, Volume 14, Issue 6, pp 1021–1037 | Cite as

What Have Stable Isotope Studies Revealed About the Nature and Mechanisms of N Saturation and Nitrate Leaching from Semi-Natural Catchments?

  • Chris J. CurtisEmail author
  • Chris D. Evans
  • Christine L. Goodale
  • Tim H.E. Heaton


Various studies over the last 15 years have attempted to describe the processes of N retention, saturation and NO3 leaching in semi-natural ecosystems based on stable isotope studies. Forest ecologists and terrestrial biogeochemists have used 15N labelled NO3 and NH4 + tracers to determine the fate of atmospheric deposition inputs of N to terrestrial ecosystems, with NO3 leaching to surface waters being a key output flux. Separate studies by aquatic ecologists have used similar isotope tracer methods to determine the fate and impacts of inorganic N species, leached from terrestrial ecosystems, on aquatic ecosystems, usually without reference to comparable terrestrial studies. A third group of isotopic studies has employed natural abundances of 15N and 18O in precipitation and surface water NO3 to determine the relative contributions of atmospheric and microbial sources. These three sets of results often appear to conflict with one another. Here we attempt to synthesize and reconcile the results of these differing approaches to identifying both the source and the fate of inorganic N in natural or semi-natural ecosystems, and identify future research priorities. We conclude that the results of different studies conform to a consistent conceptual model comprising: (1) rapid microbial turnover of atmospherically deposited NO3 at multiple biologically active locations within both terrestrial and aquatic ecosystems; (2) maximum retention and accumulation of N in carbon-rich ecosystems and (3) maximum leaching of NO3 , most of which has been microbially cycled, from carbon-poor ecosystems exposed to elevated atmospheric N inputs.


Nitrate 1518dual isotopes nitrogen saturation deposition catchment 



This study was part funded by the UK Department for Environment, Transport and Rural Affairs (Defra) Contract CPEA17 (CJC, CE and TH). CLG’s contribution was supported by the US National Science Foundation (NSF-CAREER DEB0845451).


  1. Aber JD. 1992. Nitrogen cycling and nitrogen saturation in temperate forest ecosystems. TREE 7:220–4.PubMedGoogle Scholar
  2. Aber JD, Nadelhoffer KD, Steudler P, Melillo JM. 1989. Nitrogen saturation in Northern forest ecosystems. Bioscience 39:378–86.CrossRefGoogle Scholar
  3. Aber JD, Goodale CL, Ollinger SV, Smith M-L, Magill AH, Martin ME, Hallett RA, Stoddard JL. 2003. Is nitrogen deposition altering the nitrogen status of northeastern forests? Bioscience 53:375–89.CrossRefGoogle Scholar
  4. Adams MB, Kochendorfer JN, Edwards PJ. 2007. The Fernow Watershed Acidification Study: ecosystem acidification, nitrogen saturation and base cation leaching. Water Air Soil Pollut Focus 7:267–73.CrossRefGoogle Scholar
  5. Ashkenas LR, Johnson SL, Gregory SV, Tank JL, Wollheim WM. 2004. A stable isotope tracer study of nitrogen uptake and transformation in an old growth forest stream. Ecology 85:1725–39.CrossRefGoogle Scholar
  6. Barnes RT, Raymond PA, Casciotti KL. 2008. Dual isotope analyses indicate efficient processing of atmospheric nitrate by forested watersheds in the northeastern U.S. Biogeochemistry 90:15–27.CrossRefGoogle Scholar
