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Limnol. Oceanogr., 33(4, part 2), 1988, 9 IO-930 0 1988, by the American Society of Limnology and Oceanography, Inc. Production and use of detritus in various freshwater, estuarine, and coastal rnarine ecosystems K. H. Mann Department Dartmouth, of Fisheries and Oceans, Marine Nova Scotia B2Y 4A2 Ecology Laboratory, Bedford Institute of Oceanography, Abstract In both freshwater and marine habitats, vascular marine plants arc little used by animals that graze directly on them, because they have a relatively high content of indigestible fiber and a low content of nitrogen. The chief emphasis of detritus research in the 1970s was to show how microorganisms progressively reduce the content of fiber and increase the content of nitrogren in vascular plant detritus, rendering it nutritious for animals. Algal (seaweed, diatom, etc.) detritus starts with a lower fiber content and a higher nitrogen content. Many animals can use it directly, and a very short period of microbial colonization renders it highly nutritious. As a result, a high proportion of the algal carbon originally produced passes into animals via detrital food webs, while a low proportion of vascular plant carbon does so. Much more of the latter simply supports microbial respiration. In the 1980s it was shown, particularly for freshwater habitats, that the dissolved organic matter (DOM) released by plants while living or in the early stages of decomposition readily precipitates on surfaces and forms amorphous particulate matter with a low content of refractory material. These particles are highly nutritious for animals and are used directly by freshwater fish such as Sarotherodon (= Tifapia), which is commercially important, especially in Africa and South America. It is suggested that the DOM pathway may be ecologically more significant than the POM (particulate organic matter) pathway and that processes analogous to those shown for lakes and rivers probably occur in estuarine and coastal waters. There is much circumstantial evidence to suggest that planktonic food webs based on DOM are much more important than previously thought. The conversion of DOM to POM through the “microbial loop” and its utilization in higher trophic levels is a.n urgent topic for further study. In most situations more energy and materials flow through detritus food webs than through grazer food webs. Of the total primary production of a system, more is transmitted to other trophic levels from dead decomposing plant tissue than from living tissue consumed by a grazer. Nevertheless, those who manage aquatic systems for high productivity of fish, shellfish, or other invertebrates will be interested not so much in the total flow of energy and materials as in those pathways leading directly to nutrition for species of interest. Hence, one question addressed here is the extent to which detritus pathways support the production of invertebrates and fish, and the extent to which they lead mainly to the production of CO, in microbial respiration and to the regeneration of nutrients. Another question concerns the relative importance of plant detritus derived from vascular plants (salt marsh grasses, seagrasses, mangroves) and that derived from seaweeds and other algae. Historically, great emphasis has been placed on studying the fate of vascular plant detritus, and the fate of algal detritus is less well understood. Finally, much more attention has been paid to particulate organic matter (POM) than to dissolved organic matter (DOM) which may be released either from living plants or from dead plants during the early stages of decomposition. We shall see that this emphasis may have been misplaced, and that the detrital pathways that begin with DOM may be ecologically more significant. Nitrogen as a limiting factor Very few aquatic macrophytes are extensively used by grazers (Teal 1962; Odum and de la Cruz 1967; Mann 1972; Fisher and Likens 1973; Dickinson and Pugh 19’74). Leaves and stems die and decay and supply large quantities of plant detritus to the systems in which they occur. This is particularly true of plants growing in the littoral zones of lakes and rivers, in freshwater and saltwater marshes, in seagrass and seaweed beds, and in mangrove swamps. Tn 910 Detritus: Production and use 911 this material was fed to Capitella, they found addition, terrestrial plants overhanging streams make a major contribution of dethat on a diet of marsh grass detritus Captritus to these systems. With the exception itella obtained about a third of its nitrogen of the algae, all of these plants tend to have ’ from the plant material; on seaweed detritus a high content of fibrous material, such as it obtained ~80%. There is other evidence that not all the lignin or cellulose and a low content of nitrogen. Such material is of limited food valdigestible nitrogen in detritus is in the form ue for animals, since the carbon is largely of microbial protein. Bowen (1980) analyzed detritus from the littoral zone of lakes indigestible and there is very little protein. Nature’s solution to this dilemma is to and found that protein accounted for less than a third of the total nitrogen present. invoke the aid of microbes, both fungi and bacteria but particularly the latter. Many of The remainder was mainly in the form of nonprotein amino acids present in the dead them have the ability to digest cellulose and particulate organic matter rather than the other refractory carbon compounds. As time microorganisms. He went on to show that progresses, the detrital material is attacked the fish Sarotherodon (=Tilapia) could use by the microbes and broken into finer parthese amino acids very efficiently (see beticles making still more surface available for colonization. Refractory carbon comlow). Two workers in my own laboratory pounds are processed to yield energy for had previously drawn attention to the exmicrobial metabolism, while additional niistence of nonprotein nitrogen in detritus, trogen for microbial protein is taken from although no further investigations had been the environment. As the ratio of microbial made (Harrison and Mann 1975a; Robinbiomass to plant tissue increases, the detrison et al. 1982). Lee et al. (1980) found that tal particles become more nutritious for inmicrobes accounted for only a minor part vertebrates. Invertebrates readily digest the of the relative increase in nitrogen observed microbial component, allowing much of the during decomposition of Spartina, and Rice refractory plant tissue to pass through their (1982) pointed out that during decompoguts. This process by which microbes make sition detritus becomes richer in reactive detrital carbon available to animals and play phenolic and carbohydrate groups, which an essential part in overcoming the nitrogen may form condensation products with amideficiency of detrital food has been demno acids, yielding precursors to complex nionstrated many times in a variety of habitrogenous humic substances. These are liketats (Newell 1965; Odum and de la Cruz ly to be indigestible to most detritivores. 1967; Mann 1972; Dickinson and Pugh Dissolved organic matter and the 1974; Fenchel and Jorgensen 1977; Pomeformation of detrital aggregates roy 1980). One of the most convincing demonstrations that the efficiency of transforWhen dead plant material begins to demation of plant detritus to animal tissue is compose, there is a rapid loss of soluble proportional to the nitrogen content and inorganic matter (Kaushik and Hynes 1971; versely proportional to the fibrous content Wetzel and Manny 1972; Harrison and was that of Tenore (1977, 198 1) who worked and Fisher Mann 1975a, b; McDowell with laboratory cultures of the polychaete 1976). Living plants also produce dissolved worm Capitella that were fed standard diets organic matter in greater or lesser amounts of different types of detritus (Fig. 1). depending on such variables as nutrient Recent work has shown that for some supply and light conditions (Sieburth 1969; kinds of detritus, especially that from algae, Gallagher et al. 1976; Fankboner and the animals can absorb substantial amounts deBurgh 1977; Azam and Ammerman of nitrogen directly from the plant material. 