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Nitrogen, macrophytes, shallow lakes and nutrient limitation: resolution of a current controversy?

  • SHALLOW LAKE ECOSYSTEMS
  • Review Paper
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Abstract

Phosphorus (P) is conventionally thought to limit production in freshwaters and nitrogen (N) that in the sea. Before much human activity, however, co-limitation by N and P was probably normal, with systems developing ratios of N to P tending to the Redfield ratio. Single-factor limitation may be a symptom of human activity in many cases. It is widely believed that N fixation should compensate for N shortage because N fixers are ubiquitous and versatile, but this is not always the case and the issue has hitherto been considered largely with respect to plankton communities. Effects of N on macrophyte communities provide justification for control of both nutrients, at least in shallow lakes and estuaries. Increased N loading reduces plant biodiversity, changes the structure, and is associated with eventual loss, of macrophyte communities. P control alone may suffice in many deep lakes where denitrification is low and stratified conditions favour cyanobacterial development. Therein may lie a resolution to current controversies.

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References

  • Abell, J. M., D. Ozkundakci & D. P. Hamilton, 2010. Nitrogen and phosphorus limitation of phytoplankton growth in New Zealand lakes: implications for eutrophication control. Ecosystems. doi:10.1007/s10021-010-9367-9.

  • Allgeier, J. E., A. D. Rosemond & C. A. Layman, 2011. The frequency and magnitude of non additive responses to multiple nutrient enrichment. Journal of Applied Ecology 48: 96–101.

    Article  Google Scholar 

  • Anonymous (ed.), 1969. Eutrophication: Causes, Consequences, Correctives. National Academy of Sciences, Washington.

  • Barker, T., K. Hatton, M. O’Connor, L. Connor & B. Moss, 2008. Effects of nitrate load on submerged plant biomass and species richness: results of a mesocosm experiment. Fundamental and Applied Limnology 173: 89–100.

    Article  CAS  Google Scholar 

  • Beklioglu, M. & C. O. Tan, 2008. Restoration of a shallow Mediterranean lake by biomanipulation complicated by drought. Fundamental and Applied Limnology 171: 105–118.

    Article  CAS  Google Scholar 

  • Bergman, B., J. R. Gallon, A. N. Rai & L. J. Stal, 1997. N2 fixation by nonheterocystous Cyanobacteria. FEMS Microbiology Reviews 19: 139–185.

    Article  CAS  Google Scholar 

  • Bergstrom, A.-K. & M. Jansson, 2006. Atmospheric N deposition has caused enrichment and eutrophication of lakes in the northern hemisphere. Global Change Biology 12: 635–643.

    Article  Google Scholar 

  • Bergstrom, A.-K., P. Blomqvist & M. Jansson, 2005. Effects of nitrogen deposition on nutrient limitation and phytoplankton biomass in unproductive Swedish lakes. Limnology and Oceanography 50: 987–994.

    Article  Google Scholar 

  • Blann, K. L., J. L. Anderson, G. R. Sands & B. Vondracek, 2009. Effects of agricultural drainage on aquatic ecosystems: a review. Critical Reviews in Environmental Science and Technology 39(11): 909–1001.

    Article  CAS  Google Scholar 

  • Blomqvist, S., A. Gunnars & R. Elmgren, 2004. Why the limiting nutrient differs between temperate coastal seas and freshwater lakes: a matter of salt. Limnology and Oceanography 49: 2236–2241.

    Article  Google Scholar 

  • Boar, R. R., C. E. Crook & B. Moss, 1989. Regression of Phragmites australis reedswamps and recent changes of water chemistry in the Norfolk Broadland. Aquatic Botany 35: 41–55.

    Article  CAS  Google Scholar 

  • Bobbink, R., M. Hornung & J. G. M. Roelofs, 1998. The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology 86: 717–738.

    Article  CAS  Google Scholar 

  • Brookshire, E. N. J., S. Gerber, J. R. Webster, J. M. Vose & W. T. Swank, 2011. Direct effects of temperature on forest nitrogen cycling through analysis of long-term watershed records. Global Change Biology 17: 297–308.

    Article  Google Scholar 

  • Camargo, J. A. & A. Alonso, 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International 32: 831–849.

    Article  PubMed  CAS  Google Scholar 

  • Camargo, J. A., A. Alonso & A. Salamanca, 2005. Nitrate toxicity to aquatic animals: a review with new data for freshwater invertebrates. Chemosphere 58: 1255–1267.

    Article  PubMed  CAS  Google Scholar 

  • Canfield, D. E., A. N. Glazer & P. G. Falkowski, 2010. The evolution and future of Earth’s nitrogen cycle. Science 330: 192–196.

    Article  PubMed  CAS  Google Scholar 

  • Cao, T., L. Ni, P. Xie, J. Xu & M. Zhang, 2011. Effects of moderate ammonium enrichment on three submersed macrophytes under contrasting light availability. Freshwater Biology 56: 1620–1629.

    Article  CAS  Google Scholar 

  • Carter, M. C. & C. D. Foster, 2004. Prescribed burning and productivity in southern pine forests: a review. Forest Ecology and Management 191: 93–109.

    Article  Google Scholar 

  • Chen, Y., J. T. Randerson, G. R. Van der Werf, D. C. Morton, M. Q. Mu & P. S. Kasibahatla, 2010. Nitrogen deposition in tropical forests from savanna and deforestation fires. Global Change Biology 16: 2024–2038.

    Article  Google Scholar 

  • China Statistical Yearbook, 2009. China Statistics Press, Beijing.

