Skip to main content
SpringerLink
Log in

Detection of nitrogen transfer from N2-fixing shade trees to cacao saplings in 15N labelled soil: ecological and experimental considerations

  • Published:
Agroforestry Systems Aims and scope Submit manuscript

Abstract

Theobroma cacao seedlings were grown alone (TCA) or associated with saplings of N2-fixing shade trees Gliricidia sepium and Inga edulis in 200 l of 15N 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 15N 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 15N than total N was found in roots. Thus, whole plant harvesting should be used in 15N 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 N2 fixation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Beer J, Muschler R, Kass D, Somarriba E (1998) Shade management in coffee and cacao plantations. Agrofor Syst 38:139–164

    Article  Google Scholar 

  • Bethlenfalvay GJ, Reyes-Solis MG, Camel SB, Ferrera-Cerrato R (1991) Nutrient transfer between the root zones of soybean and maize plants connected by a common mycorrhizal mycelium. Physiol Plant 82:423–432

    Article  CAS  Google Scholar 

  • Bolaños RA, Watson VC (1993) Mapa ecológico de Costa Rica, según el sistema de clasificación de zonas de vida del mundo de L.R Holdrige. Centro Científico Tropical, San José

    Google Scholar 

  • Chalk PM, Ladha JK (1999) Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution. Soil Biol Biochem 31:1901–1917

    Article  CAS  Google Scholar 

  • Chalk PM, Smith CJ (1994) 15N isotope dilution methodology for evaluating the dynamics of biologically fixed N in legume-non-legume associations. Biol Fertil Soils 17:80–84

    Article  CAS  Google Scholar 

  • Danso SKA, Bowen GD, Sanginga N (1992) Biological nitrogen fixation in trees in agro-ecosystems. Plant Soil 141:177–196

    Article  CAS  Google Scholar 

  • Dossa EL, Fernandes ECM, Reid WS, Ezui K (2008) Above- and below-ground biomass, nutrient and carbon stocks contrasting an open-grown and a shaded coffee plantation. Agrofor Syst 72:103–115

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Enríquez G (1985) Curso sobre el cultivo del cacao. CATIE, Turrialba, 239 pp

  • Frey B, Schüepp H (1993) A role of vesicular-arbuscular (VA) mycorrhizal fungi in facilitating interplant nitrogen transfer. Soil Biol Biochem 25:651–658

    Article  Google Scholar 

  • Fried M, Middelboe V (1977) Measurement of amount of nitrogen fixed by a legume crop. Plant Soil 47:713–715

    Article  CAS  Google Scholar 

  • Giovannetti M, Luciano A, Fortuna P, Pellegrino E, Sbran C, Strani P (2006) At the root of the wood wide web: self recognition and non-self incompatibility in mycorrhizal networks. Plant Signal Behav 1:1–5

    PubMed  Google Scholar 

  • Gómez Luciano CA (2008) Distribución de raíces finas de Inga edulis y Theobroma cacao en el suelo de un sistema agroforestal orgánico. Proyecto de Graduación, Universidad EARTH, Guácimo, 26 pp

  • Gylfadóttir T, Helgadóttir Á, Høgh-Jensen H (2007) Consequencies of including adapted white clover in northern European grassland: transfer and deposition of nitrogen. Plant Soil 297:93–104

    Article  Google Scholar 

  • Hairiah K, van Noordwijk M, Cadisch G (2000) Quantification of biological N2 fixation of hedgerow trees in Northern Lampung. Neth J Agric Sci 48:47–59

    CAS  Google Scholar 

  • He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks. Crit Rev Plant Sci 22:531–567

    Article  Google Scholar 

  • He XH, Critchley C, Hock N, Bledsoe C (2004) Reciprocal N (15NH4 + or 15NO3 −) transfer between non-N2-fixing Eucalyptus maculata and N2-fixing Casuarina cunninghamiana linked by the ectomycorrhizal fungus Pisolithus sp. New Phytol 163:629–640

    Article  Google Scholar 

  • Högberg P (1997) Tansley review no. 95. 15N natural abundance in soil-plant systems. New Phytol 137:179–203

    Article  Google Scholar 

  • Høgh-Jensen H, Schjoerring JK (2000) Below-ground nitrogen transfer between different grassland species: direct quantification by 15N leaf feeding compared with indirect dilution of soil 15N. Plant Soil 227:171–183

