Water, Air, & Soil Pollution: Focus

, Volume 7, Issue 1–3, pp 99–109 | Cite as

Nitrogen Saturation of Terrestrial Ecosystems: Some Recent Findings and Their Implications for Our Conceptual Framework

  • Bridget A. EmmettEmail author


The consequences of nitrogen (N) enrichment for terrestrial and freshwater ecosystems are of increasing concern in many areas due to continued or increasing high emission rates of reactive N. Within terrestrial ecosystems various conceptual frameworks and modelling approaches have been developed which have enhanced our understanding of the sequence of changes associated with increased N availability and help us predict their future impacts. Here, some recent findings are described and their implications for these conceptual frameworks and modelling approaches discussed. They are: (a) an early loss of plant species that are characteristic of low N conditions as N availability increases and a loss of species with high N retention efficiencies (so called N ‘filters’), (b) suppression of microbial immobilisation of deposited \({\text{NO}}^{ - }_{3} \) due to increased \({\text{NH}}^{ + }_{4} \) availability in the early stages of N saturation, (c) the early onset of \({\text{NO}}^{ - }_{3} \) leaching due to these changes (a and b above) in both plant and microbial functioning, (d) reduced sensitivity of vegetation to N additions in areas with high historical N deposition, (e) delayed changes in soil C:N changes due to increased net primary productivity and reduced decomposition of soil organic matter. Some suggestions of early indicators of N saturation are suggested (occurrence of mosses; \({\text{NH}}^{ + }_{4} :{\text{NO}}^{ - }_{3} \) ratio in surface soils) which indicate either a shift in ecosystem function and/or structure.


diversity eutrophication nitrate leaching nitrogen saturation microbial immobilisation soil C:N ratio species composition 



The UK Department of the Environment, Food and Rural Affairs and the Natural Environment Research Council provided the funding for many of the UK studies reported here and the time for this synthesis. My thanks to the Acid Rain 2005 Organising Committee for giving me the opportunity to share these ideas and to the many colleagues and two referees for their helpful comments.


  1. Aber, J. D. (1992). Nitrogen cycling and nitrogen saturation in temperate forest ecosystems. Trends in Ecology & Evolution, 7, 220–224.CrossRefGoogle Scholar
  2. Aber, J. D., Goodale, C., Ollinger, S. V., Smith M., Magill, A., & Martin, M. E., et al. (2003). Is nitrogen deposition altering the nitrogen status of Northeastern forests? Bioscience, 53, 375–389.CrossRefGoogle Scholar
  3. Aber, J. D., McDowell, W., Nadelhoffer, K., Magill, A., Berntson, G., & Kamakea, M., et al. (1998). Nitrogen saturation in temperate forest ecosystems: Hypotheses revisited. Bioscience, 48, 921–934.CrossRefGoogle Scholar
  4. Aber, J. D., Nadelhoffer, K. J., Steudler, P., & Melillo, J. M. (1989). Nitrogen saturation in northern forest ecosystems. Bioscience, 39, 378–386.CrossRefGoogle Scholar
  5. Adams, M., Ineson, P., Binkley, D., Cadisch, G., Scholes, M., Hicks, K., & Tokuchi, N. (2004). Soil functional responses to excess nitrogen inputs at global scale. Ambio, 33, 530–536.Google Scholar
  6. Berg, B., & Meentemeyer, V. (2002). Litter quality in a north European transect versus carbon storage potential. Plant and Soil, 242, 83–92.CrossRefGoogle Scholar
