Plant and Soil

, Volume 311, Issue 1–2, pp 1–18 | Cite as

Global inputs of biological nitrogen fixation in agricultural systems

  • David F. Herridge
  • Mark B. Peoples
  • Robert M. BoddeyEmail author
Marschner Review


Biological dinitrogen (N2) fixation is a natural process of significant importance in world agriculture. The demand for accurate determinations of global inputs of biologically-fixed nitrogen (N) is strong and will continue to be fuelled by the need to understand and effectively manage the global N cycle. In this paper we review and update long-standing and more recent estimates of biological N2 fixation for the different agricultural systems, including the extensive, uncultivated tropical savannas used for grazing. Our methodology was to combine data on the areas and yields of legumes and cereals from the Food and Agriculture Organization (FAO) database on world agricultural production (FAOSTAT) with published and unpublished data on N2 fixation. As the FAO lists grain legumes only, and not forage, fodder and green manure legumes, other literature was accessed to obtain approximate estimates in these cases. Below-ground plant N was factored into the estimations. The most important N2-fixing agents in agricultural systems are the symbiotic associations between crop and forage/fodder legumes and rhizobia. Annual inputs of fixed N are calculated to be 2.95 Tg for the pulses and 18.5 Tg for the oilseed legumes. Soybean (Glycine max) is the dominant crop legume, representing 50% of the global crop legume area and 68% of global production. We calculate soybean to fix 16.4 Tg N annually, representing 77% of the N fixed by the crop legumes. Annual N2 fixation by soybean in the U.S., Brazil and Argentina is calculated at 5.7, 4.6 and 3.4 Tg, respectively. Accurately estimating global N2 fixation for the symbioses of the forage and fodder legumes is challenging because statistics on the areas and productivity of these legumes are almost impossible to obtain. The uncertainty increases as we move to the other agricultural-production systems—rice (Oryza sativa), sugar cane (Saccharum spp.), cereal and oilseed (non-legume) crop lands and extensive, grazed savannas. Nonetheless, the estimates of annual N2 fixation inputs are 12–25 Tg (pasture and fodder legumes), 5 Tg (rice), 0.5 Tg (sugar cane), <4 Tg (non-legume crop lands) and <14 Tg (extensive savannas). Aggregating these individual estimates provides an overall estimate of 50–70 Tg N fixed biologically in agricultural systems. The uncertainty of this range would be reduced with the publication of more accurate statistics on areas and productivity of forage and fodder legumes and the publication of many more estimates of N2 fixation, particularly in the cereal, oilseed and non-legume crop lands and extensive tropical savannas used for grazing.


Associative Cyanobacteria Dinitrogen (N2) fixation Endophytic Free-living Global Legumes Nitrogen (N) Oilseed legumes Pulses Rhizobia Soybean 


  1. Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252:1–9CrossRefGoogle Scholar
  2. Aslam M, Mahmood IA, Peoples MB, Schwenke GD, Herridge DF (2003) Contribution of chickpea nitrogen fixation to increased wheat production and soil organic fertility in rain-fed cropping. Biol Fertil Soils 38:59–64CrossRefGoogle Scholar
  3. Bell F, Nutman PS (1971) Experiments on nitrogen fixation by nodulated lucerne. In: Lie A, Mulder EG (eds) Biological nitrogen fixation in natural and agricultural habitats. Plant and soil, special volume. Martinus Nijhoff, The Hague, pp 231–264Google Scholar
