixon and Webster, 2002). While most of these studies have found that predators can cause densitydependent mortality, two important questions remain: (1) what are the mechanisms that cause density-dependent mortality and (2) does the density-dependence detected actually cause population regulation? Recent studies on coral-reef fishes (Holbrook and Schmitt, 2002; Forrester and Steele, 2004) provide excellent examples of how to discover the mechanisms of density-dependent predation. Gaining this sort of mechanistic understanding will be extremely valuable for predicting whether density-dependent predation will scale up spatially and whether it will cause temporally density-dependent mortality, which is required for population regulation. Studies like Anderson’s (2001), which test the responses of predators (functional, aggregative, developmental, and numerical), are also particularly needed. The functional and aggregative responses may play particularly important roles in driving density dependence, but effort should not be focused on them alone. To our knowledge, there has yet to be a test of developmental or numerical responses in marine fishes, which would require long-term study. Because local populations of marine fishes are usually open (i.e., new offspring arrive via planktonic dispersal from other local populations), one of the normal mechanisms that can cause a numerical response is absent in most marine fishes: enhanced fecundity in predator populations that are well fed on dense prey populations will not increase local population density. Nevertheless, the bipartite life cycle of most marine fishes provides the opportunity for a different sort of numerical response: correlated settlement patterns between predators and prey. Given that the pelagic offspring of both prey and predators are exposed to the same oceanographic features, it seems plausible that there may be correlated patterns of settlement, which may cause densitydependent prey mortality via predation. This possibility deserves attention. Field tests for temporally density-dependent predation are virtually non-existent, yet it is this sort of mortality that is required for population regulation. In this regard, we believe that two sorts of studies are necessary: field experimental manipulations of density at different times and long-term, large-scale monitoring efforts that evaluate whether natural patterns of mortality at spatial scales relevant to population management are density-dependent. Coupling these sorts of studies with explorations of the mechanisms of densitydependent predation would make them particularly valuable. Along these lines, given that most experimental studies, by necessity, are done at small scales, developing methods to extrapolate the findings of these studies to larger scales is a central, unresolved problem in ecology. The interaction between predation and habitat structure is another area in need of more detailed study. As noted earlier, it is generally not known what role, if any, predation plays in establishing relationships between fish abundance and habitat availability. Factorial studies that manipulate both predators and habitat complexity are necessary to resolve this issue. A mechanistic understanding of how predation is influenced by structural complexity is needed to predict how spatial or temporal variation in habitat structure will influence prey mortality. This level of understanding may be particularly valuable because variation in habitat quality may modify the strength of density-dependent mortality (Forrester

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and Steele, 2004) and hence the potential for population regulation. As noted earlier, studies of the nonlethal effects of predators on demographic rates of their prey, especially growth, are rare for marine animals in general and fish in particular. Because of the potential for nonlethal effects on growth to influence other demographic rates, further studies of these phenomena are needed. Beyond simply testing for nonlethal effects, which is valuable in and of itself, studies that evaluate the demographic consequences of nonlethal effects of predators would provide especially important insight into the effects of predators on their prey. To achieve their greatest utility, such studies should be coupled with behavioral studies that seek to understand the causes of nonlethal effects. Predation is a process that occurs within a matrix of other ecological interactions, yet it is often studied in isolation, in single factor experiments that seek to measure just the effects of predators. While these sorts of studies are valuable and usually logistically more manageable, factorial experiments that manipulate predation along with other potentially important processes (e.g., competition) are particularly useful because they allow the relative importance of different ecological processes to be measured and they can reveal interactions among processes. Good examples of this type of study include Steele, 1997a, 1998, Carr et al., 2002, and Almany, 2003. Such studies must become more common if we hope to understand the role of predation in a broader ecological context. Community-level effects of predation on marine fishes have seldom been explored. Given the important role of predation in structuring other marine communities (e.g., Paine, 1966; Estes et al., 1998), we view this area as a high priority for future study. Areas in need of study include cascading effects of predators, indirect effects mediated via interaction chains, and effects of predator preference on risk of predation and community composition. Comparative studies of predation in regions that are species rich (e.g., tropics) and species poor (e.g., temperate zones) would be informative. We have noted some of the reasons to expect differences between such assemblages. Such comparisons would also be valuable in determining whether the very simple systems treated by most mathematical models of predator-prey dynamics, which often have only one predator and one prey species and rarely have more than a few species, offer insight into more complex fish communities. Are tightly linked predator-prey dynamics likely, or even possible? Are different species of prey and predators functionally equivalent so that different species can be pooled in models? Are prey regulated at the assemblage-level rather than the species level? Size-selective predation is widely expected in fishes but little tested in the field (Sogard, 1997). Consequently its importance in the population dynamics of marine fishes is poorly understood. Most studies on this topic have been made in the lab, which may be too unrealistic an environment to extrapolate results to the field, or inferred from observational studies in the field which suffer from some serious problems that detract from their utility (Sogard, 1997). Many of the arguments for the importance of factors that influence fish growth hinge on there being significant size-dependent mortality (often viewed as being caused by predators). Currently, we know little about size-dependent patterns of mortality in nature, so such arguments are hollow. We hope to see more

field studies of size-dependent predation, especially because they are not technically very challenging. Recently, there has been considerable interest in the effects of condition (e.g., size, energy reserves) on risk of mortality in marine organisms (e.g., Booth and Hixon, 1999; Searcy and Sponaugle, 2001; Phillips, 2002). The goal of much of this work has been to link larval condition to post-settlement performance, but post-settlement condition should also affect demographic rates. In the context of predation, what especially needs to be determined is whether the relatively subtle differences in condition found in nature translate to measurable variation in risk of predation. Last, as any reader of this chapter will notice, work on predation in California’s marine fishes has mostly been done at Santa Catalina Island. If we hope to have any sense of the general importance of predation to the ecology of the marine fishes of California, studies must be made in other places. We hope this chapter helps to motivate work on predation in the less benign but more widespread subtidal habitats of California.

Acknowledgments We thank Mark Hixon, Dan Pondella, and Larry Allen for reviewing and improving the manuscript. Larry Allen created three figures for the chapter. M. Steele gratefully acknolwedges the National Science Foundation (grants OCE-91-82941, 9618011/00-96061, 02-22087) for supporting much of the work described in this chapter. T. Anderson gratefully acknowledges the Electric Power Research Institute, the National Science Foundation (grants OCE-96-17483 [to M. Hixon], OCE-9996053 [to M. Carr], OCE-03-31895), NOAA’s National Undersea Research Program (CMRC-97-3109 [to M. Hixon], UAF(CA)03-02 and California Sea Grant (R/F-188) for supporting his work and collaborative efforts on the ecology of temperate and tropical reef fishes.

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———. 1988. Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. J. Exp. Mar. Biol. Ecol. 124:163–174. Victor, B.C. 1983. Recruitment and population dynamics of a coral reef fish. Science 219:419–420. Webster, M.S. 2002. Role of predators in the early post-settlement demography of coral-reef fishes. Oecologia 131:52–60. Webster, M.S., and G.R. Almany. 2002. Positive indirect effects in a coral reef fish community. Ecology Letters 5:549–557. Welden, C.W., and W.L. Slauson. 1986. The intensity of competition versus its importance: an overlooked distinction and some implications. Quart. Rev. Biol. 61:23–44.

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Werner, E.E., and J.F. Gilliam. 1984. The ontogenetic niche and species interactions in size-structured populations. Ann. Rev. Ecol. Syst. 15:393–425. Werner, E.E., J.F. Gilliam, D.J. Hall, and G.G. Mittelbach. 1983. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548. Wilson, B., and L.M. Dill. 2002. Pacific herring respond to simulated odontocete echolocation sounds. Can. J. Fish. Aqua. Sci. 59: 542–553. Wootton, R.J. 1979. Energy costs of egg production and environmental determinants of fecundity in teleost fishes. Symp. Zool. Soc. London 44:133–159.

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C H A P T E R 17

Competition MAR K A. H I XO N

Introduction Competition occurs when organisms inhibit each other’s access to shared resources that are actually or potentially in short supply (Birch, 1957), and thereby have negative effects on each other at the individual or population level (Odum, 1953). Because overlap in resource use is usually greater within than between species, intraspecific (within-species) competition is typically thought to be more intense than interspecific (betweenspecies) competition, all else being equal. Competition, especially within species, can be a major mechanism regulating populations (reviews by Murdoch, 1994; Hixon et al., 2002), and interspecific competition may additionally be an important interaction structuring ecological communities (reviews by Strong et al., 1984; Diamond and Case, 1986). To my knowledge, the earliest substantial discussion of competition involving a California marine fish is Sette’s (1943) description of a comprehensive research program to understand population dynamics of the Pacific sardine (Sardinops sagax). He speculated that “the basic influence tending to keep the population in check [before fishing] must have been competition within the population.” In accepting this assumption, Sette followed the then evolving fundamental tenet of classic fisheries biology: within-species competition is the primary factor limiting population size before exploitation (review by Smith, 1994). This tenet laid the foundation for the concept of maximum sustainable yield, the attempted application of which has since proven disastrous (Larkin, 1977). Clearly, understanding the role of competition in marine fishes not only contributes to basic ecological knowledge, but also is of fundamental importance to managing and sustaining fisheries. This chapter explores the existence, mechanisms, and ecological importance of competition in California marine fishes (excluding diadromous species). Following an overview of relevant definitions and concepts, I examine representative case studies in detail, and conclude with a brief discussion of the significance of studies of competition to fisheries.

Competition: Definitions and Concepts The simple definition stated above belies the complexity of the meaning of competition, the evidence gathered to detect

and understand the mechanisms and effects of competition, and resulting controversy in interpretation of that evidence. Ample jargon has developed in the study of competition, so this section provides a primer (see Keddy, 1989, for a review). Key words from the definition of competition that require further explanation include “inhibit,” “shared resources,” and “short supply.” What are “resources” and when are they “shared”? A resource is any consumable entity—be it food, shelter, etc.—and it is shared when targeted by more than one consumer. Importantly, just because two organisms share a resource does not necessarily mean that they compete for it (e.g., all marine fishes share oxygen as a resource). The shared resource must be in “short supply,” meaning that its abundance limits the reproductive success of the individual (via growth, survival, and reproductive output), and thus the distribution or abundance of the population (either within or between species). Ultimately, a resource in short supply limits the population growth rate in a density-dependent manner (i.e., the per capita population growth rate varies inversely with population size). There are basically two ways that competing organisms of the same or different species can “inhibit” each other: interference and exploitation (Birch, 1957; see Schoener, 1983, for further subdivisions). Interference competition is a direct interaction involving some form of aggression. One common form is territoriality (chapter 19), whereby an animal defends an area and the resources within it. Exploitation competition occurs simply when one organism consumes a resource that is in short supply, thereby rendering that resource unavailable for another organism. In this case, there is no direct aggressive interaction, so that exploitation competition is actually an indirect effect between two consumers using the same limiting resource (Holt, 1984). Unlike predation (chapter 16), mutualism (chapter 21), and other ecological interactions, competition is often not selfevident in nature. Competition within species can be demonstrated by documenting demographic density dependence that is not caused by predation in the broadest sense (which includes parasitism and disease). Density dependence occurs when the per capita birth rate decreases and/or the per capita death rate increases as population size or density increases. When density dependence occurs in such ways that the

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population growth rate varies inversely with population size, the population is said to be regulated (reviews by Murdoch, 1994; Hixon et al., 2002). Within or between species, a typical manifestation of competition for food in fishes is density-dependent growth that causes either 1) density-dependent survival (proximally often due to predation) or 2) density-dependent fecundity (review by Myers, 2002). Territoriality, which is usually a withinspecies phenomenon but sometimes occurs between species, is self-evidently a mechanism of competition if resources other than eggs are defended (review by Grant, 1997). Between species, the existence and strength of ongoing competition can be detected unequivocally only by logistically difficult experimental manipulations in the field (see Connell, 1983; Schoener, 1983, for general reviews). Note that this assertion raised major debate during the late 1970s and early 1980s (e.g., the exchange in The American Scientist by Wiens, 1977; Diamond, 1978; Schoener, 1982; Conner and Simberloff, 1986). Overall, there is a spectrum of evidence for interspecific competition. In order of increasingly strong inference, there are four basic categories (Connell, 1975): 1) observations of resource partitioning, 2) comparisons of resource use in sympatry vs. allopatry (so-called natural experiments), 3) observations of direct competitive displacement via interference, and 4) true field experiments.

species in the presence vs. the absence of its presumed competitor. A natural experiment accomplishes this comparison by observing species where they occur together (sympatry, more specifically syntopy) vs. where each naturally occurs alone (allopatry). For example, the striped seaperch (Embiotoca lateralis) and the black perch (E. jacksoni) partition shallow and deep foraging zones on reefs where they are sympatric in the Santa Barbara Channel (see below). However, where each species occurs in allopatry outside of this region, each forages over both reef zones. The conventional interpretation of such patterns is that each species in sympatry is constrained by competition to use a subset of the resources it uses in allopatry (Diamond, 1978). The key assumption of a natural experiment is that the only relevant difference between sympatry and allopatry is the presence or absence, respectively, of the presumed competitor. This assumption is rarely tested by field experiments (but was in the surfperch case, see below).

Direct Observation

Between-species competition occurs by definition within guilds, which are groups of species—often but not always closely related—that share the same general categories of resources within the same general habitat. Ebeling and Hixon (1991) review the basic guilds of demersal marine fishes, including many examples from California. Resource partitioning occurs when species within a guild utilize shared resource categories in at least slightly different ways (review by Schoener, 1974). For example, five species of embiotocid surfperch form a guild of demersal microcarnivores inhabiting rocky reefs off California, and each has a detectably different combination of diet and foraging microhabitat (see below). Within this and other guilds, one often finds niche complementarity, whereby species that overlap greatly in diet tend to forage in different microhabitats, and vice versa. The conventional interpretation of resource partitioning is that between-species competition has selected for divergence in resource use between species in ecological and possibly evolutionary time. Observations of resource partitioning are abundant in studies of marine fish communities in general (reviews by Helfman, 1978; Sale, 1979; Ross, 1986; Ebeling and Hixon, 1991). The interpretation that such patterns are caused by competition is problematic because different species are different by definition. Therefore, the specific use of resources by members of a guild is bound to be somewhat different regardless of whether or not those species have ever competed. Resource partitioning resulting from evolutionary divergence due to competition— sometimes called the “ghost of competition past” (Connell, 1980)—is particularly problematic because it is usually impossible to document unequivocally (Abrams, 1983).

Occasionally, between-species competition can be directly observed in nature when its manifestation is self-evident. The two most obvious cases are 1) interspecific territoriality, when it is known that territorial individuals clearly prevent intruders from using shared resources (accepting the argument that territoriality between species occurs only when resources are actually or potentially limiting, in accordance with Brown’s, 1964, concept of economic defendability); and 2) direct displacement of one species by another, as occurs when sea urchins overgraze the territories of kelp-forest fishes (see below). Note that an inverse relationship between the abundances of two species through time does not necessarily imply direct displacement due to interspecific competition. For example, the Pacific sardine fishery in California collapsed in the late 1940s due to a combination of overfishing and environmental shifts (review by Murphy, 1966). One of the proposed mechanisms contributing to this decline was competition with the northern anchovy (Engraulis mordax), which increased in abundance following the decline in sardines (Ahlstrom, 1966). From the perspective of competition, this “biomass dominance flip” (sensu Sherman, 1990) was interpreted as a direct species replacement. However, competition between these species has not in fact been demonstrated. Scale deposits in stratified seafloor sediments dated over the past two millennia have demonstrated that the relative abundance of sardine and anchovy alternate in cycles lasting several decades (Soutar and Isaacs, 1974; Baumgartner et al., 1992; see fig. 17-3, chapter 25). These cycles are correlated with oceanic environmental regime shifts that affect similar species worldwide (Lluch-Belda et al., 1989, 1992). Sardines are more abundant during warmer periods and vice versa. There are thus two alternative explanations for biomass dominance flips: 1) environmental variation shifts competitive dominance between species (similar to Hutchinson’s, 1961, “paradox of the plankton”) or 2) environmental variation shifts the relative abundance of species via mechanisms other than competition, be they biotic (e.g., concomitant shifts in predator and prey species) or abiotic (e.g., via physiological constraints linked with water temperature). This issue remains unresolved.

Natural Experiments

Field Experiments

Whether resource partitioning is caused by ongoing competition can be tested by examining patterns of resource use of a

The most rigorous test for detecting and understanding ongoing interspecific competition is to manipulate the density of

Resource Partitioning

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putative competitors or their resources via true field experiments, which include controls for the secondary effects of the manipulation, and preferably, site replication (Connell, 1974, 1975). If competition is occurring, then a species should expand its resource use (and ultimately its population size) in the experimental absence of the other species. In the parlance of Diamond (1978), one observes a niche shift when comparing the ecology of a species when its competitor is removed (fundamental niche) compared to when its competitor is present (realized niche). The extent of both the niche shift and the expansion of population size and distribution following experimental manipulations provide a measure of the relative strength of competition, as well as mechanisms of coexistence. If both species respond fairly equally to removal of the other species, then the interaction is relatively symmetrical between evenly matched competitors, a case of what Colwell and Fuentes (1975) have called either the coextensive niche model (fig. 17-1A) or the niche overlap model with competitive symmetry (fig. 17-1B). If one species responds more than the other, but both undergo substantial niche shifts, then the niche overlap model with competitive asymmetry is occurring (fig. 17-1C). If only one species undergoes a substantial niche shift, then that species is an inferior competitor and relative generalist normally confined to a competitive refuge by the superior competitor and relative specialist—the included niche model (fig. 17-1D). In ecological jargon, the fundamental niche of the competitively-subordinate generalist in the absence of competition is broader than its realized niche (competitive refuge) in the presence of competition (Colwell and Fuentes, 1975). For the competitively superior specialist, the fundamental and realized niches are similar in the included niche model. As reviewed in detail below, several of the most complete examples of the logistically challenging experimental approach to understanding competition in nature have focused on marine fishes of California.

Evidence Regarding Intraspecific Competition Data indicating within-species competition in California marine fishes are of two kinds: the first an effect of competition (density-dependent growth) and the second a mechanism (intraspecific territoriality).

Density-dependent Growth Density-dependent growth is well documented in fishes, and is generally assumed to be the result of competition for food (reviews by Weatherley, 1972; Wootton, 1990). Reduced growth due to increasing competition at higher population densities can ultimately regulate a population via two mechanisms: 1) density-dependent survival due to size-selective mortality, especially via predation (review by Sogard, 1997) and/or 2) density-dependent fecundity (review by Lorenzen and Enberg, 2002). Although I found no explicit studies from California per se, density-dependent growth has been documented off the Pacific coast of Canada in various species that range into California, including Pacific herring (Clupea pallasii) (Tanasichuk, 1997) and English sole (Parophrys vetulus) (Peterman and Bradford, 1987). Off California, there is evidence for intraspecific competition in the feeding, growth, and fecundity patterns of striped

seaperch, a benthic microcarnivore (Holbrook and Schmitt, 1992). At Santa Cruz Island, some individuals apparently specialize on caprellid amphipods, whereas others specialize on gammarid amphipods (Alevizon, 1975a). The caprellid specialists have fuller guts, are larger at age, and consequently, have higher calculated fecundity than gammarid specialists, with generalists lying midway between these extremes (fig. 17-2). Importantly, this pattern appeared to be maintained by aggressive displacement of smaller fish by larger fish from the foraging microhabitat that harbored caprellids (the red alga, Gelidium), rather than from active prey selection by different fish (see also Hixon, 1980a). Unknown was what came first: differential aggressive dominance between individuals of initially the same size that ultimately led to differential growth, or differential birth sizes that led to differential dominance.

Intraspecific territoriality A variety of nearshore California fishes exhibit obvious territorial behavior (table 17-1), a clear form of within-species interference competition when resources other than demersal eggs are defended (review by Grant, 1997). Chapter 19 examines territorial behavior in detail. Typically, individual territories are permanent, cover the entire small home range, involve defense of both shelter and food (and often nests and eggs), and are defended mostly against members of the same species. Note that species with demersal eggs almost invariably defend clutches during the spawning season (e.g., cottids and hexagrammids), but this behavior is defense against egg predation rather than competition. The question here is whether territoriality has significant effects on local population size within a species. This issue has been examined most explicitly in five species: the mussel blenny (Hypsoblennius jenkensi) (Stephens et al., 1970), the garibaldi (Hypsypops rubicundus) (Clarke, 1971), the black-and-yellow rockfish (Sebastes chrysomelas) and gopher rockfish (S. carnatus) (Larson, 1980ab), and the black perch (Hixon, 1981). In each case, local population sizes were manipulated then observed to return to original densities. M US S E L B LE N NY

Mussel blennies defend individual subtidal crevices and abandoned invertebrate burrows, from which they feed on benthic and planktonic invertebrates (see table 17-1 for other details). Stephens et al. (1970) conducted a population enhancement manipulation on pier pilings off Palos Verdes. A total of 42 fish (the 10 largest were tagged) were translocated from one piling to another inhabited by 17 fish (the 12 largest were tagged). After about 50 days, the local population returned to its original size, 27% of the enhanced population being lost in the first 3 days, and 50% lost by 18 days. Although uncontrolled and unreplicated, this manipulation indicated that the local adult population was saturated, suggesting regulating within-species competition for territory sites. GAR I BALDI

Adults of the garibaldi (the California State marine fish) defend permanent territories in kelp forests off southern California (Clarke, 1970; see table 17-1 for other details). All territorial individuals defend a shelter site and a food supply

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F I G U R E 17-1 Niche shifts demonstrating competition between two species (solid and dashed curves). The “realized niches” (left) depict the distribution of two species (resource use measured typically as abundance or density (N) along some resource gradient, e.g., reef depth), where both species occur in the same general habitat (e.g., kelp forest) yet manifest some kind of resource partitioning (note low niche overlap). Bars along the x-axis depict niche breadths. Following the experimental removal of each species, one observes the “fundamental niche” of the remaining species, and both species can again be plotted on the same axes for comparison (right). The null outcome, indicating no interspecific competition, occurs when the realized and fundamental niches of each species are identical (not pictured). Four alternative outcomes indicate the presence and strength of interspecific competition (note greater overlap in fundamental compared to realized niches), as well as the mechanisms of coexistence: (A) Coextensive niche model, where each species can use the same range of resources in the absence of its competitor, yet each is the dominant competitor at opposite ends of that range. Each species excludes the other from opposite ends of the resource gradient in a fairly symmetrical way. (B) Niche overlap model with symmetrical competition, where both species undergo fairly equal niche shifts. (C) Niche overlap model with asymmetrical competition, where the dominant competitor (Dom) undergoes a substantially smaller niche shift than the subordinate competitor (Sub). (D) Included niche model, where a dominant specialist (S) eliminates a subordinate generalist (G) from most of the region of niche overlap, leaving the generalist to survive in a competitive refuge (CR).

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F I G U R E 17-2 Size at age (mean
SEM) of striped seaperch

(Embiotoca lateralis) in each dietary category at Santa Cruz Island, California. Size at age differed significantly among the dietary groups for ages 2–4, but growth rates did not. After Holbrook and Schmitt (1992).

TA B L E 17-1

Representative Examples of Territoriality in Marine Fishes of California

Family Common Name (Scientific name)

Territory Size (m2)

Intruders Chased

Resources Defended

Reference

Scorpaenidae Black-and-yellow rockfish (Sebastes chrysomelas) Gopher rockfish (Sebastes carnatus)

ca.5–10

conspecifics, congenerics, some others

shelter, food

Larson, 1980ab

Embiotocidae Black perch (Embiotoca jacksoni)

ca.20–30

conspecifics, confamilials, some others

shelter/mating site, food

Hixon, 1981

Pomacentridae Garibaldi (Hypsypops rubicundus)

ca.6–12

conspecifics, egg predators

shelter, food, eggs

Clarke, 1970, 1971

Blenniidae Mussel blenny (Hypsoblennius jenkinsi)

ca.0.04

conspecifics, congenerics

shelter, eggs, (food?)

Stephens et al.,1970

Gobiidae Bay goby

no data (small)

conspecifics

shelter, food, eggs

Grossman, 1980

(Lepidogobius lepidus)

of benthic invertebrate prey, and some males additionally defend cultivated mats of red algae that serve as nest sites for demersal eggs. Clarke (1971) noted that there was no evidence for fluctuations in adult population sizes off San Diego over 3 years, and that recruitment of new settlers more than balanced adult mortality. Given that the maximum life span of the garibaldi exceeds a decade, these patterns suggested that local populations were both saturated and regulated. To test these ideas, Clarke (1971) removed most adults at three sites (19, 15, and 71 fish), then re-censused the removal areas over 21 months, ultimately finding 39, 14, and 43 adults, respectively. Thus, two sites fully recovered from the removals (one doubling in density), and one was partially repopulated. Most of the immigrants were smaller than the removed fish, and were either females or bachelor males that had not been defending well-developed nests. These results suggested that within-species interference competition played a role in regulating local populations of adult garibaldi.

ROCKFI S H E S

On subtidal rocky reefs in the Santa Barbara Channel, adult black-and-yellow rockfish and gopher rockfish (very similar sibling species) defend permanent territories that include benthic prey and individual shelter holes, although some individuals are nonterritorial floaters and commuters (Larson, 1980a; see table 17-1 for other details). As part of a comprehensive study of competition within and between these species (see below), Larson (1980b) tested whether adult density was limited by territorial behavior. At three sites, he removed 2, 2, and 4 territorial fish, respectively, with an additional 2 fish disappearing naturally at the third site (all but 2 of the removed individuals were gopher rockfish). Relative to control territories, intrusion rates into the 10 emptied territories increased significantly. Neighboring conspecific or congeneric adults recolonized all of the emptied territories, and all but one of the colonizers thereby obtained a smaller and more exclusive home range. These results were consistent with the

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TA B L E 17-2

Representative Examples of Resource Partitioning in Marine Fishes of California

Guild

Study Area

Partitioned Resources

Reference

Rocky intertidal sculpins (3 species)

Pescadero Point

space, food

Yoshiyama, 1980, 1981

Coastal blennies (3 species)

Palos Verdes

space, food

Stephens et al., 1970

Breakwater surfperches (5 species)

Redondo Beach

food

Ellison et al., 1979

Rocky-reef planktivores (8 species)

Catalina Island

space, food, time

Hobson and Chess, 1976

Rocky-reef microcarnivores (3 species)

Santa Barbara Channel

space, food

Bray and Ebeling, 1975

Rocky-reef surfperches (5 species)

Santa Barbara Channel

space, food

Alevizon, 1975a; Ebeling and Laur, 1986

Rocky-reef macrocarnivores (3 species)

Santa Barbara Channel

space, food

Love and Ebeling, 1978

Rocky-reef rockfishes (6 species)

Carmel Bay

space, food

Hallacher and Roberts,1985

Deep-sea thornyheads

Central California

space

Jacobson and Vetter, 1996

(2 species)

hypothesis that competition via territorial behavior limited local adult density.

B LACK P E R CH

Large male black perch, a viviparous species, defend reef caves as courtship and mating sites (Hixon, 1981). On a rocky reef off Santa Barbara, 12 territorial fish were experimentally removed, and all were replaced by other males within 4 days such that the number and distribution of territories was identical to that before the manipulation. During the same period, there was no change in the configuration of 8 adjacent control territories, suggesting the existence of a pool of non-territorial floaters (sensu Brown, 1969). Natural disappearances were also followed by rapid replacements. These results indicated that the population density of mating males was limited by competition for a fixed number of courtship and mating sites. However, this result did not necessarily indicate overall population regulation because those males holding territories could nonetheless have fertilized all available females.

Evidence Regarding Interspecific Competition The evidence that competition is an ecologically significant interaction between species of California marine fishes runs the full spectrum, from purely circumstantial to experimentally compelling. This review focuses on representative case studies that illustrate this spectrum.

1991). These studies have taken two perspectives: the entire community or a specific guild. Examination of an entire community always detects differences in resource use among species because such comparisons include between-guild contrasts (e.g., bay fishes: Allen, 1982; rocky intertidal fishes: Grossman, 1986; kelp-forest fishes: Larson and DeMartini, 1984; nearshore sand-bottom fishes: Hobson and Chess, 1986; pelagic fishes: Allen and DeMartini, 1983; mesopelagic fishes: Lavenberg and Ebeling, 1967). There is also temporal partitioning between diurnal and nocturnal species at the community level in nearshore California fishes, which has been ascribed to competitive interactions in the evolutionary past (Ebeling and Bray, 1976; Hobson et al., 1981). Such community-level surveys certainly provide valuable insight on the organization of entire assemblages. However, it is the within-guild perspective that offers the strongest inference regarding the possibility of ongoing competition between species. As summarized in table 17-2, studies within guilds of demersal California fishes have invariably detected betweenspecies differences in microhabitat use and/or diet, often in complementary ways (i.e., high overlap in space with low overlap in food, or vice versa). As discussed above, these patterns can be used to hypothesize which species are likely competitors, but do not actually demonstrate competition. More convincing evidence of competition requires one to build a case by combining observational data from a variety of sources, observing overt competitive displacement, or conducting a field experiment.

Direct Observation Resource Partitioning There are numerous examples of resource partitioning among marine fishes of California (review by Ebeling and Hixon,

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Self-evident competition involving California marine fishes is of two kinds: (1) between-species territoriality where resources other than eggs are defended, and (2) displacement of territorial fish by sea urchins.

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densities along the California coast, sometimes overgrazing the seafloor and causing barrens (reviews by Dayton, 1985; Schiel and Foster, 1986). Two studies at Naples Reef off Santa Barbara indicated overgrazing of fish territories, which are cases of a morphologically defended and superior exploitative competitor (an urchin) locally displacing an ineffective interference competitor (a fish). Hixon (1981) witnessed a foraging front of S. purpuratus slowly denude two permanent territories of adult male black perch to the point where the fish eventually abandoned their territories. Breitburg (1987) documented that urchins and territorial blackeye gobies (Rhinogobiops nicholsi) used the same rocky microhabitats, yet their co-occurrence at the same specific location was
3% vs. an expected value of 36%. It appeared that urchins dislodged demersal eggs defended by male gobies, suggesting local competition for space as well as possible egg predation.

Experimental Evidence

F I G U R E 17-3 Sebastes congeners experimentally demonstrated to com-

pete with each other in kelp forests at Santa Cruz Island, California: the shallow-water black-and-yellow rockfish (S. chrysomelas) and the deep-water gopher rockfish (S. carnatus).

Between-species competition and its ecological ramifications have been explored experimentally in three pairs of fish species inhabiting rocky reefs off southern California. To my knowledge, these labor-intensive studies comprise the most complete investigations to date of competition in any marine fishes. Because scientists at the University of California at Santa Barbara (UCSB) conducted all these studies, I present them in temporal sequence as a historical narrative.

ROCKFI S H E S I NTE R S P ECI F IC T E R R ITOR IALIT Y

Fishes that defend permanent territories from members of the same species almost invariably also exclude other species that are potential threats to food or shelter (reviews by Grant, 1997; chapter 19). In studies of within-species territoriality in California marine fishes, there is often evidence of such between-species interference (table 17-1). For example, laboratory behavioral observations indicated that the territorial mussel blenny is aggressively dominant over a nonterritorial congener, the bay blenny (H. gentilis), and may therefore limit habitat use by the bay blenny where these species co-occur (Stephens et al., 1970). Large males of the viviparous black perch defend permanent territories that include courtship and mating sites, as well as surrounding foraging areas (Hixon, 1981). Although most aggression is among conspecific males, permanently territorial males also exclude intruding members of the same foraging guild (including 4 other species of perch—see below) in proportion to interspecific overlap in diet. The mechanism underlying this correlation is that territorial males tend to chase only intruders that actively forage within their territories—non-feeding intruders are generally ignored. The fact that food supplies comprise a defended resource was confirmed by manipulations of foraging substrata that demonstrated an inverse relationship between territory area and food availability (see also Hixon, 1980b). D I S P L ACE M E N T OF T E R R ITOR IAL F I S H BY U RCH I N S

In the absence of predation by sea otters and other predators, sea urchins (Strongylocentrotus spp.) often attain high

Alfred Ebeling started the first field studies of marine fishes based at UCSB, shifting emphasis from deep-sea to kelp-forest systems in the late 1960s. His doctoral student, Ralph Larson (1980c), was the first to provide unequivocal evidence for population-level, between-species competition in marine fishes: a sibling pair of rockfishes (fig. 17-3). In the Santa Barbara Channel, the black-and-yellow rockfish dominates shallow reef areas, whereas the gopher rockfish dominates deeper areas (fig. 17-4). The transition depth between the species is about 10-15m. The specific transition depth between sites is inversely correlated with shading by seaside cliffs, which probably affects the density of benthic invertebrate prey. In any case, prey density decreases with depth. Overlap in diet is high, so these congeners partition space and not food. In 1974 at Santa Cruz Island, Larson (1980c) cleared one site of black-and-yellow rockfish (removing 209 fish), and cleared another site of gopher rockfish (removing 159 fish), leaving a third site as an unmanipulated control. Over the next 3 years, the treatments were maintained by additional removal of 125 black-and-yellow rockfish and 59 gopher rockfish. In response to these population manipulations, the deep-living gopher rockfish moved into shallow water where the shallow-living black-and-yellow rockfish had been removed, and the black-and-yellow rockfish moved slightly into deeper water where the gopher rockfish had been removed, while the distributions of both species did not change at the control site (fig. 17-5). The fish that moved were slightly smaller than average, and by the time new recruits could be identified to species, they had already segregated by depth. In

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F I G U R E 17-4 Segregation by depth of the black-and-yellow rockfish (Sebastes chrysomelas) and the gopher rockfish (S. carnatus) off Santa Cruz Island, California. Data are median number of fish (
quartile range) along 30  2 m transects (n  30 censuses per transect). After Larson (1980c).

paired contests over shelter holes in the laboratory, black-andyellow rockfish tended to dominate gopher rockfish, winning 69% of 48 trials. Larson (1980c) concluded that between-species competition was partly responsible for the bathymetric segregation of these species. He speculated that this segregation begins with differential larval settlement by depth, and is then reinforced by territorial behavior, with a strong prior residency effect (i.e., territory residents win encounters). What allows these species to coexist without one species eliminating the other? Larson suggested that black-and-yellow rockfish are the aggressive dominant, but may be constrained to occupy food-rich shallow zones. If so, gopher rockfish have a competitive refuge in food-poor deeper zones. As such, this system fits the included niche model of coexistence of competing species (Colwell and Fuentes, 1975). In the parlance of niche jargon reviewed above, the fundamental niche of a relatively specialized dominant competitor (black-andyellow rockfish) is a subset of the fundamental niche of a relatively generalized subordinate competitor (gopher rockfish). This situation results in the dominant having a realized niche similar to its fundamental niche, and the subordinate being restricted to the portion of its fundamental niche that does not overlap with that of the dominant (i.e., a competitive refuge). This scenario allows coexistence of species despite ongoing between-species competition (fig. 17-1D).

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S U R F P E RCH E S

Concurrent with Larson’s work on rockfishes, another of Ebeling’s graduate students, Bill Alevizon, began observational studies of a guild of two congeneric pairs of kelp-forest surfperches, which are viviparous demersal microcarnivores. Alevizon (1975b) showed that the congeners that were more dissimilar in feeding morphology—the pile perch (Rhacochilus vacca) and the rubberlip seaperch (R. toxotes)—overlapped substantially in microhabitat use, whereas the more trophicly similar Embiotoca congeners—the striped seaperch and the black perch—showed greater microhabitat segregation. These patterns were later substantiated in much greater detail by Schmitt and Coyer (1982), Laur and Ebeling (1983), Schmitt and Holbrook (1984), Ebeling and Laur (1986), and Holbrook and Schmitt (1986). Ebeling and Laur (1986) most thoroughly quantified the two contrasting modes of niche complementarity in this guild at Naples Reef off Santa Barbara: the Rhacochilus congeners overlapped only 32% in diet but 84% in foraging microhabitat, whereas the Embiotoca congeners overlapped 56% in food but only 35% in space (fig. 17-6). These patterns of complementarity are especially impressive given that, first, dietary data were gathered during the relatively food-rich summer period when competition was least likely, and second, microhabitat use data were gathered on a relatively small rocky reef lacking the substantial vertical relief of more

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F I G U R E 17-5 Responses of rockfish (Sebastes) species to reciprocal removals of congeners at Santa Cruz Island, California. Vertical dashed lines

show dates of manipulations. Data are number of fish along 30  2 m transects, and error bars give mean
range of 5 counts repeated on the same date. After Larson (1980c).

continuous habitats at the California Channel Islands (see below). Note, however, that not all pairwise comparisons within the guild showed complementarity, leading Ebeling and Laur (1986) to conclude that resource overlap of most pairs of species within this guild were not influenced by competition. In particular, a fifth species, the rainbow seaperch (Hypsurus caryi), overlapped substantially in both food and space with both rubberlip seaperch and black perch (fig. 17-6), but the rainbow seaperch is a seasonal resident of kelp forests during only the food-rich summer months. Overall, these patterns suggested the hypothesis that between-species competition organized patterns of resource use in at least the two congeneric pairs of species in the kelp-forest surfperch guild. As another of Ebeling’s students, I combined Alevizon’s observational approach with Larson’s experimental approach, focusing on the Embiotoca congeners (fig. 17-7). Like Larson’s rockfishes, these surfperches were segregated by depth where they co-occurred at Santa Cruz Island (fig. 17-8A). This spatial separation was clearly correlated with the distribution of the major foraging microhabitats of these species, from which they picked small invertebrate prey: striped seaperch on shallow understory algae, especially Gelidium robustum (from which they took 96% of their foraging bites), and black perch on deeper benthic turf (from which they took 85% of their foraging bites) (fig. 17-8B). In a natural experiment, each species occupied and foraged over the full range of depth

zones where each naturally occurred in the near-absence of the other species (Hixon, 1980a): striped seaperch to the north of Pt. Conception (fig. 17-8C, see also Haldorson and Moser, 1979) and black perch to the south of Santa Cruz Island (Fig. 17-8D, see also Schmitt and Coyer, 1983). From this perspective, the niche relations of the species are coextensive (fig. 17-1A). The small benthic prey of these fishes, mostly amphipods, were more abundant on shallow than deep substrata (Schmitt and Holbrook, 1986). When shallow algae and deep turf were offered side-by-side on experimentally translocated trays, striped seaperch at shallow depths still took significantly more bites from algae, whereas black perch in deeper water foraged over both substrata more equally, expanding their foraging microhabitat to include prey-rich shallow algae (Hixon, 1980a). Schmitt and Coyer (1983) observed that black perch consumed a broader range of prey taxa and sizes in allopatry than in sympatry. Moreover, the diet of black perch in allopatry was similar to that of striped seaperch in sympatry (i.e., more free-living amphipods and fewer tubiculous amphipods), even accounting for between-site differences in prey availability. Balanced time-budget analyses in sympatry, stratified by species, time of day, and season, showed that striped seaperch were aggressive toward black perch about 3.5 times as much as the converse, and a statistical spacing analysis suggested that black perch avoided striped seaperch (Hixon, 1980a).

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F I G U R E 17-6 Percent overlap in foraging space and diet within a guild of five surfperches at Naples Reef,

California. Species are the black perch (EJ, Embiotoca jacksoni), the striped seaperch (EL, E. lateralis), the pile perch (RV, Rhacochilus vacca), the rubberlip seaperch (RT, Rhacochilus toxotes), and a seasonal guild member, the rainbow seaperch (HC, Hypsurus caryi). Note niche complementarity in the two pairs of congeners (EJ, EL and RT, RV). After Ebeling and Laur (1986).

Combined, these observational data were consistent with the hypothesis that the Embiotoca congeners competed with each other. In 1977 at Santa Cruz Island, the critical experimental test for competition was conducted by clearing one reef of striped seaperch (removing 56 fish), and clearing another reef of black perch (removing 130 fish), leaving a third reef as a control (Hixon, 1980a). Over the next 3 months, the treatments were maintained by the additional removal of 45 striped seaperch and 63 black perch. During this period, striped seaperch did not change their distribution in response to the removal of black perch, but black perch immediately expanded their distribution into shallow water in response to the removal of striped seaperch (fig. 17-9). There were no changes at the control reef. Despite the lack of site replication, these results demonstrated that striped seaperch competitively excluded black perch from food-rich shallow habitats, but did not explain why striped seaperch did not colonize deeper areas formerly occupied by black perch. In 1978, shallow algae were removed from one reef, leaving another reef as a control (Hixon, 1980a). In response, striped seaperch abandoned the denuded reef rather than displacing black perch from deeper water (with no changes at the control site). Later that year, the original experiment was repeated, this time switching species-removal treatments

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among reefs and additionally denuding shallow algae at the site where black perch were removed. Over the next 3 months, striped seaperch finally did shift their distribution into deeper water, abandoning the denuded shallow zone and colonizing the deep zone formerly occupied by black perch (fig. 17-10). At the reef where striped seaperch were removed, black perch again quickly shifted their distribution into the shallow zone, as had occurred the previous year at another site (fig. 17-10). As before, no change occurred at the control reef. Based on both experimental and observational results, I concluded that interactions between the Embiotoca congeners at Santa Cruz Island fit the included niche model of coexisting competitors (fig. 17-1D) in a scenario similar to Larson’s rockfishes (see above). Striped seaperch were the dominant competitors and occupied only the food-rich shallow zone preferred by both species. Why did striped seaperch not also competitively exclude black perch from the deep zone, as indicated by the natural experiment reviewed above? I speculated that the abundance of striped seaperch was limited by factors other than competition here at the southern limit of its contiguous geographical range. This geographical limit is probably associated with water temperature because the Santa Barbara Channel is a major biogeographic transition zone, separating the cold-temperate Oregonian Province north of Point

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F I G U R E 17-7 Embiotoca congeners experimentally demonstrated to

compete with each other in kelp forests at Santa Cruz Island, California: the shallow-water striped seaperch (E. lateralis) and the deep-water black perch (E. jacksoni).

Conception from the warm-temperate Californian Province to the south (Briggs, 1974). South of the Santa Barbara Channel, the striped seaperch is found only in areas of intense yearround, cold-water upwelling along the Baja peninsula (Love, 1996). In any case, striped seaperch populations limited by temperature or some other factor did not shift to the food-poor deep zone over the 3-month duration of my experiments, even if the black perch there were removed, unless the shallow zone was denuded of prey-bearing algae, thereby exacerbating competition (Hixon, 1980a). In ecological jargon, the black perch was the subordinate competitor relegated to a competitive refuge provided by the food-poor deep zone (realized niche), and readily inhabited the shallow zone as well whenever striped seaperch were removed (fundamental niche). Therefore, in sympatry, the striped seaperch was the competitively dominant specialist and black perch was the competitively subordinate generalist, allowing coexistence despite ongoing between-species competition (fig. 17-1D). However, in allopatry north of Point. Conception, striped seaperch occupied and foraged over both reef zones, being more abundant in the more central portion of their geographical range. Black perch also inhabited both reef zones in allopatry south of Pt. Conception, so that the fundamental niches of the two species where each naturally occurred alone were relatively coextensive (fig. 17-1A). In the early 1980s, the surfperch project was taken over by Russell Schmitt and Sally Holbrook, who repeated and

extended previous research on the Embiotoca congeners with unparalleled thoroughness. Schmitt and Holbrook (1986) duplicated much of Hixon’s (1980a) study at Santa Cruz Island, independently corroborating patterns of resource partitioning (bathymetric segregation and foraging patterns) and repeating the short-term population manipulations. However, unlike the previous study, they were able to include site replication in their experiments, and overall, documented patterns in much greater detail. Importantly, this was perhaps the first time an experimental field study of competition had been replicated by two different research groups, providing the kind of independent repeatability often advocated but seldom accomplished in the science of ecology (Fretwell, 1981; Connell, 1983). Besides confirming previous research, Schmitt and Holbrook greatly extended the duration of the populationremoval experiments at Santa Cruz Island, providing unprecedented insight on the role of competition in seasonal and regional patterns of resource use and long-term population dynamics. Regarding seasonal patterns, there was four times as much invertebrate prey available in the summer as during the winter, so the intensity of competition was greater during the winter (Holbrook and Schmitt, 1989). This cycle affected seasonal patterns of overlap in use of foraging microhabitats (algae vs. turf) between the two surfperches. High overlap occurred in the food-rich shallow zone during the summer, when competition was least intense. Low overlap occurred in the depleted shallow zone during the winter, as well as in the relatively food-poor deep zone year-round. Long-term changes in the abundance of giant kelp (Macrocystis pyrifera) during the 1980s indirectly altered competitive interactions between the Embiotoca congeners. Comparisons among 18 reefs at Santa Cruz Island had shown that the abundance of striped seaperch was correlated with the cover of shallow Gelidium algae, whereas the abundance of black perch was correlated with the cover of deeper benthic turf (Hixon, 1980a; Holbrook et al., 1990ab). When kelp became abundant, Gelidium declined and the turf increased in cover, and consequently, striped seaperch declined and black perch increased in abundance (Schmitt and Holbrook, 1990a). Repeating and extending Hixon’s (1980a) manipulations of foraging habitat, Holbrook et al. (1990b) reduced Gelidium cover by 80% at two sites by clipping algal holdfasts in 50 m  15 m plots. They also increased turf cover fourfold on four 2m  2m plots by removing overlying seaweeds, with the same number of replicates used as controls in each case. In response, the striped seaperch decreased in abundance and black perch increased in abundance, with no change in the controls (fig. 17-11). Thus, variation in food availability in both time and space clearly affected the intensity of competition and the local abundance of the two surfperches. Complimentary to these patterns, after a severe storm removed kelp, and urchins subsequently overgrazed turf from Naples Reef off Santa Barbara, the Embiotoca congeners converged in their foraging effort on the remaining Gelidium (Stouder, 1987). The density of striped seaperch at Naples Reef (40 per hectare) was apparently so low that black perch (327 per hectare) could effectively overwhelm them (data from Ebeling and Laur, 1986). As the abundance of surfperch declined after the storm, and subsequently as the turf recovered, partitioning of foraging microhabitat by the Embiotoca congeners resumed (Stouder, 1987).

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F I G U R E 17-8 (A) Segregation by depth of the striped seaperch (Embiotoca lateralis) and the black perch (E. jacksoni) off Santa Cruz Island, California. (B) The depth distribution of these species at Santa Cruz Island is closely correlated with the distribution of shallow algae and deep turf foraging substrates. (C) Depth distribution of these species at Lone Black Reef, north of Pt. Conception, where the striped seaperch predominates and occupies all depth zones. (D) Depth distribution of these species at Anacapa Island, south of Pt. Conception, where the black perch predominates and occupies all depth zones. Data in plots A, C, and D are number of fish along 30  4 m transects (mean
range, n  3, 5, and 5 transects, respectively). Data in plot B are percent cover (line intercept) along 10 m lines (mean
range, n  10 lines). After Hixon (1980a).

Sustaining the population-removal experiments for multiple years, Schmitt and Holbrook (1990b) found that competitive effects between the Embiotoca congeners were more symmetrical than the short-term manipulations of Hixon (1980a) and Schmitt and Holbrook (1986) had indicated. In fact, the abundance of each species increased approximately 40% in the absence of its congener over 4 years (fig. 17-12), a pattern best described as coextensive niches (fig. 17-1A). Schmitt and Holbrook speculated that release from interference competition explained the short-term results manifested as behavioral shifts in depth distribution, whereas release from exploitation competition appeared over a longer time frame that involved population shifts in abundance. From this perspective, coexistence of these species was ensured by the effective ability of each to exploit different foraging microhabitats when prey are scarce: striped seaperch on the alga Gelidium as superior visual predators, and black perch on benthic turf as superior “winnowing” predators (Laur and Ebeling, 1983). In any case, it was clear that striped seaperch were superior at utilizing the mutually preferred foraging substratum (Gelidium) that normally covered shallow reef surfaces (Holbrook and Schmitt, 1995).

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GOB I E S

It is important to mention at least one case where the presence of competition within and between-species was examined experimentally and found to be negligible. One of Holbrook’s graduate students, Mark Steele, conducted a thorough study of potential competition involving two species of goby (Gobiidae): the blackeye goby and the bluebanded goby (Lythrypnus dalli). It was known that blackeye goby are territorial (Cole, 1984) and that bluebanded goby compete for shelter holes (Behrents, 1987). Steele (1997, 1998) constructed a matrix of 36 metersquare rock reefs on a sand bottom adjacent to the main reef in Big Fisherman Cove, Catalina Island. Gobies of each species were added to these reefs in a variety of combinations of abundance, both in the presence or absence of predatory fishes (using cages). The recruitment and fates of gobies on the reefs was subsequently monitored for about 3 weeks during each of three experiments. Overall, any effects of competition were minor compared to the strong effects of predation (chapter 16). Regarding within-species competition, blackeye gobies suffered no effects on growth, but survival was slightly lower at higher densities. Growth of bluebanded gobies was slightly lower at

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F I G U R E 17-9 Responses of surfperch (Embiotoca) species to

reciprocal removals of congeners at Santa Cruz Island, California. Vertical lines show dates of manipulations. Data are number of fish along 30  4 m transects. After Hixon (1980a).

higher densities, but there was no effect on survival. Recruitment was actually enhanced at higher conspecific densities for bluebanded gobies, with no effects for blackeye gobies. There was no detectable-between-species competition.

Competition in Context This review documents substantial evidence that competition is an ecologically significant interaction both within and between several species of Californian marine fishes. The majority of evidence has come from nearshore fishes along the coast of southern California, especially at SCUBA depths on rocky reefs and associated kelp forests. Perhaps the most

exhaustive study of interspecific competition between any marine fish species worldwide was on California surfperches. Unfortunately, from the perspective of generality, surfperches are viviparous and thus have closed populations much different in demographic structure from most marine fishes (Caley et al., 1996). Surfperches are also not major fishery species. Thus, studies of competition most relevant to California marine fisheries have involved rockfishes. Because rockfishes are increasingly overfished (Parker et al., 2000), understanding and conserving natural mechanisms of population regulation, such as competition, is of great relevance to fisheries management (see also Hixon and Webster, 2002). The fact that there is substantial competition between at least two species of rockfishes lends credence to the concept of ecosystem-based

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F I G U R E 17-10 Responses of (A) black perch (Embiotoca jacksoni) to removal of striped seaperch (E. lateralis), and (B) striped seaperch to removal of both black perch and shallow algae, compared to (C) an unmanipulated control site, all at Santa Cruz Island, California. Vertical lines show dates of manipulations. Data are number of fish along 30  4 m transects. After Hixon (1980a).

precautionary management and less reliance on clearly ineffective single-species fishery models (Weeks and Berkeley, 2000). Despite the relevance of studies of competition to fisheries management, there have been few studies of competitive interactions in California marine fishes since the 1980s. Has competition become irrelevant or out-of-date? Certainly, in general ecology, competition is no longer seen as the all-important predominant biotic interaction, as it was during the heyday of resource partitioning studies and niche theory in the late 1960s and early 1970s. However, competition is still common in nature (reviews by Connell, 1983; Schoener, 1983) and is now considered an interaction that occurs regularly when predation, physical disturbance, or harsh conditions do not

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preclude it. Clearly, there is much still to be learned regarding the role of competition in the dynamics of populations and the organization of natural communities of marine fishes of California and elsewhere.

Acknowledgments Many thanks to Larry Allen for inviting my participation, drawing figures (especially of fish), and editing the manuscript. Thanks also to Glenn Almany, Michael Horn, Michael Webster, and two anonymous referees for constructive reviews. Support during preparation of this chapter was partially provided by NSF grant OCE-00-93976 (Hixon). This chapter is dedicated to

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F I G U R E 17-11 Responses of (A) striped seaperch (Embiotoca lateralis) following removal of its primary foraging substrate (the dominant shallow alga Gelidium robustum, GR) at Santa Cruz Island, California (mean
SEM of two 40  2  2 m transects each), and (B) black perch (E. jacksoni) following addition of its primary foraging substrate (benthic turf) at Catalina Island, California (mean
SEM of four 2  2 m plots each). After Holbrook et al. (1990b).

F I G U R E 17-12 Long-term responses of surfperch (Embiotoca) species to reciprocal removals of congeners (“experimental sites”) compared to unmanipulated control sites at Santa Cruz Island, California. Solid symbols and lines are before manipulations, and open symbols and dashed lines are 4 years after manipulations. Data are number of fish along 40  2 m transects (mean
SEM, n  2 sites each). After Schmitt and Holbrook (1990b).

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Alfred Ebeling, a true pioneer in subtidal studies of the ecology of marine fishes of California.

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Ebeling, A.W., and R.N. Bray. 1976. Day versus night activity of reef fishes in a kelp forest off Santa Barbara, California. Fish. Bull. 74:703–717. Ebeling, A.W., and M.A. Hixon. 1991. Tropical and temperate reef fishes: comparison of community structures, p. 509–563. In: The ecology of fishes on coral reefs. P.F. Sale (ed.). Academic Press, San Diego, CA. Ebeling, A.W., and D.R. Laur. 1986. Foraging in surfperches: resource partitioning or individualistic responses? Environ. Biol. Fish. 16:123–133. Ellison, J.P., C. Terry, and J.S. Stephens, Jr. 1979. Food resource utilization among five species of embiotocids at King Harbor, California, with preliminary estimates of caloric intake. Mar. Biol. 52:161–169. Fretwell, S. 1981. Bringing ecology to scientific maturity. Am. Nat. 118:306. Grant, J.W.A. 1997. Territoriality, p. 81–103. In: Behavioral ecology of teleost fishes. J.-G.J. Godin (ed.). Oxford University Press, Oxford, UK. Grossman, G.D. 1980. Food, fights, and burrows: the adaptive significance of intraspecific aggression in the bay goby (Pisces: Gobiidae). Oecologia. 45:261–266. ———. 1986. Food resource partitioning in a rocky intertidal fish assemblage. J. Zool. 1:317–355. Haldorson, L., and M.G. Moser. 1979. Geographic patterns of prey utilization in two species of surfperch (Embiotocidae). Copeia 1979:567–572. Hallacher, L.E., and D.A. Roberts. 1985. Differential utilization of space and food by the inshore rockfishes (Scorpaenidae: Sebastes) of Carmel Bay, California. Environ. Biol. Fish. 12:91–110. Helfman, G.S. 1978. Patterns of community structure in fishes: summary and overview. Environ. Biol. Fish. 3:129–148. Hixon, M.A. 1980a. Competitive interactions between California reef fishes of the genus Embiotoca. Ecology 61:918–931. ———. 1980b. Food production and competitor density as the determinants of feeding territory size. Am. Nat. 115:510–530. ———. 1981. An experimental analysis of territoriality in the California reef fish Embiotoca jacksoni (Embiotocidae). Copeia 1981:653–665. Hixon, M.A., S.W. Pacala, and S.A. Sandin. 2002. Population regulation: historical context and contemporary challenges of open vs. closed systems. Ecology 83:1490–1508. Hixon, M.A., and M.S. Webster. 2002. Density dependence in reef fish populations, p. 303–325. In: Coral reef fishes: dynamics and diversity in a complex ecosystem. P.F. Sale (ed.). Academic Press, San Diego, CA. Hobson, E.S., and J.R. Chess. 1976. Trophic interactions among fishes and zooplankters nearshore at Santa Catalina Island, California. Fish. Bull. 74:567–598. ———. 1986. Relationships among fishes and their prey in a nearshore sand community off southern California. Environ. Biol. Fish. 17:201–226. Hobson, E.S., W.N. McFarland, and J.R. Chess. 1981. Crepuscular and nocturnal activities of Californian nearshore fishes, with consideration of their scotopic visual pigments and the photic environment. Fish. Bull. 79:1–30. Holbrook, S.J., M.H. Carr, R.J. Schmitt, and J.A. Coyer. 1990a. Effect of giant kelp on local abundance of demersal fishes: the importance of ontogenetic resource requirements. Bull. Mar. Sci. 47:104–114. Holbrook, S.J., and R.J. Schmitt. 1986. Food acquisition by competing surfperch on a patchy environmental gradient. Environ. Biol. Fish. 16:135–146. ———. 1989. Resource overlap, prey dynamics, and the strength of competition. Ecology 70:1943–1953. ———. 1992. Causes and consequences of dietary specialization in surfperches: patch choice and intraspecific competition. Ecology 73:402–412. ———. 1995. Compensation in resource use by foragers released from interspecific competition. J. Exp. Mar. Biol. Ecol. 185:219–233. Holbrook, S.J., R.J. Schmitt, and R.F. Ambrose. 1990b. Biogenic habitat structure and characteristics of temperate reef fish assemblages. Aust. J. Ecol. 15:489–503. Holt, R.D. 1984. Spatial heterogeneity, indirect interactions, and the coexistence of prey species. Am. Nat. 124:377–406. Hutchinson, G.E. 1961. The paradox of the plankton. Am. Nat. 95:137–145. Jacobson, L.D., and R.D. Vetter. 1996. Bathymetric demography and niche separation of thornyhead rockfish: Sebastolobus alascanus and Sebastolobus altivelis. Can. J. Fish. Aquat. Sci. 53:600–609.

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Keddy, P.A. 1989. Competition. Chapman and Hall, London, UK. Larkin, P.A. 1977. An epitaph for the concept of MSY. Trans. Am. Fish. Soc. 107:1–11. Larson, R.J. 1980a. Territorial behavior of the black and yellow rockfish and gopher rockfish (Scorpaenidae, Sebastes). Mar. Biol. 58:111–122. ———. 1980b. Influence of territoriality on adult density in two rockfishes of the genus Sebastes. Mar. Biol. 58:123–132. ———. 1980c. Competition, habitat selection, and the bathymetric segregation of two rockfish (Sebastes) species. Ecol. Monogr. 50:221–239. Larson, R.J., and E.E. DeMartini. 1984. Abundance and vertical distribution of fishes in a cobble-bottom kelp forest off San Onofre, California. Fish. Bull. 82:37–53. Laur, D.R., and A.W. Ebeling. 1983. Predator-prey relationships in surfperches. Environ. Biol. Fish. 8:217–229. Lavenberg, R.J., and A.W. Ebeling. 1967. Distribution of midwater fishes among deep-water basins of the southern California shelf, p. 185–201. In: Proceedings of the symposium on the biology of the California Islands. R. N. Philbrick (ed.). Santa Barbara Botanic Garden, Santa Barbara, CA. Lluch-Belda, D., R.J.M. Crawford, T. Kawasaki, A.D. MacCall, R.H. Parrish, R.A. Schwartzlose, and P.E. Smith. 1989. World-wide fluctuations of sardine and anchovy stocks: the regime problem. So. African J. Mar. Sci. 8:195–205. Lluch-Belda, D., R.A. Schwartzlose, R. Serra, R.H. Parrish, T. Kawasaki, D. Hedgecock, and R.J.M. Crawford. 1992. Sardine and anchovy regime fluctuations of abundance in four regions of the world oceans: a workshop report. Fish. Oceanogr. 1:339–347. Lorenzen, K., and K. Enberg. 2002. Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proc. R. Soc. Lond. B. 269:49–54. Love, M. 1996. Probably more than you want to know about the fishes of the Pacific coast. Really Big Press, Santa Barbara, CA. 2nd edition. Love, M.S., and A.W. Ebeling. 1978. Food and habitat of three switchfeeding fishes in the kelp forests off Santa Barbara, California. Fish. Bull. 76:257–271. Murdoch, W.W. 1994. Population regulation in theory and practice. Ecology. 75:271–287. Murphy, G.I. 1966. Population biology of the Pacific sardine (Sardinops caerulea). Proc. Calif. Acad. Sci. 34:1–84. Myers, R.A. 2002. Recruitment: understanding density-dependence in fish populations, p. 123–148. In: Handbook of fish biology and fisheries. 1. Fish biology. P.J.B. Hart and J.D. Reynolds (eds.). Blackwell Science, Malden, MA. Odum, E. P. 1953. Fundamentals of ecology. W. B. Saunders, Philadelphia, PA. Parker, S.J., S.A. Berkeley, J.T. Golden, D.R. Gunderson, J. Heifetz, M.A. Hixon, R. Larson, B.M. Leaman, M.S. Love, J.A. Musick, V.M. O’Connell, S. Ralston, H.J. Weeks, and M.M. Yoklavich. 2000. Management of Pacific rockfish. Fisheries 25:22–30. Peterman, R.M., and M.J. Bradford. 1987c. Density-dependent growth of age 1 English sole (Parophrys vetulus) in Oregon and Washington coastal waters. Can. J. Fish. Aquat. Sci. 44(1):48–53. Ross, S.T. 1986. Resource partitioning in fish assemblages: a review of field studies. Copeia 1986:352–388. Sale, P.F. 1979. Habitat partitioning and competition in fish communities, p. 323–331. In: Predator-prey systems in fisheries management. H. Clepper (ed.). Sport Fishing Institute, Washington, DC. Schiel, D.R., and M.S. Foster. 1986. The structure of subtidal algal stands in temperate waters. Oceanogr. Mar. Biol. Ann. Rev. 24:265–307. Schmitt, R.J., and J.A. Coyer. 1982. The foraging ecology of sympatric marine fish in the genus Embiotoca (Embiotocidae): importance of foraging behavior in prey size selection. Oecologia 55:369–378.

———. 1983. Variation in surfperch diets between allopatry and sympatry: circumstantial evidence for competition. Oecologia 58:402–410. Schmitt, R.J., and S.J. Holbrook. 1984. Gape-limitation, foraging tactics and prey size selectivity of two microcarnivorous species of fish. Oecologia 63:6–12. ———. 1986. Seasonally fluctuating resources and temporal variability of interspecific competition. Oecologia 69:1–11. ———. 1990a. Contrasting effects of giant kelp on dynamics of surfperch populations. Oecologia 84:419–429. ———. 1990b. Population responses of surfperch released from competition. Ecology 71:1653–1665. Schoener, T.W. 1974. Resource partitioning in ecological communities. Science 185:27–39. ———. 1982. The controversy over interspecific competition. Am. Sci. 70:586–595. ———. 1983. Field experiments in interspecific competition. Am. Nat. 122:240–285. Sette, O.E. 1943. Studies of the Pacific pilchard or sardine (Sardinops caerulea). I. Structure of a research program to determine how fishing affects the resource. U.S. Fish Wildlife Serv, Speci. Sci. Rept., 19. Sherman, K. 1990. Productivity, perturbations, and options for biomass yields in large marine ecosystems, p. 206–219. In: Large marine ecosystems: patterns, processes, and yields. K. Sherman, L. M. Alexander, and B.D. Gold (eds.). AAAS, Washington, DC. Smith, T.D. 1994. Scaling fisheries: the science of measuring the effects of fishing, 1855–1955. Cambridge University Press, Cambridge, UK. Sogard, S.M. 1997. Size-selective mortality in the juvenile stage of teleost fish: a review. Bull. Mar. Sci. 60:1129–1157. Soutar, A., and J.D. Isaacs. 1974. Abundance of pelagic fish during the 19th and 20th centuries as recorded in anaerobic sediment off the Californias. Fish. Bull. 72:257–273. Steele, M.A. 1997. The relative importance of processes affecting recruitment of two temperate reef fishes. Ecology 78:129–145. ———. 1998. The relative importance of predation and competition in two reef fishes. Oecologia 115:222–232. Stephens, J.S., R.K. Johnson, G.S. Key, and J.E. McCosker. 1970. The comparative ecology of three sympatric species of California blennies of the genus Hypsoblennius Gill (Teleostomi, Blenniidae). Ecol. Monogr. 40:213–233. Stouder, D.J. 1987. Effects of a severe-weather disturbance on foraging patterns within a California surfperch guild. J. Exp. Mar. Biol. Ecol. 114:73–84. Strong, D.R., D. Simberloff, L.G. Abele, and A.M. Thistle. 1984. Ecological communities: conceptual issues and the evidence, p. 613. Princeton University Press, Princeton, NJ. Tanasichuk, R.W. 1997. Influence of biomass and ocean climate on the growth of Pacific herring (Clupea pallasi) from the southwest coast of Vancouver Island. Can. J. Fish. Aquat. Sci. 54:2782–2788. Weatherley, A.H. 1972. Growth and ecology of fish populations. Academic Press, London. Weeks, H., and S. Berkeley. 2000. Uncertainty and precautionary management of marine fisheries: Can the old methods fit the new mandates? Fisheries. 25(12):6–15. Wiens, J.A. 1977. On competition and variable environments. Am. Sci. 65:590–597. Wooton, R.J. 1990. “Dynamics of population abundance and production.” Ecology of Teleost Fishes, Chapter 10, R.J. Wooton, Chapman and Hall, NY. Yoshiyama, R.M. 1980. Food habits of three species of rocky intertidal sculpins (Cottidae) in central California. Copeia 1980:515–525. ———. 1981. Distribution and abundance patterns of rocky intertidal fishes in central California. Environ. Biol. Fish. 6:315–332.

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CHAPTER 18

Disturbance D EAN NA J. STO U D E R AN D M I C H E LLE L. McM U LLI N

Introduction Disturbance influences all elements of ecological organization (Pickett & White, 1985). Previous chapters on community organization (unit IV) have discussed important biological elements that may contribute to the organization of California marine fish assemblages, yet physical disturbance affects all of these (i.e., feeding and trophic interactions, dispersal, recruitment, predation, and competition). Despite limited information on the role of natural disturbance in California marine systems, we will describe examples on the effects of hypoxia, freshwater inflows, salinity changes, and storms on fish assemblages. We use Pickett and White’s (1985) definition of disturbance as “any relatively discrete event in time that disrupts ecosystem, community, or population structure and changes resources, substrate availability, or the physical environment.” There is some disagreement and confusion among ecologists in defining disturbance. While the above definition is commonly used and includes both the cause and effect, others advocate referring only to the causes of disturbance without referring to the effects (Lake, 2000). However, the purpose of this chapter is to present a generalized perspective on the influence of disturbance on assemblage organization. It remains important, especially for scientific study of disturbance ecology, to understand that the characteristics of disturbances differ. A general definition of disturbance is useful because it necessitates specification of scale and process for every event in relation to the organism(s) and ecosystem(s) involved. Natural disturbance is a natural occurrence! It is an intrinsic property of ecosystems and is not a deviation from a normal state. Thus the definition must be understood relative to spatial and temporal contexts and relative to the appropriate hierarchical levels of community and assemblage organization. Not only does this definition require a description of the cause (mechanism) of disturbance, it also requires a description of the effect (response). It is useful to describe the mechanism and response of disturbances while maintaining the premise that disturbance happens at different frequencies and magnitudes. Thus, responses reflected in marine temperate fish assemblages, as in many others, will vary widely. Disturbance may incorporate both short- and long-term changes at both local and larger spatial scales; examples of

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disturbances that result in long-term changes include El NiñoSouthern Oscillation (ENSO) and global warming (see chapters 1 and 26). Disturbance may elicit both physiological and behavioral responses in fishes, but in this chapter we will include mostly behavioral responses (especially those behaviors included in unit IV). Anthropogenic disturbances will be covered in Unit V.

Theoretical Context A whole host of theoretical constructs exist to describe the outcomes of disturbance. These theories operate with the premises of equilibrium or non-equilibrium conditions. For equilibrium conditions to occur, the rate of increase (e.g., immigration, population increase) must equal the rate of decrease (e.g., emigration, mortality). These constructs of equilibrium can be applied to ecological processes and species changes. Several equilibrium-based hypotheses have been suggested including Niche Diversification and Compensatory Mortality (Connell, 1978). Ebeling and Hixon (1991) noted that there is no evidence in temperate reef fish systems to support or refute another equilibrium hypothesis—Circular Networks (Jackson and Buss, 1975; Connell, 1978). The Niche Diversification Hypothesis predicts that because populations are at equilibrium, competition either past (“ghost of competition past,” Connell, 1980) or present drives the evolution of specializations to minimize competition among species. In other words, species within assemblages partition resources (i.e., habitat, prey, time) to coexist. Ebeling and Hixon (1991) reviewed 26 studies of temperate rocky reef fishes and determined that 88% supported, or could support, the concept of competition and therefore niche diversification among species. They noted that the experimental evidence is even stronger (all 12 experimental studies they reviewed generally supported the Niche Diversification Hypothesis; Ebeling and Hixon (1991)). In contrast, the Compensatory Mortality Hypothesis (Connell, 1978) predicts that highest mortality will occur on the strongest competitors or the most abundant species within the community. Mortality is therefore density dependent and elimination by competition among species is absent.

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Equilibrium seldom occurs. Changes and disruptions occur often, therefore species assemblages are rarely constant. Nonequilibrium theories include: the Intermediate Disturbance (Connell, 1978), Equal Chance or Lottery (Sale, 1977, Hubbell, 1979), and Gradual Change (Hutchinson, 1961, Connell, 1978) Hypotheses. The Intermediate Disturbance Hypothesis suggests that at low levels or rates of disturbance species diversity will be low due to the predominance of dominant or climax species. When disturbances are large or frequent, diversity will also be low because colonizing or pioneer species will be prevalent. At intermediate levels of disturbance, species diversity is highest because neither biological (i.e., competition, predation) nor physical (i.e., habitat change) processes are favored keeping local assemblages at a non-equilibrium state. However, Mackey and Currie (2000) reviewed 130 published studies examining the relationship among species richness, for a range of terrestrial and aquatic systems, and disturbance and found that only 19% exhibited highest levels of species richness with intermediate disturbance levels. In the Equal Chance or Lottery Hypothesis species composition and total abundance of individuals within a guild should remain relatively constant, even though local populations may vary in size. In these situations space is limited and unpredictable disturbances create open spaces. Patches or entire reefs may become available and filled, in a random order, by individuals from the plankton. Therefore, the unpredictability of the process prohibits one species from dominating or displacing another. Environmental variation that occurs on seasonal and even decadal to longer time scales (e.g., El Niño, global climate change) favors a Gradual Change in species composition. This occurs because the changing environment favors different species over time, therefore preventing one species becoming more dominant within the assemblage. Species will track the environment but the populations never reach equilibrium because resource availability changes at a different rate than species’ responses. Temperate reef fishes (e.g., Embiotocids, Scorpeanids), in regions where seasonal variation in temperature is common, exhibit patterns consistent with this hypothesis (see Ebeling and Hixon, 1991 for review).

Defining Disturbance It is our premise that natural disturbances are important agents of change in ecosystems. Various characteristics such as spatial scale and time of disturbance result in differential abilities of species (and ecosystems) to respond. Generally, the impacts of disturbance can be addressed by asking questions such as: How big is it?; How complete is the disturbance?; and How close are disturbances to each other? Disturbance characteristics include distribution, area (or size affected), frequency, predictability, magnitude (intensity versus severity), and the synergism or interactions among these characteristics (White & Pickett, 1985, see table 1-1 chapter 1). Fishes are, by definition, mobile, however, the relative types and rates of mobility differ. The size and distribution of disturbances across a particular location or ecosystem can influence whether mobile organisms can avoid or respond. If the disturbed area is small, mobile species or individuals may take advantage of adjacent undisturbed areas. In contrast if the affected areas include an entire reef or bay, organisms may be unable to leave the location (due to physiological

constraints), to respond without risk of predation (by the need to travel across large open areas), or successfully compete for remaining intact locations. Both the frequency and predictability of disturbance can affect the ability (and adaptability) of fishes to respond. If disturbance events are frequent (i.e., the time interval between disturbances is short) and predictable (e.g., always occur at the same time of year), species that are successful in seeking refuges during disturbances may be able to survive. However, frequent or unpredictable disturbances may only enable the existence of those individuals or species that just happened to be “in the right place at the right time.” As the interval between disturbances becomes longer and possibly more predictable (e.g., winter storms on coastal reefs or estuaries) species may have adapted responses to these local conditions. Assemblages, and therefore ecosystems, may be incapable of changing in any predictable way to even longer interval duration events such as ENSO and global climate change. In situations, such as these, physiological constraints may be the primary driver in species’ responses and therefore the resulting community and assemblage structure. The disturbance magnitude, either intensity (force per event per unit time) or severity (impact) can also affect species’ and ecosystem responses. It would not be unusual for some or all of the above mentioned disturbance characteristics to interact and work synergistically. This may increase the relative impact of any particular disturbance. In general, physical disturbance decreases the benefits gained by fishes but this can vary by species, life stage, and assemblage structure. Disturbances lead to spatial and temporal variation in habitat and ultimately species composition. Biologically driven (e.g., predation, grazing, parasites, and disease) and anthropogenic (e.g., pollution, habitat destruction, and low oxygen) disturbances also affect fish assemblages, however, anthropogenic disturbances will be described in the Pollution and Habitat Alteration chapter within this volume (see chapter 24). Relevant questions for organisms responding to disturbance include. Where is the organism at the time?; What is the organism doing?; and At what life stage is the organism? Thus, the impacts of disturbance vary with habitat type (e.g., estuaries, tidal habitats, and rocky reefs), life history stages (e.g., eggs, larvae, and adults), behavior (e.g., habitat use, feeding), and timing (i.e., are the organisms in the right/wrong place at the right/wrong time?).

Natural Disturbance Natural disturbances occur at different frequencies and magnitudes in marine coastal systems. Seasonal changes including variation in tidal heights and magnitude of wave and wind action can affect organisms and ecosystems in predictable ways. For example, California giant kelp (Macrocystis pyrifera) beds change seasonally, and as a result of decadal oscillations. These changes alter habitat characteristics for fish use, recruitment, prey availability, and a host of other conditions. When the magnitude or frequency of winter storms increases the impact of these disturbances can be devastating to marine communities and assemblages. Climatic change (discussed in more detail in chapter 1) can cause unusual or unseasonal temperature shifts. In addition, climate changes that alter seasonal rains and influence temperature (e.g., causing droughts, higher than average rainfall, etc.) can affect aquatic systems by changing water quality. Increased runoff from higher than

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average rainfall can decrease salinity in coastal areas (e.g., bays, estuaries, and sea grass beds), whereas droughts may cause increased salinity in these areas. Similarly, as temperatures increase above historical normal levels (possibly as a consequence of pollution), coastal areas may develop depleted oxygen levels (hypoxic) and become lethal to many organisms.

Direct versus Indirect Effects of Disturbance Although disturbance may affect fish assemblages directly due to instantaneous mortality (i.e., death) and subsequent disruption of interrelationships among species, this has been documented infrequently. Indirect effects may ultimately be a more pervasive impact for mobile organisms. If habitat structure is of primary importance in characterizing the fish assemblages then disturbances that result in habitat modification or degradation are likely to assert more profound or long-term effects (Jones and Syms, 1998, Syms and Jones, 1999). Impacts of disturbances can be negative if habitat changes affect habitat heterogeneity and complexity, prey distribution and abundance, and limit refuges and spawning habitat. The potential costs to fishes are weight loss, decreased or zero fitness, increased vulnerability to predators and disease, and eventually death. Fishes have ways to minimize costs so the consequences of disturbance do not always have to be strongly negative. Individuals can move away from the affected area by changing location or leave the disturbed site. For generalist fishes, they may be able to alter what they eat, where they eat, and possibly how much they eat to adjust to changes in prey types, abundance, and locations. Fishes can also change behaviors to minimize energy expenditures. For example, it may be beneficial for territorial fishes (e.g., garibaldi (Hysypops rubicundus)) to minimize energy spent defending territories. Similarly, some fishes may postpone reproduction or produce fewer offspring to minimize the energy expenditures to eggs and young. In general the costs of disturbance can be negative, but unless the direct effect of disturbance is death, fishes usually have mechanisms to minimize the costs to enable them to survive.

Examples of Disturbance Hypoxia Hypoxia in coastal marine environments is an example of disturbance affecting assemblage structure and function through behavioral and physiological responses of predators and prey. Due to vertical stratification on a seasonal or tidal basis, low oxygen concentrations occur in bottom waters. As a consequence, hypoxia can reduce the availability of suitable habitat. The increased frequency of hypoxia occurrence is usually due to high nutrient loading resulting from human activities. Mortality is a direct result of hypoxia, but tolerances differ among species and life stages, potentially affecting species composition and abundance. Other physiological responses may include reduced fitness and growth. Hypoxia also affects organisms through indirect effects such as distribution or habitat shifts, and behavioral changes (Wannamaker and Rice, 2000). This combination of individual physiological and behavioral responses to hypoxia may ultimately influence community structure and function. Hypoxia occurs in many locations worldwide. Hypoxia off the California coastline may be an infrequent or rare occurrence

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due to predominant and persistent upwelling and this is not a well-studied subject in California. Oxygen levels can decrease as a consequence of local and climatic conditions. Climate shifts change the amount of upwelling off coastal California, thereby altering the distribution of the oxygen minimum layer. Prior to upwelling, this layer (comprised of low oxygenated and high salinity water) remains offshore and fishes are distributed throughout inshore waters (fig. 18-1). During periods of upwelling, the oxygen minimum layer becomes distributed in shallower and inshore areas causing increased concentrations of benthic and epipelagic fishes. In tidepools with algae or marine plants, oxygen concentrations and pH can increase during the day and decrease at night. Congleton (1980) observed species distributions in tidepools near La Jolla, California. Despite being one of the most common southern California tidepool fishes, spotted kelpfish (Gibbonsia elegans) were never observed in tidepools at night. Woolly sculpin (Clinocottus analis) and reef finspot (Paraclinus integripinnis) were present, but were observed to move to the surface or to shallow water and performed ventilation (i.e., passed water over gills). Using cage and respirometry experiments Congleton (1980) determined a higher critical oxygen concentration level for the spotted kelpfish than that of the woolly sculpin or the reef finspot. As oxygen concentrations in the tidepools decreased below the critical oxygen concentration levels for all three species, behavioral responses including ventilation proved useful and may be necessary for survival. These results explain the absence of spotted kelpfish in tidepools at night. Although oxygen depletion may be historically uncommon, it may become more common as anthropogenic disturbances become more prevalent. Estuaries, including those in California, are highly productive habitats containing important refuge, nursery, and nutrient-rich habitats for ecologically and economically valuable fishes. Persistent hypoxia may influence distribution and abundance patterns of important commercial and recreational fisheries. For this discussion, we will primarily use two other locations to illuminate the effects of hypoxic disturbance on community structure of estuarine and marine fishes, and to demonstrate differences in size, duration, and timing that may explain differential responses of fishes exposed to these events. Spatial and temporal patterns of hypoxia may differ among locations. In the Kattegat, Sweden, annual autumn hypoxia occurs at depths of one to ten meters above seabed over a 3,000-km2 area for approximately four months (fig. 18-2; Pihl, 1994). Such extensive and prolonged seasonal periods of hypoxia have resulted in decreased demersal fish biomass, decreased benthic invertebrates, changing species composition, potential dominance of pelagic over demersal species, and both long-term and seasonal shifts in fish diets and available prey items (Pihl, 1994; also see review by Breitburg, 2002). In the mouth of the York River, Chesapeake Bay, hypoxia occurs on a cyclical basis throughout the summer lasting only six to 14 days at depths greater than ten meters (fig. 18-3; Pihl et al., 1992). Shorter duration, cyclical hypoxic episodes affecting a smaller area may allow exploitation of sensitive benthic invertebrates by mobile opportunistic fishes resulting in short term diet shifts (Pihl et al., 1992). Other studies in the Chesapeake Bay have focused on episodic intrusions of oxygen depleted bottom waters into nearshore shallow waters (fig. 18-4; Breitburg, 1992). Diel fluctuations characterized by rapidly changing dissolved oxygen concentrations can shift spatial distributions and bias population size structure toward older and larger or younger and smaller individuals depending on

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F I G U R E 18-1 Impact of upwelling on the distribution of benthic and pelagic fishes along the coast of southern California

(after and with permission of Southern California Coastal Water Research Project).

the timing of recruitment (Breitburg, 1992). Alterations in community structure may also affect trophic interactions, food web structure, and reproductive behavior. HAB ITAT S E LECTION AN D US E

Direct mortality is an immediate result of disturbance. Under low oxygen concentrations, decreased survival of many fishes occurs. However, mortality can vary with age, size, or species, and this variability is the result of a range of tolerances to the event itself, mobility, and behavior. Fish larvae may be more susceptible to hypoxic exposure because they lack fully devel-

oped sensory and motor capabilities. For example, dissolved oxygen concentrations significantly decreased pre- and postflexion naked goby (Gobiosoma bosc) larvae survival in experimental studies, but not larger juvenile or adult survival (Breitburg, 1992, 1994). Larvae also exhibited an immediate behavioral avoidance response to low bottom water oxygen concentrations. While naked goby larvae avoided oxygen concentrations of 0.75 mgL
1, adults did not respond until oxygen concentrations fell below this level. Many fishes, including naked goby, bay anchovy (Anchoa mitchilli), juvenile spot (Leiostomus xanthurus), pinfish (Lagodon rhomboids), croaker (Micropogonias undulates), menhaden (Brevoortia tyrannus),

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FIGURE 18-2 Mean (and SD) oxygen concentration in bottom water in the study area in the southeast

Kattegat from 1984 to 1988. Measurements where conducted at five to six stations (0.5 m above the sediment surface) on each sampling occasion. Dates for demersal fish sampling are indicated by arrows. (after Pihl, 1994).

F I G U R E 18-3 Daily mean salinity, temperature, and oxygen concentration in the bottom water (18 m depth) in the York River (26 June to 20 October 1989) (after Pihl et al., 1992).

white mullet (Mugil curema), mummichog (Fundulus heteroclitus), striped bass (Morone saxatilis), and flounder (Paralichthys lethostigma) are capable of detecting and responding to hypoxia (Breitburg, 1994, Wannamaker and Rice, 2000). Because hypoxia typically occurs only in bottom waters, mobile fishes may utilize surface waters as refuges (i.e., vertical water column migration in stratified waters), or fishes may

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also migrate to shallow waters where oxygen levels are sufficient. Although some species may detect hypoxic conditions, they may not avoid the area (e.g., mummichog) or the response may differ by species (Wannamaker and Rice, 2000). Differential mortality, avoidance ability, and subsequent recolonization following hypoxia may ultimately result in modified distributional patterns.

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F I G U R E 18-4 Daily maximum (open circle) and minimum (closed circle) dissolved oxygen concentrations at the mid (4 m) site during 1987 and at the mid and shallow (2 m) sites during 1988. Data are from DataSonde deployments. Arrows indicate severe intrusions (after Breitburg, 1992).

F E E DI NG AN D TROP H IC I NTE RACTION S

Seasonal variation in fish diet has been linked with seasonal variation in mean oxygen concentrations (Pihl, 1994). Both fish feeding behavior and food resources may be altered by hypoxic conditions (e.g., limiting or changing availability, increasing or decreasing food amounts, altering nutritional values) (Pihl et al., 1992, Pihl, 1994). Fishes may also reduce the time spent searching for food and feeding due to lowered oxygen levels (Bejda et al., 1987, Breitburg et al., 1994). Lower oxygen levels may inhibit prey escape behaviors, increase prey vulnerability or predation risk, and reduce predator attack rates (Breitburg et al., 1997). Predator and prey species may experience differential tolerances, detection rates, migration responses, and survival to hypoxia, which may ultimately influence encounter rates

(Breitburg et al., 1997, Keister et al., 2000). At higher dissolved oxygen levels predation rates may increase as well as prey migration toward these locations thereby crowding predators and prey and potentially increasing prey mortality (Breitburg, 1994). These various combinations of behavioral and physiological responses of individual predator and prey species to hypoxia may ultimately lead to changes in the trophic structure. R E P RODUCTION

Reproductive behaviors may also change due to hypoxia. For naked gobies exposed for extended periods of time to nearlethal oxygen concentrations, fish abandoned nests and shelters because of a lack of embryo tolerance (Breitburg, 1992). Prior to abandonment, guarding males appeared stressed and

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F I G U R E 18-5 Ventilation rates for spot, pinfish, mul-

let, and croaker at all dissolved oxygen levels tested. Ventilation rate increased with declining oxygen for all species tested. Regression equations and P values for each species are given in the legend (after Wannamaker and Rice, 2000).

increased ventilation rates, and some males died without abandoning nests or shelters. Obligation to nest or shelter may reduce mobility and limit survival by negating avoidance or migration capabilities. Yet early escapement may be selected against because males typically have only one year of reproductive output and because of increased predation risk when they move away from shelter. In addition, because fecundity is generally size-dependent, a disturbance that affects the population size structure may alter reproductive output. R ECR U ITM E NT

Newly settled recruits may have increased sensitivity to low dissolved oxygen and lower survival rates than larger juveniles and adults (see Habitat Selection and Use above). If the highest settlement occurs in deep and mid-waters where hypoxic events are more common, recruitment can be hampered and population structure affected by hypoxia if the timing is coincident with settlement (Breitburg, 1992). Therefore, post-disturbance recolonization may not be dependent upon reproduction if large juveniles and adults that escape or migrate to avoid hypoxic conditions can later recolonize the deeper water habitats. C OM P ETITION

Hypoxia may also influence intraspecific competitive interactions as demonstrated by red hake (Urophycis chuss; Bejda et al., 1987). Agonistic encounters significantly decreased for age 0
red hake with decreasing dissolved oxygen. There was also a trend toward increased agonistic behavior for age 1
red hake.

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In addition, multiple age 1
fish were observed resting together in shelters, a highly unusual behavior. F ITN E S S AN D G ROW TH

In addition to mortality and behavioral changes, hypoxia can also affect growth through increased energy allocation to ventilation. These rates increase with decreased oxygen levels for several species including spot, pinfish, croaker, and white mullet, and rates were higher for pinfish and mullet than for spot and croaker (fig. 18-5; Wannamaker & Rice, 2000). Any deviation from normal energy allocations during a disturbance may result in decreased fitness. Some fishes may benefit from disturbance. Avoidance through migration for mobile organisms is an ideal means to mitigate for potentially harmful environmental conditions. Mobile foraging on vulnerable prey may allow for continued feeding and growth during hypoxic conditions (Pihl et al., 1992, Pihl, 1994, Rahel and Nutzman, 1994). Other fishes may use aquatic surface respiration (e.g., gulping) during hypoxic conditions, thereby allowing for survival, normal activity, and even growth. Todd and Ebeling (1968) determined that longjaw mudsucker (Gillichthys mirabilis), from Californian lagoons and tidal sloughs, is capable of aerial respiration when inhabiting poorly oxygenated waters. Although hypoxia is a rare or unstudied disturbance in California estuaries, it does occur commonly worldwide. Hypoxia may become more common with increasing anthropogenic activities and with natural climate shifts that influence patterns of upwelling, stratification, or nutrient enrichment. In other locations as described above, hypoxia causes

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F I G U R E 18-6 Mean delta smelt catches

per trawl (lines) in the three regions in the Sacramento-San Joaquin estuary during the periods before (January 1981–September 1984) and after (October 1984–December 1988) the collapse of delta smelt populations. The location of the mixing zone is indicated by large differences (bars, parts per thousand) between salinities of surface and bottom waters in upstream areas. Upstream stations are to the right (after Moyle et al., 1992).

mortality, reduces suitable habitat, and affects all levels of assemblage organization.

Freshwater Inflows and Salinity Freshwater from streams, rivers, and across impermeable surfaces can alter local circulation patterns, salinity, and sediment in coastal marine systems. This is especially true in bays, estuaries, lagoons, and tidal pools where freshwater can become concentrated. These areas can also become isolated from adjacent coastal marine water due to the formation of sand bars and extremely low tides. As water chemistry and quality change, tolerance by fishes to adjust to new conditions varies with species. HAB ITAT S E LECTION AN D US E

Drought conditions may also influence the assemblage structure of coastal California fishes through the role of freshwater inflow. The distribution of some marine, estuarine, freshwater, and anadromous species within San Francisco Bay varied in response to wet or dry years (Armor and Herrgesell, 1985). Observed distributional changes appeared to be associated mostly to flowrelated changes in salinity and circulation patterns. Some species, particularly the endemic delta smelt (Hypomesus transpacificus), were declining in abundance and experiencing persistent distribution shifts due to increased salinity concentrations with decreased riverine inflow (fig. 18-6; Moyle et al.1992; but see Moyle et al., 1986). Decreased riverine inflow may also reduce and shift the mixing zone to the river mouths or even confine it within the river channel. In addition to habitat reduc-

tion, decreased riverine inflow may also decrease availability of food. While decreased riverine inflows associated with drought are usually sporadic (except in the case of prolonged drought), anthropogenic disturbance in the form of water diversion for urban and agricultural uses potentially mimics drought year conditions but has far more persistent effects. As a consequence, the lower San Joaquin River essentially flows upstream at certain times of the year, and often during the delta smelt spawning season, a result of diversion (Moyle et al., 1992). During drought years human and industrial demand for water often increases. F ITN E S S AN D G ROW TH

Intertidal areas, bays, lagoons, and estuaries can experience higher than normal salinity. High salinity concentration may be lethal to some species. Often salinity changes can be confounded by temperature, pH, dissolved oxygen, and food availability. Carpelan (1961) describes a study in a coastal California lagoon of increasing salinity levels and serial elimination of fishes when species became trapped in the lagoon by a sand bar. Of 10 species trapped when lagoon closed, only three species were still present at salinity levels of 60%. These three remaining species were euryhaline species.

Storms Severe storms off the southern California coast in the 1970’s and 1980’s were excellent opportunities to study the effects of disturbance on near shore lagoons and marine temperate reef assemblages. These natural disturbances, combined with

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F I G U R E 18-7 A) Naples Reef near Santa Barbra, California prior to the severe storm of February 1980. B) Naples Reef

after the storm eliminated overstory kelp and sea urchins grazed much of the reef flat microhabitat. RS, reef slope; RCr, reef crest; RF, reef flat; RCo, reef cobble; DCo, deep cobble (after Stouder, 1987).

experimental studies in California, provided a wealth of information regarding how disturbance may affect multiple aspects of temperate reef and lagoon assemblages. Storm disturbances have also influenced the organization in other marine assemblages including coral reefs (Kaufman, 1983, Lassig, 1983, Woodley et al., 1991). On temperate Californian reefs, macroalgal stands provide physical habitat structure. The physical substratum upon which the kelp grows provides additional habitat. Rock, sand, and cobble are predominate substrates and reef contour ranges from nearly flat to large rocky outcrops with high vertical relief and complex structure (Bodkin, 1988). Macroalgal stands are primarily composed of giant kelp, a surface canopy species, and Laminaria spp., Pterygophora californica, and Eisenia arborea as understory components, and associated turf algae (see chapter 7 for additional information on rocky reefs and kelp beds). Macroalgal abundance, density, and biomass fluctuate in time through biotic disturbance (e.g., grazing) and abiotic disturbance (e.g., severe turbulence associated with storms, water temperature, nutrient availability) (Carr, 1994a). The size, shape, and structural architecture of individual plants can change in response to changes in plant density (Carr, 1994a). Seasonal variation in macroalgal stands can occur due to plant life cycles (e.g., growth and senescence). Storm effects on kelp beds vary as a function of frequency, magnitude, exposure, timing, and macrophyte and substratum characteristics (Dayton and Tegner, 1984). These effects also result from “storm of the century” type

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events including hurricanes and ENSO-related events, but any severe storm occurring with greater than expected magnitude can be a disturbance. Severe storms often change the physical habitat of temperate reefs and the typical result of these storms is reduction in overstory canopy, primarily by decreasing giant kelp stands (see fig. 18-7). However, this depends on the status of the temperate reef community at the time of disturbance; at times when kelp stands are not present storms may create conditions allowing for enhanced kelp growth (Ebeling et al., 1985). As macroalgal stands compose a large portion of the physical structure on temperate reefs, many fish species are associated with the habitat they provide. Due to differential relationships between macroalgal habitat and fish species and age classes, responses to disturbances will be species and age dependent. Because disturbance alters habitat characteristics we will focus this discussion on those species and age classes affected by modification and potential simplification of physical structure (i.e., macroalgal stands). Disturbance may also result in direct mortality of kelp-forest fishes in the event of extraordinarily large waves and resultant stranding (Bodkin et al., 1987). HAB ITAT S E LECTION AN D US E

On Naples Reef near Santa Barbara, CA, adult and young-ofyear (YOY) surfperch are differentially distributed (Ebeling and Laur, 1985). Young surfperch use the kelp canopy as refuge from predation and are most abundant on the portion of the reef

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F I G U R E 18-8 Bimonthly means ( SEM) of pooled sea urchin counts (Strongylocentrotus franciscanus  S. purpuratus), percent cover of understory kelp (mosly Pterogophora californica), surfperch (Embiotocidae) densities, and percent cover of algal turf at monitored transect sites on Naples Reef before and after Storms I and II. Numbers next to urchins and fish means are sample sizes (after Ebeling et al, 1985).

with significantly higher percent algal cover. Their densities vary seasonally and most young surfperch regularly disappear in autumn as kelp senesces. When kelp stands were diminished in 1980 by storms, YOY surfperch were no longer observed and remained absent during 1981. However, YOY surfperch were once again sighted in 1983 concurrent with kelp stand recovery. Adult surfperch and kelp bass densities were not correlated with kelp loss (fig. 18-8). In an experimental kelp thinning study on Naples Reef to evaluate the influence of structure for YOY surfperch, counts were consistently lower in the thinned treatment plot than in the control plot, and thinning had no effect on adult surfperch (Ebeling and Laur, 1985). At Pt. Piedras Blancas, a similar kelp removal experiment was performed to test the effect on Sebastes (rockfish) spp. (Bodkin, 1988). Prior to treatment, midwater rockfish species composition was very similar with juveniles more abundant in the treatment site and adults more abundant on control site; benthic species were consistent in composition and abundance. After treatment, the assemblage in the treatment site changed, but there was no assemblage change in the control site. In the experimental site, seven species declined in the abundance following removal of the giant kelp canopy. In addition, the estimated overall biomass decreased approximately 63%. Within the control site, juvenile rockfish decreased in abundance while adult S. melanops (black rockfish) increased. The changes in abundance at the control site may have resulted from emigration out of the experimental site. Benthic species changed little as midwater species accounted for 65% of post-treatment changes. Storms can also effect habitat changes in near shore soft bottom ecosystems through sediment deposition. In Mugu Lagoon, a small estuary in southern California, sedimentation has been associated with very severe, normally rare, storms resulting in increased rainfall (Onuf and Quammen, 1983). The wettest season in the 36-year history of the Point Mugu meteorological station occurred between March 10, 1977 and May 16, 1978. One storm episode, occurring between February 5 and 13, 1978, released 20.7 cm of precipitation in nine days; a second major storm episode occurred

in February 1980 (Onuf, 1987). As a result of these two storm episodes the average lagoon depth and volume at low tide decreased 38% (Onuf and Quammen, 1983). Sediment deposition affected sample sites differently. In two sample sites (Sites 2 and 3; See fig. 18-9) large proportions of eelgrass (Zostera marina) were entirely or partially covered by sediment and declined through time. Prior to the storm episodes, one site (Site 1) increased from 1% eelgrass to 20% by the end of the study (Onuf and Quammen, 1983). From 1978 to 1981 fish catch and abundance exhibited both short-term and persistent changes. After storms shortterm effects were evidenced by decreases followed by slight increases, while persistent effects were supported by approximately 50% overall reduction (fig. 18-9). If changes in substrate strongly influenced fish abundance and composition, then demersal fishes should have changed accordingly. However, only one (i.e, California tonguefish (Symphurus atricauda)) of the seven demersal species exhibited a storm-associated change in abundance (Onuf and Quammen, 1983). Although bottom substrates became finer following sediment deposition, substrate was not a primary determinant of fish abundance patterns. Sediment deposition resulted in an overall decrease in lagoon water depth. Water column species, topsmelt (Atherinops afffinis), shiner perch (Cymatogaster aggregata), and bay pipefish (Syngnathus leptorhynchus) decreased in abundance as water became shallower. In one site, bay pipefish increased in areas where remnants of eelgrass beds remained (Site 1) although overall numbers decreased. Shiner perch, however, disappeared from the lagoon and did not recover pre-storm abundances (Onuf and Quammen, 1983, Onuf, 1987). Depth and cover were important determinants of fish abundance, and acted synergistically for a number of species. Species are positively or negatively associated with macroalgal stands for multiple reasons. Younger fishes may rely on the refuge the plants provide from predation and all ages may forage on prey within the stands. So, in addition to habitat selection and use, disturbance may also influence feeding and trophic relationships, reproduction, and recruitment.

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F I G U R E 18-9 The characteristics of sampling sites in Mugu Lagoon, California and the locations where different species were most commonly caught in 1977 and in 1981. Significantly higher (up) abundance in 1981 than 1977 are represented by arrows; lower (down) (after Onuf, 1987).

F E E DI NG AN D TROP H IC I NTE RACTION S

In another study on Naples Reef, surfperch species altered microhabitat use following the 1980 storm (Stouder, 1987). Fishes concentrated on reef slope and reef crest microhabitats, and spent less time in reef cobble, deep cobble, and reef flat microhabitats. These changes in microhabitat use were associated with changes in food abundance. Microhabitat overlap also increased following the storm (fig. 18-10). Although foraging patterns changed, diet did not change significantly. Ebeling et al. (1985) also examined surfperch abundance patterns following storms on Naples Reef. They monitored components of the reefs detrital-based food chain from 1979 through 1983, a period which incorporated two important storms. The 1980 storm removed the giant kelp canopy and created bare rock conditions. Understory and turf algae persisted for a short time, but removal of the giant kelp stands also reduced available detrital drift, a major food source of sea urchins. Sea urchin grazing removed any remaining macroalgae, new sporophytes, and the understory and turf algae creating a barrens-type habitat on the reef as sea urchin populations increased. Surfperch densities were correlated with turf algae and declined during the barrens period (fig. 18-11). A second severe storm occurred in 1983, which killed large portions of the sea urchin population, allowing recruitment and regrowth of giant kelp stands and an increase in detrital drift and surfperch densities. Trophic connections may be altered as prey species shift habitat use in response to disturbance. In the Pt. Piedras Blancas kelp thinning experiment discussed above, juvenile

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rockfish species, principally blue rockfish (S. mystinus), declined following treatment (Bodkin, 1988). For blue rockfish, a reduction in giant kelp translated into a reduction in foraging substrata and refugia. Juvenile blue rockfish are important prey for piscivorous kelp forest fishes, thus the removal of blue rockfish foraging base and nursery habitat leads to loss of prey for predators, which may limit overall kelp forest fish abundance (Bodkin, 1988).

R E C R U ITM E NT

Attributes of the benthic environment effect settlement and post-settlement survival in temperate reef fishes (Carr, 1994b). Therefore, disturbance events that change the benthic environment may change patterns in recruitment, potentially leading to changes in size and age structure, abundance, distribution, and dynamics of local populations. For example, YOY rockfish shifted their use of substrata and algal habitat types in response to diminished giant kelp and drift algae abundance following annual winter storms (Carr, 1991). Species recruitment is often positively influenced by the presence of giant kelp on temperate reefs. For other species, including island kelpfish (Alloclinus holderi) and other kelpfishes (Gibbsonia spp.), recruitment is negatively associated with macroalgal stands, usually due to indirect effects upon the understory algae (Carr, 1989). Fishes respond to the presence or absence of macroalgal stands, as well as the architectural features of individual plants that may change based on plant density (Carr, 1994a). For example, larval recruitment of kelp bass (Paralabrax clathratus) increases linearly with increasing structural com-

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on Recruitment). Based on these interspecific differences, Carr (1994a) developed a predictive recruitment response model for three species [using data for kelp bass (Carr, 1994b) and kelp perch (Brachyistius frenatus; Anderson, 1993) from California, and spotty (Notolabrus celidotus; Choat and Ayling, 1987) from New Zealand] to changes in macroalgal density due to disturbance (fig. 18-12). Thus recruitment of fish can change as algal and plant structure varies. Macrophytes also function as a source of habitat structure and refuge in other aquatic systems (Orth et al., 1984, Heck and Crowder, 1991). C OM P ETITION

F I G U R E 18-10 Mean percent similarity of microhabitat and diet for species of surfperches (Embiotoca jacksoni, E. lateralis, Rhacochilus toxotes, and R. vacca) for baseline data (1973) and seasons following the storm (September 1980—November 1981) at Naples Reef (after Stouder, 1987).

plexity of giant kelp, while structural complexity of giant kelp decreases with increasing plant density. Therefore, kelp bass recruitment decreases at high plant density. Individual species relationships vary with structural complexity and plant density, and recruitment density and plant density. Therefore, disturbance can affect larval recruitment differentially depending on species relationships (see also chapter 15

Disturbance may also influence competitive interactions as a result of shifts in habitat use, foraging patterns, trophic interactions, reproduction, or recruitment. For example, when surfperch species on Naples Reef converged to one microhabitat type in response to changing food abundance, the one nonresident species, rainbow seaperch (Hypsurus caryi), reduced the time spent on the reef (Stouder, 1987). Typically rainbow seaperch migrated to the reef and remained for four to five months, but following the 1980 storm they stayed just one month. Food abundance is typically highest during the period of rainbow seaperch visitation. When confronted by low food abundances and aggressive resident species, these fish may have left to seek more abundant food sources in other locations. The influence of storm disturbance on many aspects of community organization of Californian temperate reef

F I G U R E 18-11 Mean percent cover of understory kelp compared to mean densities of young-of-year and adult surfperch and large kelp bass at the east-end study site at Naples Reef from January, 1979 (before a storm deforested the reef in February, 1980) to December, 1981. Vertical bars are the (asymmetric) 95% confidence intervals of means (after Ebeling and Laur, 1985).

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F I G U R E 18-12 Predicted relative effects of disturbance on recruitment of three temperate reef-fish species, as mediated by reduced kelp density (after Carr 1994).

assemblages has been well documented. Even so, gaps in our knowledge exist, especially pertaining to the effects on fish reproduction.

Conclusions and Implications Disturbances are common occurrences in all ecosystems. Although disturbances and their effects on fishes in all California marine systems have not been completely documented and studied, there are relevant examples from other temperate and tropical systems (e.g., intertidal areas, bays, estuaries, sea grass beds, coral and rocky reefs, kelp beds). These other studies can lend insights into potential effects of disturbance on California marine fishes. As evidenced by the few examples provided above, physiological and behavioral constraints result in different responses. Disturbances in a variety of habitats may produce similar results with regard to fish behavior (e.g., changes in feeding relationships and habitat use) while at other times disturbance may produce different results (e.g., differences in mobility affect some species or life stages ability to respond). Ultimately behavioral and physiological responses to disturbance may alter or influence community structure. Do disturbances lead to long-term change? They can. If fish species are lost as a consequence of disturbance, and they are unable to re-colonize the area when conditions become favorable (i.e., source populations are too remote to facilitate colonization), then the fish assemblage structure in that location or habitat may be different than before the event. If conditions never return to the pre-event condition (e.g., irreversible habitat destruction), then assemblage characteristics may reflect the new set of habitat conditions. Rare and extreme disturbances, as well as those associated with global climate change or anthropogenic alterations and impacts, can especially give rise to long-term changes. Are short-term changes bad? Not necessarily. Some disturbances can “reset the clock” by moving an assemblage away from equilibrium. The disturbance may clear some habitats and allow colonizing species to reinvade. At the same time species that were successful competitive dominants may be reduced to lower population levels thereby enabling other species to become more prevalent. It may be that non-equilibrium states

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created by disturbances are critical to long-term population stability and viability because assemblages never reach climax conditions. Disturbance functions to structure marine fish assemblages by changing habitats (structurally, chemically, and thermally) and altering food resources. Fishes respond to these changes physiologically and behaviorally. Some fishes are capable of surviving in a wider range of oxygen levels, salinity and temperature ranges than others. These fishes may be much more physiologically tolerant and therefore able to remain in affected habitats until conditions become more favorable. Others will possibly die, grow more slowly, or move to habitats with more favorable conditions. Some fish life stages (i.e., eggs, larvae, some juveniles) have limited abilities to escape adverse conditions and may therefore be negatively and disproportionately affected. Adults tend to be more mobile. When mortality is not imminent, changes in juvenile and adult behaviors provide us with information on responses to disturbances. Fishes may alter their habitat selection or use, feeding behavior, reproductive activities, and movement patterns. Changes can also be represented by increases or decreases in competition among affected assemblage members, increased vulnerability to predation, decreased or postponed reproductive activities, and emigration from affected areas. Fishes have a suite of responses that make them more or less vulnerable to the effects of disturbance. How we evaluate and view disturbance is largely the result of our perspective. Understanding disturbance lends insights to natural processes. Scientists and managers used to believe that disturbances were negative and disruptive to assemblages and ecosystems. Increasing evidence has indicated a common absence of assemblages or ecosystems at equilibrium. Improved understanding, and hence better management, of ecosystems includes knowledge and acceptance of the role of disturbance in natural systems. The larger the scale (e.g., pelagic marine) and the greater the disturbance the less we know. Although we can find some studies of natural disturbance in California marine systems, there are many other relevant examples in other marine systems (e.g., Atlantic coastal estuaries, Florida sea grass beds). Understanding community response to natural disturbances can provide us with a better template to understand the role of human impacts on natural systems. As anthropogenic influences increase, many assemblages become more sensitive to natural disturbances. Disturbance plays a critical role in the structure and stability of California marine fish assemblages and therefore it becomes crucial for us to increase our understanding of the range of conditions it creates.

Future Studies Understanding disturbance and its effects on California marine fishes requires a strong foundation of intact marine ecosystems and assemblages. It also requires scientists and researchers to respond quickly in establishing or continuing a study examining the effects of the disturbance. Without an adequate foundation, or a slow response, it becomes increasingly difficult to understand the effects of disturbance related changes. There are, however, numerous and lengthy studies of California marine systems upon which to base comparisons of disturbance. Serendipity is in charge! With this in mind, we recommend the following initial list for future fish studies in California marine ecosystems:

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1. Evaluation of hypoxia in estuaries, bays, and lagoons and the effects on fishes. 2. Examination of the consequences of increased sedimentation on vegetated (e.g., sea grasses) coastal areas including tide pools, bays, estuaries, lagoons, and near shore areas. 3. Evaluation of climatic change and its effects on current patterns, including inflow of freshwater, drought, floods, and temperature on fish assemblages. 4. Examinations of tsunamis and other severe storms provide information on catastrophic change and its influence on fishes. 5. Biological disturbances, use of combined lab and field experiments to understand observed responses.

Acknowledgments We thank Denise L. Breitburg and Charlie Crisafulli for their insightful and diligent reviews of this chapter. Our work would not have been possible without the tireless assistance and support of Mary Jane Bergener. Financial support for Deanna J. Stouder and Michelle L. McMullin was provided by the USDA Forest Service’s Pacific Northwest Research Station.

Literature Cited Anderson, T. W. 1993. An evaluation of density dependence in a marine temperate reef fish: competitive and predatory effects. Ph.D. Dissertation. University of California, Santa Barbara. Armor, C., and P.L. Herrgesell. 1985. Distribution and abundance of fishes in the San Francisco Bay estuary between 1980 and 1982. Hydrobiologia 129:211–227. Bejda, A.J., A.L. Studholme, and B.L. Olla. 1987. Behavioral responses of red hake, Urophycis chuss, to decreasing concentrations of dissolved oxygen. Env. Biol. Fish. 19:261–268. Bodkin, J.L. 1988. Effects of kelp forest removal on associated fish assemblages in central California. J. Exp. Mar. Biol. Ecol. 117: 227–238. Bodkin, J.L., G.R. VanBlaricom, and R.J. Jameson. 1987. Mortalities of kelp-forest fishes associated with large oceanic waves off central California, 1982–1983. Env. Biol. Fish. 18:73–76. Breitburg, D.L. 1992. Episodic hypoxia in Chesapeake Bay: interacting effects of recruitment, behavior, and physical disturbance. Ecol. Monogr. 62:525–546. ————. 1994. Behavioral response of fish larvae to low dissolved oxygen concentrations in a stratified water column. Mar. Biol. 120: 615–625. ————. 2002. Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheries. Estuaries 25:767–781. Breitburg, D.L., N. Steinberg, S. DuBeau, C. Cooksey, and E.D. Houde. 1994. Effects of low dissolved oxygen on preation on estuarine fish larvae. Mar. Ecol. Progr. Ser. 104:235–246. Breitburg, D.L., T. Loher, C.A. Pacey, and A. Gerstein. 1997. Varying effects of low dissolved oxygen on trophic interactions in an estuarine food web. Ecol. Monogr. 67:489–507. Carpelan, L.H. 1961. Salinity tolerances of some fishes of a southern California coastal lagoon. Copeia 1961:32–39. Carr, M.H. 1989. Effects of macroalgal assemblages on the recruitment of temperate zone reef fishes. J. Exp. Mar. Biol. Ecol. 126:59–76. ————. 1991. Habitat selection and recruitment of an assemblage of temperate zone reef fishes. J. Exp. Mar. Biol. Ecol. 146:113–137. ————. 1994a. Predicting recruitment of temperate reef fishes in response to changes in macrophyte density caused by disturbance. In D.J. Stouder, K.L. Fresh, and R.J. Feller (eds.) Theory and Application in Fish Feeding Ecology. University of South Carolina Press, Columbia.

————. 1994b. Effects of macroalgal dynamics on recruitment of a temperate reef fish. Ecology 75:1320–1333. Choat, J.H., and A.M. Ayling. 1987. The relationship between habitat structure and fish faunas on New Zealand reefs. J. Exp. Mar. Biol. Ecol. 110:257–284. Congleton, J.L. 1980. Observations on the responses of some southern California tidepool fishes to nocturnal hypoxic stress. Comp. Biochem. Physiol. 66A:719–722. Connell, J.H. 1978. Diversity in tropical rain forests and coral reefs. Science 199:1302–1310. ————. 1980. Diversity and coevolution of competition, or the ghost of competition past. Oikos 35:131–138. Dayton, P.K., and M.J. Tegner. 1994. Catastrophic storms, El Niño, and patch stability in a southern California kelp community. Science 224:283–285. Ebeling, A.W., and D.R. Laur. 1985. The influence of plant cover on surfperch abundance at an offshore temperate reef. Env. Biol. Fish. 12:169–179. Ebeling, A.W., D.R. Laur, and R.J. Rowley. 1985. Severe storm disturbances and reversal of community structure in a southern California kelp forest. Mar. Biol. 84:287–294. Ebeling, A.W., and M.A. Hixon, 1991. Tropical and temperate reef fishes: comparisons of community structure. p. 509–563. In: Sale, P.F. (ed), The ecology of fishes on coral reefs. Academic Press, Inc. Heck, K. L., and L. B. Crowder. 1991. Habitat structure and predatorprey interactions in vegetated aquatic systems. p. 281–289. In: Bell, S. S., E. D. McCoy and H. R. Mushinsky (eds.), Habitat structure: the physical arrangement of objects in space. Academic Press, San Diego, CA. Hutchinson, G.E. 1961. The paradox of the plankton. American Naturalist 95:137–145. Jackson, J.B.C., and L.W. Buss. 1975. Allelopathy and spatial competition among coral reef invertebrates. Proc. Nat. Acad. Sci. U.S.A. 72:5160–5163. Jones, G.P., and C. Syms. 1998. Disturbance, habitat structure and the ecology of fishes on coral reefs. Austr. J. Ecol. 23:287–297. Kaufman, L.S. 1983. Effects of Hurricane Allen on reef fish assemblages near Discovery Bay, Jamaica. Coral Reefs 2:43–47. Keister, J. E., E. D. Houde, and D. L. Breitburg. 2000. Effects of bottomlayer hypoxia on abundances and depth distributions of organisms in Patuxent River, Chesapeake Bay. Mar. Ecol. Progr. Ser. 205: 43–59. Lake, P.S. 2000. Disturbance, patchiness, and diversity in streams. J. No. Am. Benth. Soc. 19:573–592. Lassig, B.R. 1983. The effects of a cyclonic storm on coral reef fishes. Env. Biol. Fish. 9:55–63. Mackey, R.L., and D.J. Currie. 2000. A re-examination of the expected effects of disturbance on diversity. Oikos 88:483–493. Moyle, P.B., R.A. Daniels, B. Herbold, and D.M. Baltz. 1986. Patterns in distribution and abundance of a noncoevolved assemblage of estuarine fishes in California. U.S. Fish. Bull. 84:105–117. Moyle, P.B., B. Herbold, D.E. Stevens, and L.W. Miller. 1992. Life history and status of delta smelt in the Sacremento-San Joaquin estuary, California. Trans. Am. Fish. Soc. 121:66–77. Onuf, C.P., 1987. The ecology of Mugu Lagoon, California: an estuarine profile. U.S. Fish Wildl. Ser. Biol. Rep. 85:122 pp. Onuf, C.P., and M.L. Quammen. 1983. Fishes in a California coastal lagoon: effects of major storms on distribution and abundance. Mar. Ecol. Progr. Ser. 12:1–14. Orth, R.J., K.L. Heck, Jr., and J. van Montfrans. 1984. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7:339–350. Petraitis, P.S., R.E. Latham, and R.A. Niesenbaum. 1989. The maintenance of species diversity by disturbance. Quart. Rev. Biol. 64: 393–418. Pickett, S.T.A., and P.S. White. 1985. The ecology of natural disturbance and patch dynamics. Academic Press, Orlando. Pihl, L. 1994. Changes in the diet of demersal fish due to eutrophication-induced hypoxia in the Kattegat, Sweden. Can. J. Fish. Aquat. Sci. 51:321–336. Pihl, L., S.P. Baden, R.J. Diaz, and L.C. Schaffner. 1992. Hypoxiainduced structural changes in the diet of bottom-feeding fish and crustacea. Mar. Biol. 112:349–391. Rahel, F.J., and J.W. Nutzman. 1994. Foraging in a lethal environment: fish predation in hypoxic waters of a stratified lake. Ecology 75: 1246–1253.

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Sale, P.F. 1974. Mechanisms of co-existence in a guild of territorial reef fishes at Heron Island. Proc. Intern. Coral Reef Symp., 2nd 1:193–206. ————. Maintenance of high diversity in coral reef fish communities. Am. Nat. 111:337–359. Stouder, D.J. 1987. Effects of a severe-weather disturbance on foraging patterns within a California surfperch guild. J. Exp. Mar. Biol. Ecol. 114:73–84. Syms, C., and G.P. Jones. 1999. Scale of disturbance and the structure of a temperate fish guild. Ecology 80:921–940.

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Todd, E.S., and A.W. Ebeling. 1966. Aerial respiration in the longjaw mudsucker Gillichthys mirabilis (Teleostei: Gobiidae). Biol. Bull. 130: 265–288. Wannamaker, C.M., and J.R. Rice. 2000. Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. J. Exp. Mar. Biol. Ecol. 249:145–163. Woodley, J.D., E.A. Chornesky, P.A. Clifford, J.B.C. Jackson, L.S. Kaufman, N. Knowlton, J.C. Lang, et al. 1981. Hurricane Allen’s impact on coral reefs. Science 214:749–755.

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PART IV

B E HAVI O RAL E C O LO GY

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CHAPTER 19

Reproduction E DWAR D E. DeMARTI N I AN D PAU L C. S I K K E L

Introduction An overview of fundamental natural and life histories must first set the stage for any comprehensive review of reproductive ecology. An expanded construct of more quantitative, behavioral and other, higher-order ecological information can then be built atop this base. We have therefore organized the present chapter into four major parts. We begin with a section on reproductive natural history providing summary data on reproductive modes and spawning types, courtship, and a taxonomic survey of their distributions. This brief review of key life history topics such as body size-related reproductive effort and tradeoffs between the number and size of offspring produced next leads to an in-depth section on the behavioral and evolutionary aspects of reproductive ecology focused on mating systems and gender allocation, sexual selection, and parental care. We follow this with a section that reviews the poorly recognized occurrence of secondary gonochorism in warm temperate representatives of several tropical fish lineages, and discuss the unusual Californian/eastern North Pacific preponderance of species with extensive investment in individual offspring (via viviparity and post-zygotic parental care in oviparous species). Both of these phenomena are interpreted in terms of differences between temperate and tropical reefs in benthic habitat persistence and on- versus off-reef predation risk to propagules and in environmental potentials for mate monopolization and related development of polygamous mating systems. Also considered is the possible influence of the temporally and spatially unpredictable upwelling regime of the eastern North Pacific. A concluding summary section identifies data deficiencies and suggests promising topics for future research, with special emphasis on the patterns of extensive and diverse maternal investment and parental care for which California marine fishes provide ideal subjects for comparative study. The scope of this review is consistent with other chapters of this book: the primary geographic focus is on the fishes of California and the Pacific coast of Baja California. Habitat considerations within the marine realm span the intertidal to the abyssal, from the pelagic to the benthic; partly marine (estuarine and anadromous/catadromous species) as well as fully marine fishes are considered. The taxonomic scope

includes all of the native California marine species of elasmobranchs and teleosts listed in Fitch and Lavenberg (1968), Miller and Lea (1972), and De la Cruz Aguero et al. (1997), with more recent species nomenclature following Eschmeyer (1998). Select exotics (including species purposely and accidentally introduced to the Californias) are used to further illustrate patterns. Species occurring in California are used as primary examples of patterns recognized from studies of fishes in other habitats and geographic regions of the world. Taxonomic relationships higher than the generic level follow Nelson (1994).