1984). As a result, there is an influx of DOM Findlay and Tenore ( 1982) succeeded in into all aquatic environments. A proportion producing marsh grass detritus and seaweed of this is rapidly taken up by bacteria (which detritus in which a 15N label had been inmay themselves be grazed and contribute corporated into only the plant material, only to invertebrate and vertebrate food chains), the coating of microbes, and both. When which also deposit organic matter in par- Mann 912 MARSH GRASS 2 EEL GRASS tt F MIXED CEREAL FUCUS GRACILARIA t t t N ‘E 600 mg Table 1. Survival and mean final weight of groups of 10 tadpoles (Bz@ americanus) fed test diets for 6 d. FOOD / DAY : a a i 400 w + E -- 8 3 200 t? a F o.I- NITROGEN IN FbOD SOURCE (% 1 Fig. 1. Production of the worm C’apiMia as a fimction of the nitrogen content of its food and the level of ration (from Tenore 1977). ticulate form, such as exoenzymes, mucus, and the ropelike aggregates described by Paerl(1978). Another fraction of the DOM is converted to particulate form by physicochemical processes that occur on interfaces, e.g. on plant and on rock surfaces, on sediment particles, at the surfaces of bubbles, and at the surface of any water body. Detritus formed in this way reveals no cellular structure and may thus be clearly distinguished from plant detritus. Bowen (1984) referred to the two types as amorphous and morphous particulate organic matter (POM) and has shown that the amorphous material is often readily digestible by animals without the aid of microbes (Table 1). Camilleri and Ribi ( 1986) showed that DOM released by mangrove leaves can be converted to flakes, which are used as food by copepods, amphipods, isopods, and shrimps. The eficiency of various detrital pathways There are five different pathways by which the energy and materials of primary production may be transferred to invertebrates and vertebrates in aquatic habitats, three of which involve microbes as essential intermediaries (Fig. 2). The processes of fragmentation, colonization by microbes, and enrichment with nitrogen, often called aging of detritus, proceeds more or less rapidly according to the nature of the original plant material and the environmental conditions. During decay, microorganisms use the plant detritus for their own metabolism. If the interval between the onset of detritus for- Test diet DOM precipitated with FeCl, DOM precipitated, no added agent DOM with bacterial suspension Leached plant fragments Control I (starved) Control II (starved) Cumulative survival (tadpole days) Final wt (mg) 38 17.2-t 1.23 58 28.3-+ 1.59 54 5 10 2 37.3k3.43 -- mation and consumption by an animal is long, microbes convert a large proportion of the plant material to CO*, in which case the efficiency of transfer of energy and materials from plant to invertebrate will be very low. By contrast, a trophic transfer in which plant organic matter is assimilated directly by invertebrates or fish may have a relatively high efficiency. In what follows, we enquire about the efficiency of detrital utilization in a range of habitats and use this information to try to assess the relative importance of detritus and grazer pathways in supporting the productivity of fish and shellfish. De&us in streams IJpper reaches- There is no doubt that the detritus pathway is dominant in tributaries of rivers originating in forested uplands. In Bear Brook, a small headwater stream in the eastern United States (Fisher and Likens 1973), almost all input of energy and materials is from forest detritus. Trees shade the stream and inhibit primary production in the streambed. New Hope Creek, studied by Hall (1972) is more open, and there is a significant product of periphyton in the stream, but even there the input of carbon from dead leaves from the trees was twice as large as the carbon fixed by periplhyton. Leaf packs provide habitats for aquatic invertebrates that shred and collect leaves and leaf fragments. Examples of shredders are stonefly larvae and some kinds of caddis fly larvae, while blackfly larvae and netspinning caddis larvae are collectors. Short Detritus: Production and use 913 Animals - Digest * Morphous Particles Particulate Detritus (Morphous) \ / Dead Plant Tissue Animals Colonization :;&I / %Zes Microbes \ / Dissolved Organic Matter Formation of Amorphous Particles \ \ :;gE, Precipitation Animals Digest Amorphous Particles / Fig. 2. Pathways of utilization Discussion given in text. of plant detritus. and Maslin (1977) labeled leaves of a young alder tree with 32P. When these were exposed as leaf packs in an artificial stream along with various combinations of insect larvae, Short and Maslin found that the presence of the stonefly Pteronarcys as a shredder increased the uptake of 32P by the net-spinning caddis Hydropsyche by 35100% and the uptake of the blackfly larva Simulium by 600-700% (Fig. 3). This is a direct demonstration both of the transfer of detrital material into invertebrate food webs and of the importance of shredder species in preparing the material for collector species. Stream ecologists have also demonstrated experimentally the importance of DOM in supporting the production of stream insects, and hence of fish. Rounick and Winterbourn (1983) showed that DOM in stream water will precipitate on stone surfaces, both in the light and in the dark, to form a slime layer which stream insects readily ingest. In nature, the upper surfaces of stones have a layer consisting of periphyton algae, the organic slime layer, and associated bacteria and fungi, and it is clear that the removal of this layer by browsing insects provides surfaces on which precipitation of DOM is a continuous process. The supply of DOM to a stream community is difficult to quantify. Fisher and Likens (19 73), working in an upland stream, found that almost 50% of the energy passing through their study area was in the form of DOM, half of which came from upstream and half from groundwater entering the study area. McDowell (1985), working in Fig. 3. 12P activity of the collector insects Hydrapsyche californica and Simulium arcticum in an artificial stream. Controls 1 and 2 show levels when radioactive leaves and the insects were placed in the stream for 7 d. Experiments l-3 show elevated levels when the experiments were repeated with the addition of a shredder species, Pteronarcys calijbrnica (from Short and Maslin 1977). the same stream, concluded that the rapid precipitation of DOM is mainly an abiotic adsorption phenomenon. Hynes (198 3) drew attention to the need to make more detailed studies of DOM inputs to river systems from groundwater. He pointed out that groundwater may have an extremely long residence time in the water table before being discharged into a riverbed and that the largest quantities enter the river through the streambed, from below. He suggested that in the process, large quantities of DOM may be precipitated and made available to the infauna. Lower reaches of streams- Farther downstream, the amount of in situ primary production increases. Periphyton algae may be used by grazing invertebrates, but macrophytes mostly complete their growth cycles, decay, and enter detritus food webs. Macrophytes such as Ranunculus, Potamogeton, Nuphar, Typha, and other fringing reeds and rushes all liberate DOM when they become senescent and also contribute particulate detritus that moves downstream with the current. Cummins (1975) showed that there is a tendency for the mean size of particles in suspension to decrease with distance downstream with the result that communities upstream tend to have a higher pro- 914 Mann .IC _ T = .oa T r.06 LARGE LARGE PARTICLES, so.5 mm ISOPODS, - II mm - p\I NUP 0 2 70$ 8 65 ;; 60 25 2 do o” ,000 k z E" -.04 8 .02 fr 0 PARTICLE SIZE (pm) Fig. 4. Mean content of refractory organic matter as