, Volume 13, Issue 2, pp 87–115 | Cite as

Nitrogen limitation on land and in the sea: How can it occur?

  • Peter M. Vitousek
  • Robert W. Howarth


The widespread occurrence of nitrogen limitation to net primary production in terrestrial and marine ecosystems is something of a puzzle; it would seem that nitrogen fixers should have a substantial competitive advantage wherever nitrogen is limiting, and that their activity in turn should reverse limitation. Nevertheless, there is substantial evidence that nitrogen limits net primary production much of the time in most terrestrial biomes and many marine ecosystems.

We examine both how the biogeochemistry of the nitrogen cycle could cause limitation to develop, and how nitrogen limitation could persist as a consequence of processes that prevent or reduce nitrogen fixation. Biogeochemical mechansism that favor nitrogen limitation include:

  • the substantial mobility of nitrogen across ecosystem boundaries, which favors nitogen limitation in the “source” ecosystem — especially where denitrification is important in sediments and soils, or in terrestrial ecosystems where fire is frequent;

  • differences in the biochemistry of nitrogen as opposed to phosphorus (with detrital N mostly carbon-bonded and detrital P mostly ester-bonded), which favor the development of nitrogen limitation where decomposition is slow, and allow the development of a positive feedback from nitrogen limitation to producers, to reduced decomposition of their detritus, and on to reduced nitrogen availability; and

  • other more specialized, but perhaps no less important, processes.

A number of mechanisms could keep nitrogen fixation from reversing nitrogen limitation. These include:

  • energetic constraints on the colonization or activity of nitrogen fixers;

  • limitation of nitrogen fixers or fixation by another nutrient (phosphorus, molybdenum, or iron) — which would then represent the ultimate factor limiting net primary production;

  • other physical and ecological mechanisms.

The possible importance of these and other processes is discussed for a wide range of terrestrial, freshwater, and marine ecosystems.

