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The Ocean's Food Web, A Changing Paradigm Author(s): Lawrence R. Pomeroy Source: BioScience, Vol. 24, No. 9 (Sep., 1974), pp. 499-504 Published by: University of California Press on behalf of the American Institute of Biological Sciences Stable URL: http://www.jstor.org/stable/1296885 . Accessed: 24/10/2011 08:56 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. University of California Press and American Institute of Biological Sciences are collaborating with JSTOR to digitize, preserve and extend access to BioScience. http://www.jstor.org The Ocean's Food Web, A Changing Paradigm Lawrence R. Pomeroy Few of us may ever live on the sea or under it, but all of us are making increasing use of it either as a source of food and other materials, or as a dump. As our demands upon the ocean increase, so does our need to understand the ocean as an ecosystem. Basic to the understanding of any ecosystem is knowledge of its food web, through which energy and materials flow. Flux of both energy and essential elements shapes or limits ecosystems, but only energy and organic compounds are considered here. The related problems of limiting supplies of essential elements (N, P, Si, Fe) will be considered elsewhere (Pomeroy'). Although the ocean's food web has been studied for more than a century, several recent discoveries lead us to believe that the classical textbook description of a chain from diatoms through copepods and krill to fishes and whales may in fact be only a small part of the flow of energy. Recent studies of microorganisms, dissolved organic matter, and nonliving organic particles in the sea suggest the presence of other pathways through which a major part of the available energy may be flowing. Marine scientists have been approaching this view of the food web cautiously for decades, and caution is to be expected whenever an established paradigm is questioned (Kuhn 1962). Now there are many lines of evidence which suggest that a new paradigm of the ocean's food web is indeed emerging. Ryther (1969) recognizes three regions of differing productivity. The open ocean, with 90% of the total area and the lowest mean rate of photosynthesis, accounts for 81.5% of primary production. Coastal waters over the continental shelves, with 9.9% of the total area and twice the rate of photosynthesis of the open ocean, account for 18% of primary production. The major upwellings, with 0.1% of the total area and a rate of photosynthesis nearly 10 times that of the open ocean, account for 0.5% of primary production. The real accuracy of these estimates is not as good as the three digit numbers suggest. The usual methods of estimating the photosynthetic rate of phytoplankton do not measure all organic matter produced, and there is rarely enough replication to give us confidence limits for the values. The most obvious plants in the sea are the seaweeds, but they probably are not the most significant primary producers. Ryther (1963) estimates that seaweeds account for 10% of the primary production of the ocean. Recent data on photosynthetic rates of kelp and other large seaweeds (Mann 1973) make that estimate seem high, although it is still difficult to make a good estimate on a planetary scale. Certainly, seaweeds and sea grasses are of major importance in the coastal zone. On a planetary scale phytoplankton are the major producers. Phytoplankton have been divided into two size groups, net plankton and nannoplankton. The separation is arbitrary, based on the THE ROLESOF MICROORGANISMS aperture of what was once the finest bolting cloth for making plankton nets. Net plankton (>60 pm) have received Photosynthesis considerable attention and form the basis of the established paradigm of the Photosynthesis is the best understood biological process in the ocean. food web, but nannoplankton (<60 pm) have proven more difficult to study and Many thousands of measurements of until recently they have been neglected. photosynthesis have been made, fairly well distributed over the World Ocean. The author is with the Departmentof Zoology, University of Georgia, Athens, GA 30602. September 1974 IPomeroy, L. R. Mineral cycling in marine ecosystems. In F. G Howell, ed. Mineral Cycling in Southeastern Ecosystems. USAEC Conf. In press. Like net plankton, they are so sparsely distributed in the water that it is necessary to concentrate them in some fashion to see them at all. Because