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

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Abstract

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.

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References

  • Aber JD, Nadelhoffer JK, Steudler PA amp; Melillo JM (1989) Nitrogen saturation in northern forest ecosystems — hypotheses and implications. BioScience 39: 378–386

    Google Scholar 

  • Agren GI (1983) Nitrogen productivity of some conifers. Can J Forest Res 13: 494–500

    Google Scholar 

  • Alexander M (1977) An Introduction to Soil Microbiology. John Wiley and Sons, New York

    Google Scholar 

  • Atkinson MJ amp; Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol. Oceanogr. 26: 1074–1083

    Google Scholar 

  • Banse K (1990) Does iron really limit phytoplankton production in the offshore subarctic Pacific? Limnol. Oceanogr. 35: 772–775

    Google Scholar 

  • Bhella HS amp; Dawson MD (1972) The use of anion exchange resin for determining available soil molybdenum. Soil Sci. Soc. Amer. Proc. 36: 177–178

    Google Scholar 

  • Binkley D (1986) Forest Nutrition Management: John Wiley and Sons, New York. 299 pp

    Google Scholar 

  • Birk EM amp; Vitousek PM (1984) Patterns of N retranslocation in loblolly pine: response to N availability. Ecol. Soc. Amer. Bull. 65: 100

    Google Scholar 

  • Bliss LC (1963) Alpine plant communities of the Presidential Range, New Hampshire. Ecology 44: 678–697

    Google Scholar 

  • Bonan GB (1990) Carbon and nitrogen cycling in North American boreal forests. II. Biogeographic patterns. Can. J. Forest Res. 20: 1077–1088

    Google Scholar 

  • 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: 119–159

    Google Scholar 

  • Bormann BT amp; Gordon JC (1984) Stand density effects in yound red alder planations: productivity, photosynthate partitioning, and nitrogen fixation. Ecology 65: 394–402

    Google Scholar 

  • Bormann FH amp; Likens GE (1979) Pattern and Process in a Forested Ecosystem. Springer-Verlag, NY. 253 pp

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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: 631–637

    Google Scholar 

  • 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: 665–676

    Google Scholar 

  • Broecker WS (1982) Glacial to interglacial changes in ocean chemistry. Prog. Oceanogr. 2: 151–197

    Google Scholar 

  • 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: 846–854

    Google Scholar 

  • Caraco N, Cole JJ amp; Likens GE (1989) Evidence for sulfate-controlled phosphorus release from sediments of aquatic systems. Nature 341: 316–318

    Google Scholar 

  • Caraco N, Cole JJ amp; Likens GE (1990) A comparison of phosphorus immobilization in sediments of freshwater and coastal marine systems. Biogeochemistry 9: 277–290

    Google Scholar 

  • 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 York

    Google Scholar 

  • Carpenter EJ amp; Capone DG (Ed) (1983) Nitrogen in the Marine Environment. Academic Press, New York. 900 pp

  • Carpenter EJ amp; Price CC (1976) Marine Oscillatoria (Trichodesmium): Explanation for aerobic nitrogen fixation without heterocysts. Science 191: 1278–1280

    Google Scholar 

  • Chapin FS III, Vitousek PM amp; Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am. Nat. 127: 48–58

    Google Scholar 

  • Coats RN, Leonard RL amp; Goldman CR (1976) Nitrogen uptake and release in a forested watershed, Lake Tahoe Basin, California. Ecology 57: 995–1004

    Google Scholar 

  • Cole CV amp; Heil RD (1981) Phosphorus effects on terrestrial nitrogen cycling. Ecol. Bull. (Stockholm) 33: 363–374

    Google Scholar 

  • 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, Dordrecht

    Google Scholar 

  • Cornaby BW amp; Waide JB (1973) Nitrogen fixation in decaying chestnut logs. Plant Soil 39: 445–448

    Google Scholar 

  • 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: 89

    Google Scholar 

  • Crutzen PJ amp; Andreae MO Biomass burning in the tropics: impact on atmospheric chemistry and biogeochemical cycles. Science 250: 1669–1678

  • 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: 466–472

    Google Scholar 

  • Cuevas E amp; Medina E (1988) Nutrient dynamics within Amazonian forests. II. Fine root growth, nutrient availability, and leaf litter decomposition. Oecologia 76: 222–235