  7. Battin TJ, Kaplan LA, Findlay S, Hopkinson CS, Martí E, Packman AI, Newbold JD, Sabater F. 2008. Biophysical controls on organic carbon fluxes in fluvial networks. Nat Geosci 1:95–100.CrossRefGoogle Scholar
  8. Bernot MJ, Dodds WK. 2005. Nitrogen retention, removal and saturation in lotic ecosystems. Ecosystems 8:442–53.CrossRefGoogle Scholar
  9. Berntson GM, Aber JD. 2000. Fast nitrate immobilization in N saturated temperate forest soils. Soil Biol Biochem 32:151–6.CrossRefGoogle Scholar
  10. Bradley RL. 2001. An alternative explanation for the post-disturbance NO3 flush in some forest ecosystems. Ecol Lett 4:412–16.CrossRefGoogle Scholar
  11. Brandes JA, McClain ME, Pimental TP. 1996. 15N evidence for the origin and cycling of inorganic nitrogen in a small Amazonian catchment. Biogeochemistry 34:45–56.CrossRefGoogle Scholar
  12. Bredemeier M, Blanck K, Xu Y-J, Tietema A, Boxman AW, Emmett B, Moldan F, Gundersen P, Schleppi P, Wright RF. 1998. Input-output budgets at the NITREX sites. For Ecol Manag 101:57–64.CrossRefGoogle Scholar
  13. Brookshire ENJ, Valett HM, Gerber S. 2009. Maintenance of terrestrial nutrient loss signatures during in-stream transport. Ecology 90:293–9.PubMedCrossRefGoogle Scholar
  14. Burgin AJ, Hamilton SK. 2007. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96.CrossRefGoogle Scholar
  15. Burgin AJ, Hamilton SK. 2008. NO3 driven SO4 2− production in freshwater ecosystems: Implications for N and S cycling. Ecosystems 11:908–22.CrossRefGoogle Scholar
  16. Burns DA. 1998. Retention of NO3 in an upland stream environment: a mass balance approach. Biogeochemistry 40:73–96.CrossRefGoogle Scholar
  17. Burns DA, Kendall C. 2002. Analysis of δ15N and δ18O to differentiate NO3 sources in runoff at two watersheds in the Catskill Mountains of New York. Water Resour Res 38. doi:  10.1029/2001WR000292.
  18. Burns DA, Boyer EW, Elliott EM, Kendall C. 2009. Sources and transformations of nitrate from streams draining varying land uses: evidence from dual isotope analysis. J Environ Qual 38:1149–59.PubMedCrossRefGoogle Scholar
  19. Campbell DH, Kendall C, Chang CCY, Silva SR, Tonnessen KA. 2002. Pathways for nitrate release from an alpine watershed: determination using δ15N and δ18O. Water Resour Res 38. doi:  10.1029/2001WR000294.
  20. Campbell JL et al. 2004. Input-output budgets of inorganic nitrogen for 24 forest watersheds in the northeastern United States: a review. Water Air Soil Pollut 151:373–96.CrossRefGoogle Scholar
  21. Campbell JL, Mitchell MJ, Mayer B. 2006. Isotopic assessment of NO3 and SO4 2− mobility during winter in two adjacent watersheds in the Adirondack Mountains, New York. J Geophys Res 111:G04007. doi: 10.1029/2006JG000208,2006.CrossRefGoogle Scholar
  22. Curtis CJ, Allott TEH, Reynolds B, Harriman R. 1998. The prediction of nitrate leaching with the first-order acidity balance (FAB) model for upland catchments in Great Britain. Water Air Soil Pollut 105:205–15.CrossRefGoogle Scholar
  23. Curtis CJ, Emmett BA, 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. J Appl Ecol 42:507–17.CrossRefGoogle Scholar
  24. Curtis C, Simpson G, Eds. 2007. Freshwater umbrella—the effects of nitrogen deposition and climate change on freshwaters in the UK. Report to DEFRA under Contract CPEA17, July 2007. ECRC Research Report No. 115, Environmental Change Research Centre, University College London, London.Google Scholar
