Why should we bother to study deep-sea biology?

1. Why should we bother to study deep-sea biology? “..we know more about the moon’s behind than the ocean’s bottom…” Dr. Cindy Lee Van Dover New Yorker classic

2. Most of “biology” (~80%) takes place in the deep sea:The deep sea is the most common habitat in the biosphere! Average depth = 3,800 m

3. Deep Sea • Life strongly influenced by environmental conditions • Conditions • Temperature • Cold – Typically -1 to 4 oC • Exceptions • Deep Mediterranean is ca. 13 oC • Red Sea can be 21.5 oC @ 2000 m depth • Weddell Sea can be -1.9 oC • Hydrothermal vent effluent can approach 400 oC • Pressure • Increases predictably by 1 atmosphere (14.7 psi) every 10 m • Mean depth of oceans – 3800 m = 5600 psi • Affects biological molecules – Membranes, enzymes • Light • Decreases with depth • Sunlight present in mesopelagic zone; absent below 1000 m • Affects development of eyes

4. Deep Sea • Conditions • Dissolved Oxygen • Near saturation and not limiting in most of the deep sea • Exceptions: OMZ and certain enclosed basins (Santa Barbara Basin, Cariaco Basin, Black Sea) • OMZ and anoxic basins may act as barriers • Substrate • Exposed hard rock is uncommon • Biogenic hard substrate may be important • Sediment is common • Continental margins – coarse terrigenous material • Deep-sea floor – biogenic oozes, terrigenous clays • Deep-sea sediments typically very low in organic carbon – 0.5% beneath productive areas and <0.1% beneath oligotrophic waters

5. Oxygen Minimum Zone (OMZ)

6. Oxygen Minimum Zone (OMZ) • How do OMZ species adapt to low levels of oxygen? • Metabolic rate (O2 consumption) declines • Gill ventilation rates increase • Hemoglobin binds oxygen at lower saturation • Gene expression: enzyme isoforms for anaerobiosis • Some may be food-deprived

7. Oxygen Minimum Zone (OMZ)

8. Deep Sea • Conditions • Dissolved Oxygen • Near saturation and not limiting in most of the deep sea • Exceptions: OMZ and certain enclosed basins (Santa Barbara Basin, Cariaco Basin, Black Sea) • OMZ and anoxic basins may act as barriers • Substrate • Most of deep sea floor covered by sediments • Margins – Coarse terrigenous sediments • Basins – Biogenic oozes (>30% biogenic skeletal material) and terrigenous clays (depth related) • Siliceous oozes – Diatoms (high latitudes) or radiolarians (tropics) • Calcareous oozes – Foraminiferans (productive areas) • Low organic content (typically <1%) • Exposed hard substrate uncommon • Rocks, manganese nodules, biogenic

9. Deep Sea • Conditions • Currents • Generally slow – Mean speeds typically <5 cm s-1, with peaks less than 20 cm s-1 in most areas • Periodically, certain areas experience benthic storms • Typically last days to weeks • Tidal currents • Source of temporal and spatial variability • Food Supply • Variable in time and space • Seasonal variation • Seasonality in productivity, migration patterns, storms, etc. • May produce seasonal patterns in biological processes (Ex:behavior, feeding, metabolism, reproduction, recruitment) • Episodic large inputs may introduce variability on other time and space scales • Trends • Gigantism – Ex: Xenophyophores, Amphipods, Isopods • Miniaturization – Ex: Ostracods, Tanaids, Harpacticoid Copepods

10. Philippine Trench Hirondellea gigas – Scavenging Amphipods

11. Deep Sea • Conditions • Currents • Generally slow – Mean speeds typically <5 cm s-1, with peaks less than 20 cm s-1 in most areas • Periodically, certain areas experience benthic storms • Typically last days to weeks • Tidal currents • Source of temporal and spatial variability • Food Supply • Variable in time and space • Seasonal variation • Seasonality in productivity, migration patterns, storms, etc. • May produce seasonal patterns in biological processes (Ex:behavior, feeding, metabolism, reproduction, recruitment) • Episodic large inputs may introduce variability on other time and space scales • Trends • Gigantism – Ex: Xenophyophores, Amphipods, Isopods • Miniaturization – Ex: Ostracods, Tanaids, Harpacticoid Copepods

