The Ecology of Deep-Sea Hydrothermal Vents

"PREFACE xvii ACKNOWLEDGMENTS xix 1. The Non-Vent Deep Sea 3 1.1 The Physical Environment in the Deep Sea 4 1.2 The Deep-Sea Fauna 5 1.3 Deep-Sea Diversity 8 1.4 Biogeography and Population Genetics 11 1.5 Biochemical and Physiological Adaptations to the Deep-Sea Environment 13 1.6 Benthopelagic Coupling between Surface Productivity and the Deep Sea 15 1.7 Rates of Biological Processes in the Deep Sea 18 1.8 The Vent Contrast 19 References 20 2. Geological Setting ot Hydrothermal Vents 25 2.1 What Are Mid-Ocean Ridges? 25 2.1.1 How Spreading Rates for Ridge Axes Are Determined 28 2.1.2 Spreading Rates 29 2.1.3 Segmentation 31 2.1.4 Magma Supply and Spreading Rate 34 2.2 Back-Arc and Fore-Are Spreading Centers 36 2.3 Seamounts 37 2.4 Volcanic and Tectonic Seafloor Features 39 2.4.1 Crustal Structure 39 2.4.2 Volcanic and Tectonic Fissures 39 2.4.3 Lava Lakes, Drainback. Features, and Lava Pillars 41 2.4.4 Axial Boundary Faults 41 2.4.5 Lava Flow Morphologies 43 2.4.6 Emplacement of Lavas and the Time-Course of a Diking Event 43 2.4.7 Lava Dating 45 2.5 Deep-Sea Hydrothermal Fields 47 2.5.1 Missing Heat and Hydrothermal Cooling at Ridge Crests 47 2.5.2 Sulfide Deposits 48 Morphological Variations 48 Columnar Chimneys and Black Smokers 49 White Smokers 50 Beehives and Flanges 50 Complex Sulfide Mounds 53 Weathering of Seafloor Sulfides 56 Dimensions and Ages of Active Hydrothermal Fields 56 2.5.3 Low-Temperature Diffuse Flows 58 2.5.4 Sediment-Hosted Hydrothermal Systems 60 2.5.5 Ophiolites 61 Appendix 63 References 70 3. Chemical and Physical Properties of Vent Fluids 76 3.1 Submarine Hydrothermal Circulation Cells: High-Temperature Reaction Zones 76 3.2 Phase Separation 78 3.3 Flow Rates, Transit Times, and Temperature of Formation 80 3.4 End-Member Fluids 80 3.4.1 Composition 80 Basic Controls on Chemistry 81 3.4.2 Magmatic Inputs 82 3.4.3 Evolution of Vent-Fluid Chemistry 83 3.4.4 Back-Arc Fluid Chemistries 83 3.5 Thermal Radiation 84 3.6 Axial Low-Temperature, Diffuse-Flow Chemistry 85 3.6.1 Flow Rates, Temperature, and Temperature Variability 86 3.6.2 Silicate 87 3.6.3 Sulfide 87 3.6.4 Oxygen 89 3.6.5 Profiles of Oxygen, Sulfide, Silicate, and Temperature 89 3.6.6 Methane, Manganese, and Iron 91 3.6.7 Nitrogen and Phosphorus Compounds 92 3.7 Flank Low-Temperature Fluids 92 3.8 Global Fluxes and the Hydrothermal Influence on Ocean Chemistry and Currents 92 References 94 4. Hydrothermal Plumes 99 4.1 Anatomy of a Black-Smoker Plume 99 4.1.1 Orifice 99 4.1.2 Buoyant Plume 100 4.1.3 Effluent Layer 101 4.2 Megaplumes 104 4.3 Spatial and Temporal Distributions of Plumes 106 4.3.1 Relationship between Plume Distributions and Geophysical Parameters 106 4.4 Plume-DTiven Mesoscale Circulation 110 4.4.1 Plume Vortices 110 4.4.2 Advection and Downwelling 110 4.4.3 Basin-Scale Circulation 111 4.5 Diffuse-Flow Plumes 112 References 112 5. Microbial Ecology 115 5.1 Autotrophic Organisms at Vents 117 5.1.1 Nomenclature 117 5.1.2 Aerobic and Anaerobic Chemoautotrophy at Vents 117 Methanotrophy 119 5.1.3 Carbon Dioxide Fixation 120 5.1.4 Mixotrophy 120 5.1.5 Net Chemoautotrophic Production in Free-Living Hydrothermal-Vent Microorganisms 120 Alternatives to Chemoautotrophy 120 Organic Thennogenesis Hypothesis 121 Detrital Thennal Alteration Hypothesis 121 5.2 Ecology of Free-Living Microorganisms122 5.2.1 Microbial Habitats 122 5.2.2 Hyperthen-nophiles and Superthermophiles 122 Flange Microbial Ecology and the Archaea 125 Microorganisms in Black-Smoker Fluids 125 The ""Endeavour Model"" 125 The Subsurface Biosphere 127 5.2.3 Plume Microbiology 127 