Skip to main content
SpringerLink
Log in

“A strikingly rich zone”—Nutrient enrichment and secondary production in coastal marine ecosystems

  • Published:
Estuaries Aims and scope Submit manuscript

Abstract

Despite a recent review concluding that there is little or no reason to expect that the production of fish and other animals will increase with nutrient enrichment or eutrophication, there is a variety of evidence that anthropogenic nutrients can stimulate secondary production in marine ecosystems. Unique multiple-year fertilization experiments were carried out over fifty years ago in Scottish sea lochs that showed dramatic increases in the abundance of benthic infauna and greatly enhanced growth of fish as a result of inorganic nitrogen (N) and phosphorus (P) additions. These experiments appear to have provided a good qualitative model for the responses of the Baltic Sea to nutrient enrichment and resulting eutrophication. Historical comparisons by others have shown that the weight of benthic animals per unit area above the halocline in the Baltic is now up to 10 or 20 times greater than it was in the early 1920s and that the total fish biomass in the system may have increased 8 fold between the early part of the 1900s and the 1970s. While there are no similar data for the highly enriched central and southern North Sea, there is convincing evidence that the growth rates of plaice, sole, and other species have increased there since the 1960s or 1970s. Cross-system comparisons have also shown that there are strong correlations between primary production and the production and yield of fish and the standing crop and production of benthic macrofauma in phytoplankton-dominated marine ecosystems. Concerns over the growing nutrient (especially N) enrichment of coastal marine waters are clearly valid and deserve the attention of scientists and managers, but the recent demonizing of N ignores the fact that nutrients are a fundamental requirement for producing biomass. Decisions regarding the amount of N or P that will be allowed to enter marine ecosystems should be made with the full knowledge that there may be tradeoffs between increases in water clarity and dissolved oxygen and the abundance of oysters, clams, fish, and other animals we desire.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature Cited

  • Asman, W. A. H., B. Drukker, and A. J. Janssen. 1988. Modelled historical concentrations and depositions of ammonia and ammonium in Europe.Atmospheric Environment 22:725–735.

    Article  CAS  Google Scholar 

  • Asman, W. A. H., O. Hertel, R. Berkowicz, J. Christensen, E. H. Runge, L. L. Sørensen, K. Granby, H. Nielsen, B. Jensen, S.-E. Gryning, A. M. Sempreviva, S. Larsen, P. Hummelshøj, N. O. Jensen, P. Allerup, J. Jørgensen, H. madsen, S. Overgaard, and F. Vejen. 1995. Atmospheric nitrogen input to the Kattegat.Ophelia 42:5–28.

    Google Scholar 

  • Becker, G. A. andM. Pauly. 1996. Sea surface temperature changes in the North Sea and their causes, p. 887–898.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Beukema, J. J. 1989. Long-term changes in macrozoobenthic abundance on the tidal flats of the western part of the Dutch Wadden Sea.Helgoländer Meeresuntersuchungen 43:405–415.

    Article  Google Scholar 

  • Beukema, J. J. 1991. Changes in the composition of bottom fauna of a tidal-flat area during a period of eutrophication.Marine Biology 111:293–301.

    Article  Google Scholar 

  • Beukema, J. J., G. C. Cadée, and R. Dekker. In press. Phytoplankton abundance as a limiting factor for zoobenthic biomass: A review of the evidence from parallel changes in two long-term data series in the Wadden Sea.Journal of Sea Research.

  • Blanton, J. O., K. R. Tenore, F. Castillejo, L. P. Atkinson, F. B. Schwing, andA. Lavin. 1987. The relationship of upwelling to mussel production in the rias on the western coast of Spain.Journal of Marine Research 45:497–511.

    CAS  Google Scholar 

  • Boddeke, R. 1996. Changes in the brown shrimp (Crangon crangon L.) population off the Dutch coast in relation to fisheries and phosphate discharge, p. 995–1002.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Boddeke, R. andP. Hagel. 1991. Eutrophication on the North Sea continental zone, a blessing in disguise.International Council for the Exploration of the Sea 7:1–29.