  7. Betlach, M. R., Tiedje, J. M., & Firestone, R. B. (1981). Assimilatory nitrate uptake in Pseudomonas fluorescens studied using Nitrogen-13. Archives of Microbiology, 129, 135–140.CrossRefGoogle Scholar
  8. Bobbink, R., Hornung, M., & Roelofs, J. G. M. (1998). The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology, 86, 717–738.CrossRefGoogle Scholar
  9. Bradley, R. L. (2001). An alternative explanation for the post-disturbance \( NO^{ - }_{3} \) flush in some forest ecosystems. Ecology Letters, 4, 412–416.CrossRefGoogle Scholar
  10. Bredemeier, M., Blanck, K., Xu, Y. J., Tietema, A., Boxman, A. W., & Emmett, B. A., et al. (1998). Input–output budgets at the NITREX sites. Forest Ecology and Management, 101, 57–64.CrossRefGoogle Scholar
  11. Carreiro, M. M., Sinsabaugh, R. L., Repert, D. A., & Parkhursts, D. F. (2000). Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology, 81, 2359–2365.Google Scholar
  12. Carroll, J. A., Caporn, S. J. M., Cawley, L., Read, D. J., & Lee, J. A. (1999). The effect of increased deposition of atmospheric nitrogen on Calluna vulgaris in upland Britain. New Phytologist, 141, 423–431.CrossRefGoogle Scholar
  13. Carroll, J. A., Caporn, S. J. M., Johnson, D., Morecroft, M. D., & Lee, J. A. (2003). Interactions between plant growth, vegetation structure and soil processes in semi-natural acidic and calcareous grasslands receiving long-term inputs of simulated pollutant nitrogen deposition. Environmental Pollution, 121, 363–376.CrossRefGoogle Scholar
  14. Carroll, J. A., Johnson, D., Morecroft, M., Taylor, A., Caporn, S. J. M., & Lee, J. A. (2000). The effect of long-term nitrogen additions on the bryophyte cover of upland acidic grasslands. Journal of Bryology, 22, 83–89.Google Scholar
  15. Cooper, D. M. (2005). Evidence of sulphur and nitrogen deposition signals at the United Kingdom acid waters monitoring network sites. Environmental Pollution, 137, 41–54.CrossRefGoogle Scholar
  16. Curtis, C. J., Emmett, B. A., Grant, H., Kernan, M., Reynolds, B., & Shilland, E. (2005). Nitrogen saturation in UK moorlands: The critical role of bryophytes and lichens in determining retention of atmospheric N deposition. Journal of Applied Ecology, 42, 507–517.CrossRefGoogle Scholar
  17. Davidson, E. A., Hart, S. C., & Firestone, M. K. (1992). Internal cycling of nitrate in soils of a mature coniferous forest. Ecology, 73, 1148–1156.CrossRefGoogle Scholar
  18. Davidson, E. A., Hart, S. C., Shanks, C. A., & Firestone, M. K. (1991). Measuring gross nitrogen mineralization, immobilization and nitrification by 15N isotopic pool dilution in intact soil cores. Journal of Soil Science, 42, 335–349.CrossRefGoogle Scholar
  19. De Vries, W., Kros, H., Reinds, G. J., Wamelink, W., Van Dobbven, H., & Bobbink, R., et al. (2006). Development in modelling critical nitrogen loads for terrestrial ecosystems in Europe. Alterra, CCE report 2006. pp. 186 (in preparation).Google Scholar
  20. Dise, N., & Wright R. F. (1995). Nitrogen leaching in European forests in relation to nitrogen deposition. Forest Ecology and Management, 71, 153–162.CrossRefGoogle Scholar
  21. Ellenberg, H., Weber, H. E., Dull., R., Wirth, W., Werner, W., & Paulissen, D. (1991). Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobotanica, 18, 1–248.Google Scholar