many of them cannot be preserved well, they must be studied at sea while alive. Only recently has high magnification, oilimmersion microscopy at sea permitted the study of living nannoplankton aboard ships. Efforts to understand the relative importance of net and nannoplankton have been made by several investigators, using the 14C technique (SteemanNielsen 1952), by counting separately the radioactivity retained on discs of bolting cloth and on fine membrane filters. This was a crude separation. Some organisms larger than the aperture of the bolting cloth would be forced through it in fragments, and if a sufficiently thick layer of plankton accumulated on the bolting cloth, nannoplankton would be retained by it. In spite of these shortcomings, at least a dozen studies produced consistent results showing that the large diatoms and other net plankton, although highly visible and beautiful, account for a small fraction of total primary production. In a majority of cases nannoplankton account for more than 90% of total photosynthesis (Table 1). This is true not only in the central gyres of the ocean, but in upwellings, coastal waters, and estuaries. No one seems to have made the separation in polar regions. However, Digby (1953) found that in Scoresby Sound, Greenland, nannoplankton chlorophyll was always equal to and sometimes three times as abundant as net plankton chlorophyll. English (1961) found proportionately greater amounts of nannoplankton chlorophyll than net plankton chlorophyll at drift station Alpha in the arctic. Some remaining doubts about the validity of the results of physical separation of net plankton from nannoplankton have been dispelled by Watt (1971) who measured the rates of photosynthesis of individual phytoplankters 499 most of the energy made available by primary production. The numerical abundance of various size classes of heterotrophs has been examined by Beers, using a plankton Photosynthesis Reference Location net/nanno pump which brings water aboard ship where it passes through a series of fine meshes (Beers et al. 1967, Beers and Malone1971 Pacific Neritic 0.5 Mexico, Stewart 1969), concentrating organisms Malone1971 PeruCurrent(Equador) 0.09 Malone1971 E. tropicalPacific 0.12 in several size classes. This work focuses Malone1971 CaribbeanSea 0.10 on the abundance and description of the Watt1971 Atlanticslope, May 0.6 smaller heterotrophs, but the results Watt1971 GrandBanks,August 0.4 imply that the smaller plankton, espeWatt1971 Gulf Stream,400N, August 0.05 cially the microorganisms, should be Anderson1965 0.04 Washingtonshelf significant consumers of energy. MicroAnderson1965 0.03 Washingtonslope organisms as they are discussed in this Anderson1965 N. Pacific 0.03 paper include all Protista and not Yentsch& Ryther 1959 Sound 0.02 Vineyard bacteria alone. Only when bacteria are Teixeiraet al 1967 0.6 Mangroveestuary considered specifically will they be so Ocean Central Indian 0.04 1964 Saijo 0.07 E. IndianOcean called. Saijo& Takesue1965 0.01 Gilmartin1964 Canadianfjord New techniques for measuring in situ 0.11 Teixeira1963 TropicalAtlantic rates of respiration through biochemical 0.4 Holmes& Anderson1963 FridayHarbor,Wash. techniques offer perhaps the greatest 0.01 Holmes1958 E. tropicalPacific hope for measuring and understanding the metabolic processes of microorganisms in the sea. Two of these now Respiration by '4C autoradiography. He found that in use are the measurement of the in most cases the large diatoms and of Weknowmuchlessaboutrespiration electron transport system (ETS) dinoflagellates showed little photomeathe and in the oceanthanaboutphotosynthesis. plankton (Packard 1969) synthetic activity while nannoplankton Consumersin the ocean covera much surement of adenosine triphosphate showed much activity. In the Sargasso (ATP) content of plankton (Holmbroader spectrum of sizes than proSea one nannoplankton species, CocHansen and Booth 1966). Both methods ducers do. Even if we dismiss as insignifcolithus huxleyi, appears to be responof organisms on a icantthe respirationof all marinemam- require concentration sible for most of the photosynthesis do not necessarily give any and filter mals (cf. Holdgate 1967), it is still during most of the year. Far from being indication of the size or identity of the net of the the grasses plankton sea, impossible to collect all sizes of organorganisms. Sensitivity is isms in a single measurementof respira- respiring