Journal of Soils and Sediments

, Volume 12, Issue 2, pp 150–160 | Cite as

Impact of global climate change and fire on the occurrence and function of understorey legumes in forest ecosystems




The objective of this review was to provide a better understanding of how global climate change and fire influence the occurrence of understorey legumes and thereby biological nitrogen (N) fixation rates in forest ecosystems. Legumes are interesting models since they represent an interface between the soil, plant, and microbial compartments, and are directly linked to nutrient cycles through their ability to fix N. As such, they are likely to be affected by environmental changes.

Result and discussion

Biological N fixation has been shown to increase under enriched CO2 conditions, but is constrained by the availability of phosphorus and water. Climate change can also influence the species composition of legumes and their symbionts through warming, altered rainfall patterns, or changes in soil physicochemistry, which could modify the effectiveness of the symbiosis. Additionally, global climate change may increase the occurrence and intensity of forest wildfires thereby further influencing the distribution of legumes. The establishment of leguminous species is generally favored by fire, as is N2 fixation. This fixed N could therefore replenish the N lost through volatilization during the fire. However, fire may also generate shifts in the associated microbial community which could affect the outcome of the symbiosis.


Understorey legumes are important functional species, and even when they cannot reasonably be expected to reestablish the nutrient balance in forest soils, they may be used as indicators to monitor nutrient fluxes and the response of forest ecosystems to changing environmental conditions. This would be helpful to accurately model ecosystem N budgets, and since N is often a limiting factor to plant growth and a major constraint on C storage in ecosystems, would allow us to assess more precisely the potential of these forests for C sequestration.