Key words

biogeochemistry energetic constraints nitrogen fixation phosphorus succession trace elements 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aber JD, Nadelhoffer JK, Steudler PA amp; Melillo JM (1989) Nitrogen saturation in northern forest ecosystems — hypotheses and implications. BioScience 39: 378–386Google Scholar
  2. Agren GI (1983) Nitrogen productivity of some conifers. Can J Forest Res 13: 494–500Google Scholar
  3. Alexander M (1977) An Introduction to Soil Microbiology. John Wiley and Sons, New YorkGoogle Scholar
  4. Atkinson MJ amp; Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol. Oceanogr. 26: 1074–1083Google Scholar
  5. Banse K (1990) Does iron really limit phytoplankton production in the offshore subarctic Pacific? Limnol. Oceanogr. 35: 772–775Google Scholar
  6. Bhella HS amp; Dawson MD (1972) The use of anion exchange resin for determining available soil molybdenum. Soil Sci. Soc. Amer. Proc. 36: 177–178Google Scholar
  7. Binkley D (1986) Forest Nutrition Management: John Wiley and Sons, New York. 299 ppGoogle Scholar
  8. Birk EM amp; Vitousek PM (1984) Patterns of N retranslocation in loblolly pine: response to N availability. Ecol. Soc. Amer. Bull. 65: 100Google Scholar
  9. Bliss LC (1963) Alpine plant communities of the Presidential Range, New Hampshire. Ecology 44: 678–697Google Scholar
  10. Bonan GB (1990) Carbon and nitrogen cycling in North American boreal forests. II. Biogeographic patterns. Can. J. Forest Res. 20: 1077–1088Google Scholar
  11. Boring LR, Swank WT, Waide JB amp; Henderson GS (1988) Sources, fates, and impacts of nitrogen inputs to terrestrial ecosystems: review and synthesis. Biogeochemistry 6: 119–159Google Scholar
  12. Bormann BT amp; Gordon JC (1984) Stand density effects in yound red alder planations: productivity, photosynthate partitioning, and nitrogen fixation. Ecology 65: 394–402Google Scholar
  13. Bormann FH amp; Likens GE (1979) Pattern and Process in a Forested Ecosystem. Springer-Verlag, NY. 253 ppGoogle Scholar
  14. Boynton WR, Kemp WM Keefe CW (1982) A comparative analysis of nutrients and other factors influencing estuarine phytoplankton production. In: Kennedy VS (Ed) Estuarine Comparisons (pp 69–91). Academic Press, New YorkGoogle Scholar
  15. Bradshaw AD, Chadwick MJ, Jowett D, Lodge RW amp; Snaydon RW (1960) Experimental investigations into the mineral nutrition of several grass species. III. Phosphate level. J. Ecology 48: 631–637Google Scholar
  16. Bradshaw AD, Chadwick MJ, Jowett D amp; Snaydon RW (1964) Experimental investigations into the mineral nutrition of several grass species. IV. Nitrogen level. J. Ecology 52: 665–676Google Scholar
  17. Broecker WS (1982) Glacial to interglacial changes in ocean chemistry. Prog. Oceanogr. 2: 151–197Google Scholar
  18. Campbell CE amp; Prepas EE (1986) Evaluation of factors related to the unusually low chlorophyll levels in prairie saline lakes. Can. J. Fish. Aquat. Sci. 43: 846–854Google Scholar
  19. Caraco N, Cole JJ amp; Likens GE (1989) Evidence for sulfate-controlled phosphorus release from sediments of aquatic systems. Nature 341: 316–318Google Scholar
  20. Caraco N, Cole JJ amp; Likens GE (1990) A comparison of phosphorus immobilization in sediments of freshwater and coastal marine systems. Biogeochemistry 9: 277–290Google Scholar
  21. Carpenter EJ (1983) Nitrogen fixation by marine Oscillatoria (Trichodesmium) in the World's oceans. In: Carpenter EJ amp; Capone DG (Eds) Nitrogen in the Marine Environment (pp65–103). Academic press, New YorkGoogle Scholar
  22. Carpenter EJ amp; Capone DG (Ed) (1983) Nitrogen in the Marine Environment. Academic Press, New York. 900 ppGoogle Scholar
  23. Carpenter EJ amp; Price CC (1976) Marine Oscillatoria (Trichodesmium): Explanation for aerobic nitrogen fixation without heterocysts. Science 191: 1278–1280Google Scholar
  24. Chapin FS III, Vitousek PM amp; Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am. Nat. 127: 48–58Google Scholar
  25. Coats RN, Leonard RL amp; Goldman CR (1976) Nitrogen uptake and release in a forested watershed, Lake Tahoe Basin, California. Ecology 57: 995–1004Google Scholar
  26. Cole CV amp; Heil RD (1981) Phosphorus effects on terrestrial nitrogen cycling. Ecol. Bull. (Stockholm) 33: 363–374Google Scholar
  27. Cole CV, Stewart JWB, Ojima DS, Parton WJ amp; Schimel DS (1989) Modelling land use effects of soil organic matter dynamics in the North American Great Plains. In: Clarholm M amp; Bergström L (Eds) Ecology of Arable Land: Perspectives and Challenges (pp 89–98). Kluwer Academic, DordrechtGoogle Scholar
  28. Cornaby BW amp; Waide JB (1973) Nitrogen fixation in decaying chestnut logs. Plant Soil 39: 445–448Google Scholar