  4. Bergersen FJ, Brockwell J, Gault RR, Morthorpe LJ, Peoples MB, Turner GL (1989) Effects of available soil nitrogen and rates of inoculation on nitrogen fixation by irrigated soybeans and evaluation of the δ15N methods for measurement. Aust J Agric Res 40:763–780CrossRefGoogle Scholar
  5. Biggs I, Stewart GR, Wilson JR, Critchley C (2002) 15N natural abundance studies in Australian commercial sugarcane. Plant Soil 238:21–30CrossRefGoogle Scholar
  6. Boddey RM (1987) Methods for quantification of nitrogen fixation associated with gramineae. Crit Rev Plant Sci 6:209–266Google Scholar
  7. Boddey RM, de Oliveira O, Urquiaga S, Reis V, Olivares F, Baldani V et al (1995) Biological nitrogen fixation associated with sugarcane and rice: contributions and prospects for improvement. Plant Soil 174:195–209CrossRefGoogle Scholar
  8. Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosyst 57:235–270CrossRefGoogle Scholar
  9. Boddey RM, Polidoro JC, Resende AS, Alves BJR, Urquiaga S (2001) Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses. Aust J Plant Physiol 28:889–895Google Scholar
  10. Boddey RM, Urquiaga S, Alves BJR, Reis V (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252:139–149CrossRefGoogle Scholar
  11. Boyer EW, Howarth RW, Galloway JN, Dentener FJ, Cleveland C, Asner GP et al (2004) Current nitrogen inputs to world regions. In: Mosier AR, Syers JK, Freney JR (eds) Agriculture and the nitrogen cycle. Island, Washington, pp 221–230Google Scholar
  12. Burns RC, Hardy RWF (1975) Nitrogen fixation in bacteria and higher plants. Springer-Verlag, BerlinGoogle Scholar
  13. Burris RH (1980) The global nitrogen budget—science or séance? In: Newton WE, Orme-Johnson WH (eds) Nitrogen fixation, volume I. University Park Press, Baltimore, pp 7–16Google Scholar
  14. Burris RH, Eppling FJ, Wahlin HB, Wilson PW (1942) Studies of biological nitrogen fixation with isotopic nitrogen. Soil Sci Soc Am Proc 7:258–262Google Scholar
  15. Carlsson G, Huss-Danell K (2003) Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353–372CrossRefGoogle Scholar
  16. Chalk PM (1985) Estimation of N2 fixation by isotope dilution: an appraisal of techniques involving 15N enrichment and their application. Soil Biol Biochem 17:389–410CrossRefGoogle Scholar
  17. Chalk PM (1991) The contribution of associative and symbiotic nitrogen fixation to the nitrogen nutrition of non-legumes. Plant Soil 132:29–39CrossRefGoogle Scholar
  18. Chalk PM (1998) Dynamics of biologically fixed N in legume–cereal rotations: a review. Aust J Agric Res 49:303–316CrossRefGoogle Scholar
  19. Chalk PM, Ladha JK (1999) Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution. Soil Biol Biochem 31:1901–1917CrossRefGoogle Scholar
  20. Chapman AL, Myers RJK (1987) Nitrogen contributions by grain legumes to rice grown in rotation on the Cununurra soils of the Ord irrigation area, Western Australia. Aust J Exp Agric 27:155–163CrossRefGoogle Scholar
  21. Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO et al (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochem Cycles 13:623–645CrossRefGoogle Scholar
  22. Crews TE (1999) The presence of nitrogen fixing legumes in terrestrial communities: evolutionary vs. ecological considerations. Biogeochemistry 46:233–246Google Scholar
  23. Crews TE, Peoples M (2005) Can the synchrony of nitrogen supply and crop demand be improved in legume and fertilizer-based agroecosystems?: a review. Nutr Cycl Agroecosyst 72:101–120CrossRefGoogle Scholar