Fire Global climate change Nitrogen fixation Rhizobia Understorey legumes 


  1. Abera G, Wolde-meskel E, Bakken LR (2011) Carbon and nitrogen mineralization dynamics in different soils of the tropics amended with legume residues and contrasting soil moisture contents. Biol Fertil Soils. doi:10.1007/s00374-011-0607-8
  2. Adams MA, Simon J, Pfautsch S (2010) Woody legumes: a (re)view from the South. Tree Physiol 30:1072–1082CrossRefGoogle Scholar
  3. Allen CD (2007) Interactions across spatial scales among forest dieback, fire, and erosion in northern New Mexico landscapes. Ecosystems 10:797–808CrossRefGoogle Scholar
  4. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EHT, Gonzales P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684CrossRefGoogle Scholar
  5. Atkin OK, Schortemeyer M, McFarlane N, Evans JR (1999) The response of fast- and slow-growing Acacia species to elevated atmospheric CO2: an analysis of the underlying components of relative growth rate. Oecologia 120:544–554CrossRefGoogle Scholar
  6. Barrios B, Arellano G, Koptur S (2011) The effects of fire and fragmentation on occurrence and flowering of a rare perennial plant. Plant Ecol 212:1057–1067CrossRefGoogle Scholar
  7. Bastias BA, Huang ZQ, Blumfield T, Xu ZH, Cairney JWG (2006a) Influence of repeated prescribed burning on the soil fungal community in an eastern Australian wet sclerophyll forest. Soil Biol Biochem 38:3492–3501CrossRefGoogle Scholar
  8. Bastias BA, Xu Z, Cairney JWG (2006b) Influence of long-term repeated prescribed burning on mycelial communities of ectomycorrhizal fungi. New Phytol 172:149–158CrossRefGoogle Scholar
  9. Beedlow PA, Tingey DT, Phillips DL, Hogsett WE, Olszyk DM (2004) Rising atmospheric CO2 and carbon sequestration in forests. Front Ecol Environ 2:315–322CrossRefGoogle Scholar
  10. Blankinship JC, Niklaus PA, Hungate BA (2011) A meta-analysis of responses of soil biota to global change. Oecologia 165:553–565CrossRefGoogle Scholar
  11. Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449CrossRefGoogle Scholar
  12. Busse MD, Jurgensen MF, Page-Dumroese DS, Powers RF (2007) Contribution of actinorhizal shrubs to site fertility in a Northern California mixed pine forest. For Ecol Manage 244:68–75CrossRefGoogle Scholar
  13. Caldwell TG, Johnson DW, Miller WW, Qualls RG (2002) Forest floor carbon and nitrogen losses due to prescription fire. Soil Sci Soc Am J 66:262–267CrossRefGoogle Scholar
  14. Canadell JG, Raupach MR (2008) Managing forests for climate change mitigation. Science 320:1456–1457CrossRefGoogle Scholar
  15. Cardinale BJ (2011) Biodiversity improves water quality through niche partitioning. Nature 472:86–89CrossRefGoogle Scholar
  16. Chen CR, Xu ZH (2010) Forest ecosystem responses to environmental changes: the key regulatory role of biogeochemical cycling. J Soils Sediments 10:210–214CrossRefGoogle Scholar
  17. IPCC Climate Change (2007) Synthesis Report. Summary for Policymakers.
  18. Coetsee C, Bond WJ, February EC (2010) Frequent fire affects soil nitrogen and carbon in an African savanna by changing woody cover. Oecologia 162:1027–1034CrossRefGoogle Scholar
  19. Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332:53–58CrossRefGoogle Scholar
  20. DeLuca TH, Aplet GH (2008) Charcoal and carbon storage in forest soils of the Rocky Mountain West. Front Ecol Environ 6:1–7CrossRefGoogle Scholar
  21. DeLuca TH, Zackrisson O, Gundale MJ, Nilsson MC (2011) Ecosystem feedbacks and nitrogen fixation in boreal forests. Science 320:1181CrossRefGoogle Scholar
  22. Diédhiou AG, Guèye O, Diabaté M, Prin Y, Duponnois R, Dreyfus B, Bâ AM (2005) Contrasting responses to ectomycorrhizal inoculation in seedlings of six tropical African tree species. Mycorrhiza 16:11–17CrossRefGoogle Scholar
  23. Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357CrossRefGoogle Scholar
  24. Drigo B, Kowalchuk GA, van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679CrossRefGoogle Scholar
  25. Duponnois R, Colombet A, Hien V, Thioulouse J (2005) The mycorrhizal fungus Glomus intraradices and rock phosphate amendment influence plant growth and microbial activity in the rhizosphere of Acacia holosericea. Soil Biol Biochem 37:1460–1468CrossRefGoogle Scholar
  26. Essendoubi M, Brhada F, Eljamali JE, Filali-Maltouf A, Bonnassie S, Georgeault S, Blanco C, Jebbar M (2007) Osmoadaptative responses in the rhizobia nodulating Acacia isolated from south-eastern Moroccan Sahara. Environ Microbiol 9:603–611CrossRefGoogle Scholar