  • Conley, D. J., H. W. Paerl, R. W. Howarth, D. F. Boesch, S. P. Seitzinger, K. E. Havens, C. Lancelot & G. E. Likens, 2009. Controlling eutrophication: nitrogen and phosphorus. Science 323: 1014–1015.

    Article  PubMed  CAS  Google Scholar 

  • Dalton, H. & R. Brand-Hardy, 2003. Nitrogen: the essential public enemy. Journal of Applied Ecology 40: 771–781.

    Article  CAS  Google Scholar 

  • Davies, H. & C. Neal, 2007. Estimating nutrient concentrations from catchment characteristics across the UK. Hydrology and Earth System Science 11: 550–558.

    Article  CAS  Google Scholar 

  • De Tezanos Pinto, P. & E. Litchman, 2009. Interactive effects of N:P ratios and light on nitrogen-fixer abundance. Oikos 119: 567–575.

    Article  CAS  Google Scholar 

  • Declerck, S., J. Vandekerkhove, L. Johansson, K. Muylaert, J.-M. Conde-Porcuna, K. Van der Gucht, T. Lauridsen, K. Schwenk, G. Zwart, W. Rommens, E. Jeppesen, W. Vyverman, L. Brendonck & L. De Meester, 2005. Biodiversity in shallow lakes: patterns of taxon richness at multiple trophic levels along a gradient in phosphorus and water plant cover. Ecology 86: 1905–1915.

    Article  Google Scholar 

  • Deegan, L. A., A. Wright, S. G. Ayvazian, J. T. Finn, H. Golden, R. R. Merson & J. Harrison, 2002. Nitrogen loading alters seagrass ecosystem structure and support of higher trophic levels. Aquatic Conservation, Marine and Freshwater Ecosystems 12: 193–212.

    Article  Google Scholar 

  • Department of the Environment, Food and Rural Affairs (UK), 2011. Fertiliser Use on Farm Crops for Crop Year 2010. H.M. Government, London.

    Google Scholar 

  • Diaz, M., F. Pedrozo, C. S. Reynolds & P. Temporettia, 2007. Chemical composition and the nitrogen-regulated trophic state of Patagonian lakes. Limnologica 37: 17–27.

    Google Scholar 

  • Dodds, W. K., W. W. Bouska, J. L. Eitzmann, T. J. Pilger, K. L. Pitts, A. J. Riley, J. T. Schloesser & D. J. Thornbrugh, 2009. Eutrophication of U.S. freshwaters; analysis of potential economic damage. Environmental Science and Technology 43: 12–19.

    Article  PubMed  CAS  Google Scholar 

  • Downing, J. A., Y. T. Prairie, J. J. Cole, C. M. Duarte, L. J. Tranvik, R. G. Striegl, W. H. McDowell, P. Kortelainen, N. F. Caraco, J. M. Melack & J. J. Middelburg, 2006. The global abundance and size distribution of lakes, ponds, and impoundments. Limnology and Oceanography 51: 2388–2397.

    Article  Google Scholar 

  • Downing, J. A., J. J. Cole, J. J. Middelburg, R. G. Striegl, C. M. Duarte, P. Kortelainen, Y. T. Prairie & K. A. Laube, 2008. Sediment organic carbon burial in agriculturally eutrophic impoundments over the last century. Global Biogeochemical Cycles 22: GB1018.

    Article  CAS  Google Scholar 

  • Edmondson, W. T., 1991. The Uses of Ecology, Lake Washington and Beyond. University of Washington Press, Seattle, London.

    Google Scholar 

  • Edmondson, W. T., G. C. Anderson & D. R. Peterson, 1956. Eutrophication of Lake Washington. Limnology and Oceanography 1: 47–53.

    Article  Google Scholar 

  • Ellis, E. C., 2011. Anthropogenic transformation of the terrestrial biosphere. Philosophical Transactions of the Royal Society A 369: 1010–1035.

    Article  Google Scholar 

  • Elser, J. J., M. E. S. Bracken, E. A. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin & J. E. Smith, 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135–1142.

    Article  PubMed  Google Scholar 

  • Elser, J. J., T. Andersen, J. S. Baron, A. K. Bergstrom, M. Jansson, M. Kyle, K. R. Nydick, L. Steger & D. O. Hessen, 2009. Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science 326: 835–836.

    Article  PubMed  CAS  Google Scholar 

  • Engstrom, D. R., S. C. Fritz, J. E. Almendinger & S. Juggins, 2000. Chemical and biological trends during lake evolution in recently deglaciated terrain. Nature 408: 161–166.

    Article  PubMed  CAS  Google Scholar 

  • Feuchtmayr, H., R. Moran, K. Hatton, L. Connor, T. Heyes, B. Moss, I. Harvey & D. Atkinson, 2009. Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental, hypertrophic, shallow lake mesocosms. Journal of Applied Ecology 46: 713–723.

    Article  Google Scholar 

  • Foy, R. H. & S. D. Lennox, 2006. Evidence for a delayed response of riverine phosphorus exports from increasing agricultural catchment pressures in the Lough Neagh catchment. Limnology and Oceanography 51: 655–663.

    Article  Google Scholar 

  • Friberg, N., J. B. Dybkjær, J. S. Olafsson, G. M. Gıslason, S. E. Larsen & T. L. Lauridsen, 2009. Relationships between structure and function in streams contrasting in temperature. Freshwater Biology 54: 2051–2068.

    Article  CAS  Google Scholar 

  • Galloway, J. N., A. R. Townsend, J. W. Erisman, M. Bekunda, Z. Cai, J. R. Freney, L. A. Martinelli, S. P. Seitzinger & M. A. Sutton, 2008. Transformations of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320: 889–892.

