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An isotopic proxy for nitrogen redistribution from Alnus acuminata to wheat intercrop

Published online by Cambridge University Press:  18 February 2022

Celestin Ukozehasi Open the ORCID record for Celestin Ukozehasi [Opens in a new window]  and
Howard Griffiths
Celestin Ukozehasi*
Affiliation:
School of Agriculture and Food Sciences, University of Rwanda, Kigali 6605, Rwanda
Howard Griffiths
Affiliation:
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK
*
*Corresponding author. Email: [email protected]
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Summary

Direct belowground nitrogen (N) transfer has often been reported where plants with contrasting nutrients acquisition strategies (N2-fixing and non-fixing) co-occur, and there is still a gap in the knowledge of the extent of this transfer in the top soil under the field conditions. However, assessment under field conditions is challenging. We hypothesized a practical application of the analysis of natural abundance of δ15N supplemented with an isotopic mixing model ‘IsoSource’ to understand the relative direct contribution of N2-fixing Alnus acuminata to wheat intercrop (non-fixing) N isotopic signatures. A field experiment was conducted in an andic soil of high lands in northern Rwanda to quantitatively determine the proportional contribution of nitrogen by Alnus acuminata to wheat vegetative tissue isotope signatures at different distances from the trees (1 m, 3 m, 5 m, and 7 m). The study involved the measurements and analyses of natural abundance of stable isotopes δ15N and isotopic mixing modeling by IsoSource. Leaf samples were collected from twigs of 10 years old Alnus acuminata grown on the terrace-risers, along with soil samples (0–20 cm) and wheat flag leaf samples across terrace at 1 m, 3 m, 5 m, and 7 m from trees for isotopic measurement. The chlorophyll content index of wheat flag leaf at the four points across terrace was estimated by means of SPAD meter 502. The δ15N proportional contribution by Alnus acuminata to wheat was obtained through IsoSource analysis. We noted a significant (p < 0·01) gradient in depletion of wheat δ15N signatures moving further away from the tree line of Alnus acuminata. The wheat at 1 m from the trees exhibited the δ15N values closer to that of the tree, while at 7 m, the crop δ15N signature was significantly different from that of the tree. An isotopic mixing model ‘IsoSource’ indicated that the tree N may have provided 33·6 ± 4·3 % of the wheat intercrop N at 1 m distance from the trees. Therefore, this study shows that the understanding of field-based crop N and nutrient transfer in agroforestry may be enhanced by analysis of the physiological basis of stable isotopes signatures.

