The Ecology of Deep-Sea Hydrothermal Vents 9780691239477

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The Ecology of Deep-Sea Hydrothermal Vents

CINDY LEE VAN DOVER

The Ecology of Deep-Sea Hydrothermal Vents

P R I N C E T O N

U N I V E R S I T Y

P R E S S

• P R I N C E T O N ,

N E W

J E R S E Y

Copyright © 2000 by Princeton University Press Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540 In the United Kingdom: Princeton University Press, Chichester, West Sussex All Rights Reserved Library of Congress Cataloging-in-Publication Data Van Dover, Cindy. The ecology of deep-sea hydrothermal vents / Cindy Lee Van Dover. p. cm. Includes bibliographical references (p. ). ISBN 0-691-05780-X (cloth : alk. paper). — ISBN 0-691-04929-7 (pbk. : alk. paper) 1. Hydrothermal vent ecology. I. Title. QH541.5.D35V34 2000 577.7'9—dc21 99-16545 CIP This book has been composed in Times Roman The paper used in this publication meets the minimum requirements of ANSI/NISO Z39.48-1992 (R1997) (Permanence of Paper) http://pup.princeton.edu Printed in the United States of America

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For Bob Hessler and Fred Grassle

Contents

PREFACE ACKNOWLEDGMENTS

1. The Non-Vent Deep Sea 1.1 1.2 1.3 1.4 1.5

The Physical Environment in the Deep Sea The Deep-Sea Fauna Deep-Sea Diversity Biogeography and Population Genetics Biochemical and Physiological Adaptations to the Deep-Sea Environment 1.6 Benthopelagic Coupling between Surface Productivity and the Deep Sea 1.7 Rates of Biological Processes in the Deep Sea 1.8 The Vent Contrast References

2. Geological Setting of Hydrothermal Vents 2.1 What Are Mid-Ocean Ridges? 2.1.1 How Spreading Rates for Ridge Axes Are Determined 2.1.2 Spreading Rates 2.1.3 Segmentation 2.1.4 Magma Supply and Spreading Rate 2.2 Back-Arc and Fore-Arc Spreading Centers 2.3 Seamounts 2.4 Volcanic and Tectonic Seafloor Features 2.4.1 Crustal Structure 2.4.2 Volcanic and Tectonic Fissures 2.4.3 Lava Lakes, Drainback Features, and Lava Pillars 2.4.4 Axial Boundary Faults 2.4.5 Lava Flow Morphologies

xvii xix

3 4 5 8 11 13 15 18 19 20

25 25 28 29 31 34 36 37 39 39 39 41 41 43

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2.4.6 Emplacement of Lavas and the Time-Course of a Diking Event 2.4.7 Lava Dating 2.5 Deep-Sea Hydrothermal Fields 2.5.1 Missing Heat and Hydrothermal Cooling at Ridge Crests 2.5.2 Sulfide Deposits Morphological Variations Columnar Chimneys and Black Smokers White Smokers Beehives and Flanges Complex Sulfide Mounds Weathering of Seafloor Sulfides Dimensions and Ages of Active Hydrothermal Fields

2.5.3 Low-Temperature Diffuse Flows 2.5.4 Sediment-Hosted Hydrothermal Systems 2.5.5 Ophiolites Appendix References

3. Chemical and Physical Properties of Vent Fluids 3.1 Submarine Hydrothermal Circulation Cells: High-Temperature Reaction Zones 3.2 Phase Separation 3.3 Flow Rates, Transit Times, and Temperature of Formation 3.4 End-Member Fluids 3.4.1 Composition Basic Controls on Chemistry 3.4.2 Magmatic Inputs 3.4.3 Evolution of Vent-Fluid Chemistry 3.4.4 Back-Arc Fluid Chemistries 3.5 Thermal Radiation 3.6 Axial Low-Temperature, Diffuse-Flow Chemistry 3.6.1 Flow Rates, Temperature, and Temperature Variability 3.6.2 Silicate 3.6.3 Sulfide 3.6.4 Oxygen 3.6.5 Profiles of Oxygen, Sulfide, Silicate, and Temperature 3.6.6 Methane, Manganese, and Iron 3.6.7 Nitrogen and Phosphorus Compounds

43 45 47 47 48 48 49 50 50 53 56 56 58 60 61 63 70

76 76 78 80 80 80 81 82 83 83 84 85 86 87 87 89 89 91 92

CONTENTS

3.7 Flank Low-Temperature Fluids 3.8 Global Fluxes and the Hydrothermal Influence on Ocean Chemistry and Currents References

4. Hydrothermal Plumes 4.1 Anatomy of a Black-Smoker Plume 4.1.1 Orifice 4.1.2 Buoyant Plume 4.1.3 Effluent Layer 4.2 Megaplumes 4.3 Spatial and Temporal Distributions of Plumes 4.3.1 Relationship between Plume Distributions and Geophysical Parameters 4.4 Plume-Driven Mesoscale Circulation 4.4.1 Plume Vortices 4.4.2 Advection and Downwelling 4.4.3 Basin-Scale Circulation 4.5 Diffuse-Flow Plumes References

5- Microbial Ecology 5.1 Autotrophic Organisms at Vents 5.1.1 Nomenclature 5.1.2 Aerobic and Anaerobic Chemoautotrophy at Vents Methanotrophy 5.1.3 Carbon Dioxide Fixation 5.1.4 Mixotrophy 5.1.5 Net Chemoautotrophic Production in Free-Living Hydrothermal-Vent Microorganisms Alternatives to Chemoautotrophy Organic Thermogenesis Hypothesis Detrital Thermal Alteration Hypothesis 5.2 Ecology of Free-Living Microorganisms 5.2.1 Microbial Habitats 5.2.2 Hyperthermophiles and Superthermophiles Flange Microbial Ecology and the Archaea Microorganisms in Black-Smoker Fluids The "Endeavour Model" The Subsurface Biosphere 5.2.3 Plume Microbiology 5.2.4 Suspended Microbial Populations

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99 99 99 100 101 104 106 106 110 110 110 111 112 112

115 117 117 117 119 120 120 120 120 121 121 122 122 122 125 125 125 127 127 128

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5.2.5 Microbial Community Composition Dominance of a Single Bacterial Phylotype at a Mid-Atlantic Ridge Vent Diversity and Community Structure in Microbial Mats, Loihi Seamount Sulfur-Oxidizing Heterotrophs at Vents 5.2.6 Bacterial Blooms 5.2.7 Microbial Mats 5.2.8 The Link between Chemoautotrophic and Photosynthetic Processes 5.3 A Search for In Situ Bacterial Photosynthesis 5.4 Microbial Genesis of Hydrothermal Mineral Deposits 5.5 Microbial Exploitation of Particulate Sulfides 5.6 Biotechnology References 6. Symbiosis 6.1. Discovery 6.1.1 Sustenance of Gutless Tubeworms 6.1.2 Endosymbiotic Bacteria in Vent Mollusks 6.1.3 Episymbionts 6.2 Methanotrophic Symbioses 6.2.1 Dual Symbioses 6.2.2 Methanotrophs in Sponges 6.3 Adaptive Characteristics of Symbiosis 6.4 Host Nutrition 6.4.1 Digestive Enzymes 6.5 Symbiont Phylogeny 6.5.1 Endosymbiont Phylogeny and Host Fidelity 6.5.2 Episymbiont Phylogeny 6.6 Symbiont Acquisition References

7. Physiological Ecology 7.1 Novel Metabolic Demands 7.2 Riftia pachyptila 7.2.1 Anatomy of a Tubeworm 7.2.2 The Tubeworm Environment 7.2.3 Adaptations for Carbon Uptake and Transport in Riftia pachyptila Host Respiratory Inorganic Carbon

129 130 130 132 132 134 135 137 137 138 139 140 145 145 146 150 150 153 153 156 157 158 160 162 162 165 166 167

173 173 114 174 177 111

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Environmental Sources of Inorganic Carbon and the Role of Carbonic Anhydrase pH Regulation Carbon Transport Inorganic Carbon Capacity Carbon Fixation Rates 7.2.4 Sulfide Sulfide Toxicity Sulfide Uptake and Transport Coupling of Sulfide Detoxification and Energy Exploitation 7.2.5 Oxygen 7.2.6 Nitrogen Nitrate Respiration 7.3 Seep Vestimentiferans and Methanotrophic Pogonophorans 7.4 Vent and Seep Bivalve-Mollusk Symbioses 7.4.1 Calyptogena magnified 7.4.2 Bathymodiolid Mussels Bathymodiolus thermophilus Methanotrophic Mussels 7.4.3 Other Mollusk Symbioses 7.5 Physiological Ecology of Episymbiont-Invertebrate Associations 7.5.1 Alvinella pompejana 7.6 Sulfide Detoxification 7.7 Growth Rates 7.8 Thermal Adaptations 7.8.1 Indices of Thermal Tolerance and Adaptation Thermal Tolerance in Alvinellid Species 7.9 Heavy Metals and Petroleum Hydrocarbons 7.10 Sensory Adaptations 7.10.1 Novel Photoreceptors in Vent Shrimp 7.10.2 Chemoreception References

8. Trophic Ecology 8.1 The Food Web 8.1.1 The Rose Garden Food Web 8.2 Biological Sleuthing: Biomarker Assays 8.2.1 Stable Isotope Techniques

Notation Stable Isotope Evidence for the Role of Free-Living Microorganisms in Vent Food Webs

179 180 182 182 182 183 183 183 186 187 187 188 188 189 189 192 192 193 194 196 196 197 201 202 203 204 208 209 210 214 216

227 227 228 231 231

231 233

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8.2.2 Fatty Acids, Sterols, and Carotenoids Fatty-Acid Nomenclature Fatty-Acid Biomarkers Comparison of Lipid Characteristics of Tubeworms (Riftia pachyptila), Mussels (Bathymodiolus thermophilus), and Amphipods (Halice hesmonectes) on the East Pacific Rise "Essential" Fatty Acids Lipid-Condition Indices Sterols Carotenoids 8.3 Integrated Approaches to Trophic Ecology 8.3.1 Trophic Ecology of Vent Mussels, Bathymodiolus

236 236 237

237 240 240 240 241 241

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thermophilus 8.3.2 Trophic Ecology of Vent Shrimp, Rimicaris exoculata, and an Anecdote about Who Eats Them 8.4 Export of Chemosynthetic Production from Vents References

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Reproductive Ecology

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9.1 Gametogenesis 9.1.1 Evidence for Synchronous Gametogenesis

259 260 261 264 264 264 265 266 266 267 268 269 271 271 273 273 276 277 277 278 279

Environmental Cues Recruited Synchrony

9.1.2 Evidence for Asynchronous Gametogenesis Release of Gametes and Larvae Riftia pachyptila Bythograea sp. Calyptogena soyae

9.2 Larval Development 9.2.1 Vestimentifera 9.2.2 Bathymodiolid Mussels 9.2.3 Bythograeid Crabs 9.2.4 Alvinocarid Shrimp 9.3 Larval Dispersal and Retention 9.3.1 Alvinellid Dispersal Model 9.3.2 Plume Dispersal 9.3.3 Megaplume Dispersal 9.3.4 Mesoscale Flows 9.3.5 Dispersal by Non-Larval Stages 9.4 Settlement Cues

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9.5 Recruitment Appendix References

10. Community Dynamics 10.1 The Early Work 10.2 Dynamic Succession at Northeast Pacific Vents 10.2.1 High-Resolution Time-Series Studies on the Juan de Fuca Ridge 10.3 Community Dynamics on the Mid-Atlantic Ridge 10.4 Eruptions 10.4.1 The 9°N Event 10.4.2 The CoAxial Event 10.4.3 Sweepstakes versus Predictable Sequences References

11. Evolution and Biogeography 11.1 Origins of Vent Fauna 11.1.1 Immigrants from the Surrounding Deep Sea 11.1.2 Immigrants with Close Shallow-Water Relatives 11.1.3 Vent Taxa Shared with Other Chemosynthetic Ecosystems Taxonomic Position and Origin of the Vestimentifera 11.1.4 Vent Taxa Shared with Both Other Chemosynthetic Ecosystems and Nonchemosynthetic Habitats 11.1.5 Specialized Taxa Found Only at Hydrothermal Vents 11.1.6 The "Ancient" Taxa Ancient Barnacles Ancient Mollusks 11.1.7 The Newman and McLean Hypothesis of Relict Vent Faunas Hickman's Counterhypothesis 11.2 Fossil Vent Communities 11.3 Vent Ecosystems as Refuges from Major Planetary Extinction Events 11.4 Species Diversity 11.5 Taxonomic Cautionary Tales 11.5.1 Cryptic Species 11.5.2 Phenotypic Plasticity 11.5.3 Ontogenetic Stages 11.6 Biogeography

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290 290 293 298 299 301 301 303 308 309

313 313 313 314 314 316 319 320 320 320 322 323 323 324 325 325 328 328 329 329 330

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11.6.1 Pacific Biogeographic Patterns Missing Mussels {Bathymodiolus thermophilus) Centers of Diversity along Linear Arrays of Habitat North America as a Biogeographical Barrier Mariana Hydrothermal-Vent Fauna 11.6.2 Paleotectonic Controls on the Atlantic Vent Fauna 11.6.3 Similarities among Global Vent Biogeographic Provinces 11.6.4 Biogeography of Fast- versus Slow-Spreading Centers 11.6.5 Physical Oceanography and Bathymetry The Romanche Fracture Zone 11.6.6 Shallow-Water Vents 11.7 Gene Flow and Genetic Diversity References

12. Cognate Communities 12.1 Atlantic Sites 12.1.1 Florida Escarpment (Gulf of Mexico) 12.1.2 Louisiana Slope Hydrocarbon and Brine Seeps (Gulf of Mexico) 12.1.3 The Laurentian Fan 12.1.4 Barbados Subduction Zone 12.1.5 North Sea Pockmarks 12.1.6 Skagerrak Methane Seep 12.1.7 The Francois Vieljeux 12.1.8 Coral Reefs 12.2 Pacific Sites 12.2.1 Cascadia Subduction Zone 12.2.2 Western Pacific Subduction Zones Kaiko Project Sagami Bay 12.2.3 Peruvian Subduction Zone 12.2.4 Monterey Canyon 12.2.5 Northern California Methane Hydrate Field 12.2.6 Guaymas Basin Transform Margin Seeps 12.2.7 Shallow-Water Hydrocarbon Seeps 12.2.8 British Columbia Fjords 12.2.9 Aleutian Subduction Zone 12.3 Whale Skeletons 12.4 Fossil Seeps References

330 331 332 332 333 335 337 340 342 342 343 343 347

355 360 360 363 367 369 372 374 31A 375 375 375 376 376 379 379 381 383 383 384 384 384 385 389 390

CONTENTS

13. Hydrothermal Systems and the Origin of Life 13.1 Earth's Early Environment 13.2 Evolution of Hydrothermal Systems 13.3 Heterotrophic versus Chemosynthetic Hypotheses for the Origin of Life 13.4 Evidence for Thermophilic, Autotrophic Ancestors 13.4.1 Wachterhauser's Outline for the Origin and Evolution of Life 13.4.2 Synthesis of Organic Compounds in Hydrothermal Systems 13.5 Extraterrestrial Hydrothermal Systems and the Search for Life in Outer Space References INDEX

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397 397 398 399 402 404 406 407 409 413

Preface Deep-sea hydrothermal vents and their attendant faunas were discovered in 1977. While the hot-water springs were predicted to occur at seafloor spreading centers, no one expected to find them colonized by exotic invertebrate faunas. Accustomed to a view of the deep sea as a food-limited environment, the puzzle of how lush communities could be maintained provoked biologists into a flurry of research activity. Based on collections from the early expeditions to hydrothermal vents in 1979 and 1982, investigators identified the significance of chemoautotrophic primary production in these systems and described for the first time the endosymbiotic relationships between sulfide-oxidizing bacteria and their invertebrate hosts. Physiological studies focused on adaptations that allow invertebrates with aerobic respiration to survive in environments with millimolar concentrations of sulfide, a compound that inhibits the cytochrome-c oxidase system at micro- to nanomolar concentrations. As field programs multiplied and more vent communities were discovered, biogeographic patterns in the distributions of faunas became apparent and ecological issues of habitat requirements, dispersal, and population genetics began to be addressed. New chemosynthetic faunas were discovered associated with diverse settings, from brine and hydrocarbon seeps to whale skeletons. Massive bacterial blooms triggered by the release of nutrients during a volcanic eruption, rapid colonization of new vents by invertebrates, and burial of extant vent communities by lava flows demonstrate the dynamic nature of hydrothermal systems. Perhaps the most provocative consequence of the discovery of seafloor hydrothermal vents is the suggestion that these vents may have been the site where life originated. It has been more than two decades since these discoveries began, and there are now thousands of publications on hydrothermal vents in the primary literature, yet there has been no textbook available for a course in hydrothermal vent biology. Those of us who teach the subject rely on collections of reprints from the primary literature and on review articles. While such literature will continue to be essential for any intensive course on vent ecology, this textbook serves as a guide to the field and provides reference material for understanding the context in which current research at deep-sea vents is progressing.

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PREFACE

Although written for advanced undergraduate students, graduate students, and the professional scientist, this book should be accessible and of interest to the nonspecialist as well. After all, how often can you find volcanic eruptions, hot springs, symbioses, whale skeletons, and new ideas about the origin of life, all within the covers of one textbook? I have made a considerable effort to be thorough, but citations in this book are by no means exhaustive. I tend not to reference review papers, unless they provide syntheses or access to literature not normally available to the biologist. I prefer instead to give credit to the original authors. There are undoubtedly omissions; I trust that my colleagues will notify me of errors and oversight, and of new observations, so that subsequent editions may be corrected and amended. I have also chosen to provide no comprehensive bestiary, since this already exists as a stunning collection of photographs, illustrations, and text in a volume published by my French colleagues, Daniel Desbruyeres and Michel Segonzac, Handbook of Deep-Sea Hydrothermal Vent Fauna (1997, IFREMER, Brest, France, 279 pp.). Readers should also venture onto the Internet in search of sites with color photos of vent ecosystems. They are easy to find and are invaluable as means of visualizing the extreme habitats and unusual faunas found at vents and related chemosynthetic communities.

Acknowledgments A book like this is a celebration of the work of many individuals. What I write about here is the result of the dedication and passion of my colleagues, and so it is the authors cited in the text whom I must acknowledge first. Many of these individuals have been my shipmates and submates; we have shared the adventure together. I hope that I have told their stories with due credit and as clearly as they have related them to me. Paul Tyler and Colleen Cavanaugh read a draft of the entire manuscript and provided invaluable suggestions and corrections. I am also grateful to reviewers of individual chapters, including Joe Cann, Colleen Cavanaugh, Margaret Chadsey, Jim Childress, John Edmond, Susan Humphris, and John Rummel. Tom Beatty, Dave Brenner, Craig Cary, Colleen Cavanaugh, Steve Chamberlain, Dan Fornari, Chris Fox, Olav Giere, Marty Kleinrock, Ian MacDonald, David Piper, Walter Roest, Veronique Robigou, Tim Shank, Craig Taylor, Verena Tunnicliffe, Vladimir Yurkov, Bob Vrijenhoek, and Carl Wirsen were especially helpful in providing illustrations. Jewel Thomas was a wizard at photographic reproduction of fine details, and Keli Mingin devoted long hours to scanning and modifying graphics. There are always a few individuals whose support makes the completion of a task such as this a little bit easier. Jack Repcheck, the editor who started me on this project, has a priceless talent for offering praise just when it is needed most. Cheryl Jenkins greeted this project with enthusiasm and corrected many editorial details; her assistance has been invaluable. Both Paul Heideman and Cheryl Jenkins welcomed me to Williamsburg, and their friendship, together with the support of the Biology Department at the College of William and Mary, has made completion of this project easier. I am particularly grateful to John Rummel, whose enduring good humor and compassion holds me steady. This book would not exist were it not for the support of mid-ocean ridge research by the National Science Foundation. I am extremely grateful for this support, which is expressed not just in funded proposals, but in the remarkably efficient infrastructure that allows the big ships to operate and scientists to gather together to coordinate programs and brief each other and the public on their findings. The idea for a textbook on vents developed during my tenure as the

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ACKNOWLEDGMENTS

McCurdy Scholar at the Duke Marine Laboratory, where I first taught courses on hydrothermal vents to undergraduates. I am grateful to my students for the eagerness with which they approached this subject and the thoroughness with which they convinced me that a textbook on hydrothermal vents would find an enthusiastic audience. I am also obliged to Joe Ramus and my Duke Marine Laboratory colleagues who first gave me the opportunity to teach. This project continued through my tenure at the University of Alaska, Fairbanks, where I found further support from the staff of the West Coast and Polar Regions Undersea Research Center. My thanks to Ray Highsmith, Geoff Wheat, Dave Doudna, and Dana Kapla for all of their help. My deepest debts are to my graduate mentors, Fred Grassle and Bob Hessler, who gave me the knowledge and skills and freedom I needed to explore the deep sea. This work would not exist were it not for their willingness to encourage the twists of my career.

The Ecology of Deep-Sea Hydrothermal Vents

1 The Non-Vent Deep Sea This chapter provides an overview of some dominant themes in non-vent deep-sea research that serve to place the ecology of hydrothermal-vent faunas in the larger context of deep-sea biology. Over the past several decades, our knowledge of the deep-sea environment and fauna has increased substantially. Much of this new knowledge is presented in a textbook by Gage and Tyler (1991) titled Deep Sea Biology: A Natural History of Organisms at the Deep-Sea Floor, and in an addendum by Tyler (1995). The student who seeks more information and further access to the non-vent deepsea literature should turn to Gage and Tyler (1991) for direction. Most of the non-vent deep-sea terrain is abyssal plain, much like the proverbial Kansas: flat, sometimes marked by rolling hills, with a mindnumbing sameness in larger perspective, though on local scales heterogeneity abounds. Mud is the operative descriptor (fig. 1.1). Carbonate and siliceous oozes—long-dead, microscopic bodies of foramaniferans, diatoms, and radiolarians that have drifted down from surface waters—pile up over eons, not ankle- or knee- or even chin-deep, but kilometers-deep, covering the landscape. Bathymetric relief begins at the continental margins, where large depth gradients are traversed by steep slopes and where deep canyons may cut into and drain the continental shelf. Other features can also provide relief: volcanic seamounts stud the seafloor, sometimes extending from bathyal depths to just below the surface, and subduction zones (the deep trenches of the ocean) devour the seafloor along margins of crustal plates. Despite still prevailing wisdom, the deep sea is not a desert. It meets Webster's definition of desert as a "desolating or forbidding prospect," but only if one takes an anthropocentric view. True, in most places, the biomass of animal life is insubstantial, measured by teaspoons rather than buckets. What life there is, though, is remarkably diverse. In any one square meter of mud, more than 100 species of small worms and mollusks and crustaceans might be found. An adjacent square meter of mud may hold just as many different species. The deep sea is a food-limited environment. All of the food reaching the seafloor derives from primary production in sunlit surface waters. It is comprised of small, even minute, bits and pieces of organic material that have

CHAPTER 1

Figure 1.1. A rat-tail fish cruises above the mud at 2200 m off the coast of New Jersey. Photo by C. L. Van Dover.

cycled through organisms several times, always losing some portion of their nutritive value along the way, during their slow drift to the seafloor. Organic content of seafloor sediments is on the order of a few tenths of a percent by weight; contrast this with the 5% or more organic content of muds in shallow-water regimes of estuaries and bays. Food does not arrive to the ocean depths in a constant rain everywhere. It is not distributed evenly in time or in space. This is contrary to the perception of the deep sea that persisted until the late 1960s. The deep sea was long thought to be the epitome of a constant environment: devoid of light, untouched by climate and seasons, uniformly food limited, with constant cold temperature and high pressure. In such a homogeneous environment, competition among species was thought to resolve infinitesimal niches, accounting for the rich biodiversity observed in the deep sea. 1.1 THE PHYSICAL ENVIRONMENT IN THE DEEP SEA Light penetration and sunlight-driven photosynthesis are limited to the first several hundred meters of the water column; much below 300 m, penetration

THE NON-VENT DEEP SEA

5

of light is inadequate to support photosynthesis. Increasing depth means increasing hydrostatic pressure, one atmosphere for every 10 m of water depth, and decreasing temperature. Below 1000 m, seawater is < 5°C. Deep-sea water forms in the North Atlantic by the sinking of cold, relatively fresh water at latitudes near Greenland. This North Atlantic bottom water migrates southward as cold, oxygen-rich plumes to mix eventually with newly formed circumpolar Antarctic bottom water. The combined Atlantic and Antarctic deep waters spread northward into the Pacific and Indian Oceans (Gordon 1996). Residence times for deep water are on the order of hundreds of years. Because oxygen demand by deep-sea organisms is relatively small, deep-sea water retains its oxygen, except in localized downwelling regions. Most hydrothermal systems are located on mid-ocean ridges at bathyal to abyssal depths of 1500-4000 m. At comparable depths (e.g., 3000 m), the typical abyssal plain environment is characterized as follows: Sediment Sediment deposition rate Organic content of sediments Temperature Pressure Currents Tidal component Salinity O 2 concentration Light

Soft clay or siliceous or carbonaceous oozes Millimeters to centimeters per thousand years < 0.1% beneath oligotrophic waters, > 0.5% under productive areas 1-2°C 300 atm Sluggish (1 cm s" 1 , or < 1 km d" 1 ) Present 34.8%c (oceanic) 5-6 ml I " 1 (near saturation) None, except bioluminescence and Cerenkov radiation (40K decay)

1.2 THE DEEP-SEA FAUNA Apart from their tremendous biomass, a striking aspect of hydrothermal-vent faunas is their divergence in general character from typical non-vent deepsea invertebrates. On abyssal plains, echinoderms are often the most conspicuous fauna. These include sea stars and brittle stars, sea cucumbers, sea urchins, and sea lilies. Coelenterates—sea anemones and solitary corals— and a variety of glass or hexactinellid sponges may also be present. Where there is elevated current activity (e.g., on the tops of seamounts or other types of topographic relief), meadowlike stands of large, suspension-feeding corals and sea pens, sponges, and brachiopods may flourish (fig. 1.2; e.g.,

CHAPTER 1

Figure 1.2. Gorgonian whip corals (~ 50-100 cm in length) dominate the volcanic top of Fieberling Guyot in the eastern Pacific. Photo courtesy of Woods Hole Oceanographic Institution.

Genin et al. 1986, 1992). Within soft sediments, myriad smaller, "infaunal" forms prevail, mostly bivalve and gastropod mollusks, polychaete worms, and a variety of diminutive crustaceans including amphipods, isopods, tanaids, and copepods (table 1.1). The deep-sea fauna itself includes many "celebrity" taxa, including relict forms such as sea lilies (crinoids, phylum Echinodermata) and members of the primitive molluscan genus Neopilina (class Monoplacophora), colossal forms such as giant scavenging isopods and amphipods (class Crustacea, phylum Arthropoda) and fist-sized protozoans (class Xenophyophorea, phylum Rhizopoda), and bizarre forms such as the stalked culeolid tunicates, which look like brown paper sacks suspended on sticks (phylum Chordata). There are sea cucumbers that swim through the water column by undulations of their thick gelatinous bodies and tripod fish that perch on the seafloor using the trio of elongated pelvic fins and tail fin ray. Depending on the group, the origin of deep-sea fauna has been either by evolution within the deep sea or by migration from shallow water. Faunal similarities between the deep sea and shallow Antarctic regions indicate an

THE NON-VENT DEEP SEA

TABLE 1.1. Taxa collected in 21 m2 of sediment from 2100 m off New England Number of Species Coelenterata (Hydrozoa) (Anthozoa) (Scyphozoa) Nemertea Priapulida Annelida (Polychaeta) (Oligochaeta) Echiura Sipuncula Pogonophora Mollusca (Bivalvia) (Gastropoda) (Scaphopoda) (Aplacophora) Arthropoda (Cumacea) (Tanaidacea) (Isopoda) (Amphipoda) (Pycnogonida) Bryozoa Brachiopoda Echinodermata (Echinoidea) (Ophiuroidea) (Asteroidea) (Holothuroidea) Hemichordata Chordata TOTALS

19 (6) (12) (1) 22 2 385 (367) (18) 4 15 13 106 (45) (28) (9) (24) 185 (25) (45) (59) (55) (1) 1 2 39 (9) (16) (3) (11) 4 1 798

Number of Families 10 (3) (6) (1) 1 1 49 (47) (2) 2 3 5 43 (18) (18) (4) (3) 40 (4) (8) (11) (16) (1) 1 1 13 (2) (6) (3) (2) 1 1 171

From Gage and Tyler 1991.

avenue for dispersion of taxa, which may possibly be bidirectional. Similar ambiguities exist in determining the direction of migration of species along the depth gradients between continental shelves and the deep sea. Molecular studies of the phylogenetics of deep-sea species should provide additional scope for assessing the origins of the deep-sea fauna.

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CHAPTER 1

1.3 DEEP-SEA DIVERSITY In the late 1960s, biologists Howard Sanders and Robert Hessler dispelled for good the long-held myth that the deep sea is occupied only by a small number of specialized species (Hessler and Sanders 1967; Sanders and Hessler 1969). Their semiquantitative sampling of benthos along a transect from shallow waters off Gay Head on Martha's Vineyard, Massachusetts, to deep waters near Bermuda showed an increasing diversity with depth (fig. 1.3). Grassle and Maciolek (1993) analyzed species diversity in quantitative box cores collected from the Atlantic slope of the United States and confirmed the high diversity of species in the deep sea, finding 798 species in 233 box cores. These authors extrapolated the rate of species accumulation in their set of box cores (equal to 21 m2, an unimaginably minute fraction of the total area of Earth's seafloor) to the diversity of the global abyss, projecting a tally of more than 10 million species—more than enough species to rival the celebrated diversity of tropical rainforests. While the extrapolation method is controversial (May 1993), the critical point is not so much the exact number of species in the deep sea but rather our profound ignorance of a property as fundamental as a simple list of species for the ecosystem that covers most of our planet. While there is little doubt that the deep sea is rich in species, the model of increasing diversity with depth set out by Sanders and Hessler (1969) is on tenuous ground. Partly at issue is one's choice of shallow-water location used for comparison. For example, the fauna of the Norwegian continental shelf (70-300 m) has a species diversity equal to that of the deep sea (Gray 1994). In coastal sediments of Australia, Poore and Wilson (1993) found 800 species in an area of shallow seafloor half as great as the accumulated sample size of Grassle and Maciolek (1993), suggesting again that diversity might not always increase with depth. Rex and his colleagues (reviewed in Rex et al. 1997) demonstrate that the depth-diversity relationship, instead of monotonically increasing as proposed by Sanders and Hessler (1969), is more likely parabolic, with an initial increase in species diversity with depth to a maximum at intermediate depths and decreasing diversity at extreme depths (fig. 1.4). How can high diversity be established and maintained in an environment that is as reputedly homogeneous as the deep sea? This question continues to motivate considerable discussion and theorizing, and no single answer is satisfying. Sanders (1968) invoked what he called the "stability-time" hypothesis (fig. 1.5). In physically constant environments such as the deep sea, where physiological stresses are historically low, "biologically accommodated" communities can evolve. In such a situation, biological stress caused by intense competition, simple food webs, or imbalances in predator-prey

THE NON-VENT DEEP SEA Tropical Shallow Water Deep Sea

Boreal Shallow

500

1000

1500

2000

2500

Number of Individuals

Figure 1.3. Comparison of species diversity among polychaetes and bivalves in a variety of marine environments, emphasizing the high diversity found in deep-sea samples. From Sanders 1968. 70 60.~ 50-

!

4 0 H

.9 30-

1,0-

10500

1000

1500

2000

2500

Depth (m)

Figure 1.4. Parabolic pattern of macrofaunal invertebrate diversity vs. depth off the coast of Massachusetts. Diversity is expressed as the expected number of species in a sample of 100 individuals. Note that variability in diversity at a given depth is high. This pattern is not repeatable at all other geographic locations. From Rex et al. 1997.

10

CHAPTER 1

Gradient of Physiological Stress ' . ; ' ^

High

Low

Number of Species Predominantly Biologically Accommodated

Predominantly Physically Controlled

Abiotic

Figure 1.5. Sanders' (1968) representation of the stability-time hypothesis. Along a gradient of physiological stress from low to high, the number of species diminishes as conditions change from those that promote biological accommodation to those in which species' presence is determined by physical factors. interactions is an adaptive force and is gradually mediated by evolution of "biologically accommodated" or specialized species. Area is a recurring correlate with diversity in a variety of ecosystems. High diversity in tropical terrestrial regions is in part attributed to the greater areal extent of this terrestrial habitat compared to any other. The same argument has been made for the deep sea (Abele and Walters 1979). Other investigators see the deep seabed as an extremely heterogeneous environment on the scale of macrofaunal organisms. In these models, small features such as animal tubes, burrows, and tracks are resources to be partitioned among species (e.g., Jumars and Eckman 1983). Dayton and Hessler (1972) were the first to argue that disturbance in the deep sea (referring primarily to predation and cropping effects) limits the populations of competitors, such that resources are rarely limiting and species can coexist on the same resources. The intermediate-disturbance hypothesis of Connell (1978), proposed to account for maintenance of the high diversity of coral reefs and tropical rainforests, has been invoked to account for patterns in deep-sea diversity with depth (Rex 1981). In this model, disturbance caused by storms or tree falls in coral reefs and forests, respectively, generates openings for new colonists, typically of species different from those occupying the undisturbed areas. With no disturbance or with too

THE NON-VENT DEEP SEA

11

much disturbance, species diversity is low, but at some intermediate point in this gradient of disturbance, diversity is maximal. In the ocean, productivity and predation are presumed to interact, such that in productive shallow waters, predation does not facilitate maintenance of high diversity, while at intermediate depths, where the flux of organic material to the seafloor is reduced, predation mediates coexistence of multiple species on the same resource. At still deeper depths, both predation and production rates are low and diversity drops again. The result is thus a parabolic curve of species richness with depth. Actual data on species richness with depth are strikingly variable, however (Rex et al. 1997). Grassle and Morse-Porteous (1987) integrate several mechanisms into their theory of a dynamic mosaic of habitats to account for maintenance of deep-sea diversity. They suggest that patchy organic inputs in a low-productivity environment, small-scale disturbances in an otherwise constant environment, and the lack of barriers to dispersal in the vast deep sea allow large numbers of species to avoid extinction despite low abundances. The view that is evolving from current deep-sea research is that the contemporaneous deep sea is a dynamic environment on temporal scales relevant to organisms living there. Historically, on time scales of thousands of years, the deep sea has also been dynamic, undergoing periods of lesser and greater flux of organic material related to changes in the tilt of the earth, glacial-interglacial periods, and the waxing and waning of surface primary productivity. On this larger temporal scale, benthic diversity may be coupled to surface productivity, with diversity 3-4 times as high during periods of high productivity than during periods of low productivity (Cronin and Raymo 1997). 1.4 BIOGEOGRAPHY AND POPULATION GENETICS During the 1800s, the general biogeographic pattern discerned in the deep sea was one of cosmopolitan faunas undifferentiated between ocean basins. This was a pattern that mirrored the prevailing view of a constant, globally undifferentiated environment. In the 1960s and 1970s, Russian investigators undertook extensive global ocean sampling programs (e.g., Vinogradova 1979). Combined with other expeditionary data, including those of the British Galathea expedition of the 1950s, deep-sea species lists suggest coarse, basin-scale variations in species composition (fig. 1.6), but at the generic level, there is little basin-to-basin difference. Depth seems less of a barrier to species dispersal than mere distance, except where shallow sills prohibit free exchange of deep-water masses, as in the Arctic Ocean and Mediterranean Sea (Ekman 1953). Some accounts of distinct, endemic species in deep

12

CHAPTER 1

Figure 1.6. Major zoogeographic divisions of the deep sea. I: Indo-Pacific; II: Atlantic; III: Antarctic; IV: Arctic; shaded areas within these regions represent subdivisions. Elongate regions in western and southeastern Pacific represent distinctive trench faunas. From Vinogradova 1979. trenches conflict with opinions that trench fauna are differentiated mostly at the subspecies level (Gage and Tyler 1991). Submarine canyons that cut through continental shelves may also support distinctive faunas (Rowe 1971). As deep-ocean exploration continues, it seems likely that the current models of deep-sea biogeography will undergo further revision. In terrestrial ecosystems, limited dispersal capabilities, physical barriers (e.g., oceans, rivers, mountains, etc.), and habitat patchiness act as filters to dispersal, resulting in isolation of populations and genetic differentiation of species. Are there barriers to dispersal in the deep sea? In one of the few studies done to date, France (1994) hypothesized that topographic features may act as barriers to dispersal in the deep sea and tested his hypothesis in populations of the benthic amphipod Abyssorchomene spp. from six basins in the Southern California Continental Borderlands region. Abyssorchomene spp. proved to be panmictic in five shallow basins (sill depth 982-1372 m), while a second species, significantly genetically differentiated from the first, occupied the deeper, sixth basin (sill depth 1816 m). It was not possible from this set of observations to determine

THE NON-VENT DEEP SEA

13

whether hydrography associated with the basin topography or environmental parameters associated with bathymetric intervals affects the isolation of the two Abyssorchomene populations. Rather than expecting to recognize barriers to dispersal in the vastness of the deep sea, it may prove more expeditious to study geographic patterns in genetic divergence among broadly distributed populations and then use these data to infer locations and types of significant "invisible" barriers. Such a strategy evolved in a study of mitochondrial 16S rRNA sequences in a panoceanic, deep-sea amphipod species (Eurythenes gryllus; France and Kocher 1996). Sequence divergences indicate a genetic barrier associated with a specific bathymetric interval, wherein deep-water (> 3500 m) populations are differentiated from shallower (< 3200 m) populations. A similar depth-related isolation of E. gryllus was observed in a shallow (1440 m) seamount population compared to deeper-dwelling (5100-5900 m) populations at the base of the seamount and elsewhere in the Pacific (Bucklin et al. 1987). Mechanisms to account for these apparent bathymetric isolations are not yet identified. Alternative hypotheses include pressure or temperature-related biochemical adaptations and hydrographically controlled and restricted dispersal. 1.5 BIOCHEMICAL AND PHYSIOLOGICAL ADAPTATIONS TO THE DEEP-SEA ENVIRONMENT Animals living in the deep sea, whether at hydrothermal vents or abyssal plains, must adapt to conditions particular to their environment. The two most obvious extreme physical conditions at depth are low temperature and high pressure. Both of these conditions influence the biochemistry of living cells. A brief overview of their effects on membrane structure and enzyme function serves here to illustrate general principles of biochemical adaptations in deep-sea organisms. Hochachka and Somero (1984) and Somero (1992) provide more thorough reviews of these adaptations. Both increasing pressure and decreasing temperature favor tighter packing of molecules in the lipid bilayer of membranes. Tighter packing alters membrane fluidity and, potentially, the activity of enzymes incorporated in the membranes. In simplest terms, the membranes begin to solidify, interfering with the lock-and-key mechanisms of membrane-bound enzymes. Adaptations that preserve some specific state of membrane viscosity or fluidity (homeoviscosity) in response to low temperatures include an increase in the percentage of unsaturated fatty acids (Cossins and Bowler 1990). Unsaturated fatty acids are those that have carbon-to-carbon double bonds, resulting in molecules that are more rigid and less likely to be affected by extremes in temperature or pressure. Homeoviscous adaptation is implicated in control-

14

CHAPTER 1

I I j I


75% of the total volcanism on our planet. Most hydrothermal systems studied by biologists so far (fig. 2.1) are located either in the eastern Pacific (on the East Pacific Rise and the Juan de Fuca, Gorda, and Explorer Ridges) or the north-central Atlantic (on the northern Mid-Atlantic Ridge), a circumstance driven by the expense and logistics of mounting expeditions remote from the countries primarily involved in vent biological research. Because vent ecology and geology vary between the two ocean basins, and even within a basin, geographical relationships of vent sites are useful to keep in mind. Table 2.A (see chapter 2 appendix) summarizes general characteristics of the sites where most of the biological research at mid-ocean ridges has taken place to date. Geological settings of vent sites are important on a variety of scales. For example, global variations in ridge crest dynamics—the rate at which new crust is formed, the amount of tectonic activity, etc.—influence the spatial and temporal scales of venting and the biogeography of vent faunas. Regional scales of ridge crest morphology—the depth of the axial valley, the presence of sills and basins, etc.—affect bottom currents and the dispersal potential of larval stages of vent invertebrates. Local patterns of faulting and fissuring influence the style of venting and the longevity and distribution of low-temperature fluid outlets. This chapter brings forward some of the geological concepts and observations useful in developing an understanding of hydrothermal systems.