  25. Dail DB, Davidson EA, Chorover J. 2001. Rapid abiotic transformation of nitrate in an acid forest soil. Biogeochemistry 54:131–46.CrossRefGoogle Scholar
  26. Darling WG, Bath AH, Talbot JC. 2003. The O & H stable isotopic composition of fresh waters in the British Isles. 2. Surface waters and groundwater. Hydrol Earth Syst Sci 7:183–95.CrossRefGoogle Scholar
  27. Davidson EA, Janssens IA. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–73.PubMedCrossRefGoogle Scholar
  28. Davidson EA, Stark JM, Firestone MK. 1990. Microbial production and consumption of nitrate in an annual grassland. Ecology 71:1968–75.CrossRefGoogle Scholar
  29. Davidson EA, Hart SC, Firestone MK. 1992. Internal cycling of nitrate in soils of a mature coniferous forest. Ecology 73:1148–56.CrossRefGoogle Scholar
  30. Dise NB, Wright RF. 1995. Nitrogen leaching from European forests in relation to nitrogen deposition. For Ecol Manage 71:153–62.CrossRefGoogle Scholar
  31. Dise NB, Matzner E, Gundersen P. 1998. Synthesis of nitrogen pools and fluxes from European forest ecosystems. Water Air Soil Pollut 105:143–54.CrossRefGoogle Scholar
  32. Durka W, Schulze E-D, Gebauer G, Voerkellus S. 1994. Effects of forest decline on uptake and leaching of deposited nitrate determined from 15N and 18O measurements. Nature 372:765–7.CrossRefGoogle Scholar
  33. Earl SR, Valett HM, Webster JR. 2006. Nitrogen saturation in stream ecosystems. Ecology 87:3140–51.PubMedCrossRefGoogle Scholar
  34. Earl SR, Valett HM, Webster JR. 2007. Nitrogen spiralling in streams: comparisons between stable isotope tracer and nutrient addition experiments. Limnol Oceanogr 52:1718–23.CrossRefGoogle Scholar
  35. Emmett BA. 2007. Nitrogen saturation of terrestrial ecosystems: some recent findings and their implications for our conceptual framework. Water Air Soil Pollut Focus 7:99–109.CrossRefGoogle Scholar
  36. Emmett BA, Reynolds B, Silgram M, Sparks TH, Woods C. 1998a. The consequences of chronic nitrogen additions on N cycling and soilwater chemistry in a Sitka spruce stand, North Wales. For Ecol Manage 101:165–75.CrossRefGoogle Scholar
  37. Emmett BA, Boxman D, Bredemeier M, Gundersen P, Kjønaas OJ, Moldan P, Schleppi P, Tietema A, Wright RF. 1998b. Predicting the effects of atmospheric nitrogen deposition in conifer stands: evidence from the NITREX ecosystem-scale experiments. Ecosystems 1:352–60.CrossRefGoogle Scholar
  38. Evans CD, Reynolds B, Jenkins A, Helliwell RC, Curtis CJ, Goodale CL, Ferrier RC, Emmett BA, Pilkington MG, Caporn SJM, Carroll JA, Norris D, Davies J, Coull MC. 2006. Evidence that soil carbon pool determines susceptibility of semi-natural ecosystems to elevated nitrogen leaching. Ecosystems 9:453–62.CrossRefGoogle Scholar
  39. Evans CD, Norris D, Ostle N, Grant H, Rowe EC, Curtis CJ. 2008. Rapid immobilisation of wet-deposited nitrate in upland organic soils. Environ Pollut 156:636–43.PubMedCrossRefGoogle Scholar
  40. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ. 2003. The nitrogen cascade. Bioscience 53:341–56.CrossRefGoogle Scholar
  41. Goodale CL, Aber JD, Vitousek PM, McDowell WH. 2005. Long-term decreases in stream nitrate: successional causes unlikely; possible links to DOC? Ecosystems 8:334–7.CrossRefGoogle Scholar
  42. Goodale CL, Thomas SA, Fredriksen G, Elliott EM, Flinn KM, Butler TJ, Walter MT. 2009. Unusual seasonal patterns and inferred processes of nitrogen retention in forested headwaters of the Upper Sasquehanna River. Biogeochemistry 93:197–218.CrossRefGoogle Scholar