with appear to be the Sequoias of the sea, achieved enzyme assays. In its while the major part of photosynthesis tory rate. Moreover, total respiratory ETS method measures the form present is done by C. huxleyi and other nannorate is so low that it is necessary to in the presence of activity potential concentrate the organisms from a large plankton. a rather arbitrary and excess substrates, volume of water in order to achieve The relative importance of nannoactual electron estimate to used is factor enough sensitivity to measure changes in plankton is also suggested by recent observed the from potential transport dissolved oxygen or any other paramstudies of numerical abundance. ConThis introduces an error of unknown time. short a in of of eter ventional methods respiration studying phytomagnitude. The ATP method was origiAny concentration process has ineviplankton populations from preserved proposed as a measure of micronally table uncertainties and difficulties. samples often result in descriptions of bial biomass, but it also shows promise Despite these difficulties, several in4ominance by a succession of large as a parameter of respiration (Hobbie et diatom and dinoflagellate species. In vestigators have made physical separaal. 1972). tions of two or more size classes of reality there is usually a constant All of these approaches to measuring numerical dominance of nannoplankton plankton and have measured various each size. biochemical, microscopic, of respiration, of often respiration which are less well preserved and parameters collected suggest that microand respirometric, Johannes and Semina (1966) Pomeroy 1972, ignored (Bernard 1967, organisms are major consumers of enorganisms with a No. 2 net (366 pm) and Steidinger 1973). There is some eviergy in the sea. In the central oceanic concentrated the smaller organisms (indence that within the nannoplankton reverse-flow gyres a significant component of this is by cluding phytoplankton) (<60 gm) much of the photosynthesis of the may be the respiration of the phytojim 30 respiration than smaller comparing filtration, by organisms plankton. In the gyres growth of phytonet plankton and microorganisms. (Holmes and Anderson 1963, Saijo plankton is limited by the supply of Several similar studies have since been 1964). However, these separations, essential elements, and the ratio of World of the various in made filters membrane parts with made which were photosynthesis to respiration is low. Ocean (Pomeroy and Johannes 1968, of different porosities, have been critiIn Turner A different approach to the question 1974). Hobbie et al. 1972, cized because of the possibility of fragmicroof the relative significance of net plankof cases all respiration virtually mentation of fragile nannoplankton. ton and microorganisms is that of ShelVerification of the results by microorganisms exceeds that of net plankton don et al. (1972) who used a particle and is usually 10 times as great, suggestscopic methods such as Watt's autoare counter together with existing data on consuming ing that microorganisms radiography is needed. TABLE1. Estimates of the relativeimportanceof net phytoplanktonand nannoplanktonin photosynthesis.Mostof the valuesare mediansof sets of observations. 500 BioScience Vol. 24 No. 9 large organisms to suggest that the biomass of all size classes of organisms in the sea, from bacteria to whales, is about the same. There are problems to be resolved in discriminating living from dead particles counted. Some verification of the findings of Sheldon et al. by an independent method is needed. One such independent verification within the size range of net plankton and microorganisms seems to have been provided by Beers and Stewart (1969), albeit at a different time in a different part of the ocean. If the concept of uniform biomass distribution among size classes of organisms in the ocean is even approximately correct, the inverse relation between size and metabolic rate (Zeuthen 1947) makes the smallest organisms the largest consumers of energy. If microorganisms are major consumers in the sea, we need to know what kinds are the metabolically important ones and how they fit into the food web. At present we do not even know the relative abundance of the various kinds of protists. Few investigators have examined freshly collected populations of living microorganisms at sea. Each investigator has used his own distinctive method with little collaboration or