The Ecology of Deep-Sea Hydrothermal Vents

About this book

Teeming with weird and wonderful life – giant clams and mussels, tubeworms, "eyeless" shrimp, and bacteria that survive on sulfur – deep-sea hot-water springs are found along rifts where sea-floor spreading occurs. The theory of plate tectonics predicted the existence of these hydrothermal vents, but they were discovered only in 1977. Since then the sites have attracted teams of scientists seeking to understand how life can thrive in what would seem to be intolerable or extreme conditions of temperature and fluid chemistry. Some suspect that these vents even hold the key to understanding the very origins of life. Here a leading expert provides the first authoritative and comprehensive account of this research in a book intended for students, professionals, and general readers. Cindy Lee Van Dover, an ecologist, brings nearly two decades of experience and a lively writing style to the text, which is further enhanced by two hundred illustrations, including photographs of vent communities taken in situ.

The Ecology of Deep-Sea Hydrothermal Vents begins by explaining what is known about hydrothermal systems in terms of their deep-sea environment and their geological and chemical makeup. The coverage of microbial ecology includes a chapter on symbiosis. Symbiotic relationships are further developed in a section on physiological ecology, which includes discussions of adaptations to sulfide, thermal tolerances, and sensory adaptations. Separate chapters are devoted to trophic relationships and reproductive ecology. A chapter on community dynamics reveals what has been learned about the ways in which vent communities become established and why they persist, while a chapter on evolution and biogeography examines patterns of species diversity and evolutionary relationships within chemosynthetic ecosystems.

Cognate communities such as seeps and whale skeletons come under scrutiny for their ability to support microbial and invertebrate communities that are ecologically and evolutionarily related to hydrothermal faunas. The Ecology of Deep-Sea Hydrothermal Vents concludes by exploring the possibility that life originated at hydrothermal vents, a hypothesis that has had tremendous impact on our ideas about the potential for life on other planets or planetary bodies in our solar system.

Contents

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 Seeps 384
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

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