  24. Dalal RC, Strong WM, Doughton JA, Weston EJ, McNamara GT, Cooper JE (1997) Sustaining productivity of a vertisol at Warra, Queensland, with fertilisers, no-tillage or legumes 4. Nitrogen fixation, water use and yield of chickpea. Aust J Exp Agric 37:667–676CrossRefGoogle Scholar
  25. Danso SKA, Hardarson G, Zapata F (1993) Misconceptions and practical problems in the use of 15N soil enrichment techniques for estimating N2 fixation. Plant Soil 152:25–52CrossRefGoogle Scholar
  26. Delwiche CC (1970) The nitrogen cycle. Sci Am 223:136–146CrossRefGoogle Scholar
  27. Di Ciocco C, Álvarez R, Andrada Y, Momo F (2004) Balance de nitrogeno en un cultivo de soja de segunda en La Pampo ondulada. Cienc Suelo 22:48–51 Buenos AiresGoogle Scholar
  28. Dobereiner J, Burris RH, Hollaender A (1978) Limitations and potentials for biological nitrogen fixation in the tropics. Plenum, New York, p 398Google Scholar
  29. Dong Z, Hunt S, Dowling AN, Winship LJ, Layzell DB (2001) Rapid measurement of hydrogen concentration and its use in the determination of nitrogenase activity of legume plants. Symbiosis 29:71–81Google Scholar
  30. Evans J, Herridge DF (1987) Nitrogen inputs and utilization in crop legumes. In: Bacon PE, Evans J, Storrier RR, Taylor AC (eds) Nitrogen cycling in temperate agricultural systems. Australian Society of Soil Science, Wagga Wagga, pp 14–43Google Scholar
  31. Evans J, McNeill AM, Unkovich MJ, Fettell NA, Heenan DP (2001) Net nitrogen balances for cool-season grain legume crops and contributions to wheat nitrogen uptake: a review. Aust J Exp Agric 41:347–359CrossRefGoogle Scholar
  32. Galloway JN, Schlesinger WH, Levy H II, Michaels A, Schnoor JL (1995) Nitrogen fixation: atmospheric enhancement–environmental response. Global Biogeochem Cycles 9:235–252CrossRefGoogle Scholar
  33. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP et al (2004) Nitrogen cycles: past, present and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  34. Gan Y, Stulen I, Posthumus F, van Keulen H, Kuiper PJC (2002) Effects of N management on growth, N2 fixation and yield of soybean. Nutr Cycl Agroecosyst 62:163–174CrossRefGoogle Scholar
  35. Gan Y, Stulen I, van Keulen H, Kuiper PJC (2003) Effect of N fertilizer top-dressing at various reproductive stages on growth, N2 fixation and yield of three soybean (Glycine max (L.) Merr.) genotypes. Field Crops Res 80:147–155CrossRefGoogle Scholar
  36. Garcia FO (2004) Soil fertility management for soybean in Argentina. In: Moscardi F, Hoffmann-Campo CB, Saraiva OF, Galerani PR, Krzyzanowski FC, Carrao-Panizzi MC (eds) Proceedings VII World Soybean Research Conference. Brazilian Agricultural Research Corporation, National Soybean Research Center, Brazil, pp 392–399Google Scholar
  37. Gehring C, Vlek PLG (2004) Limitations of the 15N natural abundance method for estimating biological nitrogen fixation in Amazonian forest legumes. Basic Appl Ecol 5:567–580CrossRefGoogle Scholar
  38. Giller KE (2001) Nitrogen fixation in tropical cropping systems, 2nd edn. CABI, Wallingford, p 423Google Scholar
  39. Giller KE, Merckx R (2003) Exploring the boundaries of N2-fixation in cereals and grasses: an hypothetical and experimental framework. Symbiosis 35:3–17Google Scholar
  40. Goulding KWT, Bailey NJ, Bradbury NJ, Hargreaves P, Howe M, Murphy DV et al (1998) Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytol 139:49–58CrossRefGoogle Scholar
