Agronomy for Sustainable Development

, Volume 34, Issue 2, pp 417–427 | Cite as

N2-fixing trees and the transfer of fixed-N for sustainable agroforestry: a review

Review Article

Abstract

Many tropical areas lack soil nitrogen (N), an essential nutrient for plant growth and the production of food. Commercial N fertilisers are expensive, with only a fraction of this nutrient reaching the plant, which limits efficiency and potentially increases water contamination. Dinitrogen (N2)-fixing trees are a promising alternative to sustainably fertilise crops. The use of N2-fixing trees in tropical agriculture has garnered attention from researchers, development organisations, governments, and farmers in recent years as a revival of pro-environmental practices. Dinitrogen (N2)-fixing trees can establish in N-deficient soils, replace N lost in harvest and provide an as-of-yet not fully realised benefit to ecosystem services. High N2-fixation rates, upwards of 92 %, have been measured in some N2-fixing trees, using the 15N natural abundance method. The recovery of this fixed-N by associated perennial crops is of particular interest in tropical agroforestry systems. Here, we review N transfer pathways from trees to perennial crops in agroforestry. We focus on Theobroma cacao and Coffea arabica. We also draw on agroforestry systems with herbaceous alleys. We identify three pathways of N transfer from N2-fixers to non-N2-fixing crops: (1) decomposition and mineralisation of organic compounds, e.g., litter, prunings, roots, and nodules, (2) root-to-root direct transfer via exudation, and (3) common mycorrhizal networks. Both 15N natural abundance and 15N enrichment techniques have been used to study N transfer. However, various factors limit the accuracy of estimates within agroforestry systems. Under field conditions, the major limits are (1) improper reference selection and (2) unrepresentative sampling of the receiver plant and/or donor N source. We highlight key findings and provide recommendations to tackle these obstacles.

Keywords

Agriculture and biodiversity Coffea arabica N2-fixing trees 15N natural abundance 15N isotopic dilution Root exchange Theobroma cacao Tropical agroforestry 

