Ecological Research

, Volume 24, Issue 5, pp 955–964 | Cite as

Ecological risks in anthropogenic disturbance of nitrogen cycles in natural terrestrial ecosystems

Special Feature Ecological risk management

Abstract

Anthropogenic addition of reactive nitrogen (Nr) to the biosphere is increasing globally and some terrestrial ecosystems are suffering from a state of excess Nr for biological nitrogen (N) demand, termed N saturation. Here, we review the ecological risks in relation to N saturation and prospective responses to N saturation. Excess Nr increases the risks of local extinction of rare plant species, encouragement of exotic plant species, disturbance of nutrient balance in plant organs, and increase of herbivory in plant communities. On the ecosystem scale, excess bioavailable N induces forest decline, disturbance of nutrient cycling within ecosystems, depending on vegetation, soil, land-use, and N-loading history. These Nr risks will increase in the Asian region, where impacts of Nr in natural terrestrial ecosystems have been scarcely studied. Whether much of the terrestrial ecosystems on a global level are in the sate of N saturation or not is still controversial, but the potential risks of excess Nr seem to be increasing. The fundamental ways to mitigate Nr risks are to reduce Nr production, prevent Nr translocation, and promote conversion of Nr to N2. Temporal, but promising actions against ecological N risks may include management of forests and riparian zones, and carbon addition in grassland.

Keywords

Reactive nitrogen (Nr) Nitrogen saturation Forest ecosystem Vegetation change Ecosystem management 

Notes

Acknowledgments

This study was supported by the twenty-first Century Centers of Excellence Program (Environmental Risk Management for Bio/Eco-Systems), Global Centers of Excellence Program (Global Eco-Risk Management from Asian Viewpoints) and Grant-in-Aid for Scientific Research (C19570017), from the Ministry of Education, Science, Culture and Sports, Japan.

