Conus of the Southeastern United States and Caribbean [Course Book ed.] 9781400853014

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Conus of the Southeastern United States and Caribbean

•••

Conus of the Southeastern United States and Caribbean

••• ALAN J. KOHN

PRINCETON UNIVERSITY PRESS PRINCETON AND OXFORD

Copyright © 2014 by Princeton University Press Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540 In the United Kingdom: Princeton University Press, 6 Oxford Street, Woodstock, Oxfordshire OX20 1TW nathist.princeton.edu All Rights Reserved Library of Congress Cataloging-in-Publication Data Kohn, Alan J. Conus of the Southeastern United States and Caribbean / Alan J. Kohn. pages cm Includes bibliographical references and index. ISBN 978-0-691-13538-0 (hardback : alk. paper)  1.  Conus—Southern States—Classification.   2. Conus—Caribbean Area—Classification.  I. Title. QL430.5.C75K744 2014 594′.3—dc23 2013014701 British Library Cataloging-­in-­Publication Data is available This book has been composed in Palatino Printed on acid-­free paper. ∞ Printed in China 1 3 5 7 9 10 8 6 4 2

We come from halls of Academe And, on an inspiration, Alone, or in a learned team, Embark on publication. We seek to teach, or disabuse, Where controversy rages, And press our honest facts, or views, On academic pages. Then, if our theories endure, Maintained by erudition, Our luck and virtue should assure A third or fourth edition. For ultimately all should know The fruits of our endeavour. Though scholars come and scholars go, Our books go on for ever. —­Ralph Lewin, “The Book”

••• Often when I do a search, what is in a book is miles ahead of what I find on a Web site. —­Sergey Brin

••• Study nature, not books. —­Louis Agassiz

•••

Contents ••

1 2 3 4 5

Preface

ix

Acknowledgments

xi

Introduction

1

Abbreviations Used in the Text

7

Setting the Stage: Approaches

9

Setting the Stage: The Geological Theater and the Evolutionary Play

18

This Book and How to Use it

32

Behind the Scenes: Technical Aids to the Species Accounts

44

Species Accounts

56

Conus granulatus Linnaeus Conus glenni Petuch Conus ritae Petuch Conus jaspideus Gmelin Conus pealii Green Conus stearnsii Conrad Conus pusio Hwass in Bruguière Conus mindanus Hwass in Bruguière Conus bahamensis Vink and Röckel Conus puncticulatus Hwass in Bruguière Conus mazei Deshayes Conus rainesae McGinty Conus janowskyae (Tucker and Tenorio) Conus armiger Crosse Conus sauros Garcia Conus lenhilli Cargile Conus delessertii Récluz Conus centurio Born Conus cedonulli Linnaeus Conus pseudaurantius Vink and von Cosel

56 62 64 67 74 80 84 89 95 97 106 114 117 120 126 129 130 137 146 156

viii  • Contents Conus aurantius Hwass in Bruguière Conus mappa [Lightfoot] Conus curassaviensis Bruguière Conus regius Gmelin Conus cardinalis Hwass in Bruguière Conus arangoi Sarasua Conus explorator Vink Conus hieroglyphus Duclos Conus ziczac Megerle von Mühlfeld Conus sahlbergi da Motta and Harland Conus daucus Hwass in Bruguière Conus amphiurgus Dall Conus sanderi Wils and Moolenbeek Conus eversoni Petuch C. ceruttii Cargile Conus ignotus Cargile Conus cancellatus Hwass in Bruguière Conus stimpsoni Dall Conus villepinii Fischer and Bernardi Conus attenuatus Reeve Conus flavescens Sowerby I Conus cingulatus Lamarck Conus largillierti Kiener Conus anabathrum Crosse Conus gibsonsmithorum Petuch Conus garciai da Motta Conus harlandi Petuch Conus sunderlandi Petuch Conus spurius Gmelin Conus mus Hwass in Bruguière Conus patae Abbott Conus ermineus Born Conus lightbourni Petuch Nomina dubia

160 164 174 178 188 204 206 209 212 217 226 239 250 255 257 260 264 274 281 288 296 302 306 312 324 329 334 340 345 358 363 367 379 382

6

Synthesis and Conclusions

395

Appendix 1.

Molecular Phylogeny of Conus

419

Appendix 2.

Morphology-­Based Phylogeny of Conus

422

General Glossary

425

Bibliography

431

Index of Species-group Names

449

General Index

453

Preface ••

T

his book explores the taxonomy and relationships of species of the marine snail Conus. Broadly considered, it is the most diverse, species-­ rich genus of animals in the sea and a most attractive as well as scientifically and biomedically important group of gastropod molluscs. Here I revise the taxonomy of the species that occupy the Western Central Atlantic and Caribbean region, home to arguably the least known assemblage of species in a genus whose distribution is worldwide but predominantly tropical. As the first attempt in 70 years to treat the genus as a whole in the region, this book includes accounts of nearly twice as many species as the earlier report (Clench 1942). To the extent possible, the book also addresses the roles of Conus in the ecology, evolution, and biogeography of the region; provides information to help understand an important branch on the tree of life; and contributes to documenting the diversity of life in the sea. The adverse effects on and threats to the world’s natural environments by human activities have stimulated biologists to evaluate biodiversity, particularly in places where it has been underappreciated in the past. This also motivated the research that resulted in this book. In the less than 20 years since its predecessor on the Indo-­West Pacific Conus fauna appeared (Röckel, Korn, and Kohn 1995), technological innovations have transformed the practice of systematics. The most profound changes have been new insights into both classification and phylogeny from knowledge of molecular genetics, and the burgeoning of computerized and web-­ based methods to more efficiently manage, present, and communicate information. I have attempted to take advantage of these advances to incorporate both molecular genetic information and quantitative morphometric methods into conclusions on the validity of described species and interpretations of their evolutionary relationships. I apply and statistically analyze morphometry of shells and of radular teeth, the hollow spears that Conus uses to inject toxic venoms in its rapid-­strike,

chemically aided prey-­capture method. Descriptions of these traits should help readers assess differences among species and their genealogic relatedness. These are nontraditional character sets that are not usually found in books on the taxonomy of shelled molluscs. In order to link scientific research more closely with public understanding, I have attempted to explain these new approaches in order to increase their accessibility and use to nonspecialist readers. In addition, unlike earlier identification guides, this book takes advantage of the resources offered by the worldwide web to complement the printed version. While the book adopts the general format of Röckel, Korn, and Kohn (1995), the new sources of data have begun to help unravel the especially challenging taxonomic problems of the Western Atlantic species. The Conus Biodiversity Website (http:// biology.burke.washington.edu/Conus/) also serves a number of complementary functions to the book. It is an accessible repository of digital images of primary type specimens of most described species, it provides the original descriptions of most species in pdf format, and it is linked to the National Center for Biotechnology Information (NCBI) (www.ncbi.nim .nih.gov) to access gene sequences of species across the genus. Updates and corrections will be posted to the Conus Biodiversity Website as new information emerges, as they have been for the earlier book. In addition, databases listing all specimens used in the comparative morphological and molecular analyses and in establishing the geographic and bathymetric distributions are available as electronic supplementary material, accessible at http://press.princeton .edu/titles/10229.html. The electronic supplementary material also includes summarizing graphs and statistical analyses of these data that support the taxonomic conclusions reached in the text. In the spirit of the epigrammatic epigraphs prefacing this Preface, I have sought to write a scientifically accurate yet accessible work useful to a diverse readership. However, I have intended to speak

x  • Preface particularly to present and future biologists, especially those interested in biodiversity and its evolution. I hope this book will encourage students with fresh perspectives to make new observations and studies that will overcome the limitations of our current knowledge of the systematics, ecology, and evolutionary history of a scientifically and medically important taxon. A number of promising research projects lurk in the unanswered broader questions raised—­for example the unexplored relationships of specificity of venom actions, genetic structure of populations, evolution of life history traits, and geographic distributions of species. Others will perhaps emerge from the incidental reports of unusual events in the lives of Conus, such as pearl secretion, masculinization of

females by endocrine disruptors pervasive in 21st-­ century environments, relations with symbionts, survival from near-­fatal predator attack, and injury to humans from venom injection. Thus I also direct the book to other marine scientists, neurobiologists, natural products chemists interested in sources of pharmaceuticals from marine organisms, to nonscientist conchologists and conservationists, and to all who are attracted by the wondrous variety and elegance of molluscs and their shells. As Godfray and Knapp (2004) stated, professional and amateur biologists and naturalists alike want and need “stable, informative and accessible classifications that enable easy identification.” That may not have been attained, but progress along the road in that direction has been the goal.

Acknowledgments ••

T

his project originated with an invitation from José Leal to serve as the R. T. Abbott Visiting Curator at the Bailey-­Matthews Shell Museum in Sanibel, Florida, in November, 2000. My research there made it clear that a systematic revision of the Western Atlantic Conus was needed, and that it was a major task that could not be undertaken without considerable external financial support. Award of a National Science Foundation grant (No. 0316338), including a Consortium of European Taxonomic Facilities supplement, supported much of the research leading to this book. At the University of Washington, Trevor Anderson created the project’s web site and served outstandingly as research technician. Postdoctoral research associates Thomas Duda and Christopher Meyer obtained all of the molecular genetic data and carried out the phylogenetic analyses. The following University of Washington undergraduates participated in data analysis as research students and research assistants: Amanda Bruner, Kathryn Engel, Emily Evenson, Joshua Kubo, Megan Mach, Jennifer Marsh, Amber Matheny, Brenda Mathis, Daniel Okamoto, Michael Queisser, Kamila Rikhsieva, Pairin Schofield, Jessica Smith, Rachel Winstedt, Jihye Won, and Matthew Zhang, as well as a then Yale undergraduate, Kaitlin Curran. Kathy Carr, University of Washington Biological Sciences Librarian, assisted in providing access to resource materials. This work could not have been completed without the very generous assistance of numerous colleagues in the United States, Latin America, Europe, and Japan. Danker and Elise Vink generously accommodated my study of the Vink collection in their home in Curaçao before donating it to Naturalis, the National Museum of Natural History in Leiden. Emilio Garcia was particularly helpful in providing access to specimens and supplied many images for publication. John Tucker and Manuel Tenorio generously shared specimens, images, and evidence concerning taxonomy. Others who provided helpful

information and discussion, and generously made specimens and images available for reproduction in cases of scarce representation in museums and of living specimens, include Cynthia Abgarian, Carlos Afonso, Randy Allamand, Adolfo Borges, Christopher Boyko, Marcus Coltro, Juan Manuel Díaz, Gene Everson, Marien Faber, Bill Fenzan, Mike Filmer, Bill Frank, Frank Frumar, Richard Goldberg, Jon Greenlaw, Wayne Harland, Thomas Honker, Manuel Vinent, Afonso Jório, Paul Kersten, Lee Iturralde-­ Kremer, Harry Lee, Virginia Orr Maes, Robert Masino, Alexander Medvedev, Paula Mikkelsen, Patricia Miloslavich, Antonio Monteiro, Marc Nathanson, Bette Nybakken, Howard Peters, Richard Petit, Kenneth Piech, Andre Poremski, Colin Redfern, Dieter Röckel, Emilio Rolán, Maria Cristina Sanchez Sarasua, George and Korina Sangiouloglou, Stanley Taylor, Charlotte Thorpe, David Touitou, Amelia Tripp, Everett Turner, Roberto Ubaldi, and Robert Work. I thank Elaina Jorgensen, who prepared the range maps, and along with Rüdiger Bieler, Elizabeth Boulding, Fabio Moretzsohn, and Gary Rosenberg also provided cogent comments that improved the text; Ursula Smith for suggesting the measure of typical shell length used; and Marla Coppolino, who assisted with preparation of some of the text-­figures. Klaus Groh (Conchbooks) permitted the use of material from Röckel, Korn, and Kohn (1995). At Princeton University Press, Dimitri Karetnikov, illustrations manager, was especially helpful in advising about and ensuring quality control of the illustrations, and Jessica Massabrook executed some of the improvements. Sheila Ann Dean, copyeditor, corrected a number of errors in the author’s manuscript. Mark Bellis, production editor, and Robert Kirk, acquisitions editor, provided assistance and discussion throughout the project. Specialists on other animal groups who generously helped with identifications of fauna associated with Conus include Stephen Cairns, Gerhard Jarms and Wolfgang Sterrer (Cnidaria); Darryl Felder and

xii  • Acknowledgments Patsy McLaughlin (Crustacea); Harry Lee, Rüdiger Bieler, Matthew Campbell, and Lyle Campbell (Mollusca); and Theodore Pietsch, William Smith-­Vaniz, David Johnson, and Ralf Britz (fishes). Researchers and curators at the following museums and research and academic institutions generously provided access to study material: Academia Canaria de la Lengua, Spain: Juan José Bacallado Academy of Natural Sciences of Drexel University, Philadelphia: Gary Rosenberg, Paul Callomon, Robert Robertson American Museum of Natural History, New York: Paula Mikkelsen, Marla Coppolino, Ross MacPhee, Bushra Hussaini, Sarfraz Lodhi Bailey-­Matthews Shell Museum, Sanibel, Florida: José Leal Bermuda Aquarium, Natural History Museum and Zoo: Wolfgang Sterrer, Lisa Greene Burke Museum of Natural History and Culture, University of Washington, Seattle: Robert Faucett, Ronald Eng Carnegie Museum of Natural History, Pittsburgh: Tim Pearce Department of Geology, San José State University, California: Jonathan Hendricks Delaware Museum of Natural History, Wilmington: Elizabeth Shea, Leslie Skibinski Field Museum of Natural History, Chicago: Rüdiger Bieler, Jochen Gerber Florida Fish and Wildlife Research Institute, St. Petersburg: Sandra Farrington, Scott Woodruff. Florida Museum of Natural History, Gainesville: Gustav Paulay, John Slapcinski, Roger Portell Harte Research Institute, Texas A&M University, Corpus Christi: Fabio Moretzsohn, Noe Barrera Houston Museum of Natural Science: Tina Petway Institute of Malacology, Tokyo: Sadao Kosuge Instituto de Oceanologia, Havana: José Espinosa Instituto de Neurobiología, Universidad Auto­ nóma de México: Edgar Heimer de la Cotera Instituto Alexander von Humboldt, Bogota: Juan Manuel Díaz Löbbecke Museum, Düsseldorf: Jürgen Jungbluth Museu Nacional, da Universidad Federal do Rio de Janeiro: Renata dos Santos Gomes, Paolo Márcio Costa. Museu Oceanográfico “Prof. E. C. Rios,” Rio Grande, Brazil: Paula Spotorno de Oliveira Muséum d’Histoire Naturelle, Geneva: Yves Finet Muséum National d’Histoire Naturelle, Paris: Philippe Bouchet, Rudo von Cosel, Virginie Héros