    Article  Google Scholar 

  • Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330

    Article  CAS  PubMed  Google Scholar 

  • Iglesias L, Salas E, Leblanc HA, Nygren P (2007) Characterization and host preference of arbuscular mycorrhizae associated to a Theobroma cacao–Inga edulis agroforestry system in the humid tropics of Costa Rica. In: 2nd international symposium on multi-strata agroforestry systems with perennial crops, CATIE, Turrialba, Costa Rica, 17–21 Sept 2007, Posters Session 1

  • 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

    Article  CAS  Google Scholar 

  • Izaguirre-Mayoral ML, Sinclair TR (2005) Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture. Ann Bot 96:149–158

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jayasundara HPS, Dennett MD, Sangakkara UR (1997) Biological nitrogen fixation in Gliricidia sepium and Leucaena leucocephala and transfer of fixed nitrogen to an associated grass. Trop Grasslands 31:529–537

    Google Scholar 

  • Johansen A, Jensen ES (1996) Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol Biochem 28:73–81

    Article  CAS  Google Scholar 

  • Kadiata BD, Mulongoy K, Isirimah NO (1998) Effect of tree pruning and pruning application to trees on nitrogen fixation by Leaucaena and Gliricidia. Agrofor Syst 39:117–128

    Article  Google Scholar 

  • Leblanc HA (2004) Evaluation of Inga spp. for dinitrogen fixation and nitrogen release in humid-tropical alley cropping. Ph.D. dissertation, Department of Agronomy, University of Missouri, Columbia, MO, USA

  • Leblanc HA, McGraw RL, Nygren P, Le Roux C (2005) Neotropical legume tree Inga edulis forms N2-fixing symbiosis with fast-growing Bradyrhizobium strains. Plant Soil 275:121–133

    Article  Google Scholar 

  • Leblanc HA, McGraw RL, Nygren P (2007) Dinitrogen-fixation by three neotropical agroforestry tree species under semi-controlled field conditions. Plant Soil 291:199–209

    Article  CAS  Google Scholar 

  • Lehmann J, Gebauer G, Zech W (2002) Nitrogen cycling assessment in a hedgerow intercropping system using 15N enrichment. Agrofor Syst 62:1–9

    CAS  Google Scholar 

  • Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci USA 104:11192–11196

    Article  CAS  PubMed  Google Scholar 

  • Mariotti A (1983) Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements. Nature 303:685–687

    Article  CAS  Google Scholar 

  • Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell M, Robertson GP, Santos OC, Treseder K (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65

    CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • McNeill AM, Wood M (1990) Fixation and transfer of nitrogen by white clover to ryegrass. Soil Use Manage 6:84–86

    Article  Google Scholar 

  • Muñoz F, Beer J (2001) Fine root dynamics of shaded cacao plantations in Costa Rica. Agrofor Syst 51:119–130

    Article  Google Scholar 

  • Nair PKR, Buresh RJ, Mugendi DN, Latt CR (1999) Nutrient cycling in tropical agroforestry systems: myths and science. In: Buck LE, Lassoie JP, Fernandes ECM (eds) Agroforestry in sustainable agricultural system. CRC Press, Boca Raton, pp 1–31

    Google Scholar 

  • Newman EI, Eason WR (1989) Cycling of nutrients from dying roots to living plants, including the role of mycorrhizas. Plant Soil 115:211–215

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 20:41–48

    PubMed  Google Scholar 

  • Okon IE, Osonubi O, Sanginga N (1996) Vesicular-arbsucular mycorrhiza effects on Gliricidia sepium and Senna siamea in a fallowed alley cropping system. Agrofor Syst 33:165–175

    Article  Google Scholar 

  • Paparciková K, Brienza S Jr, Kato OR, Vlek PLG (2000) Field estimation of biological N2-fixation by five tropical species using two 15N isotope dilution methods. In: German-Brazilian workshop on neotropical ecosystems—achievements and prospects of cooperative research, Hamburg, 3–8 Sept 2000. http://www.biologie.uni-hamburg.de/bzf/oknu/proceedingsneotropecosys/p0639_paparcikova.pdf

  • Paul EA, Clark FE (1996) Soil microbiology and biochemistry. Academic Press, San Diego

    Google Scholar 

  • Paynel F, Murray PJ, Cliquet J (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229:235–243

    Article  CAS  Google Scholar 

  • Peoples MB, Palmer B, Lilley DM, Duc LM, Herridge DF (1996) Application of 15N and xylem ureide methods for assessing N2 fixation of three shrub legumes periodically pruned for forage. Plant Soil 182:125–137

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Rowe EC, Cadisch G (2002) Implications of heterogeneity on procedures for estimating plant 15N recovery in hedgerow intercropping systems. Agrofor Syst 54:61–70