References

  1. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39:378–386CrossRefGoogle Scholar
  2. Aber JD, McDowell W, Nadelhoffer K, Magil A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems: hypotheses revisited. Bioscience 48:921–934CrossRefGoogle Scholar
  3. Aber JD, Goodale SL, Ollinger SV, Smith M-L, Magill AH, Martin ME, Hallet RA, Stoddard JL (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? Bioscience 53:375–389CrossRefGoogle Scholar
  4. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a reevaluation of process and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  5. Aiba Y, Haibara K, Kawabata S (1983) The effects of intensive tending work on soil productivity (II) decomposition and movement of potential nutrients of fallen sugi (Cryptomeria japonica D. Don) foliage from green pruning. J Jpn For Soc 65:215–219 (in Japanese with English summary)Google Scholar
  6. Aiba Y, Haibara K, Kondo H, Ikeda N (1985) The effects of intensive tending works on soil productivity (III) nutrient discharge from young stands caused by weeding, fertilization, and the first pruning. J Jpn For Soc 67:73–81 (in Japanese with English summary)Google Scholar
  7. Basynat P, Teeter LD, Lockaby BG, Flynn KM (2000) The use of remote sensing and GIS in watershed level analyses of non-point source pollution problems. For Ecol Manage 128:65–73CrossRefGoogle Scholar
  8. Bigelow SW, Canham CD (2007) Nutrient limitation of juvenile trees in a northern hardwood forest: calcium and nitrate are preeminent. For Ecol Manage 243:310–319CrossRefGoogle Scholar
  9. Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615CrossRefGoogle Scholar
  10. Cassidy TM, Fownes JH, Harrington RA (2004) Nitrogen limits an invasive perennial shrub in forest understory. Biol Invasions 6:113–121CrossRefGoogle Scholar
  11. Castro MS, Eshleman KN, Pitelka LF, Frech G, Ramsey M, Currie WS, Kuers K, Simmons JA, Pohlad BR, Thomas CL, Johnson DM (2007) Symptoms of nitrogen saturation in an aggrading forested watershed in western Maryland. Biogeochemistry 84:333–348CrossRefGoogle Scholar
  12. Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S (2000) Consequence of changing biodiversity. Nature 405:234–242PubMedCrossRefGoogle Scholar
  13. Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715PubMedCrossRefGoogle Scholar
  14. Currie WS (1999) The responsive C and N biogeochemistry of the temperate forest floor. Trends Ecol Evol 14:316–320PubMedCrossRefGoogle Scholar
  15. Del Grosso SJ, Parton WJ, Mosier AR, Ojima DS, Kulmala AE, Phongpan S (2000) General model for N2O and N2 gas emissions from soil due to denitrification. Global Biogeochem Cycles 14:1045–1060CrossRefGoogle Scholar
  16. Dijkstra FA, West JB, Hobbie SE, Reich PB, Trost J (2007) Plant diversity, CO2, and N influence inorganic and organic N leaching in grasslands. Ecology 88:490–500PubMedCrossRefGoogle Scholar
  17. Dillon PJ, Molot LA (1990) The role of ammonium and nitrate in acidification of lakes and forested catchments. Biogeochemisitry 11:23–44Google Scholar
  18. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  19. Enoki T, Kawaguchi H, Iwatsubo G (1997) Nutrient-uptake and nutrient-use efficiency of Pinus thunbergii Parl. along a topographical gradient of soil nutrient availability. Ecol Res 12:191–199CrossRefGoogle Scholar
  20. Erinsman JW, de Vries W (2000) Nitrogen deposition and effects in European forests. Environ Rev 8:65–93CrossRefGoogle Scholar
  21. Eschen R, Mortimer SR, Lawson CS, Edwards AR, Brook AJ, Igual JM, Hedlund K, Schaffner U (2007) Carbon addition alters vegetation composition on ex-arable fields. J Appl Ecol 44:95–104CrossRefGoogle Scholar
  22. Feller MC (2005) Forest harvesting and streamwater inorganic chemistry in western North America: a review. J Am Water Resour Assoc 41:785–811Google Scholar
  23. Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly AD, McNulty SG, Ryan DF, Stottlemyer R (1998) Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8:706–733CrossRefGoogle Scholar
  24. Fujimaki R, Kawasaki A, Fujii Y, Kaneko N (2008) The influence of topography on the stream N concentration in the Tanzawa Mountains, Southern Kanto District, Japan. J For Res 13:380–385CrossRefGoogle Scholar
  25. Fukushima K, Tokuchi N (2008) Effects of forest clearcut and afforestation on streamwater chemistry in Japanese cedar (Cryptomeria japonica) forests: comparison among watersheds of various stand ages. J Jpn For Soc 90:6–16 (in Japanese with English summary)CrossRefGoogle Scholar