Museum of Comparative Zoology, Harvard University, Cambridge: Adam Baldinger, Murat Recevik Museum Victoria, Melbourne: Ursula Smith National Museum of Natural History—­Naturalis, Leiden: Jeroen Goud, Frank Wesselingh, Bert Hoeksema, Willem Renema National Museum of Natural History, Smithsonian Institution, Washington, DC: Christopher Meyer, Jerry Harasewych, Ellen Strong, Stephen Cairns, Alan Kabat, Yolanda Villacampa, Tijuana Nickens, Paul Greenhall National Museum of Wales, Cardiff: Harriet Wood, Mary Seddon, Graham Oliver Naturhistorisches Museum Basel: Olivier Schmidt, Felix Wiedenmeyer, Walter Etter Naturhistorisches Museum, Vienna: Anita Eschner North Carolina State Museum of Natural Sciences, Raleigh: Arthur Bogan, Jamie Smith Peabody Museum of Natural History, Yale University: Eric Lazo-­Wasem Rosenstiel School of Marine and Atmospheric Sciences, University of Miami: Nancy Voss Santa Barbara Museum of Natural History, Santa Barbara: Henry Chaney, Patricia Sedhagian, Daniel Geiger, Eric Hochberg Senckenberg Research Institute and Natural History Museum, Frankfurt: Ronald Janssen, Rudo von Cosel Smithsonian Tropical Research Institute, Panama: Félix Rodriguez, Biff Bermingham, Aaron O’Dea Staatliches Museum für Naturkunde, Stuttgart: Hans-­ Jörg Niederhöfer, Ira Richling, Annette Schultheiss Texas A&M University, College Station: Mary Wicksten, Heather Prestridge Texas A&M University, Corpus Christi: Fabio Moretzsohn, Noe Barrera. The Natural History Museum, London: Kathie Way, John Taylor, Roberto Miquez Universidad Central de Venezuela: Adolfo Borges, Cecilia Naranjo Universidad Nacional Autónoma de México, Querétaro: Edgar Heimer de la Cotera, Manuel Aguilar Universidad de Cadiz, Spain: Manuel Jimenez Tenorio Universidad de Oviedo, Spain: Jesus Ortea Universidade do Algarve, Portugal: Carlos Afonso Universität Hamburg, Germany: Klaus Bandel University of Louisiana at Lafayette: Emilio Garcia, Darryl Felder, Suzanne Fredericq University of Michigan Museum of Zoology, Ann Arbor: Thomas Duda

Acknowledgments 

University of North Carolina Institute of Marine Sciences, Morehead City: Glenn Safrit University of South Carolina Upstate, Spartanburg: Lyle Campbell University of Utah: Baldomero Olivera, Maren Watkins Uppsala University Museum of Evolution, Sweden: Mats Eriksson Zoological Museum, University of Copenhagen, Denmark: Antonia Vedelsby, Kathe Jensen, Jørgen Knudsen, Ole Tendahl, Danny Eibye-­Jacobsen Zoologisch Museum, University of Amsterdam, Netherlands: Robert Moolenbeek, Bram van der Bijl

• xiii

Lanna Cheng graciously permitted use of the poem “The Book” by her late husband Ralph Lewin, and published in Verses (Halobates Press, La Jolla, CA, 2008). The quotation from Sergey Brin appeared in an interview with Motoko Rich published in The New York Times, January 5, 2009. Louis Agassiz’s dictum was posted on the wall of the first seaside teaching laboratory, the Anderson School of Natural History. He founded the school at Penikese Island, Massachusetts, in 1873, and after its closure, the sign was moved to the new nearby Marine Biological Laboratory at Woods Hole (McMurrich 1892; Lillie 1944).

Conus of the Southeastern United States and Caribbean

•••

Introduction ••

The Purposes of This Book The main purpose of this book is to present a systematic revision and to facilitate identification of the extant species of Conus in the Southeastern United States and Caribbean region. To accomplish this goal, each species is discussed and described objectively and consistently, including estimating within-­species variation, and as clearly as possible differentiating each from its most similar congeners. In biology a picture is worth far more than the proverbial thousand words, and more than 2100 color photographs of shells, on 109 plates, an average of two per species, seek to illustrate the extent of within-­species variation and between-­species differences. Both the images and the species accounts emphasize the characteristics of the shells of Conus, because most users of the book will probably seek to identify these most durable parts of the animals. In some cases, less commonly used characters, such as shell and radular tooth morphometry, are also described quantitatively. More than 100 text-­figures illustrate these and other aspects of Conus biology, which are generally not remarked on. They include photographs of living animals of about 40% of the species covered and radular teeth of about one-­third, as well as predation by and on Conus, egg capsules and larval shells, and other organisms associated with their shells. Similarities and differences in sequences of key genes are analyzed both as taxonomic characters and to evaluate evolutionary or phylogenetic relatedness among species. The rapid advance of molecular genetics during the late 20th and early 21st centuries belies the author’s statement just 17 years ago that “the application of additional character sets, e.g. from molecular biological study, awaits the next generation of researchers” (Röckel, Korn, and Kohn 1995, 13). Although other attributes of Western Atlantic Conus—for example, specific habitats, feeding biology, reproduction, and geographic distribution—are far less known than for their Indo-­West Pacific rela-

tives, available information on these biological features is included. Fossil shells of Conus in the Western Atlantic region extend back at least to the Late Eocene, about 37 million years ago (Hendricks and Portell 2008), but the geologic record of the genus still remains too poorly known to provide useful insights into the evolution of the region’s modern Conus fauna. For this reason, known fossils of extant species are mentioned, but other aspects of the geologic history of the genus are largely left to future researchers. Surveying and evaluating the validity of all available described or nominal species proposed for the focal geographic region is a necessary but secondary purpose of the book. Valid nominal species can only be justified by documenting those that are invalid. To accomplish this, separate accounts in Chapter 5 detail each species concluded to be valid, and list and discuss its synonyms and homonyms. The chapter ends with a table summarizing the concluded dispositions of all nominal species known to occur in the region covered by the book.

Why Is Conus Important? In addition to the fact that for centuries its shells have caught and held the attention of diverse enthusiasts—collectors, naturalists, and artists as well as biologists—Conus is important for several reasons, as discussed below. Biodiversity. Conus is the largest genus of marine animals, with probably more than 600 species worldwide in tropical and subtropical seas. It is thus a major contributor to biodiversity in the sea. Different marine habitats support different numbers of species, and diversity gradients observed in nature have aided testing hypotheses of the factors that determine why some environments support more co-­occurring species than others. Diversity of Conus is highest in the tropical Indo-­West Pacific region, where more

2  • Introduction  than 300 species occur. West Africa and its offshore islands constitute the next most diverse region, with 92 species (Monteiro et al. 2004). Remarkable and geologically recent adaptive radiations of Conus in the Cape Verde Islands contribute importantly to this diversity (Cunha et al. 2005; Cunha et al. 2008; Duda and Rolán 2005). The Western Atlantic and Caribbean area ranks third in diversity with at least the 53 species treated here. For reasons explained in Chapter 6, additional species are likely to be validated in the future, and others occur beyond the scope of this volume in Brazil. However, if one calculated diversity as the number of species per unit of the region’s ocean area, the Western Atlantic and Caribbean Conus fauna would probably be more diverse than that of the Indo-­West Pacific. The Eastern Pacific tropics are next with 44 species according to a very recent revision (Tenorio et al. 2012), followed by South Africa with about 20 species south of the Indo-­West Pacific region (Tenorio and Monteiro 2008). These figures sum to about 525 species worldwide. This is doubtless a conservative estimate, because new species continue to be discovered, including “cryptic species” whose shells are so similar as to be indistinguishable, but their genes show that they do not interbreed. Of all these regions, the Western Atlantic and Caribbean is taxonomically the least known. That fact most strongly dictated the need for this book. Distribution and abundance. Conus is exceedingly widespread, occurring primarily throughout the world’s tropical and subtropical oceans. The animals are relatively large (2–10 cm in shell length in the Western Atlantic region, and to 20 cm in the Eastern Atlantic and Indo-­West Pacific. In the latter region they are particularly abundant in intertidal and shallow subtidal habitats, and most diverse in depths of one to several meters of water. In the Western Atlantic and Caribbean, however, Conus is generally less abundant, less diverse and less conspicuous in intertidal and shallow subtidal environments. The preferred coral reef habitats are usually deeper, and a higher proportion of species is known only from deeper water than in the Indo-­West Pacific. In all geographic regions fewer species occur on continental shelves and slopes. None is known from deeper than 1000 m, less than one-­third of the world ocean’s average depth. Some species of Conus are narrowly restricted geographically, while others are extremely widespread. In the Indo-­West Pacific region, some species appear to maintain continuous populations from eastern Polynesia to the Red Sea, across an area comprising one-­fourth of the entire world ocean. Many species occupy rather high proportions of this broad expanse,

and a few cross the Eastern Pacific to the Pacific coast of Central America. In the Western Atlantic and Caribbean, a smaller proportion of species occupy the entire region, and many are more narrowly restricted, in some cases to one or a few islands or to narrow stretches of the continental coast. Ecology. In addition to its importance for general marine biodiversity, Conus is notable in that several to many very similar species often co-­occur in the same habitat. Up to 36 co-­occurring species are known to inhabit single Indo-­West Pacific coral reefs. Ecological studies of these assemblages have helped show why tropical reef-­associated habitats support such high biodiversity (e.g., Kohn 1959, 2001). The reduced abundance, diversity, and accessibility of Conus populations in the Western Atlantic have impeded comparable studies. Conus snails possess remarkable chemical expertise, and all whose diets are known are predatory carnivores. They inject potent venoms called conotoxins into their prey through a hypodermic needlelike radular tooth in a unique, rapid-­strike process. The venom quickly paralyzes the prey—usually a polychaete worm, fish, or another gastropod—that is then swallowed whole. In past studies, primarily in the Indo-­West Pacific and to a lesser extent in the Eastern Pacific, this has aided identification of the natural prey, led to the demonstration that different co-­ occurring species specialize on different food types, and enhanced understanding of coral reef ecology. As yet very few comparable data exist for Western Atlantic species. Neurobiology and medicine. Practical applications of Conus to neurobiology and medicine are increasing rapidly. All Conus species that have been examined produce the potent conotoxins mentioned above. Several of these small peptides have been sequenced and synthesized, some are now available commercially, and their genes are also being sequenced. Because most conotoxins block the transmission of nerve impulses, they are now widely used in research on neurobiology. During the 21st century, an average of 180 scientific reports on conotoxins have appeared every year. The use of conotoxin derivatives in medicine is also expanding rapidly. At least three are in current use, and one, a painkiller, has been marketed since its approval by the US Food and Drug Administration in 2004. Several others are in clinical trials, and about 300 patents for medical uses have been awarded. Evolution. Conus is not only the largest marine gastropod genus, but its number of species is increasing

Introduction 

more rapidly than any other whose speciation rates have been studied. Since its origin about 55 million years ago, the fossil record indicates that the number of species has doubled on the average every 6 million years, a diversification rate at least twice that of most tropical marine gastropod genera and families. Although Indo-­West Pacific Conus are currently better known, new species may well be evolving more rapidly in the Western Atlantic and Caribbean. Conservation. Science-­based knowledge of the most diverse genus of marine animals is essential for the maintenance and sustainable use of biodiversity. The most important practical applications of such information on Conus have been in neurobiology and medicine as mentioned above, but its susceptibility to very low concentrations of the endocrine disruptor tributyltin, until recently a common component of anti-­fouling paints applied to ships, has been demonstrated in widely separate parts of the world. This indicates its ability to serve as an early warning system for marine pollutants. Despite this abundant evidence of its importance, knowledge of the Conus fauna of the Western Atlantic region remains in a confused state. In fact, Todd et al. (2002, 572) noted when characterizing general molluscan taxonomy and its Neogene geological history in the modern Caribbean area, “taxonomic compendia covering the whole of this time interval or region are lacking” and “the difficulties inherent in accurate taxonomic compilation have, to our knowledge, previously gone unmentioned.” In addition, the first species-­level, molecular-­based phylogenetic hypotheses proposed for Conus (Duda and Palumbi 1999a, 1999b; Monje et al. 1999) appeared little more than a decade ago, and subsequent studies have expanded the coverage to about 40% of the species in the genus (Duda et al. 2001; Espiritu et al. 2001; Duda and Kohn 2005; Kraus et al. 2011; N. Puillandre, P. Bouchet, T. F. Duda, S. Kauferstein, A. J. Kohn, B. M. Olivera, M. Watkins, and C. Meyer, unpublished data1). The time is thus appropriate for systematic revisions in the light of modern molecular genetic analyses.

Why Is Systematics Important? Biological systematics is a rather broad term, often defined as the scientific study of diversity or, as Simpson (1961) put it even more broadly: “Systemat1  At the time of writing, a manuscript on species-­level molecular phylogeny of Conus by these authors was being prepared for publication. Hereafter it is referred to in the text as “Puillandre, et al. unpublished data.”

