, Volume 363, Issue 1–3, pp 1–12 | Cite as

Interactions of top-down and bottom-up control in planktonic nitrogen cycling

  • Patricia M. Glibert


Although our understanding of the complexity of theplankton and microbial food webs has increasedsubstantially over the past decade or two, there hasbeen little appreciation to date of the interactionsbetween top-down (grazing) control and bottom-up(nutrient supply) control on the structure andnutrient cycling processes within these webs. Thequality of nutrient supply, both in terms of therelative proportion of inorganic: organic nitrogen,as well as the relative proportion of inorganicnitrogen substrates has a direct impact on rates ofnitrogen uptake, and ultimately on the relativecomposition of phytoplankton and bacteria. At thesame time, grazing by microzooplankton andmacrozooplankton also influences both thecomposition of the food web and the rate of supplyof nitrogen. The impact of macrozooplankton onrates of nitrogen cycling in a microbial communityis complex: macrozooplankton release NH4 +,urea, and amino acids by direct excretion and by’sloppy feeding‘, but they also control both therates of nitrogen regeneration and uptake within thecommunity by grazing the microzooplankton, theprimary regenerators of NH4 +, and thephytoplankton, the primary consumers of nitrogen. Thus, grazing and nitrogen recycling are intricatelyconnected: the presence of large zoooplanktonsimultaneously provides top-down control of biomassand bottom-up nutrient supply. These relationshipsvary depending on the scale of interest, and haveimportant consequences for how we measure and modeltotal nitrogen cycling in a natural food web.

top-down control bottom-upcontrol NH4+regeneration nutrientlimitation trophodynamics 


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  1. Antia, N. J., P. J. Harrison & L. Oliveira, 1991. The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology. Phycologia 30: 1–89.Google Scholar
  2. Azam, F. T., T. Fenchel, J. G. Field, 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
  3. Banse, K., 1994. Grazing and zooplankton production as key controls of phytoplankton production in the open ocean. Oceanography 7: 13–20.Google Scholar
  4. Bidigare, R. R., 1983. Nitrogen excretion by marine zooplankton. In Carpenter, E. J. & D. G. Capone (eds), Nitrogen in the Marine Environment. Academic Press: 385–409.Google Scholar
  5. Boicourt, W. C., S.-Y. Chao, H. W. Ducklow, P. M. Glibert, T. C. Malone, M. R. Roman, L. P. Sanford, J. A. Fuhrman, C. Garside & R. W. Garvine, 1987. Physics and microbial ecology of a buoyant estuarine plume on the continental shelf. EOS 68: 666–668.Google Scholar
  6. Bronk, D. A. & P. M. Glibert, 1991. A 15N method for the measurement of dissolved organic nitrogen release by phytoplankton. Mar. Ecol. Prog. Ser. 77: 171–182.Google Scholar
  7. Bronk, D. A. & P. M. Glibert, 1994. The fate of the missing 15N differs among marine systems. Limnol. Oceanogr. 39: 189–195.Google Scholar
  8. Carlsson, P., E. Granéli, P. Tester & L. Boni, 1995. Influences of riverine humic substances on bacteria, protozoa, phytoplankton, and copepods in a coastal plankton community. Mar. Ecol. Prog. Ser. 127: 213–221.Google Scholar
  9. Caron, D. A. & J. C. Goldman, 1990. Protozoan nutrient regeneration. In Capriulo, G. M. (ed.), Ecology of Marine Protozoa. Oxford, 283–306.Google Scholar
  10. Chisholm, S. W., 1992. Phytoplankton size. In Falkowski, P. G. & A. D. Woodhead (eds), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum, 213–238.Google Scholar
  11. Christaki, U. &F. Van Wambeke, 1995. Simulated phytoplankton bloom input in top–down manipulated mesocosms: comparative effect of zooflagellates, ciliates and copepods. Aquat. Microb. Ecol. 9: 137–147.Google Scholar
  12. Dagg, M. J., 1974. Loss of prey contents during feeding by an aquatic predator. Ecology 55: 903–906.CrossRefGoogle Scholar