intercomparison. What evidence we have is filled with contradictions. Large numbers of small palmelloid algae, or something of that general description, have been reported, even at considerable depth (Bernard 1967). Other investigators report large populations of bacteria (Kriss 1963, Seki 1972). Still other investigators have rarely found substantial populations of these or other recognizable microorganisms (Wiebe and Pomeroy 1972). Further studies of the systematics, abundance, and metabolic activity of the communities of microorganisms of the open sea are needed to resolve these conflicting reports. (Riley 1970, Gordon 1970a and 1970b, Wiebe and Pomeroy 1972). Several mechanisms of aggregate formation have been proposed (Nishizawa 1969, Riley 1970). Recent work suggests that some aggregates form as the result of the adherence of soluble organic molecules to the surface film of bubbles (Wheeler 1972). Other naturally occurring particles are flocculent and may be fecal or the remains of mucous nets. The proportion of particulate organic matter in the ocean which consists of authigenic aggregates, rather than fecal products or other materials, is not known, but most particulate organic matter represents secondary production of one sort or another. The fate of aggregates and other particles is uncertain, although aggregates produced in the laboratory from natural sea water can support the growth of zooplankton. It is not known whether bacteria or other protists can utilize them, but bacteria rarely are found attached to them in freshly collected samples of sea water (Wiebe and Pomeroy 1972). HeterotrophicConsumptionof DissolvedOrganicMaterial The dissolved organic matter in the World Ocean is one of the largest reserves of organic carbon on the planet. Most of it is refractory, with a residence time of thousands of years (Williams et al. 1969). Yet we know that perhaps one-fourth of the organic matter synthesized by marine phytoplankton is lost as dissolved material (Anderson and Zeutschel 1970, Thomas 1971). Most of this material probably consists of early products of photosynthesis, such as glucose or glycolic acid. There is also a substantial release of dissolved organic material during digestion, defecation, and excretion all along the food web (Webb and Johannes 1967, Corner and Davies 1971). Some of this probably is material or its precursors, but refractory INDIRECTAND ABIOTICPATHWAYS most of it is readily assimilable amino acids and larger protein fragments, Other Sources of Particulate and carbohydrates. The imlipids, OrganicMatter portance of the production of assimilable dissolved organic material has been The paradigm of the ocean's food suggested repeatedly (Khailov 1952, web is also being changed through recStrickland 1971). In a recent series of ognition of the potential importance of papers P.J. leB. Williams and his colmatter nonliving particulate organic leagues have shown that these assimiwhich does not come directly from lable compounds, which may be released primary production. Nonliving particles by either plants or animals, are removed than more abundant are of several types from sea water rapidly and efficiently. living organisms in the sea. Some reWilliams (1970) suggests that the microsemble aggregates produced from gram amounts of glucose and amino natural sea water in the laboratory September 1974 acids that we find in the sea are the concentrations below which microorganisms can no longer remove them efficiently. As soon as photosynthetic or digestive activities of plankton increase the concentration of any assimilable organic compound, the microorganisms take it up, quickly bringing the concentration of the assimilable materials back to the basal concentration. According to Andrews and Williams (1971) direct consumption of dissolved organic matter may account for half of the total degradation of organic matter in the ocean. They estimate that the consumption of glucose and amino acids by microorganisms amounted to 35% of total annual primary production. When glycolate and other carbohydrates are included, the total could indeed be 50%. This is beginning to look like a much more significant pathway than we had suspected. The identity of the microorganisms which may consume such a major share of available energy is uncertain, but the evidence points to bacteria or very small flagellates. Williams (1970) found that 80% of the microorganisms responsible for the utilization