• 3

ics is the scientific study of the kinds and diversity of organisms and any and all relationships among them.” Taxonomy and classification are parts or subdivisions of systematics. Taxonomy is the naming, describing, and distinguishing of species, genera, and higher taxa of organisms. Classification is the hierarchical ordering of biological diversity in those categories. Taxonomy and classification are essential to enable us to understand and communicate about organisms and biodiversity. They also provide the basic data for interpreting the ecological interactions of species (e.g., Kohn 2001) and the hypotheses of phylogenetic, other evolutionary and biogeographic patterns (e.g., Duda and Kohn 2005). The species-­ level taxonomy of Conus is also increasingly important to human health (e.g., Olivera and Teichert 2007). Conus venoms are being modified as pain-­ killers and other medicines. Because every species has up to 100 or more active venom components, and those of every species differ, accurate documenting of source species is required. Thus taxonomy is important because it has a “multitude of end users” (Godfray and Knapp 2004). For Conus, these include amateurs and naturalists as well as professional biologists across the spectrum from basic physiologists, ecologists, biogeographers, and evolutionists, to more applied conservation biologists, resource managers, and natural product chemists. This book is thus directed to all with a desire to learn about the systematics of sea life.

The Geographic Scope of This Book The region covered by this book extends from the northern limits of Conus in the western North Atlantic Ocean, along the coast of the United States from North Carolina southward, including the offshore islands of Bermuda and encompassing the Gulf of Mexico and Caribbean Sea, eastward to French Guiana. It is almost exactly the area defined by the United Nations as the Western Central Atlantic or Major Fishing Area 31: “It includes the tropical and subtropical waters of the western Atlantic and is bordered by 35º north latitude corresponding to Cape Hatteras in North America, 40º west longitude, 5º north latitude corresponding to the coast of French Guiana of South America, and in the west by the corresponding coastline of South, Central, and North America” (Carpenter 2002, iv; www.fao.org /fishery/area/Area31/en). I define the southeastern United States as the Atlantic coastal region from North Carolina to southern Florida, as well as the Gulf of Mexico coastal region from southern Florida to the Texas-­Mexico

4  • Introduction boundary. The Gulf of Mexico continues southward to the Yucatan Peninsula. A recent compendium also considers the north coast of western Cuba as part of the Gulf of Mexico (Felder and Camp 2009). The Caribbean region is defined as the “Caribbean Sea and all of its contents, plus the facing continental margins of North, South, and Central America” (Iturralde-­Vinent and MacPhee 1999, 6). Although the Bahamas are geographically and geologically separate, I include them in the Caribbean region because their marine biota is closely related. The Caribbean region’s boundaries vary with different authors; Petuch (1987) defines it much more broadly (see Chapter 2 of this book). Subdivisions of the region also vary markedly among authors. I use a rather conservative system based on that of the Atlantic and Gulf Rapid Reef Assessment Program (Kramer 2003). It reflects the region’s tectonic history, so it is presented in Chapter 2 following a brief account of historical geology. I exclude consideration of the Conus fauna of Brazil for two main reasons. First, Brazil’s marine as well as its terrestrial biodiversity is very high, and numerous species that occur there appear morphologically within the range of variation of more northerly species. Some workers have treated these as conspecifics while others have considered them distinct. However, character analyses remain very limited and molecular genetic data in particular are even sparser. A study of Brazilian reef corals that combined morphological and molecular data (Nunes et al. 2008) showed that some species considered congeneric with northern forms on morphological grounds more likely evolved from southern members of a quite different genus in striking cases of convergent evolution. Their results provide a cautionary lesson for revisionary systematics of other Brazilian marine taxa. A second reason for excluding Brazil from this treatment is its “good connections with systematics institutions in richer countries and a strong program of its own” (Hine 2008); better positioned Brazilian biologists are beginning to investigate the challenging problems presented by its complex, distinctive, and understudied Conus fauna (e.g., Gomes 2004, 2009, 2011; Gomes et al. 2007).

The Format of This Book This book’s format generally follows that of an antecedent work on the Indo-­West Pacific species of Conus (Röckel, Korn, and Kohn1995). Chapter 1, “Setting the Stage: Approaches,” outlines the general principles and methods followed to resolve problems of determining both the species to

which a specimen belongs and the classification of species of Conus. It introduces the newer methodology that has become available since the 1995 book was published and that has been incorporated in this one. Chapter 1 also explains and defends retaining all Western Atlantic species in Conus in this book, although some authors have subdivided the original genus into various numbers of other genera. Chapter 2, “Setting the Stage: The Geological Theater and the Evolutionary Play,” briefly describes the complex geologic history of the focal geographic area and the evolutionary and biogeographic history of Conus worldwide and particularly in the Southeastern United States and Caribbean region. It ends with a brief history of the study of Conus in the Western Atlantic. Chapter 3, “How to Use This Book,” discusses how Conus species are identified and classified, the salient features that each species account addresses, how each account is organized, and the rationale for the order of accounts that comprise Chapter 5. Chapter 4, “Behind the Scenes: Technical Aids to the Species Accounts,” gives more details of the topics presented in Chapter 3. It includes glossaries of specialized terms used in shell and radular tooth descriptions and statistical analyses, and brief primers to aid in understanding the statistical methods and molecular genetic analyses. Chapter 5, “Systematic Section: Species Accounts,” is the heart and most of the bulk of the book. It follows the principles discussed in the earlier chapters to present the results of the study that assesses the validity of the described extant species of Conus in the focal geographic region. Chapter 6, “Synthesis and Conclusions,” summarizes and synthesizes information primarily on taxonomy, natural history, biogeography, and phylogeny, and to a lesser extent on ecology and fossil history; this is based mainly on the species accounts in Chapter 5. A general glossary, bibliography of literature cited, and index follow.

Access to Additional Information The Conus Biodiversity Website (http://biology .burke.washington.edu/Conus/) provides considerable important supplementary information, including PDF’s of original descriptions. It also includes videos of behavior in living animals, a format impossible to convey in a printed book. The website also periodically updates Röckel, Korn, and Kohn (1995), and updates to this book will be posted in the future as well.

Introduction 

A companion web site containing the data files and statistical analyses used in the research for this book has been developed and is available from the publisher’s web page (http://press.princeton.edu /titles/10229.html). The data files include collection and repository records and shell and radular tooth morphometric data for the specimens studied, and images of some that could not be included in the book. The statistical analyses summarize how the data were used to test whether characters differ between groups hypothesized as indicating different species. As Chapter 4 describes in more detail, tests of statistical significance yield values of P. The

• 5

P value is the probability that if the null hypothesis (i.e., that the populations being sampled do not really differ from each other) is correct, the value of the test statistic would be as extreme or more so than the observed value. Thus, the smaller the value of P, the more strongly the test rejects the null hypothesis, and the more likely that the difference between populations is real. The supplementary material therefore presents the analyses resulting in the P values that appear in the text. It enables readers who so wish to replicate, extend, and improve the analyses of data, and it avoids cluttering the species accounts in Chapter 5 with details that not all readers will require.

Abbreviations Used in the Text ••

Abbreviations of repositories. The following is a guide to the abbreviations of museums and other institutions whose collections were used in the research leading to the species accounts in this book. Abbreviation Repository

AMNH ANSP BAMZ BMSM BMUW CMNH DMNH FLMNH FMNH HMNS IESH IMS INVC LMD LSL MCZH MDNG MHNG

American Museum of Natural History, New York Academy of Natural Sciences of Drexel University, Philadelphia Bermuda Aquarium, Museum, and Zoo, Flatts, Bermuda Bailey-­Matthews Shell Museum, Sanibel, Florida Burke Museum of Natural History and Culture, University of Washington, Seattle Carnegie Museum of Natural History, Pittsburgh Delaware Museum of Natural History, Wilmington Florida Museum of Natural History, Gainesville Field Museum of Natural History, Chicago Houston Museum of Natural Science, Texas Instituto de Ecologia y Sistemática, Havana Institute of Marine Science, University of North Carolina, Morehead City INVEMAR, Instituto de Investigaciones Marinas y Costeras, Santa Marta, Colombia Löbbecke Museum, Düsseldorf Linnean Society of London Museum of Comparative Zoology, Harvard University, Cambridge Museum der Natur, Gotha, Germany Muséum d’Histoire Naturelle, Geneva

MNHN MNRJ MORG MPUH MZSP NCSM NHMUK NHMW NMW PRI RMNH

SBMNH SMF SMNS STRI TAMU TAMUCC UMML UMMZ UPSZ USNM

Muséum National d’Histoire Naturelle, Paris Museu Nacional da Universidade Federal do Rio de Janeiro, Brazil Museu Oceanográfico “Prof. E. C. Rios,” Rio Grande, Brazil Museum Poey, University of Havana Museo de Zoologia da Universidade de São Paulo, Brazil North Carolina State Museum, Raleigh Natural History Museum, London Naturhistorisches Museum, Vienna National Museum of Wales, Cardiff Paleontological Research Institute, Ithaca, New York National Museum of Natural History Naturalis, Leiden, Netherlands (formerly Rijksmuseum van Natuurlijke Historie) Santa Barbara Museum of Natural History, California Senckenberg Museum, Frankfurt Staatliches Museum für Naturkunde, Stuttgart Smithsonian Tropical Research Institute, Panama Texas A&M University, College Station Texas A&M University, Corpus Christi University of Miami Marine Laboratory, Florida University of Michigan Museum of Zoology, Ann Arbor Uppsala University Museum of Evolution, Zoology, Sweden National Museum of Natural History, Smithsonian Institution, Washington, DC

8  • Abbreviations Other abbreviations used in the text. (For abbreviations of shell and radular tooth characters and statistical terms, see the specialized glossaries in Chapter 4.)

marine tropical regions with mainly endemic biotas. The Indo-­West Pacific ranges from the Red Sea and East Africa to Easter Island. See also Eastern Atlantic, Western Atlantic, and Eastern Pacific.

CBW The Conus Biodiversity Website (http://biology.burke.washington .edu/conus/)

ma

Millions of years ago.

Code

The International Code of Zoological Nomenclature (see ICZN, below).

mm

coll

Collection. Usually used to cite a specimen in a private collection.

Millimeters. Measurements of shells in this book are in millimeters. For users wedded to the English system, 25.4 mm = 1 inch.

DFA

Discriminant Function Analysis. See Chapter 4 for explanation.

EA

Eastern Atlantic; used as an adjective or noun. One of the world’s four major marine tropical regions with mainly endemic biotas. The Eastern Atlantic comprises the West African coastal region and offshore islands. See also Western Atlantic, Eastern Pacific, and Indo-­West Pacific.

EP

ICZN

IWP

Eastern Pacific; used as an adjective or noun. One of the world’s four major marine tropical regions with mainly endemic biotas. The Eastern Pacific comprises the western American coastal region and offshore islands including the Galapagos. See also Western Atlantic, Eastern Atlantic, and Indo-­West Pacific. International Commission on Zoological Nomenclature. Also sometimes used for International Code of Zoological Nomenclature. See ICZN (1999) in the Bibliography and iczn. org/code. The Commission is the international governing body of the scientific names of animals. It provides and regulates the system that ensures every animal taxon from the species-­group to the family-­group has a unique and universally accepted scientific name. Indo-­West Pacific, or the Indo-­West Pacific marine biogeographic region; used as an adjective or noun. The largest of the world’s four major

mtDNA The deoxyribonucleic acid or genetic material that forms the genome of the mitochondrion, an organelle in the cytoplasm of cells that provides the cell’s energy. P

Probability; in reporting results of a statistical test, P is usually the probability that a null hypothesis is correct, i.e., the probability that one is wrong to assert that the different groups really differ from each other, based on the samples and characters being tested. See Chapter 4 for further explanation.

PCA

Principal Components Analysis. See Chapter 4 for explanation.

PETM

The Paleocene-­Eocene Thermal Maximum, a rapid increase in ocean temperature. This was presumably due to increased concentration of greenhouse gases, and lasted for 10,000–20,000 years about 55.5 ma.

WA

Western Atlantic; used as an adjective or noun. One of the world’s four major marine tropical regions with mainly endemic biotas. The Western Atlantic comprises the eastern American coastal region, including the Gulf of Mexico and Caribbean Sea. As used here, it is essentially the Western Central Atlantic region as defined by the Food and Agriculture Organization (Carpenter 2002). See Chapter 2 for further explanation. See also Eastern Atlantic, Eastern Pacific, and Indo-­West Pacific.

1

•••

Setting the Stage: Approaches The first step in wisdom is to know the things themselves; this consists in having a true idea of the objects; objects are distinguished and known by classifying them methodically and giving them appropriate names. Therefore, classification and name-­giving will be the foundation of our science. —C. Linnaeus (1735) Natural scientists are aware that no amount of observational evidence can prove one right, whereas a single new observation may prove one wrong. —Z. F. Danes (2008) Scientific hypotheses, no matter how firmly established, are never “proved” right. They are inherently provisional. Scientists know that the door is always open for new evidence and stronger theories. —G. Schwed (2011)

B

ecause this book intends mainly to characterize a regional Conus fauna and to aid the identification of its species, we need to first address some general and basic questions about species: What is a species? How are species named? How are species characterized? How are species related to each other? The rest of this chapter outlines some of the methodology that allows pursuit of these questions for specific cases.