  43. Granger SJ, Heaton THE, Bol R, Bilotta GS, Butler P, Haygarth PM, Owens PN. 2008. Using δ15N and δ18O to evaluate the sources and pathways of NO3 in rainfall event discharge from drained agricultural grassland lysimeters at high temporal resolutions. Rapid Commun Mass Spectrom 22:1681–9.PubMedCrossRefGoogle Scholar
  44. Gruber N, Galloway JN. 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451:293–6.PubMedCrossRefGoogle Scholar
  45. Gundersen P. 1998. Effects of enhanced nitrogen deposition in a spruce forest at Klosterhede, Denmark, examined by moderate NH4NO3 addition. For Ecol Manage 101:251–68.CrossRefGoogle Scholar
  46. Gundersen P, Callesen I, de Vries W. 1998a. Nitrate leaching in forest ecosystems is controlled by forest floor C/N ratio. Environ Pollut 102:403–7.CrossRefGoogle Scholar
  47. Gundersen P, Emmett BA, Kjønaas OJ, Koopmans CJ, Tietema A. 1998b. Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. For Ecol Manage 101:37–55.CrossRefGoogle Scholar
  48. Hagedorn F, Mohn J, Schleppi P, Flühler H. 1999. The role of rapid flow paths for nitrogen transformations in a forest soil: a field study with micro suction cups. Soil Sci Soc Am J 63:1915–23.CrossRefGoogle Scholar
  49. Hales HC, Ross DS, Lini A. 2007. Isotopic signature of nitrate in two contrasting watersheds at Brush Brook, Vermont, USA. Biogeochemistry 84:51–66.CrossRefGoogle Scholar
  50. Hamilton SK, Tank JL, Raikow DF, Wollheim WM, Peterson BJ, Webster JR. 2001. Nitrogen uptake and transformation in a Midwestern U.S. stream: a stable isotope enrichment study. Biogeochemistry 54:297–340.CrossRefGoogle Scholar
  51. Heaton THE. 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chem Geol 59:87–102.CrossRefGoogle Scholar
  52. Helliwell RC, Coull MC, Davies JJL, Evans CD, Norris D, Ferrier RC, Jenkins A, Reynolds B. 2007. The role of catchment characteristics in determining surface water nitrogen in four upland regions in the UK. Hydrol Earth Syst Sci 11:356–71.CrossRefGoogle Scholar
  53. Hessen DO, Henriksen A, Smelhus AM. 1997. Seasonal fluctuations and diurnal oscillations in nitrate of a heathland brook. Water Res 31:1813–17.CrossRefGoogle Scholar
  54. Hodson A, Heaton T, Langford H, Newsham K. 2010. Chemical weathering and solute export by meltwater in a maritime Antarctic glacier basin. Biogeochem 98:9–27.CrossRefGoogle Scholar
  55. Houlton BZ, Bai E. 2009. Imprint of denitrifying bacteria on the global terrestrial biosphere. PNAS 106:21713–16.PubMedCrossRefGoogle Scholar
  56. Kämäri J, Jeffries DS, Hessen DO, Henriksen A, Posch M, Forsius M. 1992. In: Grennfelt P, Thörnelöf E, Eds. Nitrogen critical loads and their exceedance for surface waters. Report from a workshop held at Lökeborg, Sweden, 6–10 April 1992, Nord 1992:41. Copenhagen: Nordic Council of Ministers. pp 161–200.Google Scholar
  57. Kendall C. 1998. Tracing nitrogen sources and cycling. In: Kendall C, McDonnell JJ, Eds. Isotope tracers in catchment hydrology. New York: Elsevier. p 519.Google Scholar
  58. Kendall C, Elliott EM, Wankel SD. 2007. Tracing anthropogenic inputs of nitrogen to ecosystems. In: Michener R, Lajtha K, Eds. Stable isotopes in ecology and environmental science. Boston: Blackwell Publishing. p 375–449.CrossRefGoogle Scholar