2.1 WHAT ARE MID-OCEAN RIDGES? Mid-ocean ridges are surficial expressions of planetary-scale processes of ocean crust formation, plate separation, and global heat loss. As the name implies, mid-ocean ridges are mountain ranges: linear oceanic features with

26

CHAPTER 2

Figure 2.1. Major hydrothermal vent sites mentioned in this text: Mid-Atlantic Ridge East Pacific Rise 12. Guaymas Basin 1. Lucky Strike, Menez Gwen 13. 21°N 2. Broken Spur 3. TAG 14. 13°N (Venture Hydrothermal Field), 9°N 4. Snake Pit 15. Southern East Pacific Rise (17°S) 5. Logatchev Galapagos Spreading Center 16. Rose Garden Northeast Pacific 6. Explorer Ridge 7. Middle Valley Western Pacific (Back-Arc Basins) 8. Endeavour 17. Okinawa 9. CoAxial 18. Mariana 10. Axial Seamount 19. Manus 11. Gorda Ridge 20. Fiji 21. Lau

high relief. Girdling the globe like seams on a baseball, they total more than 75,000 km. Mid-ocean ridges are located at the boundaries between the tectonic plates that make up the Earth's crust, and they are the locus of incremental seafloor spreading (hence, they are also known as spreading centers). As plates are pulled apart by distant tectonic forces, hot, soft rock from deep in the Earth rises to fill the gap between them. As it rises, the soft rock

27

SETTING OF HYDROTHERMAL VENTS 400,000

300,000

200,000

Estimated I CrustalAge

(

100,000

Axial Spreading Center 3500«

30

25

20

15

10

5

0

5

Kilometers West of Spreading Axis

Figure 2.2. Gradient of sediment thickness and seafloor depth along a 35 km western traverse from the ridge axis (right-hand side). The eastern traverse from the same point is a mirror image. Depth of sediment increases on older seafloor as a result of accumulation over time. From Lonsdale 1977. partially melts, feeding volcanoes that construct the ocean crust. This zone of crustal accretion is narrow, only a few kilometers wide at most, with an axial valley or trough that marks the spreading axis. Except in a few localized areas of extremely rapid sedimentation, the neovolcanic zone of a ridge axis—the zone where zero-age (newly erupted) basaltic lava is emplaced—is devoid of sediment cover. As ocean crust is generated and moved laterally away from the ridge axis, the age of the crust and the depth of the sediment cover increase systematically (fig. 2.2). Observing from a submersible during a transit away from the trend of the ridge axis in either direction, one initially views a hard rock bottom composed of fresh, glassy basalt lava. Within a few tens to hundreds of meters, the basalt is weathered and a dusting of sediment is apparent, especially in pockets between lobes of the lava. Continue to move off-axis, and the sediment layer increases until the shapes of the underlying lavas become indistinct. Usually within a few kilometers of the ridge axis, the lavas are completely buried by sediment except where exposed by tectonic fissures or faults. On the East Pacific Rise at 3°S, sediment on wide, level surfaces thickens at a rate of about 1 m every 3.25 km. For a half-spreading rate of 76 mm yr~ l (the rate at which one plate moves away from the spreading axis), this sediment thickness corresponds to a deposition rate of about 22 m per million years (Lonsdale 1977). Deposition rates in the open ocean range from 1 to 50 m per million years.

28

CHAPTER 2

T0

Figure 2.3. Magnetic anomalies. At time To, basaltic lava is extruded onto the ridge crest, where it takes on the prevailing magnetic polarity (black); at Tu a magnetic reversal occurs and subsequent ocean crust takes on this new polarity. As the plates continue to move apart, bands of positive and negative polarities move outward. The spreading rate is determined by measuring the distance from the ridge axis for a band of known age. From Nicolas 1995.

2.1.1 How Spreading Rates for Ridge Axes Are Determined As lava emplaced at spreading centers cools below a critical temperature known as the Curie point, magnetic minerals in the rock take on the prevailing polarity of the Earth's magnetic field. Because the polarity of the Earth's magnetic field reverses at intervals of a few tens of thousands to a few hundred thousand years, the polarity of ocean crust formed along ridge axes also reverses. As the crust moves apart, it retains its magnetic signature, resulting in symmetrical bands of "normal" and "reversed" polarities along transects away from the ridge axis (fig. 2.3). It was the compelling symmetry of magnetic anomalies about ridge axes and the correspondence of the

SETTING OF HYDROTHERMAL VENTS

29

anomaly pattern with the pattern of magnetic reversals that led to general acceptance of plate tectonic theory in the early 1960s (Vine and Matthews 1963). Global maps of these magnetic anomalies are used to measure present and past spreading rates and directions, with narrow bands corresponding to slow-spreading ridge segments and wide bands indicative of fast-spreading centers (plate I; Miiller et al. 1997). This information is useful for biogeographers who wish to understand the vicariant history of ridge crest spreading centers and the influence of paleohistorical factors on distributions of organisms. A second class of much smaller-scale magnetic anomalies is commonly investigated at ridge axes using magnetometers towed close to the ocean floor. These magnetic anomalies are deviations from the magnetic signal expected from a basalt crust and may reflect the presence of subsurface lavas above the Curie point (Tivey and Johnson 1995). Newly erupted lavas are highly magnetized relative to the surrounding older lavas (Tivey and Johnson 1995), with magnetization decaying rapidly at first (by 10% the first year) and then more slowly as weathering and oxidation take place (Johnson and Tivey 1995). Magnetic anomalies may thus be a means of locating subsurface, partially cooled lavas and may be used as measures of recent or possibly imminent volcanic activity. 2.1.2 Spreading Rates The average rate at which the seafloor spreads apart at mid-ocean ridges is not uniform throughout the entire ridge system. Lonsdale (1977), plotting the frequency distribution of full rates of plate separation (the rate at which two plates spread apart from each other) at presently active oceanic spreading centers (fig. 2.4), identified a natural division into slow (10-50 mm yr" 1 ), medium or intermediate (50-90 mm yr" 1 ), and fast (> 90 mm yr" 1 ) variants. Almost 50% of the presently active ridges are slow spreading, including the Mid-Atlantic Ridge. The East Pacific Rise is the only presently active fast to superfast-spreading center. More than 50% of the extant ocean crust, however, was formed at rates of > 90 mm yr" 1 (i.e., at fast-spreading ridges), based on magnetic anomalies (Lonsdale 1977). The cross-sectional morphology of ridge axes typically varies dramatically with spreading rate (fig. 2.5; Macdonald et al. 1991). At a slow-spreading ridge, the paired flanks of the ridge axis are separated by a deep (typically 1-3 km) and wide (5-15 km) rift valley. Extension along slow-spreading centers gives rise to earthquakes, large-scale normal faulting, and development of the deep, median rift valley bounded by a nested series of fault blocks that rise outward to the mountain crests. A shallow (10-50 m), narrow (50-1000 m) linear summit caldera or volcanic, eruptive fissure typically defines the neovolcanic zone of a fast-spreading ridge axis and may be

20 18 16 jg

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20-

10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 Full Spreading Rate (mm yr"1)

Figure 2.4. Histogram showing the distribution of spreading rates of mid-ocean ridges. "Full spreading rate" refers to the rate at which the two plates move apart from each other. From Lonsdale 1977. Slow-Spreading Rate < 40 mm yr 1

TAG 26°04'N

3000-,

38004200-

Fast-Spreading Rate >80 mm yr 1

East Pacific Rise 3°25'S

3000 3400

Axis •

i

5km

Figure 2.5. Comparison of ridge-crest relief between slow-spreading (top) and fastspreading (bottom) ridge systems. Slow-spreading ridge systems characteristically have a very broad, deep axial valley, while fast-spreading ridges have a narrow, shallow axial valley. From Macdonald 1982.

31

SETTING OF HYDROTHERMAL VENTS 2000

-i

2200 2400

-

2600

-

2800

-

£* 3000

-

50 X 105 slow-spreading > 50 X 105 Offset (km)

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Depth anomaly of offset (m) fast spreading 300-600 slow spreading 500-2000

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Order 3

Order 4

overlapping spreading centers

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deviations (devals) and offsets

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30-100 50-300

0-50 70-100

Between-segment breaks in hightemperature venting?

yes

yes

yes

often

Between-segment differences in basalt geochemistry?

yes

yes

usually

30-50%

From Macdonald et al. 1991. Slow spreading = < 60 mm yr" 1

mentation gives the ridge axes the distinctive stepped appearance that can be seen in satellite sea-surface images (plate I; Smith and Sandwell 1997) as well as in conventional bathymetric maps. Where these linear segment boundaries have become locked into a plate, they are called fracture zones and can often be traced as fault scars across entire ocean basins. They define distinctive tectonic units of the ridge axis that persist for millions of years and that undergo independent volcanic evolution (Macdonald et al. 1988). Second-, third-, and fourth-order segmentation with more subtle and less persistent morphological boundaries—such as small overlapping or nonoverlapping offsets in the location or trend of the axis of the most recent volcanism—can further subdivide a first-order ridge segment into discrete units tens to a few hundred km in length (table 2.1; fig. 2.7). These subunits typically vary systematically in overall depth and cross-sectional shape and in the distribution of tectonic and hydrothermal features along the axis

33

SETTING OF HYDROTHERMAL VENTS

A ^

Rivera F Z N / (RFZ)

20

z

Latitude(

\

10

^

^

^

^

Orozco FZ " W (OFZ) I

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12 13 14 15 Latitude °N

16 17 18

B 2500

9

10 11

Long-Wavelength Undulation of Axis Short-Wavelength Undulations of Axis

si 2500 n

_ eg

1

3000

\ 3500

Figure 2.7. Nested scales of ridge segmentation. A. Map view of first-order (transform faults) and second-order segmentation (indicated by circles) of the northern East Pacific Rise. B. Axial depth profile illustrating the undulating bathymetry correlated with first-, second-, third, and fourth-order ridge-crest segmentation. Fourth-order discontinuities are recognized by the geochemistry of basalts rather than morphology. C. Proposed model of magmatic along-strike segmentation for the East Pacific Rise. The numbers refer to first-, second-, and third-order segmentation. The capital letters represent melt events, with enhanced up welling beneath the shallowest portions of the ridge axis. From Macdonald et al. 1988.

34

CHAPTER 2 Axial Depth Profile

Axial Magma Chamber

o.sr

Paths of Hydrothermal Fluid Flow

J km Km 1I

Zones of Recent Dike Injection

0

km

J 20 m/ 20 /lK

High Hii -Temperature/Low -Temperature

vent Areas A Ve

Figure 2.8. Hydrothermal segmentation. Proposed model for along-strike hydrothermal circulation on the East Pacific Rise, where episodes of dike injection (shaded) create thermal gradients that drive convective circulation. From Haymon 1997. (Francheteau and Ballard 1983; Schouten et al. 1985; Macdonald et al. 1988; Haymon et al. 1991). The depth of the ridge axis undulates from lowest to highest orders of segmentation, with along-strike axial lows at the ends of segments and axial highs in the centers of segments (fig. 2.7). Geological segmentation of the mid-ocean ridges influences the spacing of hydrothermal sites and the intervening topography, with vent distribution ultimately controlled by the location, volume, and timing of magma injection (fig. 2.8; Haymon 1997). 2.1.4 Magma Supply and Spreading Rate Few biologists concern themselves with magma chambers, yet the spacing and longevity of hydrothermal-vent habitats are directly related to the character of the underlying magma, so it helps to appreciate what seismologists have learned about ridge-crest magma chambers. Both the forms of segmentation and the seismic structure and tectonic fabric of the crust differ between relatively fast- (> 70 mm yr" 1 ) and slow-spreading (< 70 mm yr" 1 ) ridges. At fast-spreading ridges, plate divergence is accommodated almost entirely by magmatic accretion (Solomon and Toomey 1992). The rich magma budget associated with fast-spreading ridge axes is expressed within

35

SETTING OF HYDROTHERMAL VENTS 3.0

W

-+

approximately 4 km

•

E

Figure 2.9. Seismic signature (two-way acoustic travel times) of the axial magma chamber (AMC) at 14°15'S on the East Pacific Rise (cross-sectional view). From Kent et al. 1994. the ocean crust by a seismically detectable, shallow (1300 to 1600 m), axially discontinuous melt lens (axial magma chamber [AMC]), underlain by a continuous zone of hot crystal/magma mush (fig. 2.9; Detrick et al. 1987; Kent et al. 1994). Within cross-sections of the East Pacific Rise between 9° and 13°N, this melt lens ranges from 500 m to 20 km in width and underlies the axial summit valley. An axial magma chamber is present along 60% of this portion of the East Pacific Rise, with discontinuities near fracture zones and at boundaries of second-order segments. Not surprisingly, the thermal and magmatic segmentation of the fast-spreading ridge axis is coregistered with the tectonic segmentation of the axis (Macdonald and Fox 1988). At the axis of the superfast-spreading Southern East Pacific Rise (13°17°S), the extrusive volcanic layer is also extremely thin above the magma chamber (< 200 m), suggesting that the volume of extrusive lava at the ridge axis does not vary significantly across a 40% difference in spreading rate (Detrick et al. 1993). A narrow (< 1 km) axial magma chamber lies at depths < 1000 m below the seafloor, consistent with a model of inverse correlation between magma chamber depth and spreading rate (Detrick et al. 1993). The axial magma chamber is typically detected beneath inflated (broad and shallow) regions of the superfast-spreading East Pacific Rise and is absent or less commonly observed beneath narrow, deep regions (Mutter et al. 1995). Mutter et al. (1995) show that the magma lens varies regularly

36

CHAPTER 2

in depth and width as ridge morphology (axial depth) changes along the axis, confirming the notion that axial morphology can be used to infer magmatic state. Magmatic activity may be indicated in situations where the magma chamber is broader and shallower than predicted by regional trends. At slow-spreading centers, where there is a thick lithosphere, the ridge crest is significantly cooler than along faster-spreading ridges (Sleep 1975). Instead of extensive magma lenses as detected on fast-spreading centers (Detrick et al. 1990), magma chambers are thought to exist in the crust as spatially and temporally discontinuous bodies (fig. 2.10; Smith and Cann 1993).

2.2 BACK-ARC AND FORE-ARC SPREADING CENTERS Back-arc spreading centers form behind island arcs along active plate margins where thick, old ocean crust is undergoing subduction beneath a continental plate moving in the same direction (fig. 2.11). The sinking oceanic slab pulls on the edge of the overlying plate until it splits open, forming a zone of extension. Where there is sufficient heat, crustal accretion takes place by upwelling of magmas in the extensional zone. This mechanism of oceanic crust formation is thus very different from open-ocean seafloor spreading. Extension of a back-arc spreading center takes place periodically, on a scale of millions of years, rather than continuously as at mid-ocean ridges. Because water from the sinking oceanic slab may be injected into hot mantle, thereby modifying the chemistry of the melt, the geochemistry of back-arc basin spreading center volcanics is heterogeneous, unlike the relatively uniform mid-ocean ridge basalt (Stern et al. 1990). Most common in the western Pacific, back-arc spreading centers are often found in basins isolated by shallow sills. Further, they are distinctive in being discrete, episodic units of crustal generation, unconnected in space and time to spreading centers elsewhere, and are thus of particular biogeographic significance with respect to their hydrothermal faunas (Hessler et al. 1988). Isolated back-arc spreading centers in other oceans include the Scotia (southern Atlantic Ocean) and Andaman (northwest Indian Ocean) Ridges. New Ireland and Woodlark Basins of the western Pacific are situated in fore-arc regions, between arc and trench. Fore-arc settings are normally magmatically "cold," since subducted ocean crust effectively cools the mantle. The New Ireland and Woodlark Spreading Centers are thus exceptional in supporting volcanism. Woodlark Basin results from volcanic and extensional splitting of formerly contiguous continental crusts and is a consequence of changes in plate motions and complex tectonic interactions (Taylor et al. 1995).

37

SETTING OF HYDROTHERMAL VENTS

^ , .

,

-

-

urn

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' / ? i \ , ^

v» r * , . - , '

>

'

'

'

•

-

' , '.

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l

>

/"

•

Figure 2.10. Model of magmatic delivery on the slow-spreading Mid-Atlantic Ridge. A schematic cutaway perspective view illustrating the topography of the axial valley floor and boundary fault and the discrete magma bodies feeding the ridge. From Smith and Cann 1993.

2.3 SEAMOUNTS Hot springs on the seafloor are not restricted to spreading centers along the mid-ocean ridges and island-arc systems. They occur wherever there is sufficient heat and porosity to drive hydrothermal convection; active submarine volcanoes in the centers of plates also host hydrothermal vents. Loihi, a mid-

38

CHAPTER 2

Retreating Continent

Back-Arc Spreading Center _ A r c

Oceanic Lithosphere

tension and up-welling of magma

B

Accretionary Wedge

Advancing Continent

Oceanic Lithosphere

Sinking Slab

Figure 2.11. A. Subduction of a relatively thick, old ocean plate (oceanic lithosphere) beneath a retreating continental crust. In this situation, the subducting oceanic crust pulls on the overlying continental crust, causing tension and generation of an extensional spreading center behind the deformation rim or arc and there is a deep trench. This is the typical subduction setting of western Pacific back-arc basins. Hydrothermal systems are supported at the spreading center. B. When a thin, relatively young oceanic plate subducts beneath an advancing continental crust, an accretionary wedge forms and there is a shallow trench. This is the typical subduction setting in the Atlantic. It does not support hydrothermal systems, but compression of sediments does result in venting of porewater fluids (see chapter 12) From Nicolas 1995. plate hot-spot volcano that will eventually emerge as a new Hawaiian island, is perhaps the best-studied seamount and hydrothermal system (Karl et al. 1988, 1989). Other hydrothermally active seamounts that have been explored include Pito Seamount near the East Pacific Rise at 22°S (Francheteau et al. 1994) and Peep's Seamount in the Bering Sea (Sagalevitch et al. 1992). Remote hydrothermal sites on seamounts have the potential to serve as stepping stones for dispersal of vent taxa and thus, like island-arc-associated systems, they are of particular interest to vent biogeographers and population geneticists.

SETTING OF HYDROTHERMAL VENTS

39

2.4 VOLCANIC AND TECTONIC SEAFLOOR FEATURES 2.4.1 Crustal Structure Recent suggestions of the potential for an extensive "subsurface biosphere" (see chapter 5.2.2) make it imperative that biologists gain some appreciation for crustal structure and properties. Seismologists determine the structure of the ocean crust by studying the velocity of propagation of compressional waves (P-waves, analogous to sound waves in air). Propagation velocities vary systematically with depth in the crust in a layered manner that reflects crustal accretion processes. Except at the neovolcanic zone of zero-age lava along the strike of a spreading center, the upper layer of the seafloor is typically pelagic sediment (the seismologist's Layer 1), which increases in depth along transects away from a ridge axis. Layer 2, exposed along the neovolcanic zone of actively spreading ridge segments, comprises basaltic lavas with high bulk porosity (10-20%) in the top 200-400 m (fig. 2.12; Becker et al. 1989; Vera et al. 1990). The upper part of Layer 2 (Layer 2A) is extrusive lavas, primarily pillow lavas, sheet flows, and breccia (fragmented volcanic debris). Layer 2A, down to a depth where temperatures are < 150°C or so, is the region of the putative subsurface biosphere. Microorganisms are presumed to occupy the cracks and voids that constitute the porosity of the upper lava layers. These extrusive lavas are fed by underlying, planar sheets of much less porous lavas called dikes (Layer 2B). For fast-spreading ridges, Hooft et al. (1996) infer two different modes of lava extrusion—one primarily composed of frequent, low-volume flows erupted within the axial valley and a second composed of more voluminous flows overflowing the axial valley or erupting less frequently off-axis—to account for the thickening of Layer 2A as one moves away from the axis (fig. 2.12 B,C). Layer 3 comprises still less porous gabbro, derived from crystallization of axially located magma chambers. A sharp velocity (seismic) discontinuity (the Mohorovicic or Moho Discontinuity) is observed at the base of Layer 3, marking the boundary between ocean crust and mantle. Although long thought to be of uniform thickness (6-7 km), evidence is accumulating that crustal thickness varies by as much as a factor of two from place to place. 2.4.2 Volcanic and Tectonic Fissures Fissures or cracks in the seafloor are common features of mid-ocean ridge crests. In at least some regions of fast-spreading centers, the widest cracks are associated with the youngest, most hydrothermally active portions of the ridge. These fissures probably lie above dikes that failed to reach the sea-

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2B

B

Figure 2.12. Subsurface crustal structure. A. Estimated crustal porosities and permeabilities. Note that upper volcanic layers (extrusives) are highly porous but subsurface sheeted dikes are not. From Becker et al. 1989. B. {Top) Across-axis seismic section from the southern East Pacific Rise showing the location of the axial magma chamber (AMC) and Layer 2A. Note that Layer 2A thickens on either side of the ridge axis. {Bottom) Line drawing of layer 2A emphasizing the relative thickness of extrusive lavas produced at the ridge axis (constant thickness; dark grey) and off-axis (thin at the axis; light grey). The difference between the on-axis-generated lavas and the total thickness of Layer 2A suggests that there are two modes of lava emplacement as described in the text. From Hooft et al. 1996. C. Diagram of the bimodalflow model of lava emplacement on a fast-spreading ridge system. Frequent low-

SETTING OF HYDROTHERMAL VENTS

41

floor. The thicker the dike, the greater the upward driving pressure and the larger the crack (Rubin and Pollard 1987). Eruptive fissures may also facilitate the flux of vapor-rich hydrothermal fluids through the overlying lavas. Wide, deep fissures are loci for the formation of high-temperature hydrothermal vents. Along the East Pacific Rise, the axial valley of Haymon et al. (1993) is an eruptive fissure (also called an "axial summit caldera") and a locus for a linear array of hydrothermal sites (fig. 2.13). The narrowest cracks of a fast-spreading ridge segment are found in highest density in older seafloor and are interpreted as primarily tectonic rather than volcanic in origin; they are associated with plate stress during crustal extension (Wright et al. 1995). Some tectonic fissures undoubtedly serve as conduits for recharge zones, delivering volumes of ambient seawater to subsurface networks where it can react with hot rock. On the slow-spreading Mid-Atlantic Ridge, cross-cutting ridge-parallel and -oblique fissures and faults are thought to contribute to the location and hydraulic stability of a 200-m-diameter hydrothermal mound known as TAG (Trans-Atlantic Geotraverse) by providing permeable pathways through fault breccias (Kleinrock and Humphris 1996). 2.4.3 Lava Lakes, Drainback Features, and Lava Pillars In places where an eruptive fissure or volcanic vent feeds lava into a depression at high effusion rates and low viscosity, lava lakes may form. The surface skin of the lava lake chills to generate a glass veneer overlying a basalt rind often 2-3 cm thick. As molten lava drains away from the depression, either laterally through lava tubes, or by overflowing the walls of the depression, or by drainback into the source vent or fissure, the solidified roof of the lake is left largely unsupported and collapses into rubble at the floor of the lake. Hollow lava pillars, formed around conduits of cooling water, are typically found along edges of lava lakes. Sides of the lakes and of the pillars are marked by "bathtub rings"—a pseudo-stratigraphy created by chill margins of ponded and draining lavas (fig. 2.13; Fornari and Embley 1995). 2.4.4 Axial Boundary Faults Where the magma budget is high, seafloor spreading is accommodated primarily through dike injection and accretion, and faulting generates relatively

Figure 2.12. (Cont.) volume flows (shown in dark grey) are confined to the axial valley and build up half the volume of the extrusive Layer 2A. Occasional, more voluminous lavas (light grey) flow down the flanks of the ridge crest or erupt outside the axial valley. Accompanying sheeted dikes are shown as vertical bars in white. From Hooft et al. 1996.

42

CHAPTER 2

Figure 2.13. Perspective drawing of the eruptive fissure (axial valley) at 9°N on the East Pacific Rise. The linearfissuredefines the ridge axis and the locus of incremental spreading. Note the "bathtub rings" along the margin of thefissure,lava tubes and other drainback features, and thefissure-controlleddistribution of high-temperature vents along the one wall. From Fornari and Embley 1995 (artist: P. Oberlander, Woods Hole Oceanographic Institution). low en echelon relief (on the order of tens of meters). On slow-spreading ridge systems, magma supply is episodic, with magmatic periods followed by long periods of intense tectonism that result in faults hundreds of meters high. Major faults that bound the median valley of slow-spreading ridges rise in a series of steps, with each step forming on the valley floor and migrating outward and upward "like a slow escalator" (fig. 2.14; McAllister and Cann

43

SETTING OF HYDROTHERMAL VENTS Fault Growth Window' ~2km

Figure 2.14. Model of formation of boundary-wall faults on the Mid-Atlantic Ridge. A fault is initiated on the axial valley floor by strain associated with outward spreading of the crust and coalescence of fault segments. Faults propagate downward through the cooling and thickening lithosphere as they move outward. From McAllister and Cann 1996. 1996). Such major faults may be important in hydrothermal circulation as conduits for transport of water into the crust. 2.4.5 Lava Flow Morphologies Solidified lavas that pave the neovolcanic zone of mid-ocean ridges can be visually categorized by their shape and texture. According to Gregg and Fink (1995), jumbled, folded, sheet, and pillow lava forms (fig. 2.15) may be diagnostic of specific volumetric effusion rates (flow rates, usually expressed as m3 s" 1 ). A single eruption can result in a lineated sheetlike flow near the volcanic vent where effusion rate is highest, with degradation downstream to lobate flow as local effusion rate declines and the flow spreads outward, and formation of pillows at the flow margins, where effusion rate and slopes are lowest and cooling rates are highest. Identification of these relations and estimation of the physical processes for their formation allow calculation of effusion rates and emplacement times for those submarine lava flows whose morphology can be categorized and whose total volume (determined, for example, by measurable changes in bathymetry), viscosity and eruption temperature (determined geochemically from samples of erupted lavas), and underlying slope can be estimated (Gregg and Fink 1995). 2.4.6 Emplacement of Lavas and the Time-Course of a Diking Event Magma is fed to the upper ocean crust through vertical dikes oriented parallel to the ridge axis during discrete, quantum units of seafloor spreading (Delaney et al. 1998). Not all dikes reach the seafloor or produce lava flows.

44

CHAPTER 2

Figure 2.15. Top: Sheet flow lightly dusted with sediment. Bottom: Pillow basalt. Photos courtesy Woods Hole Oceanographic Institution.

Between 1986 and 1998, ten diking-eruptive events have been inferred or directly observed along various ridge systems (table 2.2; Delaney et al. 1998). Much of what we know about the time-course of a dike injection of lava along a mid-ocean ridge comes from acoustic signals and visual

SETTING OF HYDROTHERMAL VENTS

45

TABLE 2.2. Recent observed or inferred diking or eruptive events Site

Year

Axial Seamount Loihi Seamount North Gorda Ridge 17°S, East Pacific Rise CoAxial Segment, Juan de Fuca Ridge 9°N, East Pacific Rise Iceland MacDonald Seamount, SE Pacific Cleft Segment, Juan de Fuca Ridge 17°S East Pacific Rise

1998 1998 1996 1993 1993 1991 1990 1988 1986 1983, 1984

From Delaney et al. 1998.

ground-truthing of the 1993 CoAxial eruption on the Juan de Fuca Ridge. A network of acoustic hydrophones deployed in the northeast Pacific for military use routinely monitors sound over frequencies that are generated during volcanic events (see chapter 10.4.2). Five million cubic meters of lava are estimated to have been emplaced within two hours during the CoAxial event (Gregg and Fink 1995) from a dike on the order of 3 to 5 m wide (Cherkaoui et al. 1997). Eruptions may be longer lived on slow-spreading centers (Gregg 1995). Thermal and mechanical modeling suggests that 3-6 million m3 of lava was emplaced during the April 1991 eruption at 9°N on the East Pacific Rise (Haymon et al. 1993) within 30 min, a rate of emplacement comparable to that observed in Hawaii at Kilauea Volcano's East Rift Zone (Gregg et al. 1996). The faster delivery rate at 9°N is attributed to the lower viscosity of lavas there compared to the CoAxial lavas. Lava was delivered through a primary eruptive fissure system that was nearly continuous over a distance of - 8 . 5 km within the 9°N axial valley (fig. 2.16). 2.4.7 Lava Dating Until recently, geologists could only guess at relative ages of young midocean ridge basalts based on degree of weathering, freshness of the glass, abundance of buds on surfaces of pillows (sloughed off as lavas age), and amount of sediment cover. New geochemical techniques allow geologists to constrain the age of very young basalts (up to 3 yr) to within a few months using the radioactive disequilibrium between 210Po and 210 Pb. The technique relies on the significant volatilization (75-100%) of Po, but not Pb, during an eruption. The age of a lava flow is calculated by monitoring the rate of return to radioactive equilibrium between these two nuclides following the

46

CHAPTER 2

t=0

t = +10min

Lava ' Pillars >

Fresh Basalt Volume {after drainbaek and collapse)

= + 100h

Figure 2.16. Time course of the 1991 eruption at 9°50'N on the East Pacific Rise. Pre-emption: The axial valley before the eruption, t = 0: At the onset of the eruption, magma intrudes the primary fissure, t — +10 min: Lava begins to fill the valley, t = + 30 min: Maximum depth attained in 1-2 h ( = lava pond), t = +100 h: As eruptive activity wanes, part of the lava drains laterally out of the valley or back into the primary fissure. From Gregg et al. 1996.

47

SETTING OF HYDROTHERMAL VENTS

0

50

100 Age (Ma)

Figure 2.17. The crustal heat deficit. Measured values of heat flux from the ocean crust (circles) fall below expected values based on conductive heat loss alone (solid line). Convective hydrothermal heat loss at the ridge axis (i.e., hydrothermal venting) accounts for the deficit. From Alt 1995 (originally from Stein and Stein 1994). eruption (Rubin et al. 1994). A series of other radioactive disequilibria allows lavas to be aged over time scales of 2 to > 10,000 yr (Rubin et al. 1989). On fast-spreading centers, where volcanism is frequent and closely linked to hydrothermal activity, the capability of dating host basalts should permit determination of the maximum likely age of extant hydrothermal fields. 2.5 DEEP-SEA HYDROTHERMAL FIELDS 2.5.1 Missing Heat and Hydrothermal Cooling at Ridge Crests Among the several clues that suggested to geologists that there must be hydrothermal circulation on the seafloor was the poor fit of measurements of heat flow from young ocean crust (< 50-70 Ma) to thermal models of cooling of the lithosphere in which upward heat transfer takes place only by conduction through rock. Heat flow is typically measured by inserting a vertical array of temperature probes into sediment along transects away from a ridge crest, that is, into increasingly older sediments. These thermal gradient data are scaled with a measured or inferred thermal conductivity to estimate the heat flow. The seafloor has a heat deficit that can be mapped along lines perpendicular to the ridge crest out to about 65 ± 10 Ma (fig. 2.17; Stein et al. 1995). This heat deficit, or excess cooling, is attributed to hydrothermal circulation. In

48

CHAPTER 2

"Active" Axial

"Passive" Off-Axis

Heat source

Figure 2.18. Model of convective regimes in the ocean crust. High-temperature, axial circulation is driven by a magmatic or hot rock source; lower-temperature off-axis circulation is driven by passive cooling. From Alt 1995 (originally from Lister 1982). other words, the missing heat is convective heat driven by cells of seawater percolating into the crust and subsequent heating and buoyancy-driven flux out of the crust, which generate hot springs on the seafloor (fig. 2.18). In older seafloor (> 65 Ma), observed and predicted heat flow coincide, indicating that convection in these regions is no longer important. Although initially thought to be sealed or "capped" by thick, hydraulically nonconductive sediments, increasing evidence suggests that the porosity and permeability of aging crustal rock decrease to a point where the rock becomes sealed by hydrothermal deposition of minerals (Stein et al. 1995). Thus, the primary process that blocks hydrothermal circulation in aging crust is mineralization, with at best secondary influences from increasing sediment thickness. While hydrothermal circulation at the ridge crest is inferred to account for some of the missing heat (about 30%), approximately 70% of the hydrothermal heat flux is off-axis, that is, in seafloor > 1 million years. Heat flow measurements taken systematically along off-axis transects map out the presence of large convection cells, on the order of 10-15 km in width (fig. 2.18). The biological significance of the large volume of low-temperature hydrothermal fluid off-axis is largely unexplored (but see chapter 3.7). 2.5.2 Sulfide Deposits Morphological Variations Different styles of mineralization and evolution of massive sulfide deposits are found at seafloor hydrothermal vents, ranging from subseafloor deposi-

SETTING OF HYDROTHERMAL VENTS

49

tion within conduits to simple columnar chimneys, to larger, complex structures, to ore bodies that are equal in size to commercially important deposits on land. In its geological context, "massive sulfides" refers not to the volume of a sulfide deposit, but to material made up entirely of sulfide minerals. Thus a very small black smoker chimney can be a massive sulfide deposit. The simplest of sulfide structures is the columnar chimney typical of hydrothermal vents on the East Pacific Rise (plate II, top left panel). As described by Haymon et al. (1993), these chimneys can form early in the evolution of a hydrothermal site, in the aftermath of a volcanic eruption. Observations of 400°C fluids pouring directly from cracks and crevices in bare basalt or through small, newly forming chimneys were made within days to weeks of the eruption. Within a year, high-temperature fluids were focused through "mature" sulfide chimneys (5 m and more in height) at the same location. Formation of a simple black-smoker chimney begins as metal- (e.g., iron, copper, and zinc) and sulfide-rich, high-temperature, acidic fluids mix with the surrounding cold, alkaline seawater, causing the metal sulfides to precipitate and form particle-rich "black-smoker" plumes. The first stage of chimney growth is precipitation of a friable, porous anhydrite (calcium sulfate, CaSO4) sheath or tube around the exiting fluids (fig. 2.19; Tivey 1995). Anhydrite precipitates from seawater when it is heated above 150°C. Development of anhydrite deposits can be extremely rapid, with vertical growth rates of as much as 30 cm in one day (Goldfarb et al. 1983). The anhydrite walls insulate and isolate hydrothermal fluids from the surrounding seawater, resulting in high-temperature deposition of an inner zone of chalcopyrite (CaFeS2). Horizontal flux of fluids across the chimney walls continues at this stage until the pore spaces are filled with anhydrite and other copper-iron sulfide minerals (Hannington et al. 1995). Some black-smoker chimney mineral assemblages include an abundance of zinc sulfides. As the outer anhydrite walls cool to temperatures below 150°C, the anhydrite starts to dissolve back into seawater again. Most mature chimneys have tortuous plumbing and complex mineralogies with zones of horizontal porosity and diffuse warm-water flow at temperatures and fluxes suitable for exploitation by organisms (figs. 2.20A, 2.21). Columnar chimneys grow to heights of 10-20 m, often with multiple high-temperature orifices at the top. Tall, active chimneys unfortified by secondary siliceous (SiO2), barite (BaSO4), or calcite (CaCO3) deposits are fragile and can be knocked over by slight jarring with a submersible or by minor earthquake tremors. Chimney orifices can be sealed through mineralization but made to flow again by breaking off a piece of the chimney.

COLUMNAR CHIMNEYS AND BLACK SMOKERS.

50

CHAPTER 2

B

Anhydrite Matrix* Copper-Iron Suifides Magnesium Silicates and Suifides Sulfide Weathering Assemblage *With Fine-Grained Zinc, Iron, and Iron-Copper Suifides

Figure 2.19. Schematic vertical and horizontal sections through (A) the early stage of chimney growth (anhydrite-dominated stage) and (B) a more mature chimney, where anhydrite walls prevent mixing with seawater in the chimney, leading to precipitation of copper and iron suifides. The walls of a chimney may be porous, allowing for both lateral influx of cold ambient seawater, as indicated by the arrow, and leakage of vent fluids. From Tivey 1995. White smokers are those chimneys from which fluids at intermediate temperatures (100-300°C) are emitted. At these lower temperatures, silica, anhydrite, and barite (BaSO4) precipitate as white particles (Hannington et al. 1995). The white-smoker fluids either are not hot enough to carry high enough concentrations of metals and sulfide to produce "black smoke" on mixing with ambient seawater, or if the fluids were hot at depth, they have been conductively cooled or mixed with ambient seawater below the surface so as to have deposited their metals at depth (Tivey et al. 1995).

WHITE SMOKERS.

While the simplest black-smoker chimney structure is a simple tube with exit of fluids through an apical orifice or orifice com-

BEEHIVES AND FLANGES.

SETTING OF HYDROTHERMAL VENTS

51

A

Figure 2.20. Comparative morphology of typical sulfide structures. A. Typical East Pacific Rise columnar chimney (as in figure 2.19). B. Beehive structure showing horizontal layering and conduits for diffuse 350°C fluid flow. C. Flange structure with pooled 350°C fluids trapped beneath the sulfide shelf. D. Complex smoker with multiple 350°C chimneys and internal circulation, typical of sulfide mounds at the Endeavour hydrothermal fields on the Juan de Fuca Ridge. From Alt 1995 (after Haymon 1983; Tivey and Delaney 1986; Delaney et al. 1992; Fouquet et al. 1993).

52

CHAPTER 2

Silica-Suifate Walls Porous, Massive Sulfides Massive Barite and Fossil Worm Tubes Mineral-Lined Cavities

Figure 2.21. Cross-section of a chimney illustrating the presence of porous sulfides and the absence of a central conduit. From Hannington and Scott 1988. plex, two other exit morphologies are common at some hydrothermal fields. Bulbous beehive or wasp-nest-like structures occur as outgrowths on the sides or tops of sulfide chimneys (fig. 2.20B) at a variety of hydrothermal fields, including the type locality at Beehive (Snake Pit, 23°N on the MidAtlantic Ridge). They are extremely porous and often very friable structures through which high-temperature fluids (as high as 300°C or more) diffuse. Sulfides precipitated within beehives are layered, resulting in a distinctive concentrically ribbed or shingled outer surface (Fouquet et al. 1993). Because of their high surface temperatures, they are typically bare of organisms, and thus their surfaces are often in conspicuous contrast to the animalor bacteria-covered surfaces of sulfide chimneys on which they occur (plate III, middle row, right panel).

SETTING OF HYDROTHERMAL VENTS

53

Flanges are accretionary sulfide structures that are lateral outgrowths from the supporting sulfide mound, where 350°C fluid escapes from fractures (figs. 2.20C, 2.22; plate II, top row, middle panel; Lonsdale and Becker 1985; Lisitsyn et al. 1989; Delaney et al. 1992). They are especially common at the Endeavour Field on the Juan de Fuca Ridge and at Guaymas Basin vents in the Gulf of California. Flanges can be quite large, projecting outward as much as a meter or more, and several centimeters thick. The undersurface of a flange traps pools of buoyant, high-temperature (near 350°C) fluids, resulting in temperature gradients of 200-300°C across the thickness of the flange. Residence time of hydro thermal fluids under a flange is short, on the order of 100 s, and it is this short time scale that ensures high temperatures of the ponded fluid under simultaneous conditions of high convective heat transfer (Kerr 1997). Thermal gradients are even more extreme across the thin (millimeters) reflective interface between pooled vent fluids and ambient seawater. Upper surfaces of flanges, where there is diffuse flow of 10-80°C fluids that have percolated through the flange matrix, often support dense invertebrate and microbial populations. Columnar chimneys are most characteristic of fast-spreading centers, where the pace of volcanic eruptions and consequent alteration of subsurface and surface plumbing systems to a large extent disallows development of extensive deposits with complex mineralogical features. At the Endeavour hydrothermal field on the intermediate-spreading Juan de Fuca Ridge, free-standing sulfide mounds 10-30 m in diameter and up to 40 m or more in height (figs. 2.20, 2.22) are distributed along a major fissure that runs subparallel to the ridge axis. Multiple short, apical and lateral black-smoker chimneys project from the mounds, as do horizontal flanges. Stability is conferred to the structure by silicification of the mineral assemblage (Tivey and Delaney 1986). Each sulfide mound at Endeavour appears to overlie and be dimensionally constrained by pipelike subsurface conduits or stockworks (Hannington et al. 1995). In contrast, large-diameter (up to 200 m), low-relief mounds (—50 m) characteristic of TAG on the Mid-Atlantic Ridge and the fossil sulfide deposits of the Galapagos Spreading Center appear to overlie a more diffuse, branching stockwork system consisting of a network of fine fractures and veins (fig. 2.23). The mounds themselves probably originated as multiple individual structures that eventually coalesced to form a single larger mound with multiple high-temperature orifices (Hannington et al. 1995; Humphris et al. 1995). Collapsed chimneys and sulfide debris can contribute to the coalescing mound structure. Shallow hydrothermal recirculation may occur within large mounds, producing high-temperature fluids substantially modCOMPLEX SULFIDE MOUNDS.

54

CHAPTER 2

Figure 2.22. "Godzilla," a 45-m-high sulfide mound with flanges on the Juan de Fuca Ridge. The submersible Alvin is drawn to scale. From Robigou et al. 1993.

55

SETTING OF HYDROTHERMAL VENTS

A

350C

Sedtmerrt

Broad Alteration Zone Branching Stockwork

B

380-400C

Tall, Free-Standing Suifide Structure

/

\

Bare Basalt

Narrow Alteration Zon# Relatively Unbraoclied Stoclwork

20 m

Figure 2.23. The role of subseafloor permeabilities in controlling styles of venting. A. TAG-type mound of large diameter, underlain by an extensive subsurface stockwork. B. Endeavour-type mound with high relief and limited subsurface stockwork. From Hannington et al. 1995.

56

CHAPTER 2

ified from the pure, "end-member" fluid composition arising directly from high-temperature reactions at depth. Much of the heat and fluid flux from a large mound is emitted as diffuse flow at temperatures low enough to permit colonization by organisms. Schultz et al. (1992) show, for example, that the heat flux from diffuse flow may exceed that from high-temperature focused flow by a factor of 5 at a large sulfide mound in Endeavour Field (Juan de Fuca Ridge). Large gradients of temperature and chemistry within such mounds must accommodate mineralogical and microbiological zonations that have yet to be explored in detail. When hot fluids ultimately cease to flow through a black-smoker chimney, the metal sulfides slowly begin to oxidize, turning to iron oxyhydroxides, and the chimney matrix becomes soft and unstable. Dense hydrothermal vent communities on the chimneys die off and are often replaced by a few suspension-feeding brisingid sea stars or sponges, which take advantage of the richer supply of food delivered on currents modified by the local topographic relief. In a process similar to acid mine drainage, reaction of cold oxygenated seawater with exposed sulfides produces highly acidic pore fluids. Facilitated by iron-oxidizing bacteria, pore fluids mobilize metals to the outer surfaces of deposits, where they precipitate as oxide-rich crusts (Juniper and Fouquet 1988; Hannington et al. 1995). Mass-wasting, erosion, and re-sedimentation of iron oxides produces metalliferous sediments that deposit as debris-flow aprons at the base of large mounds.