    Google Scholar 

  • Brandt, K. 1901. Life in the ocean. Annual Report of the Board of Regents of the Smithsonian Institution for the year ending June 30, 1900. United States Government Printing Office, Washington, D.C.

    Google Scholar 

  • Cadée, G. C. and J. Hegeman. In press. Phytoplankton in the Marsdiep at the end of the 20th century—30 years monitoring biomass, primary production, andPhaeocystis blooms.Journal of Sea Research.

  • Caddy, J. F. 1993. Toward a comparative evaluation of human impacts on fishery ecosystems of enclosed and semi-enclosed seas.Reviews in Fisheries Science 1:57–95.

    Article  Google Scholar 

  • Caddy, J. F. 2000. Marine catchment basin effects versus impacts of fisheries on semi-enclosed seas.ICES Journal of Marine Science 57:628–640.

    Article  Google Scholar 

  • Caddy, J. F. 2001. A brief overview of catchment basin effects on marine fisheries, p. 355–370.In N. N. Rabalais and R. E. Turner (eds.), Coastal Hypoxia: Consequences for Living Resources and Ecosystems. Coastal and Estuarine Studies 58. American Geophysical Union, Washington, D.C.

    Google Scholar 

  • Cederwall, H. andR. Elmgren. 1980. Biomass increase of benthic macrofauna demonstrates eutrophication of the Baltic Sea.Ophelia Supplement 1:287–304.

    Google Scholar 

  • Committee on the Environment and Natural Resources. 2000. Integrated Assessment of Hypoxia in the Northern Gulf of Mexico. National Science and Technology Council Committee on Environment and Natural Resources, Washington, D.C.

    Google Scholar 

  • Cloern, J. E. 1999. The relative importance of light and nutrient limitation of phytoplankton growth: A simple index of coastal ecosystem sensitivity to nutrient enrichment.Aquatic Ecology 33:3–15.

    Article  Google Scholar 

  • Cloern, J. E. 2001. Our evolving conceptual model of the coastal eutrophication problem.Marine Ecology Progress Series 210: 223–253.

    Article  CAS  Google Scholar 

  • Colijn, F., U. Tillmann, and K.-J. Hesse. In press. A large-scale uncontrolled fertilization experiment carried out in the North Sea.Hydrobiologia.

  • Cooper, L. H. N. andG. A. Steven. 1948. An experiment in marine fish cultivation.Nature 161:631–633.

    Article  Google Scholar 

  • CPR Survey Team. 1992. Continuous plankton records: The North Sea in the 1980s. 243–248.In R. R. Dickson, P. Mälkki, G. Radach, R. Saetre, and M. P. Sissenwine (eds.), Hydrobiological Variability in the ICES Area, 1980–1989. ICES Marine Science Symposia 195. International Council for the Exploration of the Sea, Copenhagen, Denmark.

    Google Scholar 

  • Cushing, J. D. H. 1975. Marine Ecology and Fisheries. Cambridge University Press, London, U.K.

    Google Scholar 

  • Daan, N. andK. Richardson (eds.) 1996. Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Daan, N., K. Richardson, andJ. G. Pope. 1996. Introdution, p. 879–883.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • de Leiva Moreno, J. V., V. N. Agostini, J. F. Caddy, andF. Carocci. 2000. Is the pelagic-demersal ratio from fishery data exploration for the semi-enclosed seas around Europe.ICES Journal of Marine Science 57:1091–1102.

    Article  Google Scholar 

  • Dowidar, N. M. 1984. Phytoplankton biomass and primary productivity of the south-eastern Mediterranean.Deep-Sea Research 31:983–1000.

    Article  CAS  Google Scholar 

  • Ecological Society of America. 2000. Nutrient pollution of coastal rivers, bays, and seas.issues in Ecology 7:1–15.

    Google Scholar 

  • Elmgren, R. 2001. Understanding human impact on the Baltic ecosystem: Changing views in recent decades.Ambio 30:222–231.

    Article  CAS  Google Scholar 

  • Elmgren, R. andU. Larsson. 2001. Nitrogen and the Baltic Sea: Managing nitrogen in relation to phosphorus.The Scientific World 1:371–377.