  26. Fukuzawa K, Shibata H, Takagi K, Nomura M, Kurima N, Fukazawa T, Satoh F, Sasa K (2006) Effects of clear-cutting on nitrogen leaching and fine root dynamics in a cool-temperate forested watershed in northern Japan. For Ecol Manage 225:261–275CrossRefGoogle Scholar
  27. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53:341–356CrossRefGoogle Scholar
  28. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vörösmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  29. Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191CrossRefGoogle Scholar
  30. Gilliam FS, Yurich BM, Adams MB (2001) Temporal and spatial variation of nitrogen transformations in nitrogen saturated soils of a Central Appalachian hardwood forest. Can J For Res 31:1768–1785CrossRefGoogle Scholar
  31. Gress SE, Nichols TD, Northcraft CC, Peterjohn WT (2007) Nutrient limitation in soils exhibiting differing nitrogen availabilities: what lies beyond nitrogen saturation? Ecology 88:119–130PubMedCrossRefGoogle Scholar
  32. Gundersen P, Emmett BA, Kjønaas OJ, Koopmans CJ, Tietema A (1998) Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. For Ecol Manage 101:37–55CrossRefGoogle Scholar
  33. Gundersen P, Schmidt IK, Raulund-Rasmussen K (2006) Leaching of nitrate from temperate forests - effects of air pollution and forest management. Environ Rev 14:1–57CrossRefGoogle Scholar
  34. Haibara K, Aiba Y (1990) Effects of tending practice on nutrient dynamics in a young stand of sugi (Cryptomeria japonica) and hinoki (Chamaecyparis obtusa). For Ecol Manage 30:233–246CrossRefGoogle Scholar
  35. Hansen K, Rosenqvist L, Vesterdal L, Gundersen P (2007) Nitrate leaching from three afforestation chronosequences on former arable land in Denmark. Global Chang Biol 13:1250–1264CrossRefGoogle Scholar
  36. Haycock NE, Pinay G, Waker C (1993) Nitrogen retention in river corridors: European perspective. Ambio 22:340–346Google Scholar
  37. Hefting MM, Bobbink R, Janssens MP (2006) Spatial variation in denitrification and N2O emission in relation to nitrate removal efficiency in a N-stressed riparian buffer zone. Ecosystems 9:550–563CrossRefGoogle Scholar
  38. Hill AR (1996) Nitrate removal in stream riparian zones. J Environ Qual 25:743–755CrossRefGoogle Scholar
  39. Hill AR, Devito KJ, Campagnolo S, Sanmugadas K (2000) Subsurface denitrification in a forest riparian zone: interaction between hydrology and supplies of nitrate and organic carbon. Biogeochemistry 51:193–223CrossRefGoogle Scholar
  40. Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308PubMedCrossRefGoogle Scholar
  41. Holland EA, Dentener FJ, Bobby HB, Sulzman JM (1999) Contemporary and pre-industrial global reactive nitrogen budgets. Biogeochemistry 46:7–43Google Scholar
  42. Homyak PM, Yanai RD, Burns DA, Briggs RD, Germain RH (2008) Nitrogen immobilization by wood-chip application: protecting water quality in a northern hardwood forest. For Ecol Manage 255:2589–2601CrossRefGoogle Scholar
  43. Hong B, Swaney DP, Woodbury PB, Weinstein DA (2005) Long-term nitrate export pattern from Hubbard Brook watershed 6 driven by climatic variation. Water Air Soil Pollut 160:293–326CrossRefGoogle Scholar
  44. Hutchings MJ, John EA, Wijestinghe DK (2003) Toward understanding the consequence of sol heterogeneity for plant populations and communities. Ecology 84:2322–2334CrossRefGoogle Scholar
  45. Ito A (2002) Soil organic carbon storage as a function of the terrestrial ecosystem with respect to the global carbon cycle (in Japanese with English summary). Jpn J Ecol 52:189–227Google Scholar
  46. Jonasson S, Vestergaard P, Jensen M, Michelsen A (1996) Effects of carbohydrate amendments on nutrient partitioning, plant and microbial performance of a grassland-shrub ecosystem. Oikos 75:220–226CrossRefGoogle Scholar
  47. Judd KE, Likens GE, Groffman PM (2007) High nitrate retention during winter in soils of the Hubberd Brook Experimental Forest. Ecosystems 10:217–225CrossRefGoogle Scholar
  48. Laverman AM, Borgers P, Verhoef HA (2002) Spatial variation in net nitrate production in a N-saturated coniferous forest soil. For Ecol Manage 161:123–132CrossRefGoogle Scholar
  49. Likens GE, Borman FH, Johnson NM, Fisher DW, Pierce RS (1970) Effects of forest cutting and herbicide treatment on nutrient budgets in the Hubbard Brook ecosystem in New Hampshire. Ecol Monogr 40:23–47Google Scholar
  50. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomyocrrizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115Google Scholar
  51. Lovett GM, Weathers KC, Arthur MA (2002) Control of nitrogen loss from forested watersheds by soil carbon:nitrogen ratio and tree species composition. Ecosystems 5:712–718CrossRefGoogle Scholar
