3597_book.fm Page 211 Friday, May 20, 2005 6:26 PM Oceanography and Marine Biology: An Annual Review, 2005, 43, 211-278 © R N Gibson, R J A Atkinson, and J D M Gordon, Editors Taylor & Francis ZONATION OF DEEP BIOTA ON CONTINENTAL MARGINS ROBERT S CARNEY Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, Louisiana, U.S E-mail: rcarne1@lsu.edu Abstract Pioneering deep-sea surveys established that the fauna of the continental margins is zoned in the sense that individual species and assemblages occupy restricted depth bands It has been speculated that the causes of this wide-spread pattern might involve cold temperatures, high pressures and limited food availability Increased sampling over the past two decades has confirmed the global presence of depth zonation Well-defined zonation in the cold polar oceans and the warm Mediterranean indicate that temperature per se may be of less importance on ecological timescales than originally proposed Strong alternatives are range restriction by pressure and food availability Understanding of pressure physiology has advanced greatly, and it is to be expected that all deep organisms possess some form of genetic adaptation for pressure tolerance Since high pressure and low temperatures affect membrane and enzyme systems similarly, combined piezo-thermal thresholds may limit depth ranges There is a negative, exponential gradient of food availability caused by the decrease in labile carbon influx to bottom The TROX model linking carbon influx with interstitial oxygen levels has been successful in explaining deep distributions of benthic Foraminifera and may be more broadly applicable Current efforts to relate metazoan ranges to food availability are, however, hindered by limited understanding of how organisms recognise and utilise the nutritious content of detritus Thus, the exact controls of depth zonation remain conjectural Zonation studies are gaining in importance due to the increasing availability of deep fauna databases and the need to establish regulatory boundaries Future studies may benefit from a growing body of biogeographic theory, especially the understanding of bounded domains It is proposed that continental slope fauna may be more effectively studied if viewed as the overlapping of three components: species extending down from the shelf, species extending up from the abyss and species truly restricted to the slope Introduction Justification At the end of the first century of deep-sea ecological studies, comparatively scant trawling, dredging and coring had provided preliminary sketches of three large-scale patterns that seemed to widely characterise the biology of continental margins and abyssal plains (Mills 1978) The first pattern was that abundance measured as either population density or biomass decreased rapidly with depth similar to a negative exponential curve (Rowe 1983) The second pattern was zonation, a progression with depth of changing species such that continental slope fauna was distinct from that of the shelf above and abyssal plain below (Carney et al 1983) Finally, a pattern that along a wide depth transect, the greatest diversity of species lay at some mid or deeper level on the slope (Rex 1973, 1983) In the following decades, the global generality of the first pattern, biomass decrease, has 211 © 2005 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon 3597_book.fm Page 212 Friday, May 20, 2005 6:26 PM ROBERT S CARNEY been repeatedly confirmed However, the generality of diversity patterns continues to be debated (Gray 1994, Ugland et al 2003), and convincing causal mechanisms remain elusive (Gage 1996, Snelgrove & Smith 2002) In contrast, the validity of the zonation pattern has gone virtually unchallenged with the main discussion centering on causes The primary intent of this review is to place the accumulated findings about deep-sea faunal zonation into the similar scientific contexts of contemporary biogeography and oceanography The timeliness for the review, however, arises less from scientific advancement than from the rapidly increasing need for scientific-based management of deep-sea habitats and the rapidly changing mode of information synthesis Scientifically, the oceanographic community is making rapid progress toward whole-ocean syntheses of geology, geophysics and geochemistry The initial ‘generic bug’ phase of incorporating biological processes into these models is coming to an end as temporal and spatial variation must be understood The study of species distributions is part of the process of understanding what happens where and when Organisms of differing capabilities interact with their environment differently at different times and different places Depth zonation is directly relevant to understanding the processes on the deep-sea floor Resource exploitation for petroleum and fisheries beyond the depths of the continental shelf is now routine and advancing faster than any new understanding of how that environment functions (Glover & Smith 2003, Thiel 2003) Ideally, the effective management of any ecosystem should be based upon a full understanding of ecological processes (Carney 1997, Gage 2001) At a minimum, management requires maps: maps that delineate regions for use from regions of conservation, and maps that assign authority for regulation Extensively on land and to a lesser degree in the shallow (500 m is sufficient for visual prey detection and predator avoidance For some species, evolutionary success in this twilight zone required retention or adoption of locomotor capabilities of high metabolic cost These same capabilities have been lost during the evolution of fauna successful in deeper, dark waters While Childress exempts the benthos from the twilight hypothesis it may apply to some epifauna and benthopelagic forms Hydrostatic pressure and a piezo-barrier to distribution Hydrostatic pressure is the only environmental variable of the deep sea directly related