    Google Scholar 

  • Frid, C. L. J. andN. V. Huliselan.. 1996. Far-field control of long-term changes in Northumberland (NW North Sea) coastal zooplankton, p. 972–977.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Gaud, D. T. 1950. A fish cultivation experiment in an arm of a sea-loch. III. The plankton of Kyle Scotnish.Proceedings of the Royal Society Edinburgh 64:36–64.

    Google Scholar 

  • Gross, F. 1947. An experiment in marine fish cultivation: I. Fish, plaice, flounders, growth in a fertilized sea-loch.Proceedings of the Royal Society Edinburgh 63:56–95.

    CAS  Google Scholar 

  • Gross, F. 1950a. A fish cultivation experiment in an arm of sealoch. V. Fish growth in Kyle Scotnish.Proceedings of the Royal Society Edinburgh 64:109–135.

    Google Scholar 

  • Gross, F. 1950b. A fish cultivation in an arm of sea-loch. I. Introduction.Proceedings of the Royal Society Edinburgh 64:1–4.

    Google Scholar 

  • Halim, H. 1960. Observations on the Nile bloom of phytoplankton in the Mediterranean.Journal du Conseil International pour L’exploration de la Mer 26:57–67.

    Google Scholar 

  • Halim, Y., S. K. Guergues, andH. H. Saleh. 1967. Hydrographic conditions and plankton in the south east Mediterranean during the last normal Nile flood (1964).Internationale Revue der Gesamten Hydrobiologie 52:401–425.

    Article  Google Scholar 

  • Halim, Y., S. A. Morcos, S. Rizkalla, andM. Kh. El-Sayed. 1995. The impact of the Nile and the Suez Canal on the living marine resources of the Egyptian Mediterranean waters (1958–1986), p. 19–57.In Effects of Riverine Inputs on Coastal Ecosystems and Fisheries Resources. FAO Fisheries Technical Paper, No. 349. Food and Agriculture Organization, Rome, Italy.

    Google Scholar 

  • Hanson, J. M. andW. C. Leggett. 1982. Empirical prediction of fish biomass and yield.Canadian Journal of Fisheries and Aquatic Sciences 39:257.

    Article  Google Scholar 

  • Heessen, H. J. L. 1996. Time-series data for a selection of 40 fish species caught during the International Bottom Trawl Survey, p. 1079–1084.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Heilmann, J. P., K. Richardson, andG. Aertebjerg. 1994. Annual distribution and activity of phytoplankton in the Skagerrak-Kattegat frontal region.Marine Ecology Progress Series 112: 213–223.

    Article  Google Scholar 

  • Hempel, G. 1978. Synopsis of the symposium on North Sea fish stocks—Recent changes and their causes.Rapports et Procesverbaux des Reunions Conseil International pour L’exploration de la Mer 172:445–449.

    Google Scholar 

  • Herman, P. M. J., J. J. Middelburg, J. van de Koppel, andC. H. R. Heip. 1999. Ecology of estuarine macrobenthos.Advances in Ecological Research 29:195–240.

    Article  Google Scholar 

  • Houde, E. D. andE. S. Rutherford. 1993. Recent trends in estuarine fisheries: Predictions of fish production and yield.Estuaries 16:161–176.

    Article  Google Scholar 

  • Howarth, R. W., G. Billen, D. Swaney, A. Townsend, N. Jaworski, K. Lajtha, J. A. Downing, R. Elmgren, N. Caraco, T. Jordan, F. Berendse, J. Freney, V. Kudevarov, P. Murdoch, andZ. Zhao-Liang. 1996. Regional nitrogen budgets and riverine N and P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences.Biogeochemistry 35:75–139.

    Article  CAS  Google Scholar 

  • Hubbard Brook Research Foundation. 2002. Nitrogen Pollution: From the Sources to the Sea. Hubbard Brook Research Foundation. Hanover, New Hampshire.

    Google Scholar 

  • Iverson, R. L. 1990. Control of marine fish production.Limnology and Oceanography 35:1593–1604.