    Google Scholar 

  • 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: 397–406

    Google Scholar 

  • 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, Corvallis

    Google Scholar 

  • 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 Hague

    Google Scholar 

  • 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 York

    Google Scholar 

  • Doremus C (1982) Geochemical control of dinitrogen fixation in the open ocean. Biol. Oceanogr. 1: 429–436

    Google Scholar 

  • Dugdale RC amp; Wilkerson FP (1990) Iron addition experiments in the Antarctic: a reanalysis. Global Biogeochemical Cycles 4: 13–19

    Google Scholar 

  • Edmondson WT (1970) Phosphorus, nitrogen, and algae in Lake Washington after diversion of sewage. Science 169: 690–691

    Google Scholar 

  • Eisele KA, Schimel DS, Kapustka LA amp; Parton WJ (1989) Fire-stimulated N2 fixation as a result of altered N:P ratios. Oecologia 79: 471–464

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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, England

    Google Scholar 

  • 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: 387–395

    Google Scholar 

  • 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: 795–817

    Google Scholar 

  • Flett RJ, Schindler DW, Hamilton RD amp; Campbell NER (1980) Nitrogen fixation in Canadian Precambrian Shield lakes. Can. J. Fish. Aquat. Sci. 37: 494–505

    Google Scholar 

  • 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): 1100

    Google Scholar 

  • 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: 114–127

    Google Scholar 

  • Goldman CR (1988) Primary productivity, nutrients, and transparency during the early onset of eutrophication in ultra-oligotrophic Lake Tahoe. California-Nevada. Limnol. Oceanogr. 33: 1321–1333

    Google Scholar 

  • 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: 53–88

    Google Scholar 

  • Graneli E (1978) Algal assay of limiting nutrients for phytoplankton production in the Oresund. Vatten 2: 117–128

    Google Scholar 

  • Graneli E (1981) Bioassay experiments in the Falsterbo channel — nutrients added daily. Kieler Meeresforch., Sonderh. 5: 82–90

    Google Scholar 

  • Graneli E (1984) Algal growth potential and limiting nutrients for phytoplankton production in Oresund water of Baltic and Kattegat origin. Limnologica (Berlin) 15: 563–569

    Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. Am. Nat. 118: 607–637

    Google Scholar 

  • Gutschick VP (1987) A Functional Biology of Crop Plants. Timber Press, Portland. 230 pp

    Google Scholar 

  • 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 pp

  • 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: 214–218

    Google Scholar 

  • 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: 796–822

    Google Scholar 

  • Hines ME amp; Lyons WB (1982) Biogeochemistry of nearshore Bermuda sediments. I. Sulfate reduction rates and nutrient regeneration. Mar. Ecol. Progr. Ser. 8: 87–94

    Google Scholar 

  • 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: 402–405

    Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Ann. Rev. Ecol. Syst. 19: 89–110

    Google Scholar 

  • Howarth RW amp; Cole JJ (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229: 653–655

    Google Scholar 

  • 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, 1990

  • 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: 669–687

    Google Scholar 

  • Howarth, RW, Marino R amp; Cole JJ (1988b) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33: 688–701

    Google Scholar 

  • 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: 478–491

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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: 1009–1016

    Google Scholar 

  • Jackson GA amp; Williams PM (1985) Importance of dissolved organic nitrogen and phosphorus to biological nutrient cycling. Deep-Sea Res. 32: 223–235

    Google Scholar 

  • Jarrell WM amp; Dawson MD (1978) Sorption and availability of molybdenum in soils of Western Oregon. Soil. Sci. Soc. Amer. J. 42: 412–415

    Google Scholar 

  • Jordan CF (1985) Nutrient Cycling in Tropical Forest Ecosystems: Principles and Their Application in Conservation and Management. John Wiley and Sons, Chichester, England. 179 pp

    Google Scholar 

  • 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: 218–237

    Google Scholar 

  • Keller M, Kaplan WA amp; Wofsy SC (1986) Emissions of N2O, CH4, and CO2 from tropical soils. J. Geophys. Res. 91: 11,791–11,801

    Google Scholar 

  • 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). Reidel

  • Khalid RA, Patrick WH amp; DeLaune RD (1977) Phosphorus sorption characteristics of flooded soils. Soil. Sci. Soc. Am. J. 41: 305