What Is a Species? This question is really two questions, and each has more than one answer. The first is conceptual: How is species as an entity defined? For organisms that reproduce sexually, most biologists will answer that a species is a group of individual organisms and populations of organisms whose members are capable of reproducing by mating among themselves, but not with members of other such groups. A second answer, favored by evolutionary biologists who emphasize that species have an important time or historical

dimension, adds that species are evolutionary lineages of ancestors and descendants with spatial and temporal boundaries. Biologists generally accept these definitions, but they do not always make answering the second question any easier! It is the practical or operational question: How can we take Linnaeus’s first step of discovering, characterizing, delimiting, and identifying particular species? We have only to look at our own species, Homo sapiens, to appreciate that no two members of a species are exactly identical; all individual organisms vary from one another, even identical or monozygotic twins. Our task is to distinguish this within-­species variation from the attributes that distinguish similar but different species from each other. We know very well these characteristics of our own species, and the differences between Homo sapiens and the other primate species that we do not interbreed with. When we attempt to characterize species of animals that are more different from ourselves, however, our options are more limited. In most other

10  • Chapter 1 animal groups, including gastropods, we know too little to use the breeding criterion, so we are limited to less direct approaches. Practically speaking we use other, more easily observable traits that differ among animals as stand-­ins or “proxies” for the criterion of non-­interbreeding. If we find that these traits vary continuously from individual to individual in a large sample, we usually conclude that they all can likely interbreed and share genes, and thus all belong to the same species. On the other hand, if we identify sharp discontinuities or gaps in how several of these characters are distributed among the individuals, we conclude that the sample more likely contains members of more than one species. The key word in this distinction is “likely.” In more formal language, we hypothesize that our sample comprises representatives of several species. Thus a classification, or an identification of a specimen as a member of a particular species, is a scientific hypothesis. And like any hypothesis in science, it is unlikely that it can ever really be proven to be correct. The best we can hope for is that the various traits of the animals we observe differ consistently among the same individuals, further supporting and strengthening our hypothesis. As in other areas of science we accept those hypotheses for which the supporting evidence is strong and contrary evidence absent or weak (see Sites and Marshall 2004). A further complicating factor is the time dimension or history mentioned above, because all species change over time. Just as individual organisms have genetically different parents, at any given time a species or population includes members of one or more parental generations and generation(s) of offspring. All of these individuals also differ genetically (except for identical twins), so the variation in a population, and hence in a species, is dynamic, changing from generation to generation. This change of inherited characteristics in time is, by definition, a type of evolution, and it can substantially alter the appearance and other characteristics of a single species during its history. Finally, there is another definition of the term “species,” as opposed to “a species.” Species is a category in the classification of organisms. Because classifications are nested hierarchies, species are, as noted above, groups of individual organisms and populations of individuals, but they are also members of a genus, the next more inclusive category. And genera (the Latin plural is usually used in English) are nested in the next more inclusive or “higher” category, the family, and so on up the scale of classification to order, class, phylum, and kingdom.

How Are Species Named and Classified? This framework of our current systems of the nomenclature and classification of organisms dates to the pioneering work of Carl Linnaeus in the mid-­18th century. Although primarily a botanist, Linnaeus (1707–1778) viewed nature as a whole and titled his seminal work the Systema Naturae per Regna Triae Naturae, (The System of Nature through the Three Kingdoms of Nature), animal, vegetable, and mineral. Although he recognized that members of all three kingdoms could grow, he distinguished the first two from the third as living, or as he put it succinctly in the first edition of the Systema Naturae (1735), “there is no generation from an egg in the mineral kingdom.” Today we might express this by saying that a rock lacks a genetic code that would enable it to reproduce another rock. Linnaeus also argued cogently, first at age 28 in the epigraph of this chapter, in other writings, and in his teaching, for the importance of a uniform system of naming animals and plants. Like babies, these organisms do not come with names; people must name them in order to designate and communicate about them. As Wheeler (2008) aptly stated, “Linnaeus captured the imagination of his generation with clever and provocative classifications and a sense of discovery. He opened the world of biological diversity to an ever widening audience and sparked an age of species exploration.” Taxonomists had been interested in Conus before Linnaeus, but the system of naming and classifying organisms that he finalized in the Systema Naturae (Linnaeus 1758) is now universally applied to all animals. His names are binominal and, as the page reproduced from his book shows (Text-­fig. 1.1), his classification system takes the form of a nested hierarchy. Linnaeus thus solved “the first bio­informatics crisis” of the 18th century (Godfray 2002) by providing a single, straightforward method for both naming and classifying any type of organism, and the basic principles of his system remain in use today. By agreement among zoologists, the tenth edition of the Systema Naturae (Linnaeus 1758) is the starting point of zoological nomenclature, and the oldest acceptable scientific names of animals date from it. In mid-­18th century fashion, Carl Linnaeus wrote it and most of his other scholarly works in Latin, and his name appears on the title page as Carolus Linnaeus rather than the native Swedish form. To this day organisms are named in Latin for universality, and because it does not favor any currently used national language.

Setting the Stage: Approaches 

• 11

names in a font, usually italics, different from the rest of the text, and we follow Linnaeus in capitalizing the first letter of the genus name. Some Latin words, including their plurals, have become so firmly incorporated into the English language that we no longer distinguish them by italics. Commonly used in this book are species (plural: species) and genus (plural: genera), as well as taxon, originally coined in German (plural: taxa).

How Are Species Described?

Text-­fig. 1.1. Reproduction of p. 712 of the 10th edition of Systema Naturae (Linnaeus 1758), the first page of Linnaeus’s original description of the genus Conus, including his first infrageneric group (“* Truncati”), and his first three species. This illustrates how Linnaeus described the genus, infrageneric groups, and species, as well as his numbering system, descriptions comprising diagnoses and subdescriptions, and synonymy with references to prior literature. His system has of course been modified and updated over the last 250 years, but the basic framework persists as the standard in zoology.

In his book, Linnaeus (1758) introduced the genus Conus and described 35 species, including one from the Western Atlantic region. He based the genus on the rather simple conical shape of its shells. Part of his original description is “Testa univalvis, convoluta, turbinata” (shell univalve, spiral, conical) (Linnaeus 1758, 712) (Text-­fig. 1.1). The next category lower than and within the genus was the species, and the combination of genus and species names is the scientific name of the species and hence of each individual it includes. We no longer write our books in Latin, so modern standard practice is to indicate scientific

The rules for introducing previously undescribed species, often referred to as new species, are now set out in the International Code of Zoological Nomenclature (ICZN 1999), specifically in its chapter 3, “Criteria of Publication,” and chapter 4, “Criteria of Availability.” Until 1999, publication meant printed on paper, but the Code specifies little about the nature of the paper and printing. New species of animals are typically described in scientific journals that require submitted manuscripts to be refereed and are deemed worthy of publication by knowledgeable experts in a process known as peer review. While scientists, students, and serious amateurs adhere to this highly desirable principle of scientific publication, the Code does not require it. It considers anything printed on any paper to be a publication, as long as it meets a few basic requirements: its purpose must be providing a permanent and public scientific record, and it “must have been produced in an edition containing simultaneously obtainable copies by a method that assures numerous identical and durable copies” (Code, Art. 8.1) when it is first issued. Although the Code thus allows anyone to say essentially anything in such a document without jeop­ ardizing its publication status, its Appendix A is titled a “Code of Ethics” (ICZN 1999). It urges against, but does not prohibit, offensive names and intemperate language. An 18th-­century movement urged the rejection of Linnaeus’s names on the grounds that many were pornographic; his anatomical allusions in some descriptions of molluscs, but mainly bivalves, were also considered pornographic. A contemporary proponent of that effort railed, perhaps with some justification: “Science should be chaste and delicate. Ribaldry at times has been passed for wit; but Linnaeus alone passes it for terms of science” (Da Costa 1776, iv). However, Linnaeus’s names became universally accepted and remain so under today’s code. Since 1999, methods other than publication on printed paper that mainly entail forms of electronic distribution are accepted as long as the relevant Code

12  • Chapter 1 requirements are met (Code, Art. 8.6). More recently, amendment of several articles of the Code modified the rules for electronic publication of new names after 2011. The main change requires registration in ZooBank, the official registry of zoological nomenclature, of the work they appear in prior to its publication (ICZN 2012). Regardless of the mode of publication, it is important to remember that the description of a new species is the hypothesis that the species differs from all others described in its genus, according to a biological, phylogenetic, or other species concept. Like other hypotheses in science it cannot be proven, but can potentially be refuted (see this chapter’s epigraph by Danes 2008). Much more responsibility than honor accrues to the person who describes a new species. The author’s responsibility is to present all possible relevant evidence for and against the hypothesis, and to staunchly defend his/her conclusion.

How Are Species Characterized? Biologists usually define a species, at least among sexually reproducing animals like humans and Conus, as made up of all the populations of individuals that are capable of mating with each other to produce offspring. For most kinds of animals this interbreeding criterion of the biological species definition cannot be critically tested; one must rely on characters—usually morphological—that are observed or hypothesized to be associated with the capacity to interbreed. Taxonomists frequently use terms like “describe a new species” and “species descriptions.” In truth it is not possible to describe a species fully, especially among sexually reproducing species as noted above. And one can never hope to examine every individual of a species to know the full range of variation of all its characters. By describing species, biologists really mean that they are presenting a hypothesis and supporting it with evidence of how much its characters vary among the individuals of the species, and which characters distinguish it from the different species that are most similar to it. Shell characters. The shell is the mollusc’s castle, and traditionally and historically the shell’s traits have exclusively been used in classifying shelled molluscs. Relatively few original descriptions of shelled marine gastropods mention anatomical features of the animal’s body. Specialists sometimes refer to the body as the “soft parts.” Some recommend using only shell characters, others recommend using only anatomical information. In an assessment of these disparate approaches to gastropod taxonomy, Schander and Sun-

dberg (2001) found that the outcomes did not differ very much, and they recommended using all available data. However, the identification and classification of Conus species has been based almost exclusively on shell characters. A good example is our earlier book on Indo-­West Pacific Conus (Röckel, Korn and Kohn, 1995; hereafter cited as “RKK”1). There we attempted to highlight at least two observable shell characters that differed between the most similar species. We also provided other kinds of information, including color patterns of the body, geographic distribution, habitat and habits, form of radular teeth, and characteristics of eggs and egg capsules. But shell characters determined the decisions that led to our conclusions about species identities. The shape, sculpture, and color pattern of the durable shells of Conus provide the most easily accessible and practical characters for identification. For that reason this book also primarily emphasizes shell characters and clarifies our present understanding of their usefulness in distinguishing the Conus species of the Southeastern United States and Caribbean region. Chapter 3 defines each shell character and the terms that are used to describe their variation in the systematic accounts of each species in Chapter 5. In particular, shell shape characteristics are described and compared more objectively than in past treatments, by applying quantitative methods to fairly large samples. The section on shell morphometry in Chapter 3 presents the specific characters used, and the General Glossary defines more generally used terms. Anatomical characters. Except for a few that depict radular teeth, all original descriptions of Conus from the Southeastern United States and Caribbean region were based only on empty shells, and many remain known only in that state to the present time. Unfortunately, the time available to this project permitted obtaining relatively few living and preserved specimens for anatomical study. Among the latter that were available, modes of fixation and preservation varied widely, rendering accurate description of anatomical features of the body impossible in most cases. Observation of living specimens proved even more challenging, but very limited field work and the generosity of several collectors provided photographs that give important information on color patterns of the exposed body in life. These are reproduced as text-­figures in the species accounts. 1  Pronunciation of this acronym (“RKiK”) alludes only partly to that book’s rather 19th-­century approach.

Setting the Stage: Approaches 

The chitinous, hypodermic needlelike radular teeth of Conus, the animal’s key weapon in its venom-­ aided rapid-­strike predation arsenal, often remain in even poorly preserved specimens. Asymmetrical unitary structures of complex shape, the teeth are also suitable for morphometric analysis. Chapter 3 describes the radular tooth characters that are treated qualitatively and quantitatively, Chapter 4 again provides more precise definitions, and the species accounts of Chapter 5 include descriptions and comparisons from all species whose teeth could be characterized. As was the case in RKK, the shell and animal characters defined in Chapter 3 for species determinations do not always lead to clear decisions about species-­level identifications and distinctions. Likely reasons for this region include the following: 1.  The reproductive biology of many Western Atlantic species is characterized by lack of a planktonic larval stage that reduces the ability to disperse and tends to isolate populations, in striking contrast to most Indo-­ West Pacific species. 2.  The evolutionary history of the Caribbean region and its marine (as well as terrestrial) biota is highly complex. 3.  The accessibility of specimens for morphological study is limited, in large part because of their characteristically deeper habitats and sparser populations. Offsetting this to some extent are recent scientific developments and the new tools derived from them. These are allowing us to assess additional characters that are likely independent of those used previously. The new procedures can thus help test our hypotheses of species identity and classification more robustly. The most important tools in this new kit are the macromolecules that parents pass to their offspring in the egg and sperm cells at reproduction. Because these new genetic characters may be unfamiliar to many readers, the next section introduces them. Molecular characters. Recent advances in molecular genetics provide the most important of the new tools for systematics research. This revolution began only 25 years ago with the first successful application of molecular data to elucidate broad patterns of evolutionary relationships among the animal phyla (Field et al. 1988). The first publications employing molecular genetic information to help understand the classification and evolution of Conus appeared scarcely a decade later (Duda and Palumbi 1999b; Monje et al.

