Abstract
N limitation to primary production and other ecosystem processes is widespread. To understand the causes and distribution of N limitation, we must understand the controls of biological N fixation. The physiology of this process is reasonably well characterized, but our understanding of ecological controls is sparse, except in a few cultivated ecosystems. We review information on the ecological controls of N fixation in free-living cyanobacteria, vascular plant symbioses, and heterotrophic bacteria, with a view toward developing improved conceptual and simulation models of ecological controls of biological N fixation.
A model (Howarth et al. 1999) of cyanobacterial fixation in lakes (where N fixation generally increases substantially when N:P ratios are low) versus estuaries (where planktonic N fixation is rare regardless of N:P ratios) concludes that an interaction of trace-element limitation and zooplankton grazing could constrain cyanobacteria in estuaries and so sustain N limitation. Similarly. a model of symbiotic N fixation on land (Vitousek & Field 1999) suggests that shade intolerance, P limitation, and grazing on N-rich plant tissues could suppress symbiotic N fixers in late-successional forest ecosystems. This congruence of results raises the question – why do late-successional tropical forests often contain many potentially N-fixing canopy legumes, while N fixers are absent from most late-successional temperate and boreal forests? We suggest that relatively high N availability in lowland tropical forests permits legumes to maintain an N-demanding lifestyle (McKey 1994) without always being required to pay the costs of fixing N.
Overall, both the few simulation models and the more-numerous conceptual models of ecological controls of biological N fixation suggest that there are substantial common features across N-fixing organisms and ecosystems. Despite the many groups of organisms capable of fixing N, and the very different ecosystems in which the process is important, we suggest that these common controls provide a foundation for the development of regional and global models that incorporate ecological controls of biological N fixation.
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References
Aber JD, McDowell W, Nadelhoffer K, Magill A, Berntson G, KamakeaM, McNulty S, Currie W, Rustad L & Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems: hypothesis revisited. Bioscience 48: 921–934
Allen O & Allen E (1981) The Leguminosae: A Source Book of Characteristics, Uses, and Nodulation. University of Wisconsin Press, Madison, WI
Allen S, Raven JA & Sprent JI (1988) The role of long-distance transport in intracellular pH regulation in Phaseolus vulgaris grown with ammonium or nitrate as nitrogen source, or nodulated.J. Exp. Bot. 39: 513–528
Allos HF & Bartholomew WV (1959) Replacement of symbiotic fixation by available nitrogen. Soil Sci. 87: 61–66
Anderson DC, Harper KT & Holmgren RC (1982) Factors influencing development of cryptogamic soil crusts in Utah deserts. J.Range Manage. 35: 180–185
Arnone JA III & Gordon JC (1990) Effect of nodulation, nitrogen fixation and CO2 enrichment on the physiology, growth and dry mass allocation of seedlings of Alnus rubra Bong. New Phytol. 116: 55–66
Austin AT & Vitousek PM (1998) Nutrient dynamics on a precipitation gradient in Hawai'I. Oecologia 113: 519–529
Barber SA (1984) Soil Nutrient Bioavailability: A Mechanistic Approach. JohnWiley & Sons, New York
Bebout BM, Fitzpatrick MW & Paerl HW (1993) Identification of the sources of energy for nitrogen fixation and physiological characterization of nitrogen-fixing members of a marine microbial mat community.Appl. Environ. Microb. 59: 1495–1503
Bebout BM, Paerl HW, Crocker KM & Prufert LE (1987) Diel interactions of oxygenic photosynthesis and N2 fixation (acetylene reduction) in a marine microbial mat community. Appl. Environ. Microb. 53: 2353–2362
Belnap J, Harper KT & Warren SD (1994) Surface disturbance of cryptobiotic soil crusts: nitrogenase activity, chlorophyll content, and chlorophyll degradation. Arid Soil Res.Rehab. 3: 1–8