to depth throughout the ocean The hydrostatic pressure experienced at the seafloor is determined by the weight of the overlying water column Precise calculation of pressure requires integration of the 217 © 2005 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon 3597_book.fm Page 218 Friday, May 20, 2005 6:26 PM ROBERT S CARNEY water’s mass from surface to bottom As defined by the equation of state (Feistal 2003), density varies through this depth range due to temperature, salinity, compression and local gravity The net effect is that pressure is a curvilinear function of depth and latitude A quadratic approximation (Saunders 1981) has been developed assuming a standard ocean at 0ºC and 35 Practical Salinity Units (PSU) from surface to bottom The high precision of this approximation is considered unnecessary for biological studies, and the common practice is to calculate pressure as a linear function of depth equating 10 m with an increase of 101.3 kPa (1 atmosphere) assuming a uniform water density of 1.028 103 kg m–3 The error associated with the simpler linear function vs the quadratic is only 1% at 1000 m and 2% at 10,000 m Basis for pressure effects The primary effect of high hydrostatic pressure on living and abiotic systems can be expected to cause shifts in chemical reaction rates because pressure is a thermodynamic parameter that accelerates or retards reaction rates The theoretical effect of pressure is predicted from the partial molar volume (volume of one mole) change during reaction Formally termed the ‘Le Châtelier effect’ (Hamann 1980), the thermodynamic equation predicts that pressure promotes reactions in which the molar volume of the products of a chemical reaction are less than the molar volumes of the reactants Pressure retards reactions in which there is a volume expansion Conceptually, the Le Châtelier effect applies to a wide range of biologically important reactions involving covalent bonding, ionic dissociations and enzyme kinetics The actual nature and extent of pressure effects, however, may or may not be well predicted for macromolecules and other complex systems in which structural conformations are important to reaction rates Pressure effects on abiotic chemical systems Sea water is a solution of ions, many of which are biochemically important The exact chemical species in which these ions exist is determined by dissociation kinetics As with other reactions, hydrostatic pressure can be important in controlling ionic equilibria and may be a factor in adaptation to great depth Unfortunately, the full breadth of pressure effects on biologically important inorganic reactions can not be determined since very few reactions have been studied at greatly elevated pressures The known effects are effectively treated by Millero (2000) The most often mentioned ionic equilibrium as a factor in depth restriction is the solubility of calcium carbonate Increased dissolution is promoted by hydrostatic pressure, due to a slightly reduced molar volume of the dissociated ions Ca++ and CO4– Therefore, the metabolic cost of maintaining calcium carbonate shells and ossicles must be progressively greater in deep water This could explain the limited molluscan fauna below 3000 m which are typified by simple shell morphologies (McClain et al 2004), a decline in carbonate Foraminifera (Gooday 2002, 2003), and a similar decline in heavily ossified echinoderms It can be speculated that pressure also influences chemosynthesis based upon H2S by altering the ionic equilibria among its chemical species Hydrostatic pressure is also a critical factor in the phases of gases Usually in the deep sea, biologically important gases like oxygen, carbon dioxide, methane and hydrogen sulphide exist in under-saturated solutions, and gas/liquid/solid phase is not an issue It is now very well established that solid methane hydrates are stable and form outcrops on the deep-sea floor even when the source solutions are very dilute (Sloan 2003) Hydrates consist of a cage of water molecules filled with gas molecules Methane hydrates are stable at temperatures below 5°C and at pressures greater than 450 kPa (450 m depth) Exposed hydrates have been found to support dense, single species populations of polychaetes (Fisher et al 2000) and shrimp (Van Dover et al 2003), presumably by 218 © 2005 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon 3597_book.fm Page 219 Friday, May 20, 2005 6:26 PM ZONATION OF DEEP BIOTA ON CONTINENTAL MARGINS providing a rich microbial food source A more conjectural relationship may exist between the fauna at hydrocarbon seeps such that seeps associated with methane hydrates have greater longterm stability and an associated fauna (Carney 1994, Sahling et al 2002, 2003) Pressure effects on organic systems Virtually all discussions of deep-sea distributions mention pressure as a possibly important factor Typically, a reference or two to the literature of high pressure physiology are made, and then the discussion moves to another topic Such polite brevity stemmed from two problems First, there was not much research to reference, and second, the most substantial studies were so molecular as to have little immediate ecological application Fortunately, the situation has now progressed to the point at which such studies are becoming more prevalent and ecologically relevant It is increasingly obvious that the deep-sea fauna must have adaptations to high hydrostatic pressure The absence of such adaptation or pre-adaptation prevents shallow species from entering deep water The reverse may also be true; organisms adapted to high pressure may be unable to successfully expand upward into lower pressure environments What is still lacking, unfortunately, is a good sense of what pressures and pressure changes are important to species depth limitation Pressure research on isolated biochemical systems has focused on enzymatic proteins and lipoprotein membranes Much