  59. Kernan M, Battarbee RW, Curtis CJ, Monteith DT, Shilland EM, editors. 2010. UK Acid Waters Monitoring Network 20 Year Interpretive Report. ECRC Research Report #141, University College London. London, UK. 477 pp.Google Scholar
  60. Kjønaas OJ, Wright RF. 2007. Use of 15N-labelled nitrogen deposition to quantify the source of nitrogen in runoff at a coniferous-forested catchment at Gårdsjön, Sweden. Environ Pollut 147:791–9.PubMedCrossRefGoogle Scholar
  61. Kopácek J, Stuchlík E, Wright RF. 2005. Long-term trends and spatial variability in nitrate leaching from alpine catchment-lake ecosystems in the Tatra Mountains (Slovakia-Poland). Environ Pollut 136:89–101.PubMedCrossRefGoogle Scholar
  62. Kortelainen P, Saukkonen S, Mattsson T. 1997. Leaching of nitrogen from forested catchments in Finland. Global Biogeochem Cycles 11:627–38.CrossRefGoogle Scholar
  63. Kroopnick PM, Craig H. 1972. Atmospheric oxygen: isotopic composition and solubility fractionation. Science 175:54–5.PubMedCrossRefGoogle Scholar
  64. Lewis WM Jr, Melack JM, McDowell WH, McClain M, Richey JE. 1999. Nitrogen yields from undisturbed watersheds in the Americas. Biogeochemistry 46:149–62.CrossRefGoogle Scholar
  65. MacDonald JA, Dise NB, Matzner E, Armbruster M, Gundersen P, Forsius M. 2002. Nitrogen input together with ecosystem nitrogen enrichment predict nitrate leaching from European forests. Glob Change Biol 8:1028–33.CrossRefGoogle Scholar
  66. Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. For Ecol Manage 196:7–28.CrossRefGoogle Scholar
  67. Michalski G, Meixner T, Fenn M, Hernandez L, Sirulnik A, Allen E, Thiemens M. 2004. Tracing atmospheric nitrate deposition in a complex semiarid ecosystem using δ17O. Environ Sci Technol 38:2175–81.PubMedCrossRefGoogle Scholar
  68. Moldan F, Wright RF. 2011. Nitrogen leaching and acidification during 19 years of NH4NO3 additions to a coniferous-forested catchment at Gårdsjön, Sweden (NITREX). Environ Pollut 159:431–40.PubMedCrossRefGoogle Scholar
  69. Monteith DT, Shilland EM, Eds. 2007. United Kingdom acid waters monitoring network: assessment of the first 18 years of data. Report to the Department for Environment, Food and Rural Affairs (Contract EPG 1/3/160). London: Ensis Ltd., University College London.Google Scholar
  70. Mulholland PJ, Thomas SA, Valett HM, Webster JR, Beaulieu J. 2006. Effects of light on NO3 uptake in small forested streams: diurnal and day-to-day variations. J North Am Benthol Soc 25:583–95.CrossRefGoogle Scholar
  71. Mulholland PJ et al. 2008. Stream denitrification across biomes and its response to anthropogenic nitrate loading. Nature 452:202–6.PubMedCrossRefGoogle Scholar
  72. Müller C, Rütting T, Abbasi MK, Laughlin RJ, Kammann C, Clough TJ, Sherlock RR, Kattge J, Jager HJ, Watson CJ, Stevens RJ. 2009. Effect of elevated CO2 on soil N dynamics in a temperate grassland soil. Soil Biol Biochem 41:1996–2001.CrossRefGoogle Scholar
  73. Nadelhoffer K, Downs M, Fry B, Magill A, Aber J. 1999. Controls on N retention and exports in a forested watershed. Environ Monit Assess 55:187–210.CrossRefGoogle Scholar
  74. Newbold JD, Elwood JW, O’Neill RV, van Winkle W. 1981. Measuring nutrient spiralling in streams. Can J Fish Aquat Sci 38:860–3.CrossRefGoogle Scholar
  75. Ohte N, Sebestyen SD, Shanley JB, Doctor DH, Kendall C, Wankel SD, Boyer EW. 2004. Tracing sources of nitrate in snowmelt runoff using a high-resolution isotopic technique. Geophys Res Lett 31:L21506.CrossRefGoogle Scholar