  29. Crews T, Marino R amp; Howarth RW (1989) Constraints on the availability of molybdenum to plants and nitrogen fixers at Hubbard Brook, New Hampshire. Suppl. Bull. Ecol. Soc. Am. 70: 89Google Scholar
  30. Crutzen PJ amp; Andreae MO Biomass burning in the tropics: impact on atmospheric chemistry and biogeochemical cycles. Science 250: 1669–1678Google Scholar
  31. Cuevas E amp; Medina E (1986) Nutrient dynamics within Amazonian forests. I. Nutrient flux in fine litter fall and the efficiency of nutrient utilization. Oecologia 68: 466–472Google Scholar
  32. Cuevas E amp; Medina E (1988) Nutrient dynamics within Amazonian forests. II. Fine root growth, nutrient availability, and leaf litter decomposition. Oecologia 76: 222–235Google Scholar
  33. D'Elia CF, Sanders JG amp; Boynton WR (1986) Nutrient enrichment studies in a coastal plain estuary: Phytoplankton growth in large-scale, continuous cultures. Can. J. Fish. Aquat. Sci. 43: 397–406Google Scholar
  34. Denison WC (1979) Lobaria oregana, a nitrogen fixing lichen in old growth Douglas-fir forests. In: Gordon JC, Wheeler CT amp; Perry DA (Eds) Symbiotic Nitrogen Fixation in the Management of Temperate Forests (pp 266–275). Oregon State University, CorvallisGoogle Scholar
  35. Dixon ROD amp; Wheeler CT (1983) Biochemical, physiological, and environmental aspects of symbiotic nitrogen fixation. In: Gordon, JC amp; Wheeler CT (Eds) Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Application (pp 108–171). Nijhoff/Junk Publishers, The HagueGoogle Scholar
  36. Dodd JL amp; Lauenroth WK (1979) Analysis of the response of a grassland ecosystem to stress. In: French NR (Ed) Perspectives in Grassland Ecology (pp 43–58). Springer-Verlag, New YorkGoogle Scholar
  37. Doremus C (1982) Geochemical control of dinitrogen fixation in the open ocean. Biol. Oceanogr. 1: 429–436Google Scholar
  38. Dugdale RC amp; Wilkerson FP (1990) Iron addition experiments in the Antarctic: a reanalysis. Global Biogeochemical Cycles 4: 13–19Google Scholar
  39. Edmondson WT (1970) Phosphorus, nitrogen, and algae in Lake Washington after diversion of sewage. Science 169: 690–691Google Scholar
  40. Eisele KA, Schimel DS, Kapustka LA amp; Parton WJ (1989) Fire-stimulated N2 fixation as a result of altered N:P ratios. Oecologia 79: 471–464Google Scholar
  41. Evans JR amp; Seeman JR (1989) The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. In: Briggs W (Ed) Photosynthesis (pp 183–205). Alan R. Liss, New YorkGoogle Scholar
  42. Field CB amp; Mooney HA (1986) The nitrogen/photosynthesis relationship in wild plants In: Givnish TJ (Ed) On the Economy of Plant Form and Function (pp 25–55). Cambridge University Press, Cambridge, EnglandGoogle Scholar
  43. Fisher FM, Zak JC, Cunningham GL amp; Whitford WG (1988) Water and nitrogen effects on growth and allocation patterns of creosote bush in the northern Chihuahuan Desert. J. Range. Manag. 41: 387–395Google Scholar
  44. Flanagan PW amp; Van Cleve K (1983) Nutrient cycling in relation to decomposition and organic matter quality in taiga ecosystems. Can. J. Forest Res. 13: 795–817Google Scholar
  45. Flett RJ, Schindler DW, Hamilton RD amp; Campbell NER (1980) Nitrogen fixation in Canadian Precambrian Shield lakes. Can. J. Fish. Aquat. Sci. 37: 494–505Google Scholar
  46. Frithsen JB, Oviatt CA, Pilson MEQ, Howarth RW amp; Cole JJ (1988) A comparison of nitrogen vs. phosphorus limitation of production in coastal marine ecosystems. EOS 69 (44): 1100Google Scholar
  47. Gadgil RL, Knight PJ, Sandberg AM amp; Allen PJ (1981) Molybdenum, sulphur, and boron deficiency in lupin (Lupinus arboreus Sims) at Pouto Forest. N.Z. J. For. Sci. 11: 114–127Google Scholar
  48. Goldman CR (1988) Primary productivity, nutrients, and transparency during the early onset of eutrophication in ultra-oligotrophic Lake Tahoe. California-Nevada. Limnol. Oceanogr. 33: 1321–1333Google Scholar
  49. Gorham E, Vitousek PM amp; Reiners WA (1979) The regulation of chemical budgets over the course of terrestrial ecosystem succession. Ann. Rev. Ecol. Syst. 10: 53–88Google Scholar
  50. Graneli E (1978) Algal assay of limiting nutrients for phytoplankton production in the Oresund. Vatten 2: 117–128Google Scholar
  51. Graneli E (1981) Bioassay experiments in the Falsterbo channel — nutrients added daily. Kieler Meeresforch., Sonderh. 5: 82–90Google Scholar
  52. Graneli E (1984) Algal growth potential and limiting nutrients for phytoplankton production in Oresund water of Baltic and Kattegat origin. Limnologica (Berlin) 15: 563–569Google Scholar
