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AMER. ZOOL., 22:647-659 (1982) The Role of Dissolved Organic Matter in the Nutrition of Deep-Sea Benthos1 ALAN J. SOUTHWARD AND EVE C. SOUTHWARD Marine Biological Association of the United Kingdom, Citadel Hill, Plymouth, Devon, PL1 2PB, United Kingdom SYNOPSIS. Deep-sea sediments contain less particulate organic matter and lower biomass than shallow-water sediments, but the dissolved organic matter in pore water varies less with depth and may provide a significant food source for deep-sea benthos. Pogonophora are a phylum of predominantly deep-sea animals, all without an internal digestive system. Experiments show that one or two species ought to be able to live by uptake of dissolved organic matter from pore water in deep-sea deposits: some other species may need local enrichment of the habitat for such uptake to be useful. Less is known about nutrition of other deep-sea animals, but dissolved organic matter may supplement a conventional diet in several groups. Chemoautotrophy, using endosymbiotic bacteria, may be important for the large vestimentiferan Pogonophora in the high-sulfide conditions of the hydrothermal vents. INTRODUCTION We define deep-sea benthos as those animals that live on or in the sea-bed deeper than the shelf-slope faunistic boundary, which normally lies between 200 and 300 m (Grassle et al, 1979). The animals are separated into macrobenthos and meiobenthos by size, usually whether or not they are retained by a sieve with holes 0.5 mm across (Holme and Mclntyre, 1971); megabenthos is a term loosely applied to large animals caught in trawls or traps or seen in bottom photographs. All deep-sea animals apart from Pogonophora have an apparently functional alimentary canal, and would be expected to eat organic particles or living prey. However, there are few observations on live animals and the type of food has to be deduced from stomach contents or comparative morphology. On the basis of deduced feeding habits the proportion of deposit feeders changes with depth and distance from the coast, and a characteristic zonation of feeding type has been described (Sokolova, 1972). This trophic zonation is most obvious in the Pacific, where abyssal regions with very poor food supply are reported to have a ' From the Symposium on The Role of Uptake of Organic Solutes in Nutrition of Marine Organisms presented at the Annual Meeting of the American Society of Zoologists, 27-30 December 1980, at Seattle, Washington. dominance of suspension feeders in an otherwise sparse population of macrobenthos (Filatova, 1969; Sokolova, 1969; but see Hessler, 1974). Both trophic relations and depth are important in controlling the distribution of deep-sea benthos and great care is required in assigning a species to its trophic niche. The environment of the deep-sea is better known than the biology of the animals: hydrostatic pressure is high, temperatures are low, and average water currents slight (Marshall, 1979). The deep-sea floor is mainly fine sediments, and there is little solid substratum other than manganese nodules except near the continents and at the mid-ocean ridges where rocks are exposed. Biologically the deep-sea bottom differs from shallow water in having less organic matter, fewer bacteria (Sorokin, 1970, 1972a; Morita, 1979) and a lower biomass of macrofauna. The biomass of meiofauna and Pogonophora changes less with depth and these groups become relatively more important (A. J. Southward, 1975; Thiel, 1979). Metabolism and growth rates are slower at all levels of organization (Smith, 1978; Allen, 1979; Jannasch, 1979). The high pressure should have little general effect on the benthic invertebrates since their body fluids will be at ambient pressure and they are without flotation organs. However, pressure can alter molecular volume, and this may influence metabolism and behaviour (Brauer, 1972). 