References

  1. Araujo ASF, Leite LFC, Iwata BF, Lira MA, Xavier GR, Figueiredo MVB (2012) Microbiological process in agroforestry systems. A review. Agron Sustain Dev 32:215–226. doi:10.1007/s13593-011-0026-0 CrossRefGoogle Scholar
  2. Bainard LD, Klironomos JN, Gordon AM (2011) Arbuscular mycorrhizal fungi in tree-based intercropping systems: A review of their abundance and diversity. Pedobiol Int J Soil Biol 54:57–61. doi:10.1016/j.pedobi.2010.11.001 Google Scholar
  3. Bala A, Murphy PJ, Osunde AO, Giller KE (2003) Nodulation of tree legumes and ecology of their native rhizobial populations in tropical soils. Appl Soil Ecol 22:211–223. doi:10.1016/S0929-1393(02)00157-9 CrossRefGoogle Scholar
  4. Barea JM, Azcon-Aguilar C, Azcon R (1987) Vesicular-arbuscular mycorrhiza improve both symbiotic N2 fixation and N uptake from soil as assessed with a 15N technique under field conditions. New Phytol 106:717–725. doi:10.1111/j.1469-8137.1987.tb00172.x CrossRefGoogle Scholar
  5. Beer J, Muschler R, Kass D, Somarriba E (1998) Shade management in coffee and cacao plantations. Agrofor Syst 7:103–114. doi:10.1007/978-94-015-9008-2_6 CrossRefGoogle Scholar
  6. 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 57:235–270. doi:10.1023/A:1009890514844 CrossRefGoogle Scholar
  7. Bouillet JP, Laclau JP, Gonçalves JLM, Moreira MZ, Trivelin PCO, Jourdan C, Silva EV, Piccolo MC, Tsai SM, Galiana A (2008) Mixed-species plantations of Acacia mangium and Eucalyptus grandis in Brazil: 2: Nitrogen accumulation in the stands and biological N2 fixation. For Eco Manage 255:3918–3930. doi:10.1016/j.foreco.2007.10.050 Google Scholar
  8. Carlsson G, Huss-Danell K (2013) Does nitrogen transfer between plants confound 15N-based quantifications of N2 fixation? Plant Soil. doi:10.1007/s11104-013-1802-1 Google Scholar
  9. Danso SKA, Bowen GD, Sanginga N (1992) Biological nitrogen fixation in trees in agro-ecosystems. Plant Soil 141:177–196. doi:10.1007/978-94-017-0910-1_10 CrossRefGoogle Scholar
  10. Daudin D, Sierra J (2008) Spatial and temporal variation of below-ground N transfer from a leguminous tree to an associated grass in an agroforestry system. Agric Ecosyst Environ 126:275–280. doi:10.1016/j.agee.2008.02.009 CrossRefGoogle Scholar
  11. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559. doi:10.1146/annurev.ecolsys.33.020602.095451 CrossRefGoogle Scholar
  12. Dommergues YR (1995) Nitrogen fixation by trees in relation to soil nitrogen economy. Fertil Res 42:215–230. doi:10.1007/BF00750516 CrossRefGoogle Scholar
  13. Dulormne M, Sierra J, Nygren P, Cruz P (2003) Nitrogen-fixation dynamics in a cut-and-carry silvopastoral system in the subhumid conditions of Guadeloupe, French Antilles. Agrofor Syst 59:121–129. doi:10.1023/A:1026387711571 CrossRefGoogle Scholar
  14. Elgersma A, Schlepers H, Nassiri M (2000) Interactions between perennial ryegrass (Lolium perenne L.) and white clover (Trifolium repens L.) under contrasting nitrogen availability: productivity, seasonal patterns of species composition, N2 fixation, N transfer and N recovery. Plant Soil 21:281–299. doi:10.1023/A:1004797106981 CrossRefGoogle Scholar
  15. FAOStat (2011) http://www.fao.org/corp/statistics/en/. Accessed on 15 March 2013
  16. Giller KE (2001) Nitrogen fixation in tropical cropping systems, 2nd edn. CABI Publishing, WallingfordCrossRefGoogle Scholar
  17. Gylfadóttir T, Helgadóttir A, Høgh-Jensen H (2007) Consequences of including adapted white clover in northern European grassland: transfer and deposition of nitrogen. Plant Soil 297:93–104. doi:10.1007/s11104-007-9323-4 CrossRefGoogle Scholar
  18. Haggar JP, Tanner EVJ, Beer JW, Kass DCL (1993) Nitrogen dynamics of tropical agroforestry and annual cropping systems. Soil Biol Biochem 25:1363–1378. doi:10.1016/0038-0717(93)90051-C CrossRefGoogle Scholar