Keywords

IntercroppingIsotopic proxyN transferIsoSourceWheatAlnus acuminataRwanda
Type
Research Article
Information
Experimental Agriculture , Volume 57 , Issue 5-6 , December 2021 , pp. 316 - 323
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Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Akinnifesi, F.K., Ajayi, O.C., Sileshi, G., Chirwa, P.W. and Chianu, J et al. (2010). Fertiliser treesfor sustainable food security in the maize-based production systems of East and Southern Africa: a review. Agronomy for Sustainable Development 30, 615–629.CrossRefGoogle Scholar
Arnebrant, K., Finlay, E.K.H. and Söderström, B. (1993). Nitrogen translocation between Alnus glutinosa L. Gaertn. Seedlings inoculated with Frankia sp. and Pinus contorta Doug, ex Loud seedlings connected by a common ectomycorrhizal mycelium. The New Phytologist 124, 231–242.CrossRefGoogle ScholarPubMed
Baisden, W.T., Amundson, R., Brenner, D.L., Cook, A.C., Kendall, C. and Harden, J.W. (2002). A multi-isotope C and N modeling analysis of soil organic matter turnover and transport as a function of soil depth in a California annual grassland soil chronosequence. Global Biogeochemical Cycles 16, 1120–1135.CrossRefGoogle Scholar
Bardgett, R.D., Mommer, L. and De Vries, F.T. (2014). Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution 29, 692–699.CrossRefGoogle ScholarPubMed
Barea, J-M., Pozo, M.J., Azcon, R. and Azcon-Aguilar, C. (2005). Microbial co-operation in the rhizosphere. Journal of Experimental Botany 56, 1761–1778.CrossRefGoogle ScholarPubMed
BassiriRad, H. and Caldwell, M.M. (1992). Temporal changes in roots growth and 15N uptake and water relations of two tussock grass species recovering from water stress. Physiology Plantarum 86, 525–531.CrossRefGoogle Scholar
Battie-Laclau, P., Taschen, E., Plassard, C., Dezette, D., Abadie, J., Arnal, D, Benezech, P., Duthoit, M., Laure Pablo, A., Jourdan, C., Laclau, J.P., Bertrand, I., Taudiere, A. and Hinsinger, P. et al. (2020). Role of trees and herbaceous vegetation beneath trees in maintaining arbuscular mycorrhizal communities in temperate alley cropping systems. Plant Soil. https://doi.org/10.1007/s11104-019-04181-z.CrossRefGoogle Scholar
Bayala, J. and Prieto, I. (2020). Water acquisition, sharing and redistribution by roots: applications to agroforestry systems. Plant Soil. https://doi.org/10.1007/s11104-019-04173-z.CrossRefGoogle Scholar
Brenner, D.L., Amundson, R., Baisden, W.T., Kendall, C. and Harden, J. (2001). Soil N and 15N variation with time in a California annual grassland ecosystem. Geochimica et Cosmochimica Acta 65, 4171–4186.CrossRefGoogle Scholar
Caldwell, M.M. and Richards, J.H. (1986). Competing root systems: Morphology and models of absorption. In: Givnish, T.J. (ed.), On the economy of plant form and function, UK: Cambridge University press, pp. 251–273.Google Scholar
Cardinael, R., Hoeffner, K., Chenu, C., Chevallier, T., Béral, C., Dewisme, A. and Cluzeau, D. et al. (2019b). Spatial variation of earthworm communities and soil organic carbon in temperate agroforestry. Biology and Fertility of Soils 55, 171–183.CrossRefGoogle Scholar
Clivot, H., Petitjean, C., Marron, N., Dalle, E., Genestier, J., Blaszczyk, N., Santenoise, P, Laflotte, A. and Piutti, S. et al. (2020). Early effects of temperate agroforestry practices on soil organic matter and microbial enzyme activity. Plant Soil. https://doi.org/10.1007/s11104-019-04320-6.CrossRefGoogle Scholar
Criss, E.R. (1999). Principles of Stable Isotopes Distribution. Oxford University Press.CrossRefGoogle Scholar
Dawson, T.E. and Brooks, P.D. (2001). Fundamentals of stable isotopes chemistry and measurements. In Unkovich, M., et al. (eds.), Stable Isotope Techniques in the Study of Biological Processes and Functioning of Ecosystems. Kluwer Academic Publishers, pp. 1–18.Google Scholar
Dawson, T.E., Mambell, S., Plamboeck, A.H., Templer, P.H. and Tu, K.P. (2002). Stable isotopes in plant ecology. Annual Review Ecology Systems 33, 507–559.CrossRefGoogle Scholar
Dupraz, C., Wolz, K.J., Lecomte, I., Talbot, G., Vincent, G., Mulia, R., Bussière, F., Lafontaine, H.O., Andrianarisoa, S., Jackson, N., Lawson, G., Dones, N., Sinoquet, H., Lusiana, B., Harja, D., Domenicano, S., Reyes, F., Gosme, M. and van Noordwijk, M. (2019) Hi-sAFe: A 3D agroforestry model for integrating dynamic tree-crop interactions. Sustainability 11, 1–25.CrossRefGoogle Scholar
Erskine, P.D., Bergstrom, D.M., Schmit, S., Stewart, G.R., Tweedie, C.E. and Shaw, J.D. et al. (1998). Subantarctic Macquarie Island: A model ecosystem for studying animal derived nitrogen sources using 15N natural abundance. Oecologia 117, 187–193.CrossRefGoogle Scholar