13. Deep Sea • Fauna • Most animal phyla present • Total faunal abundance decreases sharply with depth • Pelagic community biomass at 4000 m ca. 1% of surface values • Sinking food accumulates at interfaces (e.g. sediment surface) • Pelagic biomass 10 mab double that at 200 mab (Wishner) • Changes in relative abundance of faunal taxa with depth • Kurile-Kamchatka Trench - Sponges dominant component of benthic macro-/megafauna to 2000 m • Holothuroids important below 2000 m and dominant below 8000 m • Asteroids important to 7000 m and absent below that

14. Deep Sea • Fauna • Trophic modes • Detritivores and scavengers dominant • Good chemosensory capabilities • Distensible guts • Predators relatively uncommon • Opportunistic feeding strategies especially useful • Why?

15. Scavengers converge on a food fall 2000m deep off coast of Mexico http://news.bbc.co.uk/1/hi/sci/tech Dec 11 2006

16. Deep Sea • Fauna • Fishes relatively scarce and modified to various degrees, compared to shallow living relatives • Typically have reduced or large eyes, watery tissues, low muscle protein content, reduced skeletons, oil-filled swim bladders, body forms not designed for rapid swimming • Most important mobile scavengers in deep sea, along with amphipods & isopods • Many apparently find food using olfaction • Some sit-and-wait predators (e.g.Bathypterois) • Some nomadic foragers (e.g.Coryphaenoides)

17. Coryphaenoides Bathypterois Lycodes

19. Whale skull • Deep Sea • Fauna • Sessile organisms may be attached to hard substrate of many types • Exposed rock • Manganese nodules or bits of geological material • Biogenic hard substrate (sponges, shells, wood, bone) • Occurrence limited by • Available substrate • Flux of POM (food)

20. Crinoids Gorgonians Barnacle Antipatharians

21. Brachiopods Bryozoan Stalked tunicate

22. Deep Sea • Diversity • Through 1960s, deep sea perceived as highly uniform and consistent over time/space • Prevailing ecological theory predicted that spatial and temporal uniformity plus sparse, low-grade food resources should lead to an equilibrium condition with a few competitively dominant species • Mid-1960s: epibenthic sled developed and deployed by Howard Sanders and Bob Hessler (WHOI) • Covered much smaller area than conventional deep-sea bottom trawl but sampled upper few cm of sediments and retained organisms in a fine-meshed sampling bag • Samples effectively ended notion of low diversity in deep sea

24. Deep Sea • Diversity • Number of spp. within many taxa (e.g. bivalves, gastropods, polychaetes) tends to increase from surface to mid-slope depths (ca. 2000 m) then decrease with increasing depth

25. Deep Sea • Diversity • Trend suggests low species diversity in deep sea • Pattern could be artifact of reduced sampling effort with increasing depth • How do we know if we’ve sampled enough area and organisms to generate a meaningful picture of the actual diversity of the deep-sea benthic community?

27. Deep Sea • Diversity • Rarefaction curves for most deep-sea habitats never approach an asymptote • Largest quantitative data set to date for deep-sea macro- and meiofauna was obtained during early 1980s from Atlantic slope off US • 554 box cores (30 x 30 cm) from depths to 3000 m • Over 1600 species identified • Factoring out depth, 233 cores taken at 2100 m depth along 176-km long transect • Samples: 798 species from 14 invertebrate phyla

28. Deep Sea • Diversity • Rarefaction curves for most deep-sea habitats never approach an asymptote • Expected number of species increasing at about 25 m-2 • Prediction: 5-10 million species in deep sea!! • No single species >8% of community • Similar to other deep-sea sites (except HEBBLE, where single species may be 50-64% of community)