  19. Haystead A, Malajczuk N, Grove TS (1988) Underground transfer of nitrogen between pasture plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytol 108:417–423. doi:10.1111/j.1469-8137.1988.tb04182.x CrossRefGoogle Scholar
  20. He X, Xu M, Qiu GY, Zhou J (2009) Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. J Plant Ecol 2:107–118. doi:10.1093/jpe/rtp015 CrossRefGoogle Scholar
  21. Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330. doi:10.1038/nature07028 PubMedCrossRefGoogle Scholar
  22. Ingleby K, Wilson J, Munro RC, Cavers S (2007) Mycorrhizas in agroforestry: spread and sharing of arbuscular mycorrhizal fungi between trees and crops: complementary use of molecular and microscopic approaches. Plant Soil 294:125–136. doi:10.1007/s11104-007-9239-z CrossRefGoogle Scholar
  23. Isaac ME, Kimaro AA (2011) Diagnosis of nutrient imbalances with vector analysis in agroforestry systems. J Environ Qual 40:860–866. doi:10.2134/jeq2010.0144 PubMedCrossRefGoogle Scholar
  24. Isaac ME, Timmer VR, Quashie-Sam SJ (2007) Shade tree effects in an 8-year-old cocoa agroforestry system: biomass and nutrient diagnosis of Theobroma cacao by vector analysis. Nutr Cycl Agroecosyst 78:155–165. doi:10.1007/s10705-006-9081-3 CrossRefGoogle Scholar
  25. Isaac ME, Harmand JM, Lesueur D, Lelon J (2011) Tree age and soil phosphorus conditions influence N2-fixation rates and soil N dynamics in natural populations of Acacia senegal. For Ecol Manag 261:582–588CrossRefGoogle Scholar
  26. Isaac ME, Hinsinger P, Harmand JM (2012) Nitrogen and phosphorus economy of a legume tree-cereal intercropping system under controlled conditions. Sci Total Environ. doi:10.1016/j.scitotenv.2011.12.071 PubMedGoogle Scholar
  27. Jalonen R, Sierra J (2012) Temporal variation of N isotopic composition of decomposing legume roots and its implications to N cycling estimates in 15N tracer studies in agroforestry systems. Appl Environ Soil Sci Artic. doi:10.1155/2012/506302, ID 506302Google Scholar
  28. Jalonen R, Nygren P, Sierra J (2009a) Root exudates of a legume tree as a nitrogen source for a tropical fodder grass. Nutr Cycl Agroecosyst 85:203–213. doi:10.1007/s10705-009-9259-6 CrossRefGoogle Scholar
  29. Jalonen R, Nygren P, Sierra J (2009b) Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant Cell Environ 32:1366–1376. doi:10.1111/j.1365-3040.2009.02004.x PubMedCrossRefGoogle Scholar
  30. Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, Alves BJR, Morrison MJ (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries—a review. Agron Sustain Dev 32:329–364. doi:10.1007/s13593-011-0056-7 CrossRefGoogle Scholar
  31. Kähkölä A-K, Nygren P, Leblanc HA, Pennanen T, Pietikäinen J (2012) Leaf and root litter of a legume tree as nitrogen sources for cacaos with different root colonisation by arbuscular mycorrhizae. Nutr Cycl Agroecosyst 92:51–65. doi:10.1007/s10705-011-9471-z CrossRefGoogle Scholar
  32. Kurppa M, Leblanc HA, Nygren P (2010) Detection of nitrogen transfer from N2-fixing shade trees to cacao saplings in 15N labelled soil: ecological and experimental considerations. Agrofor Syst 80:223–239. doi:10.1007/s10457-010-9327-6 CrossRefGoogle Scholar
  33. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207. doi:10.1111/j.1469-8137.2008.02630.x PubMedCrossRefGoogle Scholar
  34. Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochem 46:45–65. doi:10.1007/BF01007573 Google Scholar
  35. Moyer-Henry KA, Burton JW, Israel DW, Rufty TW (2006) Nitrogen transfer between plants: a 15N natural abundance study with crop and weed species. Plant Soil 282:7–20. doi:10.1007/s11104-005-3081-y CrossRefGoogle Scholar
  36. Nair PKR, Buresh RJ, Mugendi DN, Latt CR (1998) Nutrient cycling in tropical agroforestry systems: myths and science. In: Buck LE, Lassoie JP, Fernandes ECM (eds) Agroforestry in sustainable agriculture. CRC Press, Boca Raton, pp 1–32Google Scholar
