Biogeochemistry

, Volume 46, Issue 1–3, pp 233–246

The presence of nitrogen fixing legumes in terrestrial communities: Evolutionary vs ecological considerations

  • Timothy E. Crews
Article

Abstract

Nitrogen is often a limiting factor to net primary productivity (NPP) and other processes in terrestrial ecosystems. In most temperate freshwater ecosystems, when nitrogen becomes limiting to NPP, populations of N-fixing cyanobacteria experience a competitive advantage, and begin to grow and fix nitrogen until the next most limiting resource is encountered; typically phosphorus or light. Why is it that N-fixing plants do not generally function to overcome N limitation in terrestrial ecosystems in the same way that cyanobacteria function in aquatic ecosystems? To address this question in a particular ecosystem, one must first know whether the flora includes a potential set of nitrogen fixers. I suggest that the presence or absence of N-fixing plant symbioses is foremost an evolutionary consideration, determined to a large extent by constraints on the geographical radiation of woody members of the family Fabaceae. Ecological factors such as competition, nutrient deficiencies, grazing and fire are useful to explain the success of N-fixing plants only when considered against the geographical distribution of potential N-fixers.

Key words

biogeography Fabaceae legumes nitrogen fixation nutrient limitation 

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References

  1. Allen ON & Allen EK (1981) The Leguminosae. The University of Wisconsin Press, Madison, WisconsinGoogle Scholar
  2. Alexander M (1984) Ecology ofRhizobium. In: Alexander M (Ed.) Biological Nitrogen Fixation (pp 39–50). Plenum Press, New York, U.S.A.Google Scholar
  3. Bahre CJ (1995) Human impacts on the grasslands of Southeastern Arizona. In: McClaran MP & Van Devender TR (Eds) The Desert Grassland (pp 230–264). The University of Arizona Press, Tucson, Arizona, U.S.A.Google Scholar
  4. Becker DA & Crockett JJ (1976) Nitrogen fixation in some prairie legumes. The American Midland Naturalist 96: 133–143Google Scholar
  5. Beevers L & Hageman RH (1969) Nitrate reduction in higher plants. Annual Review of Plant Physiology 20: 495–522Google Scholar
  6. Blydenstein J (1967) Tropical savanna vegetation of the Llanos of Colombia. Ecology 48: 1–15Google Scholar
  7. Bordeleau LM & Prévost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant and Soil 161: 115–125Google Scholar
  8. Boring LR, Swank WT, Waide JB & Henderson GS (1988) Sources, fates, and impacts of nitrogen inputs to terrestrial ecosystems: Review and synthesis. Biogeochemistry 6: 119–159Google Scholar
  9. Brown DE (1994) Biotic Communities: Southwestern United States and Northwestern Mexico. University of Utah Press, Salt Lake, Utah, U.S.A.Google Scholar
  10. Chapin FS III (1980) The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11: 233–260Google Scholar
  11. Crews TE (1993) Phosphorus regulation of nitrogen fixation in a traditional Mexican agroecosystem. Biogeochemistry 21: 141–166Google Scholar
  12. Croat T (1978) Flora of Barro Colorado Island. Stanford Univ. Press, Stanford, California, U.S.A.Google Scholar
  13. de Faria SM, Lewis GP, Sprent JI & Sutherland JM (1989) Occurrence of nodulation in Leguminosae. New Phytologist 111: 607–619Google Scholar
  14. Eskew DL & Ting IP (1978) Nitrogen fixation by legumes and blue-green algal-lichen crusts in a Colorado desert environment. Am. J. Botany. 65: 850–856Google Scholar
  15. Foster RB (1990) The floristic composition of the Rio Manu floodplain forest. In: Gentry AH (Ed.) Four Neotropical Rainforests (pp 99–111). Yale University Press, New Haven, Connecticut, U.S.A.Google Scholar
  16. Foster RB & Hubbell SP (1990) The floristic composition of the Barro Colorado Island forest. In: Gentry AH (Ed.) Four Neotropical Rainforests (pp 85–98). Yale University Press, New Haven, Connecticut, U.S.A.Google Scholar
  17. Gentry HS (1942) Rio Mayo Plants. Carnegie Inst. Washington Publ. 527, Washington, DC, U.S.A.Google Scholar
  18. Gessel SP, Cole DW & Steinbrenner EC (1973) Nitrogen balances in forest ecosystems of the Pacific Northwest. Soil Biology and Biochemistry 5: 19–34Google Scholar