    Article  Google Scholar 

  • Johnstone, J. 1908. Conditions of Life in the Sea. Cambridge University Press, Cambridge. Reprinted by Arno Press, New York, 1977.

    Google Scholar 

  • Joint, I. andA. Pomroy. 1993. Phytoplankton biomass and production in the southern North Sea.Marine Ecology Progress Series 99:169–182.

    Article  Google Scholar 

  • Jørgensen, B. B. andK. Richardson (eds.), 1996. Eutrophication in Coastal Marine Ecosystems. American Geophysical Union, Washington, D.C.

    Google Scholar 

  • Josfson, A. B. andB. Rasmussen. 2000. Nutrient retention by benthic macrofaunal biomass of Danish estuaries: Importance of nutrient load and residence time.Estuarine, Coastal and Shelf Science 50:205–216.

    Article  CAS  Google Scholar 

  • Laane, R. W. P. M., G. Groeneveld, A. DeVries, J. Van Bennekom, andS. Sydow. 1993. Nutrients (P, N, Si) in the Channel and the Dover Strait: Seasonal and year-to-year variation and fluxes to the North Sea.Oceanologica Acta 16:607–616.

    CAS  Google Scholar 

  • Laane, R. W. P. M., A. J. Southward, D. J. Slinn, J. Allen, G. Groeneveld, andA. de Vries. 1996. Changes and causes of variability in salinity and dissolved inorganic phosphate in the Irish Sea, English Channel, and Dutch coastal zone, p. 933–944.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Larsson, U. 1986. The Baltic Sea, p. 16–70.In R. Rosenberg (ed.), Eutrophication in Marine Waters Surrounding Sweden—A Review. Report 3054. The National Swedish Environmental Protection Board, Solna, Sweden.

    Google Scholar 

  • Larsson, U., R. Elmgren, andF. Wulff. 1985. Eutrophication and the Baltic Sea: Causes and consequences.Ambio 14:9–14.

    CAS  Google Scholar 

  • Lee, G. F. andR. A. Jones. 1991. Effects of eutrophication on fisheries.Reviews in Aquatic Sciences 5:287–305.

    Google Scholar 

  • Marshall, S. M. 1947. An experiment in marine fish cultivation: III. The plankton of a fertilized loch.Proceedings of the Royal Society Edinburgh 63:21–33.

    CAS  Google Scholar 

  • Marshall, S. M. and A. P. Orr. 1948. Further experiments on the fertilization of a sea loch (loch Craiglin), the effect of different plant nutrients on the phytoplankton.Journal Marine Biological Association, United Kingdom 27:360–379.

    CAS  Google Scholar 

  • Mccomb, A. J. ed.). 1995. Eutrophic Shallow Estuaries and Lagoons. CRC Press, Inc., Boca Raton, Florida.

    Google Scholar 

  • Micheli, F. 1999. Eutrophication, fisheries, and consumer-resource dynamics in marine pelagic ecosystems.Science 285: 1396–1399.

    Article  CAS  Google Scholar 

  • Millner, R. S. andC. L. Whiting. 1996. Long-term changes in growth and population abundance of sole in the North Sea from 1940 to the present, p. 1185–1195.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Mills, E. L. 1989. Biological Oceanography. An Early History 1870–1960. Cornell University Press, Ithaca, New York.

    Google Scholar 

  • National Research Council. 2000. Clean Coastal Waters: Understanding and Reducing the Effects of Nutrient Pollution. National Academy Press, Washington, D.C.

    Google Scholar 

  • Nielsen, E. andK. Richardson. 1996. Can changes in the fisheries yield in the Kattegat (1950–1992) be linked to changes in primary production, p. 988–994.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Nixon, S. W. 1982. Nutrient dynamics, primary production and fisheries yields of lagoons.Oceanologica Acta 4:357–371.

    Google Scholar 

  • Nixon, S. W. 1986. Physical energy inputs and the comparative ecology of lake and marine ecosystems.Limnology and Oceanography 33:1005–1025.

    Google Scholar 

  • Nixon, S. W. 1992. Quantifying the relationship between nitrogen input and the productivity of marine ecosystems, p. 57–83.In M. Takahashi, K. Nakata, and T. R. Parsons (eds.), Proceedings of Advanced Marine Technology Conference (AMTEC), Volume 5, Tokyo, Japan.