5.2.4 Suspended Microbial Populations 128 5.2.5 Microbial Community Composition 129 Dominance of a Single Bacterial Phylotype at a Mid-Atlantic Ridge Vent 130 Diversity and Community Structure in Microbial Mats, Loihi Seamount 130 Sulfur-Oxidizing Heterotrophs at Vents 132 5.2.6 Bacterial Blooms 132 5.2.7 Microbial Mats 134 5.2.8 The Link between Chemoautotrophic and Photosynthetic Processes 135 5.3 A Search for In Situ Bacterial Photosynthesis 137 5.4 Microbial Genesis of Hydrothermal. Mineral Deposits 137 5.5 Microbial Exploitation of Particulate Sulfides 138 5.6 Biotechnology 139 References 140 6. Symbiosis 145 6. 1. Discovery 145 6.1.1 Sustenance of Gutless Tubeworms 146 6.1.2 Endosymbiotic Bacteria in Vent Mollusks 150 6.1.3 Episymbionts 150 6.2 Methanotrophic Symbioses 153 6.2.1 Dual Symbioses 153 6.2.2 Methanotrophs in Sponges 156 6.3 Adaptive Characteristics of Symbiosis157 6.4 Host Nutrition 158 6.4.1 Digestive Enzymes 160 6.5 Symbiont Phylogeny 162 6.5.1 Endosymbiont Phylogeny and Host Fidelity 162 6.5.2 Episymbiont Phylogeny 165 6.6 Symbiont Acquisition 166 References 167 7. Physiological Ecology 173 7.1 Novel Metabolic Demands 173 7.2 Riftia pachyptila 174 7.2.1 Anatomy of a Tubeworm 174 7.2.2 The Tubeworm Environment 177 7.2.3 Adaptations for Carbon Uptake and Transport in Riftia pachyptila 177 Host Respiratory Inorganic Carbon 177 Environmental Sources of Inorganic Carbon and the Role of Carbonic Anhydrase 179 pH Regulation 180 Carbon Transport 182 Inorganic Carbon Capacity 182 Carbon Fixation Rates 182 7.2.4 Sulfide 183 Sulfide Toxicity 183 Sulfide Uptake and Transport 183 Coupling of Sulfide Detoxification and Energy Exploitation 186 7.2.5 Oxygen 187 7.2.6 Nitrogen 187 Nitrate Respiration 188 7.3 Seep Vestimentiferans and Methanotrophic Pogonophorans 188 7.4 Vent and Seep Bivalve-Mollusk Symbioses 189 7.4.1 Calyptogena magnifica 189 7.4.2 Bathymodiolid Mussels 192 Bathymodiolus thennophilus 192 Methanotrophic Mussels 193 7.4.3 Other Mollusk Symbioses 194 7.5 Physiological Ecology of Episymbiont-Invertebrate Associations 196 7.5.1 Alvinella pompejana 196 7.6 Sulfide Detoxification 197 7.7 Growth Rates 201 7.8 Thermal Adaptations 202 7.8.1 Indices of Thermal Tolerance and Adaptation 203 Thermal Tolerance in Alvinellid Species 204 7.9 Heavy Metals and Petroleum Hydrocarbons 208 7.10 Sensory Adaptations 209 7.10.1 Novel Photoreceptors in Vent Shrimp 210 7.10.2 Chemoreception 214 References 216 8. Trophic Ecology 227 8.1 The Food Web 227 8.1.1 The Rose Garden Food Web 228 8.2 Biological Sleuthing: Biomarker Assays 231 8.2.1 Stable Isotope Techniques 231 Notation 231 Stable Isotope Evidence for the Role of Free-Living Microorganisms in Vent Food Webs 233 8.2.2 Fatty Acids, Sterols, and Carotenoids 236 Fatty-Acid Nomenclature 236 Fatty-Acid Biomarkers 237 Comparison of Lipid Characteristics of Tubeworms (Riftia pachyptila), Mussels (Bathymodiolus thermophilus), and Amphipods (Halice hesmonectes) on the East Pacific Rise 237 ""Essential"" Fatty Acids 240 Lipid-Condition Indices 240 Sterols 240 Carotenoids 241 8.3 Integrated Approaches to Trophic Ecology 241 8.3.1 Trophic Ecology of Vent Mussels, Bathymodiolus thermophilus 242 8.3.2 Trophic Ecology of Vent Shrimp, Rimicaris exoculata, and an Anecdote about Who Eats Them 244 8.4 Export of Chemosynthetic Production from Vents 246 References 253 9. Reproductive Ecology 259 9.1 Gametogenesis 259 9.1.1 Evidence for Synchronous Gametogenesis 260 Environmental Cues 261 Recruited Synchrony 264 9.1.2 Evidence for Asynchronous Gametogenesis 264 Release of Gametes and Larvae 264 Riftia pachyptila 265 Bythograea sp. 266 Calyptogena soyae 266 9.2 Larval Development 267 9.2.1 Vestimentifera 268 9.2.2 Bathymodiolid Mussels 269 9.2.3 Bythograeid Crabs 271 9.2.4 Alvinocarid. Shrimp 271 9.3 Larval Dispersal and Retention 273 9.3.1 Alvinellid Dispersal Model 273 9.3.2 Plume Dispersal 276 9.3.3 Megaplume Dispersal 277 9.3.4 Mesoscale Flows 277 9.3.5 Dispersal by Non-Larval Stages 278 9.4 Settlement Cues 279 9.5 Recruitment 279 Appendix 281 References 285 10. Community Dynamics 290 10. 