of soluble organic compounds would pass through an 8 iim membrane filter and 50% would pass a 1 pm filter. Here again there are questions about the validity of using membrane filters in this way which should be answered by autoradiography or electron microscopy. The production of soluble organic compounds and utilization of them by microorganisms occurs in all parts of the ocean. The percentage of photosynthate that is lost by phytoplankton in dissolved form varies with their nutritional state. In the central gyres, where the supply of essential elements limits growth, as much as 40% of fixed carbon is lost as soluble organic compounds, while in nutrient-rich coastal waters and upwellings only 10% is lost (Thomas 1971). Although it may seem paradoxical, the largest rate of production of soluble organic compounds by phytoplankton is in the coastal waters and upwellings, because 10% of the photosynthesis in upwellings is greater than 40% of the photosynthesis in the central gyres. It is also in the highly productive regions of the ocean that respiration is highest (Pomeroy and Johannes 1966, 1968). If small Protista are important both as primary producers and as primary consumers, this may have implications 501 PARTICULATE ORGANIC MATTER ZFECES AND D tEXCRETA DISSOLVED NET ORGANIC MATTER ZOOPLANKTON PHYTOPLANTO N FISHES NANNOPL ANKTON TOP MUCUS BACTERIA NET CARNIVORES POMAKERS PROTOZOA Fig. 1. The classical paradigm of the ocean's food web in simplified form is enclosed within the circle. More recently conceived pathways are outside the circle. The possible relative magnitude of the pathways is discussed in the text. for the remainder of the food web, including fisheries. Actively growing bacteria have high assimilation efficiency. Payne (1970) found assimilation of individual substrates by bacteria to be around 60% in laboratory cultures (compared to 10-20% for many larger organisms). Andrews and Williams (1971) and others before them found that the assimilation efficiency for glucose in the sea is as much as 65%, and the efficiency for assimilation of individual amino acids is nearly 80%. This strongly suggests that the primary consumers are active bacteria, and that they are converting a substantial fraction of primary photosynthate, and secondarily produced dissolved organic materials as well, into microbial protoplasm. This could channel into higher trophic levels at least 30% more energy than we now estimate. However, if there are long periods when no substrates are available, microorganisms may ultimately respire all they have assimilated. In this case there would be a major shunt of high grade organic energy to heat. The widely dispersed condition of bacteria and other small protists presents another problem. They can be consumed directly by other microorganisms, by mucus-net feeders such as salps or certain pteropods (Gilmer 1972), and according to laboratory ex502 periments, by some copepods. However, the highly dispersed condition of the protists may provide an effective refuge for them from filter feeders, particularly for those under 5 gm and in the open sea where their absolute abundance is lowest. We have quite limited information on the mean residence time of Protista in the open sea. If it is very short (hours), then Protista probably are an active link in a major pathway in the food web. If it is long (days or weeks), the Protista may be consuming most of the energy they capture. In this case they will be a major energy sink. Jannasch's (1969) chemostat experiments with bacteria in natural sea water indicate a generation time for bacteria of several days. If something like half of the ocean's total primary production is really moving through this pathway, we need to find out whether it is going to consumers or is lost as CO2. A NEW PARADIGM The Web of Consumers In the classical paradigm of the ocean's food web (Fig. 1) the primary consumers are thought to be net zooplankton, such as copepods, mysids, and euphausiids. The secondary and tertiary consumers are nekton, including fishes, cephalopods, and cetaceans. Microorganisms are assigned the role of decomposers (Strickland 1965, p. 585). Now there is increasing evidence that net zooplankton are not metabolically dominant. Microorganisms (whose biomass is approximately equal to that of the net plankton) are greater movers of energy and materials because of their higher metabolic rate per unit mass. The relative impact of microorganisms