647 648 A. J. SOUTHWARD AND E. C. SOUTHWARD Enzymes of shallow water species can be inactivated, and shallow water microorganisms can show reduced uptake and use of dissolved organic matter (DOM), when compressed (Paul and Morita, 1971). On the other hand, deep-sea animals that have been studied possess enzymes whose structure allows them to function under pressure (Low and Somero, 1975). We can presume that intestinal absorption must be efficient in deep-sea animals, hence epidermal uptake of DOM need not be more difficult in the deep-sea than in shallow water. The temperature in the deep sea is no lower than shallow arctic and boreal seas, but is less variable. The few studies on the temperature coefficient of uptake of DOM give conflicting results. Uptake rates do increase with rising temperature, but acclimation may alter the rate in either direction (Schlichter, 1975; Shick, 1975; Tempel and Westheide, 1980). Experiments on uptake of DOM by deep-sea species have been carried out successfully at environmental temperatures of 4-6°C, so we suppose that the animals are adapted to their environment. In deciding the nutritional role of DOM in the deep-sea great importance attaches to the Pogonophora (including Vestimentifera). This phylum is found mainly in the deep-sea and none of the known representatives has an internal digestive system (Ivanov, 1963; Webb, 1969; E. C. Southward, 1975; van der Land and N^rrevang, 1977). This offers a strong presumption that nutrition takes place through the epidermis, in solution. T H E SUPPLY OF ORGANIC MATTER IN THE DEEP SEA Input of paniculate and dissolved material Deep-sea organisms are assumed to depend on production of organic matter near the surface, in the euphotic zone. In the open ocean, away from land, it is supposed that organic matter reaches the bottom in three ways: 1) as infrequent "large lumps," the rapidly sinking carcasses of large fish and cetaceans which are unlikely to be totally consumed by scavengers on the way TABLE 1. Examples of input of particulate organic matter to deep-sea sediments compared with metabolic needs of the benthic fauna." Input of particulate carbon, g/mVyr In situ Calculated input of carbon respiration as O ; uptake in ml/m2/hr for oxygen uptake Upper slope 1,050-1,350 m 4.4-10.9 1.31" Lower slope 1,850-3,650 m 2.0-6.4 0.24-0.50 Abyssal plain 4,670-5,582 m 0.24-0.62 0.02-0.09 6.14 1.12-2.34 0.09-0.42 "Smith, 1974, 1978; Wiebe el ai, 1976; Hinga el al, 1979; Knzuer etai, 1979; Miiller and Suess, 1979; Rowe and Gardner, 1979; Deuser and Ross, 1980; Honjo, 1980. b For nearshore sediment only (San Diego Trough). down; 2) as a "rain" of small particles, mostly faecal pellets; and 3) in solution, in a form which may or may not be available for nutrition (Krogh, 1934). The "large lump" contribution has not yet been seen from manned submersibles, though baited cameras and traps show how the megafauna and some smaller epifauna can congregate on and eat such "lumps" when they are supplied (Isaacs and Schwartslose, 1975; Rowe and Staresinic, 1979). The "rain" of small particles has been measured in several places with moored traps. Sinking rates are of the order of 100 m/day and the amount reaching the bottom is related to surface production and inversely to depth (Shanks and Trent, 1980; Suess, 1980). Although 20% of daily production (measured as carbon fixed) sinks below the euphotic zone, only about 1% reaches 3,000 m and only about 0.4 g carbon/mVyr reaches the abyssal plain (Table 1). We can also compare the input of organic matter to the bottom at different depths with the biomass of the fauna. The biomass values quoted by Filatova (1969), Rowe (1971) and Menzies et al. (1973) show a clear relation to depth. Below the faunistic boundary between shelf and slope, the biomass per unit area decreases exponentially with depth so that at 1,000 m there is 1% and at 3,000 m onlv 0.1% of the bio- DOM AND NUTRITION OF DEEP-SEA BENTHOS mass on the bottom of shallow seas. The benthic biomass is thus related to surface production of organic matter and the proportion of it that reaches the bottom (Filatova, 1969; Rowe, 1971; Vinogradova, 1979; Suess, 1980). There are two other sources of organic matter. One is evident where ocean depths come close to land, in canyons that dissect the slope, in deep-sea trenches or in basins close to continents. In such places benthic samples contain much terrestrial plant debris, including leaves, root masses and tree trunks, and the supply is regular enough to support a specialised fauna (Wolff, 1979). A further supply of organic matter to the deep-sea may be through chemoautotrophy. This possibility, based on the existence of microorganisms that can use energy derived from the oxidation of sulfide and other reduced inorganic compounds to fix CO2 and inorganic nitrogen into organic matter, was first