Reproductive Natural History Taxonomic Survey of Reproductive Modes and Spawning Types The fishes of the Californias and elsewhere represent two major modes of offspring production: 1) the direct production of juveniles that are miniature adults and 2) the indirect production of pre-juvenile stages (eggs, larvae). These two modes are really extremes on a continuum of parental investment in individual offspring. At one extreme, reproduction is oviparous, maternal provisioning is lecithotrophic (limited to the yolking of ovarian oocytes prior to fertilization), and zygotes develop outside of the maternal environment and independent of further energetic investment by either parent. The ova of egg layers are usually fertilized externally, but notable exceptions include the oviparous sharks (e.g., heterodontids and scyliorhinids) and skates (Rajidae), which lay horny egg cases after copulation and internal fertilization, and the scorpaeniform family Cottidae. At the other extreme, there is matrotrophic viviparity (live-bearing of young provisioned extensively beyond the nutrition provided by ovum yolk). This contemporary view of oviparity and viviparity as degrees of maternal investment distinguishable by birth mode alone removes the need for the outdated concept of ovoviviparity, once considered to be a discrete intermediate between the two extremes (Wourms et al., 1988). In strict ovoviviparity, embryos are provisioned entirely pre-fertilization even though some embryogenesis occurs internally. Recent

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F I G U R E 19-1 (A) Near-term female of the embiotocid Hysterocarpus traski aborting embryos upon capture; the length-specific fecundity of this freshwater species is the highest among embiotocids, followed by the marine species Brachyistius frenatus (Baltz, 1984). Photo by D. Baltz. (B) Pregnant female of the sebastine scorpaenid Sebastes paucispinis with ovarian embryos exposed by dissection (from Moser, 1967, with permission from Allen Press).

research has shown that ovoviviparity is not a discrete intermediate, but rather encompasses a broad range of provisioning post-fertilization (Wourms et al., 1988). Thus, we consider ovoviviparity as a less extreme type of viviparity, while acknowledging the existence of a range of intermediates along a continuum approaching matrotrophy. Reproductive specialization has evolved from oviparity to viviparity independently within diverse lineages of elasmobranchs (sharks and rays) and teleosts (bony fishes) in California, as elsewhere (Wourms et al., 1988; Wourms and Lombardi, 1992). Viviparity ranges from the strictly lecithotrophic (live-bearing of young provisioned entirely by ovum yolk) to matrotrophic viviparity. The latter is an extreme type of parental care in which the developing young receive total protection within, as well as energy provisioning by, the mother. Examples of lecithotrophic viviparity include some sharks such as the spiny dogfish (Squalus acanthias) and perhaps some scorpaenids of the genus Sebastes. Extensive matrotrophic nourishment by yolk sac placentae occurs in certain viviparous sharks (some triakids and most carcharhinids including sphyrnines) and (via several types of placentae and placenta-like structures) in the viviparous brotulas (Bythitidae) and surfperches (Embiotocidae). Of the four genera of bythitids known from California waters (Ogilbia, Cataetyx, Grammonus and Brosmophycis), viviparity has been documented for only one species, B. marginatus (Hart, 1973) but information on bythitids elsewhere indicates extensive matrotrophy in all genera (Wourms et al., 1988). In between the strict lecithotrophs and extreme matrotrophs occurs a continuum of provisioning, with the relative degree of embryo nourishment by ovum yolk and maternal-embryo nutrient exchange varying among families and species in both elasmobranchs and teleosts. Included are aplacental viviparity supplemented by production of nurse eggs for consumption by embryos (oophagy) in alopiid (thresher) and cetorhinid (basking) sharks and intrauterine cannibalism of sibling embryos (adelphophagy: literally “eating one’s brother”), as well as oophagy in odontaspid (sand tiger) and lamnid sharks, and limited matrotrophy by placenta-like maternal-fetal connections in many viviparous rays. Also included is likely oophagy by developing embryos (Boehlert et al., 1986) in the more K-selected Sebastes spp. Syngnathid

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pipefishes and seahorses (eight California species) brood embryos within or on their bodies and likely contribute substantially to their nutrition; the syngnathid reproductive mode, however, represents post-zygotic paternal care, not viviparity. The time frame of maternal provisioning varies greatly among viviparous fishes. Gestation is typically several months long in the embiotocids (Baltz, 1984) and Sebastes spp. (Love et al., 1990) but is nearly 2 years long in the spiny dogfish (Jones and Geen, 1977). Viviparity in California marine fishes would be almost entirely limited to elasmobranchs (and in that regard, unexceptional), were it not for the embiotocids (fig. 19-1A) and the sebastine genus Sebastes (fig. 19-1B). Because of these latter two groups, however, viviparity in California marine fishes is unusually well expressed. The embiotocids (20 marine species) plus Sebastes (nearly 70 species) comprise about 12% of all of the coastal shelf and slope fishes of the Californias (Miller and Lea, 1972; De la Cruz Aguero et al., 1997). Elasmobranchs comprise another 56 viviparous species. Including elasmobranchs, viviparous species total nearly 18% of the California marine fish fauna; this contrasts markedly with an overall value of less than 3% for marine elasmobranchs and teleosts worldwide (Wourms and Lombardi, 1992). Table 19-1 summarizes patterns of viviparity within and between both major groups of California marine fishes. Appendix 19-1 provides a more comprehensive list by (sub)family within order, with species examples and key references. Parental provisioning of offspring often extends to parental care (guarding or brooding of eggs) in fishes. Postoviposition (egg-laying) parental care is limited to teleosts in California as elsewhere. There are no known or likely cases of post-parturition parental care in viviparous elasmobranchs, although there are several well-documented cases (e.g., the soupfin shark, Galeorhinus galeus: Ripley, 1946) of sexual segregation in schooling species of viviparous sharks, presumably as a female adaptation to reduce predation of post-partum young by males. The types of teleost parental investment include the physiological nurturing and anti-predator defense of eggs (typically attached to some substrate, many California species) and sessile larvae (described for one California batrachoidid toadfish, the plainfin midshipman Porichthys notatus

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TA B L E 19-1

Contrasts Between Latitudes and Oceans in Reproductive Modes (A) Viviparity Subclass Elasmobranchs Teleosts

California 81.0 (79) 10.3 (798)

Pacific Canada 68.0 (19) 15.0 (301)

Atlantic USA 85.5 (76) 0.3 (1232)

Atlantic Canada 55.6 (36) 0.6 (492)

(B) Teleost Parental Care Taxon level Species

California 15.5 (798)

Pacific Canada 19.3 (301)

Atlantic USA 16.9 (1232)

Atlantic Canada 7.9 (492)

15.5 (161)

22.5 (80)

13.4 (186)

8.5 (142)

Families

NOTE: In A the proportional presence of viviparity (as percentage) is compared among species of California marine elasmobranch and teleost fishes. In B the presence of post-zygotic parental care (as percentage) is compared among oviparous species and families of California marine teleosts. Sources: Miller and Lea, 1972; De La Cruz Aguero et al., 1997; Fitch and Lavenberg, 1968; see Appendix 19-1 for complete listing. Also provided are comparative data for marine fishes of the Pacific (Hart, 1973) and Atlantic (Scott and Scott, 1988) coasts of Canada and the Atlantic USA excluding the Gulf of Mexico (Robins et al., 1986). Atlantic USA data for Alepocephalidae and Moridae are supplemented by Haedrich and Merrett (1988). Numbers in parentheses indicate total number of taxa.

[fig. 19-2], and likely for its congener the specklefin midshipman P. myriaster). Care of embryos or mouth-brooded fry (young juveniles) is undocumented for native California fishes, but the former is likely for the ariid catfishes Arius planiceps, A. platypogon, and Bagre panamensis, and the jawfish, Opistognathus punctatus. Oral-brooding males of the Guadalupe cardinalfish Apogon guadalupensis have recently been observed at San Clemente Island (Lea and Rosenblatt, 2000). Care of free-swimming fry is unknown and unlikely in native California fishes, although the triggerfish Balistes polylepis has been observed in the Gulf of California guarding free-swimming fry after swim-up from tended demersal spawn (Strand, 1978 and pers. comm. in Barlow, 1981). The introduced euryhaline cichlids Oreochromis mossambicus and Tilapia zillii (Knaggs, 1977) also brood both eggs and freeswimming fry (El-Zarka, 1956; Loiselle, 1977). Parental tending of demersal eggs is the most prevalent form of care in California marine teleosts. About 16% of the species and over 15% of the families of oviparous California teleosts tend demersal eggs after oviposition (table 19-1). Although not unique to the Californias or the Pacific coast of North America, oviparous fishes that provide some sort of post-zygotic parental care of eggs are noteworthy for their divergent lineages as well as species diversity among the California and eastern north Pacific ichthyofauna. The presently recognized 43 species of California marine cottids and cottoids (Rhamphocottidae, Hemitripteridae) are the second most diverse lineage of California marine fishes, and many genera and species of cottids exhibit parental care. Parental care is apparently ubiquitous in the Hexagrammidae and is present in at least some Liparidae. Care is the norm in the gobioids and throughout the zoarcoid, blennioid, and gobiesocoid perciforms (Anarhichadidae, Blenniidae, Chaenopsidae, Gobiesocidae, Labrisomidae, Pholididae, Stichaeidae, Tripterygiidae). Parental care would not be unexpected in the Scytalinidae, Cryptacanthodidae, and Zoarcidae, the latter based on observations of species elsewhere, although care has thus far been anecdotally noted for only one species of California zoarcid (Levings, 1969). Most cases of care in native California marine fishes are paternal although a minority of exclusively maternal (one species—the triggerfish Balistes polylepis: Strand, 1978); biparental (the gunnels Pholis laeta: Hughes, 1986; and Apodichthys flavidus: Wilkie, 1966; the wolf-eel Anarhichthys ocellatus: Marliave, 1987); and maternal and facultatively biparental (the red Irish lord cottid

Hemilepidotus hemilepidotus: Fig. 19-3; DeMartini and Patten, 1979) care states are known. One western North Pacific species of the cottid genus Hemilepidotus is also known to exhibit facultative biparental care (Hayakawa and Munehara, 1996). Care can include some type of physiological nurturing (fanning eggs to enhance gas exchange, developmental rate, and survivorship: buffalo sculpin Enophrys bison: DeMartini, 1978b; lingcod Ophiodon elongatus: Giorgi and Congleton, 1984), passive to active defense of eggs against conspecific and extraspecific predators (many species, including the painted greenling Oxylebius pictus: DeMartini, 1987), or both (DeMartini, 1999). Protective functions appear most widespread based on taxonomic prevalence (Coleman, 1999). Overall, 32% and 26% of species and families, respectively, of all California marine fishes (elasmobranchs plus teleosts) are either viviparous or oviparous and exhibit parental care. The total proportion of viviparous and egg-tending species (36%) and families (34%) is even greater in the waters off Pacific Canada. In comparison, the marine fish faunas of both Atlantic USA and Atlantic Canada include relatively few viviparous and egg-tending species and families (2
4 chi-square tests: P  0.0001; table 19-1A, B). The lack of increase with latitude in proportion of parental-caring teleosts in the western North Atlantic (table 19-1B) argues against a simple latitudinal explanation. Several families of viviparous or predominantly to exclusively parental-caring fishes are either conspicuously absent (embiotocids, hexagrammids) or comprise few species (sebastine scorpaenids, cottids) on the Atlantic seaboard. Table 19-1B also summarizes parental care patterns among families of California marine fishes, and a complete listing of parental care in California fishes is provided in Appendix 19-1. To our knowledge, ours is the first explicit documentation of the unusual preponderance of viviparity and parental care in California marine fishes. Kendall (1981) and Hobson (1994) were among the first to note the prevalence of parental-caring demersal spawners among eastern North Pacific fishes. Care in some cases involves alloparental (genetically unrelated) adult conspecifics, other fish species, and associations with benthic invertebrates. Evaluation of alloparental care is deferred to a later section on mating systems and sexual selection. There is one known eastern Pacific example of extraspecific reproductive association among fishes (akin to some described associations of cyprinids spawning in the nests of centrarchids in North American freshwater systems—see review by Johnston,

REPRODUCTION

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FIGURE 19-2 Parental male of the plainfin midshipman, Porichthys notatus,

placed upon an overturned, intertidal rock with a mass of large-yolky eggs. Midshipman males tend eggs layed by females on the underside of rocks in intertidal and subtidal areas. Photo by M.H. Horn.

1994). The small-bodied sculpin Asemichthys taylori spawns its eggs on the surface of much larger egg masses tended by males of another cottid, the relatively large-bodied buffalo sculpin. Both sexes of A. taylori desert after spawning, and the association may represent a parasitism if peripheral spawns of the small species hinder gas exchange, developmental rate, or survival of the larger species’ spawn (Kent et al., 1997). The association is at least as likely to be a commensalism whereby the small species alone benefits from the larger species’ spawn defense without appreciable cost to the latter. One other case of extraspecific egg tending has been recently described, involving two species of freshwater cottids in Lake Baikal, which might represent interspecific competition for spawning sites, the acquisition of subordinate species’ eggs by the dominant species for consumption while tending its own eggs, or both (Munehara et al., 2002). These and other possible sculpin nesting associations need further study. Many demersal spawners lay eggs attached to algae or benthic invertebrates; in many cases eggs are hidden within benthic fouling organisms (DeMartini, 1999). Many species of aparental northeastern Pacific sculpins, for example, deposit spawns in places inaccessible to predators within rock crevices and kelp holdfasts or among barnacle tests and mussel valves. Some species, like the silverspotted sculpin Blepsias cirrhosus, sequester eggs within sponges and perhaps benefit from the chemical defense afforded by sponge toxins as well as by physical protection and ventilation within the sponge structure (Munehara, 1991). Some liparid snailfishes of the genus Careproctus have evolved yet another unique invertebrate association: females deposit eggs within the gill chambers of lithodid crabs, and embryos benefit from enhanced ventilation as well as physical protection in a parasitic relationship with a survivorship cost to the crab host (Somerton and Donaldson, 1998). The numerous and diverse examples of post-zygotic parental care in oviparous species and viviparity represent a suite of adaptations for improving offspring survival; such adaptations are likely antipredatory because of the dominant influence of predation in marine ecosystems (Valiela, 1995). Without the pervasive influence of predation countering offspring survival, the present variety of investment patterns and related parental care systems in California marine fishes surely would be much less developed. We next briefly review key issues in the reproductive life histories of fishes and provide

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F I G U R E 19-3 Parental female of the sculpin Hemilepidotus hemilepidotus reclining atop mass of demersal spawn. H. hemilepidotus is an atypical cottid (perhaps representative of the subfamily Hemilepidotinae) which exhibits primarily maternal and facultatively biparental guarding of spawn (from DeMartini and Patten, 1979 with permission from the Royal British Columbia Museum).

California examples as prelude to a discussion of courtship behaviors and other aspects of the behavioral and evolutionary ecology of reproduction in these fishes.

Key Attributes of Reproductive Life Histories Optimizing offspring production inevitably leads to tradeoffs between the number versus size of offspring (“many small versus few large”; Winemiller and Rose, 1992b) and to the evolution of adaptations which both augment investment in individual offspring while maximizing the numbers of offspring produced (Elgar, 1990). The former includes traits that enhance the survival of individual propagules after parturition or oviposition—greater maternal investment per offspring (larger eggs, viviparity) and parental care after egg-laying. The latter includes the production of multiple broods in both egg-layers and live-bearers. Adaptations that maximize offspring production in California marine fishes, and fishes in general elsewhere, are centered on rates of egg production by females. Even though seasonal productivity cycles influence the timing of reproduction, the females of many if not most species of oviparous teleosts, in California and other temperate marine ecosystems, ripen and spawn multiple clutches of eggs over a protracted reproductive period and repeat this process over many years once sexual maturity has been attained. Numerous case studies (e.g., DeMartini, 1991) illustrate how annual per capita offspring allocation is increased through multiple spawning events. As a consequence, gonadal investment is typically severalfold larger than somatic production in adult fishes (DeMartini et al., 1994). Some of the more r-selected species of viviparous Sebastes in California (Moser, 1967; Love et al., 1990), like both freshwater live-bearers (guppies, F. Poeciliidae) and some marine live-bearers elsewhere (viviparous Australian [Gunn and Thresher, 1991] and South African [Prochazka, 1994] clinids), have evolved the analogous process of superfoetation (the livebearing of multiple broods whose embryos are produced in partially overlapping series). Superfoetation has not evolved in any embiotocid (Baltz, 1984). Perhaps superfoetation to some extent augments offspring number at the expense of offspring size and

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any reduction in offspring size would oppose this major selective factor favoring the maintenance of viviparity in the group. Or, perhaps the restricted seasonal timing of offspring production in embiotocids precludes superfoetation, given the recognized importance of brood timing among females of differing sizes and ages in one species (Schultz et al., 1991). Fishes, being the most primitive and developmentally plastic of the vertebrates (Francis, 1992), have the further capability of adjusting reproductive effort by flexible gender allocation (Warner, 1978). That is, it is within the evolutionary scope of teleost fishes for individuals to not only change sex ontogenetically (sequential hermaphroditism) but to concurrently maintain both egg as well as sperm-producing capabilities (simultaneous hermaphroditism). In the two basic types of sequential sex change—changing from adult male to adult female (protandry) or from female to male (protogyny)—the sexes are dioecious (separate) and individuals do not function as both sexes at the same time. A local example of a protogynous teleost is the California sheephead Semicossyphus pulcher (Warner, 1975a). Some dioecious species have evolved more than one morphotype of one of the sexes (e.g., diandry involving two male types: Reinboth, 1970). In sex-changing species, multiple morphs typically occur only in the nonlimiting, usually male, sex. Diandry has been most frequently described in protogynous wrasses of the Labridae. It has been widely theorized but rarely demonstrated that the proportion of the different morphs in reproducing population units is dynamic and subject to frequency-dependent selection such as might occur under different population densities. The evolution of multiple within-sex morphs has not been limited to sex-changing species, however. California marine examples include the jack and hooknose males of salmonids like Oncorhynchus kisutch (Healey and Prince, 1988), and the so-called Types I and II males of the plainfin midshipman (Brantley and Bass, 1994; Barni et al., 2001). Other well-studied examples of satellite and sneaker males (subordinates that use deceptive tactics to counter the defense of females or spawning sites by dominant males) include freshwater sunfishes like bluegill Lepomis macrochirus (Gross, 1982) and bluehead wrasse Thalassoma bifasciatum (a sex-changing species) of Caribbean coral reefs (Warner and Schultz, 1992). In monoecious (simultaneous) hermaphrodites, individuals can perform both sexual functions at the same time. Many deep-sea fishes throughout the world’s oceans are monoecious hermaphrodites (Mead, 1960; Mead et al., 1964; Smith and Atz, 1973; Fishelson and Galil, 2001). It is likely that simultaneous hermaphroditism has provided a solution to the general problem of locating sparsely distributed mates (Tomlinson, 1966) in diverse lineages of deep-sea fishes (Smith, 1975). Functional rather than anatomical hermaphroditism has been another solution for deep-sea fishes. The most extreme examples of the latter are the deep-sea ceratioids, in particular ceratiids such as Cryptopsaras couesii, in which tiny males once having encountered a female, become little more than ectoparasitic testes on females’ bodies (Pietsch, 1976). Among nearshore California fishes, examples of simultaneous hermaphrodites include gobies of the genus Lythrypnus. In bluebanded (L. dalli) and zebra (L. zebra) gobies, the proportion of gonad allocated to the two sexual functions is variable and dynamic, dependent on diverse aspects of the social environment including the relative body sizes, density, behavioral gender, and spatial distributions of conspecifics (St. Mary, 1993, 2000). Studies of the complex interplay between the social environment and the neuroendocrine bases of sex

change have been conducted for the bluebanded goby (Reavis and Grober, 1999; Carlisle et al., 2000) and for California sheephead and rock wrasse Halichoeres semicinctus (Diener, 1976). Maximizing fitness in some cases appears to have selected for multiple types of gender allocation within populations. Populations of the bluebanded goby for example contain sequential hermaphrodites (protogynous pure males) as well as simultaneous hermaphrodites (St. Mary, 2000). Simultaneous hermaphroditism and bidirectional sex change (either from mature female to mature male, or vice versa) are known to occur in several genera of tropical gobiids, but as yet both have not been described within the same species-population (Kuwamura et al., 1994; Nakashima et al., 1995, 1996). Mixtures of protogynous and gonochoric (non-sex changing) individuals occur in populations of a warm-temperate serranine (the spotted sand bass Paralabrax maculatofasciatus) in Baja and southern California (Hovey and Allen, 2000). Populations of several tropical serranines (e.g., Serranus psittacinus  S. fasciatus of Hastings and Petersen, 1986; Petersen, 1990a) also simultaneously include hermaphroditic and protogynous individuals. Gender allocation patterns exhibited by families of California marine fishes are summarized in tables 19-2 and 19-3 and catalogued in greater detail in Appendix 19-1. The most likely selective agents favoring the evolution of hermaphroditism in fishes are discussed in the third section. Fitness is influenced by the per capita survival of offspring after oviposition or parturition. Larger propagules have higher survivorship (Ware, 1975; Pepin, 1991; Wootton, 1994), so selection for greater energetic investment per offspring occurs coincident with selection to produce greater numbers of offspring. This is why, within-species, larger-bodied females, which are both capable of (having a greater body cavity volume) and selected for (being generally older and consequently of lower reproductive value) allocating a larger proportion of their available energy to reproduction, typically compromise between producing more and larger offspring. As predicted by optimization theory (Chambers and Leggett, 1996), the larger-bodied, older females of many species of California marine fishes produce larger, as well as more numerous eggs (e.g., Engraulis mordax: Parrish et al., 1986; Seriphus politus: DeMartini, 1991). The eggs produced by pelagic spawners average smaller in size than those produced by demersal spawning fishes (Duarte and Alcaraz, 1989); brooded eggs in general tend to be larger than untended demersal eggs (Sargent et al., 1987; Winemiller and Rose, 1992a); and the embryos of larger eggs hatch as larger larvae (Chambers and Leggett, 1996). Viviparity and post-zygotic parental care to some extent involve increased investment per offspring (hence larger individual offspring) at the expense of the numbers of offspring in which the total investment is made. Selection for the production of relatively few but large offspring has been disproportionately frequent in the marine fishes of California and the Pacific coast of North America. In Section IV we will discuss some likely reasons why this has come about.

Courtship Courtship behavior and the events that often accompany it has been a favorite topic among lay persons and field biologists alike. In part this is probably because such acts contrast strongly with the background of normal behavior. While many aspects of reproductive ecology can be inferred from surveys (e.g., paternal care can be assessed by the presence of males guarding eggs, which may last weeks) or collection of

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TA B L E 19-2

Shallow-Water Marine Fish Families with One or More Species Having Known or Likely Non-Gonochoric Gender Allocation

Teleost Family

Type(s) of gender Allocation

California Representation?

Muraenidae Caracanthidae Platycephalidae Centropomidae Serranidae Malacanthidae Sparidae Lethrinidae Nemipteridae Polynemidae Cirrhitidae Pomacentridae Labridae Scaridae Trichonotidae Creediidae Gobiidae

protogynous, protandrous, simultaneous, gonochoric protogynous protogynous, gonochoric protandrous simultaneous, protogynous, gonochoric protogynous, gonochoric protogynous, protandrous protogynous protogynous, gonochoric protandrous protogynous, bidirectional protandrous, protogynous, gonochoric protogynous, gonochoric protogynous, gonochoric protogynous protandrous, gonochoric protogynous, simultaneous, bidirectional

yes; no no no yes; yes; yes; no no yes; no yes; yes; yes; no no yes;

Ostraciidae

protogynous

no

lone sp. likely gonochoric

all three types likely lone sp either one or other type lone sp likely protogynous

both spp likely protandrous all spp gonochoric both types represented lone expatriate sp likely protogynous

all three types represented

NOTE: List of 18 families excludes those in the deep sea. A subset representing California marine fishes is provided for comparison. Additional details are listed in Appendix 19-1.

TA B L E 19-3

Proportional Distribution of Gender Allocation Among Reef and Other Inshore Teleosts of California Versus the Tropics

California

Tropics

Percentage (N Families)

Percentage (N Families)

gonochore protogynous hermaphrodite protandrous hermaphrodite sequential or bidirectional hermaphrodite

87.2 (34) 10.3 (4) 0

67.1 (53) 21.5 (17) 7.6 (6)

2.5(1)

3.8 (3)

total hermaphrodites

12.8 (39)

32.9 (26)

Gender Allocation Type

NOTE: Tropical families include Indo-Pacific, Caribbean, and Atlantic. Numbers of allocations for families outnumber families due to multiple allocation types within some families like the Serranidae and Gobiidae.

individuals (e.g., sex change), details of courtship and spawning require direct observation in the right place at the right time. Thus, data are biased toward species that are most easily observed and for which spawning is most predictable in time and space. For purposes of this review, we define courtship as a form of communication that increases the likelihood of the receiver spawning or copulating with, and thus benefiting, the sender (e.g., Myrberg and Fuiman, 2002). For an excellent review of communication in animals generally, including courtship, we refer the reader to Bradbury and Vehrencamp (1998). In fishes, courtship may involve impressive visual displays such as rapid body movements and conspicuous changes in coloration and sounds, often easily detectable by unaided human observers, along with chemical and electrical signals that are not detectable by the unaided observer. Courtship per se is a sexually selected trait that is usually associated with males, ostensibly because males are more often the limited sex. However, courtship behavior has been described for females of many fish species as well, perhaps most notably in syngnathids where males are often the limiting sex (e.g., Gronell, 1984;

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Berglund and Rosenqvist, 2001). Courtship activity in fishes and other organisms appears to have at least four functions. The simplest and most obvious of these is species identification and an indication of individual reproductive state. Courtship may also help synchronize the release of gametes. This would seem to be particularly important in pair or group-spawning species that release gametes directly into the water column. Courtship may provide information about the quality of the individual or the spawning site. For example, female bicolor damselfish (Stegastes partitus) spawn preferentially with males that court more vigorously and more vigorous courtship is correlated with both male fat reserves and hatching success of the eggs guarded by parental males (Schmale, 1981; Knapp and Kovach, 1991). In the bluehead wrasse, aspects of male courtship are influenced by the presence of piscivores known to feed on spawning adults and thus courtship display can provide information about the safety of the spawning site (Warner and Dill, 2000). In some three-spined stickleback (Gasterosteus aculeatus) populations the intensity of red coloration may be a reliable indicator of male parasite loads

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(Milinski and Bakker, 1990). The function of courtship, or a given component of courtship, in a given species likely depends on its spawning mode and mating system, and courtship and spawning behavior can be expected to reflect and respond to the tradeoffs between maximizing the benefits of courtship favored by sexual selection (increasing reproductive success), relative to their costs (e.g., energy expenditure, predation on adults or offspring, opportunity costs). Research on courtship in fishes, as in other organisms, has focused on the full range of levels of inquiry, including proximate/physiological mechanisms (e.g., Stacey, 1987; Bass, 1993), the evolutionary history of courtship signals (Basolo, 1990a; Foster, 1994), and the function of courtship signals. However, as with other types of behavior, most research on courtship and spawning behavior in temperate marine fishes, including those off the coast of California and adjacent waters, has not progressed beyond the descriptive phase, often coming from opportunistic observations, and has focused on relatively few species. Below we summarize descriptive studies of courtship and spawning behavior in these species as well as the few studies that have gone beyond the descriptive phase. Of the range of spawning modes and reproductive tactics found in marine fishes off the coast of California, details of courtship and spawning are probably best documented for fishes in which males defend reproductive territories. These include species with internal fertilization and no subsequent male care (e.g., some Sebastes and Cottidae), but especially those in which male territories include egg-deposition sites. This bias exists despite the fact that reproductive territoriality remains poorly documented (discussed below), probably because the site, and often the timing, of reproduction are predictable: Male reproductive territories are easily identified by conspicuous male behavior and/or the location of a nest site. Thus, by remaining at that site, a patient observer is likely to witness courtship and spawning. Of course, patience wears thin in the cold waters of the temperate eastern Pacific and most of the work has still focused on a small number of common, conspicuous, and shallow-water species, much of it under laboratory conditions. Moreover, in many field studies, observations have been opportunistic and courtship was inferred from the location of the interaction and the sex and reproductive status of interacting individuals, rather than observations of events actually culminating in spawning or copulation. In addition to Tinbergen’s (1952) classic description for sticklebacks, Myrberg (1972), Losey (1976), and Munehara (1988) provide good examples and detailed ethograms of typical courtship behavior in male-territorial species. Where males guard egg-deposition sites or mating territories that do not include females (as occurs in haremic species which defend access to members of the opposite sex), males must attract females to their territory in order to spawn or copulate. Similarly, ripe females must have the opportunity to enter the territory and assess the quality of prospective mates, rather than being evicted as an intruder or ignored, and thus must at least advertise their gender, if not their reproductive status. This would appear to favor displays that increase male conspicuousness against the visual, auditory and/or chemical background of the environment, while inhibiting or concealing territorial keep out signals, and female displays that are reliable indicators of female fecundity and readiness. The types of signals used should reflect the resolution of the tradeoff between the specific costs and benefits of signaling and mate-visiting for each sex, local or species-average environmental variables that affect signal detectability, and phyloge-

netic constraints. Costs of courting for territorial males include increased conspicuousness to predators or other males (e.g., sneak spawners), and energy expenditure. Predation risk is also a potential cost for females, whose often swollen abdomen may both increase conspicuousness and reduce swimming efficiency. For both sexes, these costs should be affected by body size and morphology that affect susceptibility to predators and swimming efficiency. If males leave the territory to court, they further risk injury from other territorial fishes, losing eggs to predators, and territorial resources (or the entire territory) to competitors. Females that occupy territories similarly risk losing resources to competitors (Karino and Kuwamura, 1997; Sikkel, 1998) and risk injury when crossing territories of other fish (Reynolds and Côté, 1995). One perhaps counterintuitive cost of courtship for males in nestguarding species is that females, attracted to the nest, are often themselves egg-predators (e.g., Foster, 1990; Fitzgerald, 1991; Sikkel, 1994b). In males, courtship activities that reduce costs for females may be favored even if (or possibly because) they are costly for males. For example, female travel costs may be offset by increasing the conspicuousness of the signal, making it easier for females to locate the territory, or by courting females in their own territories and leading them to the spawning site, as occurs in many damselfish species (Karino, 1995). Numerous examples demonstrate the effects of the costs and/ or benefits of courtship mentioned above on different components of courtship and mating in fishes (e.g., Reynolds, 1993; Godin and Briggs, 1996; Foster 1994). Among male-territorial species represented in California, male garibaldi (Hypsypops rubucundus) (Fig. 19-4), painted greenling, and plainfin midshipman have been observed to decrease courtship when eggs are in an advanced stage of development (DeMartini, 1987, 1988b; Sikkel, 1989). Where it has been measured, this change in male behavior is associated with a decrease in plasma levels of androgens (Sikkel, 1993; Knapp et al., 1999). At least in the first two species, females virtually never spawn in such nests (low benefit to courtship) but may eat eggs (high cost to courtship). These patterns have also been well-documented for populations of three-spined sticklebacks (Rohwer, 1978) although they cannot be assumed to be universal given the high degree of among-population variation in behavior in this species (Bell and Foster, 1994). Courtship effort in nesting male garibaldi also appears to be sensitive to the quality of the nest, which similarly affects the probability of female spawning. Females prefer to spawn in nests with thicker algal growth, and males whose nest quality has been reduced decrease their courtship activity relative to controls (Sikkel, 1995a). Among territorial female garibaldi, those with higher apparent intruder pressure have shorter bouts of mate-sampling and thus visit fewer males per bout (Sikkel, 1998). Visible elements of courtship displays in territory-guarding species include some combination of rapid body movements, including dips, loops, zig-zag swimming, lateral undulations, rapid swimming toward the nest (leading), opercular flaring, and conspicuous coloration. Coloration can be of two types: structural colors which are relatively permanent, and pigments, usually found in chromatophores, that can be differentially deposited into or expressed by their contraction or expansion within the chromatophores (e.g., Bagnara and Hadley, 1973; Endler, 1991). One constraint imposed on the use of visual signals underwater is the differential absorption of light wavelengths with depth and limited horizontal visibility. The latter may be particularly problematic in coastal areas, especially above Point

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F I G U R E 19-4 Male of the garibaldi, Hypsypops rubicundus guarding its nest (right). From March-July, the male builds a nest on the reef. He cleans away all growth except for filamentous red turf algae and trims the nest into an oval about 50 cm in diameter. The male garibaldi displays near the nest and makes clicking noises to lure females. After entering, a female lays her eggs within the nest and the male fertilizes them externally. The eggs attach to the nest where the male aggressively guards them for up to two weeks at which time the larvae hatch and enter the plankton. Photo by P. C. Sikkel.

Conception, where the effects of upwelling are most prominent and visibility is reduced, and less so around the Channel Islands offshore of southern California. Thus, carotenoidbased pigmentation will only be visible in shallow water, and the effectiveness of any color, along with behavioral displays, will often only be effective over short distances. Sex-specific coloration (sexual dichromatism) used in reproductive communication falls into three categories. First, dichromatism can be present year-round, with no change between spawning and nonspawning periods. Second, it can be seasonally permanent (always present during the spawning period) but disappear during the nonspawning period. Color differences may persist only during mate-visiting, pairing, or spawning. Selective forces other than reproduction that affect selection on background coloration will place constraints on the types of permanent or temporary sex-specific coloration, and in our ability to determine what, if any, role those colors play in courtship and mate choice. In many cases, coloration can serve more than one function. For example, color patterns used by males to attract females may simultaneously serve as warning signals directed at conspecific males (e.g., Xiphophorus swordtails: Morris et al., 1995; painted greenling: DeMartini, 1985). Moreover, some species exhibit considerable amonghabitat color variation that represents differences in habitat use, rather than the influence of sexual selection. Finally, some fishes may detect light wavelengths, such as ultraviolet (McFarland and Loew, 1994; Losey et al., 1999), that are not

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perceived (and are thus ignored) by human investigators. Nevertheless, some studies have found evidence of a role of male-specific coloration and female mate choice in some maleterritorial marine fishes (e.g., Warner and Schultz, 1992). All types of reproductive coloration are represented among California’s territorial or reef-associated marine fishes. Among the temperate reef fishes found off California’s coast, highly conspicuous (at least to humans) coloration for either sex is extremely rare, unlike their tropical counterparts, and is limited to a few tropical derivatives usually found south of Point Conception. In three of these (the orange garibaldi damselfish, the blue and red bluebanded and zebra gobies), there is no apparent sexual dichromatism. In contrast, the large, male-territorial (Adreani et al., 2004) sheephead wrasse (fig. 19-5) is conspicuously dichromatic and dimorphic, and the smaller, also male-territorial rock wrasse less so (fig. 19-6). None of these species, except perhaps male rock wrasse (DeMartini, pers. obs.), exhibit seasonal or spawning-specific changes in coloration. Among the generally less conspicuous male territorial species, easily distinguishable permanent or seasonal dichromatism is also uncommon. Notable exceptions include two hexagrammids (kelp greenling Hexagrammos decagrammus; painted greenling: DeMartini, 1985, 1986; figs. 19-7 and 19-8), in which males and females occupy different microhabitats. Both of these species also exhibit additional sex-specific color patterns during courtship and spawning, which seems to be almost universal among the cryptically

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F I G U R E 19-5 Terminal phase male (top),

primary phase female (middle), and juvenile phase (bottom) California sheephead Semicossyphus pulcher (artwork by L. G. Allen).

F I G U R E 19-6 Terminal phase male (top),

primary phase male/female (middle), and juvenile phase (bottom) rock wrasse Halichoeres semicinctus (artwork by L. G. Allen).

colored (see Eschmeyer et al., 1983) hexagrammids, scorpaenids, cottids, blenniids, and clinids that have been studied. Most commonly, the courtship-associated color patterns involve an overall or partial darkening or paling relative to their typical color pattern. In some species males and females intensify the sex-specificity of colors and patterns during courtship (e.g., pale head spots are emphasized and dark trunk speckles are suffused as blotches by male and female kelp greenling, respectively; pale spots on the head and trunk are contrasted against a deeply darkened background color by male painted greenling: fig. 19-8; DeMartini, 1985). One of the more intriguing forms of courtship display that involves temporary color change is light produced by bioluminescent photophores. Although bioluminescent communication is found in some terrestrial organisms, it appears to be particularly common among nocturnal and deep-water marine organisms (Lloyd, 1977; Herring 2000). However, at the low densities often characteristic of some deep-sea fishes for which bioluminescence is thought to be important, it is unclear whether light can be seen at sufficient distances to

F I G U R E 19-7 Male (top) and female (bottom) kelp greenling Hexagrammos decagrammus. Dark-blotched pattern appears on female only during courtship (artwork by L. G. Allen).

serve as a primary attractant (Baird and Jumper, 1995; Herring, 2000). Instead, chemical or other factors may serve as the primary attractant, with bioluminescence functioning at closer distances. Among coastal California species, the use of photophores during courtship has been suggested for plainfin midshipman (Crane, 1965; Christophe and Baguet, 1985). However, in their detailed laboratory studies of courtship in this species, Brantley and Bass (1994) did not observe bioluminescence during courtship. Given the geographic variation in the expression of bioluminescence in this species, their observations may reflect a local anomaly. Clearly more work is needed to resolve the role of bioluminescence in courtship in this species. The typical motor patterns described above that are performed during courtship appear to be visual signals; however, they may often be perceived instead or additionally through the acoustico-lateralis system or may provide a means of dispersing reproductive pheromones (Shinomiya and Ezaki, 1991). In many paternal-caring species, if the male is successful in attracting a female to the nest, he will often swim rapidly around and may even bite her until or even during spawning, and may also chase her from the nest before, during, or after spawning. However, it is unclear whether the female is being evicted from the nest or is being chased in response to her deviation from spawning-typical motor patterns or position, which could signal her intention to eat eggs. Among species found in the region covered by this review, courtship displays such as these have been observed in pomacentrids (Sikkel, 1988; Lott, 1995), clinids (Coyer, 1982), hexagrammids (DeMartini, 1985, 1986), gobiids (Cole, 1982), cottids (Munehara, 1988; Hayakawa and Munehara, 1996); and scorpaenids (Helvey, 1982; Shinomiya and Ezaki, 1991; Gingras et al., 1998). Courtship-associated motor patterns, morphology, and color-changes also occur in females, perhaps most notably, but not solely, in those species in which males are frequently the limiting sex (e.g., syngnathids). Perhaps the simplest form of female visual display indicative of spawning-readiness, and potentially quality, is a swollen abdomen often associated with ripe eggs in the ovary. The best documented example of female courtship in paternal-caring fishes is the solicitation display of female threespine sticklebacks, which approach nesting males in a head-up posture, exposing their egg-

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F I G U R E 19-8 Juvenile (top left), adult female (mid and lower left), and adult male (top-bottom right) painted greenling

Oxylebius pictus (after DeMartini, 1985 with permission from Allen Press).

swollen abdomen. The use of dummies to isolate the effects of morphological features from other, potentially confounding, effects of female behavior has shown that male courtship response is positively influenced by the head-up posture and size of the swollen abdomen (Rowland 1982, 1989, 1994; Bakker and Rowland, 1995). More recently, the effect has been shown to be strongest when models are shaped to include the lordosis posture exhibited by females with the highest degree of spawning readiness (Rowland et al., 2002). However, visible (to the human observer) swelling or lordosis does not appear to be universal in fishes. In garibaldi, females searching for males do not

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appear obviously swollen but erect their median and pelvic fins and swim with exaggerated lateral undulations. Males court a female that swims in such a manner but when she retracts her fins and resumes swimming in a normal fashion, she is ignored or chased (Sikkel, 1988). Female painted greenling similarly exhibit stereotyped swimming movements a meter above the substratum, associated with a distinctive color change when approaching territories of nesting males who subsequently court them (DeMartini, 1985), and female Hypsoblennius exhibit a distinctive color change along with a submissive posture when approaching male nests (Losey, 1976). As with males, temporary color changes in females typ-

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ically involve an overall or partial darkening or paling, relative to typical background coloration and to male coloration. Acoustic signals associated with courtship occur in a wide range of fishes, and, where males defend reproductive territories, are typically performed by males (e.g., Myrberg, 1972; Hawkins, 1993). Sounds have also been recorded during spawning itself (e.g., Lobel, 1992; Lobel and Mann, 1995). Muscular squeezing of the swimbladder often produces sounds, and some species rapidly chatter the pharyngeal teeth (Rice and Lobel, 2002). To our knowledge, courtship sounds have been reported for only two male-territorial species found off California’s coast: garibaldi and midshipman toadfishes. However, it is likely that use of acoustic signals during courtship, much of it inaudible to human observers, is quite common. For example, while acoustic courtship signals are unknown for California’s gobies, drumming and tonal sounds, which appear to be produced by contraction of the swimbladder, have been recorded for nesting males of other goby species in the presence of females (Tavolga, 1958a; Lugli et al., 1995). Courtship sounds have also been reported in male blennies (Tavolga, 1958b). The gasbladder musculature of Sebastes rockfishes is indicative of a sound-producing function (Hallacher, 1974) although no studies have described the use of sound during courtship in this genus. Like many other pomacentrids (e.g., Myrberg, 1972), male garibaldi produce loud chirping or thumping sounds during signal jumping displays, when leading females to the nest, and occasionally while spawning (Sikkel, 1988). Because they occur simultaneously, it is difficult to decouple the function or effect of sound versus the visual component of the display. However, females of at least some species respond to recorded courtship sound, independent of the presence of a courting male, and only during the spawning period and when their eggs are ripe (Mohler, 1984; Myrberg et al., 1986). This suggests that sound at least can have an independent effect. Unique sounds associated with spawning itself have also been reported in pomacentrids (Lobel and Mann, 1995). The mechanism of sound production in pomacentrids is still uncertain. Whether sounds produced by garibaldi convey information aside from the male’s location, reproductive state, and likely species identity is unknown. Acoustically based species and even individual recognition have been reported in some pomacentrids (Myrberg and Spires, 1972; Myrberg et al., 1978; Spanier, 1979; Myrberg and Riggio, 1985), and sound is also a reliable indicator of male size, with larger males producing lower frequency sounds (Myrberg et al., 1993; Lobel and Mann, 1995). Among the best documented examples of auditory courtship signals in fishes are the batrachoidid toadfishes (e.g., Gray and Winn, 1961), including the nocturnally spawning plainfin midshipman (Ibara et al., 1983). Although both Type I (nesting) and Type II (sneaking) male midshipman, as well as females, are capable of producing grunts, used in agonistic interactions, only nesting males produce the long-duration (up to 14 min) hums, which can be heard over many kilometers during the spring-summer spawning period. Type I males are much larger and have a sixfold larger sonic muscle than do Type II males (Brantley and Bass, 1994). Nest-guarding Type I males begin humming shortly after dusk. Under laboratory conditions, ripe females appear excited when in the presence of a humming male and orient toward the source of the sound. The fundamental frequency of the hum is temperature dependent (Brantley and Bass, 1994). Again however, whether

sufficient among-male variation in hum characteristics exists and whether it is used by females during mate choice is unclear: captive females attracted to nests of humming males spawned or exited the nest without spawning in approximately equal proportion, suggestive of female discrimination among males. The release of water borne molecules that affect the reproductive behavior of conspecifics and thereby act as reproductive pheromones has been reported for males and females of some fish species. Many, perhaps most, of these pheromones appear to be steroid hormones, prostaglandins, or their metabolites that leak from or are excreted by the fish and thus can be used to convey information about the reproductive status and possible quality of individuals. Such hormonal pheromones can affect same and/or opposite sex conspecifics and can have either priming or releasing effects on the receiver. For recent, thorough reviews on the role of hormonal pheromones in fish reproduction, see Sorensen and Stacey (1999), and Stacey and Sorensen (2002). Evidence for hormonal or other reproductive pheromones has been found in over 100 species that include six orders found off California and adjacent waters (Clupeiformes, Osmeriformes, Salmoniformes, Scorpaeniformes, Perciformes, and Petromyzontiformes). Interestingly, in the latter (lampreys), a bile steroid appears to serve as the sexual attractant (Li et al., 2002). Thus, it seems likely that the use of pheromones in at least some aspects of courtship and spawning in reproductively territorial fishes off California is widespread. Direct or circumstantial evidence of the production of pheromones that affect female reproductive behavior has been reported for males of at least seven fish families that include California residents, although to our knowledge this list does not specifically include members that are found off California’s coast. Among the earliest documented indications of male courtship pheromones comes from studies on nesting male gobiids (Tavolga, 1956), which also provided the first evidence of the use of hormone-derived pheromones for courtship in male fishes (Colombo et al., 1980). In many gobies, males possess a specialized testicular gland (Miller, 1984). This gland contains high concentrations of Leydig cells that produce androgen conjugates that appear to attract and stimulate ovoposition in females of at least one species (Gobius niger  G. jozo of Columbo et al., 1980), and evidence of physiological response to both conjugated and unconjugated steroids has been found in another goby (Murphy et al., 2001; Murphy and Stacey, 2002). Male reproductive pheromones also occur in nest-guarding cottids (Dmitrieva et al., 1988) and blenniids, the latter including at least one species (Salaria pavo) that appears to possess a specialized organ for pheromone production (Stacey et al., 1986; Zeeck and Ide, 1996; Oliveira et al., 2001). Losey (1969) described the release of pheromones produced by males of the genus Hypsoblennius that included two species found off California. However, these pheromones, produced by courting and spawning males, appeared to attract other males and not females. Territorial male Sebastes inermis and S. miniatus (not a confirmed male-territorial species) direct their urogenital region toward the head of females during courtship, suggesting release of a pheromone (Shinomiya and Ezaki, 1991; Gingras et al., 1998). Release of reproductive pheromones appears to be much more common in females, even among male-territorial species (Stacey, 1987). Tavolga’s (1956) classic work on Bathygobius soporator included the demonstration of a female pheromone

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that triggers courtship in males. Similarly, exposure to water from peri-ovulatory females increases courtship rates by male blackeye gobies (Rhinogobiops  Coryphopterus nicholsi) compared to water from empty tanks or water from non periovulatory females (P. Sikkel and B. Shoplock, unpubl. data). In paternal-caring species where male courtship and female spawning site choice appear to be affected by egg developmental stage, the proximate causes are not well understood. Given the widespread occurrence of reproductive pheromones released by adults, the release of inhibitory or stimulatory compounds from the eggs themselves is an intriguing possibility. In species that live or spawn in aggregations or schools, or in which males are haremic and thus control access to females, prospective mates are usually in close proximity and thus the challenge of attracting or locating a mate is greatly simplified. However, in all cases in which fertilization is external and gametes are released into the water column, spawning must be highly synchronized, especially when spawning occurs in pairs. As in other organisms, this can be accomplished by some combination of tactile, visual, olfactory, and auditory cues. For example, male nudging of the female’s abdomen is an extremely common prelude to spawning ascent in many reef fishes (Thresher, 1984), and sound production associated with the spawning rush has been reported in some (Lobel, 1992). In captive studies, Hovey (2001, unpublished data) reported temporary sex-specific color patterns and male nudging of females prior to release of gametes in giant sea bass (Stereolepis gigas: Polyprionidae) and white seabass (Atractoscion nobilis: Sciaenidae), and suggested that auditory croaking may also be important for the latter. In nonharemic pair-spawners with internal or external fertilization, courtship may also be used in partner choice. The best known examples among internal fertilizers are various poeciliid species in which males circle and perform lateral displays to females, many displaying sexually dimorphic coloration or appendages (e.g., guppies: Kodric-Brown, 1985; swordtails: Basolo, 1990b). Observations of courtship have been described for at least three group-living and internally fertilizing species of the northeastern Pacific: the shiner perch, Cymatogaster aggregata and kelp perch, Brachyistius frenatus (Wiebe, 1968; Shaw and Allen, 1977; DeMartini, 1988a), and the blue rockfish Sebastes mystinus (Helvey, 1982). In outdoor aquaria, male shiner perch established courting sites of about 2 m diameter and courted females as they passed. Males courted females regardless of female reproductive state. Moreover, they courted males that were not exhibiting the male courtship coloration and chased those that were. Courting males often darken, and follow females, quiver and perform lateral displays, often in a rapid pattern in front or alongside of the female. Whether males also release pheromones during this behavior is unknown. Gravid females have blue, black, and gold bars, compared with the more silvery coloration of other females and perform courtship displays similar to those of males. Male darkening during apparent courtship and intermale visual displays has also been observed in three other silvery embiotocids: rubberlip seaperch (Rhacochilus toxotes), white seaperch (Phanerodon furcatus), and pile perch (Rhacochilus vacca) (E. DeMartini, unpubl. obs.). In the blue rockfish, males perform stereotyped lateral displays and caudal fin fanning that includes presentation of the male’s highly visible genital papilla to the female (Helvey, 1982). As expected, the least amount of data on any details of courtship or spawning behavior are available for pelagic

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species that do not spawn close to shore, such as all or most scombrids, some clupeids, and engraulids. To our knowledge, the only data on the behavior patterns involved in courtship and spawning in pelagic fishes found off California’s coast come from captive studies of Pacific bonito (Sarda chiliensis) (Magnuson and Prescott, 1966). Courtship in this species is behaviorally dimorphic—females swim with a wobbling motion caused by tilting the body 5–15 degrees from the vertical and depressing the dorsal fin while being propelled by low amplitude, high frequency tail beats; other characteristic female behaviors include circle swimming near the water surface. Males “follow” females, sometimes assume vertically barred feeding colors, often nose the female’s caudal fin to initiate wobbling, and perform lateral displays of intense feeding colors, with all vertical fins erected, to other male followers. Actual spawning (evidenced by release of a visible cloud of milt) occurs only if the male and female physically separate from the school to form a temporary pair; females flee from groups of following males (Magnuson and Prescott, 1966). The spawning habits of coastal pelagic species that groupspawn are better documented, although it is difficult to observe individual behavior. Spawning has been observed in Pacific herring (Clupea pallasii), California grunion (Leuresthes tenuis), surf smelt (Hypomesus pretiosus), and Pacific sandlance (Ammodytes hexapterus). During the late fall-winter spawning period, herring amass over shallow algal or seagrass beds along shores of northwest North America. Fertilization is external, and adhesive eggs attach to the vegetation. The release of gametes is so synchronized and massive that water visibility can be reduced to centimeters, and a milt cloud, visible over kilometers, can persist for several days. Although the factors that influence and synchronize the movement of herring to the inshore spawning grounds are unclear, once inshore, spawning appears to be synchronized by a sex pheromone (Stacey and Hourston, 1982; Sherwood et al., 1991; Carolsfeld et al., 1997). Herring collected from spawning aggregations and held in tanks rarely spawn. However, adding a small amount of milt or extracts of dissected testes can induce spawning. This is a rare example of a bisexual releasing pheromone in fishes. Most visitors to the beaches of southern California are familiar with the massive nocturnal runs of pelagic grunion on fine-sand beaches from March to August. The southern California species (L. tenuis) is one of only two known species of grunion and is strictly a nocturnal spawner. Large numbers of grunion wash ashore on waves during two monthly bouts lasting about 3 days, beginning approximately 3 or 4 days after full and new moons. Spawning begins just after high tide and continues for 1 or 2 hours thereafter. Females position themselves vertically (tail-first) in the sand and deposit eggs. Males encircle the bodies of females, releasing large volumes of milt (fig. 19-9). Individuals are then washed back into the water by the next wave. Eggs hatch and larvae are dispersed 2 weeks later during the next series of high tides. In contrast, the other species, L. sardina, found in the Gulf of California, spawns during day and night between January and May, depending on the time of highest high spring tide (Thomson and Muench, 1976). The spawning act of this species is also much shorter (less than 10 sec). Thomson and Muench (1976) speculated that this could be attributable to the shorter period, lower amplitude waves of the northern Gulf compared with coastal southern California. Surf smelt spawn on gravel (rather than sand) substrata in intertidal zones along shores of the Pacific Northwest. Sandlance spawn on fine sand to mixed sand-gravel substrates.

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F I G U R E 1 9 - 9 Spawning California grunion (Leuresthes tenuis) on a beach in southern California. Females position themselves vertically (tail-first) in the sand and deposit eggs. Males encircle the bodies of females, releasing large volumes of milt. Photo by M. H. Horn.

Unlike grunion, surf smelt and sandlance eggs are scattered over gravel as the female swims, rather than buried in the substratum (Thompson et al., 1936; Penttila, 1997). Spawning male surf smelt are smaller than females; males are gold compared to the silver-white females. Also unlike grunion, surf smelt runs occur only during the day, from May to September. Sandlance spawn from November to mid-February in Puget Sound, Washington; their diel spawning periodicity however is unknown (Penttila, 1997). Given the evidence for the use of hormonal pheromones to synchronize spawning in osmerids (Stacey and Sorensen, 2002), their use in surf smelt, at least, seems likely.

Diel Spawning and Hatching Patterns The time of day during which reef-associated fishes spawn and the time of day at which zygotes or larvae enter the plankton have received considerable attention in tropical reef fishes, and sufficient data are available in tropical species to search for or detect generalities and to test predictions of hypotheses to explain the observed patterns (Johannes, 1978; Barlow, 1981; Thresher, 1984; Robertson, 1991; Sancho et al., 2000; Petersen and Warner, 2002). For fishes that release gametes directly into the water column, the time of spawning corresponds precisely with the time zygotes enter the plankton, and the time of day during which fish spawn should reflect the (potentially opposing) effects of time of day on predation risk to and dispersal of propagules as well as adult predation risk, conflicting behavioral demands (e.g., feeding, visiting cleaning stations), and interference with other species. For those species that deposit eggs on the substratum, the time of day of spawning and emergence of larvae into the plankton may not be linked, although the time of laying may affect the diel time of hatching. Thus, the time of spawning may be more likely to be affected solely or primarily by adult biology, and hatching time should be affected by predation risk and possibly factors that affect dispersal in benthic spawners. Existing data for tropical reef fishes suggest that water-column spawners might differ from benthic spawners in diel time of spawning. Among tropical reef species that release gametes into the water column, spawning times are variable among and

even within species and the factors responsible for these differences are unclear. Trends in diel peaks in spawning and egg hatching are much more discernible, however, for tropical reef fishes that deposit eggs on the substratum. Spawning most often occurs during early morning in substrate spawners. Some variation exists that appears to be linked to social structure: dawn spawning peaks appear to be more common among species in which both sexes are territorial than in species in which only nest-guarding males are territorial (Kohda, 1988). It has been suggested that this behavior reflects an adaptive response to changes in the activity patterns of territory intruders, which are lower at dawn than during other daytime periods (Kohda, 1988). Given that most of these data come from studies on damselfishes, which are mostly tropical in distribution, it is noteworthy that garibaldi at Santa Catalina Island, where both sexes are also territorial, spawn throughout the day with no dawn peak (Sikkel, 1995b). Again, sufficient data on diel spawning periods and territorial intruder pressure are lacking for most temperate pomacentrids or temperate representatives for other predominantly tropical groups (e.g., blennioids) to determine whether the departure exhibited by garibaldi is representative of temperate conditions. Among truly temperate families, or families with many temperate representatives, the hexagrammids, cottids, and clinids appear to exhibit sufficient variation in social structure and other aspects of reproductive ecology to warrant further investigation on determinants of diel spawning cycles in benthic spawners. For example, in the painted greenling (in which both sexes defend territories) back-calculations using egg developmental stages suggest early morning spawning activity (DeMartini, 1985). Opportunistic observations of the confamilial kelp greenling suggest that at least some spawning might occur during mid-day in this species (DeMartini, 1986). Hatching of substratum-attached eggs occurs exclusively at night among tropical reef species that have been examined (Thresher, 1984; Robertson et al., 1990; McAlary and McFarland, 1993) and is thought to be an adaptive response to predation on emerging larvae. A patient observer can wait near a nest with advanced-stage embryos at dusk and, with the aid of a red light, observe larvae emerging from eggs and swimming toward the surface as darkness falls. Exposure to light during the hatching phase will inhibit hatching (McAlary and McFarland, 1993). To our knowledge, among benthic-spawning representatives found off California and adjacent waters, data are available only for one tropical derivative (garibaldi), which also has nocturnal hatching (Alcalay and Sikkel, 1994). Diel time of hatching in general might be less predictable, hence less subject to related adaptations in diel time of spawning, in temperate species whose spawn masses contain large embryos that develop slowly (often requiring a month or longer to hatch) at cold water temperatures.

Behavioral and Evolutionary Ecology of Reproduction The reproductive ecology of California marine fishes is certainly most unique and interesting because of its taxonomic diversity and biogeographic variability, attributes which make many of these fishes ideal candidates for comparative studies of mating systems, gender allocation, sexual selection, and parental care. In this section, each of these topics will be considered in turn. California species representatives of several tropical lineages (the serranid subfamily Serraninae, the fami-

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lies Labridae and Gobiidae) exhibit uniquely diverse gender allocation patterns and mating systems. Representatives of the boreal-cold temperate Scorpaeniformes (the family Cottidae in particular), including but not limited to Californian species, are obvious candidates for both phylogenetic and biogeographic studies of parental care.

Mating Systems and Gender Allocation A fundamental aspect of reproductive ecology is the suite of behaviors, collectively described as mating systems, which describe the reproductive interrelations of individuals in population units (Berglund, 1997). Mating systems in all organisms can be categorized based on the manner in which adults associate to reproduce. Basically there are two qualitatively different modes of mating association: polygamy (in which multiple partners of one or both sexes associate for reproduction) and monogamy (associations limited to singletons of each sex). The former span a range of degrees of extra-pair associations from polygamy to promiscuity (Berglund, 1997). P ROM I SCU IT Y

Truly promiscuous spawning, in which two or more (often many more than two) individuals briefly associate to exchange gametes, is the most prevalent type of mating system in marine and freshwater fishes (Thresher, 1984; Berglund, 1997). Promiscuity is the most prevalent mating type in schooling and migratory (e.g., coastal and open-ocean pelagic) species such as clupeids (sardines, herrings), scombrids (mackerels, tunas), and other open-water fishes. Representative California marine examples among pelagicspawners span a diverse array of families, from tiny schooling forage fishes like anchovies to huge apex predators such as swordfish. Promiscuous spawners also include site-attached reef-dwellers like painted greenling (DeMartini, 1987) and garibaldi (Sikkel, 1988, 1989) in which individuals of each sex court and spawn sequentially with multiple members of the opposite sex and the male remains to tend broods of benthic spawn. Individual females in paternal egg-tending species that exhibit the latter type of promiscuity include those in which entire clutches (discrete egg productions of females) are completely allocated to one male (painted greenling: DeMartini, 1987) as well as those like garibaldi in which clutches are only partially spawned per spawning bout and the eggs within clutches are distributed among multiple males (Sikkel, 1988). Promiscuous spawning entails more than the absence of any predictable association between the reproductive act and the use of spatial resources such as mating (or feeding) areas. Rather, the fundamental characteristic of promiscuity is successive spawning by both sexes with multiple partners with minimal or no pair-bonding. Brief pair-spawns in which one male and one female exchange gametes usually involve the association of multiple partners in rapid succession and hence constitute promiscuity rather than serial monogamy. P OLYGAMY

Reproductive associations among one male and multiple females (polygyny) and among one female and multiple males (polyandry) conceptually bridge the extremes of promiscuity and monogamy. All polygamous systems entail at least a short-term pair-bond between partners. Included are mate

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defense systems in which one large, typically male, individual is able to socially dominate a harem of smaller, usually female, individuals. In another type of haremic (resource defense) system, the dominant individual of one sex (again, usually male) has the capability of controlling smaller subordinate (usually female) individuals’ access to environmental resources. Fishes like many tropical labrids (wrasses) in which the sizes of individual and collective feeding territories are both a response to and predetermined by body size (Robertson and Hoffman, 1977; Hoffman, 1983, 1985) are representative. Two likely California marine fish examples are California sheephead (Warner, 1975a; Cowen, 1990) and rock wrasse (Diener, 1976; E. DeMartini, unpubl. obs.). A common feature of all polygamous mating systems is that they evolve and are maintained only if the fitness benefits to individuals at a minimum meet some system-specific environmental potential for polygamy, above which polygamous individuals enjoy disproportionate fitness benefits (Emlen and Oring, 1977). Haremic resource defense systems by definition usually involve some type(s) of reproductive territoriality, which, as already stated, has been well documented for very few California marine fishes. Territoriality in California marine and other fishes is of course not limited to reproduction only. Again, few documented cases exist for California marine fishes. A conspicuous exception is the black perch Embiotoca jacksoni, for which an important secondary function of territoriality (feeding) has been experimentally demonstrated by Hixon (1981). Grant (1997) has recently reviewed the general topic of territorial behavior in fishes. Further discussion of nonreproductive territoriality and related agonistic behaviors is beyond the scope of this chapter (see chapter 17 for more information). MONO GAMY

Monogamy requires more than a short-term, exclusive physical association between two individuals of the opposite sex. Many monogamous fishes are dioecious (Barlow, 1984), but monogamous relationships also occur in which two hermaphroditic individuals spawn with one another exclusively (Pressley, 1981) or nearly so at low population densities (Petersen, 1990b). Among the best-known examples of monogamous hermaphrodites, for which there are no described California examples, are the egg-trading hamlets, a group of small-bodied, site-attached Caribbean serranines (Fischer, 1980). Unstudied California examples of possibly monogamous hermaphrodites are Diplectrum spp, small-bodied serranines of southern Baja southward (Bortone, 1974, 1977). At its most extreme, monogamous mating systems extend beyond courtship and spawning to include mutual defense of shared spatial resources such as foraging and sheltering territories, sometimes involving lifetime pair bonds in long-lived species. There are thought to be three major selective agents favoring monogamy in fishes: the requirement of more than one parent to provide some type of post-zygotic care; paired defense of some spatially delimited resource; and restricted access to mates in sparsely distributed (e.g., small-bodied and site-attached) fishes (Berglund, 1997). The occurrence of simultaneous hermaphroditism within monogamously mated pairs has been described in many species of small-bodied, siteattached tropical serranines besides the hamlets; these likely represent cases of efficient gender allocation and monogamy within sparsely distributed, low-density populations (Pressley, 1981; Fischer and Petersen, 1987).

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Known examples of monogamous California marine fishes are few and include a single species of extremely site-attached goby (the blind goby, Typhlogobius californiensis: MacGinitie, 1939). The blind goby seems to exemplify small-bodied, siteattached, and relatively immobile species for which restricted access to mates has favored the evolution of monogamy (Barlow, 1984). Monogamous pairs of blind gobies exhibit biparental care of demersal eggs within their burrow, and the species is apparently dioecious (MacGinitie, 1939). Predation risk is a related and complementary selective agent favoring monogamy in small-bodied, site-attached species (e.g., many coral-inhabiting gobies: Munday et al., 1998). Aquarium observations suggest that monogamy may also be the norm in the large-bodied (to 2 m) wolf-eel (Marliave, 1987), but more long-term field observations are needed to substantiate this. In the freshwater tropics, many species of cichlids form monogamous bonds that are required for both parents to feed and protect free-swimming young from predators (Perrone and Zaret, 1979). There are no described or likely cases of monogamy required for biparental provisioning of young among California marine fishes. There also are no known or likely cases of paired defense of spatial resources, such as the feeding territories of corallivorous chaetodontids on coral reefs. The relation between synchronous hermaphroditism and monogamy provides but one example of the linkage between mating systems and gender allocation. The size-advantage model, whereby the largest, most dominant individuals of the limiting (usually male) sex are able to sequester the most or best of environmental resources such as spawning sites (Berglund, 1997), amply describes the evolution of promiscuity and/or harem polygyny and protogynous sex change in many lineages of tropical coral reef fishes. The size-advantage model can be briefly summarized as follows: under conditions of intense competition for resources, lifetime individual reproductive success can be maximized if individuals spawn as females when small (and incapable of securing access to highquality resources and female mates, were they to first mature as males) and as males when large and capable of securing access to resources and females (Warner, 1975b, 1988a,b). Protogyny has thus far been described for diverse lineages representing at least 17 families of reef and other inshore tropical fishes worldwide (table 19-2), a proportion greatly exceeding that in the resident California marine fauna (table 19-3). Protandry has been described in fewer families, also primarily tropical in origin. Protandry may be driven by “fecundity selection” in which the largest-bodied females are inordinately fecund, and represents another expression of the sizeadvantage model (Warner, 1975b, 1984). Three primarily tropical families (Serranidae, Labridae, and Gobiidae) are well-represented by species in California for which protogynous sex change and promiscuity/polygyny is either known or likely. It is intriguing that, in California waters, all three of these families also include species that comprise at least some gonochoric individuals (all mature individuals derived directly and independently from immature fish). For example, among California serranines, barred sand bass (Paralabrax nebulifer: Oda et al., 1993) and spotted sand bass (Hastings, 1989; Hovey and Allen, 2000) have populations composed of protogynous as well as gonochoric males. Smith and Young (1966) described the kelp bass P. clathratus as a secondary gonochore evolved from a hermaphroditic ancestor, although incomplete histological evidence presented therein and limited additional evidence (Oda et al., 1993) suggest some degree of bisexuality or sex change

in some individuals. Likewise among the California Labridae, California sheephead (Warner, 1975a; Cowen, 1990) and rock wrasse (Diener, 1976) are protogynous, while the senorita, Oxyjulis californica, is a gonochore (Diener, 1976). Rock wrasse, unlike the monandric sheephead, are diandric (populations comprise adult males derived from two sources—secondary males derived from sex-changed adult females and primary males derived directly from undifferentiated immature fish: Diener, 1976). Among the gobies of California, protogyny has been documented in the blackeye goby (Cole, 1983; Cole and Shapiro, 1990) and protogyny, simultaneous hermaphroditism, and bidirectional sex change have been described for Lythrypnus spp. (St. Mary, 1993, 2000). Gonochorism is the most probable type of sexuality, however, in several other California gobiid genera (Ilypnus, Quietula, and Clevelandia: Brothers, 1975). Whether gonochorism in these and other gobies is primary, or secondarily derived from protogynous ancestral lineage, is generally unknown but now amenable to scrutiny using a histological-morphological metric (precursive accessory gonadal structures, pAGS), whose absence in the ovarian wall of most if not all female gobiids indicates secondary gonochorism (Cole et al., 1994). There are at least another dozen species of California Gobiidae for which gender allocation is totally unknown. In all three of these groups of fishes, there appears to be a temperate-tropical pattern to the distribution of gender allocation types. For example, although some temperate-zone serranines are protogynous hermaphrodites (e.g., Centropristes striatus in the western Atlantic: Lavenda, 1949) or comprise populations of mixed gonochores and protogynous hermaphrodites (some California populations of spotted sand bass: Hovey and Allen, 2000), all of the two to four known secondarily gonochoric species of serranines occur in temperate waters. Kelp bass may be the only completely gonochoric serranine of California. All California serranines might be derived from hermaphroditic tropical ancestors (Smith and Young, 1966), but recent phylogenetic evidence casts doubt on this hypothesis (Pondella et al. 2003). The only other definite, secondarily gonochoric serranine is the South American species, Paralabrax humeralis (Borquez et al., 1988). Sex ratios suggest that the golden spotted rock bass Paralabrax auroguttatus is a gonochore in the northern Gulf of California (Pondella et al., 2001). The barred sand bass may be a functional gonochore derived from a protogynous ancestor (Hovey et al., 2002). Allied temperate-zone gonochores are the striped bass (Morone saxatilis) of the east coast of North America (purposely introduced to the San Francisco Bay estuary from the Atlantic USA in the late 1800’s: Scofield, 1931), the European sea bass Dicentrarchus labrax of the eastern Atlantic and Mediterranean (Pawson and Pickett, 1996), and the Atlantic wreckfish Polyprion americanus (Roberts, 1989). These allied species are temperate sea basses of the families Moronidae and Polyprionidae. A California example of the latter family is the fishery-protected giant sea bass (Hovey, 2001), whose gender allocation type is unknown. All serranid groupers of the subfamily Epinephelinae thus far studied are monandric protogynous hermaphrodites except for the gonochoric Nassau grouper Epinephelus striatus (Sadovy and Colin, 1995) and the diandric E. andersoni (Fennessy and Sadovy, 2002), Cephalopholis boenak, and perhaps a few others (Chan and Sadovy, 2002). Likewise, all basslets of the subfamily Anthiinae are protogynous, including the minority of species that inhabit temperate waters ( Jones, 1980; Webb and

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F I G U R E 19-10 Adult male of the cottid Clinocottus acuticeps showing highly developed intromittent organ in this copulating species (after Bolin, 1944 with permission from Stanford University Press).

Kingsford, 1990). Described gonochoric species within the primarily tropical Labridae comprise only the senorita in California; Notolabrus fuscus of temperate New Zealand waters (Denny and Schiel, 2002); and several other, also temperate, species of the genera Centrolabrus, Ctenolabrus, and Symphodus (Crenilabrus) in the northeastern Atlantic (Dipper and Pullin, 1979). The latter genera include species with reproductively territorial, dimorphic males; and some species of Symphodus care for nests of demersal eggs. It is thought that the cost of paternal care constrains the evolution of sex change in these species (Warner and Lejeune, 1985). The tautog Tautoga onitis of the west Atlantic is probably a gonochoristic species with some vestiges of protogyny (White et al., 2003). Gender allocation is unknown in one slightly dichromatic and reproductively territorial, pelagic group-spawning (Wicklund, 1970) labrid of the temperate-boreal west Atlantic, the cunner Tautogolabrus adspersus (Pottle and Green, 1979). We could find no records at all of gonochorism in tropical labrids even though a sister group of tropical labroids (parrotfishes of the family Scaridae) include species of known gonochores as well as monandric and diandric protygynous hermaphrodites (Robertson and Warner, 1978; Robertson et al., 1982). Most gonochoric species of the primarily tropical Gobiidae occur in temperate waters: these include the temperate genera Gobius and Pomatoschistus and both temperate and tropical species of the genus Bathygobius (Cole, 1988, 1990). The only other well-documented gonochores among tropical gobies are Gobiosoma illecebrosum and G. saucrum (Robertson and Justines, 1982). Most known hermaphroditic species of tropical gobies inhabit coral reefs. All three species of California gobies known to be hermaphroditic (bluebanded, zebra, and blackeye gobies) are rock reef associates; most other species of California gobies inhabit (burrows in) soft substrates. The available evidence thus strongly suggests that the development of gonochorism in some temperate species of serranine serranids, gobiids, and labrids is related to some aspect(s) of temperate zone environments. Several, possibly interacting factors are discussed in the fourth section.

Sexual Selection and Mate Choice Sexual selection, the process responsible for the evolution of secondary sexual or epigamic traits (Dugatkin and FitzGerald,

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1997), includes two components: intrasexual selection (typically male-male competition) and intersexual selection (mate choice, usually by females). The most conspicuous, hence wellknown, adaptations are the secondary sexual characteristics and sexual ornamentation used in behavioral displays between and within the sexes. Unstudied but likely California examples of the latter include the sexually dimorphic, supraorbital crests (fatty forehead tissues) of the crested prickleback Anoplarchus purpurescens (Coleman, 1992) and similar, sexually dimorphic head features of the wolf-eel (Marliave, 1987). Possibly analogous head morphologies occur in several other stichaeids (the monkeyface prickleback Cebidichthys violaceus, Xiphister atropurpureus, and X. mucosus: Hart, 1973). Whether the apparent sexual dimorphisms in some of these zoarcoids vary with reproductive seasonality—or even whether they in fact are sexual ornaments—is unknown. Moderate-to-great dimorphisms in body size are especially common and most striking in spawntending hexagrammids of the eastern and western Pacific. Sexual dimorphisms are minor or only temporary, however, in most other lineages of California fishes. Sexual dimorphisms are largely lacking in most groups in which one might expect them, such as the spawn-tending cottids. Most of the malefemale differences in cottid morphology and coloration are temporary and related to seasonal reproduction. For example, male red Irish lords (Peden, 1978; DeMartini and Patten, 1979) and scalyhead sculpin Artedius harringtoni (Hart, 1973; Ragland and Fischer, 1987) develop pectoral fin spination and hypertrophied head cirri during their respective breeding seasons. Perhaps the most striking morphological difference between the sexes in cottids is the prominent penis of males in some species, a primary rather than secondary sexual characteristic (fig. 19-10; see Bolin, 1944 for other examples). Livebearing embiotocids also copulate (e.g., see Hubbs, 1917), but male surfperches use a gonopodium of modified anterior anal fin rays (Shaw, 1971) instead of a penis for copulation. In general the extent to which sexual characteristics such as the intromittent organs of males represent intra- vs. intersexually selected traits is poorly understood in the cottids, other copulating fishes such as poeciliids, goodeids, and embiotocids, and most other organisms. Another reproductive trait subject to sexual selection is sperm storage (and related sperm competition) in copulating species with internal insemination. In this regard the North Pacific Cottidae and allied cottoids (Rhamphocottidae,

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Hemitripteridae, Psychrolutidae) provide an intriguing array of oviparous spawning traits ranging from external fertilization (Hayakawa and Munehara, 1996) to copulation with external fertilization (Munehara et al., 1989, 1991) to external fertilization after copulation by means of a protrusible/retractable female genital duct (Munehara, 1996). Fertilization modes in cottids are overlaid by parental care states that range from paternal to maternal and biparental (DeMartini, 1978b; DeMartini and Patten, 1979; Hayakawa and Munehara, 1996) to no care at all (Marliave, 1981b; Munehara, 1996). Mode of fertilization (internal versus external) has been considered as one reproductive trait that is perhaps both the result of, and further subject to, sexual selection (see Perrone and Zaret, 1979). Although viviparous species by definition copulate and have internal fertilization, some species in at least three genera of oviparous North Pacific marine cottids exhibit copulation with external fertilization (Munehara et al., 1989, 1991; Munehara, 1996). Even though the males of many North Pacific cottids have large intromittent organs (Bolin, 1944), apparently not many cottids with intromittent organs and copulation have internal fertilization. In species like the silverspotted sculpin and elkhorn sculpin (Alcichthys alcicornis) of the western North Pacific, sperm attach to, but do not penetrate, the egg micropyle within the ovary post-copulation, and fertilization occurs some time later at the time of egg extrusion. Apparently an increase in chorionic permeability resulting from a change in calcium ion concentration between the ovarian environment and seawater induces penetration of eggs by sperm (Munehara et al., 1989, 1991) as the eggs are extruded. The demersal spawns produced by these species have been described as resulting from external fertilization and internal gametic association (Munehara et al., 1989, 1991). Apparently this is also true for agonids, scorpaeniforms closely related to the cottids (Yabe, 1985); insemination in at least one agonid species occurs by eversion followed by retraction of the female genital duct (Munehara, 1997). Wonders of physiological and morphological mechanisms aside, the more pertinent questions are what ecological and evolutionary factors have selected for the decoupling of copulation and fertilization and how might this be related to sperm storage, sperm competition, and parental care in this group of fishes. Sperm storage and competition in promiscuous and polygynous species are unavoidably linked to the issue of paternity, particularly in species with paternal care (Perrone and Zaret, 1979). This is true even if the evolution of paternal care is not necessarily precluded by copulation and internal (or delayed) fertilization (Dawkins and Carlisle, 1976). Several case studies have documented paternal care in copulating cottids (Ragland and Fischer, 1987; Munehara et al., 1990, 1994). Data on the distribution of fertilization modes among species of cottids with and without intromittent organs and copulation are lacking. As far as is known, copulating cottids are either promiscuous or polygynous and thus storage of sperm within the female invariably must result in some degree of sperm competition among males (see Koya et al., 2002). Given the many parental care patterns and the diverse morphologies of spermatozoa (Hann, 1930) in North Pacific cottids, it is almost certain that sperm competition varies greatly among species of sculpins despite the present scant evidence. Unfortunately, empirical proof of sperm competition is lacking for almost all cottid species. Hayakawa et al.’s (2002a, b) recent documentation of a fertilization-shielding sperm morph in Hemilepidotus gilberti, a noncopulatory parental-guarder with sneak-spawning males, provides strong circumstantial

evidence. Petersen et al. (2004) provided another, more recent example in the roseylip sculpin, Ascelichthys rhodorus. Evidence for sperm competition can often be deduced from large testes-to-soma weight ratios (Stockley et al., 1997; e.g., the embiotocid Micrometrus minimus: Warner and Harlan, 1982). Data on relative testes weights, however, are nearly nonexistent for cottids. It is likely that copulation has evolved in numerous genera of cottids and cottoids primarily as a ploy to counter sperm competition among males (C. Petersen, pers. comm.) and might not have evolved at all in this group if not for sperm competition (Munehara, 1999). Sperm competition is a major cost of male reproduction and the storage and mixing of multiple males’ sperm within females exacerbates costs to and competition among males (Petersen and Warner, 1998; Petersen et al., 2001). The females of some cottid species store sperm for some time within their reproductive system after copulation. Species like the silverspotted sculpin (Munehara et al., 1991) and Japanese sea raven Hemitripterus villosus (Munehara, 1996) copulate some time prior to when eggs are (fertilized as they are) laid, embryos develop slowly through the wintertime period of low productivity, and large feeding larvae hatch into the early plankton bloom when the size spectrum of planktonic prey is suitably large. One possible reason for the delay between copulation and fertilization in these species might be a disconnect between the time for joining of the sexes and the initiation of embryonic development. The initiation of development is likely determined by optimal time for hatching (entry of larvae into the planktonic production cycle), which in turn is a function of the size of individual eggs (larvae-at-hatch), mean water temperature, and rate of embryonic development (Bagenal, 1971; Pauly and Pullin, 1988). Perhaps the delay in hatching of large feeding larvae until early in the next planktonic production cycle has selected for the temporal decoupling of fertilization and copulation in some sculpins. Not all copulating cottids delay fertilization or store sperm appreciably, however. Male elkhorn sculpin and perhaps scalyhead sculpin appear to tend unrelated spawn (fertilized by a previous copulation with another male) in return for the opportunity to copulate with the female whose spawn they tend (Munehara et al., 1990; Ragland and Fischer, 1987). In cottids lacking appreciable sperm storage, copulation likely has evolved primarily or solely as a response to sperm competition among males.

Parental Care Patterns and Implications Obviously the most extreme expression of parental care is matrotrophic viviparity. One fascinating group of live-bearing fishes, unique to the North Pacific except for a few species in South American and North Atlantic waters (Moser et al., 2000), are the sebastine scorpaenids of the genus Sebastes. In the past simply considered ovoviviparous, the genus Sebastes is now recognized as a complex of reproductively as well as taxonomically diverse fishes spanning a range of combinations of offspring provisioning via ovarian egg yolk and maternal nourishment in utero (Wourms, 1991; Hopkins et al., 1995). Some species might be considered nearly ovoviviparous because nearly all embryonic nutrition derives from the yolk sequestered in ovarian eggs (S. flavidus: 3% non-yolk; Hopkins et al., 1995). At the other extreme, at least one species (S. schlegeli) is extremely matrotrophic in that 92% of embryonic nutrition derives from the extra-oocyte fetal-maternal exchange

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TA B L E 19-4

Eastern North Pacific Marine Sculpins Known to Exhibit Post-Zygotic Parental Care or Aparental

Species Artedius fenestralis Artedius harringtoni Artedius lateralis Ascelichthys rhodorus Asemichthys taylori Blepsias cirrhosus Clinocottus acuticeps Clinocottus analis Clinocottus globiceps Clinocottus recalvus Enophrys bison Gilbertidia sigalutes Hemilepidotus hemilepidotus Jordania zonope Leptocottus armatus Myoxocephalus polyacanthocephalus Nautichthys oculofasciatus Oligocottus maculosus Oligocottus snyderi Orthonopias triacis Rhamphocottus richardsoni Scorpaenichthys marmoratus Synchirus gilli NOTE:

Parental Care

Reference

male male male grouped males extraspecific none none none none none male male female/biparental male male (?)

DeMartini and Patten 1979; Peterson et al. 2004 DeMartini and Patten 1979; Ragland and Fischer 1987 Petersen et al. 2005 DeMartini and Patten 1979; Peterson et al. 2004 Kent et al. 1997; D Kent pers.com Munehara 1991 Marliave 1981b DeMartini and Patten 1979 E DeMartini unpubl obs DeMartini and Patten 1979 DeMartini 1978b J Marliave (pers com) in Matarese et al. 1989 DeMartini and Patten 1979 Lamb and Edgell 1986; C. Petersen pers. com. DeMartini and Patten 1979

male none none none none male male none

D Kent, pers. comm. DeMartini and Patten 1979 DeMartini and Patten 1979 E DeMartini, unpubl. obs. Bolin 1941; E DeMartini, unpubl. obs. Munehara et al. 1999 Lauth 1989 Marliave 1975; Marliave et al. 1985

List includes Cottidae, Hemitripteridae, Psychrolutidae, and Rhamphocottidae.

of nutrients (Boehlert et al., 1986, 1991; Hopkins et al., 1995). Several of the relatively few, additional species thus far studied represent cases of intermediate maternal provisioning (S. melanops: 69%, Boehlert and Yoklavich, 1984; S. caurinus: 12%, Dygert and Gunderson, 1991). Unlike the embiotocids, some Sebastes spp. have evolved superfoetation; individuals of a dozen species produce as many as three overlapping broods per spawning season (Love et al., 1990). Spawning seasons of most eastern Pacific Sebastes are protracted even in species without superfoetation. Copulation-fertilization typically occurs at or near the end of a period of relatively high adult food abundance in the fall, when large female energy stores are available to yolk eggs. Following several months gestation, parturition of young is timed to broadly overlap with a peak in planktonic productivity sometime in the spring (Larson, 1991). It is likely that the partially lecithotrophic viviparity of Sebastes spp. is an adaptation whereby females are able to incrementally adjust the relative contributions of ovum yolk and subsequent maternal stores to embryo nutrition, depending on unpredictable fluctuations in productivity (MacFarlane et al., 1993; MacFarlane and Bowers, 1995). Parental care patterns within the order Scorpaeniformes, the family Cottidae in particular, represents an intriguing diversification that might have both phylogenetic and biogeographic elements. In the Cottidae, the locally most diverse group with prevalent parental care that has been fairly well studied to date, both phylogenetic and biogeographic influences are evident. Some genera like Oligocottus and Clinocottus appear to be aparental, whereas other genera such as Artedius and Hemilepidotus exhibit care (table 19-4). It is noteworthy that there also appears to be a geographic component to care patterns within the eastern Pacific Cottidae. The relative num-

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ber of parental caregivers tends to decrease among species with southern affinities (i.e., those whose ranges extend south of Point Conception into the Southern California Bight) although the relationship is not significant (table 19-5A). The sizes of eggs (larvae at hatching) also tend to be larger for eastern Pacific cottids with more northerly distributions (x2  5.75; df  1; 0.02  P  0.01, ns because the 26 species in 18 genera were not independent; table 19-5B). We speculate that there has been stronger selection for post-zygotic care of the larger eggs (larger larvae) necessary to overcome the vicissitudes of larval advection in the more intensely upwelled regions north of Point Conception. Larger embryos whose development is further protracted at colder water temperatures remain at risk longer to reef-based predators and are likely to benefit more from parental care. We caution however that the extent to which phylogeny and biogeography might be confounded within the Pacific marine cottids is unknown. Data are insufficient for more refined analyses of patterns within cottid genera; data on egg production (fecundity and spawning frequency), largely lacking for northeast Pacific cottids, might help clarify patterns of investment at the species level. It is beyond the scope of this review to attempt to map parental care patterns on phylogenies within the Cottidae. C.W. Petersen of the College of the Atlantic, Bar Harbor, Maine, is presently conducting studies of mating and parental care systems in northeastern Pacific cottids.

Filial Cannibalism as a Mating Tactic Filial cannibalism (the consumption by parents of related offspring) appears to be an important sexually selected trait in

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TA B L E 19-5

Parental Care and Egg Size of Eastern North Pacific Sculpins (A) Parental care with care without care

Above Point Conception 83.3 (10) 16.7 (2)

Below Point Conception 45.5 (5) 54.5 (6)

Above Point Conception 71.4 (10) 28.6 (4)

Below Point Conception 16.7 (2) 83.3 (10)

(B) Median egg size egg size above median egg size below median

NOTE: (A) Percentage of species with known parental care (versus no post-zygotic care) in eastern North Pacific (ENP) sculpins whose southern geographic range limits lie at or above versus below Point Conception, California (34.5 N). (B) Percentage of ENP sculpin species with egg size greater than (versus less than) median egg size (1.5 mm, all species) whose southern limits lie at or above versus below Point Conception. Range data: Miller and Lea (1972), Hart (1973). Egg size data: Budd (1940), Washington et al. (1984), Feeney (1987), Tokranov (1988), Matarese et al. (1989), Munehara and Shimazaki (1991), and C. Petersen (pers. comm.; Artedius fenestralis: 1.1–1.2 mm; A. harringtoni: 0.9 mm; Jordania zonope: 1.8  mm). Numbers in parentheses indicate number of species.

teleost fishes (Hoelzer, 1995; Lindstrom, 2001), and its existence has been confirmed for several species of freshwater sunfishes and darters by genetic typing using microsatellite markers present in tissues of parental males and consumed eggs (DeWoody et al., 2001). Both filial cannibalism and heterocannibalism (consumption of unrelated conspecifics) are now recognized as widespread phenomena among teleost lineages, especially spawn-tending species (Dominey and Blumer, 1984; Elgar and Crespi, 1992; Smith, 1992; Smith and Reay, 1991; Manica, 2002). Apparent filial cannibalism is widespread among hexagrammmid and cottid scorpaeniforms of the Pacific Northwest (DeMartini, 1976), and its importance is recognized for at least one spawn-tending perciform of California (garibaldi: Sikkel, 1994a, b). Although cannibalism of offspring directly benefits the male tending parent energetically, it is often utilized as a mating tactic that appears to enhance the reproductive success of the filial cannibal indirectly and, as a tactic, is thus subject to sexual selection by affecting and being affected by female mate choice (DeMartini, 1987; Sikkel, 1988, 1989, 1994a, b). We conclude this section with a brief further discussion of how filial cannibalism might importantly relate to the mating and parental care systems of the California Hexagrammidae and Cottidae. One major reason why paternal male spawn-tenders may cannibalize some of their genetic offspring is because priorspawned embryos serve, depending on context, either as a female attractant or repellant. There are at least several, nonmutually exclusive (and likely complementary) reasons for this. First, the presence of prior spawns signals to prospective future female mates that the male is a good mate/parent, and this might be important for species in which copying is an evolved basis for female choice (e.g., Sargent, 1997). Second, the presence of other females’ spawns acts to dilute predation risk over clutches within the male’s brood (akin to the “safety in numbers” effect of schooling). Third, the presence of earlydevelopment (visibly uneyed) embryos signals that a male is early in its mating cycle and hence more likely to accept and defend the prospective female’s clutch until hatching. Conversely, the presence of late-development (visibly eyed) spawn is a signal that a prospective female’s clutch would more likely be eaten as an investment towards increasing the male’s future reproductive success. In general, the younger eggs in mixed-age broods are more likely to be partially filial cannibalized and relatively small broods (e.g., single clutches) are more apt to be completely filial cannibalized by paternal males. All

of these factors have been documented to varying degrees in painted greenling (DeMartini, 1987) and garibaldi (Sikkel, 1994a,b). However in the latter, the cannibalism of relatively older (but still young) eggs is dependent on their position in the nest and the phase of the brood cycle (Sikkel, 1994a). Cannibalism by male spawn-tenders also might be a tactic to counter cuckoldry by sneak-spawning, nonterritorial males. Heterocannibalism (Rohwer, 1978) therefore is likely more complex than mere raiding among neighboring spawn-tenders. Although egg cannibalism is widespread in the Hexagrammidae, the occurrence and nature of filial cannibalism has been questioned in some species (Munehara and Miura, 1995). The occurrence and activities of sneak-spawning males have recently been documented in numerous species of western north Pacific hexagrammids (Hexagrammos otakii, H. octogrammus, H. agrammus: Munehara et al., 2000; Munehara and Takenaka, 2000). Both in situ remote video records (Munehara at al., 2000) and genetic evidence of multiple paternity in single-male-tended broods (Munehara and Takenaka, 2000) have been demonstrated. An important counterpoint: genetic evidence also has shown that multiple females contribute clutches to single-male-tended broods in kelp greenling (Crow et al., 1997) and other fishes such as mottled sculpin Cottus bairdi, a freshwater cottid (Fiumera et al., 2002). In situ observation of spawning has also confirmed multiple-female contributions to male-tended clutches in many other fishes, including garibaldi (Sikkel, 1988). The occurrence of filial cannibalism selects for additional mating ploys and counterploys. One such ploy might be alloparental care. Alloparental care of non-kin spawn has been described for males of the elkhorn sculpin. In elkhorn sculpin, males usually tend embryos that they have not fathered after they copulate with the female who has spawned them (Munehara et al., 1990, 1994). Male care of unrelated eggs in this case is not cuckoldry (as care of non-kin fertilized by sneak-spawners would be), but more likely reflects females’ trading copulation for paternal care (Munehara et al., 1994). That unrelated eggs are used as courtship dummies (Rohwer, 1978) in elkhorn sculpin is further supported by the observation of frequent male desertion of nesting sites near the end of the spawning period when the expectation of future spawnings is low. Using prior spawns to attract additional females is commonplace in promiscuous male spawn-tenders. Elkhorn sculpin are highly promiscuous and males tend the clutches of tens of females over a protracted spawning period (Munehara

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et al., 1990). Piracy, an extreme form of alloparental care in which the most dominant male individuals usurp the spawning territories and nesting materials of other, territorial but subdominant males, spawn in the latter males’ territories, then desert spawn to defense by the cuckolded males, has been described in some peacock wrasse (Symphodus tinca) populations in the Mediterranean (van den Berghe, 1988). Alloparental care and cuckoldry, however, should not be assumed prevalent in all species of paternal-tending fishes (e.g., mottled sculpin: Fiumera et al., 2002). Also documented are several other fascinating behaviors that may be evolved responses by males and females to filial cannibalism or some other tactic related to asymmetric parental investment by the two sexes. One recognized ploy involves egg mimics (egg-like protuberances and color spots on the anal, pelvic, or dorsal fins of male darters of the family Percidae: Knapp and Sargent, 1989; Strange, 2001; Porter et al., 2002), which apparently function to deceive prospective female mates by advertising that males already possess more tended spawn than they in fact do. Possible California examples include the scalyhead sculpin, in which males develop apparent egg mimics on their anal fin during the breeding season (Ragland and Fischer, 1987), and male red Irish lords and other North Pacific hemilepidotine cottids (Peden, 1978) that acquire white spotting on darkened pelvic fins during their breeding seasons. Another counterploy, this time performed by females of a species of filial cannibalistic warm-temperate blenniid (Kraak, 1996), is the partial spawning of 1 to 10 test eggs that may be used to evaluate the prospective male’s ability and willingness to tend the female’s full complement of several hundred eggs (Kraak and van den Berghe, 1992). Another recently discovered female counterploy is the provision of low-energy (unyolked) dummy eggs in the male mouth-brooding cardinalfish Apogon lineatus (Kume et al., 2002). In this species, in which males disproportionately cannibalize smaller-than-averagesized clutches, females perhaps deceive males by producing clutches that on average contain about 18% unyolked eggs; these seemingly large clutches might be less filial cannibalized by males (Kume et al., 2002).

Gender Allocation and Parental Care in Temperate versus Tropical Environments California marine fishes exhibit a diverse array of mating systems and related sexually selected traits such as dimorphisms and filial cannibalism, but neither the frequency of occurrence nor degree of expression of these traits is unusual compared to fishes elsewhere. Eastern north Pacific fishes are exceptional only in the preponderance of viviparous and parental-caring species. And, although not unique to California, the occurrence of secondary gonochorism in species within three distinct lineages of tropical origin in California showcases a phenomenon common to other temperate regions. So why might viviparity and other, less extreme forms of parental care have evolved so frequently in so many lineages of California marine fishes? And, why might the development of secondary gonochorism be such a uniquely temperate phenomenon? Perhaps these questions might be more appropriately rephrased as: “Why is parental care not more prevalent on tropical reefs?” and “Why is hermaphroditism and sex change relatively common in tropical, but not temperate, reef fishes?” We believe that the interactions among several environmental factors (habitat persistence, on- versus off-reef egg predation,

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the environmental potential for polygamy [EPP] of adults) provide at least partial answers to these questions. In the remainder of this section, we discuss each of these factors in terms of their effects on gonadal allocation and parental care.

Hermaphroditism and Secondary Gonochorism Two major factors promoting the evolution of simultaneous hermaphroditism (and monogamy) are low adult densities and small home ranges (Jones, 1980), the latter often related to small adult body size (DeMartini, 1997). Greater numbers of species of predominantly small and rare fishes occur per unit habitat area in tropical versus temperate seas (Fishelson, 1989). Home ranges of small-bodied species tend to be more constrained because smaller-bodied species must be more siteattached to avoid predation (DeMartini, 1997), and the diversity and relative abundance of predatory fishes is generally greater on tropical versus temperate reefs (Parrish, 1990; Ebeling and Hixon, 1991; Hixon, 1991; Friedlander and DeMartini, 2002). The movements of all fishes, but especially small-bodied species, are more constrained on tropical reefs—all other anti-predator tactics such as schooling being equal. It is thus easy to visualize how monogamously paired, simultaneous hermaphrodites might have evolved on tropical reefs. The evolution of sequential hermaphroditism, protogyny in particular, also might be favored on tropical reefs wherever the EPP and inter-individual variance in fitness are greater and there is more extreme intra- and inter-sexual competition for mates. In tropical reef fish populations occurring at greater than sparse densities, individuals of the same and the opposite sex typically compete for multiple partners and often exhibit sizebased dominance and related extreme variations in individual reproductive success (Warner et al., 1975; Warner, 1984). Secondary sexual dimorphisms and dichromatisms are especially pronounced in protogynous groups such as the tropical labroids. Body size obviously influences the potential for sequential sex change. Larger-bodied species have greater scope for size-based dominance relationships, and sequentially hermaphroditic fishes tend to attain larger adult size than simultaneously hermaphroditic species (Smith, 1965; Jones, 1980). The most striking examples of these are the serranine and epinepheline serranids: serranines are typically 20 cm long, whereas many of the epinepheline groupers attain lengths of more than a meter (to 2 m in Epinephelus lanceolatus; Myers, 1999). Sexual competition for mates may be less on temperate reefs because the production (and tending) of demersal eggs constrains mate monopolization. Prime spawning sites which function to launch planktonic eggs to avoid reef-based egg predators, avoid predators on spawning adults, and which provide disparately large fitness payoffs (Warner and Schultz, 1992; Warner and Dill, 2000), also may be more economically defensible and monopolizable on tropical reefs. We further suggest that tropical and temperate reef systems generally differ in the spatial and temporal dispersion patterns of reproductive resources that include available members of the potentially limiting (usually female) sex to the limited (male) sex. The evolution of resource defense mating systems is likely facilitated by fundamental territoriality (Emlen and Oring, 1977; Grant 1997) that may be more prevalent among tropical reef fishes. To the extent that reproduction is aseasonal (or at least less seasonal) and more temporally asynchronous among females on tropical reefs, there should be further selection for

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polygamous matings (Emlen and Oring, 1977). Because of the fitness costs in maintaining simultaneous hermaphroditism under conditions conducive to multiple promiscuous matings as gonochores, selection should favor the development of secondary gonochorism on temperate reefs because the potential fitness payoffs are inadequate for extreme polygamy and sequential sex change to evolve and be maintained. Hermaphroditism and parental care have variously influenced the development of one another in labrids, gobiids, and serranine serranids. Care patterns reinforce gender allocation patterns in the Labridae; at least some species in one of three temperate northeastern Atlantic genera have evolved paternal care and all of these are gonochoric (Warner and Lejeune, 1985). Parental care patterns complicate gender allocation in both temperate and tropical Gobiidae, however. Californian and other Lythrypnus spp. exhibit paternal care despite simultaneous and bidirectional hermaphroditism (St. Mary, 2000). Many tropical gobiid genera such as Gobiodon, Trimma, Priolepis, and Bryaninops exhibit paternal care, yet pair monogamously as simultaneous or even bidirectional hermaphrodites (Kuwamura et al., 1994; Nakashima et al., 1995; Sunobe and Nakazono, 1993, 1999; Munday et al., 2002). These cases may represent frequency-dependent dynamic tradeoffs between the competing benefits of hermaphroditic monogamy and paternal care-gonochorism in extremely site-attached habitatspecialists (Munday et al., 1988; Munday, 2002). Parental care of course does not complicate gender allocation in all hermaphroditic fishes—serranines for example spawn pelagic eggs and lack parental care (Thresher, 1984; Fischer and Petersen, 1987). Interestingly, the only other family of primarily tropical reef fishes that is conspicuously present in California is the Pomacentridae (damselfishes), and both of two species (garibaldi and blacksmith Chromis punctipinnis) exhibit paternal care of demersal spawn and are gonochores (Turner and Ebert, 1962; DeMartini et al., 1994). The relation between parental care and gender allocation is more complicated in tropical pomacentrids. All known species of pomacentrids exhibit paternal care and all limit care to demersal spawn except for Acanthochromis polyacanthus and two Altrichthys species in which both parents additionally tend free-swimming fry after hatching (Thresher, 1985; Leis and McCormick, 2002). But not all tropical pomacentrids are gonochores. Most or all species of the genus Dascyllus are protogynous hermaphrodites (Godwin, 1995; Asoh et al., 2001). All anemonefishes of the subfamily Amphiprioninae thus far studied are protandrous hermaphrodites, and most species are monogamous and have paternal or biparental care (Moyer and Nakazono, 1978). Presumably, protogyny in Dascyllus spp. is due to extreme male disadvantage at small body sizes (Godwin, 1995) rather than the cost of paternal care and selection against sex change, and protandry in anemonefishes likely reflects fecundity selection. It would seem that the influence of parental care on gender allocation varies among tropical fish lineages. Nonetheless, the growth (and perhaps survivorship) costs involved in sex change should select against hermaphroditism when the competing costs of parental care are as large as generally occur on temperate reefs.

Viviparity and Parental Care Parental care in tropical reef fishes is likely disfavored in part because of greater selection for the planktonic dispersal of propagules away from benthic habitats whose persistence is

less assured. The preponderance of planktonic spawners (versus live-bearers and demersal egg-brooders) on coral reefs must in part reflect the greater probability that suitable habitat patches will disappear in between fish generations due to the occurrence of relatively frequent, major physical disturbances like hurricanes (Barlow, 1981; reviewed in Sale, 1991). Parental care on tropical reefs is also likely constrained by the relatively high risk (compared to temperate reefs) of demersal egg loss to benthic-feeding fishes (Johannes, 1978). The mortality rates of planktonic eggs and larvae clearly are high for both temperate and tropical reef fishes; even so, relative on- vs. off-reef egg survivorships must differ between temperate and tropical reefs. It appears that the higher probability of predation on demersal eggs in the tropics has restricted the evolution of demersal spawning to lineages with special anti-predatory adaptations. These comprise fishes that benefit from multiple defenses by nesting in large colonies such as some pomacentrids (in California: Panamic sergeant major Abudefduf troschelii: Lott, 1995; blacksmith: Turner and Ebert, 1962) and balistids (Gladstone, 1994; Kawase, 1998), and species that utilize various types of additional protection for eggs spawned on exposed surfaces such as proximity to stinging anemones in Amphiprion spp. anemonefishes (Moyer and Nakazono, 1978) or that have toxins in eggs (the pufferfish Canthigaster valentini: Gladstone, 1987). Also included are small-bodied (5–10 cm long), burrow- and tube-dwellers (gobiids and chaenopsids like Emblemaria hypacanthus: Hastings, 1992), which possess a physical refuge for their spawn as well as themselves. Many species of small-bodied (10 cm long) tropical coral reef fishes that are site-attached to shelter both as adults and juveniles as an anti-predator adaptation might provide parental care of eggs after oviposition in part because small body size limits fecundity and low fecundities constrain dispersal (Barlow, 1981). Several species of tropical batrachoidids (e.g., Amphichthys cryptocentrus: Hoffman and Robertson, 1983) are unusual in that individual males of these relatively large-bodied (to 25 cm) species tend demersal spawn and fry within excavated burrows in which the male also shelters. Unlike the situation in California and other temperate regions, care of spawn on exposed surfaces of coral reefs by lone individual fish, without some additional means of protection such as that afforded by synchronous nesting (e.g., among neighboring male pomacentrids), is at least extremely rare because of predation risk to eggs and perhaps also egg-tenders. Demographic studies comparing populations of species inhabiting a broad range of predation intensities on temperate and tropical reefs would be needed to test this hypothesis, such as comparative characterizations of the survivorships of both adult spawners and tended demersal egg masses for matched temperate and tropical congeners like damselfishes of the genus Chromis.

Upwelling off Pacific North America and Its Effects Environmental dichotomies between tropical and temperate reefs alone cannot explain the observed differences in parental care patterns between the Pacific coast of North America and other temperate regions. Although temperate waters everywhere vary more seasonally than the tropics, environmental uncertainty in temperate regions is represented in the extreme by upwelling systems such as that off of the coast of California and the Pacific Northwest. We speculate that the dynamic nature of upwelling has influenced the proliferation of viviparity and parental care in eastern North Pacific marine fishes, particularly those off California. Much of the western

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coast of North America including California lies in an intense upwelling system that is highly productive but also spatially heterogeneous and temporally variable (Brodeur et al., 1996; McGowan et al., 1996; Rebstock, 2003). In this uncertain environment, the natural mortality rates of planktonic eggs and larvae are high, variable, and unpredictable. As part of the price paid for facilitated dispersal by currents, sufficient concentrations of the planktonic prey of fish larvae are patchily distributed, and planktonic fish eggs and larvae are also subject to advection (physical transport) offshore to habitats unsuitable for older benthic stages (Parrish et al., 1981). Upwelling markedly influences both the dispersal and survival of pelagic propagules (e.g., see Ainley et al., 1993). Environmental uncertainty has been proposed to be an important factor that explains the apparently greater preponderance of parental care in freshwater fishes, although the difference may be due to phylogenetic bias (Gebhardt, 1987). The effects of upwelling are obvious even at relatively small spatial scales in the waters off California. The Southern California Bight represents an oceanographic (Barnett and Jahn, 1987) and biogeographic (Horn and Allen, 1978) ecotone wherein the recruitment of subtropical (and occasionally some tropical) species, transported as eggs and larvae from downcoast breeding populations, is favored whenever upwelling is relaxed during El Niño Southern Oscillation (ENSO) periods (Cowen, 1985). The relatively large young produced by parental-caring and especially live-bearing species tend to more closely resemble the species’ later developmental stages, both morphologically and behaviorally, and are more capable of actively maintaining station (Marliave, 1986), thereby reducing mortality from advection. A striking example of an adaptation to disturbance-facilitated dispersal is provided by Aulorhynchus flavidus, a paternal-tending tubesnout of California and eastern North America, which disperses eggs and fry in constructed nests anchored to detachable kelp fronds that are rafted to other kelp beds following storm dislodgment (Marliave, 1976). Future evaluations should compare the patterns of viviparity and parental care among fishes of temperate and tropical lineages in other upwelling systems (e.g., the subtropical eastern South Pacific, west Africa). Potential contrasts should also include temperate regions that lack persistent upwelling, such as much of the Pacific coast of Asia. The latter contrasts should adjust, as necessary, for biogeographic influences within major taxa such as the Embiotocidae, Cottidae, and the scorpaenid genus Sebastes, whose distributions bridge the eastern and western North Pacific (see chapter 1).

A General Model of Temperate-Tropical Dichotomies In general, substantial investment in parental care reinforces selection against sex change, hence selects for gonochorism, at least in large-bodied mobile species that (unlike smaller-bodied, site-attached species for which egg defense within shelters may be less costly) are less strongly tied to shelter for protection. The energetic and survival costs of parental care are now well recognized (Sargent, 1992; Smith and Wootton, 1995), and these costs obviously can constrain the potential for sex change. Care of offspring also lowers the advantage of sex change because mate choice by the limiting sex tends to restrict the extent of mate monopolization by the limited sex (Warner and Lejeune, 1985). Parental care thus is prevalent in temperate systems but is a relatively rare phenomenon among tropical fish lineages because, we suggest, the greater costs of producing and defending large offspring, coupled with the lower payoffs for simulta-

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neous or protogynous hermaphroditism, doubly favors the development and maintenance of gonochorism in temperate reef fishes. We provide a simple graphic model (fig. 19-11) illustrating how tropical-temperate reef differences in EPP and the need for parental care of large propagules in environments with differing ratios of on- versus off-reef offspring mortality might have favored the evolution of both sequential and simultaneous hermaphroditism in coral reef fishes, countered its primary evolution in temperate-zone lineages, and may favor its secondary loss in tropical lineages on temperate reefs.

Summary of Patterns and Promising Topics for Future Research Summary Like marine and freshwater fish assemblages elsewhere, the fishes of the Californias exhibit diverse reproductive modes, life histories, and mating and parental care systems. Species exhibiting viviparity and post-spawning parental care are unusually prevalent in the California marine fish fauna, however, and this prevalence is expressed both in terms of the number of species and the number of lineages (families) represented. Altogether, about 150 species (17%) of California marine fishes are viviparous, including 56 species of elasmobranchs (32 selachians in 12 families and 24 species in eight families of rays). The remaining 93 species of viviparous teleosts include all of the 20 marine species of Embiotocidae that occur in the eastern Pacific, nearly 70 species of rockfishes of the genus Sebastes (Scorpaenidae), and four genera of viviparous brotulas of the family Bythitidae. Post-zygotic parental care of demersal eggs occurs in at least another 125 oviparous species of batrachoidids, scorpaeniforms (four families), and many gobiid and blennioid perciforms. Most (90%) California species with parental care exhibit exclusively paternal care, a fraction typical for marine bony fishes (Blumer, 1979, 1982). Another conspicuous aspect of the reproductive ecology of California marine fishes involves patterns of gender allocation within families of primarily tropical origin. Both gonochoric and hermaphroditic species are conspicuously represented within three marine fish families (the Labridae, Serranidae, and Gobiidae) in California waters. It must be more than coincidence that both gonochoric and hermaphroditic species are present in each of these three families in the temperate North Atlantic as well and that no temperate-zone lineages in either area include both hermaphrodites and secondary gonochores. Clearly, some common features of temperate zone environments influence the expression of hermaphroditism in a manner independent of phylogeny. We offer a conceptual model suggesting that both parental investment (viviparity and post-zygotic parental care) and biogeographic patterns of gender allocation are related to the unpredictably variable oceanographic environment of the California upwelling system. The rocky inshore fishes of the Californias have evolved in productivity regimes that are both spatially and temporally variable and unpredictable, even though the scope for temporal fluctuations is greater north of Point Conception compared to the Southern California Bight. Point Conception is a long-recognized biogeographic boundary that represents an important productivity threshold as well. Differences in parental care and related gonadal investment per offspring above and below Point Conception are suggestive in at least one family (Cottidae). Tropical reef fish

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F I G U R E 19-11 Conceptual model depicting the relative influences of various environmental factors selecting for sequential sex change and its loss (secondary gonochorism) in tropical and temperate fish lineages.

families are largely restricted to the generally lower productivity regime of the Southern California Bight. We argue that the more variable and less predictable environments north of Point Conception (and extending north of California through the Pacific Northwest) have placed a premium on greater degrees of parental investment (viviparity, care of benthic spawn) in temperate-boreal lineages to augment offspring survival at the expense of adaptations (such as sex change) related to inter- and intra-sexual competition for mates. The secondary loss of flexible gender expression in some species within tropical lineages (serranine serranids and labrids) most likely reflects the discontinuance of sufficient selection for sex change, resulting from lower maximum extents of polygamous mate monopolization. The next challenge will be to respecify this general model as testable hypotheses and conduct the detailed field observations and controlled experiments necessary to test them. This will not be easy. For example, a study of matched gonochoric-protogynous species or populations of Paralabrax would at a minimum require comparative estimates of size-specific egg production and the mean and variance of relative mating success, if not the absolute frequency and fertilization success of matings by numerous individuals.

Promising Research Topics A number of poorly studied families of deep-sea and open-ocean fishes like the stomiiforms, aulopiforms, and lampridiforms, and several virtually unstudied families of benthic shelf fishes

such as the agonids, cryptacanthodids and zoarcids, require fundamental surveys of their reproductive natural and life histories. Without information on these groups, our understanding of the diversity and breadth of reproductive adaptations of the California marine fish fauna will remain incomplete. The environmental and demographic factors influencing maternal investment patterns in live-bearers (embiotocids and Sebastes spp.) are another obvious research topic. Some data already exist for surfperches (Warner and Harlan, 1982; DeMartini, 1988a; Schultz et al., 1991; Schultz, 1993; Schultz and Rountos, 2001). Additional studies of the effects of differing relative maternal and paternal investments on sperm storage and sperm competition among embiotocid species are needed. Also necessary are additional characterizations of the levels of maternal investment exhibited among species of the genus Sebastes, particularly in terms of the importance of seasonal and interannual variations in upwelling and planktonic productivity on the relative contributions of lecithotrophy and matrotrophy and how these might be affected by species differences in trophic biology. No comparative information of this nature presently exists for sebastine scorpaenids. These and other topics for future research are summarized in table 19-6 and discussed in the paragraphs that follow. Further studies of the reproductive ecology of several other families of teleosts hold great promise for biogeographic (tropical versus temperate) comparisons. Studies of the relatively few Californian representatives of tropical fish families could provide much useful information for comparison with confa-

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TA B L E 19-6

Key Topics for Future Research on the Reproductive Ecology of California Marine Fishes Comparisons of relative maternal investment among species of rockfishes (F. Scorpaenidae) and surfperches (Embiotocidae) Studies of the relationship between degree of maternal investment and species’ trophic biology in rockfishes (Sebastes) Evaluation of latitudinal effects on maternal investment in species with extreme geographic ranges (Embiotocidae: shiner perch, pile perch; Gobiidae: blackeye goby) Latitudinal comparison of gender allocation patterns among populations spanning the geographic range of blackeye goby Comparative estimates of survivorship of breeding adults and tended embryos for matched temperate-tropical congeners (e.g., within the pomacentrid genus Chromis) Evaluation of relative sperm competition among species of copulating and non-copulating sculpins (Cottidae) and allied cottoids Estimation and comparison of testes weights as an index of male reproductive effort in cottoids Among-species comparisons of cottoid egg production (individual fecundity and spawning frequency) General description and comparison of gender allocation patterns within the California Gobiidae Evaluation of the relation between gender allocation and parental care in the Pomacentridae Comparisons of size-specific egg production and the mean and variance of mating success among gonochoric and protogynous individuals within populations exhibiting mixed gonochoric-protogynous gender allocation (Serranidae: spotted sand bass, barred sand bass, kelp bass) Analogous comparisons of mating success among species within families exhibiting mixed gender allocation patterns (Serranidae, Labridae, Gobiidae) General re-examination of distribution of secondary gonochorism among gonochoric species within families exhibiting mixed gender allocation patterns Comparison of viviparity and parental care patterns for fishes with temperate and tropical lineages, among lineages present in California and other NE Pacific waters, other upwelling systems (like subtropical eastern South America and west Africa), and temperate non-upwelling regions like Japan and temperate eastern Australia Evaluation of mate choice and intra- versus inter-sexual selection in local examples of likely “sex-reversed” syngnathid pipefishes Comparisons of diel spawning and demersal embryo hatching times for temperate versus tropical fish lineages of California and other regions such as temperate eastern Australia

milials in tropical regions. Tropical families represented in California and Pacific Baja waters are the Apogonidae (one species), Batrachoididae (two species), Chaetodontidae (two species), Gerreidae (at least 10 species), Gobiidae (20 species), Labridae (five species), Mullidae (two species), Pomacentridae (three species), Scaridae (one species), Serranidae (18 species), and Synodontidae (three species) (Miller and Lea, 1972; De la Cruz Aguero et al., 1997). Only the batrachoidids, gobiids, labrids, pomacentrids, and serranids, however, include species that are sufficiently common and abundant to offer further promise for detailed behavioral study. Analogous evaluations of the effects of temperate environments on reproductive strategies are needed for tropical fish lineages in other regions such as Japan and eastern temperate Australia. In particular, we stress the great potential for comparative studies of the mating systems and sex allocation patterns among gonochoric and protogynous species populations of the serranine serranids, labrids, and gobiids of California. Further studies of gender allocation patterns are needed, particularly the interplay between gonochoric and protogynous hermaphrodites within species-populations of barred sand bass and kelp bass, similar to that of Hovey and Allen (2000) for spotted sand bass. Inter-populational comparisons also are needed, particularly for species with ranges (like P. humeralis of Chile-Peru) that span tropical and warm temperate latitudes, as are interspecific comparisons within the genus Paralabrax. A general survey of gender allocation patterns in the California Gobiidae is also needed, including geographic comparisons among species-populations. Currently of great interest is the bewildering diversity of sex allocation patterns (protogyny, simultaneous hermaph-

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roditism, bidirectional sex change) exhibited within and among populations of some gobiids, both in California and on tropical coral reefs. A variety of gender allocation patterns first described for a number of small tropical serranines (Fischer and Petersen, 1987) only hinted at the great diversity of patterns now being discovered within the Gobiidae. One species whose exceptional range (nearly 3,000 km from northern British Columbia to Baja California Sur: Miller and Lea, 1972) begs for geographic comparison is the blackeye goby; this species has been described as protogynous based solely on data for populations in Barkley Sound, Vancouver Island, British Columbia (Cole, 1983), near the northern limit of its range. The only other detailed study of its reproductive ecology (Breitburg, 1987) in southern California waters demonstrated promiscuous matings and paternal care but assumed that only protogynous sex change occurred. Differences in gender allocation would not be unexpected in species like blackeye goby whose populations span several biogeographic provinces. Geographic studies of gender allocation and the comparative demography of such a species might appreciably clarify our understanding of how variable survivorship under different levels of predation influences gender allocation and mating systems in temperate and tropical reef fishes. Studies of the relations between gender allocation and parental care are generally needed for pomacentrids as well as gobiids. Also generally lacking are quantitative studies for most aspects of the behavioral ecology of temperate-boreal California fish lineages. For example, the suggestive interrelations among mate choice, sperm competition, and parental care in north Pacific Cottidae have surprisingly been ignored for several

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decades since the early studies of Patten, Marliave, and DeMartini on eastern north Pacific species in the 1970s, despite numerous studies by Munehara and coworkers on patterns of insemination and fertilization among western North Pacific species in the 1990s. A phylogenetic analysis of the distribution of copulation in eastern as well as western Pacific species of cottids (Munehara, 1999) is needed, as is a description of the patterns of male gonadal investment, including but not limited to data on size-specific testes weights for the entire family. Careful field observations and field and laboratory experiments for select species exhibiting divergent care states and mate pairing could contribute importantly to our understanding of mating and parental care systems in small site-attached fishes. Some obvious examples include intertidal spawners which lack parental care (such as Oligocottus maculosus or Clinocottus analis) and paternal-caring species with both customary, single-male spawn-tending (e.g., Artedius fenestralis) and atypical, group-male egg-tending (Ascelichthys rhodorus; DeMartini and Patten, 1979; Petersen et al., 2004). One group of California marine fishes also has special relevance for studies of the interplay between mate choice and relative maternal and paternal investments in offspring. The syngnathid pipefishes, many of which have long been suspected and have now been shown to be sex reversed (i.e., bodybrooding males are the limiting sex and females, not males, are subject to stronger sexual selection), have generated much research interest during the last decade. At least 50 papers on mate choice, sexual selection, and parental investment in syngnathids have appeared in the recent primary literature; the subjects of most of these have been a small group of pipefishes in the northeast Atlantic and Baltic Sea. Several California species such as Syngnathus californiensis would provide interesting comparative case studies. The diel time of spawning and hatching of embryos is almost completely unknown for California reef fishes. Given the ecological differences between tropical and temperate reefs, data on spawning times for the pelagic-spawning tropical derivatives found off southern California (e.g., serranids and labrids) would be instructive, as would comparative data on benthic-spawning tropical derivatives and temperate groups such as the cottids and hexagrammids. Comparisons of populations of garibaldi and other tropical derivatives (such as blacksmith, and especially species with extensive ranges like blackeye goby) from the most temperate to the most tropical extremes of their distribution also would be extremely valuable. Analogous comparative studies would be particularly useful along the east and west coasts of Australia where high levels of species diversity exist along a continuous tropical-temperate gradient. We conclude this chapter by re-emphasizing the likely great overall influence of upwelling and environmental uncertainty on the reproductive ecology of California’s marine fish fauna. While the relatively high incidence of parental care, viviparity, and secondary gonochorism each may have alternative explanations, including or confounded by phylogenetic bias, their coincidence presents a compelling correlation. We hope these patterns will stimulate and help guide future research on the reproductive ecology of fishes in the temperate eastern Pacific and elsewhere.

Acknowledgments We thank H. Munehara, R. Warner, and especially E. Schultz and C. Petersen for constructive criticisms of a manuscript

draft; N. Stacey and W. Rowland for help with references; D. Mann for explaining aspects of acoustic courtship; B. Mundy for help with references, proofreading, and his perpetual willingness to discuss fish systematics and biogeography; D. Yamaguchi for graphics assistance; L. Allen for preparation of figs. 19-5–8; S. Abbott-Stout for help with the daunting task of locating and obtaining references; and J. Kendig for editing. We gratefully acknowledge Allen Press, the Royal British Columbia Museum, and Stanford University Press for permissions to reproduce the following respective figures: fig. 19-1b (from Moser, 1967), fig. 19-3 (from DeMartini and Patten, 1979), fig. 19-8 (from DeMartini, 1985), and fig. 19-10 (from Bolin, 1944). This paper is dedicated to the memory of the late Ben Patten, a pioneer underwater naturalist of the Pacific Northwest.

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Appendix 19.1. Distribution of California and Other Marine Fishes by Reproductive Mode, Gender Allocation and Parental Care Type This table shows the distribution of reproductive modes (oviparous  ovip, viviparous  vivip), gender allocation (gonochore; or protogynous, protandrous, bidirectional, or simultaneous hermaphrodite), and post-oviposition parental care types (paternal, maternal or biparental) among orders, families, subfamilies or tribes (where variable within family), and species (where variable within subfamilies or tribes) of Californian and major, non-indigenous taxa of marine fishes. Representative species are noted in bold type if members of the California fauna. Tropical and other non-California examples are provided in support of tables 19-2 to 19-5. Gonochore-2 refers to secondary gonochore. External bodybrooding with parent-embryo nourishment indicated by superscripted asterisk (*). Taxon (Order, Family or Subfamily) Myxiniformes Myxinidae Petromyzontiformes Petromyzontidae Chimaeriformes Chimaeridae Heterodontiformes Heterodontidae Orectolobiformes Rhincodontidae Carcharhiniformes Scyliorhynidae Triakidae Carcharhinidae Lamniformes Odontaspididae Alopiidae Cetorhinidae Lamnidae Hexanchiformes Chlamydoselachidae Hexanchidae Squaliformes Dalatiidae Squalidae Squatiniformes Squatinidae Rajiformes Torpedinidae Narcinidae Rhinobatidae Rajidae Dasyatidae Urolophidae Gymnuridae Myliobatidae Mobulinae Acipenseriformes Acipenseridae Elopiformes Elopidae Megalopidae Albuliformes Albulidae Anguilliformes Muraenidae

Ophichthidae Derichthyidae

518

Mode

Gender Allocation

Parental Care

ovip

gonochore

none

ovip

gonochore

none

ovip

gonochore

none

ovip

gonochore

none

gonochore

none

gonochore

none

vivip ovip vivip vivip vivip

vivip

vivip

vivip

gonochore

gonochore

gonochore

Cox 1963; Patzner 1998

Lampetra tridentate

Michael 1984; Russell et al. 1987

Hydrolagus colliei

Cox 1963

Heterodontus francisci

Dempster and Herald 1961

Rhincodon typus

Joung et al. 1996; Colman 1997

Parmaturus xaniurus Triakis semifasciata Prionace glauca

Cross 1988; Balart et al. 2000 Kusher et al. 1992 Nakano 1994

Odontaspis taurus Alopias superciliosus Cetorhinus maximus Isurus oxyrinchus

Gilmore et al. 1983 Chen et al. 1997 Matthews 1950 Mollet et al. 2000

Chlamydoselachus anguineus Notorynchus cepedianus

Tanaka et al. 1990

Somniosus pacificus Squalus acanthias

Ebert et al. 1987 Jones and Geen 1977

Squatina californica

Natanson and Cailliet 1986

Torpedo californica Narcine brasiliensis Rhinobatos productus Raja binoculata Dasyatis longa Urolophis halleri Gymnura marmorata Myliobatis californica Manta birostris

Neer and Cailliet 2001 Villavicencio-Garayzar 1993 Timmons and Bray 1997 Zeiner and Wolf 1993 Villavicencio et al. 1994 Babel 1967 Villavicencio-Garayzar 1995 Martin and Cailliet 1988 Yano et al. 1999

Acipenser transmontanus

Chapman et al. 1996

Elops affinis Megalops atlanticus

none Crabtree et al. 1997a

Albula vulpes

Crabtree et al. 1997b

Gymnothorax fimbriata Sideria spp Rhinomuraena quaesita Gymnothorax meleagris Ophichthus rufus Derichthys serpentinus

Fishelson 1992 Fishelson 1992 Shen et al. 1979 Fishelson 1992 Casadevall et al. 2001 none

Gilbert 1981; Ebert 1989

none

none

gonochore

none

gonochore

none

ovip

gonochore

none

ovip

Eptatretus stouti

none

gonochore

gonochore

Key Reference(s)

none

vivip vivip vivip ovip vivip vivip vivip vivip vivip ovip

ovip

Representative Species

none none

protogynous simultaneous protandrous gonochore gonochore ?