  41. Guafa W, Peoples MB, Herridge DF, Rerkasem B (1993) Nitrogen fixation, growth and yield of soybean grown under saturated soil culture and conventional irrigation. Field Crops Res 32:257–268CrossRefGoogle Scholar
  42. Gupta VVSR, Roper MM, Roget DK (2006) Potential for non-symbiotic N2-fixation in different agroecological zones of southern Australia. Aust J Soil Res 44:343–354CrossRefGoogle Scholar
  43. Gutiérrez-Boem FH, Scheiner JD, Rimski-Korsakov H, Lavado RS (2004) Late season nitrogen fertilization of soybeans: effects of leaf senescence, yield and environment. Nutr Cycl Agroecosyst 68:109–115CrossRefGoogle Scholar
  44. Hardarson G, Atkins CA (2003) Optimising biological N2 fixation by legumes in farming systems. Plant Soil 252:41–54CrossRefGoogle Scholar
  45. Hardarson G, Danso SKA (1993) Methods for measuring biological nitrogen fixation in grain legumes. Plant Soil 152:19–23CrossRefGoogle Scholar
  46. Hardarson G, Bliss FA, Cigales-Rivero MR, Henson RA, Kipe-Nolt JA, Longeri L et al (1993) Genotypic variation in biological nitrogen fixation by common bean. Plant Soil 152:59–70CrossRefGoogle Scholar
  47. Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene–ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207PubMedGoogle Scholar
  48. Herridge DF, Danso SKA (1995) Enhancing crop legume N2 fixation through selection and breeding. Plant Soil 174:51–82CrossRefGoogle Scholar
  49. Herridge DF, Holland JF (1992) Production of summer crops in northern New South Wales. I. Effects of tillage and double cropping on growth, grain and N yields of six crops. Aust J Agric Res 43:105–122CrossRefGoogle Scholar
  50. Herridge DF, Peoples MB (1990) The ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by 15N methods. Plant Physiol 93:495–503PubMedGoogle Scholar
  51. Herridge DF, Peoples MB (2002) Timing of xylem sampling for ureide analysis of nitrogen fixation. Plant Soil 238:57–67CrossRefGoogle Scholar
  52. Herridge DF, Bergersen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using the ureide and natural 15N abundance methods. Plant Physiol 93:708–716PubMedGoogle Scholar
  53. Herridge DF, Marcellos H, Felton WL, Turner GL, Peoples MB (1995) Chickpea increases soil-N fertility in cereal systems through nitrate sparing and N2 fixation. Soil Biol Biochem 27:545–551CrossRefGoogle Scholar
  54. Herridge DF, Robertson MJ, Cocks B, Peoples MB, Holland JF, Heuke L (2005) Low nodulation and nitrogen fixation of mungbean reduce biomass and grain yields. Aust J Exp Agric 45:269–277CrossRefGoogle Scholar
  55. Hiep NH, Diep CN, Herridge DF (2002) Nitrogen fixation of soybean and groundnut in the Mekong Delta, Vietnam. In: Herridge D (ed) Inoculants and nitrogen fixation of legumes in Vietnam. ACIAR Proc. 109e. ACIAR, Australia, pp 10–18Google Scholar
  56. Hoa NTL, Thao TY, Lieu P, Herridge DF (2002) N2 fixation of groundnut in the eastern region of south Vietnam. In: Herridge D (ed) Inoculants and nitrogen fixation of legumes in Vietnam. ACIAR Proc. 109e. ACIAR, Australia, pp 19–28Google Scholar
  57. Hoefsloot G, Termorshuizen AJ, Watt DA, Cramer MD (2005) Biological nitrogen fixation is not a major contributor to the nitrogen demand of a commercially grown South African sugarcane cultivar. Plant Soil 277:85–96CrossRefGoogle Scholar
  58. Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151–164CrossRefGoogle Scholar
  59. Hungria M, Franchini JC, Campo RJ, Graham PH (2005) The importance of nitrogen fixation to soybean cropping in south America. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer, Dordrecht, pp 25–42CrossRefGoogle Scholar