  76. Pardo LH, Kendall C, Pett-Ridge J, Chang CCY. 2004. Evaluating the source of streamwater nitrate using δ15N and δ18O in nitrate in two watersheds in New Hampshire, USA. Hydrol Process 18:2699–712.CrossRefGoogle Scholar
  77. Payne EK, Burgin AJ, Hamilton SK. 2009. Sediment nitrate manipulation using porewater equilibrators reveals potential for N and S coupling in freshwaters. Aquat Microb Ecol 54:233–41.CrossRefGoogle Scholar
  78. Perakis SS, Hedin LO. 2001. Fluxes and fates of nitrogen in soil of an unpolluted old-growth temperate forest, southern Chile. Ecology 82:2245–60.CrossRefGoogle Scholar
  79. Perakis SS, Hedin LO. 2002. Nitrogen loss from unpolluted South American forests mainly via dissolved organic compounds. Nature 415:416–19.PubMedCrossRefGoogle Scholar
  80. Petersen BJ et al. 2001. Control of nitrogen export from watersheds by headwater streams. Science 292:86–90.CrossRefGoogle Scholar
  81. Piatek KB, Mitchell MJ, Silva SR, Kendall C. 2005. Sources of nitrate in snowmelt discharge: evidence from water chemistry and stable isotopes of nitrate. Water Air Soil Pollut 165:13–35.CrossRefGoogle Scholar
  82. Providoli I, Bugmann H, Siegwolf R, Buchmann N, Schleppi P. 2005. Flow of deposited inorganic N in two gleysol-dominated mountain catchments traced with 15NO3 and 15NH4 +. Biogeochemistry 76:453–75.CrossRefGoogle Scholar
  83. Rennenberg H, Gessler A. 1999. Consequences of N deposition to forest ecosystems–recent results and future research needs. Water Air Soil Pollut 116:47–64.CrossRefGoogle Scholar
  84. Roberts BJ, Mulholland PJ. 2007. In stream biotic control on nutrient biogeochemistry in a forested stream, west fork of Walker Branch. J Geophys Res Biogeosci 112. doi:  10.1029/2007JG000422.
  85. Rütting T, Huygens D, Müller C, van Cleemput O, Godoy R, Boeckx P. 2008. Functional role of DNRA and nitrite reduction in a pristine south Chilean Nothofagus forest. Biogeochemistry 90:243–58.CrossRefGoogle Scholar
  86. Schiff SL, Devito KJ, Elgood RJ, McCrindle PM, Spoelstra J, Dillon P. 2002. Two adjacent forested catchments: dramatically different NO3 export. Water Resour Res 38:1292. doi: 10.1029/2000WR000170.CrossRefGoogle Scholar
  87. Schleppi P, Muller N, Feyen H, Papritz A, Bucher JB, Flühler H. 1998. Nitrogen budgets of two small experimental forested catchments at Alptal, Switzerland. For Ecol Manage 101:177–85.CrossRefGoogle Scholar
  88. Schleppi P, Hagedorn F, Providoli I. 2004. Nitrate leaching from a mountain forest ecosystem with Gleysols subjected to experimentally increased N deposition. Water Air Soil Pollut Focus 4:453–67.CrossRefGoogle Scholar
  89. Scholefield D, Le Goff T, Braven J, Ebdon L, Long T, Butler M. 2005. Concerted diurnal patterns in riverine nutrient concentrations and physical conditions. Sci Total Environ 344:201–10.PubMedCrossRefGoogle Scholar
  90. Scott D, Harvey J, Alexander R, Schwarz G. 2007. Dominance of organic nitrogen from headwater streams to large rivers across the conterminous United States. Glob Biogeochem Cycles 21:GB1003. doi: 10.1029/2006GB002730.CrossRefGoogle Scholar
  91. Sebesteyn SD, Boyer EW, Shanley J, Kendall C, Doctor DH, Aiken GR, Ohte N. 2008. Sources, transformations and hydrological processes that control stream nitrate and dissolved organic matter concentrations during snowmelt in an upland forest. Water Resour Res 44:W12410. doi: 10.1029/2008WR006983.CrossRefGoogle Scholar