    Article  PubMed  CAS  Google Scholar 

  • Ganff, G. G. & A. J. Horne, 1975. Diurnal stratification, photosynthesis and nitrogen fixation in a shallow, equatorial lake (Lake George, Uganda). Freshwater Biology 5: 13–39.

    Article  Google Scholar 

  • Genkai-Kato, M., L. Liboriussen, Y. Vadeboncoeur & E. Jeppesen, in press. Benthic-pelagic coupling and regime shifts in shallow lakes, and the consequences for whole-lake primary production. Ecology

  • Goldman, C. R., 1988. Primary productivity, nutrients, and transparency during the early onset of eutrophication in ultraoligotrophic Lake Tahoe, California-Nevada. Limnology and Oceanography 33: 1321–1333.

    Article  CAS  Google Scholar 

  • Goldman, J. C., J. J. McCarthy & D. G. Peavey, 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279: 210.

    Article  CAS  Google Scholar 

  • Golterman, H. L., 2000. Denitrification and a numerical modelling approach for shallow waters. Hydrobiologia 431: 93–104.

    Article  CAS  Google Scholar 

  • Gondwe, M. J., S. J. Guildford & R. E. Hecky, 2008. Planktonic nitrogen fixation in Lake Malawi/Nyasa. Hydrobiologia 596: 251–267.

    Article  CAS  Google Scholar 

  • Gonzales Sagrario, M. A., E. Jeppesen, J. Goma, M. Søndergaard, T. Lauridsen & F. Landkildehus, 2005. Does high nitrogen loading prevent clear-water conditions in shallow lakes at moderately high phosphorus concentrations? Freshwater Biology 50: 27–41.

    Article  CAS  Google Scholar 

  • Gruber, N. & J. N. Galloway, 2008. An earth-system perspective of the global nitrogen cycle. Nature 451: 293–296.

    Article  PubMed  CAS  Google Scholar 

  • Gudmundsdottir, R., J. Olafsson, S. Palsson, G. M. Gislason & B. Moss, 2011. How will increased temperature and nutrient enrichment affect primary producers in sub-Arctic streams? Freshwater Biology 56: 2045–2058.

    Article  Google Scholar 

  • Guildford, S. J. & R. E. Hecky, 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship? Limnology and Oceanography 45: 1213–1223.

    Article  CAS  Google Scholar 

  • Halm, H., N. Musat, P. Lam, R. Langlois, F. Musat, S. Peduzzi, G. Lavik, C. J. Schubert, B. Singha, J. LaRoche & M. M. M. Kuypers, 2009. Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environmental Microbiology 11: 1945–1958.

    Article  PubMed  CAS  Google Scholar 

  • Hameed, H. A., S. Kilinc, S. Mcgowan & B. Moss, 1999. Physiological tests and bioassays – aids or superfluities to the diagnosis of phytoplankton nutrient limitation? A comparative study in the Broads and Meres of England. European Phycological Journal 34: 253–270.

    Article  Google Scholar 

  • Hansson, L.-A., 1988. Effects of competitive interactions on the biomass development of planktonic and periphytic algae in lakes. Limnology and Oceanography 33: 121–128.

    Article  CAS  Google Scholar 

  • Hansson, L.-A., 1990. Quantifying the impact of periphytic algae on nutrient availability for phytoplankton. Freshwater Biology 24: 265–273.

    Article  Google Scholar 

  • Hasler, A. D., 1947. Eutrophication of lakes by domestic drainage. Ecology 28: 383–395.

    Article  Google Scholar 

  • Hauxwell, J., J. Cebrian & I. Valiela, 2003. Eelgrass, Zostera marina, loss in temperate estuaries: relationship to land-derived nitrogen loads and effect of light limitation imposed by algae. Marine Ecology-Progress Series 247: 59–73.

    Article  CAS  Google Scholar 

  • Haworth, E. Y., 1969. The diatoms of a sediment core from Blea Tarn, Langdale. Journal of Ecology 57: 429–439.

    Article  Google Scholar 

  • Hecky, R. E. & P. Kilham, 1988. Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment. Limnology and Oceanography 33: 796–822.

    Article  CAS  Google Scholar 

  • Hecky, R. E., P. Campbell & L. L. Hendzel, 1993. The stoichiometry of carbon, nitrogen, and phosphorus in particulate matter of lakes and oceans. Limnology and Oceanography 38: 709–724.

    Article  CAS  Google Scholar 

  • Herrman, K. S., V. Bouchard & R. H. Moore, 2008. Factors affecting denitrification in agricultural headwater streams in Northeast Ohio, USA. Hydrobiologia 598: 304–314.

    Article  CAS  Google Scholar 

  • Hoffmann, C. C. & A. Baattrup-Pedersen, 2007. Re-establishing freshwater wetlands in Denmark. Ecological Engineering 30: 157–166.

    Article  Google Scholar 

  • Horne, A. J. & G. E. Fogg, 1970. Nitrogen fixation in some English lakes. Proceedings of the Royal Society of London Series B 175: 351–366.

  • Horne, A. J. & C. R. Goldman, 1972. Nitrogen fixation in Clear Lake, California. I. Seasonal variation and the role of heterocysts. Limnology and Oceanography 17: 678–692.

    Article  Google Scholar 

  • Howarth, R. W., R. Marino, J. Lane & J. J. Cole, 1988. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnology and Oceanography 33(4): 669–687.

    Article  CAS  Google Scholar 

  • Hutchinson, G. E., 1973. Eutrophication. American Scientist 61: 269–279.

    CAS  Google Scholar 

  • Interlandi, S. J. & S. S. Kilham, 2001. Limiting resources and the regulation of diversity in phytoplankton communities. Ecology 82: 1270–1282.