    Google Scholar 

  • Kimmins JP (1987) Forest Ecology. Macmillian Publishing, New York. 531 pp

    Google Scholar 

  • Kinjo T amp; Pratt PF (1971) Nitrate adsorption. II. In competition with chloride, sulfate, and phosphate. Soil. Sci. Soc. Amer. Proc. 35: 725–728

    Google Scholar 

  • 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: 97–108

    Google Scholar 

  • Knowles R (1982) Denitrification. Microbiol. Rev. 46: 43–70

    Google Scholar 

  • Krom MD amp; Berner RA (1980) Adsorption of phosphate in anoxic marine sediments. Limnol. Oceanogr. 25: 797–806

    Google Scholar 

  • 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: 243–255

    Google Scholar 

  • 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, Oxford

    Google Scholar 

  • 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, Colorado

    Google Scholar 

  • Levine SN amp; Lewis WM (1987) A numerical model of nitrogen fixation and its application to Lake Valencia, Venezuela. Freshwater Biology 17: 265–274

    CAS  PubMed  Google Scholar 

  • Lewis WM (1986) Losses of nitrogen and phosphorus from a nutrient-poor moist tropical forest. Ecology 67: 1275–1282

    Google Scholar 

  • Likens GE, Bormann FH, Pierce RS, Eaton JS amp; Johnson NM (1977) Biogeochemistry of a forested ecosystem. Springer-Verlag, New York. 146 pp

    Google Scholar 

  • 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: 219–225

    Google Scholar 

  • 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: 552–554

    Google Scholar 

  • 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: 245–259

    Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Martin JH amp; Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the northeast Pacific subarctic. Nature 331: 341–343

    Google Scholar 

  • Martin JH, Gordon RM, Fitzwater S amp; Broenkow WW (1989) VERTEX: Phytoplankton/ iron studies in the Gulf of Alaska. Deep-Sea Res. 36: 649–680

    Google Scholar 

  • Martin, JH, Fitzwater SE amp; Gordon RN (1990) Iron deficiency limits phytoplankton growth in Antarctic waters. Global Biogeochem. Cycles 4: 5–12

    Google Scholar 

  • Matson PA amp; Boone RD (1984) Natural disturbance and nitrogen mineralization: waveform dieback of mountain hemlock in the Oregon Cascades. Ecology 65: 1511–1516

    Google Scholar 

  • Matson PA amp; Vitousek PM (1987) Cross-system comparison of soil nitrogen transformations and nitrous oxide fluxes in tropical forests. Global Biogeochem. Cycles 1: 163–170

    Google Scholar 

  • 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: 491–502

    Google Scholar 

  • 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 York

    Google Scholar 

  • McCarthy JJ amp; Goldman JC (1979) Nitrogenous nutrition of marine phytoplankton in nutrient-depleted waters. Science 203: 670–672

    Google Scholar 

  • McGill WB amp; Cole CV (1981) Comparative aspects of cycling of organic C, N, S, and P through soil organic matter. Geoderma 26: 267–286

    Article  Google Scholar 

  • McGlathery KJ, Howarth RW amp; Marino R (1991) Nutrient limitation of the macroalga, Penicillus capitatus, associated with subtropical seagrass meadows in Bermuda. Estuaries, in press

  • 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: 321–326

    Google Scholar 

  • Melillo JM, Aber JD amp; Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63: 621–626

    CAS  Google Scholar 

  • 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, England

    Google Scholar 

  • Miller HG (1981) Forest fertilization: some guiding concepts. Forestry 54: 157–167

    Google Scholar 

  • 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: 233–248

    Google Scholar 

  • Mitchell HL amp; Chandler RF Jr (1939) The nutrition and growth of certain deciduous trees of northeastern United States. Black Rock For. Bull. 11: 1–94

    Google Scholar 

  • 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: 147–185

    Google Scholar 

  • 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). Humana

  • 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 York

  • 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 Carolina

  • Norin LL (1977)14C-bioassays with the natural phytoplankton in the Stockholm archipelago. Ambio. Spec. Report 5: 15–21

    Google Scholar 

  • Ojima DS (1987) The short-term and long-term effect of burning on tallgrass prairie ecosystem properties and dynamics. PhD Diss., Colorado State University

  • Paerl HW (1985) Microzone formation: Its role in the enhancement of aquatic N2 fixation. Limnol. amp; Oceanogr. 30: 1246–1252