  13. Dam, H. G., X. Zhang, M. Butler & M. R. Roman, 1995. Mesozooplankton grazing and metabolism at the equator in the central Pacific: Implications for carbon and nitrogen fluxes. Deep-Sea Res. 42: 735–756.CrossRefGoogle Scholar
  14. DeBaar, H. J. W., 1994. VonLiebig’s law of the minimum and plankton ecology (1899–1991). Prog. Oceanogr. 33: 347–386.CrossRefGoogle Scholar
  15. Ducklow, H. W., M. J. R. Fasham & A. F. Vezina, 1989. Derivation and analysis of flow networks for oceanic plankton systems. In F. Wulff, J. G. Field & K. H. Mann (eds), Network Analysis in Marine Ecology. Springer 159–205.Google Scholar
  16. Dugdale, R. C. & J. J. Goering, 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12: 196–206.Google Scholar
  17. Eppley, R. W., S. G. Horrigan, J. A. Fuhrman, E. R. Brooks, C. C. Price & K. Sellner, 1981. Origins of dissolved organic matter in Southern California coastal water: experiments on the role of zooplankton. Mar. Ecol. Rog. Ser. 6: 149–159.Google Scholar
  18. Eppley, R. W. & B. J. Peterson, 1979. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282: 677–680.CrossRefGoogle Scholar
  19. Fenchel, T. & P. Harrison, 1976. The significance of bacterial grazing and mineral cycling for the decomposition of particulate detritus. In Anderson, J. M. & A. MacFayden (eds), The Role of Terrestrial and Aquatic Organisms in Decomposition Processes. Blackwell, Oxford, 285–299.Google Scholar
  20. Fisher, T. R., P. R. Carlson & R. T. Barber, 1982. Carbon and nitrogen primary productivity in three North Carolina estuaries. Estuar. coast. Shelf Sci. 15: 621–644.CrossRefGoogle Scholar
  21. Fuhrman, J. A., 1987. Close coupling between release and uptake of dissolved free amino acids in seawater studies by an isotope dilution approach. Mar. Ecol. Prog. Ser. 37: 45–52.Google Scholar
  22. Fuhrman, J. A., 1990. Dissolved free amino acid cycling in an estuarine outflow plume. Mar. Ecol. Prog. Ser. 66: 197–203.Google Scholar
  23. Fuhrman, J. A., 1992. Bacterioplankton roles in cycling of organic matter: the microbial loop. In Falkowski, P. G. & A. D. Woodhead (eds), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum, 361–383.Google Scholar
  24. Gebbing, J., 1910. Über den Gehalt des Meeres an Stickstoffnährsalzen. Untersuchungergebnisse der von der Deutschen Südpolar-Expedition (1901–1903) gesammelten Meerwasserproben. Internationale Revue der gestamten Hydrobiologie 3: 50–66.Google Scholar
  25. Glibert, P. M., 1988. Primary productivity and pelagic nitrogen cycling. In T. H. Blackburn & J. Sørensen (eds), Nitrogen Cycling in Coastal Marine Environments. SCOPE 33, J. Wiley & Sons 3–31.Google Scholar
  26. Glibert, P. M., 1993. The interdependence of uptake and release of NH4 + and organic nitrogen. Mar. Microb. Food Webs 7: 53–67.Google Scholar
  27. Glibert, P. M. & D. G. Capone, 1993. Mineralization and assimilation in aquatic, sediment, and wetland systems. In Knowles, R. & T. H. Blackburn (eds), Nitrogen Isotope Techniques, 243–272.Google Scholar
  28. Glibert, P. M., C. Garside, J. A. Fuhrman & M. R. Roman, 1991. Time-dependent coupling of inorganic and organic nitrogen uptake and regeneration in the plume of the Chesapeake Bay estuary and its regulation by large heterotrophs. Limnol. Oceanogr. 36: 895–909.CrossRefGoogle Scholar
  29. Glibert, P. M., J. C. Goldman & E. J. Carpenter, 1982. Seasonal variations in the utilization of ammonium and nitrate by phytoplankton in Vineyard Sound, Massachusetts, USA. Mar. Biol. 70: 237–249.CrossRefGoogle Scholar
  30. Glibert, P. M., C. A. Miller, C. Garside, M. R. Roman & G. B. McManus, 1992. NH4 + regeneration and grazing: interdependent processes in size–fractionated 15NH4 + experiments. Mar. Ecol. Prog. Ser. 82: 65–74.Google Scholar
  31. Goldman, J. C., 1993. Potential role of large oceanic diatoms in new primary production. Deep Sea Res. 40: 159–168.CrossRefGoogle Scholar
  32. Goldman, J. C., D. A. Caron & M. R. Dennett, 1987. Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnol. Oceanogr. 32: 1239–1252.Google Scholar