  • Nixon, S. W. 1993. Nutrients and coastal waters: Too much of a good thing.Oceanus 36:38–47.

    Google Scholar 

  • Nixon, S. W. 1995. coastal marine eutrophication: A definition, social causes, and future concerns.Ophelia 41:199–219.

    Google Scholar 

  • Nixon, S. W. 1998. Enriching the sea to death.Scientific American 9:48–53.

    Google Scholar 

  • Nixon, S. W. 2000. A review of the final report from Environmental Resources Management Ltd. to the European Commission, “Verification of Vulnerable Zones Identified Under the Nitrate Directive and Sensitive Areas Identified Under the Urban Wastewater Treatment Directive—United Kingdom” and Associated Documents. Prepared for Water Quality Division, U. K. Department of the Environment, Transport and the Regions, London, U.K.

  • Nixon, S. W. 2001. Some reluctant ruminations on scales (and claws and teeth) in marine mesocosms, p. 183–195.In R. H. Gardner, W. M. Kemp, V. S. Kennedy, and J. E. Petersen (eds.), Scaling Relations in Experimental Ecology. Columbia University Press, New York.

    Google Scholar 

  • Nixon, S. W. In press. Replacing the Nile—Are anthropogenic nutrients providing the fertility once brought to the Mediterranean by a great river?Ambio

  • Nixon, S. W., J. W. Ammerman, L. P. Atkinson, V. M. Berounsky, G. Billen, W. C. Boicourt, W. R. Boynton, T. M. Church, D. M. DiToro, R. Elmgren, J. H. Garber, A. E. Giblin, R. A. Jahnke, N. J. P. Owens, M. E. Q. Pilson, andS. P. Seitzinger. 1996. The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean.Biogeochemistry 35:141–180.

    Article  CAS  Google Scholar 

  • Nixon, S., B. Buckley, S. Granger, andJ. Bintz. 2001. Responses of very shallow marine ecosystems to nutrient enrichment.Human and Ecological Rish Assessment 7:1457–1481.

    Article  Google Scholar 

  • Nixon, S. W. andM. E. Q. Pilson. 1983. Nitrogen in estuarine and coastal marine ecosystems, p. 565–648.In E. J. Carpenter and D. G. Capone (eds.), Nitrogen in the Marine Environment. Academic Press, New York.

    Google Scholar 

  • Nixon, S. W., C. A. Oviatt, J. Frithsen, andB. Sullivan. 1986. Nutrients and the productivity of estuarine and coastal marine ecosystems.Journal of the Limnological Society of Southern Africa 12:43–71.

    CAS  Google Scholar 

  • Nixon, S. andA. Thomas. 2001. On the size of the Peru upwelling ecosystem.Deep-Sea Research I 48:2521–2528.

    Article  CAS  Google Scholar 

  • Nutman, S. R. 1950. A fish cultivation experiment in an arm of a sealoch. II. Observations on some hydrographic factors in Kyle Scotnish.Proceedings of the Royal Society Edinburgh 64:5–35.

    Google Scholar 

  • Oglesby, R. T. 1977. Relationships of fish yield to lake phytoplankton standing crop, production, and morphoedaphic factors.Journal Fisheries Research Board Canada 34:2271.

    Google Scholar 

  • Ophelia 1995. Proceedings of the International Symposium on Nutrient Dynamics in Coastal and Estuarine Environments, 1993. Volumes 41 and 42. Ophelia Publications, Marine Biological Laboratory, Helsingør, Denmark.

    Google Scholar 

  • Orr, A. P. 1947. An experiment in marine fish cultivation: II. Some physical and chemical conditions in a fertilized sea-loch (Loch Craiglin, Argyll).Proceedings of the Royal Society Edinburgh 63:3–20.

    CAS  Google Scholar 

  • Paerl, H. W. 1995. Coastal eutrophication in relation to atmospheric nitrogen deposition: Current perspectives.Ophelia 41: 237–259.