B E H AV I O R A L E C O L O G Y

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Appendix 19.1. (continued) Taxon (Order, Family or Subfamily) Congridae Nettastomatidae Serrivomeridae Nemichthyidae Saccopharyngiformes Cyematidae Saccopharyngidae Eurypharyngidae Clupeiformes Clupeidae Engraulidae Gonorhynchiformes Chanidae Siluriformes Ariidae Plotosidae Osmeriformes Argentinidae Microstomidae Bathylagidae Opisthoproctidae Alepocephalidae Platytroctidae Osmeridae Salmoniformes Salmonidae Stomiiformes Gonostomatidae Sternoptychidae Phosichthyidae Stomiidae Giganturidae Aulopiformes Scopelarchidae Notosudidae Synodontidae

Mode

Gender Allocation

ovip

gonochore ? ? gonochore ?

Parental Care

Representative Species

Key Reference(s)

Gnathophis spp Venefica tentaculata Serrivomer sector Nemichthys scolopaceus

Fishelson 1994 none none Fishelson 1994

Cyema atrum Saccopharynx lavenbergi Eurypharynx pelecanoides

none none none

Opisthonema libertate Anchoa spp

Torres-Villegas and Perez-Gomez 1988 Caddell 1988

Chanos chanos

Delsman 1929

Arius graeffei Plotosus lineatus

Rimmer 1985a, b Thresher 1984

Argentina sialis Nansenia crassa Bathylagus ochotensis Opisthoproctus soleatus Alepocephalus bairdii Sagamichthys abei Hypomesus pretiosus

Bergstad 1993 none Miya 1995 Alekseyev et al. 1982 Allain 1999 none Middaugh et al. 1987

Oncorhynchus nerka

McPhee and Quinn 1998

Cyclothone atraria Sternoptyx diaphana Vinciguerria nimbaria Chauliodus macouni Gigantura indica

Miya and Nemoto 1991 Baird et al. 1990 Tomas and Panfili 2000 none none

simultaneous ?simultaneous gonochore

Benthalbella infans Scopelosaurus spp Synodus spp

Paralepididae

simultaneous

Anotopteridae Alepisauridae Myctophiformes Neoscopelidae Myctophidae

?simultaneous simultaneous

Lestidium pseudosphyraenoides Anotopterus pharao Alepisaurus ferox

Merrett et al. 1973 none Zaiser and Moyer 1981; Donaldson 1990 Mead et al. 1964

Lampridiformes Lamprididae Lophotidae Trachipteridae Regalecidae Ophidiiformes Carapidae Ophidiidae Bythitidae Gadiformes Moridae Melanonidae Macrouridae Bregmacerotidae Merlucciidae Gadidae

ovip

gonochore

ovip

gonochore

ovip

gonochore

ovip

gonochore

none

none

none

paternal paternal none

ovip gonochore ovip

maternal none

protandry ? ? ? ? ovip

none

ovip

none gonochore

ovip

?gonochore

gonochore ovip vivip ovip

none Mead 1960; Smith and Atz 1973

gonochore

Scopelengys tristis Stenobrachius leucopsaurus

none Childress et al. 1980

Lampris guttata Lophotus lacepede Zu cristatus Regalecus glesne

none none Olney and Naplin 1980 Montero et al. 1995

Carapus spp Ophidion barbatum Brosmophycis marginata

none Breder and Rosen 1966 Hart 1973

Antimora rostrata Melanonus zugmayeri Coryphaenoides spp Bregmaceros atlanticus Merluccius productus Theragra chalcogramma

Jakobsdottir and Magnusson 2001 none Stein and Pearcy 1982 Clancey 1956 McFarlane and Saunders 1997 Hinckley 1987

none

none

none

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Appendix 19.1. (continued) Taxon (Order, Family or Subfamily)

Mode

Batrachoidiformes Batrachoididae

ovip

Lophiiformes Lophiidae Antennariidae

ovip

Ogcocephalidae Caulophrynidae Melanocetidae Oneirodidae Ceratiidae Gigantactinidae Linophrynidae Mugiliformes Mugilidae Atheriniformes Atherinidae Beloniformes Belonidae Scomberesocidae Exocoetidae Hemiramphidae Cyprinodontiformes Fundulidae Stephanoberyciformes Melamphaeidae

Rondeletiidae Cetomimidae Beryciformes Anoplogastridae Anomalopidae Trachichthyidae Berycidae Holocentridae Zeiformes Zeidae Oreosomatidae Gasterosteiformes Aulorhynchidae Gasterosteidae Pegasidae Solenostomidae Syngnathidae Aulostomidae Fistulariidae Macroramphosidae Scorpaeniformes Dactylopteridae Scorpaenidae Sebastinae Scorpaeninae Sebastolobinae Caracanthidae Triglidae

520

Gender Allocation

gonochore

Parental Care

Key Reference(s)

Porichthys notatus

DeMartini 1988b, 1990; Brantley and Bass 1994

Lophiomus setigerus Antennarius striatus Lophiocharon trisignatus Zalieutes elater Caulophryne spp (jordani) Melanocetus spp (johnsonii) Oneirodes spp (acanthias) Cryptopsaras couesii Gigantactis spp (macronema) Linophryne spp (coronata)

Yoneda et al. 1997, 1998 Pietsch and Grobecker 1987 Pietsch and Grobecker 1987 none Pietsch 1976 Pietsch 1976 Pietsch 1976 Pietsch 1976 Pietsch 1976 Pietsch 1976

Mugil cephalus

Greeley et al. 1987

Leuresthes tenuis

Griem and Martin 2000

ovip ovip ovip

Strongylura exilis Cololabis saira Cheilopogon heterurus

ovip

Hyporhamphus unifasciatus

Ambrose and Moser 1988 Kosaka 2000 Dasilao et al. 1998; Ichimaru and Nakazono 1999 Durai et al. 1988

gonochore gonochore

ovip

?gonochore gonochore gonochore gonochore gonochore gonochore gonochore gonochore

ovip

gonochore gonochore

ovip

gonochore

ovip

gonochore

ovip

ovip

ovip

ovip vivip vivip ovip ovip ovip ovip

gonochore

gonochore

paternal

Representative Species

none paternal ?none none none none none none none none

none none

none none

Fundulus heteroclitus

Able 1984

Scopelogadus mizolepis

Keene et al. 1987; Andrianov and Bekker 1989; Ebeling and Weed 1963

Rondeletia loricata Cetomimus sp

none none

Anoplogaster cornuta Phthanophaneron harveyi Hoplostethus atlanticus Beryx splendens Myripristis amaena

none none Clark et al. 1994 Lehodey et al. 1997 Dee and Parrish 1994

Zenopsis nebulosus Allocyttus verrucosus

Parin et al. 1988 Lyle and Smith 1997

paternal paternal none maternal* paternal* none none none

Aulorhynchus flavidus Gasterosteus aculeatus Eurypegasus draconis Solenostomus spp Syngnathus fuscus Aulostomus chinensis Fistularia commersonii Macroramphosus gracilis

Marliave 1976 Wootton 1984 Herold and Clark 1993 Wetzel and Wourms 1995 Campbell and Able 1998 Thresher 1984 Delsman 1921; Watson and Leis 1974 Arruda 1988

none none

Dactylopterus volitans

none

Sebastes flavidus Sebastes schlegelii Scorpaena guttata Sebastolobus alascanus Caracanthus spp Prionotus evolans

Hopkins et al. 1995 Boehlert et al. 1986 Orton 1955 Erickson and Pikitch 1993 Cole 2003 McBride and Able 1994

none

none

gonochore

gonochore gonochore

?protogynous gonochore

B E H AV I O R A L E C O L O G Y

none none

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Appendix 19.1. (continued) Taxon (Order, Family or Subfamily)

Mode

Gender Allocation

Anoplomatidae Hexagrammidae Rhamphocottidae Cottidae

ovip ovip ovip ovip ovip ovip

protandrous gonochore-2 gonochore gonochore gonochore gonochore

Hemitripteridae Psychrolutidae

ovip ovip

gonochore gonochore

Agonidae Cyclopteridae Liparidae

ovip ovip ovip

gonochore gonochore gonochore

none paternal paternal none

ovip ovip ovip ovip ovip

protandrous gonochore gonochore ?gonochore

none none none none none none

Platycephalidae

Perciformes Centropomidae Moronidae Polyprionidae Howellidae Serranidae Serraninae Diplectrum spp Serranus spp

Parental Care none none none paternal paternal paternal maternal none none paternal

simultaneous simultaneous protogynous protogynous

Paralabrax spp

gonochore-2 Anthiinae Epinephelinae

ovip ovip ovip ovip

protogynous protogynous gonochore-2 protogynous ?gonochore-2 gonochore-2

tr. Grammistini Pseudochromidae Grammatidae

none none none paternal paternal

Plesiopidae Opistognathidae Priacanthidae

ovip ovip ovip

?gonochore-2 gonochore ?gonochore

paternal paternal none

Apogonidae Malacanthidae

ovip ovip

gonochore ?protogynous

paternal none

Pomatomidae Nematistiidae Echeneidae Rachycentridae Coryphaenidae Carangidae Leiognathidae Bramidae Caristiidae Lutjanidae Caesionidae Lobotidae Gerreidae Haemulidae Sparidae

ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip

none none none none none none none none none none none none none none none

Lethrinidae

ovip

gonochore ?gonochore gonochore gonochore gonochore gonochore gonochore gonochore ?gonochore gonochore gonochore ? gonochore gonochore protogynous protandrous gonochore-2 protogynous

none

Representative Species

Key Reference(s)

Inegocia japonica Platycephalus speculator Anoplopoma fimbria Oxylebius pictus Rhamphocottus richardsoni Scorpaenichthys marmoratus Hemilepidotus hemilepidotus Clinocottus acuticeps Hemitripterus villosus Gilbertidia sigalutes; Psychrolutes phrictus Podothecus sachi Eumicrotremus orbis Liparis fucensis Careproctus spp

Fujii 1971 Hyndes et al. 1992 Hunter et al. 1989 DeMartini and Anderson 1980 Munehara et al. 1999 Lauth 1989 DeMartini and Patten 1979 Marliave 1981b Munehara et al. 1997 Marliave 1981a; Drazen et al. 2003 Munehara 1997 Able et al. 1984; Matarese et al. 1989 DeMartini 1978 Somerton and Donaldson 1998

Centropomis undecimalis Morone saxatilis Polyprion americanus Howella sp

Taylor et al. 2000 Scofield 1931; Woodhull 1947 Peres and Klippel 2003 none

Diplectrum pacificum Serranus tabacarius Serranus fasciatus Paralabrax maculatofasciatus Paralabrax clathratus

Bortone 1977 Petersen 1995 Petersen 1990a Hastings 1989; Hovey and Allen 2000 Smith and Young 1966; Oda et al. 1993 Webb and Kingsford 1992 Shapiro et al. 1994 Sadovy and Colin 1995 Smith 1965 Fishelson 1989; Thresher 1984 Asoh and Yoshikawa 1996; Shapiro 1997 Fishelson 1989; Thresher 1984 Hess 1993 Colin and Clavijo 1978

Hypoplectrodes maccullochi Epinephelus guttatus Epinephelus striatus Rypticus spp Pseudochromis olivaceus Gramma loreto Plesiops nigricans Opistognathus aurifrons Heteropriacanthus cruentatus Apogon lineatus Caulolatilus princeps Pomatomus saltatrix Nematistius pectoralis Remora osteochir Rachycentron canadensis Coryphaena hippurus Trachurus symmetricus Leiognathus brevirostris Brama japonica Caristius macropus Lutjanus spp Pterocaesio diagramma Lobotes surinamensis Gerres cinereus Haemulon sciurus Calamus brachysomus Lithognathus mormyrus Diplodus sargus Lethrinus miniatus

Kume et al. 2000 Elorduy-Garay and Ramirez-Luna 1994 Conand 1975 none Morota and Fujita 1995 Brown-Peterson et al. 2001 Oxenford 1999 Macewicz and Hunter 1993 Jayawardane and Dayaratne 1998 Yoon and Shimazaki 1981 none Grimes 1987 Choi et al. 1996 none Baez and Alvarez-Lajonchere 1983 Garcia-Cagide 1986 Druzhinin 1976 Besseau and Brusle-Sicard 1995 Buxton and Garratt 1990 Bean et al. 2003

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Appendix 19.1. (continued) Taxon (Order, Family or Subfamily)

Mode

Nemipteridae

Gender Allocation

Parental Care

ovip

protogynous gonochore-2

none none

Scolopsis spp Nemipterus virgatus

Young and Martin 1985 Lau and Sadovy 2001

Polynemidae Sciaenidae Mullidae Pempheridae Chaetodontidae Pomacanthidae Pentacerotidae Kyphosidae Girellinae Kyphosinae Teraponidae Kuhliidae Cirrhitidae

ovip ovip ovip ovip ovip ovip ovip ovip

protandrous gonochore gonochore gonochore gonochore gonochore gonochore gonochore

none none none none none none none none

Polydactylus sexfilis Seriphus politus Pseudupeneus maculatus Pempheris vanicolensis Chaetodon spp Centropyge, Pomacanthus spp Pseudopentaceros wheeleri

Szyper et al. 1991 DeMartini 1991 Colin and Clavijo 1978 Golani and Diamant 1991 Hourigan 1984, 1989 Sakai 1997 Yanagimoto and Humphreys unpubl

Cheilodactylidae Cepolidae Cichlidae Embiotocidae Pomacentridae Amphiprioninae

ovip ovip ovip vivip ovip

ovip ovip ovip

Pomacentrinae Dascyllus spp Labridae

ovip

Scaridae

ovip

Pinguipedidae Bathymasteridae Zoarcidae Zoarces spp other genera Stichaeidae

ovip ovip

Cryptacanthodidae Pholidae Anarhichadidae Ptilichthyidae Zaproridae Scytalinidae Chiasmodontidae Trichodontidae Trichonotidae Creediidae Ammodytidae Trachinidae Uranoscopidae Tripterygiidae Dactyloscopidae Labrisomidae Clinidae Myxodini Ophiclinini Clinini Chaenopsidae Blenniidae

522

vivip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip vivip

?gonochore ?gonochore protogynous bidirectional gonochore gonochore gonochore gonochore protandrous

gonochore protogynous protogynous gonochore-2 protogynous gonochore protogynous ?gonochore gonochore

gonochore ?gonochore gonochore ? ? ? gonochore ? ?gonochore protogynous protandrous gonochore ?gonochore gonochore ?gonochore gonochore gonochore gonochore

Representative Species

Key Reference(s)

Girella tricuspidata Scorpis lineolata none Terapon jarbua none Kuhlia sandwichiensis none Neocirrhites armatus none Cirrhitichthys aureus none Cheilodactylus spectabilis none Cepola rubescens biparental Tilapia zillii none Embiotoca jacksoni

Pollock 1981 Dedual and Pankhurst 1992 none Tester and Takata 1953 Sadovy and Donaldson 1995 Kobayashi and Suzuki 1992 McCormick 1989 Sergiou et al. 1996 El-Zarka 1956; Loiselle 1977 Baltz 1984

paternal biparental paternal paternal none none paternal none none none paternal

Amphiprion melanopus Amphiprion clarkii Hypsypops rubicundus Dascyllus albisella Semicossyphus pulcher Oxyjulis californica Symphodus ocellatus Scarus spp, Nicholsina spp Leptoscarus vaigiensis Parapercis snyderi Rathbunella hypoplecta

Ross 1978 Moyer and Bell 1976 Clarke 1970; DeMartini et al. 1994 Godwin 1995; Asoh et al. 2001 Warner 1975a; Cowen 1990 Diener 1976 Warner and Lejeune 1985 Robertson et al. 1982 Robertson et al. 1982 Kobayashi et al. 1993 Fitch and Lavenberg 1975

none ?biparentl paternal maternal ? biparental biparental ? ?none ? ?none none none ?none

Koya et al. 1995 Levings 1969 Marliave and DeMartini 1977 Coleman 1992 Shiogaki 1982 Hughes 1986 Marliave 1987 none Fitch and Lavenberg 1971 none none Marliave 1981c; Okiyama 1990 Kusen et al. 1991 Langston 2003

none ?none ?none paternal paternal paternal none

Zoarces elongatus Lycodopsis pacificus Xiphister atropurpureus Anoplarchus purpurescens Cryptacanthodes bergi Pholis laeta Anarrhichthys ocellatus Ptilichthys goodei Zaprora silenus Scytalina cerdale Chiasmodon niger Trichodon trichodon Trichonotus filamentosus Crystallodytes cookei Apodocreedia vanderholsti Ammodytes hexapterus Trachinus vipera Uranoscopus scaber Axoclinus carminalis Dactyloscopus spp Malacoctenus hubbsi Starksia hoesii

paternal none none paternal paternal

Heterostichus rostratus Ophiclinus spp Heteroclinus spp Emblemaria hypacanthus Hypsoblennius spp

Coyer 1982 George and Springer 1980 Gunn and Thresher 1991 Hastings 1992 Stephens et al. 1970

Robards et al. 1999 none Boundka et al. 1998 Petersen 1989 Dawson 1982 Petersen 1988 Rosenblatt and Taylor 1971

gonochore ovip vivip vivip ovip ovip

?gonochore gonochore

B E H AV I O R A L E C O L O G Y

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Appendix 19.1. (continued) Taxon (Order, Family or Subfamily)

Mode

Icosteidae Gobiesocidae Callionymidae Eleotridae Gobiidae

ovip ovip ovip ovip ovip

Microdesmidae Ephippidae Siganidae Luvaridae Zanclidae Acanthuridae Sphyraenidae Gempylidae Trichiuridae Scombridae Xiphiidae Xiphiinae Istiophorinae Centrolophidae Nomeidae Tetragonuridae Stromateidae Pleuronectiformes Bothidae Paralichthyidae Pleuronectidae Achiridae Cynoglossidae Tetraodontiformes Balistidae

ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip ovip

ovip ovip ovip ovip ovip

Gender Allocation ? gonochore gonochore ?gonochore protogynous bidirectional simultaneous gonochore gonochore ? gonochore gonochore ? ?gonochore gonochore gonochore gonochore ? gonochore gonochore

? ? ? gonochore gonochore

Parental Care none paternal none paternal paternal paternal paternal biparental ?paternal none none none none none none none none none none

none none none none

Representative Species

Key Reference(s)

Icosteus aenigmaticus Gobiesox maeandricus Diplogrammus pauciradiatus Gobiomorphus breviceps Rhinogobiops nicholsii Lythrypnus spp Lythrypnus spp Clevelandia ios Typhlogobius californiensis Gunnellichthys spp Chaetodipterus zonatus Siganus canaliculatus Luvarus imperialis Zanclus cornutus Acanthurus nigrofuscus Sphyraena argentea Thyrsites atun Lepidopus caudatus Thunnus albacares

Fitch and Lavenberg 1971 Marliave and DeMartini 1977 Harrington 1997 Hamilton and Poulin 1999 Ebert and Turner 1962; Cole 1983 St. Mary 2000 St. Mary 2000 Brothers 1975 MacGinitie 1939 none Martinez-Pechero et al. 1990 El-Sayed and Bary 1994 Nishikawa 1987 none Myrberg et al. 1988 Walford 1932 Griffiths 2002 Demestre et al. 1993 Schaefer 1998

Xiphias gladius Istiophorus spp Hyperoglyphe antarctica Cubiceps gracilis Tetragonurus spp Peprilus simillimus

DeMartini et al. 2000 DeSylva and Breder 1997 Baelde 1996 none none Goldberg 1981b

Bothus constellatus Citharichthys spp Microstomus pacificus Achirus mazatlanus Symphurus atricaudus

Tapia-Garcia et al. 2000 Goldberg and Pham 1987 Hunter et al. 1992 Amezcua-Linares et al. 1992 Goldberg 1981a

ovip gonochore

Monacanthidae

?

Ostraciidae Tetraodontidae Diodontidae

?protogynous ? ?

maternal Balistes polylepis biparental Pseudobalistes flavimarginatus none Oxymonacanthus longirostris biparental Paramonacanthus japonicus ?none Ostracion meleagris none Canthigaster rostrata none Diodon holacanthus

Molidae

?

none

Mola mola

Strand 1978 Gladstone 1994

none

Kokita and Nakazono 2001 Nakazono and Kawase 1993 Moyer 1979; Leis and Moyer 1985 Sikkel 1990 Sakamoto and Suzuki 1978

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CHAPTER 20

Movement and Activity Patterns C H R I STO P H E R G. LOW E AN D R I C HAR D N. B RAY

Introduction Few aspects of fish behavior have been of greater interest to humans than movement and activity patterns. The rapid increase in our knowledge about where fish go and why has transformed us into the most efficient predator in the marine environment. At first, knowledge of movement and activity patterns of marine fishes was essential for human subsistence, but over time this information became vital to development and economic growth of nations. Unfortunately, a little knowledge can be a dangerous thing. Along with the rapid development in fishing technology, this knowledge of movement and activity patterns has resulted in over-harvesting of many marine fish species and has even led to wars between countries (Kurlanski, 1997; Parrish, 1999). On the other hand, this information can be valuable for fisheries management. For example, information on temporal and spatial aspects of spawning aggregations can be used to prevent excessive harvesting of species at a time and location where they may be most vulnerable. Knowledge of fish movements is essential to understand and model stock structure and design marine reserves, yet obtaining this information poses many challenges. Nevertheless, from an academic standpoint, knowledge of fish movement and activity patterns may offer unique insight into the ecological role fish play in marine ecosystems. Understanding the mechanisms behind the drive to move, orient to environmental and social cues, or regulate where fish go and when, is essential for quantifying fish population dynamics, community structure, and distribution. Understanding these mechanisms can also be beneficial in understanding how these behaviors have evolved as well as how these patterns have influenced form and function in marine fishes. What defines a movement pattern in fishes? In order to contemplate the ultimate (evolutionary) mechanisms behind why and when fish move, one must first understand the proximate (causatory) mechanisms that enable fish to exhibit these movement patterns. Most fish movements are directed or intentional, and thus require the fish to orient to some environmental or social cue. Fish use a variety of sensory information to detect and orient to these cues; however, basic orientation does not require the fish to travel anywhere.

524

Nevertheless, in many cases, orientation to some cue provides the means by which a fish can make a directed movement (e.g. patrol its home range, follow prey, guard its territory, and migrate). In addition, there are spatial and temporal components to fish movements that can vary considerably over geographical area and time span, and a wide variety of abiotic and biotic factors can affect these components. While almost all fishes exhibit some degree of ontogenetic shift in space utilization as they mature, as adults the degree of movement or area used may vary depending on the species and location. For example, some fishes such as gobies are highly residential and may not move more than a few meters over the course of their adult lives, whereas highly migratory fishes such as salmon shark (Lamna ditropis) or blue shark (Prionace glauca) may move thousands of kilometers in a single season. The timing of movements or activity patterns may vary considerably among fish species as well as individuals. While most biological cycles in fishes are regulated or maintained by exogenous cues such as light, lunar phase, tide, salinity or temperature, some deepwater fishes live in habitats where these cues are greatly reduced or absent. Do they exhibit rhythmic patterns of activity, and if so, how do they keep time? Other fishes such as lie-and-wait or opportunistic predators may apply a more energetically conservative approach to movement and only become active if prey are present. Obviously, there are plenty of examples of fishes that exhibit activity patterns over daily, monthly, or seasonal time scales. In some cases the timing of movements of fishes is relatively fixed and tightly programmed, such as in seasonal spawning migrations, while other movement patterns such as those related to feeding may be more plastic due to variations in availability of food or presence of predators. Variations in movement and activity patterns can occur over broad temporal and spatial scales among individuals of the same species. Some individuals of the same species show little movement, while other individuals are more transient. This intraspecific variability may explain much of the long-range dispersal events for some species in California waters, particularly during El Niño periods. Some individuals may exhibit high site fidelity and specificity for part of their life, but then exhibit a radical change in home range due to competition,

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decline in habitat quality, or increase predation pressure. Much of the variation in these types of behaviors for species presumably has been shaped through selection as the result of tradeoffs between feeding, reproduction, and predation risk (Covich, 1976; Pyke, 1983). To begin to understand the evolution of these behaviors and the mechanisms that affect the movement and activity patterns of marine fishes, one might start by asking the question—why do fish move at all? From an energetic standpoint, movement is costly and therefore should not be exhibited unless there is some intrinsic value to the fish. Considering the rich diversity of marine fishes in California waters and the variety of ecosystems and communities they inhabit, it becomes obvious that there is a great and varied need for fish to move. In this chapter we will address methods for quantifying movement and activity patterns of California marine fishes and discuss some of the proximate and ultimate mechanisms that may have led to the evolution of these behaviors.

How Can You Quantify Where Fish Go and When? Our knowledge of the movement and activity patterns of marine fishes has grown rapidly over the last few decades due to advances in technology. The development of new tools and techniques has expanded our understanding of where fish go and when. However, there is still a lot we do not know and new technology is evolving to help answer questions about hard to study species. In order to understand what we really know about fish behavior, it is important to carefully examine the methods that are used to determine movement and activity. Certain methods may be useful in addressing questions about dispersal, but may be inappropriate or inadequate for answering questions about fish home range. In addition, there are often trade-offs between the number of fish that can be sampled and the quality of data obtained.

Fishing Most of what we know about fish movement and activity patterns comes from fishing (or catch) data. Finfish have been systematically harvested from coastal waters for thousands of years. During this time, fishers have made careful observations of where and when they catch the most fish. The accumulation of these data over time has provided a vast knowledge base on when fish can be found in certain habitats and locations, as well as their activity periods. However, catch data are most useful in estimating spatial and temporal distributions of fishes and their dispersal over large geographical areas and time. For example, catch data from commercial fisheries in California have been used to determine geographic distributions of many fish species (Miller and Lea, 1972). However, like many methods, catch data can also be ambiguous and misleading due to inherent biases in the method. The main limitations of this method are attributed to issues related to catchability, size selection, and data collection accuracy. For example, just because a fisher does not catch any fish at a particular location does not necessarily mean that there are no fish there. It is possible that fish are present, but may not be caught using that particular method. Thus, without being able to physically detect the fish at that time, one might conclude that there are no fish there at all. It is also possible that the method of fishing being used is size selective and may not allow for catch of a

certain size. This may be common with hook and line or gillnet fishing methods, which tend to select for larger fish and may lead to the conclusion that juveniles are not present in that habitat. Because most catch data are fishery-dependent (generated by commercial and sport fisheries), landings and catch locations are provided by fishers who may not be forthcoming in revealing their favorite fishing spot. As a result, positional information on fish catch may be lacking in accuracy, therefore further reducing the resolution of the method for determining movement patterns. In addition, commercial and sport fishers are very good at optimizing take, which results in biased sampling. However, fishery derived catch data have been calibrated by using scientific fishing methods. Scientific fishing generally employs the same types of fishing techniques and gear as used by commercial and sport fishers, but uses controls and random sampling techniques to more fairly assess fish distribution and abundance. When coupled with tagging or marking of fish, catch data can yield important information on growth, size distribution, mortality, dispersal rates and distances. Marking fish to quantify their movement patterns started as early as the 1600s and tagging methods have varied widely over the years (McFarlane et al., 1990). Large-scale tag and release programs in California for highly mobile pelagic species such as tunas, billfishes, and sharks have yielded important information about dispersal and migration, particularly in relation to their movement across Economic Exclusion Zones (EEZ) (Laurs and Lynn, 1977). Most tagging studies require tagging large numbers of fish to ensure a sufficient return rate. In some cases there are intense fisheries that increase the rates of recapture of target species and facilitate the collection of data. The International Pacific Halibut Commission (IPHC) has been tagging Pacific halibut (Hippoglossus stenolepis) in the Bering Sea since 1925, tagging over 350,000 and recapturing 35,000 fish as of 1990. This 60 year tagging program has demonstrated that juvenile Pacific halibut disperse farther than adults and that mature fish annually migrate thousands of kilometers from spawning to feeding grounds (Trumble et al., 1990). In addition, tagging studies of kelp bass (Paralabrax clathratus) in southern California have shown increased dispersal distances for juveniles and greater site fidelity of adults (fig. 20-1) (Collyer and Young, 1953; Young, 1963). As a general rule, most fish tagging programs exhibit recapture rates of 3–10%, which suggests that a lot of fish must be tagged in order to obtain enough data to quantify movements. Caution must be used when interpreting tag and recapture data. First, tag and recapture data only indicate where the fish was tagged and the location it was recaptured. In many tag and recapture studies, a large percentage of the recaptured fishes are found close to the location where they were originally tagged. One might assume from these findings that the fish do not travel far, and thus may have a small home range. It is also possible the fish had traveled thousands of kilometers, but returned to the site of initial capture. This brings about another important point about the ambiguity of catch data. Some fish may be more susceptible to capture during certain seasons, and thus may be more likely to be caught in one location even though they used other areas where they are not caught. This also influences the effectiveness of tag and recapture as a tool to examine dispersal or migration due to effects of catchability. Second, there are other experimental artifacts of tag and recapture studies such as tag retention, physiological and behavioral impacts from catch and handling, effects of the

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F I G U R E 20-1 Dispersal distances of four size classes of kelp bass, Paralabrax clathratus, tagged with standard identification tags at Santa Catalina Island. After Young (1963, p. 361).

tags themselves, and underreporting of recaptured fish—all of which can influence estimates of movement patterns. Therefore, tag and recapture studies should be preceded with preliminary tag retention and growth effect studies to determine how often tags might be shed by fish and to quantify the effects of tagging on the fish’s health. Lack of participation by fishers can also hamper data collection. Many fishers may be reluctant to turn in tags for fear that additional information may result in more restrictions on the fishery. Catch data, and tag and release studies have been the largest sources of information about movement and activity patterns of fishes, despite their lack of spatial and temporal resolution and the impact it has had on many populations.

In Situ Monitoring Aside from catch data, few other methods have provided more detailed information on behavioral patterns of fishes than in situ observations made via snorkeling, scuba, remotely operated vehicles (ROVs), or manned submersibles. Early direct observations of fish behavior were made from the surface along coastal habitats such as tide pools, lagoons, and shallow coral reefs. The development of scuba in the 1950s provided fish biologists with a powerful tool for directly observing fishes underwater. Scuba allowed researchers to observe the types of habitats fish use, how they interact with other fishes, and how and when they feed and mate. For example, most of what we know about California reef fish behavior comes from scuba studies. Although scuba has provided more resolution and fine-scale information on fish movement and activity patterns, this method is limited to shallow waters (
30 m) and short observation durations (1–2 hour dives). Another logistical problem with scuba diving involves poor water conditions (cold, turbid water, surge), especially north of Point Conception (e.g., studies of the blue rockfish, Sebastes mystinus by Hobson and Chess, 1988). Study sites are understandably selected for their optimal diving conditions and we know far less about fish activities in less hospitable areas. These logistical problems were humbly summarized by Ebeling and Hixon (1991). In addition, there is some evidence that fish behavior is influenced by diver presence (Stanley and Wilson, 1995; Kulbicki, 1998) and nighttime observations may be problematic due to the use of lights and more restricted vision. Research divers have always strived to increase the amount of time they could spend underwater observing fishes; however, the dive time is

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greatly limited by air supply and nitrogen gas accumulation in the blood and tissues of the diver. A valuable diving system that was available in the mid 1980s at the Wrigley Marine Science Center at Santa Catalina Island involved surface-supplied tether gear, which provided divers an unlimited supply of air, voice communication, warm-water circulation, and a decompression bell. This system enabled prolonged bottom time for various projects involving reef fish (e.g., Bray et al., 1988). To provide divers even more observation time, several underwater research laboratories (SeaLab, Habitat, Hydrolab) have been established over the years that allow divers to live underwater and make longer dives at deeper depths without the burden of daily decompression. By placing these underwater laboratories on coral or rocky reefs, researchers have been able to monitor fish behavior over longer periods of time (Johnson and Ruben, 1988). Nevertheless, some fishes are more wary of divers, who tend to be noisy due to exhalation of bubbles and equipment. Recent developments in rebreather diving technology have increased the amount of time a diver can spend underwater observing fishes by more carefully regulating the mixture of gases the diver breathes at different depths, allowing divers to venture significantly deeper (
150 m). Most importantly, this technology seems to be less disturbing to many fishes and allows divers to get closer to hard-to-study species because there are no exhalation bubbles (Pyle, 1996; Lobel, 2001; Pyle, 2001). Direct observations of deepwater fishes have come from ROVs and manned submersibles (e.g., PISCES subs), which can go to much greater depths and allow researchers to observe fishes for longer periods of time than standard scuba will allow. These studies have provided some of the first detailed observations of fishes rarely seen alive. Video collected during dives can be archived and reviewed by others at later dates and provide a hard record of observations, not always afforded by diver observations. The use of parallel laser sights attached to cameras can be used to quantify lengths of fishes being observed. Much like diver observations, ROVs and submersibles also are likely to influence fish behavior particularly because bright lights are often needed to see fish in the deep sea. It is possible that the light might attract or repel fish, thereby reducing the effectiveness of this technique for assessing whether fish are normally present in the habitat or not. Because of the relatively short durations of dives and the high cost of this type of deepwater research, determining movement and activity patterns of deepwater fishes using direct in situ observations is logistically more difficult than for shallow water species.

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Coupling of direct observations with tagging studies can greatly facilitate data collection on movement patterns. For example, Matthews and Reavis (1990) tagged rockfish underwater and used diver surveys to subsequently look for tagged fish. Tagging fish underwater reduces barotrauma and handling stress that may result in high mortality rates and lower recapture rates (Parrish and Moffitt, 1992; Adkison et al., 1995; Starr et al., 2000). In addition, surveying for tagged fish via scuba allows for multiple visual recaptures and more accurate descriptions of the recapture location can be made. Using this technique, Matthews and Reavis (1990) found significantly higher recapture rates (48%) compared with other conventional tagging studies on rockfish (
2–3%) and that the rockfish species they observed showed relatively high site fidelity and the ability to home after being displaced up to 6 km away. The main limitations of this technique are that it can only be done over small geographical areas and the method may not be feasible for highly mobile species that have large home ranges. Even by combining methods of tag and recapture and direct observations, there are still problems with resolution of position and influences on behavior from the presence of a diver, ROV or submersible. Another technique used for direct observation that is growing in popularity is the use of remote cameras that can be fixed and camouflaged on the substratum. These cameras can use time-lapse photography to sample fishes in the vicinity or video cameras can be used to record movements and activity. These cameras have an advantage in that fish habituate to their presence, whereas they may not to a diver or ROV. These cameras are generally limited to daylight hours when ambient light is available, but CCD chip cameras sensitive to infrared and visible light, coupled with infrared illumination at night, may represent a significant breakthrough in the study of fishes at night, at least at close range (Holbrook and Schmitt, 1999).

Remote Sensing Techniques Because methods such as fishing and resulting catch data are limited in spatial resolution and in situ observations are limited in duration and by influences of the technique on the fish’s behavior, there has been a need for less intrusive, more accurate means of quantifying fish movements. The development of remote sensing techniques to monitor fish movements underwater has been promoted largely due to the shortcomings of these other methods. A variety of remote sensing technologies have evolved over the last 50 years, including sonar, LIDAR, radio and acoustic telemetry. SONAR

The earliest form of remote sensing technology came in the development of sonar as a way to monitor the location and movement of fishes (MacPhee, 1988). Sonar uses a pulsed acoustic signal ranging from 12–500 kHz produced from a hydrophone attached to a boat to detect objects of differing densities in the water column or on the seafloor. Because fish possess tissues that vary in density compared with seawater, some of the pulsed sound signals that hit the fish get reflected back to the boat. The electronics of the sonar can determine how far away the fish is from the boat and where the fish is relative to the seafloor (fig. 20-2a). Sonar systems have become so sophisticated that researchers (and fishers) can now identify fish to species and approximate size based on the acoustic signal that is reflected back to the boat. High-resolution sonar (e.g., side-scan, scanning, and multi-beam sonar) has been used

to track schools of fishes and even determine swimming speeds of large individuals (Harden-Jones, 1973). In addition, these types of sonar can be used to count fish as well as monitor their movements through the water column. Sonar has been used to monitor the vertical movements of fish relative to prey, thermocline, or deep scattering layer (Robinson et al., 1995; Stanley and Wilson, 1995). This method is most useful in monitoring an entire school of fish, but is not very effective for monitoring movements of individuals. LI DA R

Another technique similar in principle to sonar is the use of LIDAR (LIght Detection And Ranging) systems. These systems employ the use of a plane or helicopter-borne laser to shine a beam of light into the water and then measure the spectral characteristic and intensity of the light that is reflected back. LIDAR can be used to identify and follow fish that are found near the surface or in shallow water (
40 m) based on the light reflective properties of their skin (Gauldie et al., 1996) (fig. 20-2b). Much like sonar, this method is best for following schools of fishes and not individuals. In addition, it is expensive and is limited to fish found in shallow, clear water. TE LE M ETRY

Telemetry is another method that can be used to quantify the movement and activity patterns of fishes. Unlike sonar and LIDAR, which detect the reflection of a sound or light signal off a fish, telemetry relies on detection of a radio or acoustic signal emitted from a transmitter attached to the fish. This technique enables monitoring of movements of an individual fish and provides better spatial resolution for geo-positioning, and therefore allows for determination of home range size, habitat utilization, and environmental preferences. Radio telemetry uses pulsed high frequency radio signals (MHz) as the carrier signal. Although radio waves readily pass through air and freshwater, they are rapidly attenuated in seawater. As a result, radio telemetry is not typically used for marine fishes. Acoustic or ultrasonic telemetry uses pulsed, lower frequency sound (12–250 kHz) as a carrier signal. Because lower frequency sounds attenuate less in seawater, acoustic telemetry offers the best application for marine fishes. Transmitters are usually attached to the outside of the fish but can also be surgically implanted into the musculature or body cavity (Holland et al., 1993; Holland et al., 1996; Meyer et al., 2000). Fine-scale geographical movement can be determined by following the acoustic signal generated by the transmitter attached to the fish (fig. 20-2c). Due to the large, bulky size of early electronics, the first applications of acoustic telemetry were used for studying the movement patterns of large fishes such as sharks (Nelson, 1990). Much of what we know about diel movement patterns of blue sharks, shortfin mako sharks (Isurus oxyrinchus), Pacific angel sharks (Squatina californica), and leopard sharks (Triakis semifasciata) comes from acoustic telemetry studies (Sciarrota and Nelson, 1977; Standora and Nelson, 1977; Holts and Bedford, 1993; Ackerman et al., 2000). As the technology improved and electronics became miniaturized, studies on smaller species have ensued. Acoustic telemetry tracking has been used to quantify the diel movement patterns and home ranges of smaller nearshore fishes such as kelp bass and California sheephead (Semicossyphus pulcher)(Lowe et al., 2003; Topping, 2003), and monkeyface pricklebacks (Cebidichthys violaceus) (Ralston and Horn, 1986).

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F I G U R E 20-2 Depiction of remote sensing methods used to determine the movement patterns of fishes. Fig. 2a and 2b represent passive remote sensing methods, whereas fig. 2c–e represents active remote sensing methods based on whether the detection signal is generated from a device on or in the fish itself. (a) sonar, (b) LIDAR, (c) acoustic telemetry tracking, (d) acoustic telemetry monitoring, and (e) satellite telemetry. (Illustration by K. Anthony).

In addition, various sensors can be added to the acoustic transmitters that can relay information such as the fishes’ depth in the water column, body temperature, heart rate, water temperature, tail beat frequency, and swimming speed (Lowe et al., 1998; Lowe and Goldman, 2001). By coupling these sensors with the ability to geographically position the fish, it is possible to examine movement patterns in three dimensions relative to environmental factors. For example, by using acoustic transmitters that sense depth and water temperature, researchers have found that blue and mako sharks spend most of their time swimming in the mixed layer of the water column, but occasionally dive through the thermocline (Sciarrota and Nelson, 1977; Holts and Bedford, 1993; Nelson et al., 1997) (fig. 20-3a). These movement patterns are very different than those observed for a megamouth shark (Megachasma pelagios) that was tracked by Nelson et al. (1997) off the coast of southern California. This shark remained relatively deep in the water column (
150 m) during the day, but moved to within 15 m of the surface at night (fig. 20-3b). Goldman (1997) fed acoustic transmitters with temperature sensors to adult white sharks (Carcharodon carcharias) at the Farallon Islands to monitor diurnal movement patterns and body core temperature. White sharks were found to maintain an average elevated body temperature of 29°C regardless of the ambient water temperature, providing direct evidence of endothermy in this species.

528

B E H AV I O R A L E C O L O G Y

Although acoustic telemetry tracking has significantly increased our ability to quantify the movement patterns of fishes relative to their environments, this technique is very labor intensive and is restricted to short durations (few hours to a few days). The development of hydrophone arrays and acoustic transmitters with longer battery life has increased the duration of fish movement monitoring. Acoustic listening stations have been used to study site fidelity in fishes (fig. 20-2d). These stations constantly listen for fish that are carrying individually coded acoustic transmitters. As the fish swims by the listening station, it records the fish’s identification code, the time and date that it was detected, and duration of the stay. By placing an array of these monitors around an area, it is possible to monitor larger-scale movement patterns and site fidelity. Coded transmitters allow for a large number of fish to be tagged and tags can last up to several years. Movement patterns and site fidelity of deepwater bocaccio (Sebastes paucispinis) and greenspotted rockfish (Sebastes chlorostictus) in Monterey Bay, California were determined over a 1–2 year period using an array of acoustic listening stations placed along the canyon (Starr et al., 2000). Another derivation of this technology allows for more precise positioning of a fish within a given area, again using an array of hydrophones. By placing a triangle or polygon array of hydrophones on the seafloor and measuring the time it

GRBQ065-2067G-C20[524-553].qxd 11/8/05 23:06 Page 529

F I G U R E 20-3 Vertical movement patterns of shortfin mako, Isurus oxyrinchus, and a megamouth, Megachasma pelagios, shark. (a) vertical

movement patterns of shortfin mako sharks acoustically tracked in the southern California Bight. After Holts and Bedford (1993, p. 140). (b) vertical movement patterns of a megamouth shark acoustically tracked in the southern California Bight. After Nelson et al. (1997, p. 100).

GRBQ065-2067G-C20[524-553].qxd 11/8/05 23:06 Page 530

takes for the acoustic signal produced by a transmitter within the array to reach each hydrophone, it is possible to determine the precise position of the fish (1 m) within the array. This automated geographical positioning system is particularly useful in examining fine-scale movement patterns over relatively small geographical areas. For example, Ralston and Horn (1986) used a geo-positioning hydrophone array to examine tidal related movements of the monkeyface prickleback. Using this array, they found that these fish venture up into the intertidal zone as the tide rises, but then return back to their home rock after foraging. This system has also been used to monitor foraging and social behavior of white sharks around an elephant seal rookery (Klimley et al., 2001). A similar design has been used to look at movement patterns of abyssal rattails (Coryphaenoides spp.) attracted to a baiting station at 6000 m depth (Priede et al., 1991). While these systems have significantly reduced the labor involved in manual tracking, they are expensive and restricted to small geographical areas. If the fish moves outside the detection range of one of more of the hydrophones, it is not possible to derive a position. Acoustic telemetry has greatly improved our ability to more accurately quantify movement patterns of fishes; however, it is still restricted for use in fine-scale, short-term movement patterns. This technology is not adequately suited for determining long-range migrations. Researchers have begun to develop and apply the use of satellite telemetry to quantify long-range movement patterns of highly migratory fishes. Satellite telemetry uses transmitters that emit radio signals to satellites, and because radio signals are quickly attenuated in seawater, satellite transmitters only work when they are at the surface. Although satellite telemetry has been primarily used on marine mammals and reptiles, it has been adapted for use on fishes by incorporating sensors that record light levels, depth, and water temperature. The transmitters have a data logger that records and summarizes the data, so that when the transmitter is at the surface the data can be downloaded to the satellite. However, the trick is getting the transmitter to the surface. Because very few species of fishes spend enough time near the surface to warrant the use of this expensive technology, researchers have developed timed-release mechanisms that allow the transmitter to be detached from the fish on a programmed time and date. The transmitter pops-up to the surface and downloads its information to a satellite (fig. 20-2e). Although these tags have provided long-term detailed data on the depth of the fishes and the water temperature they moved through, deriving accurate geographical positions has been problematic. In some cases, periodic positions are made when the satellites triangulate the position of the tag while the fish is at the surface (fig. 20-2e); however, those instances may be infrequent. Light levels recorded by the tag along with remote sensing oceanographic data can be used to position the fish. For example, it is possible to determine the latitude and longitude of the fish by accurately determining the times of sunrise and sunset. While these two measures can be used to determine longitude, by knowing the length of the daylight period (day length) at the tag location, it is possible to determine latitude. Unfortunately, using light levels to determine these parameters can be confounded as the fish swims deeper and light is attenuated or if water clarity changes. Nevertheless, this method can be effective in demonstrating large-scale movements (over hundreds or thousands of kilometers). Pop-up satellite transmitters (PSAT tags) have been used to characterize the migratory movement patterns of pelagic tunas, billfishes, and sharks (Block et al., 1998; Block et al., 2001; Boustany et al., 2002). This technology

530

B E H AV I O R A L E C O L O G Y

has greatly enhanced our ability to quantify migratory movement patterns of open ocean fishes. It is far less labor intensive compared to acoustic telemetry tracking and can collect data over longer durations; however, it is limited in application due to the size and expense of the transmitters and positional accuracy.

Genetic Techniques Another way to examine long-range dispersal and movement patterns over longer time periods is through the use of genetic markers. Genetic variability among different populations of fish can be used as a means of determining whether two populations located in different areas emigrate. If the two populations are genetically dissimilar then it is likely there is little movement between the two areas. This does not necessarily mean that fish do not move between these two areas at all; however, it does suggest that movement between the two areas is very minimal and/or the fish that move between the two areas do not interbreed. This particular method is very beneficial in examining long-term stability of dispersal pattern. A wide variety of methods and technologies have evolved to quantify movement patterns of fishes and new methods are constantly being introduced. Due to the limitations of many of these methods, more than one technique may be needed to answer a question about movement or activity patterns of a fish.

Spatial Patterns—Where Fish Go One approach that can be used to understand the evolution of space use patterns of fishes is through the use of cost-benefit models. Because of the inherent costs of locomotion (e.g., in expended energy, increased threat of predation), one might expect the cheapest and easiest thing for a fish to do is to remain in one place and move very little. However, even though the fish may be sedentary and its metabolic costs minimal, there may not be enough food or mates nearby or possibly there may be too many predators to justify this strategy. In this case, the costs will likely outweigh the benefits (Covich, 1976; Pyke, 1983), and as a result, fish will move. A wide variety of space use patterns can be seen within and among species of Pacific coast fishes that range from little or no movement to long-range migration. While some fishes may exhibit little pattern in defined space use, others show clear space use patterns over a range of scales. In addition, all fishes exhibit some ontogenetic shift in space use patterns, resulting in a change in habitat or the amount of space used. These ontogenetic shifts are likely attributed to changes in cost-benefit ratios as the fish matures.

Home Ranging The area a fish uses on a regular basis is typically defined as a home range (Mace et al., 1983). The size of a home range may vary with the size of the fish, water temperature, inter- and intra-specific competition, habitat composition and quality, food, shelter, and mate availability. It has been hypothesized that the home range size of an organism increases with its energetic demand (Mace et al., 1983), yet there are situations where using less area may be more beneficial.

GRBQ065-2067G-C20[524-553].qxd 11/8/05 23:06 Page 531

F I G U R E 20-4 Cost optimization model of ontogenetic changes in home range sizes of territorial and non-territorial fishes. Dotted line represents predicted increase change in home range size with increase fish size of non-territorial fishes. Solid line represents predicted decrease change in home range size with increase fish size of territorial fishes.

In general, two cost-optimization models may explain ontogenetic changes in home range size observed in fishes, but they differ depending on whether or not the species is territorial. Non-territorial species might have small home ranges when they are young, but they might expand their home ranges as they get larger to accommodate greater energetic demands (fig. 20-4). This trend is likely reversed for territorial species, where juveniles often have large home ranges because they are too small to effectively defend their own territory and continuously get displaced by other territorial individuals. Eventually, they may get large enough to occupy and defend a small territory; and in many cases, these territories expand as the fish gets larger (fig. 20-4). These home range strategies have likely evolved to enable fishes to optimize energy intake based on the particular habitat type with which they may be associated.

High Relief Rock Substratum From an ecological standpoint, complex habitats such as rocky reefs usually support a higher species diversity of fishes, due to the increased availability of substratum, shelter, and prey (Allen, 1985). Therefore, one might expect a large proportion of fishes that occupy these habitats to have small home ranges because of the greater availability of food and shelter (Barrett, 1995). In some cases, increased competition for limited resources in these small areas results in territorial behavior (Sale, 1971; Reese, 1973). While a territory is only that portion of the fish’s home range that it will actively defend or exclude from other individuals, its territory size relative to the home range size may vary with competitor density, resource availability, or resource quality. Many small, benthic, reef-associated fishes tend to exhibit small home ranges due to the availability of high quality essential habitat and resources (Sale, 1971). The blackeye goby (Rhinogobiops nicholsii) is commonly found at the interface between rock and sand substrata. These gobies have small home ranges and establish territories around primary shelters in the rock or holes in the sand. In a manipulative field study, Kroon et al. (2000) found that blackeye gobies had home ranges that varied in size from 0.01–1.18 m2 and that larger

fish usually held larger territories within their home range than do smaller individuals (table 20-1). Home range sizes decreased by 35% during breeding season. They found that if they removed a territory holder or added new habitat in the form of an artificial reef, the space was quickly recolonized by other blackeye gobies. Based on these findings, they concluded that suitable shelter habitat was limited. The importance of shelter habitat for blackeye gobies was further supported by a study done by Steele (1996) who found that predators such as kelp bass and barred sand bass impact blackeye goby survivorship by up to 75%. Thus, for the blackeye goby, home range size appears to be more constrained by the risk of predation rather than requirements for foraging. Therefore, it must be more beneficial to defend a good shelter than to move from area to area trying to find shelter along the way. In addition, the contraction of home range size during breeding season indicates a shift in the cost-benefit ratio towards more closely guarding nests versus increased foraging space, which suggests that food is not as limited as quality nest location. While complex habitats offer more resources and thus increased species diversity, this higher diversity may also be accompanied by increased competition (summarized by Ebeling and Hixon, 1991). Therefore, competition between species may drive evolutionary changes in space use patterns. For example, two sympatric, closely related species of blennies, rockpool blenny (Hypsoblennius gilberti) and mussel blenny (Hypsoblennius jenkinsi), exhibit different space use patterns. Rockpool blennies typically inhabit the rocky intertidal and subtidal cobble, while mussel blennies are found subtidally and occupy Serpulorbis clam tubes and mussel beds. Stephens et al. (1970) found that rockpool blennies have a larger home range, moving up into intertidal areas (up to 15m) with the rising tide, whereas mussel blennies are territorial and rarely moved more than 1 m from their hole. Because rockpool blennies are the larger of the two blennies, it may have fewer shelters available to it in the subtidal area than mussel blennies, and/or may be less susceptible to predation by exploiting food resources found in the intertidal areas. It is possible that these behavioral differences in space use evolved as a way of reducing competition between these two species or may simply be adaptations to prey availability or predation pressure. Some rock-associated territorial fishes have small home ranges, but defend area based on food availability rather than shelter quality. The black and yellow rockfish (Sebastes chrysomelas) and gopher rockfish (Sebastes carnatus) are two closely related species found in shallow water rocky reef habitats (Love et al., 2002). In a field study at Santa Cruz Island off southern California, Larson (1980) found that individuals of both species had restricted home ranges (3–15 m2) (table 201). The smallest rockfish had the largest home ranges and were not territorial. The largest fish, however, held territories and had larger home ranges than smaller territorial individuals. Consequently, territorial fish found in areas of lower prey density tended to have larger home ranges. Larson (1980) concluded that these two species of rockfishes were likely competing for shelters in the areas where food was most abundant. Because these rockfishes are larger than the blackeye goby, they are less susceptible to predation, but have higher energetic requirements. In this case, home range size may have been more determined by food availability than the quality of the shelter. Interestingly, while most demersal, rock-associated rockfishes probably have relatively small home ranges, not all are

F I S H M O V E M E N T A N D A C T I V I T Y PA T T E R N S

531

Hydrolagus colliei Gibbonsia elegans Heterostichus rostratus Chitonotus pugetensis Clinocottus analis Icelinus quadriseriatus Leiocottus hirundo Leptocottus armatus

Rocky Mixed Mixed Zostera beds

Batrachoididae Batrachoididae Blennidae

Spotted ratfish Spotted kelpfish Giant kelpfish Roughback sculpin Woolly sculpin Yellowchin sculpin Lavender sculpin Pacific staghorn sculpin

Rockpool blenny Mussel blenny Blue shark

Soft bottom Rocky, intertidal Soft bottom

Cottidae Cottidae

Cottidae

Cottidae

Sand-rock ecotone Soft bottom

Rocky, kelp

Clinidae

Cottidae

Rocky

Clinidae

Open ocean (pelagic)

Carcharhinidae

Mixed

Rocky

Blennidae

Chimaeridae

Rocky, intertidal

Blennidae

Mixed

Bathymasteridae

Grunion

Stripefin ronquil Specklefin midshipman Plainfin midshipman Bay blenny

Soft bottom Soft bottom

Albulidae Anoplopomatidae Mixed

Soft bottom

Agonidae

Habitat

Atherinopsidae (Atherinidae) Atherinopsidae

Blacktip poacher Bonefish Sablefish

Xeneretmus latifrons Albula vulpes Anoplopoma fimbria Atherinops affinis Leuresthes tenuis Rathbunella hypoplecta Porichthys myriaster Porichthys notatus Hypsoblennius gentilus Hypsoblennius gilberti Hypsoblennius jenkinsi Prionace glauca

Family

Topsmelt

Common Name

Species

TA B L E 20-1

Nomadic

15 m radius (DO) 15 m radius (DO) 1 m (DO)

Home Range

Tidal (U)

Ontogenetic, diel (AT), seasonal (TO, TR)

Seasonal (OT)

Seasonal (OT)

Tidal (SO,N)

Migrations

Movement Patterns

No diel (OT, GA,M,) No diel (DO,GA) Nocturnal and tidal (GA)

Nocturnal (OT, GA,M) Diurnal (DO,GA) Diurnal (DO,GA) No diel (OT, GA,M,) Tidal (U)

Diurnal (DO)

Diurnal (DO)

Nocturnal (GA,OT, M) Nocturnal (GA,M, OT) Diurnal (DO)

Diurnal (U)

Nocturnal (GA,M) Diurnal (U) No diel (GA,M) Diurnal (DO,GA) Diurnal (U)

Other Activity

Source

(Tatso 1975, Love 1996, Bond et al. 1999)

(Hobson et al. 1981)

(Allen 1982)

(Love 1996)

(Allen 1982)

(Hobson et al. 1981, Bond et al. 1999)

(Hobson et al. 1981, Bond et al. 1999)

(Allen 1982)

(Sciarrota and Nelson 1977, Tricas 1979)

(Stephens et al. 1970, Bond et al. 1999)

(Stephens et al. 1970, Bond et al. 1999)

(Stephens et al. 1970, Bond et al. 1999)

(Allen 1982)

(Fitch and Lavenberg 1975, Allen 1982)

(Bond et al. 1999)

(Bond et al. 1999)

(Hobson et al. 1981, Bond et al. 1999)

(Bond et al. 1999) (Allen 1982, Bond et al. 1999)

(Allen 1982, Bond et al. 1999)

Movement and Activity Patterns of California Marine Fishes—Species Are Arranged Alphabetically by Family

GRBQ065-2067G-C20[524-553].qxd 11/8/05 23:06 Page 532

Embiotocidae Embiotocidae

Dwarf perch

White seaperch Pile perch

Longjaw mudsucker

Rubberlip seaperch Pink seaperch California killifish Yellowfin goby Arrow goby

Inshore, water column, kelp Inshore, water column Inshore, water column Rocky subtidal

Embiotocidae

Bays

Bays

Gobiidae Gobiidae

Bays

Water column
10 m Bays

Embiotocidae Fundulidae (Cyprinodontidae) Gobiidae

Rocky subtidal

Embiotocidae

Embiotocidae

Rocky subtidal

Embiotocidae

Embiotocidae

Bays, rocky subtidal Inshore, water column

Rainbow seaperch Kelp perch

Hypsurus caryi Brachyistius frenatus Micrometrus minimus Phanerodon furcatus Rhacochilus (Damalichthys) vacca Rhacochilus toxotes Zalembius rosaceus Fundulus parvipinnis Acanthogobius flavimanus Clevelandia ios Gillichthys mirabilis

Embiotocidae

Black perch

Embiotocidae

Embiotocidae

Shiner perch

Striped seaperch Walleye surfperch

Inshore, water column, kelp Mixed

Embiotocidae

Rocky subtidal

Soft bottom

Rocky, intertidal Rocky, intertidal Rocky intertidal and subtidal Rocky

Cynoglossidae

Cottidae

Cottidae

Cottidae

Cottidae

California tonguefish Kelp perch

Tidepool sculpin Snubnose sculpin Roughcheek sculpin Cabezon

Embiotoca lateralis Hyperprosopon argenteum

Oligocottus maculosus Orthonopias triacis Ruscarius creaseri Scorpaenichthys marmoratus Symphurus atricauda Brachyistius frenatus Cymatogaster aggregata Embiotoca jacksoni

Tidal (O,N)

Seasonal (DO) Seasonal (DO)

Seasonal (DO)

Seasonal (DO) Seasonal (DO)

Ontogenetic (U)

Tidal (SO,N,T)

Nocturnal(U)

Diurnal(U)

Nocturnal (DO,GA) Diurnal (GA,M) Diurnal, tidal(O,N) Diurnal(U)

Diurnal (DO, GA) Diurnal (
60 mm SL), Nocturnal 60 mm SL (DO, GA) Diurnal (DO, GA) Diurnal (GA, DO, AO) Diurnal (DO,GA) Diurnal (DO,GA,AO) Diurnal (DO,GA)

Nocturnal (GA,M) Diurnal (GA, DO, AO) Diurnal (DO,GA) Diurnal (DO,GA)

Nocturnal (U)

Tidal (SO,N,T) Nocturnal (U)

(Bond et al. 1999)

(Bond et al. 1999)

(Bond et al. 1999)

(Fritz 1975)

(Allen 1982, Bond et al. 1999)

(Ebeling and Bray 1976)

(Bray and Ebeling 1975, Terry and Stephens 1976, Ellison et al. 1979, Bond et al. 1999) (Ebeling and Bray 1976, Terry and Stephens 1976, Ellison et al. 1979)

(Ebeling and Bray 1976, Terry and Stephens 1976, Ellison et al. 1979, Bond et al. 1999) (Bray and Ebeling 1975) (Hobson and Chess 1976, Hobson et al. 1981) (Ellison et al. 1979)

(Ebeling and Bray 1976, Hobson and Chess 1976, Bond et al. 1999)

(Bray and Ebeling 1975) (Hobson and Chess 1976, Hobson et al. 1981) (Hobson et al. 1981, Stephens and Zerba 1981, Shrode et al. 1983) (Ebeling and Bray 1976, Terry and Stephens 1976, Ellison et al. 1979, Hixon 1980, 1981, Bond et al. 1999) (Ebeling and Bray 1976, Hixon 1980)

(Allen 1982, Bond et al. 1999)

(O’Connell 1953)

(Bond et al. 1999)

(Bond et al. 1999)

(Green 1971)

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Cheekspot goby Bay goby

Ilypnus gilberti Lepidogobius lepidus Lythrypnus dalli Lythrypnus zebra Quietula y-cauda Rhinogobiops (Coryphopterus) nicholsii Anisotremus davidsonii Xenistius californiensis Heterodontus francisci

Lamnidae Mugilidae

White shark

Striped mullet

Carcharodon carcharias Mugil cephalus

Labridae

California Sheephead Labrisomidae (Clinidae) Labrisomidae

Labridae

Señorita

Island kelpfish Reef finspot

Labridae

Rock wrasse

Alloclinus holderi Paraclinus integripinnis

Kyphosidae

Halfmoon

Medialuna californiensis Halichoeres semicinctus Oxyjulis californica Semicossyphus pulcher

Kyphosidae

Opaleye

Heterodontidae

Haemulidae (Pristopomatidae) Haemulidae

Gobiidae

Gobiidae

Gobiidae

Habitat

Intertidal and shallow subtidal rock Coastal (epipelagic) Bays, nearshore surface

Rocky intertidal and subtidal Water column, kelp Shallow rock and kelp (pelagic) Shallow rock and kelp (pelagic) Shallow rock and kelp (epibenthic) Shallow rock

Subtidal rock and sand Subtidal rock and sand Rock, sand, and kelp (benthic)

Subtidal and/cobble

Rocky subtidal Rocky subtidal Bays

Bays

Gobiidae Gobiidae

Bays

Gobiidae

Family

Girella nigricans

Californian salema Horn shark

Xantic sargo

Shadow goby Blackeye goby

Bluebanded goby Zebra goby

Common Name

Species

(continued)

1.8–9.1 km2 (AT)

1000–23000 m2 (AT)

2148–17024 m2 (AT)

0.01–1.18 m2 (TO)

Home Range

4500 km (ST); ontogenetic, seasonal (TO)

Ontogenetic, diel (DO, AT)


500 m (TO)

17 km; ontogenetic, diel, seasonal (TO,TR, DO)

Migrations

Movement Patterns

TA B L E 20-1

Diurnal(U)

Diurnal (DO,GA) Diurnal(U)

Diurnal (DO,GA) Diurnal (GA) Diurnal (DO,GA) Diurnal (DO,GA) Diurnal (DO,GA)

Nocturnal (DO,GA) Nocturnal (AT,DO,AO)

Nocturnal(U)

Diurnal (DO,GA)

Diurnal (DO,GA) Diurnal (DO,GA) Diurnal(U)

Diurnal(U)

Diurnal(U)

Other Activity

(Goldman and Anderson 1999, Klimely et al. 2001, Boustany et al. 2002) (Bond et al. 1999)

(Bond et al. 1999)

(Hobson et al. 1981)

(Bray and Ebeling 1975), (Hobson and Chess 1976, Hartney 1996) (Ebeling and Bray 1976, Cowen 1983, Hobson and Chess 2001, Topping 2003)

(Hobson and Chess 2001)

(Ebeling and Bray 1976, Hobson et al. 1981, Bond et al. 1999) (Ebeling and Bray 1976, Hobson et al. 1981)

(Hobson and Chess 1976, Hobson et al. 1981, Bond et al. 1999) (Nelson and Johnson 1970, Finstad and Nelson 1975, Strong Jr. 1989)

(Bond et al. 1999)

(Hobson et al. 1981, Cole 1984, Bond et al. 1999, Kroon et al. 2000)

(Bond et al. 1999)

(Hartney 1989, Bond et al. 1999)

(Hartney 1989, Bond et al. 1999)

(Bond et al. 1999)

(Bond et al. 1999)

Source

GRBQ065-2067G-C20[524-553].qxd 11/8/05 23:06 Page 534

Sand (benthic) Sand (benthic)

Pleuronectidae Pleuronectidae Pleuronectidae Pleuronectidae

Pleuronectidae Pleuronectidae

Slender sole

Dover sole

English sole

Diamond turbot

C-O sole (turbot) Curlfin sole

Bays (brackish)

Poeciliidae Pomacentridae Pomacentridae Sciaenidae Sciaenidae

Blacksmith

Garibaldi

Black croaker

White croaker

Shallow rock and kelp Shallow rock and kelp Shallow rock and sand Bays, sand (water column)

Sand (benthic)

Pleuronectidae

Sand (benthic)

Sand (benthic)

Sand (benthic)

Sand (benthic)

Sand (benthic)

Sand (benthic)

Sand (benthic)

Sand (benthic)

Hornyhead turbot Mosquitofish

Paralichthyidae (Bothidae) Paralichthyidae (Bothidae) Paralichthyidae (Bothidae) Paralichthyidae (Bothidae)

Ophidiidae

Sand (benthic)

Paralichthyidae (Bothidae) Pleuronectidae

Hippoglossina stomata Glyptocephalus zachirus Lyopsetta (Eopsetta) exilis Microstomus pacificus Parophrys vetulus Pleuronichthys (Hypsopsetta) guttulatus Pleuronichthys coenosus Pleuronichthys decurrens Pleuronichthys verticalis Gambusia affinis Chromis punctipinnis Hypsypops rubicundus Cheilotrema saturnum Genyonemus lineatus

Otophidium scrippsae Citharichthys sordidus Citharichthys stigmaeus Citharichthys xanthostigma Paralichthys californicus

Ophidiidae

Spotted cusk-eel Basketweave cusk-eel Pacific sanddab Spotted sanddab Longfin sanddab California flounder (halibut) Bigmouth flounder (sole) Rex sole

Sand/mud substratum (benthic) Sand (benthic & epibenthic) Sand (benthic & epibenthic) Sand (benthic)

Chilara taylori

Myliobatidae

Bat ray

Myliobatis californica


500 m (TO)

Ontogenetic, diel (DO,GA)

Tidal (AO)

Ontogenetic (GA,M)

Seasonal (OT)

Diel (OT)

Tidal, diel, seasonal (AT)

Diurnal (
100 mm SL) diurnal and nocturnal (100 mm) (DO, GA, M)

Diurnal (DO,GA) Diurnal (DO) Nocturnal(U)

No diel (DO,GA) No diel (GA,M) Nocturnal (GA,M) Diurnal(U)

No diel (GA,M) Nocturnal (GA,M) No diel (GA,M) Diurnal (GA,M) Diurnal (DO,GA) Diurnal, tidal(AO,GA)

Diurnal (GA,M) Diurnal (U) No diel (GA,M)

Nocturnal (DO,GA,M) Nocturnal (OT, DO, AO) No diel(GA,M)

(Allen 1982, Bond et al. 1999)

(Bond et al. 1999)

(Ebeling and Bray 1976, Hobson and Chess 1976, Bray 1981, Hartney 1996) (Clarke 1970)

(Bond et al. 1999)

(Allen 1982)

(Allen 1982)

(Hobson et al. 1981)

(Lane 1975)

(Allen 1982)

(Allen 1982)

(Allen 1982, Bond et al. 1999)

(Allen 1982, Bond et al. 1999)

(Allen 1982)

(Haaker 1975, Allen 1982)

(Bond et al. 1999)

(Ehrlich et al. 1979, Allen 1982)

(Allen 1982)

(Greenfield 1968)

(Allen 1982, Hobson and Chess 1986)

(Matern et al. 2000)

GRBQ065-2067G-C20[524-553].qxd 11/8/05 23:06 Page 535

California kingcroaker Queen croaker

Yellowfin croaker Pacific albacore

California scorpionfish Swell shark

Menticirrhus undulatus Seriphus politus

Umbrina roncador Thunnus alalunga

Scorpaena guttata Cephaloscyllium ventriosum Sebastes atrovirens Sebastes auriculatus Sebastes carnatus

Copper rockfish

Greenspotted rockfish Black & yellow rockfish

Calico rockfish

Splitnose rockfish

Sebastes caurinus

Sebastes chlorostictus Sebastes chrysomelas

Sebastes dallii

Sebastes diploproa

Gopher rockfish

Brown rockfish

Kelp rockfish

Common Name

Species

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae) Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae) Scorpaenidae (Sebastidae) Scorpaenidae (Sebastidae)

Scyliorhinidae

Scorpaenidae

Scombridae

Sciaenidae

Sciaenidae

Sciaenidae

Family

Recruit to drift kelp, deepwater (benthic)

Deep rocky reefs Shallow water, demersal (territorial) Shallow subtidal rock, epibenthic

Subtidal rock and kelp Shallow water, demersal Shallow water, demersal (territorial) deeper than S. chrysomelas Shallow water, demersal

Subtidal rock, sand Subtidal rock

Shallow sand (epibenthic) Open ocean (pelagic)

Shallow sand (epibenthic) Sand/mud (epibenthic)

Habitat

(continued)

Ontogenetic (GA,M)

50 m;
1500 m (TO); ontogenetic

6.4 km (TO); ontogenetic, seasonal Ontogenetic (U)

10–4000 m2 (AT, DO) 0.58–1.6 km2 (AT) 2–10 m2 (DO)

8 km (TO); ontogenetic Ontogenetic (DO, GA)

Ontogenetic, diel, seasonal (FO,TR)

Diel (DO,GA)

Ontogenetic, diel (DO,GA,M)

Migrations

400–1500 m2 (TO) 2–10 m2 (DO)

Nomadic

Home Range

Movement Patterns

TA B L E 20-1

Diurnal (juveniles), nocturnal (adults) (GA,M) Diurnal (juveniles), nocturnal (adults) (GA,M)

No diel (DO,GA)

No diel (DO, GA)

Nocturnal (GA,DO,M) Nocturnal (DO,GA) Nocturnal (GA,DO)

Diurnal (
100 mm), nocturnal (100 mm) (DO,GA,M) Nocturnal (DO,GA)

Nocturnal(U)

Other Activity

(Boehlert 1977, Allen 1982)

(Allen 1982, Bond et al. 1999)

(Ebeling and Bray 1976, Larson 1980, Hallacher 1984)

(Love et al. 2002, Starr et al. 2002)

(Matthews 1990a,b)

Ebeling and Bray 1976, Larson 1980, Hoelzer 1988)

(Ebeling and Bray 1976, Hobson and Chess 1976, Hobson et al. 1981, Bond et al. 1999) (Matthews 1990a)

(Nelson and Johnson 1970) (Tricas 1982)

(Hobson et al. 1981, Allen 1982, Bond et al. 1999)

(Laurs and J. 1977)

(Hobson et al. 1981, Bond et al. 1999)

(Hobson and Chess 1978, Allen 1982, DeMartini et al. 1985, Bond et al. 1999)

(Bond et al. 1999)

Source

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Greenstriped rockfish

Yellowtail rockfish

Shortbelly rockfish Cowcod

Quillback rockfish

Blue rockfish

Bocaccio

Greenblotched rockfish

Stripetail rockfish

Olive rockfish

Treefish

Shortspine thornyhead

Longspine thornyhead

Kelp bass

Sebastes elongatus

Sebastes flavidus

Sebastes jordani Sebastes laevis

Sebastes maliger

Sebastes mystinus

Sebastes paucisipinis Sebastes rosenblatti

Sebastes saxicola

Sebastes serranoides

Sebastes serriceps Sebastolobus alascanus

Sebastolobus altivelis

Paralabrax clathratus

Serranidae

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae) Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae) Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae) Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Scorpaenidae (Sebastidae)

Sand/mud substratum, deepwater (epibenthic) Sand/mud substratum, deepwater (epibenthic) Shallow rock and kelp (pelagic)

Shallow rock

Shallow water, pelagic, kelp/rock

Mud,cobble, (benthic, epibenthic)

Shallow to deep water, kelp, pelagic (schooling) Deep rocky reefs Deep rocky reefs

Shallow water, demersal

Deep pinnacles (schooling, pelagic) Water column Deep rocky reefs

Deep mud, cobble, rock

40–11000 m2 (AT)

800 m (DO,TR)

Little in juveniles (TO); ontogenetic

Ontogenetic (OT)

Ontogenetic (U)

Ontogenetic (TR)

12 km2 (AT)

1.3 km

6.4 km (TO); ontogenetic, seasonal Ontogenetic, seasonal (DO,TO)

22.5 km (TR), 3.7 km (AT)

10–4000 m2 (AT, DO)

0.2–1.7 km (AT, DO)

Diurnal (DO,GA)

Diurnal (juveniles), nocturnal (adults) (GA,M) Diurnal juveniles, nocturnal adults (U) Diurnal (
55 mm SL, inconsistent to 65 mm, nocturnal 65 mm)(DO,GA) Nocturnal (GA) Nocturnal(U)

Diurnal(U)

No diel (GA,M) Diurnal (juveniles), nocturnal (adults) (GA,M)

Diurnal (juveniles) nocturnal (adults) (GA,M)

(Hobson et al. 1981, Hartney 1996, Bond et al. 1999, Lowe et al. 2003)

(Wakefield and Smith 1990)

(Bond et al. 1999)

(Hobson et al. 1981)

(Hobson and Chess 1976, Love 1980, Bond et al. 1999)

(Allen 1982, Bond et al. 1999)

(Hartmann 1987, Love et al. 2002, Starr et al. 2002) (Allen 1982)

(Miller and Geibel 1973, Bond et al. 1999)

(Matthews 1990a, b)

(Allen 1982)

(Allen 1982)

(Carlson and Haight 1972, Pearcy 1992)

(Allen 1982)

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Spotted sand bass Barred sand bass Scalloped hammerhead

Pacific angel shark Monkeyface prickleback

California lizardfish Pacific electric ray Leopard shark

Painted greenling Shortspine combfisn Longspine combfish Blackbelly eelpout

Paralabrax maculatofasciatus Paralabrax nebulifer Sphyrna lewini

Squatina californica Cebidichthys violaceus

Synodus lucioceps Torpedo californica Triakis semifasciata

Oxylebius pictus Zaniolepis frenata Zaniolepis latipinnis Lycodes (Lycodopsis) Sand (benthic) Sand (benthic)

Zaniolepididae Zaniolepididae Zoarcidae

Shallow rock

Sand, subtidal rock (at night) Rock, sand, mud, estuarine (epibenthic)

Rocky inter and subtidal (benthic) Sand (benthic)

Bays, shallow coast Sand, sand/ rock interface Deep water pinnacle (pelagic) Sand (benthic)

Habitat

Zaniolepididae

Triakidae

Torpedinidae

Synodontidae

Stichaeidae

Squatinidae

Sphyrnidae

Serranidae

Serranidae

Family

6634 m2 (AT)

2 m2 (AT)

2.1–19 km (AT)

Home Range


1.4–6.4 km ontogenetic diel, tidal seasonal (TO)

Tidal (AT)

Diel (AT)

ontogenetic seasonal (TO)

Seasonal (FO)

Migrations

Diurnal(GA,M)

Diurnal(GA,M)

Diurnal(GA,M)

Diurnal(U)

Nocturnal (DO,AT)

No diel(GA,M)

No diel(AT)

Nocturnal(AT)

Diurnal(U)

Diurnal(U)

Other Activity

(Allen 1982)

(Allen 1982)

(Allen 1982, Bond et al. 1999)

(Bond et al. 1999)

(Ebeling and Bray 1976, Bray and Hixon 1978, Lowe et al. 1994) (Manley 1995, Ackerman et al. 2000)

(Allen 1982)

(Ralston and Horn 1986)

(Standora and Nelson 1977)

(Klimley et al. 1988, Klimley 1993)

(Love 1996, Bond et al. 1999)

(Bond et al. 1999)

Source

NOTE: Family names in parentheses indicate previously recognized nomenclature. Codes for evidence of behavior AO: aquarium observations; AT: acoustic telemetry; DO: diver observation; GA: gut analyses; M: morphological inference; OT: otter trawl; N: netting; SO: surface observations; ST: satellite telemetry; T: traps; TO: tag and observation; TR: tag and recapture; FO: fishery observation; U: unspecified

pacifica

Common Name

Species

(continued)

Movement Patterns

TA B L E 20-1

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territorial. Because, for most territorial organisms, territory size or space use is constrained by the amount of area they realistically can defend, non-territorial species should have larger home ranges than those that are territorial. Matthews (1990b) found home range sizes of shallow water copper (Sebastes caurinus) and quillback rockfish (Sebastes maliger) ranged from 30–1500 m2, depending on the quality of the habitat (table 20-1). While it is not known whether these fish are territorial or not, they tend to have larger home ranges than territorial black and yellow and gopher rockfishes (3–15 m2) studied by Larson (1980). Because Matthews (1990a) also found that fish moved seasonally from one location to another, these differences in home range size and space use between the two groups of rockfishes are most likely attributed to variability of food resources. In the case of copper and quillback rockfishes, it is possible that prey resources were more variable in the area where they were studied, thereby requiring the fish to have larger home ranges and reducing the benefits of being territorial. Similar observations have been made for two species of deepwater rockfishes in a Monterey Bay canyon. Starr et al. (2002) used an array of acoustic listening stations to quantify the movements of the demersal greenspotted rockfish and the more epibenthic bocaccio. They found that greenspotted rockfish used a much smaller area (0.5–1.6 km2) than bocaccio, which more frequently moved beyond the study area (12 km2)(table 20-1). In addition, bocaccio exhibited more vertical movements and were thought to be moving along the ledge and rim of the canyon. Although it is unlikely that either of these species is territorial, the species most closely associated with the substratum had the smallest home range. Like juvenile bocaccio, some rockfishes, such as yellowtail (Sebastes flavidus) and blue rockfish, are associated with rocky substratum, but are not demersal. These water column species form dense schools, usually around kelp beds or over rock banks and pinnacles. While there is much less known about the home range sizes of water-column rockfishes, one might expect there to be even larger home ranges for these species due to their decreased association with the substratum. In a tag and recapture study by Miller and Geibel (1973), juvenile blue rockfish tagged in shallow kelp bed habitats in central California exhibited little movement (
60 m) from their home reef. Juvenile blue rockfish tagged on deeper reefs were found to meander more along the reefs (
1.3 km) (table 20-1). They attributed those differences to possible variations in prey availability. Unfortunately, tag and recapture studies lack the resolution of acoustic tracking studies, so it is difficult to determine how realistic these methods may be in quantifying home range. In an acoustic telemetry study of yellowtail rockfish on an offshore bank, Pearcy (1992) found that these fish moved considerable distances over the bank (0.2–1.3 km) and made regular dives from 25 to 75 m depth (table 20-1). In comparison with their demersal congeners, yellowtail rockfish have significantly larger home ranges in both the horizontal and vertical plane. For these species, schooling may reduce predation risks, thereby reducing their dependence on shelters and allowing them more freedom to search out prey in the water column. Prey may be patchier in distribution and require the fish to move more to locate prey. Movements of these fish throughout the water column may enable them to locate prey that exhibit diel vertical migrations or may aid the fish in maintaining their position over the bank. Although there are common trends in space use patterns among species, there is a large degree of variability observed in

home range size within species and even individuals. Some fish home range studies have demonstrated that habitat quality significantly affects home range sizes of fishes. Matthews (1990a,b) found that copper and quillback rockfish had significantly smaller home ranges when occupying high relief habitats (
10 m2) than when they were over low relief habitat (
4000 m2). In addition, she found that the method used to quantify home range had a significant effect on area size estimates. Using a combination of visual underwater monitoring and acoustic telemetry, she found that acoustic telemetry measurements provided a more conservative measure of home range size. Lowe et al. (2003) observed similar trends in kelp bass acoustically tracked at Santa Catalina Island. Although there was no relationship in home range size with fish size, kelp bass residing under a pier showed significantly less movement (
40 m2) than similar size kelp bass occupying native habitat (
8000 m2) (table 20-1). Fish counts in these habitats indicate significantly higher densities of kelp bass in the vicinity of the pier than in natural habitats. This suggests that high quality habitats not only reduce the home range sizes of fishes, but can increase the densities of fishes as well. Kelp bass preferred this artificial habitat because it offered more shade, holes, and a light source that attracted prey at night. Although substratum availability may be limiting, the increased productivity of these habitats allows for greater fish density and less movement. Resource managers should keep this in mind when designing marine reserves. Setting aside areas of higher habitat quality could support larger numbers of fishes in a smaller area, potentially reducing the size requirements of marine reserves.

Low Relief Soft Substratum If an inverse relationship exists between home range size and habitat complexity, then fishes that occupy low relief or soft substratum habitats should have larger home ranges than those found over rocky reef habitats. Unlike rock-associated fishes, flatfishes, sand basses, coastal sharks, rays, croakers, and some surfperches found over soft substrata have received less study in terms of their movement patterns and home range sizes. Most of the movement pattern studies done on this assemblage of fishes have primarily utilized tag and release methods to quantify the degree of movement of the species. Tagging studies done on adult California halibut (Paralichthys californicus) suggest these fish show limited movement (
8 km) (Posner and Lavenberg, 1999). While these types of studies are most effective in quantifying dispersal and lack the resolution needed to determine home range size, observations by researchers such as Posner and Lavenberg (1999) provide evidence that sand-associated species, like halibut, move more than is typically seen in rock-associated species. This increased home range size is likely attributed to feeding requirements and food availability. Anecdotal observations of adult halibut based on fishing indicate California halibut may follow schools of anchovies and sardines, which can move over considerable distances (Love, 1996). While flatfishes appear lethargic and not highly mobile, large-scale movements are not uncommon. For example, studies of plaice (Pleuronectes platessa) in the English Channel have demonstrated that these flatfish move through out the entire channel (900 km) using tidal currents to assist their movements (Metcalfe and Arnold, 1997). Many species of croakers (Sciaenidae) found over sand habitats exhibit greater diel movement than rock-associates species.

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Using various fishing methods, Allen and DeMartini (1983) found that white croaker (Genyonemus lineatus) and queenfish (Seriphus politus) may exhibit considerable diel onshore/offshore movements, suggesting more extensive home ranges. Many species of soft substratum fishes have been shown to exhibit longshore movement patterns. The round stingray (Urobatis halleri), a common benthic stingray found in nearshore waters in southern California, can occur in high density patches (20 rays/m2) in bays and estuaries in the summer and fall months. Tag and recapture and acoustic telemetry studies have indicated that these rays move more than previously thought and appear to show seasonal site fidelity (Lowe et al. unpubl.; Vaudo, 2004). Therefore it is possible that these rays continually meander along the coast. The Pacific electric ray (Torpedo californica) is another highly mobile species that can be found over sand substratum. In an acoustic telemetry study (Bray and Lowe, unpubl.), rays were found to move at night, cruising over rock substratum bordering sand, but would settle and rest on sand substratum during the day. Rays exhibited a longshore movement from day to day. These types of space use patterns are similar to those observed for Pacific angel sharks. Pittenger (1984) acoustically tracked angel sharks around Santa Catalina Island and found they exhibited irregular movement patterns. Tagged angel sharks would spend several days in one area and then swim along the coastline at night, eventually circumnavigating the island (73 km). This type of longshore movement may be typical of many sand substratum oriented species (Love et al., 1986). Due to lack of habitat structure and more patchy food availability, many species commonly found over low relief soft substratum may have to move more to find food in this less complex habitat or to avoid predation. Regardless of this trend, movement patterns of fishes vary depending on resource availability. A good example of this may be seen in some deepwater fishes. Priede et al. (1986; 1990; 1991) used acoustic tracking to monitor the movement patterns of abyssal grenadiers (Coryphaenoides yaquinae) attracted to a baiting station at 6000 m depth. Scavenging grenadiers were allowed to swallow bait containing acoustic transmitters and were subsequently tracked using an array of hydrophones deployed around the seafloor. They found that the fish moved more than 1 km away within 8 hrs after feeding at the baiting station. Based on these movement patterns, they concluded that a scavenging grenadier might move up to 3000 km/year in search of food. In contrast, the longspine thornyhead (Sebastolobus altivelis), a deepwater rockfish, is one of the most abundant fish at depths of 700–900 m in the Southern California Bight (SCB) and are found over sand/mud substratum, yet it is thought to move very little. Stomach content studies of this species indicate they feed on brittlestars (Ophiopthalmus normani), which litter the sea floor at depths where Sebastolobus are found (Neighbors and Wilson, chapter 14). In a bioenergetics study by Vetter and Lynn (1997), longspine thornyheads were found to have a very low metabolism and it was concluded that these fish may only need to eat 3 or 4 meals per year! Therefore, they may not have to move about to find food because their energy requirements are so low, and in this case food is readily available and abundant.

Open Ocean Not all fishes show distinct home ranges. As one might expect, pelagic, open-ocean fishes, which may have little or

540

B E H AV I O R A L E C O L O G Y

no association with a substratum, may constantly be meandering about searching for food or mates. For example, movement studies of blue sharks and shortfin mako sharks in the SCB have provided little evidence for home ranging or site fidelity in these species (Sciarrota and Nelson, 1977; Holts and Bedford, 1993). Both blue and shortfin mako sharks have been observed swimming for kilometers without changing direction. Although it is possible that these tracking studies have been too short in duration to discern movement back to the area they were first tagged, standard tagging of these species also indicates they have high dispersal rates, which further indicates a lack of home ranging. Similar small-scale movement patterns have been observed for yellowfin tuna (Thunnus albacares) in the SCB. In an acoustic telemetry tracking study, Block et al. (1997) found that small (8–16 kg) yellowfin tuna moved extensively over a 2–3 day period, traveling more than 70 km in the SCB. They also observed that these fish remained in the mixed layer of the water column, but made occasional dives through the thermocline. Compared with movements of yellowfin tuna studied in more tropical regions (Holland et al., 1990), yellowfin tuna at higher latitudes exhibit a more compressed vertical distribution due to the thermocline being at shallower depths (Block et al., 1997). Other pelagic species such as the ocean sunfish (Mola mola) may also fit into this category and lack a home range. Cartamil and Lowe (2004) tracked ocean sunfish in the San Pedro Channel and found continuous and directed movement over periods up to 48 hrs. Unlike pelagic sharks that may be searching for schools of mobile pelagic fishes and squids, ocean sunfish are thought to be planktivores, and feed primarily on gelatinous zooplankton, which vertically migrate daily and are transported by ocean currents. In addition, sunfish are seasonally abundant in southern California waters and are thought to migrate, possibly following blooms of pelagic zooplankton. Similar movement patterns have been observed for planktivorous sharks, such as whale sharks (Rhincodon typus). Eckert and Stewart (2001) used satellite transmitters to track the movement patterns of whale sharks in the Sea of Cortez. They found extensive movement of tagged sharks throughout the Sea of Cortez and had several sharks move across the Pacific. They suggested that the sharks’ movements were influenced by oceanographic features corresponding with upwelling and increased plankton production. Most open ocean fish movements appear to be correlated more with movements of water masses, which can vary with season, current, and decadal weather pattern. However, due to the vast three-dimensional habitat that most open ocean fishes occupy, finding patches of prey may require development of specific strategies and result in more movement. Dagorn et al. (2000) developed a computer model to examine the evolution of movement patterns of predatory pelagic fishes (tunas, billfishes, and sharks) based on prey availability. Existing behavioral data on movement patterns of these fishes, as well as distributions and patchiness of prey species were factored into the model. Prey density and availability were found to greatly influence the evolution of movement patterns for each species of fish. Therefore, many open ocean species lack defined home ranges and may be more appropriately defined as “nomadic” in that they simply search for environmental conditions most likely to contain prey patches. Moving along the edges of water masses and eddies and making dives through the thermocline may increase the rate with which open ocean fishes encounter prey.

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M IG RATION—S PATIAL PAT TE R N S

Because of variability in resource availability or environmental conditions in most habitats, along with ontogenetic shifts in resource demands, it is not surprising that many species of fishes exhibit some sort of spatial movement pattern beyond that of typical home ranging. In its broadest sense, migration has been described as the undistracted movement an animal makes from one location to another, which can vary over a wide range of spatial and temporal scales (Dingle, 1996). The term “migration” has been used quite loosely throughout the fish literature, probably due to the difficulty in quantifying the movement patterns of individuals as well as the motivations for these movements. Nevertheless, there are numerous examples of spatial movement patterns of fishes that occur over various temporal scales, which may or may not meet the strict definition of a migration. For example, a fish may exhibit ontogenetic, seasonal (mating and reproduction), and diel (tidal, vertical, onshore-offshore) movements, all of which involve traveling from one habitat type to another. These movements may be influenced by the reproductive or developmental state of the fish, its susceptibility to predation, the availability of suitable food, or changing environmental conditions. In addition, because many of these movements may be bi-directional, fish must be able to find their way back to their original location, requiring an ability to home. The mechanisms that regulate these types of movements rely on a combination of innate and learned behaviors as well as the ability to use predictable information about environmental factors that would benefit moving (Dodson, 1988; Dingle, 1996). In this section, we will address the processes involved in these various types of movement and how they relate to a fish’s spatial requirements.

Ontogenetic Related Movements Because most species of fishes have a planktonic larval stage, many exhibit some ontogenetic movement from one habitat to another over the course of their lives. This is particularly true for demersal species of fishes such as flatfishes, some rockfishes, and labrids (Boehlert, 1977; Boehlert, 1978; Cowen, 1985; Brewer and Kleppel, 1986; Moser and Boehlert, 1991; Sakuma et al., 1999). For example, adult California halibut are commonly found over sand substratum on the shelf to depths of 90 m. Adults spawn throughout the year with a peak in winter and spring, which corresponds with a period of minimal offshore transport by currents (Lavenberg et al., 1986). Thus, the eggs and larvae remain over the shelf with the greatest densities found in waters less than 75 m deep, and the planktonic larval stage is relatively short (usually less than 30 d). Kramer (1991) suggested that transforming larvae may get pushed towards shore by being up in the neuston at night, but settling back down to the bottom during the day. Settled larvae may find bays and lagoons following longshore currents, and get transported into these habitats via tidal transport (Kramer, 1991). Juveniles emigrate from bays back to the open coastline after about one year, where they become more piscivorous as they mature. Kramer (1991) hypothesized that larval halibut move into the bays to escape predation pressure common along the coastline, but later leave the bays to obtain more oceanic prey such as anchovies, squid, and nektonic fishes. California sheephead spawn from May through August, and their larvae spend 34–78 d in the plankton before settling out

to the substratum (Cowen, 1985; Cowen, 1991). Sheephead larvae have been found many kilometers offshore, therefore their protracted larval duration may be necessary to allow the larvae to reach suitable habitat for settlement. There is some evidence that newly settled juveniles may be more abundant at deeper depths in nearshore environments, but they move to shallower depths as they mature (J. Caselle, pers. comm.). The opaleye (Girella nigricans) also undergoes a distinct ontogenetic shift in habitat use. They have a pelagic larval phase, which can be found out to 120 km offshore (Stevens et al., 1990). Preferring warmer water, pelagic juveniles (
2.5 cm) venture inshore and move into warm tide pools in the intertidal where they feed on invertebrates (Norris, 1963) (table 20-1). When these fish are about 7–15 cm long, they move out of the tide pools and into the subtidal zone where they form schools and shift their diets to algae. Many species of rockfishes exhibit ontogenetic shifts in habitat use. For example, juvenile deepwater longspine thornyhead are found up in the water column at depths or 500–600 m for their first 18–20 months before settling to the bottom where they are found as adults (Wakefield and Smith, 1990). Some larval rockfishes may be carried hundreds of kilometers offshore, and thus remain in the water column for several months up to a year recruiting to pieces of drift kelp and floating debris (Moser and Boehlert, 1991). Eventually, these larvae settle out of the water column and utilize benthic habitats. Ovoviviparous female splitnose rockfish (Sebastes diploproa) release larvae from February to July and the larvae recruit to drift kelp. They emigrate from the surface to bottom depths greater than 180 m starting around July, which suggests these fish may be in the water column from 6 months to 1 year (Boehlert, 1977). Once splitnose rockfish settle they assume their adult habitat over sand/mud substratum. This represents the typical ontogenetic habitat shift observed in most rockfishes. Bocaccio form schools when they are subadults and exhibit greater movements; however, they become more sedentary as they get larger and tend to refuge more (Starr et al., 2002). Many species of rockfishes, settle out in shallow waters and the adults migrate deeper as they get larger (Love, 1980). These ontogenetic movements may serve to minimize predation risks at more vulnerable stages of their life cycle, but shift to optimize feeding needs at another stage. In addition, this type of spatial movement is the primary dispersal mechanism for many species, yet it is still unclear what cues may induce settlement or to what extent dispersal may occur. Nevertheless, these migratory shifts exemplify the tradeoffs in cost optimization that fishes experience throughout their lives and how these tradeoffs shape their movement patterns and spatial needs.

Seasonally Related Movements In temperate regions, seasonal migrations of fishes are common. Although these migrations are usually elicited based on seasonal environmental changes, the reasons for the habitat shift may vary. Certain species of pelagic predatory fishes such as California barracuda (Sphyraena argentea), Pacific mackerel (Scomber japonicus) and bonito (Sarda chiliensis) show seasonal shifts in habitat use. Using scientific fishing methods, Allen and DeMartini (1983) found that Pacific mackerel and bonito were more common inshore in summer and early fall months than during winter months. They also attributed some of

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these movements to possible longshore migrations. These inshore/longshore movements are likely attributed to the movements and concentrations of prey inshore during summer and fall months. Seasonal inshore and longshore migrations are common in many benthic species like the round stingray and the Pacific electric ray, which may only be found close to shore at certain times of the year. It is thought that rays congregate nearshore for mating and pupping purposes, as mature males and females are most common during later summer and fall (Babel, 1967; Bray and Lowe, unpubl.). Thus, some seasonal inshore migrations may facilitate the concentrating of potential mates. Temperature can play a central role in influencing the seasonal movements and distributions of fishes. The fish assemblage inhabiting the artificial breakwater at King Harbor in Los Angeles experiences a structured and seasonally dynamic thermal regime caused in part by the proximity of warm water discharged from a power plant and cool water upwelled from a nearby submarine canyon. This setting provided Stephens and coworkers a unique opportunity to relate seasonal changes in fish distributions to water temperature (Terry and Stephens, 1976; Stephens and Zerba, 1981; Shrode et al., 1982; Stephens et al., 1994). The distributions of adult black perch (Embiotoca jacksoni), rainbow seaperch (Hypsurus caryi), pile perch (Rhacochilus vacca), and white seaperch (Phanerodon furcatus) shift to deeper cooler water during the late summer and fall, and return to shallower water when surface temperatures cooled. Subadults are more evenly distributed throughout the water column and do not vary seasonally. Juveniles appear in shallower warmer water than adults, suggesting an ontogenetic move to deeper water as they grow (Terry and Stephens, 1976). Laboratory studies, in which fish were placed in horizontal temperature gradients, indicate that the observed seasonal distribution patterns can be explained by thermal preferences, not depth per se. In addition to the rainbow seaperch, shiner perch (Cymatogaster aggregata), blacksmith (Chromis punctipinnis), and calico rockfish (Sebastes dalli), selected temperatures that were similar to temperatures where they occurred in the field (Shrode et al., 1982). While it is thought that most rockfishes do not seasonally migrate (Love, 1980), a number of species have been shown to home after being displaced from their original site of capture (Carlson and Haight, 1972; Miller and Geibel, 1973; Hallacher, 1984; Matthews and Reavis, 1990; Matthews, 1990b; Pearcy, 1992) (table 20-1). The ability to home often implies the capacity to navigate or orient to landmarks, which are skills often used in migrations. For example, some rockfishes have been reported to move to deeper waters during winter months, particularly populations north of Point Conception, California. Miller and Geibel (1973) found fewer juvenile blue rockfish off shallow reefs in Monterey Bay during winter months and concluded that these fish may have been moving to deeper water to avoid turbulence due to winter storms. However, they also acknowledged that it was possible that the fish had not actually moved to deeper water, but they may have counted fewer fish due to the poor water conditions. Although there is no direct evidence of movement back and forth, the shift in abundances could indicate seasonal migratory movements. Not all seasonal movements of rockfishes are related to avoiding rough conditions. For example, the demersal California scorpionfish (Scorpaena guttata) apparently makes extensive migrations in late spring and early summer to spawn in groups; in this case, however, movements are vertical because the aggregations form in the water column during

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spawning (Love et al., 1987). Matthews (1990a) found that copper, quillback and brown (Sebastes auriculatus) rockfishes would move from low relief reefs in the winter to other suitable habitats. She hypothesized that this seasonal movement was related to the annual disappearance of kelp on these reefs. In this particular case, rockfish might be migrating to find suitable habitat, which is often accompanied by additional food. Many pelagic fishes such as tunas, marlins, and sharks also make seasonal migrations for the purpose of mating and spawning. The SCB is thought to be an important pupping and nursery area for blue, shortfin mako, white, and common thresher sharks (Alopias vulpinus). Blue sharks are thought to migrate south in spring and summer months to mate, but venture north to pup and feed (Strasburg, 1958; Nakano, 1994). Common thresher sharks are also thought to show north-south seasonal migrations along the eastern Pacific through Baja, Mexico (D. Holts, pers. comm.). Pacific bluefin tuna (Thunnus thynnus) have been found to swim across the Pacific. Tunas tagged off California and Mexico have been recaptured off Japan (7500 km) and bluefin tagged off Japan have been recaptured off California and Mexico (Clemens and Flittner, 1969). Although these tagging data do not indicate whether these are seasonal migrations they do imply bidirectional movement between the two locations. Similar seasonal migrations have been suggested for Pacific albacore tuna (Thunnus alalunga). Laurs and Lynn (1977) used commercial catch data and tag and recapturing information to quantify the seasonal migration of Pacific albacore. They found that these tunas may be following transition zone waters as they move east during summer months. Future studies using satellite telemetry tags will undoubtedly help answer questions about migration routes and oceanographic correlates for these pelagic fishes. Studying the movement patterns of large predatory fishes such as white sharks poses distinct challenges. The occurrence of white sharks at the Farallon Islands, California during fall months has been correlated with the arrival of juvenile elephant seals, which haul out on the island at this time of year. Goldman and Anderson (1999) acoustically tracked adult white sharks around the Farallon Islands during daylight hours and found that they repeatedly use certain areas near the seal haulout areas. The areas covered ranged from 1.84–4.34 km2 and the size of the daytime home ranges increased with the size of the shark. As winter arrives and the seals leave, so do the sharks. Although the same sharks were found to return to the Farallon Islands every year, of six adult white sharks tagged with pop-up satellite tags at the Farallon Islands one was found to travel to the Hawaiian Islands and back and three were detected in open ocean off Baja, Mexico (Boustany et al., 2002). While white sharks have been previously documented in Hawaii, these findings indicate that they may behave more like pelagic sharks than previously thought. Nevertheless, it is still not clear whether these oceanic movements are related to breeding migrations or following prey—there have been anecdotal observations of white sharks following migrating humpback whales near the Hawaiian Islands.

Tidally Related Movements Tidal flux provides an excellent cue for timing migrations, but also allows for increased access to habitat not normally accessible to many fishes. Some species of fishes, particularly those

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found in the sublittoral zone, make migrations into the intertidal zone during periods of high tide. For example, rockpool blennies migrate up into tide pools during high tides and then migrate back down to the subtidal zone when the tide is out (Stephens et al., 1970). This species has been shown to home back to its home pool after being displaced 45 m. The monkeyface prickleback also undergoes tidal migrations, moving farther up into the intertidal zone with flooding tides (Ralston and Horn, 1986). As juveniles, these fish live in intertidal pools and are carnivorous, feeding on copepods, amphipods, isopods, and polychaetes. However, as they get larger they shift to an herbivorous diet, feeding on a wide variety of algae. Moving into the intertidal provides herbivorous adult fish access to more algae. Both Green (1971) and Williams (1957) observed that different species of sculpins (wooly sculpin, Clinocottus analis and tidepool sculpin, Oligocottus maculosus) migrate up into the intertidal pools as the tide flooded. Smaller individuals move the farthest, but usually at a distance less than 10 m. Other studies have shown that the intermediate-sized tidepool sculpin can home from a distance of up to 100 m, probably using olfaction (Khoo, 1974). Some fish like the California grunion (Leuresthes tenuis) make a seasonal, tidal, spawning migration. Grunion time their spawning movements with high spring tides, which allow them to come up onto the beach and spawn in the sand. The eggs remain buried in the sand until the following spring tides, at which time the eggs hatch and the larvae are carried offshore (Walker, 1952; Speer-Blank and Martin, 2004).

Diel Related Movements Diel migrations of fishes are particularly common because the rhythmic changes in light associated with day and night provide one of the best cues for setting biological clocks. Many fishes exhibit distinct changes in habitat use between day and night. While some species move into holes and shelters and become quiescent, others become active and move into the water column. Some species may move extensively during these diel habitat shifts regardless of their life stage. For example, many species of fishes exhibit diel vertical migrations even during their pelagic larval stage. Postflexion larval Pacific and speckled sanddabs (Citharichthys sordidus and C. stigmaeus) were found to vertically migrate from deeper water depths during the day through the pycnocline into shallower waters at night (Sakuma et al., 1999). Schools of northern anchovies (Engraulis mordax) have been shown to exhibit both vertical and onshore-offshore diel migrations (Allen and DeMartini, 1983; Robinson et al., 1995). Northern anchovy schools were found to move to deeper offshore waters during the day, but ventured inshore to shallower waters at night. Robinson et al. (1995) also found a strong correlation between anchovy movement and euphausiid abundance and concluded that anchovies may be exhibiting this diel migratory pattern as the result of following prey. Even pelagic fishes that may exhibit little or no home range pattern still show diel movement patterns. For example, blue sharks tracked off Santa Catalina Island during winter months were found to move inshore at night and swim along the bottom, but would move back into offshore waters more near the surface during the day. This diel pattern was only observed during winter months and is thought to be attributed to the local abundance of prey inshore (squid—Loligo opalescens) at

that time of year (Sciarrota and Nelson, 1977; Tricas, 1979). An opposite pattern of movement was observed in swordfish (Xiphias gladius) acoustically tracked in the Sea of Cortez by Carey and Robison (1981). Several swordfish were found to move inshore over a 91 m deep bank during the day and swim just above the bottom, whereas at night they moved offshore to open water and would swim near the surface. Carey and Robison (1981) hypothesized that these swordfish may be venturing inshore to feed on demersal fish moving on and off the bank, then venturing offshore to feed on abundant pelagic squid that would migrate towards the surface. Obviously many of these types of migrations require the ability to orient to environmental cues or the ability to discern landmarks. While we have learned a lot about why fish move, when and where, we still know very little about how they achieve some of these impressive migrational movements. Space use patterns seem to be governed by tradeoffs between feeding, mating, and avoiding predation.

Activity Patterns—When Do Fish Move? The high diversity of fish species off California results in a wide range of activity patterns. These patterns make up a time dimension of the niche that has presumably evolved in response to many selective forces. Environmental situations, such as the availability of prey, nearness and activities of predators, level of the tide, etc., can affect activity levels of fish at a particular time and place. The broad patterns of California fish activities—when fish are prone to be active and inactive—also may be influenced by internal biological clocks. We will first provide a review of the wide range and nature of activity patterns displayed by California marine fishes with an emphasis on subtidal rocky reefs and surrounding areas. Later, we will briefly consider the control of these activity patterns by external and internal factors. It is important to understand the vocabulary used to describe activity patterns. The commonly used terms relate to environmental rhythms created by the rotations of the earth and the moon. These terms include diel (24-hr day), diurnal (daytime), nocturnal (nighttime), crepuscular (dawn and dusk), tidal (one high and one low tide), semilunar (twice per month), lunar (each month), and annual (year). We will avoid the term “daily” because of its inconsistent usage. Although daily normally refers to diel, authors occasionally use it when describing only diurnal activities. Activity patterns are usually inferred from five general sources of information: 1) direct observations of location and behavior; 2) monitoring individuals using remote sensing methods (i.e., sonar, LIDAR, telemetry); 3) examination of gut fullness of fish collected throughout the diel period; 4) knowledge of the diel availability of prey; and 5) inferences from morphology. Most of these methods are adequate for species that display consistent and obvious rhythmic behavioral patterns. For other species, none of these methods provides a comprehensive picture. For example, while direct observations may reveal patterns of planktivores or herbivores, they are less useful for making inferences about study sit-and-wait predators (e.g., some rockfishes) that rarely move. Remote sensing studies tend to be restricted to fairly large fish and resolving ability may vary considerably depending on the species being studied and methods used. Gut content analyses can be

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ambiguous in situations where diel patterns in fullness are not evident. Species like the blacksmith consistently have food in their guts during the day and early evening but have empty guts just before dawn. In such situations, it can be inferred that it takes less than 24 hr for a food bolus to pass though the fish, enabling a crude estimate of feeding times. On the other hand, species like the giant kelpfish (Heterostichus rostratus) have items in their guts in both day and night collections (Hobson et al., 1981). In such cases, additional knowledge of movement and digestive rates of food in the gut, or knowledge about the diel habits of their prey, is required before feeding times can be estimated. We raise several precautionary notes before summarizing the activity patterns of some California fishes. First, many fish are opportunistic. For example, the walleye surfperch (Hyperprosopon argenteum) feeds mainly at night as evidenced by the relatively full guts of individuals collected at night, but empty guts of individuals collected during the day (Hobson and Chess, 1976). Nevertheless, walleye surfperch are often caught on baited hooks during the day by shore fishers (Frey, 1971). The activity of cuskeels (Ophidiidae) is another example. These fishes normally bury in sand during the day and emerge at night (Greenfield, 1968; Hobson and Chess, 1986a); however, when the water is extremely turbid, they appear above the sand during the day and assume their nighttime behavior (Greenfield, 1968). Thus, a fish species might show overall general patterns of activities but the pattern can be altered under the appropriate environmental conditions. Second, as reported in the section above entitled, Ontogenetic migrations, activity patterns may change as fish age. In many cases where studied, juveniles are diurnally active while the adults may be nocturnal. Various rockfishes (Sebastes spp.) are examples of this pattern (table 20-1). Third, behavior might vary substantially among individuals. For example, a small number of subtidal reef fishes engage in removing ectoparasites and scales from other fish species. The best-known California example is the señorita (Oxyjulis californica) (Hobson, 1971). Careful observations on the rock wrasse (Halichoeres semicinctus) by Hobson (1976), and zebraperch (Hermosilla azurea) and opaleye by DeMartini and Coyer (1981) indicate that a few individuals of these species also clean—and these individuals do so frequently. This suggests that specialization can occur among individuals within a species. Thus, pooling individual behaviors to characterize a species’ activity pattern masks these complex, but more realistic pictures of fish behavior. Cleaning behavior is discussed in detail in chapter 22. With these reservations in mind, we examined the literature to gain insight on the activity patterns of California marine fishes. This information is summarized in the column labeled Other Activity in table 20-1. The longest activity pattern in table 20-1 is tidal; longer patterns mainly involve large-scale movements (see above and the Migrations column in table 20-1) or reproduction, which is covered elsewhere (DeMartini and Sikkel, chapter 19). Seventy-nine of the 105 species with activity data in table 20-1 demonstrate clear diel patterns (51 primarily diurnal, 28 primarily nocturnal). An additional 10 species (one embiotocid, two sciaenids, and seven sebastids) display mixed patterns, with the juveniles being active during the day and the adults being active at night. We suspect that additional studies of younger life-history stages will reveal that many other species also shift their activity patterns as they age. Most of the detailed information on activity patterns involves fish that inhabit subtidal rocky reefs—and our sum-

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mary reflects this bias. Our survey is not complete but hopefully covers research on the most conspicuous and intensely studied species.

Diel Activity Patterns on Subtidal Rocky Reefs Since the advent of scuba, southern California has been a major focal point of studies of diel activities of subtidal fishes. Outside of the tropics, probably more is known through direct observation about the diel activities of fish inhabiting subtidal reefs and surrounding sand flats in southern California than in any other region. Because of this rich knowledge base, we focus on diel activity patterns in and around rocky-reefs. One of the first studies, by Nelson and Johnson (1970), described the nocturnal activities of horn sharks (Heterodontus francisci) and swell sharks (Cephaloscyllium ventriosum) off Santa Catalina Island. Since then, the daytime and nighttime activities of numerous fishes have been conducted, mainly in the southern California Bight. Most of the community-level studies have centered around Big Fisherman Cove, Santa Catalina Island (33°27’N, 118°29’W) (e.g., Hobson and Chess, 1976; Hobson et al., 1981; Hobson and Chess, 1986a) and at Naples Reef (34° 25’N 119°57’W) (e.g., Bray and Ebeling, 1975; Ebeling and Bray, 1976; Bray and Hixon, 1978). Naples Reef is 24 km west of the city of Santa Barbara and less than 50 km from the major zoogeographic boundary at Pt. Conception. Additional long-term studies of the daytime and seasonal distributions of fishes have been conducted along the rocky breakwater at King Harbor (33°50’N, 118°20’W) (Terry and Stephens, 1976; Stephens and Zerba, 1981; Shrode et al., 1982; Stephens et al., 1994). In the following paragraphs, we describe the typical day and nighttime situation on rocky reefs at Santa Catalina Island and Naples Reef during clear and calm conditions (fig. 20-5a–d). We grouped the fishes according to broad foraging guilds (Ebeling and Hixon, 1991) because of the dominance of foraging behavior when fish are active.

Patterns in Feeding and Distribution During the day, the water column is filled with aggregations of planktivorous fishes numerically dominated by blacksmiths (fig. 20-5a, c) but also juveniles of various species. At dawn, blacksmiths emerge from their nighttime shelters among the rocks and swim into the water column where they feed on zooplankton; at dusk, they descend from the water column and move into their nighttime shelters (Ebeling and Bray, 1976; Hobson and Chess, 1976; Bray, 1981). Smaller blacksmiths do not stray far from kelp or rocky cover; however, larger individuals may migrate hundreds of meters and gather where water currents bring in oceanic zooplankton (Bray, 1981). Other common midwater inhabitants are the pickertype microcarnivores, including señoritas and kelp perch (Brachyistius frenatus) and occasional omnivores, such as halfmoon (Medialuna californiensis) and opaleye. Closer to the bottom, many of the obvious activities are by large-bodied microcarnivores such as demersal surfperches, garibaldi, and by various juveniles. Several species of surfperches (Embiotocidae) are commonly found in rocky reefs off southern California (Hobson and Chess, 1976; Ebeling et al., 1979; Stephens et al., 1994). These species include the black perch, rainbow seaperch, and the pile perch. An additional species, the striped

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F I G U R E 20-5 Depiction of day-night shifts in fish activity and water column distributions over rocky reefs. (a) Naples Reef day, (b) Naples Reef night, (c) Santa Catalina Island day, (d) Santa Catalina Island night, (e) Bahia de Palmas, Baja California, Mexico day, (f) Bahia de Palmas night. Fig. 20-5a after Ebeling and Hixon (1991); fig. 20-5e, f after Hobson (1965). (Fish drawings by L. Allen and illustration by K. Anthony.)

seaperch (Embiotoca lateralis) becomes abundant from Santa Barbara northward. Diving observations and gut analyses indicate that most of these feed mainly during the day (Ebeling and Bray, 1976); at night these fishes are inactive but often remain exposed just above the bottom. Other conspicuous fishes that are diurnally active are the opaleye, halfmoon, and juveniles and subadults of the kelp bass (fig. 20-5a–d). Along the bottom, careful observation has shown that many smaller benthic reef fishes are also diurnally active. Blackeye gobies typically position themselves at the rock-sand interface, where they periodically dart out and snap zooplankton or benthic prey; at night, they take shelter in rocks and do not feed (Hobson et al., 1981). Brightly colored bluebanded gobies (Lythrypnus dalli) and the more reclusive zebra

goby (Lythrypnus zebra) feed during the day, mainly on benthic prey (Hartney, 1989; Hobson and Chess, 2001). Some of the larger macrocarnivores (such as kelp rockfish Sebastes atrovirens) may sit motionlessly on rocks or hang among kelp fronds. Holes and crevices may be occupied by California morays (Gymnothorax mordax), zebra gobies, and a few demersal rockfishes Sebastes spp., but in general are not heavily occupied (fig. 20-5a,c). The nighttime picture of fish activity is more subdued. Fewer fishes occupy the water column and more fishes occur in rocky shelters. This vertical day-night pattern was observed qualitatively at Santa Catalina Island by Hobson et al. (1981) and quantitatively off the Santa Barbara mainland by Ebeling and Bray (1976). One of the most abundant midwater nocturnal

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fishes is the walleye surfperch, which school inshore during the day and migrate offshore at night to feed on emergent zooplankton (Ebeling and Bray, 1976; Hobson and Chess, 1976). Another embiotocid, the rubberlip seaperch (Rhacochilus toxotes) is nocturnally active off Santa Barbara (Ebeling and Bray, 1976). Notably, both the walleye surfperch and rubberlip seaperch have enlarged eyes compared to other embiotocids of comparable body size. Most of the fish at night are either positioned quietly right above the bottom (e.g., most surfperches), nestled in benthic algae (e.g., rock wrasse), or are in rock shelters. California sheephead typically rest under overhangs or in rocky crevices although they have also been seen fully exposed on the substratum (Hobson and Chess, 2001). Rock wrasse spend the night under sand or rocks or amid benthic algae (as summarized in Hobson and Chess, 2001). Señoritas spend the night underneath the sand. Diving and aquarium observations at dusk indicate that señoritas first descend to a sandy patch, roll on their sides just above the substratum, then swim into the sand headfirst with a flick of the caudal fin (Bray and Ebeling, 1975). They remain buried in sand throughout the night, as evidenced by aquarium observations and the lack of reported sightings at night during numerous night dives (Bray and Ebeling, 1975; Ebeling and Bray, 1976; Hobson et al., 1981; Hobson and Chess, 1986b; Hobson and Chess, 2001). The horizontal distributional pattern of some fishes in the water column also differs between night and day. The blacksmith, a numerically dominant daytime planktivore, forages on oceanic zooplankton transported by water currents. Adult fish gather at the incurrent end of offshore reefs (Bray, 1981) or at the mouths of coves and headlands along the shore (Hobson and Chess, 1976; Bray, pers. obs.). While the actual feeding location can vary, according to tides and other determinants of nearshore currents, the result is a clumped spatial distribution of fish at certain locations above or near the reef. At night, however, the midwater planktivores such as the walleye surfperch are more dispersed throughout reefs instead of being aggregated at the incurrent end. This difference in spatial distribution of fish in the water column is likely due to the distribution of their prey. Unlike the oceanic zooplankters that make up the diet of diurnal fish, the zooplankters eaten by nocturnal fish are resident forms that emerge from the substratum at night. These zooplankters are broadly distributed throughout the reef and avoid currents that would sweep them away (Hobson, 1991). At night, more fishes occupy open sand habitats than during the day (Hobson and Chess, 1986b) (fig. 20-5d). These species include the spotted cuskeels (Chilara taylori), walleye surfperch, shiner perch, yellowfin croaker (Umbrina roncador) and horn shark. At Abalone Cove on the Palos Verdes Peninsula in Los Angeles County, we have also seen substantial numbers of California scorpionfish dispersed over the sand at night where we have not seen them during the day (Bray and Lowe, pers. obs.). Most of the fishes that appear over sand flats at night spend the day elsewhere, resulting in crepuscular migrations. An exception is the spotted cuskeel, which remains buried in sand during the day and emerges to feed in the same habitat. Hobson and Chess (1986a) hypothesized that the diel activity patterns of fishes over sand flats is possibly due to the nocturnal increase in prey availability at night and a decrease in number of predators.

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Patterns of Egestion and Excretion While most obvious and well-documented diel activities in California reef fishes involve the feeding of diurnally-active fishes, this behavior also results in regular patterns of egestion of fecal matter and excretion of ammonium. In tropical reefs, large quantities of fecal material are released in the water column during the day by planktivorous fishes; much of this fecal material is consumed by other fishes before it reaches the reef’s surface (Robertson, 1982). A similar phenomenon occurs above rocky reefs off California. Hobson et al. (2001) observed that halfmoon and señoritas consume the fecal material from planktivores, mostly blacksmiths. At least some the diurnal feeders also defecate at night. One line of evidence comes from comparison of the fullness and location of food items in the digestive tract. The gut fullness of many fishes collected throughout the diel period show a progressive filling of the foregut, stomach, and intestine as the day passes, followed by similar pattern of elimination at night (e.g., Ebeling and Bray, 1976; Hobson and Chess, 1976; Cowen, 1983). Although this evidence has been used to support visual observations that the fish are diurnal feeders, it also means that the fish egest fecal material at night. For example, Cowen (1983) reported that the intestinal tracts of California sheephead are empty at dawn; that, coupled with the observation that sheephead were never seen defecating during the daytime, led Cowen to conclude that they defecate at night. Blacksmiths follow a similar diel pattern of gut fullness, with full guts in the afternoon and empty guts at dawn (Hobson and Chess, 1976; Bray, 1981). Nighttime defecation was confirmed when fecal material was found at dawn in pipes occupied by sheltering blacksmiths (Bray et al., 1981). The fecal material does not accumulate along the rocky reefs. Detritivores such as shrimps and other crustaceans consume the feces (Rothans and Miller, 1991). Tagging evidence indicates some blacksmiths tend to return to the same nocturnal shelter, so the fecal material egested in nocturnal shelters represents a food source to detritivores that is predictable in time and space (Bray et al., 1981). For more discussion of feeding and trophic interactions please see chapter 13. This is but one example in which the diel cycles of activity of fishes may affect other members of the reef community. Another possible community-level impact of fish activities involves excretion of ammonium as a result of nitrogen metabolism. Ammonium levels are higher in the vicinity of schools of Atlantic menhaden (Brevoortia tyrannus) (Oviatt et al., 1972) and juvenile grunts (Haemulon flavolineatum and H. plumieri) (Meyer et al., 1983). Off California, ammonium levels are higher within and just downstream of blacksmith aggregations during the daytime, and in shelters occupied by blacksmiths at night (Bray et al., 1986). Ammonium is an important nitrogen source for many algae so the excretion by fishes might contribute to the nutrient status of primary producers in inshore communities.