  33. Goldman, J. C. & M. R. Dennett, 1991. Ammonium regeneration and carbon utilization by marine bacteria grown on mixed substrates. Mar. Biol. 109: 369–378.CrossRefGoogle Scholar
  34. Goldman, J. C. & P. M. Glibert, 1983. Kinetics of inorganic nitrogen uptake by phytoplankton. In Carpenter, E. J. & D. G. Capone (eds), Nitrogen in the Marine Environment. Academic: 233–274.Google Scholar
  35. Hagström, Å., F. Azam, A. Andersson, J. Wikner, & F. Rassoulzadegan, 1988. Microbial loop in an oligotrophic pelagic ecosystem: Possible roles of cyanobacteria and nanoflagellates in the organic fluxes. Mar. Ecol. Prog. Ser. 49: 171–178.Google Scholar
  36. Hansen, B., P. K. Bjørnsen & P. J. Hansen, 1994. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 39: 395–403.Google Scholar
  37. Harris, E., 1959. The nitrogen cycle of Long Island Sound. Bull. Bingham, oceanogr. Coll. 17: 31–64.Google Scholar
  38. Harvey, H. W., 1945. Recent Advances in the Chemistry and Biology of Seawater. Cambridge University Press.Google Scholar
  39. Hunter, M. D. & P. W. Price, 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73: 724–732.Google Scholar
  40. Johannes, R. E., 1965. Influence of marine protozoa on nutrient regeneration. Limnol. Oceanogr. 10: 433–442.Google Scholar
  41. Johannes, R.W., 1968. Nutrient regeneration in lakes and oceans. In Droop, M. R. & E. J. F. Wood (eds), Advances in Microbiology of the Sea. Academic Press 203–213.Google Scholar
  42. Jørgensen, N. O. G., N. Kroer & R. B. Coffin, 1993. Dissolved free amino acids, combined amino acids, and DNA as sources of carbon and nitrogen to marine bacteria. Mar. Ecol. Prog. Ser. 98: 135–148.Google Scholar
  43. Kokkinakis, S. A. & P. A. Wheeler, 1988. Uptake of ammonium and urea in the northeast Pacific: comparison between netplankton and nanoplankton. Mar. Ecol. Prog. Ser. 43: 113–124.Google Scholar
  44. Lampert, W., 1978. Release of dissolved organic carbon by grazing zooplankton. Limnol. Oceanogr. 23: 831–835.Google Scholar
  45. Legendre, L. & F. Rassoulzadegan, 1995. Plankton and nutrient dynamics in marine waters. Ophelia 41: 153–172.Google Scholar
  46. Liebig, J. Von (1855) Principles of agricultural chemistry with special reference to the late researches made in England, 17–34. Reprinted in: Cycles of Essential Elements (Benchmark papers in Ecology, Vol. I, L. R. Pomeroy, 1974, Dowden, Hutchinson & Ross, Inc., Straussburg, Pennsylvania, 11–28.Google Scholar
  47. Lindeman, R. L., 1942. The trophic-dynamic aspect of ecology. Ecology 23: 399–418.CrossRefGoogle Scholar
  48. MacIsaac, J. J. & R. C. Dugdale, 1972. Interactions of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Res. 19: 209–232.Google Scholar
  49. Malone, T. C., D. J. Conley, T. R. Fisher, P. M. Glibert, L.W. Harding & K.G. Sellner, 1996. Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay. Estuaries 19: 371–385.CrossRefGoogle Scholar
  50. Malone, T. C. & H. W. Ducklow, 1990. Microbial biomass in the coastal plume of Chesapeake Bay: Phytoplanktonbacterioplankton relationships. Limnol. Oceanogr. 35: 296–312.Google Scholar
  51. McCarthy, J. J., 1982. The kinetics of nutrient utilization. In Platt, T. (ed.), Physiological Bases of Phytoplankton Ecology. Can. J. Fish. aquat. Sci 210: 211–233.Google Scholar
  52. McCarthy, J. J. & J. C. Goldman, 1979. Nitrogenous nutrition of marine phytoplankton in nutrient depleted waters. Science 203: 670–672.PubMedGoogle Scholar
  53. Miller, C. A., 1992. Effects of food quality and quantity on nitrogen excretion by the copepod, Acartia tonsa, PhD dissertation, University of Maryland, College Park.Google Scholar
  54. Miller, C. A., D. L. Penry & P. M. Glibert, 1995. The impact of trophic interactions on rates of nitrogen regeneration and grazing in Chesapeake Bay. Limnol. Oceanogr. 40: 1005–1011.Google Scholar
  55. Miller, C. A., P. M. Glibert, G. M. Berg & M. R. Mulholland, 1997. The effects of grazer and substrate amendments on nutrient and plankton dynamics in estuarine enclosures. Aquat. Microb. Ecol., 12: 251–261.Google Scholar