a function of particle size in detritus collected from eight running-water habitats (from Bowen 1984). portion of shredders and browsers, while the downstream communities have a higher proportion of species that collect fine particulate matter. Bowen (1984) demonstrated that very fine particles often have no visible microscopic structure, i.e. they are amorphous and contain less refractory material (Fig. 4), so they are probably derived from DOM by precipitation. Bowen (1984) also showed that these particles are a good source of nutrition to animals (Table 1); thus, it is not surprising that the lower reaches of rivers tend to support rich faunas of filter feeders such as bivalve molluscs and simuliid and chironomid larvae, as well as deposit feeders in the sediments. In running water, inputs of allochthonous materials in the upper reaches and growth of rooted macrophytes in the lower reaches lead to a situation in which most river communities process the greater part of their energy and materials through detritus food webs rather than grazer pathways. Isotope labeling of both particulate and dissolved detritus fractions has demonstrated that detrital carbon and phosphorus does indeed find its way into the invertebrates and, by implication, into the fish. An understanding of detritus pathways is necessary for good river management. For example, Bilby and Likens (1980) found that natural organic dams in streams perform a major role in processing organic detritus. Pools form on the upstream side of the dams. Sandy silt and fine organic particles accu- SMALL SMALL PARTICLES, co.5 ISOPODS,-4mm mm 17 OF CONDITIONING 45 .I2 CI G .I0 T m.08 E F .06 V CK .04 tz .02 0 0 7 DAYS Fig. 5. Relative growth rates (RGR) of the isopod Asellusforbesi when fed large-particle (above) and smallparticle (below) macrophyte detritus conditioned for various lengths of time. Key to macrophytes: NUPNuphar h&urn; PEL- Peltandra virginica; SAU Saurus cernuus; PON-Pontederia cordata. (From Smock and Hawlowe 1983.) mulate in the pools, retaining coarse organic particles during the aging process of detritus. When organic debris dams were removed experimentally from an upland stream, the coarse organic matter was exported directly downstream in the unprocessed state, and the normal functioning of the stream ecosystem was disrupted. Detritus in lakes and marshes The relative amounts of production by macrophytes and by phytoplankton in lakes vaq greatly according to the shape and successional stage of the lake basin. There are lakes with steep-sided rocky basins that 915 Detritus: Production and use 1 8 Consumption 0 m I T NO ANilBlOTlCS ANTIBIOTICS .I0 Growth th I T Protein content of food ,^ .08 I, -I tii r.06 E” - .04 h .02 Pet Sau Pon ” Nup Pel Sau ‘Pon MACROPHYTE SPECIES Pel Sau Pon Fig. 6. Effect of aging macrophyte detritus with antibiotics. Figures show changes in food consumption and growth of Asellus forbesi when feeding on the detritus and changes in protein content of food. Relative consumption rate--CR; relative growth rate-RGR. Key to macrophytes as in Fig. 5. (From Smock and Harlowc 1983.) have minimal areas of littoral habitat and associated macrophytes. At the other end of the scale, there are shallow, eutrophi? lakes in which the littoral zone extends almost to the middle of the lake. Such lakes grade insensibly into marshes and wetland where macrophyte production clearly dominates and almost all production of invertebrates and fish is supported by detritus food webs. There have been numerous studies on the decomposition of wetland plants such as Typha (Davis and van der Valk 1983), Nymphoides (Brock 1984), or Eichornia (DeBusk and Dierberg 1984) and several useful reviews in Good et al. (1978). As mentioned earlier, decomposition of macrophytes commonly found in the littoral zone of lakes follows the classical pattern: first, liberation of large quantities of DOM; second, progressive shredding to smaller particle size with increasing nitrogen content. Smock and Harlowe (1983) studied the food consumption and growth of the isopod Asellus forbesi given detritus of various ages derived from Nuphar, Peltandra, Saururus, and Pontederia (Figs. 5, 6). They found that the isopods grew better on ZVupharand Pel- tundra, which had a higher protein content than the other species. When the detritus was aged for various lengths of time, there was the expected initial increase in nitrogen content, and this was reflected in improved growth of the isopods. When aging took place in the presence of antibiotics, the protein content of the food and the growth of the animals was correspondingly depressed. Clearly, Asellus benefits greatly by the accumulation of microbial protein during the aging of macrophyte detritus. Bowen (1979a, 198 1) reported from Lake Valencia in Venezuela that the littoral zone was occupied by dense beds of Potamogeton, the leaves of which were covered to a depth of about 5 mm with a complex mixture of filamentous blue-greens, amorphous organic detritus, diatoms, and sponges. This material was the prime food of an introduced cichlid fish Sarotherodon (= Tilapia) mossambicus which dominated fish biomass. The fish assimilate the total amino acids of the aggregate with an efficiency of 63% (Fig. 7). Most of these dietary amino acids were nonprotein in nature and were believed to have originated from the precipitation of DOM. This is a clear example Mann SAROTHERODON \ (=TILAPIA I MOSSAMBICUS PROTEIN b I l/4 STOMACH a l I I 2/4 DIGESTIVE I 3/4 TRACT 4/4 Fig. 8. Total organic content, protein content, and algal volume of detrital aggregate samples taken from sites of differing bottom slope in Lake Valencia, Venezuela (from Bowen 1979a). SEGMENT Fig. 7. Analysis of samples from stomach (on left) and four successive quarters of the digestive tract of Saroherodon mossambicus to show changes in protein and total amino acids. Note large quantities of nonprotein amino acids (from Bowen 1980). of fish production being supported directly by detritus food chains. A detailed study of periphytal detrital aggregate (PDA) in different parts of Lake Valencia (Bowen 1979a) showed that the slope of the littoral bottom had a marked effect on the composition of PDA (Fig. 8). On steeply sloping sites, the aggregate was relatively rich in algae, protein, and total organic matter; on gently sloping sites, the content of these materials was much lower. Apparently, there is an accumulation on the sand surface of old, refractory detritus of low organic content. On gently sloping shores, wave action suspends this material, and much of it gets incorporated in the periphyton aggregate. On steeply sloping shores, the effect of wave action is to move the refractory material offshore into deeper water. As mentioned earlier, it was found that nonprotein amino acids were three times as abundant as protein amino acids in this detrital aggregate, and the fish were able to extract the former as it passed slowly through the gut. Whether these amino acids occur singly or as polypeptides is not known. A parallel study in Lake Sibaya, South Africa (Bowen 19793, 1980, 1981), showed a rather different set of feeding relationships. Sarotherodon mossambicus was pres- ent and fed exclusively on detrital aggregate that occurred as loose flocculated material overlying a sandy bottom. The juveniles fed on nearshore sand terraces, while the adults fed in deeper offshore waters. The caloric content of the detritus was about the same in all areas, but the protein content varied with depth from > 10% at depths of 0.5 m o only 2% at 5 m (Fig. 9). Not surprisingly, 4 he juvenile fish grew rapidly and were healthy, but the adults, which fed in deeper Walter, grew slowly and appeared to suffer from severe malnutrition. The reason for the higher protein content of shallow-water detritus is not entirely clear, but it seems probable that it is newly formed detritus with a rich coating of microorganisms and the detritus in deeper water is old and consists primarily of refractory material. When th’e detrital aggregates of Lake Sibaya were analyzed for amino acids, the content averaged 4.4% of organic matter, compared with 14.6% in Lake Valencia. This difference probably accounts for good growth of Sarotherodon in Lake Valencia, but poor growth of the adults in Lake Sibaya. However, the ability of the tilapia family (Cichlidae) to make extensive direct use of detritus is good evidence of the transfer of detrital energy and materials into species of commercial interest. In general, what proportion of lake primary production reaches fish by the grazing pathway and what proportion by the detritus food web? It used to be assumed that Detritus: Production and use X 14 12 0 f a 10 : 8 a-” I X X XX I 26 z ii L’ E 2t xx x x x x XX X )$(xX x xxx & “%x x X X Fig. 9. Protein content of detrital aggregate samples taken from various depths in Lake Sibava, South Africa (from Bowen 19793).