Bergmann MA & Welch HE (1990) Nitrogen fixation by epilithic periphyton in small arctic lakes in response to experimental nitrogen and phosphorus fertilization.Can. J. Fish. Aquat. Sci. 47: 1545–1550
Beymer RJ & Klopatek JM (1992) Effects of grazing on cryptogamic crusts in pinyon-juniper woodlands in Grand Canyon National Park. Am. Midl. Nat. 127: 139–148
Binkley D & Ryan M (1998) Net primary production and nutrient cycling in replicated stands of Eucalyptus saligna and Albizzia facultaria. Forest Ecol. Manag. 112: 79–85
Bloom AJ, Chapin FS III & Mooney HA (1985) Resource limitation in plants, an economic analogy. Annu. Rev. Ecol. Syst. 16: 363–392
Boring LR, Swank WT, Waide JB & Henderson GS (1988) Sources, fates, and impacts of nitrogen inputs to terrestrial ecosystem: review and synthesis. Biogeochemistry 6: 119–159
Campbell JL, Hornbeck JW, McDowell WH, Buso DC, Shaley JB & Likens GE (2000) Dissolved organic nitrogen budgets for upland, forested ecosystems in New England. Biogeochemistry 49: 123–142
Carpenter RC, Hackney JM & Adey WH (1991) Measurements of primary productivity and nitrogenase activity of coral reef algae in a chamber incorporating oscillatory flow. Limnol.Oceanogr. 36: 40–49
Cassman KG, Whitney AS & Stockinger (1980) Root growth and dry matter distribution of soybean as affected by phosphorus stress, nodulation and nitrogen source. Crop Sci. 20:239–244
Cassman KG, Singleton PW & Lindquist BA (1993) Input/output analysis of the cumulative soybean response to phosphorus on an Ultisol. Field Crop Res. 34: 23–36
Cassman KG, De Datta SK, Olk DC, Alcantara JM, Samson MI, Descalsota JP & Dizon MA (1995) Yield decline and the nitrogen economy of long-term experiments on continuous, irrigated rice systems in the tropics. In: Lal R & Stewart BA (Eds) Soil Management: Experimental Basis for Sustainability and Environmental Quality (pp 181–222). Lewis/CRC Publishers, Boca Raton
Chadwick OA, Derry LA, Vitousek PM, Huebert BJ & Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397: 491–497
Chapin DM, Bliss LC & Bledsoe LJ (1991) Environmental regulation of nitrogen fixation in a high arctic lowland ecosystem.Can. J. Bot. 69: 2744–2755
Chapin FS III, Bloom AJ, Field CB & Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37: 49–57
Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, VonFischer JC, Elseroad A & Wasson MF. (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochem. Cycles 13: 623–645
Coxson DS & Kershaw KA (1983) Rehydration response of nitrogenase activity and carbon fixation in terrestrial Nostoc commune from Stipa-Bouteloa grassland. Can. J. Bot. 61: 2658–2668
Crawford CS & Gosz JR (1982) Desert ecosystems: Their resources in space and time. Environ. Conserv. 9: 181–195
Crews TE (1993) Phosphorus regulation of nitrogen fixation in a traditional Mexican agroecosystem. Biogeochemistry 21: 141–166
Crews TE (1999) The presence of nitrogen fixing legumes in terrestrial communities: evolutionary versus ecological considerations. Biogeochemistry 46: 233–246
Crews TE, Kurina LM & Vitousek PM. Organic matter and nitrogen accumulation and nitrogen fixation during early ecosystem development in Hawaii. Biogeochemistry, in press.
Dart PJ & Pate JS (1959) Nodulation studies in legumes. III. The effects of delaying inoculation on the seedling symbiosis of barrel medic. Aust. J. Biol. Sci. 12: 427–456
Downs MR, Nadelhoffer KJ, Melillo JM & Aber JD (1996) Immobilization of a 15N-labelled nitrate addition by decomposing forest litter. Oecologia 105: 141–150
DuBois JD & Kapustka LA (1983) Biological nitrogen influx in an Ohio relict prairie. Am. J. Bot. 70: 8–16
Eisele KA, Schimel DS, Kapustka LA & Parton WJ (1989) Effects of available P and N:P ratios of non-symbiotic dinitrogen fixation in tallgrass prairie soils. Oecologia 79: 471–474
Eldridge DJ & Greene RSB (1994) Microbiotic soil crusts: A review of their roles in soil and ecological processes in the rangelands of Australia. Aust. J. Soil Res. 32: 389–415