    Article  Google Scholar 

  • James, C., J. Fisher & B. Moss, 2003. Nitrogen driven lakes: the Shropshire and Cheshire Meres? Archive für Hydrobiologie 158: 249–266.

    Article  CAS  Google Scholar 

  • James, C. S., J. Fisher, V. Russell, S. Collings & B. Moss, 2005. Nitrate availability and hydrophyte species richness in shallow lakes. Freshwater Biology 50: 1049–1063.

    Article  CAS  Google Scholar 

  • James, R. T., W. S. Gardner, M. J. McCarthy & S. A. Carini, 2011. Nitrogen dynamics in Lake Okeechobee, forms, functions and changes. Hydrobiologia 669: 199–212.

    Article  CAS  Google Scholar 

  • Jeppesen, E., J. P. Jensen, M. Søndergaard & T. Lauridsen, 2005a. Response of fish and plankton to nutrient loading reduction in 8 shallow Danish lakes with special emphasis on seasonal dynamics. Freshwater Biology 50: 1616–1627.

    Article  CAS  Google Scholar 

  • Jeppesen, E., M. Søndergaard, J. P. Jensen, K. Havens, O. Anneville, L. Carvalho, M. F. Coveney, R. Deneke, M. Dokulil, B. Foy, D. Gerdeaux, S. E. Hampton, K. Kangur, J. Köhler, S. Körner, E. Lammens, T. L. Lauridsen, M. Manca, R. Miracle, B. Moss, P. Nõges, G. Persson, G. Phillips, R. Portielje, S. Romo, C. L. Schelske, D. Straile, I. Tatrai, E. Willén & M. Winder, 2005b. Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.

    Article  CAS  Google Scholar 

  • Jeppesen, E., B. Kronvang, M. Meerhoff, M. Søndergaard, K. M. Hansen, H. E. Andersen, T. L. Lauridsen, M. Beklioglu, A. Özen & J. E. Olesen, 2009. Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. Journal of Environmental Quality 38: 1030–1041.

    Article  CAS  Google Scholar 

  • Jeppesen, E., M. Meerhoff, K. Holmgren, I. González-Bergonzoni, F. Teixeira-de Mello, S. A. J. Declerk, L. De Meester, M. Søndergaard, T. L. Lauridsen, R. Bjerring, J. M. Conde-Porcuna, N. Mazzeo, C. Iglesias, M. Reizenstein, H. J. Malmquist, D. Balayla & X. Lazzaro, 2010a. Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646: 73–90.

    Article  CAS  Google Scholar 

  • Jeppesen, E., B. Moss, H. Bennion, L. Carvalho, L. DeMeester, H. Feuchtmayr, N. Friberg, M. O. Gessner, M. Hefting, T. L. Lauridsen, L. Liboriussen, H. Malmquist, L. May, M. Meerhoff, J. S. Olafsson, M. B. Soons & J. T. A. Verhoeven, 2010b. Chapter 6: Interaction of climate and eutrophication. In Kernan, M., R. Battarbee & B. Moss (eds), Changing Climate and Changing Freshwaters: A European Perspective. Wiley-Blackwell, Oxford: 119–151.

    Google Scholar 

  • Jeppesen, E., B. Kronvang, J. E. Olesen, J. Audet, M. Søndergaard, C. C. Hoffmann, H. E. Andersen, T. L. Lauridsen, L. Liboriussen, S. E. Larsen, M. Beklioglu, M. Meerhoff, A. Ozen & K. Ozkan, 2011. Climate change effects on nitrogen loading from cultivated catchments in Europe: implications for nitrogen retention, ecological state of lakes and adaptation. Hydrobiologia 663: 1–21.

    Article  CAS  Google Scholar 

  • Kilham, P. & S. S. Kilham, 1990. Endless summer: internal loading processes dominate nutrient cycling in tropical lakes. Freshwater Biology 23: 379–389.

    Article  Google Scholar 

  • Kilinc, S. 1995. Limnological studies on the North West Midland meres, with special reference to White Mere. Ph.D. Thesis, University of Liverpool, UK.

  • Kilinc, S. & B. Moss, 2002. Whitemere, a lake that defies some conventions about nutrients. Freshwater Biology 47: 207–218.

    Article  Google Scholar 

  • Köhler, J., S. Hilt, R. Adrian, A. Nicklisch, H. P. Kozerski & N. Walz, 2005. Long-term response of a shallow, moderately flushed lake to reduced external phosphorus and nitrogen loading. Freshwater Biology 50: 1639–1650.

    Article  CAS  Google Scholar 

  • Kosten, S., V. L. M. Huszar, N. Mazzeo, M. Scheffer, L. da. S. L. Sternberg & E. Jeppesen, 2009. Lake and watershed characteristics rather than climate influence nutrient limitation in shallow lakes. Ecological Applications 19: 1791–1804.

    Article  PubMed  Google Scholar 

  • Kosten, S., V. Huszar, E. Becares, L. Costa, E. Van Donk, L.-A. Hansson, E. Jeppesen, C. Kruk, G. Lacerot, N. Mazzeo, L. De Meester, B. Moss, M. Lurling, T. Noges, S. Romo & M. Scheffer, 2012. Warmer climate boosts cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118–126.

    Article  Google Scholar 

  • Kronvang, B., E. Jeppesen, D. J. Conley, M. Søndergaard, S. E. Larsen, N. B. Ovesen & J. Carstensen, 2005. Nutrient pressures and ecological responses to nutrient loading reductions in Danish streams, lakes and coastal waters. Journal of Hydrology 304: 274–288.