WEATHERING OF SEAFLOOR SULFIDES.

Dimensions and Ages of Active Hydrothermal Fields Hydrothermal-vent fields, comprised of multiple zones of focused hot and diffuse outflows, are the basic unit of hydrothermal activity on ridge axes. Individual vent fields range in size from several hundred to several million square meters (Seyfried and Mottl 1995). Biological sites commonly visited by submersibles over the past decade or so range in size from tiny pockets no larger than a typical living room, to the size of baseball diamonds, or even as large as a football field or two. Many of these biological sites might be strung together to form a hydrothermal field (fig. 2.24) Large contrasts in the style and distribution of vents within a hydrothermal field are emphasized by geological maps of, for example, the Venture Hydrothermal Field at 9°50'N on the East Pacific Rise (fig. 2.25; Haymon et al. 1991), the Main Endeavour Field on the Juan de Fuca Ridge (fig. 2.26; Delaney et al. 1992), and the TAG Hydrothermal Field on the Mid-Atlantic Ridge (fig. 2.27; Kleinrock et al. 1996). At the Venture Hydrothermal Field,

57

SETTING OF HYDROTHERMAL VENTS North Wall

0°48'

T3

0°47'

South Wall

86°10

86°09'

86°08'

86°07'

Longitude (W)

Figure 2.24. The low-temperature hydrothermal field on the Galapagos Spreading Center, illustrating the linear, east-west distribution of vent sites (stars) within the axial valley. Rose Garden is to the west at 00° 48.2'N, 86°13.5'W. From Crane and Ballard 1980. black-smoker chimneys are scattered in a linear fashion along the walls of the narrow axial valley (the eruptive fissure). This kind of narrow, linearly arranged hydrothermal field is characteristic of the East Pacific Rise in general. Intermediate-sized sulfide mounds in the Main Endeavour Field are closely controlled by a major ridge-parallel fault near the western wall of the axial valley or summit graben. The active and relict TAG sulfide mounds, up to 200 m in diameter, comprise the largest seafloor sulfide deposits so far known. Unlike all other known hydrothermal systems on the mid-ocean ridge, TAG is removed from the neovolcanic zone perhaps by as much as several kilometers. There are also large contrasts among vent fields in the duration of hydrothermal activity, depending on the geological setting. On fast-spreading ridge segments, cycles of volcanism can be frequent enough to limit the life of an individual chimney or diffuse-flow area to a couple of decades or less, although the duration of hydrothermal activity within a field may be much longer. Where volcanism is less frequent, sulfide edifices can reach much greater ages. Radiometric dating of active mounds in the Main Endeavour Field suggests ages of more than 200 yr in some cases (Kim and McMurtry 1991). The TAG mound on the slow-spreading Mid-Atlantic Ridge has been intermittently active for the past 40,000 to 50,000 yr (Lalou et al. 1993).

58

CHAPTER 2

1991 Eruption Area

9°10'

9°00'

Figure 2.25. Distribution of hydrothermal features at the 9°50'N (Venture) hydrothermal fields, East Pacific Rise, emphasizing their linear and extensive nature. Filled circles in boxes indicate latitudes of active black smokers in 1989. From Haymon et al. 1991, 1993.

2.5.3 Low-Temperature Diffuse Flows It is the diffuse, warm-water flows that sustain productive populations of thermophilic microorganisms (up to 115°C) and dense invertebrate communities (sometimes up to 60°C, though usually < 40°C) at deep-sea hydro-

SETTING OF HYDROTHERMAL VENTS

59

Talus Slope

Figure 2.26. Clusters of sulflde mounds at the Main Endeavour Field, Juan de Fuca Ridge. From Delaney et al. 1992.

thermal vents. Diffuse flows may issue from porous surfaces of active mineral deposits (black smokers, white smokers, and complex sulflde mounds) or directly from fissures and cracks in basalt lavas. Where diffuse flows occur on ridge axes, they represent high-temperature fluids (~350°C) that have undergone dilution with cold seawater either below the surface or within the matrix of a sulfide structure. Diffuse venting can contribute a substantial proportion of the heat and mass flux in some vent fields—as much as an order of magnitude greater than that of focused high-temperature flows through black smokers (Rona and Trivett 1992; Schultz et al. 1992). Because of their low temperatures, diffuse flows are not responsible for significant deposition of minerals above the seafloor. Mineral precipitates associated with diffuse venting commonly include thin coatings of amorphous iron oxyhydroxides and manganese oxides (Hannington et al. 1995).

60

CHAPTER 2

SCO

Figure 2.27. Sidescan backscatter imagery (left panel) of the TAG active hydrothermal mound. Enlarged views of the TAG mound are shown in the right panels, with locations of primary features noted in the lower right. In contrast to linear and clustered arrays of active vents, TAG is a singular, large sulfide edifice. From Humphris and Kleinrock 1996; Kleinrock and Humphris 1996.

2.5.4 Sediment-Hosted Hydrothermal Systems While the seafloor at most mid-ocean ridges is exposed as bare volcanic rock, a few spreading axes are located in regions of high sediment deposition. Though not well documented, hydrothermally influenced soft sediments represent a biological habitat that likely hosts infaunal organisms unique to the sedimentary regime. "Sediment-hosted" ridge systems fall into two general classes depending on the relative importance of biogenous and terrigenous deposits. The best example of a biologically influenced sedimentary regime is

SETTING OF HYDROTHERMAL VENTS

61

Guaymas Basin in the Gulf of California. The Guaymas spreading axis is an extension of the East Pacific Rise near the junction with the North American plate and is overlain by > 500 m of sediment as a consequence of the rapid deposition rate (1-2 cm per 1000 yr; Lonsdale and Lawver 1980). The terrigenous component of Guaymas sediments is derived predominantly from Mexico. The biogenous component is the result of prolific diatom blooms in the warm nutrient-rich overlying waters, which enhance the sediments with 3-4% total organic carbon (Goldhaber and Kaplan 1974). Volcanic intrusions into the sediment emplace basaltic sills, which thermally alter the sediment and pore-fluid chemistry (Einsele et al. 1980). High-temperature, convective hydrothermal systems that pass through Guaymas sediments can carry large amounts of petroleum derived from thermal alteration of the organic components (Simoneit and Lonsdale 1982). Sediment, mineral, fluid, and biological samples collected from Guaymas vents are redolent with these naturally refined petroleum products. The hydrothermal circulation path through sediments also leads to subsurface precipitation of metal-sulfide minerals and low metal concentrations in high-temperature vent effluents and seafloor mineral chimneys (Von Damm et al. 1985; Lisitsyn et al. 1989). Sedimentation rates are also high at Middle Valley (a buried mid-ocean ridge segment on the northern Juan de Fuca Ridge) and in the Escanaba Trough of Gorda Ridge. Biogenous contributions to these off-shore ridge systems (and hence petroleum generation) are lower than in Guaymas Basin, but terrigenous inputs from the North American continental margin are high. Middle Valley is located where the Juan de Fuca Ridge makes its closest approach to the continent at Vancouver Island. Sediments deposited in the Escanaba Trough are funneled through a gap between the southern end of the ridge and the Mendocino Fracture Zone, with most of the sediment probably having been deposited during a period of low sea level in the Pleistocene (Moore 1970; Vallier et al. 1973). 2.5.5 Ophiolites Slices of crust formed on the ocean floor may be transported onto land and preserved there. Known as ophiolite complexes, these oceanic slabs can be recognized by their layered structure that progresses vertically downward from oceanic sediments to submarine lavas to sheeted dikes to gabbro to peridotite from the upper mantle. Ophiolites thus expose the full structure of the ocean crust. Where hydrothermal systems have been preserved in ophiolites, they reveal the scale and mien of subsurface hydrothermal plumbing and rock alteration by high-temperature fluids, and they yield fossil hydrothermal vent organisms (see chapter 9). The deep structure of hydrothermal systems can best be seen in the Troodos ophiolite in Cyprus (see Robertson and Xenophontos 1993 for an overview). More than 30 extinct,

62

CHAPTER 2

high-temperature sulfide deposits in the Troodos have been mined for copper and sulfur at various times, ranging from the Bronze Age to the 1960s. Most of these sulfide deposits are sandwiched between lavas, indicating that they were formed close enough to the ancient spreading axis to be overrun by flows, long before they became uplifted onto land. Under the sulfides at Troodos, hydrothermal-upflow zones are evident as areas of highly altered lavas. Tracing the path of fluid motion through vertical sheets of dikes, the "reaction zone" where cold seawater was transformed to high-temperature hydrothermal fluids by reaction with hot rock can be seen lying close to gabbros (crystallized magma chamber).

APPENDIX TABLE 2.A. Characteristics of major hydrothermal sites Site

Depth (m)

Location

Atlantic (slow-spreading ridge system) Lucky Strike 1700 37°17.5'N, 32°16'W

Geological Notes

Biological Notes

Multiple sulfide edifices are located along the margins of a lava lake at the summit of the Lucky Strike Seamount. Includes "Eiffel Tower," "Sintra," "Statue of Liberty," and "Isabel." The Lucky Strike sulfide deposits are reported to cover the greatest areal extent of any deposits discovered so far.

Dominated by an undescribed species of mussel that colonizes sulfides. Together with Menez Gwen (37°50'N; 850 m), Lucky Strike belongs to a biogeographic province distinct from that of TAG, Broken Spur, and the Logatchev site to the south. Clams are absent and, as at all Mid-Atlantic Ridge sites explored to date, there are no tube worms. Dominated by the swarming shrimp, Rimicaris exoculata. Several confamilial shrimp species co-occur with R. exoculata, albeit in far fewer numbers, as do brachyuran crabs, making this site uniquely decapodan compared to all other known vent fields. Anemones dominate the peripheral field. The fauna is similar to that of TAG, but with the presence of mussels, Bathymodiolus puteoserpentis, at the base of the sulfide mounds.

TAG (TransAtlantic Geotraverse)

3600

26°08'N, 44°49'W

A single large (200 m diameter) sulfide mound with an acentric active blacksmoker complex and lower-temperature periphery. A long-lived site (>20,000 yr) with intermittent hydrothermal activity. Large, inactive sulfide deposits are nearby.

Snake Pit (also known as "MARK")

3600

23°22'N, 44°57'W

Multiple sulfide mounds along an E-W transect, including "Moose" and "Beehive."

TABLE 2.A. (Continued) Site

Depth (m)

Location

Other Atlantic (N-S) Kolbeinsy (N of Iceland) Reykjanes

250-350

63°06'N

Rainbow

2300

36°14'N, 33°54'W

Broken Spur

2200

29°10;N, 43°10'W

Logatchev (also known as

3300

14°45'N

100-106

Geological Notes Shallow sites; boiling.

NE Pacific (intermediate-spreading ridge system) Explorer 1850 49°44-46'N, 130°17'W

Steinaholl site, south of Iceland. Originally noted by fishermen as a productive fishing hole. Gas-rich. One of the most active hydrothermal sites on the Mid-Atlantic Ridge. Multiple sulfide mounds. Includes the "Saracen's Head," "Wasp's Nest," "Spire."

Includes multiple vent sites where fluids lack dissolved sulfide. Mineral sulfide deposits are large (200-250 m maximum dimension).

Biological Notes No endemic species recognized to date. Dominated by sponges and hydroids. Bacterial mat but no macroinvertebrates. Dominated by shrimp {Rimicaris exoculata), with small mussel beds. Not all vents are colonized. Similar to Rainbow, TAG, Snake Pit Mussels and shrimp; similar to Snake Pit, but without high densities of swarming shrimp. Vesicomyid clams are reportedly present, making this site unique among Mid-Atlantic Ridge vents. Hydrothermal sites with mixed biological features: vents where dissolved sulfide was absent supported no biota; other sites were variously dominated by tubeworms (Ridgea piscesae) distinct from those of the East Pacific Rise, polychaetes (including Paralvinella spp.), and small gastropods (especially Lepetodrilus fucensis and Depressigyra globulosus).

Endeavour

2250

47°57'N, 129°05'W

CoAxial Site

2200

46°20'N, 129°40'W

Axial Seamount

1570

45°57'N, 130°02'W

Site of numerous, multidisciplinary geophysical, geochemical, and biological investigations. Sulfide mounds are often large, silicifled. One sulfide structure, "Godzilla," reached 45 m in height before it collapsed. Sulfide flanges with pooled hot water beneath them are common. Several hydrothermal fields have been mapped in the region, including the "Main Endevaour Field," "High Rise," and "Mothra." Location of a well-documented 1993 eruption.

Axial Seamount is a volcanic edifice that sits astride the ridge axis. Hydrothermal vents are located in the caldera of the volcano. A major eruption took place in 1998, reconfiguring the landscape and hydrothermal systems.

Although densities and dominance vary between sites, Endeavour, Explorer, Axial Seamount, CoAxial, and Cleft all share the same basic species list. A biological observatory has been established at the Main Endeavour Field. Observatory studies include characterization of community composition and dynamics, growth, and food webs. The eruption established new hydrothermal activity where no vent in close proximity (100s of meters) had ever been documented. Surprisingly, the first colonists included a large population of nemertean worms previously unknown from NE Pacific vent sites, as well as tubeworms and paralvinellid polychaetes. Part of the same biogeographic province as other NE Pacific vent sites. Preemption faunal characteristics (species composition and distribution) are well known so that changes can be tracked.

TABLE 2.A. (Continued) Site

Depth (m)

Location

Cleft Segment (also known as "Southern Juan de Fuca Ridge")

2250

44°38-41'N, 130°23'W

Gorda Ridge

3250

41°00'N, 127°29'W

East Pacific Rise (fast-spreading ridge system) Guaymas Basin 2000 27°00'N, 111°24'W

Geological Notes

Biological Notes

A 10-30-m-deep, 30-50-m-wide cleft marks the center of the axial valley. Hydrothermal vents lie within this cleft as clusters of large sulfide edifices. Erupted in 1986-1987. Escanaba Trough, along the southern portion of this ridge axis, hosts hydrothermal vents in soft sediments. Sulfide deposits are large and there are numerous inactive sites. These are the only known hydrothermal sites that occur wholly within the U.S. Exclusive Economic Zone. Mineral resources of Gorda Ridge were proposed for lease in 1983, but the proposal was subsequently withdrawn.

Fauna as at other NE Pacific vents, but abundances are relatively low.

In the Gulf of California, a region of rapid deposition of organic-rich sediments. Mineral mounds are thus sediment-hosted and lavas intrude as sills within the sediment. High concentrations of natural petroleum products arise from cracking of organic material in mineral sulfides and in sediments. Pagoda-like flange structures are typical at this site.

Dominated by giant tubeworms (Riftia pachyptila), with abundant scale worms and paralvinellid polychaetes. Sediment allows for development of an infaunal community which includes bivalves (e.g., Calyptogena spp., Nuculana sp.) and polychaetes. Mussels (Bathymodiolus thermophilus) and giant clams (Calyptogena magnified) are absent.

Because of the sedimented nature of the setting, Escanaba vent sites include faunal elements not found elsewhere at NE Pacific vents, including a variety of polychaete species and thyasirid clams. Tubeworms (Ridgeia piscesae), paralvinellid polychaetes and associated fauna typical of NE Pacific vents also occur. Dense populations of brachiopods and tunicates occur on fossil sulfides.

Sulfides growth as individual tall chimneys rather than mounds. Includes "Clam Acres," "Hanging Gardens," "Holger's Hole." As at 21°N. Site list includes "Genesis," "Totem," "Pogonord," "Pogosud," "Parigo."

21°N

2600

20°49~50'N, 109°05'W

13°N

2600

12°38~54'N, 103°50'~104°01'W

9°N (also known as "Venture Hydrothermal Field")

2500

9°45-9°5'N, 104°17W

As at 21°N, Multiple black smokers and low-temperature vents typically lie in nearly linear array, constrained within an axial valley or trough. Smokers often closely associated with fissures. Site of the 1991 volcanic eruption.

17°S (also known as the "Spike Area")

2600

17°24-30'S, 113°13'W

The fastest-spreading ridge axis, with high volcanic and hydrothermal output. Black smokers are abundant (dozens along a 40 km extent of ridge axis), as are low-temperature fields. Major biological sites include "Rehu Marka," "Fish Bowl."

Dominated by large fields of clams plus tube worms, alvinellid polychaetes; mussels absent during early years of exploration (1980s). Dominated by tubeworms, mussels, alvinellids with rare clams. Focus of long-term observations of community composition and structure. Location of the 1.1-km-long BioGeoTransect established after the 1991 eruption to track colonization of new hydrothermal sites. Identified as the priority site for U.S. research on reproductive biology of vent organisms (including gametogenesis, larval dispersal, recruitment, etc.). Fauna superficially resembles that of other East Pacific Rise sites (clams, tubeworms, mussels, alvinellids).

TABLE 2.A. (Continued) Site

Depth (m)

Location

Geological Notes

Biological Notes

Galapagos Spreading Center Rose Garden 2500

00°48'N, 86°13'W

No active high-temperature vents (black smokers) have yet been discovered associated with the Galapagos Spreading Center. Also nearby: "Mussel Bed," "Garden of Eden," "East of Eden," "Clam Bake."

Western Pacific Okinawa

The "textbook" vent community (tubeworms, clams, mussels, limpets, alvinocarid shrimp, bythograeid crabs, serpulid worms, anemones, etc.) with zonation from the throat of a vent to the periphery. High-temperature taxa (e.g., Alvinella spp.) are absent.

550

28°23'N, 127°38'E

Vents are located on Minami-Ensei Knoll at depressions which are likely to be small calderas. Settings include bare rock and soft sediment. Both black smokers and low temperature fields are present. Other sites in the Okinawa Trough include "Izena Caldron" and "Iheya Ridge," both at 1400 m.

Mariana

3600

18°10'N, 144°43'E 18°12'N, 144°42E 18°02'N, 144°45'E

Located in a semi-enclosed basin (Mariana Trough) with a sill depth of 3700 m. Explored vents occur on crests of narrow basalt ridges.

Minami-Ensei Knoll is one of the shallowest hydrothermal sites that supports endemic invertebrate species. The species list includes tube worms, several mussel species, including Bathymodiolus japonicus and B. aduloides, clams (Calyptogena solidissina), and bythograeid crabs. The mussel, B. japonicus, is the overwhelmingly dominant species. First of the western Pacific back-arc basin vents to be explored. Fauna is distinct from that of eastern Pacific vents. Hairy gastropods (Alviniconcha hessleri) containing chemoautotrophic endosymbionts are abundant, as are suspension-feeding barnacles. Tubeworms are not present. With alvinocarid shrimp (Chorocaris vandoverae) and bythograeid crabs (Austinograea williamsi).

Manus

2500

3°9'S, 150°17'W

Includes "Vienna Woods."

Fiji

2000

16°59'S, 173°55'E

Includes "White Lady," "Mussel Valley."

Lau

1750-1850

22°13-32'S, 176°37-43'W

Numerous black smokers at "Vai Lili" and end-member fluids with extremely low pH (2). Also includes "Valu Fa Ridge," and "Hine Hina" (low-temperature site).

From sources cited throughout the text.

Dominated by the large symbiont-bearing gastropod, Ifremeria nautilei, and sessile barnacles on sulfide chimneys, with additional taxa, including tubeworms (distinct from those on the East Pacific Rise and NE Pacific vents). Allies most closely to Fiji and Lau vent faunas rather than to Mariana and Okinawa faunas. Dominated by gastropods (Ifremeria nautilei and Alviniconcha hessleri) and mussels (Bathymodiolus brevior and B. elongatus), with other taxa. Vai Lili is dominated by gastropods (Ifremeria nautilei and Alviniconcha hessleri). Hine Hina is dominated by mussels (Bathymodiolus brevior). Tubeworms, shrimp and other faunal types are also present.

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Schouten, H., K.D. Klitgord, and J.A. Whitehead. 1985. Segmentation of mid-ocean ridges. Nature 317:225-229. Schultz, A., J.R. Delaney, and R.E. McDuff. 1992. On the partitioning of heat flux between diffuse and point source venting. J. Geophys. Res. 97:12299-12314. Seyfried, W.E., Jr., and M. Mottl. 1995. Geologic setting and chemistry of deep-sea hydrothermal vents. In: D.M. Karl (ed.). The Microbiology of Deep-Sea Hydrothermal Vents. CRC Press, New York, pp. 1-34. Simoneit, B.R.T., and P. Lonsdale. 1982. Hydrothermal petroleum in mineralized mounds at the seabed of Guaymas Basin. Nature 295:198-202. Sleep, N.H. 1975. Formation of oceanic crust: Some thermal constraints. J. Geophys. Res. 80:4037-4042. Smith, D.K., and J.R. Cann. 1993. Building the crust at the Mid-Atlantic Ridge. Nature 365:707-715. Smith, W.H.F., and D.T. Sandwell. 1997. Global sea floor topography from satellite altimetry and ship depth soundings. Science 277:1956-1962. Solomon, S.C., and D.R. Toomey. 1992. The structure of mid-ocean ridges. Ann. Rev. Earth Planet. Sci. 20:329-364. Stein, C.A., and S. Stein. 1994. Constraints on hydrothermal heat flux through the oceanic lithosphere from global heat flow. J. Geophys. Res. 99:3081-3096. Stein, C.A., S. Stein, and A.M. Pelayo. 1995. Heat flow and hydrothermal circulation. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 425-445. Stern, R.J., P.-N. Lin, J.D. Morris, M.C. Jackson, P. Fryer, S.H. Bloomer, and E. Ito. 1990. Enriched back-arc basin basalts from the northern Mariana Trough: Implications for the magmatic evolution of back-arc basins. Earth Planet. Sci. Lett. 100:210-225. Taylor, B., A. Goodliffe, F. Martinez, and R. Hey. 1995. Continental rifting and initial sea-floor spreading in the Woodlark basin. Nature 374:534-537. Tivey, M.A., and H.P. Johnson. 1995. Alvin magnetic survey of zero-age crust: CoAxial Segment eruption, Juan de Fuca Ridge 1993. Geophys. Res. Lett. 22:171— 174. Tivey, M.K. 1995. Modeling chimney growth and associated fluid flow at seafloor hydrothermal vent sites. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 158-177. Tivey, M.K., and J.R. Delaney. 1986. Growth of large sulfide structures on the Endeavour Segment of the Juan de Fuca Ridge. Earth Planet. Sci. Lett. 77:303-317. Tivey, M.K., S.E. Humphris, G. Thompson, M.D. Hannington, and P.A. Rona. 1995. Deducing patterns of fluid flow and mixing within the active TAG hydrothermal mound using mineralogical and geochemical data. J. Geophys. Res. 100:1252712555. Vallier, T.L., P.J. Harold, and W. Girdley. 1973. Provenances and dispersal patterns of turbidite sand in Escanaba Trough, Northeastern Pacific ocean. Mar. Geol. 15:6787.

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75

Vera, E.E., J.C. Mutter, P. Buhl, J.A. Orcutt, AJ. Harding, M.E. Kappus, R.S. Detrick, and T.M. Brocher. 1990. The structure of 0-0.2-m.y.-old oceanic crust at 9°N on the East Pacific Rise from expanded spread profiles. J. Geophys. Res. 95: 15529-15556. Vine, F.J., and D.H. Matthews. 1963. Magnetic anomalies over oceanic ridges. Nature 199:947-949. Von Damm, K.L., J.M. Edmond, C.I. Measures, and B. Grant. 1985. Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California. Geochim. Cosmochim. Acta 49:2221-2237. Wright, D.J., R.M. Haymon, and K.C. Macdonald. 1995. Breaking new ground: Estimates of crack depth along the axial zone of the East Pacific Rise (9°12'-54'N). Earth Planet. Sci. Lett. 134:441-457.

Chemical and Physical Properties of Vent Fluids While some hydrothermal vent organisms are adapted to high temperatures, it is the chemistry of hydrothermal fluids—not the heat—that sustains the chemosynthetic basis of life at vent ecosystems. For this reason, it behooves the biologist to appreciate how and where vent fluids arise, and especially the physical properties and chemical composition of vent effluents. At ridgeaxis hydrothermal systems, the low- to moderate-temperature fluids in which vent organisms live are usually simply diluted versions of high-temperature (~350°C) fluids of black smokers, with the diluent being cold seawater. The process of vent-fluid generation in submarine systems is analogous to that occurring at terrestrial hot springs, but the major reactants in terrestrial systems are meteoric (rain) water and continental crust, while in submarine systems the major reactants are seawater and oceanic crust. Even before high-temperature hydrothermal vents were discovered, experimental work on seawater-basalt interactions at elevated temperatures and pressures in the laboratory indicated that magnesium and sulfate would be rapidly depleted from seawater and that potassium, calcium, and silica would be enriched in the modified fluids (Bischoff and Dickson 1975). Solubilities of metals and sulfur also increase significantly at temperatures above 350°C (Seyfried et al. 1988), resulting in their mobilization from rocks into fluids. Compared to seawater, black-smoker fluids have a low pH (3-5) and are especially enriched in sulfide (H2S), hydrogen (H2), methane (CH4), manganese (Mn), and other transition metals (iron, zinc, copper, lead, cobalt, aluminum). Magnesium and oxygen are completely stripped from vent fluids (table 3.1). Most of this change in fluid chemistry takes place in a hightemperature reaction zone. 3.1 SUBMARINE HYDROTHERMAL CIRCULATION CELLS: HIGH-TEMPERATURE REACTION ZONES As seawater penetrates deep into the crust at the spreading axis, it reaches the base of the sheeted-dike complex (~2 km), and, close to an axial magma chamber where temperatures exceed 350°C, major seawater-rock reactions take place. Called the "reaction zone," this is where fluids acquire the chemi-

77

PROPERTIES OF VENT FLUIDS

TABLE 3.1. Chemical composition of typical 350°C black-smoker fluid compared to seawater

Element H2S H2 CH4 Mn Fe Be Zn Cu Ag Pb Co Si Al Ba Cs Li Rb CO2 Ca Sr B As Se P Mg SO4 Alk

Hydrothermal Fluid

3-12 0.05-1 25-100 360-1140 750-6500 10-40 40-100 10-40 25-40 10-360 20-220 15-20 5-20 10-40 100-200 410-1320 10-30 5-15 10-55 90

450-560 30-450 1-75 0.5 0 0-1

(-O.l)-(-l)

Enrichment Factor (minimum)

Seawater

Units

0 0 0 0 0 0 0.01 0.007 0.02 0.01 0.03 0.05 0.02 0.15 2 25 1 2 10 85 415 30 2 2 50 30 2

mMkg- 1 mMkg""1 1

jjiMkgMMkg- 1 jxMkg" 1

nMkg" 1 IxMkg-1 ^Mkg" 1 nMkg" 1 nMkg" 1 nMkg- 1 mMkg- 1 fxMkg"1 (juMkg-1

nMkg" 1

fjuMkg"1 fjuMkg-1 mMkg-1 mM k g " 1 fxMkg" 1 jjiMkg- 1

nMkg" 1 nMkg" 1 fxMkg'1 mMkg" 1 mMkg" 1 mMkg" 1

00 00 00 00 00 00

4000 1500 1250 1000 650 300 250 66 50 16 10 2.5 1 1 1 1 0.5 0.25 0 0 0

From summary data in Elderfield and Schultz (1996), but with numbers rounded and ranked by degree of enrichment above seawater.

cal composition characteristic of "end-member" fluids, which exit the seafloor as black smokers. Because the magma chamber is a melt or crystal mush at 1200°C and cannot maintain the porosity to permit water circulation, the lower boundary of the reaction zone is defined by the upper surface of the magma chamber in those systems where a magma chamber occurs. Along slow-spreading ridge axes where hydrothermal activity is present but no evidence for a magma chamber exists (see chapter 2.1.4), high-porosity regions are thought to extend 3 to 3.5 km below the seafloor where the rock is hot (Alt 1995).

78

CHAPTER 3

50 100~

S

Liquid + Vapor

150-

& 200o 5 250-

(t 3 0 °"

iCP

350

400-

Liquid

450500 250

300

350

400

450

500

Temperature (C) Figure 3.1. Two-phase curve for seawater. CP = critical point where seawater is 50% brine, 50% vapor. From Von Damm et al. 1995.

3.2 PHASE SEPARATION While the major reactants involved in the generation of hydrothermal fluids —seawater and basalt—are of relatively uniform composition throughout the ocean and its crust, physical conditions at the reaction zone can exert significant influences on some aspects of vent-fluid chemistry, notably its salinity (chlorinity) and gas concentrations. Temperature (7) and pressure (P) conditions within the hydrothermal cell determine whether phase separation takes place. The "two-phase curve" (fig. 3.1) separates the pressure-temperature conditions in which seawater exists as a liquid or as coexisting liquid and vapor phases. A critical point on the two-phase curve is located at 407°C and 298 bars (Bischoff 1991). At this critical point, seawater is 50% brine, 50% vapor. If seawater crosses the two-phase curve below this critical point (e.g., T = 450°C, P = 350 bars), the seawater will boil, producing a lowsalinity vapor phase (subcritical phase separation). If seawater crosses the two-phase curve above the critical point (e.g., T = 450°C, P = 250 bars), condensation will take place, producing a small amount of brine and a larger amount of vapor (supercritical phase separation). Phase separation of hydrothermal fluids can occur within the ocean crust in at least three different situations: (1) in relatively shallow vent systems where black-smoker fluid crosses the two-phase curve (e.g., Axial Seamount;

79

PROPERTIES OF VENT FLUIDS

Low Temperature Reaction Zone

High Temperature Reaction Zone

Figure 3.2. Cartoon of a seafloor hydrothermal circulation cell. Seawater flows downward into the crust, with the first major change in seawater composition occurring at ~130°C (low-temperature reaction zone) as anhydrite (CaSO4) precipitates. Other water-rock reactions occur within the downflow zone as well. In the deepest, hottest part of the system, water-rock reactions proceed more quickly, there is direct input of gases from magma to the fluids, and there may be phase separation into brine and vapor. From Von Damm 1995.

Butterfield et al. 1990); (2) in the high-temperature reaction zone close to a magma chamber as part of the heating up of fluids (seen in minute volumes of fluids trapped in vesicles within rocks; Kelley and Delaney 1987); and (3) following a submarine eruption where magma intrusion into the shallow crust has taken place (e.g., Von Damm 1995). In the case of phase separation associated with an eruption, vent-fluid chemistries within a vent field can show discernible spatial and temporal trends. Chloride compositions of end-member fluids can range from about one-twelfth the value of seawater to over twice the seawater value (Von Damm 1995). This range in chlorinities requires phase separation and physical segregation of brine from vapor (fig. 3.2); no other processes can account for such large compositional changes. A single vent can sequentially express vapor and then brine, as observed for "F" vent of the Venture hydrothermal

80

CHAPTER 3

field at 9°N on the East Pacific Rise. At "time zero," when the vent first formed following a volcanic eruption in 1991, F-vent fluids were at 388°C and 258 bars, on the two-phase curve for seawater, and were very low in chlorinity (8% that of seawater). Three years later, the same vent had cooled to 350°C and was venting fluids of —1.5 times seawater chlorinity (Von Damm et al. 1997) and with the conjugate compositional chemistry to the vapor phase. This is the first direct evidence that brines can be stored within the oceanic crust. 3.3 FLOW RATES, TRANSIT TIMES, AND TEMPERATURE OF FORMATION Exit rates of buoyant end-member fluids from hydrothermal chimneys have been measured at 0.7 to 3.4 m s" 1 (Converse et al. 1984; Ginster et al. 1994), indicating a minimum of about one hour transit from the high-temperature reaction zone depth (assumed to be at 2 km) to the surface if upflow was through a simple pipe. In fact, the upflow zone is likely to be tortuous, and fluids probably rise relatively slowly. Allowing for adiabatic cooling during ascent, fluid exiting the seafloor at 350°C corresponds to a reaction temperature of 362°C at 400 bars. Fluid chemistries, however, indicate that they must have formed at temperatures closer to 400°C and that they thus must undergo conductive cooling during their transit to the seafloor surface (Seewald and Seyfried 1990). Maximum temperatures of hydrothermal fluids appear to be constrained by quartz recrystallization, which is very rapid at about 350°C (Von Damm et al. 1991). Dilution of end-member fluids during ascent through the highly porous crustal layer 2A is presumably prevented by the formation of impermeable mineral conduits in the upflow zone (Cann and Strens 1989; Wilcock 1998). 3.4 END-MEMBER FLUIDS 3.4.1 Composition High-temperature vent fluids (table 3.1) are mixtures of three components: (1) heated seawater that has reacted with hot rock to lose magnesium, sulfate, etc., and to gain other elements; (2) vapor from phase separation, rich in volatile gases (e.g., sulfide); and (3) brine from phase separation, rich in metals and depleted in gases. Variations in vent fluids can be accounted for by mixing of different proportions of these three components (Edmonds and Edmond 1995). Because of the uniformity in composition of the two reactants in hydrothermal systems on mid-ocean ridges (seawater and mid-ocean

PROPERTIES OF VENT FLUIDS

81

ridge basalts), there is similarity in the major-element chemical composition of, for example, vent fluids collected from the TAG hydrothermal field on the Mid-Atlantic Ridge and from vents at 21°N on the East Pacific Rise (Campbell et al. 1988). These sites have presumably reached an equilibrium condition and vary little over time. Where there are large differences in fluid composition over time or within a vent field, they can usually be related to phase separation. Exceptions include situations where the chemical composition of the host basalt varies significantly from that of normal mid-ocean ridge basalts (e.g., hydrothermal vents in back arc basins; Fouquet et al. 1993) or where sediment overlies sills of extrusive volcanics (e.g., Guaymas Basin in the Gulf of California; Von Damm et al. 1985) or where sediment may be buried beneath a basalt crust (e.g., Endeavour Segment of the Juan de Fuca Ridge; Lilley et al. 1993).

Basic Controls on Chemistry When seawater passes through a deep hydrothermal cell, sulfate is completely removed through precipitation as anhydrite and through reduction reactions to sulfide at high temperatures. Alkalinity is lost through waterrock interactions, resulting in an excess of protons and an acidic pH of ~ 3 5. Chloride concentrations increase or decrease relative to seawater, depending on phase-separation events and subsequent mixing with or tapping of segregated fluids. Sulfide, derived from reduced seawater sulfate and reduced sulfur leached from rocks at high temperatures, varies inversely with chloride during phase separation. Thus, high-chlorinity fluids (brines) generally have low sulfide concentrations. As in seawater, sodium is the most abundant cation in hydrothermal fluids, followed by calcium. Magnesium is completely removed from seawater through hydrothermal processes. Because seawater is often unintentionally entrained in submersible-collected samples of high-temperature fluids from the throats of black smokers and because magnesium is conservatively mixed during this process, magnesium concentrations are used to determine the extent of mixing and to extrapolate concentrations of other conservative compounds in end-member (undiluted) fluids (Edmond et al. 1982). Alkali metals (lithium, potassium, rubidium, cesium) are preferentially leached from basalt, resulting in significant enrichments above seawater concentrations in end-member vent fluids. Silica is a major element in vent fluids, and its typical concentrations are consistent with equilibrium of vent fluids and silica-rich minerals at temperatures near 375-400°C. High concentrations are derived by dissolution of silica from altered basalt. Trace metals are mobilized from basalt during water-rock interactions at high temperatures, resulting in non-trace concentrations in end-member

82

CHAPTER 3

fluids. Millimolar concentrations of iron, manganese, and zinc are typical, while copper is present in |xM to nM concentrations. Hydrothermal vent fluids are reducing fluids, containing no oxygen and high concentrations of sulfide and hydrogen. The concentration of iron decreases exponentially as sulfide increases, a property related to changes in the proportion of vapor to brine in the three-component mixing model of Edmonds and Edmond (1995). Low Fe/H2S ratios indicate an excess of sulfide over precipitating cations and have been invoked as an important biological control (Seyfried and Ding 1995). Vent organisms do not use undiluted vent water, and it only takes a small amount of dilution of vent fluids with ambient seawater to raise the pH sufficiently to precipitate sulfides. The diluted water will thus be either rich in sulfide (where Fe/H2S ratios are low) or rich in metals (where Fe/H2S ratios are high), but not both. A similar case has been made for high ratios of Zn/H2S at a vent site on the Explorer Ridge (Tunnicliffe et al. 1986). Nitrogen and phosphorus compounds in high- and low-temperature vent fluids are of great significance, given their potential role as limiting nutrients in biological productivity. Despite this, little is known about nitrogen and phosphorus inventories and geochemical cycles within vent systems (Karl 1995). As long as bottom waters are nutrient rich, dilution of vent fluids provides adequate concentrations of nitrogen and phosphorus. If vents are situated in nutrient-poor bottom waters, as may be found in the Mediterranean Sea, these limiting nutrients may be problematic. Ammonia is significantly elevated in some high-temperature mid-ocean ridge hydrothermal settings, notably sedimented sites such as Guaymas Basin (up to 15.6 mM; Von Damm et al. 1985), where the ammonia arises from organic decomposition. Nitrate and nitrite are depleted in vent fluids (Tunnicliffe et al. 1986) and amino acids are undetectable (Haberstroh and Karl 1989). Lilley et al. (1983) observed high ammonia concentrations in vent fluids at the Main Endeavour Field on the Juan de Fuca Ridge, a nonsedimented system. They attribute these ammonia values (0.64-0.95 mM) to decomposition of subseafloor organic material associated with sediments subsequently buried by volcanics during evolution of the ridge axis. Phosphorus appears to be neither substantially enriched nor depleted in high-temperature hydrothermal fluids relative to ambient seawater (Karl 1995). 3.4.2 Magmatic Inputs In addition to seawater-rock interactions, there can be direct input of gases into hydrothermal fluids at depth from degassing of magmas and mantle. Primordial 3He (derived from the time when the Earth accreted) is enriched in vent fluids and is clearly derived from degassing of the mantle (Craig and

PROPERTIES OF VENT FLUIDS

83

Lupton 1981). A magmatic origin for CO2 in vent fluids is also indicated, based on the similarity of stable carbon isotope ratios of CO2 in vent fluids compared to values for mantle CO2 (Craig et al. 1981). Methane and hydrogen gases in vent fluids may also have magmatic contributions (Welhan 1988), although these gases evolve during reactions of seawater with rock, sediments, and sulfides and may have, in part, a biological origin (Baross et al. 1982; Lilley et al. 1993). 3.4.3 Evolution of Vent-Fluid Chemistry Repeated measurements of major-element chemistry from a number of vent sites suggest that chemical compositions of end-member fluids can be strikingly stable on a decadal time scale (Von Damm 1995). The implication is that water-rock interactions at depth are controlled by equilibrium dynamics and buffering by the assemblage of minerals produced by heating basalt in hot water to black-smoker temperatures (Bowers et al. 1988). Fluid compositions of recently developed hydrothermal systems (i.e., following diking events or eruptions), however, undergo major temperature and chemical changes within very short time frames (hours-days-weeks). These observations suggest that hydrothermal systems can undergo rapid chemical evolution, with changes decreasing in magnitude over a period of a few years, followed by a longer period of steady-state composition and temperature on a decadal time scale (Lupton 1995). Low chlorinities and enhanced volatile fluxes (H2S, CO2, He, and H2) concomitant with volcanic eruptions and the establishment of new vent sites are a consequence of the increased heat flux associated with volcanism and phase separation, with the conjugate brines tapped by temporally segregated hydrothermal systems (fig. 3.3; Von Damm et al. 1995; Butterfield et al. 1997). The time period of this evolution varies with the size of the volcanic event and may range from weeks to years (Butterfield et al. 1997). The chemistry of "early" hydrothermal fluids may be especially significant as providing settlement cues for pioneer species, but the relation between fluid chemistry and ecological response is poorly understood. 3.4.4 Back-Arc Fluid Chemistries Chemistries of venting fluids of back-arc spreading centers can be distinct from those of mid-ocean ridge vents because of contributions from watery fluids in sediments from the down-going oceanic slab to the host extrusive lavas (Fouquet et al. 1993). In particular, they may be rich in economic ores, with as much as 7 ounces of silver per ton of precipitated mineral and 1 ounce of gold (Herzig et al. 1994).

84

CHAPTER 3

Relat ive 1Interisity

Vapor Dominated

0

Brine Dominated

IX V>....... y

^

l'\

•/

1

Decay

\ ^* *» ^

.,,_

"" — — — — — _

Time

Event

Heat Flux

•Cl

Fe

Figure 3.3. Response of hydrothermal systems to a volcanic event. Systems evolve from a vapor-dominated, high-heat-flux stage accompanied by phase separation, through a transition to a brine-dominated discharge, and eventually decay back to seawater composition and no heat flux. It is possible that in some systems the brine pool is tapped separately from the vapor, so that the transition from vapor to brine phase is skipped. From Butterfleld et al. 1997.