of this research exploits pressure as a thermodynamic biotechnology tool (Balny et al 2002, Kornblatt & Kornblatt 2002) and has little apparent ecological value Somewhat greater relevance can be found in studies that seek biotechnical application for deepadapted organisms (Abe et al 1999, Ludwig 1999, Heremans 2004) All these studies show dramatic pressure effects that could restrict the depth range of organisms With respect to proteins, pressure denaturation of proteins caused by an unfolding from the native form is well known Thermodynamically, the transition is assumed to be associated with a decrease in molar volume The actual measured volume changes, however, appear to be too small to account for the profound effect on protein function (Chalikian & Breslauer 1996), indicating that a better theoretical model relating pressure to effect awaits development Hydration of the unfolded protein may be hiding a greater volume change (Hummer et al 1998) and compressibility may be a factor (Prehoda et al 1998) Coming closer to ecological application, a model of protein adaptations to low temperature and high pressure has been proposed (Hochachka & Somero 2002, Somero 2003) that stresses the necessity of adaptation to the deep-sea environment Presently, the model is still descriptive and does not lead to prediction about specific pressure barriers According to the model, maintenance of critical enzyme functionality under different conditions of temperature and pressure can be accomplished through changes in the amino acid sequence of the enzyme, or may also be controlled by stabilising compounds in the intercellular milieu Both types of pressure adaptation have been proven in vitro but for very few organisms and enzyme systems Functional depth adaptation has been shown in pressure studies on three categories of dehydrogenases, and 600 m suggested as a critical threshold depth (Somero 1998) The effect of pressure on reaction rates was minimal in deep-water species, but great on shallow-water species The genetic differences associated with these pressure adaptations have yet to be determined The presence and importance of compounds that stabilise enzymes in depth-adapted species has been confirmed for osmolyte trimethylamine oxide (Yancey & Siebenaller 1999) and a variety of suspected pressure-mediating compounds has been reported from deep fish and invertebrates and microbes (Yancey & Siebenaller 1999, Martin et al 2002, Siebenaller & Garrett 2002) The fluidity of bio-membranes is so greatly reduced by increased pressure and decreased temperature that survival at depth requires homeoviscous (Siebenaller & Garrett 2002) adaptations 219 © 2005 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon 3597_book.fm Page 220 Friday, May 20, 2005 6:26 PM ROBERT S CARNEY in membrane structure and composition (Hazel & Williams 1990) One mode of adaptation to elevated pressure is the accumulation of higher levels of lipid (Hazel 1995) The protein component of membranes may show depth adaptations similar to the Somero model; pressure-influenced changes in transmembrane signalling have been demonstrated (Siebenaller & Garrett 2002) With respect to a whole organism, behaviour responses of a deep hydrothermal vent crab to pressure and temperature were consistent with homeoviscous effects (Airriess & Childress 1994) Due to the prevalence of gelatinous and membranous megafauna in the deep sea, it is interesting to speculate that the bio-mechanical properties of these tissues are actually different at high pressure than at low Pressure may play an important role in the design of some abyssal fauna Independent of molecular results, researchers attempting to recover deep-sea organisms for laboratory studies at one atmosphere or in pressure aquaria have acquired some practical experience about pressure barriers The findings are mixed; some organisms are strongly influenced by a pressure decrease, while others are much more thermally sensitive (Childress et al 1978) Some hadal bacteria were found to die upon decompression, while other hadal and abyssal forms merely remained inactive until recompressed (Yayanos 1995, Bartlett 2002) Benthic Foraminifera collected above 2800 m survive and reproduce in cold aquaria at atm, while deeper specimens not survive decompression Only of 421 specimens of scavenging amphipods survived decompression from 1920 and 4420 m (Heinz et al 2002) Acute pressurisation of shallow-water species has been attempted to test an organism’s ability to survive in the deep sea (Menzies & George 1972a,b) but it remains unclear how to relate such short-term mortality to long-term acclimation The only long-term shallow-to-deep transplant study appears to be that of Maldonado and Young (1998) who transplanted two species of keratose sponges, normally limited to depths shallower than 40 m to 100, 200 and 300 m Transplants below 200 m depth died, but some of the others survived for as long as 12 months, the duration of the experiment It was speculated that the observed depth restriction was due to pressure sensitivity of larvae below 200 m and sensitivity of mature colonies below that depth A series of pressure studies on shallow- and deep-water echinoid larvae have produced very interesting results Larvae from shallow-water species remained viable at pressures of 10–15 MPa (1000–1500 m) This was demonstrated for three Mediterranean species (Young et al 1997) and a single Antarctic species (Tyler et al 2000) When three species of the echinoid genus Echinus were studied, larvae of the shallower forms could also survive well below the depth limit of the adults Larvae of the deep form, E echinus, to the contrary had pressure requirements similar to that of the adult, and needed 10 MPa (1000 m depth) to develop (Tyler & Young 1998) Countering the likelihood that all deep-sea animals have larvae restricted to high pressures is the finding of some deep larvae in upper ocean samples (