1 The Early Work 290 10.2 Dynamic Succession at Northeast Pacific Vents 293 10.2.1 High-Resolution Time-Series Studies on the Juan de Fuca Ridge 298 10.3 Community Dynamics on the Mid-Adantic Ridge 299 10.4 Eruptions 301 10.4.1 The 9'N Event 301 10.4.2 The CoAxial Event 303 10.4.3 Sweepstakes versus Predictable Sequences 308 References 309 11. Evolution and Biogeography 313 11.1 Origins of Vent Fauna 313 11.1.1 Immigrants from the Surrounding Deep Sea 313 11.1.2 Immigrants with Close Shallow-Water Relatives 314 11.1.3 Vent Taxa Shared with Other Chemosynthetic Ecosystems 314 Taxonomic Position and Origin of the Vestimentifera 316 11.1.4 Vent Taxa Shared with Both Other Chemosynthetic Ecosystems and Nonchemosynthetic Habitats 319 11.1.5 Specialized Taxa Found Only at Hydrothermal Vents 320 11.1.6 The ""Ancient"" Taxa 320 Ancient Barnacles 320 Ancient Mollusks 322 11.1.7 The Newman and McLean Hypothesis of Relict Vent Faunas 323 Hickman's Counternypothesis 323 11.2 Fossil Vent Communities 324 11.3 Vent Ecosystems as Refuges from Major Planetary Extinction Events 325 11.4 Species Diversity 325 11.5 Taxonomic Cautionary Tales 328 11.5.1 Cryptic Species 328 11.5.2 Phenotypic Plasticity 329 11.5.3 Ontogenetic Stages 329 11.6 Biogeography 330 11.6.1 Pacific Biogeographic Patterns 330 Missing Mussels (Bathymodiolus thermophilus) 331 Centers of Diversity along Linear Arrays of Habitat 332 North America as a Biogeographical Barrier 332 Mariana Hydrothermal-Vent Fauna 333 11.6.2 Paleotectonic Controls on the Atlantic Vent Fauna 335 11.6.3 Similarities among Global Vent Biogeographic Provinces 337 11.6.4 Biogeography of Fast- versus Slow-Spreading Centers 340 11.6.5 Physical Oceanography and Bathymetry 342 The Romanche Fracture Zone 342 11.6.6 Shallow-Water Vents 343 11.7 Gene Flow and Genetic Diversity 343 References 347 12. Cognate Communities 355 12.1 Atlantic Sites 360 12.1.1 Rofida Escaipment (Gulf of Mexico) 360 12.1.2 Louisiana Slope Hydrocarbon and Brine Seeps (Gulf of Mexico) 363 12.1.3 The Laurentian Fan 367 12.1.4 Barbados Subduction Zone 369 12.1.5 North Sea Pockmarks 372 12.1.6 Skagerrak Methane Seep 374 12.1.7 The Francois Vielieux 374 12.1.8 Coral Reefs 375 12.2 Pacific Sites 375 12.2.1 Cascadia Subduction Zone 375 12.2.2 Western Pacific Subduction Zones 376 Kaiko Project 376 Sagami Bay 379 12.2.3 Peruvian Subduction Zone 379 12.2.4 Monterey Canyon 381 12.2.5 Northern California Methane Hydrate Field 383 12.2.6 Guaymas Basin Transform Margin Seeps 383 12.2.7 Shallow-Water Hydrocarbon Seeps384 12.2.8 British Columbia Fjords 384 12.2.9 Aleutian Subduction Zone 384 12.3 Whale Skeletons 385 12.4 Fossil Seeps 389 References 39 13. Hydrothermal Systems and the Origin of Life 397 13.1 Earth's Early Environment 397 13.2 Evolution of Hydrothermal Systems 398 13.3 Heterotrophic versus Chemosynthetic Hypotheses for the Origin of Life 399 13.4 Evidence for Thermophilic, Autotrophic Ancestors 402 13.4.1 Wdchterhiiuser's Outline for the Origin and Evolution of Life 404 13.4.2 Synthesis of Organic Compounds in Hydrothermal Systems 406 13.5 Extraterrestrial Hydrothermal Systems and the Search for Life in Outer Space 407 References 409 INDEX 413"