    Article  CAS  Google Scholar 

  • Kronvang, B., J. Windolf, R. Grant, H. E. Andersen, H. Thodsen, N. B. Ovesen & S. E. Larsen, 2009. Linking monitoring and modelling for river basin management: Danish experience with combating nutrient loadings to the aquatic environment from point and nonpoint sources. Science in China Series E: Technological Sciences 52: 1–15.

    Article  CAS  Google Scholar 

  • Kuentzel, L. E., 1969. Bacteria, carbon dioxide and algal blooms. Journal of the Water Pollution Control Federation 41: 1737–1747.

    PubMed  CAS  Google Scholar 

  • Lambert, S. J. & A. J. Davy, 2011. Water quality as a threat to aquatic plants: discriminating between the effects of nitrate, phosphate, boron and heavy metals on charophytes. New Phytologist 189: 1051–1059.

    Article  PubMed  CAS  Google Scholar 

  • Latimer, J. S. & S. A. Rego, 2010. Empirical relationship between eelgrass extent and predicted watershed-derived nitrogen loading for shallow New England estuaries. Estuarine, Coastal and Shelf Science 90: 231–240.

    Article  CAS  Google Scholar 

  • Lehman, J. T., D. B. Botkin & G. E. Likens, 1975. The assumptions and rationales of a computer model of phytoplankton population dynamics. Limnology and Oceanography 20: 343–364.

    Article  Google Scholar 

  • Leopold, A., 1949, republished 1970. Odyssey. In A Sand County Almanac and Sketches Here and There. Oxford University Press, New York: 104–108.

  • Lewis, W. M. & W. A. Wurtsbaugh, 2008. Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. International Review of Hydrobiology 93: 446–465.

    Article  CAS  Google Scholar 

  • Liboriussen, L. & E. Jeppesen, 2003. Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshwater Biology 48: 418–431.

    Article  Google Scholar 

  • Loladze, I. & J. J. Elser, 2011. The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecology Letters 144: 244–250.

    Article  Google Scholar 

  • Lund, J. W. G., 1967. Eutrophication. Nature 214: 557–558.

    Article  PubMed  CAS  Google Scholar 

  • Maberly, S., L. King, M. M. Dent, R. I. Jones & C. E. Gibson, 2002. Nutrient limitation of phytoplankton and periphyton growth in upland lakes. Freshwater Biology 47: 2136–2152.

    Article  Google Scholar 

  • MAFF (Ministry of Agriculture, Fisheries and Food), 1999. Tackling Nitrate from Agriculture: Strategy from Science. MAFF Publications, London.

    Google Scholar 

  • Marcarelli, A. M. & W. A. Wurtsbaugh, 2009. Nitrogen fixation varies spatially and seasonally in linked stream-lake systems. Biogeochemistry 94: 95–110.

    Article  CAS  Google Scholar 

  • Marino, R., F. Chan, R. W. Howarth, M. Pace & G. E. Likens, 2002. Ecological and biogeochemical interactions constrain planktonic nitrogen fixation in estuaries. Ecosystems 5: 719–725.

    Article  CAS  Google Scholar 

  • Marino, R., F. Chan, R. W. Howarth, M. Pace & G. E. Likens, 2006. Ecological constraints on planktonic nitrogen fixation in saline estuaries. I. Nutrient and trophic controls. Marine Ecology Progress Series 309: 25–39.

    Article  CAS  Google Scholar 

  • McGowan, S., G. Britton, E. Haworth & B. Moss, 1999. Ancient blue-green blooms. Limnology and Oceanography 44: 436–439.

    Article  Google Scholar 

  • Mckee, D., D. Atkinson, S. E. Collings, J. W. Eaton, A. B. Gill, I. Harvey, K. Hatton, T. Heyes, D. Wilson & B. Moss, 2003. Response of freshwater microcosm communities to nutrients, fish, and elevated temperature during winter and summer. Limnology and Oceanography 48: 707–722.

    Article  Google Scholar 

  • Ministry of Food, Agriculture and Fisheries, Denmark, 2010. Danmarks salg af handelsgødning 2009/2010. The Plant directorate: 18 pp. ISBN 978-87-7083-999-0 (in Danish).

  • Mithen, S., 2010. The domestication of water: water management in the ancient world and its prehistoric origins in the Jordan Valley. Philosophical Proceedings of the Royal Society 368: 5249–5274.

    Google Scholar 

  • Moss, B., 1969. Limitation of algal growth in some central African waters. Limnology and Oceanography 14: 591–601.

    Article  Google Scholar 

  • Moss, B., 1990. Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components. Hydrobiologia 200(201): 367–377.

    Article  Google Scholar 

  • Moss, B., 2007. Water pollution by agriculture. Philosophical Transactions of the Royal Society, B. 363: 659–666.

    Article  CAS  Google Scholar 

  • Moss, B., S. Mcgowan & L. Carvalho, 1994. Determination of phytoplankton crops by top-down and bottom-up mechanisms in a group of English lakes, the West Midland meres. Limnology and Oceanography 39: 1020–1029.

    Article  CAS  Google Scholar 

  • Moss, B., J. Madgwick & G. Phillips, 1996. A Guide to the Restoration of Nutrient Enriched Shallow Lakes. Environment Agency, Broads Authority & European Union Life Programme, Norwich.

    Google Scholar 

  • Moss, B., D. Mckee, D. Atkinson, S. E. Collings, J. W. Eaton, A. B. Gill, I. Harvey, K. Hatton, T. Heyes & D. Wilson, 2003. How important is climate? Effects of warming, nutrient addition and fish on phytoplankton in shallow lake microcosms. Journal of Applied Ecology 40: 782–792.