suggested by Ekman (1953), quoting work by Benecke. More is now known about bacterial chemoautotrophy (Schlegel, 1975), but organic matter produced in this way is usually only a form of secondary production, since the reduced inorganic compounds are formed by anaerobic decomposition of organic matter originally produced by photosynthesis (Fenchel and Riedl, 1970; Sorokin, 19726). Cycling organic matter in this way may increase its stay in the sediment, but does not add to the total. However, in the deep sea there are autochthonous sources of reduced compounds at hydrothermal vents in rift zones (Corliss et al., 1979; RISE Project Group, 1980). This "crustal" input of hydrogen sulfide sustains a flourishing growth of microorganisms and of animals which feed on them or take up the DOM which they produce (Karl et al., 1980). Chemoautotrophic bacteria also appear to exist as endosymbionts in some of the higher animals around the vents (Cavanaugh et al., 1981; Felbeck, 1981), with the possibility of direct nutrient transfer to the host, analogous to that in shallow water animals that contain zooxanthellae (Smith, 1979). The hydrothermal vents may not be the only source of "crustal" energy. Some parts of the oceans have a circulation of sea water 649 within the sediments, down to basement rock (Langseth, 1980); the slow return flow might carry reduced compounds for chemosynthetic production on a smaller scale than at the vents. Amount of DOM in the deep-sea There are few realistic measurements of the DOM content of pore water from deepsea sediments. Many estimates are of total DOM content of sediment samples, or else the method of extraction of the pore water is not described. Harsh chemical extractants, high temperatures and prolonged slurrying have all been used, but even gentle suction or pressure can cause contamination by tissue fluids or cytoplasmic solutes from animals and microorganisms. With these reservations, there is more DOM in deep-sea sediments than in the water above, but no consistent decrease with depth as with paniculate fall-out or total biomass. The total DOM in sea water varies from 0.5 to 3 mg carbon/liter according to the method of analysis (Krogh, 1934; Plunkett and Rakestraw, 1955; Degens, 1970; Starikova, 1970), but there is twice as much in surface waters as in the deep-sea (Williams, 1975). The amounts quoted correspond to concentration range of a few to 100 \xMI liter. Nitrogenous compounds make up most of this, but only 10% has been fully identified (Degens, 1970; Mopper and Degens, 1972), and there is controversy over how much of it is complexes of high molecular weight and whether it is available to microorganisms (Hamilton et al., 1970; Williams, 1970; Sorokin, 1972a). However, there is no doubt that analyses for specific compounds show low concentrations, often in the nanomolar range (Degens et al., 1964; Vaccaro et al., 1968; Degens, 1970; Johnson and Sieburth, 1977), suggesting that the deep-sea water is not a significant source of DOM for uptake. The pore water from deep-sea sediments contains at least ten times more DOM than the overlying water (Starikova, 1970; Tanone and Handa, 1980), and a greater proportion of it is identifiable. Individual compounds are present in micromolar concentrations, with totals in the millimolar range. For example, total free 650 A. J. SOUTHWARD AND E. C. SOUTHWARD amino acids can reach 5.6 mg/liter, and single amino acids 20 /uM/liter; free sugars can total 0.4 mg/g dry weight of sediment, and pore water values of 0.74 to 1.2 fxMI liter have been reported (Degens et al., 1964; Mopper and Degens, 1972; Southward and Southward, 19726, 1980; Henrichs and Farrington, 1979; Mopper etal, 1980). Evidence from oxygen consumption and sediment build-up suggests that 2 0 ^ 0 % of the particulate fall-out becomes buried in the sediments (Rowe and Staresinic, 1979; Suess, 1980). Metabolic activity of deep-sea bacteria is low (Morita, 1979), with a low rate of breakdown of organic matter in the sediments. There should thus be a pool of buried or "historic" POM undergoing slow conversion to DOM, which then leaches out of the upper layer of sediment (Suess, 1976; Williams et al, 1980). Most bacterial activity is found in the upper 20 cm of sediment; lack of activity deeper is attributed to anoxic conditions, and it is held that anaerobic breakdown of "stable" organic matter is "energetically unprofitable at low temperatures" (Sorokin, 1970, 1972a). A more recent view takes into account bioturbation of sediments (Rowe etal., 1974; Henrikson et al., 1980) and its effect on DOM. Almost all photographs of the deep-sea floor show burrows, excavations and faeces in various stages of erosion and decomposition (Heezen and Hollister, 1971), and in some places the surface mud consists almost entirely of faecal matter undergoing continuous turnover by the benthos (personal observations). Turnover of the upper layers of deposit may account for the depth of bacterial activity and provide continual replenishment of DOM. To sum up: deep-sea sediments have much less POM and less DOM than shallow sediments, but there is still a considerable amount of DOM which could provide a significant source of food. However, compared to shallow water, the deep-sea habitat as a whole is oligotrophic, and thus all sources of energy, including POM, DOM and chemoautotrophy have to be regarded as potential food for the benthos; they might even all be used by one individual. NUTRITION OF THE POGONOPHORA The Pogonophora differ from most other free-living Metazoa in being without any internal digestive system (Ivanov, 1963, 1975). A few other metazoans do exist without a gut in the adult stage, or with a reduced gut, notably a polychaete, some oligochaetes, a bivalve mollusc and some brachiopods (McCammon and Reynolds, 1976; Erseus, 1979; Jouin, 1979; Reid, 1980), but these are rare examples compared with the whole phylum Pogonophora. Thus, examination of the nutritional status of the Pogonophora affords a critical test of the role of DOM in general, as well as in the deep-sea. Uptake of DOM by Pogonophora Pogonophora are widespread geographically, but are found mainly in the deepsea. The large species that occur below 2,000 m are difficult to locate and virtually impossible to recover alive (cf., Menzies et al., 1974). Hence experiments on uptake of DOM have been confined to the small species from shallower than 2,000 m, including one form that penetrates into cold shelf waters (Table 2). Uptake of DOM was studied using 14C and 3H labelled compounds. Except in one instance total flux was not measured, since the animals are very small and it is difficult to show a significant experimental reduction in ambient DOM. The species examined show individual and specific variation in uptake of DOM, but they can accumulate amino acids (including alanine, glutamic acid, glycine and phenylalanine) and glucose from concentrations between 1 and 10 /LtM/liter (refs. in Table 2). Lesser quantities of other compounds (galactose, mannose, acetic acid, butyric acid, palmitic acid, lactic acid and glycolic acid) are accumulated, but not apparently fructose or mannitol. The neutral amino acids are absorbed against a concentration gradient, probably by a carrier-mediated mechanism, and similar mechanisms may exist for other amino acids and for glucose. DOM is taken up by all regions of the 651 DOM AND NUTRITION OF DEEP-SEA BENTHOS TABLE 2. Species of Pogonophora investigated for ability to take-up DOM. Typical wet weight, mg Species Siboglinum mergophorum Nielsen (and Oligobrachia floridana Nielsen) Siboglinum atlanticum 1.0 15 Southward & Southward Siboglinum ekmani Jagersten 0.2 Siboglinumfiordicum Webb 1.0 Sclerolinum brattstromi Webb 0.1 Locality sampled and depth, m References Florida Straits 185 Bay of Biscay 1,500-2,000 Raunefjorden and Korsefjorden 300-750 Ypsesund and Fanafjorden 30-35 Korsefjorden 700-750 body, but the postannular part accumulates amino acids at Mi or less the rate for the preannular region; the tentacle accounts for a larger proportion of the soluble fraction accumulated by the preannular region than would be expected on a simple volume basis (Southward and Southward, 1970). The uptake rates for different species differ by one or two orders of magnitude, apparently unrelated to depth (Table 3). Siboglinum ekmani from 700 m has the highest rate of uptake of both amino acids and glucose. S. fiordicum Little and Gupta, 1968 Southward and Southward, 1968, 1970, 1972* Little and Gupta, 1969; Southward and Southward, 1970, 19726, 1980 Southward and Southward, 1970; Southward et al, 1979 Southward and Southward, 1980 from only 30 m has the lowest uptake of amino acids, while S. atlanticum from 1,800 m and Sclerolinum brattstromi from 