  52. Lovett GM, Weathers KCV, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308CrossRefGoogle Scholar
  53. Lowrance RR, Todd R, Fail J, Hendrickson O, Leonard R, Asmussen L (1984) Riparian forests as nutrient filters in agricultural watersheds. Bioscience 34:374–377CrossRefGoogle Scholar
  54. Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443PubMedCrossRefGoogle Scholar
  55. Magill AH, Aber JD, Berntson GM, McDowell WH, Nadelhoffer KJ, Melillo JM, Steudler P (2000) Long-term nitrogen addition and nitrogen saturation in two temperate forests. Ecosystems 3:238–253CrossRefGoogle Scholar
  56. 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 196:7–28CrossRefGoogle Scholar
  57. Magnani F, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Selzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentini R, Grace J (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:848–850PubMedCrossRefGoogle Scholar
  58. Mayer PM, Reynolds SK, McCutchen MD, Canfield TJ (2007) Meta-analysis of nitrogen removal in riparian buffers. J Environ Qual 36:1172–1180PubMedCrossRefGoogle Scholar
  59. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: synthesis. Island Press, Washington, DCGoogle Scholar
  60. Mitchell MJ, Iwatsubo G, Ohrui K, Nakagawa Y (1997) Nitrogen saturation in Japanese forests: an evaluation. For Ecol Manage 97:39–51CrossRefGoogle Scholar
  61. Nadelhoffer KJ, Downs MR, Fry B (1999a) Sinks for N additions to an oak forest and a red pine plantation at the Harvard Forest, Massachusetts, USA. Ecol Appl 9:72–86CrossRefGoogle Scholar
  62. Nadelhoffer KJ, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ, Schleppi P, Tietema A, Wright RF (1999b) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148CrossRefGoogle Scholar
  63. Nagakura J, Akama A, Mizoguchi T, Okabe H, Shigenaga H, Yamanaka T (2006) Effects of chronic nitrogen application on the growth and nutrient status of a Japanese cedar (Cryptomeria japonica) stand. J For Res 11:299–304CrossRefGoogle Scholar
  64. Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–917PubMedCrossRefGoogle Scholar
  65. Nordin A, Strengbom J, Ericson L (2006) Responses to ammonium and nitrate additions by boreal plants and their natural enemies. Environ Pollut 141:167–174PubMedCrossRefGoogle Scholar
  66. Ohrui K, Mitchell MJ (1998) Spatial patterns of soil nitrate in Japanese forested watersheds: importance of the near-stream zone as a source of nitrate in stream water. Hydrol Process 12:1433–1445CrossRefGoogle Scholar
  67. Ohte N, Tokuchi N, Shibata H, Tsujimura M, Tanaka T, Mitchell MJ (2001) Hydrobiogeochemistry of forest ecosystems in Japan: major themes and research issues. Hydrol Process 15:1771–1789CrossRefGoogle Scholar
  68. Oren R, Ellsworth DR, Johnsen KH, Phillips N, Ewers BE, Maier C, Schäfer KVR, McCarthy H, Hendrey G, McNulty SG, Katul GG (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472PubMedCrossRefGoogle Scholar
  69. Ozawa M, Shibata H, Satoh F, Sasa K (2001) Effects of surface soil removalon dynamics of dissolved inorganic nitrogen in a snow-dominated forest. Sci World 1(S2):527–533Google Scholar
  70. Parfitt RL, Schipper LA, Baisden WT, Elliott AH (2006) Nitrogen inputs and outputs for New Zealand in 2001 at national and regional scales. Biogeochemistry 80:71–88CrossRefGoogle Scholar
  71. 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 165:13–35CrossRefGoogle Scholar
  72. Post WM, Emanuel WR, Zinke PJ, Stangenberger AG (1982) Soil carbon pools and world life zones. Nature 298:156–159CrossRefGoogle Scholar
  73. Prober SM, Thiele KR, Lunt ID, Koen TB (2005) Restoring ecological function in temperate grassy woodlands: manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns. J Appl Ecol 42:1073–1085CrossRefGoogle Scholar
  74. Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925PubMedCrossRefGoogle Scholar
  75. Schade JD, Fisher SG, Grimm NB, Seddon JA (2001) The influence of a riparian shrub on nitrogen cycling in a Sonoran Desert stream. Ecology 82:3363–3376CrossRefGoogle Scholar
  76. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602CrossRefGoogle Scholar
  77. Shibata H, Kuraji K, Toda H, Sasa K (2001) Regional comparison of nitrogen export to Japanese forest streams. Sci World J 1(S2):572–580Google Scholar
  78. Shibata H, Sugawara O, Toyoshima H, Wondzell SM, Nakamura F, Kasahara T, Swanson FJ, Sasa K (2004) Nitrogen dynamics in the hyporheic zone of a forested stream during a small storm, Hokkaido, Japan. Biogeochemistry 69:83–104CrossRefGoogle Scholar