  60. Hungria M, Franchini JC, Campo RJ, Crispino CC, Moraes JZ, Sibaldelli RNR et al (2006) Nitrogen nutrition of soybean in Brazil: contributions of biological N2 fixation and N fertilizer to grain yield. Can J Plant Sci 86:927–939Google Scholar
  61. Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol 44:483–511CrossRefGoogle Scholar
  62. Janzen HH, Bruinsma Y (1989) Methodology for the quantification of root and rhizosphere nitrogen dynamics by exposure of shoots to 15N-labelled ammonia. Soil Biol Biochem 21:189–196CrossRefGoogle Scholar
  63. Jefing Y, Herridge DF, Peoples MB, Rerkasem B (1992) Effects of fertilization on N2 fixation and N balances of soybean grown after lowland rice. Plant Soil 147:235–242CrossRefGoogle Scholar
  64. Jensen ES (1997) The role of grain legume N2 fixation in the nitrogen cycling of temperate cropping systems. D.Sc. Thesis. Risø National LaboratoryGoogle Scholar
  65. Jørgensen FV, Ledgard SF (1997) Contribution from stolons and roots to estimates of the total amount of N2 fixed by white clover (Trifolium repens L.). Ann Bot (Lond) 80:641–648CrossRefGoogle Scholar
  66. Kennedy IR, Islam N (2001) The current and potential contribution of asymbiotic nitrogen fixation to nitrogen requirements on farms: a review. Aust J Exp Agric 41:447–457CrossRefGoogle Scholar
  67. Khan DF, Peoples MB, Chalk PM, Herridge DF (2002) Quantifying below-ground nitrogen of legumes 2. A comparison of 15N and non isotopic methods. Plant Soil 239:277–289CrossRefGoogle Scholar
  68. Khan WDF, Peoples MB, Schwenke GD, Felton WL, Chen D, Herridge D (2003) Effects of below ground nitrogen on N balances of field-grown fababean, chickpea, and barley. Aust J Agric Res 54:333–340CrossRefGoogle Scholar
  69. Lima E, Boddey RM, Döbereiner J (1987) Quantification of biological nitrogen fixation associated with sugar cane using a 15N aided nitrogen balance. Soil Biol Biochem 19:165–170CrossRefGoogle Scholar
  70. Mahieu S, Fustec J, Faure M-L, Corre-Hellou G, Crozat Y (2007) Comparison of two 15N labelling methods for assessing nitrogen rhizodeposition of pea. Plant Soil 295:193–205CrossRefGoogle Scholar
  71. Maskey SL, Bhattarai S, Peoples MB, Herridge DF (2001) On-farm measurements of nitrogen fixation by winter and summer legumes in the Hill and Terai regions of Nepal. Field Crops Res 70:209–221CrossRefGoogle Scholar
  72. McAuliffe C, Chamblee DS, Uribe-Arango H, Woodhouse WW (1958) Influence of inorganic nitrogen on nitrogen fixation by legumes as revealed by 15N. Agron J 50:334–337Google Scholar
  73. McClure PR, Israel DW, Volk RJ (1980) Evaluation of the relative ureide content of xylem sap as an indicator of N2 fixation in soybeans. Plant Physiol 66:720–725PubMedGoogle Scholar
  74. McNeill AM, Fillery IRP (2008) Field measurement of lupin belowground nitrogen accumulation and recovery in the subsequent cereal–soil system in a semi-arid Mediterranean-type climate. Plant Soil 302:297–316CrossRefGoogle Scholar
  75. McNeill AM, Unkovich MJ (2007) The nitrogen cycle in terrestrial ecosystems. In: Marschner P, Rengel Z (eds) Nutrient cycling in terrestrial ecosystems. Soil biology, vol 10. Springer-Verlag, Amsterdam, pp 37–64CrossRefGoogle Scholar
  76. McNeill AM, Zhu C, Fillery IRP (1997) Use of in situ 15N-labelling to estimate the total below-ground nitrogen of pasture legumes in intact soil-plant systems. Aust J Agric Res 48:295–304CrossRefGoogle Scholar
  77. McNeill AM, Zhu C, Fillery IRP (1998) A new approach to quantifying the N benefit from pasture legumes to succeeding wheat. Aust J Agric Res 49:427–436CrossRefGoogle Scholar