and macroorganisms on the flux of energy in the sea is still debated. Recent estimates of the microbial component of respiration vary from 50% (Riley 1972) to over 90% (Pomeroy and Johannes 1966). Both Strickland (1971) and Raymont (1971) suggest that microorganisms are a major metabolic component of the oceanic ecosystem, but they do not attempt to quantify their importance. Williams (1970) believes that the most active component has a size of less than 1 pm while Sheldon et al. (1973) present evidence that the most actively growing component has a size of around 4 /m. Unseen Strands in the Food Web The new paradigm of the ocean's food web that is developing, as a result of recent studies of protistan activities and alternative pathways of organic matter, may contain many unseen strands. We are not certain how the long recognized food web of diatoms and copepods fits into the expanded web which is gradually appearing. Quantitatively, large diatoms seem to be minor contributors to production, and net plankton seem to be a minor component of respiration; but if this is not the major link of photosynthesis to nekton, what is? Are the communities of upwellings really more efficient producers of nekton, and is the food web really different in them? These questions are important not only to the basic ecologist but to the fisheries scientist. The flow of useful information from basic ecology to fisheries research has been sparse. Fisheries scientists can predict optimal yields and fish population dynamics with good success, but relating fish production to processes at lower trophic levels has been less successful. Strickland (1969) said, "I doubt if much has been learned [about marine productivity] of direct help to fishermen that could not have been deduced equally well from oceanographic data on currents, convergences, upwellings, and mixing." BioScience Vol. 24 No. 9 While this may be an overly pessimistic view of the situation, one must admit that it is difficult to relate the production of tertiary consumers to unidentified primary consumers and controversial primary producers. Better strategies for utilizing the productivity of the sea might be devised if we understood in more detail the pathways of energy transfer and whether they really differ in the productive and unprodfuctive regions of the ocean. Hunting and catching methods for harvesting the wild populations of the sea have been perfected to the point where overfishing is possible, and less desirable populations will have to be exploited to expand or even sustain fishery yields. Nothing comparable to terrestrial agriculture has been developed in the sea, and there is little reason to believe that it is the best model on which to base new developments. Harvesting plants, other than coastal seaweeds, is out of the question. Monospecies animal cultures comparable to herds and flocks really do not exist, and only in circumstances where a species segregates itself (salmon, anchovies) is there immediate hope of intensive management. Only in salmon has there been significant progress in developing genetically defined populations. Management of existing wild populations now consists at best of controlling fishing pressure to optimize yield, where legal and political considerations permit. Greater yields would be possible if we could harvest the lower trophic levels, such as the larger zooplankton. This is technologically possible, but at existing population densities it is probably a poor trade for the energy required to do it. Enhancement of productivity by creating artificial upwellings has been discussed for many years. The technology for accomplishing this still seems to be marginal and costly, and little consideration has been given to the problem of managing the resulting successional changes in natural communities. Our understanding of the marine food web and the basic principles of stability and diversity of natural ecosystems is not yet sufficient for such tasks (cf. Pomeroy2). At the same time that we are approaching maximal yields from fisheries, we are forced to cope with increasing threats to the sea from pollution on a regional or even global scale. This creates a tendency to concentrate on 2See footnote 1, p. 499. September 1974 expensive technological solutions to immediate problems while providing little support for a better understanding of how the system works. In the long run, more satisfactory and probably less costly solutions can be achieved through knowledge gained through basic research. ACKNOWLEDGMENTS The viewpoint presented in this paper has developed over several years of research and discussion with colleagues, particularly Dirk Frankenberg, Robert E. Johannes, and William J. Wiebe. They also provided helpful criticism of the manuscript. Research contributing toward the development of this paper was supported by grants from the National Science Foundation. REFERENCES Anderson, G. C. 1965. Fractionation of phytoplankton communitiesoff the Washington and Oregon coasts. Limnol. Oceanogr.10: 477-480. Anderson,G. C., and R. P. Zeutschel. 