  53. Grubb PJ (1989) The role of mineral nutrients in the tropics: a plant ecologist's view. In: Proctor, J (Ed) Mineral Nutrients in Tropical Forest and Savanna Ecosystems (pp 417–439). Blackwell Scientific, OxfordGoogle Scholar
  54. Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. Am. Nat. 118: 607–637Google Scholar
  55. Gutschick VP (1987) A Functional Biology of Crop Plants. Timber Press, Portland. 230 ppGoogle Scholar
  56. Haas HJ, Evans CE amp; Shih SH (1957) Nitrogen and carbon changes in Great Plains soils as influenced by cropping and soil treatments. USDA Tech. Bull. 1164. 111 ppGoogle Scholar
  57. Haas, HJ, Gounes DL amp; Reichmann GA (1961) Phosphorus changes in Great Plains soils as influenced by cropping and manure applications. Soil. Sci. Soc. Amer. Proc. 25: 214–218Google Scholar
  58. Hecky RE amp; Kilham P (1988) Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment. Limonol. Oceanogr. 33: 796–822Google Scholar
  59. Hines ME amp; Lyons WB (1982) Biogeochemistry of nearshore Bermuda sediments. I. Sulfate reduction rates and nutrient regeneration. Mar. Ecol. Progr. Ser. 8: 87–94Google Scholar
  60. Hobbs NT amp; Schimel DS (1984) The effects of fire on nitrogen mineralization and fixation in mountain grassland and shrub communities. J. Range Manage. 37: 402–405Google Scholar
  61. Högberg P (1989) Root symbioses of trees in savannas. In: Proctor J (Ed) Mineral Nutrients in Tropical Forest and Savanna Ecosystems (pp 121–136). Blackwell Scientific, OxfordGoogle Scholar
  62. Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Ann. Rev. Ecol. Syst. 19: 89–110Google Scholar
  63. Howarth RW amp; Cole JJ (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229: 653–655Google Scholar
  64. Howarth RW, Hairston NG Jr, Gerardi J amp; Schaffner WR (1990) Interactions between plankton community composition and N cycling in experimental ponds. ASLO meeting, June 10–15, 1990Google Scholar
  65. Howarth RW, Marino R, Lane J amp; Cole JJ (1988a) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnol. Oceanogr. 33: 669–687Google Scholar
  66. Howarth, RW, Marino R amp; Cole JJ (1988b) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33: 688–701Google Scholar
  67. Huenneke LF, Hamburg SP, Koide R, Mooney HA amp; Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71: 478–491Google Scholar
  68. Hunt HW, Stewart JWB amp; Cole CV (1983) A conceptual model for interactions of carbon, nitrogen, phosphorus, and sulfur in grasslands. In: Bolin B amp; Cook RB (Eds) The Major Biogeochemical Cycles and Their Interactions (pp 303–326). John Wiley and Sons, New YorkGoogle Scholar
  69. Hunt HW, Ingham ER, Coleman DC, Elliott ET amp; Reid CPP (1988) Nitrogen limitation of production and decomposition in prairie, mountain meadow, and pine forest. Ecology 69: 1009–1016Google Scholar
  70. Jackson GA amp; Williams PM (1985) Importance of dissolved organic nitrogen and phosphorus to biological nutrient cycling. Deep-Sea Res. 32: 223–235Google Scholar
  71. Jarrell WM amp; Dawson MD (1978) Sorption and availability of molybdenum in soils of Western Oregon. Soil. Sci. Soc. Amer. J. 42: 412–415Google Scholar
  72. Jordan CF (1985) Nutrient Cycling in Tropical Forest Ecosystems: Principles and Their Application in Conservation and Management. John Wiley and Sons, Chichester, England. 179 ppGoogle Scholar
  73. Kamp-Nielsen L (1974) Mud-water exchange of phosphate and other ions in undisturbed sediment cores and factors affecting the exchange rate. Arch. Hydrobiol. 73: 218–237Google Scholar
  74. Keller M, Kaplan WA amp; Wofsy SC (1986) Emissions of N2O, CH4, and CO2 from tropical soils. J. Geophys. Res. 91: 11,791–11,801Google Scholar
  75. Kelly JR amp; Levin SA (1986) A comparison of aquatic and terrestrial nutrient cycling and production processes in natural ecosystems, with reference to ecological concepts of relevance to some waste disposal issues. In: Kullenberg G (Ed) The Role of Oceans as a Waste Disposal Option (pp 165–203). ReidelGoogle Scholar
  76. Khalid RA, Patrick WH amp; DeLaune RD (1977) Phosphorus sorption characteristics of flooded soils. Soil. Sci. Soc. Am. J. 41: 305Google Scholar
  77. Kimmins JP (1987) Forest Ecology. Macmillian Publishing, New York. 531 ppGoogle Scholar
  78. Kinjo T amp; Pratt PF (1971) Nitrate adsorption. II. In competition with chloride, sulfate, and phosphate. Soil. Sci. Soc. Amer. Proc. 35: 725–728Google Scholar
  79. Knauer GA, Martin JH amp; Burland KW (1979) Fluxes of particulate carbon, nitrogen, and phosphorus in the upper water column of the northeast Pacific. Deep-Sea Res. 26A: 97–108Google Scholar
  80. Knowles R (1982) Denitrification. Microbiol. Rev. 46: 43–70Google Scholar
  81. Krom MD amp; Berner RA (1980) Adsorption of phosphate in anoxic marine sediments. Limnol. Oceanogr. 25: 797–806Google Scholar