  22. Emmett, B. A., Boxman, D., Bredemeier, M., Gundersen, P., Kjonaas, O. J., & Moldan, F., et al. (1998a). Predicting the effects of atmospheric nitrogen deposition in conifer stands: Evidence from the NITREX ecosystem-scale experiments. Ecosystems, 1, 352–360.CrossRefGoogle Scholar
  23. Emmett, B. A., Jones, M. L. M., Jones, H., Wildig, J., Williams, B., & Davey, M., et al. (2004). Grazing/nitrogen deposition interactions in upland acid moorland. Contract report to Countryside Council for Wales (Contract no. FV-73-03-89B) and the National Assembly for Wales (Contract No. 182-2002). pp. 96.Google Scholar
  24. Emmett, B. A., Reynolds, B., Silgram, M., Sparks, T. H., & Woods, C. (1998b). The consequences of chronic nitrogen additions on N cycling and soilwater chemistry in a N saturated Sitka spruce stand, North Wales. Forest Ecology and Management, 101, 165–175.CrossRefGoogle Scholar
  25. Emmett, B. A., Reynnolds, B., Stevens, P. A., Norris, D. A., Hughes, H., & Gőrres, J., et al. (1993). Nitrate leaching from afforested Welsh catchments – Interactions between stand age and nitrogen deposition. Ambio, 22, 386–394.Google Scholar
  26. Ertsen, A. C. D., Alkemade, J. R. M., & Wassen, M. J. (1998). Calibrating Ellenberg indicator values for moisture, acidity, nutrient availability and salinity in the Netherlands. Plant Ecology, 135, 113–124.CrossRefGoogle Scholar
  27. Evans, C. D., Reynolds, B., Jenkins, A., Helliwell, R., Curtis, C. J., & Goodale, C. L., et al. (2006). Evidence that soil carbon pool determines susceptibility of semi-natural ecosystems to elevated nitrogen leaching. Ecosystems, 9, 453–462.CrossRefGoogle Scholar
  28. Fenn, M. E., Baron, J. S., Allen, E. B., Rueth, H. M., Nydick, K. R., & Geiser, L., et al. (2003). Ecological effects of nitrogen deposition in the Western United States. Bioscience, 53, 404–420.CrossRefGoogle Scholar
  29. Fenn, M. E., Poth, M. A., Aber, J. D., Baron, J. S., Bormann, B. T., & Johnson, D. W., et al. (1998). Nitrogen excess in North American ecosystems: Predisposing factors, ecosystems responses and management strategies. Ecological Applications, 8, 706–733.Google Scholar
  30. Galloway, J. N., Aber, J. D., Erisman, J. W., Seitzinger, S. P., Howarth, R. W., & Cowling, E. B., et al. (2003). The nitrogen cascade. Bioscience, 53, 341–356.CrossRefGoogle Scholar
  31. Gessler, A., Kopriva, S., & Rennenberg, H. (2004). Regulation of nitrate uptake at the whole-tree level: Interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiology, 24, 1313–1321.Google Scholar
  32. Gilliam, F. S., Adams, M. B., & Yurish, B. M. (1996). Ecosystem nutrient responses to chronic nitrogen inputs at Fernow Experimental Forest, West Virginia. Canadian Journal of Forest Research, 26, 196–205.CrossRefGoogle Scholar
  33. Goodale, C. L., Aber, J. D., & Vitousek, P. M. (2003). An unexpected nitrate decline in New Hampshire streams. Ecosystems, 6, 75–86.CrossRefGoogle Scholar
  34. Goulding, K. W. T., Bailey, N. J., Bradbury, N. J., Hargreaves, P., Howe, M., & Murphy, D. V., et al. (1998). Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytologist, 139, 49–58.CrossRefGoogle Scholar
  35. Gundersen, P., Callensen, I., & de Vries, W. (1998a). Nitrogen leaching in forest ecosystems is related to forest floor C/N ratios. Environmental Pollution, 102, 403–407.CrossRefGoogle Scholar