Comparison between Study Sites The intensive community-level studies at Santa Catalina Island and Naples Reef provide an opportunity to compare activity patterns at different locations within the southern California bight (Ebeling and Hixon, 1991; Helfman, 1993). The fish community at Santa Catalina Island shares similarities with counterparts on tropical reefs. Both reef communities

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have a diurnal and separate nocturnal shift of active fishes and both have daytime resting aggregations and twilight migrations of fishes (Hobson et al., 1981). The diel activity pattern of the rocky reef fish community at Naples Reef is not as distinct. At night, fewer species forage in the water column, fewer species take shelter, and no fish move from reef to sand flat to forage; overall, Naples Reef at night appeared to be loosely programmed (Ebeling and Bray, 1976). These local differences in community activity are probably due to several reasons: 1. Methodology. The Santa Catalina Island studies consist of general observations at various study sites throughout all times day and night with a focus on crepuscular hours. This approach integrates activities over large expanses of space and time but also confounds direct comparisons between day and night. The Naples Reef study involved paired day-night counts of fishes along a fixed transect line. This method allows direct comparisons of day-night activities, but observations and conclusions are focused in a small area around the line. 2. Physiography. The bottom profile at many sites around Santa Catalina Island drops off steeply from shore resulting in a horizontally compressed mixture of habitats. In contrast, Naples Reef is 1.6 km offshore and the gradually sloping bottom profile between shore and the reef consists of sand and low relief rocks. Habitats are spatially segregated and fewer fish may migrate to the reef itself. 3. Zoogeography. The species composition on rocky reefs varies along the California coast (see zoographical summaries by Cross and Allen, 1993; and Hobson, 1994). Even within the southern California region, the fish community differs between Santa Catalina Island and the cooler areas off the coast of Santa Barbara and the northern Channel Islands. Santa Catalina Island has more representatives of primarily tropical while Santa Barbara has more cold-temperate species (Hobson et al., 1981; Ebeling and Hixon, 1991). Point Conception, less than 50 km west of Naples Reef, is a major zoogeographic barrier for tropical affiliates (Horn and Allen, 1978; Hobson, 1994). Because the species with the most distinctive diel patterns are from primarily tropical families (e.g., pomacentrids and labrids), the overall distinctiveness between day and night decreases in locations where these families are rare or absent.

C OM PAR I SON B ET W E E N TE M P E R ATE AN D TROP ICAL R E E F S

Because day-night activities of reef fishes have been studied at several tropical and temperate locations, it is also possible to the compare the activities of California fishes with those found in tropical reefs. For the comparison, we chose Hobson’s study of fishes at Bahia de Palmas (23°40’N, 109°42’W) near the tip of Baja California. Bahia de Palmas is a broad (18 km) sandy bay dotted with rocky outcrops (Hobson, 1965). Corals exist in the region but do not form reefs. The fish fauna consists mostly of Panamic representatives from the south mixed with a smaller number of northern and endemic species (Hobson, 1968). The diel activities of fishes at Bahia de Palmas are similar to those described in other tropical regions

although the species richness is lower than other tropical reefs (see below).

Day-Night Differences The most distinctive diel activity patterns of reef fishes occur in the tropics (Starck and Davis, 1966, numerous papers by Ted Hobson; Collette and Talbot, 1972). During the day, the water column is occupied with various pomacentrids, labrids, and other species while the bottom is active with numerous fishes that feed on algae, sea grasses, and sessile invertebrates (fig. 20-5e). At night, many of these species take shelter deep in reefs, where they do not feed. These species are replaced by other fishes equipped with large eyes and mouths that enable them to feed on large zooplankters that emerge at night from the substratum (fig. 20-5f). Thus, the water column just above coral reefs has day and night shifts of fishes that replace each other over a diel period. The diurnal species are more derived and have feeding and digestive specializations for consuming small zooplankters or benthic algae, respectively. The nocturnal feeders species are more generalized taxonomically and eat medium-sized prey that are available only at night (Collette and Talbot, 1972; Ebeling and Hixon, 1991; Hobson, 1991). Some California reef fishes show day-night differences in magnitude comparable to those in the tropics. Conspicuous diurnal species in this category include the two pomacentrids (garibaldi, Hypsypops rubicundus and blacksmith) and three labrids (California sheephead, rock wrasse, and señorita)—all temperate representatives of primarily tropical families. These fishes are active during the daytime and seek shelter at night (fig. 20-5a–d). However, the day-night differences of many other diurnally active reef fishes off California are more subtle. For example, diurnally active bottom feeders off California, such as several species of embiotocids, spend the night in the open rather than take shelter (fig. 20-5b, d). They remain semi-alert at night and slowly move away if disturbed by divers. Gut analyses indicate that most surfperch (Embiotocidae) feed only during the daytime (Ebeling and Bray, 1976; Hobson et al., 1981). The day-night differences of some of the nocturnal fishes off California are also less distinct than those in the tropics. Many tropical planktivores that feed above reefs at night take shelter individually and in small groups in holes and crevices during the day. These species include squirrelfishes and cardinalfishes, and soldierfishes (fig. 20-5f). In contrast, of the Santa Catalina species that are nocturnally active in the open water column (e.g., walleye surfperch, queenfish and salema, Xenistius californiensis), none shelters in reefs during the day; instead, they spend the daytime in dense, inactive schools (fig. 20-5d) (Hobson and Chess, 1976; Hobson et al., 1981). Thus, a major difference in nocturnal tropical and temperate planktivores is that during the day, the species on temperate reefs do not completely vacate the water column; they form inactive schools rather than take shelter in the reef. Ebeling and Hixon (1991) compared the number of species with distinct diel activity patterns in tropical and California reefs based on a literature review. Ninety-four percent of the tropical species have a distinct activity period compared to 84% of the Californian species. The percentage was similar for fishes that were diurnal (55% tropical versus 53% Californian) and nocturnal (31% tropical versus 34% Californian) (Ebeling and Hixon, 1991). Another more dramatic tropical-temperate contrast involves the species richness. The number of species

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with known activity cycles observed in tropical studies ranged from 53 at Bahia de Palmas to 159 species in the Florida Keys. Far fewer species were reported off southern California (37 species at Santa Catalina Island and 23 species at Naples Reef). Thus, one obvious explanation for the tropical-temperate differences in diel activity patterns reflects the well-known differences in species richness between the two regions.

Dawn and Dusk Changeover The period during the diel cycle that has attracted particular interest in coral reefs is the evening and morning changeover. This is the time when the diurnal shift of fishes occupying the water column is replaced by the nocturnal shift (e.g., Hobson, 1965; Collette and Talbot, 1972; Hobson, 1972) Helfman et al. (1997) provide a nice summary of the four different stages that play out over coral reefs during the dusk changeover. Stage 1: migrations made along the bottom by diurnal fishes that forage in one location and shelter in another. Fishes involved in these migrations are the zooplanktivores (e.g., some serranids, butterflyfishes, damselfishes) and large herbivores (parrotfishes and surgeonfishes). Stage 2: sheltering in crevices, holes, or ledges by diurnally active species. The timing varies according to family. Labrids are the first to shelter, followed by pomacentrids and other fishes. Stage 3: quiet period, starting after sunset, during which the water column above the reef is largely vacant. Stage 4: emergence and migration of nocturnal fishes. Fishes once again populate the water column, but in this case the species are adapted to feeding on zooplankton that emerge from the substratum at night. These fishes include bigeyes, cardinalfishes, soldierfishes, and croakers. At dawn, the process is reversed, starting with the migrations of the nocturnal fishes towards their shelters. The order of appearance of diurnal fishes is reversed, with pomacentrids among the early risers and the labrids being among the last to appear (Helfman et al., 1997). This pattern has been reported in the Gulf of California (Hobson, 1965), Hawaii (Hobson, 1972), and the Caribbean (Collette and Talbot, 1972). What drives this well-ordered pattern of events? The best explanation for the quiet period over coral reefs is the threat of predation by piscivores at twilight. There are several lines of evidence for this. Direct observations (e.g., Hobson, 1968) indicate that large predatory fishes are more active during crepuscular hours. Additionally, studies of visual pigments and the light environment (McFarland, 1991) indicate that the sensitivity of scotopic (low-light) vision of many fishes better matches the characteristics of twilight than the starlight or moonlight. The argument is an evolutionary one: the visual sensitivity of fishes is tuned in to the lighting conditions that result in maximized fitness. Natural selection has led to the optimization of photon capture at twilight because of the increased threat of predation by large piscivores at that time (McFarland, 1991). The sheltering and emergence behaviors before and after the quiet period preempt predation on many fishes during the most vulnerable time. The dawn and dusk changeover among California reef fishes appears more drawn-out and less obvious. The most conspicuous difference according to Hobson et al. (1981) is the apparent lack of a clear “quiet period” that is so characteristic of tropical reef fishes. The most detailed description of the evening changeover of California reef fishes was reported by Hobson et al. (1981). At sunset, the major event off Santa Catalina Island is the migration of blacksmiths to their nocturnal shelters. At

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about 10 minutes after sunset, the migrating groups start breaking up as individual blacksmiths take shelter. Approximately 10 and 20 min after sunset, the last of the señoritas, rock wrasse, and California sheephead take shelter. It is also during this time that the first olive rockfish (Sebastes serranoides) appear in the water column. It is not until at least 30 min after sunset that the first queenfish and salema appear at their feeding locations. In comparison, between approximately 12 and 32 min after sunset at Kona, Hawaii, the water column is vacant, forming the quiet period (Hobson et al., 1981). The major point is that off Santa Catalina Island there is little evidence of a distinct quiet period. Instead, the water column is occupied throughout dusk by the overlap of diurnally and nocturnally active fishes. Several explanations have been forwarded for the temperatetropical differences in fish activities during crepuscular hours (summarized in Helfman, 1993). Because the most distinctive differences between day and night behaviors involve representatives from primarily tropical families, the tropical-temperate difference might result from a latitudinal decrease in the abundance of tropical derivatives (e.g., Ebeling and Bray, 1976). Alternatively, since the tropical changeover may be driven by the threat of twilight predation, perhaps predation is less prevalent during crepuscular hours off California (Hobson et al., 1981). Another explanation is that temperate fishes tend to be larger than tropical counterparts, so the threat of predation might be reduced. Also, the twilight period itself is more drawn out in temperate areas, resulting in a more gradual change in light levels (Helfman, 1981). The abrupt evacuation of the water column by fishes during twilight may be because their visual adaptation mechanisms are too slow to keep up with the ambient light changes. On the other hand, the slower change in lighting in temperate areas give fish enough time to adapt visually, thus, reducing the need to dramatically alter behavior during twilight (Helfman, 1993).

Biological Clocks A central question in the study of activity patterns is whether their control is exogenous (outside of the organism) or endogenous (inside of the organism). A set of terms describes these patterns. Circa patterns generally refer to activity patterns that are influenced by an internal biological clock (Ali et al., 1992). “Circadian” refers to a diel pattern; other common terms include circatidal, circasemilunar, circalunar, and circannual. A rhythmic pattern that continues under constant conditions (i.e., a circa pattern, is termed “free running” and is under the control of an internal time keeper). This biological clock does not keep perfect time, however, and must be reset periodically with an environmental cue, termed a Zeitgeber (German for “time giver”). Thus, many rhythmic activities, such as circadian rhythms, require at least two components: an endogenous clock and an exogenous cue to reset it. Research over the past century has revealed two patterns that depend on the period of the activities. Patterns that take place repeatedly in less than one day (termed “ultradian”) are primarily endogenous. At the subcellular level, for example, these rhythms are tied to oscillations in biochemical and neurogenic activity rather than rhythmic external factors (Peters and Veeneklaas, 1992). Activities that are diel and longer may be under endogenous and/or exogenous control (Gerkema, 1992). Endogenous biological rhythms of fishes are under control of the neuroendocrine system (Helfman et al., 1997). The

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hormone melatonin, secreted by the pineal organ on the dorsal surface of the brain, appears to be a widespread timekeeping molecule that controls many physiological and behavioral functions (Zachmann et al., 1992). Melatonin concentrations follow a circadian rhythm, with elevated levels occurring at night. Photoperiod is the probably the most important environmental cue but temperature also plays a role (Zachmann et al., 1992). Numerous studies have demonstrated the presence of circa rhythms in fish. Most studies have involved freshwater species (Ali, 1992) and only a few studies have been conducted on California marine fishes. The swell shark and horn shark display a circadian rhythm, actively swimming at night and sheltering in rocks during the day. In the lab, swell sharks maintain a distinct circadian activity under constant lighting conditions with increased movements occurring at a time that normally correspond to onset of darkness (Nelson and Johnson, 1970). Initial studies showed that horn shark activity was exogenous, not circadian (Nelson and Johnson, 1970); however, later experiments under different lighting intensities indicate that horn shark movements exhibit drifting circadian rhythm (Finstad and Nelson, 1975). Studies of relatives of California fishes demonstrate endogenous control of patterns. For example, the diel activity patterns of labrids appear to be circadian. The diel activity patterns of Halichoeres chrysus in the western tropical Pacific are similar to the rock wrasse off southern California: it is active during the day and hides in the substrate at night. Laboratory studies by Gerkema (2000) indicate that individuals maintain this free running behavior under constant dim illumination. There is similar evidence of a circadian rhythm in Coris julis, which buries in sand at night (in Gerkema, 1992). Based on the evidence collected so far, it seems reasonable to hypothesize that the diel activities of the labrids and probably other fishes off southern California are under similar endogenous control. Do fish sleep? This interesting question was discussed by Reebs (1992). The answer depends on the definition of sleep. The electroencephalograms (EEGs) of mammals, recorded in the cortex, display characteristic patterns during sleep. Fish do not have a cortex so sleep cannot be measured with this criterion. However, aquarium studies of one labrid and eight species of parrotfishes indicate that at night these fishes displayed behavior similar to a sleeping mammal: diminished overall activity, decreased responsiveness to stimuli, decreased and irregular respiratory movements—and periodic eye movement (Tauber and Weitzman, 1969). Why do fish sleep? Circadian patterns of sleep may allow fish to conserve energy. Additionally, anticipation of sleep might force fish to seek shelter during times when they may be particularly vulnerable to predation (summarized in Reebs, 1992). This latter idea has support in studies of the importance of predation on California reef fishes, especially during crepuscular hours (Hobson et al., 1981). However, this does not explain why certain fish remain in shelters throughout the night. Hobson concluded that predation was most intense during crepuscular hours and decreased towards the middle of the night. At Naples Reef and off the Palos Verdes Peninsula in Los Angeles County, however, Pacific electric rays enter rocky reefs after sunset and hunt for fish prey (Bray and Hixon, 1978; Lowe et al., 1994). The rays swim slowly above the reef substratum and have been observed close to exposed fish. The stomach contents of one Pacific electric ray collected at dawn on the sand flat adjacent the reef

contained two kelp bass and one black perch–both species that do not take shelter in rocky crevices. Additionally, California moray eels commonly feed on fishes at night. Large sheltering fish might be protected by their size but smaller fishes along the bottom may be vulnerable. The presence of nocturnal predators may help explain why many fish remain in shelters throughout the night. The threat of predation may also force small individuals to shelter deep in tiny crevices, as evidenced by the emergence of small fish, not previously seen, after application of the anesthetic quinaldine (Bray, pers. obs.). The apparent universal nature of biological clocks begs the question about their adaptive significance. The prevailing idea about the adaptive significant of biological clocks, reviewed by Gerkema (1992), is centered on anticipation and synchronization. Anticipation involves the initiation of various physiological and biochemical mechanisms in preparation for upcoming activities. For example, the semilunar spawning cycle of grunions is preceded by a whole sequence of physiological steps (e.g., gametogenesis) in advance of the actual spawning run. Synchronization involves coordination of activities with conspecifics (to engage in schooling, feeding or spawning aggregations, etc), avoiding other species such as predators, and adjusting to periodic changes in the physical environment (e.g., light, tides). Overall, the central theme to all of these examples is that biological clocks enable anticipation of regular, predictable events (Gerkema, 1992).

Summary While it is impressive to see how much we have learned about the movement and activity pattern of California fishes, there is still a lot of questions left unanswered. There are a number of good examples that suggest that fishes most closely associated with complex habitats tend to move less than those more loosely associated with habitat; however, there also appears to be a large amount of variability in behavior between species and individuals. Nevertheless, the general differences in movements are likely associated with energetic tradeoffs between finding food and mates, and avoiding predation or unsuitable abiotic conditions. In addition, many of the same tradeoffs have likely influenced the evolution of activity patterns that we see in marine fishes. The recent development of new technology and techniques has significantly furthered our knowledge of fish movement and activity and it is likely these advances will continue. Because of the economic importance of many marine fishes in California, the need to understand fish behavior has increased, particularly for its application in resource and fisheries management. While we have a better understanding of the proximate mechanisms that influence movement and activity pattern in fishes, we still do not thoroughly understand the ultimate mechanisms behind these behaviors. In addition, while there has been a lot of research done to examine the movement patterns of larger fishes, there is still relatively little known about movements and space use of small fishes. Further investigation of ontogenetic shifts in movement pattern of fishes might lend support of the cost optimization models postulated in this chapter. This information could be extremely valuable to resource managers in developing better fisheries management models and when establishing marine protected areas.

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Strong Jr., W.R. 1989. Behavioral ecology of horn sharks, Heterodontus francisci, at Santa Catalina Island, California, with emphasis on patterns of space utilization. Master’s Thesis. California State University Long Beach, Long Beach. Tatso, R. 1975. Aspects of the biology of Pacific staghorn sculpin, Leptocottus armatus Girard, in Anaheim Bay, pp. 123–135. In: The marine resources of Anaheim Bay. Vol 165, Fish Bulletin. E. D. Lane and C.W. Hill (eds.). California Department of Fish and Game. Tauber, E.S., and E.D. Weitzman. 1969. Eye movements during behavioral inactivity in certain Bermuda reef fish. Comm. Behav. Biol. A:131–135. Terry, C.B., and J.S. Stephens, Jr. 1976. A study of the orientation of selected embiotocid fishes to depth and shifting seasonal vertical temperature gradients. Bull. So. Calif. Acad. Sci. 75:170–183. Topping, D.T. 2003. Movement patterns, site fidelity, and habitat use of California sheephead (Semicossyphus pulcher) in a marine life reserve at Santa Catalina Island, California. Master’s Thesis. California State University Long Beach, Long Beach. Tricas, T.C. 1979. Relationships of the blue shark, Prionace glauca, and its prey species near Santa Catalina Island, California. U.S. Fish. Bull. 77:175–182. ———. 1982. Bioelectric-mediated predation by swell sharks, Cephaloscyllium ventriosum. Copeia. 1982:948–952. Trumble, R.J., I.R. McGregor, G. St-Pierre, D.A. McCaughran, and S.H. Hoag. 1990. Sixty years of tagging Pacific halibut: A case study, pp. 831–840. In: Fish-marking techniques. Vol. 7, American Fisheries Society Symposium. N.C. Parker, R.C. Giorgi, D.B. Heidinger, D.B. Jester Jr., E.D. Prince Jr., and G.A. Winans (eds.). Vaudo, J.J. 2004. Movement patterns of the round stingray, Urobatis halleri, at Seal Beach, California. Master’s Thesis. California State University Long Beach, Long Beach. Vetter, R.D., and E.A. Lynn. 1997. Bathymetric demography, enzyme activity patterns, and bioenergetics of deep-living scorpaenid fishes (genera Sebastes and Sebastolobus): Paradigms revisited. Mar. Ecol. Prog. Ser. 155:173–188. Wakefield, W.W., and K.L. Smith. 1990. Ontogenetic vertical migration in Sebastolobus altivelis as a mechanism for transport of particulate organic matter at continental slope depths. Limn. Oceanog. 35:1314–1328. Walker, B.W. 1952. A guide to the grunion. Calif. Fish Game, Fish Bull. 38:409–420. Williams, G.C. 1957. Homing behavior of California rocky shore fishes. University of California Publications in Zoology. 59:249–284. Young, P.H. 1963. The kelp bass (Paralabrax clathratus) and its fishery, 1947–1958. Calif. Fish Game, Fish Bull. 122:1–67. Zachmann, A., M.A. Ali, and J. Falcón. 1992. Melatonin and its effects in fishes: an overview, p. 149–165. In: Rhythms in fishes. Vol. 236. M.A. Ali (ed.). Plenum Press, New York.

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CHAPTER 21

Symbiotic Relationships J O H N E. M cC O S K E R

Introduction The symbiotic relationships of plants and animals have fascinated terrestrial biologists for centuries, and with the development and improvement of scuba and underwater photographic and recording equipments since the mid-20th century the symbiotic stories of aquatic creatures are now becoming appreciated as well. It is the intent of this chapter to report upon examples of symbioses involving fishes in California coastal and offshore waters extending south to Magdalena Bay, Baja California (note that throughout this text references to California fishes will comprise that region). The symbiotic activities of tropical and subtropical fishes that are transient in California waters, such as those that have arrived during recent El Niño events (Lea and Rosenblatt, 2000), are not treated. The common names of fishes used herein follow those of the American Fisheries Society (Robins et al., 1991). Selected literature concerning California examples of symbiosis as well as review articles involving extralimital symbiotic relationships are included. Opportunities for further research will be identified within this text. Symbiosis is a word of Greek origin, meaning living together. Current usage, although not universal, arose from an address by Anton de Bary in 1878 to the German Naturalists and Physicians at Kassel and published the following year (de Bary, 1879). De Bary introduced the term “Symbiose” to include all categories of association between dissimilar organisms, ranging from mutualism to commensalism to parasitism. Later authors redirected the term to be equivalent to mutualism and the assumption that at least some benefit occurs to either or both partners, such that many 20th century authors have considered parasitism and mutualism to be nearly antithetical (discussed in: Henry, 1966; Cheng, 1967; Goff, 1982; and Lewin, 1982). “Parasitism,” of Greek origin and whose original meaning was a guest who shares the dinner table, now conveniently “implies a detrimental effect on the host, a pathological condition that is generally and typically not compensated for by the trouble caused” (Lewin, 1982: 254). Commensalism is derived from Latin cum (together) mensalis (of the table), and had at its origin much the same meaning as parasitism. Symbiotic reality is such that categories of interspecific rela-

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tionships are rarely abruptly discontinuous, and more often the paired organisms might alternately or simultaneously occupy two or more categories. The categorization of symbiotic relationships is not easy, and made difficult by the fact that commensal or mutualistic associates can, between meals, transform from messmates to predators and prey. For example, cleaner shrimps are often found in the stomach of California moray eels, evidence of an evolutionary relationship in progress; cleaner fishes often cheat by consuming scales and mucus from an unsuspecting client; and how does one classify a remora, as a freeloading hitchhiker or a parasite picker, or both? Commensal partners rarely share the metabolic dependency involved with both parasitic and mutualistic relationships, thus the greatest overlap is likely to occur between mutualists and parasites (see Cheng, 1967, for an expanded discussion). For the purposes of this discussion, I follow Hertig et al. (1937) and Starr (1975) who have established guidelines that are generally followed but continually challenged. Simply, mutualism benefits both partners; commensalism involves benefits to one partner without harming or helping the other, and parasitism benefits one of a pair while the other suffers a reduction in fitness. I consider phoresis to be a subcategory of commensalism and treat it under that section.

Mutualism Mutualistic symbioses are among the most interesting due to the degree of fitness provided to the participants and to the evolutionary pathways along which they might have arisen. Mutualism can be obligatory or facultative, and direct or indirect. In direct mutualism, participants benefit each other through their direct contact, such as the anemonefish and the anemone, whereby the anemone provides a safe refuge from predation and the fish repels polyp-feeding fishes. Indirect mutualisms benefit species not through direct interaction between species pairs but rather by the actions taken by one participant. Cushman and Beattie (1991) assess the benefits of mutualism and cite as an example of indirect mutualism Paine’s (1966) demonstration that acorn barnacles (Balanus glandula) benefit from the action of starfish

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(Pisaster ochraceus) that prey on mussels (Mytilus californianus) that would otherwise competitively exclude barnacles from the substrate. Numerous examples of indirect mutualism might be inferred (but would be difficult to experimentally verify) from an analysis of marine food webs. Whether such associations are mutualistic requires quantitative verification of the costs and benefits to both participants (Cushman and Beattie, 1991), and undertaking those studies underwater is difficult at best. Cleaning behavior provides ample evidence for interspecific symbiosis, however debate continues concerning its categorization. Numerous species, both above and below water, are involved in cleaning behavior, and they have doubtless arrived through a variety of evolutionary pathways. At first blush, most observers reported it to be beneficial from a mutualistic standpoint, whereby guilds of cleaner fishes and shrimps establish cleaning stations and remove ectoparasites from client fishes (Limbaugh, 1961; Feder, 1966). Such reciprocal altruism seems likely and appropriate (Trivers, 1971; Poulin and Vickery, 1995; but see Gorlich et al., 1978), however despite numerous quantitative field studies involving the removal of cleaners from reefs, the seemingly obvious benefits of cleaning has been demonstrated in but few instances (Youngbluth, 1968; Losey 1972; Grutter, 1997; the exception being that of Grutter, 1999). Losey (1972) held that “although the adaptive value of cleaning is probably ectoparasite removal, the proximate causal factors are not related to ectoparasites. Thus, in some areas, the relationship of the cleaner to the host may become commensal or even parasitic.” As he aged, Losey (1987) dispassionately viewed cleaner fish as “nothing but clever behavioral parasites” that feed largely on the hosts’ tissues and mucus when the production rate of ectoparasites was low. They do this by exploiting the sensory system of their clients whose benefit is one of hedonistic tactile stimulation (Losey, 1979). The exploitative consequences of such parasitism must be small (Poulin and Grutter, 1996) when one recognizes the popularity of the symbiosis. Cleaning symbiosis is further complicated by cheating by both cleaners (who consume more client tissue than ectoparasites) and clients (who eat the cleaners), a variant that was sure to evolve, and has, several times (Poulin and Vickery, 1995). In summary, considering the various opinions and field studies mentioned above, I must categorize cleaning behavior among fishes to range gradually from mutualism, that is advantageous to clients when ectoparasite levels are critical, to parasitism, whereby cleaners feed on fish tissue and mucus when ectoparasites levels are low, but may find themselves at risk of being consumed. Limbaugh (1955, 1961) published the first descriptions of California cleaner fish and Hobson (1971) provided its first extensive survey. Limbaugh (1961) and Feder (1966) had suggested that the presence of cleaning stations along inshore kelp beds was responsible for the aggregations of sport fishes at those localities. Hobson (1971) examined their hypothesis but concluded “There is no basis for the contention that many good fishing grounds in southern California exist because fishes have congregated in these locations for cleaning.” Eighteen species from nine fish families have been shown to provide service in cleaning symbioses in California coastal waters (fig. 21-1; table 21-1). The seven species of oceanic suckerfishes, family Echeneidae, are not considered in this discussion (see chapter 12). Their symbiotic relationships are

discussed in Strasburg (1964). Hobson’s (1971) research demonstrated that the señorita is the predominant cleaner fish in California waters, and it, along with the kelp perch and the sharpnose seaperch, may be the only habitual cleaners (figs. 21-2, 21-3). The other species listed above are only sporadic cleaners as an adjunct to their normal feeding behavior. It should be noted that cleaning has not been observed in shallow intertidal waters. Such high energy environments provide a low diversity of hosts and makes coordinated movements difficult between cleaner and host. Although based only on casual observation, Losey et al. (1999) suggest that this lack of intertidal cleaning activity has no apparent cost to the fishes. Unlike their tropical counterparts, the cleaning activity of California cleaners are not centered around well-defined cleaning stations and the cleaner, rather than the client, initiates the cleaning bouts. Hobson (1971: 491) noted that “an infected fish approached by a cleaner generally drifts into an unusual attitude that advertises the temporary existence of the transient cleaning station to other fish in need of service, and these converge on the cleaner. Although señoritas, as a group, clean a number of different fishes, a given individual tends to initiate cleaning with members of just one species.” Unlike the behavior of tropical cleaners, California cleaners restrict their parasite removal to the skin and do not enter the mouth and branchial cavities of clients. The majority of parasites removed are caligid copepods and gnathiid isopod larvae. Unlike señoritas, which clean as adults and juveniles, the sharpnose seaperch cleans only as a juvenile (
125 mm length). The clients most frequently cleaned are those which were most abundant and most heavily infested, and no significant preference for client species was observed. And one may assume that, unlike many of their tropical counterparts, their roles as cleaners probably does not afford California cleaners any security from being eaten during noncleaning situations. Recently, however, island kelpfish (Alloclinus holderi), bluebanded goby (Lythrypnus dalli), juvenile giant kelpfish (Heterostichus rostratus) and juvenile kelp bass (Paralabrax clathratus) have been observed at what appears to be cleaning stations for giant sea bass (Stereolepis gigas) at Anacapa Island (DeWet-Oleson and Love 2001). The juvenile kelpfish not only entered the mouth of the giant sea bass but also had unusual behavior of 15 to 20 individuals parasite picking at a time (DeWet-Oleson and Love 2001). California marine cleaners, other than the fishes described above, include shrimps and birds. Limbaugh (1961) described the relationship between the California cleaner shrimp Hippolysmata californica (now Lysmata californica) and its clients, the California moray (Gymnothorax mordax) (fig. 21-4a), the garibaldi (Hypsypops rubicundus), and the spiny lobster (Panulirus interruptus). Lysmata californica is not an obligate cleaner, and continually feeds on the epibiose of the rocky substrate, which it occupies (Limbaugh et al., 1961). Limbaugh also discovered cleaner shrimp within the gut contents of California morays and observed the shrimps to occasionally feed upon tissue of their clients. Limbaugh et al. (1961: 251) summarized their observations by stating “Hippolysmata californica therefore exhibits a rather simple and imperfect relationship with its hosts, sometimes eating them and sometimes being eaten itself. During the cleaning process, the shrimps seem only to seek food on a new substrate. From this simple and hazardous relationship, it is easy to visualize an evolutionary path by which the more complex cleaning behavior could have developed.”

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F I G U R E 21-1 California cleaner fishes. Included are: wrasses, family Labridae, a) señorita, b) a juvenile and female rock wrasse,

and c) juvenile California sheephead; surfperches, family Embiotocidae, d) kelp perch, e) black perch, f) pile perch, g) rainbow seaperch, h) sharpnose seaperch, and i) white seaperch; kyphosids, family Kyphosidae, j) halfmoon, k) zebra perch and l) opaleye; m) blacksmith, Pomacentridae; n) salema, Haemulidae; o) island kelpfish, Labrisomidae; p) bluebanded goby, Gobiidae; q) juvenile kelp bass, Serranidae; r) juvenile giant kelpfish, Labrisomidae (see table 21-1).

Another client commonly observed off the California coast is the ocean sunfish (Mola mola, family Molidae) which can be seen off the edge of kelp beds, positioned in awkward postures while being groomed by surfperches (rainbow and/or sharpnose seaperches) (Gotshall, 1967). As well, molas are occasionally observed over deep water during the summer lying on their sides at the surface with gulls picking at their skin parasites (Tibby, 1936; King, 1978; Love, 1996); these observations are complicated but not contradicted by the fact that during

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infrequent mola die-offs, molas may be seen floating at the surface, with gulls picking at their eyes (Gotshall, 1961). Considerable opportunity for further research on cleaning behavior exists in California coastal waters. Greg Jensen of the University of Washington advises me that numerous undocumented fish and shrimp interactions remain unreported (and probably others still undiscovered) in the northwest Pacific, in part because much of that activity may be nocturnal. Hobson and others have noticed that cleaners are

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TA B L E 21-1

Fishes Known to Engage in Cleaning Behavior in California Waters

Scientific Name

Common Name

Family

References

Alloclinus holderi Brachyistius frenatus Chromis punctipinnis Embiotoca jacksoni Girella nigricans Halichoeres semicinctus Hermosilla azurea Heterostichus rostratus Hypsurus caryi Lythrypnus dalli Medialuna californiensis Oxyjulis californica Paralabrax clathratus Phanerodon atripes Phanerodon furcatus Rhacochilus vacca Semicossyphus pulcher

island Kelpfish kelp perch blacksmith black perch opaleye rock wrasse zebraperch giant kelpfish (juvenile) rainbow seaperch bluebanded goby halfmoon señorita kelp bass (juvenile) sharpnose seaperch white seaperch pile perch California sheephead

Labrisomidae Embiotocidae Pomacentridae Embiotocidae Kyphosidae Labridae Kyphosidae Labrisomidae Embiotocidae Gobiidae Kyphosidae Labridae Serranidae Embiotocidae Embiotocidae Embiotocidae Labridae

DeWet-Oleson and Love 2001 Limbaugh 1955, Hobson 1971 Turner et al. 1969 Limbaugh 1955 DeMartini and Coyer 1981, Sikkel 1986 Hobson 1971 DeMartini and Coyer 1981, Sikkel 1986 DeWet-Oleson and Love 2001 Gotshall 1967 DeWet-Oleson and Love 2001 Hixon 1979 Limbaugh 1955, Hobson 1971 DeWet-Oleson and Love 2001 Gotshall 1967, Hobson 1971 Hobson 1971 Limbaugh 1955 Coyer 1980

Xenistius californiensis

salema

Haemulidae

Sikkel 1986

Note: After DeWet-Oleson and Love 2001.

F I G U R E 21-2 Señoritas (Oxyjulis californica) cleaning blacksmiths (Chromis punctipinnis). Note the head down posture of the blacksmiths that are soliciting cleaning. (Photo courtesy of E.S. Hobson.).

F I G U R E 21-3 Sharpnose seaperches (Phanerodon atripes) cleaning blacksmiths (Chromis punctipinnis). (Photo courtesy of E.S. Hobson.).

at risk of themselves being infected by non-specific ectoparasites, but an extensive study has not been attempted. And, although much attention has been paid to the parasitized fishes, far too little is known of the biology of the parasites. The time of infestation, the mechanism of host choice, the degree of specificity, and the life history of most parasites remains to be investigated. This has value and application as has been shown in experiments with pen-cultured Atlantic salmon, which when raised in high densities become heavily parasitized, resulting in skin damage, secondary infections and impaired osmoregulation. Employing temperate wrasses as an alternative to pesticide treatment has been shown to be cost-effective and appropriate, but not without difficulties (Kvenseth, 1996; Losey et al., 1999). The introduction of exotic marine cleaner species to California waters, despite its perceived benefits, is neither legal nor appropriate, but the beneficial behaviors of native cleaner fishes and shrimps are well worth exploring.

Endosymbiotic mutualisms are probably more abundant than currently recognized and provide an area for further investigation. Two examples that I will describe briefly include the creation of light by bioluminescent bacteria and the role of microbes in assisting digestion by herbivorous fishes. Bioluminescence in marine fishes has two origins, viz. the selfluminous species such as the batrachoidid midshipmen (Porichthys spp.) and the myctophid lanternfishes (many genera and species) which, via specialized photophores, produce light primarily for counterillumination and intraspecific signaling, and those that employ bacterial symbionts to provide light that is used for a variety of purposes, including counterillumination, food detection, feed attraction, intraspecific signaling, and passive predator avoidance. California fishes that participate in bioluminescent bacterial symbioses include the ceratioid anglerfishes, an anomalopid, and certain macrourids (rattails) and morids (codlings). Most are deepwater species hence little is known of the behavior of the fishes through

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F I G U R E 21-4 Examples of symbiotic relationships in fishes off the Californias: a) the California cleaner shrimp (Lysmata californica) and its client, the California moray (Gymnothorax mordax); b) the Mexican flashlight fish (Phthanophaneron harveyi) employ bacterial symbionts in a subocular organ (arrow) to provide light; c) luminous ceratioid anglerfishes are all obligate mutualists (worldwide, females of nine of eleven recognized ceratioid families possess escas (lures) which employ bacterial symbionts).

direct observation. It can be inferred that the symbiosis is mutualistic and obligatory to both partners in the case of those fishes that employ bacteria for the attraction and gathering of food (McCosker, 1977; Haygood, 1993), and apparently commensal or mutualistic in a number of other midwater fishes that employ bacteria within their gut as an aid to digestion (the luminescence of fecal pellets thereby provide an attractive dispersal mechanism for the bacteria) (Nealson and Hastings, 1979). Those luminous ceratioids (fig. 21-4c) that live off the continental shelf and in our coastal waters are all obligate mutualists (worldwide, females of nine of eleven recognized ceratioid families possess escas which employ bacterial symbionts). The Mexican flashlight fish (Phthanophaneron harveyi; fig. 21-4b), captured in shallow water in the Gulf of California and off Thetis Bank, Baja California (McCosker and Rosenblatt, 1987), is remarkable in the amount of light that it casts as well as the mechanisms that it has developed (a dark shutter and rotation of the light organ) to occlude the light. In aquarium captivity, it is possible to darken the bacteria of another anomalopid (Anomalops katoptron) (McCosker, unpublished data); under those conditions the fish is unable to find its crustacean prey, demonstrating the obligatory nature of that symbiosis. Obligate bacterial endosymbionts have been shown to occur in some tropical surgeonfishes (family Acanthuridae), however other studies of fish gut endosymbionts suggest that

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most relationships are not obligatory and that the presence of gut microbes is often an artifact of microbial populations in the water or the food (Fishelson, et al., 1985). Horn (1992) has suggested that microbial fermentation plays a role in the digestive processes of kyphosids, including the halfmoon (Medialuna californiensis), the opaleye (Girella nigricans), and the zebraperch (Hermosilla azurea), but is not involved in the digestive process of another California herbivore, the monkeyface eel (Cebidichthys violaceous, family Cebidichthyidae).

Commensalism The relationship between various fishes and jellyfish medusae and siphonophores is often cited as an example of commensalism (reviewed by Mansueti, 1963). Juveniles of California carangids, girellids, and most notably, stromateoids (particularly the nomeids, centrolophids, and stromateids), participate in this symbiosis (see chapter 12). The young fish gain several advantages: protection from predation; food (the small invertebrates associated with the tentacles and bell of the medusae, and ultimately the host itself); and a means of dispersal. Mansueti (1963) considers this relation to be a temporary ecological phenomenon in which the medusae are passive hosts and the juvenile fishes are active opportunists. What begins as a commensal relationship in many species

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epizoites such as the pilotfish (Naucrates ductor) (see fig. 21-7; chapter 12) that accompany large sharks or the non-predatory carapids (not resident in California waters) that occupy the respiratory tract of holothurians. Commensal associations between gobiid fishes and various invertebrates are well known. Relations between gobies and the three species of Neotrypaea (as Callianassa) ghost shrimps were the subject of classic studies by MacGinitie and MacGinitie (1949: 288–290, 429–432). Their description is worth repeating, for the charm of the verse and the fact that it reinforces the difficulty in categorizing symbioses. As concerns its digging behavior, they state “Callianassa is doomed to a life of almost constant digging,” and the resultant local downside, “Oyster growers in the Puget Sound regions will also testify to the industry of Callianassa, for many oysters are buried by the soil carried to the surface by this shrimp.” Alas, they exhort, “but it is an ill wind that blows no good, and if some oysters are killed by the activities of Callianassa, other animals are afforded living quarters and refuge, and still others are provided with a set of conditions that enable them to live where they otherwise could not live.” And it is just that sort of symbiosis that the arrow goby (Clevelandia ios) enjoys with the pink ghost shrimp Neotrypaea californiensis. Arrow gobies (fig. 21-5) are not reticent to occupy other invertebrate burrows and can be found living the tubes of the fat innkeeper worm (Urechis caupo) or the mud shrimp (Upogebia pugettensis) (Fisher and MacGinitie, 1928). MacGinitie and MacGinitie (1949: 428) provided the grist for early marine symbiosis tales when they explained the relationship of arrow gobies and their co-commensals as observed in aquaria: F I G U R E 21-5 Depiction of the commensal relationship between the

fat innkeeper worm (a) Urechis caupo and three mudflat organisms including: (b) the scale worm (Hesperonoe adventor); and (c) the pea crab, Scleroplax granulata); and (d) the arrow goby (Clevelandia ios) (after Ricketts and Calvin, 1939).

gradually becomes one of parasitism as the fish consumes the tentacles and then the entire host. In a manner not unlike that practiced by tropical pomacentrids and other reef fishes, stromateoids possess a high resistance to coelenterate toxins, however they are not entirely immune to those venoms (Lane, 1960; Totten, 1960). Haedrich (1967: 47) suggests that “besides the relatively high resistance to the toxins, simple avoidance of the tentacles and the characteristic heavy coating of slime probably are important in allowing the fishes to swim with impunity under their hosts.” California stromateoids known to cohabit (at some time in their life) with scyphomedusae and siphonophores include the medusafish (Icichthys lockingtoni, family Centrolophidae), which when young are often found swimming in association with medusae (Jordan, 1923), and three stromateids, the bluefin driftfish (Psenes pellucidus), the longfin cigarfish (Cubiceps paradoxus), and the Pacific pompano (Peprilus simillimus), which as juveniles have been collected with purple-striped jellies (Pelagia colorata) (Horn, 1970). Some symbiologists recognize phoresis as a distinct category whereas others treat it as a subcategory of commensalism. I prefer the latter, and include those loose, non-obligatory relationships in which a host provides shelter, support, or transport for one or more other species. Unlike the fishes and jellyfishes described above, metabolic dependency is not involved in phoretic associations. Phoresis defined thusly would include

It was in watching these little fish in the aquarium that we first became acquainted with a habit that is possessed by Clevlandia (sic) and other fishes. If a Clevlandia finds a morsel of food that is too large for it to swallow, with true Tom Sawyerish propensity it carries the piece of food to some crustacean, and, as the latter tears the food to pieces, the fish snatches particles to eat and, at intervals, even snatches the larger piece and attempts to swallow it. . . . We have tested this trait many times by giving Clevlandias pieces of clam meat or fish which were too large for them to swallow. Clevlandias are not at all particular as to what crustaceans they put to work. We have watched Clevlandias in a burrow with Urechis, Upogebia, or Callianassa carry meat to a pea crab (Scleroplax or Pinnixa), and those in an open aquarium to such shrimps as Spirotocaris or Crago. The unsuspecting shrimps are only too glad to get the morsel of meat, but the Clevlandia watches and waits and sees that the shrimps do not get all of it. . . . Such activities as this emphasize the interrelationships of animals and how they are built up during evolutionary time.

While the symbiotic relations of most commensal gobiids are facultative, those between the blind goby (Typhlogobius californiensis) and the ghost shrimp (Neotrypaea biffari, previously Callianassa affinis) are obligatory (fig. 21-6). Pairs of adult blind gobies are always found in Neotrypaea biffari burrows (although the shrimp may be found without gobies). They are largely confined to the intertidal flats along the open coast where boulders and rocks are large enough to remain in place despite surf or tidal action. The burrows are within the sand interstices and beneath the rocks and are essentially permanent. MacGinitie (1939, summarized in MacGinitie and MacGinitie, 1949) described the natural history of the pairs and performed a series of experiments to examine the relationship. There is no apparent benefit to the partner other than shared refuge, unlike tropical shrimp/goby pairings

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F I G U R E 21-6 Depiction of the

obligate commensal relationship between the California blind goby (Typhlogobius californiensis) and the ghost shrimp (Neotrypaea biffari, previously Callianassa affinis).

wherein the fish acts as a sentry to the industrious burrowing shrimp. The adaptations of Typhlogobius are extreme such that the sighted larvae soon lose their vision through the growth of tissue over their eyes and their skin is unpigmented and scaleless. The pink coloration of the goby’s skin illustrates its role in aerial respiration; nearly anoxic conditions are reached at low tide and Typhlogobius has achieved respiratory compensation in the extreme (Congleton, 1974). Several other California gobies occupy shrimp, crab, and worm burrows, but none have evolved a commensalism as obligatory as that of the blind goby. Although no symbiotic associations of damselfishes and anemones are known from temperate waters, an intriguing facultative commensalism has arisen involving the painted

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greenling (Oxylebius pictus, family Hexagrammidae) and two sea anemones, Utricina lofotensis and U. piscivora (family Actiniidae) (fig. 21-7). Young Oxylebius associate with these anemones from southern California to British Columbia, taking refuge within the anemone’s tentacles in a manner much like the obligatory relationships of tropical Indo-Pacific anemonefishes and certain anemones (Fautin, 1991) or the facultative associations of various tropical Caribbean reef fishes and anemones (Hanlon et al. 1983). This symbiotic relationship was first reported by Herald (1972) and carefully described and experimentally demonstrated by Elliott (1992). Elliott found that the painted greenling of Vancouver Island could swim and rest unharmed among the tentacles of the large anemones. This occurred most often at night where fish

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F I G U R E 21-7 Adult painted greenling (Oxylebius pictus), ca. 15 cm

total length, upon a white-spotted rose anemone (Utricina lofotensis). (Photo courtesy of Steinhart Aquarium.)

and anemone densities were high. With increasing size, the fish became less dependant upon the anemone for shelter; however the abundance of copepods upon the anemone’s surface provided prey for young fish and older fish fed around the anemones’ bases. The fish are apparently protected from the stinging tentacles by a compound within the fish’s epidermal mucous coating. Elliott was unable to demonstrate any benefit to the anemone from the fish’s presence and therefore considered the symbiosis to be one of facultative commensalism. The survival value of schooling behavior, as a means of avoiding or reducing predation is well documented (see review by Hobson, 1978). Terrestrial ethologists suggest that bird flocks are similar to fish schools and extend those benefits through special adaptations, colorations, and visual signal patterns which promote the formation of mixed species flocks. Moynihan (1968) proposed the term “social mimicry” for this activity and predicted that the study of fishes would demonstrate the same phenomenon. Randall and McCosker (1993) showed him to be correct and provided examples of tropical anthiines, a pomacentrid, and a blenniid that are remarkably similar in coloration and appearance and school together for mutual protection. Such social mimicry can be categorized as a commensal relationship and can probably be demonstrated to occur in California coastal waters. Likely candidates include mixed schools of juvenile rockfishes (Sebastes spp., family Scorpaenidae) and juvenile and adult surfperches (family Embiotocidae), and deserve further study.

Parasitism As stated above, many symbionts that benefit from mutualistic or commensal relationships become predators or prey to the same partner under different circumstances. And, if one broadly defines parasitism to include the behavior of piscivorous fishes, then the vast majority of California fishes are gustatory parasites. I will not deal with that strained assumption in this chapter, but will instead describe the fascinating parasitic behavior of the cookiecutter shark and the relationship of lampreys and their salmonid prey (fig. 21-8). The parasitic activity of the cookiecutter or cigar shark (fig. 21-8a) was first uncovered by the clever detective work of Everet Jones. Billiard ball-sized crater wounds had been

F I G U R E 21-8 Examples of ectoparasitic fishes occurring off the

Californias: a) the cookiecutter or cigar shark (Isistius brasiliensis) and b) Pacific lamprey (Lampetra tridentata).

observed on a variety of creatures such as beaked whales, baleen whales, sperm whales, porpoises, a variety of pelagic fishes and even a nuclear submarine (Jones, 1971; Johnson, 1978). Jones convincingly demonstrated that a small squalid shark, Isistius brasiliensis, inflicted the wounds. It is a facultative ectoparasite whose dentition, suctorial lips, and modified pharynx allow it to attach to the side of large prey, drive its saw-like lower jaw teeth into the skin and flesh of its victim, rotate its body and cut a conical plug of flesh, and then pull itself free with the plug cradled by its scoop-like lower jaw and held by the hook-like upper jaw teeth. LeBoeuf et al. (1987) reported on parasitic attacks by Isistius brasiliensis on northern elephant seals (Mirounga angustirostris) at Guadalupe Island, Baja California, and at Año Nuevo Island, California. I have subsequently observed recently attacked Mirounga at southwest Farallon Island, California, and fresh scars on a harbor porpoise (Phocoena phocoena) from China Beach, San Francisco Bay. Isistius brasiliensis is an epipelagic to bathypelagic species (and occasionally seen at the surface at night) that is known from all tropical oceans, however it is probably uncommon off the California coasts. Lampreys, family Petromyzontidae, are well-known as parasitic fishes largely as a result of the havoc that the Atlantic sea lamprey (Petromyzon marinus) inflicted upon the large resident fishes once the Welland Canal allowed their entry into the Great Lakes. Many nonpredatory lampreys have evolved from predatory ancestors, and both are significant prey items for bony fishes. In California waters, their abundance has been dramatically reduced and only one of the four California species is truly predatory. The Pacific lamprey (Lampetra tridentata; fig. 21-8b) is the largest of California lampreys and,

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with the exception of landlocked populations, spends the predatory phase of its life history in the ocean. Moyle (1976: 90) states, “Little is known about their oceanic life except that they attack a wide variety of large fishes, occasionally even taking on whales. Despite far-flung ocean distribution records, it is unlikely that Pacific lampreys normally wander far from the mouths of their home spawning streams, since their prey is most abundant in estuaries and other coastal areas. The oceanic phase presumably lasts one to two years, like that of the eastern sea lamprey (Petromyzon marinus).”

Acknowledgments I dedicate this paper to John S. Stephens, Jr., mentor and friend, who introduced me to diving in California. In my career, I have been fortunate to have been underwater throughout the world’s oceans, but have made but a few hundred dives in California. For that reason, I have depended primarily on the work of others in writing this review, and am indebted to Edmund Hobson, George Losey, and Alexandra Grutter for the fine works that they have published. As well, I wish to thank Greg Jensen, Harald Ahnelt, and W. Linn Montgomery for their advice, Ted Hobson and the Steinhart Aquarium for the use of their photographs, George Losey, John E. Randall, and Ted Hobson for reviewing this manuscript, and Larry G. Allen for inviting this contribution.

Literature Cited Bray, R.N., and A.W. Ebeling. 1975. Food, activity, and habitat of three “picker-type” microcarnivorous fishes in the kelp forests off Santa Barbara, California. Fish Bull. 73(4):815–829. Cheng, T.C. 1967. Marine molluscs as hosts for symbioses. Adv. Mar. Biol. 5:1–424. Congleton, J. L. 1974. The respiratory response to asphyxia of Typhlogobius californiensis (Teleostei: Gobiidae) and some related gobies. Biol. Bull. 146:186–205. Coyer, J.A. 1980. Possible cleaning behavior by a juvenile California sheephead, Semicossyphus pulcher (Labridae). Bull. So. Calif. Acad. Sci. 79(3):125–126. Cushman, J.H., and A.J. Beattie. 1991. Mutualisms: assessing the benefits to hosts and visitors. Trends Ecol. Evol. 6:193–195. De Bary, A. 1879. Dei Erscheinung der Symbiose. Verlag von Karl J. Trübner, Strassburg. (not seen.) DeMartini, E.E., and J.A. Coyer. 1981. Cleaning and scale-eating in juveniles of the kyphosid fishes, Hermosilla azurea and Girella nigricans. Copeia 1981(4):785–789. DeWet-Olsen, K., and M. Love. 2001. Observations of cleaning behavior by giant kelpfish, Heterostichus rostratus, island kelpfish, Alloclinus holderi, bluebanded goby, Lythrypnus dalli, and kelp bass, Paralabrax clathratus, on giant sea bass, Stereolepis gigas. California Fish and Game 87(3):87–92. Elliott, J. 1992. The role of sea anemones as refuges and feeding habitats for the temperate fish Oxylebius pictus. Environ. Biol. Fishes 35:381–400. Fautin, D.G. 1991. The anemonefish symbiosis: what is known and what is not. Symbiosis 10:23–46. Feder, H. M. 1966. Cleaning symbiosis in the marine environment. pp. 327–380 In Symbiosis. Vol. 1. S.M. Henry (ed.). Academic Press. NY. Fishelson, L., W.L. Montgomery, and A.A. Myrberg, Jr. 1985. A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: Teleostei) from the Red Sea. Science 229:49–51. Fisher, W.K., and G.E. MacGinitie. 1928. The natural history of an echiuroid worm. Ann. Mag. Nat. Hist. 10(1):204–213. Goff, L. J. 1982. Symbiosis and parasitism: another viewpoint. BioScience 32(4):255–256.

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Gorlich, D.L., P.D. Atkins, and G.S. Losey, Jr. 1978. Cleaning stations as water holes, garbage dumps, and sites for the evolution of reciprocal altruism. Amer. Nat. 112:341–353. Gotshall, D.W. 1961. Observations on a die-off of molas (Mola mola) in Monterey Bay. Calif. Fish Game 47(4):339–341. ———. 1967. Cleaning symbiosis in Monterey Bay, California. Calif. Fish Game 53(2):125–126. Grutter, A.S. 1997. Effect of the removal of cleaner fish on the abundance and species composition of reef fish. Oecologia 111:137–143. ———. 1999. Cleaner fish really do clean. Nature 398:672–673. Haedrich, R.L. 1967. The stromateoid fishes: systematics and a classification. Bull. Mus. Comp. Zool. 135(2):31–139. Hanlon, R.T., R.F. Hixon, and D.G. Smith. 1983. Behavioral associations of seven West Indian reef fishes with sea anemones at Bonaire, Netherlands Antilles. Bull. Mar. Sci. 33:928–934. Haygood, M.G. 1993. Light organ symbioses in fishes. Crit. Rev. Microbio. 19(4):191–216. Henry, S.M. 1966. Foreword. pp. ix-xi in Symbiosis. Vol. 1. Ed. by S.M. Henry(ed.). Academic Press. NY. Herald, E.S. 1972. Fishes of North America. Doubleday, New York. 254 pp. Hertig, M., W.H. Taliaferro, and B. Schwartz. 1937. Report of the Committee on Terminology (American Society of Parasitologists). J. Parasitol. 23:325–329. Hixon, M.A. 1979. The halfmoon, Medialuna californiensis, as a cleaner fish. Calif. Fish Game 65(2):117–118. Hobson, E.S. 1971. Cleaning symbiosis among California inshore fishes. Fishery Bull. 69(3):491–523. ———. 1976. The rock wrasse, Halichoeres semicinctus, as a cleaner fish. Calif. Fish and Game 62(1):73–78. ———. 1978. Aggregating as a defense against predators in aquatic and terrestrial environments. pp. 219– 234 in Contrasts in Behavior. E.S. Reese and F.J. Lighter(eds.). John Wiley & Sons. Horn, M.H. 1970. Systematics and biology of the stromateid fishes of the genus Peprilus. Bull. Mus. Comp. Zool. 140(5):165–261. ———. 1992. Herbivorous fishes: feeding and digestive mechanisms. pp. 339–362. In: Plant-Animal Interactions in the Marine Benthos. D.M. John, S.J. Hawkins, and J.H. Price (eds.). Systematics Assoc. Spec. Vol. 46, Clarendon Press, Oxford. Johnson, C.S. 1978. Sea creatures and the problem of equipment damage. U.S. Naval. Inst. Proc., pp. 106–107. Jones, E.C. 1971. Isistius brasiliensis, a squaloid shark, the probable cause of crater wounds on fishes and cetaceans. Fishery Bull. 69:791–798. Jordan, D.S. 1923. Note on Icichthys lockingtoni Jordan and Gilbert, a pelagic fish from California. Proc. U.S. Nat. Mus. 63(4):1–3. King, B. 1978. Feeding behaviour of gulls in association with seal and Sun Fish. Bristol Ornithol. 11:33. Kvenseth, P.G. 1996. Large-scale use of wrasse to control sea lice and net fouling in salmon farms in Norway. pp. 196–203 in Wrasse biology and use in aquaculture. M.D.J. Sayer, J.W. Treasurer, and M.J. Costello (eds.). Oxford, Blackwell. Lane, C.E. 1960. The Portuguese man-of-war. Sci. Amer. 202(3):158–168. Lea, R.N., and R.H. Rosenblatt. 2000. Observations on fishes associated with the 1997–1998 El Niño off California. CalCOFI Rep. 41: 117–129. LeBoeuf, B.J., J.E. McCosker, and J. Hewitt. 1987. Crater wounds on Northern Elephant Seals: the Cookiecutter Shark strikes again. Fishery Bull. 85(2):387–392. Lewin, R.A. 1982. Symbiosis and parasitism—definitions and evaluations. BioScience 32(4):254, 256–260. Limbaugh, C. 1955. Fish life in the kelp beds and the effects of kelp harvesting. Univ. Calif. Inst. Mar. Res., IMR Ref. 55-9:1–156. ———. 1961. Cleaning symbiosis. Sci. Amer. 205:42–49. Limbaugh, C., H. Pederson, and F.A. Chace, Jr. 1961. Shrimps that clean fishes. Bull. Mar. Sci. 11(2):237–257. Losey, G.S., Jr. 1972. The ecological importance of cleaning symbiosis. Copeia 1972:820–833. ———. 1979. Proximate causal factors in cleaning symbiosis: host behavior. Anim. Behav. 27:669–685. ———. 1987. Cleaning symbiosis. Symbiosis 4:229–258. Losey, G.S., A.S. Grutter, G. Rosenquist, J.L. Mahon, and J.P. Zamzow. 1999. Cleaning symbiosis: a review. pp. 379–395. In: Behaviour and conservation of littoral fishes. Almada, U.C., R.F. Oliveria, and E.J. Gonçalves (eds.), I.S.P.A., Lisboa, Portugal. Love, M. 1996. Probably more than you want to know about the fishes of the Pacific coast. 2nd edition. Really Big Press, Santa Barbara. 381 pp.

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MacGinitie, G.E. 1939. The natural history of the blind goby, Typhlogobius californiensis Steindachner. Amer. Midland Natur. 21:489–505. MacGinitie, G.E., and N. MacGinitie. 1949. Natural history of marine animals. McGraw-Hill Book Co., NY. 473 pp. Mansueti, R.J. 1963. Symbiotic behavior between small fishes and jellyfishes, with new data on that between the stromateid, Peprilus alepidotus, and the scyphomedusa, Chrysaora quinquecirrha. Copeia 1963(1):40–80. McCosker, J.E. 1977. Flashlight Fishes. Sci. Amer. 236(3):106–114. McCosker, J.E., and R.H. Rosenblatt. 1987. Notes on the biology, taxonomy, and distribution of flashlight fishes (Beryciformes: Anomalopidae). Japan. J. Ichthyology 34(2):157–164. Moyle, P.B. 1976. Inland fishes of California. University of California. Press, Berkeley. 405 pp. Moynihan, M. 1968. Social mimicry; character convergence versus character displacement. Evol. 22(2):315–331. Nealson, K.H., and J.W. Hastings. 1979. Bacterial bioluminescence: its control and ecological significance. Microbio. Rev. 43(4):496–518. Paine, R.T. 1966. Food web complexity and species diversity. Amer. Natur. 100:65–75. Poulin, R., and A.S. Grutter. 1996. Cleaning symbioses: proximate and adaptive explanations. BioScience 46(7):512–517. Poulin, R., and W.L. Vickery. 1995. Cleaning symbiosis as an evolutionary game: to cheat or not to cheat? J. Theoretical Biol. 175:63–70.

Randall, J.E., and J.E. McCosker. 1993. Social mimicry in fishes. Revue fr. Aquariol. 20(1):5–8. Robins, C.R., R.M. Bailey, C.E. Bond, J.R. Brooker, E.A. Lachner, R.N. Lea, and W.B. Scott. 1991. A list of common and scientific names of fishes from the United States and Canada (fifth edition). Amer. Fisher. Soc., Spec. Pub. 20. 183 pp. Sikkel, P.C. 1986. Intraspecific cleaning by juvenile salema, Xenestius (sic.) californiensis (Pisces: Haemulidae). Calif. Fish Game 72(3): 170–172. Starr, M.P. 1975. A generalized scheme for classifying organismic associations. Symp. Soc. Exp. Biol. 29:1–20. Strasburg, D.W. 1964. Further notes on the identification and biology of echeneid fishes. Pacific Sci. 18:51–57. Tibby, R.B. 1936. Notes on the ocean sunfish, Mola mola. Calif. Fish Game 22(1):49–50. Totten, A.K. 1960. Studies on Physalia physalis (L.). Part 1. Natural history and morphology. Discovery Rep. 30:301–367. Trivers, R.L. 1971. The evolution of reciprocal altruism. Quart. Rev. Biol. 46:35–57. Turner, C.H., E.E. Ebert, and R.R. Given. 1969. Man-made reef ecology. Calif. Dept. Fish Game, Fish Bull. 146. 221 pp. Youngbluth, M.J. 1968. Aspects of the ecology and ethology of the cleaning fish Labroides phthirophagus Randall. Z. Tierpsychol. 25: 915–932.

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CHAPTER 22

Subsistence, Commercial, and Recreational Fisheries M I LTO N S. LOVE

Introduction The marine fisheries of California extend back thousands of years and encompass many dozens of species. This chapter describes the broad trends in these fisheries from the time of the first aboriginal fishermen to the present day. We can only paint with a broad brush and we will leave the mass of catch statistics and other detailed analyses for such technical works as Leet et al. (2001). It is important to note that over the years landings in both the recreational and commercial fisheries have been quite volatile. As noted by Thomson (2001), “Landings tend to increase with stock abundance, as fish are easier and less costly to locate and harvest when they are at higher levels of abundance. The availability of some species on local fishing grounds may vary across seasons or years, depending on ocean temperature and environmental factors. Weather conditions and economic circumstances (market demand and prices) may discourage or encourage fishing activity. Fishing behavior is also affected by regulatory restrictions.” Along with overfishing, which has occurred on many occasions in California’s history, perhaps the most important factor determining fish abundances is the cycle of alternating warm and cold ocean temperature regimes that occur off the coast. The warm phase brings with it large numbers of warmtemperate or even tropical species, such as Pacific sardines, Pacific mackerel, Pacific barracuda, yellowtail, and white seabass. During this phase, many of these fishes are found further north than during colder periods. For instance, during a warm water period in the eighteenth century, fishermen in San Francisco Bay caught large numbers of white seabass; while Pacific barracuda were very common in the Monterey Bay catch. These species are rare north of southern California during coldwater periods. Colder water periods appear to be marked by increased reproductive success of many species of rockfishes, lingcod, and other temperate forms (MacCall, 1996).

Subsistence Fishing Humans have lived along much of the California coast for 10,000 years and there is evidence that some occupation

occurred during the late Pleistocene, at least 12,000 years before the present (BP) (Erlandson et al., 1996; Rick, 1999). Many of these early subsistence communities utilized an extremely wide range of marine and terrestrial animals and plants. And while these earliest settlers captured fishes as part of their diet, shellfish were usually more important (Erlandson, 1991, 1994; Warren, 1968). However, it is clear that there was a great deal of variability in the food habits of the first California residents. For instance, fishes contributed 50–65% (edible meat) to the diets of the inhabitants of Daisy Cave, San Miguel Island, a site dated to at least 12,000 BP (Rick, 1999). Fish species central to the diets of coastal peoples varied with location. Most often, fishermen focussed on whatever species were abundant and readily captured with existing technology. Native Americans living on the open coast of northern and central California concentrated on intertidal and nearshore rocky reef fishes and shellfishes, primarily rockfishes, lingcod, cabezon, kelp greenling, and monkeyface eels, as Native Americans living on these wave-swept coasts did not fish far from shore. Various surfperches and such schooling nearshore species as Pacific herring were also locally important (Gobalet and Jones, 1995; Schwaderer, 1992). Inhabitants of relatively sheltered areas, such as Morro Bay and Elkhorn Slough, concentrated on small schooling species, such as Pacific herring, Pacific sardine, northern anchovy, starry flounder, and various silversides (Gobalet and Jones, 1995). Those peoples living inside San Francisco Bay caught large numbers of sturgeon and salmon, as well as a wide range of other bay and estuarine fishes (Gobalet, 1990, 1994). At least one researcher believes that the first evidence for overfishing in California comes from the middens of the peoples living around San Francisco Bay. In these kitchen waste disposal sites once-abundant sturgeon remains were later replaced by sharks and bat rays (Broughton, 1997). Wave height becomes smaller south of Point Conception, as the coastline becomes south facing and the northern Channel Islands shelter the mainland. In response, the inhabitants of the southern California Bight utilized watercraft to a much greater extent than did those peoples living further north. A number of the Channel Islands were well occupied and

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there was a very active trade between the mainland and the islands. However, as with groups further north, nearshore fishes predominated in the catches of the southern California peoples. Over reefs, sheephead were particularly important, as were rockfishes, kelp bass, cabezon, lingcod, and surfperches. Sardines, grunion, white croaker, California halibut, leopard sharks, shovelnose guitarfish, and bat rays were among the most common species captured from sandy areas. Quasipelagic or highly migratory species, such as bonito, barracuda, Pacific mackerel, and yellowtail were also commonly taken. Large pelagic species such as albacore, yellowfin and bluefin tunas and swordfish, are rarely found in the middens of these peoples (Salls, 1988, 1989; Rick, 1999). The earliest California inhabitants fished with gorges (objects, such as a piece of bone attached in the middle of a line, that were easy to swallow but difficult to eject), spears and perhaps primitive nets. However, several technological advances led to greater use of fishes by these peoples. As early as 3,300 BP, shell hooks (made from abalone, mussels, and other invertebrates) were developed and eventually these became truly elegant circle hooks, complete with barbs and flanges for line attachment (Raab et al., 1995, Strudwick, 1986). The use of hooks often led to major increases in fishing effort (Glassow, 1993; Erlandson, 1994; Raab et al., 1995; Rick, 1999). By about 1,500 BP, relatively seaworthy plank canoes were in use in southern California and this greatly expanded the range and location of fishing activities (Arnold, 1995). In general, the importance of fishes to the diets of coastal peoples increased with time. It is likely that a major factor driving this trend was an increase in population that lead to decreases in the availability of shellfish and other resources. This was coupled with the development of new fishing technologies that increased the ability of native peoples to catch fishes. In particular, around 1,000 BP the density of fish bones in middens, particularly those on the Channel Islands, increased exponentially. This massive increase in fishing appears to have occurred during a relatively cold and dry period, when ocean productivity was high and terrestrial resources scarce (Kennett and Kennett, 2000). In many locations, fishes became the most important source of protein. Fishes were often transported well away from the coast, at least as far as 50 miles inland (Gobalet, 1992). By the Spanish Period, the Chumash along the Santa Barbara Channel and the peoples on the southern California Channel Islands intensively fished nearshore waters. Fishing was also important to groups to the north and south, although they had more mixed economies. In 1770, Miguel Costanso, a member of the Portola expedition to California, wrote of the Chumash, “They know all the arts of fishing and fish abound along their coast” (King, 1990). Indeed, many of the explorers of that time commented on the importance that fishes played in diets of California coastal Native Americans and on the many ways that fishes were captured. These included sophisticated hooks and line, harpoons, various types of nets and relatively seaworthy vessels. All of these allowed for the catch of a very wide range of fish species, although nearshore fishes (found in kelp beds and over shallow reefs and in calmer sandy and muddy areas) predominated. Tragically, the convulsive effects of the Spanish and later Mexican occupation of California, particularly the removal of Native Americans to missions, destroyed this civilization and its way of life.

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Commercial Fishing While both the federal and state governments took some interest in commercial fisheries as early as 1872, monthly reports by wholesale dealers to the state did not begin until 1911 and were not universal until 1917. Until the 1920s, most fishing trips lasted only one day and the landing data from a port fairly accurately reflected the general location of each catch. By the 1920s, local depletion of fishery resources caused fishermen to build larger vessels capable of carrying ice and this allowed for trips to distant fishing grounds. In response, the Department of Fish and Game adopted a system of numbered blocks throughout California marine waters in 1933, each 20 miles on a side, in order to more precisely record the locality of each catch (Scofield, 1954). This block system is still in use today. It should be noted that fishermen are responsible for declaring the location (block) of their catches and it has long been clear that, to protect their favorite fishing locations, fishermen may give misleading block information regarding catch locations.

1850 to 1899 It is not clear when commercial fishing began in California. Certainly, early explorers bartered for fishes with Native American fishermen (Menzies, 1924). However, we know very little about California fisheries in the period between the fall of the missions (about 1834) and the Gold Rush. During this period, California was very sparsely populated and most fishing was probably for subsistence by surviving Native Americans and the local Californios (those inhabitants of Spanish and Mexican heritage). The beginnings of commercial fishing occurred with the first flood of immigrants just prior to and during the Gold Rush. Gold was discovered in 1848 and within 2 years, tens of thousands of gold seekers had made their way to San Francisco. While many of these immigrants left for the gold fields, thousands of other stayed and worked in the city, making it by far the largest settlement in California. Indeed, until the late nineteenth century, San Francisco, and to a much lesser extent Monterey and San Diego, were the only coastal population centers and almost all commercial fisheries centered on these three ports. By 1880, San Francisco handled more fishes than all the other ports combined from San Diego to Puget Sound (Scofield, 1954). In 1892, the Bay area accounted for 93% of California’s commercial fishery products (Skinner, 1962). What was the San Francisco commercial fishery like in those early years? The first full-time commercial fishermen were a group of Italians who came to San Francisco in 1848. Fishing out of lateens, small sail boats, they fished for salmon, sturgeon, various flatfishes, silversides, smelts, Pacific herring, and rockfishes using beach seines, hand or set lines (called trawl lines), and gill nets. Virtually all fishing was conducted in the Bay, just outside the Golden Gate and in the Sacramento River (Scofield, 1954). By the 1880s, there had been a marked increase in the region’s fisheries. Vessels routinely fished throughout San Francisco Bay, along the coast from Pt. Reyes to Half Moon Bay and, during calm winter days and throughout the summer, at the Farallon Islands. In addition, fishes were shipped by rail to San Francisco from as far away as Humboldt Bay on the north and San Diego Bay on the south (Jordan, 1887, 1892).

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The first major technological advance in these marine fisheries was the introduction of the paranzella net, a form of bottom trawl developed in Europe. The paranzella was shaped somewhat like a sock, with a line attached to each side of the net opening. It was towed by two vessels sailing a parallel course and was, compared to set lines, gill nets and beach seines, an efficient means of catching large numbers of fishes, particularly soles and flounders, living on muddy or sandy bottom. In 1876, a group of San Francisco fishermen secretly built and experimented with this net and it proved to be extremely cost-effective. Almost immediately, this flood of fish caused wholesale prices to plummet. By 1880, with the San Francisco fishing fleet numbering 85, the 6 paranzella vessels landed a greater volume of fish than all the other vessels combined. A further advancement in efficiency occurred in the mid-1880s, when steam powered fishing vessels replaced sailing ones in the trawl fisheries (Jordan, 1887, Scofield, 1948). The paranzella fishery was one of the first to come under fire for its perceived destructive nature. Competing fishermen did not like it and members of a nascent conservation movement feared it. It was believed that large numbers of fishes were discarded, dead at sea and that very large catches often went to waste for lack of buyers even when landed. In a statement that eerily resonates today, Jordan (1887) pointed out that, “The drag-nets destroy and waste immense quantities of fish, doubtless amounting to several hundred tons per year. Comparatively few of these, however, are immature fish, and the greater part is composed of species unmarketable, either through small size or repulsive appearance. The reason that the other fishermen are so bitterly opposed to the use of these nets is that, by means of them, a few men can bring such quantities of fish to market as greatly to reduce the price . . . Although considered as a temporary method, these nets do but little harm and have as yet probably not materially decreased the amount of fish in the vicinity of San Francisco, there is no doubt that, if continued long enough, they will do so. It is certainly the most wasteful method of fishing I know. The use of such nets should be discontinued altogether, or the nets required to be of such coarse mesh as to allow the small fish to pass through.” While most fishes taken in the San Francisco fishery were sold fresh, a substantial quantity was dried, salted, smoked, or occasionally pickled. However, because fishes were not iced after capture, even during two or three day fishing trips, and because they were mishandled after landing, the quality of “fresh” fish was often poor. Jordan (1892) described the results: “For the market of San Francisco is the poorest to be found in any large seaport in the country . . . We find that in San Francisco the fishes are brought in either from the wharves or express offices in boxes; that they are exposed to open stalls to the dust of the street, or even to the rays of the sun; that before noon a large share of the fishes are rotten; that the fresh fish of one day are mixed with the rotten fishes of the preceding day. In the stalls in Clay Street we can find at any time plenty of fishes whose scales have been dried by the rays of the sun, and whose viscera are swollen by the gas produced by the decay of the contents of the stomachs or of the internal organs themselves.” During the 1870s, the commercial fisheries of Monterey Bay were also on the increase, although they were much smaller than those of San Francisco. Salmon, flatfishes, rockfishes, cabezon, and silversides dominated the catch. Interestingly, barracuda and white seabass were also important, probably evidence of relatively warm ocean waters during that time.

Fishes were taken in the same manner as at San Francisco, except that paranzella nets were not used. Much of the catch was shipped to San Francisco, initially by stage to Salinas and then by rail, and later directly by rail from Monterey. By 1879, 200–800 pounds of fish per day were sent to San Francisco from Monterey. The fishery in San Diego occurred primarily in the bay, where beach seiners concentrated on silversides and flatfishes. There was also a small hook and line fishery on the open coast and these fishermen targeted sheephead, Pacific barracuda, and Pacific bonito. Most fishes were sold fresh or were dried and some were exported to Asia. Of supreme importance for the next century, canneries had begun to pack sardines in both San Francisco and San Pedro. The first fish cannery on the West Coast was built in 1864. It was located near Sacramento and canned chinook salmon caught in the Sacramento River. Canned salmon found a ready domestic market and, in the 1860s, was even exported to Australia. In 1889, the Golden Gate Packing Company built the first cannery on the Pacific Coast devoted solely to marine fishes. It packed anchovies and sardines caught by beach seine in the bay. Due to only sporadic availability of these fishes, the cannery was not a financial success and, in 1893, the cannery moved to San Pedro, in southern California. Here a gasolinepowered vessel using a purse seine, thought to be the first use of this net in California, caught anchovies and Pacific mackerel for the packing house (Smith, 1895; Fry, 1931; Scofield, 1951). Who were these early California fishermen? Virtually all were immigrants. Some of the first were Italian and Portuguese seaman who jumped ship for the Gold Country, then came back to San Francisco to fish. By 1854, Chinese fishermen were encamped in the Bay on the eastern shore of the San Francisco Peninsula, a spot that was to be theirs for decades. About the same time, large numbers of northern Italians, from Genoa and other ports, arrived and set up shop in North Beach. Smaller numbers of Greeks, Slavs and Spaniards also began to arrive. Harsh conditions in Sicily during the 1870s caused many to leave and join the fishing community, although perhaps communities would be the more proper term. Immigrant groups tended to live apart from one another, often plying specific niche fisheries. In San Francisco, for instance, many Chinese concentrated on shrimp, sturgeon and small fishes in the Bay, drying the seafood on the beaches and exporting it to China. Meanwhile, Europeans tended to emphasize flatfishes, salmon, and rockfishes, both inside and outside the Bay. While early fishermen made a good living at the trade, the rise of paranzallas depressed wages and many lived a marginal existence (Jordan, 1887, 1892; Scofield, 1954; Weaver, 1892). At the end of the nineteenth century, fisheries along the California coast were rapidly expanding. In particular, the influx of immigrants to southern California created new markets for fishery products and both San Pedro and San Diego began to be important ports. Salmon (almost all chinook), much of it taken in rivers but increasingly caught in the ocean, was by far the most valuable fishery. Of the strictly marine and estuarine species, flatfishes (particularly English and petrale sole, starry flounder and California halibut), sardines, Pacific herring, striped bass, rockfishes, Pacific barracuda, kelp and sand bass, and white seabass were most important (Wilcox, 1902). Most fishes were sold fresh locally. However, efficient rail service and the advent of inexpensive freezing and icing facilities began to make it possible to ship fresh and fresh-frozen fish from California throughout the United States and even to Europe. Dried and salted fishes of

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many types, but particularly tuna, Pacific barracuda, rockfishes, yellowtail, and the fins of various sharks were also very valuable. Much of this catch was shipped overseas to Asia (Weaver, 1892; Wilcox, 1902; Scofield, 1954; T. Thomas, pers. comm.). By the turn of the century, gill and trammel nets were by far the most commonly used fishing technique, but hook and line (particularly for rockfishes and kelp bed species), paranzella trawls and beach seines were also in common use. Commercial trolling for salmon was just becoming important. Most commercial fishing vessels were wind powered, but steam and gasoline engines were becoming more common in the fleets (Scofield, 1954; Ueber, 1988).

auspices of the Federal Food Administration, Bureau of Fisheries and other agencies and spearheaded by the rather blunt slogan “Eat More Fish,” seafood consumption rapidly increased, peaking in 1918. Several studies were conducted on which species were underutilized and how fish handling and storage could be improved (Starks, 1918a, b). In addition, in the effort to increase landings, a number of fishing regulations were temporarily relaxed. These included allowing the catch and sale of corbina, yellowfin and spotfin croakers, species formerly restricted to recreational anglers, and the catch of small and formerly undersized, California halibut (Anon., 1918a, b; Cobb, 1918). TH E CAN N E RY AN D R E DUCTION F I S H E R I E S

1900 to 1950 The marine fisheries of California experienced rapid growth early in the twentieth century. Within 25 years, led by sardines and tunas, a combination of events dramatically altered a rather sleepy industry into an industrialized giant. The population boom experienced throughout the state, primarily in southern California, helped drive an expanded market for fishes. Between 1900 and 1920, the population of Los Angeles alone went from 170,000 to almost one million and the state grew from 1,500,000 to 3,500,000. In addition, relatively inexpensive energy from newly developed California oil and gas fields made the creation of canneries and reduction plants more economical. As early as 1895, the first gasoline engines were used in San Francisco fishing vessels and by 1899 33 of 82 of these boats were motorized. By 1915, most of the fishing vessels on the California coast were gasoline powered. Trolling with gasoline engines was far more efficient than with sails and trawlers, too, quickly took to the new engines (Scofield, 1956). The increased demand for fish and depletion of local stocks created a need for larger vessels that could carry larger loads and work fishing grounds further from port and improved vessel designs filled this need. At the same time, continuing improvement in transportation allowed fish to be shipped much more inexpensively. As an example, an edition of Pacific Fishermen from 1914 notes that an experimental load of 40,000 pounds of albacore were shipped to Chicago and that frozen fish were being shipped to Australia and New Zealand. The early part of the century also saw the creation of inexpensive ice production, paving the way for multi-day fishing trips that allowed vessels to fish on more distant grounds. It should be noted that well into mid-century ice was not used for many short trips. As an example, Scofield (1947) stated that the rockfish fishermen in Monterey Bay usually made single day runs and that “None of the boats carried ice and all fish were delivered in the round with no cleaning at sea.” Parenthetically, some salmon trollers still do not use ice but they do clean the fish at sea. The first world war had a profound effect on California’s fisheries. Before the war, a few canneries had begun a modest business, packing Pacific sardines, albacore, and other species. When the war halted the North Sea sardine fishery, the California canneries quickly filled the gap, with sardine catches skyrocketing from about 2,000 metric tons in 1915 to 71,000 metric tons in 1918. And while there had been a handful of canneries in California in 1910, by 1919 there were 44. Moreover, after the U.S. entered the war there was a great push to increase fisheries for domestic consumption. Under the

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Historically, many California fish species, including rockfishes, California halibut, and barracuda have been canned and/or reduced for fishmeal and oil.1 However, Pacific sardines and the tunas (albacore, yellowfin, bluefin, skipjack, and Pacific bonito) and to a lesser extent jack mackerel, northern anchovy, Pacific herring, and Pacific mackerel were most important. While all of these species, particularly the tunas, also found a place in fresh fish markets, the vast majority of the catch was purchased by the odiferous plants that lined the wharves of San Francisco, Monterey Bay, Los Angeles-Long Beach Harbor and San Diego. Historically, pelagic wetfish also referred to all of these species, except for the tunas. Pelagic wetfish are packed in cans in a raw state and then cooked, hence the name wetfish. Tunas are first cooked and then packed in the can. While preserving fishes by smoking, salting and drying remained a common practice well into the mid-twentieth century, ultimately the canning and reduction industries were the driving forces behind California’s two largest fishing industries, those for Pacific sardine and the tunas. During the early part of the twentieth century, the development of canneries and reduction plants had the greatest single effect on California fisheries and it is arguable that several coastal communities would hardly exist but for those fishes. Pacific Sardine

Pacific sardines have been a part of California fisheries since prehistoric times. It was only with the rise of the fish canning industry that the fishery took on its overwhelming importance (figs. 22.1a–c). For more than three decades, ending in the late 1940s, the sardine catch dominated the California fishery, exceeding the combined catch of all other fishes. Indeed, for a number of years the fishery was the world’s largest. And the crash, when it came, had devastating and lasting effects on the fisheries of California. It is instructive, and hopefully salutary, to discuss in some detail the meteoric rise and dismal fall of that fishery. The Golden Gate Packing Company of San Francisco was the first sardine cannery on the Pacific Coast, producing canned sardines from 1890 through 1892. But the experiment did not succeed and in the late nineteenth century the machinery was shipped to San Pedro where sardines were 1 I have divided commercial fisheries into two broad categories, cannery and reduction and market, using the designations first coined in the early twentieth century by the California Division (later Department) of Fish and Game. While other terms have some currency, such as finfish for some of the species sold fresh or frozen, I believe these older terms most accurately capture the original use of the various species.

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A

C

B

F I G U R E 22-1 The Pacific sardine fishery off Monterey. (a) Setting lampara net. Photo credit: Maritime Museum of Monterey. (b) Brailing sardines from purse seine onto fishing vessel. Photo credit: Maritime Museum of Monterey. (c) Sardine-laden vessels tied up to cannery dock. Photo credit: Maritime Museum of Monterey.

more consistently abundant. Fishermen first caught these fish using primitive purse seines that were heavy and required large crews to deploy and retrieve. High costs and relatively low catches ensured that these first efforts were not successful and canners soon switched to tuna, canning only small quantities of sardines during the off-season (Thompson, 1921a). Sardine canning did not begin its wild ride until F.E. Booth erected a small shed in Monterey and packed a small amount in 1902. Sardines in the first few years were dried in the sun, placed in cans with hand solder lids and then cooked. For the first few years, because of market preferences, Mr. Booth labeled his cans of larger fish “mackerel” until the federal government requested a move toward veracity. These first fish were taken by gill nets and later by the still inefficient purse seine. In 1905, one of Booth’s fishermen, Pietro Ferrante, suggested using a Mediterranean encircling net called the lampara. Based on Ferrante’s recommendation, in 1905 Booth purchased one from Tangiers, Morocco; this was the first lampara in the United States. Compared to purse seines, lamparas were lighter and could be pulled in by fewer crew members on smaller vessels in a shorter time. The new net was a quick success and it is clear that while the canneries created the sardine industry, the lampara allowed it to flourish. After 1905, sardine fishing in Monterey greatly improved, due to the introduction of this more efficient technology and the evolution of a greater understanding of the behavior of sardines (Scofield, 1951). Southern California fishermen quickly picked up the lampara and for a number of years it was the primary method for catching sardines.

Though a lucrative fishery nearly from its inception, World War I, with its high demands for canned sardines, brought with it a large surge in catches that eventually topped 150,000,000 pounds in 1918. “The sardine industry in California is . . . essentially a product of the great war” (Thompson, 1921a). Although thought to be a remarkable amount at the time, the catch actually more than doubled every six years thereafter, reaching its peak at a billion and a half pounds in 1936. While some of this remarkable expansion was due to a growing demand (both domestic and foreign) for inexpensive canned sardines, far more important were the profits to be made from reducing sardines to oil and meal. In the California fish canning industry, reduction began in 1913 as a way to market the offal from the sardine canneries (Anon., 1914). In the reduction process, waste body parts, such as heads, but also spoiled fish were converted to oil and fishmeal. Sardine oil, in particular, found a ready market in the paint and soap industry, while the fish meal was immediately accepted as chicken feed by the farming community. Within a few years, it was clear to cannery owners that the profit margin for reduced sardines was much higher than that for fish in cans (Scofield, 1938). In fact, for most of this fishery’s life, sardine reduction drove the industry. So profitable was reduction that in the 1920s, when the California Division of Fish and Game prohibited reducing whole sardines, processors responded by placing only a small portion of each fish in a can and reducing most of the animal. As Clark (1949) noted, “As a result canning practically became a by-product of the reduction process.”

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Suspicions and uneasiness regarding the reduction industry had culminated in the State Reduction Act of 1919, prohibiting the use of fish for reduction without written permission from the California Division of Fish and Game (Hughes, 1949). Nonetheless, throughout the 1920s and 1930s, there was continuous pressure to increase the allowable take for reduction purposes. Representatives of that industry approached the California legislature year after year and generally received what they wanted. This occurred despite a clear, and everlouder, series of warnings from biologists of the Division of Fish and Game. Very early in the fishery, scientists were clearly uneasy about the state of the sardine stocks. Commenting in 1921 on the lack of basic biological knowledge on the species and on the great population fluctuations that had occurred in the Atlantic sardine fisheries, DFG biologist W.F. Thompson (1921b) wrote, “So the most ordinary business sense dictates an energetic inquiry into the probability that such great changes will occur in California, and into the chance of foreseeing them.” By 1922, Thompson went further in discussing a number of California fisheries, particularly for sardines, when he stated “If trouble were afar, and it were possible safely to say, ‘Let us overcome that problem when we get to it’, this report would not carry much weight for the ordinary man. But there is every reason to believe that the problem is near at hand. Our fishery has advanced farther than we have perhaps dreamed . . . they have perhaps gone too far.” By the late 1920s, major sardine biologists at DFG were openly convinced that there was good evidence of sardine depletion. “Although the total catch was still rising, it was not doing so in proportion to the expansion in fishing effort. The average age of fish in the catch had declined from ten years to six years. Individual boats were travelling farther from port and spending more time on the water to make their catches. All were classic signs of overfishing; Scofield [N. B.] and Frances Clark recommended an annual limit on the catch between 200,000 and 300,000 tons” (McEvoy, 1986). However, throughout the life of the fishery, and even at its downfall, many in the industry as well as in the legislature clearly believed with Knut Hovden (a major Monterey canner) that “It is absurd for anyone who really knows the facts to say that you can deplete the supply of sardines in the Pacific Ocean.” (Enea, 2000). The greater demand for sardines meant that vessels had to be larger in order for new fishing grounds further from port to be opened up and to allow greater catches to be retained. This signaled the return of the purse seine, always able to catch many more fish than a lampara net and now power (rather than hand) pulled. By 1930, purse seines were again well established in the fishery and by 1940 lampara nets had all but disappeared from the commercial sardine industry (although still used in the lucrative squid fishery). In the 1930–1931 seasons, a new factor was introduced into the mix as floating offshore reduction plants, anchored in federal waters outside state control, began processing sardines into fishmeal and oil. This privately-owned floater was followed in the 1931–1932 season by one owned by a fishermen’s cooperative, an attempt to free themselves of what they considered to be intolerable financial control by canners. Everyone in the business, including those who both reduced and canned, and those who only reduced, lobbied for a continuation and, in fact, an increase in sardine quotas. While arguments were often made in terms of resource conservation, ultimately the arguments were over who should do the reduction. Although, as Davis (2000) notes, “there were likely some owners of small canneries whose profits did not rely on fish-

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meal production and were seriously concerned about conservation.” As the reduction fishery grew and particularly as the Depression took hold, the economics of the industry were too powerful for any regulatory body to withstand. In the mid-1930s, bills were submitted to the U.S. Congress to prohibit offshore reduction and in 1936 congressional hearings were held. Fish and Game biologists repeated in strong terms their consensus that sardines were being overfished and catches had to be reduced. However, their testimony was undermined by U.S. Bureau of Fisheries spokesman Elmer Higgins when he testified that there was “no clear-cut or convincing evidence that will satisfy everyone that the sardine supply is in danger of being seriously depleted.” And he went on to state that “We believe very firmly that restrictions which are unnecessary hamper or restrict legitimate business enterprise.” A colleague added that “to us, conservation means wise use. We do not believe in hoarding our fishery resources, but, rather, believe they should be prosecuted to a degree compatible with the abundance of the species” (McEvoy, 1986). During these same hearings, the sardine industry was divided on ending the offshore reduction industry. Some canners and shoreside reducers favored the bill and, naturally, the offshore industry opposed it. In testimony that now simply resonates with the irony of subsequent events, William Denman testified that those opposed to the huge offshore reduction represented a conspiracy of canners, DFG scientists and recreational anglers. He claimed that sardines reproduced so heavily that any depression of the population would be temporary at most. And, in a statement that modern fishery managers can relate to, he said that for scientists to ignore the beliefs of commercial fishermen, who felt that sardines were abundant, was “the most brutal kind of medieval scholasticism” (McEvoy, 1986). Ultimately, no action was taken. By the late 1930s, Fish and Game biologists were extremely frustrated. An extraordinary article, published anonymously but possibly by Frances Clark, one of the great sardine experts of the twentieth century, says it best when it discusses the unequal battle that Fish and Game scientists waged with commercial fishermen, canners, reducers, their lawyers and the state legislature. Referring to those who made money from the sardine industry, Anon. (1938) writes, “People will go to absurd lengths to defend a premise which they have endorsed after accepted facts and even their own common sense have proved that it is false. . . . Having presented the results of his labors the biologist can not defend them. He must remain in the background as a spectator while lawyers, business men and others question his disinterest, deliberately misinterpret plain statements and befog simple issues with soaring flights of oratory, which admittedly are sometimes much more effective in gaining the end sought than detailed facts and cold logic.” Until the early 1940s, the Fish and Game Commission, ostensibly a guardian of the sardine continued to push for catch reductions while both state and federal legislators caved in to the sardine industries’ demands for higher quotas. In their 1938 report, they note the “unmistakable signs of depletion in the sardine population” and the “imperative need to reduce the harvest.” In 1939 the governor of California replaced all of the members of the Commission and even this token resistance disappeared, as the 1942 report concluded that there was “no reason to be concerned over the possibility of the extermination of the sardine by the fishermen” just “a possibility that if the fishery is carried on too intensively, the population will decline to a point where the success of a fishing season will depend upon the chance occurrence of an

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abundant year-class” (McEvoy, 1986). Thus, the way was clear for whatever was about to happen. Even during this period of immense catches Parrish (2000) notes that the fishery was probably only slightly overfished. The period from the mid-1920s to the mid-1940s saw relatively warm ocean conditions along the Pacific Coast; conditions conducive to successful sardine spawning and the sardine populations were relatively large. Parrish makes the case that the downfall of the fishery ultimately has its roots in World War II and a shift to colder ocean conditions beginning in the mid1940s. As he notes, “In the late 1930s a small group of heroic fishery biologists from the California Department of Fish and Game. . . . was approaching the point where I believe they would have convinced the California Legislature that a 250,000 ton quota should be adopted. I use the term heroic in the old fashioned sense, denoting those who continue to fight even though they have lost every battle they have ever been in.” During World War II, the federal government took over the regulation of the sardine industry and, with the intent of maximizing the amount of canned sardines, ignored the 250,000ton proposal. By the time the California Legislature regained control, and fisheries biologists could inventory the stock, the damage was done. The late 1940s saw the end of the Monterey fishery and the early 1950s saw the demise of the southern California sardine stock. Parrish (2000) notes that overfishing was actually most intense in the late 1950s and early 1960s, long after the sardine had essentially disappeared from central California and when the last remnants of the southern California stock were decimated. Parrish sums up this phase of the sardine story thusly, “The short of it is that the collapse occurred in slow motion and a lot of things went wrong for sardines over an extended period. The primary ingredients were overfishing, a long-term cooling in the California Current, WW II, El Niño and nobody home in the California Legislature.” Several decades of cold ocean water ended in 1976–1977 with the return of a warm water cycle. By the mid-1980s, sardines were once again back in California waters in some numbers. A small fishery was permitted in the late 1980s and it has continued throughout the 1990s. It is interesting to note that, as of 2001, ocean waters appear to be cooling and it remains to be seen what will become of the current relatively robust sardine population. The Tunas

The canned tuna industry paralleled that of the sardine. In 1903, a lack of sardines forced the San Pedro packing plant of A. P. Halfhill to turn to albacore, California halibut, and rockfishes (Clemens and Craig, 1965, quoting Halfhill, 1951). Until then, albacore and other tunas were caught in low numbers either for the fresh fish market or were salted and dried. And albacore, in particular, fetched very low prices. While halibut and rockfish canning did not pan out, albacore proved to be extremely popular and by 1911 a new industry and fishery was born. During these early years, albacore were taken from small vessels manned by three fishermen. After fish were located by trolling, the vessel was brought to a stop and live sardines, anchovies or smelt were thrown over to attract the school. Early on, fish were caught on baited handlines, but this was soon discarded for bait or barbless lures attached by short leaders to bamboo poles (Scofield, 1914). Catches less than one ton were considered poor and those of four to six tons were common. Interestingly, despite an abundance of bluefin tuna, albacore was the only tuna canned in California for a number of

years. However, the increased demand for all fish during World War I led canners to experiment with yellowfin, bluefin, and skipjack tunas. In 1918, when adverse water conditions led to a low albacore catch, purse seiners began to target bluefin off California and later yellowfin and skipjack off Mexico. By 1927, the yellowfin and skipjack catch, made almost entirely off Baja California and Mexico, had surpassed albacore and bluefin landings and this pattern held true until the demise of most canneries in the late twentieth century. Beginning about 1930, larger vessels began to explore further south and by 1934 most fishing occurred off Central America, including the Galapagos Islands. Very little of the yellowfin and skipjack landed at the many canneries of San Diego and Terminal Island were caught inside state waters (Godsil, 1949). The realities of the global market place eventually spelled the end of California tuna canning, as an industry consisting of almost 2,000 fishermen, as well as 6,000 additional cannery workers, boat builders and boatyard personnel, disappeared over a three year period. Bowing to economics, between 1982 and 1984 almost every cannery moved outside the U. S. for the greener pastures of Asia, Puerto Rico, and the South Pacific. Currently, most of the tuna caught in state waters are marketed to the fresh fish trade. Other Pelagic Wetfish

Volatile best expresses the fisheries for Pacific mackerel, jack mackerel, Pacific herring, and northern anchovy during the first half of the twentieth century. In some ways, the Pacific mackerel fishery mirrored that for Pacific sardine (Croker, 1938). Both species are more abundant during warm water cycles and both were overfished to the point of collapse. Until 1927, the Pacific mackerel was a moderately important market fish as sporadic attempts to develop a canned product had been uniformly unsuccessful. In that year, a southern California canner succeeded where others had failed, producing canned mackerel that caught the public’s fancy. The canner first tried marketing the mackerel in the Philippines, at the time a major consumer of sardines and pink salmon. To gain market share, “a ruse was resorted to in order to get the mackerel started . . . Nearly all [cans] bore a picture of a salmon-like fish and the words ‘salmon brand,’ ‘salmon style pack’ were placed in a prominent position. Naturally the buyers thought they were getting a new kind of salmon at a real low price, so sales mounted rapidly” (Croker, 1933). Pacific mackerel remained a major fishery throughout the first half of the twentieth century, ultimately crashing in the mid-1960s (Konno and Wolf, 1992). Until 1947, jack mackerel were a very minor part of the California commercial fishery. It was sold fresh or, if canned, was exported. The collapse of the sardine fishery in the 1947–1948 season led fishermen to seek out and canners to purchase large quantities of, as it was called at the time, “horse mackerel.” Clearly, this name would not appeal to domestic consumers and the California Division of Fish and Game proposed the name “jack mackerel” and this was made official in 1948. Until the collapse of the Pacific sardine fishery, the northern anchovy formed a very minor commercial fishery. Except for the period 1916–1921, when reduction was permitted, much of the catch was preserved for bait. Beginning in the late 1940s, the catch drastically increased as canneries switched to the more abundant anchovy. With a relatively few years, catches declined as the market for canned product was small (Phillips, 1949; Jacobson, 1992).

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During this period, Pacific herring catches mirrored those of northern anchovy. A large reduction fishery during World War 1 ended in 1921 with the State Reduction Act, prohibiting the use of fish for reduction purposes without written permission from the California Division of Fish and Game. Catches remained low for most of the rest of the period and most of the harvest was used for bait. As with northern anchovies and jack mackerel, catches surged in the late 1940s, as attempts were made to replace the declining sardine stock. Ultimately, herring proved to be a poor substitute and catches declined within a decade (Hughes, 1949; Spratt, 1992). TH E MAR K ET F I S H E R I E S

Market fishes are those that are sold fresh or, starting in the mid-1940s, frozen or thawed after being frozen. In the California fisheries, this includes at least 60 species. The fresh (and later frozen) fish preferences of Californians during the first half of the twentieth century were very similar to those of nineteenth century consumers. This very limited set of preferences, particularly when compared to citizens of most other countries, was noted by Starks (1918b) who lamented the small number of species that found favor in the California fish markets. As an example, Starks wondered why Pacific herring found such a poor reception in California, when European fishermen relentlessly pursued a very similar species and exported it to California in large quantity. “The 1924 Commercial Catch of Fish in California” (Scofield, 1925), reported that the most popular market species were flatfishes (primarily English sole, petrale sole, Pacific sanddab, starry flounder, and California halibut), salmon, Pacific barracuda, rockfishes, and white seabass. In general, these were to be the perennial favorites for the first half of the twentieth century. Almost 25 years later (1947), sole (of the same species as noted above), salmon, rockfishes, Pacific barracuda, lingcod, California halibut, and white seabass were the most important market fishes (Bureau of Marine Fisheries, 1949). It should be noted that yellowtail were both marketed fresh and were also canned. A number of species, particularly yellowtail, but also Pacific bonito, Pacific mackerel, and jack mackerel, enjoyed some popularity in fish markets, but most of the catch was canned. Canning of yellowtail was particularly large during years of high abundance and low wholesale price (Greenhood, 1949). And while there was always a market for many of the other species inhabiting California waters, such as surfperches, sablefish, sheephead, white croaker, smelts, silversides, cabezon, and even tunas and swordfish, they played a relatively minor role and, with the exception of tunas (including Pacific bonito) were most often a bycatch of other targeted fisheries. Only one major market fish fishery began during this period. For decades, Dover sole had been a substantial part of the trawl catch, particularly in northern and central California. However, because Dover sole flesh is very soft, there was little demand for this species and almost all of the catch was discarded at sea. The rise of the balloon trawl fishery for rockfishes (see Fishing Techniques section) and the subsequent creation of the quick-frozen fillet industry opened the way for marketing this species, as it was discovered that freezing the fillets hardens the flesh. Dover sole catches rapidly expanded from 28 tons in 1943 to 3,600 tons in 1948. Sharks, skates, and rays also comprised a minor fishery, symptomatic of a widespread prejudice on the part of many

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Californians. A small market did exist for skates, taken as bycatch in many fisheries; these were purchased almost entirely by persons who had emigrated from Asia and Western Europe. There was also a substantial trade for shark fins, most of them were shipped to Asia. Shark meat, particularly from soupfin, shortfin mako, sevengill, and thresher sharks, was widely passed off as other species, as noted by Ripley (1949), “The fact that shark fillets are used for human consumption is unknown to the consuming public in many cases. Shark has been commonly substituted for other species of fish such as the California and Pacific halibut, white sea bass [sic], barracuda, sole, rockfish, etc. [sic] and even salmon. During the summer of 1944 the author observed soupfin shark fillets purvey in a Long Beach restaurant as white sea bass, California halibut, barracuda and salmon. Upon questioning, the owner of the establishment admitted that the fillets sold for salmon had been treated with food coloring to simulate the color of salmon tissue.” A brief, but intense, fishery for soupfin sharks and later spiny dogfish occurred in the late 1930s. In 1937, a new market for soupfin sharks suddenly developed with the discovery that their livers had unusually high levels of vitamin A. At that time vitamin A could not be synthesized, and, as the onset of World War II ended the traditional sources from North Atlantic fisheries, a shark liver gold rush ensued. Within two years, 600 vessels, from large Alaskan set liners to small local gillnetters, were working the California coast. Starting at about $40 per ton, livers rose in value to $2,000 per ton in 1941. Within a few years, the fishery had overfished the sharks and the vitamin industry began importing vitamin A fish oils from Mexico and South America (Ripley, 1946). Fishing Techniques

Just as fish preferences did not appreciably change between the nineteenth and early twentieth centuries, fish harvesting methods also were very similar, although a number of technological improvements made them far more efficient. In the nineteenth century, trolling was a minor part of the commercial fishery. Jordan (1887) noted that a small-scale troll fishery in southern California caught barracuda, yellowtail, Pacific bonito, and other surface-dwellers (fig. 22-2). Interestingly, during these years commercial fishermen did not know that salmon could be caught in the open ocean in large quantities and they focussed their attention in the major rivers and in San Francisco Bay. This was despite a very popular recreational troll fishery for king and silver salmon conducted each summer in Monterey Bay. This changed drastically in 1901, with the commercial development of ‘mildcuring,’ a process of salting and brining salmon that made it possible to store large quantities of fish. By 1904, there were 175 sailing vessels trolling for salmon in Monterey Bay. With the rise of dependable gasoline engines, trolling became a major part of the state’s salmon fishing industry and by 1916 salmon trollers were found throughout northern and central California. By the early 1930s, two-thirds of the salmon catch was made in the ocean and most of the river fishery had disappeared. It was estimated that in 1947 more than 1,100 commercial vessels trolled for salmon (and over 5,000 by 1983). Early in the century, trolling also became a major factor in the albacore fishery. Although most of the fish were taken by barbless lures or bait attached by leaders to poles, the tuna were first located through trolling (Fry, 1949; Scofield, 1956).

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F I G U R E 22-2 A troller lands a Pacific barracuda. Photo credit: Ed Ries Collection.

The roundhaul nets, primarily lampara and purse seine, were widely used throughout the first half of the twentieth century. While they were virtually the sole technique for capturing Pacific sardines and northern anchovies, they were also very important in fisheries for other schooling species, such as the tunas, Pacific mackerel, jack mackerel, white croaker, and, until prohibited in 1941, California barracuda, yellowtail, and white seabass. Early purse seines were cumbersome to set and retrieve and required both a large vessel and crew. For this reason, for the first few decades of the new century, the smaller, but lighter and more user-friendly, lampara net was the net of choice. As larger vessels were built, as the demand for Pacific sardines, Pacific mackerel and other pelagic species increased and as net design improved, purse seines reclaimed most of these fisheries. By the end of the 1940s, lampara nets were used mainly to catch live bait for the recreational fishing industry and in the Monterey Bay squid fishery (Scofield, 1951). Trawl fishing was a major fishing method throughout this period. From the 1870s until the 1930s, two-vessel paranzella nets supplied millions of pounds of flatfishes (primarily English, petrale and rex sole, Pacific sanddab, and California halibut), sablefish, various rockfishes, and lingcod to fish markets around the state. Until the late 1940s, most of the product was sold fresh, except for sablefish (also known as “black cod”) most of which were smoked. Probably the greatest change in fishing technology for market fishes, particularly for rockfishes, occurred in the late 1930s and early 1940s with the demise of the paranzella and the rise of the otter trawl. Rather than depending on two vessels to keep a net’s mouth open,

the otter trawl net is spread apart by wood or metal otter boards or doors, thus allowing one vessel to do the work of two. The mouths of otter trawls had a high vertical dimension and caught more of the fish that tended to rise above the net when disturbed. Between 1930 and 1940, otter trawls were adopted in large numbers off Washington and Oregon. Late in that decade, these fishermen began to move south, first to Eureka and then to San Francisco, bringing with them this more efficient technology. By 1943 paranzellas had disappeared from California waters. It was, however, the development of a lighter and higherriding otter trawl, the balloon trawl, which opened up new fisheries. As the name implies, rather than drag along the substrate, most of a balloon trawl rides up above the bottom, allowing it to be fished over low rocks. As a result, central and northern California rockfish catches, particularly of bocaccio and chilipepper, vastly increased (Scofield, 1948; Ripley, 1949). Balloon trawls were also responsible for the advent of the frozen fillet market on the Pacific Coast. When it was demonstrated that the trawl could provide large quantities of rockfishes at low prices, the U.S. Army placed substantial orders for their California bases. With the end of World War II, these orders ceased and fish processors scrambled to find new markets for their rockfish fillets, a need that directly led to the rise of the frozen fillet industry in California. Multiple hook lines, often referred to as set, drift and hand lines, played a major role in the nineteenth and parts of the twentieth centuries, but ultimately their inherent inefficiencies drove them from most fisheries. Vertical lines often contained

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a few dozen hooks and were either attached to the vessel or buoyed off. Setlines could stretch for many hundreds of feet and often had hundreds of hooks attached. Depending on the desired species, lines were either laid along the sea floor or in the water column. Rockfishes, California halibut, Pacific mackerel, sharks, and other market species were commonly caught by this method. Early in the development of California’s fisheries, line fishing had a number of advantages. A single fisher, in a small vessel, with a low initial investment in line and hooks could enter many fisheries. Hook-and-line fisheries for rockfishes, lingcod, sablefish, Pacific mackerel, kelp and barred sand bass, sharks, and other species all flourished until about the 1940s (figs. 22-3a–c).

A

F I G U R E 22-3 Before the more efficient balloon otter trawls and gill nets were introduced hook-and-line fishing was a major part of the California commercial fishery. These images are of rockfish fishing off Monterey in the 1930s. (a) Baiting hooks. Photo credit: Maritime Museum of Monterey. (b) Landing rockfishes. Photo credit: Maritime Museum of Monterey. (c) A boat full of bocaccio. Photo credit: Maritime Museum of Monterey.

B

C

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Line fishing was competitive with nets as long as fishes were plentiful and could be located close to ports. However, as stocks were depleted and net technology improved, multihook gear tended to become unprofitable and often was used only by the most marginal of fishermen. A major exception was in the rockfish and lingcod fisheries because hook and line gear could fish the high-relief rocky outcrops inaccessible to balloon trawls. Throughout the first half of the twentieth century both gill and trammel nets were of major importance (fig. 22-4). This was particularly true in those parts of central and southern California where trawl nets were banned. While many species were taken, these nets were particularly important in the California halibut,

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F I G U R E 22-4 Monofilament gill nets revolutionized several fisheries in the 1970s and 1980s. Here is a vermilion rockfish caught in a monofilament gill net off central California. Photo credit: Milton Love.

white seabass, rockfish, Pacific barracuda, kelp and sand bass, and shark fisheries (Holmberg, 1949; Ueber, 1988). One other, rather specialized, technique was used to harvest fish; both swordfish and marlin were taken by harpoon. Vessels equipped with long bow planks sought out fish that were slowly swimming at the surface. Fishermen at the end of these planks thrust the harpoons, attached to strong lines and buoys, into the fish. When the fish had tired itself out, the buoy, line and fish was recovered. Swordfish were not a popular food until the 1930s, and then rapidly gained a large following. Commercial fishing for marlin was banned in 1937 (Greenhood and Carlisle, 1949). Fishermen

The nationalities of California fishermen changed over time. Up through the 1930s, fishermen identifying themselves as born in the United States comprised less than half of the industry. And while dozens of countries were represented, persons born in Italy (including Sicily), Japan, and those from Slavic regions were most prevalent. Up until about 1940, nationalities tended to congregate around specific ports. Scandinavians were primarily found in northern California, Italian fishermen predominated in San Francisco and Monterey, while a majority of fishermen working out of Long Beach and San Pedro were Japanese. By 1948, vast changes had occurred. As noted in Daugherty (1949), “The war [World War II] brought a number of changes. No Japanese, either United States or foreign born, was permitted to fish. Other foreign nationals were required to become naturalized citizens before they were eligible for a commercial fishing license. A number of the younger fishermen were drafted as the war continued. To replace these and to help fill

the increased demand for fish, many new fishermen appeared. Some were older men who had retired from fishing; some were young boys, particularly from fishermen’s families, but many were men from eastern and Midwestern states who had had no previous contact with fishing.” For whatever reasons, the ethnic composition of the 1949 commercial fishermen was very different from that of the past 100 years with the vast majority of fishermen identifying themselves as having been born in the United States. Italians, Yugoslavians, and Portuguese made up most of the others and there were no Japanese fishermen listed. By the early 1950s, a few Japanese fishermen had returned to the industry, but their numbers were never as large as before World War II. By mid-century, a wide range of factors had substantially altered the commercial fisheries of California. Overfishing and an oceanographic regime shift had decimated the once thriving sardine fishery and purse seine fishermen were attempting to switch to Pacific mackerel, jack mackerel, Pacific herring, and northern anchovy. Many purse seine fishermen had given up on California fisheries and spent most of their fishing time pursuing tuna south of the U.S. border. Soupfin sharks had briefly provided a very lucrative fishery, but they too, had been overfished. The introduction of the balloon trawl had created a large rockfish fishery and increased catches had given rise to the frozen fish industry. This, in turn, had stimulated a new fishery for previously discarded Dover sole. Meanwhile, continued population growth in California was creating additional demand for traditional market fishes and, while a wide variety of species were taken, popular species had changed little from the previous century. Along with Pacific sardines and soupfin sharks, there was evidence that a number of other species, such as the California halibut, were showing the early effects of overfishing at least near major ports. Early in the century, most fishermen were neither citizens nor native-born. By mid-century, most fishermen were both. Compulsory relocation during World War II had decimated the once-thriving Japanese fishing community and, while some of these fishermen returned to fisheries after the war, most did not.

1951 to 2001 A commercial fisher of 1951, suddenly thrust forward to 2001, would have difficulty comprehending the changes that had occurred. New technologies, the rise of new fisheries and the declines of some older ones, a booming export market and a troubling import one, increased competition with recreational anglers and unprecedented regulations all had profoundly reshaped the industry. A R EVO LUTION I N TECH NOLO GY

If the first half of the twentieth century saw little change in the way fishermen pursued and caught fishes, the second half was marked by revolution, as many technical improvements made commercial fishing far more efficient than in the past. The years between 1950 and 1955, for instance, saw major new developments. Nylon netting was introduced; it was lighter, stronger and resistant to rot and allowed fishermen to catch more fish at a lower price. Hydraulically operated drums were first used during this period; these laborsaving devices eased the burden of hauling in both trawls and purse seines. Engines of increased horsepower allowed trawl nets to be towed in deeper waters. Another laborsaving hauling device, the Puretic Power Block, was invented in 1955 by a California

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commercial fisher. All three devices made net retrieval much faster, allowing for additional hauls per day with a reduced crew. It has been said that the combination of nylon nets and the power block made possible the worldwide tuna seine industry (Browning, 1980). Trawls underwent a major evolution during the 1960s and 1970s. Previously designed for use on soft or low-relief sea floors, trawlers began to outfit their nets with tires, which allowed this roller gear to be towed over high-relief rocky outcrops. Fishes, such as many species of rockfishes that could previously only be fished with hook and line, could now be taken with the more efficient trawl gear. Another advancement, the monofilament gill net, first extensively used by immigrant Vietnamese fishermen in the early 1970s, had a profound effect on fisheries. Inexpensive, easy to replace, and less visible in the water than nets made of other materials, monofilament nets could be set on those rocky reefs that had often been avoided in the past. In addition, far more netting could be deployed at the same cost. Within a few years of their large-scale introduction, many commercial fishermen had turned to monofilament gillnets and they were a very visible part of the industry. After the passage of the Magnuson Act in 1976, the commercial industry underwent another revolution, as the federal government began to provide substantial funds, loan guarantees, and tax credits and shelters to commercial fishermen to upgrade their ability to catch what were now purely domestic fishes. Inevitably this produced more and larger vessels, with larger engines, capable of towing or setting larger nets and ultimately leading to overcapitalization in a number of fisheries. Lastly, the spectacular improvement in electronic tools radically altered many fisheries. Beginning with radar and loran navigation aids, and ending with sonar, global positioning systems, position (track) plotters and nearly real time satellite images of the ocean surface, the advancements in electronics revolutionized fishing operations. Vessels could now much more easily find, fish and return to productive fishing grounds. Simply put, within a short period there were too many fishermen, with too efficient equipment, chasing too few fish. FOR E IG N F I S H E R I E S, TH E MAG N USON ACT, AN D TH E G LOBALI ZATION OF CA LI FOR N I A’S F I S H E R I E S

From the earliest days of California’s commercial fisheries, fishery products have been both imported and exported. As far back as the 1860s, canned Sacramento River salmon went to Australia, while nineteenth century Chinese fishermen exported many tons of dried fishes to Asia. Canned California sardines were a staple in many countries during and after World War I, canned mackerel was very popular in the Philippines during the 1930s and beyond and, with the collapse of the sardine industry, canned anchovies were also exported. Similarly, despite large domestic herring stocks, millions of tins of higher-quality kippered North Sea herring were imported into California. However, until the 1970s the domestic market for fish products vastly outweighed the export trade. What might be termed the globalization of California’s fisheries had its birth in the 1960s and early 1970s with the massive increase in foreign vessels fishing off U.S. shores. Off California, for example, large numbers of Japanese, Soviet, South Korean, and other fishermen targeted Pacific hake,

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sablefish, and rockfishes. In response, Congress in 1976 passed the Magnuson Act that ultimately mandated the expulsion of foreign vessels within 200 miles of the U.S. coast. One of the effects of this act was to nationalize several fisheries that had been important to other countries, particularly to the Soviets and Japanese, thus creating instant export markets for California fishermen. Sablefish are a good example of this process. Historically, the domestic market for sablefish was small, with annual landings ranging from one million to four million pounds. California fishermen first started exporting sablefish in the early 1970s and by 1975 landings had risen to about 14 million pounds. In 1977, the fishery was entirely in U.S. hands, the Japanese had to import most of their sablefish, and the catch rose to 28 million pounds (Henry, 1992). The large Pacific herring fishery is also export-based although the closure of U.S. waters to foreign fishermen did not play a role in its inception. Herring roe, called “kazunoko” in Japan, is a popular and expensive delicacy. When the Japanese herring harvest declined in the late 1960s, they began to buy herring from both U.S. and Canadian sources. Since the early 1970s, but particularly after 1980, San Francisco, and to a lesser extent other northern California embayments, have played host to valuable fisheries that target spawning herring. The herring are frozen, shipped to South Korea and China, the roe removed and sent to Japan. An allied fishery, called roe-on-kelp, harvests kelp blades after spawning herring have attached their eggs. Called “kazunoko kombu”, this is also a high-value export to Japan (Spratt, 1992). California’s fisheries have benefited from the new ease with which countries trade with one another. The integration of national economies, the dropping of trade barriers and the development of new uses for fishes have all helped California gain an international market share for a number of products. Currently, along with sablefish and Pacific herring a number of other species including thornyheads, sardines, and Pacific hake are caught primarily for the export market. And while thornyheads are destined to be consumed as sushi in Japan, and many Pacific hake wind up as surimi, sardines are exported either to Asia, to be used as bait by tuna longliners, or to Australia as food for pen-reared bluefin tuna. The sardine industry has come a long way from the days of canning and reduction. While globalization has created large markets for a number of species and has certainly enriched some fishermen, it is also fraught with pitfalls. In 1900, when a Monterey fisher marketed his entire catch to a few markets on a pier, or to a wholesaler who sold his entire catch to San Francisco middlemen, a recession in Japan or a move in the relationship between the yen and the dollar meant nothing. Today, many California fisheries are as tied to the world economy as are computer chips, automobiles or wheat. This was instantly apparent to sablefish fishermen in 1978, when following their record year of 28 million pounds, the Japanese sablefish market collapsed, sablefish prices sank and fishermen were in economic shock. New export fisheries often engendered a Gold Rush mentality. Until 1988, there was no market for Pacific hagfish, although hagfish were used to make eelskin wallets and other products in Korea. In 1988, buyers from Korea began approaching fishermen in California and purchased 690,000 pounds from Monterey and San Francisco operators. Within three years, the fishery had expanded to the entire California coast (and beyond) and California landings exceeded

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2,600,000 pounds. Everyone, it seemed, wanted to enter the fishery and everyone did. Vessels that could barely float were called into service and fishermen who could barely bait a trap put out to sea. And then, within a year, the fishery disintegrated. Buyers gave a number of reasons for pulling out. They complained of the quality of the skins of California hagfish, perhaps reflecting how the fish were stored after capture. They implied that better, or perhaps less expensive, product was available on the East Coast of the United States. For whatever reason, just a few years after it started, the hagfish fishery disappeared as if it never was (E. Melvin, pers. comm.). Globalization means that California fishermen also must compete with imported fishes and salmon aquaculture. For instance, during some years, California wholesalers have purchased Asian-caught swordfish for less than California fishermen wished to be paid. California salmon fishermen must compete with Atlantic salmon farmed in Chile and Canada. California consumers are now more attracted to the bright white fillets of Chilean sea bass (Patagonian toothfish) than the faintly gray ones of the domestic white seabass. And while many of the most enthusiastic fish purchasers in California are recent Asian immigrants, they often prefer purchasing those species they grew up with, which translates to a healthy trade in frozen, imported saury, pomfret, milkfish, croakers, and cutlassfish (Kato, 1994). TRADITIONAL F I S H E R I E S

The latter half of the twentieth century saw great turmoil in and, ultimately, the near demise of, the cannery and reduction fisheries. With the collapse of their fishery in the early 1950s, many sardine fishermen moved into the tropical tuna fisheries that targeted yellowfin tuna and skipjack. The development of nylon netting and the power block net hauling system allowed these fishermen to much more efficiently purse seine tuna schools and, as larger and larger seiners were built, the tuna industry came to dominate the California commercial fishing industry. However, as the industry became more closely tied to the world economy, it became obvious that there were large cost savings in canning these tunas outside the United States. Between 1982 and 1984 most of the canneries relocated outside the continental United States, the purse seiners went with them and the industry was gone. The Pacific sardine, Pacific mackerel, and northern anchovy fisheries all had their ups and downs during this period, but at the end of the century the once thriving industry was a shadow of its former self. For two decades, beginning in 1965, northern anchovies were the basis of a large reduction fishery. However, beginning in 1983, the chronically low prices offered fishermen essentially ended that fishery. After being decimated by overfishing, both sardine and mackerel populations made a comeback in the oceanic warming trend that began in the late 1970s. Fishery managers now closely control catches and the species are caught for a variety of purposes, including canning for human consumption and pet food or export for aquaculture feed or commercial fishing bait. However, in a number of years the allowable catch quotas have not been met, the result of low prices to fishermen, sporadic fish availability, scarce market orders and the lure of more lucrative fisheries, such as squid (Jacobson, 1992, Konno and Wolf, 1992; Wolf and Smith, 1992; California Department of Fish and Game, 2000; K. Hill, pers. comm.). By the beginning of the twenty-first century, much of the catch was

exported; only relatively small amounts were destined for canning and reduction. During much of this period the traditional market fisheries flourished. Increased demand for seafood, a greatly expanded trawl and gill net fleet, along with the development of new technology to help harvest these animals, meant a surge in fisheries for such long-important species as chinook salmon, swordfish, lingcod, rockfishes, various flatfishes, California halibut, and white seabass. At the same time, increased consumer sophistication and an influx of Asian immigrants, combined with decreased stocks of traditional species led to new, or at least expanded, fisheries for previously disdained species. The market for angel, thresher, and shortfin mako sharks, white croaker, and grenadiers vastly increased during this period. Perhaps most notable were the explosive rise of these fisheries, sometimes mirrored by an equally precipitous fall. For example, while only 328 pounds of angel shark were landed in 1977 more than 1,200,000 pounds were landed in 1985 and 1986. By 1990, catches had dropped to about 200,000 pounds, the result of overfishing, belated minimum size restrictions (Richards, 1992), as well as a partial ban on gillnets. By the end of the century, almost without exception, a combination of factors had caused a marked decline in most of these fisheries. Gear restrictions, such as the nearshore gill net ban in southern California, took a heavy toll on catches of such species as white seabass, California halibut and angel shark. Overfishing had led to restrictive quotas and limited seasons on rockfishes, lingcod, and other species. The continuing degradation of spawning habitat had reduced the numbers of some runs of salmon available to fisheries. The newest commercial fishery was also one that was still evolving. Beginning in the mid-1980s, a market developed for live fish, ultimately destined for Asian restaurants and markets. Fishermen quickly found that the value of their catch was dramatically higher when kept alive (often one to six dollars per pound and occasionally much more) than when dead (rarely more than 50 cents per pound). The fishery, which began in central and southern California, soon spread to the north coast and by the end of the century ranged from the intertidal zone to a depth of about 100 feet. About 300 vessels (from kayaks to 100-foot long craft) landed 94% of a catch totaling about 478 metric tons. The same fishery brought in over 700 tons of dead fish. Cabezon, California sheephead, various nearshore rockfishes (including gopher, grass, blackand-yellow, and brown), and California scorpionfish comprised the bulk of the catch. Live fish were transported by trucks or vans equipped with aerated trucks and shipped to markets and restaurants throughout the state. Most fish were taken in traps and an assortment of hook-and-line gear (California Department of Fish and Game, 2000). The fishery was a particularly contentious one, as it, more than most commercial efforts, directly and very visibly competed with recreational anglers and spearfishermen. Responding to concerns regarding allocation and over-harvest, the California Department of Fish and Game began to place limits on the fishery through such restrictions as limited entry, size limits and quotas. The years between 1950 and 2001 saw major changes in the commercial industry. It was no longer an industry of boundless frontiers, but rather one beset with problems that included declining fish stocks, increasingly restrictive regulations and rising costs. In an attempt to lower capacity in some fisheries, managers were encouraging attrition and were not

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TA B L E 22-1

Number of Vessels that Made Commercial Landings Only in California, 1981 to 1999

NOTE :

Year

CA Only

1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998

5,832 5,762 5,257 4,779 4,451 4,305 4,162 4,204 4,376 4,155 4,032 3,536 3,271 3,102 3,074 2,994 2,857 2,505

1999

2,495

From Thomson 2001.

allowing replacements. By the end of the twentieth century, the commercial industry had shrunk to half its size of 20 years before (table 22-1). The cannery and reduction industries were but a small fraction of their previous size; much of the pelagic wetfish catch was exported. Many of the major fisheries, such as sablefish and thornyhead, were almost entirely exportbased. This globalization of California’s fisheries was not without problems, as domestic fishermen faced greater competition within the state from foreign sources. Salmon fishermen were facing lower prices due to increased supplies from Alaska and farmed fish. There was still a thriving market fish industry, although catches were almost uniformly lower than at their peaks. The live-fish fishery had become a major industry, bringing welcome revenue to many fishermen, but it was also a flash point with the recreational industry.