700 m have similar, low, rates of uptake of glucose. These species also differ in content of free amino acids and in kinetics of uptake, so they probably differ in metabolism and way of life. A different way of life is obvious for S. brattstromi; like some other species of Sclerolinum (Southward, 1972), it lives in organic substrates such as rotting wood, rope and paper. Most of the compounds taken up by the TABLE 3. Rates of uptake of four classes of dissolved organic compounds by four small pogonophores." Compound Amino acids Glucose Species Sclerolinum brattstromi Siboglinum ekmani S. fiordicum S. atlanticum Sclerolinum brattstromi Siboglinum ekmani S. fiordicum S. atlanticum Fatty acids, long chain Siboglinum ekmani S. fiordicum Fatty acids, short chain; and hydroxy acids Siboglinum ekmani S. fiordicum a Mean uptake rate" (nAf/g/hr) from 5 /xjw/liler 16 110-240 4 38 2 130 9 6 20 1.3 7 7 Environmental concentration {/JLM /liter) Nutritive valued (% O, cons.) 12.2 12.9 (5) 61 45 4 4.9 6.5 1.2 30 1 1 12 11 (5) (5) (5) (5) 16 15 Based on Southward and Southward, 1981. Uptake rate for a "standard environmental concentration" of 5 /xJW/liter. Measured, or (estimated) from published data. d Calculated nutritive value, as % contribution to O2 consumption made by uptake from environmental concentration. b c 652 A. J. SOUTHWARD AND E. C. SOUTHWARD pogonophores enter into the metabolism, and are converted to other soluble and insoluble compounds, or respired (Southward et al., 1979; Southward and Southward, 1980). Autoradiographs of sections of animals exposed to labelled amino acids and glucose show good localization of label in storage and secretory cells (Southward and Southward, 1968, 19726; unpublished observations). There is thus little doubt that the animals were "feeding" under the experimental conditions, but the experiments do not show if they can grow under the same conditions. Growth of a pogonophore was observed by Bakke (1977), who reared Siboglinum jiordicum from larva to juvenile over a period of 398 days at 6°C. Measurements from drawings of the preserved specimens show that growth was slow, but that volume increased by a factor of 8 and length by a factor of 15 in this time. The only source of nourishment was a small amount of mud from the habitat, frozen and thawed before use, and a slow flow of sub-thermocline water, cleared by sedimentation. This study does not prove that DOM alone is sufficient for growth, since chemoautotrophy could also have occurred, but it does indicate that POM is unlikely to be food for these small pogonophores. Nutritional status of the Pogonophora The small pogonophores are usually damaged by loss of the hind end during capture, and do not appear to show "feeding behaviour" in the laboratory (Southward and Southward, 1963, 1981). Their nutritional status has to be deduced from the experiments reviewed above and from morphology and distribution. There are four hypotheses to be considered: 1) that particles filtered from the water by a crown of tentacles, or collected by a single tentacle, are digested among the tentacles or in the coiled-up tentacle, possibly after withdrawal into the tube, and that the dissolved products are taken up by the epidermis of the tentacle. This hypothesis is deduced from the morphology of the multitentacular species, but is unsupported by evidence for food collection or digestive secretion; 2) that pinocytosis of large molecules (proteins etc.) occurs at the surface of epidermal cells. This process has been demonstrated (Little and Gupta, 1968, 1969; personal observations), but the species shown to have this ability seem to spend most of their time inside the tube, which is permeable only to small molecules (Southward and Southward, 1963). Pinocytosis could be more useful to species that extend their tentacles outside the tube, such as the large Vestimentifera. The choice at the moment lies between hypothesis 3) that DOM is a significant source of food; and hypothesis 4) that chemoautotrophy is significant; or else a combination of the two. As we have more data on uptake of DOM this will be considered first. DOM in pore water, or at the sediment/ water interface will be able to pass through the wall of the tube and be available for uptake at the microvillar surface of the epidermis. A wide capability for uptake of DOM has been demonstrated experimentally in