3.5 THERMAL RADIATION The idea that deep-sea hydrothermal-vent environments might represent nonsolar photic habitats arose from observations of a novel photoreceptor in vent shrimp that colonize high-temperature (350°C) black-smoker chimneys on the Mid-Atlantic Ridge (Van Dover et al. 1989; see chapter 7.10.1). Light emitted from a 350°C black body heat source peaks at long wavelengths in the mid- to far-infrared, but the tail of the spectrum extends into visible wavelengths (400-650 nm). Intrinsic attenuation of light in seawater limits significant light transmission in photic habitats at vents to visible and nearinfrared wavelengths (400 to 1050 nm). Digital imaging of ambient light conditions at a black smoker (fig. 3.4) demonstrates that light is indeed associated with high-temperature fluids as they exit the orifice and mix with seawater (Van Dover et al. 1994). Photometric data confirm that most of the light produced by a black smoker is predominantly in the near-infrared (750-1050) and that there is a small but detectable flux at shorter wavelengths (Van Dover et al. 1996). While visible wavelengths are of obvious importance in vision, near-infrared wavelengths of light are important in photobiochemical reactions of bacterial photo-

PROPERTIES OF VENT FLUIDS

85

Figure 3.4. A. Strobe-illuminated digital image of a 350°C black smoker at the Main Endeavour Field, Juan de Fuca Ridge, illustrating the sulfide mineral chimney and exiting fluids. B. Ten second exposure of ambient light at the same black smoker. All submersible lights were extinguished and portholes blacked out. Photograph by M. O. Smith, J. R. Delaney, C. L. Van Dover, J. R. Cann, and D. B. Foster.

synthesis. The latter circumstance raises the provocative possibility of geothermally driven photosynthesis at deep-sea hydrothermal vents (see chapter 5.3).

3.6 AXIAL LOW-TEMPERATURE, DIFFUSE-FLOW CHEMISTRY In the biological zones of hydrothermal systems, vent fluids are diluted and cooled, resulting in temperatures that are barely distinguishable from those of ambient waters to temperatures as high as are known to support life (~110°C). References to low-temperature, diffuse-flow vents vary in definition, however, often being restricted to vents emitting hydrothermal fluids at temperatures that sustain macroinvertebrate faunas, that is, generally less than ~60°C. Gradients of temperatures and fluid chemistries within a hydrothermal field are undoubtedly important in determining the patterns of distribution of vent organisms. Despite the significance of chemical gradients to biota living

86

CHAPTER 3

in low-temperature situations, there are surprisingly little systematic data on the relationship between particular taxa and fluid chemistry. Low-temperature hydrothermal vents on the Galapagos Spreading Center were the first deep-sea vents ever discovered, and it is from these sites that perhaps the most comprehensive low-temperature geochemical data are available. The Galapagos Spreading Center is the only ridge segment visited so far that has no extant high-temperature fluid sources, although relict sulfide deposits indicate past black-smoker activity. Low-temperature fluids at Galapagos vents arise through sub-seafloor dilution of end-member hightemperature fluids with ambient seawater, with subseafloor deposition of sulfide minerals (Edmond et al. 1979). Johnson and his colleagues (1986, 1988a, 1988b, 1994) have published accounts of the low-temperature chemistry of Rose Garden vents on the Galapagos Spreading Center as part of a multidisciplinary ecological study of invertebrate ecology and physiology at that site. Their work serves to characterize the chemical nature of low-temperature hydrothermal environments and is summarized below. 3.6.1 Flow Rates, Temperature, and Temperature Variability Flow rates at low-temperature vents are highly variable, from barely detectable to vigorous flow. Measured rates at the Galapagos vents range from 0.5 to 5 cm s" 1 (Corliss et al. 1979; Smith 1985). Flow can be modified by biological communities, as in the case of mussel beds, where fluid flow and the redox transition zone are spread over a broader area than would be the case in the absence of the mussels (Johnson et al. 1988b). Temperature is often used as a proxy measure of hydrothermal fluid chemistry in low-temperature settings, the assumption being that increasing temperatures correspond to lesser dilution of vent fluids and thus higher concentrations of sulfide, methane, metals, and other species of importance to biological systems. In many situations, temperature can be a conservative tracer of mixing, but under some circumstances, heat loss by conduction to surrounding surfaces (rock or animal) can be high (Johnson et al. 1988b). Because there can be significant variations in vent chemistry from site to site, temperature data in the absence of chemical analyses can be used only as an approximate measure of hydrothermal influence. Time-series records at a variety of low-temperature vents demonstrate the extremely time-variant nature of the temperature records. In all situations, temperature fluctuates or "flickers" over short time scales, as warm vent fluids and cold seawater undergo turbulent mixing (see chapter 7.2.2). Oscillations at the Rose Garden site vary on the order of 1°C s" 1 and 5-10°C over 10-s intervals (Johnson et al. 1988b). This kind of short-term variability is extremely important for organisms requiring simultaneous delivery of oxygen-rich seawater for aerobic respiration and sulfide-rich fluids for support

PROPERTIES OF VENT FLUIDS

87

of microbial primary production (Johnson et al. 1988a). On longer time scales, many records show periodic influences of tidal motions on temperature, due presumably to some combination of tidally induced pumping and tidal oscillations in near-bottom currents (e.g., Johnson and Tunnicliffe 1985; Little et al. 1988; Chevaldonne et al. 1991). Various attempts have been made to use chemical composition of carbonate shells of invertebrates to trace changes in temperature within low-temperature vent fields (e.g., Killingley et al. 1980; Fatton et al. 1981; Roux et al. 1985), but these efforts are often compromised by limited sample sizes (n < 2), the motility of the subjects under study (bivalve mollusks), and the sharp gradients of temperature known to exist in vent environments. Hart and Blusztajn (1998) report a 21 yr record of strontium/calcium ratios in two vent clam shells (with submonthly resolution) as a temperature proxy for hydrothermal flux at the 9°N site on the East Pacific Rise. Given simple assumptions about clam growth rates and behavior, the Sr/Ca ratios are reported to document thermal anomalies associated with two known discrete eruptive events (1991 and 1992). 3.6.2 Silicate Silicate concentrations in low-temperature fluids are usually good conservative tracers of mixing, defining linear mixing lines that reflect simple twosource mixing models (fig. 3.5). Silicate concentrations at Rose Garden extrapolated to an end-member (350°C) fluid composition are within the range of silicate concentrations measured in 350°C fluids from East Pacific Rise sites. 3.6.3 Sulfide Sulfide concentrations at Rose Garden, measured as the sum of H2S, HS~, and S 2 ~ (2H 2 S), can be correlated with temperature (fig. 3.5), but where biological uptake is rapid, the relationship becomes nonlinear. The proportion of H2S, HS~, and S 2 ~ is determined strictly by the pH of the transporting fluid. At the near neutral pH (7-7.9) of low-temperature fluids, HS~ is the prevailing species. Sulfide exposed to oxygen is inorganically oxidized, with a half-life of ~ 380 h at 2°C, pH = 7.8, and 110 fiM O2,10 yM H2S (Millero et al. 1987). Biological oxidation of sulfide by macro and microorganisms at Galapagos vents can be four to five orders of magnitude greater than spontaneous sulfide oxidation in the laboratory and appears to be responsible for most of the rapid removal of sulfide from waters flowing past dense animal communities (Johnson et al. 1988b). Under high-flow conditions, however, there is little diminution of sulfide.

88

CHAPTER 3

125100^ c

75-

g

50 H

0

o

25-I 2

0

Sulflde ( :M)

100"

x

80-

xx X

x

x

^xX

60-

x

40-

1

x Jjp 0

2

600-

^

7 X

20-

_

3 4 5 6 Temperature (°C)

3 4 5 6 Temperature (°C)

500-

x x x xx:

400-

x *

g 300W

2001000 0

2

3 4 5 6 Temperature (°C)

Figure 3.5. Low-temperature chemistry at Rose Garden; silicate, sulfide, and oxygen vs. temperature measured using an in situ chemical scanner. From Johnson et al. 1988b.

Oxidation products of sulfide include sulfate (SO4), thiosulfate (S2O3), and elemental sulfur (So). Johnson et al. (1998b) found no thiosulfate concentrations above the detection limit (0.9 |JLM), suggesting that thiosulfate is not a significant oxidation product in the vent-fluid environment.

89

PROPERTIES OF VENT FLUIDS 125 N

c

CD

6

N

! [°2l

8000

[02l Conservative \ Mixing

\ Measured

y^

/

[XH2S]

f N \ \ S \

\ \ \ N

0

S

Temperature (°C)

350

Figure 3.6. Theoretical (conservative) and measured mixing curves of oxygen vs. temperature, when end-member, 350°C vent fluid mixes with seawater. In the absence of oxidation reactions, oxygen follows a conservative, linear mixing curve. "[O2] Measured" is the observed oxygen concentration trend; "[XH2S]" is the observed trend for sulfide. From Johnson et al. 1988a. Time-varying sulfide exposure within mussel clumps at Rose Garden indicates that mussels were exposed to sulfide concentrations as high as 330 |JLM, with an average exposure of 27 |xM (Johnson et al. 1994). Sulfide gradients as great as 2-10 |ULM 2H 2 S cm" 1 were detected above tubeworms in the most vigorous flow field and were measurable to a height of several meters above the bottom (Johnson et al. 1988b). 3.6.4 Oxygen At Rose Garden, oxygen disappears from the system at silicate concentrations of 500 to 700 |JLM, corresponding to temperatures of 10-12°C (fig. 3.5). If oxygen from seawater mixed conservatively with anoxic vent fluids, measurable oxygen would be detected even at relatively high temperatures. But end-member fluids contain reduced compounds (especially Fe(II) and sulfide) at concentrations 100 times greater than that of oxygen in seawater. At these high concentrations, inorganic oxidations rapidly consume oxygen, so that even at mixtures of 90% seawater and 10% 350°C end-member fluid—corresponding to a 10°C low-temperature fluid—oxygen concentrations go to zero (fig. 3.6). 3.6.5 Profiles of Oxygen, Sulfide, Silicate, and Temperature Using an in situ chemical analyzer, Johnson et al. (1986) characterized the chemical profile of vent fluids as the analyzer probe was pushed into a

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TABLE 3.2. Rose Garden low-temperature (maximum T = 14°C; ambient T = 2.1°C) fluid chemistry Species

Maximum Concentration (\LM)

Iron Manganese Methane Sulfide Silicate Nitrate Ammonia

0.3 15.0 3.3 330.0 700.0 40.0 5.0

From Johnson et al. 1988b; methane from Lilley et al. 1983.

clump of mussels at Rose Garden (table 3.2; fig. 3.7). Silicate was linearly related to temperature (fig. 3.5). As temperature increased, oxygen levels decreased and sulfide concentrations increased. If conservative mixing controls the concentration of sulfide as it does silicate, plots of the sulfide versus 150125-

100-

500-

80-

400-

100-

75" |

4 0

.

•

60-

Silicate d

^

50-

25-

o.

20-

100-

o.

0-

10

Time (min)

20

Figure 3.7. Low-temperature chemistry at Rose Garden: temperature, silicate, sulfide, and oxygen concentrations as the chemical sensor moves progressively from ambient bottom water (left-hand side) into a clump of mussels (middle) and then back out again (right-hand side). Note that oxygen concentration is minimum at 9.5°C at the same time that temperature, silicate, and sulfide are maximum. From Johnson et al. 1986.

91

PROPERTIES OF VENT FLUIDS 100 - |

80 -

60

40 M

20

0

100

200

300 Silicate (JJLM)

Figure 3.8. Low-temperature chemistry at Rose Garden: sulfide concentration vs. silicate at two sites. The straight lines indicate the values expected if conservative mixing alone was involved. Curvature of sample values below these lines indicates nonconservative loss of sulfide, with the sulfide presumably consumed by vent organisms rather than by inorganic oxidation. From Johnson et al. 1986. silicate data will yield a straight line. There is, however, significant curvature in the sulfide-silicate plots, with lower sulfide levels than expected for a given silicate concentration (fig. 3.8). This is clear evidence that sulfide is being removed from the system. Removal of sulfide in this series of observations is primarily attributed to biological oxidation by the invertebrates. 3.6.6 Methane, Manganese, and Iron Methane and manganese are present in Rose Garden low-temperature fluids (table 3.2; Lilley et al. 1983; Johnson et al. 1988b), but no evidence for significant methane or manganese oxidation is provided by plots of these compounds against silicate concentrations. The data fall on a linear mixing trend. Where iron concentrations in Rose Garden vent fluids are elevated above the limits of detection (table 3.2), they vary nonsystematically with silicate and are difficult to interpret.

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3.6.7 Nitrogen and Phosphorus Compounds As with high-temperature fluids, the nitrogen and phosphorus chemistry of low-temperature vent fluids is poorly documented. Nitrogen (N2) is readily available from ambient seawater, but most microorganisms require nitrogen as nitrate (NO 3 ~), nitrite (NO 2 ~), ammonia (NH4 + ), or organic nitrogen (e.g., amino acids). Lilley et al. (1983) and Johnson et al. (1988b) detected nitrate and ammonia in low-temperature fluids at Rose Garden (table 3.2). 3.7 FLANK LOW-TEMPERATURE FLUIDS Flank fluxes of low-temperature hydrothermal fluids were long predicted based on heat-flow anomalies (see chapter 2.5.1), but the first warm springs on a flank of a mid-ocean ridge spreading center were not discovered until 1995 (Mottl et al. 1998). Located on the eastern flank of the Juan de Fuca Ridge in heavily sedimented 3.5 Ma crust, the warm, 25°C springs emanate from a fault near the summit of the Baby Bare basalt outcrop. The venting fluids have a hydrothermal signature, including depleted magnesium and oxygen concentrations and enriched iron, manganese, sulfide, methane, and hydrogen content. Flux estimates indicate that the thermal output of Baby Bare is comparable to that of a black-smoker vent on the ridge axis. Flank warm springs may be important as stepping stones for the dispersal of vent taxa. Baby Bare appears to support a population of bivalves belonging to a genus (Thyasira) known to host chemoautotrophic endosymbionts, but these bivalves are not known from the closest hydrothermal vents on the Juan de Fuca Ridge (Tunnicliffe et al. 1998).

3.8 GLOBAL FLUXES AND THE HYDROTHERMAL INFLUENCE ON OCEAN CHEMISTRY AND CURRENTS Hydrothermal activity is a global process that figures prominently in global heat loss, chemical weathering of oceanic crust, geochemical cycling of elements, and the biogeochemistry of deep-ocean waters and sediments. By current best estimates (Elderfield and Schultz 1996), the global ocean cycles through seafloor hydrothermal systems once every 10 to 100 million years. For comparison, the same volume of ocean cycles through rivers once every 30 to 40 thousand years. Although cycling though hydrothermal systems is slower, the magnitude of hydrothermal chemical reactions is sufficient for hydrothermal systems to serve as sources of manganese, iron, lithium, rubidium, and cesium in the global ocean equal to or greater than riverine input on an annual basis. Except for manganese, the estimated net flux of

93

PROPERTIES OF VENT FLUIDS

8( 3 He)

1000

2000

Q

3000

4000 1000 km 5000

I 120

130 3

110

Longitude (°W)

100

I 90

3

Figure 3.9. Distribution of He (8 He) across the Pacific Ocean at 15°S. This water column plume overlies the lobe of metalliferous sediment extending westward from the East Pacific Rise that is mapped infigure3.10. From Lupton and Craig 1981. metals from seafloor hydrothermal systems is negligible when compared to net anthropogenic flux (German and Angel 1995). Hydrothermal circulation contributes all of the oceanic 3He, for which there is no significant continental source (fig. 3.9). Hydrothermal systems are also significant sinks for sulfate and magnesium, which get fixed in subsurface rock. Thus, hydrothermal circulation is important in controlling at least some fundamental aspects of the chemistry of seawater. Low-temperature reactions in the upper layers of the crust are pervasive and represent a long-term seafloor weathering process. Oxidized and otherwise chemically modified halos along fractures and exposed surfaces of basalt are produced during this weathering. Below 300-400 m in the crust, porosity and volume of flow decreases, and reduction rather than oxidation takes precedence. Magnesium, calcium, and sulfate are lost from seawater at depths in the crust wherever temperatures reach 130°C, precipitating as smectite or chlorite (magnesium) and anhydrite (calcium and sulfate) (Alt 1995). Hydrothermal plumes (see chapter 4) emanating from ridge crests interact with the ocean on a much faster time scale than subsurface hydrothermal

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i i 40 E

I i I I 80 E 120 E

i I 160 E

I i 160 W

Longitude

i I 120 W

i r 80 W

r i 40 W

i

Figure 3.10. Metalliferous sediments on the seafloor as indicated by the ratio of (Al + Fe + Mn)/Al. From Bostrom et al. 1969.

circulation. Recent estimates suggest that the volume of the global ocean passes through and reacts with hydrothermal plumes every 1000 yr, which is approximately the same time scale as thermohaline circulation of surface and deep-ocean waters (Kadko 1993; Kadko et al. 1995). Plumes are sites of active inorganic scavenging of elements from seawater by reaction with manganese and iron oxyhydroxides. Perhaps most biologically significant are removal rates of phosphorus, with estimates ranging from 15 to 40% of riverine input removed by precipitation with plume elements (Froelich et al. 1977). Scavenged elements and plume fallout are deposited as particulate metalliferous sediments, which can cover substantial areas of the seafloor adjacent to ridge axes (fig. 3.10; Mills and Elderfield 1995) and have been known since 1891 from sediment samples collected during the Challenger expedition (Murray and Renard 1891).

REFERENCES Alt, J.C. 1995. Subseafloor processes in mid-ocean ridge hydrothermal systems. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Inter-

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actions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 85-114. Baross, J.A., M.D. Lilley, and L.I. Gordon. 1982. Is the CH4, H 2 and CO venting from submarine hydrothermal systems produced by thermophilic bacteria? Nature 298:366-368. Bischoff, J.L. 1991. Densities of liquids and vapors in boiling NaCl-H2O solutions: a PVTX summary from 300° to 500°C. Am. J. Sci. 291:309-338. Bischoff, J.L., and F.W. Dickson. 1975. Seawater-basalt interaction at 200°C and 500 bars: implications for origin of seafloor heavy-metal deposits and regulation of seawater chemistry. Earth Planet. Sci. Lett. 25:385-397. Bostrom, K., M.N.A. Peterson, O. Joensuu, and D.E. Fisher. 1969. Aluminum-poor ferromanganoan sediments in areas of high heat flow on the East Pacific Rise. J. Geophys. Res. 74:3261-3270. Bowers, T.S., A.C. Campbell, C.I. Measures, AJ. Spivack, M. Khadem, and J.M. Edmond. 1988. Chemical controls on the composition of vent fluids at 13°-11°N and 21°N, East Pacific Rise. J. Geophys. Res. 93:4522-4536. Butterfield, D.A., G.J. Massoth, R.E. McDuff, J.E. Lupton, and M.D. Lilley. 1990. Geochemistry of hydrothermal fluids from Axial Seamount Hydrothermal Emissions Study Vent Field, Juan de Fuca Ridge: Subseafloor boiling and subsequent fluid-rock interaction. J. Geophys. Res. 95:12895-12921. Butterfield, D.A., I.R. Jonasson, G.J. Massoth, R.A. Feely, K.K. Roe, R.E. Embley, J.F. Holden, R.E. McDuff, M.D. Lilley, and J.R. Delaney. 1997. Seafloor eruptions and evolution of hydrothermal fluid chemistry. Philos. Trans. R. Soc. Lond. A 355:369-386. Campbell, A.C, M.R. Palmer, G.R Klinkhammer, T.S. Bowers, J.M. Edmond, J.R. Lawrence, J.F. Casey, G. Thompson, S. Humphris, P. Rona, and J.A. Karson. 1988. Chemistry of hot springs on the Mid-Atlantic Ridge. Nature 335:514-519. Cann, J.R., and M.R. Strens. 1989. Modeling periodic megaplume emissions by black smoker systems. J. Geophys. Res. 94:12227-12237. Chevaldonne, P., D. Desbruyeres, and M. LeHaitre. 1991. Time-series of temperature from three deep-sea hydrothermal sites. Deep-Sea Res. 38:1417-1430. Converse, D.R., H.D. Holland, and J.M. Edmond. 1984. Flow rates in the axial hot springs of the East Pacific Rise (21°N): Implications for the heat budget and the formation of massive sulfide deposits. Earth Planet. Sci. Lett. 69:159-175. Corliss, J.B., J. Dymond, L.I. Gordon, J.M. Edmond, R.P. Von Herzen, R.D. Ballard, K. Green, D. Williams, A. Bainbridge, K. Crane, and T.H. Van Andel. 1979. Submarine thermal springs on the Galapagos Rift. Science 203:1073-1083. Craig, H., and J.E. Lupton. 1981. Helium-3 and mantle volatiles in the ocean and in the oceanic crust. In: C. Emiliani (ed.). The Sea, Vol. 7, The Oceanic Lithosphere. J. Wiley and Sons, New York, pp. 391-428. Craig, H., J.A. Welhan, K.R. Kim, R. Poreda, and J.E. Lupton. 1981. Geochemical studies of the 21°N EPR hydrothermal fluids. EOS: Trans. Am. Geophys. Union 61:992. Edmond, J.M., C. Measures, R. McDuff, L.H. Chan, R. Collier, B. Grant, L.I. Gordon, and J.B. Corliss. 1979. Ridge-crest hydrothermal activity and the balances of the major and minor elements in the ocean: The Galapagos data. Earth Planet. Sci. Lett. 46:1-18.

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Edmond, J.M., K.L. Von Damm, R.E. McDuff, and C.I. Measures. 1982. Chemistry of hot springs on the East Pacific Rise and their effluent dispersal. Nature 297:187-191. Edmonds, H.N., and J.M. Edmond. 1995. A three-component mixing model for ridge crest hydrothermal fluids. Earth Planet. Sci. Lett. 134:53-67. Elderfield, H., and A. Schultz. 1996. Mid-ocean ridge hydrothermal fluxes and the chemical composition of the ocean. Ann. Rev. Earth Planet. Sci. 24:191-224. Fatton, E., G. Marien, C. Pachiaudi, M. Rio, and M. Roux. 1981. Fluctuations de l'activitie des sources hydrothermales oceaniques (Pacifique Est, 21°N) enregistrees lors de la croissance des coquilles de Calyptogena magnified (lamellibranche,Vesicomyidae) par les isotopes stables du carbone et de l'oxygene. C. R. Acad. Sci. Ser. Ill 293:701-706. Fouquet, Y., U. Von Stackelberg, J.-L. Charlou, J. Erzinger, P.M. Herzig, R. Muhe, and M. Wiedicke. 1993. Metallogenesis in back-arc environments: The Lau Basin. Econom. Geol. 88:2122-2153. Froelich, P.N., M.L. Bender, and G.R. Heath. 1977. Phosphorus accumulation rates in metalliferous sediments on the East Pacific Rise. Earth Planet. Sci. Lett. 34:351-359. German, C.R., and M.V Angel. 1995. Hydrothermal fluxes of metals to the oceans: A comparison with anthropogenic discharge. In: L.M. Parson, C.L. Walker, and D.R. Dixon (eds.). Hydrothermal Vents and Processes. Geol. Soc. Spec. Publ. 87:365-372. Ginster, U., M.J. Mottl, and R.P. Von Herzen. 1994. Heat flux from black smokers on the Endeavour and Cleft Segments, Juan de Fuca Ridge. J. Geophys. Res. 99: 4937-4950. Haberstroh, PR., and D.M. Karl. 1989. Dissolved free amino acids in hydrothermal vent habitats of the Guaymas Basin. Geochim. Cosmochim. Acta 53:2937-2945. Hart, S.R., and J. Blusztajn. 1998. Clams as recorders of ocean ridge volcanism and hydrothermal vent field activity. Science 280:883-886. Herzig, P., M. Hannington, B. Mclnnes, P. Stoffers, H. Villinger, R. Seifert, R. Binns, and T. Liebe. 1994. Submarine volcanism and hydrothermal venting studied in Papua, New Guinea. EOS: Trans. Am. Geophys. Union 75:513-515. Johnson, H.P., and V. Tunnicliffe. 1985. Time-series measurements of hydrothermal activity on northern Juan de Fuca Ridge. Geophys. Res. Lett. 12:685-688. Johnson, K.S., C.L. Beehler, CM. Sakamoto-Arnold, and J.J. Childress. 1986. In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science 231:1139-1141. Johnson, K.S., J.J. Childress, and C.L. Beehler. 1988a. Short-term temperature variability in the Rose Garden hydrothermal vent field: an unstable deep-sea environment. Deep-Sea Res. 35:1711-1722. Johnson, K.S., J.J. Childress, R.R. Hessler, CM. Sakamoto-Arnold, and C.L. Beehler. 1988b. Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep-Sea Res. 35:1723-1744. Johnson, K.S., J.J. Childress, C.L. Beehler, and CM. Sakamoto. 1994. Biogeochemistry of hydrothermal vent mussel communities: the deep-sea analogue to the intertidal zone. Deep-Sea Res. 41:993-1011. Kadko, D. 1993. An assessment of the effect of chemical scavenging within submarine hydrothermal plumes upon ocean geochemistry. Earth Planet. Sci. Lett. 120:361-375. Kadko, D., J. Baross, and J. Alt. 1995. The magnitude and global implications of

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hydrothermal flux. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 446-466. Karl, D.M. 1995. Ecology of free-living, hydrothermal vent microbial communities. In: D.M. Karl (ed.). The Microbiology of Deep-Sea Hydrothermal Vents. CRC Press, New York, pp. 35-124. Kelley, D.S., and J.R. Delaney. 1987. Two-phase separation and fracturing in midocean ridge gabbros at temperatures greater than 700°C. Earth Planet. Sci. Lett. 83:53-66. Killingley, J.S., W.H. Berger, K.C. Macdonald, and W.A. Newman. 1980. 18O/16O variations in deep-sea carbonate shells from the Rise hydrothermal field. Nature 288:218-221. Lilley, M.D., J.A. Baross, and L.I. Gordon. 1983. Reduced gases and bacteria in hydrothermal fluids: the Galapagos Spreading Center and 21°N east Pacific Rise. In: P.A. Rona, K. Bostrom, L. Laubier, and K.L. Smith (eds.). Hydrothermal Processes at Seafloor Spreading Centers, Plenum Press, New York, pp. 441-449. Lilley, M.D., D.A. Butterfield, E.J. Olson, J.E. Lupton, S.A. Macko, and R.E. McDuff. 1993. Anomalous CH4 and NH 4 + concentrations at an unsedimented mid-ocean-ridge hydrothermal system. Nature 364:45-47. Little, S.A., K.D. Stolzenbach, and J.E Grassle. 1988. Tidal current effects of temperature in diffuse hydrothermal flow: Guaymas Basin. Geophys. Res. Lett. 15:1491-1494. Lupton, J.E. 1995. Hydrothermal plumes: Near and far field. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geological Monograph 91, Am. Geophys. Union, Washington, DC, pp. 317-346. Lupton, J.E., and H. Craig. 1981. A major helium-3 source at 15°S on the East Pacific Rise. Science 214:115-127. Millero, F.J., S. Hubinger, M. Fernandez, and S. Garnett. 1987. Oxidation of H2S in seawater as a function of temperature, pH and ionic strength. Environ. Sci. Technol. 21:439-443. Mills, R.A., and H. Elderfield. 1995. Hydrothermal activity and the geochemistry of metalliferous sediment. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 393-407. Mottl, M.J., G. Wheat, E. Baker, N. Becker, E. Davis, R. Feely, A. Grehan, D. Kadko, M. Lilley, G. Massoth, C. Moyer, and F. Sansone. 1998. Warm springs discovered on 3.5 Ma oceanic crust, eastern flank of the Juan de Fuca Ridge. Geology 26:51-54. Murray, J., and A.F. Renard. 1891. Report on Deep-Sea Deposits. Challenger Expedition Reports, 3, Her Majesty's Stationery Office, London. Roux, M., M. Rio, and E. Fatton. 1985. Clam growth and thermal spring activity recorded by shells at 21°N. Bull. Biol. Soc. Wash. 6:211-221. Seewald, J.S., and WE. Seyfried, Jr. 1990. The effect of temperature on metal mobility in subseafloor hydrothermal systems: Constraints from basalt alteration experiments. Earth Planet. Sci. Lett. 101:388-403.

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Seyfried, W. E., and K. Ding. 1995. Phase equilibria in subseafloor hydrothermal systems: A review of the role of redox, temperature, pH and dissolved Cl on the chemistry of hot spring fluids at mid-ocean ridges. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC pp. 248-272. Seyfried, W.E., M.E. Berndt, and J.S. Seewald. 1988. Hydrothermal alteration processes at mid-ocean ridges: Constraints from diabase alteration experiments, hotspring fluids, and composition of he oceanic crust. Can. Mineral. 26:787-804. Smith, K.L., Jr. 1985. Deep-sea hydrothermal vent mussels: Nutritional state and distribution in the Galapagos Rift. Ecology 66:1067-1080. Tunnicliffe, V., M. Bostros, M.E. deBurgh, A. Dinet, H.P. Johnson, S.K. Juniper, and R.E. McDuff. 1986. Hydrothermal vents of Explorer Ridge, northeast Pacific. Deep-Sea Res. 33:401-412. Tunnicliffe, V., A.G. McArthur, and D. McHugh. 1998. A biogeographic perspective of the deep-sea hydrothermal vent fauna. Adv. Mar. Biol. 34:353-442. Van Dover, C.L., E.Z. Szuts, S.C. Chamberlain, and J.R. Cann. 1989. A novel eye in "eyeless" shrimp from hydrothermal vents of the Mid-Atlantic Ridge. Nature 337:458-460. Van Dover, C.L., J.R. Cann, C. Cavanaugh, S.C. Chamberlain, J.R. Delaney, D. Janecky, J. Imhoff, J.A. Tyson, and the LITE Workshop Participants. 1994. Light at deep-sea hydrothermal vents. EOS: Trans. Am. Geophys. Union 75:44-45. Van Dover, C.L., G.T. Reynolds, A.D. Chave, and J.A. Tyson. 1996. Light at deep-sea hydrothermal vents. Geophys. Res. Lett. 23:2049-2052. Von Damm, K.L. 1995. Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 222-247. Von Damm, K.L., J. Edmond, C.I. Measures, and B. Grant. 1985. Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California. Geochim. Cosmochim. Acta 49:2221-2237. Von Damm, K.L., J.L. Bischoff, and R.J. Rosenbauer. 1991. Quartz solubility in hydrothermal seawater; an experimental study and equation describing quartz solubility for up to 0.5 M NaCl solutions. Am. J. Sci. 291:977-1007. Von Damm, K.L., S.E. Oosting, R. Kozlowski, L.G. Buttermore, D.C. Colodner, H.N. Edmonds, J.M. Edmond, and J.M. Grebmeier. 1995. Evolution of East Pacific Rise hydrothermal vent fluids following a volcanic eruption. Nature 375:47-50. Von Damm, K.L., L.G. Buttermore, S.E. Oosting, A.M. Bray, D.J. Fornari, M.D. Lilley, and W.C. Shanks III. 1997. Direct observation of the evolution of a seafloor "black smoker" from vapor to brine. Earth Planet. Sci. Lett. 149:101-111. Welhan, J.A. 1988. Origins of methane in hydrothermal systems. Chem. Geol. 71:183-198. Wilcock, W.S.D. 1998. Cellular convection models of mid-ocean ridge hydrothermal circulation and the temperature of black smoker fluids. J. Geophys. Res. 103:25852596.

Hydrothermal Plumes As hydrothermal fluids exit a black-smoker orifice, they rise buoyantly, drawing in cold water to make a widening column of turbulent eddies full of black hydrothermal precipitates ("smoke"). The effect is the same as that of smoke from a factory stack on a cold day and follows the same physical models. Because it rises in a stratified ocean, the plume (plate II, top right panel) eventually reaches a level of neutral buoyancy where it spreads laterally and is carried away by deep ocean currents. An exception to this may eventually be found in the Arctic, where the ocean is likely to be unstratified during at least some portions of the year. Plumes are important as zones of chemical reaction between vent fluids and seawater, as habitat and resource for microorganisms and zooplankton, and as advective mechanisms for chemical fluxes and dispersal stages of vent biota. Plumes have also become the first-order means of remote detection of hydrothermal activity on the seafloor. 4.1 ANATOMY OF A BLACK-SMOKER PLUME 4.1.1 Orifice The orifice of black-smoker chimneys varies in dimension, but is typically on the order of 10 cm diameter or less, except when the chimney has been broken off by submersible manipulators for fluid or mineral sampling. Clear, high-temperature fluids exit from the orifice and within centimeters quickly mix with ambient seawater. Mixing results in rapid precipitation of small flakes of iron sulfides and development of particle-rich "black smoke." Temperature gradients are at their most extreme at the throat of a vent, where horizontal gradients can reach > 350°C cm" 1 . These are the most extreme temperature gradients that occur anywhere within the biosphere of our planet. A temperature probe moved horizontally into hydrothermal fluids as they exit still reads ambient temperatures (~1-2°C) within millimeters of the visible boundaries of the hydrothermal fluid, because the rising fluid constantly draws cold seawater into the turbulent plume. Mixing with seawater also rapidly cools the plume, although the vertical gradient of tempera-

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Figure 4.1. Schematic diagram of the buoyant plume illustrating entrainment of ambient seawater by vortices on the boundary of the rising plume. At time Tu horizontal shear causes formation of a wavelike disturbance. At subsequent time intervals, the wave rolls up against the boundary, engulfing ambient seawater, and then pairs with another wave to engulf an even larger sample of ambient seawater. Vectors at the top of the plume indicate the relative velocities of inner and outer portions of the plume. From Lupton 1995 (after Turner 1986). ture is not so extreme as the horizontal gradient. Temperatures as low as 10°C are recorded within 2 - 3 m above vent orifice.

4.1.2 Buoyant Plume As the thermal plume rises above the orifice of a vent, shear flow at the boundary between the buoyant fluids and ambient seawater generates turbulent eddies, which produce rapid mixing. Where adjacent black smokers occur close to one another (tens of meters), their fluids will become entrained into a single plume. The buoyant plume ascends through the densitystratified water column, entraining cold water as it rises (fig. 4.1), until it reaches a height where it is neutrally buoyant. Plumes are diluted by a factor of 103 in the first 5-10 m above the orifice and by another order of magnitude by the time they become neutrally buoyant (Lupton et al. 1985; Feely et al. 1994). The vertical velocity of the plume and buoyancy decrease while

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101

the radius increases during the ascent. Rise heights of plumes are typically 150-200 m, although ambient currents and unusual characteristics of the venting fluids (e.g., high-chlorinity vent fluids derived from phase separation and segregation) can reduce the total rise height of the plume. The maximum height of rise of a typical plume is reached in less than an hour. The rise height of a plume is used as a measure of buoyancy flux (which in turn is related to heat flux from a given vent), based on models that include information about the local density gradient (Turner 1973; Lupton et al. 1995). 4.1.3 Effluent Layer Once the plume rises to a height of neutral density, it spreads out laterally to form the effluent layer or neutrally buoyant plume. Multiple buoyant plumes from individual black smokers may converge above the bottom (plate II, top right panel) to form a single effluent layer. Effluent layers have distinctive hydrographic, optical, and chemical characteristics and a spatial scale that can extend from tens to thousands of kilometers, and can be readily detected and sampled from surface ships. Effluent layers act as integrators of thermal and chemical flux from source fields and their characteristics are important as indicators of the location and frequency of hydrothermal activity along ridge segments. Lupton et al. (1985) provided the first characterization of the near-field effluent layer in the northeast Pacific overlying the Main Endeavour hydrothermal field, noting a 0.05°C temperature excess with a corresponding positive salinity anomaly and reduced density gradient (fig. 4.2). The temperature anomaly derives from the hot vent water. The salinity excess is attributed to upward transport of ambient seawater through entrainment since, in the deep Pacific, salinity is higher at greater depths. In the deep Atlantic, the salinity gradient decreases with depth. Through entrainment during plume rise in the Atlantic, the effluent layer acquires a lower salinity than the surrounding water. It is also colder; by the time all of the injected heat has been lost by mixing, the plume is still buoyant because it has entrained so much lower-salinity seawater at depth. When density equilibrium is finally achieved in the Atlantic, the effluent layer is stabilized at a lower temperature and salinity than the surrounding water (fig. 4.3; Speer and Rona 1989). Optical anomalies associated with the effluent layer derive from the enriched particulate load generated by most hydrothermal systems and are detected using instruments that measure light scattering. Unlike conservative hydrographic tracers, optical anomalies are nonconservative and depend on the balance between particulate production and loss through physical, chemical, and biological processes occurring within the plume. Chemical anomalies in the effluent layer include dissolved manganese,

Density (a 2 ) 36.80 •

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o Temperaiture (

o

1.9-

%

\

1.8 -

1

1.7 .

36.84

36.88

36.

Cr 2 34.62 -

15

34.60 -

CO

34.58 34.56 36.84

36.88

I 36.92

OV

Figure 4.2. Hydrographic characteristics (density, salinity, and temperature) of the effluent layer of a Pacific hydrothermal plume. A. Vertical hydrographic profile. The black smoker was located at —2200 m. The effluent layer is marked by excess potential temperature (B) and salinity (C) vs. potential density (a 2 ) relative to the linear mixing trend of nonhydrothermally influenced deep water. From Lupton et al. 1985.

103

HYDROTHERMAL PLUMES

Temperature ;S

Salinity

36003700. Salinity Temperature Nephels

34.910 2.70 2.40

34.930 2.81 2.51

34.950 2.93 2.63

34.970 3.04 4.74

Figure 4.3. Vertical profile through the effluent plume within 50 m of TAG in the Atlantic. Note the decrease in temperature and salinity associated with the increased plume particulates (measured as nephels) in the plume effluent layer. From Rudnicki and Elderfield 1992. iron, methane, and helium-3 (fig. 4.4). Because these compounds are typically enriched by 107 in vent fluids, they are often useful as long-distance tracers. For example, 3He contours emanating westward from the ridge axis at 15°S on the East Pacific Rise over a distance of more than 2000 km were one of the first indicators of the large-scale influence of ridge-crest processes on the global ocean (Lupton and Craig 1981; see chapter 3.8). Chemical transformations in the buoyant plume are dominated by sorption and scavenging processes, with enrichments of silica, phosphorus, vanadium, manganese, iron, copper, zinc, and arsenic by factors of 20 or more relative to deep-ocean suspended matter (Lilley et al. 1995). Most of the hydrothermally derived iron is precipitated as iron sulfides in the first centimeters to meters of rise of the buoyant plume (Rudnicki and Elderfield 1993). These small, platelike sulfide particles start to oxidize rapidly as they rise; soon

104

CHAPTER 4

1700

2200 0.00 0.05 Temperature Anomaly °C

0.36 0.48 Light Attenuation 1/m

0

2e-13 3He crrPg-1(STP)

0 50 Manganese nmol kg*1

0

400 Methane nmol kg"1

0 400 Radon d.p.m. per 100 kg

Figure 4.4. Typical water-column profiles of temperature, light attenuation, 3He, manganese, methane, and radon anomalies in an effluent-plume layer over the Endeavour hydrothermal site on the Juan de Fuca Ridge. From Rosenberg et al. 1988. after they have reached the neutrally buoyant height, they have all been transformed to iron oxyhydroxide particles. As the iron oxy hydroxides form, other elements are adsorbed from seawater in a conservative manner (e.g., oxyanions such as vanadium or arsenic; Feely et al. 1991; German et al. 1991a), are scavenged from seawater (e.g., rare earth elements; German et al. 1991a), or form particles, which either sink or dissolve (e.g., copper or zinc; German et al. 1991b). Adsorption of nutrients such as phosphorus onto iron oxyhydroxides can have a significant impact on local oceanic concentrations. Kadko et al. (1990) developed a method of determining plume age based on the ratio of 222Rn to 3He. 3He is stable and inert (nonreactive). 222Rn decays with a half-life of 3.85 d, is inert, and is found in high concentrations in hydrothermal fluids. The 222Rn/3He ratio decreases only as a function of plume age. This radon clock is useful for establishing uptake rates of nonconservative constituents. Using this approach, methane was found to have a residence time of 11 d in the effluent plume. 4.2 MEGAPLUMES Large-scale, episodic release of hydrothermally altered seawater is associated with volcanic eruptions on the seafloor. These plumes, driven by sudden, catastrophic release of heat, rise above the steady-state effluent layers of hydrothermal fields to heights of 800 m above the seafloor (fig. 4.5). Such "megaplume" events are characterized in addition by their large size (up to 20 km or more in diameter, 600 m thick) and their ephemerality (detectable over periods on the order of weeks to months).