  92. Spoelstra J, Schiff SL, Elgood RJ, Semkin RG, Jeffries DS. 2001. Tracing the sources of exported nitrate in the Turkey Lakes watershed using 15N/14N and 18O/16O isotopic ratios. Ecosystems 4:536–44.CrossRefGoogle Scholar
  93. Spoelstra J, Schiff SL, Hazlett PW, Jeffries DS, Semkin RG. 2007. The isotopic composition of nitrate produced from nitrification in a hardwood forest floor. Geochim Cosmochim Acta 71:3757–71.CrossRefGoogle Scholar
  94. Stark JM, Hart SC. 1997. High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385:61–4.CrossRefGoogle Scholar
  95. Stoddard JL. 1994. Long-term changes in watershed retention of nitrogen: its causes and aquatic consequences. In: Baker LA, Eds. Environmental chemistry of lakes and reservoirs. ACS Advances in Chemistry Series No. 237. Washington (DC): American Chemical Society. pp 223–284.Google Scholar
  96. Taylor PG, Townsend AR. 2010. Stoichiometric control of organic carbon–nitrate relationships from soils to the sea. Nature 464:1178–81.PubMedCrossRefGoogle Scholar
  97. Templer PH, Silver WL, Pett-Ridge J, DeAngelis KM, Firestone MK. 2008. Plant and microbial controls on nitrogen retention and loss in a humid tropical forest. Ecology 89:3030–40.CrossRefGoogle Scholar
  98. Thiemens MH, Savarino J, Farquhar J, Bao H. 2001. Mass-independent isotopic compositions in terrestrial and extraterrestrial solids and their applications. Acc Chem Res 34:645–52.PubMedCrossRefGoogle Scholar
  99. Tietema A, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ. 1998. The fate of 15N-labelled nitrogen deposition in coniferous forest ecosystems. Forest Ecol Man 101:19–27.CrossRefGoogle Scholar
  100. Van Breemen N, Van Dijk HFG. 1988. Ecosystem effects of atmospheric nitrogen deposition in the Netherlands. Environ Pollut 54:249–74.PubMedCrossRefGoogle Scholar
  101. Van Breemen N, Burrough PA, Velthorst EJ, van Dobben HF, De Wit T, Ridder TB, Reinders HFR. 1982. Soil acidification from atmospheric ammonium sulphate in forest canopy throughfall. Nature 299:548–50.CrossRefGoogle Scholar
  102. Van der Salm C, de Vries W, Reinds GJ, Dise NB. 2007. N leaching across European forests: derivation and validation of empirical relationships using data from intensive monitoring plots. Forest Ecol Man 238:81–91.CrossRefGoogle Scholar
  103. Vannote RJ, Minshall GW, Cummins KW, Sedell JR, Cushing CE. 1981. The river continuum concept. Can J Fish Aquat Sci 37:130–7.CrossRefGoogle Scholar
  104. Vitousek PM, Reiners WA. 1975. Ecosystem succession and nutrient retention: a hypothesis. Bioscience 25:376–81.CrossRefGoogle Scholar
  105. Williard KWJ, DeWalle DR, Edwards PJ, Sharpe WE. 2001. 18O isotopic separation of stream nitrate sources in mid-Appalachian forested watersheds. J Hydrol 252:174–88.CrossRefGoogle Scholar
  106. Wynn P, Hodson A, Heaton THE, Chenery SRN. 2007. Nitrate production beneath a High Arctic glacier, Svalbard. Chem Geol 244:88–102.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Chris J. Curtis
    • 1
    Email author
  • Chris D. Evans
    • 2
  • Christine L. Goodale
    • 3
  • Tim H.E. Heaton
    • 4
  1. 1.Environmental Change Research CentreUniversity College LondonLondonUK
  2. 2.CEH Bangor, Environment Centre WalesBangorUK
  3. 3.Department of Ecology & Evolutionary BiologyCornell UniversityIthacaUSA
  4. 4.NERC Isotope Geosciences LaboratoryBGS KeyworthNottinghamUK

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