- organic matter produced by phytoplankton passed directly to grazing zooplankton and thence to fish. In a major review of the trophic relationships of zooplankton of lakes and reservoirs, Hillbricht-Tlkowska (1977) concluded that in most situations, and especially in eutrophic lakes, more energy and materials reach zooplankton by detritus pathways than by direct grazing on the living cells (Fig. 10). In eutrophic lakes, the average biomass ingested by zooplankton is 5-l 5% small algae, lo-20% detritus, and 70-85% bacteria; in oligotrophic lakes, the proportion of small algae in the food was up to 50%, with the balance made up of detritus and bacteria. Larger algae, or those forming colonial groups, appear not to be readily consumed by freshwater zooplankton, but instead contribute particulate and dissolved organic matter to detritus food webs. When we also take into account particulate organic matter derived from macrophytes within the lake and allochthonous material entering the lake from inflowing streams or from the land, the possibilities for zooplankton to derive much or even most of their nutrition from detrital sources become very clear. Detritus in estuarine and coastal systems Macrophyte detritus-Studies of the fate of marine macrophyte detritus were stimulated by Teal’s (1962) observation that, on a salt marsh in Georgia, herbivores assimilated only 4.6% of the Spartina production, leaving the remainder to enter detritus food webs. Valiela et al. (1984) reported recent work on a New England marsh and reviewed what is known about the decomposition of salt marsh grasses. Three phases Mann 918 I 0 20 50 100 150 I 200 DAYS OF AGING Fig. 11. Rcsulls of culturing the worm Capitella on detritus prepared from three different sources and aged for different times. Above-ratio of worm production to total oxidation in the cultures; below-ratio of microbial biomass to total oxidation (from Tenore and Hanson 1980). were recognized: first, the leaching phase, lasting < 1 month, during which 5-40% of the biomass is lost; second, a decomposer phase, lasting up to a year, during which microbial degradation and subsequent leaching of hydrolyzed substances removes an additional 40-70% of the biomass; finally, the small fraction of refractory material remaining is slowly broken down over an additional year. They showed that the activity of invertebrates produces a small, but significant increase in the decay rate, while nutrient enrichment accelerates decomposition up to 24%. Nutrient enrichment also has a qualitative effect on decomposition. When one or another nutrient is limiting, the microbes on detritus tend to release organic matter for processing elsewhere. When there is no limitation, microbial populations use the organic matter to build up their populations on the litter (Howarth and Fisher 1976). The fate of other vascular marine plants such as seagrasses or mangroves is qualitatively similar; however, rates of microbial decomposition are variable and seem to depend not only on the content of fibrous, refractory material but also on various chemical defenses against microorganisms or grazers. Thus, Harrison and Chan (1980) showed that Zostera leaves that had been dead up to 2 weeks contained a water-soluble substance that inhibited the growth of bacteria and algae. Also, Valiela et al. (1979) showed that newly dead Spartina contains considerable amounts of ferulic and coumaric acids that are distasteful to amphipods and snails and might be expected to slow the process of shredding and grinding, which otherwise serves to accelerate the colonization of microbes. 13~ comparison with most vascular marine plants, algae have a much lower content of fibrous material and a higher content of nitrogen. When exposed to seawater under field or laboratory conditions, algae decompose much more rapidly than marsh grass, seagrass, or mangrove tissue. When a detritivore is included in laboratory experiments, the higher nutritive value and digestibility of the algae is reflected in a more rapid and efficient assimilation of the detritus by the detritivore. These differences are well illustrated by the experiments of Tenore and Hanson (1980), who prepared detritus from three sources: marsh grass (Spartina), seaweed (Gracilaria), and natural mixed periphyton. Some detritus was frozen soon after preparation; other subsamples were aged for different lengths of tirne and then frozen. This made it possible to run a series of parallel experiments under standard conditions in which the polychaete worm Capitclla was fed detritus from different plants aged for differing lengths of time (Fig. 11). Worm production was measured, as well as microcosm oxidation (the CO2 of the worm respiration plus the amount of detrital carbon converted to CO2 in the process of microbial metabolism). N’ote that the question being asked is very close to the theme of this paper, i.e. in a detritus-based system, what proportion of the carbon enters invertebrate food webs and what proportion is simply oxidized by the microbes? The upper plot of Fig. 11 shows that the ratio of worm production to microbial oxidation exceeded 80% for periphyton aged only 30 d. The seaweed Gracilaria needed aging at least 40 d and the Spartina 200 d before a similar ratio was re:ached. If seagrass tissue had been tested, it would have required even longer (Har- Detritus: Production and use rison and Mann 197 5b). When the ratio of worm production to microcosm oxidation was high, it is probable that a high proportion of energy and materials from the detritus was going to invertebrates and a low proportion to microbes. The lower part of Fig. 11 shows microbial biomass as a function of microcosm oxidation and time of aging and strongly suggests that it is the rapid buildup of microbial biomass on algal tissue that makes possible the efficient utilization of this material by Capitella. However, the experiments of Findlay and Tenore (1982), mentioned earlier, also showed that the worms derived much of their nitrogen through digestion of algal tissues. Work with stable carbon isotope ratiosThe experiments with Capitella raise important questions. If vascular marine plants are used relatively inefficiently by invertebrates over a 200-d period, and if meanwhile the fungi and bacteria convert much of the detritus to CO*, how much of the original plant energy and materials finally reaches the invertebrates in a marine system where vascular plant detritus is abundant? Fortunately, stable carbon isotopes can be used as tracers of vascular plant carbon in marine food webs, and a partial answer to our question has been obtained. When the ratio of 13C to 12C in various plants is measured and expressed as the conventional ?j13Cratio, Spartina tends to have a value around - 12 to - 14a/oo,while benthic diatoms are around - 16 to - 18o/ooand phytoplankton is -20 to -22a/oo or even more negative. The 613C value of detritus is close to that of the material from which it is derived, and that of animals is close to the 613C value of their food, but with a tendency to be shifted 1-2Ym less negative (Fry and Sherr 1984). Examination of the 