    Google Scholar 

  • Pauly, D. andV. Christensen. 1995. Primary production required to sustain global fisheries.Nature 374:255–257.

    Article  CAS  Google Scholar 

  • Postma, H. 1978. The nutrient contents of North Sea water: Changes in recent years, particularly in the southern bight.Rapports et Proces-verbaux des Reunions Conseil International pour L’exploration de la Mer 172:350–357.

    Google Scholar 

  • Proceedings of the Royal Society of Edinburgh 1947. Section B (Biology), Volume LXIII, Part I. Oliver & Boyd, Edinburg and London.

    Google Scholar 

  • Proceedings of the Royal Society of Edinburgh 1950. Section B (Biology), Volume LXIV, 1949–1952. Oliver & Boyd, Edinburg and London.

    Google Scholar 

  • Rabalais, N. N., R. E. Turner, D. Justić, Q. Dortch, W. J. Wiseman, Jr., andB. K. Sen Gupta. 1996. Nutrient changes in the Mississippi River and system responses on the adjacent continental shelf.Estuaries 19:386–407.

    Article  CAS  Google Scholar 

  • Raffaelli, D. 2000. Trends in research on shallow water food webs.Journal of Experimental Marine Biology and Ecology 250: 223–232.

    Article  Google Scholar 

  • Raymont, J. E. G. 1947. An experiment in marine fish cultivation: IV. The bottom fauna and the food of flat-fishes in a fertilized sea-loch (Loch Craiglin).Proceedings of the Royal Society Edinburgh 63:34–55.

    CAS  Google Scholar 

  • Raymont, J. E. G. 1948. A fish-farming experiment in Scottish sea lochs.Journal Marine Research 6:219–227.

    Google Scholar 

  • Raymont, J. E. G. 1949. Further observations on changes in the bottom fauna of a fertilized sea loch.Journal Marine Biological Association United Kingdom 43:9–19.

    Article  Google Scholar 

  • Raymont, J. E. G. 1950. A fish cultivation experiment in an arm of a sea-loch. IV. The, bottom fauna of Kyle-Scotnish.Proceedings of the Royal Society Edinburgh 64:65–108.

    Google Scholar 

  • Richardson, K. 1996. Carbon flow in the water column case study: The southern Kattegat, p. 95–114.In B. B. Jørgensen and K. Richardson (eds.), Eutrophication in Coastal Marine Ecosystems. Coastal and Estuarine Studies 52. American Geophysical Union. Washington, D.C.

    Google Scholar 

  • Richardson, K. andJ. P. Heilmann. 1995. Primary production in the Kattegat: Past and present.Ophelia 41:317–328.

    Google Scholar 

  • Rigler, F. H. andR. H. Peters. 1995. Science and limnology, p. 239.In O. Kinne (ed.),, Excellence in Ecology, Volume 6. Ecology Institute, Oldendorf/Luhe, Germany.

    Google Scholar 

  • Rijnsdorp, A. D. andR. S. Millner. 1996. Trends in population dynamics and exploitation of North Sea plaice (Pleuronectes platessa L.) since the late 1800s, p. 1170–1184.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Rijinsdorp, A. D. andP. I. van Leeuwen. 1994. Changes in growth of North Sea plaice since 1950 in its relation to density, eutrophication, beam trawl effort and temperature.International Council for the Exploration of the Sea 9:1199–1213.

    Google Scholar 

  • Rijnsdorp, A. D. andP. I. van Leeuwen. 1996. Changes in growth of North Sea plaice since 1950 in relation to density, eutrophication, beam-trawl effort, and temperature, p. 1199–1213.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Rijnsdorp, A. D., P. I. van Leeuwen, N. Daan, andH. J. L. Heesen. 1996. Changes in abundance of demersal fish species in the North Sea between 1906–1909 and 1990–1995, p. 1054–1062.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press. London, U.K.

    Google Scholar 

  • Ryther, J. H. 1969. Photosynthesis and fish production in the sea.Science 166:72–80.

    Article  CAS  Google Scholar 

  • Schaefer, M. B. 1970. Men, birds, and anchovies in the Peru Current—Dynamic interactions.Transactions of the American Fisheries Society 99:461–467.