105

HYDROTHERMAL PLUMES 1400-

240046.2

46.3

46.6

Latitude (°N)

Figure 4.5. Temperature anomalies on the CoAxial Segment (Juan de Fuca Ridge) immediately following a volcanic eruption. Steady-state black-smoker plumes are evident at —1900-2200 m. Two event plumes (megaplumes) are observed above the steady-state plumes (at -1500-2000 m). From Lupton et al. 1995. Megaplumes were initially documented by Baker et al. (1987) during a 1986 water column survey of the effluent layers overlying the crest of the Juan de Fuca Ridge. The large amount of excess heat (1017 J) contained in the 1986 megaplume observations led Baker et al. to suggest that the plume was created during a volcanic eruption. The link between megaplumes and seafloor volcanism was tightened in 1993 when acoustic signals received at moored hydrophones indicated that a dike-injection event was occurring at the CoAxial site on the Juan de Fuca Ridge (Fox et al. 1995; see chapter 10.4.2). Along-axis water column surveys in the vicinity of the putative eruption within days of the acoustic event located an ephemeral megaplume (Baker et al. 1995b), and subsequent visual observations confirmed that an eruption had taken place beneath the seafloor (Embley et al. 1995). Megaplumes likely do not contribute a major fraction of the hydrothermal input to the deep ocean, since 3He, a conservative tracer of hydrothermal inputs, is maximum not at megaplume depths but at depths consistent with disbursement by the effluent layer (Lupton et al. 1995). Megaplumes may be important in vertical mixing between deep and intermediate water, and megaplumes on shallow ridge segments or in weakly stratified oceans (such as the Arctic) could rise all the way to the surface. The specific mechanism of megaplume generation remains controversial (see Wilcock 1997). Models include direct interaction of hot volcanics and seawater at their interface

106

CHAPTER 4

(Baker et al. 1987; Butterfield et al. 1997; Palmer and Ernst 1998), abrupt release of trapped fluids at depth (Cann and Strens 1989), increased permeability of upflow zones (Lowell and Germanovich 1995), and fluid expansion in a depressurized reaction zone (Wilcock 1997). 4 3 SPATIAL AND TEMPORAL DISTRIBUTIONS OF PLUMES The discovery of deep-sea vent fields in the late 1970s and early 1980s relied heavily on visual observations combined with geological insight regarding likely target segments of mid-ocean ridges. In recent years, the efficiency with which new vent fields are located has been improved through prospecting techniques that rely on optical and chemical detection of hydrothermal plumes and precision navigation to trace the plumes back to their seafloor source. Plume mapping has also proven extremely useful in providing synoptic views of hydrothermal output along entire ridge segments, including timevariant properties. A series of six annual surveys of the Cleft Segment of the Juan de Fuca Ridge in the Northeast Pacific (Baker 1994) shows that hydrothermal discharge was concentrated over two hydrothermal fields (fig. 4.6). The initial 1986 survey of Cleft coincided with a megaplume event at the more northern of the two fields. The southern site always generated a weaker signal. The maximum steady-state discharge was observed in 1989, with plume contours noticeably diminished in scale by 1991. One of the more extensive plume surveys to date maps hydrothermal discharge along the superfast-spreading southern East Pacific Rise (Baker and Urabe 1996). Hydrothermal output may be greater here than anywhere else on the planet, with significant hydrothermal plumes covering more than 60% of the survey area, which extended from 13.5° to 18.5°S (fig. 4.7), and with one 150 km region supporting an uninterrupted plume. In contrast, a systematic survey of the slow-spreading Reykjanes Ridge extending south of Iceland from 63° to 57°N detected only a single, previously known, hydrothermal site (German et al. 1994). 4.3.1 Relationship between Plume Distributions and Geophysical Parameters Plume incidence is a function of mean spreading rate, with highest plume incidences on superfast ridges and lowest incidence on slow-spreading ridge systems (fig. 4.8; Baker et al. 1995a). This relationship may be particularly relevant for understanding global biogeographic patterns of vent faunas (see chapter 11), although German et al. (1998) show that hydrothermal activity occurs on slow-spreading ridges at a higher frequency than predicted by

107

HYDROTHERMAL PLUMES 1900-

2400 - Y

1

t

t

i

i

1900-

i

1987

24001900-

1990

2400-^

1991

1900-

2400' 44.5

44.7

i

44.9

r

45.1

Latitude (°N) Figure 4.6. Time-series study of water-column thermal anomalies along the Cleft Segment of the Juan de Fuca Ridge, 1986-1991. Triangles note locations of known vent sites. A megaplume is evident in the 1986 profile at 1800 m, above the steadystate plume. From Baker 1994.

spreading rate alone. These authors implicate technically generated permeability as a mechanism for creating sustained hydrothermalism under conditions of low magmatic budgets. The spreading rate-plume incidence relationship derives from average plume incidences along multiple first-order (inter-transform fault) segments for a given spreading rate. Baker (1996) finds no correlation between plume incidence and spreading rate at the second-order or higher segmentation scales along intermediate- to superfast-ridge systems (fig. 4.9). At secondorder segmentation scales (intra-transform fault), cross-sectional area and net

CHAPTER 4

2800 18.5

17.5

16.5

15.5

14.5

13.5

Latitude (°S) Figure 4.7. Light attenuation anomalies ( = hydrothermal plumes) along the superfast-spreading southern East Pacific Rise. Significant hydrothermal plumes extend along —60% of the survey area. From Baker and Urabe 1996.

/u —

'c/T

Southern East Pacific Rise %

60-

X

0 50O)

•D

ir

40-

Northern East Pacific R i s e ^ ^

& 0

O 30c0 O

_c

9^Juan de Fuca Ridge

20-

Plui

0

10-

j f Mid-Atlantic Ridge • 0

1

20

Reykjanes Ridge

1

40

1

60

1

80

1

100

1

120

1

140

1

160

1

180

Full Spreading Rate (mm yr 1 ) Figure 4.8. Relationship between plume incidence (percentage of axis length overlain by a significant plume) and average spreading rate for five ridge systems. From Baker et al. 1995.

109

HYDROTHERMAL PLUMES

1008060 40 20 40

100. 8060.

60

80 100 120 140 Spreading Rate (mm yr1)

160

0.2 0.3 0.4 Net Elevation (km)

0.5

0.6

I I I 2 3 4 2 Cross-Sectional Area (km )

I 5

6

• SEPR QNEPR AJDFR

40. 20. 0.

I 1

Figure 4.9. Relationships between plume incidence and three geological parameters for 14 segments on three intermediate- to superfast-spreading systems: (A) segment spreading rate; (B) net ridge-axis elevation ( ± standard deviation); (C) cross-sectional area of ridge axis ( ± standard deviation). From Baker 1996.

elevation are the best predictors of hydrothermal activity (fig. 4.9; Baker 1996). These correlates complement earlier observations of robust magmatic budgets associated with broadly swollen ridge crests (Macdonald and Fox 1988). According to the model of Baker (1996), episodes of dike intrusion on magmatically starved segments are uncommon in both space and time, and hydrothermal activity as detected by plume incidence is uniformly low. Segments with a relatively high magma supply rate have a greater probability of episodic dike intrusion, leading to plume incidences that are higher and more variable. On slow-spreading centers, cross-sectional area and net elevation are inap-

110

CHAPTER 4

propriate indices of hydrothermal activity at the intra-transform scale. Baker (1996) notes that gravity lows arising from focused accretion of young ocean crust are associated with major Mid-Atlantic Ridge vent fields and segment bathymetric minima. This association was not upheld by further plume surveys on the Mid-Atlantic Ridge. An alternative model by German et al. (1996) emphasizes the role that permeability may play in localization of hydrothermal activity on slow-spreading ridge systems; five of seven hydrothermal plumes on the Mid-Atlantic Ridge between 36°N and 37°N occur in highly tectonized areas of cross-cutting faults at or near the ends of secondorder ridge segments. These faults presumably allow seawater to penetrate to the deeper heat sources characteristic of slow-spreading ridges (e.g., Purdy et al. 1992). 4.4 PLUME-DRIVEN MESOSCALE CIRCULATION 4.4.1 Plume Vortices Modeling of the dynamics of hydrothermal plumes suggests that they are capable of forcing circulation on a variety of spatial and temporal scales. Plume vortices predicted by models of Helfrich and Speer (1995) may be significant mesoscale processes in the dispersal or retention of particles (including larvae of vent invertebrates) along ridge axes. In these models, the effluent layer of a hydrothermal plume spreads laterally owing to an unbalanced pressure gradient and the influence of bottom currents. Rotation of the earth retards lateral spreading, forming a horizontal vortical (geostrophic) flow at the spreading level. This circulation is unstable, leading to shedding of vortices from a steady-state plume. These can eventually be transmitted away from the ridge crest at a scale of about one kilometer. The first in situ confirmation of the existence of plume vortices came from tracking a neutrally buoyant float (at 2200 m) in a megaplume (layered at 1800-2400 m) above the southern Juan de Fuca Ridge (Lupton et al. 1998). The float track followed several large anticyclonic circles (mean diameter = 6.6 km) during a 60 d interval (fig. 4.10). Total track length was 127 km, but the net distance traveled was only 8.8 km. 4.4.2 Advection and Downwelling Ambient seawater entrained in the rising plume must be replaced by a slow radial inflow. In basin situations, such as may be found on the Mid-Atlantic Ridge, where the effluent layer lies below the height of the steep axial-valley walls, this radial inflow may drive downwelling of less dense seawater into the near-bottom layers (Helfrich and Speer 1995).

111

HYDROTHERMAL PLUMES 42.76

42.72 -

42.68 •

42.! 127.04

-126.96

-126.88

-126.80

Longitude (°W) Figure 4.10. Track of a neutrally buoyant float at 2200 m in a megaplume above the Juan de Fuca Ridge. Five-day increments are noted, beginning with day 1 at the launch point and ending on day 56 at the surface point. From Lupton et al. 1998.

4.4.3 Basin-Scale Circulation The question of whether hydrothermal activity could drive basin-scale circulation was raised when Lupton and Craig (1981) documented the huge 3He anomaly extending westward from the ridge axis at 15°S on the East Pacific Rise (see chapter 3.8). This plume is indicative of a westward flow of currents at depths of 2000-3000 m, contrary to the predictions of classical geostrophic models (Stommel and Arons 1960). The presence of the plume does not confer causality—other forces besides hydrothermal forcing could drive the westward circulation. Recent modeling efforts, however, suggest that geothermal forcing could in fact overcome the opposing eastward and poleward thermohaline circulation under some conditions (Speer 1989). Hydrographic data from the 15°S area are consistent with circulation actively driven by ridge-crest hydrothermal flux and inconsistent with other possibilities.

112

CHAPTER 4

4.5 DIFFUSE-FLOW PLUMES Although low-temperature diffuse flow has been indicted as a major source of heat and chemical flux in vent systems, the behavior of diffuse-flow plumes has not been properly studied. According to Helfrich and Speer (1995), diffuse sources should tend to be rapidly mixed and trapped near the bottom and merge quickly into ambient circulation. Because the geometry of low-temperature diffuse flows with respect to black smokers varies depending on the nature of a given vent field, in some instances the diffuse flows may be ground-hugging and horizontally advective, while in others they may be entrained into high-temperature plumes and advected vertically and then horizontally. Since vent invertebrate communities are restricted to relatively low-temperature environments, the fate of these diffuse-flow water parcels is critical to understanding the fate of invertebrate dispersive stages.

REFERENCES Baker, E.T. 1994. A 6-year time-series of hydrothermal plumes over the Cleft segment of the Juan de Fuca Ridge. J. Geophys. Res. 99:4889-4904. Baker, E.T. 1996. Geological indexes of hydrothermal venting. J. Geophys. Res. 101:13741-13753. Baker, E.T., and T. Urabe. 1996. Extensive distribution of hydrothermal plumes along the superfast-spreading East Pacific Rise, 13°50'-18°40'S. J. Geophys. Res. 101:8685-8695. Baker, E.T., G.J. Massoth, and R.E. Feely. 1987. Cataclysmic hydrothermal venting on the Juan de Fuca Ridge. Nature 329:149-151. Baker, E.T., C.R. German, and H. Elderfield. 1995a. Hydrothermal plumes over spreading-center axes: Global distributions and geological inferences. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geological Monograph 91, Am. Geophys. Union, Washington, DC, pp. 47-71. Baker, E.T, G.J. Massoth, R.A. Feely, R.W. Embley, R.E. Thomson, and B.J. Burd. 1995b. Hydrothermal event plumes from the Co Axial seafloor eruption site, Juan de Fuca Ridge. Geophys. Res. Lett. 22:147-150. Butterfield, D.A., I.R. Jonasson, G.J. Massoth, R.A. Feely, K.K. Roe, R.E. Embley, J.F. Holden, R.E. McDuff, M.D. Lilley, and J.R. Delaney. 1997. Seafloor eruptions and evolution of hydrothermal fluid chemistry. Philos. Trans. R. Soc. Lond. A 355:369-386. Cann, J.R., and M.R. Strens. 1989. Modeling periodic megaplume emissions by black smoker systems. J. Geophys. Res. 94:12227-12237. Embley, R.W., W.W. Chadwick, Jr., I.R. Jonasson, D.A. Butterfield, and E.T. Baker. 1995. Initial results of the rapid response to the 1993 Coaxial Event: Relationships between hydrothermal and volcanic processes. Geophys. Res. Lett. 22:143-146. Feely, R.A., J.H. Trefry, G.J. Massoth, and S. Metz. 1991. A comparison of scaveng-

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ing of phosphorus and arsenic from seawater by hydrothermal oxyhydroxides in the Atlantic and Pacific Oceans. Deep-Sea Res. 38:617-623. Feely, R.A., J.F. Gendron, E.T. Baker, and G.T. Lebon. 1994. Hydrothermal plumes along the East Pacific Rise, 8°40' to ll°50'N: Particle distribution and composition. Earth Planet. Sci. Lett. 128:19-36. Fox, C.G., W.E. Radford, R.P. Dziak, T.-K. Lau, H. Matsumoto, and A.E. Schreiner. 1995. Acoustic detection of a seafloor spreading episode on the Juan de Fuca Ridge using military hydrophone arrays. Geophys. Res. Lett. 22:131-134. German, C.R., A.P. Fleer, M.P. Bacon, and J.M. Edmond. 1991a. Hydrothermal scavenging at the Mid-Atlantic Ridge: Radionuclide distribution. Earth Planet. Sci. Lett. 105:170-181. German, C.R., G.P. Klinkhammer, and J.M. Edmond. 1991b. Hydrothermal scavenging at the Mid-Atlantic Ridge: Modification of trace element dissolved fluxes. Earth Planet. Sci. Lett. 107:101-114. German, C.R., J. Briem, C. Chin, M. Danielsen, S. Holland, R. James, A. Jonsdottir, E. Ludford, C. Moser, J. 6lafsson, M.R. Palmer, and M.D. Rudnicki. 1994. Hydrothermal activity on the Reykjanes Ridge: The Steinaholl vent-field at 63°06'N. Earth Planet. Sci. Lett. 121:647-654. German, C.R., L.M. Parson, and HEAT Scientific Team. 1996. Hydrothermal exploration at the Azores Triple-Junction: Tectonic control of venting at slow-spreading ridges? Earth Planet. Sci. Lett. 138:93-104. German, C.R., E.T. Baker, C. Mevel, K. Tamaki, and the FUJI Scientific Team. 1998. Hydrothermal activity along the southwest Indian Ridge. Nature 395:490-493. Helfrich, K.R., and K.G. Speer. 1995. Oceanic hydrothermal circulation: Mesoscale and basin-scale flow. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geological Monograph 91, Am. Geophys. Union, Washington, DC, pp. 347-356. Kadko, D., N.D. Rosenberg, J.E. Lupton, R. Collier, and M. Lilley. 1990. Chemical reaction rates and entrainment within the Endeavour Ridge hydrothermal plume. Earth Planet. Sci. Lett. 99:315-335. Lilley, M.D., R.A. Feely, and J.H. Trefry. 1995. Chemical and biochemical transformations in hydrothermal plumes. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geological Monograph 91, Am. Geophys. Union, Washington, DC, pp. 369-391. Lowell, R.P., and L.N. Germanovich. 1995. Dike injection and the formation of megaplumes at ocean ridges. Science 267:1804-1807. Lupton, J.E. 1995. Hydrothermal plumes: Near and far field. In: S.E. Humphris, R.A. Zierenberg, L.S. Mullineaux, and R.E. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, and Geochemical Interactions. Geological Monograph 91, Am. Geophys. Union, Washington, DC, pp. 317-346. Lupton, J.E., and H. Craig. 1981. A major helium-3 source at 15°S on the East Pacific Rise. Science 214:13-18. Lupton, J.E., J.R. Delaney, H.P. Johnson, and M.K. Tivey. 1985. Entrainment and vertical transport of deep-ocean water by buoyant hydrothermal plumes. Nature 316:621-623.

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Lupton, J.E., E.T. Baker, GJ. Massoth, R.E. Thomson, BJ. Burd, D.A. Butterfield, R.W. Embley, and G.A. Cannon. 1995. Variations in water-column 3He/heat ratios associated with the 1993 Co Axial event, Juan de Fuca Ridge. Geophys. Res. Lett. 22:155-159. Lupton, J.E., E.T. Baker, N. Garfield, GJ. Massoth, R.A. Feely, J.R Cowen, R.G. Greene, and T.A. Rago. 1998. Tracking the evolution of a hydrothermal event plume with a RAFOS neutrally buoyant drifter. Science 280:1052-1055. Macdonald, K.C., and RJ. Fox. 1988. The axial summit graben and cross-sectional shape of the East Pacific Rise as indicators of axial magma chambers and recent volcanic eruptions. Earth Planet. Sci. Lett. 88:119-131. Palmer, M.R., and G.R. Ernst. 1998. Generation of hydrothermal megaplumes by cooling of pillow basalts at mid-ocean ridges. 393:643-645. Purdy, G.M., L.S.L. Kong, G.L. Christenson, and S.C. Solomon. 1992. Relationship between spreading rate and seismic structure of mid-ocean ridges. Nature 355:815817. Rosenberg, N.D., J.E. Lupton, D. Kadko, R. Collier, M.D. Lilley, and H. Pak. 1988. Estimation of heat and chemical fluxes from a seafloor hydrothermal vent field using radon measurements. Nature 334:604-607. Rudnicki, M.D., and H. Elderfield. 1992. Theory applied to the Mid-Atlantic Ridge hydrothermal plumes: The finite-difference approach. J. Vole. Geoth. Res. 50:161— 172. Rudnicki, M.D., and H. Elderfield. 1993. A chemical model of the buoyant and neutrally buoyant plume above the TAG vent field, 26°N, Mid-Atlantic Ridge. Geochim. Cosmochim. Acta 57:2939-2957. Speer, K.G. 1989. The Stommel-Arons model and geothermal heating in the South Pacific. Earth Planet. Sci. Lett. 95:359-366. Speer, K.G., and P.A. Rona. 1989. A model of an Atlantic and Pacific hydrothermal plume. J. Geophys. Res. 94:6213-6220. Stommel, H.M., and A.B. Arons. 1960. On the abyssal circulation of the world ocean. Part II. An idealized model of the circulation and amplitude in oceanic basins. Deep-Sea Res. 6:217-233. Turner, J.S. 1973. Buoyancy Effects in Fluids. Cambridge University Press, New York, 367. Turner, J.S. 1986. Turbulent entrainment: The development of the entrainment assumption, and its application to geophysical flow. J. Fluid Mech. 173:431-471. Wilcock, W.S.D. 1997. A model for the formation of transient event plumes above mid-ocean ridge hydrothermal systems. J. Geophys. Res. 102:12109-12121.

Microbial Ecology Free-living microorganisms are important elements of vent systems as competitors and sinks for inorganic sulfur and other reduced compounds and as producers of particulate organic carbon for a variety of zooplankton and benthic organisms. They are of academic interest for their metabolic diversity and their ability to inhabit extreme thermal and chemical environments, and they are of commercial interest for the exploitative value of their enzyme systems in biotechnology industries. Hydrothermal vent ecosystems are celebrated as sites where chemosynthetic microbial processes predominate. Chemosynthesis is also well known as a significant microbial process in shallow water, yet none of the prodigious biomass we associate with deep-sea hydrothermal vents is found in chemosynthetic regimes of coastal waters and sediments. The explanation lies in an examination of inputs of chemical energy. To place vent microbial processes in context, consider the naturally occurring microbial sulfur cycle in seawater: organic material in sediments is partially consumed (oxidized) by sulfate-reducing bacteria in the absence of (or at very low levels of) oxygen, that is, under anaerobic conditions. Seawater sulfate of the sediment porewaters is converted to sulfide in this process: SO 4 2 " + 2[CH2O] -> S 2 ~ + 2CO2 + 2H2O.

(a)

Sulfide (S 2 ~ or its related species H2S and HS~) is a primary product of microbial sulfate reduction. When this sulfide becomes exposed to an oxygenated environment (aerobic conditions) either within the upper layers of sediment or at the interface with seawater, it is subject to microbial oxidation: S 2 ~ + CO2 + O 2 + H2O -> SO 4 2 ~ + [CH2O].

(b)

The oxidative portion of the sulfur cycle generates organic compounds (CH2O) from inorganic substrates and is a form of primary production. Because chemical energy—derived from the oxidation of sulfide—drives the synthesis of organic carbon, this microbial process (b) is called chemosynthesis. In the marine microbial sulfur cycle, there is no net gain of organic material, since organic carbon must be oxidized to generate the sulfide that fuels production of new organic carbon.

116

CHAPTER 5

Solar Energy

CO2 + H2O

[CH2O] + O2

Photosynthesis

CO2 + H2O + H2S + O2 —*. [CH2O] + H2SO4

C0 2 + 6H2

I

[CH2O] + CH4 + 3H2O

Aerobic Chemosynthesis

Anaerobic Chemosynthesis

Geothermal Energy

Figure 5.1. Carbonfixationin photo- and chemosynthesis and the role of oxygen in deep-sea hydrothermal vents. From Jannasch 1995b. At hydrothermal vents, sulflde originates from the geochemical interaction of seawater and hot rock deep within the ocean crust. This effectively shortcircuits the microbial sulfur cycle, allowing a net gain of organic material through oxidation of sulfide and accumulation of new biomass. While chemosynthesis is a "sloppy" term (redefined with more care below), it is a purposeful construct for analogy to photosynthesis: CO2

H2O

[CH2O] + O 2

(c)

Both chemosynthesis and photosynthesis generate organic carbon from inorganic carbon, but chemosynthesis uses chemical energy while photosynthesis uses energy from sunlight. Note that the free O 2 in (b) is derived from seawater and ultimately originates from photosynthetic processes (fig. 5.1). Equations (b) and (c) are simplistic in that they represent autotrophy as a single-step process. Of course, the actual biochemical transformations are complex, with light or chemical energy used to generate reducing power

MICROBIAL ECOLOGY

117

through production of NADPH coupled to a carbon-fixation cycle (typically the Calvin-Benson cycle). Microbiologists first observed chemosynthesis more than 100 years ago (Winogradsky 1887, cited in Jannasch 1995b). It is a process that is well known but was considered to play no significant, quantitative role in the carbon cycle of the photosynthetically dominated Earth's surface. As Jannasch (1995a) and others have emphasized, the biogeochemical significance of chemosynthesis emerged only upon discovery of deep-sea hydrothermal vent systems, where photosynthetic production of plant organic biomass at the base of the food web is hypothesized to be virtually replaced by chemosynthetic production of microbial organic carbon. 5.1 AUTOTROPHIC ORGANISMS AT VENTS 5.1.1 Nomenclature Metabolic processes of living organisms have three basic requirements: a source of energy, a source of carbon, and a source of electrons. The energy source may be light (photo-) or chemical (chemo-); the source of carbon may be inorganic (auto-) or organic (hetero-); the electron donors may also be inorganic (litho-) or organic (organo-). By this nomenclature, photosynthesis [equation c] is more thoroughly described as photoautolithotrophy (where H2O is the inorganic electron donor); chemosynthesis [equation b] is chemoautolithotrophy (where, for example, inorganic sulfide and oxygen yield the energy, and sulfide also serves as the electron donor). Animals are chemoheteroorganotrophs. Microorganisms are metabolically facile. Virtually all combinations of the three basic metabolic requirements are known in the microbial world, and any one type of microorganism may switch between metabolic modes or simultaneously use multiple modes to become a mixotroph. A classification of major physiological groups of bacteria is given in table 5.1. 5.1.2 Aerobic and Anaerobic Chemoautotrophy at Vents The sulfide oxidation reaction [equation (b)] above is one example of a chemoautotrophic aerobic process, requiring O 2 as an electron acceptor. The electron donor can be a variety of oxidizable substrates (table 5.2), including various forms of reduced sulfur (e.g., sulfide, elemental sulfur, thiosulfate), iron, manganese, and ammonia. The primary electron donor available for aerobic microbial oxidation in hydrothermal fluids is hydrogen sulfide. Energy yields (theoretical free energies; table 5.2) from aerobic chemosynthetic processes are relatively large; the presence of free oxygen in hydrothermal

118

CHAPTER 5

TABLE 5.1. Classification of major physiological groups of bacteria on the basis of electron donors and major carbon sources used in metabolism Type of Metabolism

Carbon Source

Electron Donor

Phototrophy Photoautolithotroph Photoheterolithotroph Photoautoorganotroph Photoautoorganotroph Photoheteroorganotroph Photomixotrophb

co 2

organic substrate CO2 CO organic substrate mixed: CO 2 and organic

Chemotrophy0 Chemoautolithotroph

H2O, H2S, S°, H 2 H2O, H2S, S°, H 2 organic substrate organic substrate mixed: inorganic and organic

CO2

reduced inorganic substrate (e.g., H2, H2S, S 2 O 3 2 ~, S°, N H 4 + , F e 2 + ) reduced inorganic substrate (e.g., H2, H2S, S 2 O 3 2 ~, S°, N H 4 + , F e 2 + ) organic substrate organic substrate mixed: inorganic and organic

a

TYI

. L - 1

A.

.L

Chemoheterolithotroph

organic substrate

Chemoautoorganotroph Chemoheteroorganotroph Chemomixotrophd

CO2 organic substrate mixed: CO2 and organic

From Karl 1995. a Phototrophy refers to processes dependent on light energy. b Photomixotrophs (also referred to as facultative photolithoautotrophs) can simultaneously use mixtures of inorganic and organic electron donors, or mixtures of inorganic and organic carbon sources, or mixtures of both. Simultaneous use of photo- and chemotrophic modes of metabolism is also possible. c Chemotrophy refers to processes dependent on chemical energy. d Chemomixotrophs (also referred to as facultative chemoautolithotrophs) can simultaneously use mixtures of inorganic and organic electron donors, or mixtures of inorganic and organic carbon sources, or mixtures of both. Simultaneous use of photo- and chemotrophic modes of metabolism is also possible.

ecosystems is critical for the generation of the large amounts of biomass observed (Jannasch 1995b). In the absence of free oxygen, a variety of anaerobic microbial chemosynthetic processes can be identified. The principal electron donor under anaerobic conditions at vents is hydrogen, and anaerobic hydrogen-oxidizing microorganisms have been isolated from hydrothermal systems. Nitrate, sulfate, sulfur, and carbon dioxide serve as electron acceptors. The majority of anaerobic chemosynthetic microorganisms are extremely thermophilic or hy-

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TABLE 5.2. Potential aerobic and anaerobic chemosynthetic processes at vents Condition Aerobic

Electron Donor 2

Electron Acceptor

Free Energy

ss°

S2O3 2 -

o2 o2

Fe2 + Mn 2 + NH 4 + CH4 H2 H2 H2 H2 H2

02

o2

-797 -585 -952 -44.3 -68.2 -275 -810 -237 -239 -98.3 -38.1 -34.7

Anaerobic

02 02 02 02

NO32-

s°

SO 4 2 ~

co2

m°r

Metabolic Process sulfide oxidation sulfur oxidation thiosulfate oxidation iron oxidation manganese oxidation nitrification methane oxidation hydrogen oxidation denitrification sulfur reduction sulfate reduction methanogenesis

From Jannasch 1995b. a In kJ/mol electron donor, calculated for complete oxidation and normalized conditions: pH 7, 25°C, 1 atm.

perthermophilic, growing at temperatures of 70-110°C. Hydrogen oxidation is a high-energy-yielding process, since many hydrogen oxidizers can directly reduce NAD(P) rather than relying on reverse electron transport. But because hydrogen concentrations in vent fluids are relatively low compared to sulfide and because oxygen is readily available in large areas of suitable microhabitat, primary production by anaerobic microorganisms is assumed to be much lower than that generated by aerobic chemoautotrophic processes (Jannasch 1995b). Taking thennodynamic and geochemical constraints into account, McCollom and Shock (1997) suggest that microbial processes other than sulfide oxidation contribute fewer than 4% of the calories available per kilogram of vent fluid. Methanotrophy The term autotrophy classically refers to the use of CO 2 as the primary inorganic-carbon substrate that is reduced and fixed to organic carbon. In methanotrophy, methane (CH4) is used as both the electron donor and the carbon substrate. Methane is usually an organic compound (although it may be "inorganic" if synthesized abiotically). Thus, methanotrophy is distinguished as a kind of hybrid between autotrophic and heterotrophic processes. Methane can be abundant in hydrothermal fluids, and methanotrophy is also likely to be important in nonhydrothermal reducing environments elsewhere in the deep sea (see chapter 12).

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5.1.3 Carbon Dioxide Fixation Energy-yielding chemosynthetic reactions are biochemically coupled to the reduction of CO 2 to organic carbon. The enzymatic CO2-fixation cycle used by many types of chemosynthetic bacteria is identical to the Calvin-Benson cycle used by plants. Autotrophic activity is often inferred in microbial populations by the presence of the Calvin-Benson enzyme d-ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBPCase or "Rubisco"). This pathway, however, is not used by all autotrophs; it is notably absent from all Archaea and many strict anaerobes (Karl 1995). 5.1.4 Mixotrophy The neat packaging of microorganisms into metabolic types based on electron donors, acceptors, etc. (tables 5.1, 5.2) is a convenience for describing the potential metabolic processes present at vents, but this presentation may be very misleading in terms of what microorganisms are actually doing in situ. Microorganisms are likely to take advantage of whatever conditions and processes will optimize their survival and reproduction. Hence, while an organism might be autotrophic in the laboratory, it may well use a facultative approach in its natural environment and assimilate simple organic compounds whenever they are available; heterotrophic metabolism is a highenergy-yielding process. Various kinds of mixotrophy may well be the rule, rather than the exception, for the growth of chemoautolithotrophic bacteria in nature (Karl 1995). 5.1.5 Net Chemoautotrophic Production in Free-Living Hydrothermal-Vent Microorganisms Karl (1995) makes the strong case that the chemoautotrophic nature of hydrothermal systems has not been rigorously tested. Evidence for chemoautotrophic production at vents comes from a variety of techniques, including assessment of community structure and diversity by enrichment, gene sequence, and biomarker compounds; measurements of diagnostic enzyme activities; carbon dioxide assimilation studies; and stable isotope methods. Each of these techniques has potential problems and limitations in demonstrating the chemoautotrophic nature of free-living microbial communities at vents (Karl 1995). Alternatives to Chemoautotrophy Substantial evidence suggests that there is locally enriched free-living bacterial biomass at vents compared to non-vent deep-sea environments. The ac-

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TABLE 5.3. Three hypotheses that account for elevated, free-living bacterial biomass at vents Chemoautotrophy

Organic Thermogenesis

Detrital Thermal Alteration

geothermal heat

geothermal heat

sunlight

reduced inorganic compounds

simple organic compounds (de novo)

refractory organic compounds

chemosynthetic bacterial primary production

heterotrophic bacterial primary production

geothermal alteration simple organic compounds heterotrophic bacterial secondary production

cepted explanation is that chemoautotrophy accounts for this elevated biomass. Two alternative hypotheses put forth by Karl (1995) suggest that this elevated biomass of free-living microorganisms might be maintained through heterotrophic metabolism of locally generated organic compounds (table 5.3). These alternative hypotheses (organic thermogenesis and detrital thermal alteration), outlined below, differ in the origin of the organic materials. ORGANIC THERMOGENESIS HYPOTHESIS. Hydrothermal systems are locales for abiotic organic chemical synthesis because they are systems with high thermal energy and are strongly reducing. Relatively simple organic molecules such as thiocyanate and glycine may be generated abiotically by thermal synthesis as seawater reacts with hot rock at depth (Ingmanson and Dowler 1980). Heterocyclic sulfur compounds are synthesized de novo from formaldehyde and sulfur in hydrothermal fluids (Simoneit 1995). A variety of organosynthetic processes are plausible, including Wohler synthesis of urea from ammonium cyanate and Fischer-Tropsch synthesis of aliphatic compounds (alkanes, alkenes, etc.) from carbon monoxide, a catalyst (e.g., iron), and water (Simoneit 1995). These organic compounds may be used directly by heterotrophic microorganisms, which would in effect be primary producers. DETRITAL THERMAL ALTERATION HYPOTHESIS. Old, refractory organic carbon is ubiquitous in oceanic waters and sediments and is relatively unusable by microorganisms. As refractory carbon is drawn into hydrothermal circula-

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tion cells, the carbon is thermally degraded to petroleum hydrocarbons (e.g., Simoneit 1995) and volatile fatty acids (Martens 1990), which are then available to heterotrophic microorganisms where the fluids exit the seafloor. While net chemoautotrophic production by free-living microorganisms at vents is generally accepted as a given, alternative modes of production have not been rigorously examined and eliminated. Note that none of these hypotheses need operate exclusively of the others. 5.2 ECOLOGY OF FREE-LIVING MICROORGANISMS 5.2.1 Microbial Habitats Hydrothermal systems offer environmental gradients of chemistry and temperature to suit a diverse array of obligate and facultative physiologies and tolerances in free-living microorganisms (fig. 5.2). Major habitat distinctions within vent fields are typically made on the basis of oxygen availability (aerobic vs. anaerobic, with microaerobic gradients in between); temperature (superthermophilic [> 115°C], hyperthermophilic [80-115°C], thermophilic [50-80°C], mesothermophilic [10-50°C], and psychrophilic [ 1 cm thick mats cannot be supported by molecular diffusion of essential substrates in stagnant waters. Beggiatoa sp. requires steep, op-

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Figure 5.10. Beggiatoa sp. mat on sediment at Guaymas Basin (length of mat area is approximately 60 cm). Photo courtesy of J.F Grassle.

posed microgradients of sulfide and oxygen (M0ller et al. 1985). Gundersen et al. (1992) report that on a microhabitat scale, hot pore-water fluids rise up through sediments adjacent to Beggiatoa sp. mats, creating an irregular downwelling of oxygen-rich water through the mats (fig. 5.11). It is the irregular, pulsatory nature of the downwelling flow that is critical in allowing sulfide-rich fluid beneath the mat to be intermittently refreshed with oxygen-rich seawater. 5.2.8 The Link between Chemoautotrophic and Photosynthetic Processes Jannasch and Mottl (1985) wrote that the most significant discovery related to deep-sea vents is "the dependence of entire ecosystems on geothermal (terrestrial) rather than solar energy." This intentionally provocative statement and the ensuing correspondence (Boyle 1985; Pirie 1985) provide an

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6 54 32

B

Shimmering Hot Water

Hot ' Pore-Fluid

25

50 Time (s)

Measuring Point

100

75

Beggiatoa Mat

Cold ' '. Thermal Convection 10 cm

Figure 5.11. A. Temperature record 1 cm above a Beggiatoa sp. mat in Guaymas Basin, illustrating the time-variant nature of the warm-water efflux. B. Small convection cells and fluctuating hydrothermal flow combine to maintain a deep (1-2 cm) zone of mixing of oxygen and hydrogen sulfide. From Gundersen et al. 1992.

important lesson in biochemical energetics. The statement of Jannasch and Mottl refers to sulfide and other reduced compounds emitted in vent fluids as energy sources for microbially mediated primary production. But sulfide by itself provides no energy. It is the oxidation of sulfide that yields energy; both oxidant and reductant are required. The oxidant is primarily molecular oxygen in the surrounding seawater, which is ultimately the result of photosynthetic processes. Thus, vent ecosystems do depend on solar energy to provide one-half of the reactants in the oxidation-reduction, energy-yielding process. In the event of a catastrophic darkening of the earth's surface (the nuclear winter scenario; Ehrlich et al. 1983), Jannasch and Mottl (1985)

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suggest that "the chance of survival of such ecosystems is the highest of any community in the biosphere." This is true, as long as the store of free oxygen in the oceans outlasts the catastrophe.

5.3 A SEARCH FOR IN SITU BACTERIAL PHOTOSYNTHESIS The deep sea is envisioned as an unilluminated environment, but ambient light emitted by high-temperature venting fluids (see chapter 3.5) contradicts this notion. Van Dover et al. (1996) report that the photon flux emitted by high-temperature fluids is sufficient to support facultative photosynthetic bacteria using bacteriochlorophyll or other long-wavelength light-capturing pigment systems. Yurkov and Beatty (1998) describe an obligately aerobic, anoxygenic photosynthetic bacterium isolated from black-smoker plumes on the Juan de Fuca Ridge (fig. 5.12). These organisms are facultative phototrophs under culture and contain a bacteriochlorophyll a pigment with an in vitro absorption maximum at 867 nm. Nisbet et al. (1995) propose that longwavelength light emitted by vents may have been the selective force for the evolution of phototaxis in bacteria and subsequent development of rudimentary photosynthetic capabilities. The potential for novel photobiochemical adaptations to exploit low light levels and the possibility that vents serve as a refuge for relict populations of primitive phototrophs (Van Dover et al. 1994) make the search for and characterization of vent photo trophic microorganisms a compelling area of vent research.

5.4 MICROBIAL GENESIS OF HYDROTHERMAL MINERAL DEPOSITS Most surfaces of hydrothermal-vent fields exposed to mixing of vent fluids and ambient seawater are covered with iron and manganese oxide crusts in which microorganisms are embedded (Jannasch and Mottl 1985). Juniper and Tebo (1995) explore in detail the possibility that these crusts are microbially generated (and destroyed), but are forced to conclude that there is insufficient evidence to implicate microorganisms, given the potential for rapid, spontaneous oxidation of iron (Fe 2 + ) in the presence of oxygen at near neutral pH and the rapid, inorganic coprecipitation of iron and manganese. Based on fossilization of bacterial filaments with silver-rich minerals, Zierenberg and Schiffman (1990) propose that microorganisms can be responsible for selective precipitation of precious metals from hydrothermal fluids.

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Figure 5.12. Phototrophic bacteria isolated from near high-temperature vents on the Juan de Fuca Ridge. A. Groups of cells showing polymorphism and presence of flagella. B. Cells connected by an unknown material (indicated by arrows). C. Thin section of a Y-shaped cell preceding division to form three daughter cells. D. A later stage of F-cell division. Scale bars: (A) 1 ^m; (B) 400 nm; (C) and (D) 200 nm. From Yurkov and Beatty 1998.

5.5 MICROBIAL EXPLOITATION OF PARTICULATE SULFIDES Most interest in growth of microorganisms at deep-sea hydrothermal vents has focused on microbial oxidation of dissolved sulfide and other reduced sulfur compounds emitted in vent fluids. A large amount of this sulfide precipitates as metal sulfides (including pyrite, FeS2, pyrrhotite, Fe 5 S 6 _Fe 16 S 17 , chalcopyrite, CuFeS2, and sphalerite, ZnS), creating ubiquitous deposits at

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active and relict hydrothermal sites. Oxidation of metal sulfides by marine and terrestrial chemoautotrophic bacteria generally takes place at low pH values. For this reason, poly metallic sulfide deposits in the deep sea, where pH values are near neutral, have been presumed to be unfavorable for growth of metal-sulfide-oxidizing bacteria. Wirsen et al. (1993) demonstrated that nonacidophiles isolated from vent sulfides were capable of autotrophic growth through oxidation of sulfide minerals. Further work by Eberhard et al. (1995) confirmed that polymetal sulfides (especially chalcopyrite) support the growth of chemolithotrophic bacteria at near neutral pH, although this growth is only 5-10% of the corresponding values obtained when thiosulfate is used as a substrate. They found evidence to suggest that the presence of cells on the mineral surfaces stimulates the release of oxidizable sulfur substrates. Massive sulfide deposits on the seafloor may thus serve as a potential source of electrons for chemosynthetic production of biomass in the deep sea long after hydrothermal activity has ceased. This kind of microbial production might account for the relatively rich biomass of heterotrophic invertebrates (brachiopods, tunicates, anemones, sponges, etc.) observed on inactive massive sulfide deposits in the Escanaba Trough (Gorda Ridge; Van Dover et al. 1990). 5.6 BIOTECHNOLOGY The potential for biotechnological exploitation of microbial species isolated from hydrothermal vents is considerable (Jannasch 1995a). Bacterial bioremediation of waste sulfides from industrial processes has already been developed on a laboratory scale (Jannasch et al. 1992), with the resultant sulfate harmlessly returned to the marine environment. Bacterial biomass generated by this process can be used as a food source for aquaculture or fermentation into synfuels. Mariculture of symbiont-bearing invertebrate bivalves has also been suggested as a means of treating industrial sulfur waste (Berg and Alatalo 1984). Hyperthermophilic bacteria offer the prospect of a broad range of thermostable enzymes, including polymerases useful in polymerase chain reactions (PCR) and other molecular techniques, as well as amylases, glucosidases, proteases, etc. (Kelly et al. 1994; Prieur 1997). Resistance to heat denaturation also ensures resistance to other denaturing influences such as detergents and organic solvents (Cowan 1995). Microorganisms living at meso- and thermophilic temperatures in the sediments of the Guaymas Basin vent sites are involved in transformation and decomposition of the freshly cracked organic material. One microorganism, a sulfate reducer, has been isolated and shown to use a specific fraction of the alkane series during its production of sulfide (Reuter et al. 1994).

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The search for Archaea and bacteria with novel biochemical attributes is an entire field of marine research. Deep-sea hydrothermal vents with varied and often extreme microhabitats are certain to be repositories of exploitable microbes (Pennisi 1997).