Recreational Fishing 1850 to 1940 Compared to the commercial fisheries, the early years of recreational marine angling off California are much less well documented and changes in this industry do not fall as neatly into distinct periods. One problem with documenting recreational angling is that it is difficult to determine when subsistence fishing becomes fishing for pleasure. A second complication is that, except for the barest of mentions, the Department of Fish and Game did not collect data on recreational angling until the mid-1930s. If we use paying for fishing as one marker for recreational angling it was only a few years after the Gold Rush that organized fishing trips were under way. An illustration in a mid1850s San Francisco newspaper portrays a boatload of formally dressed anglers handlining off the Farallon Islands. By the

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1870s, occasional fishing excursions were advertised in a newspaper in Humboldt County, wherein anglers could sail aboard one of several tugboats to Cape Mendocino and fish for rockfishes and Pacific halibut. In the 1890s, tourists visiting Monterey Bay regularly chartered small sail-powered commercial fishing vessels and trolled for salmon. It was, however, in southern California and with Charles Frederick Holder that California marine recreational angling received its first big boost. Born of a wealthy Massachusetts family, Holder moved to Pasadena in 1885. A tireless publicist for southern California, recreational fishing and conservation, he became a major voice for more sportsman-like fishing because of experiences such as the following, “The day of my first landing at Avalon [1886] I saw men casting big hand-lines (cod-lines) from the beach, catching yellowtails from eighteen to thirty-five pounds as fast as they could pull them in. I saw that I had stumbled upon an angling paradise; also, I recognized the fact that no fishing-ground could stand such methods” (Holder, 1910) (fig. 22-5). Holder created the Tuna Club of Santa Catalina Island in 1898, with the goal of changing fishing quantity to quality. As he noted, “The object of this club is the protection of the game fishes. . . . to encourage and foster the catching of all fishes, and especially tuna, yellowtail, seabass, black seabass, etc., with the lightest rod and reel tackle, and to discourage handline fishing, as being unsportsmanlike and against the public interest.” (Young, 1969). But these noble sentiments were really aimed at the wealthy or at least well-to-do, the few Zane Grays of the world, because hiring a launch and guide was an expensive endeavor. Through the end of the nineteenth century, relatively few average anglers fished from boats. Indeed, before World War I, pier and surf fishing were the choice of the masses. Except for the very end of some privately owned piers, both types of fishing were free and, considering the relatively primitive fishing tackle of the day, fishing from piers was often excellent (fig. 22-6). Holder (1913) observes that, “The explanation of these piers is that they are for fishing or angling. . . . On some when the fish are running you may see two or more hundred men, women and children, all fishing with long bamboo rods for surf-fish [perch], roncador [yellowfin croaker], sea-trout [young white seabass], jack-smelt, mackerel, croakers and hoping for yellowtail, sea-bass and big game which frequently come. No better evidence that there is a love of angling among all peoples can be seen than in this angling contingent, some of whom sleep on the piers Saturday night. . . . to secure a position Sunday when all the piers are crowded.” The appearance of the party vessel (now called the Commercial Passenger Fishing Vessel, CPFV) and barge fishing first allowed the average angler to enjoy deep-sea fishing (fig. 22-7). It appears that the CPFV industry had its beginnings just before World War I. At this time, converted commercial craft in Long Beach and other ports began carrying anglers on a regular schedule without the fishermen having to charter the entire vessel. In the early days of the industry, anglers either trolled or used salted bait. By the mid-1920s, operators began catching anchovies, sardines and other small fishes and the live bait boats came into vogue. In the beginning, each boat carried a bait net and passengers often helped in net deployment and retrieval. Within a few years, some vessels began to specialize in catching bait for recreational vessels and these “bait boats” have been an integral part of the CPFV industry ever since. The industry was an immediate success and by 1930 CPFVs were operating from

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F I G U R E 22-5 A large catch of yellowtail made off Santa Catalina Island in the nineteenth century. Photo credit: Ed Ries Collection.

F I G U R E 22-6 Before commercial passenger fishing vessels, fishing barges, and inexpensive private vessels, most southern California ocean anglers fished from piers. Photo credit: Ed Ries Collection.

every pier in southern California. By the late 1930s, CPFV and barge anglers accounted for the majority of fishes taken in the marine recreational fishery. Over 200 CPFVs operated out of southern California, as well as small numbers in Morro Bay, Monterey Bay and San Francisco Bay; northern

California did not host them until after World War II. Except for yachts of the wealthy, small privately owned pleasure boats were a rarity and, during this period, did not play a large role in the recreational fishery (Croker, 1939; Ries, 1997; Ries, 2000a,b).

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F I G U R E 22-7 The first commercial passenger fishing vessels were primitive, but the abundance of fishes made up for the lack of amenities.

Photo credit: Ed Ries Collection.

Most CPFV angling occurred in southern California, reflecting that region’s greater population, more equitable weather and greater numbers of the more gamy semi-pelagic species (Pacific barracuda, yellowtail, and Pacific bonito) widely sought after by anglers. Through the start of World War II, almost all CPFVs ran from April to September, that time of the year when these preferred species migrated north from Mexico. The beginnings of the industry coincided with a warm-water period and this was reflected in the species caught, with Pacific mackerel, Pacific barracuda, kelp and barred sand bass, Pacific bonito and California halibut taken in largest numbers in southern California and rockfishes predominating in central California. Both yellowtail and white seabass were also popular species, although rarely caught in the same abundance as the previous species. About 75% of all CPFV anglers fished from vessels leaving from Los Angeles or Orange County piers and these anglers fished primarily at three locations; Horseshoe Kelp off San Pedro, Santa Monica Bay and Santa Catalina Island. So important was the Pacific barracuda to the southern California fishery that during that period “the success of the entire fishing season depends on the barracuda run” (Croker, 1939). What were early vessels like? In the beginning, all were relatively small, mostly between 50 and 65 feet long, and had been converted from commercial fishing vessels. Compared to modern CPFVs, these early boats lacked almost all amenities including galleys, bunks, or any indoor space in which anglers could get out of the weather. It was not until 1934 that a boat specifically designed for sport fishing was launched. However, what the early vessels lacked in comfort, they more than made up for in quality fishing. There were simply more fishes in the 1920s and 1930s then there are today and fishing was excellent much of the time, despite the fact that even the most sophisticated fishing tackle was crude by

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today’s standards. Handlines were commonly employed aboard sportfishing vessels, and were still occasionally seen on deep-water rockfish trips well into the late 1950s. Jackpoles, long bamboo shafts to which were attached short lines and hooks, were also common. The tackle of even the most sophisticated angler left much to be desired. Rods were either stiff and broomstick-like or very long and overly supple. Until the 1930s, most reels had no drags other than a leather flange. Line, almost universally known as cuttyhunk, was made of linen and rotted easily if not dried at the end of a fishing day. Leader material was made either of wire or silkworm gut and both were easily seen by fishes. Despite C. F. Holder’s admonitions, the typical angler during this period sought quantity; notions of catch and release were not even contemplated. Indeed, the distinctions between recreational and commercial fishermen were blurred, as fishes caught aboard CPFVs and barges could be sold. At about the time that live bait fishing was in its infancy, a second kind of deep-sea fishing began. In 1921, A. B. Hohenshell, an enterprising entrepreneur purchased a dilapidated barge, anchored it two miles off Long Beach, southern California and invited the public to come fishing (fig. 22-8). For a nominal charge, anglers were ferried from a pier to the barge and, if they had no fishing equipment, provided with basic fishing tackle (bamboo poles, 20 feet of cotton line, a hook and sinker) and salted anchovies, sardine or mackerel. This first barge, the PAPROCA, was capable of holding 100 anglers and proved to be wildly popular. In the first five years, 100,000 fares were sold. By 1933, there were 25 barges situated from San Diego to Santa Barbara (and briefly in Monterey Bay), moored from 100 yards to four miles offshore. Despite their name, many of these vessels had once been large sailing schooners, now stripped down and capable of carrying 250 or more anglers. Early barges were quite primitive, but they soon

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F I G U R E 22-8 Beginning in the 1920s, reasonably priced fishing barges were extremely popular with the angling public in Southern California. Photo credit: Ed Ries Collection.

became much more refined, often including galleys, lounge rooms, restrooms and even sleeping quarters for those who might want to spend the night. Live bait was soon routinely provided. Unlike most CPFVs, some barges remained open throughout the year. Pacific mackerel was the most commonly taken species by barge anglers, although white croaker, Pacific sanddab, California halibut, Pacific barracuda, and Pacific bonito were often taken. During the 1920s and 1930s, giant sea bass and yellowtail were frequently caught. In fact, many barges had a jewfish bridge where anglers equipped with heavy gear soaked whole barracuda or mackerel and waited for a giant sea bass bite. After World War II, barge fishing slowly declined in popularity, perhaps the result of the vast increase in small boat ownership and the last fishing barge in California was removed in 1998 (Van Deventer, 1926; Fry, 1932; Clark and Croker, 1933). In an age when boat fishing was beyond the pocket book of most anglers, pier and surf fishing were very popular throughout the late nineteenth and early twentieth centuries. In the early 1920s, both CPFV and barge fishing were perfected and both allowed the average angler access to deep-sea fishing. By the late 1930s, it was estimated that the CPFV and barge catch dwarfed the other recreational fisheries. In the main, only wealthy individuals could afford private vessels. CPFVs operated out of most southern California piers and at a few sites along the central California coast. Barges were anchored throughout southern California. Fishing tackle of the times was relatively primitive; most anglers used bamboo rods and linen line although handlines were also popular.

1941 to 2001 The economic upswing that presaged the United States entrance into World War II added to the rising popularity of marine recreational angling and it was World War II that caused its abrupt halt. Even before the United States entrance into the war, a note in the September 1941 California Division of Fish and Game, State Fisheries Laboratory Monthly Report demonstrated that profound changes were coming. “The Navy has established a mine field right across Horseshoe Kelp, the best ocean sport

fishing grounds in the State. . . . this field has effectively ended fishing as far as most of the Long Beach and San Pedro sport boats are concerned”. After Pearl Harbor, all CPFVs and barges were shut down and most did not return into operation until after the end of the war (Young, 1969). However, within a few years, recreational marine angling, first from CPFVs but soon from private vessels, began a boom that lasted for decades. A number of factors led to this tremendous rise in popularity. Perhaps the most important was the rapid growth of industry in, and after, World War II that brought many immigrants to California, particularly to southern California. Ultimately, the proliferation of freeways meant that millions of potential anglers were within a short drive of the coast. Many returning veterans, both those who had been in the prewar recreational fishing industry and those who had just been avid anglers, saw the immense potential that these new immigrants represented. As a result, construction of vessels specifically designed as CPFV began in boatyards even before the war had ended. Between 1945 and 1965 about 10 newly built vessels entered the California CPFV fleet annually. Between this building surge and converting surplus navy vessels to civilian use, over 400 vessels were registered as CPFVs in 1949, twice the number from before the War. By 1955, that number had risen to about 600 vessels. While many of these new vessels were in the range of 55–65 feet long, boats up to 85 feet long soon made their appearance (Young, 1969). A major factor in the rising postwar popularity of marine angling was the introduction of new materials that made fishing easier and more fun. Fiberglass rods, clearly superior to bamboo, wood or steel, made their appearance in 1948 and quickly took over the market. Improved conventional reels with light spools that make casting much more efficient, and improved drag systems that prevented gear stripping were also soon available. By the 1960s, spinning reels that allowed novice anglers to cast baits and lures without fear of backlashes, yet were tough enough to withstand a saltwater pounding, had created a huge following. Within about 10 years of its introduction around 1950, monofilament line that was soft, clear, and rot-proof, outsold all other lines (Smith, 1979). Over the years, there would be many new additions to the marine recreational fishing

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industry, including better hooks, dazzlingly lifelike plastic lures and high tech rods, reels and lines, but none had anything like the impact of fiberglass rods, improved reels and monofilament line. During the 1950s, the CPFV fishery gradually evolved to year round service. Since its inception, most of the CPFV fleet had shut down during winter months, when the most popular game fishes, such as Pacific barracuda, were less abundant. Historically, in southern California, a few vessels shifted to fishing for deep-water rockfishes, but because the rods, reels and lines of the time were not easily adapted to deepwater fishing, most rockfishes were caught by handlines supplied by the vessels. Davis (1949) describes the experience of using a handline and eight-pound weights to catch these fishes by stating “That’s codfishing [deep-water rockfish]—and if you don’t like it I don’t blame you. However, as we have said, it provides a day out in the open, healthful exercise and some mighty ‘good-eating’ fish.” However, with improved tackle, fishing for deep-water species became far less arduous and the vastly increased number of anglers provided a ready market for all year service. As a result, southern California rockfish catches soared, at some ports increasing by 400–500% between 1947 and 1955. Since the mid-1950s, rockfishes have become a staple group at most ports. The late 1940s saw the introduction of inexpensive fiberglass boats and more user-friendly outboard engines. The relatively light, stable, mass-produced vessels allowed anglers the freedom and flexibility, and a place away from dozens of other anglers, denied those fishing on CPFVs. By the 1960s, CPFVs were being challenged by small vessels for dominance in the deep-sea fishing arena (Young, 1969; Smith, 1979). In certain respects, the recreational marine fishing industry of the early twenty first century was little changed from that of 1950. Anglers still plied beaches, piers and jetties or fished from private vessels and CPFVs. And although there had been many introductions of new materials for rods, reels, lines and lures, these had brought, at best, only incremental improvements to the fisheries. For the private boat owner (now the major force in the recreational industry) and the CPFV operator, as for the commercial fisher, the revolution had been in the great improvements in electronic devises (such as radar, fish finders, and global position systems) and in information technology. Through the use of the internet, data on water temperature, the location of oceanographic fronts and up-todate information on fish locations were readily at hand. All of these put the motivated private vessel owner on the same playing field as the CPFV skipper. In general, but with some telling exceptions, species composition in the various fisheries had changed little over the last 30–40 years (table 22-2). The faunal break between southern California and central/northern California, caused by current patterns, had always been reflected in the composition of the recreational catch. In the private vessel and CPFV fisheries of central and northern California, rockfishes, salmon, striped bass, lingcod and white sturgeon dominated the catch. Kelp and barred sand bass, rockfishes, Pacific barracuda, Pacific mackerel, yellowtail, Pacific bonito, white seabass, California halibut, and albacore played a major role in the southern California fishery. Much of the southern California fishery was based on species that were either highly migratory and whose presence was linked to water temperatures (Pacific barracuda, Pacific mackerel, yellowtail, albacore) or whose reproductive success was dependent on highly variable oceanic conditions such as upwelling (rockfishes). Hence, compared

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to fisheries in the northern part of the state, the southern California catch was always more at the mercy of the vagaries of both decadal long trends in water temperature, and such transitory events as El Niños and La Niñas. The extreme instance of this occurred during the 1980s and 1990s, when generally warmer waters and increasingly frequent El Niños brought northward large numbers of previously unusual yellowfin tuna and dorado (Dewees et al., 1990; Norton and Crooke, 1994). Of all the fisheries, the most profound changes in catch composition occurred in the southern California private vessel and CPFV fisheries (table 22-2). Most striking was the sharp decline in the numbers of certain rockfishes, particularly bocaccio, and olive and blue rockfishes. Once mainstays of the fishery, these almost disappeared from the recreational catch (Love et al., 1998a). It is likely this was caused both by overfishing (by both recreational and commercial fishermen) and 25 years of juvenile recruitment failure from adverse oceanographic conditions (Love et al., 1998a, b). During the same period, a number of warm-water species, such as yellowtail, Pacific barracuda, California scorpionfish, ocean whitefish, vermilion rockfish, and honeycomb rockfish became much more abundant. There had been large changes in some parts of the industry. Private vessels were now the single largest component of the recreational fishery (table 22-3). Throughout California, the fishing effort by private vessel anglers was almost equal to all other fishing modes combined and private vessel anglers caught almost 50% of the entire marine recreational catch. Overfishing and environmental changes had created declines of rockfish, lingcod and other stocks, changing the face of fishing. Federally mandated rebuilding plans had cut bag limits, created closed seasons, set minimum size limits and even marine reserves. In the face of these new realities, creative CPFV operators were offering sanddab specials during rockfish closures, while declines in rockfish stocks in central and northern California brought about combination Dungeness crab and rockfish trips. In an effort to reduce pressure on some stocks, some members of the industry had begun encouraging catch and release, a virtually unthinkable idea to most anglers of the past. Some CPFVs were also diversifying into such areas of ecotourism as whale and bird watching. As ocean waters warmed in the late 1970s, southern California anglers greatly benefited from the increase in abundance of such highly sought-after species as kelp bass, barred sand bass, Pacific barracuda, and yellowtail and the staggering population increase of the Pacific sardine. Because these fishes were readily available, the gradual decline of many rockfishes, long a mainstay of the fishery, was not viewed with alarm. It will be interesting to note what effect a regime shift to colder water will bring to the recreational fisheries. While it is quite possible that many of these warm temperate species will be less abundant, it is not clear that the rockfishes will return to their former abundance. Recreational angling became a very big business after World War II, the result of a burgeoning population and much better fishing tackle. Throughout this period, southern California remained the center of fishing activity, although recreational fishing was very popular around all major fishing ports in central and northern California, particularly around San Francisco Bay. The important species in the various fisheries vary between southern California and central/northern California, mirroring the faunal break at Point Conception. Many species remain important for decades, particularly in the fisheries north of Point Conception. Southern California

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TA B L E 22-2

The Ten Most Numerous Species in Four Recreational Fishing Modes

Southern CA Beach and Banka

Northern/Central CA Beach and Bankb

1995–2000 Barred surfperch Yellowfin croaker Opaleye Walleye surfperch Corbina Silver surfperch White croaker Black perch Jacksmelt Kelp bass

1958, 1960 c Barred surfp. Redtail surfp. Silver surfp. Walleye surfp. Jacksmelt Striped seap. Kelp greenling Calico surfp. Striped bass Cabezon

1995–2000 Barred surfp. Striped seap. Cabezon Silver surfp. Redtail surfp. Kelp greenl. Walleye surfp. Calico surfp. Jacksmelt Rock greenl.

Manmade Structures 1963a Queenfish White croaker Pacific bonito Walleye surfperch Shiner perch Black perch California halibut Pacific mackerel Jacksmelt Kelp bass

1995–2000 c Pacific mackerel Jacksmelt Pacific sardine Queenfish White croaker Walleye surfperch Barred surfperch Yellowfin croaker Topsmelt Opaleye

Manmade Structures 1958 White croaker Jacksmelt Shiner perch Walleye surfp. Barred surfp. Topsmelt Silver surfp. Pac.Stghrn S. Pile perch Calico surfp.

1995–2000 White croaker Walleye surfp. Shiner perch Jacksmelt Barred surfp. Striped seap. Silver seap. White seap. Pacific mack. Pac. sardine

Private and Rental Vessels 1975–1976f White croaker Pacific bonito Barred sand bass Bocaccio Kelp bass Pacific mackerel Olive rockfish Blue rockfish Sablefish Black perch

1995–2000 Pacific mackerel Barred sandbass Yellowtail Kelp bass White croaker Pacific barracuda California scorpionfish Pacific sanddab Vermilion rockfish California halibut

Private and Rental Vessels 1959–1960 c Blue rockfish White croaker Black rkf Pacific sandd. Copper rkf Lingcod Canary rkf Jacksmelt Gopher rkf Chinook sal

1995–2000 Blue rockfish Black rockfish Pac. mack. Chinook sal. Gopher rkf White croaker Brown rkf Lingcod Canary rkf Pac. sandd.

CPFV 1975–1978f Bocaccio Kelp bass Pacific mackerel Chilipepper Olive rockfish Pacific bonito Barred sand bass Blue rockfish Pacific barracuda

1995–2000 Barred sand bass Pacific mackerel Kelp bass Pacific barracuda California scorpionfish Ocean whitefish Pacific sanddab Yellowtail Vermilion rockfish

CPFV 1960 c Blue rockfish Yellowtail rkf Olive rkf Bocaccio Chinook sal. Canary rkf Vermilion rkf Striped bass Copper rkf

1995–2000 Yellowtail rkf Blue rkf Canary rkf Olive rkf Gopher rkf Chilipepper Starry rkf Widow rkf Black rkf

White croaker

Honeycomb rockfish Lingcod

a

Rosy rkf

There were no surveys of beach and bank anglers before the MFRSS.

b

These rankings do not include the surfsmelt net fishery, which represents the largest fishery by number of individuals taken. c

Miller and Gotshall (1965).

d

Pinkas et al. (1967).

e

Wine and Hoban (1976).

f

Data from a California Department of Fish and Game creel census, as reported in Love et al. (1987).

NOTE :

In each mode, comparisons are made between the most recent data and that from the earliest previous surveys. No beach and bank surveys had previously been conducted in southern California. The beach and bank mode includes both sandy beach and rocky shore habitats, manmade structures include piers and jetties. Data from 1995–2000 comes from the Marine Recreational Fisheries Statistics Survey.

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TA B L E 22-3

Average Annual Marine Recreational Fishing Effort and Harvest in California During 1998–1999 by Fishing Mode

1000s of Fish

Area/Fishing Mode

1000s of Angler Trips

Landed Whole

Released Alive

Other Disp.

Total

Southern California Man-made Beach CPFV Private Total

624 281 641 1,324 2,869

837 327 1,733 1,960 4,857

644 247 973 4,075 5,939

233 17 262 211 723

1,714 590 2,968 6,246 11,518

Central/Northern California Man-made Beach CPFV Private Total

440 344 168 921 1,872

533 1,582 1,131 1,459 4,705

192 206 122 648 1,168

67 17 171 205 460

792 1,805 1,423 2,311 6,331

Total California Man-made Beach CPFV Private

1,064 625 808 2,245

1,370 1,909 2,864 3,419

836 453 1,095 4,723

300 34 433 416

2,506 2,395 4,391 8,557

4,741

9,562

7,107

1,183

17,849

Total

NOTE : From Thomson 2001; Marine Recreational Fishery Statistics Survey. Includes harvests in U.S. waters only.“Other Disp.” refers to fish used as bait, filleted, given away or discarded dead.

fisheries are more sensitive to changes in water temperature. The number of anglers in the industry may have peaked in the late 1980s or early 1990s and private vessels are now the most important part of the industry.

Fishery Management “A self-preserving fishing industry would respect the biological limits of its resource’s productivity, limiting its seasonal take to some safe minimum so as to guarantee future harvests. Fishing industries, however, do not generally manage their affairs in such a rational way” (McEvoy, 1986).

1850 to 1899 Salmon formed the first great commercial fishery in California and it was to protect that species that the first concerns were raised. Indeed, as far back as 1852, the first law that limited commercial fishing was passed, creating a closed season for salmon in some inland waters. In these early years, local governmental entities also passed some fishing restrictions. For instance, in 1893, San Francisco County passed an ordinance prohibiting the sale of striped bass less than eight pounds in weight (Craig, 1928). In 1870, the perceived need to further protect salmon and to improve other stocks led the California legislature to establish the Board of Fish Commissioners to “provide for the

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restoration and preservation of fish in the waters of this state.” (Bryant, 1921). In 1878, the Fish and Game Commission was formed, it had additional responsibilities for fishery enhancement and protection. Some of the early efforts by the Board focussed on introducing food and game fishes to California waters, actions that soon led to booming populations of both striped bass and shad. Continuing concerns regarding salmon depletion led to efforts to reduce coastal stream pollution by sawmills, mandated the building of fishways at dams, recommended a closed salmon season on the Sacramento and San Joaquin rivers and made mesh size provisions for nets. The licensing of commercial fishermen, begun in 1887, was also an attempt to control salmon fishing. However, the only intense efforts to place limits on any marine fishery during this period was the blatantly antiChinese fishing law passed in 1880. This act, passed with other anti-Chinese laws, prohibited all aliens incapable of becoming citizens (the Chinese) from fishing in state waters. And while it was ruled unconstitutional in federal court, violating the equal protection clause of the Fourteenth Amendment, it was symptomatic of the seething hatred this group engendered. Indeed, having quickly been ousted from gold mining, attempts were often made to drive the Chinese out of the fishing industry as well as other economic sectors in California. “One government observer noted in 1873 that the salmon business on the Sacramento River was entirely controlled by whites, ‘no Chinamen being allowed to participate in it.’ ‘There is no law regulating the matter . . . but public

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opinion is so strong in relation to it that any attempt on their part to engage in salmon-fishing would meet with a summary and probably fatal retaliation’” (McEvoy, 1986). It was the Chinese prosecution of the San Francisco Bay shrimp fishery that most inspired the ire of some segments of the public. This net fishery, charged a few nascent conservationists, newspapers and the Italian Fishermen’s Union, caught large quantities of small fishes and this by-catch was impacting other fisheries (Jordan, 1887, 1892). However, from our vantage, it is difficult to know to what degree the complaints voiced represented a real problem, a perceived threat of competition in the minds of other fishermen or the pervasive racism of the times. For instance, as early as 1870, it was noted that the Italian-run beach seine fishery was very wasteful, with large numbers of small fishes discarded and allowed to drift dead on the tides and yet no complaints were voiced in this instance (Skinner, 1962). And, as noted by Scofield (1954), “Destruction of some small fish in the shrimp nets opened an opportunity for unscrupulous politicians to propose hampering legislation so that a campaign fund to kill the bill would be collected from the Chinese. The fishermen knew they were being robbed but they paid rather than fight.” Ultimately, as summarized by McEvoy (1986), the Fish and Game Commission of that time found it much easier to plant exotic species, such as striped bass and shad, in an effort to “improve” fisheries, rather than to promulgate and enforce fishery laws. The philosophical underpinnings of the concept that natural resources truly belonged to all citizens and could not be randomly harvested by anyone, in any quantity, at any time, had not yet truly flowered.

1900 to 1950 With its upsurge in fisheries, the new century brought the first large flurry of management activity. Perhaps most important was the realization that very little was known of the life histories and populations of economically-important fishes and, in consequence, the state legislature and Fish and Game Commission set about to remedy these deficiencies. By 1914, scientific investigations on the life history of California salmon and trout were underway and plans were afoot to create a research laboratory in San Pedro. In the same year, the Fish and Game Commission (soon the Division of Fish and Game and still later the Department of Fish and Game) began California Fish and Game. This journal was initially designed to provide a two-way conversation between the public and Commission and early issues contained a mixture of articles summarizing the major fishes of California, the art of dryfly trout fishing, exhortations from conservationists and summaries of new fish and game laws. However, within a few years, the journal was transformed into an outlet for much of DFG’s research activities and ultimately provided a clear picture of the organization’s thinking about fisheries management. The twentieth century also ushered in an attempt to better understand the nature of commercial fisheries. In 1909, a fisher was first required to give a detailed description of himself (including country of origin), the name of the vessel upon which he fished or the type of fishing he pursued, and his address. In 1911, a law was passed requiring that fish dealers keep a record of fish purchased. In 1915, this was amended to require monthly reports and legislation in 1919 required that every fish purchased be recorded in triplicate. The first (white)

copy went to the fisher, the second (yellow) to the buyer and the third (pink) went to the California Department of Fish and Game. Since that time, the landing data submitted to Fish and Game has been referred to as “pink ticket” data, although this particular system is not longer used (Scofield, 1954). In 1917, work was begun on a State Fisheries Laboratory (later in the century to be the home of the Department of Fish and Game) at San Pedro whose purpose it was to investigate problems connected with the rapidly growing fisheries of the state. The first state research vessel was built in 1918 (Bryant, 1921; Scofield, 1948). As the century progressed, a large number of commercial fishery laws were passed and these were generally designed to minimize the catch of juveniles, reduce fisheries during spawning seasons or reduce the overall catch. Limiting conflicts between user groups, particularly between commercial and recreational anglers, was also periodically attempted. A few areas were also set off limits to fishing. Typical examples of these types of regulations include banning the sale of sturgeon (1901), California corbina, yellowfin and spotfin croaker (1917) and striped bass (1935), mandating minimum weights on barracuda (1917), prohibiting the use of purse seines to capture yellowtail, white seabass, and Pacific barracuda (1941) and banning most commercial fishing from the area around Santa Catalina Island (1913) (Scofield, 1921; Greenhood, 1949; McCully, 1949; Scofield, 1951; Young, 1969). The trawl fisheries were the targets of some of the earliest severe regulations. Even in its infancy, many, even those in the commercial industry, disliked trawlers. As Scofield (1948) noted, “The trawlers remained the objects of bitter hatred by other fishermen because trawl-caught fish had brought down the prices paid.” Trawlers could also fish in heavier weather than smaller vessels and thus gained a competitive advantage. In addition, the heavy, and unsaleable, bycatch of these early fisheries did not sit well with many observers. Probably the last straw occurred when a number of trawlers operating in southern California destroyed large numbers of undersized California halibut. Partially in response to this perceived destructive fishery, in 1913 trawl nets were banned from state waters (to three miles offshore) throughout all southern California. A series of revisions followed and, with some exceptions, trawling remained legal in state waters in most of northern and central California and illegal from Santa Barbara to the Mexican border (Clark, 1931; Scofield, 1948). As has been previously noted regarding sardine stocks, early in the century Division of Fish and Game biologists were well aware of the potential dangers of overfishing. As early as 1919, Thompson wrote, “Fisheries are subject to depletion because of too intense exploitation, as has been proved in Europe and in our own country. It is the duty of the government, as the one element in the situation which is concerned with the perpetuation of the fisheries, to be able to recognize depletion, to know how to prevent it, and how best to promote the fisheries.” Within a few years, biologists had stated that sardines were in danger of overfishing, and that this was also true for several other fisheries, including California halibut, Pacific barracuda, and white seabass, all in southern California (Thompson and Higgins, 1923; Craig, 1927; Clark, 1931). Clark (1931) noted that the tendency for fishermen to build larger vessels and make multi-day trips was directly due to overfishing of local stocks. Until the 1930s, little attempt was made to understand marine recreational fisheries. However, during that period it became clear that recreational anglers caught large numbers of

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fishes and that estimates of this catch were necessary. As noted by Clark and Croker (1933), “from time to time controversies have arisen as to whether the sportsmen or the commercial operators are taking the greater part of the total catch...It became the duty of the California Division of Fish and Game to determine the quantities of fish caught by marine sport fishermen in order that its conservation program be administered wisely.” In 1932, a pilot system was initiated in which party vessel and barge operators and pier concessionaires were requested to keep a count on the fishes taken each day. Because these voluntary reports were undependable, in 1936, new laws mandated daily catch reports (reported monthly to the state) by skippers of party vessels (it appears that the barge and pier reports were not a success). Croker (1939), commenting on the first three years of the program, stated that “Even with a law to support the program, it is not always easy to convince the boat operator of the desirability of good reports, and frequently diplomacy is necessary and once in a while an arrest must be made.” These early problems notwithstanding, the system begun in 1936 is still in operation today. Log accuracy has always been a question and appears to be greatest for charismatic species, such as yellowtail or white seabass, and less accurate for some other species (Baxter and Young, 1953). Nevertheless, despite its weaknesses, the log system has made it possible to reasonably track broad changes in the CPFV fishery. Looking back on this era, several things are clear. First, even when there was virtual unanimity in the scientific community, particularly in the Division of Fish and Game, regarding overfishing, economics ruled fisheries management. The state legislature and other regulatory bodies were loath to either end a fishery, or even decisively reduce its size. Second, those fishery laws that were passed tended to make fishing less efficient through 1) area closures, 2) closed seasons, 3) gear restrictions, or 4) size restrictions. There was little or no attempt either to set specific quotas or limit the number of fishermen. As W. L. Scofield, one of the preeminent DFG biologists noted, “What is probably the most effective restriction has not as yet been applied to California, that is, the direct limitation of total catch by the establishment of boat catch limits or regional or state-wide bag limits for a season” (Scofield, 1951).

1951 to 2001 In 1900, a commercial fisher needed little more than a fishing license, a way to catch fish and a baloney sandwich. In 2000, a fisher’s life was much more complicated and baloney had been found to harden the arteries. Indeed, looking back from the twenty-first century, some aspects of the California commercial fisheries are almost unrecognizable. Management practices changed little during the1950s, 1960s and 1970s. Indeed, except for small adjustments in various fisheries, management was much the same as it had always been. This included, with the collapse of the Pacific mackerel fishery in the mid-1960s, the same inability on the part of the California Legislature to effectively deal with overfishing. This obvious truth was made clear in a paper by the well-known fisheries biologists J. L. Baxter, J. D. Isaacs, A. R. Longhurst, and P. M. Roedel. Writing about the collapse of the Pacific mackerel, they stated, “Parenthetically we note that the stakes in scientific management are greater than the potential yield of the Pacific mackerel fishery. Despite scientific evi-

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dence attesting to the Pacific mackerel’s decline, presented over many years, no action has yet been taken which might rehabilitate this resource. This prima facie evidence substantiates allegations that the State cannot manage its resources on a scientific basis” (Baxter et al., 1967). Ultimately, the largest shift in how California fisheries were managed had its genesis in the wave of federal environmental legislation of the late 1960s and 1970s that began to view the environment from an ecosystem perspective, rather than a series of constituent parts. It was the Magnuson Act of 1976 and the later reauthorized and broadened Magnuson-Stevens Act of 1996 that had the most profound effect. Partially driven by a fear of foreign vessels fishing off U. S. coasts, the Magnuson Act excluded foreign fishermen within 200 nautical mile of the coast, except for extraordinary circumstances. It also created a system for the monitoring and management of the fish stocks and set in motion a process that eventuated an American take over of harvesting and processing from foreign fleets. The 1976 Act also created a system of regional fishery management councils that were to act as forums for states and user groups; fisheries off California fall under the jurisdiction of the Pacific Fisheries Management Council (PFMC). In addition, the Act required that fishery management plans be drawn up to protect fish stocks. Among a number of important new developments, the Sustainable Fisheries Act (SFA), part of the 1996 reauthorization, redirected U.S. fisheries policy away from promoting fishery growth and toward conservation and sustainability of those fisheries. For the first time, managers were specifically directed to protect essential fish habitat from the adverse effects of fishing. In addition, the SFA required Management Councils to consider the plight of the fishing industry and dependent communities in their management decisions (Weber and Heneman, 2000). Over time, Magnuson and later Magnuson-Stevens have had a considerable effect on both fisheries and fishermen. For the first time, through the management plans developed for salmon, pelagic coastal species (jack mackerel, northern anchovy, Pacific mackerel, Pacific sardine), and groundfishes (flatfishes, lingcod, Pacific cod, Pacific whiting, rockfishes, sablefish, and thornyheads), limited entry fisheries were created, individual trip limits were enacted and quotas for entire fisheries were establish. Recently, both the PFMC and Congress have entered new management territory by introducing a limited observer program on commercial vessels, as well as discussing individual quotas and, in the groundfish fishery, capacity reduction through buyback programs. The sometime labyrinthine degree of complexity and control exacted on fisheries by the PFMC can be seen in the chinook salmon fishery. Commercial fishermen may only harvest chinook salmon with trolling gear, using barbless hooks. In 1983, in order to decrease competition among fishermen and to reduce fleet size the fishery was made limited entry by a moratorium on new entrants. There are minimum size limits and a limited season with various time and area closures. The difficulties faced by the Council in this effort is well summed up in California Department of Fish and Game (2000), “In 1999, the PFMC again enacted restrictive commercial and recreational ocean salmon regulations in California to achieve 1) the escapement goal for Sacramento River fall chinook salmon of 122,000 to 180,000 hatchery and natural adults combined; 2) a 12.3% exploitation rate on age-4 Klamath River fall chinook salmon to accommodate inriver [sic] recreational and tribal subsistence and commercial fisheries . . . 3) a 31% increase in adult spawner replacement rate for

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endangered Sacramento River winter chinook salmon relative to the observed 1989–93 mean rate.” Unfortunately, despite a number of efforts to control fisheries, the PMFC was unable to prevent widespread overfishing of a number of species, including bocaccio, cowcod, canary, widow, darkblotched, and yellowtail rockfishes, Pacific ocean perch and lingcod. This failure, certainly not limited to the Pacific Council or to the Council system in general, occurred through a combination of events. However, it is clear that among other factors, inaccurate models of optimal catch, bitter resistance from fishermen to any lowering of quotas and reluctance on the part of Council members to cause economic hardship, all played a role. The result is that under some rebuilding scenarios, some of these species will not return to fishable levels for many decades. It is important to note that California must make its management plans consistent with those of the federal government. In many instances, for those species for which management plans exist, federal regulations supplant those of the state and this has created a veritable tidal wave of new recreational regulations. Unlike the closely scrutinized commercial fisheries, California marine recreational fisheries were essentially unregulated until the 1950s. The earliest laws came into effect in last few years of the 1940s and these set the pattern for the next 50 years. Virtually all of the regulations dealt with limiting daily individual retention, through bag limits, or preventing large catches of immature fishes, through minimum size limits. Except for grunion and salmon caught in ocean waters, until recently there have been very few closed seasons and almost no tackle restrictions. And, while minimum size limits clearly had a biological basis, until the late 1990s daily bag limits did not. Bag limits were created to minimize fish wastage that occurred when anglers caught, and retained, more than could be used. Biological considerations, such as sustainable yield, were not considered (Miller and Gotshall, 1964). With the exception of garibaldi, and later giant sea bass, no species were prohibited from all take. However, in the 1990s, there was undeniable evidence of depletion in the rockfish and lingcod populations of California, including declarations from the National Marine Fisheries Service that some of these species were officially overfished. In response, the PMFC passed regulations drastically reducing the overall catch of these species and these regulations impinged not only on the commercial catch, but also on those of recreational anglers. As part of the same process that began to restrict commercial groundfish fisheries, California substantially lowered bag limits on rockfishes, closed seasons for rockfishes and lingcod and participated in the creation of the Cowcod Closure Areas, comprising 4,300 square miles of offshore banks in southern California. Clearly, for the first time in California history, management of commercial and recreational fisheries was viewed as two sides of the same coin. Lastly, two acts passed by the California legislature also signaled that a new day had dawned in fisheries management at the state level. The Marine Life Management Act (MLMA) of 1998 was the first act that attempted to create integrated fisheries management in California. Weber and Heneman (2000) summarized the act by noting that it “...applies not only to fish and shellfish taken by commercial and recreational fishermen, but to all marine wildlife....the MLMA was intended to shift the burden of proof toward demonstrating that fisheries and other activities are sustainable.....while the Legislature

retained its control over some of the State’s commercial fisheries, it gave the [Fish and Game] Commission new authority.” The Act was far-reaching and had several underlying goals. Chief among these was the concept of conserving entire ecosystems rather than focussing on one species. The Act also held that marine life need not be consumed to provide important benefits to citizens and that fisheries, should they be allowed, must be sustainable in the long-term. Noting that some fisheries were depressed, it called for specific rebuilding plans and for habitat maintenance, restoration or enhancement. Clean fishing, one that limits or eliminates bycatch, was to be encouraged. Lastly, the Act recognized that fisheries management may have negative impacts on fishermen and their communities and provided for minimization of these impacts (Weber and Heneman, 2000). In 1999, California passed another act that would alter marine fishing practices. The Marine Life Protection Act (MLPA), while not specifically directed toward fisheries management, required that the Department of Fish and Game develop a plan for establishing networks of marine protected areas in California waters to protect habitats and preserve ecosystem integrity. Supported by a number of conservation, diving, scientific and education groups, and some fishing interests, the MLPA, by preventing some fishing activities along the coast, would also influence marine fisheries.

The Competition between Recreational and Commercial Fishermen We have before us the fiendishness of business competition. . . (Karl Barth)

For many years, recreational anglers and commercial fishermen battled over resource allocation. And, in the early days of the twenty-first century, California recreational anglers and commercial fishermen still found themselves engaged in an intense competition for fishes. This competition was played out in the print media, over the airwaves, on the internet, in the courthouse and in legislative bodies. The battle was heightened by the often correct perception that some fish stocks are at alarmingly low levels. For a blissfully short period, when few fished California’s waters, there was little hostility among the two communities (Holder, 1913). Gradually, however, recreational anglers perceived a decline in the fish populations, and, in a pattern repeated over the years, laid the blame solely on commercial fishermen. Writing of Santa Catalina Island, Holder (1914) wrote “The angling here in 1886 to 1900 was the most remarkable in the world . . . but with the coming of power boats the seines, trawls and other nets, the fisheries began to decrease until it was evident that something must be done. The most menacing danger was the alien who attached a gill net to the kelp and ran it out into the sea. . . . I believe in developing all the sea products, intelligently, saving for the people everything that can be used; but it is very evident that the people cannot trust the army of alien market fishermen to conserve American interests.” Additionally, Holder (1913) makes a second argument that is still used in the current debates, when he writes “In the meantime from fifty to one hundred angling boatmen established themselves at Avalon, representing with various industries, dependent upon angling, a investment of three quarters of a million dollars.” These same sentiments, with its scarcely-hidden racist, or at least nativist slant, were repeated 16 years later in Thomas

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and Thomas (1930), “To insure a continuance of our Pacific fish, both for food and sport purposes, the entire Southern California coast should be kept reasonably free of live-bait [hook and line commercial vessels] and net boats. It is unreasonable and wasteful to allow one industry to destroy the fish of California’s southern coast, thereby hurting other interests. When one considers that the men doing the actual fishing often are foreigners—either Japanese or Europeans— many of who cannot speak English, the need for protection is intensified.” The Department of Fish and Game first publicly noted the potential for rivalry between the industries when Croker (1939), writing of the surging party vessel fishery noted, “This new fishery has brought its problems, particularly as it competes with the long-established commercial fishing industry for the same fishing grounds and the same kinds of fish.” Interestingly, until 1947, the distinction between recreational angler and commercial fisher was blurred as it was legal and, in fact, common for recreational anglers aboard party vessels to sell their catch or give them to crew members for later sale. In addition, it was common for crews of party vessels to use the vessel for commercial fishing during the down season (Croker, 1939; Ries, 1997). However, it was Ray Cannon, writing in the years just following the collapse of the sardine industry, in How to Fish the Pacific Coast (1953), who gave the clearest direction yet of the impending battle. “The absolute necessity for outdoor recreation for the well-being of our citizenry is no longer theory; scientific facts have proven it. . . . We must regulate or halt every fish-depleting force or agency. In regulating commercial fishing we already have enough scientific facts to warrant rigid management. In cases where a fish population is suspected of being reduced, commercializing it should be halted until research proves it has regained its former abundance, plus a surplus...There is a total lack of wisdom shown in holding angler daily-bag-limits down to two-to-ten fish, while allowing commercials to capture whole schools, and as often as they can.” Thus, for much of the last 100 years, the recreational angler’s view has been that 1) any depletion is caused by commercial fishermen, 2) recreational angling is somehow on a higher moral plain than commercial fishing, and 3) recreational angling has a greater economic importance to California. Historically, the response from commercial fishermen has been to either deny that depletion was occurring and/or either deny or minimize their role in it. In addition, the prevailing philosophy among commercial fishermen was nicely summed up in a letter by a former commercial fisherman to the industry publication National Fishermen. Commenting on the allocation conflicts he stated that, “Of all of us, the commercial fishermen have the highest right to the resource, because without them, none of us would eat fish. They should come first in considering the management of the resource.” In the 1950s and 1960s, the inherent tensions between the two industries were publicly voiced on only rare occasions. In the late 1950s, for instance, anglers in Monterey and Morro Bays believed that commercial trawling operations were responsible for a decrease in CPFV rockfish catches. California Department of Fish and Game studies demonstrated that the recreational fishes of that time targeted inshore species, such as blue and olive rockfishes, while trawlers worked offshore and caught bocaccio, chilipepper and other deeper-water

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forms. At about the same time, pier anglers on the Cayucos pier (located just north of Morro Bay) believed that live bait haulers using lampara nets were threatening pier fishing success; CDFG surveys showed that this, too, was incorrect. Ironically, when skin and scuba diving first became popular, hook-and-line recreational anglers also voiced fears regarding competition from the early spear fisher (Heimann and Miller, 1960; Heimann, 1963; Miller and Gotshall, 1965). Beginning in the 1960s, but particularly in the 1970s and 1980s, the long-simmering conflict between recreational and commercial user groups greatly intensified; this escalation of hostilities had a number of causes. First, this period saw a rapid rise in the number of recreational fishermen, particularly those relatively affluent fishermen who owned private vessels and fished aboard CPFVs. In addition, the ultimately successful attempt to develop a northern anchovy reduction fishery, despite the great fears of recreational anglers who remembered the demise of the Pacific sardine, gave public voice to nascent anti-commercial fishing sentiments. And during the same period, the well-publicized foreign fishing fleet operating just off the coast was a constant reminder of external competition for fishes. It was the burgeoning gill net fishery, however, initially spearheaded by newly arrived Vietnamese fishermen that galvanized the anti-commercial fishing community. During the mid-1970s, immigrant Vietnamese fishermen settled in California, first in central California, operating out of Monterey ports, but soon in southern California. Lacking funds to purchase large fishing vessels, these fishermen were only able to acquire small boats, often ones originally designed for recreation. After their arrival, most of these fishermen began using gill nets, particularly those made of monofilament, because, as noted by Orbach (1983): 1) they were previously familiar with that method, 2) it did not require large vessels or expensive equipment, 3) it was relatively inexpensive to purchase, and 4) because many Vietnamese started fishing for relatively unpopular species, such as white croaker, gill nets allowed the Vietnamese to avoid competition with established U.S. fishermen. It should also be noted that the Vietnamese tended to set out nets that were two or three times as long as those used by U.S. fishermen. These new fishermen brought gill netting into the public eye. Nets were often set in shallow waters, off popular beaches. In some areas, these nets caught large numbers of seabirds, whose dead bodies washed up on those beaches. In contrast to most traditional fisheries, fishes were routinely offloaded in recreational launch areas. Many established fishermen quickly saw the new potential for gill nets and they, too, began using this gear. At the same time, great publicity was given to bycatch problems, including marine mammals, sea birds and turtles, associated with drift gill nets in the central Pacific. This combination of factors culminated in considerable anti-gill net sentiment, among both recreational anglers, who clearly saw these nets as competition for desired species, and some members of the general public, many of whom were concerned about marine mammal and sea bird by-catch. The initial response by angler associations was to push for passage in the California legislature of a bill limiting gill net fisheries. When that bill failed, angler groups and some environmental organizations went through the initiative process resulting in the placement on the ballot of Proposition 132 (the Marine Resources Protection Act of 1990), that prohibited the use of gill nets within three miles of the mainland coast in

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southern California and within one mile of the Channel Islands. During the ensuing campaign, the initiative’s proponents emphasized the putative damage to marine mammal populations, despite biological studies indicating that marine mammal populations were healthy and expanding in the presence of gill net fisheries. However, it is likely that the clear subtext for most recreational anglers was that gill nets were harming recreational fish populations. Parenthetically, it should be noted that studies by the Department of Fish and Game implied that gill net activity was having little appreciable affect on the catch of most recreational species (Vojkovich et al., 1990). In 1990, voters passed the ballot initiative. In limiting a form of commercial fishing, Proposition 132 represented a defining moment when recreational anglers and their allies clearly showed their strength. The victory had a certain energizing effect on the recreational industry; it made them more willing to confront commercial fishermen in the public arena. While the trawling industry had come in for its share of criticism, it was the nearshore live-fish fishery that is seen as the most direct competitor. Many recreational anglers would prefer to see commercial fishermen driven out of the nearshore altogether or at least limited to very low quotas. However, circumstances, in the form of the reauthorized Magnuson-Stevens Act, The Marine Life Management Act and The Marine Life Protection Act, have changed the dynamics of the debate. A major effect of these acts is to link these once-separate industries together because fisheries managers have begun to understand that both industries contribute to overfishing, although the degree of responsibility varies with the fishery. Clearly, commercial fishing was responsible for overfishing Pacific mackerel, canary rockfish, and angel and thresher sharks. However, localized depletion of nearshore rockfishes by recreational anglers was well underway long before the birth of the commercial live fish fishery (Love, 1978). Regarding rockfishes, and perhaps lingcod, it might be argued that in some locations commercial fishermen first take the majority of fishes, but that recreational anglers continue to keep the populations low. As Love et al. (1998a) noted, “While commercial vessels often stop fishing an area when it is economically non-viable, recreational vessels do not. This is exemplified by the importance [in the southern California CPFV rockfish catch] of squarespot rockfish and other small species . . . On some trips most of the rockfish catch now comprises either dwarf or small species or juvenile rockfishes. Thus CPFVs tend to continue fishing reefs that harbor few, if any, larger rockfishes thereby preventing a rebound in populations.” Perhaps because of their century of rancor, it is ironic that at the beginning of the twenty-first century both the commercial and the CPFV industries found themselves almost equally under siege. In the face of clear evidence of overfishing, governmental actions in the form of drastically reduced quotas, closed seasons, and area and gear restrictions put severe pressure on both industries, placing their viability into question. In particular, the specter of marine protected areas threw together recreational and commercial entities. New Zealand recreational and commercial fishermen faced with a movement to create reserves responded with “Everyman has a right to catch a fish”, precisely the philosophy of a number of California anglers and fishermen. However, it should be noted that, despite some misgivings, New Zealand is moving ahead with reserve designations.

What some members of both industries failed to see was that Californians lived on the edge of an increasingly urban sea. The vision on the part of some commercial and recreation fishermen of operating on some unsullied frontier was untrue. It was now difficult to ignore the interests of nonconsumptive parties, such as recreational (non-spearfishing) divers, boaters and marine mammal and bird watchers, if only because they represented an increasingly powerful political voice. Obviously, it was, and will be, in the best interests of both consumptive and nonconsumptive groups to work together. As might be imagined, given their very diverse and in some cases opposing interests, this had often proven exceedingly difficult, although on occasion these parties had breached their instinctual distrust. For instance, salmon rehabilitation projects throughout the state had benefited from the cooperation of recreational anglers, commercial fishermen and environmentalists. In the future there is the real possibility that some non-governmental organizations will take management and marine reserve matters into their own hands if the contestants cannot work together. In California, it is relatively easy to bring citizen-sponsored initiatives onto the state ballot. It would be ironic, for instance, if recreational anglers, who spearheaded the anti-gill netting initiative Proposition 132, were to find 50% of the coastline unavailable to fishing through an initiative sponsored by another interest group. In the long-term, the citizens of California have to decide what they want in their marine systems; these are societal rather than scientific issues. Society will have to decide how much underwater wilderness it wants. Society will have to decide how much fish stock depletion it will tolerate. And society will have to decide how best to achieve these goals. If citizens want to have a set of more “natural” or wilderness-like marine ecosystems, then greater protection will have to be afforded and this will be at the expense of both recreational and commercial fisheries. If it is deemed most important to have relatively unfettered recreational and/or commercial fishing opportunities or if it is decided that vastly degraded fish stocks are acceptable, then the requisite laws can be altered to allow this. Before any competent decisions are made, it is important to have an understanding of fish populations and the status of major marine habitats. At the present time, there are no stock assessments for many of the economically important species, such as kelp bass, barred sand bass, spotted sand bass, California halibut, all of the nearshore rockfishes, most of the deepwater rockfishes, sea and surfperches, and black sea bass. An assessment of most nearshore and virtually all offshore habitats has not been conducted. There is also little analysis of the social or economic costs of various management options. A rational decision making process demands that this data be acquired. All of this will have an effect on the fate of both commercial fishing and recreational angling. Barring some unforeseen circumstance, it is likely that both industries will continue well into the future, albeit with substantial changes. Through the marine reserve process, both industries will be excluded from some traditional fishing grounds, although which grounds and what form of exclusion remains to be determined. Through attrition, governmental buyouts or governmental regulations, some commercial fisheries will shrink in size. It is likely that commercial fishermen will face additional restrictions on, or even banning of, some gear as well as additional reductions in some quotas. Spatial management for

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non-pelagic species and more output management (such as Individual Transferable Quotas) are also likely to occur. Recreational fishing will also evolve. Shore-based and pier fisheries will likely see little changes. However, continuing catch restrictions and the creation of marine reserves will impact CPFV and private vessel fisheries. Half day CPFV trips appear to be gaining in popularity, both with anglers and operators. As fuel costs rise, these shorter excursions to nearby fishing grounds keep expenses, and fares, down. Marine angling, particularly from CPFVs, seems to have peaked in the late twentieth century and will probably continue to trend downward, at least as a percentage of the state’s overall population. Purely as a way of maintaining some stocks, catch and release, once the bete noir of the CPFV industry, may become more popular. Lastly, as their economic clout diminishes, it is quite possible that the power of both the commercial and recreational industries will continue to be marginalized.

Acknowledgments I would like to thank Peter Paige for information of Native American subsistence fisheries and Chris Dewees, Kevin Hill, Ed Melvin, Peter Paige, Tim Thomas, and Diana Watters for helping me understand some of the nuances of the California fishing industries.

Literature Cited Anon. 1914. History of Pacific by-products industries. Pac. Fish. 12(6): 17–18. ———. 1918a. Fishing restrictions relaxed. Pac. Fish. 16(6):63. ———. 1918b. Modifying California fish laws. Pac. Fish. 16(4):17. ———. 1938. Must the scientist always be on the defensive? Calif. Fish Game 24:290–293. Arnold, J. E. 1995. Transportation innovation and social complexity among maritime hunter-gatherer societies. Amer. Anthropol. 97: 733-747. Baxter, J. L., J. D. Isaacs, A. R. Longhurst and P. M. Roedel. 1967. Report of the CalCOFI committee. CalCOFI Rep. 12:5–9. Baxter, J. L., and P. H. Young. 1953. An evaluation of the marine sportfishing record system in California. Calif. Fish Game 39:343–353. Broughton, J. M. 1997. Widening diet breadth, declining foraging efficiency, and prehistoric harvest pressure: ichthyofaunal evidence from the Emeryville shellmound, California. Antiquity 71:845–862. Browning, R. J. 1980. Fisheries of the North Pacific. Alaska Northwest Publishing, Anchorage, AK. Bryant, H. C. 1921. A brief history of the California Fish and Game Commission. Calif. Fish Game 7:73–81. Bureau of Marine Fisheries. 1949. The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Dept. Nat. Res., Div. Fish Game, Fish. Bull. 74. California Department of Fish and Game. 2000. Review of some California fisheries for 1999: market squid, dungeness crab, sea urchin, prawn, abalone, groundfish, swordfish and shark, ocean salmon, nearshore finfish, Pacific sardine, Pacific herring, Pacific mackerel, reduction, white seabass and recreational. CalCOFI Rep. 41:8–25. Clark, F. N. 1949. Sardine, p. 27–31. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Dept. Nat. Res., Div. Fish Game, Fish. Bull. 74. Clark, G. H. 1931. The California halibut (Paralichthys californicus) and an analysis of the boat catches. Calif. Div. Fish Game, Fish Bull. 32. _____., and R. Croker. 1933. A method of collecting statistics of marine sport catches in California. Trans. Amer. Fish. Soc. 63:332–337. Clemens, H.B., and W.L. Craig. 1965. An analysis of California’s albacore fishery. Calif. Fish Game, Fish Bull. 128. Cobb, J. N. 1918. Increasing our Pacific Coast fishery resources. Pac. Fish. 16(11):9–10.

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Craig, J. A. 1927. Effect of the recent law prohibiting the taking of barracuda in California waters with purse seine or round haul nets. Calif. Fish Game 13:18–25. _____. 1928. The striped bass supply of California. Calif. Fish Game 14:265–274. Croker, R. S. 1933. The California mackerel fishery. Calif. Div. Fish and Game, Fish Bull. 40. _____. 1938. Historical account of the Los Angeles mackerel fishery. Calif. Div. Fish and Game, Fish Bull. 52. _____. 1939. Three years of fisheries statistics on marine sport fishing in California. Trans. Amer. Fish. Soc. 69:117–118. Daugherty, A.E. 1949. Commercial fishermen, pp. 200–202. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Davis, J. C. 1949. California salt water fishing. A. S. Barnes and Company, NY. Davis, M. K. 2000. Factories on the water: California’s floating reduction plants. The J. B. Phillips Historical Fisheries Report 1(1):9–12. Dewees, C. M., E. M. Strange, and G. Guagnano. 1990. Competing for the recreational dollar: an analysis of the California commercial passenger-carrying fishing vessel industry. Mar. Fish. Rev. 52(1): 1–6. Enea, R. 2001. The politics of the California sardine. The J. B. Phillips Historical Fisheries Report 2(1):2–14. Erlandson, J. M. 1991. Shellfish and seeds as optimal resources: early Holocene subsistence on the Santa Barbara coast. Perspective in California Archaeology 1:89–101. Erlandson, J. M. 1994. Early hunter-gatherers of the California coast. Plenum Press, NY. Erlandson, J. M., D. J. Kennett, B. L. Ingram, D. A. Guthrie, D. P. Morris, M. A. Tveskov, G. J. West, and P. L. Walker. 1996. An archaeological and paleontological chronology for Daisy Cave (CA-SMI-261), San Miguel Island, California. Radiocarbon 38:355–373. Fry, D. H. Jr. 1931. The ring net, half ring net, or purse lampara in the fisheries of California. Calif. Fish Game, Fish Bull. 27. Fry, D.H. Jr. 1932. Barge fishing, a southern California sport. Calif. Fish Game 18:244–249. Fry, D. H. Jr. 1949. Salmon, pp. 37–49. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Glassow, M. A. 1993. Changes in subsistence on marine resources through 7,000 years of prehistory on Santa Cruz Island, pp. 75–94. In: M. A. Glassow (ed.). Archaeology on the Northern Channel Islands of California. Coyote Press, Salinas, CA. Gobalet, K. W. 1990. Fish remains from nine archaeological sites in Richmond and San Pablo, Contra Costa County, California. Calif. Fish Game 76:234–243. ———. 1992. Inland utilization of marine fishes by Native Americans along the central California Coast. J. Calif. Great Basin Anthropol. 14:72–84. ———. 1994. A prehistoric sturgeon fishery in San Pablo, Contra Costa County, California: an addendum. Calif. Fish Game 80:125–127. Gobalet, K.W., and T.L. Jones. 1995. Prehistoric native American fisheries of the central California coast. Trans. Amer. Fish. Soc. 124: 813–823. Godsil, H. C. 1949. The tunas, pp. 11–27. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Greenhood, E. C. 1949. Yellowtail, pp. 146–148. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Greenhood, E. C., and J.G. Carlisco Jr. 1949. Swordfish, pp. 84–88. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Heimann, R.F.G. 1963. Trawling in the Monterey Bay area, with special reference to catch composition. Calif. Fish Game 49:152–173. Heimann, R.F.G., and D. J. Miller. 1960. The Morro Bay otter trawl and partyboatfisheries, August 1957 to September 1958. Calif. Fish Game 46:35–58. Henry, F. D. 1992. Sablefish, pp. 107–109. In: W. S. Leet, C.M. Dewees and California’s living marine resources and their utilization. W. Haugen (eds.), Calif. Sea Grant, UCSGEP-92–12. Holder, C.F. 1910. The Channel Islands of California. Hodder and Stoughton, London. Holder, C. F. 1913. The game fishes of the world. Hodder and Stoughton, New York.

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———. 1914. Attempts to protect the sea fisheries of southern California. Calif. Fish Game 1:9–19. Holmberg, E. K. 1949. California halibut, pp. 75–77. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Hughes, E. P. 1949. Pacific herring, p. 101. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Jacobson, L.D. 1992. Northern anchovy, pp. 81–83. In: California’s living marine resources and their utilization. W. S. Leet, C. M. Dewees and C. W. Haugen (eds.), Calif. Sea Grant, UCSGEP-92–12. Jordan, D. S. 1887. The fisheries of the Pacific Coast, pp. 591–630. In: The fisheries and fishery industries of the United States. G. B. Goode (ed.) U. S. Commission of Fish and Fisheries, Section 3. Jordan, D. S. 1892. The fisheries of California. Overland Monthly 20:469–478. Kato, S. 1994. Study of ethnic markets for California’s underutilized and undermarketed fish species. Calif. Seafood Council, Final Rep. Kennett, D. J., and J. P. Kennett. 2000. Competitive and cooperative responses to climatic instability in coastal southern California. Amer. Antiquity 65:379–395. King, C.D. 1990. Evolution of Chumash Society. Garland Publishing Inc., New York. Konno, E. S., and P. Wolf. 1992. Pacific mackerel, pp. 91–93. In: W. S. Leet, C. M. Dewees and C. W. Haugen (eds.), California’s living marine resources and their utilization. Calif. Sea Grant, UCSGEP-92–12. Leet, W. S., C. M Dewees, R. Klingbeil, and E. J. Larson. 2001. California’s living marine resources: a status report. California Department of Fish and Game, 592 p. Love, M. S. 1978. Aspects of the life history of the olive rockfish, Sebastes serranoides. Ph.D. dissertation. Univ. California, Santa Barbara. Love, M. S., B. Axell, P. Morris, R. Collins, and A. Brooks. 1987. Life history and fishery of the California scorpionfish, Scorpaena guttata, within the southern California Bight. U. S. Fish. Bull. 85:99–116. Love, M. S., J. E. Caselle, and W. Van Buskirk. 1998a. A severe decline in the commercial passenger fishing vessel rockfish (Sebastes spp.) catch in the southern California Bight, 1980-1996. CalCOFI Rep. 39:180–195. Love, M. S., J. E. Caselle, and K. Herbinson. 1998b. Declines in nearshore rockfish recruitment and populations in the southern California Bight as measured by impingement rates in coastal electrical power generating stations. U. S. Fish. Bull. 96:492–501. MacCall, A. D. 1996. Patterns of low-frequency variability in fish populations of the California Current. CalCOFI 37:100–110. McCully, H. 1949. Striped bass, pp. 51–53. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. McEvoy, A. F. 1986. The fisherman’s problem. Cambridge University Press, New York. Menzies, A. 1924. California journal of the Vancouver Expedition, 1790–1794. Calif. Hist. Soc. Quart. 2:265–340. Miller, D.J., and D. Gotshall. 1965. Ocean sportfish catch and effort from Oregon to Point Arguello, California. Calif. Fish Game, Fish Bull. 130. Norton, J. G., and S. J. Crooke. 1994. Occasional availability of dolphin, Coryphaena hippurus, to southern California commercial passenger fishing vessel anglers: observations and hypotheses. CalCOFI Rep. 35:230–239. Orbach, M. K. 1983. The “success in failure” of the Vietnamese fishermen in Monterey Bay. Coastal Zone Management Journal 10:331–346. Parrish, R. H. 2000. A Monterey sardine story. The J. B. Phillips Historical Fisheries Report 1(1):2–4. Phillips, J. B. 1949. Anchovy, pp. 89–90. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Fish Game, Fish. Bull. 74. Pinkas, L., J. C. Thomas and J. A. Hanson. 1967. Marine sportfishing survey of southern California piers and jetties, 1963. Calif. Fish Game 53:88–104. Raab, L.M., J.F. Porcasi, K. Bradford, and A. Yatsko. 1995. Debating cultural evolution: regional implications of fishing intensification at Eel Point, San Clemente Island. Pac. Coast Archaeol. Soc. Quarterly 31: 3–27. Richards, J. 1992. Pacific angel shark, pp. 46–48. In: W. S. Leet, C. M. Dewees and C. W. Haugen (eds.), California’s living marine resources and their utilization. Calif. Sea Grant, UCSGEP-92–12.

Rick, T.C. 1999. From sandy beaches to rocky shores: early Holocene fishermen of the California coast. Masters Thesis, University of Oregon, 68 p. Ries, E. 1997. Tales of the golden years of California ocean fishing. Friends of the Los Angeles Maritime Museum and the Los Angeles Maritime Museum Research Society. ———. 2000a. Fishing barges of California 1921–1998. Monterey Publications, Laguna Hills, CA. ———. 2000b. Origins of open party sportfishing in California. South Coast Sportfishing 6(11):76–77. Ripley, W. E. 1946. The soupfin shark and the fishery, pp. 7–38. In: The biology of the soupfin Galeorhinus zyopterus and biochemical studies of the liver. Calif. Fish Game, Fish Bull. 64. ———. 1949. Bottom fish, pp. 63–75. In: The Commercial Fish Catch of California for the Year 1947 with an Historical Review 1916–1947. Calif. Dept. Nat. Res., Div. Fish Game, Fish. Bull. 74. Salls, R. A. 1988. Prehistoric fisheries of the California Bight. Ph.D. Dissertation, University of California, Los Angeles. 760 p. ———. 1989. To catch a fish: some limitations on prehistoric fishing in southern California with special reference to native plant fiber fishing line. J. Ethnobiol. 9:173–199. Schwaderer, R. 1992. Archaeological test excavation at the Duncans Point Cave, CA-SON-348/H, pp. 55–72. In: T. L. Jones (ed.), Essays on the prehistory of maritime California. Center for Archaeological Research Publication 10. University of California, Davis. Scofield, N. B. 1914. The tuna canning industry of southern California, pp. 111–122. In: Fish and Game Commission 23rd Biennial Report. ———. 1921. Commercial fishery notes. Calif. Fish Game 7:174–177. Scofield, W. L. 1925. The 1924 commercial catch of fish in California. Calif. Fish Game 11:162–167. ———. 1938. Sardine oil and our troubled waters. Calif. Fish Game 24:210–223. ———. 1947. Drift and set line fishing gear in California. Calif. Div. Fish Game, Fish Bull. 66. ———. 1948. Trawling gear in California. Calif. Dep. Fish Game, Fish Bull. 72. ———. 1951. Purse seines and other roundhaul nets in California. Calif. Fish Game, Fish Bull. 81. ———. 1954. California fishing ports. Calif. Fish Game, Fish Bull. 96. ———. 1956. Trolling gear in California. Calif. Fish Game, Fish Bull. 103. Skinner, J. E. 1962. An historical review of the fish and wildlife resources of the San Francisco Bay area. Calif. Dep. Fish Game, Water Proj. Branch Rept. No. 1. Smith, H. M. 1895. Notes on a reconnoissance [sic] of the fisheries of the Pacific coast of the United States in 1894: sardines, anchovies, and sardine-canning. Bull. U. S. Fish Comm., vol. 14, pp. 227–230. Smith, S. E. 1979. Changes in saltwater angling methods and gear in California. Mar. Fish. Rev. 41(9):32–44. Spratt, J. D. 1992. Pacific herring, p. 86-89. In (W. S. Leet, C. M. Dewees and C. W. Haugen (eds.), California’s living marine resources and their utilization. Calif. Sea Grant, UCSGEP-92–12. Starks, E. C. 1918a. Phases of the campaign for sea foods. Pac. Fish. 16(7):11–12. ———. 1918b. Possibilities of the California fisheries. Pac. Fish. 16(2):27, 29–31. Strudwick, I. 1986. Temporal and areal considerations regarding the prehistoric circular fishhook of coastal California. M. S. thesis, Calif. St. Univ., Long Beach. 324 p. Thomas, G. C. Jr., and G. C. Thomas III. 1930. Game fish of the Pacific. J. B. Lippincott, Philadelphia. Thomson, C.J. 2001. Human Ecosystem Dimension. pp. 47–66. In: California’s Living Marine Resources: A Status Report. W.S. Leet, C.M. Dewees, R. Klingbeil and E.J. Larson, (eds.). The Resources Agency. The California Department of Fish and Game. University of California. Thompson, W. F., 1921a. Historical review of California sardine industry. Calif. Fish Game 7:195–206. ———. 1921b. The future of the sardine. Calif. Fish Game 7:38–41. ———. 1922. The fisheries of California and their care. Calif. Fish Game 8:165–177. Thompson, W. F., and E. Higgins. 1923. Review of Dr. Skogsberg’s report on the purse seine fisheries of California. Calif. Fish Game 9:87–98. Ueber, E. 1988. The traditional central California setnet fishery. Mar. Fish. Rev. 50(2):40–48. Van Deventer, W. C. 1926. Barge fishing on the southern California shelf. Calif. Fish Game 12:19–20. Vojkovich, M., K. Miller, and D. Aseltine. 1990. A summary of 1983–1989 southern California gill net observation data with an

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overview on the effects of gill nets on recreational catches. California Department of Fish and Game. Warren, C. 1968. Cultural tradition and ecological adaptation on the southern California coast. Eastern New Mexico University Contributions to Anthropology 1:1–14. Weaver, P. Jr. 1892. Salt water fisheries of the Pacific Coast. Overland Monthly 20:149–163. Weber, M. L., and B. Heneman. 2000. Guide to California’s marine life management act. Common Knowledge Press, Bolinas, CA.

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Wilcox, W. Z. 1902. Notes on the fisheries of the Pacific Coast in 1899. Rep. U.S. Comm. Fish. 1901, pt. 27, pp. 501–574. Wine, V., and T. Hoban. 1976. Southern California independent sportfishing survey. Calif. Dep. Fish and Game, Ann. Rept. Wolf, P., and P.E. Smith. 1992. Pacific sardine, pp. 83–86. In: California’s living marine resources and their utilization. W.S. Leet, C.M. Dewees and C.W. Haugen (eds.). Calif. Sea Grant, UCSGEP-92–12. Young, P. H. 1969. The California partyboat fishery 1947–1967. Calif. Dept. Fish and Game, Fish Bull. 145.

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CHAPTER 23

Pollution M. JAM E S ALLE N

Introduction The California coast has been a focal point of human activity since the arrival of native Americans more than 10,000 years ago. While these early inhabitants may have fished some local populations heavily, they contributed little pollution and habitat alteration that might affect marine fishes. Although alteration of terrestrial habitats increased from the late 1700s onward with increasing non-native populations, significant marine habitat alteration did not begin until the mid-1800s. During the twentieth century, the production of fishing piers, alteration of coastal lagoons, and construction of artificial harbors and marinas along the coast began in earnest while rivers and streams were channelized to prevent flooding (Dailey et al., 1993). As the population centers grew, pollution problems arose as waste contaminants were discharged directly into the sea or into the waterways leading to the ocean. However, it was not until the late 1960s that the public became aware that increasing levels of pollution and increasingly altered coastal habitats might be having a detrimental effect on fish populations. With this awareness came scientific interest and political necessity for assessing and understanding the effects of pollution and habitat alteration on marine fish populations (Mearns et al. 1988, 1991; Kennish, 1998). At present, the coastal population of the Californias is distributed unevenly with high population centers in southern California and in the San Francisco Bay area, and low populations along much of the rest of the coast. In 2000, more than 20 million people were living in the coastal areas of southern California and Tijuana, Baja California, Mexico and about 7 million in the San Francisco Bay area (USCB, 2001). Because of the high human population densities in these areas, these are the primary areas of pollution and habitat alteration that has affected fish populations. This chapter describes the nature and effects of pollution and habitat alteration effects on California marine fishes. Effects of commercial and recreational fishing are discussed in chapter 22.

Marine Pollution in California Contaminants of Concern Human activities along the California coast and on the ocean itself contribute chemical contaminants, oil, and anthropogenic

debris to the marine environment. These pollutants may cause detrimental effects to individual fish, their populations, or to fish predators. Chemical contaminants that are of concern to fish biology or to the health of human or wildlife consumers include trace metals (e.g., arsenic, mercury, selenium, cadmium), chlorinated pesticides, such as DDT (dichlorodiphenyltrichloroethane) and its isomers and metabolites, chlordane, dieldrin; PCBs (polychorinated biphenyls); and PAHs (polycyclic aromatic hydrocarbons). These contaminants are of concern due to their toxicity (acute and chronic) to fish at different life stages, potential effects on their populations, and their bioaccumulation in fish tissue and the resultant health risks to wildlife or human consumers. Oil spills sometimes foul the ocean over large areas, subjecting fish at different life stages to altered ocean conditions, tar, and PAHs. Plastic bags and pellets are hazards to larger fish when they are mistakenly consumed as prey, and fish sometimes are entangled or encumbered with rubber bands, plastic packaging, and abandoned or lost fishing gear (e.g., nets, traps, set lines).

Sources of Contaminants to the Marine Environment Contaminants enter the marine environment from a variety of sources, including municipal wastewater discharge; industrial discharges, storm drains, streams, and rivers; aerial fallout; marine vessel activity; ocean dumping; oil exploration and extraction; and oil spills (Mearns et al., 1991, Anderson et al., 1993, Kennish, 1998, Schiff et al., 2000). The types of contaminants discharged vary by source. Chemical contaminants (e.g., trace metals, chlorinated pesticides, PCBs, PAHs) enter the ocean from most of the sources mentioned, although oil drilling activities and oil spills introduce a more restricted list. From the late 1940s to the late 1980s, municipal wastewater discharge was a major source of contaminants to the Southern California Bight (SCB). Of greatest concern was the discharge of DDT in southern California from the primary manufacturer of this pesticide in the United States. Extremely high levels of DDT produced by Montrose Chemical Company were discharged off the Palos Verdes Peninsula in municipal wastewater effluent from 1947 to 1970. Similarly, high levels of PCBs and metals were discharged at this site during this

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period. However, high levels of PCBs were also discharged from other wastewater dischargers in southern California during this time period. With the ban of discharge of DDT and PCBs in the early 1970s and with improved effluent quality (the net result of source control and changes to treatment process), the combined mass emissions of these and other chemical contaminants from the four major wastewater dischargers decreased greatly, such that all in southern California are now meeting California State Ocean Plan requirements. Contaminant inputs from all sources have decreased by 70% (Schiff et al., 2000). Although wastewater discharge is no longer a major source of contaminants in southern California, some environmentally persistent contaminants from historical discharges are still high in sediments on the Palos Verdes Shelf and in Santa Monica Bay (Anderson et al., 1993, Schiff et al., 2000). These historically deposited sediments are now a primary source of DDT and an important source of PCBs to the Southern California Bight. Although the quality of the effluent discharged to the ocean has improved, the coastal human population in southern California is increasing at a rate of about 3.5 million people per decade and contamination from urban runoff (which, with few exceptions, is untreated) has become a major concern. Oil intermittently enters coastal waters from a number of sources. Oil spills result from tanker leaks and occasionally from drilling operations. Some is also discharged in storm water or from marine vessel activity (Anderson et al., 1993). Natural oil seeps (e.g., in the Santa Barbara Channel, and Santa Monica Bay) are also important chronic sources. In addition to chemical contaminants, a wide variety of anthropogenic debris (primarily plastics) enters the ocean in storm water, from fishing and marine vessel activity, and from public use of beaches (Moore and M. J. Allen, 2000, Moore et al., 2001). Similar sources of contaminants exist in the San Francisco Bay area. In addition, the Bay is the receiving water for contaminants from the extensive agricultural regions of the Delta and Central Valley for which it serves as a sink (Kennish, 1998). Chemical contaminants enter San Francisco Bay from wastewater discharge, urban and non-urban runoff, dredging, and rivers. Major areas of marine pollution (and hence of contaminated fish) in coastal United States occur along the West Coast in southern California, San Francisco Bay, and Puget Sound, Washington, with much less in coastal areas between these regions (Mearns et al., 1988). On the East Coast, important areas of marine pollution occur in the New York Apex and Boston Bay, although fish contaminated at lower levels occur in estuarine and coastal areas from New England to Georgia. On the Gulf Coast, fish with low-level contamination are found from southern Florida to southern Texas. By the early 1970s, DDT in Palos Verdes Shelf sediments were the largest known area of DDT contamination in the world. Thus coastal fish near the Palos Verdes area in southern California typically had the highest levels of DDT from the late 1960s to early 1980s (fig. 23-1). Nevertheless, relatively high DDT concentrations have been found in southern Texas (Laguna Madre), San Francisco Bay, Puget Sound, Boston Bay, and various other locations along all coasts. In the 1970s, fish muscle tissue with concentrations above 0.500 ppm extended from Gray’s Harbor, Washington to the U.S.-Mexico border. In contrast to many other areas where highest DDT concentrations were in estuarine fish, highest DDT concentrations off southern California were in coastal fishes (Mearns et al., 1988).

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Fates of Contaminants The repositories of contaminants in the ocean off California are the water column, sediments, or marine organisms (Anderson et al., 1993, Schiff et al., 2000). Contaminants that enter the ocean from the various sources are distributed by ocean currents and eddies. While some remain dissolved, most are physically or chemically bound to particulate matter and settle to the bottom, resulting in contamination of the sea floor sediments. Contaminants flow to organism repositories through food-web pathways within the water column and benthic habitats resulting in bioaccumulation in fish and other organisms. The degree to which bioaccumulation occurs depends on the solubility, particle affinity, oxidation state, volatility, degradability of the chemicals. These differences influence how contaminants are distributed along the California coast and within biological communities. WATE R C OLU M N

In the water column of the SCB, near surface waters (0–200 m) are density stratified with strong vertical gradients of contaminants (Eganhouse and Venkatesan, 1993, Schiff et al., 2000). Natural (e.g., kelp) and anthropogenic debris (e.g., plastics) are most visible at the sea surface. At the surface, the sea-surface microlayer (
1 mm thick) greatly concentrates bacterioneuston, phytoneuston, and zooneuston, as well as anthropogenic contaminants (e.g., DDTs, PCBs, PAHs, chromium, copper, iron, lead, manganese, nickel, silver, and zinc) (Cross et al., 1987, Schiff et al., 2000). For example, concentrations of some trace metals, chlorinated hydrocarbons, and PAHs in the microlayer were much higher in Los Angeles–Long Beach (LA/LB) Harbors than in other nearshore locations, suggesting sources within the harbors. The distribution of high concentrations in sediments away from wastewater outfalls suggests transport of sewage particulates in the water column by currents (Zeng and Venkatesan, 1999). Dissolved contaminants (e.g., DDT, PCB, and PAHs) are generally found in very low concentrations in the water column but are generally higher above contaminated sediments, indicating fluxes between sediments and the water column. S E DI M E NTS

Sediments are major repositories of contaminants in the marine environment. In southern California, high levels of sediment contamination occur on the Palos Verdes Shelf, Santa Monica Bay, and San Diego Bay (Schiff et al., 2000). Sediments on the Palos Verdes Shelf and Santa Monica Bay are high in DDTs, PCBs, and many trace metals whereas San Diego Bay sediments are high in PCBs and PAHs (Mearns et al., 1991). Contaminants in sediments are generally highest near their sources. The discharge of 1,800 metric tons of DDT onto the Palos Verdes shelf between 1953 and 1970 created what may be the largest known area of DDT contamination in the world. Sediment concentrations of  200 ppm [parts per million  mg/kg] DDT and 10 ppm PCBs were found in sediments there in the early 1970s (MacGregor, 1976). Although surface sediment concentrations of DDT have decreased since the 1970s, the highest sediment concentrations are still on the Palos Verdes Shelf (Schiff et al., 2000; Connolly and Glaser, 2002). As of 1992, about 67 metric tons of p, p’–DDE occurred in the sediments of the Palos Verdes Shelf, with 76% of this occurring at water depths of 30 to 100 m with the highest concentrations (300 ppm) 30 cm below the sediment surface (Stull, 1995). Due to upcoast flowing currents

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F I G U R E 23-1 Total DDT in a) liver and b) muscle of coastal and estuarine fish from 19 sites sampled in 1976 and 1977. Bar represents mean of all individual or composite values for all species collected at a site (after Mearns et al. 1988).

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at the discharge depth (61 m), DDT concentrations in sediments at the Palos Verdes shelf decrease upcoast of the discharge site, with much lower levels downcoast of the site. Overall, highest concentrations of PAHs are found in San Francisco Bay and San Diego Bay sediments (Kennish, 1998). On the seafloor, natural debris (marine algae and terrestrial vegetation debris) is more common on the southern California shelf than anthropogenic debris, and is more common on the inner shelf (
30 m depth) in 1994 and 1998 (Moore and M. J. Allen, 2000; M. J. Allen et al., 2002a). Some of this contributes to a drift algae zone, which is an important habitat on the softbottom, providing cover for juvenile white seabass (Atractoscion nobilis), barcheek pipefish (Syngnathus exilis), and other species (L. G. Allen and Franklin, 1992, M. J. Allen and Herbinson, 1991, Chapter 6). Anthropogenic debris (debris consisting of plastic and metal materials, fishing gear, bottles, and cans) on the shelf of southern California was more common in bays and harbors and on the middle (31–100 m) and outer shelf (101–200 m) zones (Moore and M. J. Allen, 2000). Bay and harbor debris consisted largely of plastics and cans (suggesting land-based and boating sources) (M. J. Allen et al., 2002a) whereas the deepwater debris consisted largely of fishing gear, cans, and bottles (suggesting fishing sources) (Moore and M. J. Allen, 2000). ORGAN I S M S

Marine organisms that accumulate contaminants are an important repository and means of redistributing contaminants in the marine environment (Schiff et al., 2000). In a review of contaminant trends in the SCB (Mearns et al., 1991), trace metals, chlorinated pesticides (DDTs, chlordane, dieldrin), and PCBs were found in invertebrates, fishes, seabirds, and marine mammals. Trace metals such as silver, cadmium, chromium, and copper were accumulated in macroinvertebrates but not fish. Mercury did not accumulate in invertebrates but did in fish. Among invertebrates, elevated levels of DDTs and PCBs have been found in southern California in scallops, clams, squid, mysids, shrimp, lobsters, sand crabs, and crabs (Mearns et al., 1991). DDTs, PCBs, chlordane, dieldrin, and PAHs have been found in fishes.

Bioaccumulation of Contaminants in Fish Bioaccumulation in fish is the accumulation of contaminants in tissue as a result of dietary consumption and bioconcentration (Cardwell, 1991). Bioconcentration occurs when contaminants are absorbed from the water by the gills or epidermis. However, most bioaccumulation in fish results from dietary consumption of food organisms with relatively low levels of contaminants. Most contaminants found in marine organisms are hydrophobic, and accumulate in lipid reservoirs in the organism. As accumulation of hydrophobic contaminants from the environment occurs at a higher rate than the catabolic transformation of these compounds, concentrations increase in the fish above that of the environment or their prey. When predators consume contaminated fish and predators at higher trophic levels in turn consume these, tissue concentrations are biomagnified up the food chain. This results in species at higher trophic levels having higher levels of contaminants than those at lower levels. As noted above, marine fishes collected from contaminated bay and coastal waters of California often have elevated tissue concentrations of certain contaminants. Although assess-

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ments of chemical contaminants in some areas (e.g., parts of southern California and San Francisco Bay) find elevated concentrations of many organic compounds and trace metals in sediments, only some are elevated in fish tissue. Contaminants likely to be high in fish tissue include chlorinated hydrocarbons (e.g., PCBs and pesticides DDT, chlordane, and dieldrin in liver and muscle tissue; PAHs in stomach contents and PAH metabolites in bile) and trace metals (e.g., arsenic, mercury, selenium, and tin) (Mearns et al., 1991). The chlorinated hydrocarbons are hydrophobic and associate with lipids in fish tissue. Similarly, mercury, arsenic, selenium, and tin are complexed with organic compounds, resulting in their accumulation in lipids in fish tissues. The low rate of catabolic destruction of hydrophobic contaminants relative to a higher rate of accumulation from diet or water generally results in higher concentrations in fish tissue relative to the environment (Muir et al., 1990, Pastor et al., 1996). Bioaccumulation of trace metals occurs among those that are organically complexed (e.g., methyl mercury, arsenobetaine, and organotins). However, not all contaminants consumed by fish are bioaccumulated. Trace metals (e.g., cadmium, copper, and zinc) are detoxified in the liver and safely assimilated by California scorpionfish (Scorpaena guttata), white croaker (Genyonemus lineatus), and Dover sole (Microstomus pacificus) in southern California (Brown et al., 1985). Distribution of Contaminants in Fishes

The highest concentrations of contaminants in fish tissue are generally found in fish living near the source of the contaminants (e.g., discharge site, contaminated sediment) (Mearns et al., 1991) but pelagic fish and wide-ranging demersal fish that become contaminated in these areas may carry contaminants away from the source. In California, the highest levels of contaminants in marine fishes usually occur in coastal southern California and San Francisco Bay (Mearns et al., 1988). In a comparison of fish contamination in coastal areas around the United States (Mearns et al., 1988), DDTs in muscle and liver tissue were much higher in the SCB at the Palos Verdes Shelf than in the rest of California (fig. 23-1). The highest values in muscle tissue were 200 ppm (concentrations are reported as wet weight in this chapter) in spiny dogfish (Squalus acanthias), 176 ppm in white croaker, and 123 ppm in Dover sole (all from the Palos Verdes Shelf in the 1970s and early 1980s) (Mearns et al., 1991). Striped bass (Morone saxatilis) from the Sacramento River mouth in San Francisco Bay had 7 ppm DDT in the 1970s (Mearns et al., 1988). DDT concentrations in liver tissue are typically about 13 times higher than in muscle tissue from the same fish. The highest concentrations of DDT in fish livers were 1,589 ppm in Dover sole from the Palos Verdes Shelf in 1977 and 1,026 ppm for rockfish (Sebastes sp.) (Mearns et al., 1988, 1991). Rockfish from Santa Monica Bay had median liver values of 349 ppm in 1970 (Mearns et al., 1988). The average liver value in San Francisco Bay fish in the 1970s was 1 ppm whereas average concentrations from the Palos Verdes Shelf ranged from 0.9 to 419 ppm (Mearns et al., 1988, 1991). At depths of 500–1000 m off the Farallon Islands in central California in 1985, DDT concentrations were 9 ppm in a sablefish (Anoplopoma fimbria) and 2 ppm in a Dover sole (Melzian et al., 1987). Although the maximum Dover sole values were much lower than in the SCB, the sablefish concentration was higher (Melzian et al., 1987, Mearns et al., 1991). PCBs were also higher for muscle and liver tissue in southern California than in San Francisco Bay (fig. 23-2) (Mearns

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F I G U R E 23-2 Total PCBs (Aroclor) in a) liver and b) muscle of coastal and marine fish from 19 sites sampled in 1976 and 1977. Bar represents mean of all individuals from all species collected at a site (after Mearns et al. 1988).

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et al., 1988). Highest muscle values were 14.8, 10.4, and 10.0 ppm in spiny dogfish, Dover sole, and white croaker, respectively, from the Palos Verdes Shelf in 1975-1981 (Mearns et al., 1991). In contrast, the highest concentration in San Francisco Bay was 4.0 ppm in striped bass from the Sacramento River estuary (Gadbois and Maney, 1982, Mearns et al., 1988). Liver concentrations were highest in Dover sole (162 ppm), followed by Pacific sanddab (Citharichthys sordidus) (39 ppm), and English sole (Parophrys vetulus) (22 ppm) from the Palos Verdes Shelf in the 1977 (Mearns et al., 1991). Mean concentrations in San Francisco Bay fish were up to 2 ppm (Mearns et al., 1988). PCB concentrations at depths of 500–1000 m off the Farallon Islands were 4 ppm for sablefish and 2 ppm for Dover sole in 1985 (Melzian et al., 1987). Liver concentrations for sablefish and Dover sole were higher (28 and 162 ppm) in the SCB (Melzian et al., 1987, Mearns et al., 1991). From the late 1960s to early 1980s, PCBs in fish were high on the East Coast from New England to Georgia, along the Gulf Coast, and on the west coast in Puget Sound, San Francisco Bay, and the SCB (fig. 23-2; Mearns et al., 1988). The highest reported values were 22.0 ppm in muscle tissue of white perch (Morone americana) from the Hudson River area in 1980. The highest whole fish concentration was 6.9 ppm in Atlantic menhaden (Brevoortia tyrannus) from New Jersey in 1972 (Mearns et al., 1988). Highest liver concentrations were 162 ppm for Dover sole on the Palos Verdes Shelf (Mearns et al., 1991) and 160.0 ppm in starry flounder (Platichthys stellatus) in Puget Sound, both in 1977 (Sherwood, 1982). With the exception of southern California, PCBs were highest in urban embayments on Pacific and East Coasts, and near Pensacola, FL, but were low in fish tissue from southeastern and Gulf of Mexico estuaries (Mearns et al., 1988). In the 1970s, fish contaminated with other pesticides (chlordane, dieldrin, toxaphene) were widespread in coastal estuaries of the East and Gulf Coasts and less so on the west coast (Mearns et al., 1988). Chlordane was highest in the New Jersey area and southern Texas; dieldrin in the New Jersey area, southwest Florida, and southern Texas; and toxaphene in southern Texas, and near Louisiana and Alabama. In contrast to DDT and PCB, dieldrin was found only in estuaries, and was much higher in fish livers from San Francisco Bay than in the SCB (Mearns et al., 1988). Highest values (0.09 ppm) in San Francisco Bay were found in livers of starry flounder and white croaker. Whole tissue values for dieldrin, endrin, and chlordane in juvenile estuarine fish were low and were similar between San Francisco Bay and southern California (Mearns et al., 1988). In a regional survey of the southern California shelf (depths of 10-200 m) in 1994, flatfish (Dover sole; Pacific sanddab; longfin sanddab, Citharichthys xanthostigma) tissue was analyzed for 14 chlorinated hydrocarbons, including PCBs and 13 pesticides (including DDTs), and of these, only DDTs and PCBs were found (Schiff and Allen, 2000). Flatfishes, which live in these sediments, accumulate DDT and PCB in proportion to the concentration in the sediments (fig. 23-3) (Schiff and Allen, 2000; M. J. Allen et al., 2002a). Hence, the highest levels of DDT in southern California fish have been found near the Palos Verdes area (Mearns et al., 1988, 1991). Within the SCB, DDT concentrations are highest on the Palos Verdes Shelf near the wastewater outfall, followed by Santa Monica Bay, and from there decreasing to the northwest, although low levels of DDT are found in fish from the Palos Verdes Shelf to San Diego (Mearns et al., 1991; M. J. Allen et al et al., 2002a). Fish with highest PCB concentrations in fish tissue are also found

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F I G U R E 23-3 Relationships between a) total DDT and b) total PCB

concentrations in whole fish composites of sanddab guild species and in sediments on the southern California shelf at depths of 3–187 m, July–September 1998. Dashed lines are best fit to the data from linear regression (after M. J. Allen et al. 2002a).

on the Palos Verdes Shelf, but high concentrations are also found in bays and harbors. Chlordane concentrations in fish tissue have not been widely studied in the SCB. High muscle tissue values were 0.020 ppm for California corbina (Menticirrhus undulatus) in 2001 (M. J. Allen et al., 2004) and 0.019 ppm in kelp bass (Paralabrax clathratus) from the Palos Verdes Shelf in 1985 (Mearns et al., 1991). The highest liver concentration (162 ppm) occurred in Dover sole from the Palos Verdes Shelf (Mearns et al., 1991). In whole fish tissue, the highest concentration of 0.022 ppm was recorded in arrow goby (Clevelandia ios) from Newport Bay in 2002 (M. J. Allen et al., 2004). The Palos Verdes Shelf did not have the same importance as a locus of high fish tissue concentrations of trace metals as it did for DDTs and PCBs. High arsenic concentrations (0.012 and 0.009 ppm) were found in Pacific sanddab at Santa Catalina Island in 1973 and spotted turbot (Pleuronichthys ritteri) in Newport Bay in winter 2001, respectively (Mearns et al., 1991; M. J. Allen et al., 2004). In whole fish tissue, an arsenic concentration of 0.001 ppm was found in diamond turbot (Pleuronichthys guttulatus) and California halibut from Newport Bay (M. J. Allen et al., 2004). Highest values of selenium in fish muscle tissue (0.004 and 0.002 ppm) and have been found in Pacific bonito (Sarda chiliensis) at Huntington Beach and kelp bass on the Palos Verdes Shelf, respectively (Mearns et al.,

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1991). Finally, selenium concentrations as high as 2 ppm were found in whole fish tissue from California killifish (Fundulus parvipinnis) in Newport Bay in 2002 (M. J. Allen et al., 2004). High concentrations of mercury (10.6 ppm) have been found in muscle tissue of white shark (Carcharodon carcharias) from Santa Catalina Island as might be expected from its high trophic position (Mearns et al., 1991). Among ray-finned fishes, concentrations as high as 5.5 ppm have been found in California scorpionfish from Dana Point and 1.9 ppm in shortfin mako (Isurus oxyrinchus) from the waters over the San Pedro Basin (Mearns et al., 1991). As inputs of contaminants from all sources have decreased (Mearns, 1993, Schiff et al., 2000), concentrations of contaminants in water, sediments, and marine organisms have also decreased. Contaminants in southern California marine fishes have decreased by an order of magnitude or more in wastewater discharge and reference areas from the 1970s to the 1990s (Mearns, 1993; Schiff and Allen, 2000). However, present and historical inputs continue to contaminate California marine fishes.

Bioaccumulation of Contaminants by Trophic Types of Fish Fishes of different trophic levels and feeding habits sometimes show differences in bioaccumulation of contaminants. Within an ecosystem, the food web typically consists of primary producers (e.g., phytoplankton), primary consumers (e.g., zooplankton), secondary consumers (e.g., planktivorous fishes), tertiary consumers (e.g., carnivorous bony fishes, seabirds), and higher-level consumers (e.g., large carnivorous sharks, marine mammals). Although determination of the trophic level of a species is typically determined from examination of a species diet, it has also been determined chemically, for instance using ratios of cesium and potassium concentrations in fishes (Young et al., 1980). Potassium, an essential electrolyte, is maintained at constant levels in tissues but cesium (a trace element) is not. Cesium, however, has a half-life 2 to 3 times that of potassium and accumulates up the food chain. In a structured food web (as described above), the cesium/potassium (Cs/K) ratio increases with increasing trophic level, whereas in an unstructured food web (where species feed at more than one trophic level), an increase in CS/K ratio is not apparent with presumed trophic position (Isaacs, 1972, Young et al., 1980). The increase of Cs/K with trophic level in structured food webs parallels increases in contaminants that biomagnify in these food webs. An examination of the food web (including fish species) in the Salton Sea, Newport Bay, Palos Verdes Shelf, and San Pedro Channel of southern California from 1975 to 1978 showed that the simple food webs of the Salton Sea (all introduced species) and San Pedro Channel (pelagic) were structured and those of Newport Bay and Palos Verdes Shelf (benthic and pelagic) were unstructured. Mercury and chlorinated hydrocarbons (DDT and PCB) generally increase up structured food webs but other trace metals do not (Young et al., 1980). Contaminant concentrations from fish in a given area are often similar among fish species that feed in the same way but differ among species with different feeding habits. M. J. Allen et al. (2002b) compared bioaccumulation of DDT in sanddabguild species of southern California (speckled sanddab, Citharichthys stigmaeus; longfin sanddab; Pacific sanddab; and slender sole, Lyopsetta exilis). Species of this guild (benthic pelagobenthivore guild of M. J. Allen, 1982; also see chapter 7)

are small flatfishes with medium-sized mouths that feed on nektonic and benthic prey and represent the most widespread guild of fishes on the soft bottom shelf of southern California (M. J. Allen et al., 1998, 2002a). DDT concentrations in species pairs from the same sites increased with increasing concentrations (fig. 23-4). Log-transformed DDT concentrations in whole fish samples of different species of this guild of the same age and from the same site were highly correlated among all species of the guild. Relationships between species were linear and did not differ from unity. The variability of DDT levels in species pairs between sites was 60 times that of replicates within a species. In contrast, the variability among species and among ages was 4 and 2 times, respectively, that of replicates. The similar response of species of this guild to the same environmental exposure of DDT suggests that this widespread guild could be used as a super species to assess the extent of fish contamination in bathymetrically diverse shelf areas.

Effects of Contamination The previous sections have focused on the distribution of contaminants in the environment and specifically in fish on the California coast. In addition to accumulating in marine organisms, these contaminants can have detrimental effects on individual fish, populations and assemblages, fish predators, and human consumers of fish. The primary focus of these studies has been on human health risks to humans and to bird and mammal predators that consume them.

H U MAN H EALTH R I S K S

Public concern regarding potential health risks from eating contaminated fish and invertebrates came to light as persons consuming mercury contaminated marine organisms from Minamata Bay became ill or died in the 1950s and 1960s (Irukama, 1966, Ui, 1969). Concerns also developed for other contaminants, and in 1970–1971, white croaker, canned jack mackerel (Trachurus symmetricus), and Pacific bonito with DDT concentrations above 5 ppm were seized by the U.S. Food and Drug Administration (MacGregor, 1974, Stull et al., 1987). Further concerns regarding high levels of DDT and PCB contamination in fish caught on the Palos Verdes Shelf and Santa Monica Bay prompted posting of fish consumption guidelines for these areas by California Department of Health Services (Stull et al., 1987). This health advisory recommended that all white croaker not be consumed from these areas and no consumption of any fish caught in the outfall area of Palos Verdes Shelf and in parts of Los Angeles/Long Beach (LA/LB) Harbors. It also recommended restricted consumption by all women of childbearing age and young children; no consumption of fish livers; and healthy cooking methods. Since 1991, health advisories have been issued for about 50 species in southern California that had DDT and PCB concentrations in muscle tissue above 0.1 ppm (OEHHA, 2001). Health advisories were issued for nine locations from Point Dume to Dana Point. Advisories restricting fish consumption were posted for eight types of fish (rockfishes; California scorpionfish; kelp bass; black croaker, Cheilotrema saturnum; white croaker; California corbina; queenfish, Seriphus politus; and surfperches, Embiotocidae) at one or more locations, with white croaker having the most. Similar advisories have also been posted in San Francisco Bay for fishes with high levels of mercury, PCBs,

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F I G U R E 23-4 Total DDT concentrations in whole fish composites of sanddab guild species: Pacific sandab

(Citharichthys sordidus); longfin sanddab (Citharichthys xanthostigma); speckled sanddab (Citharichthys stigmaeus); and slender sole (Lyopsetta exilis). Sediment contamination gradient increases to right. SD stations are off San Diego, T6 to T2 on San Pedro Shelf, C9A Santa Monica Bay, Z2 outfall station Santa Monica Bay, and stations to right of Z2 are on the Palos Verdes Shelf, California. Samples collected in 1997 (after M. J. Allen et al., 2002b).

and other contaminants, including sturgeon (Ascipenser spp.), striped bass, sharks, croakers, surfperches, and gobies (OEHHA, 2001). As noted above, advisories are posted when contaminants exceed State of California (OEHHA) screening values, which are lower (and hence more conservative) than United States Environmental Protection Agency values (M. J. Allen et al., 2004). For contaminants found in California marine fishes consumed by anglers, current OEHHA screening values are 0.100 ppm DDT, 0.020 ppm for PCBs, 0.030 ppm chlordane, 0.300 ppm mercury, and 2 ppm selenium) (M. J. Allen et al., 2004). Health concerns are based on toxic or carcinogenic effects of the contaminant. Contaminants of toxic concern include trace metals (e.g., inorganic arsenic, mercury, selenium, and PCBs) and those of carcinogenic concern are DDTs, PCBs, and chlordane (USEPA, 1995). Risk-based screening values for carcinogens are based on the effective dose of the contaminant (over a 70-year period), its concentration in the tissue, the mean daily consumption rate, relative absorption coefficient, and mean body weight. For toxic contaminants, the effective dose is the effective ingested dose with a specified level of risk from dose-response studies, with the remaining variables the same as for carcinogens (USEPA, 1995). Fish consumption rates are now based on field studies that obtain species-specific consumption rates by California anglers in the

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Los Angeles area (Puffer et al., 1982), Santa Monica Bay (M. J. Allen et al., 1996), and San Francisco Bay (SFEI, 2000).

W I LDLI F E H E A LTH R I S K S

In addition to posing health-risks to humans, contaminated fish can pose health-risks to wildlife predators. Brown pelican (Pelecanus occidentalis) and double-crested cormorant (Phalocrocorax auritus) (both piscivorous) and bald eagle (Haliaeetus leucocephalus) (partly piscivorous) nesting on southern California islands had poor reproductive success during the late 1950s to 1970s due to eggshell thinning (Anderson and Hickey, 1970; Risebrough et al., 1971). Birds with high tissue DDT concentrations had thinner eggs and, over time, egg thickness increased as tissue DDT concentrations decreased (Gress, 1994). California sea lions with high levels of DDT gave birth to more premature births than those with lower levels (Connolly and Glaser, 2002). Contaminant levels in California marine fish have generally not been assessed relative to wildlife (predator) health-risk guidelines, as there are currently no accepted Federal or California State guidelines. However, Canada has developed guidelines for wildlife health-risk to marine and aquatic organisms from DDT and PCBs (Environment Canada, 1997, 1998).

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These guidelines are for DDT and PCB concentrations in whole fish tissue. The DDT guideline is 0.014 ppm (Environment Canada, 1997). The PCB guideline is 0.79 ppt (parts per trillion) toxicity equivalency quotient (TEQ) (Environment Canada, 1998). Whereas human health-risk guidelines are based on total PCB, the wildlife PCB guideline is based on concentrations of 12 toxic PCB congeners, and the relative toxicity of these to tetrachloro-dibenzo-p-dioxin (TCDD). The 12 congeners vary in toxicity to birds and mammals. In 1998, the sanddab-guild species were targeted (all of which had similar uptake of DDT with the same exposure; M. J. Allen et al., 2002b) to obtain comparable samples across the entire shelf from depths of 5–200m and assess fish contamination throughout the southern California shelf (M. J. Allen et al., 2002a). In this study, sanddab-guild fish with DDT concentrations higher than the wildlife health-risk guideline (Environment Canada, 1997) occurred in 71% of the southern California shelf area (M. J. Allen et al., 2002a). Whereas fish with DDT levels above the guideline were widespread, including on the Channel Islands, those with high PCB levels were not. Fish with PCB toxicity equivalent quotient (TEQ) concentrations higher than the mammal and bird wildlife healthrisk guideline (Environment Canada, 1998) occurred in 8% and 5% of the area, respectively. These were areas near large wastewater discharges with historically contaminated sediments, and within harbors (for marine mammal risk) and around the southeast Channel Islands (for bird risk). DDT levels above these guidelines were also widespread in Newport Bay in 2002, occurring in samples of all nine species of forage fishes examined (M. J. Allen et al., 2004). Although a large area of concern for DDT was identified using this guideline in these studies, more research is needed to determine to what degree there is a real risk to specific bird and mammal predators of marine fish in these areas.

F I G U R E 23-5 Dover sole (Microstomus pacificus) collected on the

Palos Verdes Shelf, California, in 1981: a) normal; b) epidermal tumor and fin erosion; c) fin erosion; and d) skeletal abnormality (no caudal fin). (Photos by Dario Diehl, Southern California Coastal Water Research Project).

E XTE R NAL DI S EAS E S, ANOMALI E S, AN D PARAS ITE S

Beginning in the late 1950s fisheries biologists, anglers, and divers began to note observations of morbid and abnormal fish from Santa Monica Bay, the Palos Verdes Shelf, and LA/LB Harbor area and became aware of many fish with external diseases and anomalies (Young, 1964). These were interpreted as resulting from wastewater discharge in Santa Monica Bay, the Palos Verdes Shelf, and from sites in LA/LB Harbor. Anomalies included abnormally soft California halibut, spotted turbot of low body weight, exophthalmia (abnormal protrusion of the eye) in spotfin croaker (Roncador stearnsii) and white seabass, lesions in white seabass and juvenile Dover sole, lip papillomas in white croaker, and papillomas in California tonguefish (Symphurus atricaudus), basketweave cusk-eel (Ophidion scrippsae), and Pacific sanddab (Young, 1964). As more comprehensive studies were conducted during the 1970s, several important diseases or anomalies were identified in coastal fishes of southern California: fin erosion, skin tumors in flatfishes, oral papillomas in croakers, color anomalies, exophthalmoses, and skeletal anomalies (Mearns and Sherwood, 1977). Fin erosion levels were very high in the early 1970s on the Palos Verdes Shelf near the POTW outfall, affecting 33 of 151 species examined (Mearns and Sherwood, 1977). In fin erosion disease, the fins that erode are those in contact with the sediments (i.e., dorsal, anal, and caudal fins of flatfishes; pelvic, anal, and ventral part of caudal fins in roundfishes that live or

rest on the bottom; personal observations by author). Dover sole was the species with the highest prevalence (30%) of fin erosion in the 1970s, almost all of which occurred on the Palos Verdes Shelf (fig. 23-5 and fig. 23-6). By the middle 1980s, fin erosion had nearly disappeared in Dover sole from that area (Stull, 1995) and has been virtually absent there and throughout the Southern California Bight since the early 1990s (fig. 23-6)(M. J. Allen et al., 1998, 2002a). Although intensely studied, the cause of this disease was not determined. It is assumed to be related to sediment contamination, based upon its greatest prevalence in benthic fishes found near the POTW outfall and its disappearance as wastewater effluent quality improved. Tail erosion in white croaker (in which the entire rather than the lower part caudal fin was eroded) appeared to be a different disease and was found from Santa Monica Bay to San Pedro Bay in the 1970s (Mearns and Sherwood, 1977); this disease is rarely reported at present. [As a historical side note, it is because white croaker sometimes had no caudal fin in the 1970s that all non-fisheries demersal fish surveys in southern California measure standard length rather than total length.] Tumor-like diseases have been found in Dover sole, white croaker, and occasionally in other species. These are variously called lesions, tumors, papillomas, pseudotumors, and neoplasms. Epidermal tumors were found consistently in

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F I G U R E 23-6 Distribution of fin erosion on the mainland shelf from 1973 to 1980 (only on the Palos Verdes Shelf and one record on south San Pedro Shelf) and in 1994 (one record in Santa Barbara Channel). From the mid-to-late 1990s to the present, fin erosion has been virtually absent from the Palos Verdes Shelf.
 trawl stations sampled in 1994 (after M. J. Allen et al., 1998)

Dover sole sampled from the SCB in the early 1970s (fig. 235) (Mearns and Sherwood, 1977). This disease was found almost entirely in small (6–12 cm in length) juveniles and the prevalence (percent fish affected) was similar among areas in the central mainland coast of the SCB. It was particularly noticeable on the Palos Verdes Shelf because of the large number of juvenile Dover sole found there. The prevalence of the disease on the Palos Verdes Shelf decreased with increasing distance from the wastewater outfall (Cross, 1988). The disease was found outside the SCB as far back as 1946 (Mearns and Sherwood, 1977). Incidences of this disease have decreased since the 1970s, and are presently at background levels (M. J. Allen et al., 1998, 2002a). These xcell pseudotumors are probably the result of amoeboid parasitism (Dawe et al., 1979, Cross, 1988). Oral papillomas in white croaker and other species have been found near Los Angeles, but the prevalence of these abnormalities has been low (Young, 1964, Mearns and Sherwood, 1977). In contrast to Dover sole, the prevalence of these papillomas in white croaker increased with increasing size of the fish (Mearns and Sherwood, 1977). Histological analysis of the oral papillomas in white croaker determined that they were not malignant and were likely due to mechanical, chemical, or infectious irritation (Russell and Kotin, 1957, Young, 1964). Epidermal tumors have also been found in English sole in San Francisco Bay, with a prevalence of 12% and up to 33 tumors per fish in the northern part of the bay near industrial waste discharge (Cooper and Keller, 1969; Sindermann, 1979). English sole with tumors have not been found in southern California.

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Other external anomalies, such as color anomalies (ambicoloration, albinism) in flatfishes and skeletal anomalies, have also been observed (Mearns and Sherwood, 1977). The most frequent color anomaly was ambicoloration (where eyed-side pigmentation occurs on parts of the blind side). Skeletal anomalies occur occasionally in a number of species, and include snub noses, no tail (hypural plates absent; fig. 23-5), bent fin rays, deformed spinal columns, and deformed gill rakers (Valentine, 1975, Sindermann, 1979). There is no clear evidence that the color anomalies are related to contamination. Some of these may occur during larval development in the water column. However, bent rays in fins in contact with sediments at Palos Verdes may be related to sediment contamination. The relationship of fish diseases to marine pollution has been examined primarily in southern California, Puget Sound, Gulf of Saint Lawrence, and mid-Atlantic states (e.g. Mearns and Sherwood, 1977; Sindermann, 1979, Malins et al., 1984; Stein et al., 1993; Fournie et al., 1996). The fin erosion disease of benthic fishes found in southern California occurs in fins in contact with contaminated sediments whereas that of pelagic nearshore fishes erodes the caudal fin, which is not in contact with sediments (Mearns and Sherwood, 1977, Sindermann, 1979). Fin erosion similar (but not necessarily the same) to that found in southern California Dover sole has been found on the east coast in winter flounder (Pseudopleuronectes americanus), summer flounder (Paralichthys dentatus), in Puget Sound in starry flounder and English sole, in plaice (Pleuronectes platessa) and dab (Limanda limanda) in the Irish Sea, and in Japanese stargazers (Uranoscopus japonicus) off Japan (Perkins et al., 1972,

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TA B L E 23-1

Overall Prevalence of Anomalies in Demersal Fish Populations

Years

Percent Anomalies

Study

Southern California Southern California Southern California Gulf Coast

1969–1976 1994 1998 1991–1992

5.0 1.0 0.5 0.7

Mearns and Sherwood 1977 M. J. Allen et al. 1998 M. J. Allen et al. 2002a Fournie et al. 1996

Mid-Atlantic Coast

1990

0.5

Fournie et al. 1996

Location

Nakai et al., 1973, Murchelano, 1975, Wellings et al., 1976, Sindermann, 1979). Tail erosion similar to that found in white croaker has been found in Atlantic croaker (Micropogonias undulatus) (the ecological counterpart to white croaker on the East Coast) and spot (Leiostomus xanthurus) (Couch and Nimmo, 1974). Fin erosion likely results from chemical stress and low dissolved oxygen concentrations and possibly enhanced hydrogen sulfide, and in some cases secondary bacterial infection (Sindermann, 1979). Epidermal tumors or neoplasms have been found in a variety of fishes on both coasts. In southern California, the primary occurrence is in Dover sole, and secondarily in white croaker (Mearns and Sherwood, 1977). Elsewhere in California, these have been found in English sole in San Francisco Bay (Cooper and Keller, 1969). Elsewhere on the Pacific Coast, epidermal tumors have been prevalent in Pacific cod (Gadus macrocephalus), starry flounder (Puget Sound), flathead sole (Hippoglossoides elassodon; Puget Sound), sand sole (Psettichthys melanostictus; British Columbia), and rock sole (Lepidopsetta bilineata; Bering Sea) (Nigrelli et al., 1965, McArn and Wellings, 1971, Miller and Wellings, 1971, Dawe et al., 1979, Sindermann, 1979). These tumors are likely caused by amoebic parasites or viruses, and in many cases may be a natural disease (Dawe, 1979, Sindermann, 1979). Skeletal anomalies and genetic anomalies also occur in fish from other geographic areas (Sindermann, 1979). In 1998, the prevalence of external anomalies in 1998 in demersal fishes on the southern California shelf was similar to background anomaly rates in mid-Atlantic (0.5%) and Gulf Coast (0.7%) estuaries (table 23-1) (Fournie et al., 1996; M. J. Allen et al., 2002a). Toxicopathic hepatic lesions have been found in fishes from contaminated sites from southern California to Puget Sound (Malins et al., 1984, Myers et al., 1994, Roy et al., 2003), with prevalence of hepatic lesions in English sole being highest in Puget Sound, starry flounder in San Francisco Bay, and white croaker in San Francisco Bay and LA/LB Harbors (Myers et al., 1994). Although parasitism in marine fishes is generally natural, the type and diversity of parasites and the prevalence (percent fish parasitized) and intensity (number of individual parasites) of parasites within a taxon may vary between contaminated and uncontaminated areas (Mearns and Sherwood, 1977, Perkins and Gartman, 1997, Kalman, 2001). Fish parasites may affect the health of their host fish or they may cause health problems in predators and humans that consume fish. Fish parasites consist of ectoparasites (external parasites; e.g., copepods, isopods, leeches) and endoparasites (internal parasites; e.g., nematodes, cestodes, trematodes). In the 1970s, the eye copepod (Phrixocephalus cincinnatus), which typically attaches to the eye of Pacific sanddab was not found in

contaminated areas but was abundant in reference areas, perhaps a response to high chlorinated hydrocarbon concentrations in Pacific sanddab (Mearns and Sherwood, 1977). In 1989-1994, this parasite was more abundant on Pacific sanddab at Palos Verdes and Santa Monica Bay (Perkins and Gartman, 1997). Similarly, in 1998-1999 other ectoparasites (copepods, leeches, isopods) on flatfishes and scorpaeniform fishes were significantly more prevalent near the outfall than in non-outfall areas in Santa Monica Bay (Kalman, 2001). Other studies (M. J. Allen et al., 1998, 2002a; Hogue and Paris, 2002) did not find obvious response in the prevalence of fish parasites to outfall areas.

B IOMAR K E R S AN D S U B LETHAL E F F E CTS

Although contaminants accumulate in fish and pose health risks to consumers of fish, they can also affect the health of the fish itself. Effects include acutely toxic effects, which can cause a fish to die immediately, or chronic sublethal effects, which affect its health, behavior, or ability to reproduce. Although freshwater fish kills due to human activity occur occasionally, marine fish kills along the California coast are rare and generally related to red tides (Bongersma-Sanders, 1957). An extensive red tide in 1945 that extended from San Luis Obispo to Los Angeles Harbor killed sharks, stingrays, and California halibut in Santa Monica Bay (Sommer and Clark, 1946). Trawling sometimes result in dead by-catch fish floating at the surface, which might be mistaken for a toxic fish kill. Fish kills due to acute toxicity from contaminants are more likely to occur in shallow confined areas near shore than offshore, unless a broad area is affected (e.g., an oil spill). High levels of total DDT and total PCB in white croaker from San Pedro Bay have been correlated with reproductive impairment, including decreased fecundity, decreased fertilization success, and decreased proportions of spawning females (Cross and Hose, 1988, Hose et al., 1989). Increased levels of these compounds were also correlated to subcellular damage in white croaker and kelp bass (Hose et al., 1987). An increased frequency of micronuclei, a by-product of DNA damage, was observed in blood cells of these two fish species, with increased concentrations of total DDT and total PCB. High levels of DDT and PCB of kelp bass had subtle differences in reproductive endocrine status (e.g., lower levels of maturational gonadotropin) (Spies and Thomas, 1995). Biomarkers are biochemical compounds and histological effects produced in response to contaminant exposure. Whereas some contaminants bioaccumulate in fish tissue, others do not. Biomarkers provide a measure of an organism’s exposure to potentially toxic contaminants. In the 1970s and

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1980s white croaker had high levels of enlarged fatty-vacuolated livers containing degenerating cells and hepatic lesions in the Palos Verdes-Los Angeles Harbor area and in the Oakland Estuary where DDTs, PCBs, and/or PAHs were high (Malins et al., 1987, Myers et al., 1994). In a Pacific Coast survey of hepatic lesions in fish (Myers et al., 1994), prevalence of liver lesions of white croaker were highest in San Francisco Bay and LA/LB Harbor; in starry flounder these were highest in San Francisco Bay. Another biomarker is hepatic mixed-function oxidases (Spies et al., 1982). Elevated levels of these enzymes indicate exposure to oil and PCB. Pacific sanddab and speckled sanddab near wastewater outfalls (high PCB) and crude oil seeps in southern California had high levels of these enzymes relative to reference areas (Spies et al., 1982). Bile fluorescent aromatic compounds (FAC) concentrations (an indicator of PAH exposure) were high in juvenile California halibut from Marina del Rey, Long Beach Harbor, and Alamitos Bay relative to reference areas in 1989–1999 (Brown and Steinert, 2004). Of seven species of flatfishes examined, speckled sanddab had the highest levels of DNA damage, and hornyhead turbot (Pleuronichthys verticalis) the lowest. Although overall, no significant relationship was found between bile FAC concentrations and DNA damage, the incidence of DNA damage increased with bile FAC concentrations in Ventura Harbor and Marina del Rey. In contrast to biomarker studies in other coastal Los Angeles areas, examination of biomarkers (e.g., cytochrome P450 1A; vitellogenin levels, an indicator of endocrine disruption; bile FACS; DNA damage; and liver histopathology) in hornyhead turbot, English sole, and bigmouth sole (Hippoglossina stomata) near the wastewater outfall on the San Pedro Shelf in 2000 did not find adverse effects (Roy et al., 2003).