613C ratios of animals in salt marshes or seagrass beds therefore gives an indication of the extent to which the macrophyte carbon is getting into the animals through detritus pathways. The results suggest that, even in the vicinity of dense macrophyte beds, periphyton, and benthic and planktonic algae make a greater contribution than do macrophytes to the carbon incorporated in invertebrate tissues. For example, Haines (1976) and Haines and Montague (1979) found that the 919 salt-marsh insects and snails had 613C values that corresponded with that of the Spartina; all other invertebrates, either intertidally in the marsh or subtidally in the creeks, had 613C values that were more negative, indicating a contribution from benthic or planktonic algae (Fig. 12). Using some simple assumptions, Hughes and Sherr (1983) calculated that the contribution of Spartina carbon to the carbon in animal tissues ranged from < 10% in various fish like menhaden, tongucfish, and pinfish to >40% in mummichog, with various invertebrates like crabs, shrimps, polychaetes, and squid occupying the middle of that range. Unfortunately, when there are more than two sources of food, conclusions drawn from the use of a single isotope such as 13C are ambiguous. For example, in Fig. 12 there are four food sources having 613C ratios ranging from about - 12 to -26%0. An organism with a value of, say, -2 1 could arrive at that value by consuming mostly phytoplankton, or by consuming Spartina and Juncus detritus in almost equal parts, or by numerous other combinations of foods. This kind of ambiguity can be resolved by the simultaneous use of several isotopic markers. Peterson et al. (1985) studied the distribution of 13C 15N, and 34S in upland plants, Spartina, and plankton and in ribbed mussels, Geukensia demissa. They were able to show unambiguously that the mussels consumed Spartina detritus and plankton, but not upland plant detritus. The mussels nearer the center of the marsh consumed mostly Spartina detritus, while those near the edge consumed mostly plankton. This suggests that organisms in coastal waters outside the marsh were probably receiving little Spartina detritus. Peterson et al. (1980) proposed that bacteria using sulfide derived from Spartina might fix carbon from seawater and thus have a 634Sclose to Spartina, but a FL3C close to plankton. No evidence that such sulfide oxidizers are an important food source for marine invertebrates has so far been brought forward. Hopkinson and Hoffman (1984) made organic carbon budgets for the marsh-estuarine water and nearshore waters 6-l 0 km from the coast of Georgia. They balanced community production, respiration, and Mann 920 JUNCUS SOURCE MATERIAL - BENTHIC DIATOMS PHYTOPLANKTON POM SPARTINA CREEKS - SALT MARSH INSECTS SALT MARSH SNAILS DEPOSIT-FEEDING CRABS n MUD SNAILS RIBBIED MUSSELS - INTERTIDAL INVERTEBRATES n m OYSTERS MUD CRABS SQUIID I SHRIMPS (PALAEMONETES n BLUE CRABS BROWN SHRIMPS n n SUBTIDAL INVERTEBRATES (DUPLIN RIVER) n PENAEUS) - OYSTERS n FISH (DUPL IN RIVER) n = MENHADEN II1 -25 -20 MUMMICHOG (FUNDULUS) MULLET (MUGIL) (B’REVOORTIA) I .I -15 613C -10 Fig. 12. Stable carbon isotope ratios of detritus source materials, intertidal fish in a salt-marsh area in Georgia (from Haines 1976; Haines and Montague storage against known imports and exports from the two systems. They found that production exceeded respiration in the marshestuary, providing for a net export to the turbid inner coastal zone. In this zone, respiration exceeded primary production by 210 g C me2 yr-I, which Hopkinson and Hoffman believed to be supplied by organic inputs by rivers and by export from the marsh-estuary region. Knowing the input of the rivers, they concluded that about 5% of net marsh production is required to balance the carbon budget of the turbid inner coastal waters. At this low level of dependence of the coastal waters on the salt-marsh production, it is not surprising to find that Spartina carbon constitutes a minor proportion of the carbon of subtidal invertebrates and fish. Analogous studies have been made in and around seagrass beds in various parts of the world. Thayer et al. (1978), working in the southeastern U.S.A., concluded that seagrass carbon makes a significant, but not dominant contribution to the food web of a Zostera bed. McConnaughey and McRoy -5 0 RATIO and subtidal invertebrates, 1979). and (1979) concluded that some invertebrates, such as sea stars and clams living in a seagrass bed in Alaska, derived about a quarter of their carbon from the seagrass and the remainder probably from periphyton and Shrimps and polychaete phytoplankton. worms derived even less from Zostera. Hence, in temperate and cold waters, the processing of seagrass tissue through detritus food webs appears to play a minor part in supporting invertebrates and vertebrates. In the tropics, plankton productivity tends to be limited by the existence of a permanent thermocline and low nutrient levels in surface waters, and the contribution of seagrass beds may be more significant. Fry and his coworkers (Fry and Parker 1979; Fry et al. 1982, 1983) compared the 613C ratios of animals taken offshore with those of the same or similar species taken from seagrass beds. Those from the seagrass beds were up to 8.3o/ooless negative than those from offshore, indicating that there was a substantial contribution of macrophyte carbon. These results were obtained in the Torres Strait, in the Caribbean, and off the coast of Texas. Detritus: Production and use Similarly, Rodelli et al. (1984) found that the 613C ratios of the leaves of mangroves were much more negative than those of phytoplankton or benthic algae. Of the 5 1 species of animals they studied, 29 had ratios more negative than the algae, indicating a component of mangrove detritus in the diet, and this included some commercially important species of bivalves and shrimp. Summarizing this section, detritus derived from vascular marine plants tends to have a high fiber content and low nitrogen content, so that it requires an extensive period of conditioning by microorganisms before it constitutes nutritious food for animals. In environments where less refractory algal detritus is readily available, animals may always grow up with more algal carbon than vascular macrophyte carbon in their tissues. The utilization of seaweed detritus-As one might expect, the 613C values of macroalgae are close to those of phytoplankton algae, so stable carbon isotopes are not good tracers in studies attempting to discover the relative importance of seaweeds and phytoplankton in the diet of coastal invertebrates and fish. For example, Stephenson et al. (1984) showed that the blades of Laminaria longicruris had 613C values ranging from - 12 to -20%0, according to the part of the blade from which the sample was taken, although phytoplankton (or more precisely, POC filtered from seawater) from temperate shelf and open estuarine waters normally lies between - 18 and -24?