  36. Gundersen, P., Emmett, B. A., Kjonaas, O. J., Koopmans, C. J., & Tietema, A. (1998b). Impact of nitrogen deposition on nitrogen cycling in forests: A synthesis of NITREX data. Forest Ecology and Management, 101, 37–56.CrossRefGoogle Scholar
  37. Haddad, N. M., Haarstad, J., & Tilman, D. (2000). The effects of long-term nitrogen loading on grassland insect communities. Oecologia, 124, 73–84.CrossRefGoogle Scholar
  38. Hagedorn, F., Spinnler, D., & Siegwolf, R. (2003). Increased N deposition retards mineralization of old soil organic matter. Soil Biology and Biochemistry, 35, 1683–1692.Google Scholar
  39. Haines-Young, R., Barr, C. J., Firbank, L. G., Furse, M., Howard, D. C., & McGowan, G., et al. (2003). Changing landscapes, habitats and vegetation diversity across Great Britain. Journal of Environmental Management, 67, 267–281.CrossRefGoogle Scholar
  40. Hart, S. C., Nason, G. E., Myrold, D. D., & Perry, D. A. (1994). Dynamics of gross nitrogen transformations in an old-growth forest: The carbon connection. Ecology, 75, 880–891.CrossRefGoogle Scholar
  41. Hill, M. O., Mountford, J. O., Roy, D. B., & Bunce, R. G. H. (1999). Ellenberg’s indicator values for British plants. ECOFACT Volume II, Technical Annex. Huntingdon, UK: ITE Monkswood.Google Scholar
  42. Hughes, S., Grant, H., Ostle, N., Emmett, B. A., & UKREATE. (2004). The controls on immobilisation of ammonium and nitrate and the link to the onset of N saturation. In B. A. Emmett & G. McShane (Eds.), Terrestrial Umbrella Final Report May 2004 (pp. 321–329). NERC-DEFRA Terrestrial Umbrella Contract Number EPG 1/3/186.Google Scholar
  43. Jones, M. L. M. (2005). Nitrogen deposition in upland grasslands: Critical loads, management and recovery. PhD Thesis, University of Sheffield, UK.Google Scholar
  44. Kahl, J. S., Norton, S. A., Fernandez, I. J., Nadelhoffer, K. J., Driscoll, C. T. Y., & Aber, J. D. (1993). Experimental inducement of nitrogen saturation at the watershed scale. Environmental Science & Technology, 27, 565–568.CrossRefGoogle Scholar
  45. Lamers, L. P. M., Bobbink, R., & Roelofs, J. G. M. (2000). Natural nitrogen filter fails in polluted raised bogs. Global Change Biology, 6, 583–586.Google Scholar
  46. Lovett, G. M., Weathers, K. C., & Arthur, M. A. (2002). Control of nitrogen loss from forests by soil carbon: Nitrogen ratio and tree species composition. Ecosystems, 5, 712–718.CrossRefGoogle Scholar
  47. Macdonald, J. A., Dise, N. B., Matzner, E., Armbruster, M., Gundersen, P., & Forsius, M. (2002). Nitrogen inputs together with nitrogen enrichment predict nitrate leaching in European forests. Global Change Biology, 8, 1028–1033.CrossRefGoogle Scholar
  48. Magill, A. H., Aber, J. D., Hendricks, J. J., Bowden, R. D., Melillo, J. M., & Steudler, P. (1997). Biogeochemical response of forest ecosystems to simluated chronic nitrogen deposition. Ecological Applications, 7, 402–415.Google Scholar
  49. Matzner, E., & Grosholz, C. (1998). Beziehung zwischen \( NO^{ - }_{3} \) Austrägen, C/N-Verhältnissen ser Auflage und N-Einträgen in Fichtenwald (Picea abies Karst)-Ökosystemen Mitteleuropus. Forstwissenschaftliches Centralblatt, 116, 39–44.Google Scholar
  50. McNulty, S. G., & Aber, J. D. (1993). Effects of chronic nitrogen additions on nitrogen cycling in a high-elevation spruce-fir stand across New England. Biogeochemistry, 14, 13–29.Google Scholar