Eskew D, Eaglesham AR & App AA (1981) Heterotrophic 15N2 fixation and distribution of newly fixed nitrogen in a rice-flooded soil system. Plant Physiol. 68: 48–52
Evans RD & Belnap J (1999) Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology 80: 150–160
Evans RD & Johansen JR (1999) Microbiotic crusts and ecosystem processes. Crit. Rev. Plant Sci. 18: 183–225
Evans RD & Ehleringer JR (1993) A break in the nitrogen cycle of arid lands: evidence from δ15N of soils. Oecologia 94: 314–317
Field CB, Chapin FS III, Matson PA & Mooney HA (1992) Responses of terrestrial ecosystems to the changing atmosphere: a resource-based approach. Annu. Rev. Ecol. Syst. 23: 201–235
Field CB, Behrenfeld MJ, Randerson JT & Falkowski P (1998) Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281: 237–240
Fritz-Sheridan RP & Coxson DS (1988) Nitrogen fixation on a tropical volcano, La Soufriere (Guadeloupe). Lichenologist 20: 63–81
Galloway, JN, Schlesinger WH, Levy H II, Michaels A & Schnoor JL (1995) Nitrogen fixation: atmospheric enhancement - environmental response. Global Biogeochem. Cycles 9: 235–252
Goosem S & Lamb D (1986) Measurements of phyllosphere nitrogen fixation in a tropical and two subtropical rain forests. J. Trop. Ecol. 2: 373–376
Graetz RD & Tongway DJ (1986) Influence of grazing management on vegetation, soil structure, nutrient distribution and the infiltration of applied rainfall in a semi-arid chenopod shrubland. Aust. J. Ecol. 11: 347–360
Grimm NB & Fisher SG (1989) Stability of periphyton and macroinvertebrates to disturbance by flash floods in a desert stream. J. N. Am. Benthol. Soc. 8: 293–307
Grimm NB & Petrone KC (1997) Nitrogen fixation in a desert stream ecosystem. Biogeochemistry 37: 33–61
Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. Am. Nat. 118: 607–637
Hall SJ & Matson PA (1999) Nitrogen oxide emissions after nitrogen additions in tropical forests. Nature 401: 152–155
Handley LL & Scrimgeour CM (1997) Terrestrial plant ecology and 15N natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish old field. Adv. Ecol. Res. 27: 133–212
Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S & Stewart GR (1999) The 15N natural abundance (δ 15N) of ecosystem samples reflects measures of water availability. Aust. J. Plant Physiol. 26: 185–199
Hartwig UA (1998) The regulation of symbiotic N2 fixation: A conceptual model of N feedback from the ecosystem to the gene expression level. Persepct. Plant Ecol. Evol. Syst. 1: 92–120
Hedin LO, Armesto JJ & Johnson AH (1995) Patterns of nutrient loss from unpolluted, oldgrowth temperate forests: evaluation of biogeochemical theory. Ecology 76: 493–509
Herbert DA, Rastetter EB, Shaver GR & Agren GI (1999) Effects of plant growth characteristics on biogeochemistry and community composition in a changing climate. Ecosystems 2: 367–382
Hobbie SE & Vitousek PM. (2000) Nutrient regulation of decomposition in Hawaiian forests: Do the same nutrients limit production and decomposition? Ecology 81: 1867–1877
Hoffmann L (1989) Algae of terrestrial habitats. Bot. Rev. 55: 77–105
Högberg P (1997) 15N natural abundance in soil-plant systems. New Phytol. 137: 179–203
Hooper DU & Johnson L (1999) Nitrogen limitation in dryland ecosystems: Responses to geographical and temporal variation in precipitation. Biogeochemistry 46: 247–293
Horne AJ & Carmiggelt CJW (1975) Algal nitrogen fixation in California streams: seasonal cycles. Freshwater Biol. 5: 461–470
Howarth RW & Cole JJ (1985) Molybdenum availability, nitrogen limitation, and phytoplankton growth in natural waters. Science 229: 653–655
Howarth RW, Chan F & Marino R (1999) Do top-down and bottom-up controls interact to exclude nitrogen-fixing cyanobacteria from the plankton of estuaries? An exploration with a simulation model. Biogeochemisty 46: 203–231
Howarth RW, Marino R, Land J & Cole JJ (1988a) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnol. Oceanogr. 33: 669–687