& (Fry and Sherr 1984). In a subsequent paper (Stephenson et al. 1986), the 613C ratios of animals taken from a kelp bed were compared with the ratios in animals of the same species taken from a seagrass bed. Only the small grazing gastropod Lacuna vincta had significantly different ratios, indicating that it was using carbon from the plants on which it crawled, while Littorina littorea from the eelgrass bed had the same ratio as the snails from the kelp bed, suggesting that both may have been taking mainly periphyton. Bedford and Moore (1985) made an intensive study of feeding and growth of the polychaete Platynereis dumerilii, which lives primarily on sublittoral accumulations of drifting kelp, Laminaria saccharina. The 921 worms were found to ingest fresh detritus in preference to fronds in an advanced stage of decomposition. They grew well on this diet and appeared to be a clear example of detritivores that derive their nutrition directly from the plant material without much assistance from microorganisms. Kelps of the group Laminariales have a very diverse morphology but most, if not all of them, have an active growth zone at the base of the blade and a zone of erosion at the tip of the blade. They tend to release particulate and dissolved organic matter from the erosion zone at all times of year, thus providing a continuous and dependable source of detritus for the invertebrates in the area. Perhaps the best documented study of a detritus food web in a kelp community is that carried out on the west coast of Cape Peninsula, South Africa, under the leadership of J. Field (Field et al. 1977; Newell and Field 1983; Wulff and Field 1983) and recently reviewed by Newell (1984) (Fig. 13). The kelp beds, dominated by Ecklonia maxima and Laminaria palZida, produced about 500 g C m-2 yr- 1 of POM and 250 g C me2 yr-1 of DOM. Phytoplankton production in the area was also about 500 g C m-2 yr-1 . If the system were closed, the combined phytoplankton and kelp production would just about supply the nutritional needs of the filter-feeding invertebrates. The mussels had enzyme systems capable of digesting the carbohydrates contained in the kelps (Siederer et al. 1982; Stuart 1982). By an ingenious double-labeling technique, Stuart et al. (1982) showed that the mussels in the kelp bed wcrc deriving much of their tissue carbon from the plant material rather than relying on the colonizing bacteria. The Cape Town kelp beds are adjacent to the Benguela upwelling system. During upwelling the filter feeders receive predomininantly kelp detritus, and at the time of downwelling they receive mostly phytoplankton carbon. A simulation model (Wulff and Field 1983) showed that the relative importance of phytoplankton and detritus to the filter feeders depends on the frequency of upwelling and on the rate of water movement through the kelp beds. With realistic figures for these variables, it was 922 Mann PRIMARY PRODUCTION FRAGMENTATION BACTERIAL DECOMPOSITION Bacteria 4084 CONSUMPTION ) C = 67541 Filte*,,,i;, herbivores P = 5625 y Fig. 13. Simplified energy flow diagram for a kelp bed on the west coast of Cape Peninsula, Numbers in boxes represent fluxes out of those boxes, in kJ m-2 yr-I (after Newell 1984). shown that the kelp made an important contribution. The invertebrate filter feeders supported a valuable stock of rock lobsters, so this is a good example of detritus pathways supporting a commercially important species. Observations in North America and Australia (reviewed by Mann 1982) show that kelp beds around the world provide habitat and trophic support for valuable lobster stocks. A separate study of the fate of kelp biomass cast up on beaches near Cape Town (Koop et al. 1982a,b) showed that invertebrates consumed 74% of the kelp within 8 d and bacteria consumed the remaining 26%. Invertebrate feces amounted to 67% of the kelp carbon and were in turn, metabolized by bacteria in the sand. Overall, 100 g of kelp carbon yielded 23-28 g of bacterial carbon available to higher trophic levels, but the startling finding was that this bacterial biomass contained 94% of the nitrogen originally present in the kelp. Very few studies of detritus food webs have produced budgets of both carbon and nitrogen. When we conclude that, in some situations, z4 South Africa. a relatively small proportion of detrital carbon enters invertebrate food webs, we should perhaps ask whether the proportion of nitrogen entering such webs is markedly different. Detritus in planktonic marine systemsThLeidea that detritus-based food webs might be important in planktonic marine systems was given early impetus by the work of Baylor and Sutcliffe (1963) and Sutcliffe et al. (1963) on the physical transformation of DOM to POM in the sea. Since the mass of DOM in the oceans is much greater than the biomass of living organisms, the potential biological significance of converting DOM to particles that animals could eat appeared to be considerable. The role of POM in the sea was critically reviewed by Riley (1970), who described various types of aggregates and their relationships with microbes. Then Pomeroy (1974) wrote a challenging paper entitled “The ocean’s food we:b: A changing paradigm.” He drew attention to the fact that very small cells, nannoplankton and picoplankton, are probably more important as primary producers than 923 Detritus: Production and use the well-known diatoms, and that these may be consumed by microzooplankton, about which we have very little information. More importantly from the point of view of this paper, he drew attention to the large fraction of community respiration attributable to bacteria-sized microorganisms, and he postulated that the fuel for this metabolic energy was detritus, derived from animal feces and from the DOM excreted by phytoplankton. Pomeroy (1979) followed up his ideas with a modeling exercise in which he showed that it was entirely feasible for more than half of the products of photosynthesis to pass through detritus pathways, without the observed relationship between total primary production and total fish production being violated. Pomeroy (1980) provided descriptive material to flesh out his ideas on planktonic marine detritus food webs, showing the flocculent and flake-type aggregates of POM that are probably derived from DOM by physical precipitation, the bacteria that feed on them and in turn produce strands of extracellular material, and examples of morphous detritus found within copepod fecal pellets. The question of how important detritus food webs are in supporting invertebrate and fish production in marine food webs is not yet settled. It is easy to show, using widely accepted conservative assumptions, that more phytoplankton carbon is processed by detritus pathways than by grazing pathways. As an example, in Fig. 14 (from Newell 1984) we start with 100 g C of phytoplankton production. If the herbivores consume 80 g C, 10 g C is left to decompose and 10 to sink below the thermocline. If the herbivore assimilation efficiency is 50%, then there is 40 g C of fecal pellet production. Already 10 + 10 + 40 = 60 g C has entered detritus pathways, compared with 40 assimilated by the herbivores. Such a budget leaves unanswered the question of what proportion of the detrital energy and materials ends up in stocks of commercial interest. Goldman (1984) discussed the problem of how phytoplankton cells can maintain high rates of division in a lownutrient medium such as the oligotrophic ocean. Developing the ideas of numerous earlier workers, he put forward the “aggre- =e Thermocline m Primary productlon Settlement from photic zone Fig. 14. Diagram to show how the greater part of the energy -_ in a marine planktonic system would inevitably pass through detritus pathways. Herbivore consumption- C; respiration-R; growth production - P; feces production-F. “Oxidized carbon” refers to carbon that has passed through detritus pathways. From an initial 100 g C, 49.4 in the photic zone plus 9.6 below the photic zone (i.e. 59 g C)pass through-detritus pathways (from Newell 1984). gate spinning-wheel concept” in which nutrient cycles proceed rapidly in discrete communities attached to detritus particles (Fig. 15). The community consists of small phytoplankton, bacteria which utilize the DOM produced by the phytoplankton (up to 50% of gross photosynthesis in nutrientlimited situations), and microflagellates, which consume both autotrophs and bacteria. He then suggested that in the “contemporary food chain concept,” these aggregates are the most important food source for grazers. The parallel between these ideas and those of Bowen (1984) on amorphous detrital aggregates in freshwater is very striking. Azam and Ammerman (1984), speculating along the same lines as Goldman, invoked a “cluster hypothesis” in which bacteria cluster around phytoplankton cells, making optimal use of the excreted DOM and regenerating nutrients. Mann 924 PAR \/ ,?;. . . ..