  82. Lapointe BE, Littler MM amp; Littler DS (1987) A comparison of nutrient-limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem. Aquat. Bot. 28: 243–255Google Scholar
  83. Lee JA, Harmer R amp; Ignaciuk R (1983) Nitrogen as a limiting factor in plant communities. In: Lee JA, McNeill S Rorison IH (Eds) Nitrogen as an Ecological Factor (pp 95–112). Blackwell Scientific, OxfordGoogle Scholar
  84. Lehman IT (1984) Grazing, nutrient release, and their impacts on the structure of zooplankton communities. In: Meyers DG amp; Strickland JR (Eds) Trophic Interactions Within Aquatic Ecosystems. Westview Press, Boulder, ColoradoGoogle Scholar
  85. Levine SN amp; Lewis WM (1987) A numerical model of nitrogen fixation and its application to Lake Valencia, Venezuela. Freshwater Biology 17: 265–274PubMedGoogle Scholar
  86. Lewis WM (1986) Losses of nitrogen and phosphorus from a nutrient-poor moist tropical forest. Ecology 67: 1275–1282Google Scholar
  87. Likens GE, Bormann FH, Pierce RS, Eaton JS amp; Johnson NM (1977) Biogeochemistry of a forested ecosystem. Springer-Verlag, New York. 146 ppGoogle Scholar
  88. Littler MM, Littler DS amp; Lapointe BE (1988) A comparison of nutrient- and light-limited photosynthesis in psammophytic versus epilithic forms of Halimeda (Caulerpales, Halimedacae) from the Bahamas. Coral Reefs 6: 219–225Google Scholar
  89. Lobert JM, Scharffe DH, Hao WM amp; Crutzen PJ (1990) Importance of biomass burning in the atmosphere budget of nitrogen-containing trace gases. Nature 346: 552–554Google Scholar
  90. Marino R, Howarth RW, Shamess J amp; Prepas E (1990) Molybdenum and sulfate as controls on the abundance of nitrogen-fixing cyanobacteria in a saline lakes in Alberta. Limnol. Oceanogr. 35: 245–259Google Scholar
  91. Marrs RH, Roberts RD, Skeffington RA amp; Bradshaw AD (1983) Nitrogen and the development of ecosystems. In: Lee JA, McNeill S amp; Revison IH (Eds) Nitrogen as an Ecological Factor (pp 113–136). Blackwell Scientific, OxfordGoogle Scholar
  92. Martin JH amp; Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the northeast Pacific subarctic. Nature 331: 341–343Google Scholar
  93. Martin JH, Gordon RM, Fitzwater S amp; Broenkow WW (1989) VERTEX: Phytoplankton/ iron studies in the Gulf of Alaska. Deep-Sea Res. 36: 649–680Google Scholar
  94. Martin, JH, Fitzwater SE amp; Gordon RN (1990) Iron deficiency limits phytoplankton growth in Antarctic waters. Global Biogeochem. Cycles 4: 5–12Google Scholar
  95. Matson PA amp; Boone RD (1984) Natural disturbance and nitrogen mineralization: waveform dieback of mountain hemlock in the Oregon Cascades. Ecology 65: 1511–1516Google Scholar
  96. Matson PA amp; Vitousek PM (1987) Cross-system comparison of soil nitrogen transformations and nitrous oxide fluxes in tropical forests. Global Biogeochem. Cycles 1: 163–170Google Scholar
  97. Matson PA, Vitousek PM, Ewel JJ, Mazzarino MJ amp; Roberton GP (1987) Nitrogen transformation following tropical forest felling and burning on a volcanic soil. Ecology 68: 491–502Google Scholar
  98. McCarthy JJ amp; Carpenter EJ (1983) Nitrogen cycling in near-surface waters of the open ocean. In: Carpenter EM amp; Capone DG (Eds) Nitrogen in the Marine Environment (pp 487–512). Academic Press, New YorkGoogle Scholar
  99. McCarthy JJ amp; Goldman JC (1979) Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters. Science 203: 670–672Google Scholar
  100. McGill WB amp; Cole CV (1981) Comparative aspects of cycling of organic C, N, S, and P through soil organic matter. Geoderma 26: 267–286CrossRefGoogle Scholar
  101. McGlathery KJ, Howarth RW amp; Marino R (1991) Nutrient limitation of the macroalga, Penicillus capitatus, associated with subtropical seagrass meadows in Bermuda. Estuaries, in pressGoogle Scholar
  102. Melack JM, Kilham P amp; Fisher TR (1982) Responses of phytoplankton to experimental fertilization with ammonium and phosphate in an African soda lake. Oecologia 52: 321–326Google Scholar
  103. Melillo JM, Aber JD amp; Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63: 621–626Google Scholar
  104. Mellilo JM amp; Gosz JR (1983) Interactions of the biogeochemical cycles in forest ecosystems. In: Bolin B amp; Cook RB (Eds) The Major Biogeochemical Cycles and Their Interactions (pp 177–221). John Wiley and Sons, Chichester, EnglandGoogle Scholar
  105. Miller HG (1981) Forest fertilization: some guiding concepts. Forestry 54: 157–167Google Scholar
  106. Miller HG, Cooper JM amp; Miller JD (1976) Effects of nitrogen supply on nutrients in litterfall and crown leaching in a stand of Corsican pines. J. Appl. Ecol. 13: 233–248Google Scholar