  37. Nygren P, Leblanc HA (2009) Natural abundance of 15N in two cacao plantations with legume and non-legume shade trees. Agrofor Syst 76:303–315. doi:10.1007/s10457-008-9160-3 CrossRefGoogle Scholar
  38. Nygren P, Cruz P, Domenach AM, Vaillant V, Sierra J (2000) Influence of forage harvesting regimes on dynamics of biological dinitrogen fixation of a tropical woody legume. Tree Physiol 20:41–48PubMedCrossRefGoogle Scholar
  39. Nygren P, Fernández MP, Harmand J-M, Leblanc HA (2012) Symbiotic dinitrogen fixation by trees: an underestimated resource in agroforestry systems? Nutr Cycl Agroecosyst. doi:10.1007/s10705-012-9542-9 Google Scholar
  40. Paynel F, Murray PJ, Cliquet JB (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229:235–243. doi:10.1023/A:1004877214831 CrossRefGoogle Scholar
  41. Pirhofer-Walzl K, Rasmussen J, Høgh-Jensen H, Eriksen J, Søegaard K, Rasmussen J (2011) Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant Soil. doi:10.1007/s11104-011-0882-z Google Scholar
  42. Rao AV, Giller KE (1993) Nitrogen fixation and its transfer from Leucaena to grass using 15N. N For Ecol Manag 61:221–227CrossRefGoogle Scholar
  43. Rowe EC, Hairiah K, Giller KE, van Noordwijk M, Cadisch G (1999) Testing the safety-net role of hedgerow trees by 15N placement at different soil depths. Agrofor Syst 43:81–93CrossRefGoogle Scholar
  44. Schroth G, Lehmann J, Rodrigues MRL, Barros E, Macêdo JLV (2001) Plant-soil interactions in multistrata agroforestry in the humid tropics. Agrofor Syst 53:85–102CrossRefGoogle Scholar
  45. Schroth G, da Fonseca GAB, Harvey CA, Gascon C, Vasconcelos HL, Izac A-MN (2004) Agroforestry and biodiversity conservation in tropical landscapes. Island Press, WashingtonGoogle Scholar
  46. Sierra J, Daudin D (2010) Limited 15N transfer from stem-labeled leguminous trees to associated grass in an agroforestry system. Eur J Agron 32:240–242. doi:10.1016/j.eja.2009.11.003 CrossRefGoogle Scholar
  47. Sierra J, Nygren P (2006) Transfer of N fixed by a legume tree to the associated grass in a tropical silvopastoral system. Soil Biol Biochem 38:1893–1903. doi:10.1016/j.soilbio.2005.12.012 CrossRefGoogle Scholar
  48. Sierra J, Dulormne M, Desfontaines L (2002) Soil nitrogen as affected by Gliricidia sepium in a silvopastoral system in Guadeloupe, French Antilles. Agrofor Syst 54:87–97. doi:10.1023/A:1015025401946 CrossRefGoogle Scholar
  49. Sierra J, Daudin D, Domenach A, Nygren P, Desfontaines L (2007) Nitrogen transfer from a legume tree to the associated grass estimated by the isotopic signature of tree root exudates: a comparison of the 15N leaf feeding and natural 15N abundance methods. Eur J Agron 27:178–186. doi:10.1016/j.eja.2007.03.003 CrossRefGoogle Scholar
  50. Simard SW, Durali D, Jones M (2003) Carbon and nutrient fluxes within and between mycorrhizal plants. Ecol Stud 157:33–74. doi:10.1007/978-3-540-38364-2_2 CrossRefGoogle Scholar
  51. Snoeck D, Zapata F, Domenach A-M (2000) Isotopic evidence of the transfer of nitrogen fixed by legumes to coffee trees. Biotechnol Agron Soc Environ 4:95–100Google Scholar
  52. Ståhl L, Nyberg G, Högberg P, Buresh RJ (2002) Effects of planted tree fallows on soil nitrogen dynamics aboveground and root biomass, N2-fixation and subsequent maize crop productivity in Kenya. Plant Soil 243:103–117CrossRefGoogle Scholar
  53. Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey R, Giller KE, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. ACIAR, Canberra, Australia, 258 p. http://aciar.gov.au/publication/MN136

Copyright information

© INRA and Springer-Verlag France 2013

Authors and Affiliations

  1. 1.Department of GeographyUniversity of TorontoTorontoCanada
  2. 2.Department of Physical and Environmental Sciences and the Center for Critical Development StudiesUniversity of Toronto ScarboroughTorontoCanada

Personalised recommendations