Howarth RW, Marino R & Cole JJ (1988b) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33: 688–701
Hungate BA, Dijkstra P, Johnson DW, Hinkle CR & Drake BG (1999) Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Glob. Change Biol. 5: 797–806
James EK (2000) Nitrogen fixation in epiphytic and associative symbiosis. Field Crop Res. 65: 197–209
James EK & Olivares FL (1998) Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. CRC Cr. Rev. Plant Sci. 17: 77–119
Johansen JR & Rushforth SR (1985) Cryptogamic soil crusts; Seasonal variation in algal populations in the Tintic mountains, Juab County, Utah. Great Basin Nat. 45: 14–21
Johansen JR, Ashley J & Rayburn WR (1993) Effects of rangefire on soil algal crusts in semiarid shrub-steppe of the lower Columbia Basin and their subsequent recovery. Great Basin Nat. 53: 73–88
Jones K (1992) Diurnal nitrogen fixation in tropical marine cyanobacteria: a comparison between adjacent communities of non-heterocystous Lyngbya sp. and heterocystous Calothrix sp. Brit. Phycol. J. 27: 107–118
Joye SB & Paerl HW (1993) Contemporaneous nitrogen-fixation and denitrification in intertidal microbial mats - rapid response to runoff events. Mar. Ecol.-Prog. Ser. 94: 267–274
Joye SB & Paerl HW (1994) Nitrogen cycling in microbial mats: rates and patterns of denitrification and nitrogen fixation. Mar. Biol. 119: 285–295
Kapustka LA & DuBois JD (1987) Dinitrogen fixation by cyanobacteria and associative rhizosphere bacteria in the Arapaho Prairie in the Sand Hills of Nebraska. Am. J. Bot. 74: 107–113
Keller M & Reiners WA (1994) Soil-atmosphere exchange of nitrous oxide, nitric oxide, and methane under secondary succession from pasture to forest in the Atlantic lowlands of Costa Rica. Global Biogeochem. Cycles 8: 399–409
Knapp AK & Seastedt TR (1986) Detritus accumulation limits productivity of tallgrass prairie. Bioscience 36: 662-68
Kurina LM & Vitousek PM (1999) Controls over the accumulation and decline of a nitrogen-fixing lichen, Stereocaulon vulcani, on young Hawaiian lava flows. J. Ecol. 87: 784–799
Liengen T (1999) Environmental factors influencing the nitrogen fixation activity of freeliving terrestrial cyanobacteria from a high arctic area, Spitsbergen. Can. J. Microbiol. 45: 573–581
Liengen T & Olsen RA (1997) Nitrogen fixation by free-living cyanobacteria from different coastal sites in a high arctic tundra, Spitsbergen. Arctic Alpine Res. 29: 470–477
Lüscher A, Hendry GR & Nösberger J (1998) Long-term responsiveness to free air CO2 enrichment of functional types, species and genotypes of plants from fertile permanent grassland. Oecologia113: 37–45
Marino R, Howarth RW, Shamess J & Prepas E (1990) Molybdenum and sulfate as controls on the abundance of nitrogen-fixing cyanobacteria in saline lakes in Alberta. Limnol. Oceanogr. 35: 245–259
Marino R, Chan F, Howarth RW & Pace M (Manuscript in preparation)
Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC & Treseder K (1999) Nitrogen stable isotope composition of leaves and soil: tropical versus temperate forests. Biogeochemistry46: 45–65
Matson PA & Vitousek PM (1987) Cross-system comparison of soil nitrogen transformations and nitrous oxide fluxes in tropical forests. Global Biogeochem. Cy. 1: 163–170
Matson PA, McDowell WH, Townsend AR & Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46: 67–83
McKane RB, Rastetter EB, Shaver GR, Nadelhoffer KJ, Giblin AE, Laundre JA & Chapin FS III (1997) Reconstruction and analysis of historical changes in carbon storage in arctic Tundra. Ecology 78: 1188–1198
McCollum EW, Crowder LB & McCollum SA (1998) Complex interactions of fish, snails, and littoral zone periphyton. Ecology 79: 1980–1994
McKey D (1994) Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent JL & McKey D (Eds) Advances in Legume Systematics: Part 5 - The Nitrogen Factor (pp 211–228). Royal Botanic Gardens, Kew, England
Mooney HA & Gulmon SL (1979) Environmental and evolutionary constraints on the photosynthetic characteristics of higher plants. In: Solbrig OT, Jain S, Johnson GB & Raven PH (Eds) Plant Population Biology (pp 316–337). Columbia University Press, New York