    Google Scholar 

  • 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: 1078–1087

    Google Scholar 

  • 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: 525–536

    Google Scholar 

  • Paerl HW amp; Carlton RC (1988) Control of nitrogen fixation by oxygen depletion in surface-associated microzones. Nature 332: 260–262

    Google Scholar 

  • 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: 109–131

    CAS  Google Scholar 

  • Pastor J amp; Post WM (1986) Influence of climate, soil moisture, and succession on forest carbon and nitrogen cycles. Biogeochemistry 2: 3–27

    Google Scholar 

  • Pastor J amp; Post WM (1988) Response of northern forests to CO2-induced climate change. Nature 334: 55–58

    Google Scholar 

  • 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: 256–268

    Google Scholar 

  • Peng T-H amp; Broecker WS (1991) Dynamical limitations on the Antarctic iron fertilization strategy. Nature 349: 227–229

    Google Scholar 

  • Peterjohn WT amp; Schlesinger WH (1990) Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10: 67–79

    Google Scholar 

  • Peterson BJ amp; Melillo JM (1985) The potential storage of carbon caused by eutrophication of the biosphere. Tellus 37B: 117–127

    Google Scholar 

  • Pickett STA amp; White PS (Eds) (1985) The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, Orlando. 472 pp

  • 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: 324–340

    Google Scholar 

  • Raison RJ (1979) Modification of the soil environment by vegetation fires, with particular reference to nitrogen transformations: a review. Plant Soil 51: 73–108

    Google Scholar 

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am. Scientist 46: 206–226

    Google Scholar 

  • Reiers WS (1981) Nitrogen cycling in relation to ecosystem succession: a review. Ecol. Bull. (Stockholm) 33: 507–528

    Google Scholar 

  • Reiners WS (1986) Complementary models for ecosystems. Am Nat 127: 59–73

    Google Scholar 

  • Roskoski JP (1980) Nitrogen fixation in hardwood forests of the northeastern United States. Plant Soil 54: 33–44

    Google Scholar 

  • Rowe GT, Clifford CH, Smith KL amp; Hampton PL (1975) Benthic nutrient regeneration and its coupling to primary productivity in coastal waters. Nature 225: 215–217

    Google Scholar 

  • Rueter JG (1982) Theoretical Fe Limitations of microbial N2 fixation in the oceans. EOS 63: 945

    Google Scholar 

  • Ryther JH amp; Dunstan WN (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171: 1008–1013

    Google Scholar 

  • 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: 407–415

    Google Scholar 

  • Schimel DS, Parton WJ, Cole CV, Ojima DS amp; Kittel TGF (1990) Grassland biogeochemistry: Links to atmospheric processes. Climatic Change 17: 13–25

    Google Scholar 

  • Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260–262

    Google Scholar 

  • 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 

  • 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: 190–196

    Google Scholar 

  • 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 Hague

    Google Scholar 

  • Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance. Limnol. Oceanogr. 33: 702–724

    Google Scholar 

  • Seitzinger SP, Nixon SW amp; Pilson MEQ (1984) Denitrification and nitrous oxide production in a coastal marine ecosystem. Limnol. Oceanogr. 29: 79–83

    Google Scholar 

  • 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: 662–675

    Google Scholar 

  • 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: 419–430

    Google Scholar 

  • 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: 169–174

    Google Scholar 

  • 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 Hague

    Google Scholar 

  • Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen fixation in forests of Pacific Northwest America. Soil Biol. Biochem. 21: 283–289

    Google Scholar 

  • Smith SV (1984) Phosphorus versus nitrogen limitation in the marine environment. Limnol. Oceanogr. 29: 1149–1160

    Google Scholar 

  • Smith SV amp; Atkinson MJ (1984) Phosphorus limitation of net production in a confined aquatic ecosystem. Nature 307: 626–627

    Google Scholar 

  • Smith SV, Hollibaugh JT, Dollar SJ amp; Vink S (1989) Tomales Bay, California: A case for carbon-controlled nitrogen cycling. Limnol. Oceanogr. 34: 37–52

    Google Scholar 

  • 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: 161–166

    Google Scholar 

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

    Google Scholar 

  • Smith VH (1991) Nitrogen, phosphorus, and nitrogen fixation in lacustrine and estuarine ecosystems. Limnol. Oceanogr., in press

  • 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, Oxford

    Google Scholar 

  • Sollins P, Robertson GP amp; Uehara G (1988) Nutrient mobility in variable- and permanent-charge soils. Biogeochemistry 6: 181–199