  78. Minchin FR, Witty JF, Sheehy JE, Muller M (1983) A major error in the acetylene reduction assay: decreases in nodular nitrogenase activity under assay conditions. J Exp Bot 34:641–649CrossRefGoogle Scholar
  79. Minchin FR, Sheehy JE, Witty JF (1986) Further errors in the acetylene reduction assay: effects of plant disturbance. J Exp Bot 37:1581–1591CrossRefGoogle Scholar
  80. Mosier AR, Syers JK, Freney JR (2004) Nitrogen fertilizer: an essential component of increased food, feed, and fiber production. In: Mosier AR, Syers JK, Freney JR (eds) Agriculture and the nitrogen cycle. Island, Washington, pp 3–15Google Scholar
  81. Pate JS, Stewart GR, Unkovich M (1993) 15N natural abundance of plant and soil components of a Banksia woodland ecosystem in relation to nitrate utilization, life form, mycorrhizal status and N2-fixing abilities of component species. Plant Cell Environ 16:365–373CrossRefGoogle Scholar
  82. Peloni JD (2006) Soybean driven nation. World Grain, June 2006, pp 40–46Google Scholar
  83. Peoples MB, Baldock JA (2001) Nitrogen dynamics of pastures: nitrogen fixation inputs, the impact of legumes on soil nitrogen fertility, and the contributions of fixed nitrogen to Australian farming systems. Aust J Exp Agric 41:327–346CrossRefGoogle Scholar
  84. Peoples MB, Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39CrossRefGoogle Scholar
  85. Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and subtropical agriculture. Adv Agron 44:155–223CrossRefGoogle Scholar
  86. Peoples MB, Ladha JK, Herridge DF (1995) Enhancing legume N2 fixation through plant and soil management. Plant Soil 174:83–101CrossRefGoogle Scholar
  87. Peoples MB, Bowman AM, Gault RR, Herridge DF, McCallum MH, McCormick KM et al (2001) Factors regulating the contributions of fixed nitrogen by pasture and crop legumes to different farming systems of eastern Australia. Plant Soil 228:29–41CrossRefGoogle Scholar
  88. Peoples MB, Boddey RM, Herridge DF (2002) Quantification of nitrogen fixation. In: Leigh GJ (ed) Nitrogen fixation at the millennium. Elsevier, Amsterdam, pp 357–389CrossRefGoogle Scholar
  89. Peoples MB, Brockwell J, Herridge DF, Alves BJR, Urquiaga S, Boddey RM et al (2008) Biological nitrogen fixation by food legumes. In: Kharkwal MC (ed) Food legumes for nutritional security and sustainable agriculture. Proceedings 4th International Food Legumes Research Conference (IFLRC-IV), New Delhi, India. Indian Society of Genetics and Plant Breeding, New Delhi (in press)Google Scholar
  90. Reis VM, dos Reis FB Jr, Quesada DM, de Oliveira OCA, Alves BJR, Urquiaga S et al (2001) Biological nitrogen fixation associated with tropical pasture grasses. Aust J Plant Physiol 28:837–844Google Scholar
  91. Rennie RJ, Kemp GA (1982a) N2-fixation in field bean quantified by 15N isotope dilution. I. Effect of strains of Rhizobium phaseoli. Agron J 75:640–644Google Scholar
  92. Rennie RJ, Kemp GA (1982b) N2-fixation in field bean quantified by 15N isotope dilution. II. Effect of cultivars of beans. Agron J 75:645–649Google Scholar
  93. Rochester IJ, Peoples MB, Constable GA, Gault RR (1998) Faba beans and other legumes add nitrogen to irrigated cotton cropping systems. Aust J Exp Agric 38:253–260CrossRefGoogle Scholar
  94. Rochester IJ, Peoples MB, Hulugalle NR, Gault RR, Constable GA (2001) Using legumes to enhance nitrogen fertility and improve soil condition in cotton cropping systems. Field Crops Res 70:27–41CrossRefGoogle Scholar