small pogonophores, and it can take place with the animals in situ in the tube. We can calculate the nutritional value of DOM by comparing the amount of a compound taken up from a concentration equal to that measured in the environment with the amount of the same compound that would be needed to account for the measured oxygen consumption of the species (cf., Stephens, 1968). It is assumed that the compound is efficiently deaminated and fully oxidised, and that the oxygen consumption in nature is the same as that measured in vitro. The effect of one compound on uptake of another has to be allowed for, and uptake rates and environmental concentrations have to be estimated for some compounds not fully quantified. The figures for individual contributions by the compounds are then summed to give a total potential contribution of DOM to nutrition (Table 4). This sum does not take into account the extra DOM that would be needed for growth and reproduction (Sepers, 1977). Only one pogonophore, S. ekmani, has a mean uptake of DOM high enough for the sum of all contributions to exceed 100%, and thus show that it could live entirely on DOM at the concentration measured in the DOM AND NUTRITION OF DEEP-SEA BENTHOS TABLE 4. Potential contribution of DOM to metabolic needs of Pogonophora. Species Siboglinum ekmani Siboglinum fiordicum Siboglinum atlanticum Sclerolinum brattstromi % of oxygen consumption equivalent to DOM taken up at environmental concentration 119a 73" 30° 30 c a From Southward and Southward, 1980. From Southward et al, 1979. 0 Approximate value, based on fewer experiments than with S. ekmani and S. fiordicum. b pore water. S.fiordicumshows a deficiency of 30% on the mean uptake rates, but this can be changed to a positive value if the calculations are confined to the "best" individual results. This species had a very wide range of individual uptake rates, and standard deviations up to 100% of the mean were found; removal of the low values, by assuming these particular animals were in poor condition, balances the budget. The apparent budget deficiency for the other two species cannot be balanced in this way. However, for Sclerolinum we have used environmental concentration data for pore water of mud samples, whereas this species lives in rotting wood etc., not free in the mud. Mopper and Degens (unpublished Wood's Hole Technical Report No. 68, 1972) report that as much as 15% free sugars (25 /xM/g) can be extracted from rotting wood from anoxic deposits. If we assume a local concentration of DOM greater than 100 /xM/liter in the habitat of Sclerolinum, then the budget for this species also balances. Local enrichment could also occur if pogonophores lived in association with other organisms in the community, including bacteria (Jagersten, 1957; Southward et al., 1979; Southward and Southward, 1981). For example, the pogonophores could produce local oxygenation of the deposit to benefit heterotrophic microorganisms capable of attacking refractory organic particles (cf., Stephens, 1975). Sepers (1977) has suggested that microorganisms are inherently more efficient than metazoans at uptake of DOM from low concentrations, which would put the meta- 653 zoans at a disadvantage in competition. However, there appears to be wide variation in adaptation to different levels of DOM among microorganisms, possibly related to microscale variations in concentration (Taylor and Williams, 1975; Williams, 1981). Therefore in the real world species with widely differing rates of uptake may be able to coexist. At present most of the evidence for chemoautotrophy is provided by experiments with tissue samples from the very large species of Vestimentifera which live close to the hydrothermal vents in the Pacific. These animals have three enzymes associated with the oxidation of sulfide and two associated with CO2 fixation via the Calvin cycle (Felbeck, 1981), and a ratio of carbon 13 to carbon 12 consistent with direct use of "crustal" energy rather than digestion of bacteria (Rau, 1981). Anatomical studies show the presence of bacteria (Cavanaugh et al., 1981) in the trophosome tissues where the enzymes have been detected. Elemental sulfur particles have also been seen in this tissue (Felbeck, 1981), and Arp and Childress (1981) link the rather high oxygen consumption rate of the whole animals to the possibility of chemoautotrophy. This