E F F ECTS ON P O P U LATION S AN D AS S E M B L AG E S

Fish assemblages in the SCB vary by habitat and depth, with distinct bay, rocky bottom, and soft-bottom assemblages (L. G. Allen, 1985). Demersal (soft-bottom) fish assemblages have been the focus of studies of pollution impact because wastewater outfalls in southern California are on soft-bottom habitat (M. J. Allen, 1982). Demersal fishes are relatively sedentary, easily collected by trawl, and respond to environmental stress. As there is a relatively steep bathymetric gradient along the southern California coast, demersal fish assemblages vary in species composition by depth, with different assemblages at different depths (see chapter 7). Demersal fish assemblages have shown local shifts in abundance, biomass, species richness, diversity, and species composition in response to wastewater discharge in the SCB. In the early 1970s fish abundance, species richness, and diversity was depressed in the vicinity of wastewater outfalls in Santa Monica Bay and on the Palos Verdes Shelf (M. J. Allen, 1977). Depressed average fish abundance occurred over 27 km2 and depressed species richness over 50 km2 near the White Point Outfall on the Palos Verdes Shelf. From 1963 to 1974, fish abundance and diversity was low near the Hyperion 7-mile sludge pipe. When the Orange County Sanitation District moved its outfall from shallow (15 m) to deepwater (60 m) in the early 1970s, fish abundance increased 100% at the new outfall and decreased 50% at the old outfall (M. J. Allen, 1977). In contrast to demersal fishes, the deepwater outfall pipes attracted large numbers of rockfishes and other species (M. J.

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Allen et al., 1976). These outfalls provide the only continuous hard-bottom substrate extending across the dominant softbottom habitat of the shelf in Santa Monica Bay, Palos Verdes Shelf, San Pedro Shelf, and Point Loma Shelf. Hence, they attract hard-bottom fishes characteristic of the outfall depth, and assemblages on these outfalls are quite different from those of the surrounding soft-bottom areas. Fish abundance and species richness along the Hyperion outfall pipes were much greater near the end of the outfalls in deepwater than in shallow water, in part due in part to dense populations of gigantic anemones (Metridium farcimen), which provided habitat complexity for some rockfishes, and the attraction of water-column fishes. Without comparison to assemblages on comparable natural hard-bottom habitats at the same depths, wastewater effects could not be determined (although it was apparent that the gigantic anemones and other sessile cnidarians were attracted to waste being discharged from diffuser ports) (M. J. Allen et al., 1976). Among soft-bottom fishes, some species typical of reference assemblages were absent from outfall area on the Palos Verdes Shelf, whereas others were attracted to these areas (Allen, 1977). Species in reference assemblages that were missing in the outfall area included hornyhead turbot and California tonguefish. Species attracted to the outfall area included white croaker, shiner perch (Cymatogaster aggregata), and curlfin sole (Pleuronichthys decurrens). Changes in species composition were attributable to the feeding habits of fishes. Wastewaterrelated alteration of the sediments (primarily increased organic levels) favored infaunal polychaetes over crustaceans with concomitant shifts in the demersal fish community from crustacean feeding to polychaete-feeding species (M. J. Allen, 1977; M. J. Allen, 1982; Cross et al., 1985). I developed a model of the functional organization of the soft-bottom fish communities that defined the community by the number and type of foraging guilds and dominant species within a guild at any depth (M. J. Allen, 1982). This model can be used to identify what species or guilds at a given depth are missing or added. Differences from the expected study can identify species or guilds on which to focus further studies to determine if altered components of the community are responding to a loss or gain in food (e.g., guild absent, food absent), response to a competitor (e.g., guild present, expected species different), or to other conditions (e.g., guild absent, food present—perhaps a direct response to contaminants). Application of this model to fish data from the Palos Verdes Shelf from 1972 to 1989 showed that nearest the outfall, benthic guilds (consisting of combfishes, sculpins, and poachers) that fed on small benthic gammaridean amphipods were absent (M. J. Allen unpublished data). Within the turbot (polychaete extractor) guild, the expected hornyhead turbot was replaced by curlfin sole at the outfall (M. J. Allen, 1982, Stull and Tang, 1996). White croaker and shiner perch, not consistently caught in deep water were consistently abundant near the discharge site. As conditions improved over time, these alterations generally went back to expected conditions (M. J. Allen unpublished data). In the 1970s wastewater outfalls discharged high levels of suspended solids as well as contaminants, resulting in sediments with high levels of organic carbon near the outfalls. Sediments of high organic content are typically dominated by polychaetes whereas those with less organic carbon are dominated by crustaceans (e.g., amphipods). In the 1970s, the relative abundance of sanddab-guild fishes (predominantly crustacean-feeders; M. J. Allen, 1982, M. J. Allen et al., 2002b)

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F I G U R E 23-7 Effluent, sediment, and fish health metrics at the Palos Verdes Shelf wastewater discharge site from the early 1970s to 2002: a) mass emissions of effluent suspended solids; b) mass emissions of effluent copper; c) mass emissions of effluent DDT and PCBs; d) sediment organic nitrogen; e) Benthic Response Index; f) fin erosion in fish; g) Fish Response Index; and h) inverse of Fish Foraging Guild Index. Graphs modified from Montagne (2002a,b). Benthic biointegrity index after Smith et al. (2001); fish biointegrity indices after M. J. Allen et al. (2001).

was significantly lower on the Palos Verdes Shelf than that of turbot-guild species (polychaete-feeders; M. J. Allen et al., 2001). In contrast, the relative abundance of sanddab-guild species was significantly higher in reference areas (M. J. Allen et al., 2001). This relationship was used in developing a fish foraging guild biointegrity index (FFG) for the SCB (fig. 237h). In the same study, another biointegrity index (Fish Response Index, FRI; fig. 23-7g) was developed using the abundances of all species relative to the pollution gradient away from the Palos Verdes Shelf in the 1970s (as was done for

infauna in the Benthic Response Index, BRI; Smith et al., 2001). Both indices, as well as prevalence of fin erosion (fig. 23-7e) identified a shift from impacted to reference assemblages on the Palos Verdes Shelf from the 1970s (when sediment organics and contamination was initially high) to the 1980s and later, as sediment conditions improved in response to improved effluent quality (fig. 23-7) (CSDLAC, 2002). The FFG index can be easily interpreted as shifting from an assemblage dominated by turbot-guild (benthic extracting benthivores; polychaete-feeding) fishes to sanddab-guild (benthic

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pelagobenthivore; epibenthic generalists) fishes in the early 1980s. Application of the FRI to the southern California shelf in 1998 showed reference-level fish assemblages throughout the SCB (except near the mouth of the Santa Clara River; M. J. Allen et al., 2002a). This area was severely disrupted by extremely high flow and a very large plume of suspended sediments from the Santa Clara River during the 1997–1998 El Niño, resulting in an assemblage with high abundance of shiner perch and white croaker, similar to that found on the Palos Verdes Shelf during the 1970s (M. J. Allen, 1977; M. J. Allen et al., 2002a). Other fish assemblage attributes (abundance, biomass, species richness, and diversity) did not differ at outfall areas from reference areas of similar depth on the shelf in region-wide assessments in 1994 and 1998 (M. J. Allen et al. 1998, 2002a). Natural factors also play a role in changes to fish communities, and these must be considered as part of baseline reference conditions when assessing pollution or other anthropogenic effects on fish communities. If not considered, misleading interpretations and conclusions can result. For example, demersal fish communities changed somewhat from a coldwater to a warm water regime between 1972 and 1998, following a warming trend in SCB waters (chapter 7). This has made the assessment of fish populations on the Palos Verdes Shelf difficult as many coldwater species populations were decreasing and warm water species increasing at the same time that effluent quality and sediment contamination levels were improving.

Prospectus for Future Research With rapidly increasing coastal populations in California (particularly in the south), pollution is likely to be a concern well into the future, even though the worst may be in the past. Thus there is need for much additional research to better protect fish, wildlife, and humans. Many of the obvious contaminant effects when contaminants were high have been well studied, but during that time, little effort was focused on sublethal and less obvious effects of contaminants. While work is continuing in this area, there is still a need to better understand how contaminants affect fish biology (and in particular, for species actually exposed to that contaminant in the wild). Although fin erosion has largely disappeared, the cause of this disease has not been determined. Further research as to the cause of this disease may provide insight into why it occurred, and what in the sediments should be monitored to prevent its reoccurrence. Specific, realistic food webs focused on links between fish that are contaminated, and their fish, bird, and mammal predators are needed to provide a better understanding of how contaminants of concern reach threatened predatory species. A statewide assessment of the health of fish communities along the coast and in bays and estuaries is needed to determine areas of assemblage degradation.

Acknowledgments I thank the following people for their contribution to figures used in this study: Valerie Raco-Rands, Erica T. Jarvis, Dario Diehl (all of the Southern California Coastal Water Research Project), Dr. James A. Noblet (California State University, San Bernardino, Department of Chemistry), David Montagne and Chi-Li Tang (County Sanitation Districts of Los Angeles County; CSDLAC), and Dr. Alan J. Mearns (National Oceanic

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and Atmospheric Administration, National Ocean Service, Office of Response and Restoration). I also thank Larry G. Allen (California State University, Northridge) and David Montagne (CSDLAC) for advice on this paper.

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Kalman, J. 2001. Parasites of demersal fishes as potential indicators of wastewater discharge in Santa Monica Bay. MS Thesis. Calif. St. Univ., Long Beach, Long Beach, CA. 98 pp. Kennish, M.J. 1998. Pollution impacts on marine biotic communities. CRC Press, Boca Raton, FL. 310 p. MacGregor, J.S. 1974. Changes in the amount and proportions of DDT and its metabolites, DDE and DDD, in the marine environment off southern California, 1949–1972. U.S. Fish. Bull. 72(2):275–293. ———. 1976. DDT and its metabolites in the sediments off southern California, USA. U.S. Fish. Bull. 74(1):27–35. Malins, D.C., B.B. McCain, D.W. Brown, S.L. Chan, M.S. Myers, J.T. Landahl, P.G. Prohaska, A.J. Friedman, L.D. Rhodes, D.G. Burrows, W.D. Gronlund, and H.O. Hodgins. 1984. Chemical pollutants in sediments and diseases of bottom fishes in Puget Sound, Washington. Environ. Sci. Tech. 18:705–713. Malins, D.C., B.B. McCain, D.W. Brown, M.S. Myers, M.M. Krahn, and S.L. Chan. 1987. Toxic chemicals including aromatic and chlorinated hydrocarbons and their derivatives, and liver lesions in white croaker (Genyonemus lineatus) from the vicinity of Los Angeles. Environ. Sci. Tech. 21(8):765–770. McArn, G.E., and S.R. Wellings. 1971. A comparison of skin tumors in three species of flounders. J. Fish. Res. Bd. Canada 28:1241–1251. Mearns, A.J. 1993. Contaminant trends in the Southern California Bight: the coast is cleaner. Pages 1002–1016 in Coastal Zone ‘93: Proceedings, 8th Symposium on Coastal Management. Am. Shore Beach Pres/Am Soc. Civil Eng., New Orleans, LA. Mearns, A. J., M. Matta, G. Shigenaka, D. MacDonald, M. Buchman, H. Harris, J. Golas, and G. Lauenstein. 1991. Contaminant trends in the Southern California Bight. United States Department of Commerce, NOAA, Seattle, WA. NOAA Tech. Mem. NOS ORCA 62. 413 pp. Mearns, A.J., M.B. Matta, D. Simecek-Beatty, M.C. Buchman, G. Shigenaka, and W.A. Wert. 1988. PCB and chlorinated pesticide contamination in U.S. Fish and Shellfish: A historical assessment report. U. S. Dep. Commerce, NOAA, Seattle, WA. NOAA Tech. Mem. NOS OMA 39. 140 p. Mearns, A.J., and M.J. Sherwood. 1977. Distribution of neoplasms and other diseases in marine fishes relative to the discharge of waste water. pp. 210–224. In: H.F. Kraybill, C.J. Dawe, J.C. Harshbarger, and R.G. Tardiff (eds.), Aquatic pollutants and biological effects with emphasis on neoplasia. Ann. New York Acad. Sci. 298. Melzian, B.D., C. Zoffman, and R.B. Spies. 1987. Chlorinated hydrocarbons in lower continental slope fish collected near the Farallon Islands, California. Mar. Poll. Bull. 18(7):388–393. Miller, B.S., and S.R. Wellings. 1971. Epizootiology of tumors in flathead sole (Hippoglossoides elassodon) in East Sound, Orcas Island, Washington. Trans. Am. Fish. Soc. 100:247–266. Montagne, D. 2002a. Palos Verdes Ocean Monitoring Annual Report, 2002, chapter 3: Sediments and infauna. County Sanitation Districts of Los Angeles County. Whittier, CA. Montagne, D. 2002b. Palos Verdes Ocean Monitoring Annual Report, 2002, chapter 4: Invertebrate and fish trawls. County Sanitation Districts of Los Angeles County. Whittier, CA. Moore, S.L., and M.J. Allen. 2000. Distribution of anthropogenic and natural debris on the mainland shelf of the Southern California Bight. Mar. Poll. Bull. 40(1):83–88. Moore, S.L., D. Gregorio, M. Carreons, S.B. Weisberg, and M.K. Leecaster. 2001. Composition and distribution of beach debris in Orange County, California. Mar. Poll. Bull. 42(3):241–245. Muir, D.C.G., R.J. Norstrom, and M. Simon. 1990. Organochlorine in Arctic marine food chains: accumulation of specific polychlorinated biphenyls and chlordane-related compounds. Environ. Sci. Tech. 22:1071–1079. Murchelano, R.A. 1975. The histopathology of fin rot disease in winter flounder from the New York Bight. J. Wildl. Diseases 11:263– 268. Myers, M.S., C.M. Stehr, O.P. Olson, L.L. Johnson, B.B. McCain, S.L. Chan, and U. Varanasi. 1994. Relationships between toxicopathic hepatic lesions and exposure to chemical contaminants in English sole (Pleuronectes vetulus), starry flounder (Platichthys stellatus), and white croaker (Genyonemus lineatus) from selected marine sites on the Pacific Coast, USA. Environ. Health Persp. 102(2):200–214. Nakai, Z., M. Kosaka, S. Kudoh, A. Nagai, F. Hayashida, T. Kubota, M. Ogura, T. Mizushima, and I. Uotani. 1973. Summary report on marine biological studies of Suruga Bay accomplished by Tokai University 1964–72. J. Fac. Mar. Sci. Tech., Tokai, University 7:63–117.

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Nigrelli, R.F., K.S. Ketchen, and G.D. Ruggieri. 1965. Studies on virus diseases of fishes: Epizootiology of epithelial tumors in the skin of flatfishes of the Pacific Coast, with special reference to the sand sole (Psettichthys melanostictus) from northern Hecate Strait, British Columbia, Canada. Zoologica (NY) 50:115–122. OEHHA (Office of Environmental Health Hazard Assessment). 2001. California sport fish advisories. California Environmental Protection Agency, Office of Environmental Health Hazard Assessment, Sacramento, CA. 11 pp. Pastor, D., J. Boix, V. Fernandez, and J. Albaiges. 1996. Bioaccumulation of organochlorinated contaminants in three estuarine fish species (Mullus barbatus, Mugil cephalus, and Dicentrarcus labrax). Mar. Poll. Bull. 32:257–262. Perkins, E.J., J.R.S. Gilchrist, and O.J. Abbott. 1972. Incidence of epidermal lesions in fish of the North East Irish Sea area, 1971. Nature (London) 238:101–103. Perkins, P.S., and R. Gartman. 1997. Host-parasite relationship of the copepod eye parasite, Phrixocephalus cincinnatus, and Pacific sanddab (Citharichthys sordidus) collected from sewage outfall areas. Bull. So. Calif. Acad. Sci. 96(3): 87–132. Puffer, H.W., M.J. Duda., and S.P. Azen. 1982. Potential health hazards from consumption of fish caught in polluted coastal waters of Los Angeles County. No. Am. J. Fish. Man. 2:74–79. Risebrough, R.W., F.C. Sibley, and M.N. Kirven. 1971. Reproductive failure in brown pelican of Anacapa Island in 1969. Am. Birds 25:8–9. Roy, L.A., J.L. Armstrong, K. Sakamoto, S. Steinert, E. Perkins, D.P. Lomax, L.L. Johnson, and D. Schlenk. 2003. The relationship of biochemical endpoints to histopathology and population metrics in feral flatfish species collected near the municipal wastewater outfall of Orange County, California, USA. Environ. Tox. Chem. 22(6):1309– 1317. Russell, F.E., and P. Kotin. 1957. Squamous papilloma in the white croaker. J. Nat. Cancer Inst. 18(6):857–861. Schiff, K.C. 2000. Sediment chemistry on the mainland shelf of the Southern California Bight. Mar. Pollut. Bull. 40:268–276. Schiff, K.C., and M.J. Allen. 2000. Chlorinated hydrocarbons in flatfishes from the Southern California Bight. Environ. Tox. Chem. 19(6): 1559–1565. Schiff, K.C., M.J. Allen, E.Y. Zeng, and S.M. Bay. 2000. Southern California. Mar. Poll. Bull. 41(1-6):76–93. SFEI (San Francisco Estuary Institute). 2000. San Francisco Bay seafood consumption study. San Francisco Estuary Institute, Richmond, CA., 310 pp. Sherwood, M. 1982. Fin erosion, liver condition, and trace contaminant exposure in fishes from three coastal regions. pp. 359–377. In: G.F. Mayer (ed.). Ecological Stress and the New York Bight: Science and Management. NOAA, Stony Brook, NY. Sindermann, C.J. 1979. Pollution-associated diseases and abnormalities of fish and shellfish: a review. U.S. Fish Bull. 76(4):717–749. Smith, R.W., M. Bergen, S.B. Weisberg, D. Cadien, A. Dalkey, D. Montagne, J.K. Stull, and R.G. Velarde. 2001. Benthic response

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index for assessing infaunal communities on the southern California mainland shelf. Ecol. Appl. 11(4):1073–1087. Sommer, H., and F.N. Clark. 1946. Effect of red water on marine life in Santa Monica Bay, California. Calif. Fish Game 32(2):100–101. Spies, R.B., J.S. Felton, and L. Dillard. 1982. Hepatic mixed function oxidases in California flatfishes are increased in contaminated environments by oil and PCB ingestion. Mar. Biol. 70(2):117–127. Spies, R.B., and P. Thomas. 1995. Reproductive and endocrine status of female kelp bass from a contaminated site in the Southern California Bight and estrogen receptor binding of DDTs. pp. 113–133. In: R.M. Rolland, M. Gilbertson, and R.E. Peterson (eds.), Chemically induced alterations in functional development and reproduction of fishes. SETAC Press, Pensacola, FL. Stein, J.E., T.K. Collier, W.L. Reichert, E. Casillas, T. Hom, and U. Varanasi. 1993. Bioindicators of contaminant exposure and sublethal effects in benthic fish from Puget Sound, WA, USA. Mar. Environ. Res. 35:95–100. Stull, J. 1995. Two decades of marine biological monitoring, Palos Verdes, California, 1972 to 1992. Bull. So. Calif. Acad. Sci. 94: 21–45. Stull, J.K., K.A. Dreyden, and P.A. Gregory. 1987. A historical review of fisheries statistics and environmental and societal influences off the Palos Verdes Peninsula, California. Cal COFI Rep. 28:135–154. Stull, J.K., and C.-L. Tang. 1996. Demersal fish trawls off Palos Verdes, southern California, 1973–1993. Cal COFI Rep. 37:211–240. Ui, J. 1969. Minamata disease and water pollution by industrial waste. Rev. Intern. Oceanogr. Med. 13/14:5–35. USCB (United States Census Bureau). 2001. Population change and distribution, 1999 to 2000. U. S. Dep. of Commerce, Census Bureau, Washington, DC. 7 pp. USEPA (United States Environmental Protection Agency). 1995. Guidance for assessing chemical contaminant data for use in fish advisories. Volume 1-Fish Sampling and Analysis. 2nd edition. U. S. Environmental Protection Agency, Office of Water, Washington, DC. EPA 823-R-95-007. Valentine, D.W. 1975. Skeletal anomalies in marine teleosts. pp. 695–718. In: W.E. Ribeline and G. Migaki (eds.), The pathology of fishes. University Wisconsin Press, Madison, WI. Wellings, S.R., C.E. Alpers, B.B. McCain, and B.S. Miller. 1976. Fin erosion disease of starry flounder (Platichthys stellatus) and English sole (Parophrys vetulus) in the estuary of the Duwamish River, Seattle, Washington. J. Fish. Res. Bd. Canada 33:2577–2586. Young, D.R., A.J. Mearns, T.K. Jan, T.C. Heesen, M.D. Moore, R.P. Eganhouse, G.P. Hershelman, and R.W. Gossett. 1980. Trophic structure and pollutant concentrations in marine ecosystems of southern California. CalCOFI 21:197–206. Young, P.H. 1964. Some effects of sewer effluent on marine life. Calif. Fish Game 50(1):33–41. Zeng, E.Y., and M.I. Venkatesan. 1999. Dispersion of sediment DDTs in the coastal ocean off southern California. Sci. Total Environ. 229: 195–208.

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CHAPTER 24

Alien Fishes R O B E RT E. S C H R O ETE R AN D P ETE R B. M OYLE

Introduction Over 90 species and subspecies of fish have been introduced into the waters of California; 69 of these have become established (Dill and Cordone, 1997). Although a majority of these fish are freshwater species, alien species have also become established in estuaries, bays and open water marine habitats along the Pacific Coast (Dill and Cordone, 1997; Moyle, 2002). So far, alien marine species that have achieved the greatest success are estuarine and anadromous species, although few attempts have been made to introduce true (stenohaline) marine species into coastal California waters (Dill and Cordone, 1997). The only major attempt in California to move marine fishes into new waters was the translocation of over 30 species of marine fish into the Salton Sea in southern California, resulting in the establishment of 4 species. However, given the widespread and on going introduction of alien marine organisms into coastal environments (Carlton, 1996, 2000), it is likely that additional alien fishes will become established in California. The purpose of this chapter is to describe the species and patterns of alien fish invasions in the marine environments of California in order to provide a better understanding of their past, present, and future impacts. We begin this chapter by providing an overview of marine fish introductions to date. We then provide accounts of alien fishes currently found within the marine (estuaries and open water marine) environments of California, including their origin, distribution and effects on other marine organisms, especially fishes. We conclude by briefly answering the following questions: 1) Why are there so few successful alien fishes in the marine environments of California?, 2) What has been the impact of alien fishes in the marine environments?, 3) What marine environments in California are most invasible?, and 4) What is the future of alien fishes in California, especially in conjunction with environmental change?

Overview of Marine Introductions Introductions into marine systems have been increasing as a result of intentional movement of fish and as by-products of other human activities, such as transoceanic shipping, aquaculture, and the artificial connection of major water bodies

(Cohen, 1987; Baltz, 1991; Cohen and Carlton, 1998). The most common means of by-product introductions is the movement of organisms in ballast water of ships. However, alien organisms have also been introduced following their attachment to ship hulls and to oysters and other invertebrates brought in for food or bait. In addition, introductions of plants and invertebrates that adversely affect fish populations through alteration of food webs and habitats have been on the rise (Caddy, 1993; Ruiz et al., 1997; Cohen and Carlton, 1998; Berdnikov et al., 1999). The full extent of alien introductions into marine waters worldwide has been difficult to determine given that accurate species accounts are largely unavailable, many introductions are not reported, and many species are considered to be cryptogenic (place of natural origin unknown) (Baltz, 1991; Cohen and Carlton, 1998). Nonetheless, alien fishes are now common in marine waters worldwide (Carlton, 1985; Baltz, 1991). In general, intentional and by-product fish introductions have been most successful and have had the greatest impact within estuaries and inland seas (Baltz, 1991). Moyle (1999) attributed this success to the fact that estuaries and inland seas are often significantly altered through water diversion, development and pollution; they are also places where the frequency of introductions is high and species intentionally introduced are often well matched to the environment. In addition, large numbers of non-fish invaders have become established in these waters, resulting in significant changes to the function and structure of the ecosystems (Cohen and Carlton, 1998). These changes may make these systems even more vulnerable to invasion through a process termed invasional meltdown by Simberloff and Van Holle (1999). Invasional meltdown occurs when one or more alien species change the physical or biological conditions present in an ecosystem, which in turn facilitates the invasion of additional alien species. In this situation both the biotic resistance (e.g., competition and predation by native organisms) and environmental resistance (physical and chemical conditions adverse to establishment) to invasion are reduced. The often drastic changes in aquatic communities caused by alien species in estuaries and inland seas suggests possible scenarios for other marine environments as alien species become more pervasive. In open water marine systems, the introduction of

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TA B L E 24-1

Alien Fishes Introduced Into Marine Waters of California

Species

Date

Reason

Environment

Marine Status

Striped bass, Morone saxatilis American shad, Alosa sapidissima Brown trout, Salmo trutta Western mosquitofish, Gambusia affinis Threadfin shad, Dorosoma petenense Rainwater killifish, Lucania parva Wakasagi, Hypomesus nipponensis Chameleon goby, Tridentiger trigonocephalus Yellowfin goby, Acanthogobius flavimanus Mozambique tilapia, Oreochromis mossambica Redbelly tilapia, Tilapia zilli Sailfin molly, Poecilia latipinna Inland silverside, Menidia beryllina Shimofuri goby, Tridentiger bifasciatus Shokihaze goby, Tridentiger barbatus American eel, Anguilla rostrata. Milkfish, Chanos chanos Ayu, Plecoglossu altivelis Atlantic salmon, Salmo salar

1879 1871 1893 1922 1954 1950s 1959 1960 1960s 1960s 1960s 1960s 1967 1980 1995 1874 1877 1961 1874

food, sport food, sport sport insect control forage by-product forage by-product by-product aquaculture weed control pet release insect control by-product by-product food food food, sport Food, sport

F, E, B, M F, E, B, M F, E, M F, E F, E E, B F, E, B? B, M E, B, M E, B F, E F, E, B F, E, B F, E E, B F, E, B, M E, B, M F, E, B, M F, E, B, M

Common Common Rare Locally abundant Locally abundant Locally abundant Invading Locally common common, spreading Uncommon Locally common Locally abundant Locally abundant, spreading Invading Invading Failed Failed Failed Failed

Tautog, Tautoga unitis

1874

Food

B, M

Failed

NOTE:

Date corresponds to the date of initial stocking or when species was first discovered. F
freshwater, E
estuarine, B
Bay, and M
marine.

alien species has thus far had little impact, which is likely the result of few species successfully invading these habitats (see Baltz, 1991 for exceptions). Patterns of fish introductions into California marine waters are similar to those observed worldwide. Twenty fish species, which inhabit estuaries and open marine waters in their native range, are known to have been introduced into California. Fifteen of 20 species were introduced intentionally, to provide sport, food, pets, and control of nuisance organisms (table 24-1). Only 5 of these intentional plants were unsuccessful: American eel, Atlantic salmon, ayu, milkfish and the only true open water marine introduction attempt, the tautog (Dill and Cordone, 1997). In addition, at least 2 other species of catadromous eels have been found in California waters but they seem to be individual escapees from illegal attempts to import them for food (Dill and Cordone, 1997). A majority of the established alien fish species are found in estuaries and bays, although two anadromous species, striped bass and American shad, are commonly found in the open ocean waters off the California coast. While only 5 of the 15 alien marine fishes found within estuarine and coastal habitats of California are the result of byproduct introductions (table 24-1), by-product introductions have been increasing in recent years (Moyle, 1999). In fact, Cohen and Carlton (1998) have dubbed the San Francisco Estuary “the most invaded estuary in the world” as a result of the phenomenal numbers of by-product introductions of plants, invertebrates, and fish. The most common means of by-product introductions of alien fish into California’s waters is in the ballast water of ships. Such is the case with the chameleon goby, yellowfin goby, shimofuri goby, and shokihaze goby. The most recent of the ballast water introductions is the shokihaze goby, which was first captured in the San Francisco Estuary in 1997 and has recently become abundant. The rainwater killifish apparently arrived in the railroad cars full of oyster shells and spat brought in for rearing in San

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Francisco Bay. Other fish species may have already found their way into California waters, but remain undetected.

Species Accounts In the following section, we provide descriptions of alien marine species currently found in California including their origin, current patterns of distribution, environmental tolerances relating to potential range expansions and their known and potential effects on the aquatic communities. Our discussion is limited to species that are likely to occur on a regular basis in water with salinities greater than 10–15 ppt. Consequently, we exclude many freshwater fishes that occasionally occur in estuarine environments. The species accounts are organized by physiological tolerances: a) euryhaline marine species, b) estuarine species, c) anadromous species, and d) euryhaline freshwater species.

Euryhaline Marine Species CHAM E LEON GOBY

The chameleon goby (Gobiidae) is one of three species from the genus Tridentiger introduced into California waters (see fig. 24-1). It was first found in Los Angeles harbor in 1960 and was found in San Francisco Bay in 1962 (Dill and Cordone, 1997). More recently (1995 and 1998), the chameleon goby has been found in San Diego Bay (Pondella and Chinn, 2005) providing evidence that its range continues to expand either through continued shipping transport or active migration. It is native to the Asian Pacific and is typically restricted to marine habitats, being found only occasionally in brackish waters (Matern and Fleming, 1995). The chameleon goby was likely introduced into California waters through ballast water transport (Matern and Fleming, 1995) but attachment to

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F I G U R E 24.1 Examples of alien fishes that have established populations in coastal marine waters in California.

fouling organisms on ships and on imported giant Pacific or Japanese oysters have also been suggested as transport mechanisms (Dill and Cordone, 1997). Within San Francisco Bay, chameleon goby rarely exceed 90 mm in total length and are typically short lived, with only a few individuals reaching two years of age (Baxter et al., 1999). Chameleon goby are found in a wide range of temperatures, but appear to have a restricted distribution depending on salinity. In San Francisco Bay, they are routinely found in salinities ranging from 10–35 ppt (mean salinity 27 ppt), but are most abundant in waters with salinities between 24–32 ppt (Baxter et al., 1999). The impact of chameleon goby on native fishes has not been investigated. Given their benthic habits, they may be interacting competitively with other small bottom fishes, which in San Francisco Bay, includes species in the families Gobiidae (longjaw mudsucker, bay goby, cheekspot goby, and arrow goby); Cottidae (staghorn sculpin); and Batrachoididae (plainfin midshipman). However, their low abundance suggests that it is unlikely that they are having significant adverse effects. Between 1980 and 1995, chameleon goby made up only a small percentage (1%) of the total otter trawl catch of fish in San Francisco Bay (Baxter et al., 1999).

YE LLOWF I N GOBY

The yellowfin goby is native to the shallow coastal waters of Japan, Korea, and China (see fig. 24-1). They were first collected in the San Francisco Estuary in 1963 and were found in the Los Angeles Harbor around 1977 (Brittan et al., 1963; Moyle, 2002). These populations were likely established as a result of the transfer of larvae or small juveniles in the ballast water of ships. From these two areas, yellowfin goby have spread along the California coast as far north as Tomales Bay. In northern California, they are most abundant between Elkhorn Slough and Tomales Bay (Miller and Lea, 1972). In southern California, they have spread south as far as San Diego County and have been captured in various coastal lagoons and marshes (Swift et al., 1993) including the Tijuana Estuary (Zedler, Nordby and Kus, 1992) and Sweetwater Marsh National Wildlife Refuge in San Diego Bay (Gregory et al., 1998). Within the San Francisco Estuary, the yellowfin goby is one of the most common bottom fishes and it continues to expand its range into both fresh and brackish water habitats (Baxter, 1999). The effects of the introduction of the yellowfin goby on California fishes are largely unknown, due to the lack of studies.

ALIEN FISHES

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One exception is Usui (1981), who found no impact of yellowfin goby on native staghorn sculpin in Newport Bay. Nonetheless, it appears that given their high abundance, broad tolerance of environmental conditions (freshwater to 40 ppt; temperatures to 28C), relatively large size (17  cm SL), and predatory feeding habits as adults, yellowfin goby may be adversely affecting other bottom fishes found within the same habitats. One native species, which appears to be especially vulnerable is the tidewater goby, Eucyclogobius newberryi, a federally threatened species (U.S. Fish and Wildlife Service, 1994). The tidewater goby is a small (50 mm SL) benthic fish, which is endemic to the coastal lagoons, marshes and creeks of California (Swift et al, 1989; Moyle, 2002) and would seem to be very vulnerable to yellowfin goby predation. Fortunately, the yellowfin goby has so far had difficulty in establishing itself in small lagoon habitats where tidewater goby are most likely to be found. This may be because these small lagoon habitats typically are disconnected from the ocean most of the year, which results in salinities too low for successful yellowfin goby reproduction (breeding requires at least 5 ppt; Moyle, 2002).

Estuarine Species S H I MOF U R I G O BY

The shimofuri goby is the second of three species within the genus Tridentiger to become established into California waters. It is native to Japan and the coast of northern Asia (Moyle, 2002). It was likely introduced into the San Francisco Estuary through ballast water discharge (Matern and Fleming, 1995). Shimofuri goby were first identified in Suisun Marsh, in the upper San Francisco Estuary in 1985, thus were likely introduced into the San Francisco Estuary a few years earlier. Following its introduction, it quickly became one of the most abundant species in the estuary, reflecting its high reproductive potential and pelagic larvae (Matern, 1999). It is now widely distributed in tidal habitats, but prefers shallow water habitat (2m) in areas with complex structure including rocks, logs, and tule root masses, which are used for cover and breeding (Moyle, 2002). The shimofuri goby inhabits fresh and estuarine waters with salinities up to 17 ppt and is tolerant of a wide range of temperatures (to 37C) (Matern, 2001). It is eclectic in its diet, but often eats alien invertebrates (barnacles, hydroids) that have few other predators. While the salinity tolerances of the shimofuri goby will keep it from colonizing new areas by moving through the ocean, it has demonstrated a surprising capacity to move through fresh water. It has been able move through the California Aqueduct and colonize reservoirs in southern California. By 1990, the shimofuri goby was found in Pyramid Reservoir, approximately 513 km from the San Francisco Estuary and in Piru Creek below the reservoir (Matern and Fleming, 1995). This range expansion indicates that the shimofuri goby can be expected in any of the reservoirs fed by water from the California Aqueduct and will ultimately colonize the estuaries downstream from them (Moyle, 2002). The shimofuri goby is a highly aggressive species, especially adult males, which defend territories vigorously. In a laboratory experiment it was found that the tidewater goby was considerably disadvantaged during aggressive encounters with the shimofuri goby and was even preyed upon by larger shimofuri gobies (Matern, 1999). These types of aggressive encounters can be expected with other bottom dwelling fishes with com-

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petition being most intense for limited resources such as shelters for breeding and predator avoidance. Fish species that are most likely to be adversely affected by shimofuri goby are bottom fishes found within similar habitats such as prickly sculpin, staghorn sculpin, and tidewater goby. S HOK I HAZ E GOBY

The shokihaze goby is the most recent Tridentiger species to become established in the San Francisco Estuary. It was first collected in 1997, but has increased in abundance and distribution in recent years (Slater, 2005). As is the case with the other Tridentiger species, the shokihaze goby was probably introduced into the San Francisco Estuary as a result of a ballast water transfer from Asia. Little is known about the shokihaze goby in the San Francisco Estuary, except that it has been found in both fresh and brackish water environments with salinities as high as 28 ppt (Greiner, 2002). According to Dotu (1956), shokihaze goby in Ariake Sound, Japan, can live longer than 3 years and reach a size greater than 120 mm, but may mature as early as the first year at a size of 40–85 mm. The largest shokihaze goby captured in the San Francisco Estuary was greater than 120 mm total length (Steve Slater, CDFG, personal communication). In Japan, shokihaze goby inhabit oyster beds on muddy tide flats (Dotu, 1956). Within the San Francisco Estuary, shokihaze goby are typically found in deep channel habitats. The diet of shokihaze goby in the San Francisco Estuary is unknown, but those captured in Ariake Sound consumed annelids, small crustaceans squid, and young fish including other gobies (Dotu, 1956). The shokihaze goby thus has the potential to have negative effects on small benthic fishes and invertebrates in newly invaded habitats. R A I N WATE R K I LLI F I S H

The rainwater killifish (Fundulidae) is native to the eastern United States from Cape Cod to Texas, with inland populations in New Mexico and Florida (Moyle, 2002). The first California specimens were found in 1958 in both fresh and brackish waters tributary to San Francisco Bay (Dill and Cordone, 1997). The original source of introduction in the San Francisco Bay is unknown, but may have resulted from a ballast water introduction or as a hitchhiker (as eggs) on transported eastern oysters (Hubbs and Miller, 1965). Rainwater killifish are currently found in low abundance in the San Francisco Estuary, but are locally abundant within salt marshes in the lower bay (Moyle, 2002). Outside San Francisco Bay, rainwater killifish have been collected in Orange County (Irvine Lake), Riverside County (Arroyo Seco Creek—tributary of Vail Lake) and Santa Barbara County (Swift et al., 1993). The introduction of the Irvine Lake and Arroyo Seco Creek populations may have resulted when game fish collected from the Pecos River, New Mexico, were introduced into the region (Hubbs and Miller, 1965; Dill and Cordone, 1997). Because of the small size of rainwater killifish, their current low abundance, and diet consisting mostly of small invertebrates including copepods and mosquitos (Dill and Cordone, 1997), it is unlikely that they are having a significant impact on the native species found within the system. They are, however, capable of tolerating both fresh water and highly saline conditions (twice that of seawater), so it is likely that they will expand their range along the coast of California, if they have not done so already. Rainwater killifish are easily confused

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with the widely introduced western mosquitofish; thus its current range may be under-estimated.

Anadromous Species STR I P E D BAS S

The striped bass (Moronidae) is a large voracious piscivore native to the streams and bays of the Atlantic Coast and the Gulf of Mexico extending from the St. Lawrence River in the north to Louisiana in the south (see fig. 24-1). It was first introduced to the Pacific Coast in 1879 with a plant of 135 fish from the Navasink River, New Jersey released into the San Francisco Estuary. A second plant of 300 fish from New Jersey was made in 1882 (Dill and Cordone, 1997). The introduction of striped bass was so successful that a commercial fishery for striped bass began operation as early as 1888, and by 1899 over 1.2 million pounds of striped bass were harvested (Skinner, 1962). Striped bass are now widely distributed along the Pacific Coast from 25 miles south of the Mexico border to British Columbia (Moyle, 2002). Warm water conditions associated with El Nino events result in its greatest abundance and distribution in marine waters (Moyle, 2002). Despite its broad distribution, the main breeding population for striped bass on the Pacific Coast remains within the San Francisco Estuary. A smaller breeding population is also present in Coos Bay, Oregon (Moyle, 2002). Striped bass move regularly between salt and fresh water, but spend a majority of their life cycle in estuaries (Moyle, 2002). Striped bass migrate seasonally into rivers in late winter and early spring to spawn with the largest migration occurring up the Sacramento River. Striped bass are one of the most abundant fish in the San Francisco Estuary, although their numbers have been steadily declining since the 1930s from multiple interactive causes (Moyle, 2002). In recent years there has been a decline in carrying capacity of juveniles as a result of reduced food supplies, which may be partly responsible for the overall decline in this species (Kimmerer et al., 2000), although adult fish have inexplicably increased in abundance in recent years. The marine sport fishery may also have contributed to the decline because many of the fish caught are the largest, oldest, and most fecund females (W. A. Bennett, UC Davis, pers. comm.). The impacts of striped bass on native fishes in California were likely to have been most severe during the initial years following establishment (Moyle, 2002). During this time, striped bass probably contributed to the decline of native fishes, including salmonids, through predation. Striped bass may also have played a major role in the extinction of native estuarine fishes, but this is difficult to prove with existing information (Moyle, 2002). The continued anthropogenic degradation of estuarine systems in California has made it particularly difficult to determine the effects that striped bass have had on native species. For instance a considerable decline in salmon abundance occurred at the same time as the historic increase in striped bass abundance. Yet, it is difficult to untangle striped bass predation as a cause of salmon decline from other factors that occurred simultaneously, such as excessive fisheries, alteration of the estuary through gold mining activities, watershed development, and pollution. AM E R ICAN S HAD

American shad are large clupeids (up to 48 cm FL in California waters) native to the Atlantic Coast from Labrador to the

St. Johns River, Florida (Moyle, 2002) (see fig. 24-1). Stemming from their popularity as a food fish on the east Coast, American shad were introduced into California waters in 1871 (Dill and Cordone, 1997). Between 1871 and 1881, over 800,000 fry captured from New York were transported and introduced into California in the Sacramento River (Dill and Cordone, 1997). American shad quickly increased in number and by 1879 a commercial fishery became established (Skinner, 1962). Since their introduction they have rapidly expanded their range to include waters from Todos Santos Bay in Mexico to Cook Inlet, Alaska, with spawning runs occurring in a number of rivers, including the Columbia River (Moyle, 2002). An additional population has also become established in the Kamchatka Peninsula in Russia (Moyle, 2002). The Pacific Coast populations of American shad spend 3–5 years of their life at sea where their migration routes and activities are largely unknown. What little direct information exists on extent of American shad migrations consists of data collected from a tagging study conducted in the Sacramento River, which found that tagged fish migrated as far south as Monterey Bay and north to Eureka (Moyle, 2002). The rapid and widespread colonization of habitats thousands of kilometers away from the point of original stocking clearly indicates that American shad have the ability and tendency to migrate considerable distances. Return migrations to the rivers in California tend to take place beginning in autumn and extend through early June with largest migrations occurring as water temperatures warm to 17–24C. As juveniles, American shad rear within rivers and estuaries feeding on a variety of prey including zooplankton, mysid shrimp, copepods and amphipods (Moyle, 2002). Juveniles typically spend 1-2 years in fresh water and brackish water habitats prior to migrating to the sea, with the timing being largely influenced by environmental conditions (Moyle, 2002). The effect that the American shad have had on other species is unknown, but is unlikely to be significant, given their plankton-feeding habits. While their numbers appears to be lower today than they were historically, they still support a popular sport fishery in California (Moyle, 2002). WA K A S AG I

The wakasagi, a smelt (Osmeridae) native to Japan, was introduced into California reservoirs in the 1950s as a forage species. It was originally introduced under the name pond smelt, Hypomesus olidus, because it was assumed to be the same species as the native delta smelt, Hypomesus transpacificus, now a state and federally threatened California endemic (Stanley et al., 1995; Moyle, 2002). In Japan, wakasagi are anadromous and are found in bays estuaries and coastal waters (Utoh, 1988). The wakasagi has slowly expanded its range in California, which now includes the San Francisco Estuary (Aasen et al., 1998). The history of this introduction reflects the casual attitude toward introductions of fish that once prevailed in California. By the 1950s, numerous cold-water reservoirs existed and fisheries managers decided that a planktivorous forage fish was needed to improve growth of the various salmonids planted as sport fish. Because it was difficult to collect delta smelt from the San Francisco Estuary, the Japanese pond smelt, for which a well-developed aquaculture program already existed, was selected for introduction (Wales, 1962). The original plants, in six reservoirs, resulted in the wakasagi becoming established in the Klamath and Sacramento watersheds (Moyle, 2002).

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The first reported collection of wakasagi in the San Francisco Estuary occurred in 1974 (Aasen et al., 1998) and they are now being found on a regular basis. Wakasagi were likely transported from the foothill reservoirs to the San Francisco Estuary during periods of high reservoir releases. Swanson et al. (2000) found that wakasagi are well suited to the waters of the San Francisco Estuary and are more tolerant than delta smelt to stressful environmental conditions including maximum temperatures (wakasagi 29.1  1.3C vs. delta smelt 25.4  1.7C), minimum temperatures (wakasagi 2.3  0.9C vs. delta smelt 7.5  1.2C) and high salinities (wakasagi 26.8  3.0 ppt vs. delta smelt 19.1  2.1 ppt). Given the current overlap in distributions of delta smelt and wakasagi and the increase in wakasagi abundance in recent years, it is likely that wakasagi will adversely affect delta smelt through competition for food and space, predation on their larvae, and hybridization (Stanley et al., 1995; Trenham et al., 1998). They may also have negative effects on the native longfin smelt, Spirinchus thaleichthys, which is also in decline in the estuary. The environmental tolerances of wakasagi clearly indicate that it could expand its range to include the more saline San Francisco Bay and surrounding coastal waters.

found to occur in waters with temperatures of 8–34C with optimal growth and survival in environments at 20–25C (Moyle, 2002). They have been found in waters with salinities as high as 33 ppt and are common in salinities of 10–15 ppt (Moyle, 2002). Optimal salinity for larval growth and survival is 15 ppt although they are also successful in fresh water (Moyle, 2002). The inland silverside is extremely prolific and is often one of the most abundant littoral zone species in both fresh and brackish water. They can deplete zooplankton populations and are voracious predators on larval fish (Moyle, 2002). They are thus capable of having negative effects on native fishes. Within the San Francisco Estuary, the effects of inland silverside on other organisms has not been thoroughly investigated, but given their high abundance in shallow water areas, they have the potential to affect populations of splittail, juvenile salmon and other fishes. Indeed, the decline of delta smelt has largely coincided with the silverside invasion of the estuary. Bennett and Moyle (1996) have suggested that the delta smelt is particularly vulnerable to inland silverside predation. The silverside is an unusually effective predator on fish larvae (W. A. Bennett, University of California Davis, pers. comm.) and delta smelt spawn in shallow areas where silversides are abundant.

B ROW N TROUT

Brown trout (Salmonidae) were first introduced into California in 1893 from Europe as a sport species (Dill and Cordone, 1997). They are primarily a freshwater fish in California, but adult sea-run brown trout or smolts have been found in both the Sacramento and Klamath rivers (Moyle, 2002). While anadromous populations are common in their native range, anadromous brown trout have remained rare in California, thus have probably had little impact on native fishes.

Euryhaline Freshwater Species I N LAN D S I LVE R S I DE

The inland silverside (Atherinopsidae) is a planktivore native to estuaries and lower reaches of coastal streams along the Atlantic Coast of the United States and the Gulf Coast from Florida to Veracruz, Mexico (Moyle, 2002). It was originally introduced into Clear Lake, Lake County, in 1967 from Texoma Reservoir, Oklahoma. The purpose of the introduction was to control populations of the Clear Lake gnat (Chaoborus astictopus). At the time of its introduction, the inland silverside was listed as the Mississippi silverside, M. audens, which was thought to be a freshwater form distinct from the estuarine M. beryllina (Moyle, 2002). The two forms are indistinguishable (Chernoff et al., 1981; Moyle, 2002). This finding is supported by the expansion of the inland silversides range in California following its introduction. By 1975, it had colonized the brackish waters of the San Francisco Estuary where they are now abundant (Moyle, 2002). The inland silverside has also managed to disperse through the waterways of the California Aqueduct and by 1988 had become well established in most of the reservoirs connected to this system (Swift et al., 1993). They thus are likely to eventually colonize estuaries and lagoons in southern California. The inland silverside is tolerant of a wide range of environmental conditions and is well suited for both freshwater and brackish water environments in California. They have been

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S A I LF I N M O LLY

The sailfin molly (Poeciliidae) is native to the southern United States and northern Mexico, where it is found in a variety of habitats including coastal fresh water, brackish water and salt water (Moyle, 2002) (see fig. 24-1). It became established in the Salton Sea in the 1960s, as the result of fish escaping from tropical fish farms and/or releases by aquarists. It was soon present in the Colorado River and, presumably, its delta and brackish areas along the upper Gulf of California. By the 1980s and 1990s, populations were recorded in a number of salt marshes in southern California, from Ventura County to San Diego County [and in Tijuana Marsh in Mexico] (Swift et al., 1993, Gregory, 1998). Sailfin mollies tolerate a wide range of salinities (0–87 ppt) but generally require temperatures above 20C for survival and 24–33C for reproduction and growth (Moyle, 2002). Their temperature requirements limits their ability to colonize many habitats and to move through marine waters to new areas, although their main method of dispersal seems to be humans releasing unwanted pets. They feed primarily on algae and detritus and attain a maximum total length of 15 cm (although fish over 8 cm TL are unusual) (Moyle, 2002). Sailfin mollies have been implicated in the decline of endemic pupfishes in California and Nevada deserts, but their effects on fishes and invertebrates in coastal salt marshes is not well understood. Given their small size and limited diet, it is unlikely that they have an appreciable effect on other fishes, but they apparently are important prey of herons and other predatory birds. W E STE R N MOSQU ITOF I S H

The western mosquitofish (Poeciliidae) is native to the southeastern USA and was first introduced into California in 1922 for mosquito control (Dill and Cordone, 1997) (see fig. 24-1). They are regarded as ideal for this purpose because they can survive a wide range of environmental conditions, including salt marshes and estuaries, live in the shallow quiet waters preferred

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by mosquito larvae, and are relatively non-selective predators on aquatic invertebrates. Mosquitofish can withstand large temperature fluctuations (0.5–42), but are found mainly where temperatures range from 10 to 35C. They are also typically found in habitats where salinities do not exceed 25 ppt, although they can survive salinities of up to 58 ppt (Moyle, 2002). These tolerances have allowed them to colonize most coastal marshes in the southern half of the state, often as the result of planting for mosquito control. In freshwater habitats, mosquitofish have been implicated in the decline and extinction of fish, amphibians, and invertebrates through predation and aggression (Moyle, 2002). There is so far no evidence that they have had negative impacts in salt marshes and similar habitats, but they are capable of preying on small fishes like tidewater gobies and in changing the food webs of estuarine channels. Because of their small size and littoral habits their abundance may be underestimated within the estuaries and bays of California. TH R EADF I N S HAD

Threadfin shad (Clupeidae) are native to streams, lakes, and estuaries along the coast of the Gulf of Mexico and occur as far south as Belize in South America (see fig. 24-1). They are a small, fast growing planktivore which often form large schools in surface waters. These attributes led resource managers to believe that it would be an ideal forage fish in California’s fresh waters (Dill and Cordone, 1997). Initial plantings in the 1950s in reservoirs in southern California and the Colorado River were followed by their introduction throughout the state and their subsequent invasion of estuaries downstream from the reservoirs (Moyle, 2002). They are most abundant in fresh water where summer temperatures exceed 22–24C. They become less abundant as salinity increases in estuaries, presumably because of their inability to reproduce at low temperatures or high salinities (Moyle, 2002). Within the San Francisco Estuary, threadfin shad experience heavy die offs when water temperatures cool to 6–8C (Turner, 1966). Nevertheless, they can survive and grow in sea water and are occasionally captured in salt water from Long Beach to Yaquina Bay, Oregon (Miller and Lea, 1972). Threadfin shad are often the most abundant planktivore in the low-salinity (5 ppt) waters of the San Francisco Estuary, where they may have negative effects on other estuarine fishes through depletion of zooplankton and predation on larvae. However such impacts are undocumented. They are, however, important prey for striped bass and other piscivores (Moyle, 2002). In more saline environments, they are rarely abundant enough to have much effect on other fishes. TI LAP IA

At least four species of African tilapias (Cichlidae) and their hybrids have become established in California, but only two (Mozambique tilapia and redbelly tilapia) occur in saltwater habitats outside this region (Moyle, 2002) (see fig. 24-1). The Salton Sea and the Colorado River (including its delta) are the centers of tilapia abundance in the western United States, but tilapia also are present in some southern California salt marshes and estuaries. Tilapia in general are tropical fishes, so rarely persist in areas where temperatures drop below 10–15C for extended periods. Redbelly and Mozambique tilapia can both live in sea water and Mozambique tilapia can tolerate salinities as high as 120 ppt (Moyle, 2002).

The redbelly tilapia was widely introduced into southern California in the 1970s for aquatic weed control and it is permanently established in ditches in the Salton Sea area. It became established briefly in marine waters off Huntington Beach and possibly upper Newport Bay (Knaggs, 1977), but is apparently no longer present (Dill and Cordone, 1997). Mozambique tilapia (and/or its hybrids with other tilapia species) is the most widespread tilapia in California. It appears to be established in the upper reaches of what pass for estuaries in Orange and Los Angeles counties (Knaggs, 1977; Dill and Cordone, 1997) but is only locally abundant. Its ability to persist in estuarine systems over the long term is questionable, given its temperature requirements.

Other Species: Fishes of the Salton Sea The largest experiment in marine fish introductions in California was the attempt to establish fish from the Gulf of California in the Salton Sea, as the sea changed from a freshwater system to a saltwater system as the result of evaporation (Dill and Cordone, 1997; Moyle, 2002). The Salton Sea is a large (980 km2), shallow (average depth 5 m) inland body of water located in Riverside and Imperial Counties. It was created in 1905–1907 when the Colorado River decided to make a new irrigation ditch its main channel and flowed into the Salton Basin. It started out as a freshwater lake but by the 1940s it was too salty for most freshwater fishes. The first successful marine introduction was a euryhaline goby, the longjaw mudsucker (Gobiidae) brought in from coastal California as bait in the 1930s. Between 1948 and 1956, systematic efforts by the California Department of Fish and Game resulted in about 20,000 fish representing 31 species being introduced, mostly from the Gulf of California (Dill and Cordone, 1997). Three species survived the transplantion experience and became abundant enough to support a sport fishery: bairdiella (Sciaenidae), orangemouth corvina (Sciaenidae) and sargo (Haemulidae). The salinity of the sea is still increasing, so is unlikely to be able to support their populations for much longer. The most abundant species in the sea is the Mozambique tilapia (Moyle, 2002). This experiment in marine fish introductions does demonstrate that stenohaline marine fishes can be moved and established under the right conditions.

Conclusions Why are there so few successful alien species in the marine environments of California? The patterns of alien fish invasions in marine environments of California are typical of those worldwide: most established aliens live in estuaries, bays, or enclosed basins (Baltz, 1991). There have only been 15 intentional introductions which have resulted in 10 species becoming established in estuarine and open water marine habitats off the coast of California. Eight of the 15 intentional marine introductions discussed in this chapter are freshwater fishes that have unexpectedly spread into estuarine or open marine waters. Five others are anadromous species that were first introduced into fresh water with the intention of establishing them in marine and freshwater habitats. Overall there has been a high degree of success (67%) with intentional introductions. Thus, the low number of alien species currently found in marine waters of California may be due more to the

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limited number of intentional introductions of estuarine and marine species than to a lack of invisibility of these habitats. The establishment of alien fish in the estuaries and bays of California as a result of byproduct introductions, primarily ballast water releases, has also been limited (5 species). In contrast, by 1998 over 160 species of alien invertebrates and plants had become established in salt or brackish waters in California (Cohen and Carlton, 1998). Reasons for the limited number of successfully established alien fish species, relative to the number of alien invertebrate and plant species, are unclear and complicated by the fact that the total number of alien fish species introduced, yet unsuccessfully established, is unknown. It is likely that the small number of successful byproduct introductions of alien fish species observed in California marine waters is a result of limited survival ability in ballast water of the early life history stages. Another way of addressing this question is to examine why some introduced species failed to become established. Marine introductions that failed in California include milkfish, tautog, American eel, ayu and Atlantic salmon. The introduction of milkfish, tautog, American eel and ayu most likely failed as a result of a poor match between the species and the environment into which they were introduced. This may have been the case especially for the amphidromous ayu, which failed despite heavy and repeated stocking of eggs and fry into the Eel River. In the case of the milkfish, tautog and American eel, the relatively few individuals released (100, 1000 and approximately 2000, respectively; Dill and Cordone, 1997) probably also contributed to their poor success. However, over 300,000 Atlantic salmon were stocked over several years in suitable locations in California, but this species never became established, perhaps because of interactions with native salmonids (Dill and Cordone, 1997). Arguably the high diversity of native fishes (500 species) found off California decreases the likelihood of an introduced species surviving, through mechanisms of biotic resistance. For example, a behavioral study in British Columbia, Canada, suggests that reduction of biotic resistance may be playing a large role in the establishment of Atlantic salmon there. Volpe et al. (2001) found that despite behavioral differences between steelhead and Atlantic salmon, the species with prior residency held a competitive advantage over the invading species. It has been further hypothesized that the current increase in successful natural reproduction of escaped Atlantic Salmon in British Columbia waters (Volpe et al., 2000) could be related to marked declines in the abundance of steelhead in these same locations (Volpe et al., 2001). Given the high abundance of steelhead and Pacific salmon in California, during the time Atlantic salmon were stocked (1874, 1891, and 1929–1932), there may have been considerable biotic resistance preventing the successful establishment of Atlantic salmon. If biotic resistance prevented the earlier invasion of Atlantic salmon in California waters, then the low abundance of steelhead and Pacific salmon today may leave many California waters vulnerable to future invasions. Although no Atlantic salmon have recently found their way into California waters, it remains a possibility because of their continued release from aquaculture facilities along the Pacific Coast. Another possibility is an increase in anadromous brown trout in response to reduced native salmonid populations. In any case, Moyle and Light (1997) argue that under the right circumstances most invaders can overcome biotic resistance. Indeed the ability of yellowfin goby to colonize new areas along the coast of Central California demonstrates that

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marine invasions are possible, as does the widespread distribution of striped bass and American shad. What has been the impact of alien fishes in marine environments? Major changes in aquatic communities as a result of invading alien species have been noted mainly in enclosed seas and estuaries (Baltz, 1991). The San Francisco Estuary is often dominated by alien fishes in its fresh and brackish water portions but by native marine fishes in San Francisco Bay proper, where salinities rarely drop below 25 ppt (Matern et al., 2002). Throughout the estuary, including San Francisco Bay, striped bass are the most abundant piscivore and they probably changed the trophic structure of the estuary to some degree, but the introduction occurred before any studies were done and coincided with a period in which many other changes were taking place as well. One of the more recent invaders of the estuary, the shimofuri goby, was intensively studied by Matern (1999), but he could not detect any obvious effects on the existing fauna, despite its high abundance. Presumably the specializations of this fish, combined with rapid changes in estuarine conditions during the invasion period (Bennett and Moyle, 1996), limited its ability to impact other species. Overall, the impacts of alien fishes in California’s marine environments appear to have been minimal. However, future impacts remain uncertain. What marine environments in California are most invasible? Within California, all alien species that have become established are associated with bays and estuaries for at least a portion of their life cycle. No stenohaline marine species have become established in open water marine environments, which suggests that open water marine habitats are less invasible. This is due, at least in part, to the low number of attempts to establish species in open marine waters of California and the reduced opportunity for byproduct introductions. In support of these findings, Baltz (1991) concluded in his review of worldwide marine fish introductions that fish communities in closed or semi-closed systems are more easily invaded than open water systems with only Hawaiian reefs and the Mediterranean Sea being invaded by more than a few species. Of the marine fish invasions in California waters, those in the bays and estuaries of California have probably been more successful than those in open water marine habitats because 1) bay and estuarine species are more likely to be tolerant of changing seasonal and daily fluctuations in environmental conditions; 2) there is most likely a similarity in environmental conditions and habitats within temperate bays and estuaries worldwide especially between international ports located at similar latitudes on opposite sides of the Pacific Ocean; 3) there is often a high number of larval and juvenile fish vulnerable to ballast water uptake in bays and estuaries stemming from their heavy use as spawning and rearing areas by highly fecund species; 4) few propagules are currently taken from and released into open water marine habitats; 5) susceptibility to invasion may be dependent upon original species richness, with areas of low species richness being more susceptible to invasion than those with higher species richness (Gido and Brown, 1999). The bays and estuaries in California are typically species poor, thus perhaps more invasible. Whereas open water marine habitats of California are species-rich (this volume), thus may be more resistant to invasion. What is the future of alien fishes in California, especially in conjunction with environmental change? Alien fishes will likely continue to become more abundant in California’s marine waters as the result of: 1) expansion of the ranges of established

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species, 2) new species arriving via ballast water, and 3) species arriving via aquaculture operations. It is likely that the four alien goby species in California will continue to expand their ranges with negative effects on native gobies and other benthic fishes and on invertebrates in estuaries, lagoons, and bays. They are all aggressive predators that have the potential to disperse by means of their abundant pelagic larvae, either through aqueducts, through ballast water in ships moving up and down the coast, or through natural dispersion by coastal currents. The inland silverside is also likely to invade more estuaries with negative consequences to native fishes. It is also likely that additional marine fishes commonly found within bays and estuaries in major Pacific Ocean ports will become established via ballast water of ships, unless zero tolerance limits for life in ballast water become standard practice (backed by laws which are actively enforced). Ballast water introductions occur not only from cross-ocean transport, but also from intra-regional transport of organisms from heavily invaded ports to those in outlying areas. Intra-regional transport of invertebrates already is believed to have introduced species into the waters of Elkhorn Slough, an estuary in central California, and is a mechanism that will likely further redistribute species from previously established populations in major ports to those with no international shipping (Wasson et al., 2001). It is extremely difficult to eliminate ballast water as a source of alien species because of the vast number of ships involved in global and regional transport, the volume of water taken up in ballast, and costs and time associated with current treatment strategies. Current treatment strategies for ships approaching North American ports focus on flushing of ballast tanks while at sea, because most of the organisms are unlikely to survive in the open ocean or in cold ocean water in the tanks. However, this process is time consuming, cannot always be performed for safety reasons (e.g., during rough seas) and may not be completely effective (Locke et al., 1993). Other potential methods to treat ballast water are being investigated including chemical, thermal, ultraviolet, oxygenation, deoxygenation and various combinations of the above (see National Research Council, 1996 for review; also Niimi, 1997; Rigby et al., 1999; Kuzirian et al., 2001; Suttherland et al., 2001; Browning, 2001; Tamburri et al., 2002). However, no alternative solutions have been selected or are being implemented. Thus, ballast water introductions will likely continue at least into the near future. Given the current high demand for marine fish and shellfish, aquaculture activities including the importation of shellfish and other organisms will likely continue to be a source of alien species. This includes imports for the saltwater aquarium industry (e.g., at least one species of aquarium fish, the lionfish, Pterois volitans, has already become established along the coast of Florida). Among the many organisms currently at risk of becoming established is the Atlantic salmon, as discussed previously. The concern over the potential establishment of Atlantic salmon into Pacific waters is warranted given the rapid increase in culture of Atlantic salmon over the past 29 years. By 1998, it was estimated that Atlantic salmon biomass in aquaculture worldwide had already exceeded that in its native range (Gross, 1998). Net pen culture is the primary method of raising Atlantic salmon in marine environments. This method of culture often results in significant invasions of fish into Pacific Coast waters. A single fish farm in Puget Sound, Washington in 1996 and 1997 “accidentally” released

over 460,000 Atlantic salmon (Gross, 1998). Significant releases from other fish farm operations have also occurred, such as the release of several million rainbow trout, coho salmon, and Atlantic salmon during heavy storms in 1994 and 1995 in the Pacific waters in Southern Chile (Soto et al., 2001). Although large-scale releases are a major concern, the continuous release (leakage) of fish (Alverson and Ruggerone, 1997) further increases the possibility of eventual establishment of Atlantic salmon in Pacific waters. This reality may be closer than anticipated since natural reproduction of Atlantic salmon has already been documented in coastal British Columbia rivers (Volpe et al., 2000). The probability of alien species becoming established and spreading has likely increased in recent years because marine systems have become disrupted by pollution, commercial fishing, and other major insults to ecosystem structure. As a rule, alien species are most likely to successfully invade human-disturbed environments (Elton, 1958; Moyle and Light, 1997). Global climate change, especially increases in ocean temperature, is also likely to increase the probability of new invasions being successful and of existing alien species being able to expand their range (Carlton, 2000).

Literature Cited Aasen, G.A., D.A. Sweetnam, and L. M. Lynch. 1998. Establishment of the wakasagi, Hypomesus nipponensis, in the Sacramento-San Joaquin estuary. Calif. Fish Game 84:31–35. Alverson, D. L., and G. T. Ruggerone. 1997. Escaped farm salmon: environmental and ecological concerns. Discussion Paper Part B. pp. Bi–B100. In: Salmon Aquaculture Review Technical Advisory Team Discussion Papers Vol. 3. Environmental Assessment Office, Victoria B.C. Baltz, D. M. 1991. Introduced fishes in marine systems and inland seas. Biolog. Conserv. 56:151–171. Baxter, R., K. Heib, S. Deleon, K. Fleming, and J. Orsi. 1999. Report on the 1980–1995 fish shrimp and crab sampling in the San Francisco Estuary, California. IEP Technical Report no. 63. 503 pp. Bennett, W. A., and P. B. Moyle. 1996. Where have all the fishes gone? Interactive factors producing fish declines in the Sacramento-San Joaquin estuary. pp. 519–541. In: J. T. Hollibaugh, ed. San Francisco Bay: the Ecosystem. Pacific Division, AAAS, San Francisco. Berdnikov, S. V., V. V. Selyutin, V. V. Vasilchenko, and J.F. Caddy. 1999. Trophodynamic model of the Black and Azov Sea pelagic ecosystem: consequences of the comb jelly, Mnemiopsis leydei, invasion. Fish. Res.42:261–289. Brittan, M. R., A. B. Albrecht, and J.B. Hopkirk. 1963. An oriental goby collected in the San Joaquin River Delta near Stockton, California. Calif. Fish Game 49:302–304. Browning, W. J. 2001. Method and apparatus for killing microorganisms in ship ballast water. Official Gazette of the United States Patent and Trademark Office Patents Jan. 9, 2001. 1242 (2): No Pagination US 6171508 January 09, 2001 210–750 USA Browning Transport Management, Inc., Norfolk, VA, USA Caddy, J. F. 1993. Toward a comparative evaluation of human impacts on fishery ecosystems of enclosed and semi-enclosed seas. Reviews, Fish. Sci. 1:57–95. Carlton, J. T. 1985. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr. Mar. Biol. Ann. Rev. 23:313–371. ———. 1996. Marine bioinvasions: the alteration of marine ecosystems by nonindigenous species. Oceanography 9:36–43. ———. 2000. Global change and biological invasions of the oceans. pp. 31–54. In: H. A. Mooney and R.J. Hobbs, eds. Invasive species in a changing world. Island Press, Covelo CA. Chernoff, B., J. V. Conner, and C.F. Bryan. 1981. Systematics of the Menidia beryllina complex (Pisces: Atherinidae) from the Gulf of Mexico and its tributaries. Copeia 1981:319–335. Cohen, A. N., and J. T Carlton. 1998. Accelerating invasion rate in a highly invaded estuary. Science 279:555–558.

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Dill, W.A., and A.J. Cordone. 1997. History and status of introduced fishes in California, 1871–1996. Calif. Fish Game, Fish Bull. 178. 414 pp. Dotu, Y. 1957. The bionomics and life history of the goby, Triaenopogon barbatus (Gunther) in the innermost part of Ariake Sound. Science Bulletin Fac. Agr. Kyushu University 16:261–274. Elton, C.S. 1958. The ecology of invasions of plants and animals. Methuen, London. Gido, K.B., and J.H. Brown. 1999. Invasion of North American drainages by alien fish species. Fresh. Biol., 42, 387–399. Gregory, W.D., J.S. Desmond, J.B. Zedler, and B. Joy. 1998. Extension of two nonindigenous fishes, Acanthogobius flavimanus and Poecilia latipinna, into San Diego Bay marsh habitats. Calif. Fish Game 84:1–17. Greiner, T.A. 2002. Records of the shokihaze goby, Tridentiger barbatus (Gnther), newly introduced into the San Francisco Estuary. Calif. Fish Game 88:68–74. Gross, M.R. 1998. One species with two biologies: Atlantic salmon (Salmo salar) in the wild and in aquaculture. Can. J. Fish. Aquat. Sci. 55 (Suppl. 1):131–144. Hubbs, C.L., and R.R Miller. 1965. Studies of cyprinodont fishes. XXII. Variation in Lucania parva, its establishment in western United States, and description of a new species from an interior basin in Coahuila, Mexico. Univ. Mich. Mus. Zool. Misc. Publ. 127. 104 pp. Knaggs, E.H. 1977. Status of the genus Tilapia in California’s estuarine and marine waters. Calif. Nev. Wildlife Trans. 1977:60–67. Kimmerrer, W.J., J.H. Cowan, Jr., L.W. Miller and K.A. Rose. 2000. Analysis of an estuarine striped bass (Morone saxatilis) population: influence of density dependent mortality between metamorphosis and recruitment. Can. J. Fish. Aquat. Sci. 57:478–486. Kuzirian, A.M., E.C.S. Terry, D.L. Bechtel, and P.L. James. 2001. Hydrogen peroxide: An effective treatment for ballast water (General Scientific Meeting of the Marine Biological Laboratory Woods Hole, Massachusetts, USA August 13–14, 2001). Biol. Bull. (Woods Hole) 201:297–299. Locke, A., D.M. Reid, H.C. van Leeuwen, W.G. Sprules, and J.T. Carlton. 1993. Ballast water exchange as a means of controlling dispersal of freshwater organisms by ships. Canadian Journal of Fisheries and Aquatic Science 50:2086–2093. Matern, S.A. 1999. The invasion of the shimofuri goby (Tridentiger bifasciatus) into California: establishment, potential for spread, and likely effects. Ph.D. dissertation, Univ. Calif., Davis. 167 pp. ———. 2001. Using temperature and salinity tolerances to predict the success of the shimofuri goby, a recent invader into California. Trans. Am. Fish. Soc. 130:592–599. ———., and K.J. Fleming. 1995. Invasion of a third Asian goby, Tridentiger bifasciatus, into California. Calif. Fish Game 81:71–76. ———., P.B. Moyle, and L.C. Pierce. 2002. Ecology of native and alien fishes in a California estuarine marsh: 21 years of fluctuating coexistence. Trans. Am. Fish. Soc. Miller, D.J., and R.N. Lea. 1972. Guide to the coastal marine fishes of California. Calif. Fish Game, Fish Bull. 157, 235 pp. Moyle, P.B. 1999. Effects of invading species on freshwater and estuarine ecosystems. pp. 177–191. In: O.T. Sandlund,, P.J. Schei & Å. Viken, eds. Invasive species and biodiversity management Kluwer, Leiden. ———. 2002. Inland Fishes of California, 2nd edition. University of California Press, Berkeley (in press). Moyle, P.B., and T. Light. 1996. Biological invasions of fresh water: empirical rules and assembly theory. Biol. Cons. 78:149–162. National Research Council. 1996. Stemming the tide: controlling introductions of non-indigenous species by ship’s ballast water. National Academy Press, Washington, DC. Niimi, A.J. 1997. Chemical application as a treatment option to reduce the risk of accidental transfer of exotic organisms in ballast water (24th Annual Aquatic Toxicity Workshop Niagara Falls, Ontario, Canada October 20–22, 1997). Can. Tech. Rep. Fish. Aquat. Sci. 2192: 100–101. Pondell, D.J., and Z.K.J. Chinn. 2005. Records of Chameleon Goby, Tridentiger trigonocephalus, in San Diego Bay, California. Calif. Fish Game 91:57–59. Rigby, G.R., G.M. Hallegraeff, C. Sutton. 1999. Novel ballast water heating technique offers cost-effective treatment to reduce the risk

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of global transport of harmful marine organisms. Mar. Ecol. Progr. Ser. 191:289–293. Ruiz, G.M., J.T. Carlton, E.D. Grosholz, and A.H. Hines. 1997. Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am. Zool. 37:621–632. Simberloff, D., and D. Von Holle. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions, 1:21–32. Slater, S.B. 2005. Life history and diet of the shokihaze goby, Tridentiger barbatus, in the San Francisco Estuary. M.S. Thesis, California State University, Sacramento, 77 pp. Soto, D., F. Jara, and C. Moreno. 2001. Escaped salmon in the inner seas, Southern Chile: facing ecological and social conflicts. Ecol. Appl. 11:1750–1762. Sutherland, T.F., C.D. Levings, C.C. Elliott, and W.W. Hesse. 2001. Effect of a ballast water treatment system on survivorship of natural populations of marine plankton. Mar. Ecol. Progr. Ser. 210:139–148. Skinner, J.E. 1962. An historical review of the fish and wildlife resources of the San Francisco Bay area. California Fish Game, Water Projects Branch Report 1, 225 pp. Stanley, S.E., P.B. Moyle, and H.B. Shaffer. 1995. Allozyme analysis of delta smelt, Hypomesus transpacificus, and longfin smelt, Spirinchus thaleicthys, in the Sacramento-San Joaquin Estuary. Copeia 1995: 390–396. Swanson, C., T. Reid, P.S. Young, and J.J. Cech, Jr. 2000. Comparative environmental tolerances of threatened delta smelt (Hypomesus transpacificus) and introduced wakasagi (H. nipponensis) in an altered California estuary. Oecologia 123:384–390. Swift, C.C., J.L. Nelson, C. Maslow, and T. Stein. 1989. Biology and distribution of the tidewater goby, Eucyclogobius newberryi (Pisces Gobiidae) of California. Contr. Science 404, Nat. Hist. Museum Los Angeles Co., Los Angeles. 19 pp. Swift, C.C., T.R. Haglund, M. Ruiz, and R.N. Fisher. 1993. The status and distribution of the freshwater fishes of southern California. Bull. So. Calif. Acad. Sci. 92:101–167. Tamburri, M.N., K. Wasson, and M. Matsuda. 2002. Ballast water deoxygenation can prevent aquatic introductions while reducing ship corrosion. Biolog. Conserv. 103:331–341. Trenham, P.C., B.H. Shaffer, and P.B. Moyle. 1998. Biochemical identification and assessment of population subdivision in morphologically similar native and invading smelt species (Hypomesus) in the Sacramento-San Joaquin Estuary, California. Trans. Am. Fish. Soc. 127:417–424. Turner, J.L. 1966. Distribution of threadfin shad, Dorosoma pretenense; tule perch, Hysterocarpus traskii; sculpin spp. and crawfish spp. in the Sacramento-San Joaquin Delta. pp. 160–168. In: J.L. Turner and D.W. Kelly, comps. Ecological studies of the Sacramento-San Joaquin Delta. Part II, fishes of the delta. Calif. Fish and Game, Fish Bull. 136. Usui, C.A. 1981. Behavioral, metabolic, and seasonal size comparisons of an introduced gobiid fish, Acanthogobius flavimanus, and a native cottid, Leptocottus armatus, from Upper Newport Bay, California. M.S. thesis, Calif. State Univ., Fullerton. 52 pp. U.S. Fish and Wildlife Service (USFWS). 1994. Endangered and threatened wildlife and plants: determination of endangered status for the tidewater goby. Federal Register 59:5494–5499. Utoh, H. 1988. Life history and fishery of the smelt, Hypomesus transpacificus nipponensis, McAllister (in Japanese). Japan J. Limno. 49:296–299. Volpe, J.P., B.R. Anholt, and B.W. Glickman. 2001. Competition among juvenile Atlantic salmon (Salmo salar) and steelhead (Oncorhynchus mykiss): relevance to invasion potential in British Columbia. Can. J. Fish. Aquat. Sci. 58:197–207. Volpe J.P., E.B. Taylor, D.W. Rimmer, and B.W. Glickman. 2000. Evidence of natural reproduction of aquaculture-escaped Atlantic salmon in a coastal British Columbia river. Conserv. Biol. 14:899–903. Wales, J.H. 1962. Introduction of pond smelt from Japan into California. Calif. Fish Game 48:141–142. Wasson, K., C. J. Zabin, L. Bedinger, M. C. Diaz, and J. S. Pearse. 2001. Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol. Conserv. 102: 143–153. Zedler, J.B., C.S. Nordy, and B.E. Kus. 1992. The ecology of the Tijuana Estuary, California: a national estuarine research reserve. NOAA Office of Coastal Resource Management, Sanctuaries and Reserves Division, Washington D.C. 151 pp.

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CHAPTER 25

Climate Change and Overexploitation M I C HAE L H. H O R N AN D J O H N S. STE P H E N S, J R.

Introduction The complex evolutionary and biogeographic history of the California marine fish fauna has been amply demonstrated in the preceding chapters. In this concluding chapter our purposes are to summarize concisely the historical origins of the fauna, its present status, and the future of the fauna under a scenario of ongoing and perhaps accelerated climate change. This increased rate of change is most likely to be seen as increasing ocean temperatures in the northeastern Pacific into the foreseeable future. Over the last three decades the understanding of climate change has grown dramatically in both finer resolution on different spatial and temporal scales and on greater predictability of its impacts on the distribution and abundance of coastal fish faunas and other biotic elements. Major geological events and associated climatic upheavals have been central to the development of the California fish fauna with its signatures of varied origins and high diversity. Smaller scale events and episodes in recent millennia, centuries, and decades increasingly mix with anthropogenic influences of the past 150 years to complicate the picture of faunal dynamics as seen at the present time. Predicting the future conditions of the California fish fauna, then, must somehow take into account both the anticipated impacts of climate change and the entangling influences of human activities, especially overexploitation.

Deep History: Pangaea to the Miocene The distant origins of the California fish fauna might reasonably begin with the major plate tectonic events that occurred in the middle to late Mesozoic as summarized by Brown and Lomolino (1998). The formation of the supercontinent Pangaea and the world ocean Panthalassa in the early Triassic, about 250 million years ago, and its subsequent breakup starting in the late Triassic and extending through the Cretaceous had profound consequences for global climate and biogeographic patterns of both terrestrial and marine biotas. Landmasses drifted northward, and marine basins formed and became isolated to differing degrees. Pangaea split, forming Laurasia to the north and Gondwanaland to the south, and

each of these large landmasses fragmented leading to the continental positions and configurations seen today. By the end of the Cretaceous, shallow seas had broadly transgressed onto and then receded from the land, and the Tethys Sea, an equatorial seaway, had opened. With increased longitudinal and latitudinal separation of ocean basins the opportunity for the evolution of distinct coastal marine biotas emerged. Several events occurred in the Cenozoic era that had lasting effects on coastal biotas in the Pacific including, ultimately, the development of the California fish fauna. Separation of Antarctica from Australia by the early Oligocene epoch established the cold circum-antarctic current and, in turn, the global latitudinal temperature gradient, resulting in climatic change and extinction of a variety of tropical organisms (Stanley, 1987). A mid-Miocene warming event in low latitudes then may have led to the antitropical distributions known among several groups of New World marine fishes, including the silversides (Atherinidae; now Atherinopsidae, see below) and anchovies (Engraulidae), according to evidence assembled by White (1986). His climatic vicariance hypothesis for the diversification of the silversides also involves emergence and disappearance of an early (Paleocene) Central American land barrier as well as emergence of the more well-known and existing Central American isthmus in the Pliocene about 50 million years later (fig. 25-1). White (1986) asserted that a result of this series of geological and climatic events was the antitropical distribution of the Atherinopsinae with members in both North America and South America. The more recent systematic treatment of the New World silversides (Atherinopsidae) by Dyer (1998) does not reject White’s vicariant hypothesis nor does the analysis of genetic divergence of a similarly distributed fish group, the myxodin clinids, by Stepien (1992). On the other hand, the widely differing patterns of genetic divergence among antitropical chub mackerels (Scomber), jack mackerels (Trachurus) and hakes (Merluccius) show that such distributions are not all of similar origin, and these patterns led Stepien and Rosenblatt (1996) to propose that antitropical distributions in the eastern Pacific are best understood based on varying dispersal abilities and temperature tolerances. The complex origins and distribution patterns of California marine fishes again become evident.

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F I G U R E 25-1 Biogeographic history and phylogenetic relationships of New World silversides (Atherinopsidae) from the Cretaceous period to the Pliocene epoch. Significant vicariant events in evolution of the family indicated on area cladogram at lower right: divergence of the Atherinopsinae and Mediniinae followed emergence of early Cenozoic isthmian link; divergence of modern tribes of Atherinopsinae followed climatic disruption in Miocene (after White, 1986).

The strictly marine North American atherinopsines not only provide an example of how a portion of the California fish fauna may have developed but also of species with disjunct populations or sister taxa in the upper Gulf of California and temperate northeastern Pacific including California. Six species in four genera compose the monophyletic atherinopsine group (Dyer, 1998). Three species are restricted to the upper Gulf of California. These taxa are the false grunion (Colpichthys regis and C. hubbsi) and the Gulf grunion (Leuresthes sardina), which is sister to the California grunion (Leuresthes tenuis) that occurs on the Pacific coast of California and Baja California. Topsmelt (Atherinops affinis) and jacksmelt (Atherinopsis californiensis) are distributed widely in

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the northeastern Pacific, but only the topsmelt has a disjunct population in the upper Gulf. These disjunct distributions among the atherinopsine fishes signal another set of geological processes that has fundamentally affected California fish biogeography beginning in the middle Miocene. At this time, about 15 MY ago, the peninsula that was to become Baja California began to separate from mainland Mexico and by the end of the Miocene, about 5 MY, had reached its current configuration, thus forming the Gulf of California in the process (Helenes and Carreno, 1999; see chapter 2). At least 19 species of coastal fishes representing 14 families and a wide range of ecological groups have unequivocally disjunct populations in the northern

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Gulf of California and Pacific coastal waters of California and Baja California (chapter 2). The number of disjunct taxa is likely to increase as molecular techniques continue to be applied to assessing the degree of genetic divergence between the isolated populations in the two regions within a framework of dispersal/vicariance hypotheses. According to Dawson and co-authors (chapter 2), the 12 species with disjunct distributions that have been subjected to molecular analysis show either indistinct Gulf and Pacific populations (4 species), suggesting high levels of gene flow, or distinct Gulf and Pacific clades (8 species), indicating vicariant events. Of the latter group, divergence times range from as recently as 0.2–0.4 MY in the bluebanded goby (Lythrypnus dalli) to 0.4–3.0 MY for California grunion and Gulf grunion. Whether disjunction of populations occurred via dispersal around the peninsula during episodes of Pleistocene glacial cooling or after passage through a seaway in the southern or the northern part of the peninsula remains uncertain, but, overall, generally similar historical conditions molded the population structure of these divided species (Bernardi et al., 2003). The absence of populations of these disjunct species in the southern part of the Gulf apparently cannot be explained by warmer temperatures alone but requires lack of suitable habitat and perhaps other features of the southern Gulf to exclude these species (see chapter 2). What does seem clear from the study of these disjunctions is that biogeographic provinces are the products of both evolutionary processes and ecological conditions. As an example in the same part of the world, Hastings (2000) showed that chaenopsid fishes in rocky shore habitats are isolated from one another by long stretches of soft-bottom habitat separating the Cortez and Mexican provinces and the Mexican and Panamic provinces from one another. The latitudinal temperature gradient that had developed by the Oligocene combined with this type of habitat isolation seems to have promoted speciation, produced coincident range end points, and led to recognition of faunal provinces and regions.

Shallow History: Pliocene and Pleistocene Epochs Effects of Glacial and Interglacial Periods The foregoing discussion has presaged the importance of the climatic cooling that began in the Pliocene (5.0–1.8 MY) and culminated in the glaciation cycles of the Pleistocene (1.8 MY ago—Recent) for influencing the distribution patterns of California coastal fishes. Colder temperatures during the Pleistocene realigned northeastern Pacific coastal provinces to the south (fig. 25-2) and pushed California fish species southward, allowing some populations to traverse the existing Baja California peninsula, as mentioned above, either by dispersing around the end or migrating through seaways that subsequently closed. With recession of the glaciers and warming of ocean temperatures during interglacial periods, cool-water species returned northward including into the northern Gulf of California where they became disjunct populations. Another effect of the Pleistocene glaciations was to lower sea levels and thus to lessen the distances between the California mainland and neighboring Channel Islands as well as among the islands, especially the northern group (Anacapa, Santa Cruz, Santa Rosa, and San Miguel islands). The islands formed about 5 MY ago and as a result of uplift have generally

F I G U R E 25-2 Shifts in marine biogeographic provinces along the west coast of North America between 18,000 BP (late Pleistocene) and modern times. According to Fields et al. (1993), provinces in the waters off southern California and northern Baja California may have remained relatively stable while those in other regions varied more during the same period. More recent data on coastal foraminiferan assemblages, however, suggest that temperatures were cooler in southern California waters during the last glaciation (18,000 BP) and that the northern boundary of the warm temperate region was pushed farther south along the coast of Baja California (after Kennett and Venz, 1995).

increased in area since that time (Vedder and Howell, 1980; Sorlien, 1994). These increased sizes and reduced distances stemming from glacial and tectonic activities are reflected in the population genetic structure of the few coastal fish species that have been studied. For example, Dawson and co-authors

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(chapter 2) showed that populations of black perch (Embiotoca jacksoni) around the northern Channel Islands are genetically similar to one another and, collectively, to fish at the mainland area closest to the islands. Moreover, black perch populations from the southern Channel Islands (San Nicolas, Santa Catalina, and San Clemente) are more similar to those from the northern islands than to the closest mainland populations. The authors of chapter 2 emphasize the importance of deepwater barriers in reducing gene flow and of the direction of prevailing current patterns in maintaining genetic similarity. We have focused attention above on the glacial periods and their effects, but, of course, they alternated with interglacial periods that produced opposing impacts. Overall, highly fluctuating climatic conditions dominated the coastal environment during the Pleistocene epoch. In a highly integrated analysis incorporating paleoclimatology, coastal geomorphology, paleoceanography, and archaeology, Graham et al. (2003) argued that the late Quaternary (Pleistocene
Holocene or Recent) sea-level rise of the last 18,500 years caused a major ecological shift in the Southern California Bight from highly productive rocky reefs to less productive sandy habitats, each supporting very different benthic communities. These authors argue that, until recent centuries or perhaps millennia, the southern California coastal zone alternated between long periods of rocky reef-kelp forest dominated habitats and shorter periods of sandy infaunal ecosystems at a frequency of about 100,000 years, all driven by climatic fluctuation and sea-level change. The kelp forest habitat should have been inhabited by expansive populations of seaweeds, large fishes such as giant sea bass (Stereolepis gigas), California sheephead (Semicossyphus pulcher), lingcod (Ophiodon elongatus) and numerous species of rockfishes (Sebastes spp.), rocky-reef invertebrates such as abalones, sea urchins and mussels, and the predatory sea otter (Enhydra lutris). Rocky intertidal zones in southern California might have resembled the rich and diverse rocky shore habitats now found only north of the Southern California Bight. As the climate warmed and sea level rose, productivity declined, infaunal invertebrates became prominent, and, overall, less food was available to American Indians who appeared in the southern California region at least as early as 12,000–13,000 BP. The food habits of these indigenous peoples appear to have tracked the changing marine resources although these early Americans may have influenced the ecosystems of which they were a part through selective predation but in a pattern of exploitation sustained over millennia (e.g., Erlandson, 1994).

Population Histories of Anchovies and Sardines A final observation on the temporal scale of the Pleistocene, i.e., shallow histories ranging from thousands to millions of years, offers potential insights for current problems of marine fish exploitation and for future designs on maintaining sustainable populations. Grant and Bowen (1998) point out that our increasing knowledge of past climates reveals that periodic climate changes are accompanied by strong regime shifts in the global ocean and that these changes in surface temperatures, current pathways, upwelling patterns, and retention eddies can result in severe population swings or even regional extinctions. Their molecular genetic analyses of anchovies (Engraulis) and sardines (Sardina, Sardinops) demonstrate that populations of these two clupeoid taxa, renowned for their marked fluctuations in temperate-zone boundary currents

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around the world (Schwartzlose et al., 1999), are subject to periodic extinctions and recolonizations and that mtDNA genealogies for Sardinops at least coalesce backward in less than 0.5 MY. Grant and Bowen reason that such climatedriven population changes may explain the low levels of genetic diversity and the shallow coalescence of mtDNA genealogies. The value of their analysis for halting the presentday upward spiral of exploitation is that even the most abundant marine fish populations are potentially at risk of extinction on both ecological and evolutionary time scales.

Recent History—Millennial Scale Anchovies and Sardines On a time scale of the Holocene or Recent epoch (i.e., thousands of years) we can continue with an examination of population fluctuations of anchovies and sardines in southern California that links backward to the Pleistocene patterns described above and forward to the fluctuations over the last century. Soutar and Isaacs (1969, 1974) published the first accounts of historical fluctuations of California fish populations by identifying and counting fish scales from anaerobic deposits off southern California and Baja California. Their data extended from 1810 to 1970 and included scales of northern anchovy (Engraulis mordax), Pacific sardine (Sardinops sagax), Pacific hake (Merluccius productus), Pacific saury (Cololabis saira), and Pacific chub mackerel (Scomber japonicus). Reconstruction of northern anchovy and Pacific sardine populations over the past two millennia by Baumgartner et al. (1992) using fish-scale-deposition rates in the Santa Barbara Basin revealed that these two species tend to vary over a period of about sixty years with northern anchovy also fluctuating over a period of 100 years (fig. 25-3). Anchovies and sardines show moderate correlation of population changes on time scales of centuries but not over shorter time periods. The scale-deposition record indicates nine major recoveries (increases from less than one to more than four million metric tons in biomass) and subsequent collapses of the sardine population during a 1,700-year span with an average recovery time of 30 years.

Sockeye Salmon In contrast, the abundance patterns of sockeye salmon (Oncorhynchus nerka) in Alaska based on sediment records were out of phase with those of anchovies and sardines in southern California over the past two millennia (Finney et al., 2002; fig. 25-4). Multi-century shifts of inferred sockeye abundance at about 2,100 BP and 1,200–800 BP correspond to intervals of major change in atmosphere-ocean circulation in the northeastern Pacific. At 2,100 BP sockeye abundance dropped sharply in synchrony with warming of marine waters in the Santa Barbara basin, whereas after 1,200 BP increased salmon numbers correspond to a time of glacial advances in southern Alaska and the Canadian Rockies. Both northern anchovies and Pacific sardines were more abundant from about 1,700 to 800 BP when sockeye salmon were low in numbers, whereas the reverse trend is apparent for the last 800 years. The abundances of other fishes depicted over the 2,200-year time span varied out of sequence with both the salmon and the anchovies and sardines (fig. 25-4). An important contribution of Finney

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F I G U R E 25-3 Composite time series of northern anchovy and Pacific sardine scale-deposition rates in the Santa Barbara Basin over the last
1700 years (after Baumgartner et al., 1992).

and co-workers is that their reconstructions of sockeye salmon abundances show that a shift to a regime of very low productivity, lasting centuries, can occur without the impacts of fisheries or other human influences. These results emphasize the need to understand the connections between ocean ecosystems and climate change now that fish species are seriously impacted by the additional stresses of commercial fishing, habitat deterioration, and global warming.

Historical Overfishing The analysis by Jackson et al. (2001) provides an effective transition from the millennial scale to the immediate past of the last 150 years and current conditions (see below) of coastal ecosystems in that they assess the impacts of historical overfishing from about 125,000 years ago to the present time. Their analysis of paleoecological, archaeological, and historical data provides a suggestion that overfishing of large vertebrates and shelled invertebrates has been the first and most important human disturbance to affect the coastal ecosystems that these authors examined. In historical times, overfishing would have been the only major impact of indigenous peoples on coastal resources. They expand preindustrial environmental effects to industrial societies and hypothesize a similar pattern (fig. 25-5). The sequence of other disturbances may vary, and the lag time between the onset of fishing and consequent alterations in coastal ecosystems may take decades to

centuries. They conclude that overfishing precedes all other types of disturbances but that such excessive exploitation also may often create the necessary conditions for eutrophication, disease outbreaks, and species introductions to occur. Moreover, their assessment places human-driven climate change as a now compounding force in but not the original cause of microbe population explosions, disease outbreaks, and species invasions in general. Jackson and colleagues argue that massive ecological extinctions of predators (e.g., sharks, sea otters), grazers (e.g., sea turtles, manatees), and suspension feeders (e.g., oysters) are bound to leave coastal ecosystems more vulnerable to invasion. The most relevant part of the Jackson et al. (2001) analysis for the California fish fauna is their focus on kelp forests in the northeastern Pacific (Alaska and California) as compared to those in the northwestern Atlantic (Gulf of Maine). The relatively diverse food web in southern California kelp forests historically included California sheephead as well as spiny lobsters and sea otters as predators of sea urchins and several species of abalone as competitors of sea urchins. Although sea otters were extirpated by the early 1800s, kelp forests in southern California did not begin to decline on a large scale until the 1950s when increased exploitation led to the ecological extinction of the sheephead, lobsters, and abalone. Information on these ecological extinctions is sparse, and certainly recent data show little evidence of either sheephead or spiny lobster decline in the Palos Verdes kelp forest over this period even with the loss of kelp (Stephens et al. 1984). The loss of the

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F I G U R E 25-4 Reconstruction of fish abundances in the northeastern Pacific Ocean over the past
2,200

years. Each series is plotted as the difference from the series mean calculated over this time period. Sockeye salmon abundances in Alaska are represented by the Karluk lake 15N profile (0/00). Northern anchovy and Pacific sardine abundances are represented by scale-deposition rates (no. of scales per 1,000 cm2 per year) from the Santa Barbara Basin, California (Baumgartner et al., 1992). A 50-year running average was applied to highlight long-term trends. Abundances of other fishes, including Pacific herring, Pacific hake, and cartilaginous fish, are represented by fish remains per 100 cm3 recovered from Saanich Inlet, British Columbia (Tunicliffe et al., 2001); data from two overlapping cores are presented (after Finney et al., 2002).

abalone reflects both overfishing and withering foot disease. Ironically, commercial exploitation of the largest sea urchin species in the 1970s and 1980s resulted in recovery of some of the kelp forests, but these systems now lacked substantial populations of consumers (Tegner and Dayton, 2000; see below).

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Immediate Past History: Last 150 Years to the Present Day Over the past century and a half, commercial exploitation, habitat degradation, and climate change have become increasingly serious problems for the existence and health of the California fish fauna. These major concerns have been

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F I G U R E 25-5 Historical sequence of human disturbances affecting coastal ecosystems. Fishing (step 1) always preceded other human disturbance in all cases examined. This sequence is the basis for the authors’ hypothesis of the primacy of overfishing in the deterioration of coastal ecosystems worldwide. Subsequent steps 2 through 5 have not been observed in every case and may vary in order (after Jackson et al., 2001 with permission from the American Association for the Advancement of Science).

discussed for the contemporary situation in earlier chapters of the book: biogeography of California coastal fishes by Horn, L. G. Allen and Lea in chapter 1; subsistence, commercial and recreational fisheries by Love in chapter 22, and pollution and habitat alteration by M. J. Allen and Pondella in chapter 23. In this section, we first summarize the changes in kelp forest ecosystems during the last 150 years. We then focus our attention on climate change but within a perspective that includes overexploitation and its pervasive importance as already described in the previous section. Overall, our rationale for an emphasis on climate change stems from our belief that the impacts of climate shifts ultimately will be greater and harder to manage than those resulting from overfishing, pollution, and other forms of habitat degradation.

Phase Shifts in Kelp Forest Ecosystems In their analysis of the past, present, and projected future of kelp forest ecosystems, Steneck et al. (2002) provide details of changes in these systems in southern California over the past few centuries and mainly the last 150 years that effectively links the Jackson et al. (2001) study of historical overfishing to present-day conditions that include increased attention to the effects of climate change. In the Southern California Bight, American Indians formed one of the densest concentrations of indigenous peoples in the world starting at least 12,000–13,000 BP, and they depended heavily on animals associated with kelp forests such as sheephead, abalone, and marine mammals, especially sea otters. Based on analysis of middens on San Clemente Island, increased fishing activity by maritime Indians appears to have caused a decline in sheephead size leading to a subsequent increase in purple sea urchin populations (Salls, 1991, 1995). Although Indians may have created local sea urchin barrens by hunting sea urchin predators such as sheephead and sea otters, any such effects were short-lived because Indian fishing activities essentially ended upon European contact as old world diseases and colonial oppression devastated American Indian societies (Erlandson et al., 2004). The 150-year lag between sea otter extinction in the early 1800s and the phase shift in kelp forests during the mid-twentieth century induced by sea urchin overgrazing (fig. 25-6) may have resulted from the countering effects of alternate competitors, herbivores, and predators of sea urchins (Cowan, 1983; Tegner and Levin,

1983; Schmitt, 1987). By the 1950s and 1960s, excessive harvesting of abalone, lobster, and sheephead may have greatly reduced these strong interactors in the kelp forest food web. These reductions freed urchins to overgraze kelp forests, and, along with a series of El Niño events, led to the virtual absence of kelp during the mid-twentieth century (fig. 25-6). The commercial harvesting of urchins that began in the 1970s reduced the urchin stocks and facilitated a shift back to a forested state (Tegner and Dayton, 1991; Steneck et al., 2002). Sheephead harvesting, however, accelerated again in the late 1980s with the development of a live fish market, reducing the importance of this predator in the system (Tegner and Dayton, 2000). Even though the relatively high diversity of southern California kelp forests probably has been important in maintaining the presence of these ecosystems in the region as currently recognized, kelp forests nevertheless have been subjected to “serial trophic-level dysfunction” (Steneck et al., 2002).

Climate Change, Fishing Pressure, and the Accelerating Dynamics of Coastal Fish Populations Both climate change and overexploitation have contributed in recent decades to an increasingly dynamic fish fauna in California coastal waters and to an extremely challenging set of problems threatening the continued health of marine ecosystems in the northeastern Pacific. Knowledge of climate change accelerated during the twentieth century such that, by the dawn of the present century, we have become much more adept at identifying and predicting shifts in climate over a wide range of spatial and temporal scales. Recent climate change can now be placed in a more global and longer-term perspective, and different types of climatic conditions, occurring over varying geographic expanses and time intervals, can be recognized. The importance of climate change now has global attention with an international scientific committee providing advice to stakeholders (Pittock, 2002). Present situations are being assessed and future conditions predicted for many marine ecosystems and their fish populations (e.g., Beamish and Noakes, 2002; McFarlane et al., 2002; Scavia et al., 2002; Wang and Schimel, 2003). Together, climate change and overexploitation have the potential to act synergistically to shift production areas and alter community composition and dominance (Verity et al., 2003) and most likely to multiply the problems each creates for the sustainability of marine ecosystems.

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F I G U R E 25-6 Temporal trends in kelp forests at Point Loma near San Diego in southern California. Width of arrows represents the magnitude

of the impact of the forcing function. The boxed area on the right of the figure indicates a period of high resolution subtidal data (after Steneck et al., 2002).

Types of Climatic Change Affecting the California Marine Fish Fauna At least three major kinds of climatic events influence the distribution and abundance of California marine fish species: 1) El Niño Southern Oscillation (ENSO) episodes, 2) Pacific Decadal Oscillations (PDO), and 3) global warming (see next section), in order of increasing spatial and temporal scales.

E L N IÑO SOUTH E R N OSCI LLATION (E N SO)

ENSOs comprise alternating warm El Niño and cool La Niña intervals. As described in chapter 1, El Niño events clearly affect fish distributions in the northeastern Pacific. Radovich (1961) documented the change in the fish fauna related to coastal warming in 1957–1959 (now recognized as a large ENSO event, and Mearns (1988) described unusual geographic occurrences of certain fish species along the Pacific coast. Lea and Rosenblatt (2000) documented the appearance of numerous warmer-water, Panamic species in the Southern California Bight during the 1997–1998 El Niño event, and Horn and co-authors (chapter 1) list 20 species, mostly of southern affinities, that have been added to the California fauna over the last 25 years. The majority of these added species appeared in California waters during this most recent El Niño episode. The alternating La Niña events are often of shorter duration (Kousky and Bell, 2000) and can cause reduced abundance among species of warm-water affinities (e.g., reef finspot,

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Paraclinus integripinnis) or increased abundance of even a transitional species such as the woolly sculpin (Clinocottus analis) in the same rocky intertidal habitat (Davis, 2000; chapter 8). Species of ichthyoplankton also showed predictable changes in abundance as well as in latitudinal distribution during the ENSO periods of the last half century based on analysis of CalCOFI samples (Moser and Watson, chapter 11). Among commercially important species, the cool-temperate chinook salmon (Oncorhynchus tshawytscha) was caught in much smaller numbers during the strong 1982–1983 El Niño event, whereas several warm-water species including yellowtail (Seriola lalandi) and skipjack tuna (Katsuwonus pelamis) were landed in much greater numbers (McGowan, 1985; Tegner and Dayton, 1987). Early juvenile Pacific hake (Merluccius productus), a member of the cool temperate and polar family Merlucciidae, responded to the 1997–1998 El Niño event in central California waters by broadening their zooplankton diet in response to low zooplankton biomass and then suffering poor growth and lowered survival rates in the face of the reduced food supply (Grover et al., 2002). PACI F IC DECADAL OSCI LL ATION (P D O): CLI MATE AN D O CEANO G RAP HY

Like an ENSO event, the PDO comprises a warm and a cool interval, but the PDO regimes are each 20–30 years in duration (Mantua et al., 1997; Hare et al., 1999; Hare and Mantua, 2000; Chavez et al., 2003; Levin, 2003). Major ecological

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F I G U R E 25-7 Condensed synthesis of oceanographic and biological conditions in the northeastern Pacific during sardine (warm) and anchovy

(cool) regimes (after from Chavez et al., 2003).

events occur on the decadal scale and in response to a shift from one regime to another (McGowan et al., 2003). The warm regime is characterized by above average sea-surface temperatures (SSTs) along the coasts of the Americas and in the tropics, cooler than average SSTs in the central North Pacific, anomalously low atmospheric pressure at sea level over the north Pacific and eastern Tropical Pacific, and high pressure anomalies in the western tropical Pacific centered over northern Australia. These conditions are basically reversed during the cool regime. Over the past century, two cool ocean regimes (1900–1924 and 1947–1976) and two warm regimes (1925–1946 and 1977–1999) have been generated by PDOs. The regime shift of 1976–1977 in the California Current was characterized by an abrupt rise in upper-ocean temperature associated with an intensified Aleutian Low-pressure system and a large, decadal decline in zooplankton biomass (McGowan et al., 2003). P D O: E F F E CTS ON ANCHOVI E S AN D SAR DI N E S

The multidecadal shifts in northern anchovy and Pacific sardine populations in boundary currents around the Pacific Ocean basin over the last century are now better understood with the discovery of the biological regime shifts associated with PDO events. Chavez et al. (2003) summarized these anchovy and sardine fluctuations in the context of cyclic changes in atmospheric and oceanographic conditions in the Pacific basin (fig. 25-7) and in doing so provided a more comprehensive explanation for the population variations

than does fishing pressure alone (cf. Murphy, 1966). The discovery of these biological regime shifts occurring about every 25 years preceded the description of the underlying physical processes and led to the suggestion (Hare and Mantua, 2000) that regime shifts may be better detected by monitoring marine organisms rather than climate. Synchrony exists among air and ocean temperatures, atmospheric carbon dioxide levels, coastal and open-ocean productivity, and anchovy and sardine landings as shown by Chavez et al. (2003), particularly for the southwestern tropical Pacific off Peru. Their extension of the analysis to the northeastern Pacific shows that the cool-water northern anchovy increases in abundance during a cool regime lasting about 25 years followed by a shift to a warm regime during which the warm-water Pacific sardine becomes relatively more abundant. The strength of these associations is demonstrated by Chavez and co-workers identifying these periods as an anchovy regime and a sardine regime, respectively. The commercial landings of northern anchovy and Pacific sardine in California over the better part of the twentieth century reflect these regime shifts reasonably well (fig. 25-8). P D O: E F F E CTS ON OTH E R S P E C I E S

The conditions that prevail during anchovy and sardine regimes affect more than just these two taxa (Chavez et al., 2003) as both commercial and non-commercial species are affected. During an anchovy regime at latitudes encompassing California, Oregon, and Washington, there are, relatively

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F I G U R E 25-8 Commercial landings (log10 kg) of northern anchovy and Pacific sardine in California from 1916–2001 with cool and warm regimes superimposed on this time period. Landings data for 1916–1999 obtained from Leet et al. (2001) and updated to 2001 from the California Department of Fish and Game website (www.dfg.ca.gov).

speaking, fewer sardines, higher nutrients, primary production, and zooplankton levels, and more salmon, rockfish, and seabirds; in contrast, during a sardine regime, the opposite conditions predominate (fig. 25-7). Although these alternating situations describe the big picture for each regime, a closer examination reveals greater complexity and variability. For example, larvae of mesopelagic fishes of southern offshore species responded to the regime shift of 1976–1977 by increasing markedly in the Southern California Bight after 1977, whereas no consistent response was detected in larval abundance of Subarctic-Transitional mesopelagic species or nearshore taxa (Smith and Moser, 2003). Moreover, chinook salmon populations showed differences in productivity in response to the 1976–1977 regime shift even among three adjacent regions: Snake River, upper Columbia River, and middle Columbia River (Levin, 2003). In addition, long-term studies (1974–1993 and continuing to the present) on subtidal reef fishes at two mainland sites in southern California, King Harbor and Palos Verdes, further demonstrate the effects of the 1976–1977 regime shift on fish populations (Stephens and Zerba, 1981; Stephens et al., 1994; Holbrook et al., 1997; fig. 25-9). Abundances of northern (cool-temperate) species declined abruptly with the onset of the warming event then remained relatively constant for 12 years before declining further in the 1990s. In contrast, abundances of southern species increased over the first 10–12 years of the study then declined sharply starting in the mid1980s. Finally, so-called Bight species increased sharply in abundance at the outset of the warm regime then declined followed by stable abundances over the next 16 years. Species

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richness declined by 15–25%, and, by 1993, 95% of the fish species had fallen in abundance by an average of nearly 70% because of drastic recruitment failure over the two decades. Ecosystem effects were similar over a study period of 1982–1995 at Santa Cruz Island, an island site to the north, where the surfperch (Embiotocidae) populations, their crustacean prey, and understory macroalgae all declined by about 80% (Holbrook et al., 1997). At King Harbor, recruitment and larval abundance have been at a low level since the late 1980s (Pondella and Stephens, 2002; Stephens and Pondella, 2002). At Palos Verdes, fish density appears to increase, sometimes sharply, during each El Niño event and then to recover to more long-term averages (J. S. Stephens, Jr., unpubl. data), an indication of the confounding effects of ENSO episodes when they overlay decadal regime conditions. Long-term studies of rocky intertidal fish assemblages are scarce in southern California compared to somewhat more extensive data available for central California shores. At Palos Verdes, Stephens (unpubl. data) noticed an increased abundance of zebraperch (Hermosilla azurea) following the 1976– 1977 shift to a warm regime, an observation that matches the overall increased occurrence of the species in the Southern California Bight during the sustained warm period from 1977 to 1999 (Sturm and Horn, 2001). Shorter-term effects of ENSO periods on the structure and habitat use by rocky intertidal fish assemblages near San Diego also have been documented (Davis, 2000; see chapter 8). On the central California coast near Piedras Blancas, a tidepool removal study that began in 1978 and spanned the 1982–1983 El Niño episode and a discontinuous 23-year period showed virtually no detectable

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politus) and white croaker (Genyonemus lineatus), as well as the walleye surfperch (Hyperprosopon argenteum), white seaperch (Phanerodon furcatus) and speckled sanddab (see chapter 10). The most comprehensive trawl studies of soft-bottom fishes in the Bight since the 1980s have been conducted by the Southern California Coastal Water Research Project (SCCWRP). Their results show that in 1994 and 1998 the number of fish per trawl were still low compared to those obtained in the mid1970s and that species, including queenfish and white croaker, began disappearing in the 1980s (Allen et al., 2001, 2002; see chapter 6). The most recent SCCWRP survey (2003) documents a return of some species not commonly observed since the regime change in the late 1970s (M. J. Allen, pers. comm.) P D O: U NAN SW E R E D QU E STION S

F I G U R E 25-9 Temporal patterns in the mean

standardized abundances of temperate reef fishes at King Harbor (dots) and Palos Verdes (triangles) in southern California for species belonging to the Northern, Bight, and Southern geographical range groups. The dashed line at 0 represents the 20-yr mean abundance of all species. Arrows indicate the 1976–1977 climatic shift from a cool regime to a warm regime (after Holbrook et al., 1997 with permission from the Ecological Society of America).

response either to the El Niño condition or to the presumed shift to a cool regime in 1999 (Horn, Allen and Boyle, unpubl. data). Trawl studies of near shore fish assemblages in the Southern California Bight (see chapters 4 and 6) that began in the 1960s as part of monitoring programs associated with ocean sewage outfalls and hot-water effluent from coastal power plants also show changes in fish populations that may, in retrospect, be related to the 1976–1977 regime shift. A significant drop in total number of fish caught per trawl occurred between 1976 and 1980 as well as reduction or loss of some dominant species such as halfbanded rockfish (Sebastes semicinctus), stripetail rockfish (S. saxicola), shiner perch (Cymatogaster aggregata), and speckled sanddab (Citharichthys stigmaeus) (Mearns et al., 1980; Stephens et al., 1983). Both shiner perch and sanddab disappeared from the shallow sand substratum at King Harbor during this time period and have not returned in large numbers. In a study conducted during the strong El Niño/La Niña episode of 1982–1984, Love et al. (1986) documented reduced recruitment in 10 southern California coastal species including the dominant sciaenids, queenfish (Seriphus

As Chavez et al. (2003) point out, several fundamental questions associated with regime shifts remain to be answered. These questions pertain to the underlying forcing behind these shifts, the mechanisms through which they influence fish populations, the time frame for a regime shift, and their relationship to El Niño and La Niña events. Determining that the late 1970s regime shift occurred took more than a decade, but these investigators assert that verification of the late 1990s shift will occur much sooner. Chavez and colleagues appeared confident of the 1999 shift citing the changes in fish abundance off Peru (fig. 25-7) as probably the strongest evidence for a long-term, late 1990s regime shift. They also mention declining sardine abundance off California (fig. 25-8) and Japan as further evidence. Still other signs of a recent shift to a cool regime include increasing anchovy abundance (fig. 25-8), recruitment failure of all three species of Paralabrax (kelp bass, P. clathratus; barred sand bass, P. nebulifer; and spotted sand bass, P. maculatofasciatus) during the last two years, and heavy recruitment of several species of cool-temperate fishes, including olive rockfish (Sebastes serranoides), vermilion rockfish (S. miniatus), cabezon (Scorpaenichthys marmoratus), and lingcod (Ophidion elongatus), based on diving and fishing observations at 10–30 m depth in the vicinity of Los Angeles Harbor (L. G. Allen, pers. comm.). ENSO episodes complicate the matter, as mentioned above, because although cool conditons prevailed all through 1999, 2000, and early 2001, warm or neutral conditions prevailed for the rest of 2001 and 2002 (data from the Climate Prediction Center, Camp Springs, Maryland, www.cpc.ncep.noaa.gov). Only more time and further studies will verify or refute the existence of a regime shift in the late 1990s.

Future Status: Next 100 Years Overexploitation The twenty-first century has begun with fishery decline representing a major problem in the northeastern Pacific and other ocean regions and climate change looming as a crisis of uncertain magnitude for marine ecosystems. Quantitative assessments of fishery catch data have demonstrated that intense, size-selective fishing mortality over the last 50 years has resulted in a decline in the mean trophic level of exploited fish groups (Pauly et al., 1998, 2000; Sala et al., 2004). This “fishing down the food web” means that the world fish catch has shifted gradually from primarily long-lived, high trophic-level

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F I G U R E 25-10 Global mean temperature projections from 1990 to 2100 for the six illustrative scenarios generated in the Special Report on Emissions Scenarios (SRES) based on a simple climate model tuned to a number of complex models with a range of climate sensitivities. The darker shading represents the envelope of the set of 35 scenarios employed to force climate models, using the average of the simple model results (mean climate sensitivity is 2.8o C). The lighter shading is the envelope based on all seven model projections (with climate sensitivity in the range of 1.7 to 4.2o C). The bars show, for each of the six illustrative SRES scenarios, the range of simple model results in 2100 for the seven model tunings. For comparison, the IS92 range of warmings in 2100 generated by the International Panel on Climate Change also is shown (after Pittock, 2002, as adapted from Houghton et al., 2001 with permission of Springer Science & Business Medic B.V.).

species to short-lived, low trophic level species. The evidence is staggering in its magnitude. Recent assessments report world declines in biomass of large predatory fishes of 90% from pre-industrial levels in the last 40 or so years (Myers and Worm, 2003), precipitous declines in large shark abundance (Baum and Myers, 2003; Baum et al., 2004), and collapse in abundance (median reduction of 83%) of principal fishery species groups from known historic levels with slow, even improbable, prospects for recovery (Hutchings and Reynolds, 2004). In the northeastern Pacific, recent assessments indicate that the biomass of at least seven species of rockfishes (Sebastes spp.) are at or below 25% of that estimated in the 1970s, and one of these species, bocaccio (S. paucispinis), has fallen in biomass by about 98% from its 1969 level (Love et al., 2002). Interestingly, the decline of northeastern Pacific rockfish species is coupled to the change in PDO, which clearly affected recruitment of cool-water species. This lack of adequate recruitment without compensatory reductions in fishing effort is overexploitation because of poor management and the lack of adequate fishery data. Worldwide, more than 80 fish stocks have recently been recognized as at risk of extinction (Musick et al., 2000). Although reduction in fishing pressure is clearly necessary, persistence and recovery also are influenced by life history features, habitat alteration, changes in food webs, genetic responses to exploitation, and declines in population growth as a result of the Allee effect (Hutchings and Reynolds, 2004). These authors emphasize that effective recovery strategies require greater understanding of how fish behavior, habitat, ecology, and evolution impact population growth at low abundance. A case in point is a recent study of the Atlantic cod (Gadus morhua), which shows that, up until the population collapse and fishing moratorium on this

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species in eastern Canada, the species gradually shifted toward maturation at earlier ages and smaller sizes, suggesting predictable fishery-induced evolution of maturation patterns (Olsen et al., 2004). The existence of multiple factors compounding the effects of overexploitation seem particularly relevant for the species of Pacific salmon (not included in the Hutchings and Reynolds survey), which use marine, estuarine, and freshwater habitats in their life history and therefore are imperiled by habitat alterations in each of these systems (see chapter 5). In summary, all of these recent revelations indicate strongly that fisheries management needs to be spatially explicit (e.g., to protect spawning aggregations) and to regulate according to fishing effort (Sala et al., 2004). No-take zones and networks of marine reserves are seen as necessary parts of management strategies (Murray et al., 1999; Sala et al., 2002), as are the rebuilding and restoring of depleted marine ecosystems (Pitcher, 2001).

Global Warming Evidence for global warming over the last 100 years is widespread, including melting of glaciers, elevated sea level, earlier onset of growing seasons, and distributional shifts in both terrestrial and marine organisms (e.g., Walther et al., 2002; Root et al., 2003). Uncertainty still exists on the amount of human contribution to this warming trend although anthropogenic factors appear to have become increasingly important compared to natural forcings in recent decades (Stott et al., 2000). The climate models for the next century predict accelerated warming within a range of scenarios (fig. 25-10). Overall warming in the twentieth century was about 0.6o C, a rate

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much faster than the average warming at the end of the last glaciation (Pittock, 2002). In contrast, projections made by the Intergovernmental Panel on Climate Change for surface warming by the end of the present century (2100) range from 1.4 to 5.8o C, or about 2–10x that of the last century (Pittock, 2002; fig. 25-10). Warming in the Pacific Northwest during the 20th century has been estimated at 0.7–0.9o C, higher than the global average, and with the highest warming rates occurring in the maritime zone of the region (Mote, 2003). Global warming casts a shadow of uncertain magnitude over the shorter-term and more regional ENSO and PDO conditions. Clearly, ENSO events and PDO regimes affect the distribution and abundance of fish populations, and they may act in conflict or in consort with each other. Nevertheless, the global warming occurring at the present time and predicted to increase over the next century promises to be the most important influence on the California marine fish fauna in the future. Overexploitation and various types of habitat alteration including nitrogen loading, sediment accumulation, and heavy metal contamination seem tractable and manageable on a regional basis given appropriate application of scientific information and sufficient public pressure and political will. In California, legislation to curtail overfishing and to establish marine reserves are tangible efforts that have begun to be implemented. Global warming, on the other hand, is so pervasive, so difficult to predict on a region by region basis, and still often ignored or suppressed, that it must be regarded as the major environmental problem for the future. Combined with continued overexploitation and habitat deterioration, worldwide warming presents a crisis-level threat to the coastal zone and marine environment in general.

Predictions A prognosis for the California fish fauna over the next century almost certainly needs to include marked changes in the species composition and dominance of fish communities in most coastal habitats. Continued warming of California waters will be accompanied by a shift of warm- and cool-temperate fish species northward with replacement by tropical and warm temperate species depending upon the particular degree of latitude. The ability of organisms to survive in a changing thermal environment depends upon their ability to extract sufficient oxygen from the reduced oxygen levels of heated waters and to effect growth and reproduction using thermally sensitive metabolic pathways (Fields et al., 1993). The rockfish (Sebastes spp.) fishery in southern California can be expected to fail (if it, in fact, recovers from its current low ebb) because of the inability of rockfish larval stages to survive in warm surface waters. Surfperches (Embiotocidae) also will be restricted to more northerly sites, probably only northward of Point Conception, while families with tropical affinities such as Labridae, Pomacentridae, Kyphosidae, Haemulidae, perhaps Serranidae, and some species of Sciaenidae will dominate the expanded warm-temperate zone in coastal waters. Of interest here is the notion first offered by Hobson (1994) that relates the success of rockfishes and surfperches north of Point Conception to their development of viviparity as a successful adaptation to offshore larval dispersal in areas of intense upwelling. Assuming that climate change will not affect the level of upwelling, then Point Conception may limit the northward expansion of species in the Southern California Bight even if conditions warm. Transitional mesopelagic

communities will be diminished or become dominated by eastern tropical Pacific species. Benthic species on the continental slope also may collapse as a community because of low survival of their larvae in the warmer surface layers. Pacific sardines may increase in abundance throughout California waters while northern anchovies retreat northward even during a cool regime. Tropical and subtropical pelagic species may flourish in the warmer waters, especially in the Southern California Bight, and also occur with increasing abundance in more northerly waters. Anadromous salmonids are likely to disappear from waters south of Point Conception or even San Francisco Bay. Persistent warm periods, as in a warm-regime PDO, appear to diminish salmon abundance in the Pacific Northwest (Mote et al., 2004), an effect that will likely extend into California and that could be exacerbated by long-term global warming. In summary, the Southern California Bight looks to become primarily a marginal Panamic and Mexican fauna of conspicuous warm-water affinities with the marine regions of central and northern California increasingly warm-temperate in character. The disjunct temperate populations of the northern Gulf of California, although tolerant of wide temperature fluctuations, may become ecologically extinct or entirely extinct as separate taxa and replaced by more southerly Gulf elements. Some cause for optimism emerges with regard to overexploitation and habitat deterioration in California marine waters given that these mounting problems have been met somewhat by deeper understanding, fresh approaches, and new techniques aimed at solving or ameliorating the developing crises. If equal or greater attention and ingenuity can be applied to climate change issues, the threats posed by global warming perhaps can be anticipated and managed. In this regard, long-term monitoring of marine fish populations certainly needs to be continued and expanded, and comparative and experimental studies initiated to predict and meet the looming challenges.