  27. Finzi A, Norby RJ, Calfapietra C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Iversen CM, Jackson RB, Kubiske ME, Ledford J, Liberloo M, Oren R, Polle A, Pritchard S, Zak DR, Schlesinger WH, Ceulemans R (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci USA 104(35):14014–14019CrossRefGoogle Scholar
  28. Finzi AC, Austin AT, Cleland EE, Frey SD, Houlton BZ, Wallenstein MD (2011) Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9(1):61–67CrossRefGoogle Scholar
  29. Forrester DI, Bauhus J, Cowie AL (2005) Nutrient cycling in a mixed-species plantation of Eucalyptus globulus and Acacia mearnsii. Can J For Res 35:2942–2950CrossRefGoogle Scholar
  30. Gebrekirstos A, van Noordwijk M, Neufeldt H, Mitlöhner R (2011) Relationships of stable carbon isotopes, plant water potential and growth: an approach to asses water use efficiency and growth strategies of dry land agroforestry species. Trees 25:95–102CrossRefGoogle Scholar
  31. Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296CrossRefGoogle Scholar
  32. Guinto DF, House APN, Xu ZH, Saffigna PG (1999a) Impacts of repeated fuel reduction burning on tree growth, mortality and recruitment in mixed species eucalypt forests of southeast Queensland, Australia. For Ecol Manage 115:13–27CrossRefGoogle Scholar
  33. Guinto DF, Saffigna PG, Xu ZH, House APN, Perera MCS (1999b) Soil nitrogen mineralization and organic matter composition revealed by 13C NMR spectroscopy under repeated prescribed burning in eucalypt forests of south-east Queensland. Aust J Soil Res 37:123–135CrossRefGoogle Scholar
  34. Guinto DF, Xu ZH, House APN, Saffigna PG (2000) Assessment of N2 fixation by understorey acacias in recurrently burnt eucalypt forests of subtropical Australia using 15N isotope dilution techniques. Can J For Res 30:112–121Google Scholar
  35. Hainds MJ, Mitchell RJ, Palik BJ, Boring LR, Gjerstad DH (1999) Distribution of native legumes (Leguminoseae) in frequently burned longleaf pine (Pinaceae)–wiregrass (Poaceae) ecosystems. Am J Bot 86:1606–1614CrossRefGoogle Scholar
  36. Hart SC, DeLuca TH, Newman GS, MacKenzie MD, Boyle SI (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. For Ecol Manage 220:166–184CrossRefGoogle Scholar
  37. Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 45:289–292CrossRefGoogle Scholar
  38. Hendricks JL, Boring LR (1999) N2-fixation by native herbaceous legumes in burned pine ecosystems of the southwestern United States. For Ecol Manage 113:167–177CrossRefGoogle Scholar
  39. Hiers JK, Wyatt R, Mitchell RJ (2000) The effects of fire regime on legume reproduction in longleaf pine savannas: is a season selective? Oecologia 125:521–530CrossRefGoogle Scholar
  40. Hoque MS, Broadhurst LM, Thrall PH (2011) Genetic characterization of root-nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across south-eastern Australia. Int J Syst Evol Microbiol 61:299–309CrossRefGoogle Scholar
  41. Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330CrossRefGoogle Scholar
  42. Hughes L (2003) Climate change and Australia: Trends, projections and impacts. Austral Ecol 28:423–443CrossRefGoogle Scholar
  43. Hungate BA, Stiling PD, Dijkstra P, Johnson DW, Ketterer ME, Hymus GJ, Hinkle CR, Drake BG (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291CrossRefGoogle Scholar
  44. Jablonski LM, Wang X, Curtis PS (2002) Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol 156:9–26CrossRefGoogle Scholar
  45. Johnson DW, Susfalk RB, Dahlgren RA, Klopatek JM (1998) Fire is more important than water for nitrogen fluxes in semi-arid forests. Environ Sci Pol 1:79–86CrossRefGoogle Scholar
  46. Johnson DW, Murphy JF, Susfalk RB, Caldwell TG, Miller WW, Walker RF, Powerset RF (2005) The effects of wildfire, salvage logging, and post-fire N fixation on the nutrient budgets of a Sierran forest. For Ecol Manage 220:155–165CrossRefGoogle Scholar
  47. Langley JA, Megonigal JP (2010) Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466:96–99CrossRefGoogle Scholar
  48. Laurance WF, Dell B, Turton SM, Lawes MJ, Hutley LB, McCallum H, Dale P, Bird M, Hardy G, Prideaux G, Gawne B, McMahon CR, Yu R, Hero JM, Schwarzkopf L, Krockenberger A, Douglas M, Silvester E, Mahony M, Vella K, Saikia U, Wahren CH, Xu ZH, Smith B, Cocklin C (2011) The ten Australian ecosystems most vulnerable to tipping points. Biol Conserv 144:1472–1480CrossRefGoogle Scholar
  49. Leach MK, Givnish TJ (1996) Ecological determinants of species loss in remnant prairies. Science 273:1555–1558CrossRefGoogle Scholar