  79. Shibata H, Ozawa M, Satoh F, Sasa K (2007) The effect of treatment for land surface during forest practice on soil nitrogen dynamics (in Japanese with English summary). J Jpn For Soc 89:314–320CrossRefGoogle Scholar
  80. Shindo J, Okamoto K, Kawashima H (2006) Prediction of the environmental effects of excess nitrogen caused by increasing food demand with rapid economic growth in eastern Asian countries, 1961–2020. Ecol Model 193:703–720CrossRefGoogle Scholar
  81. Smil V (2002) Nitrogen and food production: proteins for human diets. Ambio 31:126–131PubMedGoogle Scholar
  82. Stevens CJ, Dise NB, Moundford JO, Gowing DJ (2004) Impact of nitrogen deposition on the specie richness of grasslands. Science 303:1876–1879PubMedCrossRefGoogle Scholar
  83. Stevens CJ, Dise NB, Gowing DJG, Mountford JO (2006) Loss of forb diversity in relation to nitrogen deposition in the UK: regional trends and potential controls. Global Change Biol 12:1823–1883CrossRefGoogle Scholar
  84. Stoddard JL (1994) Long-term changes in watershed retention of nitrogen, its causes and aquatic consequences. In: Baker AL (ed) Environmental chemistry of lakes and reservoirs. Am Chem Soc, Washington, DC, pp 223–284Google Scholar
  85. Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci USA 102:4387–4392PubMedCrossRefGoogle Scholar
  86. Takahashi T, Shoji S (2002) Distribution and classification of volcanic ash soils. Global Environ Res 6:83–97Google Scholar
  87. Takahashi T, Haibara K, Aiba Y, Toda H, Fukuda M (1995) Effects of weeds and weeding on nutrients dynamics in young stands (in Japanese with English summary). Jpn J For Environ 37:67–76Google Scholar
  88. Tateno R, Hishi T, Takeda H (2004) Above- and belowground biomass and net primary production in a cool temperate deciduous forest in relation to topographical changes in soil nitrogen. For Ecol Manage 193:297–306CrossRefGoogle Scholar
  89. Throop HL, Lerdau MT (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7:109–133CrossRefGoogle Scholar
  90. Tilman D, Knops J, Peter B, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302CrossRefGoogle Scholar
  91. Tokuchi N, Takeda H, Yoshida K, Iwatsubo G (1999) Topographical variations in a plant-soil system along a slope on Mt. Ryuoh, Japan. Ecol Res 14:361–369CrossRefGoogle Scholar
  92. Tokuchi N, Hirobe M, Koba K (2000) Topographical differences in soil N transformation using 15N dilution method along a slope in a conifer plantation forest in Japan. J For Res 5:13–19CrossRefGoogle Scholar
  93. Török K, Szili-Kovács T, Halassy M, Tóth T, Zs Hayek, Paschke MW, Wardell LJ (2000) Immobilization of soil nitrogen as a possible method for the restoration of sandy grassland. Appl Veg Sci 3:7–14CrossRefGoogle Scholar
  94. Townsend AR, Braswell BH, Holland EA, Penner JE (1996) Spatial and temporal patterns in terrestrial carbon storage due to deposition of fossil fuel nitrogen. Ecol Appl 6:806–814CrossRefGoogle Scholar
  95. Urakawa R, Toda H, Haibara K (2007) Retardation of nitrogen leaching by the NO3 adsorption in the subsoil in a watershed of old Japanese cedar and cypress stands (in Japanese with English summary). J Jpn For Soc 89:190–199CrossRefGoogle Scholar
  96. van Dobben HF, van Hinsberg A, Schouwenberg EPAG, Jansen M, Mol-Dijkstra JP, Wieggers HJJ, Kros J, de Vries W (2006) Simulation of critical loads for nitrogen for terrestrial plant communities in the Netherlands. Ecosystems 9:32–45CrossRefGoogle Scholar
  97. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  98. Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. Bioscience 25:376–381CrossRefGoogle Scholar
  99. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750Google Scholar
  100. Yanai RD (1998) The effect of whole-tree harvest on phosphorus cycling in a northern hardwood forest. For Ecol Manage 104:281–295CrossRefGoogle Scholar
  101. Zaccherio M, Finzi AC (2007) Atmospheric deposition may affect northern hardwood forest composition by altering soil nutrient supply. Ecol Appl 17:1929–1941PubMedCrossRefGoogle Scholar
  102. Zak DR, Groffman PM, Pregitzer KS, Christensen S, Tiedje JM (1990) The vernal dam: plant-microbe competition for nitrogen in northern hardwood forests. Ecology 71:651–656CrossRefGoogle Scholar

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© The Ecological Society of Japan 2009

Authors and Affiliations

  1. 1.Graduate School of Environment and Information SciencesYokohama National UniversityYokohamaJapan

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