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. I.Deep Sea Life strongly influenced by environmental conditionsLife strongly influenced by environmental conditions A.Conditions 1.Temperature Cold – Typically -1 to 4 o CCold – Typically -1 to 4 o C ExceptionsExceptions Deep Mediterranean is ca. 13 o CDeep Mediterranean is ca. 13 o C Red Sea can be 21.5 o C @ 2000 m depthRed Sea can be 21.5 o C @ 2000 m depth Weddell Sea can be -1.9 o CWeddell Sea can be -1.9 o C Hydrothermal vent effluent can approach 400 o CHydrothermal vent effluent can approach 400 o C 2.Pressure Increases predictably by 1 atmosphere (14.7 psi) every 10 mIncreases predictably by 1 atmosphere (14.7 psi) every 10 m Mean depth of oceans – 3800 m = 5600 psiMean depth of oceans – 3800 m = 5600 psi Affects biological molecules – Membranes, enzymesAffects biological molecules – Membranes, enzymes 3.Light Decreases with depthDecreases with depth Sunlight present in mesopelagic zone; absent below 1000 mSunlight present in mesopelagic zone; absent below 1000 m Affects development of eyesAffects development of eyes

4. I.Deep Sea A.Conditions 4.Dissolved Oxygen Near saturation and not limiting in most of the deep seaNear saturation and not limiting in most of the deep sea Exceptions: OMZ and certain enclosed basins (Santa Barbara Basin, Cariaco Basin, Black Sea)Exceptions: OMZ and certain enclosed basins (Santa Barbara Basin, Cariaco Basin, Black Sea) OMZ and anoxic basins may act as barriersOMZ and anoxic basins may act as barriers 5.Substrate Exposed hard rock is uncommonExposed hard rock is uncommon Biogenic hard substrate may be importantBiogenic hard substrate may be important Sediment is commonSediment is common Continental margins – coarse terrigenous materialContinental margins – coarse terrigenous material Deep-sea floor – biogenic oozes, terrigenous claysDeep-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 watersDeep-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. How do OMZ species adapt to low levels of oxygen? Metabolic rate (O 2 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. I.Deep Sea A.Conditions 4.Dissolved Oxygen Near saturation and not limiting in most of the deep seaNear saturation and not limiting in most of the deep sea Exceptions: OMZ and certain enclosed basins (Santa Barbara Basin, Cariaco Basin, Black Sea)Exceptions: OMZ and certain enclosed basins (Santa Barbara Basin, Cariaco Basin, Black Sea) OMZ and anoxic basins may act as barriersOMZ and anoxic basins may act as barriers 5.Substrate Most of deep sea floor covered by sedimentsMost of deep sea floor covered by sediments Margins – Coarse terrigenous sedimentsMargins – Coarse terrigenous sediments Basins – Biogenic oozes (>30% biogenic skeletal material) and terrigenous clays (depth related)Basins – Biogenic oozes (>30% biogenic skeletal material) and terrigenous clays (depth related) Siliceous oozes – Diatoms (high latitudes) or radiolarians (tropics)Siliceous oozes – Diatoms (high latitudes) or radiolarians (tropics) Calcareous oozes – Foraminiferans (productive areas)Calcareous oozes – Foraminiferans (productive areas) Low organic content (typically <1%)Low organic content (typically <1%) Exposed hard substrate uncommonExposed hard substrate uncommon Rocks, manganese nodules, biogenicRocks, manganese nodules, biogenic

9. I.Deep Sea A.Conditions 6.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 weeksTypically last days to weeks Tidal currentsTidal currents Source of temporal and spatial variabilitySource of temporal and spatial variability 7.Food Supply Variable in time and spaceVariable in time and space Seasonal variationSeasonal variation Seasonality in productivity, migration patterns, storms, etc.Seasonality in productivity, migration patterns, storms, etc. May produce seasonal patterns in biological processes (Ex:May produce seasonal patterns in biological processes (Ex: behavior, feeding, metabolism, reproduction, recruitment) Episodic large inputs may introduce variability on other time and space scalesEpisodic large inputs may introduce variability on other time and space scales 8.Trends Gigantism – Ex: Xenophyophores, Amphipods, IsopodsGigantism – Ex: Xenophyophores, Amphipods, Isopods Miniaturization – Ex: Ostracods, Tanaids, Harpacticoid CopepodsMiniaturization – Ex: Ostracods, Tanaids, Harpacticoid Copepods