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Van Dover, C.L., G.T. Reynolds, A.D. Chave, and J.A. Tyson. 1996. Light at deep-sea hydrothermal vents. Geophys. Res. Lett. 23:2049-2052. Walsby, A.E. 1983. Bacteria that grow at 250°C. Nature 303:381. Winn, CD., D.M. Karl, and G.J. Massoth. 1986. Microorganisms in deep-sea hydrothermal plumes. Nature 320:744-746. Wirsen, CO., J.H. Tuttle, and H.W. Jannasch. 1986. Activities of sulfur-oxidizing bacteria at the 21°N East Pacific Rise vent site. Mar. Biol. 92:449-456. Wirsen, CO., H.W. Jannasch, and S.J. Molyneaux. 1993. Chemosynthetic microbial activity at Mid-Atlantic Ridge hydrothermal vent sites. J. Geophys. Res. 98:96939703. Woese, CR. 1987. Bacterial evolution. Microbiol. Rev. 51:221-271. Yurkov, V., and J.T. Beatty. 1998. Isolation of obligately aerobic anoxygenie photosynthetic bacteria from "Black Smoker" plume waters of the Juan de Fuca Ridge in the Pacific Ocean. Appl. Environ. Microbiol. 64:337-341. Zierenberg, R.A., and P. Schiffman. 1990. Microbial control of silver mineralization at a seafloor hydrothermal site on the Northern Gorda Ridge. Nature 348:155-157.

6 Symbiosis Deep-sea vent ecosystems are distinguished from their shallow-water and terrestrial hydrothermal counterparts by the hugely successful associations between chemoautotrophic, symbiotic microorganisms and their macroinvertebrate hosts. The discovery and characterization of these symbioses, related below, is a tale of exploration and biological insight worthy of underscore and exclamation. Equally remarkable are the numerous anatomical, physiological, and biochemical adaptations of hosts in support of their symbionts' requirements, discussed in the subsequent chapter. 6.1 DISCOVERY When dense populations of bivalves were first reported from deep-sea camera-sled transects along the Galapagos Spreading Center, they were described as suspension-feeding organisms dependent on local enrichments in food associated with hydrothermal plumes (Lonsdale 1977). According to this argument, entrainment of bottom water by the rising, buoyant hydrothermal plume creates local convection cells where in-flowing bottom currents deliver food to animals (fig. 6.1). This thesis was further developed by Enright et al. (1981), who added the condition of repetitive reentrainment of advected material through cycles of suspension and sinking as a means of concentrating particles within the near-vent field. Lonsdale (1977) also suggested an alternative: by analogy to microbial production in terrestrial hydrothermal systems, chemoautotrophic production by bacteria might be significant in the diet of the putative suspension feeders. This idea was reinforced by Corliss et al. (1979), who measured high concentrations of sulfide and bacteria in the first samples collected from warm-water vents during an Alvin dive series coincident with the preparation of Lonsdale's 1977 report. Support for the chemoautotrophic hypothesis came quickly through the use of stable isotope techniques. The relative abundance of the naturally occurring isotopes of carbon, 13C and 12C (expressed as 813C in units of per mil, or %o\ see chapter 8.2.1), is controlled in part by the uptake kinetics of the enzymes involved in biosynthetic pathways of autotrophic organisms.

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CHAPTER 6

Buoyant Plume precipitating Manganese as it Mixes with Oxygenated Seawater

Rain of Fine-Grained Metalliferous Sediment

Clams Straining Food Out of Inflow Current

Adjacent Water Entrained by Plume

Fissure and Nearby Joints

Figure 6.1. Illustration of an initial hypothesis for the source of nutrition for clams at a hydrothermal vent. From Lonsdale 1977. Marine phytoplankton have 813C values typically around —15 to —2\%c (Gearing et al. 1984). Consumers of this photosynthetically derived carbon retain the carbon isotope composition of their diet; where two putative diets differ in their isotope composition, isotope analysis of the consumer reveals the source diet (see chapter 8). Consider the deep-sea vent scenario: if vent bivalves consume organic material derived from surface primary production, their isotopic composition should fall within the —15 to —21%c range. Rau and Hedges (1979) found that carbon isotope values for a vent mussel (Bathymodiolus thermophilus) collected from Galapagos vents averaged ~ - 33%c, well outside the range of values expected for a diet of organic material derived from the euphotic zone and consistent with limited evidence for more negative carbon isotopic compositions in organic material produced through bacterial chemoautotrophic production. The inference: vent mussels are dependent on in situ nonphotosynthetic production by suspended microorganisms. 6.1.1 Sustenance of Gutless Tubeworms The initial concept of suspended chemosynthetic microorganisms as primary sustenance for the concentrated invertebrate biomass found at vents was challenged by the discovery of mouthless, gutless, giant tubeworms up to 2 m in length (Riftia pachyptila, plate II, middle row, left panel; Corliss et al. 1979). Southward et al. (1979) had suggested that smaller pogonophoran relatives of the giant tubeworms might rely on uptake of dissolved organic material (e.g., amino acids), but they found uptake rates inadequate to ac-

SYMBIOSIS

147

count for the metabolic rates observed in pogonophorans. Reliance on dissolved organic material seemed even more problematic for the Galapagos tubeworms. The riddle of the nutrition of giant tubeworms was solved by 1981 through converging evidence for bacterial chemoautotrophic endosymbionts from microscopy (Cavanaugh et al. 1981), enzymology (Felbeck 1981), and stable isotope data (Rau 1981). Elemental sulfur inclusions (an oxidized form of sulfide) in the highly vascularized trophosome of the tubeworm, an organ that fills much of the cavity of the trunk of the worm (see chapter 7.2), were suggestive of microbially mediated sulfide oxidation, making the trophosome the target for a search for symbiotic microorganisms. Light and scanning microscopy of trophosome tissue revealed lobes densely packed with prokaryotic cells (figs. 6.2 and 6.3; Cavanaugh et al. 1981). Lipopolysaccharide, a constituent of gram-negative bacterial cell walls, was found in abundance in trophosome tissue, providing further evidence for a prokaryotic component to this tissue (Cavanaugh et al. 1981). Felbeck (1981) assayed trophosome tissues for enzymes indicative of sulfur metabolism (rhodanese, APS-reductase, ATP-sulfurylase) and diagnostic for the Calvin-Benson cycle (ribulose-l,5-bisphosphate carboxylase [Rubisco], ribulose 5-phosphate kinase). As outlined in chapter 5, sulfur chemoautotrophy is a two-step process involving production of ATP by oxidation of sulfide and fixation of inorganic carbon through a biosynthetic pathway (e.g., the Calvin-Benson cycle). Felbeck's enzyme assays in tubeworm trophosome tissue were all positive, with high activities. No activity for any of these enzymes was observed in control muscle tissue from tubeworms. Further evidence for autotrophic production was indirectly obtained by measuring activities of enzymes involved in assimilation of inorganic nitrogen, a process restricted to autotrophs. Stable isotope analysis of tubeworm tissues provided further evidence for a nonphotosynthetic diet in these gutless organisms (Rau 1981), although 813C values found in vent tubeworms (~ - ll%o) were very different from 813C values of vent bivalves (~ — 33%o). Explanations for the divergence of carbon stable isotope compositions in vent bivalves versus vent tubeworms, including effects of CO2 limitation and different forms of enzymes, are discussed in Robinson and Cavanaugh (1995). To date, no single explanation prevails. The combined observations of a bacteria-rich trophosome, the sulfide-oxidizing chemoautotrophic potential of trophosome tissues, and 813C values that cannot be reconciled with a diet of photosynthetically derived organic carbon led to the conclusion that the endosymbiotic bacteria are chemoautotrophic sulfide oxidizers that generate organic material from inorganic compounds delivered to the trophosome by the host vascular and coelomic

Branchial Filaments/Obturaculum

Trophosome

;

/

Opisthosome

Figure 6.2. Mosaic of longitudinal sections of a small tubeworm (Ridgeia piscesae) showing the lobular trophosome tissue that fills the saclike body. In situ hybridization identifies the symbiont 16S rRNA as black-staining granules. The detail shows that larger bacteria are concentrated toward the periphery of each lobe. From Cary et al. 1993.

149

SYMBIOSIS

Outer Membrane

Host Cell Membrane

5 :m Figure 6.3. A. Scanning electron micrograph of trophosome tissue from Riftia pachyptila showing the prokaryotic cells and a sulfur granule (lower right); photo by C. Wirsen in Jannasch 1984. B. Diagram of a tubeworm (host) cell (bold lines) containing intracellular bacteria. All bacteria in the trophosome are surrounded by a presumed host membrane (drawn here for only a few bacteria) either individually or in clusters, b = bacteria (not all are labeled); N = host cell nucleus. From Cavanaugh 1983a. systems. The bacteria in turn must transfer adequate amounts of this fixed organic material to the host for its nourishment. Once this bacterial symbiosis was recognized in Riftia pachyptila, the symbiont condition of pogonophoran tubeworms was quickly confirmed and generalized (Southward 1982).

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CHAPTER 6

6.1.2 Endosymbiotic Bacteria in Vent Mollusks Lonsdale's beds of "suspension-feeding bivalves" on the Galapagos Spreading Center were comprised of vesicomyid clams (Calyptogena magnified; plate III, middle row, left panel). Dense beds of mytilid mussels (Bathymodiolus thermophilus; plate III, bottom row, left panel) were also reported at Galapagos vents (Corliss et al. 1979). Detailed anatomical studies of the clams undertaken by Boss and Turner (1980) called into question their ability to filter-feed; the clams have a reduced filter-feeding apparatus and digestive system, manifest by a degenerate feeding groove on the ventral margin of the gills, small labial palps, and simple gut. They also have markedly enlarged, fleshy, vascularized gills. Felbeck et al. (1981) turned again to Rubisco enzyme assays to demonstrate the autotrophic potential of clams and mussels, this time exhibited only in gill tissues, while Cavanaugh (1983b) presented microscopic confirmation of the presence of bacterial endosymbionts in clam gill tissue. Further examples of bacterial chemoautotrophic symbioses were soon discovered in bivalves from shallow-water environments where sulfide and oxygen both occur, for example, bivalves in the families Solemyidae and Lucinidae from reducing sediments of coastal embayments and sewage outfalls (Cavanaugh 1983a; Felbeck 1983; Distel and Felbeck 1987). Fiala-Medioni (1984) and Le Pennec and Hily (1984) localized endosymbiotic bacteria in the gills of the vent bathymodiolid (mytilid) mussels as well as vesicomyid clams (fig. 6.4). In addition to vent clams and mussels, another vent bivalve type—a pectinid scallop that lives in the periphery of vent fields (Hessler et al. 1988)—also has bacterial endosymbionts in its primitive-looking, voluminous gills (Le Pennec et al. 1988b). Bacterial density is low and this scallop is likely to be less dependent on its symbiotic bacteria for nutrition than are other vent bivalve types. In hydrothermal systems of the western Pacific back-arc spreading systems (e.g., Mariana, Lau, Fiji, Manus), large gastropod mollusks may attain a dominant ecological role. Alviniconcha hessleri (family Provannidae) was the first gastropod shown to contain thiotrophic (sulfide-oxidizing) endosymbiotic bacteria in its gills (Stein et al. 1988). Ifremeria nautilei, another hydrothermal gastropod (family Provannidae) has also been shown to host thiotrophic bacteria (fig. 6.5). Morphological adaptations to endosymbionts in /. nautilei include 15-20 times more gill filaments than in aposymbiotic Provanna species and a stomach that is 1/10 the size (Windoffer and Giere 1997). 6.1.3 Episymbionts When vents on the Mid-Atlantic Ridge were discovered to be dominated by swarming masses of shrimp (Rimicaris exoculata; plate III, middle row, right

151

SYMBIOSIS

bl

\

Figure 6.4. Schematic illustration of bacterial endosymbionts of bathymodiolid mussels (Type I) and vesicomyid clams (Type II). In mussels, bacteria typically colonize only the apical part of gill-filament cells. In clams, bacteria are located throughout the host gill-filament cells, b = bacteria, n = nucleus, m = mitochondria, er = endoplasmic reticulum, L = lipids, Ls = lysosomes, bm = basal membrane, bl = blood lacuna, h = hemocyte, mv = microvilli. From Fiala-Medioni and Le Pennec 1987.

panel) that lacked endosymbionts, the model of high vent invertebrate biomass supported by the symbiont condition seemed to find an exception (Van Dover et al. 1988). As discussed in more detail in chapter 8, the swarming shrimp in fact support dense populations of chemoautotrophic episymbiotic bacteria that may contribute significantly to the nutrition of the adult animals. Episymbiont bacteria are also conspicuous on the backs of the Pompeii

152

CHAPTER 6

dorsal

ciliated epithelium

gland

bacteriocytes

bacteriocytes

ventral Figure 6.5. Schematic section through a gill filament of the gastropod Ifremeria nautilei. Endosymbiont-bearing bacteriocytes (zone 5) are the dominant host cell type. From Windoffer and Giere 1997.

SYMBIOSIS

153

worm Alvinella pompejana (Desbruyeres et al. 1985), on the epithelial gill surface of the vent limpet Lepetodrilis fucensis (de Burgh and Singla 1984), and on a variety of other vent invertebrates. Their significance in the nutrition of their hosts remains elusive. 6.2 METHANOTROPHIC SYMBIOSES Host-symbiont relationships found at hydrothermal vents on the Galapagos Spreading Center and East Pacific Rise emphasized the importance of chemoautotrophic production based on sulfide oxidation by thiotrophic endosymbiotic bacteria. Discovery of taxonomically and ecologically related invertebrates (tubeworms, vesicomyid clams, and bathymodiolid mussels) at cold seeps (see chapter 12), where both sulfide and methane are available as reduced compounds, quickly led to the discovery of methane-based endosymbioses in the bathymodiolid mussels (Childress et al. 1986; Cavanaugh et al. 1987). As in thiotrophic symbioses, methanotrophic endosymbionts of mussels are intracellular, housed in gill tissues, and cannot be grown in pure culture (Cavanaugh 1992). Methanotrophic endosymbionts have a distinctive morphology, with stacked intracytoplasmic arrays (fig. 6.6). Enzyme assays diagnostic of methylotrophic bacteria (especially methanol dehydrogenase) are used to confirm the methanotrophic activity of the endosymbionts, as are uptake experiments using 14C-labeled methane. Methane-based symbioses have also been discovered in a pogonophoran tubeworm from methane-rich sediments of the Danish slope of the central Skagerrak (Schmaljohann and Fliigel 1987) and in bathymodiolid mussels from hydrothermal vents on the Mid-Atlantic Ridge (Cavanaugh et al. 1992; Fiala-Medioni et al. 1996). 6.2.1 Dual Symbioses Dual symbiosis is an unusual condition in metazoans and is so far best known in mussels from chemosynthetic environments. Support of two metabolically distinct symbioses has obvious advantages to the host mussel in allowing it to adapt to spatially and temporally unpredictable or changing chemical environments. There may also be physiological or metabolic advantages in the coexistence of the symbionts through enhanced stability and reduced intraspecific competition. Vent mussels {Bathymodiolus puteoserpentis) from the Snake Pit vent site on the Mid-Atlantic Ridge host two phylogenetically distinct prokaryotic bacterial symbionts within their gill cells (Distel et al. 1995). The symbiont species are also morphologically distinct; the large morphotype (1.5-2.0 jxm diameter) contains complex stacked membranes characteristic of methanotrophic bacteria; the small morphotype (< 0.5 |mm diameter) lacks the stacked membranes (Cavanaugh

154

CHAPTER 6

ss

s^

^VS^-i**",^

Figure 6.6. Transmission electron micrograph of a methanotrophic endosymbiont (upper left) of a mytilid mussel (Bathymodiolus puteoserpentis) from the Mid-Atlantic Ridge showing the characteristic stacked lamellae. A sulfide-oxidizing bacterium is also highlighted (arrow pointing down). Scale bar = 0.5 |xm. From Cavanaugh et al. 1992.

et al. 1992; fig. 6.7). Enzymes characteristic of thiotrophic metabolism (Rubisco) and of methane assimilation (methanol dehydrogenase) are detectable in gill extracts of mussels containing both morphotypes of endosymbiotic bacteria (Cavanaugh et al. 1987, 1992; Fisher et al. 1993). More recently, physiological and immunological evidence for two distinct carbon fixation pathways in vent mussels has been demonstrated (Robinson et al. 1998). In situ hybridization of DNA probes for thioautotrophic and methanotrophic phylotypes cloned from mussel gill tissue map to the distribution patterns of small and large morphotypes, respectively (Distel et al. 1995). A second Mid-Atlantic Ridge mussel species also harbors dual symbionts (Bathymodiolus sp. from Lucky Strike; Fiala-Medioni et al. 1996), as do two other undescribed mussel species (Bathymodiolus spp.) from Gulf of Mexico seep sites (Florida Escarpment [Cavanaugh et al. 1987] and Alaminos Canyon [Fisher et al. 1993]). There are some indications that the large vent gastro-

SYMBIOSIS

155

Figure 6.7. Transmission electron micrograph of Bathymodiolus puteoserpentis gill tissue (lower magnification of the specimen in figure 6.6). One thiotrophic (small arrow) and one methanotrophic (large arrow) endosymbiont are highlighted; numerous endosymbiotic bacteria of both types are present in a single host cell, bl = blood space; 1 = lysosome-like body; m = mitochondria; n = bacteriocyte (host cell) nucleus. Scale bar = 3 |xm. From Cavanaugh et al. 1992.

156

CHAPTER 6

TABLE 6.1. Site-specific differences in carbon isotope composition and estimates of proportion of methanotrophs (of total endosymbionts) in the gills of the mussel Bathymodiolus sp.

Sintra Eiffel Tower

Mean h13C in Muscle (Range)

% Methanotrophs (C.I.)

-21.3 (-23.6, -15.7) - 30.7 ( - 32.9, - 28.9)

15 (12, 19) 6 (3, 9)

From Trask and Van Dover 1999. Stable isotope ratios were measured in 24 individuals per site; % methanotrophs was determiend for 5 individuals per site. C.I. = 95% confidence interval.

pods found at western Pacific vents (Alviniconcha hessleri and Ifremeria nautilei) may also support dual endosymbioses (Endow and Ohta 1989; Galchenko et al. 1992). The relative abundance of the dual symbionts should reflect the environmental availability of sulfide versus methane (Cavanaugh 1993). For mussels examined from the Snake Pit hydrothermal field on the Mid-Atlantic Ridge, the smaller thiotrophic morphotype is dominant, consistent with observations of the relative abundances of sulfide (5.9 mM; Campbell et al. 1988) and methane (100 |JLM; Charlou et al. 1987) in vent fluid from Mid-Atlantic Ridge vent sites. Relative abundances of methanotrophs and thiotrophs in mussels from two sites within the Lucky Strike vent field are site specific in a manner consistent with site-specific variations in their carbon stable isotope compositions (Trask and Van Dover 1999; table 6.1). Although separated by only 400 m, the Lucky Strike sites are fed by two distinct hydrothermal plumbing systems (Von Damm et al. 1998; M. Lilley, pers. comm.). More than one endosymbiont morphotype has been reported for vestimentiferan worms (e.g., Cavanaugh et al. 1981; de Burgh et al. 1989), but these morphotypes have been ascribed to pleomorphism of a single species. Naganuma et al. (1997), using 16S rDNA sequences and in situ hybridizations, identified two new endosymbionts belonging to the e-subdivision of the Proteobacteria in the tubeworm Lamellibrachia sp. from a methane seep. The metabolic roles of these e-proteobacterial endosymbionts are not known, but they are presumed to be involved in autotrophic production. 6.2.2 Methanotrophs in Sponges A recent addition to the cast of extraordinary nutritional symbioses in invertebrates is the finding of methanotrophs in carnivorous sponges reported from a mud volcano (seep) site in the Barbados Trench (Vacelet et al. 1995). Carnivory in sponges in itself is an oddity, since the basic sponge body plan, comprised of an aquiferous system pumped by special flagellated cells called choanocytes, is designed as an elaborate filtering device for retention of food

SYMBIOSIS

157

particles. Carnivorous sponges lack this aquiferous system. Instead, filaments with hook-shaped spicules passively capture and engulf small crustaceans, an adaptation that allows them to colonize the food-poor deep sea (Vacelet and Boury-Esnault 1995). A newly reported species of carnivorous sponge, Cladorhiza sp., grows in large bushes at > 4900 m depths at the mud volcanoes. Symbiotic bacteria with stacked membranes characteristic of methanotrophs were discovered in the somatic tissues of these sponges. Significant activities of methanol dehydrogenase and light stable carbon isotope values ( 50%o) support the idea that the endosymbionts are methanotrophs. Based on observations of symbionts associated with embryos, Vacelet and Boury-Esnault (1995) suggest direct transmission of endosymbionts between generations. 6.3 ADAPTIVE CHARACTERISTICS OF SYMBIOSIS Symbiotic associations between chemoautotrophic bacteria and marine invertebrates are now recognized to be widely distributed in nature (table 6.2; Cavanaugh 1994). The role of autotrophic symbionts in the nutrition of their hosts ranges from being the principal source for host species lacking a functional digestive system (e.g., tubeworms) to being an additional source for host species with functional guts (e.g., mussels, shrimp). In some species, symbionts may also play a significant role in sulfide detoxification, although this role is not well defined for any vent species (see chapter 7.6). Host physiological adaptations to the autotrophic symbiont condition are taken up in the next chapter. The host provides the symbiont population with a regulated supply of substrates required for chemosynthesis (e.g., sulfide, carbon dioxide, oxygen). Without the biochemical or physiological control of a eukaryotic host, the zone where sulfide and oxygen can coexist is spatially limited and temporally fluctuating. Taking a symbiocentric view, Cavanaugh (1994) describes this association between a eukaryote and its symbionts as "an adaptation by aerobic sulfur bacteria to 'bridge' oxic-anoxic interfaces." Cavanaugh's examples of eukaryote-symbiont bridges found in vent organisms include eukaryotic partners that can (1) move quickly to track fluctuating oxic/anoxic interfaces (alvinocarid shrimp); (2) take up substrates in the mixing zone of anoxic and oxic water and transport these substrates to remote endosymbionts (vestimentiferan tubeworms); or (3) use oxic and anoxic environments by segregating the uptake of oxygen and sulfide in different body parts (vesicomyid bivalves). The thioautotrophic condition in bivalves is at least 35 million years old, based on geological, biogeographical, and isotope characteristics of fossil paleo-seep communities (Campbell 1992; Goedert and Squires 1993). Phy-

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TABLE 6.2. Invertebrate-chemo(or methano)autotrophic symbioses

Host Taxonomy Porifera Family Cladorhizidae Nematoda Subfamily Stilbonematinae

Endo- or Episymbiont

Symbiont Location

Symbiont Autotrophic Condition

Adult Digestive System

endosymbiont

"sponge tissue"

methanotrophic

nonexistent

episymbiont

cuticle, intraepidermal

thiotrophic

functional

endosymbiont

intestinal intracellular

thiotrophic

functional

endosymbiont

gills

thiotrophic

nonfunctional

endosymbiont

gills

functional

Family Pectinidae Class Gastropoda: Family Provannidae

endosymbiont

gills

thio- and methanotrophic presumed thiotrophic

endosymbiont

gills

functional

Echiura Annelida Class Polychaeta Family Alvinellidae Class Oligochaeta Subfamily Phallodrilinae Vestimentifera Pogonophora

endosymbiont

intraepidermal

thio- and ?methanotrophic thiotrophic

episymbiont

dorsal surface

thiotrophic

functional

endosymbiont

subcuticular

thiotrophic

functional

endosymbiont endosymbiont

trophosome trophosome

thiotrophic thio- and methanotrophic

lost lost

episymbiont

branchial chamber

thiotrophic

functional

Mollusca Class Bivalvia: Family Vesicomyidae Family Mytilidae

Arthropoda Family Alvinocaridae

functional

functional

From references cited in text.

logenetic data on the relationship of thyasirid and lucinid symbionts within the Lucinacea suggest that the symbionts arose from a common chemoautotrophic ancestor; if so, this symbiosis must have been established before the divergence of these bivalve lineages, that is, about 250 Ma (Boss 1970). Symbiotic association of bivalves with thioautotrophic bacteria is thus an ancient phenomenon that influenced the course of evolution in these and possibly other bivalve lineages (Reid and Brand 1986; Distel et al. 1994). 6.4 HOST NUTRITION One of the more difficult issues regarding the symbiotic condition in vent organisms is the mechanism by which organic material generated by bacteria is delivered to the host. That such a mechanism exists is inferred from sev-

SYMBIOSIS

159

eral lines of circumstantial evidence, including the elimination or reduction of digestive systems in host invertebrates, the specialization of body systems to support endosymbionts, and habitat preferences for chemical milieus normally deemed inhospitable to eukaryotes (Fisher 1990). Direct physiological evidence for net CO 2 uptake (autotrophy) in vestimentiferan symbioses comes from respiration experiments that track the flux of total inorganic carbon dioxide (2CO2) using a dual pressure chamber design (Anderson et al. 1987). Childress et al. (1991) placed whole tubeworms in one chamber, with the second chamber serving as a control reservoir. The 2CO 2 flux in outflowing water was measured under varying sulfide concentrations. With no sulfide added, 2CO 2 flux is positive, indicating heterotrophic respiration of the worm/symbiont association. With increasing sulfide concentration, autotrophic metabolism by the symbionts results in XCO2 loss from the system (negative flux). Potential growth rates for the tubeworm/symbiont association, expressed as % organic carbon uptake per day relative to total organic carbon, were on the order of 1.4%, indicative of very rapid growth. A similar technique was used by Kochevar et al. (1992) to document functional autotrophy in methanotrophic mussels from a Gulf of Mexico seep. Mussel/symbiont associations produced —0.3 mol CO2 per mole of CH4 consumed, indicating that ~ 70% of the CH4 is presumably incorporated into organic compounds. Kochevar et al. (1992) suggest that these methane mussels may assimilate carbon at rates of more than 2% per day solely through methane fixation. This is greater than uptake rates measured by Childress et al. (1991) in Riftia pachyptila. Cary et al. (1988) provide direct evidence that an inorganic carbon source (methane) alone can support net shell growth in a mussel with methanotrophic gill symbionts from Gulf of Mexico hydrocarbon seeps, and infer from this observation that organic material has been contributed to the host's nutrition by the endosymbionts. Variable concentrations of methane provided as the sole carbon source to an array of mussels over a 74 d period resulted in correlated variations in daily growth rates (fig. 6.8), with a lag time of 2 d between exposure to methane and maximal growth rates at a given methane concentration (Cary et al. 1988). As these authors point out, methane supplies only carbon and energy to the host, presumably via the endosymbionts; other essential elements must be derived from other sources. Fisher (1990) reviews evidence for two methods by which symbionts might contribute this net carbon to the host: (1) symbionts can translocate organic material across their cell walls in a manner analogous to many algalinvertebrate symbioses; and (2) symbionts can be digested by the host. Rapid translocation of radioactively labeled fixed carbon from symbionts to host tissues (fig. 6.9) has been demonstrated in some invertebrate-bacterial symbioses (e.g., the bivalves Solemya reidi [Fisher and Childress 1986] and Loripes lucinalis [Herry et al. 1989]). In purified symbiont preparations from

160

CHAPTER 6

16' 12' 2 CD

8' 4. 0

B

_ 400-

1000 -800? .600 o

! = : 300O 3 200100'

. - 200

"

0

2

6 10 14 18 22 26 30 34 38 42 46 50 54 58 62 66 70 74

Time (d)

Figure 6.8. A. Shell growth in a symbiont-containing mussel fed methane. B. Experimental conditions for methane (solid lines) and oxygen (dashed lines). Note that when the methane supply was cut off (days 34-46), shell growth went to zero. From Cary et al. 1988. tube worms (Riftia pachyptila), succinate and glutamate were excreted into the incubation medium, suggesting these compounds as candidates for translocatable metabolites (Felbeck and Jarchow 1998). In Solemya reidi, as much as 40% of symbiont-fixed carbon is translocated to the host in the form of soluble organic compounds (Fisher and Childress 1986), and aspartate has been implicated as the transferred compound in the symbiotic association of the bivalve Lucinoma aequizonata (Distel and Felbeck 1988). While "leaky" symbionts may provide a significant portion of a host's organic requirements, there is also evidence in several species for intracellular lysis of symbiotic bacteria. Bosch and Grasse (1984) describe digestion of symbionts in lysosomes in the tubeworm Riftia pachyptila, and Fiala-Medioni et al. (1986) report digestion of symbionts in lysosomes of the mussel Bathymodiolus thermophilus. Gathering evidence suggests that the relative importance of leaky symbionts and symbiont digestion varies from species to species (Streams et al. 1997). The nutritional relation between host and symbiont may also depend on environmental conditions. 6.4.1 Digestive Enzymes In any animal, complex organic compounds must be hydrolyzed to simple monomeric subunits such as glucose, acetate, or amino acids if they are to be

161

SYMBIOSIS

100

80 -

O

60

40 -

20

0

10

20

30

40

50

60

70

Elapsed Time (min) Figure 6.9. Evidence of translocation of fixed organic carbon in two tissue types in the bivalve Solemya reidi from pulse-chase experiments using 14C-labeled bicarbonate as the inorganic substrate. Fixed 14C first appears in the gills, which house the autotrophic endosymbionts. As fixed carbon moves out of the gill tissue, it is incorporated in other host tissues, such as the foot. Data from Fisher and Childress 1986.

used in metabolic pathways. The types of hydrolytic enzymes produced by an organism can be indicative of the organic resources available. For example, digestion of bacteria as a main food source would require cellwall-cleaving enzymes like lysozymes as well as proteases and peptidases (Gonzales et al. 1993). Activities of carbohydrases that hydrolyze structural polysaccharides of plants are generally higher in detritivores and herbivores than in bacteriovores (Onishi et al. 1984). If organic compounds are translocated from symbionts to hosts, other kinds of hydrolases might be expected (e.g., glycosidases), depending on the type of organic compounds transferred. Boetius and Felbeck (1995) investigated the digestive enzymes of several vent invertebrates, including the tubeworm Riftia pachyptila, the clam Calyptogena magnified, and the mussel Bathymodiolus thermophilus. A variety of host-derived hydrolytic enzymes measured in crude extracts of symbiontcontaining tissues of tubeworms, clams, and mussels indicate that the hosts have the physiological ability to digest a variety of organic compounds. In tubeworms, highest protease activity was found in the trophosome, suggesting digestion of macromolecular peptides (as bacteria or their products). Ac-

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tivities of peptidases were high compared to glycosidases, further suggesting an abundance of proteinaceous rather than glycosidic substrates. Lysozyme activities in vent clam and mussel tissues are much higher than in bivalves that lack bacterial symbionts (Fiala-Medioni et al. 1994; Boetius and Felbeck 1995), and tubeworm lysozyme activity is in the same range as for the vent bivalves (Boetius and Felbeck 1995). All of the symbiotic species have similar levels of hydrolytic enzymes in symbiont-free and symbiont-containing tissues, suggesting that products of chemoautotrophy can be distributed throughout the host tissues for further hydrolyzation. This observation is especially relevant for tubeworms, which completely lack a specialized digestive system, and vesicomyid clams with greatly reduced guts. Unexpectedly high activities of the enzyme a-fucosidase are found in symbiont associations (Fiala-Medioni et al. 1994; Boetius and Felbeck 1995). Fucosides are most commonly known as polysaccharide storage compounds in algae, a source that can be ruled out for the vent symbioses. Hydrolytic enzyme activity specific for fucosides in vent symbioses indicates that a fucoside substrate may be produced by chemoautotrophic bacteria. 6.5 SYMBIONT PHYLOGENY 6.5.1 Endosymbiont Phytogeny and Host Fidelity Functional similarities in sulfur-oxidizing chemoautotrophic endosymbiotic bacteria from diverse bivalve hosts raise the issue of whether the symbiotic condition arose independently multiple times or if the condition arose once in a single ancestor (Distel et al. 1988). Congruence between host and symbiont phylogenies is not always the case for associations between marine animal hosts and symbiotic microorganisms. Strict species specificity is also not a requisite for symbiosis. For example, single symbiont strains can be distributed across a broad range of host taxa, as in the case of some bacterial symbionts in light organs of fish and squid (McFall-Ngai and Ruby 1992), cellulolytic symbionts in gills of wood-boring mollusks (Distel et al. 1991), and algal symbionts of corals and hydroids (Rowan and Powers 1991). Some degree of symbiont autonomy and potential for host exchange is suggested in situations where symbiont phylogenies are not congruent with host phylogenies. The association between bivalve hosts and thioautotrophic endosymbionts can be highly specific (Distel et al. 1994; Peek et al. 1998). Within five bivalve families (Vesicomyidae, Lucinidae, Thyasiridae, Mytilidae, and Solemyidae), 16S rRNA sequences of symbiont bacteria all fall within the 7-subdivision of the Proteobacteria (fig. 6.10; Distel et al. 1994). Sulfurbased chemoautolithotrophy is known in four of the five proteobacterial sub-

163

SYMBIOSIS

I

fam. Solemyidae

I T. hydrothermophilis

1 ^ s. fam. Lucinacea

L. aequizonata sym.

am. I nacea I I

P. testosteroni

L floridana sym. c. costata sym. A. phillipiana sym.

N. gonorrhoeae

T. flexuosa sym. fam. Mytilidae

B. thermophilus sym. V. chordata sym. C. magnifica sym. C. sp. monterey sym. C. sp. Oregon sym. C. elongata sym.

R. rickettsii A. tumefaciens

a

Thiomicrospira L-12 I thyasirae

5.0%

V. harveyi

E. coli

Gram+

Figure 6.10. Evolutionary-distance tree based on 16S rRNA sequences, comparing thiotrophic symbionts of bivalves (listed as "host species sym."; host families are indicated by internal brackets) and selected free-living bacteria. Large, exterior brackets indicate the subdivisions of the eubacterial class Proteobacteria. Numbers represent bootstrap values for selected nodes supported by > 75 of 100 trees by distance analysis (upper numbers) and parsimony analysis (lower numbers). Symbionts of bivalves are clearly related phylogenetically. Co-speciation between host and symbiont is suggested by the match between host bivalve families and their respective endosymbiont phylogenies. From Distel et al. 1994.

divisions (Lane et al. 1992), so association of the bivalve symbionts with the 7-subdivision is not constrained by phylogenetic history. Instead, constraint appears to be at the level of the host bivalve family; symbionts from species within a bivalve family are often more similar to each other than symbionts from bivalve species in other families (Distel et al. 1994; see Krueger and Cavanaugh 1997 for some exceptions). Evidence for co-speciation of hosts and symbionts is presented by Peek et al. (1998), whose map of the remarkable congruence of vesicomyid and symbiont phylogenies is shown in figure 6.11. Congruence may be host and/or symbiont driven, with speciation events in one partner resulting in subsequent isolation of the other partner. Although functionally distinct, methanotrophic symbioses bear some striking resemblances to sulfur-oxidizing chemoautotrophic associations within bivalve (mytilid) systems. There are similarities in host-symbiont physiological relationships, anatomical organization, and habitat. Do methanotrophic and thioautotrophic symbioses have a common ancestry? Phylogenetic anal-

164

CHAPTER 6 • Mercenaria

mercenaria

Escherichia coli

*——JA

Calyptogena elongata 44

Vesicomya gigas Ectenagena extenta Calyptogena kilmeri Calyptogena magnifica Calyptogena phaseoliformis Calyptogena n. sp. Vesicomya lepta Calyptogena pacifica

Clams

Symblonts

Figure 6.11. Congruence of vesicomyid clam and clam endosymbiont phylogenies as evidence for co-speciation. Numbers are percentage bootstrap support for nodes in 1000 resamplings. From Peek et al. 1998. ysis of 16S rRNA sequences from the methanotrophic symbiont of a Louisiana mytilid indicates that this symbiont arose from a lineage distinct from that which gave rise to chemoautotrophic symbionts of bivalves and tubeworms, and similar to the lineage that gave rise to Type I and Type X freeliving methanotrophs (fig. 6.12; Distel and Cavanaugh 1994). Thus, bacterial endosymbiosis in vent and seep bivalves arose at least twice from phylogenetically divergent bacterial lineages (Distel and Cavanaugh 1994). Using DNA-DNA hybridization techniques, sulfur-oxidizing chemoautotrophic symbionts of two co-occurring vestimentiferan tubeworm species belonging to different genera (Riftia pachyptila and Tevnia jerichonana) were found to be identical (Edwards and Nelson 1991). Geographically distant populations of R. pachyptila also hosted this same symbiont species, as did the tubeworm species Ridgeia piscesae from geographically disjunct sites (Laue and Nelson 1997). The singularity of the symbiont in phylogenetically distinct host species R. pachyptila, T. jerichonana, and R. piscesae indicates that the symbionts have not co-speciated with their respective hosts. A second thioautotrophic endosymbiont species is hosted by Lamellibrachia sp., a tubeworm species that occurs in the Gulf of Mexico

165

SYMBIOSIS

Thiomicrospira thyasirae kThiomicrospira L12

7 Methanotrophs

Methytomonas. rubta Methylomcinas methanica-

Chemoautotrophlc Symbionts

albus BOB

Splemya reidi symbiont Splemya velum symbiont

•Typei

issp,A4

Methylococcus luteus.

Hiftia pachyptjla symbiont. Thyasira flexuosa symbiont Lucinomaaequtzonata symbiont Baihymodiolusthermophifus 'symbiont CafyptogenatriaghWca . symbiont Vesicomya cordata symbiont

•"' Louisiana Mytifid symbiont ./ MethytococcuscapsulatusBaXh J»Type X

Methylobacilius flageiiatum Methylophilus methylotrophus Neisseria gonorrhoeae

Escherichia coii Chromatium vinosum

Psuedomonas testosteroni

Thiobacillus hydrothermalis Nitrosococcus oceanus

Agrobacterium turnefaciens Methylosinus sporium Methylobacterium extorquens Rickettsia rickettsii

a

Figure 6.12. Evolutionary-distance tree based on 16S rRNA, comparing thiotrophic and methanotrophic symbionts of bivalve molluscs (listed as "host species" symbiont) and selected free-living bacteria. Large brackets indicate the subdivisions of the eubacterial class Proteobacteria. Numbers represent bootstrap values for selected nodes supported by > 75 of 100 trees by distance analysis. The tree shows that methanotrophic endosymbionts are phylogenetically distinct from the thiotrophic endosymbionts, each with independent phylogenetic origins despite the similarity in symbiotic habit and habitat. From Distel and Cavanaugh 1994.

(Edwards and Nelson 1991), suggesting that there are basin-scale differences in infective symbiont stages. Contrasting modes of symbiont acquisition between bivalve and tubeworm systems (described below) may provide at least a partial explanation for contrasting host/symbiont specificities between the two groups. 6.5.2 Episymbiont Phytogeny Filamentous episymbiotic bacteria are conspicuous on host alvinocarid shrimp (especially Rimicaris exoculata) and alvinellid polychaetes (Alvinella pompejana) (see chapter 7.5). 16S rRNA sequence analysis of these episym-

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biotic bacteria places them in the e-subdivision of the Proteobacteria (Haddad et al. 1995; Polz and Cavanaugh 1995). These bacteria are not restricted to the host surface; the epibiont of R. exoculata has been found to be a dominant element of the free-living microbial community on sulfide surfaces (Polz and Cavanaugh 1995), and the epibiont of Alvinella pompejana has been identified on surfaces of rocks and on other invertebrates, including the congeneric species Alvinella caudata (Cary et al. 1997). Association with animals is the most common habit of e-proteobacteria (although all prior examples of association are parasitic), and the group as a whole favors environments low in oxygen. Bacterial mats dominated by e-proteobacteria have been described from Pele's Vent on Loihi Seamount (Moyer et al. 1995). 6.6 Symbiont Acquisition As soon as the symbiotic nature of vent tubeworms and bivalves was evident, the question of how symbiont populations are acquired became paramount. Inclusions resembling gill endosymbionts were observed in primary oocytes of Calyptogena soyae (Endow and Ohta 1990) and Solemya reidi (Gustafson and Reid 1988), providing the first indications that symbiont acquisition might be "vertical," that is, passed from generation to generation. At the same time, Le Pennec et al. (1988a) documented bacterial endocytosis by gill epithelium in Bathymodiolus thermophilus, supporting the hypothesis that symbiont acquisition in this species may be "horizontal," that is, from the external environment. Molecular techniques reveal that transmission is vertical in vent clams (Calyptogena magnifica, C. pacifica, and C phaseoliformis; Cary and Giovannoni 1993; Cary et al. 1993). Symbionts have been detected in bivalve ovarian tissues through 16S rRNA gene amplification; hybridization methods localize the symbionts to follicle cells surrounding the primary oocytes (Cary and Giovannoni 1993). Contrary to the hypothesis of Le Pennec et al. (1988a), Cary and his colleagues also find molecular evidence for vertical transmission of endosymbionts in the vent mussel (Bathymodiolus thermophilus). In tubeworms (Riftia pachyptila and Ridgeia piscesae), transmission is likely to be through direct infection from an environmental stock of microorganisms. Molecular techniques applied to tubeworm reproductive tissues provide negative results, suggesting that endosymbionts may be acquired from the environment through ingestion of free-living forms by the transient digestive tract found in newly settled juvenile vestimentiferans (Cary et al. 1993). Vertical transmission ensures hostsymbiont fidelity in bivalves, while infection de novo each generation in tubeworms is consistent with multiple host species for a given symbiont species within a geographic region.

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Streams, M.E., C.R. Fisher, and A. Fiala-Medioni. 1997. Methanotrophic symbiont location and fate of carbon incorporated from methane in a hydrocarbon seep mussel. Mar. Biol. 129:465-476. Trask, J., and C.L. Van Dover. 1999. Site-specific and ontogenetic variations in nutrition of mussels from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol. Oceanogr. 44:334-343. Vacelet, J., and N. Boury-Esnault. 1995. Carnivorous sponges. Nature 373:333-335. Vacelet, J., N. Boury-Esnault, A. Fiala-Medioni, and C.R. Fisher. 1995. A methanotrophic carnivorous sponge. Nature 377:296. Van Dover, C.L., B. Fry, J.F. Grassle, S.E. Humphris, and P.A. Rona. 1988. Feeding biology of the Mid-Atlantic Ridge hydrothermal vent shrimp: functional morphology, gut content analyses, and stable isotopic compositions. Mar. Biol. 98:209216. Von Damm, K.L., A.M. Bray, L.G. Buttermore, and S.E. Oosting. 1998. The geochemical relationships between vent fluids from the Lucky Strike vent field, MidAtlantic Ridge. Earth Planet. Sci. Lett. 160:521-536. Windoffer, R., and O. Giere. 1997. Symbiosis of the hydrothermal vent gastropod Ifremeria nautilei (Provannidae) with endobacteria—Structural analyses and ecological considerations. Biol. Bull. 193:381-392.