  56. Mousseau, L., L. Legendre & L. Fortier, 1996. Dynamics of size-fractionated phytoplankton and trophic pathways on the Scotian Shelf and at the shelf break, Northwest Atlantic. Aquat. Microb. Ecol. 10: 149–163.Google Scholar
  57. Mulholland, M. R., P. M. Glibert, G. M. Berg, L. Van Heukelem, S. Pantoja & C. Lee, in press. Extracellular amino acid oxidation by microplankton: A cross-ecosystem comparison. Aquat. microb. Ecol.Google Scholar
  58. Nathansohn, A., 1908. Über die allgemeinen Produktionsbedingungen im Meere, Beiträge zur Biologie des Planktons, von H. H. Gran und Nathansohn. Internationale Revue der gestamten Hydrobiologie 1: 38–72.Google Scholar
  59. Oviatt, C. A., 1994. Biological considerations in marine enclosure experiments: Challenges and revelations. Oceanography 7: 45–51.Google Scholar
  60. Palenik, B. & F. M. M. Morel, 1990a. Amino acid utilization by marine phytoplankton: a novel mechanism. Limnol. Oceanogr. 35: 260–269.Google Scholar
  61. Palenik, B. & F. M. M. Morel, 1990b. Comparison of cell-surface L-amino acid oxidases from several marine phytoplankton. Mar. Ecol. Prog. Ser. 59: 195–201.Google Scholar
  62. Pantoja, S. & C. Lee, 1994. Cell-surface oxidase of amino acids in sea water. Limnol. Oceanogr. 39: 1718–1725.CrossRefGoogle Scholar
  63. Paerl, H. W., 1988. Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol. Oceanogr. 33: 823–847.Google Scholar
  64. Probyn, T. A., 1985. Nitrogen uptake by size-fractionated phytoplankton population in the southern Benguela upwelling system. Mar. Ecol. Prog. Ser. 22: 249–258.Google Scholar
  65. Proctor, L. M. & J. A. Fuhrman, 1991. Roles of viral infection in organic particle flux. Mar. Ecol. Prog. Ser. 69: 133–142.Google Scholar
  66. Riemann, B., N. O. G. Jørgensen, W. Lampert & J. A. Fuhrman, 1986. Zooplankton induced changes in dissolved free amino acids and in production rates of freshwater bacteria. Microb. Ecol. 12: 247–258.CrossRefGoogle Scholar
  67. Roman, M. R., H. W. Ducklow, J. A. Fuhrman, C. Garside, P. M. Glibert, T. C. Malone & G. B. McManus, 1988. Production, consumption, and nutrient cycling in a laboratory mesocosm. Mar. Ecol. Prog. Ser. 42: 39–52.Google Scholar
  68. Roman, M. R., M. J. Furnas & M. M. Mullin, 1990. Zooplankton abundance and grazing at Davies Reef, Great Barrier Reef, Australia. Mar. Biol. 105: 73–82.CrossRefGoogle Scholar
  69. Schnepf, E. M. & M. Elbrächter, 1992. Nutritional strategies in dinoflagellates. Eur. J. Protistol. 28: 3–24.Google Scholar
  70. Suttle, C. A., A. M. Chan & M. T. Cottrell, 1991. Use of ultrafiltration to isolate viruses from seawater which are pathogens of marine phytoplankton. Appl. envir. Microbiol. 57: 721–726.Google Scholar
  71. Tupas, L. & I. Koike, 1990. Amino acid and ammonium utilization by heterotophic marine bacteria grown in enriched seawater. Limnol. Oceanogr. 35: 1145–1155.Google Scholar
  72. Vaqué, D., C. Marrasé, V. Iñiguez & M. Alcarez, 1989. Zooplankton influence on phytoplankton-bacterioplankton coupling. J. Plankton Res. 11: 625–632.Google Scholar
  73. Vezina, A. F. & T. Platt, 1987. Small-scale variability of new production and particulate fluxes in the ocean. Can. J. Fish. aquat. Sci. 44: 198–205.Google Scholar
  74. Wikner, J. & Å. Hagström, 1988. Evidence for a tightly coupled nanoplanktonic predator-prey link regulating the bacteriovores in the marine environment. Mar. Ecol. Prog. Ser. 50: 137–145.Google Scholar
  75. Williams, P. J. LeB., 1990. The importance of losses during microbial growth: Commentary on the physiology, measurement and ecology of the release of dissolved organic material. Mar. Microb. Food Webs 4: 175–193.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Patricia M. Glibert
    • 1
  1. 1.Horn Point Environmental Laboratory, Center for Environmental and Estuarine StudiesUniversity of MarylandCambridgeUSA

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