evidence, coupled with the restriction of the giant Vestimentifera to sulfide-rich vents suggests that the sulfide-oxidising and carbon-fixing enzymes belong to endosymbiotic microorganisms, on which the animals depend for nutrition (Felbeck, 1981). However, we must remember that the vestimentiferans have a crown of many thousand fine tentacles which could provide a large surface area for uptake of DOM, hence there could be a combination of two types of "feeding." The small pogonophores are not associated with noticeably high levels of sulfide (Southward et al., 1979), though they occur in deposits which are probably anoxic below the upper few mm. We find (Southward et al., 1981) that some of them have bacteria-like inclusions in the peritoneal cells of the postannular region. Tissue extracts of S. atlanticum contain two Calvin cycle enzymes (ribulose phosphate kinase and ribulose biphosphate carboxylase). The latter is also present in extracts of S.fiordi- 654 A. J. SOUTHWARD AND E. C. SOUTHWARD T A B L E 5. Dei'.p-sea Species metazoan species, otherthan Pogonophora, tested for ability totake up DOM.* Compound Maldanid polychaete Amino acids (mixed) Plutonaster sp. Glucose Tharyx sp. Glycine 1 Locality and depth N. Bay of Biscay 1,800 m N. Bay of Biscay 1,800 m Korsefjorden 700 m Ratio of uptake of DOM by this species to uptake of DOM uy pogonophore species from same place 1.16 2.09 0.27 Southward and Southward, 1972a, 1980. cum, but not apparently in S. ekmani. A few experiments with the intact animal suggest that in S. fiordicum fixation of CO2 might provide 20 times more carbon than is provided by the low rate of uptake of glucose by this species. If all the fixation of CO2 was made available to the host, in addition to uptake of DOM, then the nutritional budget would be near balance. It is, of course, possible that the observed uptake of DOM is part of a mechanism whereby the host induces the symbiont to part with some of its manufactured organic compounds. The role of photosynthetic algae present in invertebrate tissues is not fully understood yet (Smith, 1979): a similar controversy seems likely over the symbionts in pogonophores, since it is quite easy to postulate a role for bacteria in removal of harmful sulfides (cf., Theede et ai, 1969; Powell et ai, 1979), which might diffuse inward from the anoxic surroundings of the posterior part of the animal. and the starfish from the Bay of Biscay have uptake rates of the same order of magnitude as those of S. atlanticum. All three species can be assumed to be capable of obtaining some part of their nutritional needs by uptake of DOM, though all have apparently functional digestive systems. For deep-sea species in general some deductions can be made from what is known about the uptake abilities of their shallow water relatives. Groups with an impervious cuticle such as Arthropoda and Nematoda can be excluded; soft-bodied animals with large surface areas in proportion to body volume may have significant uptake of DOM. In this category in the deep sea we could include most of the meiofauna, longbodied worms, animals with long tentacles, bivalve molluscs and some echinoderms. Shallow water There is now a large body of literature on uptake and incorporation of DOM by shallow water invertebrates (Stephens, COMPARISON OF UPTAKE OF DOM BY 1968,1981;J(zfrgensen, 1976; Sepers, 1977; POGONOPHORA AND OTHER INVERTEBRATES Stewart, 1979). We have compared uptake Deep-sea by intertidal polychaetes with uptake by The few deep-sea animals tested for pogonophores (Southward and Southability to take up DOM were all collected ward, 1972a, 1980). In general, uptake with pogonophores (Table 5). Since only rates by shallow water invertebrates vary one species was tested from each habitat between species and between groups over and there is specific as well as individual a range of at least two orders of magnivariation in uptake capacity, caution is tude. Calculations of potential contribuneeded in assessing these results. The tion of DOM to nutrition range from only polychaete Tharyx takes up glycine at only a few % in the meiofauna of coarse sands 25% of the rate shown by S. ekmani, but its (Tempel and Westheide, 1980) to over rate is still quite high compared with other 200% in polychaetes from fine deposits species of Pogonophora. The polychaete with high organic content (Costopulos et DOM AND NUTRITION