  51. McNulty, S., & Aber, J. D. (1996). Nitrogen saturation in a high elevation New England spruce-fir stand. Forest Ecology and Management, 84, 109–121.CrossRefGoogle Scholar
  52. Moldan, F., Kjønaas, O. J., Stuanes, A. O., & Wright, R. F. (2006). Increased nitrogen in runoff and soil following thirteen years of experimentally increased nitrogen deposition to a coniferous-forested catchment at Gårdsjön, Sweden. Environmental Pollution 144(2):610–620.CrossRefGoogle Scholar
  53. Nadelhoffer, K., Downs, M., Fry, B., Magill, A., & Aber, J. (1999a). Controls on N retention and exports in a forested watershed. Environmental Monitoring and Assessment, 55, 187–210.CrossRefGoogle Scholar
  54. Nadelhoffer, K. J., Emmett, B. A., Gundersen, P., Kjønaas, O. J., Koopmans, C. J., & Schleppi, P., et al. (1999b). Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature, 398, 145–148.CrossRefGoogle Scholar
  55. Nihlgård, B. (1985). The ammonium hypothesis: An additional explanation to the forest dieback in Europe. Ambio, 14, 2–8.Google Scholar
  56. Nilsson, J., & Grennfelt, P. (Eds.) (1988). Critical Loads for Sulphur and Nitrogen. Report of the Skokloster Workshop. Miljörapport 15. Nordic Council of Ministers, Copenhagen.Google Scholar
  57. Pardo, L. H., Kendall, C., Pett-Ridge, J., & Chang, C. C. Y. (2004). Evaluating the source of streamwater nitrate using delta N-15 and delta O-18 in nitrate in two watersheds in New Hampshire, USA. Hydrological Procedure, 18, 2699–2712.CrossRefGoogle Scholar
  58. Pennings, S. C., Clark, C. M., Cleland, E. E., Collins, S. L., Gough, L., & Gross, K. L., et al. (2005). Do individual plant species show predictable responses to nitrogen addition across multiple experiments. Oikos, 110, 547–555.CrossRefGoogle Scholar
  59. Persson, J., & Näsholm, T. (2002). Regulation of amino acid uptake in conifers by exogenous and endogenous nitrogen. Planta, 215, 639–644.CrossRefGoogle Scholar
  60. Power, S. A., Ashmore, M. R., & Cousins, D. A. (1998). Impacts and fate of experimentally enhanced nitrogen deposition on a British lowland heath. Environmental Pollution, 102(Suppl. 1), 27–34.CrossRefGoogle Scholar
  61. Press, M. C., Woodin, S. J., & Lee, J. A. (1986). The potential importance of increased nitrogen supply to the growth of the ombrotrophic Sphagnum species. New Phytologist, 138, 45–55.CrossRefGoogle Scholar
  62. Preston, C. D., Pearman, D. A., & Dines, T. D. (2002). New Plant Atlas of the British and Irish Flora (p. 42). New York: Oxford University Press.Google Scholar
  63. Providoli, I., Bugmann, H., Siegwolf, R., Buchmann, N., & Schlepp, P. (2005). Flow of deposited inorganic N in two Gleysol-dominated mountain catchments traced with \( {}^{{15}}NO^{ - }_{3} \) and \( {}^{{15}}NH^{ + }_{4} \). Biogeochemistry, 76, 453–475.CrossRefGoogle Scholar
  64. Rice, C. W., & Tiedje, J. M. (1989). Regulation of nitrate assimilation by ammonium in soils and in isolated soil microorganisms. Soil Biology & Biochemistry, 21, 597–602.CrossRefGoogle Scholar
  65. Schimel, J. P., & Bennett, J. (2004). Nitrogen mineralization: Challenges of changing paradigm. Ecology, 85, 591–602.CrossRefGoogle Scholar
  66. Smart, S. M., Bunce, R. G. H., Marrs, R. H., LeDuc, M., Firbank, L. G., & Maskell, L. C., et al. (2005). Large-scale changes in the abundance of common plant species across Britain between 1978, 1990 and 1998 as a consequence of human activity: Tests of hypothesised changes in trait representation. Biological Conservation, 124, 355–371.CrossRefGoogle Scholar