1970. Release of dissolved organic matter by marine phytoplankton in coastal and offshore areas of the northeast PacificOcean. Limnol.Oceanogr.15: 402-407. Andrews, P., and P. J. leB. Williams.1971. Heterotrophic utilization of dissolved organic compounds in the sea. III. Measurement of the oxidation rates and concentrations of glucose and amino acids in sea water. J. Mar. Biol Assoc. U. K. 51: 111-125. Beers, J. R., and G. L. Stewart. 1969. Microzooplanktonand its abundancerelative to the larger zooplankton and other seston components. Mar.Biol. 4: 182-189. Beers, J. R., G. L. Stewart, and J.D.H. Strickland. 1967. A pumping system for samplingsmallplankton.J. Fish. Res. Board Can.24: 1811-1818. Bernard,F. 1967. Contributionai l' tude du 3000 m, dans les nannoplancton de 0 zones atlantiqueslusitanienneet mauritanienne (Campagnesde la "Calypso,"1960 et du "Coriolis,"1964). Pelagos7: 4-81. Corner, E.D.S., and A. G. Davies. 1971. Plankton as a factor in the nitrogen and phosphorus cycles of the sea. Adv. Mar. BioL 9: 101-204. Digby, P.S.B. 1953. Plankton production in Scoresby Sound, East Greenland.J. Anim. EcoL 22: 289-322. English, T. S. 1961. Some biologicaloceanographic observationsin the central North Polar Sea, Drift Station Alpha, 1957-1958. Arctic Instituteof North America,Research Paper13. 31 pp. Gilmartin,M. 1964. The primaryproduction of a British Columbia fjord. J. Fish. Res. BoardCan.21: 505-538. Gilmer, R. W. 1972. Free-floating mucus webs: a novel feeding adaptation for the open sea.Science 176: 1239-1240. Gordon,D. C. 1970a. A microscopicstudy of non-living organic particles in the North Atlantic Ocean.Deep-SeaRes 17: 175-185. .1970b. Some studies on the distribution and composition of particulate organiccarbonin the North AtlanticOcean. Deep-SeaRes. 17: 233-243. Hobbie,J. E., O. Holm-Hansen,T. T. Packard, L. R. Pomeroy, R. W. Sheldon, J. P. Thomas,and W.J. Wiebe. 1972. A study of the distribution and activity of microorganismsin ocean water. Limnol. Oceanogr. 17: 544-555. Holdgate, M. W. 1967. The Antarctic ecosystem. Phil, Thans. Roy. Soc. Lond. B252:363-383. Holm-Hansen,0., andC. R. Booth. 1966. The measurementof adenosine triphosphatein the ocean and its ecological significance. Limnol. Oceanogr.11: 510-519. Holmes, R. W. 1958. Size fractionation of photosynthetic phytoplankton. U.S. Fish and Wildlife Ser., Spec. Sci. Rep't. Fish. 279: 69-71. Holmes, R. W., and G. C. Anderson. 1963. Size fractionation of C14-labellednatural phytoplanktoncommunities.Pages241-250 in C. H. Oppenheimer,ed. Symposiumon Marine Biology. C. C. Thomas, Springfield, Ill. Jannasch,H.W. 1969. Estimationof bacterial growth rates in naturalwaters.J. Bacteriol 99: 156-160. Khailov, K. M. 1952. Dynamic marinebiochemistry-developmentprospects.Okeanologiya 2: 1-9. Kriss,A. E. 1963. MarineMicrobiology.Tran. J. M. Shewan and Z. Kabata. Oliver and Boyd, London. Kuhn,T. S. 1962. The Structureof Scientific Revolutions.Univ.ChicagoPress. Malone,T. C. 1971. The relativeimportance of nannoplankton and net plankton as primary producersin tropical oceanic and neritic phytoplankton communities. Limnol Oceanogr.16: 633-639. Mann, K. H. 1973. Seaweeds:their productivity and strategy for growth. Science 182: 975-981. Nishizawa,S. 1969. Suspendedmaterialin the sea. II. Re-evaluationof the hypotheses. Bull PlanktonSoc. Japan. 16: 1-42. Packard, T. T. 1969. The estimation of oxygen utilization rate in sea water from the activity of the respiratory electron transport system in plankton. Ph.D. dissertation,Univ.Washington,Seattle. Payne, W. J. 1970. Energy yields and growth of heterotrophs. Annu. Rev. Microbiol. 24: 17-52. Pomeroy, L. R., and R. E. Johannes. 1966. Total plankton respiration.Deep-Sea Res. 13: 971-973. .1968. Respirationof ultraplankton in the upper 500 meters of the ocean. Deep-SeaRes. 15: 381-391. 