Physiological Ecology Vent organisms exist far outside the familiar domain of our own physiological boundaries. By combining studies of form and function, we can begin to understand the ways in which vent organisms have evolved to exploit their environment. Invertebrate/bacterial symbiont relationships are-especially effective strategies for dealing with nutritional requirements in vent ecosystems: Host invertebrates provide their symbionts with a rich and stable internal supply of nutrients obtained from an external environment where these same nutrients fluctuate wildly; in return, symbionts provide their hosts with a steady supply of organic carbon. While the physiology of host-symbiont interactions is the principal focus of this chapter, other important aspects of physiological ecology are covered, including adaptations to vent chemistry and temperature, growth rates, and sensory adaptations 7.1 NOVEL METABOLIC DEMANDS Where sulfide-oxidizing chemoautotrophic bacteria are internal symbionts, there are novel uptake requirements that the host must accommodate. Carbon—The usual flow of CO2 is out of an animal, as an end product of animal metabolism, while autotrophic symbionts require a net uptake of CO2 into the animal. Sulfide—There is a completely new demand for uptake and transport of sulfide, a compound that can poison aerobic metabolism and interfere with hemoglobin function in oxygen transport. Sulfide spontaneously reacts with molecular oxygen in seawater to form sulfate, making sulfide and the oxygen required to metabolize it mutually exclusive, except on a transient basis. Oxygen—O2 uptake must supply not only the demands of the aerobic metabolism of the host and symbiont, but also the oxidation of sulfide. Nitrogen—The necessary uptake of inorganic nitrogen is contrary to the usual heterotrophic situation where nitrogenous wastes (e.g., ammonium, urea, uric acid) are excreted. Ammonium is the usual waste nitrogen product of marine invertebrate metabolism and likely contributes to symbiont requirements along with uptake of nitrate from seawater. Of all the invertebrate/bacterial symbioses discovered to date, none is

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more morphologically and physiologically specialized for the vent environment than the giant tubeworm, Riftia pachyptila, of the East Pacific Rise and Galapagos Spreading Center (plate II, middle row, left panel). As such, the giant tubeworm will be considered in detail below as an example of the physiological adaptations that can evolve to deal with this demanding environment. 7.2 RIFTIA PACHYPTILA 7.2.1 Anatomy of a Tlibeworm There are two strange anatomical features of the adult tubeworm. Though they are large animals (1-2 m in length, several centimeters in diameter) with rapid growth rates, adult tubeworms (1) completely lack a mouth and digestive system and (2) have a specialized organ, the trophosome, that houses sulfide-oxidizing, chemoautotrophic bacteria deep inside the animal. Much of the anatomy of a tubeworm can be understood once it is placed in the context of the substrate demands of the symbiotic bacteria on which the gutless worm depends for sustenance. Relying primarily on accounts by Jones (1981, 1985) and Gardiner and Jones (1993), tubeworm anatomy is summarized here. Riftia pachyptila has four distinct body regions (fig. 7.1; table 7.1): (1) an anterior tentacular plume (obturaculum), blood-red in life; (2) a muscular vestimentum or collar; (3) the trunk; and (4) a short, segmented opisthosome. The animal lives its entire postlarval life in a chitinous, cylindrical tube secreted primarily by the vestimentum. The tube is sealed basally and attached permanently to the substratum. When undisturbed, the animal ascends the tube to expose the full length of the plume to the surrounding water, but never the vestimentum or lower body parts. When disturbed by a crab or the probing fingers of a submersible arm, the worms "duck" into their tubes. The plume of the worm is complexly structured, comprised of tightly stacked sheets of finely divided tentacles, which in turn bear smaller tentacles or pinnules. The sheets are attached to a central, supporting obturaculum. The result is a gill-like organ with a large surface area for uptake of nutrients from the surrounding environment. Accordingly, the plume is highly vascularized, allowing efficient exchange of dissolved molecules between the blood and the environment. Two primary vessels of the worm's closed vascular system circulate blood from the trophosome (in the trunk) through the vestimentum to the plume (via the dorsal blood vessel) and from the plume through the vestimentum and vestimental ciliary field and back to the trophosome (via the ventral

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PHYSIOLOGICAL ECOLOGY

Tube

Obturacular Region Plume

Vestimentum

Trunk

Gonad

I

Trophosoi Coelomic Cavity

Opisthosome-

Figure 7.1. Tubeworm external anatomy. Photo by D. Brenner. blood vessel). The blood of the vascular system is rich in extracellular hemoglobin. This characteristic, together with the rich nexus of blood vessels infiltrating the plume tentacles and pinnules, accounts for the red color of the plume. The total vascular compartment of the worm represents 9-20% of the body weight (Sanders and Childress 1993).

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TABLE 7.1. Tubeworm anatomical statistics Relative Lengths Plume Vestimentum Trunk Opisthosome

Vascular blood Coelomic fluid Trophosome

22% 17% 60% 1%

Reference Fisher Fisher Fisher Fisher

et et et et

al. al. al. al.

1988c 1988c 1988c 1988c

Biomass (wet weight)

Reference

9-20% 20-26%

Sanders and Childress 1993 Fisher et al. 1988c; Felbeck and Childress 1988 Childress et al. 1984

15%

The muscular vestimentum assists in holding the animal in the tube and allowing it to move up and down. The heart and brain of the worm lie in this region, as do the paired genital pores. As noted above, a ciliary field rich with capillaries and of uncertain metabolic function (Felbeck and Turner 1995) is located on the ventral surface of the vestimentum. The trunk of the worm houses the cream-colored gonads and the trophosome. Trophosome tissue is soft and lobular, dark-green with yellow flecks of elemental sulfur, and rich with blood vessels. The outer layers of the lobes are comprised of only worm cells. Internally, the lobes are lined with host cells, or bacteriocytes, each densely packed with bacteria, 3-5 |xm in size. No bacterial cell is more than 10 jxm from a blood capillary (Cavanaugh et al. 1981). Several trillion bacteria are found in each gram (wet weight) of trophosome tissue (Cavanaugh et al. 1981), and the trophosome in toto comprises about 15% of the biomass of the organism. The trophosome lies between two fluid-filled coelomic cavities. Like the vascular system, coelomic fluid contains extracellular hemoglobin, but there are differences in hemoglobin types and concentrations between the two fluid systems, indicating that the two systems are not confluent. A smaller hemoglobin is found in approximately equal concentrations in vascular blood and coelomic fluid. The larger hemoglobin is only present in the vascular blood. Small molecules such as CO 2 and H + are in equilibrium between the two fluids, indicating that there is some diffusionary exchange possible between the two fluid compartments. The coelomic fluid compartment accounts for the largest fraction of the biomass of an adult tubeworm (about 20-26%; Felbeck and Childress 1988; Fisher et al. 1988c). At the posterior end of the worm is the short opisthosome region, which secretes the basal lining of the tube and seems to serve as an anchor. Opisthosomal segments are small and separated internally by muscular septa.

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7.2.2 The Tbbeworm Environment Riftia pachyptila is found in areas of strong flow of dilute vent fluid at maximum temperatures typically around 15-20°C (Hessler et al. 1988). Like all organisms that require simultaneous supply of oxygen and sulfide, tubeworms live at the interface between sources of these chemically reactive compounds. Sulfide concentrations in 15°C vent fluid are on the order of 1-3 millimolar, and oxygen content goes to zero at just above 11 °C. Warm vent fluid mixes turbulently with cold (~2°C) ambient seawater to create an extremely variable thermal and chemical environment, on time scales of a few seconds (fig. 7.2; Johnson et al. 1988a). Tubeworms thus experience erratic bursts of sulfide-rich vent fluids mixed with bursts of exposure to oxygenrich seawater. Mean concentrations of inorganic substrates are inadequate measures of the uptake environment of the worm. Instead, it is the concentration of metabolites in either venting fluids or ambient seawater that defines the uptake environment of the worm (Johnson et al. 1988b). The body of a tubeworm experiences a gradient of temperature, warmest at the base of the tube and coolest at plume height where the vent water mixes with ambient seawater (fig. 7.3). 7.2.3 Adaptations for Carbon Uptake and Transport in Riftia pachyptila The autotrophic condition of bacterial endosymbiosis in Riftia pachyptila dictates a nontrivial requirement for inorganic carbon provided by the host to the symbiont. Rapid growth of R. pachyptila and the complete nutritional dependence of the host worm on organic carbon fixed by its symbiotic bacteria place a further premium on effective means of uptake of large amounts of inorganic carbon. The anatomically remote position of the bacteria in the trophosome relative to the environmental source of inorganic carbon available at the plume of the worm demands an effective means of transporting inorganic carbon from the site of uptake to the site of carbon fixation. Thus, the challenge for the tubeworm is to maintain extracellular CO 2 partial pressures in the trophosome vascular system at high enough levels to sustain fixation via the Calvin-Benson biochemical pathway at a rate that supports both the symbionts and the rapid growth of the host. Host Respiratory Inorganic Carbon For ordinary heterotrophic animals, there is a net outward flux of CO 2 generated by respiration. Tubeworms are heterotrophs, but to satisfy autotrophic demands for carbon by their bacterial symbionts, the net flux of CO2 must be inward. Only about half of the inorganic carbon fixed by the symbionts is derived from respiratory CO2 generated by the host tissue through hetero-

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120 140

Figure 7.2. Time-series measurements of temperature at the Rose Garden hydrothermal vent, Galapagos Spreading Center. The temperature probe was placed on a clump of mussels (Bathymodiolus thermophilus) and tubeworms (Riftia pachyptila). A. Maximum and minimum temperatures from 256 "burst" readings (taken every 0.5 s for —130 s) at 15 min intervals. Note that the mean temperature (5.54°C) would be a misleading measure of the fluid environment bathing the animals. B. An example of a "burst" reading used to obtain maximum and minimum temperatures. From Johnson et al. 1988a. trophic metabolism (Childress et al. 1991a). The remainder of the CO 2 demand for autotrophy in tubeworm symbionts is derived from the environment surrounding the tubeworm plume.

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179

.3-2.4

14.8

9.6-10.5 12.7-12.8

Figure 7.3. Temperature distribution in the tubeworm {Riftia pachyptila) environment at a Galapagos vent. Circles indicate the position of the probe tip. Note that the warmest temperatures are in the throat of the vent. Plumes of the worms are located where warm vent fluids mix with ambient seawater, —1-2 m above the vent orifice. From Hessler and Kaharl 1995.

Environmental Sources of Inorganic Carbon and the Role of Carbonic Anhydrase While seawater contains an abundance of inorganic carbon in the form of bicarbonate ions (HCO 3 ~), bicarbonate is not readily diffusible across living tissues. Dissolved CO2 gas, the freely diffusible form of inorganic carbon readily taken up by organisms and the form used in autotrophic carbon fixation, is normally at low partial pressures at the pH of seawater. As pH decreases, the concentration of bicarbonate ions decreases and the partial pressure of CO2 increases (fig. 7.4). CO2 partial pressures in vent effluents surrounding tubeworms are elevated by as much as three orders of magnitude above deep-sea water as a result of a combination of the lower pH (—6.0) and enriched inorganic carbon content of the venting fluids (Childress et al. 1993b). The result is an

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O ,

7

12

PH

Figure 7.4. Relationship between pH and concentration (log C) of inorganic carbon species. [H2CO3*] is the sum of aqueous CO2 and carbonic acid (H2CO3). Note that below pH 6.8, CO2 and H2CO3 predominate. From Morel 1983. environmental CO2 milieu that facilitates CO 2 uptake by diffusion into the tubeworm plume across steep gradients. Between-site differences in pH and total CO2 (expressed as 2CO 2 = CO2 + HCO 3 ") of vent effluents correspond to between-site differences observed in tubeworm blood 2CO 2 (fig. 7.5; Goffredi et al. 1997a). CO 2 uptake in tube worms is enhanced by the more alkaline pH of the tubeworm blood (7.3-7.4), which favors the bicarbonate ion, and by the enzyme carbonic anhydrase, which catalyzes the rapid internal conversion of CO 2 to bicarbonate. The worm thus maintains a steep gradient of CO 2 from outside to inside, which facilitates CO 2 diffusion (Goffredi et al. 1997a). High activities of two forms of carbonic anhydrase have been identified, one in tubeworm plume tissue, where CO 2 uptake takes place, and the other in the trophosome, where gas exchange with the symbionts occurs (Kochevar and Childress 1996). A similar role of carbonic anhydrase in expediting inorganic carbon uptake has been described for a variety of marine algae, cyanobacteria, and algal/invertebrate symbioses (e.g., Yellowlees et al. 1993). pH Regulation Tubeworm regulation of pH is "unprecedented" (Goffredi et al. 1997a) in comparison to other animals. Riftia pachyptila maintains a large pH gradient between itself and its environment and holds its extracellular pH constant (7.3-7.4), even in the face of erratically fluctuating environmental pH and internal metabolic processes that release protons (including conversion of CO2 into H + and HCO 3 " and sulfide oxidation resulting in H + and SO 4 2 ~).

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PHYSIOLOGICAL ECOLOGY 601

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Figure 7.5. Environmental inorganic carbon availability and internal inorganic carbon in Riftia pachyptila. A. Correlation of 350°C "hot water" (i.e., 35O°C black-smoker fluid) total inorganic carbon (2CO2) and coelomic fluid ECO2. B. Correlation of CO2 partial pressure (PQO2) in warm water bathing tubeworm plumes in situ and coelomic 2CO 2 of those worms. C. Correlation of CO2 partial pressure in laboratory aquaria and coelomic ECO 2 of tubeworms after 12-24 hr maintenance at a given Pco2- From Goffredi et al. 1997a.

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Goffredi et al. (1997a) propose that a proton-pumping mechanism acts at high rates to maintain the internal, extracellular pH within narrow tolerances. The alkaline internal pH facilitates carbon uptake, and its maintenance is a critical specialization for the autotrophic functioning of the tubeworm/bacterial symbiosis. Carbon Transport Carbon dioxide in Riftia pachyptila appears to be transported freely dissolved in the blood as CO2 or HCO 3 ~ (Childress et al. 1991a) rather than bound to extracellular hemoglobins (Arp et al. 1985; Toulmond et al. 1994). Based on radioactive tracer experiments, some inorganic carbon may rapidly be incorporated into 4-carbon organic acids (Felbeck 1985). This initial fixation takes place in the plume, which releases mainly succinate into the blood, and in the vestimentum region, which releases mainly malate. In isolated physiological preparations, carbon transport by organic acids may match transport of dissolved CO2 (Felbeck and Turner 1995). Once the organic acids reach the trophosome, they are readily decarboxylated, releasing CO2 for the symbionts (Felbeck 1985). Inorganic Carbon Capacity Total inorganic carbon in Riftia pachyptila is correlated with the partial pressure of environmental CO 2 and can reach such high levels (exceeding 60 mM) that they approach CO2 levels of carbonated beverages (Goffredi et al. 1997a). This high capacity for CO2 is essential for an animal that must supply its autotrophic symbionts with inorganic carbon. As described above, maintenance of high concentrations of inorganic carbon in the blood is facilitated by high external CO2 partial pressure and the alkaline internal pH (7.3-7.4), both of which favor the bicarbonate form. There is thus a gradient for diffusion of CO 2 across worm tissues, and the host can maintain a critical reservoir of inorganic carbon substrate for autotrophic primary production by the symbionts under conditions of fluctuating environmental supply. Carbon Fixation Rates Of all the known sulfide-oxidizing chemoautotrophic symbioses, tubeworms have the greatest autotrophic (i.e., primary production) potential (table 7.2). Such large carbon-fixation rates can supply more than twice the maintenance organic carbon demand of the tubeworm, providing tremendous potential for growth (Childress et al. 1991a). Optimal conditions for CO 2 fixation in Riftia pachyptila include moderate or mesophilic temperatures (22-35°C; Belkin et al. 1986; Scott et al. 1994) and low-oxygen conditions (Fisher et al. 1989).

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183

TABLE 7.2. Comparison of carbon fixation rates in tubeworms, clams, and mussels Type Tubeworm Clam Mussel

Species Name

Carbon Fixation Rate

Riftia pachyptila Calyptogena magnifica Bathymodiolus thermophilus

1

1

35 fxMCg" h" 0.3 fjiMCg"1 h" 1 3.4 |xM C g " 1 h " 1

Reference Childress et al. 1991a Childress et al. 1991b Nelson et al. 1995

7.2.4 Sulfide Sulfide Toxicity In addition to CO2, the list of raw materials that the host worm must supply to its symbionts includes a source of reduced sulfur in the form of hydrogen sulfide (table 7.3). Hydrogen sulfide yields considerable energy when oxidized (Jannasch and Mottl 1985), and it is this energy that fuels the chemoautotrophic production of organic carbon by the tubeworm endosymbionts. But sulfide is an extremely toxic compound at the micromolar concentrations found at vents (Smith et al. 1979). Primary toxicity of sulfide arises from it ability to bind to cytochrome-c oxidase, blocking the function of this critical enzyme in the electron transport chain of cellular aerobic respiration. The active form of sulfide in this toxicity is the undissociated form, H2S (Powell and Somero 1986a). Early work demonstrated that Riftia pachyptila tissues have a fully active electron transport system, showing no special resistance to sulfide poisoning, and that oxygen-consumption rates of tubeworms are comparable to those of the aerobic tissues of invertebrates from nonsulfide environments (e.g., Hand and Somero 1983; Powell and Somero 1986a). Free (dissolved) sulfide reacts spontaneously with oxygen and other oxidants to form less reduced compounds (table 7.3), which, while less toxic, are of no use as an energy source for tubeworm symbionts (Belkin et al. 1986; Fisher et al.1989; Wilmot and Vetter 1990). The trick for the tubeworm is to sequester high concentrations of sulfide and to transport this sulfide from the plume to the trophosome without poisoning the worm's aerobic respiration or allowing the sulfide to react spontaneously with oxygen. Sulfide Uptake and Transport At the acidic pH of vent water, sulfide is present predominantly as H2S (fig. 7.6), providing a strong gradient for diffusion into plume tissues. In Riftia pachyptila, this diffusion is limited by some currently unknown mechanism (Goffredi et al. 1997b). Instead, HS~ is the species that is taken up and is predominant at the physiological pH of R. pachyptila blood (fig. 7.7). HS~

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TABLE 7.3. Sulfur species Species

Common Name

Oxidation State

H2S, HS~, S 2 ~

hydrogen sulfide

fully reduced

thiosulfate

intermediate

elemental sulfur

intermediate

sulfite sulfate

intermediate fully oxidized

SO 3 2 " SO 4 2 "

Comments Concentrations of sulfide species depend on the pH of the solution. In acidic vent fluids, sulfide is present exclusively as dissolved H2S gas. At physiological pH (—7.5), unbound sulfide in tubeworm blood is present as HS ~ and H2S in approximately equal amounts. HS~ is the species that binds to hemoglobin and is used by the symbiotic bacteria. H2S is the species that blocks cytochrome-c oxidase activity. In some bacterial/invertebrate symbioses, especially those involving bivalve mollusks, thiosulfate is the active form of sulfide oxidized by the symbionts. An intermediate in the oxidation of sulfide by tubeworm symbionts. May serve as a short-term storage function, to be oxidized further for energy production. The ultimate end-product of sulfide oxidation, presumably transported as free ions though the blood and eliminated across plume membranes by diffusion.

binds rapidly and with high affinity to hemoglobins in the vascular blood and in coelomic fluid of R. pachyptila (e.g., Arp and Childress 1983; Arp et al. 1987, 1990). As Goffredi et al. (1997b) emphasize, it is advantageous for the worm to exclude H2S, since H2S is believed to be the toxic form of sulfide with respect to the cytochrome-c oxidase activity. Sulfide-hemoglobin interactions in R. pachyptila and other vestimentiferans are unusual in that the sulfide does not compete for the oxygen binding site (Somero et al. 1989), eliminating this secondary toxic effect of sulfide. By transporting sulfide bound to hemoglobins, tube worms can concentrate sulfide from the environment while maintaining a very low internal free-sulfide concentration (fig. 7.8; Childress et al. 1991a). In its bound form, sulfide is chemically

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PHYSIOLOGICAL ECOLOGY

o

3~-

Co §

12

7

PH

Figure 7.6. Relationship between pH and concentration (log C) of inorganic sulfide species. Note that below pH 7.0, H2S predominates. From Morel 1983.

o o o

D •

1

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t

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0

0.1

0.2

0.3

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0.2

0.3

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Figure 7.7. Correlation of environmental sulfur species (HS~ and H2S) with total inorganic sulfide (XH2S) in coelomic and vascular fluids of Riftia pachyptila. The correlations are significant for HS" (A: P < 0.0001; C: P = 0.0004) but not for H2S (B or D), consistent with HS ~ being the primary uptake species. From Goffredi et al. 1997b.

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g

100-

| j 80-

|

60i

^

4020 10"1

10°

101

102

Free Sulfide (JXM)

103

104

Figure 7.8. Sulfide binding to Riftia pachyptila hemoglobin (% saturation) as a function of unbound (free) sulfide concentration. Bound sulfide was removed from fresh tubeworm blood (coelomic plus vascular fluids) by acidification and purging with N 2 for 24 h. The resulting blood (at 0% hemoglobin saturation) was placed in dialysis tubing and allowed to equilibrate with various concentrations of sulfide in the dialysate. The amount of bound sulfide was calculated as the difference between the blood sulfide and the dialysate sulfide. At sulfide concentrations of 100 [xM in the initial dialysate, 80% of the hemoglobin is saturated, resulting in low levels of free sulfide in the blood. From Fisher et al. 1988b.

stable and physiologically benign. It cannot react with oxygen or interfere with cytochrome-c oxidase function. The larger hemoglobin of the vascular blood has three times the sulfidebinding capacity of the smaller hemoglobin found in both vascular and coelomic fluids. This capacity for binding sulfide, together with the high hemoglobin concentration in the vascular blood, allows the animal to concentrate sulfide from the environment by one to two orders of magnitude (Childress et al. 1991a). The high affinity for sulfide also allows the animal to retain sulfide when the animal is exposed intermittently to a low-sulfide environment. Coupling of Sulfide Detoxification and Energy Exploitation Once delivered to the trophosome, symbiotic sulfide-oxidizing bacteria harvest the energy from the sulfide to generate ATP needed to fuel inorganic carbon fixation. This sulfide sink frees the circulating hemoglobins to bind additional sulfide, maintaining negligible concentrations of unbound sulfide in the blood. The symbionts detoxify the sulfide through oxidation via energy-deriving sulfur metabolism. Of the potential sulfide-oxidation reactions, oxidation of sulfide to sulfate has the largest decrease in free energy per atom of sulfur (table 7.4). Partial oxidation leads to the formation of elemental sulfur (S°) in trophosome tissue, which can contribute useful energy to the symbionts (Wilmot and

PHYSIOLOGICAL ECOLOGY

187

TABLE 7.4. Standard free-energy changes associated with reactions involving oxidation of sulfur compounds Reaction

Free-Energy Change (kJmol~])

H2S + l/2O2 = S° + H2O HS" + 2O2 = SO 4 2 ~ + H + + S° + ll/2O 2 + H2O = H 2 SO 4 " S 2 O 3 " + 2O2 4- H2O = 2SO 4 2 " + 2H +

-210 -716 -496 -936

From Jannasch 1984.

Vetter 1990). The ultimate waste products of sulfide oxidation are sulfate ions (the fully oxidized form of sulfur) and protons (H + ). 7.2.5 Oxygen High concentrations of tubeworm hemoglobins appear to be necessary to support the large amount of O 2 consumed by the sulfide-oxidizing symbionts (Childress and Fisher 1992) as well as for controlling sulfide toxicity and facilitating sulfide transport. Symbiont demands for O 2 can exceed those of the host by more than a factor of two (Childress et al. 1991a). Tubeworm hemoglobin has a high affinity for oxygen. This is important in enabling the worms to take up and transport large amounts of O 2 while maintaining low internal dissolved O2. Maintenance of low dissolved O 2 partial pressures ensures diffusion of oxygen across a gradient from seawater to blood and prevents the spontaneous oxidation of free sulfide in the blood (Childress and Fisher 1992). Microaerophilic optima for CO2 fixation by tubeworm symbionts also argue for a mechanism to maintain very low partial pressures of oxygen in the blood. At elevated temperatures, tubeworm hemoglobins have a reduced affinity for O 2 (Arp et al. 1985) and increased rates of O 2 dissociation (Wittenberg et al. 1981). These characteristics may be important in unloading O 2 at the trophosome, which is surrounded by wanner water than the plume of the worm (Childress and Fisher 1992). 7.2.6 Nitrogen Tubeworms from hydrothermal vents have isotope ratios of 15N:14N that suggest assimilation of a local, inorganic source of nitrogen rather than consumption of organic nitrogen (Rau 1985). While ammonia concentrations in the tubeworm habitat are generally (but not uniformly) low, nitrate is always

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present in the ambient seawater (Johnson et al. 1988b). Mechanisms of nitrate uptake, concentration, and transport are unknown at this time. Nitrate Respiration Nitrate-reductase activity was demonstrated in tubeworm trophosome (Felbeck 1981) and presumed to represent the first step in inorganic nitrogen assimilation where nitrate (NO 3 2 ~) is reduced to nitrite (NO 2 ~). Johnson et al. (1988a) implicated tubeworms in the removal of nitrate from vent water. Nitrate has only recently been discovered to play a role as an oxidant in the cellular respiration of tubeworm symbionts, in addition to O 2 (Hentschel and Felbeck 1993). Nitrate respiration allows O 2 concentrations around symbionts to be extremely low, yet energy can be gained through respiratory pathways by reduction of nitrate to nitrite.

7.3 SEEP VESTIMENTIFERANS AND METHANOTROPHIC POGONOPHORANS Seep vestimentiferans share the same general body plan and, presumably, the same physiological scheme as the giant tubeworm Riftia pachyptila, but the low sulfide flux of the seep environment is radically different from that of a hydrothermal vent (Scott and Fisher 1995). Details of the physiological ecology of seep organisms are likely to be different as well. Environmental sulfide concentrations at the level of the plume and blood sulfide levels are far lower in seep tubeworms (low micromolar range) than in vent R. pachyptila (low- to mid-millimolar range). Growth rates of seep tubeworms are extremely slow, with average tube growth rates of less than 1 c m y r ' 1 (Fisher et al. 1997) and calculated longevities of >100 yr (Fisher 1996; Fisher et al. 1997). Unlike Riftia pachyptila, which grows upright from the surface of hard basalt, seep vestimentiferans live in tubes that penetrate sediment as much as one meter (MacDonald et al. 1989). While oxygen must be taken up at the level of the plume, there is speculation that sulfide uptake may be greatest in the buried portion of the worm, across the very thin tube and body wall (Scott and Fisher 1995). Sulfide concentrations in the subsurface sediments at seeps may be as great as 1 mM (Fisher 1996). The only methanotrophic tubeworm symbiosis recognized to date is in a small pogonophoran tubeworm, Siboglinum poseidoni, which lives in reducing sediments of Norwegian fiords (Schmaljohann and Fliigel 1987; Schmaljohann et al. 1990; see chapter 12).

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189

7.4 VENT AND SEEP BIVALVE-MOLLUSK SYMBIOSES Once sulfide-oxidizing bacterial symbiosis was discovered in giant tubeworms of Galapagos and East Pacific Rise spreading centers, other invertebrate/bacterial symbioses were quickly recognized. The physiological ecology of the giant clam, Calyptogena magnified, and the vent mussel, Bathymodiolus thermophilus, highlight additional host and symbiont strategies for exploiting the energy-rich environment of hydrothermal vents. 7.4.1 Calyptogena magnified Giant, dinner-plate-sized (up to 26 cm in length) clams of the Galapagos Spreading Center and East Pacific Rise are distinctive for their large fleshy gills, red meat, greatly reduced (presumably nonfunctional) digestive system, and large, vascularized, muscular foot (fig. 7.9; Boss and Turner 1980; Le Pennec et al. 1990). As in other bivalves, the gills of Calyptogena magnifiea, which account for nearly 20% of the wet weight of the clam tissue (Fisher et al. 1988a), are exposed to seawater ("mantle fluid") in the mantle cavity, drawn in through the inhalant siphon. Symbiotic, sulfide-oxidizing bacteria are housed in vacuoles which in turn lie in clam cells (bacteriocytes). The bacteriocytes are arranged on the gill filaments with their absorptive apical ends exposed to mantle fluid and their basal ends in blood-filled lacunae (see fig. 6.4; FialaMedioni and Le Pennec 1987). Bacteria-filled vacuoles within the bacteriocytes are distributed evenly throughout the cell. Like symbionts of Riftia pachyptila, clam symbionts require a source of inorganic carbon, sulfide, oxygen, and nitrogen. But the anatomy of the clam, the location of the symbionts, and the chemical characteristics of its habit are very different from those of tubeworms. Calyptogena magnifiea typically live nestled in cracks in the basalt crust, with their siphons extended into ambient CO2- and O2-rich seawater, and their foot thrust deep into the crack, exposed to warm, H2S- and CO2-rich vent fluids (fig. 7.10). Temperatures measured 10-30 cm in the cracks are as high as 14°C (Hessler et al. 1985). Rather than temporal separation of sulfide and O 2 uptake as seen in the tubeworm plume exposed to turbulent mixing of vent fluids and ambient seawater, the clam strategy, described below, is to take advantage of the spatial separation of sulfide and oxygen pools. The circulatory system of the clam is open and voluminous (24-44% of the body wet weight; Fisher et al. 1988a) and contains hemoglobin in cellular erythrocytes, rather than having extracellular hemoglobin as in Riftia pachyptila. Circulating hemoglobins of the clam bind and transport O 2 to meet the host's aerobic metabolic requirements. There is no special binding

190

CHAPTER 7

Figure 7.9. A. Shell of Calyptogena magnifica. Total length = —17 cm. B. Internal anatomy of C. magnifica with removal of the overlying mantle to expose the massive gills, the foot, mantle, and adductor muscles (Add). Photographs by D. Brenner.

B

Rose Garden

gA O

0-0,25

Clam Acres 0.9°C

85 cm yr" 1 (Lutz et al. 1994) during the first year of their growth, and the worms were sexually mature within two years (Lutz et al. 1994). While explicit tube growth in this species of worms is not necessarily a correlate of living biomass production (Gaill et al. 1997), their rapid growth is incontestable. Chitin production in R. pachyptila is among the highest of any known aquatic species (Gaill et al. 1997), and the claim that R. pachyptila has "the fastest rates of growth documented for any marine invertebrate" (Lutz et al. 1994) is reasonable in its hyperbole. A second, smaller species of tubeworm (Tevnia jerichonana) colonizing the same new vent sites grew at a rate of > 30 cm yr~ l (i.e., reaching full size within one year; Lutz et al. 1994). Ridgeia piscesae, a smaller species of tubeworm inhabiting vent fields on the Juan de Fuca Ridge, can increase its tube length at a rate of 30-50 cm yr" 1 (Tunnicliffe et al. 1990). DeBevoise and Taghon (1988) used ratios of RNA to DNA to investigate variations in tubeworm growth rates over small spatial scales (2-50 m). While the DNA content of an individual is essentially constant, the RNA content in a variety of species is positively correlated with growth rate. Despite large within-site variations in RNA:DNA ratios, there are significant between-site differences, attributed to differences in the quality of the environment (DeBevoise and Taghon 1988). Growth rates of vent bivalve species have been measured using a variety of techniques, including radiochronometry (Turekian et al. 1979, 1983; Turekian and Cochran 1981), direct measurements of shell growth on marked and recaptured individuals (e.g., Rhoads et al. 1981), and shell dissolution analyses (e.g., Roux et al. 1983; Rio and Roux 1984; Lutz et al. 1985, 1988). Growth rates for the giant clam, Calyptogena magnifica, range from 0.5 to 4-6 cm yr" 1 , depending on the technique, the size of the clam, and the site. Similar growth rates have been measured in the mussel, Bathymodiolus thermophilus. Growth curves developed for vent and shallow-water bivalves

202

CHAPTER 7 Calyptogena magnifies Vent Clam Bathymodiolus thermophilus Vent Mussel Geukensia demissa Shallow-Water Mussel

Tindaria callistiformis Deep-Sea Clam » lOOYears

1

3

5

7

9

11 13 15 17 19 21 23 25 27 29

Age (years)

31

Figure 7.14. Growth curves for various species of bivalves. Note that the vent clam (Calyptogena magnifica) and mussel (Bathymodiolus thermophilus) have growth curves comparable to those of shallow-water mussel species (Mytilus californianus, Geukensia demissa), while the non-vent deep-sea clam Tindaria callistiformis has an extremely slow growth rate. From Turner and Lutz 1984. (plots of age vs. shell length) illustrate the rapid growth rates of vent clams and mussels (fig. 7.14; Turner and Lutz 1984). Radiometric ages of four adult vent crabs (Bythograea thermydron; 54-65 mm carapace width) from the Galapagos spreading center provide the only measure of age or growth rates in this species. These ages are determined by analysis of crab exoskeletons, so that the age represents only the length of time since the last molt. One specimen had an age of 0.1 yr, indicating it had just undergone a molt; the other three specimens were 3-4 yr old, indicating a molt interval for adults of at least 3 yr (Bennett and Turekian 1984). 7.8 THERMAL ADAPTATIONS Verification of the thermal extremes at which multicellular eukaryotic organisms live has become a competition worthy of the Guinness Book of World Records. Accounts of ants foraging in the midday sun at body temperatures in excess of 50°C (Wehner et al. 1992) and of Namib pseudoscorpions thriving under the 65°C heat of the desert (Heurtault and Vannier 1990) prompted vent biologists to up the ante. Alvinellid polychaetes living on the sides of black-smoker chimneys have been nominated as the hottest of invertebrates (Chevaldonne et al. 1992), based on a single observation of survival of an individual after brief exposure to 105°C fluids in situ. Alvinellid polychaetes routinely live in tubes bathed by 30-70°C fluids (Desbruyeres et al. 1982;

203

PHYSIOLOGICAL ECOLOGY

100 O o

8.

Inside Tube

80 60 40 20 10:00

Outside Tube ••. 1 0 0 -

3

^150J

07 Jan 92 26 Dec 91

200.

250-

19 Mar 921 31 Mar 92 \

300-

350-

-150

-100

-50

0

50

100

150

Km East of Starting Point Figure 9.9. Progressive vector diagram of currents recorded at 13°N on the East Pacific Rise. Note the net flow to the SSE and reversals of current direction over the recording interval. From Chevaldonne et al. 1997.

ployed 100 m above bottom at a 13°N site for 159 d indicated a net southsoutheast current of 2.2 cm s" 1 (fig. 9.9) comprised of two components: one month of net flows to the north-northwest (5.2 cm s" 1 ) alternating with 2 months of net flows to the south-southeast (4.2 cm s" 1 ). Given this variability in current regimes, the timing of release of gametes or larvae and the duration of the planktonic phase can greatly affect the maximum possible transport and direction in a linear field. The model developed by Chevaldonne et al. (1997) incorporates life-history attributes, including effective population size, fecundity, larval mortality, and post-settlement mortality. No empirical measures of mortality are available, but reasonable constraints on these parameters can be borrowed from the literature. The output of the model is the number of migrants (Nm) surviving for a continuum of travel times, where Nm of 1 is the critical value within the framework of population genetics: at Nm > 1, there is genetic mixing of two populations. For standard input parameters deemed "most probable" by the authors,

276

CHAPTER 9 100n

0.10.01

Figure 9.10. The number of migrants exchanged during one generation by two populations (Nm) of alvinellid polychaetes over time (t, in days), using life-history parameters deemed most representative of the worms. The model does not adequately characterize iVm' when t < 0.1 d. For t > 0.1 d, Nm never exceeds 45.6 individuals per generation; it reaches the critical value of 1 after 8 d. From Chevaldonne et al. 1997. critical travel times (where Nm > 1) correspond to 8 d of transport, or distances of 8-40 km (fig. 9.10). For very short travel durations, propagules from one population never reach the next; small effective population sizes and high mortality limit Nm at longer travel durations. Genetic data indicate that mixing in alvinellid polychaetes occurs over distances far greater than the model critical value of 8-40 km (Jollivet et al. 1995). The discrepancy between genetic data and the results of the model seems most reasonably reconciled by noting that, unlike the assumptions of the model, mixing in the natural system takes place gradually, over multiple generations, and, more importantly perhaps, in the context of temporally shifting locations of vent sites. While the model suggests that the duration of larval transport cannot reasonably exceed 15-30 d, the authors do not yet discount the possibility of teleplanic larvae or some other means of longdistance dispersal in alvinellid polychaete species. 9.3.2 Plume Dispersal With the description of advective plumes of 350°C fluids and entrainment of large volumes of bottom water up to the height of the neutrally buoyant plume (Lupton et al. 1985), the potential for entrainment of passive larvae and vertical transport was patent. Kim et al. (1994) used a standard plume buoyancy model and field-measured larval abundances to estimate a mean vertical flux of 100 vent larvae h " 1 at a single black smoker, with an order of magnitude variation in larval flux across multiple samples. Reported as number of larvae per 1000 m3, maximum larval density in samples of Kim

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277

et al. (1994) reaches as high as 280 individuals per 1000 m3 for limpets, though, since the actual sample volume was only 25 m3, the number of individuals on which this extrapolation is based is extremely small (7 limpet larvae). Mullineaux et al. (1995) use the collection of 4 clam larvae in two plankton tows taken in the neutrally buoyant plume versus no clam larvae in a single plankton tow taken outside the plume at Juan de Fuca Ridge vents to state that "larvae of vent bivalves (Calyptogenal sp.) occur exclusively in the plume." Such extremely low larval abundances in samples taken at and near vents make it difficult to measure and interpret their distributions with any statistical confidence. The significance of plumes in dispersal of vent larvae and subsequent colonization of vents for at least some species is brought into question when one considers the dense communities of tubeworms, mussels, clams, and other invertebrates at Galapagos Spreading Center vents, where no evidence of recent black smokers has ever been observed. While the Galapagos situation suggests that vertical transport in plumes is not essential in dispersal of vent larvae over distances of several kilometers, a vertical component to transport must enhance long-distance dispersal capacity and genetic mixing. More recent data and models by Kim and Mullineaux (1998) suggest that plume transport may indeed be less important in larval dispersal than tidally driven cross-axis flows. 9.3.3 Megaplume Dispersal Plumes from steady-state black smokers reach only 100-200 m above the seabed. Volcanic eruptions generate infrequent, massive pulses of warm water, which are injected as high as 1000 m in the water column. Because large volumes of bottom water are entrained into these megaplumes, it is expected that megaplumes may provide a vehicle for episodic, large-scale dispersal events of vent larvae (Mullineaux and France 1995), but no direct evidence for this is available. 9.3.4 Mesoscale Flows Bottom currents, plumes, and megaplumes not only disperse larvae, they dilute them. Yet clearly large numbers of larvae can plaster a new seafloor vent in a short period of time—possibly in a matter of days and weeks, based on the uniform sizes of individuals following the eruption at 9°N on the East Pacific Rise. Mesoscale flows generated by buoyant plumes have the potential to aggregate and either retain or transport pools of larvae (Mullineaux and France 1995). These mesoscale vortices are predicted by theory (e.g., Speer 1989) and have been demonstrated in the laboratory (Helfrich and Battisti 1991) and in the field (Lupton et al. 1998). A plume eddy is

278

CHAPTER 9

Anticyclonic Circulation

Figure 9.11. Vorticity in a hydrothermal vent plume. Cyclonic and anticyclonic pairs form above an axial-valley hydrothermal vent on a mid-ocean ridge. Entrainment brings larvae into the anticyclonic plume vortex, from which they may sink and be carried back into the plume vortex, together with newly produced larvae. As vortices periodically shed from the plume, they may transport larvae as concentrated patches downstream. Modified from Mullineaux and France 1995. expected to remain over a vent for —45 d before being shed downstream, carrying its vent-derived properties, including larvae entrained from the underlying vent community. As a plume eddy sits over a vent field, it may accumulate larvae; new larvae could continually be entrained to rise up and then sink; if on sinking, the larvae do not settle and metamorphose at or near their source, they can be reentrained in the convection cell to cycle through again. When the vortex is shed, it can potentially transport a concentrated patch of larvae to a downstream site (fig. 9.11; Mullineaux and France 1995). 9.3.5 Dispersal by Non-Larval Stages For species with mobile post-larvae, juveniles, and adults, dispersal need not be restricted to the larval stage. Post-larvae of several species have been found in plankton tows taken above vent sites on the East Pacific Rise and Galapagos Spreading Center (Berg and Van Dover 1987), in Guaymas Basin (Wiebe et al. 1988), and on the Juan de Fuca Ridge (Mullineaux et al. 1995). Though not proven, it seems likely that adult crabs can scavenge their way for long distances over the seafloor, from one vent field to another. While

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279

crab abundances are clearly maximal at vents and decrease exponentially away from vent sites (see fig. 8.14), scattered individuals occur well outside the boundaries of vent fields (by 100s of meters). These and other organisms that can walk or swim between vent sites have been implicated in zoochory—the dispersal of smaller invertebrates by "hitch-hiking" on larger, motile species (Zal et al. 1995). On the slow-spreading Mid-Atlantic Ridge, where the average distance between vent sites is greater than it is on the fastspreading East Pacific Rise, it may be no coincidence that the large, longlived, deep-water vent fields are often dominated by highly mobile shrimp rather than sessile or sedentary species. 9.4 SETTLEMENT CUES Most marine invertebrates have a specialized larval settlement stage that responds to environmental signals presumably indicative of a suitable location for survival and successful reproduction. Almost since vents were discovered, biologists have suggested a variety of settlement cues that might be active in stimulating metamorphosis in vent invertebrates, including temperature, sulfide concentration, bacterial populations, and established adult colonies (Lutz et al. 1980; Lutz 1988; Tunnicliffe et al. 1997; Shank et al. 1998). To date, there has been little experimental test of these hypotheses. An exception is a preliminary experiment briefly reported in Rittschof et al. (1998), where dissolved sulfide was tested as a cue for settlement stages of obligate vent organisms. Conducted at vents of the High Rise Field, Juan de Fuca Ridge, treatments consisted of short-term deployments (—24 h) of replicate alginate slabs, in which sulfide is trapped and allowed to release slowly, and non-sulfide-impregnated alginate controls. On recovery, 5 replicate sulfide alginate slabs contained a total of 20 living, burrowed post-larvae of vent polychaete worms (Paralvinella sp.), compared to no polychaete worms in any of 6 control slabs. In shallow-water studies of settlement cues, Cuomo (1985) reported greater settlement by capitellid polychaete larvae in response to elevated sulfide, but Dubilier (1988) suggests this enhancement may have been a sublethal toxic effect. However, active burrowing by paralvinellid post-larvae into sulfide treatments at vents (Rittschof et al. 1998) is taken as evidence of an active response rather than a passive sublethal response to sulfide. 9.5 RECRUITMENT In an early study of recruitment to slate panel arrays elevated several centimeters off the seafloor (Van Dover et al. 1988), populations of vent poly-

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CHAPTER 9

chaetes, mollusks, and barnacles colonizing the panels were predominantly post-larval, juvenile, or sub-adult stages, regardless of the length of deployment (ranging from 26 d to 260-320 d to 3 yr). Predatory cropping by marauding fish, crabs, and other organisms was considered the most likely process accounting for the immaturity of the colonists. The only adult polychaete was found in crevices made by a knot of polypropylene line. No vestimentiferans were found on any arrays. Within a given species, ontogenetic series were recovered from individual arrays, indicating that more than a single size class was represented. Vent species recruited to non-vent panels, but abundances were highest on panels placed within sites of active warm-water venting. Though infrequently reported in other types of vent studies, folliculinid and foraminiferan protozoans are the most abundant eukaryotic organisms colonizing long-term deployments (1216 d) at 21°N on the East Pacific Rise (Van Dover et al. 1988). Tunnicliffe (1990) deployed recruitment panels at Juan de Fuca vents, and after 2 yr found 3 tubeworm recruits, all in the slots of screws and thus protected from predation. Additional recruitment experiments are in progress at the 9°N vent fields on the East Pacific, with preliminary results from a 3 yr deployment of basalt plates reported in Mullineaux et al. (1998). As in the work reported by Van Dover et al. (1988), most species and species groups colonized plates positioned within and outside of warm venting water, leading to the inference that adult distributions are determined by post-settlement processes such as stage-specific nutritional requirements and predation. Mullineaux et al. (1998) suggest that microhabitat variation in hydrothermal flux may influence settlement, based on their observation that all 18 vestimentiferans recruiting to 2 (of 5) basalt plates deployed in warm water were found on the undersides of the plates. Larval recruitment studies are a significant component of a major National Science Foundation-supported research initiative (LARVE) at vents, and the next decade should see publication of significant new findings in this field.