‘. . ..:. ..:.. . . . ’ . .f-)o&. / y measure the latter. For example, Hargrave (1973, 1975) used this technique to determine that the sedimentation of organic carbon, S, is proportional to primary production, C, (as measured by 14C uptake), and inversely proportional to the mixed layer depth, Z,,, according to the equation s = 4.9 + 3.9g Fig. 15. Diagram of a postulated “aggregate spinning-wheel” community of phytoplankton, bacteria, and flagellates on an amorphous detrital aggregate (from Goldman 1984). Williams (1984) discussed whether the very considerable biomass of bacteria in the sea is contributing significantly to food web productivity or whether it is mainly mineralizing the materials on which the bacteria feed. He concluded that there is insufficient evidence to provide an answer. Azam et al. (1983) postulated that the bacteria are indeed extensively grazed by heterotrophic flagellates and microzooplankton, which in turn are preyed upon by larger zooplankton. They pointed out that this is a mechanism for returning DOM released by phytoplankton back to the main food chain and called the mechanism a “microbial loop.” The evidence for such a pathway had already been reviewed by Mann (1982), but convincing evidence from the natural environment is still lacking. For example, Tanoue and Hara (1986) showed that Antarctic krill feed heavily on choanoflagellates, which in turn feed on bacteria, but the relative importance of this pathway compared with that based on diatoms has not yet been demonstrated. Detrital food webs in the marine benthos-If we consider the oceans as whole, by far the greater part of the sea floor is below the photic zone; thus, its communities depend entirely on the rain of detritus to provide energy and materials for food web productivity. One way of quantifying the flux of detritus into such systems is to ignore any net accumulation in sediments, assume a balance between input of detritus and metabolism of the community, and ?,Z whlen sedimentation and production are in g C m-2 yr- l. The probable explanation is that in a deep mixed layer, the phytoplankton is kept in suspension by turbulence long enough for the zooplankton to consume most of it. When the mixed layer is shallow (as in many coastal waters), however, a good proportion of the phytoplankton sinks rapidly through it to less turbulent waters below the thermocline and then continues on to the bottom. The net result is that in coastal waters with primary production on the order of 200 g C mm2 yr-l, up to 80 g C m -2 yr-. l may reach the bottom, whereas in the great ocean basins, < 5 g C m-2 yr- l reaches the bottom. One of the interesting questions about the processing of detritus in benthic communities is this: If the carbon in the detritus were to be processed through the food chain, as follows: organic detritus -+ bacteria --$ ciliates + meiobenthos -+ macrobenthos, with an ecological efficiency of 10% at each step, the net overall efficiency of macrobenthos production as a percentage of detrital input would be only 0.0 1%. At 20% efficiency at each step it would be only 0.16%. Yet, models of benthic fish production demand an efficiency of something like 20% overall (Steele 1974; Mills 1975). Clearly, the postulated food chain is quite wrong. The evidence was reviewed in detail by Mann (1982: chapter 7), and the most logical explanation seems to be that many prominent macrofaunal species such as the filter-feeding bivalves and polychaetes, browsing epifauna such as gastropods and amphipods, and even tube-dwelling infauna are capable of intercepting newly settled de- Detritus: Production and use tritus at the sediment surface and using it directly with an efficiency up to 40%. It is worth noting that in many coastal waters, bottom-feeding fish constitute 30-50% of the commercial catches, and these benthic detritus food webs, so poorly understood, are directly responsible for supporting these valuable fisheries. Some indication of the kinds of adaptations that may make possible this high efficiency of detritus use are the demonstrations by Foulds and Mann (1978), Wainwright and Mann (1982), and Friesen et al. (1986) that the epibenthic mysid, Mysis stenolepis, can digest cellulose with endogenously produced enzymes, or that of Fong and Mann (1980) that sea urchins have a gut flora that can digest cellulose. In shallow water and intertidal areas, living benthic diatoms are available to supplement the detritus accumulating at the sediment surface. Stuart et al. (1985) showed that the amphipod Corophium volutator feeds mainly on benthic diatoms during the spring-summer period when its population growth is most rapid, but that it relies on Spartina detritus to carry it through the fallwinter period when diatom biomass is low. There is indirect evidence from a number of sources that although fresh algal cells are a superior food source to detrital particles, they are often available for only a part of the year, and that detritus particles, which tend to be available year round, serve as a supplementary food source to carry the invertebrates through periods of low algal abundance. An ecosystem view of detritus Up to now, this paper has had a rather anthropocentric flavor, revolving around the question of how important detritus is in supporting food webs leading to fish or shellfish. By implication, detrital carbon that is converted to CO, in bacterial respiration is “wasted.” Many contemporary ecosystem theorists have quite a different point of view (for review, see Rich 1984a,b, 1988) that can be traced back to Herbert Spencer with important contributions by Lovelock and Prigogine. The essence is that life and the physicochemical environment of the biosphere coevolved in a mutually depen- 925 dent manner, beginning about 3.6 billion years ago with the origin of self-reproducing organisms in a virtually oxygen-free atmosphere. During the Proterozoic Eon (2.60.6 x log yr B.P.), photolithotrophy evolved into photosynthesis, electrons were transferred from the environment to organic matter, and organic matter was transferred to the lithosphere by sedimentation. During this period, the oxygen concentration of the atmosphere rose from essentially zero to about 20%; there resulted a redox potential of about 1.5 V between upper aerobic environments and sedimented anaerobic environments. The scene was set for the evolution of eucaryotic cells and ultimately invertebrates and vertebrates. In this view of the world, the energy captured by photosynthesis is not stored in the products of photosynthesis but rather between the products of photosynthesis as redox potential (Rich 1988). Detritus in the modern world is seen as the vestige of conditions that existed before the evolution of eucaryotes. Respiration of eucaryotes is a process that also evolved in the Proterozoic Eon, providing the energy for predation (both herbivorous and carnivorous) and hence for food web linkages. Detailed consideration of the “evolutionary arms race,” in which prey evolved defenses against predation by increasing their content of indigestible material, leads to the view that detritus production from feces, etc., is an inevitable concomitant of predation, and that processes leading to fish and shellfish production (regarded by man as desirable) must of necessity be accompanied by detrital processes that renew the pool of electron-rich sedimented organic matter and, indirectly, maintain the environment for ecosystem function. When biosphere function is viewed in this detached manner, man’s preoccupation with maximizing the production of vertebrate and invertebrate food is seen as a trivial concern compared with the need to maintain a viable environment for the whole biosphere process. If predatory food webs and detritus are simply two essential aspects of heterotrophy, it is idle to speculate on whether detritus food webs are important. It is analogous to the question, at the organismal 926 level, is respiration than growth? Mann more or less important Conclusions The principles of detritus production and utilization are the same in all aquatic habitats. Dead organic matter takes two