29. Deep Sea • Diversity • Patterns • Deep-sea species diversity differs among ocean basins • Differences may be related to oxygen content, nutritional input, geological history, etc. • High species diversity may be due to • Processes that establish diversity (speciation) • Process that maintain diversity (extinction)

30. Deep Sea • Diversity • Maintenance • Equilibrium processes • Ex: Resource partitioning, habitat partitioning • Species that are well-adapted to a particular set of conditions co-exist at densities near carrying capacity of environment • Disequilibrium processes • Ex: Local disturbance • Patchy habitat supports many populations at early growth stages, hence at relatively low densities (not near carrying capacity), reducing competitive exclusion as an important structuring mechanism • Connell (1978) suggested that highest diversity maintained at intermediate levels of disturbance

32. Hydrothermal Vents

34. Hydrothermal Vent fluids: Acidic (pH 2.8), Hydrogen Sulfide >1mM Temperature up to 400°C

35. Chemosynthetic Food Web: Sulfide Oxidizing Bacteria Riftia pachyptila (2 m tall)

36. Fine-scale adaptation to thermal niches Distribution patterns at the vents. Black Smoker Warm vent Alvinella pompejana & A. caudata Bythograea thermydron Riftia pachyptila Cool vent Cool vent Deep Sea- Vent H2S 0->1mM Temp 2-400°C pH 8 -2.8 Bathymodiolus thermophilus Calyptogena magnifica

37. Vents are short-lived.

38. Seamounts have higher biomass and different communities

39. Seamount Food Webs • Vertical migrators move to regions with more food • Swept over seamounts by currents • Trapped on top at dawn • Abundance of predators high, musculature robust, but SLOW growth

40. What types of adaptations are needed to support life at depth? • Tolerance Adaptations: adapt to perturbation from abiotic conditions, e.g., hydrostatic pressure and temperature • Capacity Adaptations: adjust rates of life in accord with the abiotic and biotic conditions

41. ‘Rate of living’ falls for visual predators, but notfor gelatinous ‘float and wait’ predators. For review, see: Childress, J.J. (1995). Trends Ecol. Evol. 10: 30-36

42. “Float-and-wait” feeding may become more important than intense predation with reduced visual predation

43. Capacity Adaptations: conclusions • Reduced intensity of locomotory activity less reliance on visual predation = lower metabolic capacity. • Reduced muscle protein levels = lower costs of maintenance metabolism & growth • Lower O2 consumption • Reduced/Absent swim bladders; reduced calcification • Migrators and Non-Migrators differ

44. Tolerance Adaptations:Pressure & Temperature • Adaptive Solutions: a cooperative venture between macro- and ‘micro’molecules. • Proteins: amino acid substitutions • Enhance flexibility • Conserve Km (substrate binding) at habitat pressure • Osmolytes: protein-stabilizing solutes • Lipids & membranes: fluidity-effects • Homeoviscous adaptation • More unsaturated acyl phospholipid chains

45. Gas-filled spaces—obvious problemsV = nRT/P

46. PRESSURE EFFECTS IN THE LIQUID PHASE— • PROTEIN conformational changes a problem! • Movement during substrate binding/release • Subunit polymerization Lactate Dehydrogenase (LDH) Pyruvate + NADH + H+ lactate + NAD+

47. Pressure inhibits membrane-spanning proteins:resistance to conformational change. Membrane-spanning protein Conformational change Low resistance—high activity High resistance--inhibition

48. Homeoviscous Adaptation Shifts in acyl chain ‘saturation’ (double-bond content: =) saturated mono-unsaturated poly-unsaturated Viscous Fluid

49. Homeoviscous adaptation Change lipid composition (saturation of fatty acid side chains, cholesterol) Maintain stable fluidity at habitat conditions Preserve membrane permeability and membrane enzyme function C B A Viscosity A B C Temperature (°C) Pressure (atms)