APPENDIX TABLE 9.A. Reproductive characteristics of vent and seep taxa

Species and Location Mollusca Calyptogena magnifica EPR, Gal

Calyptogena sp Monterey Seep Bathymodiolus thermophilus EPR

Sexuality

Egg Dia. (/urn)

Mode of Development

Gametogenesis

gonochoric

150

lecithotrophic

asynchronous

gonochoric

180-220

lecithotrophic

synchronous

50

planktotrophic

asynchronous

possible protandric hermaphrodites

Comments Clams are immature up to ~ 6 cm length; at 9-10 cm clams are ripe (i.e., at 40% of maximum size); at 12-14 cm, gonads are completely full. Large clams remain at this nearly full ripe stage, indicating no spawning or release of only a small proportion of gametes at any one time. First signs of sexual maturity are estimated to occur at between 1 and 4 yrs, with fully ripe condition at 3-15 yrs. Increased reproductive effort in late fall and spring. Gonads are undifferentiated at < 4 cm; at 7-16 cm, males are fully ripe. Undifferentiated gonads and hermaphrodites are observed in 7-13 cm size classes. Females are ripe at 9-16 cm. Males are presumed to develop first, and some males change to females after spawning. Associated with this protandric hermaphroditism is sexual dimorphism in shell length, with

References Berg 1985

Lisin et al. 1997 Berg 1985

TABLE 9.A. (Continued)

Species and Location

Bathymodiolus puteoserpentis MAR (Snake Pit)

Sexuality

—

Egg Dia.

(fjm)

Mode of Development

Gametogenesis

-50

—

synchronous?

—

Bathymodiolus sp. MAR (Lucky Strike)

hermaphrodites

—

demersal plantigrade?

Bathymodiolus elongatus N. Fiji (BAB)

possible protandric hermaphrodites

—

—

synchronous?

Acharax alinae Lau (BAB)

gonochoric

600-660

extended lecithotrophic or benthic

asynchronous

Neomphalus fretterae EPR Turrid gastropods (2 species) EPR Archaeogastropods (24 species) EPR Helicoradomenia juani JdF

asynchronous

planktotrophic lecithotrophic hermaphroditic

90

lecithotrophic

Comments females being larger. Males are estimated to mature at 3 yrs, females ripe at 4 yrs or more. High fecundity; spermatozoa are of the primitive type, indicative of broadcast fertilization. No evidence for endosymbiont transmission associated with spermatozoa. Abundant late larval stages found among adult mussels. Spermatozoa are of the primitive type, indicative of broadcast fertilization. No evidence for endosymbiont transmission associated with spermatozoa. Both oocytes and sperm are the largest reported for any bivalve species. Multiple shell layers of protoconch suggest a long planktonic existence. Planktotrophy determined by larval shell morphology. Lecithotrophy determined by larval shell morphology.

asynchronous

References

Le Pennec and Beninger 1997

Comtet and Desbruyeres 1998; Trask and Van Dover, 1999; Tyler and Young, in press Le Pennec and Beninger 1997

Benninger and Le Pennec 1997 McLean 1981 Batten 1984 Lutz et al. 1986 Lutz et al. 1986 Savage 1997

Polychaetes Alvinella pompejana EPR

gonochoric

200

lecithotrophic

synchronous

Paralvinella grasslei EPR

gonochoric

275

direct

synchronous

Paralvinella pandorae pandorae JdF, Ex Paralvinella palmiformis JdF, Ex Paralvinella sulfincola JdF Paralvinella pandorae irlandei EPR

gonochoric

215

brooder

asynchronous

gonochoric

260

lecithotrophic

synchronous

gonochoric

250

?lecithotrophic

asynchronous

104 to 105 oocytes in coelomic cavity; fertilization internal by pseudocopulation; larvae believed to be benthic. 4000 ± 1400 oocytes in coelomic cavity; sexual dimorphism; compulsory passage of oocytes through inseminated spermathecae; suggestions of pairing and brooding. 4500 oocytes per worm; sperm morphology suggests specialized mode of fertilization. 18,000 oocytes per worm; demersal larvae.

Chevaldonne and Jollivet 1993; JouinToulmond et al. 1997; Jollivet et al. 1998 Zal et al. 1995

McHugh 1989 McHugh 1989 Copley 1998

Pairs of large individuals have been found together inside cocoons, with 2-3 small individuals at the base of tubeworm (Tevnia jerichonana) tubes.

Jollivet 1993

TABLE 9.A. {Continued)

Species and Location

Sexuality

Egg Dia.

(jjum)

Mode of Development

Gametogenesis

Amphisamytha galapagensis JdF

gonochoric

240

lecithotrophic

asynchronous

Branchipolynoe seepensis MAR (Lucky Strike)

gonochoric or protandric hermaphrodism

395

lecithotrophic or direct

asynchronous

Opisthotrochopodus n. sp. MAR (Lucky Strike)

gonochoric

420

lecithotrophic or direct

asynchronous

gonochoric

116

lecithotrophic

asynchronous

gonochoric

110

lecithotrophic

asynchronous

Vestimentifera Ridgeia piscesae JdF Riftia pachyptila EPR

Comments

References

5600-9600 oocytes per worm (max = 12,500); early maturation; external fertilization; demersal larvae. Up to 300 mature oocytes (>300 ixm) per worm; sexual dimorphism (number of nephridial papillae and size); rapid oogenesis; sperm storage and internal fertilization. 100-600 oocytes (>25 |jim) per worm; sexual dimorphism (number of nephridial papillae); rapid oogenesis; sperm storage and internal fertilization.

McHugh and Tunnicliffe 1994

Sperm in oviduct support the notion of sperm transfer.

Southward 1988; Goodson et al., in press

Van Dover et al. 1999; Hourdez in Jollivet 1996

Van Dover et al. 1999

Jones 1981; Gardiner et al. 1992

BAB = Back-Arc Basin; EPR = East Pacific Rise; Gal = Galapagos; JdF = Juan de Fuca Ridge; Ex = Explorer Ridge; MAR = Mid-Atlantic Ridge.

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285

REFERENCES Batten, R.L. 1984. Shell structure of the Galapagos Rift limpet Neomphalus fretterae McLean 1981, with notes on muscle scars and insertions. American Museum of Natural History Novitates 2776:1-13. Beninger, P.G., and M. Le Pennec. 1997. Reproductive characteristics of a primitive bivalve from a deep-sea reducing environment: Giant gametes and their significance in Acharax alinae (Cryptodonta: Solemyidae). Mar. Ecol. Prog. Ser. 157:195-206. Berg, C.J., Jr. 1985. Reproductive strategies of mollusks from abyssal hydrothermal vent communities. Biol. Soc. Wash. Bull. 6:185-197. Berg, C.J., and C.L. Van Dover. 1987. Benthopelagic macrozooplankton communities at and near deep-sea hydrothermal vents in the eastern Pacific Ocean and the Gulf of California. Deep-Sea Res. 34:379-401. Cary, S.C., H. Felbeck, and N.D. Holland. 1989. Observations on the reproductive biology of the hydrothermal vent tubeworm Riftia pachyptila. Mar. Ecol. Prog. Ser. 52:89-94. Chevaldonne, P., and D. Jollivet. 1993. Videoscopic study of deep-sea hydrothermal vent alvinellid polychaete populations: Biomass estimation and behaviour. Mar. Ecol. Prog. Ser. 95:251-262. Chevaldonne, P., D. Desbruyeres, and M. Le Haitre. 1991. Time-series of temperature from three deep-sea hydrothermal vent sites. Deep-Sea Res. 38:1417-1430. Chevaldonne, P., D. Jollivet, A. Vangreisheim, and D. Desbruyeres. 1997. Hydrothermal vent alvinellid polychaete dispersal in the eastern Pacific. 1. Influence of vent site distribution, bottom currents and biological features. Limnol. Oceanogr. 42:6780. Comtet, T., and D. Desbruyeres. 1998. Population structure and recruitment in mytilid bivalves from the Lucky Strike and Menez Gwen hydrothermal fields (37°17'N and 37°50'N on the Mid-Atlantic Ridge). Mar. Ecol. Prog. Ser. 163:165-177. Copley, J.T. 1998. The Ecology of Deep-Sea Hydrothermal Vents. Ph.D. Thesis, University of Southampton, 204 pp. Cuomo, M.C. 1985. Sulphide as a larval settlement cue for Capitella sp. I. Biogeochemistry 1:169-181. Desbruyeres, D., and L. Laubier. 1983. Primary consumers from hydrothermal vent animal communities. In: P.A. Rona, K. Bostrom, L. Laubier, and K.L. Smith (eds.). Hydrothermal Processes at Seafloor Spreading Centers. Plenum Press, New York, pp. 711-734. Dixon, D.R., D. Jollivet, L. Dixon, J. Nott, and P. Holland. 1995. The molecular identification of early life-history stages of hydrothermal vent organisms. In: L.M. Parson, C.L. Walker, and D.R. Dixon (eds.). Hydrothermal Vents and Processes. Geol. Soc. Spec. Publ. 87:343-350. Dubilier, N. 1988. H2S—A settlement cue or a toxic substance for Capitella sp. I larvae? Biol. Bull. 174:30-38. Eckelbarger, K.J., and L. Watling. 1995. Role of phylogenetic constraints in determining reproductive patterns in deep-sea invertebrates. Invert. Biol. 114:256-269. Fujioka, K., K. Kobayashi, K. Kato, M. Aoki, K. Mitsuzawa, M. Kinoshita, and A.

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Nishizawa. 1997. Tide-related variability of TAG hydrothermal activity observed by deep-sea monitoring system and OBSH. Earth Planet. Sci. Lett. 153:239-250. Fujiwara, Y., J. Tsukahara, J. Hashimoto, and K. Fujikura. 1998. In situ spawning of a deep-sea vesicomyid clam: Evidence for an environmental cue. Deep-Sea Res. 45:1881-1889. Gage, J.D., and P.A. Tyler. 1991. Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor. Cambridge University Press, Cambridge, UK. Gardiner, S.L., and M.L. Jones. 1985. Ultrastructure of spermiogenesis in the vestimentiferan tubeworm Riftia pachyptila (Pogonophora: Obturata). Trans. Am. Microscop. Soc. 140:19-44. Gardiner, S.L., S.E. Shrader, and M.L. Jones. 1992. Preliminary observations on oogenesis in the tubeworm Riftia pachyptila Jones (Vestimentifera). Am. Zool. 32:124A. Giese, A.C., and H. Kanatani. 1987. Maturation and spawning. In: A.C. Giese and J.S. Pearse (eds.). Reproduction of Marine Invertebrates, vol. 9. Blackwell/Boxwood, Pacific Grove and Palo Alto, CA, pp. 252-329. Helfrich, K.R., and T.M. Battisti. 1991. Experiments on baroclinic vortex shedding from hydrothermal plumes. J. Geophys. Res. 96:12511-12518. Jollivet, D. 1993. Distribution et evolution de la faune associee aux sources hydrothermales a 13°N sur la dorsale du Pacifique oriental: Le cas de polychetes Alvinellidae. These de doctorat. Universite de Bretagne Occidentale, Brest. Jollivet, D. 1996. Specific and genetic diversity at deep-sea hydrothermal vents: An overview. Biodivers. Conserv. 5:1619-1653. Jollivet, D., D. Desbruyeres, F. Bonhomme, and D. Moraga. 1995. Genetic differentiation of deep-sea hydrothermal vent alvinellid populations (Annelida: Polychaeta) along the East Pacific Rise. Heredity 74:376-391. Jollivet, D., L.J.R. Dixon, D. Desbruyeres, and D.R. Dixon. 1998. Ribosomal (rDNA) variation in a deep-sea hydrothermal vent polychaete, Alvinella pompejana, from 13°N on the East Pacific Rise. J. Mar. Biol. Assoc. U.K. 78:113-130. Jones, M.L. 1981. Riftia pachyptila, new genus, new species, the vestimentiferan worm from the Galapagos Rift hydrothermal vent (Pogonophora). Proc. Biol. Soc. Wash. 93:1295-1313. Jones, M.L., and S.L. Gardiner. 1988. Evidence for a transient digestive tract in Vestimentifera. Proc. Biol. Soc. Wash. 101:423-433. Jones, M.L., and S.L. Gardiner. 1989. On the early development of the vestimentiferan tube worm Ridgeia sp. and observations on the nervous system of Ridgeia sp. and Riftia pachyptila. Biol. Bull. 177:254-276. Jouin-Toulmond, C , F. Zal, and S. Hourdez. 1997. Genital apparatus and ultrastructure of the spermatozoa in Alvinella pompejana (Annelida: Polychaeta). Cah. Biol. Mar. 38:128-129. Kim, S.L., and L.S. Mullineaux. 1998. Distribution and near-bottom transport of larvae and other plankton at hydrothermal vents. Deep-Sea Res. 45:423-440. Kim, S.L., L.S. Mullineaux, and K.R. Helfrich. 1994. Larval dispersal via entrainment into hydrothermal vent plumes. J. Geophys. Res. 99:12655-12665. Lee, R.F., and J. Hirota. 1973. Wax esters in tropical zooplankton and nekton and the geographical distribution of wax esters in marine copepods. Limnol. Oceanogr. 18:227-239.

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Le Pennec, M., and P.G. Beninger. 1997. Ultrastructural characteristics of spermatogenesis in three species of deep-sea hydrothermal vent mytilids. Can. J. Zool. 75:308-316. Lisin, S.E., E.E. Hannan, R.E. Kochevar, C. Harrold, and J.R Barry. 1997. Temporal variation in gametogenic cycles of vesicomyid clams. Invert. Reprod. Dev. 31:307318. Little, S.A., K.D. Stolzenbach, and J.F. Grassle. 1988. Tidal current effects on temperatures in diffuse hydrothermal flow: Guaymas Basin. Geophys. Res. Lett. 15:1491-1494. Lupton, J.E., J.R. Delaney, H.R Johnson, and M.K. Tivey. 1985. Entrainment and vertical transport of deep-ocean water by buoyant hydrothermal plumes. Nature 316:621-623. Lupton, J.E., E.T. Baker, N. Garfield, G.J. Massoth, R.A. Feely, J.R Cowen, R.G. Greene, and T.A. Rago. 1998. Tracking the evolution of a hydrothermal event plume with a RAFOS neutrally buoyant drifter. Science 280:1052-1055. Lutz, R.A. 1988. Dispersal of organisms at deep-sea hydrothermal vents: A review. Oceanol. Acta, Special Volume, pp. 23-29. Lutz, R.A., D. Jablonski, D.C. Rhoads, and R.D. Turner. 1980. Larval dispersal of a deep-sea hydrothermal vent bivalve from the Galapagos Rift. Mar. Biol. 57:127133. Lutz, R.A., D. Jablonski, and R.D. Turner. 1984. Larval development and dispersal at deep-sea hydrothermal vents. Science 226:1451-1454. Lutz, R.A., P. Bouchet, D. Jablonski, R.D. Turner, and A. Waren. 1986. Larval ecology of mollusks at deep-sea hydrothermal vents. Am. Malacol. Bull. 4:49-54. McHugh, D. 1989. Population structure and reproductive biology of two sympatric hydrothermal vent polychaetes, Paralvinella pandorae and P. palmiformis. Mar. Biol. 103:95-106. McHugh, D., and V. Tunnicliffe. 1994. Ecology and reproductive biology of the hydrothermal vent polychaete Amphisamytha galapagensis (Ampharetidae). Mar. Ecol. Prog. Ser. 106:111-120. McLean, J. 1981. The Galapagos Rift limpet Neomphalus: Relevance to understanding the evolution of a major Paleozoic-Mesozoic radiation. Malacol. 21:291-336. Momma, H., Mitzusawa, Y. Kaiho, R. Iwase, and Y. Fujiwara. 1995. Long-term deep sea floor observation off Hatsushima Island in Sagami Bay—One year in the Calyptogena soyae clam colony. JAMSTEC J. Deep-Sea Res. 11:249-268. Mullineaux, L., and S. France. 1995. Dispersal mechanisms of deep-sea hydrothermal vent fauna. In: S.E. Humphris, R. Zierenberg, L. Mullineaux, and R. Thomson (eds.). Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions. Geophysical Monograph 91, Am. Geophys. Union, Washington, DC, pp. 408-424. Mullineaux, L.S., P.H. Wiebe, and E.T. Baker. 1995. Larvae of benthic invertebrates in hydrothermal plumes over Juan de Fuca Ridge. Mar. Biol. 122:585-596. Mullineaux, L.S., S.L. Kim, A. Pooley, and R.A. Lutz. 1996. Identification of archaeogastropod larvae from a hydrothermal vent community. Mar. Biol. 124:551-560. Mullineaux, L.S., S.W. Mills, and E. Goldman. 1998. Recruitment variation during a pilot colonization study of hydrothermal vents (9°50'N, East Pacific Rise). DeepSea Res. 45:441-464.

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Orton, J.H. 1920. Sea temperature, breeding, and distribution in marine animals. J. Mar. Biol. Assoc. U.K. 12:339-366. Pond, D., D. Dixon, and J. Sargent. 1997. Wax-ester reserves facilitate dispersal of hydrothermal vent shrimp. Mar. Ecol. Prog. Ser. 146:289-290. Rittschof, D., R.B. Forward, G. Cannon, J.M. Welch, M. McClary, E.R. Holm, A.S. Clare, S. Conova, L.M. McKelvey, P. Bryan, and C.L. Van Dover. 1998. Cues and context: Larval responses to physical and chemical cues. Biofouling 12:31-44. Savage, A.M. 1997. Life History Biology of Helicoradomenia juani, a Hydrothermal Vent Aplacophoran (Mollusca: Neomeniomorpha). Master's Thesis, University of Southampton, 71 pp. Schultz, A., J.R. Delaney, and R.E. McDuff. 1992. On the partitioning of the flux between diffuse and point source seafloor venting. J. Geophys. Res. 97:1229912314. Shank, T.M., DJ. Fornari, K.L. Von Damm, M.D. Lilley, R.M. Haymon, and R.A. Lutz. 1998. Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents ( 9°N, East Pacific Rise). Deep-Sea Res. 45:465-515. Southward, E.C. 1988. Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): Implications for relationships between Vestimentifera and Pogonophora. J. Mar. Biol. Assoc. U.K. 68:465-487. Southward, E.C, and K.A. Coates. 1989. Sperm masses and sperm transfer in a vestimentiferan, Ridgeia piscesae Jones, 1985 (Pogonophora: Obturata). Can. J. Zool. 67:2776-2781. Speer, K.G. 1989. A forced baroclinic vortex around a hydrothermal plume. Geophys. Res. Lett. 16:461-464. Thorson, G. 1950. Reproduction and larval ecology of marine bottom invertebrates. Biol. Rev. 25:1-45. Trask, J., and C.L. Van Dover. 1999. Site-specific and ontogenetic variations in nutrition of mussels from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol. Oceanogr. 44:334-343. Tunnicliffe, V. 1990. Observations on the effects of sampling on hydrothermal vent habitat and fauna of Axial Seamount, Juan de Fuca Ridge. J. Geophys. Res. 95:12961-12966. Tunnicliffe, V, R.W. Embley, J.F. Holden, D.A. Butterfield, G.J. Massoth, and S.K. Juniper. 1997. Biological colonization of new hydrothermal vents following an eruption on Juan de Fuca Ridge. Deep-Sea Res. 44:1627-1644. Turner, R.D., R.A. Lutz, and D. Jablonski. 1985. Modes of molluscan larval development at deep-sea hydrothermal vents. Biol. Soc. Wash. Bull. 6:167-184. Tyler, P.A. 1988. Seasonality in the deep sea. Oceanogr. Mar. Biol. Ann. Rev. 26:227-258. Tyler, P.A., and CM. Young. 1992. Reproduction of marine invertebrates in stable environments: The deep-sea model. Invert. Reprod. Dev. 22:185-192. Tyler, P.A. and CM. Young. 1999. Reproduction and dispersal at vents and cold seeps: A review. J. Mar. Biol. Assoc. U.K. (in press). Van Dover, C.L. 1994. In situ spawning of hydrothermal vent tube worms (Riftia pachyptila). Biol. Bull. 186:134-135. Van Dover, C.L., A.B. Williams, and J.R. Factor. 1984. The first zoeal stage of a

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hydrothermal vent crab (Decapoda: Brachyura: Bythograeidae). Proc. Biol. Soc.Wash. 97:413-418. Van Dover, C.L., J.R. Factor, A.B. Williams, and C.J. Berg, Jr. 1985. Reproductive biology of decapod crustaceans from hydrothermal vents. Biol. Soc. Wash. Bull. 6:223-227. Van Dover, C.L., C.J. Berg, and R.D. Turner. 1988. Recruitment of marine invertebrates to hard substrates at deep-sea hydrothermal vents on the East Pacific Rise and Galapagos spreading center. Deep-Sea Res. 35:1833-1849. Van Dover, C.L., D. Desbruyeres, M. Segonzac, T. Comtet, L. Saldanha, A. FialaMedioni, and C. Langmuir. 1996. Biology of the Lucky Strike hydrothermal field. Deep-Sea Res. 43:1509-1539. Van Dover, C.L., J. Trask, J. Gross, and A. Knowlton. 1999. Reproductive biology of free-living and commensal polynoid polychaetes at the Lucky Strike hydrothermal vent field (Mid-Atlantic Ridge). Mar. Ecol. Prog. Ser. (in press). Wiebe, P.H., N. Copley, C. Van Dover, A. Tamse, and F. Manrique. 1988. Deep-water zooplankton of the Guaymas Basin hydrothermal field. Deep-Sea Res. 35:9851013. Williams, A.B. 1980. A new crab family from the vicinity of submarine vents on the Galapagos Rift (Crustacea: Decapoda: Brachyura). Proc. Biol. Soc. Wash. 93:443472. Young, CM., E. Vazquez, A. Metaxas, and PA. Tyler. 1996. Embryology of vestimentiferan tube worms from deep-sea methane/sulfide seeps. Nature 381:514-515. Zal, F., D. Jollivet, P. Chevaldonne, and D. Desbruyeres. 1995. Reproductive biology and population structure of the deep-sea hydrothermal vent worm Paralvinella grasslei (Polychaeta: Alvinellidae) at 13°N on the East Pacific Rise. Mar. Biol. 122:637-648.

10 Community Dynamics When vent communities were discovered in 1977, geologists and biologists appreciated their transitory nature and puzzled over the hydrothermal cycle through which venting and fauna became established, evolved, and declined. Clambake, a field of dead clam shells on the Galapagos spreading center (fig. 10.1), provided compelling evidence that cessation of flow was catastrophic to a community (Corliss and Ballard 1977). Pompeiian lava flows on the East Pacific Rise obliterated entire communities or, worse for the empathic observer, covered some portion of a flourishing bed of mussels or clams, leaving untouched and unharmed the adjacent organisms. While the demise of vent systems had thus been witnessed, the early sequence of events that initiated venting was the subject of deduction and debate. A combination of scientific insight and serendipity led to the observation of a seafloor volcanic eruption in 1991 and the initiation of new vent sites, barely a decade after the early major biological expeditions to vents. Technological advances in remote sensing of seafloor volcanic events now allow scientists to respond to eruptions as they occur, giving biologists the opportunity to follow colonization of virgin vents. 10.1 THE EARLY WORK When vents were first discovered on the Galapagos spreading center and East Pacific Rise, biologists observed the patterns of animal distributions closely to deduce the sequence of colonization and succession that might characterize communities in what were obviously ephemeral habitats. At the 21°N site on the East Pacific Rise, Hessler et al. (1985) inferred that fluid flow changes over time within a vent field as a result of reorganization of subsurface plumbing caused by tectonic events, subsurface mineralization, and, ultimately, quenching of the heat engine underlying the field by cold seawater. These fluid-flow changes in turn affect the composition of the vent community, most conspicuously by die-off of populations of tubeworms or clams. With only two visits separated by a 5.25 yr interval (1979-1985), Hessler's time-series work at Rose Garden laid the foundation for the succes-

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Figure 10.1. Clam Bake on the Galapagos Spreading Center showing the remains of a once active clam (Calyptogena magnified) bed. Photo courtesy of Woods Hole Oceanographic Institution.

sional sequence of a "typical," low-temperature, East Pacific Rise/Galapagos vent site (Hessler et al. 1988). Vestimentiferan tubeworms were hypothesized to be among the initial colonists, and Rose Garden in 1979, one of the first vent sites ever visited, was in an early stage of development. Mussels, being mixotrophs tolerant of a wide range of hydrothermal conditions and capable of shifting to optimize their position in the fluid flow, are effective competitors in the system and eventually overwhelm the tubeworms. Based on an assessment of size and growth rates, clams and mussels enter the system at approximately the same time. Other elements of the community (suspension-feeders, grazers, etc.) are less well constrained in the cycle, presumably entering wherever they can find refuge from predation and suitable

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food resources. Mussels are likely to be among the last survivors in the system, apart from the final populations of carnivores and scavengers. What is "typical" along a lengthy stretch of mid-ocean ridge is subject to some debate. Rose Garden and other Galapagos spreading center vents lack the high-temperature black-smoker habitat that is found at all other vent fields to date. And while Galapagos sites are characterized by abundant bivalves, clams are extremely rare in vent fields at 13°N on the adjacent East Pacific Rise, and mussels, while present at 13°N, never form the extensive beds commonly observed at Galapagos vents or even just a few degrees south on the East Pacific Rise at 9-10°N (Desbruyeres 1995). Fustec et al. (1987) undertook a comparison of vent community structure at 13°N based on site visits separated by 2 yr (1982-1984). Seven sites along a north-south transect were studied. At two of these sites, there was little change in community structure apart from noticeable growth in tubeworm colonies and increases in serpulid worm abundances in the peripheral areas. Mass wasting of a large tubeworm colony, either from its own weight or from tectonic activity, accounted for its demise and for reorganization of fluid flow to support colonization by alvinellid polychaetes that tolerate high temperatures. At other sites, Fustec et al. (1987) noted regression of peripheral serpulid worm populations (presumably in response to changes in availability of suspended particles) and migration of alvinellid polychaetes as they tracked the precipitation of new sulfide habitat. Although there were only relatively minor changes within subpopulations of fauna at 13°N sites over a 2 yr interval, in subsequent years (through 1994) 4 of Fustec's original 7 sites had shut down completely or greatly degenerated (Desbruyeres 1995). Where this happened, tubeworms died off quickly and scavenger concentrations (especially turrid gastropods and galatheid squat lobsters) increased. Mussels were able to teeter on the edge of survival for more than 6 yr after venting had ceased at one site. Another site, formerly marked by small populations of mussels and no detectable thermal anomalies, was reactivated and colonized by two tubeworm species (Tevnia jerichonana and Riftia pachyptila) and bythograeid crabs. A fossil 75yr-old sulfide structure was also reactivated and colonized by alvinellid polychaetes. Early explorations of the superfast-spreading southern East Pacific Rise at 17°S provided the first glimpse of sites thought to be in the early stages of colonization immediately following a volcanic eruption (Juniper et al. 1990). Volcanic rock in the region was so fresh that hairline fissures were rare and the surfaces were unweathered and glassy (Renard et al. 1985). Active lowtemperature vents were colonized by suspension feeders, including mobile shrimp and amphipods and sessile serpulid worms. Tubeworms (Riftia pachyptila and Tevnia jerichonana) were present only as isolated individuals or small clumps.

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Clearly, extant hydrothermal sites on the East Pacific Rise can undergo intervals of relative stability and dramatic change over periods of years without any surface expression of eruptive activity, although reactivation of sites may be elicited by subsurface dike activity. Desbruyeres (1995) emphasizes the lack of synchrony and independent evolution in community dynamics along a given ridge segment for systems that have not undergone recent eruptive activity. The result is a complex mosaic of habitat of different ages and relative abundance of species in both time and space (Van Dover and Hessler 1990). In contrast, as will be reported below, where new vents have been established following a major eruptive event, there can be extraordinary synchrony in community development along at least 1.4 km of ridge axis (Shank et al. 1998), when the development is witnessed from its earliest, "time zero" inception. 10.2 DYNAMIC SUCCESSION AT NORTHEAST PACIFIC VENTS There is a different style of venting and faunal "texture" at vents on the ridges of the northeast Pacific, compared to that found on the East Pacific Rise. While some vent taxa colonize extensive low-temperature vent fields on bare basalt (notably the strawlike form of the tubeworm Ridgeia piscesae; plate II, middle row, center panel), most of the fauna is associated with large, topographically complex sulfide mounds with heterogeneous styles of fluid flow, including black smokers, flanges, shimmering surfaces, and areas of less obvious venting. Dominant species are heterogeneously distributed over the surface of the mounds, with distributions apparently controlled primarily by environmental features, including fluid flow, chemistry, substratum, and temperature. One site known as Smoke and Mirrors (S&M), named for the black smokers and reflecting pools of hot water trapped beneath flanges, has been the subject of repeated detailed mapping efforts that reveal how the community has changed over time (figs. 10.2, 10.3; Sarrazin et al. 1997). S&M is located in the Main Endeavor Field on the Juan de Fuca Ridge (fig. 2.26). Six distinct faunal assemblages (differing in species composition or in relative abundances of species) can be recognized on the S&M sulfide mound at the decimeter scale using video imagery (table 10.1). During a 4 yr interval, hydrothermal activity at S&M evolved from primarily focused flow through black smokers to increasingly extensive diffuse flow. Specific assemblages tracked these changes, indicating a link to fluid-flow conditions. Sarrazin et al. (1997) found no evidence for ordered, or linear, succession of species (fig. 10.4A); that is, Assemblage I did not develop into Assemblage II, etc. Instead, S&M supports a temporally and spatially dynamic mosaic of species assemblages that respond to the frequent disturbances that alter flow

CHAPTER 10

Giraffe Dog Head Northern Cluster Southern Cluster

Legend: A Black Smoker 3 Sulfide Flange with Pool 0 Beehive 1 Sulfide Talus h Fault © Beehive covered by Paralvinella sulfincola *o. Sulfide'Landslide1 (8) Elevation of sulfide edifice (m)

Figure 10.2. Structural changes at the Smoke and Mirrors (S&M) sulfide mound (Main Endeavour Field, Juan de Fuca Ridge). Observations were made in September 1991 (A), July 1994 (B), and September 1995 (C). From Sarrazin et al. 1997.

conditions and substratum stability. The result is a diverse range of possibilities for assemblage replacement over time, analogous to change observed in plant communities under conditions of chronic disturbance (fig. 10.4B; Horn 1976). While there may be no ordered succession at the S&M site, there are assembly rules, such that in a transitive system progressing from high to low temperature there is a predictable sequence of assemblages or "dynamic succession" (fig. 10.5; Sarrazin et al. 1997). Perturbations can cause abrupt changes in fluid flow that initiate jumps in either direction, but forces mediating assemblage transitions are not strictly physical. Two biological processes influencing transitions from one assemblage to another are recognized in this system: (1) High-temperature sulfides are populated by a single paralvinellid polychaete species (Paralvinella sulfincola). These polychaete populations (Assemblage I) mediate deposition of the mineral marcasite, which then allows colonization by a second paralvinellid polychaete species (Paralvinella palmiformis), creating Assemblage II (Juniper et al. 1992). (2) Assemblages IV and V are both dominated by tubeworms (Ridgeia piscesae) and the same three gastropod species. They are visually distinctive because

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Southern Cluster\ Northern Cluster

1991

Dog Head

1994

(HiT) , III (MedT) 3 IV ( V,Vi(LoT) j 1 Uncolonized

1995

Figure 10.3. Changes in assemblage distribution mapped on the west face of the Smoke and Mirrors sulfide mound from 1991 to 1995. Species that make up assemblages are indicated in table 10.1. From Sarrazin et al. 1997.

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TABLE 10.1. Distinctive assemblages at the Smoke and Mirrors (S&M) site at the Main Endeavour Field (Juan De Fuca Ridge) based on video imagery Assemblage II Organisms Tubeworms Ridgeia piscesae Paralvinella sulfincola Paralvinella palmiformis Gastropods Bacterial mats Polynoid polychaetes Pycnogonids Protozoans (folliculinids) Habitat Characteristics Flow Features Visible shimmering Relative temperature Substratum: Sulfide Basalt

-

III

IV

VI

(+)

+++

+++

—

+++

+++

(+)

— (+)

+++ — +++

-

-

+ —

+

+

+

high

mediumhigh

medium

+

+

+

low

low

low

From Sarrazin et al. 1997. Abundances: — = absent; + = low abundance or present (shimmering); + + = medium abundance; + + + = high abundance; ( + ) = occasionally present. Temperature: low = 0 to 10°C; medium = 10 to 20°C; high = above 20°C.

tubeworms of Assemblage IV are shorter. Growth of the tubeworms results in the transition of Assemblage IV into Assemblage V (plate II, middle row, right panel). Repeated visits to vent sites and careful imaging thus reveal that changes take place on time scales of years, but only by extended monitoring of shortterm dynamics will interactions among species and other processes that influence faunal composition and distributions be determined.

Observed Community Changes on S&M < •

B

Chronic Disturbance Model A w*

*>. B
600 |xM), no methanotrophic symbioses are evident at Monterey Canyon seeps (Barry et al. 1997a). Indeed, methanotrophic invertebrate symbioses are not yet recognized from any eastern or western Pacific sites, seep or vent, although methane is clearly an autotrophic resource for free-living microorganisms at some Pacific hydrothermal vents (e.g., Endeavour Field, Juan de Fuca Ridge; de Angelis et al. 1991). In contrast, at Atlantic seep and vent sites in various geological and geochemical settings, methanotrophic mussels, pogonophorans, or sponges are characteristic. Barry et al. (1996, 1997a) hypothesize that evaporite deposits, common along continental margins in the Atlantic but rare in the Pacific, may be important in enhancing habitat quality for methanotrophic symbioses. The assumption is that the high density of methane-rich brines evolved from the evaporites reduces the dilution rate and advection of methane from the seep locale, making the substrate more readily available for uptake. A counterargument to this hypothesis is the presence of methanotrophic symbioses in habitats where evaporites are not present (e.g., Barbados Subduction Zone seeps, above). 12.2.5 Northern California Methane Hydrate Field Geophysical surveys off the Eel River Basin in northern California provide seismic records of an extensive methane hydrate field underlying sediments at shallow to bathyal depths (450 to >3000 m; Field and Kvenvolden 1987). This geochemical setting is comparable to that found at hydrocarbon seeps of the Louisiana Slope. Trawls taken at 400-600 m sampled vesicomyid clams tentatively identified as Calyptogena pacifica, and stable isotope evidence suggests that these bivalves, like their congeners, support sulfide-oxidizing chemoautotrophic endosymbioses (Kennicutt et al. 1989). 12.2.6 Guaymas Basin Transform Margin Seeps Hydrocarbon seeps are located only a few kilometers away from high-temperature hydrothermal vents in the Southern Trough of Guaymas Basin (Gulf of California). The seep setting (1550 m) is associated with a seismically active, strike-slip transform fault, with chemosynthetic communities clustered around outcrops of methanogenic carbonate and shallow mud-filled craters or pockmarks. Despite their proximity to one another and the shared sediment regime, faunas of the vent and seep sites of Guaymas Basin are strikingly dissimilar (Simoneit et al. 1990), placing emphasis on the observation that vent and seep species are adapted to conditions specific to their respective environments, despite alliances at higher taxonomic levels. While

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Riftia pachyptila dominates the landscape at Guaymas hot springs, Lamellibrachia sp. is characteristic of the Guaymas seep environment. Vesicomyid clams collected from Guaymas seeps are distinct from the vent vesicomyid species but probably belong to the same species complex as clams found at Oregon and Monterey seep sites (Peek et al. 1997). 12.2.7 Shallow-Water Hydrocarbon Seeps Natural hydrocarbon seeps are common in some shallow-water settings, but to date, chemoautotrophic endo- or episymbioses at these sites are not described. At the Isla Vista oil seeps off Santa Barbara, California (20 m), mats of bacteria {Beggiatoa sp.) are observed (Montagna and Spies 1985), along with enrichments of nematodes and other macrofauna. A chemical-trophic pathway has been proposed as follows (Spies and Des Marais 1983): hydrocarbon -> sulfate-reducing microorganisms —» sulfide —> Beggiatoa sp. —> nematodes —> other infauna. Steichen et al. (1996) confirm a positive correlation between nematode density and hydrocarbon concentration. Shortterm (24 hr) colonization experiments with hydrocarbon-enriched sediments show preferential migration of nematodes to hydrocarbon treatments over controls by a factor of 3 (fig. 12.20; Steichen et al. 1996). While these nematode populations seem likely candidates as hosts for chemoautotrophic bacteria, either on their cuticle or as endosymbionts, such symbioses are not reported for these populations to date. 12.2.8 British Columbia Fjords Large samples of pogonophorans are reported in invertebrate resource surveys undertaken in open seas and fjords of British Columbia from 1950 to 1972 (Southward and Southward 1992). The dominant species, Polybrachia canadensis, grows in narrow (0.4 to 1.0 cm) tubes up to 50 cm in length. The species was found to have a broad depth range from 200 m in British Columbia fjords to >2600 m in nearby open-ocean environments. At offshore sites, the pogonophoran is presumed to occupy seep sites; in fjords, Southward and Southward (1992) suggest that it lives in soft mud bottoms, where reducing conditions are established by sulfate-reducing bacteria involved in decomposition of rich organic debris of terrestrial forest origin (mainly wood and bark), but no ecological studies of these populations have yet been undertaken. Pogonophorans are also known from Norwegian fjords (Southward 1979). 12.2.9 Aleutian Subduction Zone Among the most recent Pacific seep sites to be discovered are the Edge and Shumagin sites located in the Gulf of Alaska in the eastern Aleutian subdue-

385

COGNATE COMMUNITIES

6B

O