Moreira FMS, Silva MF & Faria SM (1992) Occurence of nodulation in legume species in the Amazon region of Brazil. New Phytol. 121: 563–570
Nutman PS (1948) Physiological studies on nodule formation. I. The relation between nodulation and lateral root formation in red clover. Ann. Bot. N.S. 12: 81–96
Paerl HW (1985) Microzone formation: its role in the enhancement of aquatic N2 fixation. Limnol. Oceanogr. 30: 1246–1252
Parrotta JA, Baker DD & Fried M (1996) Changes in dinitrogen fixation in maturing stands of Casuarina equisetifolia and Leucaena leucocephala. Can. J. Forest Res. 26: 1684–1691
Pastor J & Binkley D (1998) Nitrogen fixation and the mass balances of carbon and nitrogen in ecosystems. Biogeochemistry43: 63–78
Paul EA & Clark FE (1989) Soil Microbiology and Biochemistry. Academic Press, London
Peterjohn WT & Schlesinger WH (1990) Nitrogen loss from deserts in the southwestern United States. Biogeochemistry 10: 67–79
Peterjohn WT & Schlesinger WH (1991) Factors controlling denitrification in a Chihuahuan desert ecosystem. Soil Sci. Soc. Am. J. 55: 1694–1701
Prance GT, Rodrigues WA & Silva MF (1976) Inventário florestal de um hectare de mata de terra-firme km 30 da estrada Manaus-Itacoatiara. Acta Amazon. 6: 9–35
Prescott CE (1995) Does nitrogen availability control rates of litter decomposition in forests? Plant Soil143: 1–10
Rastetter EB & Shaver GR (1992) A model of multiple-element limitation for acclimating vegatation. Ecology 73: 1157–1174
Rastetter EB, Ågren GI & Shaver GR (1997) Responses of N-limited ecosystems to increased CO2: A balanced-nutrition, coupled-element-cycles model. Ecol. App. 7: 444–460
Ribet J & Drevon J-J (1996) The phosphorus requirement of N2-fixing and urea-fed Acacia Mangium. New Phytol. 132: 383–390
Rychert RD & Skujins J (1974) Nitrogen fixation by blue-green algae-lichen crusts in the Great Basin Desert. Soil Sci. Soc. Amer. Proc. 38: 768–771
Ritchie ME & Tilman D (1995) Responses of legumes to herbivores and nutrients during succession on a nitrogen-poor soil. Ecology 76: 2648–2655
RitchieME, Tilman D & Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79: 165–177
Robson AD (1983) Mineral nutrition. In: Broughton WJ (Ed) Nitrogen Fixation Vol 3 Legumes (pp 36–55). Clarendon Press, Oxford
Sanginga N, Danso SKA, Zapata F & Bowen GD (1995) Phosphorus requirements and nitrogen accumulation by N2-fixing and non-N2-fixing leguminous trees growing in low P soils. Biol. Fert. Soils 20: 205–211
Schaffner WR, Hairston NG & Howarth RW (1994) Feeding rates and filament clipping by crustacean zooplankton consuming cyanobacteria. Verh. Internat. Verein. Limnol. 25: 2375–2381
Schimel DS, Brassell BH & Parton WJ (1997) Equilibration of the terrestrial water, nitrogen, and carbon cycles. PNAS94: 8280–8283
Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260–267
Schultze LS, Ferris FG, Sherwood-Lollar B & Gerits JP (1996) Ultrastructure and seasonal growth patterns of microbial mats in a temperate climate saline alkaline lake: Goodenough Lake, British Columbia, Canada. Canadian Journal of Microbiology 42: 147–161
Sellers PJ, Dickenson RE, Randall DA, Betts AK, Hall FG, Berry JA, Collatz GJ, Denning AS, Mooney HA, Nobre CA, Sato N, Field CB & Henderson-Sellers A (1997) Modeling the exchanges of energy, water, and carbon between continents and the atmosphere. Science 275: 502–509
Shields LM & Durrell LW (1964) Algae in relation to soil fertility. Bot. Rev. 30: 92–128
Skujins J (1981) Nitrogen cycling in arid ecosystems. In: Clark FE & Rosswall T (Eds) Terrestrial Nitrogen Cycles: Processes, Ecosystem Strategies and Management Impacts (pp 477–491). Ecological Bulletins (Stockholm) 33, Swedish Natural Science Research Council, Stockholm, Sweden
Smith VH (1992) Effects of nitrogen:phosphorus supply ratios on nitrogen fixation in agricultural and pastoral systems. Biogeochemistry 18: 19–35
Smith VH & Bennett SJ (1999) Nitrogen:Phosphorus supply ratios and phytoplankton community structure in lakes. Arch. Hydrobiol. 146: 37–53