  19. Goi SR, Sprent JI, Games EL & Jacob-Neto J (1992) Influence of nitrogen form and concentration on the nitrogen fixation of Acacia auriculiformis. Symbiosis 14: 115–122Google Scholar
  20. Gorham E, Vitousek PM & Reiners WA (1979) The regulation of chemical budgets over the course of terrestrial ecosystem succession. Annual Review of Ecology and Systematics 10: 53–84Google Scholar
  21. Greller AM (1988). Deciduous Forest. In: Harbour M & Billings WD (Eds) North American Terrestrial Vegetation (pp 288–316). Cambridge University Press, CambridgeGoogle Scholar
  22. Gutschick VP (1980) Energy flows in the nitrogen cycle, especially in fixation. In: Newton WE & Orme-Johnson WH (Eds) Nitrogen Fixation, Vol. I. (pp 17–27). University Park Press, Baltimore, Maryland, U.S.A.Google Scholar
  23. Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. The American Naturalist 118: 607–637Google Scholar
  24. Gutschick VP (1987) A Functional Biology of Crop Plants. Timber Press, Portland, Oregon, U.S.A.Google Scholar
  25. Hammel B (1990) The distribution of diversity among families, genera, and habit types in the La Selva Flora. In: Gentry AH (Ed.) Four Neotropical Rainforests (pp 75–84). Yale University Press, New Haven, Connecticut, U.S.A.Google Scholar
  26. Hedin LO, Armesto JJ & Johnson AH (1995) Patterns of nutrient loss from unpolluted, old-growth temperate forests: evaluation of biogeochemical theory. Ecology 76: 493–509Google Scholar
  27. Herendeen PS, Crepet WL & Dilcher DL (1992) The fossil record. In: Herendeen PS & Dilcher DL (Eds) Advances in Legume Systematics, Part 4 (pp 303–316). Royal Botanic Gardens, KewGoogle Scholar
  28. Högberg P & Alexander IJ (1995) Roles of root symbioses in African woodland and forest evidence from N abundance and foliar analysis. J. Ecology 83: 217–224Google Scholar
  29. Hulme PE (1994) Seedling herbivory in grassland: relative impact of vertebrate and invertebrate herbivores. J. Ecology 82: 873–880Google Scholar
  30. Hulme PE (1996) Herbivores and the performance of grassland plants: a comparison of arthropod, mollusc and rodent herbivory. J. Ecology 84: 43–51Google Scholar
  31. Leigh EG Jr, & Wright SJ (1990) Barro Colorado Island and tropical biology. In: Gentry AH (Ed.) Four Neotropical Rainforests (pp 28–47). Yale University Press, New Haven, Connecticut, U.S.A.Google Scholar
  32. Likens GE, Bormann FH, Pierce RS, Eaton JS & Johnson MM (1977) Biogeochemistry of a Forested Ecosystem. Springer-Verlag, New York, U.S.A.Google Scholar
  33. Lovejoy TE & Bierregaard RO Jr (1990) Central Amazonian forests and the minimum critical size of ecosystems project. In: Gentry AH (Ed.) Four Neotropical Rainforests (pp 60–71). Yale University Press, New Haven, Connecticut, U.S.A.Google Scholar
  34. Marschner H (1995) Mineral Nutrition of Higher Plants. 2nd edn. Academic Press, New York, New York, U.S.A.Google Scholar
  35. Martínez-Yrízar AM, Búrquez A & Maass M (in press) Structure and functioning of tropical deciduous forests in Western Mexico. In: Robichaux RH (Ed.) The Tropical Deciduous Forest of Southern Sonora Mexico: Ecology and Conservation of a Threatened EcosystemGoogle Scholar
  36. McKey D (1994) Legumes and nitrogen: The evolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent JI & McKey D (Eds) Advances in Legume Systematics 5: The Nitrogen Factor (pp 211–228). Royal Botanic Gardens, KewGoogle Scholar
  37. Median E & Bilbao B (1991) Significance of nutrient relations and symbiosis for the competitive interaction between grasses and legumes in tropical savannas. In: Esser G & Overdieck D (Eds) Modern Ecology (pp 295–319). Elsevier, Amsterdam, The NetherlandsGoogle Scholar
  38. Moreira de Souza FM, da Silva MF & de Faria SM (1992) Occurrence of nodulation in legume species in the Amazon region of Brazil. New Phytologist 121: 563–570Google Scholar
  39. NAS (1979) Tropical Legumes: Resources for the Future. National Academy of Sciences, Washington, DC, U.S.A.Google Scholar
  40. Neyra CA (1978) Interactions of plant photosynthesis with dinitrogen fixation and nitrate assimilation. In: Döbereiner J, Burris RH, Hollaender A (Eds) Limitations and Potentials for Biological Nitrogen Fixation in the Tropics (pp 111–120). Plenum Press, New York, U.S.A.Google Scholar
