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 freegrowing 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-cropmicrobia interactions is needed for fully understanding and managing N2 fixation in AFS. (Résumé d'auteur
Theobroma cacao seedlings were grown alone (TCA) or associated with saplings of N 2 -fixing shade trees Gliricidia sepium and Inga edulis in 200 l of 15 N labelled soil within a physical root barrier for studying direct nitrogen transfer between the trees and cacao. Root:shoot partitioning ratio for sapling total N was lower than biomass root:shoot ratio in all species. Sapling total 15 N was partitioned between root and shoot in about the same ratio as total N in cacao and inga but in gliricidia much higher proportion of 15 N than total N was found in roots. Thus, whole plant harvesting should be used in 15 N studies whenever possible. Average percentage of fixed N out of total tree N was 74 and 81% for inga estimated by a yield-independent and yield-dependent method, respectively, and 85% for gliricidia independently of estimation method. Strong isotopic evidence on direct N transfer from trees to cacao was observed in two cases out of ten with both tree species. Direct N transfer was not correlated with mycorrhizal colonisation of either donor or receiver plant roots. Direct N transfer from inga and gliricidia to cacao is conceivable but its prevalence and the transfer pathway via mycorrhizal connections or via reabsorption of N-rich legume root exudates by cacao require further study. Competition in the restricted soil space may also have limited the apparent transfer in this study because the trees accumulated more soil-derived N than cacao in spite of active N 2 fixation.
Inga edulis Mart. is a tropical legume tree used for shade in coffee and cacao plantations and as a hedgerow in alley-cropping practices. Little information can be found concerning N 2 fixation in this species. This study was conducted to characterize the rhizobia of I. edulis and determine if it is capable of fixing substantial amounts of N 2 . Four strains of fast-growing, Gram-negative rhizobia-type bacteria were isolated from I. edulis nodules. The strains were identified by sequencing of partial 16S-23S rDNA internal spacer region. Nitrogenase activity was determined using acetylene reduction assay (ARA). Dinitrogen fixation was measured under controlled conditions by the 15 N isotope dilution technique using two non-N 2 -fixing reference species, Vochysia guatemalensis Donn. Sm, and Gmelina arborea Roxb. ex. Sm. Seedlings were grown in three growth media: native soil and naturally N-depleted sand amended to a low and high N level. The four strains of symbiotic bacteria were closely related to Bradyrhizobium japonicum and to Bradyrhizobium liaoningense. Nodules demonstrated nitrogenase activity as measured by ARA. Vochysia guatemalensis was a better non-N 2 -fixing reference than G. arborea. When V. guatemalensis was used as the non-N 2 -fixing reference, the estimate of the percentage of N fixed from atmosphere out of total N in I. edulis seedlings was ca. 40% in the two sand media treatments and 10% in the native soil.
Natural abundance of 15 N was sampled in young and mature leaves, branches, stem, and coarse roots of trees in a cacao (Theobroma cacao) plantation shaded by legume tree Inga edulis and scattered nonlegumes, in a cacao plantation with mixed-species shade (legume Gliricidia sepium and several non-legumes), and in a tree hedgerow bordering the plantations in Guácimo, in the humid Caribbean lowlands of Costa Rica. The deviation of the sample 15 N proportion from that of atmosphere (d 15 N) was similar in non-legumes Cordia alliodora, Posoqueria latifolia, Rollinia pittieri, and T. cacao. Deep-rooted Hieronyma alchorneoides had lower d 15 N than other non-N 2 -fixers, which probably reflected uptake from a partially different soil N pool. Gliricidia sepium had low d 15 N. Inga edulis had high d 15 N in leaves and branches but low in stem and coarse roots. The percentage of N fixed from atmosphere out of total tree N (%N f ) in G. sepium varied 56-74%; N 2 fixation was more active in July (the rainiest season) than in March (the relatively dry season). The variation of d 15 N between organs in I. edulis was probably associated to 15 N fractionation in leaves. Stem and coarse root d 15 N was assumed to reflect the actual ratio of N 2 fixation to soil N uptake; stem-based estimates of %N f in I. edulis were 48-63%. Theobroma cacao below I. edulis had lower d 15 N than T. cacao below mixed-species shade, which may indicate direct N transfer from I. edulis to T. cacao but results so far were inconclusive. Further research should address the 15 N fractionation in the studied species for improving the accuracy of the N transfer estimates. The d 15 N appeared to vary according to ecophysiological characteristics of the trees.
Cultivating dinitrogen-fixing legume trees with crops in agroforestry is a relatively common N management practice in the Neotropics. The objective of this study was to assess the N 2 fixation potential of three important Neotropical agroforestry tree species, Erythrina poeppigiana, Erythrina fusca, and Inga edulis, under semi-controlled field conditions. The study was conducted in the humid tropical climate of the Caribbean coastal plain of Costa Rica. In 2002, seedlings of I. edulis and Vochysia guatemalensis were planted in one-meter-deep open-ended plastic cylinders buried in soil within hedgerows of the same species. Overall tree spacing was 1 · 4 m to simulate a typical alley-cropping design. The 15 N was applied as (NH 4 ) 2 SO 4 at 10% 15 N atom excess 15 days after planting at the rate of 20 kg [N] ha -1 . In 2003, seedlings of E. poeppigiana, E. fusca, and V. guatemalensis were planted in the same field using the existing cylinders. The 15 N application was repeated at the rate of 20 kg [N] ha -1 15 days after planting and 10 kg [N] ha -1 was added three months after planting. Trees were harvested 9 months after planting in both years. The 15 N content of leaves, branches, stems, and roots was determined by mass spectrometry. The percentage of atmospheric N fixed out of total N (%N f ) was calculated based on 15 N atom excess in leaves or total biomass. The difference between the two calculation methods was insignificant for all species. Sixty percent of I. edulis trees fixed N 2 ; %N f was 57% for the N 2 -fixing trees. Biomass production and N yield were similar in N 2 -fixing and non-N 2 -fixing I. edulis. No obvious cause was found for why not all I. edulis trees fixed N 2 . All E. poeppigiana and E. fusca trees fixed N 2 ; %N f was ca. 59% and 64%, respectively. These data were extrapolated to typical agroforestry systems using published data on N recycling by the studied species. Inga edulis may recycle ca. 100 kg ha -1 a -1 of N fixed from atmosphere to soil if only 60% of trees fix N 2 , E. poeppigiana 60-160 kg ha -1 a -1 , and E. fusca ca. 80 kg ha -1 a -1 .
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