Soltis DE, Soltis PS, Morgan DR, Swenson SM, Mullin BC, Dowd JM & Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. PNAS 92: 2647–2651
Sprent JI (1999) Nitrogen fixation and growth of non-crop legume species in diverse environments. Perspect. Plant Ecol. Evol. Syst. 2: 149–162
Sprent JI & Raven JA (1985) Evolution of nitrogen fixing symbioses. Proceedings of the Royal Society of Edinburgh B85: 215–237
Sprent JI & Sprent P (1990) Nitrogen Fixing Organisms. Chapman and Hall, London
Sprent JI, Geoghegan IE, Whitty PW & James EK (1996) Natural abundance of 15N and 13C in nodulated legumes and other plants in the Cerrado and neighboring regions of Brazil. Oecologia 105: 440–446
Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol. 131: 1–32
Stewart WDP (1974) Blue-green algae. In: Quispel A (Ed) North Holland Research Monographs. Front. Biol. 33: 202–237
Sylvester-Bradley R, Oliveira LA, Podestá Filho JA & St. John TV (1980) Nodulation of legumes, nitrogenase activity of roots and occurrence of nitrogen-fixing Azospirillum spp. in representative soils of Central Amazonia. Agro-Ecoystems 6: 249–266
Thompson MV & Vitousek PM (1997) Asymbiotic nitrogen fixation and decomposition during long-term soil development in Hawaiian montane rain forest. Biotropica 29: 134–144
Tuchman NC & Stevenson RJ (1991) Effects of selective grazing by snails on benthic algal succession. J. N. Am. Benthol. Soc. 10: 430–443
Tyrrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400: 525–531
Villbrandt M, Krumbein WE & Stal LJ (1991) Diurnal and seasonal variations of nitrogen fixation and photosynthesis in cyanobacterial mats. Plant Soil 137: 13–16
Vitousek PM & Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46: 179–202
Vitousek PM & Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory.Biogeochemistry 37: 63–75
Vitousek PM & Hobbie SE. The control of heterotrophic nitrogen fixation in decomposing litter. Ecology 81: 2366-2376
Vitousek PM & Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13: 87–115
Vitousek PM & Sanford RL Jr. (1986) Nutrient cycling in moist tropical forest. Annu. Rev. Ecol. Syst. 17: 137–167
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH & Tilman D (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Applic. 7: 737–750
Vitousek PM, Hedin LO, Matson PA, Fownes JH & Neff J (1998) Within-system element cycles, input-output budgets, and nutrient limitation. In: Pace M & Groffman P (Eds) Successes, Limitations, and Frontiers in Ecosystem Science (pp 432–452). Springer-Verlag, Berlin
Walker TW & Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15: 1–19
Warren SD (1995) Ecological role of microphytic soil crusts in arid ecosystems. In: Allsopp D, Colwell RR & Harksworth DL (Eds) Microbial Diversity and Ecosystem Function (pp 199–209). CAB International
West NE (1990) Structure and function of microphytic soil crusts in wildland ecosystems of arid to semi-arid regions. Adv. Ecol. Res. 20: 179–223
Wiebe WJ, Johannes RE & Webb KL (1975) Nitrogen fixation in a coral reef community. Science 188: 257–259
Williams SL & Carpenter RC (1997) Grazing effects on nitrogen fixation in coral reef algal turfs. Mar. Biol. 130: 223–231
Williams SL & Carpenter RC (1998) Effects of unidirectional and oscillatory water flow on nitrogen fixation (acetylene reduction) in coral reef algal turfs, Keneohe Bay, Hawaii. J Exp. Mar. Ecol. Biol. 226
Wilson JT & Alexander M(1979) Effect of soil nutrient status and pH on nitrogen-fixing algae in flooded soils. Soil Sci. Soc. Am. J. 43: 936–939
Yoneyama T, Moraoka T, Murakami T & Boonkerd N (1993) Natural abundance of 15N in tropical plants with emphasis on tree legumes. Plant Soil 153: 295–304
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Vitousek, P.M., Cassman, K., Cleveland, C. et al. Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45 (2002). https://doi.org/10.1023/A:1015798428743
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DOI: https://doi.org/10.1023/A:1015798428743