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Energetics of microbial food webs

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Abstract

The energetic demand of microorganisms in natural waters and the flux of energy between microorganisms and metazoans has been evaluated by empirical measurements in nature, in microcosms and mesocosms, and by simulation models. Microorganisms in temperate and tropical waters often use half or more of the energy fixed by photosynthesis. Most simulations and some experimental results suggest significant energy transfer to metazoans, but empirical evidence is mixed. Considerations of the range of growth yields of microorganisms and the number of trophic transfers among them indicate major energy losses within microbial food webs. Our ability to verify and quantify these processes is limited by the variability of assimilation efficiency and uncertainty about the structure of microbial food webs. However, even a two-step microbial chain is a major energy sink.

As an energetic link to metazoans, the detritus food web is inefficient, and its significance may have been overstated. There is not enough bacterial biomass associated with detritus to support metazoan detritivores. Much detritus is digestible by metazoans directly. Thus, metazoans and bacteria may to a considerable degree compete for a common resource. Microorganisms, together with metazoans, are important to the stability of planktonic communities through their roles as rapid mineralizers of organic matter, releasing inorganic nutrients. The competition for organic matter and the resultant rapid mineralization help maintain stable populations of phytoplankton in the absence of advective nutrient supply.

At temperatures near O °C, bacterial metabolism is suppressed more than is the rate of photosynthesis. As a result, the products of the spring phytoplankton bloom in high-temperate latitudes are not utilized rapidly by bacteria. At temperatures below 0°C microbial food webs are neither energy sinks or links: they are suppressed. Because the underlying mechanism of low-temperature inhibition is not known, we cannot yet generalize about this as a control of food web processes.

Microorganisms may operate on several trophic levels simultaneously. Therefore, the realism of the trophic level concept and the reality of the use of ecological efficiency calculations in ecosystem models is questionable.

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References

  • Andrews, P. & P. J. leB. Williams, 1971. Heterotrophic utilisation 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. Ass. U.K. 51: 111–126.

    Article  CAS  Google Scholar 

  • Azam, F. T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257–263.

    Google Scholar 

  • Bardach, J. E. & R. M. Santerre, 1980. Climate and aquatic food production. In: Proceedings of an International Workshop on Climate/Food Interactions. D. Riedel, Boston.

    Google Scholar 

  • Benner, R. & R. E. Hodson, 1985. Efficiency of conversion of lignocellulosic detritus to bacterial biomass in aquatic ecosystems. Eos 66: 1334.

    Google Scholar 

  • Bird, D. F & J. Kalff, 1986. Bacterial grazing by planktonic algae. Science 231: 493–495.

    PubMed  Google Scholar 

  • Burney, C. M., P. G. Davis, K. M. Johnson, J. McN. Sieburth, 1982. Diel relationships of microbial trophic groups and in situ dissolved carbohydrate dynamics in the Caribbean Sea. Mar. Biol. 67: 311–322.

    Article  CAS  Google Scholar 

  • Caron, D. A. & J. C. Goldman, 1987. Nutrient regeneration. In G. R. Caprulio (ed.), Ecology of Marine Protozoa. Academic Press, London.

    Google Scholar 

  • Christian, R. R. & W. J. Wiebe, 1974. Effect of temperature upon the reproduction and respiration of a marine obligate psychrophile. Can. J. Microbiol. 20: 1341–1345.

    Article  Google Scholar 

  • Darnell, R. M., 1967. Organic detritus in relation to the estuarine ecosystem. In G. H. Lauff (ed.), Estuaries. Amer. Assoc. Adv. Sci., Washington, pp. 376–382.

    Google Scholar 

  • Denman, K. L. & A. E. Gargett, 1983. Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean. Limnol. Oceanogr. 28: 801–815.

    Google Scholar 

  • Denman, K. L. & T. M. Powell, 1984. Effects of physical processes on planktonic ecosystems in the coastal ocean. Oceanogr. Mar. Biol. Ann. Rev. 22: 125–168.

    CAS  Google Scholar 

  • Ducklow, H. W. & S. M. Hill, 1985. The growth of heterotrophic bacteria in the surface waters of warm core rings. Limnol. Oceanogr. 30: 239–259.

    Google Scholar 

  • Ducklow, H. W., D. A. Purdie, P. J. leB. Williams, J. M. Davies, 1986. Bacterioplankton: A sink for carbon in a coastal marine plankton community. Science 232: 865–867.

    CAS  PubMed  Google Scholar 

  • Fasham, M. J. R., 1985. Flow analysis of materials in the marine auphotic zone. In R. E. Ulanowicz & T Platt (eds.), Ecosystem Theory for Biological Oceanography. Can. Bull. Fish. Aquat. Sci. 213: 139–162.