  50. Liu JX, Zhou GY, Zhang DQ, Xu ZH, Duan HL, Deng Q, Zhao L (2010) Carbon dynamics in subtropical forest soil: effects of atmospheric carbon dioxide enrichment and nitrogen addition. J Soils Sediments 10:730–738CrossRefGoogle Scholar
  51. Liu JX, Zhou GY, Xu ZH, Duan HL, Li YL, Zhang DQ (2011a) Photosynthesis acclimation, leaf nitrogen concentration, and growth of four tree species over 3 years in response to elevated carbon dioxide and nitrogen treatment in subtropical China. J Soils Sediments 11:1155–1164CrossRefGoogle Scholar
  52. Liu JX, Xu ZH, Zhang DQ, Zhou GY, Deng Q, Duan HL, Zhao L, Wang CL (2011b) Effects of carbon dioxide enrichment and nitrogen addition on inorganic carbon leaching in subtropical model forest ecosystems. Ecosystem 16:683–697CrossRefGoogle Scholar
  53. Lüscher A, Hartwig UA, Suter D, Nösberger J (2000) Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Glob Change Biol 6:655–662CrossRefGoogle Scholar
  54. Magnani F, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Delzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentini R, Grace G (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:848–850CrossRefGoogle Scholar
  55. Mao XA, Xu ZH, Luo RS, Mathers NJ, Zhang YH, Saffigna PG (2002) Nitrate in soil humic acids revealed by nitrogen-14 nuclear magnetic resonance spectroscopy. Aust J Soil Res 40:717–726CrossRefGoogle Scholar
  56. Mohamed A, Härdtle W, Jirjahn B, Niemeyer T, von Oheimb G (2007) Effects of prescribed burning on plant available nutrients in dry heathland ecosystems. Plant Ecol 189:279–289CrossRefGoogle Scholar
  57. National Forest Inventory (2007) Australia’s Forests at a Glance. National Forest Inventory, Bureau of Rural Sciences, CanberraGoogle Scholar
  58. Neary DG, Klopatek CC, DeBano LF, Folliott PF (1999) Fire effects on belowground sustainability: a review and synthesis. For Ecol Manage 122:51–71CrossRefGoogle Scholar
  59. Nelson JA, Morgan JA, LeCain DR, Mosier AR, Milchunas DG, Parton BA (2004) Elevated CO2 increases soil moisture and enhances plant water relations in a long-term field study in semi-arid shortgrass steppe of Colorado. Plant Soil 259:169–179CrossRefGoogle Scholar
  60. Newland JA, DeLuca TH (2000) Influence of fire on native nitrogen-fixing plants and soil nitrogen status in ponderosa pine—Douglas-fir forests in western Montana. Can J Forest Res 30:274–282CrossRefGoogle Scholar
  61. Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci U S A 101(26):9689–9693CrossRefGoogle Scholar
  62. Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C, Schäfer KVR, McCarthy H, Hendrey G, McNulty SG, Katul GG (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472CrossRefGoogle Scholar
  63. Owens PN, Xu ZH (2011) Recent advances and future directions in soils and sediments research. J Soils Sediments 11:875–888CrossRefGoogle Scholar
  64. Penman TD, York A (2010) Climate and recent fire history affect fuel loads in Eucalyptus forests: implications for fire management in a changing climate. For Ecol Manage 260:1791–1797CrossRefGoogle Scholar
  65. Peñuelas J, Rutishauser T, Filella I (2009) Phenology feedbacks on climate change. Science 324:887–888CrossRefGoogle Scholar
  66. Pritchard SG (2011) Soil organisms and global climate change. Plant Pathol 60:82–99CrossRefGoogle Scholar
  67. Räsänen LA, Saijets S, Jokinen K, Lindström K (2004) Evaluation of the roles of two compatible solutes, glycine betaine and trehalose, for the Acacia senegalSinorhizobium symbiosis exposed to drought stress. Plant Soil 260:237–251CrossRefGoogle Scholar
  68. Reich PB, Tilman D, Craine J, Ellsworth D, Tjoelker MG, Knops J, Wedin D, Naeem S, Bahauddin D, Goth J, Bengtson W, Lee TD (2001) Do species and functional groups differ in acquisition and use of C, N and water under varying atmospheric CO2 and N availability regimes? A field test with 16 grassland species. New Phytol 150:435–448CrossRefGoogle Scholar
  69. Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925CrossRefGoogle Scholar
  70. Rogers A, Gibon Y, Stitt M, Morgan PB, Bernacchi CJ, Ort DR, Long SP (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell Environ 29:1651–1658CrossRefGoogle Scholar
  71. Rogers A, Ainsworth EA, Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 151:1009–1016CrossRefGoogle Scholar
  72. Sarr A, Lesueur D (2007) Influence of soil fertility on the rhizobial competitiveness for nodulation of Acacia senegal and Acacia nilotica provenances in nursery and field conditions. World J Microbiol Biotechnol 23:705–711CrossRefGoogle Scholar