    Article  Google Scholar 

  • Smil, V. 1990. Nitrogen and phosphorus, p. 423–436.In B. L. Turner, II, W. C. Clark, R. W. Kates, J. F. Richards, J. T. Mathews, and W. B. Meyer (eds.), The Earth as Transformed by Human Action: Global and Regional Changes in the Biosphere Over the Past 300 Years. Cambridge University Press, Cambridge, U. K.

    Google Scholar 

  • Sparholt, H. 1990. An estimate of the total biomass of fish in the North Sea.Journal du Conseil International Pour L’exploration de la Mer 46:200–210.

    Google Scholar 

  • Steeman Nielson, E. 1964. Investigations of the rate of primary production at two Danish light ships in the transition area between the North Sea and the Baltic.Meddelelser fra Danmarks Fishen-Og Havundersøgelser, Ny Serie 4:31–77.

    Google Scholar 

  • Taylor, A. H. 1996. North-south shifts of the Gulf Stream: Ocean-atmosphere interactions in the North Atlantic.International Journal of Climatology 16:559–583.

    Article  Google Scholar 

  • Tett, P. andA. Walne. 1995. Observations and simulations of hydrography, nutrients and plankton in the southern North Sea.Ophedia 42:371–416.

    Google Scholar 

  • Thurow, F. 1997. Estimation of the total fish biomass in the Baltic Sea during the 20th century.ICES Journal of Marine Science 54:444–461.

    Article  Google Scholar 

  • Turrell, W. R. 2000. Nutrient inputs to the North Sea: A comparison of U.K. urban waste water inputs with other fluxes. Report in preparation from the Fishery Research Services Marine Laboratory, Aberdeen, Scotland.

  • Turrell, W. R., G. Slesser, R. Payne, R. D. Adams, andP. A. Gillibrand. 1996. Hydrography of the East Shetland Basin in relation to decadal North Sea variability, p. 899–916.In N. Daan and K. Richardson (eds.), Changes in the North Sea Ecosystem and Their Causes: Aarhus 1975 Revisited. ICES Journal of Marine Science Symposium Edition 53(6). Academic Press, London, U.K.

    Google Scholar 

  • Vidal, M., C. M. Duarte, andM. C. Sanchez. 1999. Coastal eutrophication research in Europe: Progress and imbalances.Marine Pollution Bulletin 38:851–854.

    Article  CAS  Google Scholar 

  • Vitousek, P. M., J. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, W. H. Schlesinger, andG. D. Tilman. 1997. Human alteration of the global nitrogen cycle: Sources and consequences.Ecological Applications 7:737–750.

    Google Scholar 

  • Vollenweider, R. A. 1968. Scientific Fundamentals of the Eutrophication of Lakes and Flowing Waters, with Particular Reference to Nitrogen and Phosphorus as Factors in Eutrophication. Organization for Economic Co-operation and Development, Paris, France.

    Google Scholar 

  • Vollenweider, R. A., R. Marchetti, andR. Viviani, (eds.) 1992. Marine Coastal Eutrophication—The Response of Marine Transitional Systems to Human Impact: Problems and Perspectives for Restoration. Proceedings of an International Conference, Bologna, Italy, 21–24 March 1990. Elsevier Science Publishers, Amsterdam, The Netherlands.

    Google Scholar 

  • Wulff, F., L. Rahm, andM. Rodriguez-Medina. 1994. Longterm and regional variations of nutrients in the Baltic Sea: 1972–1991.Finnish Marine Research 262:35–50.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Oceanography, University of Rhode Island, South Ferry Road, 02882-1197, Narragansett, Rhode Island

    Scott W. Nixon & Betty A. Buckley

Authors
  1. Scott W. Nixon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Betty A. Buckley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott W. Nixon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nixon, S.W., Buckley, B.A. “A strikingly rich zone”—Nutrient enrichment and secondary production in coastal marine ecosystems. Estuaries 25, 782–796 (2002). https://doi.org/10.1007/BF02804905

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02804905

Keywords

Search

Navigation