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Symbiotic dinitrogen fixation by trees: an underestimated resource in agroforestry systems?

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Abstract

We compiled quantitative estimates on symbiotic N2 fixation by trees in agroforestry systems (AFS) in order to evaluate the critical environmental and management factors that affect the benefit from N2 fixation to system N economy. The so-called “N2-fixing tree” is a tripartite symbiotic system composed of the plant, N2-fixing bacteria, and mycorrhizae-forming fungi. Almost 100 recognised rhizobial species associated with legumes do not form an evolutionary homologous clade and are functionally diverse. The global bacterial diversity is still unknown. Actinorrhizal symbioses in AFS remain almost unstudied. Dinitrogen fixation in AFS should be quantified using N isotopic methods or long-term system N balances. The general average ± standard deviation of tree dependency on N2 fixation (%Ndfa) in 38 cases using N isotopic analyses was 59 ± 16.6 %. Under humid and sub-humid conditions, the percentage was higher in young (69 ± 10.7 %) and periodically pruned trees (63 ± 11.8 %) than in free-growing trees (54 ± 11.7 %). High variability was observed in drylands (range 10–84 %) indicating need for careful species and provenance selection in these areas. Annual N2 fixation was the highest in improved fallow and protein bank systems, 300–650 kg [N] ha−1. General average for 16 very variable AFS was 246 kg [N] ha−1, which is enough for fulfilling crop N needs for sustained or increasing yield in low-input agriculture and reducing N-fertiliser use in large-scale agribusiness. Leaf litter and green mulch applications release N slowly to the soil and mostly benefit the crop through long-term soil improvement. Root and nodule turnover and N rhizodeposition from N2-fixing trees are sources of easily available N for the crop yet they have been largely ignored in agroforestry research. There is also increasing evidence on direct N transfer from N2-fixing trees to crops, e.g. via common mycelial networks of mycorrhizal fungi or absorption of tree root exudates by the crop. Research on the below-ground tree-crop-microbia interactions is needed for fully understanding and managing N2 fixation in AFS.

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Notes

  1. In fact, no tree fixes atmospheric N2 because all organisms capable of N2 fixation are Bacteria or Archae. However, in order to avoid repeating the long correct expression “trees forming N2-fixing symbiosis with bacteria” we use the common though inaccurate term “N2-fixing trees” for referring to these trees as a group.

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Acknowledgments

An early version of this review was presented in the 2nd World Congress of Agroforestry (Nairobi, August 2009). We thank Dr Anne-Marie Domenach for inspiring discussions and comments on a draft of this review. The contribution of PN was funded by the Academy of Finland (grant 129166).

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Authors and Affiliations

  1. Department of Forest Sciences, P.O. Box 27, 00014, University of Helsinki, Finland

    Pekka Nygren

  2. Ecologie Microbienne, UMR5557, USC 1193, Université Lyon1, 43 boulevard du 11 novembre 1918, 69622, Villeurbanne Cedex, France

    María P. Fernández

  3. CIRAD, UMR Eco&Sols, 2 Place Viala, 34060, Montpellier Cedex 01, France

    Jean-Michel Harmand

  4. EARTH University, 4442-1000, San José, Costa Rica

    Humberto A. Leblanc

  5. Finnish Society of Forest Science, P.O. Box 18, 01301, Vantaa, Finland

    Pekka Nygren

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  1. Pekka Nygren
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  2. María P. Fernández
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  3. Jean-Michel Harmand
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  4. Humberto A. Leblanc
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Correspondence to Pekka Nygren.

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Nygren, P., Fernández, M.P., Harmand, JM. et al. Symbiotic dinitrogen fixation by trees: an underestimated resource in agroforestry systems?. Nutr Cycl Agroecosyst 94, 123–160 (2012). https://doi.org/10.1007/s10705-012-9542-9

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