10. Philippine Trench Hirondellea gigas – Scavenging Amphipods

11. I.Deep Sea A.Conditions 6.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 weeksTypically last days to weeks Tidal currentsTidal currents Source of temporal and spatial variabilitySource of temporal and spatial variability 7.Food Supply Variable in time and spaceVariable in time and space Seasonal variationSeasonal variation Seasonality in productivity, migration patterns, storms, etc.Seasonality in productivity, migration patterns, storms, etc. May produce seasonal patterns in biological processes (Ex:May produce seasonal patterns in biological processes (Ex: behavior, feeding, metabolism, reproduction, recruitment) Episodic large inputs may introduce variability on other time and space scalesEpisodic large inputs may introduce variability on other time and space scales 8.Trends Gigantism – Ex: Xenophyophores, Amphipods, IsopodsGigantism – Ex: Xenophyophores, Amphipods, Isopods Miniaturization – Ex: Ostracods, Tanaids, Harpacticoid CopepodsMiniaturization – Ex: Ostracods, Tanaids, Harpacticoid Copepods

13. I.Deep Sea B.Fauna Most animal phyla present Total faunal abundance decreases sharply with depth PPelagic 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 thatAsteroids important to 7000 m and absent below that

14. I.Deep Sea B.Fauna Trophic modes Detritivores and scavengers dominantDetritivores 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/techhttp://news.bbc.co.uk/1/hi/sci/tech Dec 11 2006

16. I.Deep Sea B.Fauna Fishes relatively scarce and modified to various degrees, compared to shallow living relativesFishes 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 swimmingTypically 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 & isopodsMost important mobile scavengers in deep sea, along with amphipods & isopods Many apparently find food using olfactionMany apparently find food using olfaction Some sit-and-wait predators (e.g. Bathypterois)Some sit-and-wait predators (e.g. Bathypterois) Some nomadic foragers (e.g. Coryphaenoides)Some nomadic foragers (e.g. Coryphaenoides)

17. Bathypterois Lycodes Coryphaenoides

19. I.Deep Sea B.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) Whale skull

20. CrinoidsGorgonians Antipatharians Barnacle

21. Stalked tunicateBryozoan Brachiopods

22. I.Deep Sea C.Diversity Through 1960s, deep sea perceived as highly uniform and consistent over time/space Prevailing ecological theory predictedPrevailing 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. I.Deep Sea C.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. I.Deep Sea C.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. I.Deep Sea C.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. I.Deep Sea C.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. I.Deep Sea C.Diversity 1. 1.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 1) 1)Processes that establish diversity (speciation) 2) 2)Process that maintain diversity (extinction)

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

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 Vertical migrators move to regions with more food Swept over seamounts by currents Swept over seamounts by currents Trapped on top at dawn Trapped on top at dawn Abundance of predators high, musculature robust, but SLOW growth 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 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 Capacity Adaptations: adjust rates of life in accord with the abiotic and biotic conditions

41. ‘Rate of living’ falls for visual predators, but not for 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. Reduced intensity of locomotory activity Reduced intensity of locomotory activity less reliance on visual predation = lower metabolic capacity. Reduced muscle protein levels Reduced muscle protein levels = lower costs of maintenance metabolism & growth Lower O 2 consumption Lower O 2 consumption Reduced/Absent swim bladders; reduced calcification Reduced/Absent swim bladders; reduced calcification Migrators and Non-Migrators differ Migrators and Non-Migrators differ Capacity Adaptations: conclusions

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

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

46. PRESSURE EFFECTS IN THE LIQUID PHASE— PROTEIN conformational changes a problem! Movement during substrate binding/release Movement during substrate binding/release Subunit polymerization 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 activityHigh resistance--inhibition

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

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 Temperature (°C) Viscosity A B C A B C Pressure (atms)