• 13

1999). This line of research has burgeoned in the last decade, and the species accounts of this book incorporate results to date. Thus, a brief general explanation follows that attempts to present this new information in an accessible and understandable way, so that readers unfamiliar with it will be able to appreciate its application to specific cases. The introduction and appendix of Avise (2002) provide a précis of the field and methods in a few pages. For a more general account, consult a good modern basic biology textbook. In the mid-­20th century, scientists first identified the molecules that comprise our genes and determined how their chemical structure codes genetic information. The field of molecular genetics developed rapidly, vastly increasing our understanding of how the molecular organization of genes provide “blueprints” for the structure and control of the development and functioning of organisms; the genetic differences among individuals, species, and higher taxa; and their evolutionary histories as well. An early remarkable finding was that whether an organism is a mushroom, mimosa, mouse, or mollusc, or even human, its genetic language is the same. Its genes are large molecules, or macromolecules, of deoxyribonucleic acid (DNA), whose function is conveying information. Although many gene sequences have been elucidated, as yet they have played little role in identification guides and monographic treatments of shelled molluscs. However as we will see, a few particular genes whose attributes make them quite helpful in determining species relationships have now been rather widely studied. In all organisms, the genetic language in the information-­carrying part of DNA macromolecules uses the same small component molecules, called nucleotides or bases, to encode its message, much as written languages employ letters of an alphabet. The sequences of nucleotides, the units or building blocks of DNA, function for the same reason that we use letters, words, and sentences to communicate complex concepts. In both cases, a relatively small number of different units can be combined in many different ways to create many different meanings. The genetic language is quite simply expressed. It uses only four different nucleotides as “letters,” and these are strung together in a line to make “words” (each of three nucleotides), sentences (bounded by specific nucleotide combinations), paragraphs, etc., which we call genes. Genes are often several thousand nucleotides long. They carry the information that enables them to replicate themselves when cells divide, so that all cells in the body contain identical genes. Different individuals of the same species have slightly

14  • Chapter 1 different genes, different species in the same genus differ somewhat more, and so on. Most species of animals have a few tens of thousands of genes. Just as the order of the letters in words, the order of words, etc., determine the message in written language, the order of nucleotides in a gene determines its message. This message tells the cell to replicate the DNA, or to make another nucleic acid (RNA), also with a defined order of nucleotides, and the RNA may in turn serve as a template to produce a protein with a certain order of its component amino acids. In animals that reproduce sexually, like people and Conus, most of the genes are arranged in chromosomes in the nucleus of the cells, and each individual inherits one set of chromosomes from each parent. At fertilization the sperm delivers the paternal set to the egg, which already has its maternal set. Thus we receive all of our genes from our parents in the fertilized egg that is the one-­celled stage in our life cycle. The chromosomes then replicate as the egg divides repeatedly to form the multicellular organism. As a result, we can compare the sequences of nucleotides that make up the genes of different individuals; their degree of similarity tells us how closely related they are. Genetic similarity or distance between organisms is often determined by measuring how similar the sequences of nucleic acids are in their genes, and this is the approach we have taken with Conus. As mentioned, most genes in animal cells occur in the nucleus, where half come from each parent in sexual reproduction. But some genes are not in the nucleus; they are outside it in the cell’s cytoplasm, and their mode of inheritance differs dramatically. They are transmitted asexually rather than sexually. These are the genes in small structures in the cytoplasm called mitochondria. Little power plants that convert energy essential for the cell’s metabolism, mitochondria have their own DNA. Mitochondrial DNA, usually abbreviated mtDNA, has several functions, including coding for enzymes important in cell energetics and replicating itself. Mitochondria with replicated DNA divide and are distributed to the increasing number of cells in the embryo as it develops after fertilization. Most importantly for taxonomy, the mtDNA of most animals is inherited only from mothers. They pass mitochondria to their offspring in the cytoplasm of their eggs. In contrast, the father’s mitochondria do not enter the egg at fertilization with his nuclear chromosomes. They usually stay behind along with the sperm’s cell membrane and tail. Mitochondrial DNA is much smaller than nuclear DNA, with only

30–40 genes instead of the 10–20,000 in the nuclear DNA, and its inheritance is much simpler. Also in contrast to nuclear genes that make up a number of chromosomes, mitochondrial genes form a single circular unit. Because this mitochondrial genome is inherited only in the cytoplasm of the cell, it almost never recombines with other DNA—for example, with chromosomes in the nucleus. Finally, while some portions of the mitochondrial genes used in taxonomy have essentially identical sequences in all organisms, the nucleotides in other parts have changed more frequently than in most nuclear genes. That is, they evolve more rapidly, so that the sequences vary measurably in different species of the same genus and, to a lesser extent, within species. These factors usually cause the rapidly evolving nucleotide sequences in the mtDNA genes of populations of a species that become isolated from each other to differentiate more rapidly from one another than their nuclear genes do. This high rate of evolution facilitates using the similarity of nucleotide sequences in the mtDNA of different animals to determine their taxonomic and genealogical relationships. For these reasons, mitochondrial genes have become the most widely used for genetic assessment. These applications range from determining taxonomic position and genealogical relationships to forensic detections at crime scenes to the history of early humans, and they will be the main molecular character set used in this book. Conus and other members of the higher taxa to which it belongs, the family Conidae and superfamily Conoidea, have become notorious in recent years because numerous studies have shown that shell characters alone are often inadequate to distinguish very similar but demonstrably reproductively distinct species. Most of these studies initially discovered gene sequences that are so different in animals with nearly identical shells that they likely could not interbreed, and belong to different but “cryptic” species. Duda et al. (2008, 2009) describe some examples from IWP Conus. In other cases nearly identical shells house animals with fundamentally different feeding mechanisms (Taylor et al. 1993). Such instances of unexpected hidden biological diversity are being discovered with increasing rapidity, and molecular genetic data are becoming simpler and cheaper to obtain. Consequently, systematics of the group has reached the point where new species descriptions will very soon require inclusion of gene sequence data to have any hope of being widely accepted as demonstrating species-­level differences. However, the reader of this book will soon become aware that

Setting the Stage: Approaches 

for Western Atlantic Conus, we are not there yet. We have some mitochondrial gene sequence data for only about one-­third of the recognized species, and most are represented by minuscule sample sizes, often from single individuals. Most taxonomic data derived from molecular genetics study are thus still suggestive rather than definitive; also, the dispersal powers of the majority of species are probably limited because of their nonplanktonic development, and this increases the importance of obtaining samples from more geographic localities, as well as from more individuals. The more accessible and durable shell characters that this book emphasizes still deserve the attention given them, but this status may not last long. The information presented in the species accounts in Chapter 5 also reveals a trend toward disparity between shell and molecular genetic characters, and a trend toward increasing congruence of the latter with radular tooth characters, as more data accumulate.

How Species Are Related to Each Other: Phylogenetics A genealogy or family tree is a model that shows how the individual people comprising a family at a particular time descended from their forebears and how they are related to each other. Like the individuals that populate them, species also have genealogical lineages extending back in time to common ancestral species. The genealogies of species (and of broader taxa in categories like genera, families, and phyla) are called phylogenies, and the study of these evolutionary relationships is called phylogenetics. Charles Darwin’s breakthrough explanation in 1859 showed that like a genealogy or family tree of individuals, the tree model suitably depicts how the different species in a genus or higher taxon living today descended from their ancestors over longer periods of time, often referred to as “geologic time.” The living species at the tips of the tree’s twigs connect historically to ancestral species that are represented in the larger twigs and branches toward the trunk. While family trees span decades, generations, and centuries, phylogenetic trees may have time scales of millions or tens or even hundreds of millions of years (see Baum et al. 2005). Like taxonomies, phylogenies are deduced from characters. In recent years, molecular genetic characters have increasingly served as the basis of phylogenetic hypotheses across the biotic world, and this has markedly enhanced the objectivity of phylogenetics and its contribution to understanding evolutionary relationships.

• 15

In the 18th century, Linnaeus was only dimly aware of evolutionary processes in animals, but he recognized that different species did not differ from each other either equally or randomly. Rather, they could be classified so that the species within each group were more similar to each other than they were to any species outside the group. Each such group or taxon that comprised these similar species became a genus, and each species was given a two-­word name: the first is the name of its genus, followed by the specific or trivial name that designates the species within the genus. This part of the system is analogous to the family or surname and given name of people in many human cultures. Linnaeus also arranged the species within genera into smaller infrageneric groups. For example, he recognized four such groups within Conus, distinguished by quantitative differences in shell shape. Over the years, Linnaeus’s successors sought to improve on his classification; RKK summarized these efforts at the infrageneric level. In addition, Linnaeus grouped similar genera into higher taxa, in categories equivalent to the families, orders, and phyla in use today. Above the genus level, Conus was one of many genera under Linnaeus’s next higher taxon, Vermes Testacea or “shelled worms,” the shelled molluscs of modern parlance. Despite long and considerable interest in its systematics, the history of phylo­genetic studies of Conus is remarkably brief. Linnaeus (1758) divided Conus into four infrageneric taxa distinguished by quantitative differences in shell shape, and several subsequent authors proposed subgenera, genera, or subfamilies. The CBW, and Tucker and Tenorio (2009) list the more than 120 genus-­group names proposed in Conus over the years. Until nearly the end of the 20th century, these varied classifications were based almost only on external shell character sets, they were inconsistent and incongruent, and none gained wide acceptance. No one had ever attempted a classification incorporating a hypothesis of the phylogenetic or genealogical relationships of species in the genus based on either morphology or the fossil record until Tucker and Tenorio’s (2009) analysis of shell and radular tooth morphological characters. In the meantime, less than five years after RKK appeared, Duda and Palumbi (1999b) published the first species-­level molecular phylogenetic analysis of Conus. This was based on sequences from 70 predominantly IWP species of a region of about 300 nucleotides in the nuclear gene whose function is to code for the protein calmodulin. They used this phylogenetic tree to examine the distribution of non-

16  • Chapter 1 planktonic development among these species, and their results supported the hypothesis that this biogeographically important life history attribute originated independently several different times in the genus. Their study was followed only a month later by the first application of mitochondrial DNA sequencing to Conus (Monje et al. 1999). Of the seven species analyzed, their results were consistent with those of Duda and Palumbi for the three used in both studies. Research of this type expanded briskly during the ensuing years. Studies evaluated the phylogenetic relationships of different feeding ecologies (Duda, Kohn, and Palumbi 2001; Duda and Palumbi 2004; Espino et al. 2008), elucidated rapid adaptive radiations in the Eastern Atlantic (Duda and Rolán 2005; Cunha et al. 2005; Cunha et al. 2008) and Indo-­West Pacific (Williams and Duda 2008), improved species-­level taxonomic decisions including identification of cryptic species (Duda et al. 2008; Duda et al. 2009), increased efficiency of discovering new venom peptides (e.g., Holford et al. 2009), and expanded phylogenetic trees to cover more species and more geographic regions (Duda and Kohn 2005). The Duda and Kohn (2005) report extended phylogenetic analyses of the Western Atlantic (WA) region from 1 to 13 species. It also demonstrated the divergence of two major branches or clades of Conus species that occurred in the early history of the genus, probably more than 30 million years ago (ma) in the Oligocene epoch. We called these the small and large major clades, because the former comprised only nine species and the latter included all but one of the remaining 126 species whose mitochondrial genes had been sequenced at that time. The “small major clade” contained primarily WA (3) and EP (5) species, and only one from the Indo-­West Pacific (IWP). Except for the genetically very distant Conus californicus that occupies its own major branch, all other species from all three regions comprised the large major clade, with the vast majority from the IWP. Appendix 1 shows a phylogenetic tree of Conus species from Duda and Kohn (2005). While the phylogram shown in Appendix 1 remains the most inclusive molecular species-­level tree published for Conus to date, during the past eight years subsequent research has added many additional species to these analyses, and they continue to confirm this major division (Bandyopadhyay et al. 2008; Williams and Duda 2008; Puillandre et al., unpublished data). In an as yet unpublished work (Puillandre et al., unpublished data), the small major clade has now grown to comprise nearly 40 species, of which 70% are IWP, with the remainder more eq-

uitably distributed geographically between the WA and EP regions. The large major clade has also grown considerably, to include nearly 300 species from all of the world’s oceans where Conus occurs. Meanwhile, the first morphology-­based phylogenetic hypothesis for what has been generally considered the entire genus Conus as well as its closest relatives has recently appeared (Tucker and Tenorio 2009; Appendix 2).

Phylogenetics and Classification of Conus above the Species Level Above the species, the next more inclusive level in the taxonomic hierarchy, the genus, is a group of species that are hypothesized to be monophyletic. That is, they descend from a common ancestor and are thus more closely related to each other than any one is to all species outside the group. As with individuals and species, in the absence of genetic information about relationships, morphology serves as a proxy to determine relatedness. Various authors starting with Linnaeus (1758) divided Conus into infrageneric taxa, variously called subgenera, genera, and even subfamilies (Cotton 1945) or families (Tucker and Tenorio 2009). Well over 100 genus-­group names have now been proposed in Conus (Bouchet et al. 2011); the CBW also lists them, and RKK (p. 14ff.) discussed earlier schemes. Appendixes 1 and 2 illustrate two current hypotheses of phylogenetic relationships, based on molecular genetics and morphology, respectively. The former shows the most extensive Conus species-­ level phylogenetic tree published to date on the left. It is based on sequences of the 16S mitochondrial gene of 135 species. To the right are smaller trees representing several subclades. They are based on sequences of three different mitochondrial genes, and the subclades are rather tentative because not all of their elements have yet been published in the scientific literature. Appendix 2 shows a tree that Tucker and Tenorio (2009) used as a basis for the higher taxa that they proposed, applying 28 shell characters, 17 radular characters, and one diet character to species interpreted as representing exemplars of 83 genus-­ level taxa. The levels of taxonomic names applied to the branches thus differ strikingly between the trees of Appendix 1 and 2. Tucker and Tenorio conclude that the traditional genus Conus should be split into three families—two with two subfamilies each— containing a total of 83 genera. Eleven of these are monotypic, that is each contains only a single species, and ten contain only two. In the most recent compilation, Bouchet et al. (2011) list 82 generic

Setting the Stage: Approaches 

names that have “not been synonymized in the literature,” and 32 additional names that have been synonymized under those. A particularly useful feature of Tucker and Tenorio’s work is that it compares their morphology-­based phylogeny with previously published molecular-­ based hypotheses, and the main branching patterns of Appendixes 1 and 2 are rather similar overall. Most importantly, the Tucker and Tenorio tree recovers the small and large major clades of Conus first identified from molecular analysis (Duda and Kohn 2005), for which Tucker and Tenorio (2009) proposed separate families. The most important study to date relating molecular genetics to classification and phylogeny of the Superfamily Conoidea (Bouchet and Rocroi 2005; Bouchet et al. 2011) as a whole is that of Puillandre et al. (2011). It provides a phylogenetic tree of 14 families and more than 100 putative genera based on sequences of the mitochondrial genes CO1, 16S, and 12S. These authors argue cogently for a hierarchical classification based on molecular phylogenetics of a single exemplar species of each genus. Their well-­ supported genus-­level phylogeny assigns five monophyletic genera containing extant species, Profundiconus, Californiconus, Taranteconus, Conasprella, and Conus, to the monophyletic family Conidae. The first

• 17

three include only 1–8 species each, Conasprella contains at least 38, and Conus comprises more than 600. Only the last two occur in the Western Atlantic region. Although Puillandre et al. (2011) analyzed only a single exemplar species of each genus that they characterized, their concept of Conus (represented by the IWP exemplar C. consors Sowerby I) is generally congruent with the large major clade, while their Conasprella (represented by the IWP exemplar C. pagodus Kiener) comprises at least a portion of the small major clade (Appendix 1). However, the 21st-­century studies just described have appeared too recently to have met the test of time. To gain acceptance, a new classification must demonstrate that it facilitates and does not complicate communication and the retrieval and storage of information (Godfray and Knapp 2004; Avise and Mitchell 2007). Therefore, this book follows its predecessor in assigning all extant species of the traditional family Conidae to the genus Conus, as discussed there (RKK, 16). Chapter 3 describes how the information in these phylogenetic models was applied to determine the arrangement of the species accounts in this book. But first Chapter 2 sets the geographic and temporal or geological stage on which Conus has evolved and diversified in the Western Atlantic region.