    Article  Google Scholar 

  • Rowe EC, van Noordwijk M, Suprayogo D, Hairiah K, Giller KE, Cadish G (2001) Root distributions partially explain 15N uptake patterns in gliricidia and peltophorum hedgerow intercropping systems. Plant Soil 235:167–179

    Article  CAS  Google Scholar 

  • Sancho F, Mata R, Molina E, Salas R (1989) Estudio de suelos, finca de la Escuela de Agricultura de la Región Tropical Húmeda, Guácimo, Provincia de Limón. Universidad EARTH, Guácimo, 151 pp

  • Sanginga N, Danso SKA, Zapata F, Bowen GD (1995) Phosphorus requirements and nitrogen accumulation by N2-fixing and non-N2-fixing leguminous trees growing in low P soils. Biol Fertil Soils 20:205–211

    Article  CAS  Google Scholar 

  • Schimann H, Ponton S, Hättenschwiler S, Ferry B, Lensi R, Domenach AM, Roggy J-C (2008) Differing nitrogen use strategies of two tropical rainforest late successional tree species in French Guiana: evidence from 15N natural abundance and microbial activities. Soil Biol Biochem 40:487–494

    Article  CAS  Google Scholar 

  • Schroth G, Zech W (1995) Root length dynamics in agroforestry with Gliricidia sepium as compared to sole cropping in the semi-deciduous rainforest zone of West Africa. Plant Soil 170:297–306

    Article  CAS  Google Scholar 

  • Sierra J, Nygren P (2005) Role of root inputs from a dinitrogen-fixing tree in soil carbon and nitrogen sequestration in a tropical silvopastoral system. Aust J Soil Res 43:667–675

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sierra J, Daudin D, Domenach AM, 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

    Article  CAS  Google Scholar 

  • Snoeck D, Zapata F, Domenach AM (2000) Isotopic evidence of the transfer of nitrogen fixed by legumes to coffee trees. Biotechnol Agron Soc Environ 4:95–100

    CAS  Google Scholar 

  • Ståhl L, Nyberg G, Högberg P, Buresh RJ (2002) Effects of planted tree fallows on soil nitrogen dynamics, above-ground and root biomass, N2-fixation and subsequent maize crop productivity in Kenya. Plant Soil 243:103–117

    Article  Google Scholar 

  • Ståhl L, Högberg P, Sellstedt A, Buresh RJ (2005) Measuring nitrogen fixation by Sesbania sesban planted in fallows using 15N tracer technique in Kenya. Agrofor Syst 65:67–79

    Article  Google Scholar 

  • Ta TC, Faris MA (1987) Species variation in the fixation and transfer of nitrogen from legumes to associated grasses. Plant Soil 98:265–274

    Article  CAS  Google Scholar 

  • Tilki F, Fisher RF (1998) Tropical leguminous species for acid soils: studies on plant form and growth in Costa Rica. For Ecol Manage 108:175–192

    Article  Google Scholar 

  • Vallis I, Haydock KP, Ross PJ, Henzell EF (1967) Isotopic studies on the uptake of nitrogen by pasture plants. III. The uptake of small additions of 15N-labelled fertilizer by Rhodes grass and Townsville lucerne. Aust J Agric Res 18:865–877

    Article  CAS  Google Scholar 

  • van Kessel C, Farrell RE, Roskoski JP, Keane KM (1994) Recycling of the naturally-occurring 15N in an established stand of Leucaena leucocephala. Soil Biol Biochem 26:757–762

    Article  Google Scholar 

  • 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. Biogeochemistry 57(58):1–45

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, 929 pp

Download references

Acknowledgements

The contribution of M.K. was supported by the Finnish Cultural Foundation and the University of Helsinki Funds, the contribution of H.A.L. by the EARTH University Research Committee, and the contribution of P.N. by the Academy of Finland (grant # 111796).

Author information

Authors and Affiliations

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

    Miika Kurppa & Pekka Nygren

  2. EARTH University, 4442-1000, San Jose, Costa Rica

    Humberto A. Leblanc

Authors
  1. Miika Kurppa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Humberto A. Leblanc
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pekka Nygren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pekka Nygren.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kurppa, M., Leblanc, H.A. & Nygren, P. Detection of nitrogen transfer from N2-fixing shade trees to cacao saplings in 15N labelled soil: ecological and experimental considerations. Agroforest Syst 80, 223–239 (2010). https://doi.org/10.1007/s10457-010-9327-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10457-010-9327-6

Keywords

Search

Navigation