  • Ferguson, R. L. E. N. Buckley, A. V. Palumbo, 1984. Response of marine bacterioplankton to differential filtration and confinement. Appl. Environ. Microbiol. 47: 49–55.

    PubMed  CAS  Google Scholar 

  • Findlay, S., L. Carlough, M. T. Crocker, H. K. Gill, J. L. Meyer. & P. J. Smith, 1986. Bacterial growth on macrophyte leachate and fate of bacterial production. Limnol. Oceanogr. in press.

  • Foulds, J. B. & K. H. Mann, 1978. Cellulose digestion in Mysis stenolepis and its ecological implications. Limnol. Oceanogr. 23: 760–766.

    CAS  Google Scholar 

  • Fuhrman, J. A. & F. Azam, 1980. Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl. Environ. Microbiol. 39: 1085–1095.

    PubMed  Google Scholar 

  • Gillespie, P. A., R. Y. Morita & L. P. Jones, 1976. The heterotrophic activity for amino acids, glucose, and acetate in antarctic waters. J. Oceanogr. Soc. Japan. 32: 74–82.

    Article  CAS  Google Scholar 

  • Hagström, Å, U. Larsson, P. Norstedt & S. Normark, 1979. Frequency of dividing cells, a new approach to the determination of bacterial growth rates in aquatic environments. Appl. environ. Microbiol. 37: 805–812.

    PubMed  Google Scholar 

  • Hanson, R. B. & H. K. Lowery, 1983. Nucleic acid synthesis in oceanic microplankton from the Drake Passage, Antarctica: Evaluation of steady-state growth. Mar. Biol. 73: 79–89.

    Article  CAS  Google Scholar 

  • Hanson, R. B. & W. J. Wiebe, 1977. Heterotrophic activity associated with particulate size fractions in a Spartina alterniflora salt-marsh estuary, Sapelo Island, Georgia, U.S.A. and the continental shelf waters. Mar. Biol. 42: 321–330.

    Article  Google Scholar 

  • Hanson, R. B., H. K. Lowery, D. Shafer, R. Sorocco & D. H. Pope, 1983a. Microbes in Antarctic waters of the Drake Passage: Vertical patterns of substrate uptake, productivity, and biomass in January, 1980.

  • Hanson, R. B., D. Shafer, T. Ryan, D. H. Pope & H. K. Lowery, 1983b. Bacterioplankton in Antarctic Ocean waters during late austral winter: Abundance, frequency of dividing cells, and estimates of production. Appl. Environ. Microbiol. 45: 1622–1632.

    PubMed  Google Scholar 

  • Hempel, G., 1985. Antarctic marine food webs. In W. R. Siegfried, P. R. Condy & R. M. Laws (eds.), Antarctic Nutrient Cycles and Food webs. Springer, Berlin: 266–270.

    Google Scholar 

  • Ho, K. P. & W. J. Payne, 1979. Assimilation efficiency and energy contents of prototrophic bacteria. Biotechnol. Bioeng. 21: 787–802.

    Article  CAS  Google Scholar 

  • Hodson, R. E., F. Azam, A. F. Carlucci, J. A. Fuhrman, D. M. Karl & O. Holm-Hanson, 1981. Microbial uptake of dissolved organic matter in McMurdo Sound, Antarctica. Mar. Biol. 61: 89–94.

    Article  Google Scholar 

  • Hobbie, J. E. & C. C. Crawford, 1969. Respiration corrections for bacterial uptake of dissolved organic compounds in natural waters. Limnol. Oceanogr. 14: 528–532.

    CAS  Google Scholar 

  • Hobbie, J. E., R. J. Daley & S. Jasper, 1977. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. environ. Microbiol. 33: 1225–1228.

    PubMed  CAS  Google Scholar 

  • Hopkinson, C. S., B. Sherr, W. J. Wiebe, Size fractionated coastal plankton metabolism. Ms.

  • Imberger, J., T. Berman, R. R. Christian, E. B. Sherr, D. E. Whitney, L. R. Pomeroy, R. G. Wiegert & W. J. Wiebe. 1983. The influence of water motion on the distribution and transport of materials in a salt marsh estuary. Limnol. Oceanogr. 28: 201–214.

    Google Scholar 

  • Jacobsen, T. R., L. R. Pomeroy & J. O. Blanton, 1983. Autotrophic and heterotrophic abundance and activity associated with a nearshore front off the Georgia coast, U.S.A. Estuar. Coast, Shelf Sci. 17: 509–520.

    Article  Google Scholar 

  • Jenkins, W. J. & J. C. Goldman, 1985. Seasonal oxygen cycling and primary production in the Sargasso Sea. J. mar. Res. 43: 465–491.

    Article  CAS  Google Scholar 

  • Johannes, R. E. & M. Satomi, 1966. Composition and nutritive value of fecal pellets of a marine crustacean. Limnol. Oceanogr. 11: 191–197.