    Article  Google Scholar 

  • Moss, B., T. Barker, D. Stephen, A. E. Williams, D. Balayla, M. Beklioglu & L. Carvalho, 2005. Consequences of reduced nutrient loading on a lake system in a lowland catchment: deviations from the norm? Freshwater Biology 50: 1687–1705.

    Article  CAS  Google Scholar 

  • Moss, B., S. Kosten, M. Meerhoff, R. W. Battarbee, E. Jeppesen, N. Mazzeo, K. Havens, G. Lacerot, Z. Liu, L. De Meester, H. Paerl & M. Scheffer, 2011. Allied attack: climate change and eutrophication. Inland Waters 1: 101–105.

    Google Scholar 

  • Naumann, E., 1931. Limnologische Terminologie. Handbuchen biologische Arbeitsmethoden 9(8): 1–776.

    Google Scholar 

  • Netten, J. C., G. H. P. Arts, R. Gylstra, E. van Nes, M. Scheffer & M. M. Roijackers, 2010. Effect of temperature and nutrients on the competition between free-floating Salvinia natans and submerged Elodea nuttallii in mesocosms. Fundamental and Applied Limnology 177: 125–132.

    Article  Google Scholar 

  • Newman, E. I., 1997. Phosphorus balance of contrasting farming systems, past and present. Can food production be sustainable? Journal of Applied Ecology 34: 1334–1347.

    Article  Google Scholar 

  • Oglesby, R. T. & W. T. Edmondson, 1966. Control of eutrophication. Journal of the Water Pollution Control Federation 38: 1452–1460.

    Google Scholar 

  • Özen, A., B. Karapınar, I. Kucuk, E. Jeppesen & M. Beklioglu, 2010. Drought-induced changes in nutrient retention and concentrations in Mediterranean shallow lakes, one biomanipulated and the other not. Hydrobiologia 646: 61–72.

    Article  CAS  Google Scholar 

  • Özkan, K., E. Jeppesen, L. S. Johansson & M. Beklioglu, 2010. The response of periphyton and submerged macrophytes to nitrogen and phosphorus loading in warm lakes: a mesocosm experiment. Freshwater Biology 54: 463–475.

    Article  CAS  Google Scholar 

  • Paerl, H., 2009. Controlling eutrophication along the freshwater–marine continuum: dual nutrient (N and P) reductions are essential. Estuaries and Coasts 32: 593–601.

    Article  CAS  Google Scholar 

  • Paerl, H. W., L. M. Valdes, A. R. Joyner & M. F. Piehler, 2004. Solving problems resulting from solutions: evolution of a dual nutrient management strategy for the eutrophying Neuse river estuary, North Carolina. Environmental Science and Technology 38: 3068–3073.

    Article  PubMed  CAS  Google Scholar 

  • Paterson, M. J., D. W. Schindler, R. E. Hecky, D. L. Findlay & K. J. Rondeau, 2011. Comment: Lake 227 shows clearly that controlling inputs of nitrogen will not reduce of prevent eutrophication of lakes. Limnology and Oceanography 56: 1545–1547.

    Article  CAS  Google Scholar 

  • Patoine, A., M. D. Graham & P. R. Leavitt, 2006. Spatial variation of nitrogen fixation in lakes of the northern great plains. Limnology and Oceanography 51: 1665–1677.

    Article  CAS  Google Scholar 

  • Phillips, G. L., D. F. Eminson & B. Moss, 1978. A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquatic Botany 4: 103–126.

    Article  Google Scholar 

  • Pinay, G., B. Gumeiro, E. Tabacchi, O. Giminez, A. M. Tabacchi-Planty, M. M. Hefting, T. P. Burt, V. A. Black, C. Nilsson, V. Lordache, F. Bureau, L. Vought, G. E. Petts & H. Decamps, 2007. Patterns of denitrification rates in European alluvial soils under various hydrological regimes. Freshwater Biology 52: 252–266.

    Article  CAS  Google Scholar 

  • Reay, D. S., F. Dentener, P. Smith, J. Grace & R. A. Feely, 2008. Global nitrogen deposition and carbon sinks. Nature Geoscience 1: 430–437.

    Article  CAS  Google Scholar 

  • Redfield, A. C., 1934. On the proportions of organic derivations in sea water and their relation to the composition of plankton. In Daniel, R. J. (ed.), James Johnstone Memorial Volume. University Press of Liverpool, Liverpool: 177–192.

    Google Scholar 

  • Redfield, A. C., 1958. The biological control of chemical factors in the environment. American Scientist 46: 205–221.

    CAS  Google Scholar 

  • Reynolds, C. S., 1979. The limnology of the eutrophic meres of the Shropshire-Cheshire plain – a review. Field Studies 5(1): 93–173.

    Google Scholar 

  • Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.

    Google Scholar 

  • Rhee, G.-Y. & I. J. Gotham, 1980. Optimum N:P ratios and coexistence of planktonic algae. Journal of Phycology 16: 486–489.

    Article  CAS  Google Scholar 

  • Round, F. E., 1961. The diatoms of a core from Esthwaite Water. New Phytologist 60: 43–59.

    Article  Google Scholar 

  • Ryther, J. H. & W. M. Dunstan, 1971. Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171: 1008–1013.

    Article  PubMed  CAS  Google Scholar 

  • Saunders, D. L. & J. Kalff, 2001. Nitrogen retention in wetlands, lakes and rivers. Hydrobiologia 443: 205–212.

    Article  CAS  Google Scholar 

  • Sawyer, C. N., 1966. Basic concepts of eutrophication. Journal of the Water Pollution Control Federation 38: 737–744.