  95. Roper MM, Ladha JK (1995) Biological N2 fixation by heterotrophic and phototrophic bacteria in association with straw. Plant Soil 174:211–224CrossRefGoogle Scholar
  96. Ruiz Sainz JE, Zhou JC, Rodriguez-Navarro DN, Vinardell JM, Thomas-Oates JE (2005) Soybean cultivation and BNF in China. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer, Dordrecht, pp 67–87CrossRefGoogle Scholar
  97. Rupela OP, Johansen C, Herridge DF (1997) Extending nitrogen fixation research to farmers’ fields. ICRISAT, India, p 404Google Scholar
  98. Russell CA, Fillery IRP (1996a) In situ 15N labelling of lupin below-ground biomass. Aust J Agric Res 47:1035–1046CrossRefGoogle Scholar
  99. Russell CA, Fillery IRP (1996b) Estimates of lupin belowground biomass nitrogen, dry matter, and nitrogen turnover to wheat. Aust J Agric Res 47:1047–1059CrossRefGoogle Scholar
  100. Russelle MP, Birr AS (2004) Large-scale assessment of symbiotic dinitrogen fixation by crops: soybean and alfalfa in the Mississippi River basin. Agron J 96:1754–1760Google Scholar
  101. Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crop Res doi: 10.1016/j.fcr.2008.03.001
  102. Schollhorn R, Burris RH (1967) Acetylene as a competitive inhibitor of N2 fixation. Proc Natl Acad Sci USA 58:213–216PubMedCrossRefGoogle Scholar
  103. Schulz S, Keatinge JDH, Wells GJ (1999) Productivity and residual effects of legumes in rice-based cropping systems in a warm-temperate environment. I. Legume biomass production and N fixation. Field Crops Res 61:23–35CrossRefGoogle Scholar
  104. Schwenke GD, Peoples MB, Turner GL, Herridge DF (1998) Does nitrogen fixation of commercial, dryland chickpea and faba bean crops in north-west New South Wales maintain or enhance soil nitrogen? Aust J Exp Agric 38:61–70CrossRefGoogle Scholar
  105. Shah Z, Shah SH, Peoples MB, Schwenke GD, Herridge DF (2003) Crop residue and fertiliser N effects on nitrogen fixation and yields of legume–cereal rotations and soil organic fertility. Field Crops Res 83:1–11CrossRefGoogle Scholar
  106. Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756Google Scholar
  107. Sheldrake AR, Narayanan A (1979) Growth, development and nutrient uptake in pigeon peas (Cajanus cajan). J Agric Sci 92:513–526CrossRefGoogle Scholar
  108. Shutsrirung A, Sutigoolabud P, Santasup C, Senoo K, Tajima S, Hisamatsu M et al (2002) Symbiotic efficiency and compatibility of native rhizobia in northern Thailand with different soybean cultivars. Soil Sci Plant Nutr 48:491–499Google Scholar
  109. Smil V (1999) Nitrogen in crop production: an account of global flows. Global Biogeochem Cycles 13:647–662CrossRefGoogle Scholar
  110. Stewart WDP, Sampaio MJ, Isichei AO, Sylvester-Bradley R (1978) Nitrogen fixation by soil algae of temperate and tropical soils. In: Dobereiner J, Burris RH, Hollaender A (eds) Limitations and potentials for biological nitrogen fixation in the tropics. Plenum, New York, pp 41–63Google Scholar
  111. Toomsan B, McDonagh JF, Limpinuntana V, Giller KE (1995) Nitrogen fixation by groundnut and soybean and residual nitrogen benefits to rice in farmers’ fields in Northeast Thailand. Plant Soil 175:45–56CrossRefGoogle Scholar
  112. Turpin JE, Herridge DF, Robertson MJ (2002) Nitrogen fixation and soil nitrate interactions in field-grown chickpea (Cicer arietinum) and fababean (Vicia faba). Aust J Agric Res 53:599–608CrossRefGoogle Scholar
  113. Unkovich MJ, Pate JS (2000) An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crops Res 65:211–228CrossRefGoogle Scholar