2

•••

Setting the Stage: The Geological Theater and the Evolutionary Play

I

ts subtitle a variation on a theme by G. Evelyn Hutchinson (1965), this chapter sets the historical geological context that fostered Conus becoming such a diverse taxon in modern tropical seas. The chapter first outlines the complex geologic history of the western central Atlantic area, mainly during the Cenozoic era. This is the span of time that followed the last mass extinction of life in both terrestrial and marine biospheres at the end of the preceding Mesozoic era 65 million years ago (ma). Regional geology has profoundly influenced the composition of the modern marine biota of the focal region, including of course the evolutionary history of Conus and its complex modern taxonomy. The chapter also summarizes the evolutionary and biogeographic history of Conus worldwide but with a Western Atlantic emphasis. It ends with a brief outline of the history of study of the genus in the region. It is not possible to understand and appreciate the modern diversity and geographic complexity of such an extremely species-­ rich marine taxon as Conus without seriously considering not only its evolutionary history, but also how its environmental setting has changed during that time. A basic understanding of this history of land masses, islands, and ocean depths and currents, and of the limited dispersal abilities of many benthic invertebrates, is necessary to appreciate the patterns of distribution and connectivity of populations of marine animals. This information also helps to explain why the taxonomy of modern Conus species continues to be so challenging. The historical geology and paleoceanography in this account are drawn primarily from the following sources: Coates (1997), Droxler et al. (1998), Iturralde-­ Vinent and MacPhee (1999), Todd et al. (2002), Cowen et al. (2006), D’Hondt (2005), and Iturralde-­Vinent

(2006). For a broad view of plate tectonics and the geography of land masses and oceans prior to the times considered here, see Murphy et al. (2008).

Historic Trends in Positions of Tectonic Plates, Continents, and Seas, and the Evolution of Conus This section reviews current understanding of the complex geological dynamics of the Southeastern United States coast and Caribbean region. It summarizes both geological and environmental processes and how they changed over long periods of time to shape the region’s present-­day geography and oceanography. The section emphasizes the most important of these factors, plate tectonic history and ocean hydrodynamics. For an excellent series of maps that show Earth’s tectonic plates and the positions of continents and oceans at each of the geologic spans of time described below, see The Paleomap Project website (www .scotese.com). The maps in Iturralde-Vinent and MacPhee (1999) show details of tectonic changes in the Caribbean region during each time period, and two are reproduced here (Text-figs. 2.1, 2.2). Mesozoic. About 200 ma in the Early Jurassic period of the Mesozoic era, the world’s single supercontinent, Pangaea, began to be sundered onto smaller, separate tectonic plates. Much of present-­day Europe was covered by a broad shallow sea that geologists call the Tethys Sea. It connected the North Atlantic and Indian Oceans, but was beginning to narrow as the African Plate moved northward, to eventually cut off the modern Mediterranean Sea. At about the same time the Atlantic Ocean, the focal region of this book,

Setting the Stage: The Geological Theater 

was born as the newly forming North American Plate swung westward from the Eurasian Plate, which still comprised most of the old Pangaea. By the Middle Jurassic, about 175–185 ma, the first Caribbean Seaway formed, separating northern and southern Pangaea into continents referred to as Laurasia (the antecedent of present North America, Europe, and Asia) and Gondwana (antecedent of South America, Africa, India, Australia, and Antarctica). The Caribbean Seaway connected the Pacific and North Atlantic Oceans, and it widened during the late Jurassic and the following Cretaceous period, as sea floor spreading continued. This process formed oceanic crust that became the incipient Caribbean Plate, between the North American Plate to the north, the South American Plate to the south and east, and the Cocos Plate to the west. By the Late Cretaceous, the Cocos and Caribbean Plates were separated by a volcanic arc of widely separated islands. This Central American Arc would eventually form the Central American land mass that connected North America and South America some 70 million years later. As the Caribbean Plate moved northeastward, its leading edge, called the Antillean Volcanic Arc, subducted under the North American Plate, causing volcanism that formed emergent islands along the arc from modern western Cuba to the Netherlands Antilles. Coral reefs occurred along the coasts of some these islands as early as the Late Cretaceous. Their fossil remains are found today, for example in Jamaica (Mitchell 2002). Study of ancient sediments from cores indicates that the Gulf of Mexico was forming simultaneously, first as a shallow sea and then as the deepening basin it is today. The incipient Atlantic Ocean separated the South American and African Plates at the Mid-­Atlantic spreading center, starting in the Early Cretaceous and continuing to widen thereafter. North America separated from Laurasia about 90 ma, and the North and South Atlantic Oceans became continuous. Active seafloor spreading along elevated midoceanic ridges raised sea level, and the volcanic activity increased atmospheric carbon dioxide (CO2) concentration to even higher levels than at present. This resulted in globally warm climatic conditions, often referred to as a “greenhouse world.” Volcanic activity along the Antillean Arc had ceased by the time of the transition from the Mesozoic to the Cenozoic era 65 million years ago, when a very large extraterrestrial projectile, probably an asteroid, collided with Earth at the site of the modern Yucatan Peninsula. That impact caused profound worldwide environmental disruption and one of Earth history’s most severe terrestrial and marine

• 19

mass extinction events (e.g., D’Hondt 2005; Schulte et al. 2010). The effects must have been most severe nearest the impact, at the center of this book’s modern geographic focus. Geological study of the impact area (Tada et al. 2003) indicates that these included collapse of marine carbonate platforms, large tsunamis, rapid and deep deposition of sediments that engulfed and buried benthic organisms, and the extinction of most of the Cretaceous marine biota. Geological evidence of expansive marine sediments indicates a general absence of emergent land throughout the Caribbean region at that time. The Cretaceous Antillean islands had vanished beneath the sea. Mass extinctions including this one that ended the Cretaceous period are aptly described by Erwin (2004, 218) as “a critical driving force for evolutionary change.” He continues: “They prune the tree of life and the subsequent evolutionary rebounds provide an opportunity for previously minor clades to become dominant, for dramatic reorganizations of ecosystems, and for the appearance of significant evolutionary innovations.” Among molluscs as a whole, this phenomenon is far better documented for the class Bivalvia (Krug et al. 2009) than for Gastropoda (Tracey et al. 1993). The nature of the record dictates that fossil shells are more reliably identified to genera than to species, and Krug et al. (2009) demonstrated a rapid increase in the number of bivalve genera from 63–50 ma, globally as well as specifically within both northern and southern provinces of the Western Central Atlantic region. Of course we cannot know whether or not Conus would have diverged from its ancestors had the end-­Cretaceous mass extinction not occurred, but its “pruning” may well have abetted the subsequent significant evolutionary innovations that allowed a previously minor clade to diversify and become ecologically important quite soon, in geological terms, after its origin. Paleocene. In the first Cenozoic epoch, the Paleocene (65–56 ma), volcanic activity resumed along the Antillean Volcanic Arc. Igneous and other rocks of this age are found in the Greater Antilles. However, this episode of volcanism lasted only until the boundary between the Early and Middle stages of the Eocene epoch about 52ma, when the present islands began to emerge. Throughout the nearly 10 million years of the Paleocene, the earth’s biosphere was still experiencing the effects of the great end-­Cretaceous mass extinction. In the sea, primary productivity of new organic matter by photosynthesizing algae and bacteria returned quickly to pre-­impact levels (Sepulveda et al. 2009). However, recovery of animal diversity was slow and the fossil record indicates that the

20  • Chapter 2 majority of Paleocene invertebrates were suspension feeders on small organic particles and hosts of photosynthetic symbiotic microorganisms (Hansen et al. 1993; Håkansson and Thomsen 1999; D’Hondt 2005). The first subsequent phase of evolutionary radiation involved mainly speciation in genera that survived from the Cretaceous, and of course as noted above Conus was not yet present. During this time, molluscan faunas of the Gulf of Mexico region recovered diversity more rapidly than those in other parts of the world, particularly Europe and the entire Tethyan region. While particulate-­ feeding bivalves and gastropods predominated, some predatory gastropods are present in Paleocene deposits, including members of three questionably identified neogastropod genera in what is now Alabama (Bryan and Jones 1989), unidentified Turridae in Texas (Hansen, et al. 1993), and the volutid Volutospira in New Jersey (Gallagher 2002). Members of the Naticidae or moon snails, a family of shell-­drilling predatory taenioglossan gastropods, occurred at all three sites. Eocene. In the second radiation phase of Cenozoic molluscs, beginning in the Early Eocene, Conus was one of a number of new molluscan genera and families that arose and diverged more strikingly from their Cretaceous ancestors than did their Paleocene predecessors (Tracey et al. 1993). As these new groups of organisms diversified, they also spread rapidly around the world’s oceans, especially over tropical belts that were much wider than they are now. The planet’s marine fauna was beginning to attain a modern aspect. Rates of speciation were high and the diversity of carnivorous neogastropods in particular increased. These trends continued for about the next 25 million years as biodiversity returned to levels that preceded the mass extinction (Hansen 1988). The ancestor of the family Conidae was likely a member of the Turridae. That family first appeared in the Cretaceous and is noted for its baroque evolution of diverse forms of predatory radular tooth weaponry, most likely including the needlelike teeth capable of injecting paralytic venom into prey inherited by Conus from its turrid ancestor (Taylor et al. 1993). The oldest known fossil shells of Conus appear in sedimentary rocks that date to the beginning of the Eocene, 55–56 ma, in what are now England and France. At that time the Tethys Sea still covered those parts of modern Europe, but the continents and oceans were beginning to approach positions familiar to us today. In addition to paleogeographic reconstructions, geological studies can now inform about environ-

mental attributes of former seas, such as temperature, productivity, and the nature of benthic habitats. We can thus seek at least limited understanding of the lives of Conus and other genera known only from fossil shells found in sedimentary rocks. The ratio of the different isotopes of oxygen in the calcium carbonate of shells varies depending on the sea temperature when the shell was secreted. Such information from fossil shells, when calibrated with independent data on the age of sediments derived from the decay rates of radioactive elements, can indicate the temperature of the sea when the molluscs that produced the shells lived. Oxygen isotope ratios show that the Eocene was also one of the warmest periods in earth history, with tropical conditions extending about twice as far north and south of the equator as they do today. The earliest Eocene is particularly interesting geologically, in part because it shares some features with the present-­ day phenomenon of global warming. In both cases, “greenhouse gases” that cause the atmosphere to warm were probably responsible for the rapid increase in temperature, but their sources and natures may have differed between Eocene time and today. Geologists call the rapid warming at about 55 ma the Paleocene-­Eocene Thermal Maximum (PETM), because it occurred close to the boundary between those two epochs. Tropical sea temperatures rose very quickly from a geological viewpoint, more than 5ºC over a few tens of thousands of years. And this short-­lived sharp rise was superimposed on a longer, slower, but steady temperature rise throughout Early Eocene time, as evidenced by the trends in oxygen isotope ratios determined in fossil foraminiferan shells from ocean sediments (Zachos et al. 2001; Zachos et al. 2003). Five Early Eocene (55–49 ma) Conus species are known, all from the Tethyan region. During the Middle Eocene (49–39 ma), the genus experienced its first major radiation, reaching about 40 species (Kohn 1990), although these data from more than 20 years ago need updating. As tropical conditions expanded to about twice their present latitude, the geographic range of Conus extended rapidly and widely to include the coasts of modern Asia, Africa, and North America, where members of the genus colonized the then warm but now temperate zone as far north as present Washington State in North America (Weaver 1943). Shells of several Middle Eocene Conus species are found in sedimentary rocks from that time period in and around the author’s home city of Seattle, now some 700 km north of the nearest extant species in California. Contemporaneous Conus fossils are similarly common throughout present-­day Europe, oc-

Setting the Stage: The Geological Theater 

90°W

80°W

85°W

75°W

70°W

55°W

60°W

65°W

High land

FLORIDA

25°N

• 21

Low land

GULF OF MEXICO

G YUCATAN Wes tern Maya Block

20°N

Shallow marine Deep marine

A

A

Cuba

Western Blue Jamaica Mts.

?

L

A

Chortis Block

N

?