    CAS  Google Scholar 

  • Joiris, C., 1977. On the role of heterotrophic bacteria in marine ecosystems: some problems. Helgoländer wiss. Meeresunters 30: 611–621.

    Article  CAS  Google Scholar 

  • Karl, D. M., 1978. Distribution, abundance, and metabolic states of microorganisms in the water column and sediments of the Black Sea. Limnol. Oceanogr. 23: 936–949.

    CAS  Google Scholar 

  • Karl, D. M., 1979. Measurement of microbial activity and growth in the ocean by rates of stable ribonucleic acid synthesis. Appl. environ. Microbiol. 38: 850–860.

    PubMed  CAS  Google Scholar 

  • King, G. M. & T. Berman, 1985. Potential effects of isotopic dilution on apparent respiration in 14C heterotrophy experiments. Mar. Ecol. Prog. Ser. 19: 175–180.

    Google Scholar 

  • Kottmeier, J. K. T., S. M. Grossi & C. W. Sullivan, 1985. Bacterial production in annual sea ice of McMurdo Sound, Antarctica. Eos 66: 1323.

    Google Scholar 

  • Larsson, U. & Å. Hagström, 1982. Fractionated phytoplankton primary production, exudate release, and bacterial production in a Baltic eutrophic gradient. Mar. Biol. 67: 57–70.

    Article  Google Scholar 

  • Li, W. K. W., J. C. Smith & T. Platt, 1984. Temperature response of photosynthetic capacity and carboxylase activity in arctic marine phytoplankton. Mar. Ecol. Prog. Ser. 17: 237–243.

    CAS  Google Scholar 

  • Linley, E. A. S. & R. C. Newell, 1984. Estimates of bacterial growth yields based on plant detritus. Bull. mar. Sci. 35: 409–425.

    Google Scholar 

  • Martinez, L., M. W. Silver, J. M. King & A. L. Alldredge, 1983. Nitrogen fixation by floating diatom mats: A source of new nitrogen to oligotrophic ocean waters. Science 221: 152–154.

    CAS  PubMed  Google Scholar 

  • Meyer, J. L.,1986. Dissolved organic carbon dynamics in two subtropical blackwater rivers. Arch. Hydrobiol. In press.

  • Meyer-Reil, L.-A., 1978. Autoradiography and epifluorescence microscopy combined for the determination of number and spectrum of actively metabolizing bacteria in natural waters. Appl. environ. Microbiol. 36: 506–512.

    PubMed  CAS  Google Scholar 

  • Morita, R. Y., 1975. Psychrophilic bacteria. Bact. Rev. 39: 144–167.

    PubMed  CAS  Google Scholar 

  • Morita, R. Y., R. P. Griffiths & S. S. Hayasaka, 1977. Heterotrophic activity of micro-organisms in Antarctic waters. In G. A. Llano (ed.), Adaptations within Antarctic Ecosystems. Smithsonian Institution, Washington: 99–113.

    Google Scholar 

  • Newell, R. C., 1965. The role of detritus in the nutrition of two marine deposit feeders, the prosobranch Hydrobia ulvae, and the bivalve Macoma baltica. Proc. zool. Soc. Lond. 144: 25–45.

    Google Scholar 

  • Odum, E. P. & A. A. de la Cruz, 1967. Particulate organic detritus in a Georgia salt-marsh estuarine ecosystem. In G. H. Lauff (ed.), Estuaries. Amer. Assoc. Adv. Sci., Washington: 383–388.

    Google Scholar 

  • Odum, H. T., 1960. Ecological potential and analogue circuits for the ecosystem. Amer. Sci. 48: 1–8.

    Google Scholar 

  • Pace, M. L., J. E. Glasser & L. R. Pomeroy, 1984. A simulation analysis of continental shelf food webs. Mar. Biol. 82: 47–63.

    Article  Google Scholar 

  • Payne, W. J. & W. J. Wiebe, 1978. Growth yield and efficiency in chemosynthetic microorganisms. Ann. Rev. Microbiol. 32: 155–183.

    Article  CAS  Google Scholar 

  • Petersen, G. H., 1984. Energy flow in comparable aquatic ecosystems from different climatic zones. Rapp. P.-v. Réun. Cons. int. Explor. Mer. 183: 119–125.

    Google Scholar 

  • Phillips, N. W., 1984. Role of different microbes and substrates as potential suppliers of specific essential nutrients to marine detritivores. Bull. Mar. Sci. 35: 283–298.

    Google Scholar 

  • Pilson, M. E. Q. & S. W. Nixon, 1980. Marine microcosms in ecological research. In J. P. Geisy (ed.), Microcosms in Ecological Research. Tech. Information Center, U.S. Dept. Energy, Washington: 78–86.