  73. Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Change Biol 1:77–91CrossRefGoogle Scholar
  74. Schortemeyer M, Atkin OK, McFarlane N, Evans JR (2002) N2 fixation by Acacia species increases under elevated atmospheric CO2. Plant Cell Environ 25:567–579CrossRefGoogle Scholar
  75. Serraj R, Sinclair TR, Allen LH (1998) Soybean nodulation and N2 fixation response to drought under carbon dioxide enrichment. Plant Cell Environ 21:491–500CrossRefGoogle Scholar
  76. Sitch S, Huntingford C, Gedney N, Levy PE, Lomas M, Piao SL, Betts R, Ciais P, Cox P, Friedlingstein P, Jones CD, Prentice IC, Woodward FI (2008) Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs). Glob Change Biol 14:2015–2039CrossRefGoogle Scholar
  77. Soussana JF, Hartwig UA (1996) The effects of elevated CO2 on symbiotic N2 fixation: a link between the carbon and nitrogen cycles in grassland ecosystems. Plant Soil 187:321–332CrossRefGoogle Scholar
  78. Sprent JI (1995) Legume trees and shrubs in the tropics: N2 fixation in perspective. Soil Biol Biochem 27:401–407CrossRefGoogle Scholar
  79. Sun F, Kuang Y, Wen D, Xu Z, Li J, Zuo W, Hou E (2010) Long-term tree growth rate, water use efficiency, and tree ring nitrogen isotope composition of Pinus massoniana L. in response to global climate change and local nitrogen deposition in Southern China. J Soils Sediments 10:1453–1465CrossRefGoogle Scholar
  80. Thorne SH, Williams HD (1997) Adaptation to nutrient starvation in Rhizobium leguminosarum bv. phaseoli: analysis of survival, stress resistance, and changes in macromolecular synthesis during entry to and exit from stationary phase. J Bacteriol 179:6894–6901Google Scholar
  81. Thrall PH, Bever JD, Slattery JF (2008) Rhizobial mediation of Acacia adaptation to soil salinity: evidence of underlying trade-offs and tests of expected patterns. J Ecol 96:746–755CrossRefGoogle Scholar
  82. Thrall PH, Broadhurst LM, Hoque MS, Bagnall DJ (2009) Diversity and salt tolerance of native Acacia rhizobia isolated from saline and non-saline soils. Austral Ecol 34:950–963CrossRefGoogle Scholar
  83. Thrall PH, Laine AL, Broadhurst LM, Bagnall DJ, Brockwell J (2011) Symbiotic effectiveness of rhizobial mutualists varies in interactions with native Australian legume genera. PLoS One 6(8):e23545CrossRefGoogle Scholar
  84. Tobita H, Uemura A, Kitao M, Kitaoka S, Utsugi H (2010) Interactive effects of elevated CO2, phosphorus deficiency, and soil drought on nodulation and nitrogenase activity in Alnus hirsuta and Alnus maximowiczii. Symbiosis 50:59–69CrossRefGoogle Scholar
  85. Treseder KK, Mack MC, Cross A (2004) Relationships among fires, fungi, and soil dynamics in Alaskan boreal forests. Ecol Appl 14:1826–1838CrossRefGoogle Scholar
  86. van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occuring plant. New Phytol 157:569–578CrossRefGoogle Scholar
  87. van Groenigen KJ, Six J, Hungate BA, de Graaff MA, van Breemen N, van Kessel C (2006) Element interactions limit soil carbon storage. Proc Natl Acad Sci U S A 103(17):6571–6574CrossRefGoogle Scholar
  88. Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochem 46:179–202Google Scholar
  89. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochem 57:1–45CrossRefGoogle Scholar
  90. West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530CrossRefGoogle Scholar
  91. Westerling AL, Hidalgo HG, Cayan DR, Swetnam TW (2006) Warming and earlier spring increase Western U.S. forest wildfire activity. Science 313:940–943CrossRefGoogle Scholar
  92. Xu ZH, Chen CR (2006) Fingerprinting global climate change and forest management within rhizosphere carbon and nutrient cycling processes. Environ Sci Pollut Res 13:293–298CrossRefGoogle Scholar
  93. Xu ZH, Chen CR, He JZ, Liu JX (2009) Trends and challenges in soil research 2009: linking global climate change to local long-term forest productivity. J Soils Sediments 9:83–88CrossRefGoogle Scholar
  94. Zahran HH (2001) Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. J Biotech 91:143–153CrossRefGoogle Scholar
  95. Zanetti S, Hartwig UA, Lüscher A, Hebeisen T, Frehner M, Fischer BU, Hendrey GR, Blum H, Nosberger J (1996) Stimulation of symbiotic N2 fixation in Trifolium repens L. under elevated atmospheric pCO2 in a grassland ecosystem. Plant Physiol 112:575–583Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Environmental Futures Centre and School of Biomolecular and Physical SciencesGriffith UniversityNathanAustralia

Personalised recommendations