Hispaniola

Pedro Bank 15°N

Marine currents

B A H A M A S

R

D

AT LAN T I C OCEAN

I

A

P. Rico

Virgin Is. St. Croix

Nicaraguan Rise

Lesser Antilles

Beata Ridge

Grenada Basin

PAC I F I C OCEAN 10°N

Aves Ridge

CARIBBEAN SEA

Tobago Guajira

Southern Central America 5°N

Trinidad

Paraguaná ORINOCO SEAWAY

Magdalena Basin

GUYANA SHIELD

Text-­fig. 2.1. Reconstruction of Late Eocene to Early Oligocene paleogeography and ocean current patterns of the Caribbean region, indicating conditions during the Cenozoic time of maximum land exposure. GAARlandia refers to the continuous emerged Greater Antillean-­Aves Ridge system at the eastern margin of the Caribbean Plate. Narrow black lines outline present land boundaries. From Iturralde-­Vinent and MacPhee 1999, Paleogeography of the Caribbean region: Implications for Cenozoic biogeography. Bulletin of the AMNH, no. 238, fig. 6; courtesy of M. A. Iturralde-­Vinent, R.D.E. MacPhee, and The American Museum of Natural History.

curring as far north as Denmark. In the Western Atlantic region only eight Middle Eocene Conus species are known, from deposits along the Gulf of Mexico coast from modern Alabama to Mexico. Through most of the Eocene, the prevailing ocean surface current was the westward-­flowing Circumtropical Current from the Tethys Sea, across the widening Atlantic, and through the Caribbean Seaway to the Pacific (Text-­fig. 2.1). This current probably carried planktonic larvae of benthic invertebrates, including Conus, to the Western Atlantic region. During the Middle and Late Eocene, about 45–36 ma, sediments of the Caribbean seafloor record uninterrupted deposition, and a shallow sea with a sedimentary floor also occupied what is now land east, north, and west of the present Gulf of Mexico. Also at this time, extensive tectonic uplift characterized the entire region, and shallow carbonate platforms occurred in the vicinity of Florida, the Bahamas, and Yucatan. By about 37 ma, in the Late Eocene, the Caribbean Plate had moved far enough northeastward so that

the Antillean Volcanic Arc just beyond its leading edge collided with the Florida-­Bahamas Platform (Text-­fig. 2.1). This blocked further northeastward movement, and the resulting uplift produced the Greater Antilles islands of Cuba and Hispaniola. The Caribbean Plate then shifted direction and began to move eastward, subducting under the North American Plate south of the Antillean Arc. This caused new volcanic activity east of the subduction zone, which formed a new Lesser Antilles Volcanic Arc. The new land barriers interrupted the Circumtropical Current, probably causing loop currents in the Gulf of Mexico and Caribbean. This interruption initiated the Gulf Stream and reduced the westward flow into the Pacific (Text-­fig. 2.1). Meanwhile, new oceanic crust continued to emerge along the Mid-­Atlantic spreading center, causing continued westward movement of the North American Plate. To the west, this resulted in the North American Plate overriding the subducting Farallon Plate. Eventually a new spreading center appeared, located at the modern Galapagos Islands; this split the Farallon Plate in two, and

22  • Chapter 2 thus formed the Cocos Plate to the north and the Nazca Plate to the south. Globally, warm conditions continued through the Late Eocene. In spite of apparently favorable temperatures and the widespread occurrence of diverse shallow water habitats in the entire Gulf and Caribbean region, however, coral reefs were sparsely developed (Budd et al. 1992). Fossils of only four Conus species are reported from Late Eocene deposits in that region, all from Florida and Mexico (Hendricks and Portell 2008). More than 100 fossil species of Conus are recorded from the entire Eocene epoch, the majority from the Tethyan region (Kohn 1985, 1990). Oligocene. The Eocene-­Oligocene transition (34 ma) heralded a cooler earth with narrowing of the tropics. Continued general tectonic uplift resulted in more extensive land areas accompanied by relatively lower sea levels, and greater isolation of the Caribbean Sea (Text-­fig. 2.1). When this episode of tectonic uplift peaked, about 35–33 ma, it likely left either a continuous peninsula or a series of large islands separated by narrow channels from South America all the way north through the Greater Antilles. This was the time of greatest land exposure during the Cenozoic era in the Caribbean (Text-­fig. 2.1). Coral reefs remained rare in the region (Budd et al. 1992). However, in the Late Oligocene (27–25 ma), sea level again rose, and marine transgression reduced the sizes of the islands and increased the distances between them. This also restored the major impact of the Circumtropical Current (Iturralde-­Vinent and MacPhee 1996, figs. 7, 10), and coral reefs began to flourish throughout the region from the Gulf of Mexico to the Greater Antilles and to Venezuela (Johnson et al. 2009). In the Oligocene, the total number of known Conus species decreased to 67, and reduced diversity was by no means restricted to this genus. Throughout the world oceans, gastropods and other invertebrates represented in the fossil record shared this decrease (Raup 1976), suggesting that extrinsic environmental factors affecting the entire globe were the major cause. However, WA Conus were a more important component of the genus as a whole, comprising about 40% of the world’s species in the Oligocene epoch. Miocene. The westward movement of the North and South American Plates continued through those epochs and into the next, the Miocene (23–5 ma), as well. Simultaneously, the Cocos and Nazca Plates under the Pacific Ocean moved northeastward, as did the subduction zone between the former and the Caribbean Plate, and the Central American Volcanic Arc just downstream. These movements gradually re-

duced the broadly open and deep connection between the Pacific Ocean and the Caribbean Sea, and eventually (in the Middle Miocene, ca. 12 ma) the southern end of the Central American Arc collided with South America (Text-­figs. 2.1, 2.2). At that time the future Isthmus of Panama was a submarine sill estimated at 1000 m deep (Coates 1997). The shoaling of the prior oceanic communication of about twice that depth may have been the event that began to separate the Pacific and Caribbean and to cause what would eventually be profound differences in their water masses and biotas. Meanwhile at the northeastern edge of the Caribbean Plate, tectonic movements of the Greater Antilles Arc moved and deformed its crust and created the broad and deep troughs that separate the islands to this day. Thus, by the Middle Miocene (16–11 ma) the modern features of the Caribbean Sea and its surrounding islands and continents were mainly in their familiar places, with the major exception that present Central America was then a series of a few large islands separated by broad connections between the Pacific and Caribbean (Text-­fig. 2.2). Despite this interoceanic communication, several lines of evidence indicate that separation of the marine faunas of the modern EP and Caribbean began in the Middle Miocene about 15 ma (Lessios 2008), more than 10 million years before the final closure of the isthmus. Fossil evidence suggests that the southerly flowing California Current brought cold water much farther south along the west side of the Central American Arc than it does today. Late Miocene (11–6 ma) sediments from as far south as Ecuador contain fossil foraminifera of species characteristic of today’s California Current farther north. On both sides of the isthmus, closely related “geminate species pairs” or “sister species” have now been subjected to molecular analysis; these include pairs of fishes and several invertebrate groups, including sea urchins, crustaceans, and other bivalve and gastropod molluscs, along with Conus. Reviewed by Lessios (2008), these provide consistent evidence for at least partial isolation several million years prior to final closure of the isthmus. Tectonic activity elsewhere in the world was also profoundly affecting oceanography and paleobiogeography. The African Plate that had separated from the rest of Pangaea began moving northward. In the Middle Miocene it collided with the Eurasian Plate, severing the old Tethys Sea at the eastern end of the modern Mediterranean and separating it and the Atlantic from the Indian and Pacific oceans. This was also a major factor in the creation and boundaries of the continents and oceans familiar to us today. Oxy-

Setting the Stage: The Geological Theater 

90°W 25°N

80°W

85°W

75°W

70°W

55°W

60°W

65°W

High land

FLORIDA

GULF OF MEXICO

• 23

Low land Shallow marine

B A H A M A S YUCATAN

20°N

Western Cuba

Marine currents

East Central Cuba

West Central Cuba

Maya Block

AT LAN T I C OCEAN

Eastern Cuba

C AY

Chortis Block

15°N

Deep marine

MA

N

T

N RE

CH

Jamaica

Hispaniola

Pedro Bank

Puerto Rico Virgin Islands Virgin Is.

Nicaraguan Rise

Saba Bank

Lesser Antilles

Aves Ridge Grenada Basin

PACIFIC OCEAN CARIBBEAN SEA

Tobago Guajira

10°N

Paraguan á

Trinidad

Falcón Basin Southern Central America

Magdalena Basin

5°N

ORINOCO SEAWAY

GUYANA

SHIELD

Text-­fig. 2.2. Reconstruction of Middle Miocene paleogeography and ocean current patterns of the Caribbean region, 16–14 ma. Compared with the Eocene and Oligocene (Text-­fig. 2.1), “Neogene tectonic movements and deformations along the margins of the Caribbean Plate subdivided former structural ridges (Greater Antilles and Aves Ridges), creating isolated tectonic blocks and terranes separated by deep-­water gaps” (Iturralde-­Vinent and MacPhee 1999, 38). Narrow black lines outline present land boundaries. From Iturralde-­Vinent and MacPhee, 1999, Paleogeography of the Caribbean region: Implications for Cenozoic biogeography. Bulletin of the AMNH, no. 238, fig. 8; courtesy of M. A. Iturralde-­Vinent, R.D.E. MacPhee, and The American Museum of Natural History.

gen isotope ratios show that tropical temperatures prevailed for most of the Miocene in a broader band than at present, but somewhat narrower than during the Paleocene-­Eocene Thermal Maximum. The fossil record of the Caribbean region indicates that the massive reef-­building declined after the Oligocene. Miocene coral reefs were common but smaller and more scattered throughout the region (Johnson et al. 2009). The Miocene epoch saw major adaptive radiations of Conus in all parts of the world occupied by the genus. About half of the 350 Miocene Conus species are known from European fossils, indicating that diversity was likely highest in the Tethys Sea. Prior to the reduction of communication across the future isthmus, several Conus species were distributed widely throughout what are now the distinct EP and WA regions (Woodring 1974). As it became increasingly isolated through the Miocene, the WA region ranked next to the Tethyan in diversity, with about 90 species (25% of the world Conus fauna) along the

North American coast from the present location of Maryland south, the Gulf of Mexico, and the Caribbean region. Only one of these, Conus spurius Gmelin from the Middle and Late Miocene of Panama and Costa Rica, is extant today. It is likely the living species with the longest known fossil record. Worldwide, about 3% of living Conus species have fossil records that extend back to Miocene time (Kohn 1990). Geographic division into distinct northern and southern marine faunal assemblages within the present WA region was also occurring, probably from early Miocene time. Woodring (1974) first noted this briefly, and Petuch (1982) formalized and described them as two biogeographic provinces. The northern Caloosahatchian province comprised fossil assemblages from Virginia to southern Florida. The southern Gatunian province spanned the Caribbean Islands, northern South America, and Central America. The Central American fossil assemblages contain the shells of animals that lived both before and during

24  • Chapter 2 the tectonic events that later isolated the EP and WA regions. More recently, Vermeij (2005) has traced the major features of the fossil molluscan faunas of both provinces from the Miocene to Pleistocene epochs immediately preceding the Recent. Here I adopt Vermeij’s delineation of the extent of these provinces through most of Neogene time, the last 24 million years: Caloosahatchian, “along the North American coast from North Carolina to the Yucatan peninsula,” and Gatunian, “tropical America south of the Gulf of Mexico and Florida” (Vermeij 2005, 626–627). Although some islands of the Bahamas extend north of southernmost Florida, that entire archipelago is here assigned to the Gatunian for simplicity. The Caloosahatchian and Gatunian provinces of early Miocene time were both tropical; although not separated by a land barrier, they supported distinctly different marine faunas. Ocean current patterns presumably inhibited interchange between the two regions (see the upper left quadrant of Text-­fig. 2.3). Vermeij’s (2005) analysis of the temporal history of these faunas is based on six gastropod and two bivalve family-­group taxa (not including Conidae). He showed that by the late Miocene, about one-­third of Caloosahatchian species in the groups studied had extended their range southward into the Gatunian province where fewer species in these groups occurred, while no southern species had successfully invaded the northern province. Pliocene. By the time of the Miocene-­Pliocene boundary (5.3 ma), tectonic uplift of the Central American Volcanic Arc resulted in numerous large islands that were subject to considerable subaerial erosion, factors that reduced the water depths between them to only about 150 m (Coates 1997, figs. 1–19). “The Pliocene was also a time of general uplift in many areas of the Caribbean, providing the backbone of today’s relief” (Iturralde-­Vinent 2006, 811). This epoch also marked the onset of a series of glaciations and interglacial periods and associated wide excursions of ocean temperature at approximately 105-­year intervals to the present. The most important paleogeographic event of the Pliocene epoch (5.3–2 ma), however, was the final closure of the Isthmus of Panama (3.5 ma), completing the separation of the Atlantic and Pacific Oceans and permanently disrupting the Circumtropical Current. Because the isthmus closed gradually over some 10 million years, it also slowly but profoundly affected sea temperature, primary productivity, seasonality, the development of coral reefs, other major environmental features, and the entire marine biota.