  107. Mitchell HL amp; Chandler RF Jr (1939) The nutrition and growth of certain deciduous trees of northeastern United States. Black Rock For. Bull. 11: 1–94Google Scholar
  108. Morse JW, Zullig JJ, Bernstein LD, Millero FJ, Milne P, Mucci A amp; Choppin GR (1985) Chemistry of calcium carbonate-rich shallow water sediments in the Bahamas. Am. J. Sci. 285: 147–185Google Scholar
  109. Myers VB amp; Iverson RI (1981) Phosphorus and nitrogen limited phytoplankton productivity in northeastern Gulf of Mexico coastal lagoons. In: Neilson BJ amp; Cronin LE (Eds) Estuaries and Nutrients (pp 569–581). HumanaGoogle Scholar
  110. Nixon SW amp; Pilson MEQ (1983) Nitrogen in estuarine and coastal marine ecosystems. In: Carpenter EM amp; Capone DG (Eds) Nitrogen in the Marine Environment (pp 565–648). Academic Press, New YorkGoogle Scholar
  111. Nixon SW, Kelly JR, Furnas BN, Oviatt CA amp; Hale SS (1980) Phosphorus regeneration and the metabolism of coastal marine bottom communities. In: Tenore DR amp; Coull BC (Eds) Marine Benthic Dynamics (pp 219–242). Univ South CarolinaGoogle Scholar
  112. Norin LL (1977)14C-bioassays with the natural phytoplankton in the Stockholm archipelago. Ambio. Spec. Report 5: 15–21Google Scholar
  113. Ojima DS (1987) The short-term and long-term effect of burning on tallgrass prairie ecosystem properties and dynamics. PhD Diss., Colorado State UniversityGoogle Scholar
  114. Paerl HW (1985) Microzone formation: Its role in the enhancement of aquatic N2 fixation. Limnol. amp; Oceanogr. 30: 1246–1252Google Scholar
  115. Paerl HW amp; Prufert LE (1987) Oxygen-poor microzones as potential sites of microbial N2 fixation in nitrogen-depleted aerobic marine waters. Appl. Env. Micro. 53: 1078–1087Google Scholar
  116. Paerl HW, Crocker KM amp; Prufert LE (1987) Limitation of N2 fixation in coastal marine waters: Relative importance of molybdenum, iron, phosphorus, and organic matter availability. Limnol. Oceanogr. 32: 525–536Google Scholar
  117. Paerl HW amp; Carlton RC (1988) Control of nitrogen fixation by oxygen depletion in surface-associated microzones. Nature 332: 260–262Google Scholar
  118. Parton WF, Cole CV, Stewart JWB, Ojima DS amp; Schimel DS (1988) Dynamics of C, N, P, and S in soils: a model. Biogeochemistry 5: 109–131Google Scholar
  119. Pastor J amp; Post WM (1986) Influence of climate, soil moisture, and succession on forest carbon and nitrogen cycles. Biogeochemistry 2: 3–27Google Scholar
  120. Pastor J amp; Post WM (1988) Response of northern forests to CO2-induced climate change. Nature 334: 55–58Google Scholar
  121. Pastor JJ, Aber JD, McClaugherty CA amp; Melillo JM (1984) Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65: 256–268Google Scholar
  122. Peng T-H amp; Broecker WS (1991) Dynamical limitations on the Antarctic iron fertilization strategy. Nature 349: 227–229Google Scholar
  123. Peterjohn WT amp; Schlesinger WH (1990) Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10: 67–79Google Scholar
  124. Peterson BJ amp; Melillo JM (1985) The potential storage of carbon caused by eutrophication of the biosphere. Tellus 37B: 117–127Google Scholar
  125. Pickett STA amp; White PS (Eds) (1985) The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, Orlando. 472 ppGoogle Scholar
  126. Powell GVN, Kenworthy WJ amp; Fourqurean JF (1989) Experimental evidence for nutrient limitation of seagrass growth in a tropical estuary with restricted circulation. Bull. Mar. 44: 324–340Google Scholar
  127. Raison RJ (1979) Modification of the soil environment by vegetation fires, with particular reference to nitrogen transformations: a review. Plant Soil 51: 73–108Google Scholar
  128. Redfield AC (1958) The biological control of chemical factors in the environment. Am. Scientist 46: 206–226Google Scholar
  129. Reiers WS (1981) Nitrogen cycling in relation to ecosystem succession: a review. Ecol. Bull. (Stockholm) 33: 507–528Google Scholar
  130. Reiners WS (1986) Complementary models for ecosystems. Am Nat 127: 59–73Google Scholar
  131. Roskoski JP (1980) Nitrogen fixation in hardwood forests of the northeastern United States. Plant Soil 54: 33–44Google Scholar
  132. Rowe GT, Clifford CH, Smith KL amp; Hampton PL (1975) Benthic nutrient regeneration and its coupling to primary productivity in coastal waters. Nature 225: 215–217Google Scholar
  133. Rueter JG (1982) Theoretical Fe Limitations of microbial N2 fixation in the oceans. EOS 63: 945Google Scholar
  134. Ryther JH amp; Dunstan WN (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171: 1008–1013Google Scholar
  135. Schelske CL, Fahnenstiel GL amp; Haiback M (1986) Phosphorus enrichment, silica utilization, and biogeochemical silica depletion in the Great Lakes. Can. J. Fish. Aquat. Sci. 43: 407–415Google Scholar