  41. Paul EA, Myers RJK & Rice WA (1971) Nitrogen fixation in grassland and associated cultivated ecosystems. Plant and Soil Special Volume: 495–507Google Scholar
  42. Peoples MB & Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant and Soil 141: 13–39Google Scholar
  43. Polhill RM, Raven PH & Stirton CH (1981) Evolution and systematics of the Leguminosae. In: Polhill RM & Raven PH (Eds) Advances in Legume Systematics, Part 1 (pp 1–26). Royal Botanic Gardens, KewGoogle Scholar
  44. Robson AD & Bottomley PJ (1991) Limitations in the use of legumes in agriculture and forestry. In: Dilworth MJ & Glenn AR (Eds) Biology and Biochemistry of Nitrogen Fixation (pp 320–349). Elsevier, Amsterdam, The NetherlandsGoogle Scholar
  45. Rundel RW (1989) Ecological success in relation to plant form and function in the woody legumes. In: Stirton CH & Zarucchi JL (Eds) Advances in Legume Biology Monogr. Syst. Bot. Missouri Bot. Gard. 29: 377–398Google Scholar
  46. Rundel PW & Gibson AC (1996) Ecological Communities and Processes in a Mojave Desert Ecosystem: Rock valley, Nevada. Cambridge University Press, Cambridge, U.K.Google Scholar
  47. Ryle GJA, Powell CE & Gordon AJ 1979. The respiratory costs of nitrogen fixation in soyabean, cowpea, and white clover. II. Comparisons of the cost of nitrogen fixation and the utilization of combined nitrogen. J. Exp. Bot. 30: 145–153Google Scholar
  48. Smith VH (1992) Effects of nitrogen:phosphorus supply ratios in nitrogen fixation in agricultural and pastoral systems. Biogeochemistry 18: 19–35Google Scholar
  49. Solbrig OT (1996) The diversity of the savanna ecosystem. In: Solbrig OT, Medina E & Silva JF (Eds) Biodiversity and Savanna Ecosystem Processes. Springer, Berlin, GermanyGoogle Scholar
  50. Sprent JI (1994a) Nitrogen acquisition systems in the Leguminosae. In: Sprent JI & McKey D (Eds) Advances in Legume Systematics 5: The Nitrogen Factor (pp 1–16). Royal Botanic Gardens, KewGoogle Scholar
  51. Sprent JI (1994b) Evolution and diversity in the legume-rhizobium symbiosis: chaos theory? Plant and Soil 161: 1–10Google Scholar
  52. Sprent JI (1995) Legume trees and shrubs in the tropics: N2 fixation in perspective. Soil Biol. Biochem. 27: 401–407Google Scholar
  53. Sprent JI & Sprent P (1990) Nitrogen Fixing Organisms. Chapman and Hall, London, U.K.Google Scholar
  54. Turkington RA, Cavers PB & Aarssen LW (1977) Neighbor relationships in grass-legume communities. I. Interspecific contacts in four grassland communities near London, Ontario. Can. J. Botany 55: 2701–2711Google Scholar
  55. Turner RM, Bowers JE & Burgess TL (1995) Sonoran Desert Plants: An ecological atlas. University of Arizona Press, Tucson, Arizona, U.S.A.Google Scholar
  56. Velásquez J (1965) Estudio fitosociológico acerca de los pastizales de las sabanas de Calabozo, Estado Guárico. Bol. Soc. Venezolana Cienc. Nat. 25: 59–101Google Scholar
  57. Virginia RA, Jarrell WM, Rundel PW, Shearer G & Kohl DH (1989) The use of variation in the natural abundance of15N to assess symbiotic nitrogen fixation by woody plants. In: Rundel PW, Ehleringer JR & Nagy KA (Eds) Stable Isotopes in Ecological Research (pp 375–394). Springer-Verlag, New York, U.S.A.Google Scholar
  58. Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. The American Naturalist 119: 553–572Google Scholar
  59. Vitousek PM & Sanford RL Jr (1986) Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics 17: 137–167Google Scholar
  60. Vitousek PM & Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13: 87–115Google Scholar
  61. Vitousek PM & Field, CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry, this issueGoogle Scholar
  62. Waterer JG, Vessey JK & Raper CD Jr (1992) Stimulation of nodulation in field peas (Pisum sativum) by low concentrations of ammonium in hydroponic culture. Physiol. Plant. 86: 215–220Google Scholar
  63. Woodmansee RG, Vallis I & Mott JJ (1981) Grassland nitrogen. In: Clark FR & Rosswall T (Eds) Terrestrial Nitrogen Cycles. Ecological Bulletin (Stockholm) 33: 443–462Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Timothy E. Crews
    • 1
  1. 1.Environmental Studies ProgramPrescott CollegePrescottUSA

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