These effects, summarized by Lessios (2008), differed strikingly between the two newly separated oceans, as they do today. On the EP side, sea temperatures fluctuate much more widely, upwelling deep water carries more nutrients to the surface, the primary productivity of new organic matter by photosynthesis is much higher, and coral reefs, which require warm, clear, well-­lighted water, are much less prominent. Attributes of the WA marine molluscan biota reflect these differences in that part of the focal region of this book. For example, detailed analysis of the fossil record indicates that both suspension-­ feeding bivalves and predatory gastropods decreased in abundance but changed little in diversity at the genus-­level on the Caribbean side of the isthmus, from the Miocene to Pleistocene and Recent time. Predators, including Conus, comprised 63% of all tropical WA gastropods in the Miocene, but only 36% in the Late Pliocene to Recent. These trends most likely reflect the major environmental changes during this part of the Neogene, including increasing sea temperature, lower primary productivity, diversification of reef corals, and increasing predominance of coral reefs and seagrass beds (Todd et al. 2002). As was the case earlier in earth history, the fact that several independently evolving animal groups show parallel or similar evolutionary patterns strongly suggests that these extrinsic environmental factors selected for adaptations. These are reflected particularly in life history differences between closely related geminate or sister species on the two sides of the isthmus (Lessios 1990; Moran 2004), as well as in their genetic differences mentioned above. Only about 180 fossil Conus species are recorded worldwide during the short Pliocene epoch, perhaps due to extinctions caused by low temperatures during ice ages. Geologically speaking, this was not very long ago, and about one-­third of the Pliocene species are considered extant, because their shells are indistinguishable from those of living species. As in the Miocene, about 25% of all known Pliocene species occurred in the northwestern Atlantic, while nearly half occurred in the Indo-­West Pacific region. The Miocene biogeographic pattern of molluscan invasions from the Caloosahatchian to the Gatunian province did not continue into the Pliocene. Now species richness was higher in the warmer Gatunian, and Vermeij (2005) demonstrated that about one-­ third of Gatunian species successfully invaded the northern province, presumably during warm, interglacial periods. In contrast, only about 2% of species from the now more depauperate Caloosahatchian province migrated into the more diverse Gatunian during the Pliocene and early Pleistocene.

Setting the Stage: The Geological Theater 

Pleistocene. Although the Pleistocene was the briefest epoch, from about 2 million to about 10,000 years ago, profound changes occurred in the abundance and diversity of different groups of molluscs. The alternating glacial and interglacial periods, and the declining productivity of the Caribbean after its final Pliocene separation from the Pacific, probably drove these changes. Predatory gastropods declined markedly in abundance in the Caribbean region during the first half of the Pleistocene. Although many Pliocene species went extinct during that time, so many new species originated that diversity did not change significantly (Jackson et al. 1996; Todd et al. 2002; Lessios 2008). Some predatory gastropods, particularly of the Superfamily Tonnoidea, survived into the Pleistocene on both sides of the isthmus, then became extinct on one side or the other, leading Beu (2001) to hypothesize that transport across the isthmus by planktonic larvae occurred during high sea stands associated with interglacial periods into the Early Pleistocene. Tonnoids have notoriously long larval lives; larvae of one species settled, metamorphosed, matured, and reproduced successfully after having been afloat in an aquarium for more than four years (Strathmann and Strathmann 2007). The Pleistocene was also the epoch immediately preceding our own, the Holocene, yet environmental factors occurring since then have militated against adequate sampling of fossils. Not only was the epoch short, but the currently high (and rising) sea level reduces the areas of outcrops on land available to study. And former tropical marine habitats, such as coral reefs that occur in areas of tectonic uplift, are subject to rain that dissolves shells. The shells of Conus and other caenogastropods are constructed of aragonite, a more soluble form of calcium carbonate than the calcite of some other molluscs. Although many extant species of Conus probably lived through much of the Pleistocene, only about 130 species are known as fossils from that epoch. Again, about 25% of these are known from the Western Atlantic, the vast majority (29/36) from Florida. In summary, the evolutionary history of Conus since its origin about 55 ma in the early Cenozoic Era is one of overall expansion in species numbers but with some periods of rapid diversification and other times when the fossil record indicates reduced diversity (see Kohn 1990, fig. 2). These temporal patterns of changing species richness are by no means confined to Conus and other gastropod taxa. Rather, they exemplify more general evolutionary patterns. Other invertebrate groups that have left fossil records follow similar trends (Raup 1976), waxing and waning contemporaneously. The major periods of rapid di-

• 25

versification were during the Early and Middle Eocene (55–39 ma), various times during the Miocene, and in the Pliocene and Pleistocene (about the last 5 my). The fact that so many of the animal groups that leave skeletal evidence in the fossil record share the same patterns of diversity over time strongly suggests that they represent responses by disparate taxa to the same extrinsic environmental changes. These most likely include the processes discussed above, especially the relationships of tectonic and climatic changes and how these changed sea level, sea bottom topography, and ocean circulation patterns. Iturralde-­ Vinent concisely summarizes Mesozoic and Cenozoic evolution of ocean circulation patterns and the changing distributions of land and sea in the Caribbean region (2006, figs. 9 and 10, respectively). An important corollary effect of these processes was the expansion of coral reefs in shallow, warm seas around the world. The activities of corals and reef-­building algae fostered the complex topography of reef habitats and the intricate biotic communities that have come to occupy them (Kohn 1997; Clarke and Crame 2003). Moreover, tropical terrestrial plant communities of northern South America have left fossil evidence of similar contemporaneous trends (Jaramillo et al. 2006), providing independent support of the strong influence of environmental change on patterns of diversity on land as well as in the sea.

Oceanography and Paleoceanography The period in Earth history discussed in the previous section, from the Mesozoic to the present, was one of dynamic tectonic activity and the associated elevation changes of islands, continents, and oceans. These regional events profoundly affected the movements of deep water masses as well as the surface currents that transport the planktonic larvae of bottom-­dwelling invertebrates. Smith et al. (2002) and Iturralde-­Vinent and MacPhee (1999; see Text-­figs. 2.1 and 2.2) concisely summarize interpretation of past current patterns, based on the known positions of land masses and oceans and on how the general pattern of surface currents today relates to the position of major seas, gulfs, island groups, and continents in the WA region. In the Atlantic and Caribbean, the North Atlantic Equatorial Current is the southern part of the large clockwise gyre set in motion mainly by the effect of Earth’s rotation on the fluid in the ocean basin. The North Equatorial Current flows westward at approximately 10º north latitude toward the north coast of South America. At the Lesser Antilles it splits, with one main part continuing northwestward in the Atlantic east of the Lesser Antilles and north of the

26  • Chapter 2 Greater Antilles to join the Gulf Stream that flows out of the Strait of Florida and north along the United States Atlantic coast. The other portion of the North Atlantic Current, known as the Guiana Current, passes through the southern Lesser Antilles into the Caribbean Sea, becoming the Caribbean Current. This also swings northward along the west coast of the Yucatan Peninsula and through the Yucatan Strait to become the Gulf of Mexico Loop Current. It then passes eastward through the Florida Strait, becoming the Gulf Stream as it joins the Antilles current and re-­enters the main clockwise circulation of the North Atlantic. Text-­fig. 2.2 shows this pattern, adapted to the relatively higher sea level of Miocene time, as the black outlines of modern land boundaries indicate (see also Smith et al. 2002, fig. 5). The North Atlantic gyre is known to transport planktonic gastropod larvae, including those of Conus (Scheltema 1989) and has likely been a source of colonizing species in the region since Eocene time. However, even at the present time little is known about which WA Conus species have larvae capable of transport, how long they are able to remain afloat, and how these factors affect their geographic distributions. These are all questions for future research.

Evolution and Biogeography of Western Atlantic Conus Within the Caribbean region, including the Gulf of Mexico and northern Brazil, there are upwards of twenty discrete faunal subregions, each with its own endemic mollusks. If malacologists wished to complete their collections of a certain group of mollusks, say the Muricidae or Conidae, they would need to sample all of these areas, and different depths, to ensure the completeness of the collections. For this reason, the Caribbean region, for its geographically small size when compared to other faunal regions such as the Indo-­Pacific, contains the richest tropical marine molluscan fauna in the world. —Petuch 1987

A few authors have subdivided The Western Central Atlantic region (Carpenter 2002) into more than 20 marine biogeographic subregions (Cowen et al. 2006), but most employ fewer (Sullivan Sealey and Bustamante 1999; Kramer 2003; Spalding et al. 2007). The criteria for subregions are mainly geographic and physical, the broad environmental factors that determine the distribution of organisms on land and in the sea. Geographic criteria important to primarily coastal benthic marine animals like Conus are the con-

figurations of continental coasts and islands. Important physical factors include bathymetry and the extent of areas at different depths, ocean currents, and patterns of temperature and salinity. The scheme used in this book is based primarily on that developed by Kramer (2003) (Text-­fig. 2.3), because its subregions are broad and with minor modifications it encompasses the distribution of both coral reefs and deeper areas appropriate to WA Conus. How did this region become such a rich source of marine biodiversity? Petuch’s generalization holds for Conus as well as Mollusca generally, and Conus at the genus level with more than 50 species likely contributes more to the phylum’s species diversity than any other genus. The geologic history outlined earlier in this chapter that led to such complexity of marine environments in the region provides a large part of the answer. So does the environmental complexity added by coral reefs, the complex, extensive three-­ dimensional biogenic structures that provide habitat for many other species and are particularly well suited to many Conus species. Additionally, several intrinsic aspects of the biology of Conus, and of other diverse neogastropod genera, also likely fostered their striking diversity, but rather little evidence is available as yet for WA species. In the better known IWP, three dozen Conus species may live on a single coral reef (Kohn 2001), equal numerically to two-­thirds of the entire Southeastern United States and Caribbean Conus fauna! Those co-­ occurring, similar IWP species tend to specialize ecologically both as predators on different food species and as occupiers of different microhabitat types. By doing so they avoid interspecific competition for the necessities of life. To what extent this partitioning of resources occurs in the Western Atlantic, where both species diversity and population density are reduced compared with the Indo-­West Pacific, remains a subject for future study. Another aspect of Caribbean Conus biodiversity in particular is that the geographic ranges of most species are much smaller than in the Indo-­West Pacific. Rather few species extend throughout the entire region, and several appear to be restricted to archipelagoes and in some cases to single islands. This statement is really a hypothesis in need of testing, because information on genetic relationships of populations in different geographic areas is still very limited. Several Brazilian Conus species whose shells closely resemble those of the Caribbean region especially need investigating to determine if (1) they are conspecific; (2) the allopatric populations have diverged at the species level (see e.g., Van Mol et al. 1967; Rios 1994; Gomes 2004, 2011); or, (3) like the corals Nunes et al.

• 27

Setting the Stage: The Geological Theater 

Bermuda U.S. East Coast

30°N

Gulf of Mexico

Ba

ha

ma

s

Gre ate r

20°N

Lesser Antilles

Western

Antilles

.

Caribbean Northern South America .

Br

10°N

az

0

300

il

600 Km

98°W

78°W

58°W Text-­fig. 2.3. Subregions of the Western Central Atlantic region used in this book. The map and subregions are based on Kramer (2003) but this figure adds Bermuda, omits Florida as a separate subregion; some other terms differ as follows: This book

Kramer (2003)

Greater Antilles Lesser Antilles Western Caribbean (Caribbean Mexico + Central America) Northern South America and offshore islands

Central Caribbean Eastern Caribbean Western + Southern Caribbean (part) Southern Caribbean (part)

The blue line separates the Caloosahatchian paleobiogeographic province (to the north and west) from the Gatunian province (to the south and east); the western portion of the latter indicates the southeast boundary of the Gulf of Mexico. This book’s demarcation of the Gulf of Mexico thus conforms more closely with that of the International Hydrographic Organization (1953,14) than that of Kramer (2003).

(2008) studied, they evolved from quite distinct ancestors but converged on common morphologies. A factor that likely restricts the geographic ranges of many western Atlantic Conus species is their limited ability to disperse, alluded to briefly above in the discussion of how ocean currents affect distribution. Gastropod shells grow by accretion, adding new shell material to the pre-­existing shell. Because they also coil around a central axis, they leave a record of their earlier life history in the persistent, visible older parts of the shell that form its spire. In well-­preserved specimens, this includes the protoconch, the part of the shell produced by the developing embryo and by the

larva after hatching, but prior to metamorphosis to a true bottom-­dwelling juvenile snail. The form and size of protoconchs are well known to differ according to the type of early life history that characterizes the species, but most of this knowledge derives from IWP species (Kohn and Perron1994). The species accounts in Chapter 5 include the known information for WA species and illustrate some of their protoconchs. Protoconch size reflects egg size, because the more yolk the mother snail puts in the egg, the larger the egg and the embryonic body will be. When larvae hatch from small eggs (usually 0.1–0.4 mm diameter

28  • Chapter 2 in Conus), the hatchling is a freely floating and swimming veliger larva. It must feed and grow as a member of the plankton. Usually its larval shell must exceed 1 mm in length before it is competent to settle down and metamorphose into a benthic juvenile. In contrast, larvae that develop from eggs that are 0.5 mm or more in diameter usually have a very short or no free-­swimming stage, and their yolk provides enough energy so that they do not need to feed before they are able to metamorphose (Kohn and Perron 1994). More than 80% of all Indo-­West Pacific Conus species examined have planktonic larvae, and some are distributed over that entire vast realm that occupies one-­fourth of the world’s ocean area (Kohn and Perron 1994). However, the proportion of Conus species that lack planktonic larvae in their life histories increases markedly in other geographic regions. In the WA, the proportion seems to be completely reversed. Nearly 80% (11/14) of Caribbean species examined had protoconchs with the characteristic features of nonplanktonic early development (Fortunato 2004). This is likely a general phenomenon among tropical Western Atlantic gastropods. Fortunato studied 23 other Caribbean neogastropods in the families Olividae and Columbellidae with similar results; only four of the 37 species in the three families had planktonic, planktotrophic larvae. Although her samples were smaller, about half of the EP species of the same families had planktotrophic larvae: 4/8 Conus species and 21/47 species in all (45%). The WA-­EP difference was not significant for Conus because of the small number of species (G test: P > 0.1) but was highly significant (P  0.70; PMD > 0.85 broadly and ventricosely conical: RD > 0.70; PMD 0.75–0.85 broadly ovate or broadly cylindrical: RD > 0.70; PMD  0.85 ventricosely conical or conoid-­cylindrical: RD 0.50–0.70; PMD 0.75–0.85 ovate or cylindrical: RD 0.50–0.70; PMD