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Able, K. W., 139 Abudefduf troschelli (Panamic sergeant major), 92f, 235t, 237f, 241f abundance/richness, 5, 9, 81, 547–48; habitat and, 109–12; in kelp bed/rocky reef, 228–32; patterns of, 6–8, 626f, 630; in rocky intertidal zone, 215, 217, 221 abyssal grenadier (Coryphaenoides armatus variabilis), 353t, 369, 372f, 374–76 Acanthochromis polyacanthus, 503 Acanthocybium solandri (wahoo), 333, 337t Acanthogobius flavimanus (yellowfin goby), 95f, 533t, 612t, 613–14, 618; in bays and estuaries, 126t, 130t, 131, 132f, 142f acanthopterygians, 55, 57, 63, 73–74 Acanthurus spp. (surgeonfishes), 329, 523t Achiridae (American soles), 175, 179t, 180t Acipenser spp. (sturgeon), 125, 587, 602; A. medirostris (green sturgeon), 18t, 125, 126t, 128f, 130t; A. transmontanus (white sturgeon), 18t, 125, 126t, 128f, 518t acoustico-lateralis system, 343 acoustic signals, in courtship, 493 acoustic telemetry, 527–30, 539 actinopterygian fishes, 56–57, 63, 172 activity patterns, 543–49; biological clocks and, 548–49; dawn and dusk changeover and, 548; day-night differences in, 547–48; diel, 188, 507, 544, 545f; egestion and excretion, 546; nocturnal, 545–46. See also under feeding; movement Adams, P. B., 421 Adey, W. H., 5–6 Agonidae (poachers), 9f, 10f, 70, 189, 263t, 505; A. acipenserinus, 17t, 21t; on continental shelf, 175, 178t, 180t; reproduction and, 499 Agonomalus mozinoi (kelp poacher), 70 Agonopsis sterletus (southern spearnose poacher), 19t, 24t, 178t, 183f, 196f Agonopsis vulsa, 17t, 21t Ahlstrom, Elbert A., 269, 305 albacore (Thunnus alalunga), 18t, 23t, 89f, 389, 401f; fisheries and, 573–74, 575, 584; in pelagic zone, 326f, 327f, 330, 336t, 337t; seasonal movement of, 536t, 542 Albatrossia pectoralis. See Coryphaenoides pectoralis Albula vulpes (bonefish), 20, 135t, 145t, 518t, 532t

Alcichthys alcicornis (elkhorn sculpin), 499, 501–2 Alepisaurus ferox (longnose lancetfish), 327f, 330, 519t Alepocephalidae (slickheads), 106t, 349t, 353t, 354; A. bairdii, 519t; A. tenebrosus (California slickhead), 20t, 21t, 101f, 353t Aleutian Province, 3, 4f Alevizon, W. S., 457 algae, 5, 74, 218–19, 220, 329, 422; Gelidium robustum, 457, 459–60; Gracillaria spp., 111, 159; herbivores and, 394, 403, 404; Pterygophora californica, 228, 246, 437–38, 474; Sargassum spp., 228, 324, 419, 430, 436f alien species, 611–19; in bays and estuaries, 130–31, 142f; Japanese gobies, 130t, 131, 134, 142f, 614, 618–19; overview of, 611–12; rainwater killifish, 130, 131, 134f, 612t, 614; yellowfin goby, 95f, 126t, 130t, 131, 132f, 142f, 612t, 613–14, 618. See also American shad; Morone saxitalis (striped bass); specific aliens Allen, Larry G., 5, 9, 75, 81, 109, 506, 540, 541; bay and estuary study, 6, 10, 122, 135, 137–38, 140, 143; on harbors, 158, 159, 163; on pollutants, 601; on surf zone, 151, 153, 154; on trophic relations, 398, 403 Allen, M. J., 174, 186, 187, 188, 189, 193, 197 Alloclinus holderi (island kelpfish), 19t, 24t, 92f, 162t, 236t, 477, 534t; cleaner behavior of, 555, 556f, 557t Allocyttus folletti, 17t, 21t Allocyttus verrucosus, 520t Allosmerus elongatus, 17t Allothunnus fallai, 20t, 24t almaco jack (Seriola rivoliana), 20t, 25t, 62 Almany, G. R., 435, 437, 443, 444, 445 Alopias superciliosus, 17t, 21t, 518t Alopias vulpinus (thresher shark), 19t, 233t, 542; bigeye thresher, 89f, 326f, 337t; and commercial fishing, 579, 591 Alosa sapidissima. See American shad Altrichthys spp., 503 Ambrose, R. F., 135 ambushers, 59–62, 68, 190, 395 American eel (Anguilla rostrata), 612t, 618 American Indians, 624, 627

American shad (Alosa sapidissima), 88, 157t, 587; as alien species, 130–31, 612t, 613f, 615; in bays and estuaries, 93f, 126t, 128f, 130t Ammodytes hexapterus (Pacific sand lance), 17t, 75, 153t, 296f, 494–95, 522t amphibious fishes, 208, 209, 213 Amphiprioninae, 503, 522t Amphisticus spp. (surfperch): A. argenteus (barred surfperch), 18t, 150t, 151f, 154f, 155t, 160t; A. koelzi (calico surfperch), 19t, 97f, 150t, 151, 152f, 153t, 585t; A. rhodoterus, 17t. See also Embiotocidae anadromous fishes, 27, 88; alien, 615–16; in bays and estuaries, 124, 125, 128f; phyogeography and, 29–32. See also Oncorhynchus spp. Anaheim Bay, 135 Anarhichthys ocellatus (wolf-eel), 17t, 75, 75f, 91f, 255; in kelp bed/rocky reef, 236t, 240t; reproduction and, 485, 497, 498, 522t Anchoa spp. (anchovies), 519t, 570, 573–74, 574, 579; commercial fishing of, 569, 576, 578–79; larval stage, 304f. See also Engraulis mordax Anchoa compressa (deepbody anchovy), 18t, 95f, 160t, 173; in bays and estuaries, 126t, 134f, 136t, 138t, 145t; in surf zone, 150t, 151, 154, 159f; trophic relations and, 396f, 401 Anchoa delicatissima (slough anchovy), 19t, 396f, 401–2; in bays and estuaries, 93f, 126t, 134f, 138t, 145t anchovy and sardine regimes, 15, 281–82, 283–84f, 289; climate change and, 624, 625f, 633; competition and, 450; PDO and, 629–30, 629f, 630f, 631; trophic relations and, 403, 405 Andersen’s lanternfish (Diaphus anderseni), 351t Anderson, Todd W., 229, 421, 542; predation studies of, 436, 438–41, 442, 444 Andrews, A. H., 373 anemones (Actrinidae), 220, 560–61, 606 angel shark (Squatina californica), 19t, 95f, 184, 233t, 390, 518t; commercial fishing and, 579, 591; movement of, 538t, 540; in surf zone, 153, 156f, 157t, 158t; and telemetry, 527

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anglerfish (ceratoids), 324, 358, 406, 487, 520t, 558f. See also dreamers (Oneirodes) Anguillidae (freshwater eels), 329, 348, 349t; A. anguilla (European eel), 307; A. rostrata (American eel), 612t, 618 Anisotremus davidsonii (sargo), 19t, 66, 67f, 74, 89, 94f, 136t, 534t; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 235t, 239f, 241f; phylogenetic relations and, 43, 44f, 45t, 46t Anisotremus interruptus (burrito grunt), 235t Anomalopidae (flashlight fishes), 66, 370f, 520t, 558f. See also California flashlight fish Anomalops katoptron (anomalopid), 558 Anoplarchus insignis (slender cockscomb), 17t, 21t, 235t Anoplarchus purpurescens (high cockscomb), 17t, 35t, 90f, 498, 522t; in rocky intertidal zone, 209t, 210, 213, 215, 216f, 220; trophic relations and, 399f, 403 Anoplogaster cornuta (fangtooth), 311f, 402f, 520t; as bathypelic fish, 348, 352t, 358, 366t Anoplopoma fimbria (sablefish), 18t, 101f, 106t, 306, 521t, 532t; in bathypelagic zone, 353t, 369, 372f; commercial fisheries and, 574, 575, 578, 580; on continental shelf, 172, 178f, 185f, 187; foraging guild, 192f, 197f; pollution and, 598 Anoplopomatidae (sablefishes), 106t, 175, 180t Anotopterus pharao (daggertooth), 327f, 330, 519t Antennarius spp., 20t, 24t, 520t Antimora microlepsis (Pacific flatnose), 18t, 21t, 353t, 372f Antimora rostrata, 519t Apadocreedia vanderholsti, 522t Apodichthys flavidus (penpoint gunnel), 17t, 90f, 111f, 129f, 151, 153t, 485; in rocky intertidal zone, 209t, 215t, 216f, 221 Apogonidae (cardinalfishes), 66, 234t, 506, 547, 548; A. guadalupensis (Guadalupe cardinalfish), 19t, 24t, 234t, 485; A. lineatus (mouth-brooding cardinalfish), 502, 521t; A. pacificus (pink cardinalfish), 7t, 20t, 25t, 234t Apristurus brunneus (brown cat shark), 18t, 21t, 101f, 177t, 184, 185f, 197f Apristurus kampae (longnose cat shark), 353t, 372f Argentina sialis (Pacific argentine), 19t, 22t, 100f, 177t, 182f, 195f, 519t Argentinidae (argentines), 106t, 180t, 354 Argyropelecus spp. (hatchetfish), 306, 350t, 354, 356f, 367; A. affinis (slender hatchetfish), 350t, 354, 356f, 359, 366t; A. hemigymmus (spurred hatchetfish), 350t, 361; A. lychnus (tropical hatchetfish), 350t, 356f, 359, 366t; A. sladeni (lowcrest hatchetfish), 350t, 354, 356f, 366t Aristostomias scintillans (shining loosejaw), 350t, 356, 357f Arius graeffei, 519t Arius planiceps (ariid catfish), 485 Armor, C., 123 Arnoglossus japonicus, 308f arrow goby (Clevelandia ios), 11, 19t, 34t, 159, 161t, 523t, 533t, 600; in bays and estuaries, 93f, 126t, 128f, 129f, 132f, 134f, 136t, 138t, 143f, 145t; larval stages of, 294, 298, 303, 304f; symbiosis and, 559, 559f; trophic relations of, 396f, 401 arrowtooth flounder (Atheresthes stomias), 17t, 179t, 185f, 197f

638

INDEX

Artedius spp. (sculpins), 295, 296f; A. corallinus (coralline sculpin), 18t, 22t, 91f, 234t, 238f; A. creaseri (roughcheek sculpin), 75, 92f, 238f; A. fenestralis, 17t, 500t, 507; A. meanyi, 17t; A. notospilotus (bonehead sculpin), 18t, 153t Artedius harringtoni (scalyhead sculpin), 17t, 91f, 213, 234t, 238f; reproduction and, 498, 500t, 502 Artedius lateralis (smoothhead sculpin), 18t, 90f, 500t; feeding of, 392, 394; in rocky intertidal zone, 209t, 215t, 217f, 220f Ascelichthys rhodorus (rosylip sculpin), 17t, 91f, 209t, 499, 500t, 507 Asemichthys taylori (small-bodied sculpin), 486, 500t Assurger anzac, 20t, 24t Asterotheca infraspinata, 17t Asterotheca pentacantha, 17t, 22t Atheresthes stomias (arrowtooth flounder), 17t, 179t, 185f, 197f Atherinidae (smelt and grunions), 73, 304, 306, 321, 323, 329. See also Leuresthes tenuis/sardina (grunion) Atherinops affinis (topsmelt), 19t, 73, 73f, 88–89, 94f, 475, 532t, 622; in bays and estuaries, 127t, 128f, 129f, 134f, 138t, 143f, 145t, 398; feeding and trophic relations of, 389, 394, 396f, 404; fisheries and, 585t; habitat of, 102, 103, 105t; in kelp bed/rocky reef, 233t, 239f; larval forms of, 303, 304f; in surf zone, 150t, 151–52f, 153t, 161t Atherinopsidae (silversides), 105, 106t, 149, 233t; and commercial fisheries, 574; genetic divergence in, 621–22, 622f; in harbors, 159f, 160t; larval stage of, 289, 304; in surf zone, 150, 154, 155, 156 Atherinopsis californiensis (jacksmelt), 18t, 73, 89, 94f, 233t, 303, 585t; in bays and estuaries, 127t, 128f, 129f, 134f, 138t, 145t; genetic divergence in, 622; in surf zone, 150t, 151f, 153t, 157t, 161t Atlantic menhaden (Brevoortia tyrannus), 469, 546, 600 Atlantic-Pacific connection, 68–69 Atlantic salmon (Salmo salar), 612t, 618, 619 Atlantic wreckfish (Polyprion americanus), 497, 521t Atractoscion nobilis (white sea bass), 19t, 96f, 111f, 336t, 337t, 432, 603; commercial fishing of, 574, 579, 588; in kelp bed/rock reef, 235t, 239f, 241f; larval stages of, 274, 275f; pollutants and, 598, 603; recreational fishing of, 580, 582, 584; reproduction and, 494; in surf zone, 151, 154f, 155t, 156f, 157t, 158t Attia, P., 375 Aulostomus chinensis, 520t aurora rockfish (Sebastes aurora), 18t, 22t, 101f, 278 Autorhynchus flavidus (tubesnout), 18t, 91f, 111f, 504, 520t; in kelp bed/rocky reef, 233t, 240f, 243f Auxis rochei, 20t, 24t Auxis thazard, 20t, 24t Avise, John C., 5 Avocettina bowersii (snipe eel), 349t Avocettina infans (blackline snipe eel), 354, 355f Axoclinus carminalus, 522t ayu (Plecoglossu altivelis), 612t, 618 Azurina hirundo (swallowtail damsel), 235t bacterial endosymbionts, 558 Bagre panamensis, 20t, 24t Bailey, T. G., 359, 360t, 364, 376

Baja California, 27, 41, 43–46t; bays and estuaries in, 120, 121f, 136–37; kelp reef species, 92f, 239–40 Bajacalifornia burragei (sharpchin slickhead), 349t bald sculpin (Clinocottus recalvus), 19t, 90f, 209t, 215t, 216f, 394, 403 Balistes polylepis (finescale triggerfish), 21t, 23t, 236t, 309f, 523t; on continental shelf, 179t, 194f; reproduction and, 485 Balistidae (triggerfishes), 175, 179t, 180t, 236t balloonfish (Diodon holocanthus), 7t, 21t, 25t, 523t balloon trawl, 575, 577 Baltz, D. M., 618 banded guitarfish (Zapteryx exasperata), 20t, 135t, 137f, 233t; on continental shelf, 177f, 183f, 194, 196f bank rockfish (Sebastes rufus), 18t, 23t, 100f, 102, 105t, 262f Barathronus pacificus, 353t barcheek pipefish (Syngnathus exilis), 111f, 151f, 154f, 155t, 598 barge fishing, 580, 582–83, 583f, 588 Barham, E. G., 368 barracuda (Sphyraena argentea), 19t, 61, 96f, 236t, 293, 330, 332f, 390, 523t; abundance of, 336, 337t; and commercial fishing, 574, 575f, 587; larval stages of, 295f, 297f, 300f, 302, 311; and recreational fishing, 581, 582, 583, 584, 585t; seasonal movement of, 541–42; in surf zone, 150t, 154, 155t, 158t in harbors, 157t, 158t, 159f, 160–61t; in kelp bed/rocky reef, 239f, 241f barracuda (Sphyraena ensis), 7t, 20t, 25t, 236t barracudinas (Paralepididae), 279f, 351t; Lestidiops ringens, 277, 280, 351t, 355f, 370f barred pipefish (Syngnathus auliscus), 20t, 88, 97f, 111f, 152; in bays and estuaries, 93f, 126t, 134f, 145t barred sand bass. See Paralabrax nebulifer barred surfperch (Amphisticus argenteus), 18t, 150t, 151f, 154f, 155t, 160t barreleye (Macropinna microstoma), 349t Barry, J. P., 133 basketweave cusk-eel (Ophidion scrippsae), 96, 98f, 163, 181f, 182f; larval stages of, 277t, 280f, 293, 295f, 297f, 298; trophic relations and, 397f basking shark (Cetorhinus maximus), 19t, 326f, 336t, 390, 518t bass. See Morone saxatalis; Paralabrax spp.; Serranidae (seabasses) Bass, A. H., 491 Bassozetus spp. (cusk-eel), 360. See also cuskeels (Ophididae) Bathophilus filifer (threadfin dragonfish), 350t Bathophilus flemingi (highfin dragonfish), 351t, 357f Bathyagonus spp.: B. infraspinatus, 21t; B. nigripinnis, 17t, 21t; B. pentacanthus (bigeye poacher), 178t, 197f Bathygobius spp., 211, 493, 498 Bathylagidae (deep-sea smelts), 349t, 354, 365, 370t; B. bericoides, 310f; B. nigrigenys (blackchin blacksmelt), 349t; B. ochotensis (popeye blacksmelt), 276t, 277–78f, 365, 519t Bathylagus pacificus (Pacific blacksmelt), 310f, 349t, 354, 355f, 370f; swim bladder of, 365, 366t Bathylagus wesethi (snubnose blacksmelt), 349t, 354, 355f, 360t, 370f; larval stages of, 276t, 277f, 279f, 280, 285–86, 289f, 368; swimbladder of, 365, 366t

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Bathylychnops exilis (javelin spookfish), 349t Bathymasteridae (ronquils), 100f, 186, 238f; Rathbunella spp., 18t, 72, 72f, 235t, 522t, 532t bathypelagic zone (deep sea), 320, 321f, 342–77; benthic and benthopelagic fishes, 369–77; bioluminescence and, 342, 343, 345t, 354, 356; chemistry of buoyancy in, 365–68; ecological groupings in, 363–64; feeding in, 364–65; geographic variations, 359; geologic features, 344, 346; grenadier spp., 353t, 369, 373–77, 390; growth and reproduction, 368–69; mesopelagic fishes and, 343, 345t, 346, 348, 406; midwater fishes, 348, 354–59; physical features of, 344–48; trophic relations in, 402f, 406; vertical distribution in, 363; water types and currents, 346–48. See also bristlemouths; lampfish; specific species Bathyraja spp. (deep-sea skates): B. abyssicola, 19t, 22t, 353t, 372f; B. interrupta, 17t, 22t; B. spinosissima, 19t, 22t; B. trachura (black skate), 18t, 353t Bathysaurus mollis (highfin lizardfish), 353t, 369, 372f, 374 Batoidae (rays), 184, 539, 574. See also bat ray; Myliobatiformes; Rajidae; Torpedinidae Batrachoididae (toadfishes), 106t, 178t, 180t, 210, 532t; reproduction and, 493, 503, 504, 506. See also Porichthys spp. bat ray (Myliobatis californicus), 19t, 95f, 233t, 337t, 429, 518t, 535t; in bays and estuaries, 127t, 128f, 132f, 134f, 137f; feeding of, 394; subsistence fishing and, 568; in surf zone, 150t, 153, 156f, 157t, 158t, 160t Baumgartner, T. R., 624 Baxter, J. L., 588 bay blenny (Hypsoblennius gentilis), 19t, 95f, 111f, 236t, 455, 532t; in bays and estuaries, 126t, 134f, 136t, 137f, 145t bay goby (Lepidogobius lepidus), 18t, 98f, 155t, 158, 161t, 453t, 534; in bays and estuaries, 126t, 128f, 132f; larval stages of, 292, 294f, 298, 300, 303, 304f bay pipefish (Syngnathus leptorhyncus), 18t, 95f, 111f, 429, 475; in bays and estuaries, 126t, 128f, 129f, 132f, 134f, 136t, 137f, 145t; in surf zone, 151, 152f, 153t; trophic relations and, 396f, 402 bays and estuaries (BE), 82t, 84f, 85t, 86f, 88, 119–45; alien species in, 130–31, 618–19; analysis of, 104t; background to, 120–22; Baja California, 120, 121f, 136–37; central California, 121f, 131–33; dendograms, 8, 11f, 14f, 124f; ecological classification, 123–24; future studies, 144–45; high productivity and biomass, 138–39; interannual variability, 140–42; introduction to, 119–20; larval assemblages in, 303–5; latitudinal distribution, 122–23; northern California, 124–25, 128–31; nursery function of, 142–43, 303–5, 468; salinity in, 120, 122f, 123f; seasonality in, 139–40; southern California, 121f, 133–36; species, 93f, 95f; species diversity in, 137–38; species in jeopardy, 125, 128–30; trophic relationships in, 396–98, 400–402 Beamish, R. J., 306 bearded eelpout (Lyconema barbatum), 18t, 22t, 179t, 183f, 185f; foraging guild, 196f, 197f Beattie, A. J., 554 Beck, M. W., 119, 143, 223 Behrents, K. C., 214, 247, 435–36, 438, 441 Bellator gymnostetus (nakedbelly sea robin), 178t, 183f, 196f Bellator xenisma, 20t, 24t

Bellwood, D. R., 57 Belonidae (needlefishes), 73 belt transect sampling, 229–30, 231, 232 Bennett, W. A., 616 Benthalbella spp. (pearleyes): B. dentata (northern pearleye), 351t, 370f; B. infans, 519t; B. linguidens (longfin pearleye), 351t benthic eggs, 77 benthivores, 65, 395 benthopelagic fishes, 345t benthopelagivores, 193, 403 benttooth bristlemouth. See Cyclothone acclinidens Bernardi, Giacomo, 5 Berry, F. H., 359, 361 beryciforms, 57, 66 Beryx splendens, 520t bigeye poacher (Bathyagonus pentacanthus), 178t, 197f bigeye thresher shark, 89f, 326f, 337t bigeye trevally (Caranx sexfasciatus), 7t, 21t bigeye tuna, 89f, 326f, 337t bigfin eelpout (Lycodes cortezianus), 18t, 22t, 179t, 184, 185f, 197f bigmouth sole (Hippoglossina stomata), 19t, 23t, 98f, 236t, 398f, 535t, 606; on continental shelf, 179t, 182f, 183f; foraging guild, 192f, 195f, 196f; larval stages of, 293, 295, 302 bigscale goatfish (Pseudupeneus grandisquamis), 7t bigscale pomfret (Taractes longipinnis), 327f, 330 bigscales (Melamphaes spp.), 279f, 280, 352t, 359; M. acanthomus (slender bigscale), 352t; M. lugubris (highsnout bigscale), 277, 308f, 352t, 358f; M. parvus (little bigscale), 277, 352t; Scopelogadus mizolepsis bispinosus, 352t, 361, 365, 366t big skate (Raja binoculata), 18t, 177t, 181f, 182f, 183f, 518t; foraging guild, 194f, 195f, 196f billfishes, 335t, 429, 530. See also Makaira; swordfish (Xiphias gladius) biogeography, 3–15, 190, 622; climatic perspectives and, 4–5, 14–15; cluster analysis of bay and non-bay species, 10–11; dendrograms, 7–8, 8, 11f; distribution patterns and, 5–6; end points of species ranges, 8–9, 12f, 13f; latitude and ordination, 11–14, 243; phylogeography and, 26; regions and provinces, 3–4; species richness and, 5, 6–8 biological clocks, 548–49 bioluminescence, 342, 343, 345t, 354, 356; reproduction and, 491; symbiotic relations and, 557–58 birds, and pollutants, 602 black-and-yellow rockfish (Sebastes chrysomelas), 19t, 67f, 91f, 162t, 215t, 219t; in kelp bed/rocky reef, 234t, 237f, 240f; movement of, 531, 536t; recruitment of, 415, 420; territoriality of, 453t, 455–56f, 457f; trophic relations and, 399t, 403 blackbelly dragonfish (Stomias atriventer), 351t, 356, 357f, 366t, 370f; larval stages of, 277, 279f, 280; trophic relations of, 402f, 406 blackbelly eelpout (Lycodes pacificus), 18t, 98f, 179t, 183f, 192f, 196f, 538t black bullhead, 129f black croaker (Cheilotrema saturnum), 95f, 145t, 153, 155t, 156f, 157t black cusk-eel (Cherublemma emmelas), 177t, 197t black eelpout (Lycodes diapterus), 17t, 22t, 354t

blackeye goby (Rhinogobiops nicholsii), 19t, 60, 61f, 76, 162t, 420, 506; habitat of, 102, 105t; in kelp bed/rocky reef, 236t, 238f, 239f, 240f, 247; in mid-depth rocky reef, 99f, 255, 260f, 263t; movement and activity patterns of, 523t, 531, 534t, 545; predation study of, 431–32f, 434–37f, 438, 439–42, 460–61; reproduction and, 494, 497; territoriality of, 455 blackfinned snailfish (Careproctus cypselurus), 353t blackgill rockfish (Sebastes sp.), 101f black hagfish (Eptatretus deani), 18t, 101f, 353t, 372f blackline snipe eel (Avocettina infans), 354, 355f blacklip dragonet (Synchiropus atrilabiatus), 7t, 20t, 25t, 179t, 183f, 196f black marlin (Makaira indica), 20t, 25t, 323, 333 blackmouth eelpout (Lycodapus fierasfer), 17t, 22t, 354t black perch. See Embiotoca jacksonii black prickleback (Xiphister atropurpureus), 18t, 90f, 236t, 498, 522t; in rocky intertidal zone, 209t, 210, 211f, 215t, 216f; trophic relations and, 394, 399f, 403 blackrag (Psenes pellucidus), 328f, 330 black rockfish (Sebastes melanops), 17t, 70, 70f, 91f, 111f, 255, 475, 585t; in kelp bed/rocky reef, 237f, 240f; rocky intertidal zone, 215t, 216f, 217t, 219t; in surf zone, 151, 152f, 155t black skate (Bathyraja trachura), 18t, 353t blacksmelt. See Bathylagus spp. blacksmith. See Chromis punctipinnis blackspot wrasse (Decodon melasma), 7t, 20t, 24t black swallower (Chiasmodon niger), 344, 522t blacktail snailfish (Careproctus melanurus), 18t, 22t, 353t, 372f; on continental shelf, 178t, 184, 185f, 197f blacktip poacher (Xeneretmus latifons), 18t, 23t, 98f, 178t, 183f, 192f, 196f, 532t blackwing flyingfish, 326f bleeding wrasse (Polylepium cruentum), 179t, 183f, 196f Blenniidae (combtooth blennies), 236t, 289, 532t; reproduction and, 485, 491, 493, 502, 504. See also Hypsoblennius spp. Blepsias cirrhosus (silverspotted sculpin), 17t, 151, 152f, 153t; reproduction in, 486, 499 500t blind goby (Typhlogobius californiensis), 19t, 24t, 211, 497, 532t; symbiotic relations of, 559–60, 560f blob sculpin (Psychrolutes phrictus), 353t, 372f, 521t bluebanded goby (Lythrypnus dalli), 19t, 23t, 61f, 92f, 236t; activity patterns of, 534t, 545; in kelp bed/rocky reef, 236t, 238f, 247; phylogenetic characteristics of, 43, 44f, 45t, 46t, 49, 623; predation and, 431–32f, 434–37f, 438, 439–42, 460–61; recruitment of, 419–20, 422; reproduction and, 487; symbiotic relations of, 555, 556f, 557t bluebanded ronquil, 100f, 238f blue chromis. See Chromis punctipinnis bluefin tuna (Thunnus thynnus), 89f, 401f, 542; commercial fishing of, 573, 578; feeding behavior of, 389, 390; in pelagic zone, 326f, 330, 336t, 337t bluefish (Pomatomus saltatrix), 149, 521t bluehead wrasse (Thalassoma bifasciatum), 487, 488

INDEX

639

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blue lanternfish (Tarletonbeania crenularis), 306, 351t, 357f, 359, 368; swimbladder of, 366t, 367; trophic relations of, 402f blue marlin (Makaira nigricans), 332 blue rockfish (Sebastes mystinus), 18t, 59f, 91f, 215, 416; in deep rock habitat, 255, 260f; fishing and, 584, 585t, 590; in kelp bed/rocky reef, 234t, 237f, 240f, 242, 243f; reproduction and, 494; seasonal movement of, 537t, 542; trophic relations and, 394, 404 blue shark (Prionace glauca), 20t, 89f, 326f, 330, 337t, 389, 518t; movement of, 524, 532t, 540, 542, 543; telemetry and, 527–28; trophic relations and, 401f bocaccio (Sebastes paucipinnis), 18t, 59, 234t, 334f, 484f, 632; commercial fishing of, 575, 589, 590; in deep rock habitat, 256, 260f, 261f, 263t; epibenthic, 539; habitat for, 100f, 103; larval stages of, 276t, 309f; movement of, 528, 537t, 541; recreational fishing and, 584, 585t; young-ofyear (YOY), 111f, 261, 262f Bodianus diplotaenia (Mexican hogfish), 235t Bodkin, J. L., 241, 244, 246 Boehlert, George W., 270, 305 Bone, Q., 368 bonefish (Albula vulpes), 20, 135t, 145t, 518t, 532t bonehead sculpin (Artedius notospilotus), 18t, 153t bonito (Sarda chiliensis), 20t, 87, 89f, 236t, 585t; in coastal pelagic zone, 154, 157t, 158t, 159f, 160t; commercial fisheries and, 574, 575; feeding of, 406; in pelagic zone, 330, 332f, 336t, 337t; pollution and, 600, 601; recreational fishing and, 581, 583, 584; reproduction and, 494; seasonal movement of, 541–42; trophic relations and, 401f Booth, F. E., 571 boreal region, 330 Borostomias panamensis (Panama snaggletooth), 351t, 357f, 366t Bothidae (lefteye flounders), 176, 180t, 329. See also Paralichthyidae Bothragonus swanii (rockhead), 17t, 70 Bothrocara brunneum (two-line eelpout), 18t, 22t, 354t, 372f Bothrocara molle, 18t, 22t bottlelight (Danaphos oculatus), 350t, 359, 366t, 370f Bowen, B. W., 624 Boyle, K. S., 403 Brachyistius frenatus (kelp perch), 19t, 71f, 75, 111f, 162t, 422, 477, 494; in kelp bed/rocky reef, 92f, 235, 239f, 240f; movement and activity patterns of, 533t, 544, 556f, 557t; predation and, 431f, 438–39, 440f, 442f; trophic relations and, 395, 400f, 404 Bradbury, J. W., 488 Brama japonica, 20t, 22t, 521t Brantley, R. K., 491 Bray, Richard N., 433, 524 breeding, 531. See also reproduction Bregmaceros atlanticus, 519t Breitberg, D. L., 455 Brevoortia tyrannus (Atlantic menhaden), 469, 546, 600 Brewer, G. D., 305, 362 Briggs, J. C., 174 bristlemouths (Gonostomatidae), 290, 350t, 354, 359, 365, 370f. See also Cyclothone spp. brittlestar (Ophiopthalmus normani), 371, 540

640

INDEX

broadfin lanpfish (Nannobrachium ritteri), 351t, 356, 357f, 359, 368, 370f; larval stages of, 276t, 277f, 279, 280, 305; swimbladder of, 366t, 367; trophic relations of, 402f bronzespotted rockfish (Sebastes gilli), 18t, 24t, 258t bronzestripe grunt (Orthopristis reddingi), 178t, 181f, 182f, 194f, 195f Brooks, A. J., 249–50 broomtail grouper (Mycteroperca xenarcha), 20t, 23t, 58, 234t Brosmophycis marginata (red brotula), 18t, 186, 233t, 238f, 519t brotulas. See Bythitidae (brotulas) Brown, D. W., 359, 360t Brown, James H., 5, 621 brown algae (Pterygophora californica), 228, 246 brown cat shark (Apristurus brunneus), 18t, 21t, 101f, 177t, 184, 185f, 197f brown Irish lord (Hemilepidotus spinosus), 17t, 91f, 234t, 238f, 296f brown rockfish (Sebastes auriculatus), 19t, 22t, 111f, 255, 270; in kelp bed/rocky reef, 92f, 234t, 240f; movement of, 536t, 542; in surf zone, 152, 155t brown smoothhound (Mustelus henlei), 19t, 95f, 127t, 128f, 233t; in surf zone, 153, 156f, 157t, 158t brownsnout spookfish (Dolichopteryx longipes), 349t brown trout (Salmo trutta), 612t, 616 buffalo sculpin (Enophrys bison), 17t, 234t, 485, 486, 500 bulbous dreamer (Oneirodes eschrichtii), 352t bullet mackerel, 337t bull sculpin (Enophrys taurus), 17t bullseye puffer (Sphoeroides annulatus), 20t, 25t, 95f, 96, 137f, 236t, 237f, 241f buoyancy and swim bladders, 365–68 Bureau of Commercial Fisheries (BCF), 269 Burge, R. T., 245 Busby, P. J., 31 butterflyfishes (Chaetodontidae), 63–64, 235t, 394, 506, 522t; Chaetondon humeralis, 20t, 24t, 235t; Prognathodes falcifer, 20t, 24t, 220, 235t butterfly ray (Gymnura marmorata), 20t, 135t, 518t butter sole (Isopsetta isolepis), 17t, 174, 179t, 181f, 194f, 296f Bythitidae (brotulas), 185f, 186, 484, 504; red brotula (Brosmophycis marginata), 18t, 186, 233t, 238f, 519t cabezon. See Scorpaenichthys marmoratus Cabrillo Beach, 161f, 162, 164f Caelorinchus scaphopsis (shoulderspot), 369 Caillet, G. M., 154, 364, 371 Calamus brachysomus (Pacific porgy), 20, 24t, 137f, 235t, 521t CalCOFI. See California Cooperative Oceanic Fisheries Investigations (CalCOFI) calico rockfish (Sebastes dallii), 19t, 98f, 187, 234t, 398f, 416; movement of, 536t, 542 calico surfperch (Amphisticus koelzi), 19t, 97f, 585t; in surf zone, 150t, 151, 152f, 153t California barracuda. See barracuda (Sphyraena argentea) California butterfly ray (Gymnura marmorata), 20t, 135t, 518t California Channel Islands, 33, 36, 46–49, 228, 240, 603, 624 California clingfish (Gobiesox rhessodon), 19t, 90f, 212–13, 215t, 216f, 238f, 403 California Cooperative Oceanic Fisheries Investigations (CalCOFI), 269–70, 271,

275–302, 313, 361, 362, 368–69, 628. See also ichthyoplankton assemblages California corbina. See corbina California Counter Current, 47, 347 California Current, 47, 320, 329, 347, 368, 629; pelagic fishes and, 333–36; phylogeography and, 38, 40, 41 California Current region, ichthyoplankton studies in, 269, 270, 280, 283, 287–88, 306. See also ichthyoplankton assemblages California Department of Fish and Game (CDFG), 168, 169, 269, 587, 588, 617; and recreational fishing, 580, 583, 590, 591; and sardine industry, 571, 572, 573 California Fish and Game (journal), 587 California flashlight fish (Protomyctophum crockeri), 351t, 357f, 359, 370f; larval stages of, 276t, 277f, 279f, 280, 306, 368; swimbladder of, 366t, 367 California grenadier. See Nezumia stelgidolepsis California grunion (Leuresthes tenuis), 95f, 145t, 161t; in surf zone, 150t, 151f California halfbeak (Hyporhampus rosea), 19t, 73, 88, 93f, 135t, 136t, 328 California halibut. See Paralichthys californicus California headlightfish (Diaphus theta), 305, 351t, 356, 357f, 359, 360t, 363, 366t; trophic relations of, 402f California killifish (Fundulus parvipinnis), 10–11, 19t, 34t, 41, 42f, 88, 533t; abundance of, 142, 143f, 145t; in bays and estuaries, 93f, 120, 126t, 129f, 132f, 134f, 137f, 138; pollution and, 601; trophic relations and, 396f, 401 California lanternfish (Symbolophorus californiensis), 351t, 357f, 358, 359, 402f; larval stages of, 276t, 277f, 279f, 280, 282f; swimbladder of, 366t, 367 California lizardfish (Synodus lucioceps), 18t, 98f, 155t, 538t; on continental shelf, 173, 177, 181f, 182f, 183f; foraging guilds, 192f, 194f, 195f, 196f; larval stages of, 277, 293, 295f, 301, 302f; trophic relations and, 395, 397f, 398f California moray (Gymnothorax mordax), 19t, 24t, 95f, 545, 555, 558f; activity patterns of, 545, 549; in harbors, 157t, 158t; in kelp bed/rocky reef, 233t, 238f, 239f, 241f, 243f California needlefish (Strongylura exilis), 73, 135t California rattail, 101f, 372f California roach, 128f, 129f California sardine. See Sardinops sagax California sheephead. See Semicossyphus pulcher California skate (Raja inornata), 18t, 98f, 177t, 181f, 182f, 183f; foraging guild, 194f, 195f, 196f California slickhead (Alepocephalus tenebrosus), 20t, 21t, 101f, 353t California smoothtongue: See Leuroglossus stilbius California subregion, 27 California tonguefish. See Symphurus atriacauda California Transition Zone, 5 Callionymidae (dragonets), 176, 180t. See also blacklip dragonet camouflage. See cryptic species canary rockfish (Sebastes pinniger), 18t, 99f, 255, 260f, 263t; fisheries and, 585t, 589, 591 canneries, 569, 570–74, 579 cannibalism, 436, 500–502 Cannon, Ray, 590 Canthigaster spp. (pufferfish), 503, 523t

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canyon species, 100f Caracanthus spp., 520t Carangidae (jacks), 9f, 10f, 62, 77, 106, 150, 329, 393; C. caballus, 20t, 23t; C. caninus (Pacific crevalle jack), 7t, 20t, 25t; C. sexfasciatus (bigeye trevally), 7t, 21t; C. vinctus (cocinero), 7t, 20t Carapus spp., 308f, 519t Carcharhinidae (sharks), 9f, 10f; C. brachyurus, 20t; C. leucas, 20t, 24t; C. longimanus (whitetip shark), 19t, 25t, 328f, 331; C. obscurus, 19t, 24t; C. remotus, 24t. See also Scyliorhinidae (cat sharks); Squalidae (dogfish sharks); Triakis (hound sharks) Carcharodon carcharias (white shark), 20t, 22t, 89f, 337t, 390; movement of, 530, 534t, 542; pollution and, 601 carcinogens. See DDT and PCB contamination cardinalfishes (Apogonidae), 66, 234t, 506, 547, 548. See also Apogon spp. Careproctus spp. (snailfishes), 353t, 486, 521t. See also Liparis spp. Careproctus melanurus (blacktail snailfish), 18, 22t, 353t, 372f; on continental shelf, 178t, 184, 185f, 197f Carey, F. G., 543 Caristius macropus, 521t Carlisle, J. G., Jr., 150 Carlton, J. T., 612 carnivores, 394. See also piscivorous fish Carpelan, L. H., 473 Carr, M. H., 248, 419, 436, 441, 445 Carroll, R. L., 57 Cartamil, D. P., 540 Case, J. F., 358 Cass-Calay, S. L., 305 catadromous fishes, 124, 126t, 134f Cataetyx rubrirostris (rubynose brotula), 186 catch data, 525, 585t catch per unit effort (CRUE), 229, 371 cat sharks. See Apristurus spp.; Scyliorhinidae (cat sharks) Caulolatilus princeps (ocean whitefish), 20t, 22t, 35t, 87, 311f, 521t; in kelp bed/rocky reef, 92f, 234t, 237f, 239f; and recreational fishing, 586 Caulophryne spp., 309f, 520t Cebidichthys violaceus (monkeyface prickleback), 18t, 75, 90f, 235t, 558; feeding and trophic relations, 389, 394, 399f, 403; movement and activity of, 527, 530, 538t, 543; in rocky intertidal zone, 207, 209t, 211, 212, 215t, 216f, 219, 220f Cech, J. J., 123 Cenozoic influences, 58, 68–70, 621 Centrarchidae (sunfishes), 393. See also Mola mola (ocean sunfish) Centro Interdisciplinario de Ciencias Marinas (CICIMAR), 270 Centropomis undecimalis, 521t Centropyge spp., 522t Centroscyllium nigrum (combtooth dogfish), 353t Centrostephanus coronatus (sea urchin), 441. See also sea urchins Cephalopholis boenak, 497 Cephaloscyllium ventriosum (swell shark), 21t, 23t, 95f, 153, 156f, 157t, 158t; activity patterns of, 536t, 544, 549; in kelp bed/rocky reef, 233t, 239f Cepola rubenscens, 522t ceratioids (angler fish), 324, 358, 406, 487, 520t, 558f Ceratoscopelus townsendi (dogtooth lampfish), 351t, 358, 366t, 369; larval stages of, 276t, 277f, 279, 280, 305

Ceratoscopelus warmingii (lampfish), 280 Cetengraulis mysticetus, 20t, 24t Cetomimus sp, 520t Cetorhinus maximus (basking shark), 19t, 326f, 330, 336t, 518t Chaenopsidae (pikeblennies), 236t, 289; Chaenopsis alepidota (orangethroat pikeblenny), 19t, 24t, 43, 44f, 45t, 46t, 137f. See also Neoclinus spp. Chaetodipterus zonatus, 20t, 25t, 523t Chaetodontidae (butterflyfishes), 63–64, 235t, 394, 506, 522t; C. humeralis (threebanded butterflyfish), 20t, 24t, 235t; Prognathodes falcifer, 20t, 24t, 220, 235t chameleon goby (Tridentiger trigonocephalus), 612–13, 612t chameleon rockfish (Sebastes phillipsi), 17t, 23t, 258t chameleon wrasse (Halichoeres dispilus), 92f, 235t, 237f, 241f Channel Islands. See California Channel Islands Channel Islands clingfish (Rimicola cabrilloi), 7t, 17t, 24t Chanos chanos (milk fish), 519t, 612t, 618 Chauliodus macouni (Pacific viperfish), 351t, 356, 357f, 365, 366t, 370f, 519t; trophic relations and, 395, 402f, 406 Chavez, F. P., 5, 15, 629, 631 cheekspot goby (Ilypnus gilberti), 95f, 154f, 155t, 159, 161t, 534; in bays and estuaries, 126t, 134f, 136t, 137f, 145t, 303; trophic relations and, 396f, 401 Cheilodactylus spectabilis, 522t Cheilopogon spp. (flyingfish), 323, 328, 331, 405; C. heterurus, 20t, 25t, 520t; C. pinnatibarbatus (California flyingfish), 19t, 22t, 405 Cheilotrema saturnum (black croaker), 19t, 95f, 145t, 153, 535t; in kelp bed/rocky reef, 235t, 239f Cherublemma emmelas (black cusk-eel), 177t, 197f Chess, J. R., 75, 188, 546 Chess, Tony, 55 Chiasmodon niger (black swallower), 344, 522t Chilara taylori (spotted cusk-eel), 19t, 98f, 163, 176, 177t, 398f; on continental shelf, 182f, 183f, 185f; foraging guild, 192f, 194f, 195f, 196f, 197f; movement patterns of, 535t, 546 Childress, J. J., 406 chilipepper (Sebastes goodei), 19t, 100f, 172, 262f; fisheries and, 575, 585t, 590 Chiloconger dentatus (thicklip conger), 177t, 183f, 195f, 196f Chilomycterus reticulatus, 20t, 24t Chimaeridae (chimaeras), 106t; on continental shelf, 175, 177t, 180t china rockfish (Sebastes nebulosus), 17t, 76, 76f, 234t, 240t chinook salmon (Oncorhynchus tshawytscha), 17t, 153t, 233t, 330, 331f, 630; in bays and estuaries, 93f, 126t, 128f, 130t, 131; fisheries and, 569, 579, 585t, 589, 628; phylogeography and, 30t, 31–32, 32t, 39 Chirolophus decoratus (decorated warbonnet), 7t, 17t, 236t Chirolophus nugator (mosshead warbonnet), 17t, 236t Chitonotus pugetensis (roughback sculpin), 19t, 22t, 98f, 398f, 532t; on continental shelf, 176, 178t, 182f, 189; foraging guild, 192f, 195f Chlamydoselachus anguineus, 17t, 21t, 518t Chloroscrombrus orqueta, 20t, 24t

Choat, J. H., 57 Chotkowski, M. A., 221 Chromis alta (silverstripe chromis), 235t Chromis atrilobata (scissortail chromis), 92, 235t, 241f Chromis punctipinnis (blacksmith), 19t, 35t, 74, 87, 92f, 157t, 416; cleaner behavior of, 556f, 557f; feeding of, 63f, 390; in harbors, 157t, 159, 162t; in kelp bed/rocky reef, 235t, 237f, 239f, 241f, 242, 243f; larval stages of, 293, 295f, 301, 302; movement and activity patterns of, 535t, 542, 544, 546, 548; trophic relations and, 400f chub mackerel. See Scomber japonicus chum salmon (Oncohynchus keta), 17t, 21t, 130t, 233t Cichlidae (cichlids), 72, 497. See also Tilapia spp. (cichlids) cigarfish (Cubiceps spp.), 333, 523t, 559 cigar shark (Isistius braziliensis), 561, 561f circadian rhythms, 548–49 Cirrhitichthys aureus, 522t Cirriformia luxuriosa (polychaete worm), 220 Citharichthys spp. (sanddabs), 193, 294, 305, 606–7; C. fragilis (gulf sanddab), 7t, 20t, 277f, 278f, 280; C. gordae (mimic sanddab), 179t, 183f, 193, 196f; DDT concentrations in, 601, 602f, 603; larval stages of, 276t, 280, 291, 297 Citharichthys sordidus (Pacific sanddab), 98f, 157t, 299, 403, 535t; on continental shelf, 172, 173, 179t, 182f, 258; diel movement of, 543; foraging guild, 192f, 195f; larval stages of, 19t, 98f, 157t, 276t; pollution and, 600, 601, 602f, 605, 606; recreational fishing and, 583, 585t; trophic relations and, 398f, 403 Citharichthys stigmaeus (speckled sanddab), 19t, 60, 61f, 236t, 258, 631; in bays and estuaries, 127t, 128f, 132f; on continental shelf, 96, 97f, 103, 176, 179t, 181f; foraging guilds, 192f, 194f; in harbors, 158, 161t; larval stages of, 276t, 277–78f, 280, 298, 299; movement of, 535t, 543; pollution and, 601, 602f, 606; in surf zone, 152f, 153t, 155t; trophic relations and, 397f, 403 Citharichthys xanthostigma (longfin sanddab), 19t, 23t, 98f, 398f, 535t; on continental shelf, 179t, 181f, 182f, 183f; foraging guild, 193, 194f, 195f, 196f; larval stages of, 276, 277–78f, 280; pollutant concentrations in, 600, 601, 602f Clark, Frances, 572, 588 Clarke, G. L., 365 Clarke, T. A., 227, 453 cleaning symbiosis, 555–57, 556f, 557t Clevelandia ios (arrow goby), 11, 19t, 34t, 159, 161t, 523t, 533t, 600; in bays and estuaries, 93f, 126t, 128f, 129f, 132f, 134f, 136t, 138t, 143f, 145t; larval stages of, 294, 298, 303, 304f; symbiotic relations of, 559, 559f; trophic relations of, 396f, 401 climate change, 4–5, 14–15, 36–38, 47, 621–33; in Baja California, 41; eutrophication and, 145; global warming and, 632–33; overfishing and, 625–26; rocky intertidal zone, 205, 221–22, 630; trophic interactions and, 631–32. See also ENSO; PDO clingfish (Rimicola spp.): R. cabrilloi (Channel Islands clingfish), 7t, 17t, 24t; R. dimorpha, 18t, 24t; R. eigenmanni (slender clingfish), 19t, 25t, 92f, 111f, 236t, 238f; R. muscarum (kelp clingfish), 18t, 111f, 155t, 236t, 238f, 405. See also Gobiesox spp.

INDEX

641

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Clinidae (kelpfish), 9f, 10f, 71–72, 105, 106t, 217f, 236t, 532t; reproduction and, 491, 495 Clinocottus spp. (sculpins), 128f, 500; C. acuticeps (sharpnose sculpin), 17t, 209t, 498f, 500t, 521t; C. embryum, 18t, 420; C. recalvus (bald sculpin), 19t, 209t, 215t, 394, 500t Clinocottus analis (wooly sculpin), 35t, 90f, 399f, 403, 532t, 628; hypoxia and, 468; parental care in, 500t, 507; in rocky intertidal zone, 209t, 211, 215t, 217f, 220f Clinocottus globiceps (mosshead sculpin), 17t, 21t, 209t, 215t, 217f, 420, 500t; feeding of, 390, 392 Clupea pallasi (Pacific herring), 72, 152f, 153t, 214, 304f, 331f, 429; in bays and estuaries, 93f, 127t, 128f, 129f, 132f, 138t; commercial fishing of, 574, 576; on continental shelf, 172, 195f; feeding of, 390, 393, 394; and reproduction, 494 Clupeidae (herrings), 72, 106t, 149, 304, 570, 574; C. harengus, 17t, 303, 325; commercial fishing of, 578; and reproduction, 494, 496 coastal pelagic (CP) zone, 82t, 85t, 86f, 89f, 91, 96f, 106, 109, 154–56; analysis of, 104t coastal species, 8, 17–21t; dendrogram for, 11, 11f; phylogreographic characteristics of, 34–35t cocinero (Caranx vinctus), 7t, 20t cockscombs. See Anoplarchus spp. cod. See Gadidae (cods) codlings (Moridae), 175, 177t, 180t Cohen, A. N., 612 coho salmon (Oncorhynchus kisutch), 18t, 30t, 31, 32, 88, 330, 331f; in bays and estuaries, 126t, 128f, 130t Collisella limatula (limpet), 220 Cololabis saira (Pacific saury), 19t, 330, 405, 520t, 624 coloration: anti-predatory, 428–29; courtship and, 488, 489, 490, 493, 494. See also crypsis Colpichthys regis (false grunion), 622 Columbia River, 31 Colwell, R. K., 451 combfishes. See Zaniolepsis spp. combtooth blennies (Blenniidae), 236t, 289, 532t; reproduction and, 485, 491, 493, 502, 504 combtooth dogfish (Centroscyllium nigrum), 353t commensalism, 554, 558–61 commercial fisheries, 337t, 525, 567, 568–80, 587; (1850-1899), 568–70; (1900-1950), 570–77; (1951-2001), 577–80; balloon trawls and, 575, 577; canneries and, 570–74, 579; competition with recreational fishing, 589–92; drying/salting, 569–70; fishing techniques, 575–76; freezing and, 569, 575, 577, 579; globalization of, 578–79; landings made (1981-1999), 580t; market fisheries, 574–77; nets, 571, 575, 576, 578f, 579–80, 589, 590–91; pelagic wetfish and, 570, 573–74; purse seines, 571, 572, 573, 575, 577, 588; racism and, 586–87; reduction in, 570–74, 579; regulation of, 572, 573, 580, 586–89; sardines, 569, 570–73, 578–79, 588, 590; technology revolution in, 577–78; traditional, 579–80; trawling and, 570, 575, 577; tuna, 333f, 337t, 570–77, 579 Commercial Passenger Fishing Vehicles (CPFVs), 580–84, 583f, 584f, 588

642

INDEX

competition, 415, 449–65; in context, 461–62; definition and concept of, 449–51; density-dependent, 449, 453; direct observation of, 450, 454; disturbance and, 472, 477; exploitation, 449; interference, 429, 449; interspecific, 443, 450, 451–61; niche overlap and, 451, 452f, 456, 457, 458f; predation and, 438, 443; resource partitioning and, 450, 454; territoriality and, 450, 451, 453t, 454, 455–56 Congleton, J. I., 468 Congridae (conger eels), 175, 177t, 180t, 183f, 195f, 196f Connell, J. H., 311, 434, 442, 466 conservation, 569, 572, 587, 589; recruitment and, 422–23 continental shelf and slope, 96, 167–99; assemblages, 172–73; deep shelf assemblages, 258t; diel behavior, 188; distribution of families in, 175–76; ecological segregation, 190–95; feeding and foraging, 188–92, 192f, 194–97f; foraging guilds, 190–92; interactions with other organisms, 195–95; life zones, 174–75; mobility and migration on, 187–88; morphological attributes, 184, 186; natural history traits, 185; other regions compared, 196–98; overview of scientific studies, 168–71; physical and biological conditions, 167–68; physical changes with depth, 168; population characteristics, 171–72; sampling methods, 170–71; soft-bottom habitat, 167–68; taxonomic composition, in surveys, 172; topography, 167; trawl survey assessments, 171–73; zoogeographic provinces, 173–74. See also inner shelf (IS); outer shelf (OS) Cook, A. E., 219–20, 223, 407 copper rockfish (Sebastes caurinus), 17t, 111f, 255, 260f, 270, 585t; on continental shelf, 178t, 182f, 195f; in kelp bed/rocky reef, 92f, 234t, 240t; recruitment of, 415; seasonal movement of, 536t, 539, 542; in surf zone, 152, 155t coralline scuplin (Artedius corallinus), 18t, 22t, 91f, 234t, 238f coral reef communities, 57, 58, 63, 69, 71, 420, 437 corbina (Menticirrhus undulatus), 19t, 95f, 136t, 149, 293, 536t; commercial fishing and, 587; in harbors, 157t, 158t, 160–61t; larval stages of, 293, 295f; pollutants and, 600; in surf zone, 150t, 151 Cordilleran region, 27, 36 Cordone, A. J., 130 Coris julis, 549 cornetfish (Fistularia corneta), 7t, 14, 20t, 25t Cortez angelfish (Pomacanthus zonipectus), 235t Cortez gregory, 92f, 241f Cortez Province, 3, 4f Cortez stingray, 137f Coryphaena spp., 519t; C. hippurus (dolphinfish), 20t, 22t, 324, 332, 521t Coryphaenoides spp. (grenadiers), 353t, 369, 373–77, 530; C. acrolepis (Pacific grenadier), 18t, 22t, 353t, 369, 372f, 373, 374; C. armatus (abyssal grenadier), 353t, 369, 372f, 374–76; C. filifer (threadfin grenadier), 353t, 369; C. leptolepsis (ghostly grenadier), 353t, 369, 374, 376; C. pectoralis (giant grenadier), 101f, 353t, 369, 372f, 373–74; C. yaquinae (rough abyssal grenadier), 353t, 369, 374–77, 540 Coryphopterus (goby), 76, 494 Cosmocampus arctus (snubnose pipefish), 19t, 92f, 234t, 238f

C-O sole (Pleuronichthys coenosus), 18t, 60, 61f, 70, 236t, 535t Costa, M. J., 144 Costanso, Miguel, 568 Cottidae (sculpins), 9f, 10f, 90f, 91f, 105, 106t, 329; on continental shelf, 172, 175, 178t, 180t, 186; egg size and, 501t; in kelp bed/rocky reef, 70, 234t; larval stages of, 289, 304f; movement of, 532t–533t, 543; reproduction and, 483, 491, 493, 495, 498–99, 500, 502, 504, 507; in rocky intertidal zone, 209t, 210, 212, 215, 217f. See also Artedius spp.; Clinocottus; Oligocottus Cottus asper (prickly sculpin), 126t, 128f, 129f, 132f, 296 Cottus bairdi (mottled sculpin), 501 courtship, 487–95; acoustic signals and, 493; coloration and, 488, 489, 490, 493, 494; functions of, 488–89; spawning and, 488–89, 494 cow cod (Sebastes levis), 18t, 23t, 100f, 103, 537t, 589; in deep rock habitat, 255, 262f, 263t; larval stages of, 285, 288f Cowen, R. K., 76, 241, 417, 546 Coyer, J. A., 544 crepuscular patterns, 543, 549 crescent gunnel (Pholis laeta), 17t, 21t, 209t, 485, 522t crested bigscale (Poromitra crassiceps), 352t, 358f, 365, 366t, 370f; trophic relations of, 402f crevice kelpfish (Gibbonsia montereyensis), 18t, 90f, 111f , 215t, 216f, 238f, 399f crisscross prickleback (Plagiogrammus hopkinsii), 17t, 24t, 91f, 236t, 238f croakers. See Genyonemous spp.; Sciaenidae (croakers) Croker, R. S., 588, 590 Cross, J. N., 170, 212, 398 crustaceans, as foodsource, 361, 394, 403, 406, 606 Cryptacanthodidae, 485, 505, 522t cryptic species, 64, 91f, 92f, 106, 109f; predation and, 428–29, 432; in rocky subtidal reefs, 238f; surveys of, 231–32 Cryptopsaras couesii, 487, 520t Cryptotrema corallinum, 18t, 24t Crystallodystes cookei, 522t Cubiceps spp. (cigar fish), 333, 523t, 559 cunner (Tautogolabrus adspersus), 419 curlfin turbot (Pleuronichthys decurrens), 18t, 98f, 398, 535t, 606; on continental shelf, 179t, 181f; foraging guild, 192f, 194f Cushing, D. H., 308–9 Cushman, J. H., 554 cusk-eels (Ophididae), 106, 177t, 180t, 197f, 353t, 369; Lepophidium spp., 177t, 182f, 183f, 195f, 196f; movement and activity of, 535t, 544. See also Chilara taylori cutlassfish (Trichiurus nitens), 20t, 25t, 327f, 332 cutthroat trout (Oncorhynchus clarkii), 17t, 21t, 29, 130t Cyaena sp. (scyphomedusa), 328f Cyclopsetta panamensis, 308f Cyclothone acclinidens (benttooth bristlemouth), 350t, 354, 356f, 360t, 362–63, 370f, 402f; larval forms of, 276, 280; swimbladder of, 365, 366t, 367 Cyclothone spp. (bristlemouths), 354, 365, 368, 370f; C. atraria, 519t; C. pallida (tan bristlemouth), 350t; C. pseudopallida (slender bristlemouth), 276, 280; C. signata (showy bristlemouth), 276t, 350t, 354, 356f, 360t, 362–63, 366t, 370f; larval stages of, 276, 277f, 279f, 280, 368

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Cyema atrum, 519t Cymatogaster aggregata (shiner perch), 18t, 71, 72f, 88–89, 94f, 475, 631; in bays and estuaries, 127t, 128f, 129f, 132f, 134f, 136t, 138t, 145t; on continental shelf, 176, 178t, 181f; distribution patterns of, 546; foraging guilds, 192f, 194f; habitat of, 102, 103, 105t, 111f; in kelp bed/rocky reef, 235t, 248; pollution and, 606; reproduction of, 494; seasonal movement by, 533t, 542; in surf zone, 150, 152f, 153t, 154f, 160–61t; trophic relations and, 396f, 397f, 402, 403 Cynoglossidae (tonguefishes), 298, 329; on continental shelf, 175, 179t, 180t, 189. See also Symbolophorus spp. Cynoscion spp. (sea trout), 150; C. parvipinnis, 19t, 24t Dactylopterus volitans, 520t Dactyloscapus spp., 522t daggertooth (Anotopterus pharao), 327f, 330, 519t Dagorn, L., 540 Dalatiidae (dwarf sharks), 329, 353t damselfish (Pomacentridae), 65, 74, 76, 106t, 506, 547; in kelp bed/rocky reef, 235t, 237f; movement of, 535t, 548; reproduction and, 488, 489, 491, 493, 495, 503. See also Chromis spp.; garibaldi (Hypsypops rubicundus) Danaphos oculatus (bottlelight), 306, 350t, 354, 356f darkblotched rockfish (Sebastes crameri), 17t, 21t, 257, 589 darkwing flyingfish (Hirundichthys rondeletii), 331f Darling, J. D. S., 220 Dascyllus spp., 503, 522t Dasyatis spp. (stingrays): D. dipterura, 20t; D. longa, 518t; D. violacea, 326f, 331, 337t data matrix, 83 Daugherty, 576 Davidson Current, 347, 361 Davis, G. E., 229 Davis, J. C., 584 Davis, J. L. D., 208, 212 Davis, M. K., 572 Dawson, Michael N., 5, 11, 14, 623 DDT and PCB contamination, 595–603, 605, 607f. See also pollution de Bary, Anton, 554 Decapterus muroadsi, 20t, 23t Decodon melasma (blackspot wrasse), 7t, 20t, 24t decorated warbonnet (Chirolophis decoratus), 7t, 17t, 236t deep bank (DBNK), 82t, 85t, 86f, 99, 104t deepbody anchovy (Anchoa compressa), 18t, 95f, 159f, 160t, 173; in bays and estuaries, 126t, 134f, 136t, 138t, 145t; in surf zone, 150t, 151, 154; trophic relations and, 396f, 401 deep reef (DRF), 82t, 84f, 100f, 104t deep rocky reef (DDRF), 85t, 86f, 253–64; anthropogenic structures, 260–64; bottom assemblage, 261, 263; midwater assemblages, 260–62; natural outcrops, 255; overview of fish assemblages, 255–59; pipelines and, 264; shell mound and, 264 deep sea. See bathopelagic zone (deep sea) deep-sea skate (Bathyraja abyssicola), 19t, 22t, 353t, 372f deep-sea sole (Embassichthys bathybius), 354t, 372f deep slope (DSLP), 85t, 86f

deepwater cornetfish (Fistularia corneta), 7t, 14, 20t, 25t deepwater eelpout (Lycodapus endemoscotus), 354t deepwater serrano (Serranus aequidens), 178t, 180t, 196f Delolepsis gigantea, 17t, 21t delta smelt (Hypomesus transpacificus), 126t, 128, 129, 130t, 131, 473, 615 DeMartini, E. E., 152, 154, 159, 507; on kelp bed/rocky reef habitat, 231, 241, 244, 245, 246; on movement patterns, 540, 541, 544 dendrograms, 7–8, 11f, 14f, 86f; of bays and estuaries, 8, 11f, 14f, 124f Denman, William, 572 Denton, E., 73 Derichythys serpentinus, 518t desiccation, resistance to, 212 Desmodena lorum, 20t, 23t Desmond, J. S., 138, 139 detritivores, 394 Diablo Canyon, 294 diadromous fishes, 124 Diamond, J., 451 diamond stingray, 137f diamond turbot (Hypsopsetta guttulata), 19t, 181f, 396f, 402, 535t, 600; in bays and estuaries, 127t, 129f, 136t, 137f; larval stages of, 291, 294f, 299 diaphanous hatchetfish (Sternoptyx diaphana), 350t, 354, 356f, 402f, 519t Diaphus spp. (headlightfish), 276t; anderseni (Andersen’s lanternfish), 351t; D. theta (California headlightfish), 305, 351t, 356, 357f, 359, 360t, 363, 366t, 402f Dicentrarchus labrax (European sea bass), 497 diel behavior, 188, 468, 507, 543–44 diet. See feeding Dill, W. A., 130 Diodon spp. (porcupinefish), 77; D. holocanthus (balloon fish), 7t, 21t, 25t, 523t; D. hystrix, 21t, 236t Diogenichthys atlanticus (longfin lanternfish), 351t, 370f; larval stages of, 276t, 277f, 279, 282f, 290f, 368 Diogenichthys laternatus (Diogenes lanternfish), 351t, 370f; larval stages of, 277, 277f, 279, 280, 287, 293f Diplectrum spp. (sand perch), 496; D. labarum (highfin sand perch), 178t, 182f, 183f, 195f, 196f; D. maximum (greater sand perch), 7t, 20t, 24t; D. pacificum (Pacific sand perch), 178t, 181f, 194f, 521t Diplodus sargus, 521t Diplogrammus pauciradiatus, 523t Diplophus taenia (bristlemouth), 365 Diplospinus multistratus, 309f Diretmus argenteus, 311f disease, pollution-related, 603–7 dispersal, 49, 526f distribution patterns, 5–6, 8, 76, 546 disturbance, 466–79; anthropogenic, 467, 473 (See also pollution); competition and, 472, 477; defined, 467; direct versus indirect effects, 468; fitness and growth, 472, 473; freshwater inflows and salinity, 473; habitat selection and use, 469–70, 473, 474–75; hypoxia and, 468–73; natural disturbance, 467–68; predation and, 442; rate of, 108; storms, 473–77; theoretical context of, 466–67 diurnal patterns, 75, 543, 547 diversity patterns, 83, 85, 107–12, 442–43 dogfish sharks (Squalidae), 106t, 175, 177t, 180t. See also Squalus acanthias

dogtooth lampfish (Ceratoscopelus townsendi), 359, 366t, 369, 370f; larval stages of, 276t, 277f, 279, 280, 305 Dolan, R., 3 Dolichopteryx longipes (brownsnout spookfish), 349t dolphinfish (Coryphaena hippurus), 20t, 89f, 324, 326, 331f, 332, 333, 337t Dormitator latifrons, 20t, 24t Dorosoma petenense (threadfin shad), 161t, 612t, 613f, 617 Dover sole. See Microstomus pacificus dragonfishes (Stomiidae), 329, 350–51t Drazen, J. C., 373, 374 dreamers (Oneiroididae), 17t, 352t, 358, 390, 395, 402t, 520t drift algal beds, 111, 151–52, 154f driftfish (Psenes spp.), 328f, 333, 559 dusky shark, 337t dwarf lanternfish, 370f dwarf perch. See Micrometrus minimus dwarf perch (Micrometrus minimus), 18t, 111f, 145t, 161t, 213, 235t, 499, 533t; in surf zone, 95f, 150t, 151f, 152, 154f, 155t Dyer, B. S., 621 East Pacific Barrier, 69 Ebeling, A. W., 359, 363–64, 437–38, 456–57, 466; on kelp bed/rocky reef habitat, 231, 241, 244, 245, 246; on movement and activity patterns, 526, 531, 547; on storm disturbance, 475, 476 Eber, L. E., 6 Echeneidae (suckerfishes), 324–25. See also Remora spp. Echeneis naucrates (sharksucker), 20t, 24t, 324, 329f Echinomacrurus occidentalis, 353t Echinorhinus cookei, 20t, 23t ecological classification, 81–112; abundance within species groups, 88t; approach to, 81, 83–85; bay and estuary, 123–24; biological basis for, 85–87; habitat generalists, 102–3; patterns of diversity and, 107–12; physical bases for, 97–102; species richness and, 109–12; taxonomic composition of assemblages, 103, 105–6. See also specific habitat ecological variables, 5 economic exclusion zones (EEZs), 525 ecosystem collapse, 56, 58 ecosystem conservation, 589–90 eelgrass (Zostera marinus), 111, 134, 397, 475 eelpout (Melanostigma pammelas), 18t, 22t, 348, 352t. See also Lycodapus; Lycodes spp.; Zoarcidae eels. See Anguillidae (freshwater eels) egg laying. See oviparity (egg laying) Eigenmann, Carl and Rosa, 253 Ekman, S., 69 elasmobranches, 94, 484, 504 electric ray. See Pacific electric ray (Torpedo californica) Elegatis bipinnulatus (rainbow runners), 324 elephant seals (Mirounga angustirostris), 530, 542, 561 elkhorn sculpin (Alcichthys alcicornis), 499, 501–2 Elkhorn Slough, 8, 131–32, 133, 400, 619 Elliot, M., 119 Elliott, J., 560–61 El Nino Southern Oscilation. See ENSO Elops affinis (machete), 7t, 20t, 518t Embassichthys bathybius (deep-sea sole), 354t, 372f

INDEX

643

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Embiotoca jacksonii (black perch), 5, 19t, 34t, 75, 92f, 111f, 150t, 585t; activity patterns of, 544, 547, 549, 633; in bays and estuaries, 127t, 128f, 132f, 134f, 136t, 145t; in Channel Islands, 48f, 49f; competition and, 450, 457–60, 461–62f, 463f; feeding of, 390; habitat range of, 102, 103, 105t; in harbors, 157t, 159, 161t, 162t; in kelp bed/rocky reef, 235t, 237f, 239f, 240f, 241f, 404; movement of, 533t, 542; phylogeographic structures of, 34t, 38, 39f, 40, 41, 624; predators and, 64, 430, 431; recruitment of, 412f, 415, 416; reproduction of, 496, 522t; in surf zone, 150t, 154f, 155t; symbiotic relations of, 556f, 557t; territoriality of, 453t, 454, 455; trophic relations and, 400f Embiotoca lateralis (striped seaperch), 18t, 75, 92f, 533t, 585t; activity patterns of, 544–45; competition and, 450, 453f, 457–60, 461–62f, 463f; in kelp bed/rocky reef, 235t, 237f, 240f, 404; phylogenetic structures of, 34t, 40; recruitment of, 415, 416; in surf zone, 111f, 151, 152f, 153t Embiotocidae (surfperches), 9f, 10f, 106t, 235t, 557t, 591, 630; activity patterns of, 533t, 539, 544; on continental shelf, 175, 178t, 180t, 186, 258t; evolution of, 71, 72, 74, 75, 77; as habitat generalists, 87, 105; pollution and, 602; predation and, 437–38; recreational fishing of, 581; reproduction of, 484, 498, 504, 505; storm disturbance and, 474–77, 478f; subsistence fishing of, 567, 568; in surf zone, 152f, 153t, 155t Emblemaria hypacanthus (signal blennies), 432, 503, 522t emergence behavior, 208, 210 Emery, K. O., 228 Emmet, R. L., 125 endangered species, 125, 128–30 endosymbiotic mutualism, 557 Engle, J. M., 229 English sole. See Pleuronectes/Parophrys vetulus Engraulidae (anchovies), 72, 106t, 149, 494. See also Anchoa spp.; anchovy-sardine regimes Engraulis mordax (northern anchovy), 19t, 72, 186, 233t, 260, 429, 590; abundance of, 89, 91, 160t, 161t, 336t; in bays and estuaries, 125, 127t, 128f, 129, 132f, 138t, 145t; competition and, 450; diel movement of, 543; feeding of, 390, 394; habitat of, 102, 103, 105t; larval stages of, 273–78f, 280, 281–84f, 291, 292, 294f, 299, 303–5; in pelagic zone, 94f, 159f, 330, 332f, 335t, 337t; schooling by, 324; in surf zone, 150t, 151f, 152, 155t; trophic relations and, 397f, 398f, 401f Engyophrys sanctilaurentii (speckletail flounder), 7t, 20t, 25t, 179t, 182f, 195f Enhydra lutris (sea otter), 624, 627, 628 Enneanectes reticulatus (flag triplefin), 236t Enophrys bison (buffalo sculpin), 17t, 234t, 485, 486, 500t Enophrys taurus (bull sculpin), 17t ENSO (El Niño-Southern Oscillation), 174, 240, 330, 466, 504, 615, 630–31; bay habitat and, 129, 135, 141; distributional patterns and, 4–5, 6, 14–15; La Niña event and, 4–5, 222, 283, 286; larval populations and, 282–84, 285–93f, 298–302, 303, 628; phylogeography and, 37, 41; recruitment and, 414, 417; reef coral damage by, 69; rocky intertidal

644

INDEX

zone and, 221–22; species density and, 249 environmental legislation, 588, 591 environmental potential for polygamy (EPP), 502 Environmental Protection Agency (USEPA), 168, 170, 602 Eopsetta exilis. See Lyopsetta exilis Eopsetta jordani (petrale sole), 18t, 179t, 182f, 183f, 185f, 193; foraging guild, 193, 195f, 196f, 197f epibranchial organs, 392–93 Epinephelinae spp., 58, 497 Epinephelus spp. (cabrilla): E. analogus (spotted cabrilla), 20t, 24t, 234t; E. guttatus, 521t; E. labriformis (flag cabrilla), 234t; E. niphobles, 20t, 25t; E. striatus, 521t epipelagic fishes, 320, 330, 342–43, 345t, 368; trophic relations in, 401f, 405–6 Eptatretus deani (black hagfish), 18t, 22t, 101f, 353t, 372f Eptatretus stoutii, 18t, 518t Erilepsis zonifer, 17t, 21t Ernogrammus walkeri (masked prickleback), 7t, 17t, 24t Erres zachirus (rex sole), 333. See also Glyptocephalus zachirus Eschmeyer, W. N., 483 escolar (Lepidocybium flavobrunneum), 20t, 22t, 327f, 330 Estero de Punta Banda, 136t estuaries. See bay/estuaries (BE) Etrumeus teres, 21t, 23t, 280f Eucinostomus spp. (mojarra): E. argenteus (spotfin mojara), 178t, 181f, 182f, 194f, 195f; E. currani, 20t, 24t; E. dowii, 20t, 25t Eucyclogobius newberryi (tidewater goby), 5, 18t, 132f, 614; in bays and estuaries, 126t, 128f, 129f, 130t, 134f; phylogeography and, 34t, 38, 39f eulachon (Thaleichthys pacificus), 128–29, 130t Euleptorhampus longirostris (half beak), 20t, 24t Euleptorhampus viridis (ribbon halfbeak), 331f, 333 Eumicrotremus orbis, 521t Euphausia pacifica (krill), 371 Euprotomicrus bispinatus (pygmy shark), 17t, 331 Euryhaline species, 88 Eurypegasus draconis, 520t Eurypharynx pelecanoides (umbrellamouth gulper), 348, 519t Eutaeniophorus festivus, 310f Euthymus spp.: E. affinis, 20t, 25t; E. lineatus, 20t, 24t; E. pelamis, 22t eutrophication, 145 evolution, 50, 55–77; Cenozoic influences, 68–70; distribution and latitude, 68–70; extinction-resurgence episodes and, 55–56, 62; for feeding effectiveness, 59–62; mainstream feeding relations and, 58–59; modern teleost fishes, 58; new modes of feeding and, 62–68; other evolutionary lines, 72–73; perciformes, 71–72; percoids, 57–58; pleuronectiformes and, 70–71; predation and, 428–33; scorpaeniformes and, 70; smallness and, 62–64; species composition and, 73–77; teleost history and, 55, 68; teleost-scleractinia connection, 56–57 Exocoetidae. See flyingfish (Exocoetidae) extinction-resurgence episodes, 55–56, 62, 625

Fagerstrom, J. A., 56 fangtooth (Anoplogaster cornuta), 311f, 402f, 520t; as bathypelagic fish, 348, 352t, 358, 366t fantail sole (Xystreurys liolepis), 19t, 145t, 155t, 158t; on continental shelf, 179t, 181f, 182f; foraging guilds, 192f, 194f, 195f; larval stages of, 293, 295f, 300, 301f, 302 Feder, H. M., 227, 555 Federal Food Administration, 570 feeding: biting, 390–91; commensalism, 554, 558–61; competition in, 389, 613; by deep sea fishes, 344, 361, 364–65, 375–76; distribution and, 544–46; epibranchial organs, 392–93; factors determining diet, 388–89; larval survival and, 311, 312; mechanisms in, 387–95; oophagy, 484; overview of, 387–88; pharyngeal and oral jaws, 393–94; in rocky intertidal zone, 218–20; by soft-bottom fishes, 188–90; suction and ram feeding, 391–92; suspension feeding, 392–94; types of prey capture, 389–90 feeding divergence, 59–68; ambushers, 59–62, 68, 190; dissemblance, 64; herbivores, 65, 66f, 74, 207, 390; increased effectiveness in, 59–62; inedibility, 64–66; new modes, 62–68; nocturnality, 66–68; piscivorous fish, 131, 395, 402; planktivores, 63, 65, 131, 189, 420, 547; smallness, 62–64; straightforward rush, 61–62, 68 Ferrante, Pietro, 571 Ferren, W. R., Jr., 120 Fierstine, H. L., 133 filetail cat shark (Parmaturus xaniurus), 19t, 23t, 101f, 353t, 518t fin erosion disease, 603, 604f, 605, 607f finescale cusk-eel (Lepophidium microlepis), 177t, 183f, 196f finescale triggerfish (Balistes polylepis), 21t, 23t, 236t, 309f, 523t; on continental shelf, 179t, 194f; reproduction and, 485 Finney, B. P., 624–25 fishing and fisheries, 540, 575–76; climate change and, 625–26, 627, 633; foreign, 578–79; management of, 461–62, 586–90; overfishing, 567, 572, 573, 576, 580, 588; subsistence, 524, 567–68, 580. See also commercial fisheries; recreational fishing Fistularia commersonii, 520t Fistularia corneta (deepwater cornetfish), 7t, 14, 20t, 25t Fitch, J. E., 348, 483 flag cabrilla (Epinephelus labriformis), 234t flag flounder (Perissias taeniopterus), 179, 183f, 193, 196f flag rockfish (Sebastes rubrivinctus), 7t, 18t, 99f, 255, 260f, 263t flashlight fishes (Anomalopidae), 66, 370f, 520t, 558f. See also Protomyctophum flatfishes. See Pleuronectiforms flathead sole (Hippoglossoides elassodon), 21t, 605 flounders, 179t, 183f, 185f, 195f, 196f. See also Paralichthyidae; Pleuronectidae fluffy sculpin (Oligocottys snyderi), 18t, 90f, 399f, 500t; in rocky intertidal zone, 209t, 215t, 216f, 217f, 218, 220f flyingfish (Exocoetidae), 73, 326f, 331f, 401f; Cheilopogon heterurus, 20t, 25t, 520t; Cheilopogon pinnatibarbatus, 19t, 22t, 405; Cheilopogon spp., 323, 328, 331, 405; Cypselurus californicus, 73

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Fodiator acutus, 20t, 24t food web. See trophic interactions foraging behavior, 67–68, 189–90, 190–92, 531; guilds, 190–92, 192f, 194–97f. See also feeding Forcipiger flavissimus (longnose butterfyfish), 63 Forrester, G. E., 422, 430, 434, 439–40 freckled rockfish (Sebastes lentiginosus), 18t, 25t, 255 freshwater fishes: in bays and estuaries, 124, 128f, 132f, 134f fringed flounder, 137f fringeheads (Neoclinus spp.), 18t, 19t, 23t, 97f, 236t, 238f, 247; in kelp bed/rocky reef, 236t, 238f, 247 Fuentes, E. R., 451 Fundulus heteroclitus (mummichog), 139, 470, 520t Fundulus parvipinnis (California killifish), 10–11, 19t, 34t, 41, 42f, 88, 533t; abundance of, 142, 143f, 145t; in bays and estuaries, 93f, 120, 126t, 129f, 132f, 134f, 137f, 138; pollution and, 601; trophic relations and, 396f, 401 Gadidae (cods), 175, 180t Gadus macrocephalus (Pacific cod), 17t, 21t, 605 Galeocerdo cuvier, 20t, 25t Galeorhinus galeus (soupfin shark), 19t, 89f, 233t, 337t, 576 Gambusia affinis (western mosquitofish), 126t, 132f, 535t, 612t, 616–17 garibaldi (Hypsypops rubicundus), 19t, 65f, 74, 92f, 404, 522t, 555, 589; activity patterns of, 535t, 544; in harbors, 157t, 162t; in kelp bed/rocky reef, 235t, 237f, 239f, 241f, 243f; reproduction and, 489, 490f, 493, 495, 496, 501; territoriality of, 451, 453t; trophic relations and, 400f Garrison, L., 197 Gartner, J. V., Jr., 354, 368, 406 Gasterosteus aculeatus (threespine stickleback), 18t, 153t, 520t; in bays and estuaries, 126t, 128f, 129f, 132f, 142f; reproduction and, 488, 489, 491–92 Geibel, J. J., 245–46, 539, 542 Gelidium robustum (algae), 457, 459–60 Gempylus serpens (snake mackerel), 21t, 25t, 327f, 329, 332 gender allocation, 487, 488t, 495–98, 502–4, 505f, 506 gene flow, 27, 38, 48, 49-50, 623; glaciations and, 33, 623–24 genetic divergence, 31, 32 gene trees, 27, 36. See also phylogeography Genyonemus lineatus (white croaker), 19t, 96, 102, 105t, 390, 631; commercial fishing and, 574, 579, 590; on continental shelf, 98f, 172, 178t, 181f, 182f; foraging guild, 192f, 194f, 195f; in harbors, 157t, 159f, 160–61t, 162; larval stages of, 276t, 291, 294, 297f, 299, 305; movement of, 535t, 540; pollutants and, 598, 600, 601, 603, 604, 605–6; recreational fishing and, 582; subsistence fishing and, 568; in surf zone, 150t, 154f, 155t, 156; trophic relations and, 397f Genyonemus spp. (croakers) larval stages of, 291, 295, 297–98 Gerkema, M. P., 549 Gerreidae (mojarras), 175, 180t, 506; spotfin mojarra, 178t, 181f, 182f, 194f, 195f Gerres cinereus, 521t ghostly grenadier (Coryphaenoides), 353t, 369, 374, 376

ghost shrimp (Neotrypaea spp.), 559, 560f giant grenadier (Coryphaenoides pectoralis), 101f, 353t, 369, 372f, 373–74 giant kelpfish. See Heterostichus rostratus giant kelp (Macrocystis pyrifera), 48, 67, 71f, 415, 421, 436, 438–39, 459, 477 giant lampfish (Parvilux ingens), 351t, 366t, 370f giant sea bass (Stereolepis gigas), 18t, 87, 555, 624; in kelp bed/rocky reef, 92f, 234t, 237f, 239f, 241f; recreational fishing and, 583, 589; reproduction and, 494, 497; trophic relations, 400f, 405 Gibbonsia elegans (spotted kelpfish), 19t, 60, 61f, 92f, 111f, 155t, 532t; hypoxia and, 468; in kelp bed/rocky reef, 236t, 238f; in rocky intertidal zone, 207, 215t, 216f, 217, 220f; in surf zone, 145t, 154f, 155t, 159 Gibbonsia metzi (striped kelpfish), 19t, 90f, 111f, 155t, 236t, 238f; in rocky intertidal zone, 215t, 216f; tophic relations of, 399f, 403 Gibbonsia montereyensis (crevice kelpfish), 18t, 90f, 111f, 215t, 216f, 236t, 399f Gibbonsia spp. (kelpfishes), 35t, 215t, 477 Gibson, R. N., 212, 214, 217, 218, 221, 395 Gigantactis spp. (anglefish), 358, 520t Gigantura indica, 519t Gilbertidia sigalutes, 500t, 521t Gillichthys mirabilis (longjaw mudsucker), 11, 19t, 88, 211, 533t, 617; in bays and estuaries, 93f, 126t, 129f, 132f, 134f, 136t, 138t, 143f; hypoxia and, 472; larval stages of, 303, 304f; phylogenetic relations and, 35t, 43, 44f, 45t, 46t; trophic relations and, 396f, 402 gill nets, 578f, 590–91 Girella nigricans (opaleye), 19t, 102, 105t, 136t, 150t, 585t; activity patterns of, 534t, 544–45; in harbors, 157t, 158t, 162t; as herbivore, 65, 66f, 74, 394, 403, 404; in kelp bed/rocky reef, 92f, 235t, 237f, 239f, 241f; mutualism of, 556f, 557t, 558; phylogenetic characteristics of, 35t, 41, 43, 44f, 45t, 46t; recruitment of, 414, 419; in rocky intertidal zone, 209t, 215t, 216f Girella tricuspidata, 522t glaciations, 32–33, 36, 37, 41, 69; gene flow and, 33, 623–24 global warming, 632–33. See also climate change globalization, in fishing industry, 578–79 Glyptocephalus zachirus (rex sole), 18t, 22t, 101f, 103, 307, 535t; on continental shelf, 179t, 183f; foraging guild, 192f, 194, 195f, 196f, 197f Gnathophis spp., 19t, 24t, 519t goatfishes (Mullidae), 7t, 135t, 329, 506 Gobiesox meandricus (northern clingfish), 18t, 33, 34t, 90f, 236t, 523t; in rocky intertidal zone, 209t, 215t, 216f, 220f, 221; trophic relations and, 399f, 403 Gobiesox spp. (clingfishes), 106t, 217f; G. eugrammus, 18t, 25t; G. papillifer, 20t, 25t; G. rhessodon (California clingfish), 19t, 90f, 212–13, 215t, 216f, 238f, 403; reproduction and, 485 Gobiidae (gobies), 9f, 10f, 105, 106t, 142f, 506; alien species, 612–14, 619; larval stages of, 289, 294f, 298, 303, 304; movement of, 524, 533–34t; pollution and, 602; reproduction and, 491, 493, 497, 498, 503, 504 Gobiomorphus breviceps, 523t Gobiosoma bosc (naked goby), 469

golden lanternfish (Myctophum aurolaternatum), 307, 310f, 370f golden spotted rock bass (Paralabrax auroguttatus), 234t, 497 golden wrasse (Halichoeres melanotis), 235t Goldman, K. J., 528, 542 Gonichthys tenuiculus (slendertail lanternfish), 277, 279f, 280, 370f gonochorism, 483, 497, 498, 502–3, 504, 507 Gonostomatidae (bristlemouths), 329, 354, 356f, 359, 365 gopher rockfish (Sebastes carnatus), 19t, 23t, 219t, 258, 270, 585t; in kelp bed/rocky reef, 91f, 234t, 237f, 240; movement of, 531, 536t; recruitment and, 415, 420; territoriality of, 453t, 455–56f, 457f Gorbatenko, K. M., 361 Gosline, W. A., 55, 63, 72, 73 Gotshall, D. W., 253 Gracillaria spp. (algae), 111, 159. See also algae Graham, M. H., 624 Gramma loreto, 521t Grammonus diagrammus, 25t Grant, J. W. A., 496 Grant, W. S., 624 grass rockfish (Sebastes rastrelliger), 18t, 59f, 111f, 234t, 270, 403, 430; in rocky intertidal zone, 90f, 215t, 216f, 217f, 219t; in surf zone, 152, 153t, 155t, 157t graveldiver (Scytalina cerdale), 17t, 90f, 215t, 216f, 220f, 522t; feeding of, 399f, 403 gray remora (Remora brachyptera), 21t, 25t, 325 gray smoothhound (Mustelus californicus), 19t, 95f, 127t, 132f, 233t; in surf zone, 150t, 151, 153, 156f, 157t, 158t greater sand perch (Diplectrum maximum), 7t, 20t, 24t Greely, T. M., 368 Green, J. M., 543 greenblotched rockfish (Sebastes rosenblatti), 18t, 23t, 102, 105t, 183f; in deep rock habitat, 100f, 255, 262f, 263t greenlings. See Hexagrammidae greenspotted rockfish (Sebastes chlorostichus), 18t, 22t, 178t, 183f, 196f; in deep rock habitat, 100f, 255, 262f, 263t; movement of, 528, 536t, 539 greenstripe rockfish (Sebastes longatus), 18t, 22t, 102, 105t, 537; in deep rock habitat, 100f, 255, 262f, 263t green sturgeon (Acipenser medirostrus), 18t, 125, 126t, 128f, 130t grenadiers. See Coryphaenoides spp.; Macrouridae (grenadiers); Nezumia spp. Grossman, G. D., 212, 219, 220, 221 grouper. See Mycteroperca spp. Gruber, D., 291, 297, 298 grunion. See Leuresthes tenuis/sardina grunts. See Haemulidae (grunts) grunt sculpin (Rhamphocottus richardsonii), 17t, 21t, 213, 500t, 512t Grutter, A. S., 555 Guadalupe cardinalfish (Apogon guadalupensis), 19t, 24t, 234t, 485 guitarfish, 176, 177t, 180, 183f, 189, 233t. See also banded guitarfish (Zapteryx exasperata). See Rhinobatidae; Zapterix exasperata gulf grouper (Mycteroperca jordani), 19t, 25t, 234t Gulf of California, 27, 41–43, 46 gulf sanddab (Citharichthys fragilis), 7t, 20t, 277f, 278f, 280 Gunnellichthys spp., 523t

INDEX

645

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gunnels (Pholis spp.), 9f, 10f, 72, 90f, 209t, 217f; P. clemensi, 17t, 21t; P. laeta (crescent gunnel), 17t, 21t, 209t, 485, 522t; P. ornata (saddleback gunnel), 17t, 153t, 399f; P. schultzi, 17t, 21t; Ulvicola sanctaerosae (kelp gunnel), 18t, 24t, 72, 72f, 236t. See also penpoint gunnel; rockweed gunnel Gymnothorax meleagris, 518t Gymnothorax mordax (California moray), 19t, 24t, 95f, 555, 558f; activity patterns of, 545, 549; in harbors, 157t, 158; in kelp bed/rocky reef, 233t, 238f, 239f, 241f, 243f Gymnura marmorata (butterfly ray), 20t, 135t, 518t habitat. See ecological classification; specific habitat Haedrich, R. L., 559 Haemulidae (grunts), 66, 69, 74, 235t, 393, 534t; bronzestripe (Orthopristis reddingi), 178t, 181f, 182f, 194f, 195f; on continental shelf, 175–76, 178t, 180t. See also Anistotremus spp.; salema (Xenistius californiensis) Haemulon flavoluneatum (grunt), 546 Haemulon sciurus, 521t Haemulopsis axillaris (yellowstripe grunt), 178t, 182f, 194f, 195f hagfish (Myxinidae), 103, 106t, 353t, 578–79; black hagfish (Eptatretus deani), 18t, 22t, 101f, 353t, 372f hakes, 472. See also Merluccius spp. halfbanded rockfish (Sebastes semicinctus), 19t, 23t, 99f, 178t, 183f, 196f, 631; in deep rock habitat, 255, 257, 260f, 263t halfbeak, 331f, 333. See also Hyporhamphus rosea halfmoon (Medialuna californiensis), 19t, 35t, 92f, 157t, 162t, 400f; as herbivore, 65, 66f, 74, 394, 404; in kelp bed/rocky reef, 235t, 237f, 239f, 241f; symbiotic relations and, 556f, 557t, 558 halfspotted tonguefish (Symphurus atrimentatus), 179t, 182f, 195f halibut. See Hippoglossus stenolepsis; Paralichthys californicus Halichoeres semicinctus (rock wrasse), 19t, 87, 92f, 162t, 400f; cleaner behavior of, 556f, 557t; in kelp bed/rocky reef, 235t, 237f, 239f, 241f, 404; movement and activity patterns of, 534t, 544, 546, 548; phylogenetic relations and, 44f, 45t, 46t, 49; prey dissemblance and, 64; reproduction and, 487, 490, 491f, 496, 497; in surf zone, 150t, 157t Halichoeres spp. (wrasses): H. chrysus, 549; H. dispilus (chameleon wrasse), 92f, 235t, 237f, 241f; H. (golden wrasse), 235t hammerhead shark, 89f, 337t, 538t Hanan, D. A., 336 Harbison, G. R., 307 harbors, 82t, 157–63 hardfin marlinsuckers (Rhombochirus osteochir), 25t, 325 Hare, S. R., 15 Harengula thrissina, 20t, 25t Hastings, P. A., 432, 623 hatchetfish (Sternoptyx spp.), 365, 366t, 402f, 406, 519t; S. diaphana (diaphanous hatchetfish), 350t, 354, 356f, 402f, 519t; S. obscura, 350t. See also Argyropelecus spp. Hayakawa, Y., 499 Hayden, B. P., 3

646

INDEX

headlight fish. See Diaphus spp. Hecker, B., 175 Hedgpeth, J. W., 174 Helfman, G. S., 548 Hemianthias signifer, 19t, 311f Hemilepidotus spp., 500; H. gilberti, 499; H. hemilepidotus (red Irish lord), 17t, 485, 486f, 498, 500t, 521t; H. spinosus (brown Irish lord), 17t, 91f, 234t, 238f, 296f Hemiramphus spp., 73; H. saltator, 20t, 25t Hemitripterus villosus (Japanese sea raven), 499, 521t Heneman, B., 589 Hensen, V., 271 Herbinson, K.T., 151, 187 herbivores, 394, 403, 404 hermaphroditism, 343, 374, 487, 488t, 506; gonochorism and, 502–3, 504; mating systems and, 496–98 Hermosilla azurea (zebraperch), 15, 19t, 87, 544, 630; genetic characteristics of, 44f, 45t, 46t; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 92f, 235t, 237f, 241f, 404; symbiotic relations and, 556f, 558; trophic relations and, 394, 400f Herrgesell, P. L., 123 herring. See Clupeidae (herrings) Hertig, M., 554 Hesperonoe adventor (scale worm), 559f Hessler, R. R., 373 Heteroclinus spp., 522t Heterodontus francisci (horn shark), 19t, 95f, 137f, 394, 429, 518t, 534t; activity patterns of, 544, 546, 549; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 233t, 239f, 241f; in surf zone, 153, 156f Heteropriacanthus cruentatus, 521t Heterostichus rostratus (giant kelpfish), 19t, 103, 105t, 111f, 162t, 418, 522t; in bays and estuaries, 136t, 137f, 145t; cleaner behavior of, 555, 557t; in kelp bed/rocky reef, 71, 71f, 96, 97f, 236t, 238f, 239f; movement of, 532t, 544; predation and, 430, 431f, 436; in surf zone, 150t, 151f, 152, 154f, 155t; trophic relations and, 400f, 405 Hexagrammidae (greenlings), 70, 91f, 106t, 234t, 263t, 329; on continental shelf, 175, 178t, 180t; larval stages of, 270, 295; reproduction and, 485, 490–91, 495, 501, 507; symbiotic relations of, 560–61. See also Oxylebius pictus (painted greenling) Hexagrammos decagrammus (kelp greenling), 17t, 215t, 259, 263t, 333, 585t; feeding of, 392; in kelp bed/rocky reef, 70, 71f, 91f, 234t, 237f, 240f; reproduction of, 490, 491f, 495, 501 Hexagrammos lagocephalus (rock greenling), 234t Hexagrammos superciliosus, 17t Hexanchus griseus, 18t Higgins, Elmer, 572 highbrow crestfish (Lophotus cristatus), 327f, 332 high cockscomb (Anoplarchus purpurescens), 17t, 35t, 90f, 498, 522t; in rocky intertidal zone, 209t, 210, 213, 215, 216f, 220; trophic relations and, 399f, 403 highfin dragonfish (Bathophilus flemingi), 351t, 357f highfin lizardfish (Bathysaurus mollis), 353t, 369, 372f, 374 highfin sand perch (Diplectrum labarum), 178t, 182f, 183f, 195f, 196f Hill, C. W., 135

Hippocampus ingens (Pacific seahorse), 20t, 25t, 135t, 137f, 484 Hippoglossina bollmani (spotted flounder), 179t, 182f, 195f Hippoglossina stomata (bigmouth sole), 19t, 23t, 98f, 236t, 398f, 535t, 606; on continental shelf, 179t, 182f, 183f; foraging guild, 192f, 195f, 196f; larval stages of, 293, 295f, 302 Hippoglossoides elassodon (flathead sole), 21t, 605 Hippoglossus stenolepsis (Pacific halibut), 17t, 525, 580 Hirundichthys rondeletii (darkwing flyingfish), 331 Histrio histrio (anglerfish), 324 Hixon, Mark A., 433, 441, 455, 459, 466, 496; on movement patterns, 526, 531, 547 Hjort, J., 307–8, 309, 434 Hobson, E. S., 75, 188, 214, 227, 485; on movement patterns, 544, 546, 548; on predation, 440–41; on symbiotic relations, 555, 556, 561 Hohenshell, A. B., 582 Holbrook, Sally J., 245, 429, 430–31, 459–60 Holder, Charles Frederick, 580, 582, 589 Holocentridae (soldierfishes), 329 holoepipelagic fish, 324–25, 326–28f, 330t, 331 Holthyrnia spp.: H. latifrons (streaklight tubeshoulder), 369; H. macrops (bigeye searsid), 350t; H. melanocephala (searsid), 350t home range, and habitat complexity, 525, 531, 539–40 honeycomb rockfish (Sebastes umbrosus), 19t, 24t, 99f, 255, 260f, 586 Hoplostethus atlanticus (orange roughy), 66, 520t Horn, Michael H., 5, 9, 13t, 75, 158, 628; bay and estuary study by, 6, 10, 122, 137, 140; on monkeyface prickleback, 212, 530, 558 horn shark. See Heterodontus francisi hornyheaded turbot. See Pleuronichthys verticalis hound sharks. See Mustelus spp. Hovden, Knut, 572 Hovey, T. E., 494, 506 Howard, D. F., 417, 421 Howella sp., 521t How to Fish the Pacific Coast (Cannon), 590 Hubbs, C. L., 11, 123 human-health risks, pollution and, 601–2 human impact, 270 hundred-fathom codling. See Physiculus rastrelliger Hunter, J. R., 305 Hydrolagus colliei (spotted ratfish), 18t, 177t, 183f, 185f, 394, 532t; foraging guild, 196f, 197f; habitat of, 101f, 102, 103, 105t hydrophones, 528, 530, 540 Hygophum atratum (thickhead lanternfish), 277, 279f, 280, 370f Hyperoglyphe antarctica, 523t Hyperprosopon anale (spotfin surfperch), 18t, 97f, 152f, 153t, 155t Hyperprosopon argenteum (wall-eye surfperch), 18t, 67f, 95f, 186, 397f, 585t, 631; activity patterns of, 533t, 544, 546; in coastal pelagic zone, 155t, 157t, 159f, 160–61t; in kelp bed/rocky reef, 235t, 239f; in surf zone, 150–51, 150t, 152f, 153t, 154f

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Hyperprosopon ellipticum (silver surfperch), 18t, 91f, 235t, 240f, 585t; in surf zone, 152f, 153t Hypnus gilberti, 19t Hypomesus pretiosus (surf smelt), 17t, 72, 494–95, 519; in bays and estuaries, 93f, 127t, 128f, 129f, 132f; in surf zone, 151, 152f, 153t Hypomesus spp. (smelt): H. nipponensis (wakasagi), 130t, 131, 612t, 615–16; H. transpacificus (delta smelt), 126t, 128, 129, 130t, 131, 473, 615 Hypoplectrodes maccullochi, 521t Hyporhamphus naos, 20t, 25t Hyporhamphus rosea (California halfbeak), 19t, 73, 88, 93f, 135t, 136, 328 Hyporhamphus unifasciatus, 520t hypoxia, 207, 210, 211, 468–73; effects on growth and fitness, 472–73; feeding and trophic interaction, 471; habitat selection and use, 469–70; reproduction and, 471–72 Hypsoblennius gentilis (bay blenny), 19t, 95f, 111f, 236t, 455, 532t; in bays and estuaries, 126t, 134f, 136t, 137f, 145t Hypsoblennius gilberti (rockpool blenny), 19t, 90f, 236t, 403; movement of, 531, 532t, 543; in rocky intertidal zone, 209t, 210, 211, 215t, 216f Hypsoblennius jenkinsi (mussel blenny), 19t, 92f, 136t, 236t, 238; movement patterns of, 531, 532t; phylogenetic characteristics of, 43, 44f, 45t, 46t; territoriality of, 451, 453t Hypsoblennius spp. (blennies), 236t, 333, 334f, 522t; larval forms of, 293, 295f, 298, 303, 304f; reproduction and, 492, 493. See also Blenniidae (combtooth blennies) Hypsopsetta guttulata (diamond turbot), 19t, 181f, 396f, 402, 535t, 600; in bays and estuaries, 127t, 129f, 136t, 137f; larval stages of, 291, 294f, 299 Hypsurus caryi (rainbow seaperch), 18t, 91f, 235t, 239f; cleaner behavior of, 556f, 557t; movement of, 533t, 542, 544–45; niche overlap and, 457, 458f; in surf zone, 152, 155t, 162t Hypsypops rubicundus. See garibaldi Hyrolagus colliei, 518t Hysterocarpus traski, 484f Icanberry, J. W., 294, 295 Icelinus quadriseriatus (yellowchin sculpin), 19t, 23t, 398f, 403, 532t; on continental shelf, 98f, 173, 178t, 182f; foraging guilds, 192f, 195f Icelinus spp. (sculpins): I. burchami, 17t, 22t; I. cavifrons, 19t, 23t; I. filamentosus (threadfin sculpin), 18t, 22t, 178t, 183f, 196f, 258t; I. fimbriatus, 17t, 24t; I. oculatus, 18t, 22t; I. tenuis, 18t, 22t Ichthyococcus irregularis (bullbog lightfish), 350t ichthyoplankton assemblages, 269–313; in bays and estuaries, 142–43, 303–5; CalCOFI samplings, 269–70, 271, 275–302, 313, 361, 362, 368–69, 628; coastal assemblages, 290–303; ENSO events and, 282–84, 285–93f, 298–302, 628; geographic and seasonal distribution, 277–80, 296–98; historic overview, 269–70; interannual and decadal changes, 281–87, 298–302; nearshore, 289–90; ontogenetic stages, 272–75; PDO and, 283, 284, 285–93f, 299–302f, 303;

samplings, 270–72; sardine and anchovy regimes, 281–82, 283–84f; specializations, 306–7, 308–11f; trophic relationships, 307–13; vertical distribution, 305–6 Icichthys lockingtoni (medusa fish), 18t, 22t, 328f, 330, 559; larval stages of, 276, 277–78f, 279, 286f Icosteus aenigmaticus (ragfish), 17t, 22t, 327f, 330, 523t Idiacanthus antrostomus (black dragon), 307, 310f, 351t, 356, 357f, 366t, 370f Il’inskii, E. N., 361 Ilypnus gilberti (cheekspot goby), 95f, 154f, 155t, 159, 161t, 534t; in bays and estuaries, 126t, 134f, 136t, 137f, 145t, 303; trophic relations and, 396f, 401 indigenous peoples, 624, 627 Indo-Pacific fishes, 69 Inegocia japonica, 521t inland silverside (Menidia beryllina), 612t, 616, 619 inner shelf (IS), 82t, 85t, 86f, 96, 109, 171, 176; analysis of, 104t; trophic relations and, 397f interannual variability, 140–42 International Pacific Halibut Commission (IPHC), 525 intertidal copepod (Tigriopus californicus), 38 Isaacs, J. D., 588, 624 Isistius brasiliensis (cigar shark), 561, 561f island kelpfish (Alloclinus holderi), 92f, 162t, 238f, 477, 534t; cleaner behavior of, 555, 556f, 557t; feeding by, 60, 61f island populations. See California Channel Islands Isopsetta isolepsis (butter sole), 17t, 174, 179t, 181f, 194f, 296f Istophorus spp., 523t; I. platypterus (sailfish), 21t, 25t, 333 Isurus oxyrhynchus (shortfin mako), 20t, 22t, 89f, 390, 518t, 579; movement of, 527–28, 529f, 540; in pelagic zone, 326f, 331, 337t; pollution and, 601; trophic relations and, 401f, 406 Iwama, G. K., 207 Iwamoto, T., 374 jack mackerel. See Trachurus symmetricus jacks. See Carangidae (jacks) jacksmelt. See Atherinopsis californiensis Jackson, J. B. C., 264, 625, 627 Japanese sea raven (Hemitripterus villosus), 499, 521t jawfish (Opistognathus spp.), 485, 521t Jensen, Greg, 556 Johnrandallia nigrirostris (barberfish), 235t Johnson, C. E., 485 Johnson, G. D., 62, 544 Jones, Everet, 561 Jones, J. A., 213, 223 Jordan, David Starr, 253, 569, 574 Jordania zonope (longfin sculpin), 17t, 21t, 211, 234t, 238f, 500t Kathetostoma averruncus (smooth stargazer), 20t, 23t, 179t, 185f, 197 Katsuwonus pelamis (skipjack tuna), 20t, 89f, 326f, 331, 337t, 573, 628 kelp bass. See Paralabrax clathratus kelp bed/rocky reef (KBRF), 85t, 86f, 87, 92f, 227–52; activities of fishes in, 248–49; analysis of, 104t; assessment of abundance in, 228–32; bottom depth in, 241–43; fish assemblages and, 247–48; interannual variability in, 249–50; kelp

overview, 228; latitude and, 239–41; major components of, 109f, 111; major taxa of, 232–36t; microalgae and bottom characteristics, 243–47; overfishing in, 625–26, 627; reef structure overview, 228; resource partitioning in, 454t; study localities, 82t, 84f; trophic relations in, 400f, 404–5, 625; young-of-year (YOY) and, 248 kelp clingfish (Rimicola muscarum), 18t, 111f, 155t, 236t, 238f, 405 kelpfishes. See Clinidae; Gibbonsia spp. kelp goby, 238f. See also Gobiidae kelp greenling. See Hexagrammos decagrammus kelp gunnel (Ulvicola sanctaerosae), 18t, 72, 72f, 238f kelp perch (Brachyistius frenatus), 19t, 111f, 162t, 422, 477, 494; adaptations of, 71f, 75; in kelp bed/rocky reef, 92f, 235, 239f, 240f; movement and activity patterns of, 533t, 544, 556f, 557t; predation and, 431f, 438–39, 440f, 442f; trophic relations and, 395, 400f, 404 kelp pipefish (Syngnathus californiensis), 19t, 103, 111f, 234t, 238f, 507; in surf zone, 150t, 154f, 155t kelp poacher (Agonomalus mozinoi), 70 kelp rockfish (Sebastes atrovirens), 19t, 157t, 162t, 270, 415, 536t; feeding/foraging of, 60f, 67–68; in kelp bed/rocky reef, 92f, 234t, 237f, 239f, 240f; phylogeographic structures of, 34t, 38 kelp spp. See Macrocystis spp. (kelp) Kendall, Arthur, Jr., 270, 273, 306, 485 killer whales, 429 killifish (Luacania parva), 130, 131, 134f, 612t, 614. See also Fundulus parvipinnis (California killifish) King Harbor, 244, 249, 630 king-of-the-salmon (Trachipterus altivelis), 20t, 327f, 332 Kleppel, G. S., 305 Kline, D. E., 371 Kramer, S. H., 151, 541 krill (Euphausia pacifica), 371 Kroon, F. J., 531 Kuhlia sandwichiensis, 522t Kyphosidae (sea chubs), 71, 105, 106t, 235t, 534t, 557t; feeding by, 65–66. See also Girella nigricans Kyphosus analogus, 20t Labridae (wrasses), 72, 74, 75, 106t, 235t, 393, 557t; on continental shelf, 176, 180t; feeding of, 64, 65; movement and activity patterns of, 534t, 541, 547, 548, 549; and reproduction, 496, 497, 498, 503, 507; Thalassoma spp., 235t, 487, 488. See also Halichoeres spp.; Oxyjulis californica (señorita); Semicossyphus pulcher (sheephead) Labrisomus spp., 289, 534t, 557t; L. xanti (largemouth blenny), 236t. See also Paraclinus integripinnis (reef finspot) Lactoria diaphana, 20t, 24t Lagocephalus lagocephalus (oceanic puffer), 20t, 23t, 332 Lamna ditropis (salmon shark), 17t, 22t, 89f, 326f, 330, 337t, 524 Lampadena urophaos (sunbeam lampfish), 277, 279f, 280, 351t lampara nets, 571, 575, 590 Lampetra spp. (lamprey), 128f; L. ayresii, 17t; L. tridentata (Pacific lamprey), 18t, 130t, 133, 518t, 561–62, 561f lampfish. See Nannobrachium spp.; Stenobrachius leucopsaurus; Triphoturus spp.

INDEX

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Lampris guttatus, 19t, 22t, 519t Lampris regius (opah), 89f, 321, 327f, 330, 337t Lamprogrammus niger (paperbone cuskeel), 353t Lane, E. D., 135 La Niña event, 4–5, 222, 283, 286. See also ENSO lanternfish, 351t, 370f; larval stages of, 276–80. See blue lanternfish; California lanternfish; Diogenichthys spp.; Myctophidae (lanternfish) Larson, Ralph J., 231, 244, 245, 531; competition studies of, 454, 455–56, 457 larval recruitment. See recruitment larval stages. See icthyoplankton assemblages Lasker, R., 310, 312 lateral line, 343 latitude, 8, 10, 110f; distribution and, 68–70, 122–23; kelp bed/rocky reef species and, 239–41; and ordination analysis, 11–14, 243 Laur, D. R., 246, 437–38 Laurs, R. M., 542 Lavenberg, R. J., 348, 359, 363, 483, 539 lavender sculpin (Leiocottus hirundo), 18t, 24t, 75, 76f, 532t; in kelp bed/rocky reef, 92f, 234t, 249t Lea, Robert N., 6, 483, 628 LeBoeuf, B. J., 561 Lee, W. J., 27 Leet, W. S., 125 left-coiling foram (Neogloboquadrrina pachyderma), 36 lefteye flounders. See Paralichthyidae Leiocottus hirundo (lavender sculpin), 18t, 24t, 75, 76f, 532t; in kelp bed/rocky reef, 92f, 234t, 240t, 532t Leiognathus brevirostris, 521t Leiostomus xanthurus (spot), 469, 472f leopard shark (Triakis semifasciata), 19t, 95f, 158t, 233t, 518t; in bays and estuaries, 127t, 128f, 132f; movement of, 527, 528t; in surf zone, 150t, 151, 153, 156f, 157t Lepidocybium flavobrunneum (escolar), 20t, 22t, 327f, 330 Lepidogobius lepidus (bay goby), 18t, 98f, 155t, 158, 161t, 453t, 534t; in bays and estuaries, 126t, 128f, 132f; larval stages of, 292, 294f, 298, 300, 303, 304f Lepidopsetta bilineata (rock sole), 17t, 22t, 605 Lepidopus caudatus, 523t Lepidopus fitchi (Pacific scabbardfish), 7t, 19t, 23t Lepomis macrochirus (bluegill sunfish), 487 Lepophidium microlepis (finescale cusk-eel), 177t, 183f, 196f Lepophidium stigmatisium (Mexican cusk-eel), 177t, 182f, 195f Leptocephalus giganteus (eel), 307, 310f Leptocottus armatus (staghorn sculpin), 18t, 209t, 500t, 532t, 613; in bays and estuaries, 93f, 126t, 128f, 129f, 132f, 134f, 138t, 143f; on continental shelf, 178t, 181f, 194f; in surf zone, 150, 153t, 155t, 157t; trophic relations and, 396f, 402 Leptoscarus vaigiensis, 522t Lestidiops ringens (slender barracudina), 277, 280, 351t, 355f, 370f Lestidium pseu. sphyraenoides, 519t Lethops connectens (goby), 18t, 23t, 418 Lethrinus miniatus, 521t Leuresthes tenuis/sardina (grunion), 19t, 73, 145t, 149, 233t, 621; fisheries and, 567, 568, 589; genetic characteristics of, 43, 44f, 45t, 46t, 623; larval forms of, 303; movement of, 532t, 543, 549; reproduc-

648

INDEX

tion and, 494, 495f, 520t; respiration in, 211; in surf zone, 95f, 150t, 151f Leuroglossus stilbius (California smoothtongue), 349t, 354, 355f, 360t, 368, 370f; larval stages of, 275, 276t, 277t, 278f, 292; swimbladder of, 365, 366t; trophic relations of, 402f, 406 LIDAR (light detection and ranging) systems, 527–28 Light, T., 618 lightfishes (Phosichthyidae), 350t Limbaugh, Conrad, 227, 243, 555 limpet (Collisella limatula), 220 lingcod. See Ophiodon elongata Link, J. S., 197 Linphryne coronata, 520t Liopropoma spp., 307, 308f Liparis spp. (snailfishes), 175, 178t, 180t, 353t; L. florae (tidepool snailfish), 17t, 90f, 215t, 216f, 238f; L. fucensis, 17t, 521t; L. mucosus (slimy snailfish), 18t, 151, 153t; L. pulchellus (showy snailfish), 17t, 178t, 194f; L. rutteri, 17t; reproduction and, 485, 486 Lipolagus ochotensis (popeye blacksmelt), 349t lithodid crabs, 486 Lithognathus mormyrus, 521t lizardfishes. See Synodontidae Lobianchia gemellarii (Cocco’s lanternfish), 351t Lobotes pacificus (Pacific tripletail), 7t, 20t, 25t Lobotes surinamensis, 521t locomotion, 321–23. See also movement Loligo opalescens (market squid), 406 Lomolino, M. V., 621 Long, J. A., 56 longfin dragonfish (Tactostoma macropus), 351t, 359, 370f longfin lanternfish (Diogenichthys atlanticus), 351t, 370f; larval stages of, 276t, 277f, 279, 282f, 290f, 368 longfin pearleye (Benthalbella linguidens), 351t longfin sanddab. See Citharichthys xanthostigma longfin sculpin (Jordania zonope), 17t, 21t, 211, 234t, 238f, 500t longfin smelt (Spirinchus thaleichthys), 17t, 126t, 128–29, 128f, 130t, 138t Longhurst, A. R., 588 longjaw bigscale (Scopeloberyx robustus), 352t, 365, 366t longjaw mudsucker (Gillichthys mirabilis) 11, 19t, 88, 211, 533t, 617; in bays and estuaries, 93f, 126t, 129f, 132f, 134f, 136t, 138t, 143f; hypoxia and, 472; larval stages of, 303, 304f; phylogenetic relations and, 35t, 43, 44f, 45t, 46t; trophic relations and, 396f, 402 longnose butterfyfish (Forcipiger flavissimus), 63 longnose cat shark (Apristurus kampae), 353t, 372f longnose lancetfish (Alepisaurus ferox), 327f, 330, 519t longnose puffer (Sphoeroides lobatus), 7t, 20t, 25t longnose skate (Raja rhina), 18t, 101f, 177t, 184, 185f, 197f longspine combfish. See Zaniolepis latipinnis longspine thornyhead (Sebastolobus altivelis), 19t, 23t, 96, 101f, 311f, 334f; in bathpelagic zone, 353t, 369, 371, 372f; movement of, 537t, 540, 541 loosetooth parrotfish (Nicholsina denticulata), 7t, 14, 20t, 25t, 235t Lophiocharon trisignatus, 520t Lophiodes spilurus, 308f Lophiomus setigerus, 520t Lophotus spp.: L. capellei, 20t, 24t; L. cristatus (highbrow crestfish), 327f, 332; L. lacepede, 519t

Los Angeles-Long Beach harbor, 158–62 Los Angeles Region (LAR), 40 Losey, G. S., Jr., 489, 493, 555 Los Penasquitos Lagoon, 144f lottery hypothesis of recruitment, 414–15 louvar, 326f, 337t Love, Milton S., 263, 579–80, 591, 631 lowcrest hatchetfish (Argyropelecus sladeni), 350t, 354, 356f, 366t; trophic relations of, 402f Lowe, Christopher G., 524, 539, 540 Loweina laurae, 370f Loweina rara, 308f low relief substratum, 539–40 Luacania parva (rainwater killifish), 130, 131, 134f, 612t, 614 Lumpenus sagitta, 17t lumptail sea robin (Prionotus stephenophrys), 20t, 22t, 178t, 181f, 182f, 183f; foraging guild, 194f, 195f, 196f Lutjanus spp., 309f, 521t Luvarus imperialis, 20t, 523t Lycenchelys crotalinus (snakehead eelpout), 17t, 22t, 354t Lycodapus fierasfer (black mouth eelpout), 17t, 22t, 354t Lycodapus mandibularis (pallid eelpout), 17t, 21t, 352t Lycodes spp. (eelpouts): L. cortezianus (bigfin eelpout), 18t, 22t, 179t, 184, 185f, 197f; L. diapterus (black eelpout), 17t, 22t, 354t; L. pacificus (blackbelly eelpout), 18t, 98f, 179t, 183f, 192f, 196f, 538t Lycodopsis pacificus, 522t Lyconectes aleutensis, 17t, 21t Lyconema barbatum (bearded eelpout), 18t, 22t, 179t, 183f, 185f; foraging guild, 196f, 197f Lynn, R. J., 540, 542 Lyopsetta exilis (slender sole), 18t, 403, 535t; on continental shelf, 98f, 173, 179t, 183f, 185f; foraging guild, 192f, 196f, 197f; larval stages of, 279, 296f; pollutant concentrations in, 601, 602f Lysmata californica (cleaner shrimp), 555 Lythrypnus dalli (bluebanded goby), 19t, 23t, 61f, 92f, 236t; activity patterns of, 534t, 545; in kelp bed/rocky reef, 236t, 238f, 247; phylogenetic characteristics of, 43, 44f, 45t, 46t, 49, 623; predation and, 431–32f, 434–37, 438, 439–42, 460–61; recruitment of, 419–20, 422; reproduction and, 487; symbiotic relations of, 555, 556f, 557t Lythrypnus spp. (gobies), 295f, 503, 523t; reproduction and, 487, 497 Lythrypnus zebra (zebra goby), 19t, 23t, 92t, 487; activity patterns of, 534t, 545; in kelp bed/rocky reef, 236t, 238f MacArthur, R. H., 46 MacGinitie, G. E. and N. MacGinitie, 559 machete (Elops affinis), 7t, 20t, 518 mackerel. See Trachurus symmetricus macroalgae, 437–38, 474. See also algae Macrocystis pyrifera (giant kelp), 48, 67, 71f, 415, 421, 459, 477; predation and, 436, 438–39 Macrocystis spp. (kelp), 228, 241, 243–46, 404–5, 628f. See also kelp bed/rocky reef (KBRF) macrophyte substratum, 111–12, 111f Macropinna microstoma (barreleye), 349t Macroramphosus gracilis (slender snipefish), 20t, 25t, 332, 520t Macrouridae (grenadiers), 101f, 106t, 579; bathopelagic, 353t, 369, 372–77, 390; on continental shelf, 175, 177t, 180t. See also Coryphaenoides spp.; Nezumia spp.