  136. Schimel DS, Parton WJ, Cole CV, Ojima DS amp; Kittel TGF (1990) Grassland biogeochemistry: Links to atmospheric processes. Climatic Change 17: 13–25Google Scholar
  137. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260–262Google Scholar
  138. Schindler DW (1981) Interrelationships between the cycles of elements in freshwater ecosystems. In: Likens GE (Ed) Some Perspectives of the Major Biogeochemical Cycles (pp 113–123). John Wiley and Sons, Chichester, U.K.Google Scholar
  139. Schindler DW, Fee EJ amp; Ruszczynski T (1978) Phosphorus input and its consequences for phytoplankton standing crop and production in the Experimental Lakes Area and similar lakes. J. Fish. Res. Bd. Can. 35: 190–196Google Scholar
  140. Schindler DW, Hesslein R amp; Kipphut G (1977) Interactions between sediments and overlying waters in an experimentally eutrophied Pre-Cambrian shield lake. In: Gotterman HL (Ed) Interactions Between Sediments and Fresh Water (pp 235–245). Junk, The HagueGoogle Scholar
  141. Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance. Limnol. Oceanogr. 33: 702–724Google Scholar
  142. Seitzinger SP, Nixon SW amp; Pilson MEQ (1984) Denitrification and nitrous oxide production in a coastal marine ecosystem. Limnol. Oceanogr. 29: 79–83Google Scholar
  143. Shaver GR amp; Chapin FS III (1980) Response to fertilization by various plant growth forms in an Alaskan tundra: nutrient accumulation and growth. Ecology 61: 662–675Google Scholar
  144. Short FT, Davis MW, Gibson RA amp; Zimmerman CF (1985) Evidence for phosphorus limitation in carbonate sediments of the seagrass Syringodium filiforme. Est. Coast. Shelf. Sci. 20: 419–430Google Scholar
  145. Short FT, Dennison WC amp; Cappone DG (1990) Phosphorus-limited growth of the tropical seagrass Syringodium filiforme in carbonate sediments. Mar. Ecol. Prog. Ser. 62: 169–174Google Scholar
  146. Silvester WB (1983) Analysis of nitrogen fixation. In: Gordon JC amp; Wheeler CT (Eds) Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications (pp 173–212). Nijhoff/Junk Publishers, The HagueGoogle Scholar
  147. Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen fixation in forests of Pacific Northwest America. Soil Biol. Biochem. 21: 283–289Google Scholar
  148. Smith SV (1984) Phosphorus versus nitrogen limitation in the marine environment. Limnol. Oceanogr. 29: 1149–1160Google Scholar
  149. Smith SV amp; Atkinson MJ (1984) Phosphorus limitation of net production in a confined aquatic ecosystem. Nature 307: 626–627Google Scholar
  150. Smith SV, Hollibaugh JT, Dollar SJ amp; Vink S (1989) Tomales Bay, California: A case for carbon-controlled nitrogen cycling. Limnol. Oceanogr. 34: 37–52Google Scholar
  151. Smith SV, Kimmer WJ amp; Walsh TW (1986) Vertical flux and biogeochemical turnover regulate nutrient limitation of net organic production in the North Pacific Gyre. Limnol. Oceanogr. 31: 161–166Google Scholar
  152. Smith VH (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221: 669–671Google Scholar
  153. Smith VH (1991) Nitrogen, phosphorus, and nitrogen fixation in lacustrine and estuarine ecosystems. Limnol. Oceanogr., in pressGoogle Scholar
  154. Sollins P (1989) Factors affecting nutrient cycling in tropical soils. In: Proctor J (Ed) Mineral Nutrients in Tropical Forest and Savanna Ecosystems (pp 85–95) Blackwell Scientific, OxfordGoogle Scholar
  155. Sollins P, Robertson GP amp; Uehara G (1988) Nutrient mobility in variable- and permanent-charge soils. Biogeochemistry 6: 181–199Google Scholar
  156. Stevens PR amp; Walker TW (1970) The chronosequence concept and soil formation. Quart. Rev. Biol. 45: 333–350Google Scholar
  157. Swank WT, Waide JB, Crossley DA amp; Todd RL (1981) Insect defoliation enhances nitrate export from forested ecosystems. Oecologia 51: 297–299Google Scholar
  158. Tanner EVJ, Kapos V, Freskos S, Healey JR amp; Theobald AN (1989) Nitrogen and phosphorus fertilization of Jamaican montane forest trees. J. Trop. Ecol. 6: 231–238Google Scholar
  159. Tans PO, Fung IN amp; Takahashi T (1990) Observational constraints on the global atmospheric CO2 budget. Science 247: 1431–1439Google Scholar
  160. Thomas WH (1966) Surface nitrogenous nutrients and phytoplankton in the northeastern tropical Pacific Ocean. Limnol. Oceanogr. 11: 393–400Google Scholar
  161. Tiessen H, Stewart JWB amp; Moir JO (1983) Changes in organic and inorganic phosphate in particle size fractions of two soils during 60 to 90 years cultivation. J. Soil. Science 34: 815–823Google Scholar
  162. Tilman D (1986) Nitrogen-limited growth in plants from different successional stages. Ecology 67: 555–563Google Scholar