    Google Scholar 

  • Stevens PR amp; Walker TW (1970) The chronosequence concept and soil formation. Quart. Rev. Biol. 45: 333–350

    Google Scholar 

  • Swank WT, Waide JB, Crossley DA amp; Todd RL (1981) Insect defoliation enhances nitrate export from forested ecosystems. Oecologia 51: 297–299

    Google Scholar 

  • 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: 231–238

    Google Scholar 

  • Tans PO, Fung IN amp; Takahashi T (1990) Observational constraints on the global atmospheric CO2 budget. Science 247: 1431–1439

    CAS  Google Scholar 

  • Thomas WH (1966) Surface nitrogenous nutrients and phytoplankton in the northeastern tropical Pacific Ocean. Limnol. Oceanogr. 11: 393–400

    Google Scholar 

  • 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: 815–823

    Google Scholar 

  • Tilman D (1986) Nitrogen-limited growth in plants from different successional stages. Ecology 67: 555–563

    Google Scholar 

  • Tilman D (1988) Plant Strategies and the Dynamics and Structure of Plant Communities. Princeton University Press, Princeton. 360 pp

    Google Scholar 

  • Tilman D, Kilham SS amp; Kilham P (1982) Phytoplankton community ecology: The role of limiting nutrients. Ann. Rev. Ecol. Syst. 13: 349–372

    Google Scholar 

  • 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: 473–485

    Google Scholar 

  • Uehara G amp; Gillman G (1981) The mineralogy, chemistry, and physics of tropical soils with variable charge clays. Westview Press, Boulder, Colorado

    Google Scholar 

  • 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 York

    Google Scholar 

  • Valiela I (1984) Marine Ecological Processes. New York: Springer-Verlag. 546 pp

    Google Scholar 

  • van Breman H amp; de Wit CT (1983) Rangeland productivity and exploitation in the Sabel. Science 221: 1341–1347

    Google Scholar 

  • 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: 145–152

    Google Scholar 

  • 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: 747–766

    Google Scholar 

  • 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: 69–73

    Google Scholar 

  • Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am. Nat. 119: 553–572

    Google Scholar 

  • Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65: 285–298

    CAS  Google Scholar 

  • Vitousek PM amp; Matson PA (1985) Disturbance, nitrogen availability, and nitrogen losses in an intensively managed loblolly pine plantation. Ecology 66: 1360–1376

    Google Scholar 

  • Vitousek PM amp; Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. BioScience 25: 376–381

    CAS  Google Scholar 

  • Vitousek PM amp; Sanford RL Jr (1986) Nutrient cycling in moist tropical forest. Ann. Rev. Ecol. Syst. 17: 137–167

    Google Scholar 

  • 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, Oxford

    Google Scholar 

  • 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: 155–177

    Google Scholar 

  • 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: 802–804

    Google Scholar 

  • Vitousek PM, Fahey T, Johnson DW amp; Swift MJ (1988) Element interactions in forest ecosystems: succession, allometry, and input-output budgets. Biogechemistry 5: 7–34

    Google Scholar 

  • Vitousek PM, Matson PA amp; Van Cleve K (1989) Nitrogen availability and nitrification during succession: Primary, secondary, and old-field seres. Plant Soil 115: 229–239

    Google Scholar 

  • Vollenwieder RA (1976) Advances in defining critical loading levels for phosphorus in lake eutrophication. Mem. 1st Ital. Idrobiol. Dott. Macro. de marchi 33: 53–83

    Google Scholar 

  • 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 press

  • Walker TW amp; Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15: 1–19

    Article  CAS  Google Scholar 

  • Wood T, Bormann FH amp; Voight GK (1984) Phosphorus cycling in a northern hardwood forest: Biological and chemical control. Science 223: 391–393

    CAS  Google Scholar 

  • 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: 121–130

    Google Scholar 

  • 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: 1521–1526

    Google Scholar 

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  1. Department of biological Sciences, Stanford University, Stanford, CA, 94305, USA

    Peter M. Vitousek

  2. Section of Ecology and Systematics, Cornell University, Ithaca, NY, 14853, USA

    Robert W. Howarth

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Vitousek, P.M., Howarth, R.W. Nitrogen limitation on land and in the sea: How can it occur?. Biogeochemistry 13, 87–115 (1991). https://doi.org/10.1007/BF00002772

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