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Magnuson Act (1976), 578–79, 588 Magnuson-Stevens Act (1996), 588, 591 Makaira spp. (marlin), 542, 576; M. indica (black marlin), 20t, 25t, 323, 333; M. mazana, 20t, 25t; M. nigricans (blue marlin), 332; Tetrapterus audax (striped marlin), 21t, 24t, 89f, 326f, 332, 337t, 395, 401f Malacocephalus laevis (softhead grenadier), 369 Malacoctenus hubbsi, 522t Malibu Creek Estuary, 129f Man-of-War fish (Nomeus gronovii), 324, 328f, 333 Mansueti, R. J., 558 Manta spp., 337t; M. birostris, 20t, 25t, 333, 518t Mantua, N. J., 15 Margulies, D., 274 Marine Life Management Act (1998), 589, 591 Marine Life Protection Act (1999), 589, 591 mark and recapture, 525–26; and tagging, 527, 539 marlins. See Makaira spp. (marlin) Marshall, N. J., 344, 367 Martell, S. J. D., 229 masked prickleback (Ernogrammus walkeri), 7t, 17t, 24t Matarese, A. C., 306 Matern, S. A., 131, 140, 141–42, 618 mating systems, 489, 495–98, 506. See also reproduction matrotrophy, 484, 499–500 Matsui, T., 373 Matthews, K. R., 527, 539, 542 McEvoy, A. F., 587 McFarlane, G. A., 306 McGowen, J. S., 291, 292, 294, 295, 298 McLusky, D. S., 119 Mearns, A. J., 628 Medialuna californiensis (halfmoon), 19t, 35t, 92f, 157t, 162t, 400f; activity patterns of, 534t, 544; as herbivore, 65, 66f, 74, 394, 404; in kelp bed/rocky reef, 235t, 237f, 239f, 241f; symbiotic relations and, 556f, 557t, 558 medusafish (Icichthys lockingtoni), 18t, 22t, 328f, 330, 559; larval stages of, 276, 277–78f, 279, 284, 286f Meffert, D. J., 135 Megachasma pelagios (megamouth shark), 327f, 528, 529f Megalops atlanticus, 518t Melamphaes spp. (bigscales), 279f, 280, 352t, 359; M. acanthomus (slender bigscale), 352t; M. lugubris (highsnout bigscale), 277, 308f, 352t, 358f; M. parvus (little bigscale), 277, 352t Melanocetus johnsonii, 520t Melanonus zugmayeri, 519t Melanostigma pammelas (eelpout), 18t, 22t, 348, 352t Melichthys niger, 20t, 25t Menidia beryllina (inland silverside), 612t, 616, 619 Mensinger, A. F., 358 Menticirrhus undulatus (corbina), 19t, 95f, 136t, 149, 293, 536t; commercial fishing of, 587; in harbors, 157t, 158t, 160–61t; larval stages of, 293, 295f; pollutants and, 600; in surf zone, 150t, 151 Mentodus facilis (tubeshoulder), 350t mercury pollution, 598, 601 Merluccius spp. (hakes), 106t, 177t, 180t, 621; M. angustimanus (Panama hake), 177t, 197f

Merluccius productus (Pacific hake), 19t, 305, 403, 519t, 624; and commercial fishing, 578–79; on continental shelf, 177t, 182f, 183f, 185f; as deep sea species, 336t, 337t, 353t; foraging guild, 195f, 196f, 197f; habitat for, 101f, 102, 105t; larval stages of, 275, 276t, 277f, 278f, 305 mesopelagic fishes, 343, 345t, 346, 348, 359, 364, 368, 406 mesopelagic zone, 320, 321f, 342, 343, 348 Metridium farcimen (anemones), 220, 606 Mexican barracuda (Sphyraena ensis), 7t, 20t, 25t, 236t Mexican cusk-eel (Lepophidium stigmatisium), 177t, 182f, 195f Mexican flashlight fish (Phthanophaneron harveyi), 520t, 558f Mexican goby (Bathygobius ramosus), 211 Mexican hogfish (Bodianus diplotaenia), 235t Mexican lampfish. See Triphoturus mexicanus Mexican lookdown (Selene berevoortii), 7t, 20t, 308f Mexican Province, 3, 4f. See also Baja California Mexican rockfish (Sebastes macdonaldi), 19t, 24t, 44f, 45t, 46t, 258t Microgradus proximus (Pacific tomcod), 17t, 128f, 153t, 296f; on continental shelf, 174, 177t, 181t, 182f, 183f; foraging guild, 194f, 195f microhabitats, in rocky intertidal zone, 208 Micrometrus aurora (reef perch), 18t, 90f, 235t; feeding of, 394, 399f, 403; in rocky intertidal zone, 213, 215t, 216f, 220f Micrometrus minimus (dwarf perch), 18t, 77, 111f, 145t, 161t, 213, 235t, 499, 533t; in surf zone, 95f, 150t, 151f, 152, 154f, 155t Microstoma spp., 306 Microstomus pacificus (Dover sole), 19t, 96, 188, 307, 523t, 535t; as bathopelagic species, 354t, 369; commercial fisheries and, 574, 576; on continental shelf, 172, 179t, 182f, 183f, 185f; fin erosion disease, 603–4; foraging guild, 192f, 195f, 196f, 197f; habitat of, 101f, 103, 105t; in pelagic zone, 333, 334t; phylogenetics of, 33, 34t; pollutants and, 598, 600, 605 mid-depth reef (MDR), 99f, 100f mid-depth rocky reef (MDRF), 85t, 86f, 104t middle shelf (MS), 85t, 86f, 104t, 109, 176, 258t midshipman. See Porichthys spp. midwater eelpout, 355f migration, 48–49, 322, 361, 530, 615; in bays and estuaries, 124, 128f, 132f, 134f; coastal pelagics, 89f, 187–88; crepuscular, 546; spatial patterns and, 541–43. See also movement milk fish (Chanos chanos), 519t, 612t, 618 Miller, D. J., 6, 245–46, 253, 483, 539, 542 mimic sanddab (Citharichthys gordae), 179, 183f, 193, 196f Mirounga angustirostris (elephant seals), 530, 542, 561 mitochondrial control region (MtCR), 27 Mobula japanica, 20t, 24t mojarras (Gerreidae), 175, 180t, 506; spotfin mojarra, 178t, 181f, 182f, 194f, 195f Mola mola (ocean sunfish), 20t, 77, 89f, 523t, 540, 556; in pelagic zone, 326f, 330, 336, 337t molecular clocks, 28–29, 49 monkeyface prickleback. See Cebidichthys violaceus Monocentridae (pinecone fishes), 66

monogamy, 496–98, 503 moray eel. See Gymnothorax mordax Moridae (codlings), 175, 177t, 180t Morita, T., 375 Morone saxatilis (striped bass), 18t, 88, 149–50, 390, 470, 521t; as alien species, 612t, 613f, 615, 618; in bays and estuaries, 93f, 126t, 128f, 130t, 131, 138t; fisheries and, 585t, 587; pollutants and, 598, 600, 602; reproduction of, 497; trophic relations and, 395f, 402 Morro Bay, 131, 133 Moser, H. G., 6, 273, 298, 305, 308, 368–69 mosquitofish (Gambusia affinis), 126t, 132f, 535t, 612t, 616–17 mosshead sculpin (Clinocottus globiceps), 216f, 220, 390, 500t; feeding of, 390, 392, 403 mosshead warbonnet, 91f, 238f mottled sculpin (Cottus bairdi), 501 movement and activity patterns, 187, 524–49; circa patterns, 548–49; dielrelated, 543; fishing and, 525–26; genetic markers and, 530; home ranging and, 530–31; LIDAR and, 527–28; migration and, 541–43; ontogenetic-related, 541; in open ocean, 540; remote sensing techniques and, 527–30; in rockfish, 531, 539–40; seasonal, 541–42; in situ monitoring of, 526–27; sonar and, 527–28; spatial patterns, 530–31, 539–43; telemetry and, 527–30, 539; tide-related, 542–43. See also migration Moyle, Peter B., 611, 616, 618; on bay and estuarine species, 123, 125, 130, 131 Moynihan, M., 561 Mozambique tilapia (Oreochromis mossambica), 485, 612t, 617 Muench, K. A., 494 Mugil cephalus (striped mullet), 20t, 157t, 158t, 520t, 534t; in bays and estuaries, 95f, 126t, 129f, 134f, 145t, 398; as brephoepipelagic fish, 333, 334f; feeding and trophic relations, 390, 394, 396f Mugillidae (mullets), 329, 470, 472f Mullidae (goatfishes), 7t, 135t, 329, 506 Mulligan, T. J. and H. L. Mulligan, 151 Mullin, M., 305 Mulloidichthys dentatus (Mexican goatfish), 235t mummichog (Fundulus heteroclitus), 139, 470, 520t Munehara, H., 489, 507 mussel blenny (Hypsoblennius jenkinsi), 19t, 92f, 136f, 238f, 247; movement patterns of, 531, 532t; phylogenetic characteristics of, 43, 44f, 45t, 46t; territoriality of, 451, 453t mussel (Mytilus californianus), 221, 555 Mustelus californicus (gray smoothhound), 19t, 95f, 127t, 132f, 233t; in surf zone, 150t, 151, 153, 156f, 157t, 158t Mustelus henlei (brown smoothhound), 19t, 95f, 127t, 128f, 233t; in surf zone, 153, 156f, 157t, 158t Mustelus lunulatus, 20t mutualism, 554–58. See also symbiotic relationships Mycteroperca spp. (grouper): M. jordani (gulf grouper), 19t, 25t, 234t; M. xenarcha (broomtail grouper), 20t, 23t, 58, 234t Myctophidae (lanternfish), 306, 329, 406, 557–58; deep sea species, 356, 358, 359, 368, 370f; larval stages of, 276–80; swimbladders of, 366t, 367–68 Myctophum aurolaternatum (golden lanternfish), 307, 310f, 370f

INDEX

649

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Myers, J. M., 31 Myliobatis californica (bat ray), 19t, 95f, 233t, 337t, 429, 518t, 535t; in bays and estuaries, 127t, 128f, 132f, 134f, 137f; feeding of, 394; and subsistence fishing, 568; in surf zone, 150t, 153, 156f, 157t, 158t, 160t Myoxocephalus polyacanthocephalus, 500t Myrberg, A. A., Jr., 489 Myripristis amaena, 520t Myrophis vafer, 20t, 25t Mytillus californianus (mussels), 221, 555 Myxine circifons, 20t, 25t Myxinidae (hagfishes), 103, 106t, 353t, 578–79; Eptatreus deani (black hagfish), 18t, 101f, 353t, 372f Nakano, K., 207 nakedbelly sea robin (Bellator gymnostetus), 178t, 183f, 196f naked goby (Gobiosoma bosc), 469 Nannobrachium ritteri (broadfin lampfish), 351t, 356, 357f, 359, 368, 370f; larval stages of, 276t, 277f, 279, 280, 305; swimbladder of, 366t, 367; trophic relations of, 402f Nannobrachium spp. (lampfishes), 276t, 279f, 309f, 369; N. regale (pinpoint lanternfish), 351t, 358, 365, 366t, 370f Nansenia crassa, 519t Naples Reef, 455, 456, 458f, 474f, 476, 546–47 Narcine brasiliensis, 518t National Marine Fisheries Service (NMFS), 230, 336, 589; continental shelf species and, 168, 169, 170, 171, 172, 175 Natural History Museum of Los Angeles County (LACM), 275 Naucrates ductor (pilotfish), 20t, 23t, 324, 328t Naumann, E., 306 Nautichthys oculofasciatus (sailfin sculpin), 17t, 91f, 234t, 238f, 500t Navarro River Estuary, 129f nearshore (NS) habitat, 94–96, 94f, 95f nearshore soft bottom (NSB), 95f, 96, 97f, 157t, 158t needlefishes (Belonidae), 73, 135t Neighbors, Margaret A., 6, 367 Nelson, D. R., 528, 544 Nelson, J. S., 55, 61, 73, 77 Nematistius pectoralis, 20t, 25t, 521t Nemichthyidae, 354 Nemichthys scolopaceus (slender snipe eel), 349t, 519t Nemipterus virgatus, 522t Neocirrhites armatus, 522t Neoclinus spp. (fringeheads): N. blanchardi, 18t; N. stephensae (yellowfin fringehead), 19t, 23t, 236t, 238f, 247; N. uninotatus, 18t Neogloboquadrrina pachyderma (left-coiling foram), 36 Neoscopelidae (blackchins), 358 Neotrypaea biffari (ghost shrimp), 559, 560f Neotrypaea californiensis (pink ghost shrimp), 559 Nereocystis luetkeana (bull kelp), 228, 243, 245–46 neuromasts, 343, 359 Newell, N. D., 57 Newport Bay, 135, 162, 164f Nezumia spp. (grenadiers): N. kensmithi (bluntnose grenadier), 353t; N. liolepsis (smooth grenadier), 353t, 369; N. stelgidolepsis (California grenadier), 18t, 23t, 177t, 184, 185f, 197f, 353t, 369

650

INDEX

niche overlap, competition and, 451, 452f, 456, 457, 458f Nicholsina spp. (parrotfish), 522t; N. denticulata (loosetooth parrotfish), 7t, 14, 20t, 25t, 235t Nicol, J. A. C., 73 Nielsen, J. L., 31 night smelt (Spirinchus starksi), 17t, 72, 151, 152f, 153t, 335; on continental shelf, 177, 181f, 194f Nile tilapia (Oreochromis niloticus), 393 nocturnality, 66–68, 94, 95f, 156f, 188, 189, 433f; movement patterns and, 543, 548 Nomeus gronovii (Man-of-War fish), 324, 328f, 333 non-bay species, 8, 11f, 12f nonmetric multidimensional scaling (NMDS), 144f Norris, K. S., 414, 419 northern anchovy. See Engraulis mordax northern clingfish (Gobiesox maeandricus), 18t, 33, 34t, 90f, 238f, 523t; in rocky intertidal zone, 209, 215t, 216f, 220f, 221; trophic relations and, 399f, 403 northern lampfish. See Stenobrachius leucopsarus northern pearleye (Benthalbella denatata), 351t, 370f Norton, S. F., 219–20, 223, 407 notacanthiforms, 307 Notorhynchus spp.: N. cepedianus, 518t; N. cepedianus (sevengill shark), 19t, 233t; N. valdiviae (topside lampfish), 351t, 370f nuclear power plant effects, 270 nursery, bays and estuaries as, 142–43, 303–5, 468. See also ichthyoplankton assemblages oarfish, 327f, 337t Occella vernicosa, 17t oceanic puffer (Lagocephalus lagocephalus), 20t, 23t, 332 ocean sunfish (Mola mola), 20t, 77, 89f, 523t, 540, 556; in pelagic zone, 326f, 330, 332, 336 ocean surface warming, 5, 6, 242, 257. See also temperature of water ocean whitefish (Caulolatilus princeps), 20t, 22t, 35t, 87, 311f, 521t; in kelp bed/rocky reef, 92f, 234, 237f, 239f; and recreational fishing, 586 Odontaspis ferox, 19t, 25t Odontaspis taurus, 518t Odontopyxis trispinosa (pygmy poacher), 18t, 178t, 182f, 192f, 195f oilfish (Ruvettus pretiosus), 20t, 24t, 327f, 332 oil spills, 595, 596 olfaction, 343 Oligocottus spp. (sculpins), 500; O. rimensis (saddleback sculpin), 17t, 21t, 90f, 209t, 215t, 216f, 399f Oligocottus maculosus (tidepool sculpin), 17t, 91f, 500t, 507, 533t; in rocky intertidal zone, 207, 209t, 215t, 216f, 217f, 218 Oligocottus rubellio (rosy sculpin), 17t, 23t, 90f, 234t, 238f, 399f; in rocky intertidal zone, 215t, 216f, 217f, 220f Oligocottus snyderi (fluffy sculpin), 18t, 90f, 399f, 500t; in rocky intertidal zone, 209t, 215t, 216f, 217f, 218, 220f Oligoplites saurus, 24t Oligopus diagrammus, 20t olive rockfish (Sebastes serranoides), 18t, 60f, 91f, 162t, 219t; in kelp bed/rocky reef, 234t, 237f, 240f, 243f; movement and activity of, 537t, 548; and recreational

fishing, 584, 585t, 590; trophic relations and, 400f, 405 Oncorhynchus kisutch (coho salmon), 18t, 30t, 31, 32, 88, 233t, 330, 331f, 487; in bays and estuaries, 126t, 128f, 130t Oncorhynchus mykiss (steelhead), 18t, 30t, 31, 32, 618; in bays and estuaries, 126t, 128f, 129f, 130t, 132f Oncorhynchus spp. (anadromous trout), 393; O. clarkii (cutthroat trout), 17t, 21t, 29, 130t; O. gorbusha (pink salmon), 17t, 22t, 130t; O. keta (chum salmon), 17t, 21t, 130t, 233t; O. nerka (sockeye salmon), 17t, 21t, 519t, 624–25, 626f Oncorhynchus tshawytscha (chinook salmon), 17t, 153t, 233t, 330, 331f, 630; in bays and estuaries, 93f, 126t, 128f, 130t, 131; fisheries and, 569, 579, 585t, 589, 628; phylogeography and, 30t, 31–32, 32t, 39 Oneirodes spp. (dreamers), 17t, 352t, 395, 402t; O. acanthias (spiny dreamer), 352t, 358, 390, 520t; O. eschrichtii (bulbous dreamer), 352t onespot fringehead, 97f Onuf, C. P., 140, 141 oophagy, 484 opah (Lampris regius), 89f, 321, 327f, 330, 337t opaleye (Girella nigricans), 19t, 102, 105t, 136t, 150t, 534, 585t; activity patterns of, 544–45; in harbors, 157t, 158t, 162t; as herbivore, 65, 66f, 74, 394, 400f, 403, 404; in kelp bed/rocky reef, 92f, 235t, 237f, 239f, 241f; mutualism of, 556f, 557t, 558; phylogenetic characteristics of, 35t, 41, 43, 44f, 45t, 46t; recruitment of, 414, 419; in rocky intertidal zone, 209t, 215t, 216f open ocean pelagics. See pelagic zone Ophichthus spp.: O. rufus, 518t; O. triserialis, 20t; O. zophochir, 20t Ophiclinus spp., 522t Ophididae (cusk-eels), 106, 177t, 180t, 197f, 353t, 369; Lepophidium spp., 177t, 182f, 183f, 195f, 196f; movement and activity of, 535t, 544. See also Chilara taylori Ophidion barbatum, 519t Ophidion scrippsae (basketweave cusk-eel), 18t, 163, 177t, 535t, 603; foraging guild, 194f, 195f; larval stages of, 277t, 280f, 293, 295f, 297f, 298 Ophioblennius steindachneri (Panamic fanged blenny), 236t Ophiodon elongatus (lingcod), 18t, 100f, 103, 105t, 129f, 132f, 485; as ambusher, 59f; as brephoepelagic fish, 333, 334f; climate change and, 624, 631; on continental shelf, 178t, 181f, 182f, 183f; in deep rock habitat, 262f, 263t; fisheries and, 574, 576, 579, 589, 591; foraging guild, 194f, 195f; in kelp bed/rocky reef, 234t, 237f, 240f; larval stages of, 270, 295, 297f; and subsistence fishing, 568 Ophiopthalmus normani (brittle star), 371, 540 Opisthonema libertate, 519t Opisthoproctidae (spookfishes), 349t, 519t Opistognathus spp. (jawfish), 485, 521t orange roughy (Hoplostethus atlanticus), 66, 520t orangethroat pikeblenny (Chaenopsis alepidota), 19t, 24t, 137f; phylogenetic characteristics of, 43, 44f, 45t, 46t Orbach, M. K., 590 Oregonian Province, 3, 4f, 239 Oreochromis mossambicus (Mozambique tilapia), 485, 612t, 617

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Oreochromis niloticus (Nile tilapia), 393 Orthodon microlepidotus (Sacramento blackfish), 393 Orthonopias triacis (snubnose sculpin), 18t, 23t, 60, 91f, 234t, 238t, 533t Orthopristis reddingi (bronzestripe grunt), 178t, 181f, 182f, 194f, 195f Osborn, T. R., 309 Osmeridae (true smelts), 72, 73, 77, 120, 128–29, 149; on continental shelf and slope, 175, 177t, 180t; larval stages of, 296, 304f osmoregulation, 212 Ostracion meleagris, 523t otter (Enhydra lutris), 624, 627, 628 otter trawl, 575 outer shelf (OS), 85t, 86f, 109, 176, 179–80; analysis of, 104t; trophic relations and, 398f oval flounder (Syacium ovale), 179t, 194f overfishing, 567, 572, 573, 576, 580, 588; climate change and, 625–26, 627, 633. See also fishing and fisheries oviparity (egg laying), 483–84, 486–87, 499; egg size and, 500–501 oxygen depletion. See hypoxia Oxyjulis californica (señorita), 18t, 58, 105t, 136t, 259, 522t; activity patterns of, 534t, 544, 546, 548; cleaner behavior of, 555, 556f, 557t; feeding of, 65, 389, 390, 400f; in harbors, 159, 162t; in kelp bed/rocky reef, 87, 92f, 235t, 237f, 239f, 240f, 241f, 404–5; larval stages of, 293, 295f; macrophyte substratum and, 111; predation and, 431f, 436; reproduction and, 497, 498 Oxylebius pictus (painted greenling), 18t, 162t, 295, 420, 521t, 538t; in deep rock habitat, 258, 263t; in kelp bed/rocky reef, 70, 71f, 91f, 234t, 237f, 238f, 404; phylogeography and, 33, 34t, 38, 38f; reproduction and, 489, 490, 492f, 495, 496, 501; symbiotic relations of, 560–61, 561f; trophic relations and, 400f Oxymonacanthus longirostris, 523t Pacific argentine (Argentina sialis), 19t, 22t, 100f, 177t, 182f, 195f, 519t Pacific baracuda. See Sphyraena argentea Pacific blackchin (Scopelengys tristis), 351t, 357f, 358, 366t Pacific blackdragon (Idiacanthus antrostomus), 307, 310f, 351t, 356, 357f, 366t, 370f Pacific blacksmelt (Bathylagus pacificus), 310, 349t, 354, 355f, 370f; swimbladder of, 365, 366t Pacific bonito. See Sarda chiliensis Pacific butterfish, 337t Pacific cod (Gadus macrocephalus), 17t, 21t, 605 Pacific crevalle jack (Caranx caninus), 7t, 20t, 25t Pacific Decadal Oscillations. See PDO Pacific dreamer. See spiny dreamer (Oneirodes acanthias) Pacific electric ray (Torpedo californica), 18t, 95f, 156f, 233t, 348, 405, 518; on continental shelf, 177t, 183f, 196f; hunting behavior of, 433f; movement of, 538t, 540, 542, 549; in pelagic zone, 335, 337t Pacific Fisheries Management Council (PFMC), 588, 589 Pacific flatnose (Antimora microlepsis), 18t, 21t, 353t, 372f Pacific grenadier (Coryphaenoides acrolepis), 18t, 22t, 353t, 369, 372f, 373, 374 Pacific hake. See Merluccius productus

Pacific halibut (Hippoglossus stenolepsis), 17t, 525, 580 Pacific herring. See Clupea pallasi Pacific lamprey (Lampetra tridentata), 18t, 518t, 561–62, 561f Pacific lightfish (Vinciguerria lucetia), 305, 350t, 368, 370f; larval stages of, 276t, 277f, 279f, 280, 282f, 286, 292f Pacific line sole (Achirus mazatlanus), 137f, 179t, 181f, 194f, 307, 523t Pacific mackerel. See Scomber japonicus Pacific pomfret, 326f, 337t. See also Taractes longipinnis Pacific pompano (Peprilus simillimus), 19t, 91, 94f, 103, 305; feeding of, 393; in harbors, 159f, 160–61t; in pelagic zone, 156, 330, 332f Pacific porgy (Calamus brachysomus), 20, 137f, 235t Pacific sanddab. See Citharichthys sordidus Pacific sand lance (Ammodytes hexapterus), 17t, 75, 153t, 296f, 494–95, 522t Pacific sand perch (Diplectrum pacificum), 178t, 181f, 194f, 521t Pacific sardine. See Sardinops sagax Pacific saury (Cololabis saira), 326f, 330, 335, 336t, 401f, 405 Pacific scabbardfish (Lepidopus fitchi), 7t, 19t, 23t Pacific seahorse (Hippocampus ingens), 20t, 25t, 135t, 137f, 484 Pacific sleeper shark (Somniosus pacificus), 17t, 21t, 353t, 518t Pacific tomcod (Microgradus proximus), 17t, 128f, 153t, 181t, 296f; on continental shelf, 174, 177t, 181t, 182f, 183f; foraging guild, 194f, 195f Pacific Transition Conception, 40, 240 Pacific tripletail (Lobotes pacificus), 7t, 20t, 25t Pacific viperfish (Chauliodus macouni), 351t, 356, 357f, 365, 366t, 370f; trophic relations, 395, 402f, 406 Paine, R. T., 442, 554 painted greenling. See Oxylebius pictus pallid eelpout (Lycodapus mandibularis), 17t, 21t, 352t Pallisina barbata (tubenose poacher), 17t, 153t Palos Verdes, 244, 249, 630 Palos Verdes Shelf: fin erosion disease in, 603, 604f, 607f; pollution in, 596, 598, 600, 601, 607–8 Panama hake (Merluccius angustimanus), 177t, 197f Panama lightfish. See Pacific lightfish (Vinciguerria lucetia) Panama snaggletooth (Borostomias panamensis), 351t, 357f, 366t Panamic fanged blennie (Ophioblennius steindachneri), 236t Panamic Province, 3, 4f Panamic sergeant major (Abudefduf troschelli), 92f, 235t, 237f, 241f Pangea, breakup of, 621, 622f paperbone cusk-eel (Lamprogrammus niger), 353t Paraclinus integripinnis (reef finspot), 19t, 92f, 236t, 403, 534t, 628; in bays and estuaries, 136t, 137f; hypoxia and, 468; in rocky intertidal zone, 211, 215t, 216f, 222f Paralabrax spp. (sand bass), 395, 506; larval stages, 293, 295f, 298, 300, 301–2; P. auroguttatus (golden spotted rock bass), 234t, 497; P. humeralis, 497 Paralabrax clathratus (kelp bass), 19t, 35t, 58, 111f, 260, 506, 521t; in bays and estuar-

ies, 136t, 137f, 145t; commercial fishing of, 576, 591; ENSO and, 631; feeding of, 395; growth of, 62; habitat range of, 92f, 102, 103, 105t; in harbors, 157t, 159, 162t; in kelp bed/rocky reef, 234t, 237f, 239f, 241f; movement and activity patterns of, 525, 526f, 531, 537t, 539, 545, 549; pollution and, 600, 605; predation and, 430, 431f, 437, 438–39, 441, 444; recreational fishing of, 581, 584, 585t, 586; recruitment of, 414, 418, 419, 421; reproduction and, 497; storm disturbance and, 477, 478f; subsistence fishing and, 568; in surf zone, 152, 154f, 155t; symbiotic relationships of, 555, 556f, 557t; trophic relations and, 395, 400f, 405 Paralabrax maculatofasciatus (spotted sand bass), 19t, 111f, 506, 521t, 538t, 591, 631; in bays and estuaries, 95f, 126t, 134f, 136t, 137f, 145t; on continental shelf, 178t, 181f, 194f; phylogenetic characteristics of, 43, 44f, 45t, 46t; trophic relations and, 395, 396f, 402 Paralabrax nebulifer (barred sand bass), 19t, 92f, 102, 103, 105t, 111f, 506, 631; in bays and estuaries, 127t, 136t, 137f, 145t; on continental shelf, 178t, 181f, 194f; fisheries and, 576, 582, 584, 585t, 591; in harbors, 157t, 160t, 162t; in kelp bed/rocky reef, 234t, 237f, 239f, 241f; movement of, 531, 538t; predation and, 431; reproduction and, 497; trophic relations and, 395, 397f Paralepididae (barracudinas), 279f, 351t Paralichthyidae (lefteye flounders), 70, 71, 106t, 236t, 289, 301, 535t; on continental shelf, 172, 176, 179t, 180t, 184. See also Citharichthys spp. Paralichthys californicus (California halibut), 19t, 34t, 95f, 160–61t, 236t, 305; ambush feeding of, 59f, 60, 395, 432; in bays and estuaries, 127t, 129f, 132f, 136t, 137f, 138t, 145t; commercial fisheries and, 573–74, 576, 579, 587, 591; on continental shelf, 172, 179t, 181f, 194f; habitat of, 102, 105t; larval stages of, 291, 294, 297f, 298, 299f; movement of, 535t, 539, 541; pollution and, 600, 606; recreational fishing and, 582, 583, 585t; recruitment of, 187, 420; in surf zone, 151–52, 153t, 154f, 155t, 157t, 158t; trophic relationships and, 396f, 397f, 402, 403 Paraliparis cephalus (swellhead snailfish), 353t Paramonacanthus japonicus, 523t Paranthias colonus (Pacific creolefish), 234t, 309f Parapercis snyderi, 522t parasitism, 486, 554, 555, 561–62, 605 parental care, 484–85, 495, 499–500, 502–4, 506; egg size and, 500, 501t; viviparity and, 484, 502, 503, 504, 507 Paricelinus hopliticus, 18t, 22t Parin, N. V., 324, 325, 329, 331, 333 Parmaturus xaniurus (filetail cat shark), 19t, 23t, 101f, 353t, 518t Parnulirus interruptus (spiny lobster), 555 Parophrys vetulus. See Pleuronectes/Parophrys vetulus Parques viola (rock croaker), 235t Parrish, J. K., 333, 573 Parrish, R. H., 76 parrotfishes (Scaridae), 394, 506; Nicholsina spp., 7t, 14, 20t, 25t, 235t, 522t

INDEX

651

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Parvilux ingens (giant lampfish), 351t, 366t, 370f patchwork lanternfish, 370f Patterson, C., 66 Patton, M. L., 240, 244 Paxton, J. R., 363 PCBs and DDT contamination, 595–603, 605, 607f. See also pollution PDO (Pacific Decadal Oscillations), 5, 15, 628–31; ichthyoplankton assemblages and, 283, 284, 285–93f, 299–302f, 303 peacock wrasse (Symphodus tinca), 502 Pearcy, William G., 270, 295, 296, 298, 361, 539 pearleyes (Benthalbella spp.), 351t, 370f, 519t Pearson product-moment correlation matrix, 6 pebbled butterflyfish (Chaetodon multicinctus), 63 Pelagia spp. (sea jellies), 328f pelagic egg, 77. See also oviparity pelagic larval duration, 33, 49 pelagic (PEL) zone, 82t, 85t, 86t, 89f, 104t, 106, 320–41; adaptations to, 321–24; boreal region, 330; brephoepipelagic fish, 325, 328–29, 333, 334; California Current system and, 333–36; epheboepipelagic fish, 325, 328, 331f; holoepipelagic fish, 324–25, 326–28f, 330t, 331; locomotor adaptations, 321–23; meroepelagic fish, 325, 328t; nyctoepipelagic fishes, 325, 329; prominent world-wide groups in, 320–21; schooling, 323–24; temperate region, 330; tropical region, 331–33; xenoepipelagic fishes, 325, 329, 330t, 332f pelagic stingray (Dasyatis violacea), 326f, 331, 337t Pelagophycus porra (elk kelp), 228 Pempheris vanicolensis, 522t penpoint gunnel (Apodichthys flavidus), 17t, 90f, 111f, 129f, 151, 153t, 485; in rocky intertidal zone, 209t, 215t, 216f, 221 Peprilus simillimus (Pacific pompano), 19t, 91, 94f, 103, 305; feeding of, 393; in harbors, 159f, 160–61t; in pelagic zone, 156, 330, 332f Pequegnat, W. E., 227, 229 perciforms, 71–72, 75, 105, 178, 306 Percoidei, 57–58, 321 Perissias taeniopterus (flag flounder), 179t, 183f, 193, 196f Perkins, H. C., 359, 361 Pescadero Creek Lagoon, 129f Peterson, C. W., 499 petrale sole (Eopsetta jordani), 18t, 179t, 182f, 183f, 185f, 193; foraging guild, 193, 195f, 196f, 197f Petromyzontidae, 561–62. See also Lampetra spp. (lamprey) Pfister, C. A., 214, 223, 421 Phanerodon atripes (sharpnose seaperch), 18t, 23t, 75, 235t, 555; cleaner behavior of, 556f, 557t Phanerodon furcatus (white seaperch), 18t, 75, 150t, 155t, 258, 631; cleaner behavior of, 556f, 557t; on continental shelf, 178t, 181f; foraging guilds, 192f, 194f; habitat range of, 92f, 102, 103, 105t, 127t, 132f; in harbors, 157t, 160–61t, 162t; in kelp bed/rocky reef, 235t, 240f; movement of, 533t, 542; reproduction of, 494; trophic relations and, 397f, 403 pheromones, 491, 493, 494 Pholis spp. (gunnels), 9f, 10f, 72, 90f, 209t, 217f; P. clemensi, 17t, 21t; P. laeta (crescent gunnel), 17t, 21t, 209t, 485, 522t;

652

INDEX

P. ornata (saddleback gunnel), 17t, 153t, 399f; P. schultzi, 17t, 21t; Ulvicola sanctaerosae (kelp gunnel), 18t, 24t, 72, 72f, 236t. See also penpoint gunnel; rockweed gunnel Phosichthyidae (lightfishes), 350t Photonectes margarita, 351t Phragmatopoma californica (tube worm), 228 Phthanophaneron harveyi (Mexican flashlight fish), 520t, 558f Phtheirichthys lineatus (slender sucker), 20t, 25t, 324 Phyllospadix spp. (surf grass), 228 phylogeny, 68, 195 phylogeography, 26–50; anadromous fishes and, 29–32; Baja California, 40–41, 44-46t; biogeography and, 9, 26; Channel Islands and, 33, 43, 47–49; characteristics of coastal fishes, 34–35t; climate change and, 36–38; comparative, 26–27; gene flow and, 27, 33, 38, 48, 49–50; glaciations and, 32–33, 36, 37, 41; Gulf of California, 41–43; pelagic larval duration and, 33; subregions, 27; tectonism and oceanographic patterns, 33, 36; zoographic barriers and, 26–27 Physalia spp.(siphonophores), 333 Physiculus rastrelliger (hundred-fathom codling), 20t, 23t, 98f, 177t, 185f, 197f; larval stages of, 309f Phytichthys chirus, 17t, 21t Pickett, S. T. A., 466 Pihl, L., 143 pile perch. See Rhacochilus vacca pilotfish (Naucrates ductor), 20t, 23t, 324, 328f pinecone fishes (Monocentridae), 66 pinfish (Lagodon rhomboids), 469, 472f pink cardinalfish (Apogon pacificus), 7t, 20t, 25t, 234t pinknose rockfish (Sebastes simulator), 18t, 24t, 100f, 255, 262f pink rockfish (Sebastes eos), 18t, 23t, 100f, 258t pink salmon (Oncorhynchus gorbusha), 17t, 22t, 130t pink seaperch (Zalembius rosaceus), 19t, 23t, 105t, 258, 263t, 533t; on continental shelf, 98f, 176, 178t, 182f, 183f; foraging guild, 192f, 195f, 196f; trophic relations and, 398f, 403 pinpoint lanternfish (Nannobrachium regale), 351t, 358, 365, 366t, 370f pipefishes. See Syngnathus spp. pipeline assemblages, 264 piscivores, 131, 330, 395, 402, 430, 435, 548; filial cannibalism, 436, 500–502. See also predators Pittenger, G. G., 540 Plagiogrammus hopkinsii (crisscross prickleback), 17t, 24t, 91f, 236t, 238f Plagiotremus azaleus (sabertooth blenny), 7t, 20t, 25t, 236t plaice (Pleuronectes platessa), 539, 604 plainfin midshipman. See Porichthys notatus planktivores, 63, 75, 131, 189, 420, 547 planktonic larval duration, 26, 27f Platichthys stellatus (starry flounder), 17t, 296f, 600, 605, 606; in bays and estuaries, 93f, 127f, 128f, 129f, 132f, 138t Platycephalus speculator, 521t Platyrhinidae (thornbacks), 175, 177t, 180t Platyrhinoides triseriatus (thornback), 18t, 97f, 157t, 158t, 233t; in pelagic zone, 177t, 181f, 194f Platytroctidae (tubeshoulders), 350t, 354, 355f, 369, 519t

Plecoglossu altivelis (ayu), 612t, 618 Plectobranchus evides, 17t, 22t Pleistocene epoch, 623, 624 Plesiops nigricans, 521t Pleurogrammus monopterygius, 17t, 21t Pleuronectes/Parophrys vetulus (English sole), 19t, 98f, 105t, 296f, 398f, 535t; in bays and estuaries, 127t, 128f, 132f; on continental shelf, 172, 179t, 181f, 182f; foraging guilds, 192f, 194f, 195f; pollutantrelated disease in, 600, 604, 605, 606; in surf zone, 152f, 153t, 155t Pleuronectes platessa (plaice), 539, 604 Pleuronectidae (righteye flounders), 9f, 10f, 70–71, 105, 106t, 535t; pelagic, 329, 333 pleuronectiforms (flatfishes), 59, 96, 307, 539; commercial fishing of, 569, 574, 575, 579; on continental shelf, 172, 179t, 180t, 184, 186, 189; larval stages of, 289, 306; movement of, 541; pollutants and, 600, 606 Pleuronichthys coenosus (C-O sole), 18t, 60, 61f, 70, 236t, 535t Pleuronichthys decurrens (curlfin sole/turbot), 18t, 98f, 398f, 535t, 606; on continental shelf, 179t, 181f; foraging guild, 192f, 194f Pleuronichthys guttulatus. See Hypsopsetta guttulata Pleuronichthys ritteri (spotted turbot), 19f, 95f, 151, 155t, 157t; on continental shelf, 179t, 181f, 182f; foraging guild, 194f, 195f; larval stages of, 292, 293, 294f, 300; pollution and, 600, 603; trophic relations and, 397f Pleuronichthys verticalis (hornyhead turbot), 19t, 98f, 294f, 398f, 535t, 606; on continental shelf, 179t, 181f, 182f; foraging guild, 192f, 193, 194f, 195f; larval stages of, 291, 299; trophic relations and, 397f, 398f Pliocene epoch, 622f, 623 Plotosus lineatus, 519t poachers, 18t, 70, 98f, 153t, 178t; bigeye poacher (Bathyagonus pentacanthus), 178t, 197f; pricklebreast poacher (Stellerina xyosterna), 18t, 152f, 153t, 296; pygmy poacher (Odontopyxis trispinosa), 18t, 178t, 182f, 192f, 195f; tubenose poacher (Pallasina barbata), 17t, 153t. See also Agonidae; Xeneretmus spp. Podothecus sachi, 521t Poecilia latipinna (sailfin molly), 612t, 613f, 616 Poeciliidae spp., 494, 616–17 Point Conception, 3, 5, 6, 75, 76 Polivka, K. M., 221 pollution, 121, 145, 595–608; bioaccumulation in fish and, 598–601; biomarkers and sublethal effects, 605–6; contamination effects, 601–8; DDT and PCBs, 595–603, 605, 607f; effects on populations and assemblages, 606–8; external disease, anomalies and parasites, 603–5; fin erosion disease and, 603, 604f; human health risk, 601–2; sediment contamination, 596, 598, 600f, 604, 607f, 608; sources of contaminants, 595–96; in water column, 596; wild-life health risk and, 602–3 polychaete worm (Cirriformia luxuriosa), 220 Polydactylus approximans, 20t, 23t Polydactylus operaculis, 20t, 25t Polydactylus sexfilis, 522t polygamy, 483, 496, 502–3 polygyny, 497

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Polylepium cruentum (bleeding wrasse), 179t, 183f, 196f Polyprion americanus (Atlantic wreckfish), 497, 521t Pomacanthus spp., 235t, 522t Pomacentridae (damselfishes), 65, 74, 76, 106t, 547; in kelp bed/rocky reef, 235t, 237f; movement patterns of, 535t, 548; reproduction and, 488, 489, 491, 493, 495, 503, 506. See also Chromis spp.; garibaldi (Hypsypops rubicundus) Pomatomus saltatrix (bluefish), 149, 521t Pomatoschistus, 498 Pommeranz, T., 305 pompano, 305. See also Pacific pompano Pondella, D. J., II, 153 Pontinus sierra, 311f popeye blacksmelt (Bathylagus ochotensis), 349t, 365, 366t, 370f; larval stages of, 276t, 277f, 368 porcupinefish (Diodon hystrix), 21t, 236t Porichthys spp. (midshipmen), 129f, 189, 557; P. analis (darkedge midshipman), 178t, 182f, 195f Porichthys myriaster (specklefin midshipman), 19t, 97f, 136t, 145t, 157t, 178t, 233t, 532t; foraging guild, 192f, 194f, 195f Porichthys notatus (plainfin midshipman), 19t, 38, 136t, 233t, 335, 520t; on continental shelf, 98f, 178t, 181f, 182f, 183f; foraging guild, 192f, 194f, 195f, 196f; migration of, 188, 532t; reproduction and, 486f, 487, 489, 491, 493; in rocky intertidal zone, 209t, 210, 213, 219t; trophic relations and, 398f, 403 Poroclinus rothrocki, 17t, 22t Poromitra crassiceps (crested bigscale), 352t, 358f, 365 Posner, M., 539 predation, 312, 323, 343, 428–45; adaptations of predators, 432–33; antipredatory adaptations, 428–32; behavioral responses to, 430–32; community structure and, 442–43; densitydependent, 438–41, 442, 444; evolutionary influences on, 428–33; extinction and, 625; filial cannibalism, 501; future research on, 444–45; group living and, 429–30; growth of prey and, 434–35; habitat structural complexity and, 441–42, 444; hatching and, 495; monogamy and, 497; mortality and, 434, 437–38; movement of, 542; pollutants and, 598; prey demography and, 434–41; recruitment and, 418, 420, 421, 435–37, 442; regional and geographic comparisons, 443–44; size-selective, 445. See also feeding divergence; trophic interactions Priacanthidae, 66 pricklebacks (Stichaeidae), 7t, 9f, 10f, 72, 186, 329; Plagiogrammus hopkinsii (crisscross prickleback), 17t, 24t, 91f, 236t, 238f; reproduction and, 498; in rocky intertidal zone, 90f, 207, 209t, 210, 213, 216f, 217f. See also monkeyface prickleback; Xiphister spp. pricklebreast poacher (Stellerina xyosterna), 18t, 152f, 153t, 296 prickly sculpin (Cottus asper), 126t, 128f, 129f, 132f, 296 Priede, I. G., 375–76, 377, 540 Prionace glauca (blue shark), 20t, 89f, 326f, 330, 337t, 389, 518t; movement of, 524, 532t, 540, 542, 543; telemetry and, 527–28; trophic relations and, 401f

Prionotus spp., 277f, 280f; P. evolans, 520t; P. ruscarius (rough sea robin), 178t, 181f, 194f Prionotus stephanophrys (lumptail sea robin), 20t, 22t, 178t, 181f, 182f, 277; foraging guild, 194f, 195f, 196f Pristigenys serrula, 20t, 24t, 311f productivity, 138–39, 249. See also reproduction Prognathodes falcifer (scythe butterflyfish), 20t, 24t, 220, 235t promiscuity, 496, 497, 503 Pronotogrammus multifasciatus (threadfin bass), 7t, 178t, 183f, 196f, 255 Proposition 132 (California), 590–91 Protomyctophum crockeri (California flashlightfish), 351t, 357f, 359, 370f; larval stages of, 276t, 277f, 279f, 280, 306; swim bladder of, 366t, 367 Psenes spp. (driftfish), 333; P. pellucidus (blackrag), 328f, 330, 559, 900 Psettichthys melanostictus (sand sole), 17t, 97f, 296f, 605; on continental shelf, 179t, 181f, 194f; in surf zone, 152f, 153t, 155t Pseudobalistes flavimarginatus, 523t Pseudobathylagus ochotensis (robust blacksmelt), 349t, 365 Pseudochromis olivaceus, 521t Pseudopeneus grandisquamis, 21t, 25t Pseudopeneus maculatus, 522t Pseudopentaceros wheeleri, 20t, 22t, 522t Psychrolutes phrictus (blob sculpin), 353t, 372f, 521t Pteraclis aesticola, 20t, 24t Pterocaesio diagramma, 521t Pteroplatytrygon violacea, 20t, 24t Pterygophora californica (brown algae), 228, 246, 437–38, 474 Ptilichthys goodei, 522t Pudget Sound sculpin (Ruscarius meanyi), 7t pudgy cuskeel (Spectrunculus grandis), 353t, 369 puffers (Tetraodontidae), 77, 137f, 149, 321, 394; Canthigaster spp., 503, 523t; Lagocephalus lagocephalus, 20t, 23t, 332. See also Sphoeroides spp. purse seines, 571, 572, 573, 575, 577, 588 pygmy poacher (Odontopyxis trispinosa), 18t, 178t, 182f, 192f, 195f pygmy rockfish (Sebastes wilsoni), 17t, 255, 259, 260f, 263t pygmy shark (Euprotomicrus bispinnatus), 17t, 331 Pyrosoma sp. (colonial salp), 328f Quammen, M. L., 140, 141 Quast, J. C., 232, 243–44, 404 queenfish. See Seriphus politus Quietula y-cauda (shadow goby), 19t, 88, 303, 534t; in bays and estuaries, 93f, 126t, 132f, 134f, 145t; trophic relations and, 396f, 401 quillback rockfish (Sebastes maliger), 17t, 21t, 255, 537t, 539, 542 quinaldine (ichthyocide), 231, 232 Rachycentron canadensis, 521t Radovich, J., 14, 628 Radulinus spp.: R. asprellus (slim sculpin), 17t, 22t, 178t, 195f; R. boleoides, 17t, 21t; R. vinculus, 17t, 24t ragfish (Icosteus aenigmaticus), 17t, 22t, 327f, 330, 523t rainbow runner (Elegatis bipinnulatus), 324 rainbow scorpionfish (Scorpaenodes xyris), 20t, 25t, 70, 234t

rainbow seaperch (Hypsurus caryi), 18t, 91f, 235t, 239f, 457; cleaner behavior of, 556f, 557t; movement of, 533t, 542, 544–45; in surf zone, 152, 155t, 162t rainbow surfperch, 240f rainbow trout, 31. See also Oncorhynchus spp. Rainwater, C. I., 364 rainwater killifish (Luacania parva), 130, 131, 134f, 612t, 614 Raja binoculata (big skate), 18t, 177t, 181f, 182f, 183f, 518t; foraging guild, 194f, 195f, 196f Raja inornata (California skate), 18t, 98f, 177t, 181f, 182f, 183f; foraging guild, 194f, 195f, 196f Raja rhina (longnose skate), 18t, 101f, 177t, 184, 185f, 197f Raja stellata, 17t, 22t Rajidae (skates), 106t, 175, 180t, 185f, 189, 353t; and commercial fisheries, 574; and reproduction, 483. See also Bathyraja spp. Ralston, S., 173, 417, 530 range end points, 12f, 14 Ranzania laevis (slender mola), 21t, 24t, 311f, 332 ratfish. See spotted ratfish (Hydrolagus colliei) Rathbunella spp. (ronquils): R. alleni, 235t; R. hypoplecta (stripedfin ronquil), 18t, 72, 72f, 522t, 532t; R. jordani (northern ronquil), 235t rays. See Batoidae (rays) Reavis, R. H., 527 recreational fishing, 567, 580–92; (18501940), 580–83; (1941-2001), 583–84; barge fishing and, 582–83, 583f, 588; competition with commercial, 589–92; fishing methods, 582, 583–84; regulation of, 586–89 recruitment, 187, 240–41, 388, 411–23, 631, 632; benthic environment and, 420–22; community structure and dynamics, 414–15; defined, 411; density-dependence and, 421–22; directions for research, 423; disturbance and, 472, 477; importance of, 411–12; larval dispersal and, 417–18; larval production and, 415–17; management and conservation in, 422–23; population structures and distribution, 413–14; predation and, 418, 420, 421, 435–37, 442; in rocky intertidal zone, 214; settlement phase of, 418–20, 435–37; spatial and temporal variation in, 415–22 redbanded rockfish (Sebastes babcocki), 18t, 22t, 255 redbelly tilapia (Tilapia zilli), 612t, 613f, 617 red brotula (Brosmophycis marginata), 18t, 186, 233t, 238f, 519t red drum (Sciaenops ocellatus), 150 red goatfish (Pseudoupeneus grandisquamosus), 135t red hake (Urophycis chuss), 472 red Irish lord (Hemilepidotus hemilepidotus), 17t, 485, 486f, 498, 500t, 521t redtail surfperch, 128f, 585t reduction fisheries, 570–74 Reebs, S., 549 reef finspot (Paraclinus intergripinnis), 19t, 92f, 236t, 238f, 403, 628; in bays and estuaries, 136t, 137t; hypoxia and, 468; in rocky intertidal zone, 211, 215t, 216f, 222f reef perch (Micrometrus aurora), 18t, 90f, 235t; feeding of, 394, 399f, 403; in rocky intertidal zone, 213, 215, 216f, 220f Regalecus glesne, 21t, 25t, 519t

INDEX

653

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Reinhardtius hippoglossoides, 17t, 22t Remilegia australis (whalesucker), 324 Remora spp., 324–25; R. albescens, 21t, 23t; R. australis, 20t, 22t; R. brachyptera (gray remora), 21t, 25t, 325; R. osteochir, 20t, 521t; R. remora, 21t, 23t, 324, 328f, 329f, 337t Remorina albescens (white suckerfish), 325 remote sensing technology, 527–30, 528f reproduction, 73, 76, 483–507; in bathopelagic fish, 368–69; behavioral ecology and, 495–502; body size and, 483, 493, 497, 498; coloration and, 488, 489, 490, 493, 494, 498; courtship and, 487–95; diel patterns of, 495, 507; evolutionary ecology and, 495–502; filial cannibalism and, 500–502; future research in, 505–7, 506t; gender allocation and, 487, 488t, 495–98, 502–4, 505f, 506; gonochorism and, 483, 497, 498, 502–3, 504, 507; hermaphroditism and, 487, 488t, 496–98, 502–3, 504, 506; hypoxia and, 471–72; life histories and, 187, 486–87; mating systems, 489, 495–99, 506; modes of, 483–86; monogamy, 496–98, 503; morphology and, 491–92; motor patterns and, 491; oviparity (egg laying) and, 483–84, 486–87, 499, 500–501; parental care and, 484, 485t, 486, 487, 495, 496, 499–500, 502–4, 506; pheromones in, 491, 493, 494; pollution and, 602; polygamy, 483, 496, 502–3; promiscuity and, 503; in rocky intertidal fishes, 213–14; seasonal, 498; sexual selection and, 498–99; in soft-bottom species, 186–87; spawning and, 488–89, 494, 495, 507, 587; spawning types, 483–86; species tables, 518–23t; sperm competition and, 499, 505, 506; temperate-tropical dichotomies in, 504; territoriality and, 489, 493, 495, 502; upwelling systems and, 503–4; viviparity, 483–84, 486, 502, 503, 504, 505, 507. See also ichthyoplankton respiration, 323; hypoxia and, 207, 210, 211; in intertidal fishes, 208, 210–12, 222 rex sole. See Glyptocephalus zachirus Rhacochilus toxotes (rubberlip seaperch), 19t, 75, 92f, 103, 494; activity patterns of, 533t, 546; competition and, 456–57, 458f; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 235t, 239f, 240f; prey dissemblance and, 64; trophic relations and, 400f, 405 Rhacochilus vacca (pile perch), 18t, 75, 92f, 111f, 260, 494; as benthivore, 65; habitat range of, 102, 103, 105t; in harbors, 157t, 159, 161t, 162t; in kelp bed/rocky reef, 235t, 239f, 240t, 243f; movement and activity patterns of, 533t, 542, 544–45; symbiotic relations of, 556f, 557t; trophic relations and, 400f, 405 Rhamphocottus richardsonii (grunt sculpins), 17t, 21t, 213, 500t, 521t Rhinobatidae (guitarfishes), 176, 177t, 180t, 183f, 189, 233t. See also Zapteryx exasperata Rhinobatis productus, 518t Rhinobatis productus (shovelnose guitarfish), 19t, 137f, 233t, 397f, 568; as nearshore soft bottom fish, 97f, 157t, 158t Rhinocodon typus (whale shark), 20t, 25t, 325, 331f, 333, 518t; movement of, 540 Rhinogobiops nicholsii (blackeye goby), 19t, 60, 61f, 76, 162t, 420, 506; habitat of, 102, 105t; in kelp bed/rocky reef, 236t,

654

INDEX

238f, 239f, 240f, 247; in mid-depth rocky reef, 99f, 255, 260f, 263t; movement and activity patterns of, 523t, 531, 534t, 545; predation study of, 431–32f, 434–37f, 438, 439–42, 460–61; reproduction and, 494, 497; territoriality of, 455 Rhinoliparis barbulifer, 353t Rhinomuraena quasita, 518t Rhizoprionodon longurio, 20t, 25t Rhombochirus osteochir (hardfin marlinsucker), 25t, 325 ribbon halfbeak (Euleptorhampus viridis), 331f, 333 Richardson, Sally L., 270, 295, 296, 298 Riegle, K. C., 212 Rimicola spp. (clingfish): R. cabrilloi (Channel Islands clingfish), 7t, 17t, 24t; R. dimorpha, 18t, 24t; R. eigenmanni (slender clingfish), 19t, 25t, 92f, 111f, 236t, 238f; R. muscarum (kelp clingfish), 18t, 111f, 155t, 236t, 238f, 405 Ripley, W. E., 574 RIT. See rocky intertidal (RIT) Roach, S. W., 231 Roberts, D. A., 245, 246 Robinson, C. J., 543 Robison, B. H., 543 robust black smelt (Pseudobathylagus ochotensis), 365, 370f rockfish. See Sebastes spp. (rockfish) rockhead (Bothragonus swanii), 17t, 70 rockpool blenny (Hypsoblennius gilberti), 19t, 90f, 236t, 403; movement patterns of, 531, 532t, 543; in rocky intertidal zone, 209t, 210, 211, 215t, 216f rock prickleback (Xiphister mucosus), 17t, 90f, 236t, 498, 522; in rocky intertidal zone, 207, 209t, 212, 215t, 216f, 219, 220f; trophic relations and, 394, 399f, 403 rock sole (Lepidopsetta bilineata), 17t, 22t, 605 rockweed gunnel (Xererpes fucorum), 18t, 90f, 111f; feeding of, 399f, 403; in rocky intertidal zone, 207, 208, 209t, 215t, 216f, 220 rock wrasse. See Halichoeres semicinctus rocky intertidal (RIT) zone, 82–83t, 84f, 85t, 86f, 87, 205–23; aerial and aquatic respiration, 208, 210–12; age composition, 218; amphibious fishes in, 208, 209, 213; analysis of, 104t; behavioral and physiological traits, 208, 210–13; climate change and, 205, 221–22, 630; distribution patterns, 206–8; fish habitat, 205–6; horizonatal zonation, 208; osmoregulation and desiccation risk in, 212; recruitment, 214; reproduction in, 213–14; residents and visitors, 217–18; seasonal changes, 207–8; species abundance, 215, 217, 221; species groups in, 90f; stability and persistence in, 220–21; taxonomic composition, 214–15; trophic interactions in, 218–20, 399f, 403; vertical zonation, 206–8 rocky reef. See kelp bed/rocky reef (KBRR) rocky subtidal (RST), 83t, 84f, 85t, 86f, 91f; analysis of, 104t; species groups in, 90f, 238f Roedel, P. M., 588 Roncador stearnsii (spotfin croaker), 19t, 95f, 150t, 151f, 603 Rondeletia loricata, 520t ronquils (Bathymasteridae), 100f, 186, 238f; Rathbunella spp., 18t, 72, 72f, 235t, 522t, 532t Ronquilus jordani, 17t, 21t Rosales-Casian, J. A., 139

Rosen, D. E., 55, 63 Rosenblatt, R. H., 6, 621, 628 rosethorn rockfish (Sebastes helvomaculatus), 17t, 22t, 255, 262 rosylip sculpin (Ascelichthys rhodorus), 17t, 91f, 209t, 499, 500t, 507 rosy rockfish (Sebastes rosaceus), 19t, 22t, 100f, 255, 260f, 263t rosy sculpin (Oligocottus rubellio), 17t, 23t, 90f, 234t, 238f, 399f; in rocky subtidal zone, 215, 216f, 217f, 220f Rothschild, B. J., 309 rough abyssal grenadier (Coryphaenoides yaquinae), 353t, 369, 374–77, 540 roughback sculpin. See Chitonotus pugetensis roughcheek sculpin: Artedius creaseri, 75, 92f, 238f; Ruscarius creaseri, 19t, 23t, 234t, 533t roughies (Trachichthyidae), 66 rough sea robin (Prionotus rescarius), 178t, 181f, 194f roundfishes, 189 round stingrays. See Urolophus/Urobatis halleri rubberlip seaperch. See Rhacochilus toxotes rubynose brotula (Cataetyx rubrirostris), 186 Ruscarius creaseri (roughcheek sculpin), 19t, 23t, 234t, 533t Ruvettus pretiosus (oilfish), 20t, 24t, 327f, 332 Rypticus spp., 521t sabertooth blenny (Plagiotremus azuleus), 7t, 20t, 25t, 236t sablefish (Anoplopoma fimbria), 18t, 101f, 106t, 306, 521t, 532t; in bathypelagic zone, 353t, 369, 372f; commercial fisheries and , 574, 575, 578, 580; on continental shelf, 172, 178t, 185f, 187; foraging guild, 192f, 197f; pollutants and, 598 Saccopharynx lavenbergi, 519t Sacramento blackfish (Orthodon microlepidotus), 393 Sacramento sucker, 129f saddleback gunnel (Pholis ornata), 17t, 153t, 399f saddleback sculpin (Oligocottus rimensis), 17t, 21t, 90f, 209t, 215t, 216f, 399f Sagamichthys abei (shining tubeshoulder), 350t, 354, 355f, 369, 519t sailfin molly (Poecilia latipinna), 612t, 613f, 616 sailfin sculpin (Nautichthys oculofasciatus), 17t, 91f, 234t, 238f, 500t sailfish (Istiophorus platypterus), 21t, 25t, 333 Sakuma, K. M., 305 salema. See Xenistius californica Salmonidae (salmon), 29–32, 33, 72–73, 120, 128; climate change and, 632, 633; commercial fishing of, 570, 574, 575, 579, 580, 586; recreational fishing of, 580, 589; reproduction and, 487. See also Oncorhyncus spp. salmon shark (Lamma ditropis), 17t, 22t, 89f, 326f, 330, 337t; movement of, 524 Salmo salar (Atlantic salmon), 612t, 618, 619 Salmo trutta (brown trout), 612t, 616 sampling techniques, 170–71, 229–32. See also CalCOFI samplings Sanchez, C., 305 San Clemente Islands, 47, 48 sand bass. See Paralabrax spp. sanddabs. See Citharichthys spp. Sanderson, S. L., 393, 407 San Diegan Province, 3, 4f, 239 San Diego Bay, 120, 135, 135t, 141f, 145t sandpaper skate, 185f

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sand perch. See Diplectrum spp. sand sole (Psettichthys melanostictus), 17t, 97f, 296f, 605; on continental shelf, 179t, 181f, 194f; in surf zone, 152f, 153t, 155t San Francisco Bay, 120, 129, 131, 598; alien species in, 612, 613–18 Santa Barbara Basin, 359 Santa Barbara Channel, 261, 263, 458–59 Santa Barbara Island, 48 Santa Catalina Basin, 371 Santa Catalina Island, 47, 48, 74, 422, 587, 589; Naples Reef compared to, 546–47; pollution off, 600, 601; predation study at, 430–31, 432f, 434, 441, 443 Santa Cruz Island, 455, 457f, 458–59 Sarda chiliensis (Pacific bonito), 20t, 87, 89f, 236t, 585t; in coastal pelagic zone, 154, 157t, 158t, 159f, 160t; commercial fisheries and, 574, 575; feeding of, 406; in pelagic zone, 330, 332f, 336t, 337t; pollution and, 600, 601; recreational fishing and, 581, 582, 584; reproduction and, 494; seasonal movement of, 541–42; trophic relations and, 401f sardine and anchovy regimes, 15, 89, 281–82, 283–84f, 289; climate change and, 624, 625f, 633; competition and, 450; PDO and, 629–30, 629f, 630f, 631; trophic relations and, 403, 405 sardines (Cluperidae), 72, 89, 91; commercial fishing of, 569, 570–73, 578–79, 588, 590; and subsistence fishing, 567, 568 Sardinops sagax (Pacific sardine), 19t, 72, 103, 145t, 233t, 260, 429; abundance of, 89, 91, 336t; commercial fisheries and, 570–73, 579; feeding of, 393, 394; larval stages of, 276t, 277–78f, 279, 293, 294f, 298; in pelagic zone, 94f, 330, 332f, 335t, 337t; and recreational fishing, 585t, 586; in surf zone, 150t, 153t, 157t, 160–61t; trophic relations and, 401f sargassum blenny, 137f sargassum pipefish (Syngnathus peligius), 324 Sargassum spp. (algae), 228, 324, 419; S. palmeri, 430, 436f sargo (Anisotremus davidsoni), 19t, 66, 67f, 74, 89, 94f, 136t, 534t; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 235t, 239f, 241f; phylogenetic relations and, 43, 44f, 45t, 46t Sargocentron suborbitalis, 311f Sars, G. O., 269 sawtooth eel (Serrivomer sector), 348, 349t, 355f scalyhead sculpin (Artedius harringtoni), 17t, 91f, 213, 234t, 238f; reproduction and, 498, 500t, 502 Scaridae (parrotfishes), 394, 506; Nicholsina spp., 7t, 14, 20t, 25t, 235t, 522t SCCWRP ( Southern California Coastal Water Research Project), 168, 631 Schaeffer, B., 55, 63 Schmitt, Russell, 307, 429, 430–31, 459–60 schooling species, 186, 323–24, 494; predation and, 429–30 Schultz, S. A., 245 Sciaenidae (croakers), 9f, 69, 105, 105t, 235t, 393, 581; on continental shelf, 175, 178t, 180t; larval stages of, 276t, 289, 294; movement and activity of, 535t–536t, 539–40, 548; pollution and, 602; species richness, 10f; in surf zone, 149, 150, 153. See also Genyonemus lineatus (white croaker); Seriphus politus (queenfish); white sea bass (Atractoscion nobilis) Sciaenops ocellatus (red drum), 150

scissortail chromis (Chromis atrilobata), 92f, 235t, 241f scissortail damselfish, 237f scleratinian coral reefs, 56–57 Scleroplax granulata (pea crab), 559f Scofield, W. L., 570, 587, 588 Scolopsis spp., 522t Scomber japonicus (Pacific chub mackerel), 20t, 96f, 160t, 236t, 261, 279, 429; abundance of, 336t; in coastal pelagic zone, 154, 156, 157t, 159f, 330, 332f, 335t; commercial fishing of, 337t, 574–75, 576, 579, 585t; decline of, 588; feeding of, 406; historical fluctuation in, 624; larval stages of, 276t, 277–78f, 305, 311; recreational fishing of, 582, 583, 584; seasonal movement of, 541–42; trophic relations and, 401f, 406 Scomberomorus concolor, 19t, 24t Scomberomorus sierra, 20t, 25t Scombridae (chub mackerels), 9f, 10f, 61, 105, 321, 329; genetic divergence in, 621; and reproduction, 494, 496 Scopelengys tristis (Pacific blackchin), 351t, 357f, 358, 519t Scopeleogadus mizolepis, 520t Scopeloberyx robustus (longjaw bigscale), 352t, 365 Scopelogadus mizolepsis bispinosus (twospine bigscale), 352t, 361, 365, 366t Scopelosaurus spp., 519t Scorpaena guttata (California/spotted scorpionfish), 19t, 70f, 136t, 255, 520t; fisheries and, 579, 585t, 586; foraging guild, 192f, 195f; habitat of, 99f, 102, 105t; in harbors, 157t, 160t, 162t; in kelp bed/rocky reef, 234t, 239f; in pelagic zone, 178t, 182f; pollutants and, 598; seasonal movement of, 536t, 542; trophic relations and, 395, 398f, 403 Scorpaena histrio (player scorpionfish), 234t Scorpaenichthys marmoratus (cabezon), 19t, 70f, 162t, 270, 500t, 521t, 533t; in bays and estuaries, 132f; as brephoepipelagic fish, 333, 334f; commercial fisheries and, 574, 579; ENSO and, 631; feeding of, 399t, 403; in kelp bed/rocky reef, 111f, 234t, 238f, 240f; in rocky intertidal zone, 91f, 215t, 216f, 217f, 218, 219t; subsistence fishing and, 568; in surf zone, 151, 152f, 153t, 155t Scorpaenidae (scorpionfishes and rockfishes), 59–60, 68, 77, 217f, 234t, 500; on continental shelf, 172, 175, 180t, 186, 258t; habitat for, 105, 106t; movement of, 536t–537t; in pelagic zone, 329, 333; pollution and, 601; and reproduction, 491, 499, 504. See also Cottidae; Hexagrammidae; Sebastes spp. Scorpaenodes xyris (rainbow scorpionfish), 20t, 25t, 70, 234t Scorpis lineolata, 522t Scripps Institution of Oceanography (SIO), 269 scuba diving, 526–27 sculpins. See Artedius spp.; Clinocottus spp.; Cottidae; Icelinus spp.; Oligocottus spp. Scyliorhinidae (cat sharks), 175, 177t, 180t, 485; Parmaturus xaniurus (filetail), 19t, 23t, 101f, 353t, 518t. See also Apristurus spp. Scytalina cerdale (graveldiver), 17t, 90f, 215t, 216f, 220f, 522t; feeding of, 399f, 403 scythe butterflyfish (Prognathodes falcifer), 20t, 24t, 235t sea basses. See Atractoscion nobilis; Paralabrax spp.; Serranidae

sea chubs (Kyphosidae), 7t, 105, 106t, 235t, 534t, 557t; feeding of, 65–66. See also Girella nigricans; Medialuna californiensis seahorse (Hippocampus ingens), 20t, 25t, 135t, 137f, 484 sea jellies (Pelagia spp.), 328f sea otter (Enhydra lutris), 624, 627, 628f seaperch. See Phanerodon spp.; Rhacochilus spp. sea robins (Triglidae), 176, 178t, 181f, 189. See also Prionotus spp. searsids (Holthyrnia spp.), 350t seasonality, 139–40, 248, 249; larval distribution, 296–98; in rocky intertidal zone, 207–8 sea trout (Cynoscion spp.), 19t, 24t, 150 sea urchins, 404, 441, 455, 476; climate change and, 625, 626, 627, 628f Sebastes (rockfishes), 9f, 10f, 70, 75, 76, 77, 234t; climate change and, 624, 632, 633; commercial fishing of, 573–74, 576, 579, 590, 591; in deep rock habitat, 255–56, 257f, 258t, 259–64; feeding of, 59–60; habitat for, 91f, 96, 99f, 100, 102–3, 105; larval stages of, 276t, 277, 278f, 292, 294f, 296f, 299, 305; movement and activities of, 536t–537t, 539, 541, 544; recreational fishing of, 580, 581, 584, 589; recruitment of, 417; reproduction and, 484, 486, 493, 499, 504, 505; species richness of, 10, 255; subsistence fishing and, 568; in surf zone, 152; wastewater pollution and, 606; YOY abundance, 83, 260, 261, 262f, 263t, 440–41 Sebastes spp. (rockfish): S. aleutianus, 18t, 22t; S. alutus (Pacific perch), 17t, 22t, 258t; S. aurora (aurora rockfish), 18t, 22t, 101f, 278; S. babcocki (redbanded rockfish), 18t, 22t, 255; S. borealis, 17t, 21t; S. brevispinis, 17t, 21t; S. constellatus (starry rockfish), 19t, 23t, 99f, 234t, 260f, 263t; S. crameri (darkblotched rockfish), 17t, 21t, 257, 589; S. dallii (calico rockfish), 19t, 98f, 187, 234t, 398f, 416, 536t, 542; S. ensifer (swordspine rockfish), 18t, 23t, 99f, 102, 105t, 255, 260f, 263t; S. entomelas, 17t, 22t; S. eos (pink rockfish), 18t, 23t, 100f, 258t; S. gilli (bronzespotted rockfish), 18t, 24t, 258t; S. helvomaculatus (rosethorn), 17t, 22t, 255, 262; S. hopkinsi (squarespot rockfish), 18t, 23t, 99f, 234t, 255, 257, 260f, 263t, 591; S. inermis, 493; S. lentiginosus (freckled rockfish), 18t, 25t, 255; S. macdonaldi (Mexican rockfish), 19t, 24t, 44f, 45t, 46t, 258t; S. maliger (quillback rockfish), 17t, 21t, 255, 537t, 539, 542; S. melanostomus (semaphore rockfish), 18t, 22t, 258; S. moseri (whitespeckled rockfish), 100f, 255; S. nebulosus (china rockfish), 17t, 76, 76f, 234t, 240t; S. nigrocinctus, 17t, 21t; S. ovalis (speckled rockfish), 18t, 23t, 99f, 255, 260f; S. phillipsi (chameleon rockfish), 17t, 23t, 258t; S. proriger, 17t, 22t; S. reedi, 17t, 21t; S. rosaceus (rosy rockfish), 19t, 22t, 100f, 255, 260f, 263t; S. ruberrimus (yelloweye rockfish), 17t, 22t, 255, 260f; S. rubrivinctus (flag rockfish), 7t, 18t, 99f, 255, 260f, 263t; S. rufus (bank rockfish), 18t, 23t, 100f, 102, 105t, 262f; S. schlegelii, 520t; S. simulator (pinknose rockfish), 18t, 24t, 100f, 255, 262f; S. umbrosus (honeycomb rockfish), 19t, 24t, 99f, 255, 260f, 586; S. wilsoni (pygmy rockfish), 17t, 255, 259, 260f, 263t; S. zacentrus, 18t, 23t

INDEX

655

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Sebastes atrovirens (kelp rockfish), 19t, 157t, 162t, 270, 415, 536t; feeding/foraging of, 60f, 67–68; in kelp bed/rocky reef, 92f, 234t, 237f, 239f, 240f; phylogeographic structures of, 34t, 38 Sebastes auriculatus (brown rockfish), 19t, 22t, 111f, 255, 270; in kelp bed/rocky reef, 92f, 234t, 240f; movement of, 536t, 542; in surf zone, 152, 155t Sebastes carnatus (gopher rockfish), 19t, 23t, 219t, 258, 270, 585t; in kelp bed/rocky reef, 91f, 234t, 237f, 240f; movement of, 531, 536t; recruitment and, 415, 420; territoriality of, 453t, 455–56f, 457f Sebastes caurinus (copper rockfish), 17t, 111f, 255, 260f, 270, 585t; on continental shelf, 178t, 182f, 195f; in kelp bed/rocky reef, 92f, 234t, 240t; recruitment of, 415; seasonal movement of, 536t, 539, 542; in surf zone, 152, 155t Sebastes chlorostichus (greenspotted rockfish), 18t, 22t, 178t, 183f, 196f; in deep rock habitat, 100f, 255, 262f, 263t; movement of, 528, 536t, 539 Sebastes chrysomelas (black-and-yellow rockfish), 19t, 67f, 91f, 162t, 215t, 219t; in kelp bed/rocky reef, 234t, 237t, 240f; movement of, 531, 536t; recruitment of, 415, 420; territoriality of, 453t, 455–56f, 457f; trophic relations of, 399, 403 Sebastes diploproa (splitnose rockfish), 18t, 22t, 101f, 258t, 279, 333; on continental shelf, 172, 178t, 185f; foraging guild, 192f, 197f; as generalist, 103, 105t; movement of, 536t, 541 Sebastes elongatus (greenstriped rockfish), 18t, 22t, 102, 105t, 537t; in deep rock habitat, 100f, 255, 262f, 263t Sebastes flavidus (yellowtail rockfish), 17t, 99f, 234t, 520t, 589; in deep rock habitat, 260f, 263t; movement of, 537t, 539 Sebastes goodei (chilipepper), 19t, 100f, 172, 262f; fisheries and, 576, 585t, 590 Sebastes jordani (shortbelly rockfish), 18t, 22t, 59, 100f, 178t, 183f, 192f, 537t; in deep rock habitat, 255, 262f; larval stages of, 276t, 285, 287f Sebastes levis (cow cod), 18t, 23t, 100f, 103, 537t, 589; in deep rock habitat, 255, 262f, 263t; larval stages of, 285, 288f Sebastes melanops (black rockfish), 17t, 70, 70f, 155t, 234t, 255, 475; rocky intertidal zone, 215t, 216f, 217t, 219t Sebastes miniatus (vermilion rockfish), 18t, 22t, 99f, 234t, 493, 631; in deep rock habitat, 255, 260f, 263t; fisheries and, 585t, 586 Sebastes mystinus (blue rockfish), 18t, 59f, 91f, 215t, 416; in deep rock habitat, 255, 260f; fishing and, 584, 585t, 590; in kelp bed/rocky reef, 234t, 240f, 242, 243f; reproduction and, 494; seasonal movement of, 537t, 542; trophic relations and, 394, 404 Sebastes paucipinnis (bocaccio), 18t, 59, 234t, 334f, 484f, 632; commercial fishing of, 576, 589, 590; in deep rock habitat, 256, 260f, 261f, 263t; epibenthic, 539; habitat for, 100f, 103; larval stages of, 276t, 309f; movement of, 528, 537t, 541; recreational fishing of, 584, 585t; young-of-year (YOY), 111f, 261, 262f Sebastes pinniger (canary rockfish), 18t, 99f, 255, 260f, 263t; fisheries and, 585t, 589, 591

656

INDEX

Sebastes rastrelliger (grass rockfish), 18t, 59f, 90f, 111f, 234t, 403, 430; in rocky intertidal zone, 90f, 215t, 216f, 217f, 219t; in surf zone, 152, 153t, 155t, 157t Sebastes rosenblatti (greenblotched rockfish), 18t, 23t, 178t, 192f, 196f, 537t; in deep rock habitat, 100f, 255, 262f, 263t Sebastes saxicola (stripetail rockfish), 19t, 23t, 172, 178t, 258, 537t, 631; on continental shelf, 172, 178, 182f, 183f; foraging guild, 192f, 195f, 196f; recruitment of, 416; trophic relations, 398f, 403 Sebastes semicinctus (halfbanded rockfish), 19t, 23t, 99f, 178t, 183f, 196f, 631; in deep rock habitat, 255, 257, 260f, 263t Sebastes serranoides (olive rockfish), 18t, 60f, 91f, 162t, 219t; in kelp bed/rocky reef, 234t, 237f, 240f, 243f; movement and activity of, 537t, 548; and recreational fishing, 584, 585t, 590; trophic relations and, 400f, 405 Sebastes serriceps (treefish), 18t, 23t, 67f, 162t, 537t; in kelp bed/rocky reef, 92f, 234t, 237f, 239f; trophic relations and, 400f, 405 Sebastolobus spp. (thornyheads), 34t, 333 Sebastolobus alascanus (shortspine thornyhead), 18t, 23t, 33, 353t, 369, 520t; on continental shelf, 172, 178t, 185f, 197f; habitat of, 101f, 102, 105t; movement of, 537t, 540 Sebastolobus altivelis (longspine thornyhead), 19t, 23t, 96, 101f, 311f, 334f; in bathypelgic zone, 353t, 369, 371, 372f; movement of, 537t, 540, 541 sediment contamination, 596, 598, 600f, 604, 607f, 608. See also pollution Selene brevoorti (Mexican lookdown), 7t, 20t, 308f Selene peruviana, 20t, 25t semaphore rockfish (Sebastes melanostomus), 18t, 22t, 258 Semicossyphus pulcher (California sheephead), 19t, 23t, 92f, 235t, 259, 522t; cleaner behavior of, 556f, 557t; and commercial fishing, 574, 579; feeding of, 65, 394; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 237f, 239f, 241f, 243f; larval stages of, 270, 293, 295f, 297f, 302; movement and activity patterns of, 534t, 541, 546, 548; overfishing and, 625, 627, 628f; phylogenetic relations and, 35t, 44f, 45t, 46t, 49, 624; recruitment of, 414, 417; reproduction and, 487, 490, 491f, 496, 497; subsistence fishing and, 568; telemetry and, 527; trophic relations and, 400f, 405 señorita (Oxyjulis californica), 18t, 58, 105t, 136t, 259, 522; activity patterns of, 534t, 544, 546, 548; cleaner behavior of, 555, 556f, 557t; feeding of, 65, 389, 390, 400f; in harbors, 159, 162t; in kelp bed/rocky reef, 87, 92f, 235t, 237f, 239f, 240f, 241f, 404–5; larval stages of, 293, 295f; macrophyte substratum and, 111; predation and, 431f, 436; reproduction and, 497, 498 sensory systems, 213, 223; vision, 307, 343 Seriola lalandi (yellowtail), 18t, 23t, 87, 89f, 330, 332f; abundance of, 336t, 337t, 628; commercial fisheries and, 574, 575, 588; hunting behavior of, 62, 432f; in kelp bed/rocky reef, 234t, 241f; recreational fishing of, 580, 581f, 582, 583, 584–86; trophic relations and, 401f, 406 Seriola rivoliana (almaco jack), 20t, 25t, 62

Seriphus politus (queenfish), 19t, 91, 136t, 145t, 522t, 585t, 631; activity patterns of, 536t, 548; in coastal pelagic zone, 155t, 156, 157t, 159f, 160–61t; on continental shelf, 178t, 181f; foraging guilds, 192f, 194f; larval forms of, 305; nocturnality of, 66, 67f; in surf zone, 95f, 150–51, 150t, 154f; trophic relations and, 397f Serranidae (sea basses and groupers), 87, 105, 106t, 234t, 506, 537t–538t; commercial fishing and, 579, 591; on continental shelf, 175, 178t, 180t; Mycteroperca spp. (grouper), 19t, 20t, 23t, 25t, 58, 234t; reproduction and, 487, 502, 503. See also Stereolepis gigas (giant sea bass); Paralabrax spp.; white sea bass (Atractoscion nobilis) Serranus spp. (serrano), 58, 496; S. aequidens (deepwater serrano), 178t, 180t, 196f; S. fasciatus, 521t; S. psittacinus (banded serrano), 234t; S. tabacarius, 521t Serrivomer sector (sawtooth eel), 348, 349t, 519t Setran, A. C., 214 Sette, Oscar E., 269 sexual selection, 495, 498–99. See also hermaphroditism; reproduction shad. See American shad; threadfin shad shadow goby (Quietula y-cauda), 19t, 88, 303, 534t; in bays and estuaries, 93f, 126t, 132f, 134f, 145t; trophic relations and, 396f, 401 shallow slope (SSLP), 85t, 86f Shanks, A. L., 414 Shannon-Wiener (H’) diversity index, 83, 85, 107–8 sharks, 233t, 324, 326f, 632; basking shark (Cetorhinus maximus), 19t, 326f, 336t, 390, 518t; commercial fishing and, 574, 576, 579; hammerheads, 89f, 337t, 538t; megamouth (Megachasma pelagios), 327f, 528, 529f; movement of, 527–28, 530, 542; nocturnals, 95f; pollutant concentrations in, 602; reproduction and, 483, 484; in surf zone, 153; whale shark (Rhinocodon typus), 20t, 25t, 325, 331f, 333, 518t, 540. See also Carcharhinidae; Heterodontes francisi; Scyliorhinidae (cat sharks); Squalidae (dogfish sharks); Triakidae (hound sharks) sharksucker (Echeneis naucrates), 20t, 24t, 324, 329f sharpchin rockfish, 100f, 263t sharpchin slickhead (Bajacalifornia barragei), 349t sharpnose seaperch (Phanerodon atripes), 75, 555, 556f, 557f sheephead. See Semicossyphus pulcher shelf habitat, 83t, 84f, 100f. See also continental shelf shell mound assemblage, 264 shimofuri goby (Tridentiger bifasciatus), 130t, 131, 142f, 612t, 614 shiner perch. See Cymatogaster aggregata shining loosejaw (Aristostomias scintillans), 356, 357f, 366t, 370f shining tubeshoulder (Sagamichthys abei), 350t, 354, 355f, 369, 519t shokihaze goby (Tridentiger barbatus), 130t, 131, 612t, 614 shortbelly rockfish (Sebastes jordani), 59, 100f, 183f shortfin corvina (Cynoscion parvipinnis), 135t shortfin mako (Isurus oxyrhynchus), 20t, 22t, 89f, 390, 518t, 579; movement of, 527–28, 529f, 540; in pelagic zone, 326f, 331, 337t; pollution and, 601; trophic relations and, 401f, 406

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shortspine combfish. See Zaniolepis frenata shortspine thornyhead (Sebastolobus alascanus), 18t, 23t, 33, 353t 369, 520t; on continental shelf, 172, 178t, 185f, 197f; habitat of, 101f, 102, 105t; movement of, 537t, 540 shoulderspot (Caelorinchus scaphopsis), 369 shovelnose guitarfish (Rhinobatis productus), 19t, 137f, 233t, 397f, 568; as nearshore softbottom fish, 97f, 157t, 158t showy bristlemouth (Cyclothone signata), 276t, 350t, 354, 356f, 360t, 362–63, 366t, 370f; trophic relations of, 402f shrimp spp., 555, 558f, 559–60, 560f Sidera spp., 518t Siebenaller, J. F., 374 Siganus canaliculatus, 523t signal blenny (Emblemaria hypacanthus), 432, 503, 522t silversides. See Atherinopsidae silverspotted sculpin (Blepsias cirrhosus), 17t, 151, 152f, 153t; reproduction in, 486, 499, 500t silver surfperch (Hyperprosopon ellipticum), 18t, 91f, 235, 240f, 585t; in surf zone, 152f, 153t Simberloff, D., 611 sixspot prickleback (Kasatkia seigeli), 7t skates. See Bathyraja spp.; Rajidae (skates) skipjack tuna (Katsuwonus pelamis), 20t, 89f, 326f, 331, 337t, 573, 628 skipper fishes, 211, 213 sleep patterns, 549 slender barracudina (Lestidiops ringens), 277, 280, 351t, 355f, 370f slender bigscale (Melamphaes acanthomus), 352t slender bristlemouth (Cyclothone pseudopallida), 276, 280 slender clingfish (Rimicola eigenmanni), 19t, 25t, 92f, 111f, 236t, 238f slender cockscomb (Anoplarchus insignis), 17t, 21t, 238f slender hatchetfish (Argyropelecus affinis), 354, 356f, 359, 366t slender mola (Ranzania laevis), 21t, 24t, 311f, 332 slender snipefish (Macroramphosus gracilis), 20t, 25t, 332, 520t slender sole. See Lyopsetta exilis slender sucker (Phtheirichthys lineatus), 20t, 25t, 324 slendertail lanternfish (Gonichthys tenuiculus), 277, 279f, 280, 370f slickheads. See Alepocephalidae slim sculpin (Radulinus asprellus), 17t, 22t, 178t, 195f slimy snailfish (Liparis mucosus), 18t, 151, 153t slipskin snailfish, 238f slope habitat, 83t, 84f, 258t. See also continental shelf and slope slough anchovy (Anchoa delicatissima), 19t, 396f, 401–2; in bays and extuaries, 93f, 126t, 134f, 138t, 145t smalldisk snailfish (Careproctus gilberti), 353t smallhead flyingfish, 331f, 401f small squaretail (Tetragonurus cuvieri), 18t, 23t, 328f, 330 smelts, fisheries and, 573, 574, 581. See Atherinidae; Bathylagidae; Osmerida Smith, C. I., 497 Smith, D. R., 404 Smith, G. B., 174, 197 Smith, K. L., Jr., 371, 373, 376 Smith, P. E., 305, 323 Smith, R. W., 6

Smith-Beasley, I., 348 smooth grenadier (Nezumia liolepsis), 353t, 369 smooth hammerhead, 89f, 337t smoothhead sculpin (Artedius lateralis), 18t, 90f, 209t, 216f, 238f, 399f; feeding of, 392, 394 smooth puffer, 137f smooth stargazer (Kathetostoma averruncus), 20t, 179t, 185f, 197 smoothtongue. See Leuroglossus stilbius snailfishes. See Careproctus spp.; Liparis spp. snakehead eelpout (Lycenchelys crotalinus), 17t, 22t, 354t snake mackerel (Gempylus serpens), 21t, 25t, 327f, 329, 332 snipe eels (Avocettina spp.), 349t, 354, 355f snubnose blacksmelt (Bathylagus wesethi), 349, 354, 355f, 360t, 370f; larval stages of, 276t, 277f, 279f, 280, 285–86, 289f, 368; swimbladder of, 365, 366t snubnose pipefish (Cosmocampus arctus), 19t, 92f, 234t, 238f snubnose sculpin (Orthonopias triacis), 18t, 23t, 60, 91f, 532t; in kelp bed/rocky reef, 234t, 238f sockeye salmon (Oncorhynchus nerka), 17t, 21t, 519t, 624–25, 626f soft bottom species, 111, 167, 601. See also continental shelf and upper slope softhead grenadier (Malacocephalus laevis), 369 soldierfishes, 547, 548 sole. See Pleuronectidae (righteye flounders) Solenostomus spp., 520t Somniosus pacificus (Pacific sleeper shark), 17t, 21t, 353t, 518t sonar systems, 527–28 Sorenson, P. W., 493 soupfin shark (Galeorhinus galeus), 19t, 89f, 233t, 337t, 576 Soutar, A., 624 Southern California Bight (SCB), 504, 630, 631; contaminants in, 595, 596 Southern California Coastal Water Research Project (SCCWRP), 168, 631 southern spearnose poacher (Agonopsis sterletus), 19t, 24t, 178t, 183f, 196f spatial patterns, 530–31, 539–43. See also movement and activity patterns spawning, 488–89, 494, 495, 507, 587. See also reproduction species abundance. See abundance species ranges, 8–9, 12f, 13f, 28f speckled rockfish (Sebastes ovalis), 18t, 23t, 99f, 255, 260f speckled sanddab (Citharichthys stigmaeus), 19t, 60, 61f, 236t, 258, 631; in bays and estuaries, 127t, 128f, 132f; on continental shelf, 96, 97f, 103, 176, 179t, 181f; foraging guilds, 192f, 194f; in harbors, 158, 161t; larval stages of, 276t, 277–78f, 280, 298, 299; movement of, 535, 543; pollution and, 601, 602f, 606; in surf zone, 152f, 153t, 155t; trophic relations and, 397f, 403 specklefin midshipman (Porichthys myriaster), 97f, 136t, 145t, 157t, 158t; on continental shelf, 181f, 182f; trophic relations and, 397f, 403 speckletail flounder (Engyophrys sanctilaurentii), 7t, 20t, 25t, 179t, 182f, 195f Spectrunculus grandis (pudgy cusk-eel), 353t, 369 Sphoeroides annulatus (bullseye puffer), 20t, 25t, 95f, 96, 137f, 236t, 237f, 241f

Sphoeroides lobatus (longnose puffer), 7t, 20t, 25t Sphyraena argentea (California barracuda), 19t, 236t, 330, 390, 523t, commercial fishing of, 574, 575f, 587; larval stages of, 295f, 297f, 300f, 302, 311; recreational fishing of, 581, 582, 583, 584, 585t; seasonal movement of, 541–42; in surf zone, 150t, 154, 155t, 158t Sphyraena ensis (Mexican barracuda), 7t, 20t, 25t, 236t Sphyrna spp. (hammerheads): lewini (scalloped hammerhead), 538t; S. tiburo, 20t, 25t; S. zygaena, 18t spines, and predation, 429 spiny dogfish. See Squalus acanthias spiny dreamer (Oneirodes acanthias), 352t, 358, 390, 395, 520t; trophic relations of, 402f Spirinchus starksi (night smelt), 17t, 72, 151, 152f, 153t, 335; on continental shelf, 177t, 181f, 194f Spirinchus thaleichthys (longfin smelt), 17t splitnose rockfish (Sebastes diploproa), 18t, 21t, 101f, 258t, 279, 333; on continental shelf, 172, 178t, 185f; foraging guild, 192f, 197f; as generalist, 103, 105t; movement of, 536t, 541 sponges, 486 spotfin croaker (Roncador stearnsii), 95f, 150t, 151f, 603; and commercial fishing, 587 spotfin mojarra (Eucinostomus argenteus), 178t, 181f, 182f, 194f, 195f spotfin surfperch (Hyperprosopon anale), 18t, 97f, 152f, 153t, 155t spot (Leiostomus xanthurus), 469, 472f spotted cabrilla (Epinephelus analogus), 20t, 24t, 234t spotted cusk-eel (Chilara taylori), 19t, 98f, 163, 176, 177t, 398f; on continental shelf, 182f, 183f, 185f; foraging guild, 192f, 194f, 195f, 196f, 197f; movement patterns of, 535t, 546 spotted flounder (Hippoglossina bollmani), 179t, 182f, 195f spotted kelpfish (Gibbonsia elegans), 19t, 60, 61f, 92f, 111f, 155t, 532t; hypoxia and, 468; in kelp bed/rocky reef, 236t, 238f; in rocky intertidal zone, 207, 215t, 216f, 217, 220f; in surf zone, 145t, 154f, 155t, 159 spotted lizardfish (Synodus evermanni), 177t, 182f, 183f, 195f, 196f spotted ratfish (Hydrolagus colliei), 18t, 177t, 183f, 185f, 394, 532t; foraging guild, 196f, 197f; habitat of, 101f, 102, 103, 105t spotted sand bass. See Paralabrax maculatofasciatus spotted scorpionfish. See Scorpaena guttata spotted turbot (Pleuronichthys ritteri), 95f, 151, 155t, 157t, 181f; in bays and estuaries, 127t, 133, 136t, 145t; larval stages of, 292, 293, 294f, 300; pollutants and, 600, 603; trophic relations and, 397f Squalidae (dogfish sharks), 106t, 175, 177t, 180t. See also Squatina californica Squalus acanthias (spiny dogfish), 19t, 136t, 157t, 158t, 160t, 429, 484, 518t; and commercial fisheries, 574; on continental shelf, 172, 177t, 182f, 183f, 195f, 196f; habitat of, 101f, 103; pollutants and, 598, 600 squarespot rockfish (Sebastes hopkinsi), 18t, 23t, 99f, 234t, 591; in deep rock reef, 255, 257, 260f, 263t

INDEX

657

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squaretails (Tetragonurus spp.), 324, 333, 523t; T. cuvieri (small squaretail), 18t, 23t, 328f, 330 Squatina californica (angel shark), 19t, 95f, 184, 233t, 390, 518t; commercial fishing and, 579, 591; movement of, 527, 538t, 540; in surf zone, 153, 156f, 157t, 158t squid fisheries, 401f, 406, 575 squirrel fishes, 547 Stacey, N. E., 493 staghorn sculpin (Leptocottus armatus), 18t, 209t, 500t, 532t, 613; in bays and estuaries, 93f, 126t, 128f, 129f, 132f, 134f, 138t, 143f; on continental shelf, 178t, 181f, 194f; in surf zone, 150, 153t, 155t, 157t; trophic relations and, 396f, 402 stargazers (Uranoscopidae), 175, 180t, 522t, 604 Starks, E. C., 574 Starksia hoesii, 522t Starr, M. P., 539, 554 starry flounder (Platichthys stellatus), 17t, 296f, 600, 605, 606; in bays and estuaries, 93f, 127f, 128f, 129f, 132f, 138t starry rockfish (Sebastes constellatus), 19t, 23t, 99f, 234t, 260f, 263t State Water Resources Control Board (SWRCB), 168, 169, 170 Steele, M. A., 247, 419–20, 421, 460, 531; predation study of, 430, 431–32, 434–37, 438, 439–41, 442 steelhead (Oncorhynchus mykiss), 29, 30t, 31, 32, 618; in bays and estuaries, 126t, 128f, 129f, 130t, 132f Stegastes partitus (bicolor damselfish), 488 Stegastes rectifraenum (Cortez damselfish), 235t Stein, D. L., 374 Stellerina xyosterna (pricklebreast poacher), 18t, 152f, 153t, 296 Steneck, R. S., 5–6 Stenobrachius leucopsarus (northern lampfish), 351t, 357f, 359, 361–62, 363, 519t; bioluminescence in, 356; larval stages of, 276t, 277–78f, 282f, 284, 285f, 292, 294f, 299, 305; reproduction and, 368; swim bladder of, 366t, 367; trophic relations of, 402f Stenobrachius spp., 298, 299 Stephen, C. A., 621 Stephens, John S., Jr., 158, 163, 531, 542, 630; on kelp bed/rocky reef species, 227, 230, 231, 241, 244, 246 Stephenson, W., 295 Stereolepis gigas (giant sea bass), 18t, 87, 555, 624; in kelp bed/rocky reef, 92f, 234t, 237f, 239f, 241f; recreational fishing and, 583, 589; reproduction of, 494, 497; trophic relations, 400f, 405 Sternoptyx spp. (hatchetfishes), 350t, 365, 366t, 406; S. diaphana (diaphanous hatchetfish), 350t, 354, 356f, 402f, 519t; S. obscura, 350t Stichaeidae (pricklebacks), 9f, 10f, 72, 186, 329; reproduction and, 498; in rocky intertidal zone, 90f, 207, 209t, 210, 213, 216f, 217f. See also monkeyface prickleback; Xiphister spp. sticklebacks, 120, 142f. See also three-spine stickleback stingray. See Dasyatis spp.; Urobatis/Urolophus halleri Stomias atriventer (blackbelly dragonfish), 351t, 356, 357f, 366t, 370f, 395; larval stages of, 277, 279f, 280; trophic relations of, 402f, 406 Stomiidae (dragonfishes), 307, 329, 350–51t, 354, 356

658

INDEX

storms, disturbance and, 474–77, 478f Strasburg, D. W., 555 streaklight tubeshoulder (Holthyrnia latifrons), 369 striped bass. See Morone saxatilis stripedfin ronquil (Rathbunella hypoplecta), 18t, 72, 72f, 235t, 522t, 532t striped kelpfish (Gibbonsia metzi), 19t, 90f, 111f, 155t, 236t, 238f; in rocky intertidal zone, 215t, 216f; tophic relations of, 399f, 403 striped marlin (Tetrapterus audax), 21t, 24t, 89f, 395, 401f, 433; in pelagic habitat, 326f, 332, 337t striped mullet (Mugil cephalus), 20t, 157t, 158t, 520t, 534t; in bays and estuaries, 95f, 126t, 129f, 134f, 145t, 398; as brephoepipelagic fish, 333, 334f; feeding and trophic relations, 390, 394, 396f striped sea chub (Kyphosus analogus), 7t striped seaperch (Embiotoca lateralis), 18t, 75, 92f, 585t; activity patterns of, 544–45; competition and, 450, 453t, 457–60, 461–62f, 463f; in kelp bed/rocky reef, 235t, 237f, 240f, 404; phylogenetic structures of, 34t, 38; recruitment of, 415, 416; in surf zone, 111f, 151, 152f, 153t stripefin poacher (Xeneretmus ritteri), 18t, 24t, 98f, 178t, 183, 185f, 197f stripetail rockfish (Sebastes saxicola), 19t, 23t, 100f, 103, 258, 537t, 631; on continental shelf, 172, 178, 182f, 183f; foraging guild, 192f, 195f, 196f; recruitment of, 416; trophic relations, 398f, 403 Stromateioid fishes, 321, 324, 333 Strongylocentrotus spp. See sea urchins Strongylura exilis, 20t, 520t sturgeon (Acipenser spp.), 125, 587, 602; A. medirostris (green sturgeon), 18t, 125, 126t, 128f, 130t; A. transmontanus (white sturgeon), 18t, 125, 126t, 128f, 518t subsistence fisheries, 524, 567–68, 580 subtidal and reef species, 91f suckerfishes, 324–25. See also Remora spp. Sudis atrox, 311f Suflamen verres (orange-side triggerfish), 236t sunbeam lampfish (Lampadena urophaos), 277, 279f, 280, 351t superfoetation, 486–87, 500 surf grass (Phyllospadix spp.), 228 surfperches. See Amphisticus spp.; Embiotocidae (surfperches); Hyperprosopon spp. surf smelt (Hypomesus pretiosus), 17t, 72, 494–95, 519; in bays and estuaries, 93f, 127t, 128f, 129f, 132f; in surf zone, 151, 152f, 153t surf zone (SZ), 83t, 85t, 86f, 94, 95f, 96, 97f, 149–53; analysis of, 104t; drift algal beds and, 151–52, 154f surgeonfish (Acanthurus spp.), 329, 523t surveys, 253–54. See also CalCOFI Sustainable Fisheries Act (1996), 588 swallowtail damsel (Azurina hirundo), 235t Swanson, C., 616 Sweetwater Marsh, 144f swellhead snailfish (Paraliparis cephalus), 353t swell shark (Cephaloscyllium ventriosum), 21t, 23t, 95f, 153, 156f, 157t, 158t; activity patterns of, 536t, 544, 549; in kelp bed/rocky reef, 233t, 239f swimbladders and buoyancy, 365–68 swordfish. See Xiphias gladius swordspine rockfish (Sebastes ensifer), 18t, 23t, 99f, 102, 105t; in deep rock reef, 255, 260f, 263t

Syacium ovale (oval flounder), 179t, 194f symbiotic relationships, 554–63, 558f; bioluminescence and, 557–58; cleaner behavior, 555–57, 557t; commensalism, 554, 558–61; mutualism, 554–58; parasitism, 486, 554, 555, 561–62, 605; shrimp and, 555, 558f, 559–60, 560f Symbolophorus californiensis (California lanternfish), 351t, 357f, 358, 359, 402f; larval stages of, 276t, 277f, 279f, 280, 282f; swimbladder of, 366t, 367 Symbolophorus spp. (lightfish), 286 Symphodus ocellatus, 522t Symphodus tinca (peacock wrasse), 502 Symphurus atriacaudus (tonguefish), 19t, 98f, 155t, 179t, 475, 523t, 533t; in bays and estuaries, 132f, 136t; on continental shelf, 181f, 182f, 183f, 194; foraging guild, 192f, 194f, 195f, 196f; in harbors, 158, 161t; larval stages of, 277, 293, 295f, 301, 310f; pollutants and, 603; trophic relations and, 398f Symphurus spp. (tonguefish), 277f, 280f; S. atrimentatus (halfspotted tonguefish), 179t, 182f, 195f; S. oligomerus (whitetail tonguefish), 179t, 183f, 196f Synchiropus atrilabiatus (blacklip dragonet), 7t, 20t, 25t, 179t, 183f, 196f Synchirus gilli, 17t, 21t, 500t Syngnathus spp. (pipefishes), 103, 106t, 234t, 507; and reproduction, 484; S. exilis (barcheek pipefish), 111t, 151f, 154f, 155t, 598; S. fuscus, 520t; S. peligius, 324 Syngnathus auliscus (barred pipefish), 20t, 88, 97f, 111f, 152; in bays and estuaries, 93f, 126t, 134f, 145t Syngnathus californiensis (kelp pipefish), 19t, 103, 111f, 234t, 238f, 507; in surf zone, 150t, 154f, 155t Syngnathus leptorhyncus (bay pipefish), 18t, 95f, 111f, 429, 479; in bays and estuaries, 126t, 128f, 129f, 132f, 134f, 136t, 137f, 145t; in surf zone, 151, 152f, 153t; trophic relations and, 396f, 402 Synodus spp. (lizardfishes), 277f, 280, 294, 298, 329, 353t, 506, 519t; on continental shelf, 175, 177t, 180t; S. evermanni (spotted lizardfish), 177t, 182f, 183f, 195f, 196f; S. scituliceps (lance lizardfish), 177t, 181f, 194f Synodus lucioceps (California lizardfish), 18t, 98f, 155t, 538t; on continental shelf, 173, 177t, 181f, 182f, 183f; foraging guilds, 192f, 194f, 195f, 196f; larval stages of, 277, 293, 295f, 301, 302f; trophic relations and, 395, 397f, 398f Taaningichthys bathyphilus, 351t, 366t Tactostoma macropus (longfin dragonfish), 351t, 359, 370 Talismania bifurcata (threadfin slickhead), 349t, 353t tan bristlemouth (Cyclothone pallida), 350t Taractes longipinnis (bigscale pomfret), 327f, 330 Taraictichthys steindachneri, 20t, 25t Targett, Tim, 307 Tarletonbeania crenularis (blue lanternfish), 351t, 357f, 358, 359, 360t, 370f; larval stages of, 276t, 277–78f, 279, 306 Tautoga unitis (tautog), 498, 612t, 618 Tautogolabrus adspersus (cunner), 419 Tavolga, W. N., 493 taxonomic identifications, 231 tectonism, 33, 36 telemetry, 527–30, 539

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teleosts, 501, 504; evolution and, 55, 56–57, 68; reproduction and, 484, 488t temperate region, 330, 497; tropical region compared, 483, 502–4, 547 temperature of water, 495, 499; distribution and, 76; fisheries and, 567, 579, 584, 586; movement patterns and, 542; ocean surface warming, 5, 6, 242; submergence and, 96 Tenogobius sagittula, 18t, 25t Teo, S. L. H., 139 Terapon jarbua, 522t territoriality, 531f, 539; competition and, 450, 451, 453t, 454, 455–56 Terry, C., 230, 231 Tetragonurus spp. (squaretails), 324, 333, 523t; T. cuvieri (small squaretail), 18t, 23t, 328f, 330 Tetraodontidae (puffers), 77, 137f, 149, 321, 394. See also Sphoeroides spp. Tetrapterus angustirotris, 21t, 23t Tetrapterus audax (striped marlin), 21t, 24t, 89f, 395, 401f, 433; in pelagic habitat, 326f, 332, 337t Thalassoma bifasciatum (bluehead wrasse), 487, 488 Thalassoma lucasunum (Cortez rainbow wrasse), 235t Thaleichthys pacificus, 17t Theragra chalcogramma, 17t, 21t, 519t thermogeography, 5–6 The Theory of Island Geography (MacArthur & Wilson), 43 thickhead lanternfish (Hygophum atratum), 277, 279f, 280, 370f thicklip conger (Chiloconger dentatus), 177t, 183f, 195f, 196f Thomas, C. G., Jr and C. G. Thomas III, 589–90 Thompson, W. F., 572, 587 Thomson, C. J., 494, 567 thornback (Platyrhinoides triseriatus), 18t, 97f, 157t, 158t, 233t; on continental shelf, 177t, 181f, 194f thornyheads. See Sebastolobus spp. threadfin bass (Pronotogrammus multifasciatus), 7t, 178t, 183f, 196f, 255 threadfin dragonfish (Bathophilus filifer), 350t threadfin grenadier (Coryphaenoides filifer), 353t, 369 threadfin sculpin (Icelinus filamentosus), 18t, 22t, 178t, 183f, 196f, 258t threadfin shad (Dorosoma petenense), 161t, 612t, 613f, 617 threadfin slickhead (Talismania bifurcata), 349t, 353t threebanded butterfyfish (Chaetodon humeralis), 20t, 24t, 235t three-spine stickleback (Gasterosteus aculeatus), 18t, 153t, 520t; in bays and estuaries, 126t, 128f, 129f, 132f, 142f; reproduction and, 488, 489, 491–92 thresher shark (Alopias vulpinus), 19t, 233t, 542; bigeye thresher, 89f, 326f, 337t; and commercial fishing, 579, 591 Thunnus spp. (tuna), 322–23, 335t; bigeye tuna, 89f, 326f, 337t; fisheries and, 333f, 337t, 570–77, 579, 581; seasonal movement of, 530, 542; T. obesus, 20t, 23t; T. orientalis, 20t, 23t Thunnus alalunga (albacore), 18t, 23t, 89f, 389, 401f; fisheries and, 573–74, 575, 584; in pelagic zone, 326f, 327f, 330, 336t, 337t; seasonal movement of, 536t, 542 Thunnus albacares (yellowfin tuna), 21t, 24t, 89f, 523t, 540, 573; in pelagic zone, 326f, 337t

Thunnus thynnus (bluefin tuna), 89f, 401f, 542; commercial fishing of, 573, 578; feeding behavior of, 389, 390; in pelagic zone, 326f, 330, 336t, 337t Thyrsites atune, 523t tidepool blennie, 334f tidepool sculpin (Oligocottus maculosus), 17t, 91f, 500t, 507, 533t; in rocky intertidal zone, 207, 209t, 215t, 216f, 217f, 218 tidepool snailfish (Liparis florae), 17t, 90f, 215t, 216f, 238f tidewater goby (Eucyclogobius newberryi), 5, 18t, 132f, 614; in bays and estuaries, 126t, 128f, 129f, 130t, 134f; phylogeographic structure, 34t, 38, 39f Tijuana Estuary, 135–36, 144f, 400 Tilapia spp. (cichlids): Oreochromis mossambicus (Mozambique tilapia), 485, 612t, 617; Oreochromis niloticus (Nile tilapia), 393; T. zilli (redbelly tilapia), 485, 522t, 612t, 613f, 617 timed transects, for density estimate, 230–31 Tinbergen, N., 489 toadfishes (Batrachoididae), 106t, 178t, 180t, 210, 532t; reproduction and, 493, 503, 504, 506 Todd, E. S., 472 tomcod (Microgradus proximus), 17t, 128f, 153t, 296f; on continental shelf, 174, 177t, 181t, 182f, 183f; foraging guild, 194f, 195f tonguefishes (Cynoglossidae), 298, 329; on continental shelf, 175, 179t, 180t, 189. See also Symphurus spp. topside lampfish (Notorhynchus valdiviae), 351t, 370f topsmelt. See Atherinops affinis Torpedinidae (torpedo electric rays), 175, 177t, 180t Torpedo californica (Pacific electric ray), 18t, 95f, 156f, 233t, 348, 405, 518t; on continental shelf, 177t, 183f, 196f; hunting behavior of, 433f; movement patterns of, 538t, 540, 542, 549; in pelagic zone, 335, 337f Trachichthyidae, 66 Trachinotus paitensis, 20t, 25t Trachinotus rhodopus, 20t, 24t Trachinus vipera, 522t Trachipterus altivelis (king-of-the-salmon), 20t, 327f, 332 Trachipterus fukuzaki, 21t, 25t Trachurus symmetricus (jack mackerel), 19t, 23t, 77, 96f, 172, 432f, 521t; abundance of, 336t; in coastal pelagic zones, 154, 157t, 159f, 160t; commercial fishing of, 570, 571, 573, 574, 576, 578, 579, 591; DDT levels in, 601; feeding of, 406; genetic divergence in, 621; in kelp bed/rocky reef, 234t, 239f, 241f; larval stages of, 276t, 277f, 279f, 305; as pelagic species, 330, 332f, 335t, 337t; recreational fishing of, 581, 582; schooling by, 324; trophic relations and, 401f treefish (Sebastes serriceps), 18t, 23t, 67, 67f, 162t, 537t; in kelp bed/rocky reef, 92f, 234t, 237f, 239f; trophic relations and, 400f, 405 triacylglycerols, deep water buoyancy and, 365–68 Triakidae (hound sharks), 233t; Galeorhinus galeus (soupfin), 19t, 89f, 233t, 337t, 576. See also Mustelus spp. Triakis semifasciata (leopard shark), 19t, 95f, 158t, 233t, 518t; in bays and estuaries, 127t, 128f, 132f; movement of, 527,

538t; in surf zone, 150t, 151, 153, 156f, 157t Trichiurus nitens (cutlassfish), 20t, 25t, 327f, 332 Trichodon trichodon, 17t, 522t Trichonotus filimentosus, 522t Tridentiger spp. (gobies), 131, 614; T. barbatus (shokihaze goby), 130t, 131, 612t, 614; T. bifasciatus (shimofuri goby), 130t, 131, 142f, 612t, 614; T. trigonocephalus (chameleon goby), 612–13, 612t triggerfishes (Balistes spp.), 175, 179t, 180t, 236t; B. polylepis (finescale triggerfish), 21t, 23t, 179t, 194f, 236t, 309f, 485, 523t Triglidae (sea robins), 176, 178t, 180t, 181f. See also Prionotus spp. Triphoturus mexicanus (Mexican lampfish), 351t, 357f, 359, 362, 366t, 368, 370f; larval forms of, 276t, 277f, 280, 286, 290, 291f, 293–94, 298, 305; trophic relations of, 402f Triphoturus nigrescens (highseas lampfish), 277 Triphoturus oculeus (lampfish), 277 trophic interactions, 394–407; in bays and estruaries, 396–98, 400–402; categories, 394–95; continental shelf, 397f–398f, 402–3; decline in, 631–32; deep midwater, 402f, 406; disturbance and, 471, 476; epipelagic fishes, 401f, 405–6; ichthyoplankton, 307–13; in kelp bed/rocky reef, 400f, 404–5; pollutants and, 598, 601; rocky intertidal, 399f, 403 tropical hatchetfish (Argyropelecus lychnus), 350t, 356f, 359, 366t tropical region, 331–33; temperate region compared, 483, 502–4, 547 true smelts (Osmeridae), 72, 73, 77, 120, 128–29, 149; on continental shelf and slope, 175, 177t, 180t; larval stages of, 296, 304f tubenose poacher (Pallasina barbata), 17t, 153t tubeshoulders (Platytroctidae), 350t, 354, 355f, 369, 519t tubesnout (Autorhynchus flavidus), 18t, 91f, 111f, 504, 520t; in kelp bed/rocky reef, 233t, 240f, 243f tuna. See Thunnus spp. turbots, 193. See also Pleuronichthys spp. Turner, Charles H., 227 two-line eelpout (Bothrocara brunneum), 18t, 22t, 354t, 372f twospine bigscale (Scopelogadus mizolepsis bispinosus), 352t, 361, 365, 366t Typhlogobius californiensis (blind goby), 19t, 24t, 211, 497, 523t; symbiotic relations of, 559–60, 560f Ugoretz, J., 230 Ulvicola sanctaerosae (kelp gunnel), 18t, 24t, 72, 72f, 236t umbrellamouth gulper (Eurypharynx pelecanoides), 348, 519t Umbrina roncador (yellowfin croaker), 19t, 95f, 127t, 134f, 145t; fisheries and, 581, 585t, 587; movement patterns of, 536t, 546; in surf zone, 150t, 151f, 154, 157t, 160t; trophic relations and, 396f, 402 U. S. Bureau of Fisheries, 572 United States Environmental Protection Agency (USEPA), 168, 170, 602 Upogebia pugettensis (mud shrimp), 559 upwelling systems, 503–4 Uranoscopidae (stargazers), 175, 180t, 522t, 604 Uraspis secunda, 20t, 25t

INDEX

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Urechis caupo (fat inkeeper worm), 559, 559f Urolophidae (round stingrays), 175, 177t, 180t Urolophus/Urobatis halleri (round stingray), 20t, 233t, 397f, 429, 518t, 540; in bays and estuaries, 95f, 127t, 129f, 136t, 137f, 145t; on continental shelf, 173, 177t, 181f; foraging guilds, 194f, 195f; in surf zone, 150t, 151, 157t, 158t Urophycis chuss (red hake), 472 Uticina lofotensis (white-spotted rose anemone), 561f Utter, F., 31 Van Holle, D., 611 Vehrencamp, S. I., 488 Venefica tentaculata, 519t vermilion rockfish (Sebastes miniatus), 18t, 22t, 99f, 234t, 493, 631; in deep rock habitat, 255, 260f, 263t; fisheries and, 585t, 586 vertical distributions, 206–8, 305–6, 363 Vetter, R. D., 540 vicariance, gene flow and, 50 Vinciguerria lucetia (Pacific lightfish), 305, 350t, 368, 370f; larval stages of, 276t, 277f, 279f, 280, 282f, 286, 292f Vinciguerria nimbaria, 519t vision, 307, 343 viviparity, 483–84, 486, 502, 503, 504, 507 Volpe, J. P., 618 wahoo (Acanthocybium solandri), 333, 337t wakasagi (Hypomesus nipponensis), 130t, 131, 612t, 615–16 Wakefield, W. W., 371 Walker, Boyd W., 76, 152 Walker, H. J., 297, 298 wall-eye surfperch (Hyperprosopon argenteum), 18t, 67f, 95f, 186, 397f, 585t, 631; activity patterns of, 533t, 544, 546; in coastal pelagic zone, 155t, 157t, 159f, 160–61t; in kelp bed/rocky reef, 235t, 239f; in surf zone, 150–51, 150t, 152f, 153t, 154f Waples, Robin S., 31, 375 warbonnets (Chirolophus spp.), 7t, 17t, 236t Warrant, E., 343 Watanabe, H., 361 Watson, W., 6, 291, 297–98, 369 wax esters, bouyancy and, 367–68 Weber, M. L., 589 Weitzman, S. H., 348 western mosquitofish (Gambusia affinis), 126t, 535t, 612t, 613f, 616–17 whale shark (Rhinocodon typus), 20t, 25t, 325, 331f, 333, 518t; movement of, 540 whalesucker (Remilegia australis), 324 whip nose anglerfish (Gigantactis sp.), 358 White, B. N., 621 White, P. S., 466 white croaker. See Genyonemus lineatus white sea bass (Atractoscion nobilis), 19t, 96f, 111f, 336t, 337t, 432, 603; and commercial fishing, 574, 579, 587; in kelp bed/rocky reef, 235t, 239f, 241f; larval stages of, 274, 275f; pollutants and, 598, 603; and recreational fishing, 580, 582, 584; and reproduction, 494; in surf zone, 151, 154f, 155t, 156f, 157t, 158t white seaperch. See Phanerodon furcatus white shark (Carcharodon carcharias), 20t, 22t, 89f, 337t, 390; movement of, 530, 534t, 542; pollution and, 601 whitespeckled rockfish (Sebastes moseri), 100f, 255

660

INDEX

white sturgeon (Acipenser transmontanus), 18t, 125, 126t, 128f, 518t white suckerfish (Remorina albescens), 325 whitetail tonguefish (Symphurus oligomerus), 179t, 183f, 196f whitetip shark (Carcharhinus longimanus), 19t, 25t, 328f, 331 widow rockfish, 99f, 257, 260f, 263t, 589 Williams, E. H., 173 Williams, G. C., 207, 543 Wilson, Allan, 27 Wilson, E. O., 46 Wilson, Raymond R., Jr., 6, 369, 373, 374, 375, 377 wolf-eel (Anarrhichthys ocellatus), 17t, 75, 75f, 91f, 255; in kelp bed/rocky reef, 236t, 240t; reproduction and, 485, 497, 498, 522t Wood, R., 56 wooly sculpin (Clinocottus analis), 35t, 90f, 399f, 403, 628; hypoxia and, 468; parental care in, 500t, 507; in rocky intertidal zone, 215, 216f, 217f, 219, 222f wrasses, 437; bleeding wrasse (Polylepium cruentum), 179t, 183f, 196f; Decodon melasma (blackspot wrasse), 7t, 20t, 24t; Thalassoma spp., 235t, 487, 488. See also Halichoeres spp.; Labridae (wrasses) Xanthichthys mento, 19t, 24t Xeneretmus spp. (poachers): X. latifons (blacktip poacher), 18t, 23t, 98f, 178t, 183f, 192f, 196f, 532t; X. leiops, 17t, 21t; X. ritteri (stripefin poacher), 18t, 24t, 98f, 178t, 183, 185f, 197f; X. triacanthus, 18t, 23t Xenistius californica (salema), 20t, 74, 111f, 136t, 145t, 154; activity patterns of, 534t, 548; cleaner behavior, 556f, 557t; in coastal pelagic zone, 157t, 159f, 160t; on continental shelf, 178t, 181f; foraging guilds, 194f, 195f; in kelp bed/rocky reef, 235t, 237f, 239f, 241f; as nocturnal predator, 66, 67f, 95f Xererpes fucorum (rockweed gunnel), 18t, 90f, 111f; feeding of, 399f, 403; in rocky intertidal zone, 207, 208, 209t, 215t, 216f, 220f Xiphias gladius (swordfish), 20t, 23t, 89f, 523t, 534; and commercial fisheries, 574, 579; diel movements of, 543; feeding of, 395, 433; in pelagic zone, 323, 326f, 330, 332, 337f; trophic relations and, 401f, 405, 406 Xiphister atropurpureus (black prickleback), 18t, 90f, 236t, 498, 522t; in rocky intertidal zone, 209t, 210, 211f, 215t, 216f; trophic relations and, 394, 399f, 403 Xiphister mucosus (rock prickleback), 18t, 90f, 236t, 498, 522; in rocky intertidal zone, 207, 209t, 212, 215t, 216f, 219, 220f; trophic relations and, 394, 399f, 403 Xystreurys liolepis (fantail sole), 19t, 145t, 155t, 158t; on continental shelf, 179t, 181f, 182f; foraging guilds, 192f, 194f, 195f; larval stages of, 293, 295f, 300, 301f, 302 yellowchin sculpin (Icelinus quadriseriatus), 19t, 23t, 398f, 403, 532t; on continental shelf, 98f, 173, 178t, 182f; foraging guilds, 192f, 195f yelloweye rockfish (Sebastes ruberrimus), 17t, 255, 260f, 263t

yellowfin croaker (Umbrina roncador), 19t, 95f, 127t, 134f, 145t; fisheries and, 581, 585t, 587; movement patterns of, 536t, 546; in surf zone, 150t, 151f, 154, 157t, 160t; trophic relations and, 396f, 402 yellowfin fringehead (Neoclinus stephensae), 19t, 23t, 236t, 238f, 247 yellowfin goby (Acanthogobius flavimanus), 95f, 533t, 612t, 613–14, 618; in bays and estuaries, 126t, 130t, 131, 132f, 142f yellowfin tuna (Thunnus albacares), 21t, 24t, 89f, 326f, 337t, 523t, 540, 573 yellowstripe grunt (Haemulopsis axillaris), 178t, 182f, 194f, 195f yellowtail rockfish (Sebastes flavidus), 17t, 99f, 234t, 520t, 589; in deep rock habitat, 260f, 263t; movement of, 537t, 539 yellowtail (Seriola lalandi), 18t, 23t, 87, 89f, 330, 332f; abundance of, 336t, 337t, 628; commercial fisheries and, 574, 575, 587; hunting behavior of, 62, 432f; in kelp bed/rocky reef, 234t, 241f; recreational fishing of, 580, 581f, 582, 583, 584, 585t, 586; trophic relations and, 401f, 406 Yoklavich, M. M., 123, 133, 264 Yoshiyama, R. M., 212, 214, 217, 218, 220, 221, 395 Young, P. H., 497 young-of-year (YOY), 83, 187, 248, 432, 474–75; rockfishes, 83, 260, 261, 262f, 263t, 440–41 Zalembius rosaceus (pink sea perch), 19t, 23t, 258, 263t, 533t; on continental shelf, 98f, 176, 178t, 182f, 183f; foraging guild, 192f, 195f, 196f; trophic relations and, 398f, 403 Zalieutes elater, 20t, 24t, 520t Zanclus cornutus, 523t Zaniolepis frenata (shortspine combfish), 19t, 23t, 100f, 102, 105t, 263t, 538t; on continental shelf, 178t, 183f, 258; foraging guild, 192f, 196f Zaniolepis latipinnis (longspine combfish), 19t, 23t, 98f, 195f, 263t, 398f, 538t; on continental shelf, 176, 178t, 182f, 192f, 258 Zaniolepis spp. (combfish), 186, 255 Zaprora silenus, 17t, 21t, 522t Zapteryx exasperata (banded guitarfish), 20t, 135t, 137f, 233t; on continental shelf, 177f, 183f, 194, 196f zebra goby (Lythrypnus zebra), 19t, 23t, 92t; activity patterns of, 534t, 545; in kelp bed/rocky reef, 236t, 238f zebraperch (Hermosilla azurea), 15, 19t, 87, 92f, 544, 630; genetic characteristics of, 44f, 45t, 46t; in harbors, 157t, 158t, 162t; in kelp bed/rocky reef, 92f, 235t, 237f, 241f, 404; symbiotic relations and, 556f, 558; trophic relations and, 394, 400f Zedler, Joy B., 135–36, 397 Zenopsis nebulosa, 17t, 23t, 520t Zerba, K. E., 241, 244 Zesticelus profundorum, 18t, 23t Ziegler, A. M., 68 Zoarcidae (eelpouts), 9f, 10f, 72, 352t, 354t, 355f, 505; on continental shelf, 172, 175, 179t, 180t; reproduction and, 485, 498, 522t. See also Lycodapus; Lycodes spp. zoographic barriers, 26–27 zooplanktivores, 73, 394–95, 548 Zostera marinus (eelgrass), 111, 134, 397, 475 Zu cristatus, 20t, 25t, 308f, 519t