    Google Scholar 

  • Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8: 275–279.

    Google Scholar 

  • Schindler, D. W., 1974. Eutrophication and recovery in experimental lakes: implications for lake management. Science 184: 897–898.

    Article  PubMed  CAS  Google Scholar 

  • Schindler, D. W., 1977. The evolution of phosphorus limitation in lakes. Science 195: 260–262.

    Article  PubMed  CAS  Google Scholar 

  • Schindler, D. W., 1978. Factors regulating phytoplankton production and standing crop in the world’s freshwaters. Limnology and Oceanography 23: 478–486.

    Article  Google Scholar 

  • Schindler, D. W. & E. J. Fee, 1974. Experimental lakes area – whole-lake experiments in eutrophication. Journal of the Fisheries Research Board of Canada 31: 937–953.

    Article  Google Scholar 

  • Schindler, D. W. & R. E. Hecky, 2009. Eutrophication: more nitrogen data needed. Science 324: 721–722.

    Article  PubMed  CAS  Google Scholar 

  • Schindler, D. W., H. Kling, R. V. Schmidt, J. Prokopow, V. E. Frost, R. A. Reid & M. Capel, 1973. Eutrophication of lake-227 by addition of phosphate and nitrate – second, third, and fourth years of enrichment, 1970, 1971, and 1972. Journal of the Fisheries Research Board of Canada 30: 1415–1440.

    Article  CAS  Google Scholar 

  • Schindler, D. W., R. E. Hecky, D. L. Findlay, M. P. Stainton, B. R. Parker, M. Paterson, K. G. Beaty, M. Lyng & S. E. M. Kasian, 2008. Eutrophication of lakes cannot be controlled by reducing N input: results of a 37-year whole-ecosystem experiment. Proceedings of the National Academy of Sciences, USA 105: 11254–11258.

    Article  CAS  Google Scholar 

  • Scott, J. T. & M. J. McCarthy, 2010. Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnology and Oceanography 55: 1265–1270.

    Article  CAS  Google Scholar 

  • Scott, J. T. & M. J. McCarthy, 2011. Response to comment: nitrogen fixation has not offset declines in the Lake 227 nitrogen pool and shows that nitrogen control deserves consideration in aquatic ecosystems. Limnology and Oceanography 56: 1548–1550.

    Article  CAS  Google Scholar 

  • Scott, J. T., D. A. Lang, R. S. King & R. D. Doyle, 2009. Nitrogen fixation and phosphatase activity in periphyton growing on nutrient diffusing substrata: evidence for differential nutrient limitation in stream periphyton. Journal of the North American Benthological Society 28: 57–68.

    Article  Google Scholar 

  • Seitzinger, S., J. A. Harrison, J. K. Bohlke, A. F. Bouwman, R. Lowrance, B. Peterson, C. Tobias & G. Van Drecht, 2006. Denitrification across landscapes and waterscapes: a synthesis. Ecological Applications 16: 2064–2090.

    Article  PubMed  CAS  Google Scholar 

  • Smith, V. H., 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221: 669–671.

    Article  PubMed  CAS  Google Scholar 

  • Smith, R. A., R. B. Alexander & G. E. Schwartz, 2003. Natural background concentrations of nutrients in streams and rivers of the conterminous United States. Environmental Science and Technology 37: 3039–3047.

    Article  PubMed  CAS  Google Scholar 

  • Sohm, J. A., E. A. Webb & D. G. Capone, 2011. Emerging patterns of marine nitrogen fixation. Nature Reviews Microbiology 9: 499–508.

    Article  PubMed  CAS  Google Scholar 

  • Søndergaard, M., J. P. Jensen & E. Jeppesen, 2003. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506(509): 135–145.

    Article  Google Scholar 

  • Søndergaard, M., J. P. Jensen & E. Jeppesen, 2005. Seasonal response of nutrients to reduced P loading in 12 Danish lakes. Freshwater Biology 50: 1605–1615.

    Article  CAS  Google Scholar 

  • Stal, L. J., I. Severin & H. Bolhuis, 2010. The ecology of nitrogen fixation in cyanobacterial mats. Recent advances in Phototrophic Prokaryotes 675: 31–45.

    Article  Google Scholar 

  • Steffen, W., P. J. Crutzen & J. R. McNeill, 2007. The Anthropocene: are humans now overwhelming the great forces of nature? Ambio 36: 614–621.

    Article  PubMed  CAS  Google Scholar 

  • Sterner, R. W., 2008. On the phosphorus limitation paradigm for lakes. International Review of Hydrobiology 93: 433–445.

    Article  CAS  Google Scholar 

  • Stevens, C., N. B. Dise, J. O. Mountford & D. J. Gowing, 2004. Impact of nitrogen deposition on the species richness of grasslands. Science 303: 1876–1879.

    Article  PubMed  CAS  Google Scholar 

  • Stewart, W. D. P., 1969. Biological and ecological aspects of nitrogen fixation by free-living micro-organisms. Proceedings of the Royal Society B 172: 367–388.

    Article  CAS  Google Scholar 

  • Strojsova, A., J. Nedoma, M. Strojsova, X. Y. Cao & J. Vrba, 2008. The role of cell-surface-bound phosphatases in species competition within natural phytoplankton assemblage: an in situ experiment. Journal of Limnology 67: 128–138.

    Article  Google Scholar 

  • Sutton, M. A., C. M. Howard, J. W. Erisman, G. Billen, A. Bleeker, P. Grennfelt, H. Van Grinsven & B. Grizzetti (eds), 2011. The European Nitrogen Assessment. Cambridge University Press, Cambridge.