  163. Tilman D (1988) Plant Strategies and the Dynamics and Structure of Plant Communities. Princeton University Press, Princeton. 360 ppGoogle Scholar
  164. Tilman D, Kilham SS amp; Kilham P (1982) Phytoplankton community ecology: The role of limiting nutrients. Ann. Rev. Ecol. Syst. 13: 349–372Google Scholar
  165. Tilman D, Kiesling R, Sterner R, Kilham SS amp; Johnson FA (1986) Green, blue-green, and diatom algae: Taxonomic differences in competitive ability for phosphorus, silicon, and nitrogen. Arch. Hydrobiol. 106: 473–485Google Scholar
  166. Uehara G amp; Gillman G (1981) The mineralogy, chemistry, and physics of tropical soils with variable charge clays. Westview Press, Boulder, ColoradoGoogle Scholar
  167. Valiela I (1983) Nitrogen in salt-marsh ecosystems. In: Carpenter EM amp; Capone DG (Eds) Nitrogen in the Marine Environment (pp 349–678). Academic Press, New YorkGoogle Scholar
  168. Valiela I (1984) Marine Ecological Processes. New York: Springer-Verlag. 546 ppGoogle Scholar
  169. van Breman H amp; de Wit CT (1983) Rangeland productivity and exploitation in the Sabel. Science 221: 1341–1347Google Scholar
  170. Van Cleve K amp; Zasada J (1976) Response of 70-yr-old white spruce to thinning and fertilization in interior Alaska. Can. J. For. Res. 6: 145–152Google Scholar
  171. Van Cleve K, Oliver L, Schlentner R, Viereck LA amp; Dyrness CT (1983) Productivity and nutrient cycling in taiga forest ecosystems. Can. J. For. Res. 13: 747–766Google Scholar
  172. Vince S amp; Valiela I (1973) The effects of ammonium and phosphate enrichments on chlorophyll a, pigment ratio and species composition of phytoplankton of Vineyard Sound. Mar. Biol. 19: 69–73Google Scholar
  173. Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am. Nat. 119: 553–572Google Scholar
  174. Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65: 285–298Google Scholar
  175. Vitousek PM amp; Matson PA (1985) Disturbance, nitrogen availability, and nitrogen losses in an intensively managed loblolly pine plantation. Ecology 66: 1360–1376Google Scholar
  176. Vitousek PM amp; Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. BioScience 25: 376–381Google Scholar
  177. Vitousek PM amp; Sanford RL Jr (1986) Nutrient cycling in moist tropical forest. Ann. Rev. Ecol. Syst. 17: 137–167Google Scholar
  178. Vitousek PM amp; Walker LR (1987) Colonization, succession, and resource availability; ecosystem-level interactions. In: Gray A, Crawley M amp; Edwards PJ (Eds) Colonization, Succession and Stability (pp 207–223). Blackwell Scientific, OxfordGoogle Scholar
  179. Vitousek PM, Gosz JR, Grier CC, Melillo JM amp; Reiners WA (1982) A comparative analysis of potential nitrification and nitrate mobility in forest ecosystems. Ecol. Monogr. 52: 155–177Google Scholar
  180. Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D amp; Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238: 802–804Google Scholar
  181. Vitousek PM, Fahey T, Johnson DW amp; Swift MJ (1988) Element interactions in forest ecosystems: succession, allometry, and input-output budgets. Biogechemistry 5: 7–34Google Scholar
  182. Vitousek PM, Matson PA amp; Van Cleve K (1989) Nitrogen availability and nitrification during succession: Primary, secondary, and old-field seres. Plant Soil 115: 229–239Google Scholar
  183. Vollenwieder RA (1976) Advances in defining critical loading levels for phosphorus in lake eutrophication. Mem. 1st Ital. Idrobiol. Dott. Macro. de marchi 33: 53–83Google Scholar
  184. Walbridge MR (1991) Phosphorus availability in acid organic soils of the lower North Carolina coastal plain: Estimation and control of P availability and plant response. Ecology, in pressGoogle Scholar
  185. Walker TW amp; Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15: 1–19CrossRefGoogle Scholar
  186. Wood T, Bormann FH amp; Voight GK (1984) Phosphorus cycling in a northern hardwood forest: Biological and chemical control. Science 223: 391–393Google Scholar
  187. Wurtsbaugh WA (1988) Iron, molybdenum and phosphorus limitation of N2 fixation maintains nitrogen deficiency of plankton in the Great Salt Lake drainage (Utah, USA). Verb. Internat. Verein. Limnol. 23: 121–130Google Scholar
  188. Zak DR, Host GE amp; Pregitzer KS (1989) Regional variability in nitrogen mineralization, nitrification, and overstory biomass in northern lower Michigan. Can. J. Forest. Res. 19: 1521–1526Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • Peter M. Vitousek
    • 1
  • Robert W. Howarth
    • 2
  1. 1.Department of biological SciencesStanford UniversityStanfordUSA
  2. 2.Section of Ecology and SystematicsCornell UniversityIthacaUSA

Personalised recommendations