    Google Scholar 

  • Platt, T. & W. G. Harrison, 1986. Reconciliation of carbon and oxygen fluxes in the upper ocean. Deep-Sea Res. 33: 273–276.

    Article  Google Scholar 

  • Pomeroy, L. R., 1974. The ocean's food web, a changing paradigm. BioScience 24: 499–504.

    Article  Google Scholar 

  • Pomeroy, L. R. & D. Deibel, 1980. Aggregation of organic matter by pelagic tunicates. Limnol. Oceanogr. 25: 643–652.

    Article  Google Scholar 

  • Pomeroy, L. R. & D. Deibel, 1986. Temperature regulation of bacterial activity during the spring bloom in Newfoundland coastal waters. Science. 233: 359–361.

    PubMed  Google Scholar 

  • Pomeroy, L. R. & R. E. Johannes, 1968. Respiration of ultraplankton in the upper 500 meters of the ocean. Deep-Sea Res. 15: 381–391.

    Google Scholar 

  • Pomeroy, L. R., R. B. Hanson, P. A. McGillivary, B. F. Sherr, D. Kirchman & D. Deibel, 1984. Microbiology and chemistry of fecal products of pelagic tunicates: rates and fates. Bull. mar. Sci. 35: 426–439.

    Google Scholar 

  • Riemann, B., 1985. Potential importance of fish predation and zooplankton grazing on natural populations of freshwater bacteria. Appl. Environ. Microbiol. 50: 187–193.

    PubMed  Google Scholar 

  • Robinson, J., K. Mann, J. Novitsky, 1982. Conversion of the particulate fraction of seaweed detritus to bacterial biomass. Limnol. Oceanogr. 27: 1072–1079.

    CAS  Google Scholar 

  • Schnack, S. B., V. Smetacek, B.v. Bodungen & P. Stegmann, 1985. Utilization of phytoplankton by copepods in antarctic waters during spring. In J. S. Gray & M. E. Christiansen (eds.), Marine Biology of Polar Regions and Effects of Stress on Marine Organisms. John Wiley & sons, Chichester: 65–81.

    Google Scholar 

  • Schulenberger, E. & J. L. Reid, 1981. The Pacific shallow oxygen minimum, deep chlorophyll maximum, and primary productivity reconsidered. Deep-Sea Res. 28: 901–919.

    Article  Google Scholar 

  • Sherr, B. F. & E. B. Sherr, 1984. Role of heterotrophic Protozoa in carbon and energy flow in aquatic ecosystems. In M. J. Klug & C. A. Reddy (eds.), Current Perspectives in Microbial Ecology. Amer. Soc. Microbiol., Washington: 412–423.

    Google Scholar 

  • Sieburth, J. McN., 1977. Convener's report on the informal session on biomass and productivity of microorganisms in planktonic ecosystems. Helgoländer wiss. Meeresunters. 30: 697–704.

    Article  Google Scholar 

  • Steele, J. H., 1974. The Structure of Marine Ecosystems. Harvard Univ. Press, Cambridge.

    Google Scholar 

  • Suess, E., 1980. Particulate organic carbon flux in the ocean: Surface productivity and oxygen utilization. Nature 288: 260–262.

    Article  CAS  Google Scholar 

  • Van Es, F. D. & L. A. Meyer-Reil, 1982. Biomass and metabolic activity of heterotrophic marine bacteria. In K. C. Marshall (ed.), Advances in Microbial Ecology. Plenum, New York, 6: 111–170.

    Google Scholar 

  • Vernadskii, V. I., 1926. Biosfera. Leningrad.

  • Walsh, J. J., 1969. Vertical distribution of antarctic phytoplankton. II. A comparison of phytoplankton standing crops in the Southern Ocean with that of the Florida Strait. Limnol. Oceanogr. 14: 81–94.

    Google Scholar 

  • Wiebe, W. J. & K. Bancroft, 1975. Use of adenylate energy charge ratio to measure growth state of natural microbial communities. Proc. Natl. Acad. Sci. (US.), 72: 2112–2115.

    Article  CAS  Google Scholar 

  • Wiegert, R. G., 1975. Mathematical representation of ecological interactions. In S. A. Levin (ed.), Ecosystem Analysis and Prediction. Proc. SIAM, SIMS Conf., Philadelphia Soc. Indust. Appl. Math., Philadelphia: 43–53.

    Google Scholar 

  • Williams, P. J. leB., 1981. Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meeresforsch. Sonderh. 5: 1–28.

    Google Scholar 

  • Wright, R. T. & R. B. Coffin, 1984. Measuring microzooplankton grazing on planktonic marine bacteria by its impact on bacterial production. Microb. Ecol. 10: 137–149.

    Article  Google Scholar 

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Pomeroy, L.R., Wiebe, W.J. Energetics of microbial food webs. Hydrobiologia 159, 7–18 (1988). https://doi.org/10.1007/BF00007363

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