    Google Scholar 

  • Talling, J. F. & J. Lemoalle, 1998. Ecological Dynamics of Tropical Inland Waters. Cambridge University Press, Cambridge.

    Google Scholar 

  • Ti, C., J. Pan, Y. Xia & X. Yan, 2011. A nitrogen budget of mainland China with spatial and temporal variation. Biogeochemistry. doi:10.1007/s10533-011-9606-y.

  • Tilman, D., 1977. Resource competition between planktonic algae: an experimental and theoretical approach. Ecology 58: 338–348.

    Article  CAS  Google Scholar 

  • Turner, R. E., N. N. Rabalais, D. Justic & Q. Dortch, 2003. Global patterns of dissolved N, P and Si in large rivers. Biogeochemistry 64: 297–317.

    Article  CAS  Google Scholar 

  • Ulen, B., M. Bechmann, J. Folster, H. P. Jarvie & H. Tunney, 2007. Agriculture as a phosphorus source for eutrophication in the north-west European countries, Norway, Sweden, United Kingdom and Ireland: a review. Soil Use and Management 23: 5–15.

    Article  Google Scholar 

  • Unrein, F., I. O’Farrell, I. Izaguirre, R. Sinistro, M. dos Santos Afonso & G. Tell, 2010. Phytoplankton response to pH rise in a N-limited floodplain lake: relevance of N2-fixing heterocystous cyanobacteria. Aquatic Sciences 72: 179–190.

    Article  CAS  Google Scholar 

  • Vadeboncoeur, Y., E. Jeppesen, J. Van der Zanden, H. Schierup, K. Christoffersen & D. M. Lodge, 2003. From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnology and Oceanography 48: 1408–1418.

    Article  Google Scholar 

  • Van Luijn, F., D. T. Van der Molen, W. J. Luttmer & P. C. M. Boers, 1995. Influence of benthic diatoms on the nutrient release from sediments of shallow lakes recovering from eutrophication. Water Science and Technology 32: 89–97.

    Article  Google Scholar 

  • Vanni, M., W. H. Renwick, A. M. Bowling, M. J. Horgan & A. D. Christian, 2001. Nutrient stoichiometry of linked catchment-lake systems along a gradient of land use. Freshwater Biology 56: 791–811.

    Article  CAS  Google Scholar 

  • Vitousek, P. M., J. R. Gosz, C. C. Grier, J. M. Melillo, W. A. Reiners & R. L. Todd, 1979a. Nitrate losses from disturbed ecosystems. Science 204: 469–474.

    Article  PubMed  CAS  Google Scholar 

  • Vitousek, P. M., J. R. Gosz, C. C. Grier, J. M. Melillo, W. A. Reiners & R. L. Todd, 1979b. Nitrate losses from disturbed ecosystems. Science 204: 469–474.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Vitousek, P. M., R. Naylor, T. Crews, M. B. David, L. E. Drinkwater, E. Holland, P. J. Jones, J. Katzenberger, L. A. Martinelli, P. A. Matson, G. Nziguheba, D. Ojima, C. A. Palm, G. P. Robertson, P. A. Sanchez, A. R. Townsend & F. S. Zhang, 2009. Nutrient imbalances in agricultural development. Science 324: 1519–1520.

    Article  PubMed  CAS  Google Scholar 

  • Vymazal, J., 2011. Constructed wetlands for wastewater treatment: five decades of experience. Environmental Science and Technology 45: 61–69.

    Article  PubMed  CAS  Google Scholar 

  • Wolfe, A. P., J. S. Baron & R. J. Cornett, 2001. Anthropogenic nitrogen deposition induces rapid ecological changes in alpine lakes of the Colorado Front Range (USA). Journal of Paleolimnology 25: 1–7.

    Article  Google Scholar 

  • Wolfe, A. P., S. S. Kaushal, J. R. Fulton & D. M. McKnight, 2002. Spectrofluorescence of sediment humic substances and historical changes of lacustrine organic matter provenance in response to atmospheric nutrient enrichment. Environmental Science and Technology 36: 3217–3223.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

EJ, MS and TLL were supported by the EU-WISER and EU-REFRESH projects, CLEAR (a Villum Kann Rasmussen Centre of Excellence Project), CRES and The Research Council for Nature and Universe (272-08-0406).

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Authors and Affiliations

  1. School of Environmental Sciences, University of Liverpool, Liverpool, UK

    Brian Moss

  2. Department of Bioscience, Aarhus University, Vejlsøvej 25, 8600, Silkeborg, Denmark

    Erik Jeppesen, Martin Søndergaard & Torben L. Lauridsen

  3. Sino-Danish Centre for Education and Research (SDC), Beijing, China

    Erik Jeppesen, Torben L. Lauridsen & Zhengwen Liu

  4. Greenland Climate Research Centre (GCRC), Greenland Institute of Natural Resources, Kivioq 2, P.O. Box 570, 3900, Nuuk, Greenland

    Erik Jeppesen

  5. Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences, Nanjing, 210008, China

    Zhengwen Liu

  6. Institute of Hydrobiology, Jinan University, Guangzhou, 510632, Guangdong, China

    Zhengwen Liu

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  1. Brian Moss
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  2. Erik Jeppesen
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Correspondence to Brian Moss.

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Guest editors: Zhengwen Liu, Bo-Ping Han & Ramesh D. Gulati / Conservation, management and restoration of shallow lake ecosystems facing multiple stressors

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Moss, B., Jeppesen, E., Søndergaard, M. et al. Nitrogen, macrophytes, shallow lakes and nutrient limitation: resolution of a current controversy?. Hydrobiologia 710, 3–21 (2013). https://doi.org/10.1007/s10750-012-1033-0

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