503 Raymont, J.E.G. 1971. Alternativesourcesof food in the sea. Pages 383-399 in J. D. Costlow, Jr., ed. Fertilityof the Sea, VoL 2. Gordonand Breach,New York. Riley, G. A. 1970. Particulateorganicmatter in sea water.Rec. Adv. Mar.BioL8: 1-118. . 1972. Patterns of production in marine ecosystems. Pages 91-100 in J. A. Wiens, ed. Ecosystem Structureand Function. Oregon State UniversityAnnualBiology Colloquium31. Ryther, J. H. 1963. Geographicvariationsin productivity. Pages 347-380 in M. N. Hill, ed. The Sea, Vol. 2. Wiley,New York. . 1969. Photosynthesis and fish pro- ductionin the sea. Science 166: 72-76. Saijo, Y. 1964. Size distributionof photosynthesizing phytoplankton in the Indian Ocean.J. Oceanogr.Soc. Jap. 19: 19-21. Saijo, Y., and K. Takesue. 1965. Further studies on the size distributionof photosynthesizing phytoplankton in the Indian Ocean. J. Oceanogr.Soc. Jap. 20: 264-271. in Seki, H. 1972. The role of microorganisms the marine food chain with reference to organic aggregates. Pages 245-259 in U. and J. W. Hopton, eds. Melchiorri-Santolini Detritus and its Role in Aquatic Ecosystems. Mem. Ist. Ital. Idrobiol. 28 (Suppl.). Semina, H. J. 1972. The size of phytoplankton cells in the Pacific Ocean. Int. Rev. ges. Hydrobiol 57: 177-205. Sheldon, R. W., A. Prakash, and W. H. Sutcliffe, Jr. 1972. The size distributionof particles in the ocean. Limnol Oceanogr. 17: 327-340. Sheldon, R. W., W. H. Sutcliffe, Jr., and A. Prakash.1973. The production of particles in the surfacewatersof the ocean with particular reference to the Sargasso Sea. LimnoLOceanogr.18: 719-733. Steeman-Nielsen,E. 1952. The use of radioactive carbon (14C) for measuringorganic production in the sea. J. Cons. Perm. Int. Explor.Mer. 18: 117-140. Steidinger,K. A. 1973. Phytoplanktonecology: a conceptualreviewbased on Eastern Gulf of Mexicoresearch.CriticalReviewsin Microbiology 3:49-68. Chemical Rubber Co., Cleveland,Ohio. Strickland, J.D.H. 1965. Production of organic matter in the primarystages of the marine food chain. Pages 477-610 in J. D. Riley and G. Skirrow,eds. ChemicalOceanography, Vol. 1. Academic Press, New York. 1969. The marinefood chainand its early stages; an assessment of present research, how well will it answertomorrow's problems? MorningReview Lectures, 2nd Int. Oceanogr. Congr., Moscow 1966. UNESCO.pp. 93-102. .1971. Microbialactivity in aquatic environments.Symp. Soc. Gen. MicrobioL 21: 231-253. Teixeira, C. 1963. Relative rates of photosynthesis and standingstock of net phytoplankton and nannoplankton. Bol. Inst. Oceanogr.Sdo Paulo 16: 39-42. Thomas, J. P. 1971. Release of dissolved organic matterfrom naturalpopulationsof marine phytoplankton. Mar. Biol. 11: 311-323. Turner, R. E. 1974. Community plankton respiration in a salt marsh tidal creek, estuary, and coastal waters of Georgia. Doctoraldissertation,Universityof Georgia, Athens. Watt, W. D. 1971. Measuringthe primary production rates of individual phytoplankton species in natural mixed populations.Deep-SeaRes. 18: 329-339. Webb, K. L., and R. E. Johannes. 1967. Studies of the release of dissolved free amino acids by marine zooplankton. LimnoL Oceanogr.12: 376-382. Wheeler,J. 1972. Some effects of solarlevels of ultravioletradiationon lipidsin artificial sea water. J. Geophys.Re&77: 5302-5306. Wiebe, W. J., and L. R. Pomeroy. 1972. Microorganismsand their associationwith aggregatesand detritusin the sea: a microscopic study. Pages 325-352 in U. Melchiorri-Santolini and J. W. Hopton,eds. Detritus and its Role in Aquatic Ecosystems. Mem. Ist. Ital. Idrobiol. 29(SuppL). Williams,P. J. leB. 1970. Heterotrophicutilization of dissolved organic compoundsin the sea. I. Size distributionof population and relationship between respiration and incorporationof growth substrates.J. Mar. Biol. Assoc. U. K. 50: 859-870. Williams,P. M., H. Oeschger,and P. Kinney. 1969. Natural radiocarbonactivity of the dissolved organic carbon in the north-east PacificOcean.Nature 224: 256-258. Yentsch, C. S., and J. H Ryther. 1959. Relative significance of the net phytoplankton and nannoplanktonin the water of Vineyard Sound. J. Cons. Int. Explor. Mer.24: 231-239. Zeuthen, E. 1947. Body size and metabolic rate in the animal kingdom with special regard to the marine micro-fauna.C. R. Lab. Carlsberg,Ser. Chim.26: 17-161. i s involved. Nikon The patient is waiting. A biopsy has been rushed to the lab. Rapid diagnosis is vital. 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