  114. Unkovich MJ, Pate JS, Sanford P (1997) Nitrogen fixation by annual legumes in Australian Mediterranean agriculture. Aust J Agric Res 48:267–293CrossRefGoogle Scholar
  115. Unkovich MJ, Herridge DF, Peoples MB, Cadisch G, Boddey RM, Giller KE et al (2008) Measuring plant-associated nitrogen fixation in agricultural systems. ACIAR, Canberra Australia (in press)Google Scholar
  116. Urquiaga S, Cruz KHS, Boddey RM (1992) Contribution of nitrogen fixation to sugar cane: nitrogen-15 and nitrogen balance estimates. Soil Sci Soc Am J 56:105–114Google Scholar
  117. Vallis I (1972) Soil nitrogen changes under continuously grazed legume–grass pastures in subtropical coastal Queensland. Aust J Exp Agric Anim Husb 12:495–501CrossRefGoogle Scholar
  118. van Kessel C, Hartley C (2000) Agricultural management of grain legumes: has it led to an increase in nitrogen fixation? Field Crops Res 65:165–181CrossRefGoogle Scholar
  119. Vessey JK (1994) Measurement of nitrogenase activity in legume root nodules: in defense of the acetylene reduction assay. Plant Soil 158:151–162CrossRefGoogle Scholar
  120. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750Google Scholar
  121. Walley FL, Clayton GW, Miller PR, Carr PM, Lafond GP (2007) Nitrogen economy of pulse production in the northern great plains. Agron J 99:1710–1718CrossRefGoogle Scholar
  122. Wani SP, Rupela OP, Lee KK (1995) Sustainable agriculture in the semi-arid tropics through biological nitrogen fixation in grain legumes. Plant Soil 174:29–49CrossRefGoogle Scholar
  123. Warembourg FR, Montange D, Bardin R (1982) The simultaneous use of 14CO2 and 15N2 labelling techniques to study the carbon and nitrogen economy of legumes grown under natural conditions. Physiol Plant 56:46–55CrossRefGoogle Scholar
  124. Weber CR (1966) Nodulating and nonnodulating soybean isolines: II. Response to applied nitrogen and modified soil conditions. Agron J 58:46–47Google Scholar
  125. Wetselaar R, Jakobsen P, Chaplin GR (1973) Nitrogen balance in crop systems in tropical Australia. Soil Biol Biochem 5:35–40CrossRefGoogle Scholar
  126. Witty JF, Minchin FR (1988) Measurement of nitrogen fixation by the acetylene reduction assay: myths and mysteries. In: Beck DP, Materon LA (eds) Nitrogen fixation by legumes in Mediterranean agriculture. Martinus Nijhoff, Dordrecht, pp 331–344Google Scholar
  127. Witty JF, Rennie RJ, Atkins CA (1988) 15N methods for assessing N2 fixation under field conditions. In: Summerfield RJ (ed) World crops: cool season food legumes. Kluwer Academic, London, pp 715–730Google Scholar
  128. Yasmin K, Cadisch G, Baggs EM (2006) Comparing 15N-labelling techniques for enriching above- and below ground components of the plant–soil system. Soil Biol Biochem 38:397–400Google Scholar
  129. Yoneyama T, Muraoka T, Kim TH, Dacanay EV, Nakanishi Y (1997) The natural 15N abundance of sugarcane and neighbouring plants in Brazil, the Philippines and Miyako (Japan). Plant Soil 189:239–244CrossRefGoogle Scholar
  130. Zebarth BJ, Alder V, Sheard RW (1991) In situ labelling of legume residues with a foliar application of an N-15 enriched urea solution. Commun Soil Sci Plant Anal 22:437–447Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • David F. Herridge
    • 1
  • Mark B. Peoples
    • 2
  • Robert M. Boddey
    • 3
    Email author
  1. 1.New South Wales Department of Primary IndustriesCalalaAustralia
  2. 2.CSIRO Plant IndustryCanberraAustralia
  3. 3.Embrapa-AgrobiologiaSeropédicaBrazil

Personalised recommendations