  67. Smart, S. M., Robertson, J. C., Shielf, E. J., & van de Poll, H. M. (2003). Locating eutrophication effects across Britain vegetation between 1990 and 1998. Global Change Biology, 9, 1763–1774.CrossRefGoogle Scholar
  68. Stark, J. M., & Hart, S. C. (1997). High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature, 385, 61–64.CrossRefGoogle Scholar
  69. Stevens, C. J., Dise, N. B., Mountford, J. O., & Gowing, D. J. (2004). Impact of nitrogen deposition on the species richness of grasslands. Science, 303, 1876–1879.CrossRefGoogle Scholar
  70. Stoddard, J. L. (1994). Long-term changes in watershed retention of nitrogen: Its causes and aquatic consequences. In L. A. Baker (Ed.), Environmental chemistry of lakes and reservoirs (pp. 223–284). Wahsington, DC: American Chemical Society.Google Scholar
  71. Stoddard, J. L., Jeffries, D. S., Lükewille, A., Clair, T. A., Dillon, P. J., & Driscoll, C. T., et al. (1999). Regional trends in aquatic recovery from acidification in North America and Europe. Nature, 401, 575–578.CrossRefGoogle Scholar
  72. Suding, K. N., Collins, S. L., Gough, L., Clark, C., Cleland, E. E., & Gross, K. L., et al. (2005). Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proceedings of the National Academy of Sciences of the United States of America, 102, 4387–4392.CrossRefGoogle Scholar
  73. Tietema, A. (1998). Microbial carbon and nitrogen dynamics in coniferous forest floor material collected along a European nitrogen deposition gradient. Forest Ecology and Management, 101, 29–36.CrossRefGoogle Scholar
  74. Tietema, A., Emmett, B. A., Gundersen, P., Kjønaas, O. J., & Koopmans, C. J. (1998). The fate of 15N-labelled nitrogen deposition in coniferous forest ecosystems. Forest Ecology and Management, 101, 19–27.CrossRefGoogle Scholar
  75. Van’t Riet, J., Stouthamer, A. H., & Planta, R. J. (1968). Regulation of nitrate assimilation and nitrate respiration in Aerobacter aerogenes. Journal of Bacteriology, 96, 1455–1464.Google Scholar
  76. Vitousek, P. M., Howarth, R. W., Likens, G. E., Matson, P. A., Schindler, D., & Schlesinger, W. H., et al. (1997). Human alteration of the global nitrogen cycle: Causes and consequence. Issues in Ecology, 1, 1–17.Google Scholar
  77. Waldrop, P., Zak, D. R., Sinsabaugh, R. L., Gallo, M., & Lauber, C. (2004). Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecological Applications, 14, 1172–1177.CrossRefGoogle Scholar
  78. Williard, K. W. J., DeWalle, D. R., Edwards, P. J., & Schnabel, R. R. (1997). Indicators of nitrate export from forested watersheds of the mid-Appalachians, United States of America. Global Biogeochemical Cycles, 11, 649–656.CrossRefGoogle Scholar
  79. Zak, D. R., Pregitzer, K. S., Holmes, W. E., Burton, A. J., & Zogg, G. P. (2004). Anthropogenic N deposition and the fate of (NO3-)-15N in a northern hardwood ecosystem. Biogeochemistry, 69, 143–157.Google Scholar
  80. Zogg, G. P., Zak, D. R., Pregitzer, K. S., & Burton, A. J. (2000). Microbial immobilization and the retention of anthropogenic nitrate in a northern hardwood. Ecology, 81, 1858–1866.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Centre for Ecology and HydrologyBangorUK

Personalised recommendations