forms, dissolved (DOM) and particulate (POM), and most of the earlier work was concerned with the fate of POM. It is now known, however, that DOM is readily converted to POM by physical and biological mechanisms, so that the two forms must be considered together. Many aquatic plants give off substantial quantities of DOM both during life and soon after death, and it is now believed that a large proportion of this is quickly taken up by bacteria and converted to living bacterial biomass or to slimelike aggregates. Another fraction is converted to particulate form by physical precipitation, particularly at the surfaces of bubbles or on rocks or plant surfaces. In streams, DOM originating from allochthonous or autochthonous plants is rapidly deposited on streambeds and colonized by bacteria, fungi, and algae, which form a nutritious aggregate that is readily used by stream invertebrates. In lakes, a,morphous detrital aggregates believed to be derived from DOM are found in suspension, deposited on plant surfaces, and lying on the sediments. They are readily used by fish and amphibia. It is in planktonic systems of lakes and the sea that our knowledge of the fate of DOM is most uncertain. Many now believe that bacteria are closely associated with phytoplankton and make optimal use of the DOM released by them. It is further suggested that floating detrital aggregates support communities of organisms that include protozoa, which continuously feed on the bacteria, and that the aggregate communities are themselves consumed by copepods and other zooplankton. The fate of the particulate detritus left behind after the initial leaching of DOM depends on whether the source is vascular or nonvascular. Much algal material is readily digested and used by invertebrates without further transformation. Vascular material, on the other hand, has a high con- tent of cellulose, lignin, etc. (which most animals cannot digest) and has a lower content of amino acid nitrogen. Extensive work during the 1970s showed how such material is colonized by bacteria, shredded by invertebrates, and progressively enriched in nitrogen while the content of refractory material is being reduced. After a prolonged period of such conditioning, vascular detritus becomes nutritious for invertebrates. However, there is a subsequent phase in which much of the nitrogen in the detritus becomes bound to large molecules such as phenolics, which resist digestion by detritivores (Rice 1982; Melillo et al. 1984). The question with which we began- How important are detritus food webs in supporting the secondary productivity of commercially important species?- can now be partially answered. In the upper reaches of rivers, detritus derived from terrestrial sources is often the dominant source of energy and materials and undoubtedly supports fish production. In the lower reaches of rivers, production by benthic algae and aquatic vascular plants becomes the major source of nutrition, and detritus food webs still1 predominate. In lakes, detritus pathways are undoubtedly important in littoral zones; it has been claimed that even in the plankton, more energy and materials are transferred to zooplankton by detritus pathways than by direct grazing. The earlier idea that the productivity of coastal marshes and seagrass beds supported coastal fisheries seems not to have been confirmed by recent studies, although questions still remain. In any case, it is abundantly clear that seagrass beds provide an important habitat for many species. On the other hand, seaweed detritus appears to be utilized very effectively in coastal food chalins leading to shellfish production. The question of whether the conventional phytoplankton-zooplankton-fish food chain is predominant in open ocean waters or involving whether the “new paradigm” DOM, bacteria, and protozoa is of paramount importance is an open question and a challenge to contemporary biological oceanography. Several points emerged from -this comparison of freshwater and marine systems. Detritus: Production and use One point is that the pathway of DOM from the plant which generates it, through its physicochemical precipitation as amorphous POM, to its utilization by invertebrates, fish, and amphibia has been much better documented in freshwater than in marine environments (e.g. Bowen 1979a, b, 1980, 198 1, 1984). Estuarine ecologists have much to learn from this work, and it will be interesting to know whether the juvenile fish that forage in such large numbers in shallow estuarine waters are making as extensive use of precipitated DOM as Tilapia (Sarotherodon) has been shown to do in lakes. These fish obtain much of their nourishment by browsing on the periphyton zone of rooted plants; an investigation of the epiphytic zone of seagrasses might reveal that these also play a role as surfaces for the precipitation of DOM that subsequently enters invertebrate and vertebrate food webs. The firmly established link between detritus food webs and the growth and productivity of a commercially important freshwater fish is the best evidence available for the “usefulness” of detritus from man’s point of view. It seems probable that similar links will eventually be established for the estuarine-marine environment. It is also instructive to think about the stratification with depth of detritus food webs in freshwater and marine environments. As Bowen (1979a) showed, there is a natural sorting of detritus in the littoral zone of lakes, especially on shores with a steep slope. New amorphous POM is continually being formed in the shallow water under the influence of wave action, and the readily utilizable material becomes incorporated in higher trophic levels while refractory material tends to accumulate and move down the slope to deeper water. The result is that nearshore detritivores have a nutritious diet, while organisms farther offshore do less well. It would be surprising if similar processes were not at work in estuarine and coastal environments, though modified by the influence of tides. Camilleri and Ribi (1986) showed how the process may work in mangrove forests, and Velimirov (1986) studied DOC dynamics in a Mediterranean seagrass system. An analogous vertical zonation occurs in 927 sediments of both lakes and coastal waters. Fresh, labile detritus accumulates at the sediment-water interface and is exploited by a suite of invertebrates (e.g. chironomid larvae: Jonasson and Kristiansen 1967; gastropods and bivalves: Rhoads 1974). A proportion of the organic matter becomes buried by bioturbation, but this tends to be more refractory material. The net result is that vertical profiles show a high carbon content at the sediment surface, with a progressive decrease with increasing depth. The first few centimeters are aerobic, but below a certain depth, depending on the grain size of the sediments and the amount of surface disturbance, the sediments are rendered anaerobic by the respiration of the microorganisms, and anaerobic bacteria become active. Relatively few invertebrates inhabit the anaerobic layers, and it is thought that anaerobic fermentation at these depths results in a supply of DOM which diffuses upward and enters the pool in the overlying water (Wiebe 1979). Perhaps the strongest message from this freshwater-marine comparison is that, while research over the past lo-20 yr has paid most attention to the processes associated with fragmentation and decay of vascular plant detritus, it now appears that the fate of the DOM released in the early stages of decomposition may be ecologically more significant. In planktonic environments, the detailed relationship between the DOM released by phytoplankton, the bacteria that take it up, and the protozoa that consume the bacteria (“microbial loop”) promises to be a fertile line of enquiry. References F, AND J. W. AMMERMAN. 1984. The cycling of organic matter by bacterioplankton in pelagic marinc ecosystems: Microenvironmental considerations, p. 345-360. 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