OF DEEP-SEA BENTHOS 655 ai, 1979). In effect, the ranges in uptake 1967, 1980; Shick, personal communicarates in Pogonophora and other inverte- tion). In contrast to this flexible policy, the brates are quite similar (Southward and Pogonophora would appear to have beSouthward, 1980). come specialized for a trophic niche that is not fully exploited by other metazoans: but DISCUSSION AND CONCLUSIONS if reliance is placed on DOM alone, then In comparison with other invertebrates there must be a lower limit of environfrom deep-sea and shallow-water habitats mental DOM below which survival is not there seems to be nothing exceptional about possible. From experiments on total flux the ability of Pogonophora to take up of primary amines in shallow water aniDOM. Contrary to previous statements (A. mals (Stephens, 1980) this lower limit of J. Southward, 1975), it seems that loss of DOM can be placed in the range from 1 an internal digestive system has not been to 5 juM/liter, which is close to the K, conaccompanied by any great improvement of centrations found for the best investigated the mechanism for epidermal uptake of pogonophore. The distribution of pogonDOM. Animals from the rich conditions at ophores suggests they are limited by orhydrothermal vents or from the special- ganic content of the habitat, since they are ized wood-eating community show faster most abundant on steep slopes and in growth (Turner, 1973; Turekian et al, trenches close to land masses where there 1979) than their relatives from the low or- is increased fall-out of organic matter from ganic environment of the abyssal plain. The coastal regions and the land, and where latter, with their slow metabolism and disturbance of the deposits by slumping growth rate, can be assumed to be adapted and currents may help maintain the supply to oligotrophic conditions, or to be show- of DOM. Pogonophora are notably absent ing a phenotypic response (Marshall, 1979). from the abyssal plains where the panicWe may suppose that the Pogonophora are ulate input and biomass are low (p. 649). also adapted to or are responding to oli- Other invertebrates can live in such exgotrophic conditions in their normal hab- tremely oligotrophic conditions, though itat {i.e., other than at the vents or in or- Pogonophora cannot, hence there may be ganic substrates). Their mechanism for some advantage in being able to use more uptake of DOM must function at low tem- than one source of food. peratures as well as at low concentrations. This leads to consideration of the hyIn Siboglinum ekmani the rates of uptake of pothesis that the Pogonophora are also DOM are quite high at its normal ambient polytrophic, but combine uptake of DOM temperature (6°C), and the concentration with some reliance on endosymbionts caat which uptake is half-maximal (Kt) is gen- pable of producing organic matter by cheerally lower than is found in shallow water moautotrophy. At one extreme we have the benthic animals, varying from 0.64 to 6.25 high-sulfide conditions at the hydrother/xM/liter for all compounds other than ace- mal vents, where growth is more rapid than tic acid (Southward and Southward, 1980). elsewhere in the deep-sea, and where the Adjustment of the metabolism and the up- giant Vestimentifera may rely mainly on take process to low temperatures may have their endosymbionts. At the other extreme enabled the Pogonophora to dispense with we have the conditions of the Atlantic conan internal digestive system, and thus avoid tinental slope, where only small pogonoenergy wasted in its maintenance. phores live, and where reduced sulfur compounds must be derived mostly by anIn contrast, the other deep-sea animals have kept the capacity for internal diges- aerobic breakdown of organic matter which tion, though some of them may also nour- has come from the sea surface or the land. ish their epidermis by direct uptake of In such places it might be more efficient DOM, while at the same time filling the to use DOM directly as the main energy stomach with mud or other food, as in some source rather than the indirect products of shallow-water echinoderms (Ferguson, the sulfur cycle. 656 A. J. SOUTHWARD AND E. C. SOUTHWARD starfish on epidermal uptake of dissolved organic matter. Comp. Biochem. Physiol. 66A:461 —465. We thank Dr. P. R. Dando for infor- Filatova, Z. 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