Evans, R.D. (2001). Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 6, 121–126.CrossRefGoogle ScholarPubMed
Evans, R.D. (2007). Soil nitrogen isotope composition. In: Michener, R. and Lajtha, K. (eds.), Stable Isotopes in Ecology and Environmental Science 2nd ed., Blackwell Publishing, pp. 83–94.Google Scholar
Evans, R.D. and Ehleringer, J.R. (1993). A break in the nitrogen cycle in arid lands? Evidence from δ15N of soils. Oecologia 94, 314–317.CrossRefGoogle Scholar
Evans, R.D. and Ehleringer, J.R. (1994). Water and nitrogen dynamics in arid woodland. Oecologia 99, 233–242.CrossRefGoogle ScholarPubMed
Farquhar, G.D., O’Leary, M.H. and Berry, J.A. (1982). On the relationships between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.Google Scholar
Gat, J.R. (1996). Oxygen and hydrogen isotopes in the hydrological cycle. Annual Review of Earth and Planetary Sciences 24, 225–262.CrossRefGoogle Scholar
Garten, C., Hanson, P.J., Todd, D.E., Lu, B.B. and Brice, D.J. (2007). Natural 15N and 13C abundance as indicators of forest nitrogen status and soil carbon dynamics. In: Michener, R. and Lajtha, K. (eds), Stable isotopes in ecology and environmental science, 2nd Edn, USA: Blackwell publishing ltd., pp. 61–77.Google Scholar
Handley, L.L. and Raven, J.A. (1992). The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant, Cell and Environment 15, 965–985.CrossRefGoogle Scholar
Handley, L.L. and Scrimgeour, C.M. (1997). Terrestrial plant ecology and 15N natural abundance: The present limits to interpretation for uncultivated systems with original data from a Scottish old field. Advances in Ecological Research 27, 133–212.CrossRefGoogle Scholar
Hauggaard, N.H. and Jensen, E.S. (2005). Facilitative root interactions in intercrops. Plant and Soil 274, 237–250.CrossRefGoogle Scholar
Haystead, A., Malajczuk, N. and Grove, T.S. (1988). Underground transfer of nitrogen between pasture plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytologist 108, 417–423.CrossRefGoogle Scholar
He, X., Critchley, C. and Bledsoe, C. (2003). Nitrogen transfer within and between plants through common mycorrhizal networks. Critical Review of Plant Science 22, 531–567.CrossRefGoogle Scholar
He, X., Xu, M., Qiu, G.Y. and Zhou, J. (2009). Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. Journal of Plant Ecology 2, 107–118.CrossRefGoogle Scholar
Högberg, P. (1997). The 15N natural abundance in soil plant systems. New Phytologist 137, 179–203.CrossRefGoogle ScholarPubMed
Høgh-Jensen, H. (2006). The nitrogen transfer between plants: an important but difficult flux to quantify. Plant Soil 282, 1–5.CrossRefGoogle Scholar
Ikram, A., Jensen, E. and Jakobsen, I. (1994). No significant transfer of N and P from Pueraria phaseoloides to Hevea brasiliensis via hyphal links of arbuscular mycorrhiza. Soil Biology and Biochemistry 26, 1541–1547.CrossRefGoogle Scholar
Isaac, M.E. and Borden, K.A. (2020). Nutrient acquisition strategies in agroforestry systems. Plant Soil. https://doi.org/10.1007/s11104-019-04232-5.CrossRefGoogle Scholar
Jalonen, R., Nygren, P. and Sierra, J. (2009). Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelia networks. Plant, Cell and Environemnt 32, 1366–1376.CrossRefGoogle Scholar
James, J.J. and Richards, J.H. (2005). Plant N capture from pulses: effects of pulse size, growth rate, and other soil resources. Oecologia 145, 113–122.CrossRefGoogle Scholar
Jensen, E.S. (2005). Grain legume functions in crop rotations. In: AEP (ed.), Grain legumes and the environment: how to assess benefits and impacts, Zurich, November 18–19, 2004. AEP and FAL, pp. 49–54.Google Scholar
Johansen, A. and Jensen, E. (1996). Transfer of N and P from intact or decomposition roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biology and Biochemistry 28, 73–81.CrossRefGoogle Scholar
Jones, D.L., Hodge, A. and Kuzyakov, Y. (2004). Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163, 459–480.CrossRefGoogle ScholarPubMed
Lal, R. (2004). Soil carbon sequestration impacts on global climate change and food security. Science 304, 1623–1627.CrossRefGoogle ScholarPubMed
Lu, J.K., Kang, L.H., Sprent, J.I., Xu, D.P. and He, X.H. (2013). Two-way transfer of nitrogen between Dalbergia odorifera, and its hemiparasite Santalum album is enhanced when the host is effectively nodulated and fixing nitrogen. Tree Physiology 33, 464–474.CrossRefGoogle ScholarPubMed
Luedeling, E., Smethurst, P.J., Baudron, F., Bayala, J., Huth, N.I., van Noordwijk, M., Ong, C.K., Mulia, R., Lusiana, B., Muthuri, C. and Sinclair, F.L. (2016). Field-scale modeling of tree-crop interactions: challenges and development needs. Agricultural Systems 142, 51–69.CrossRefGoogle Scholar
Michener, R. and Lajtha, K. (eds.). (2007). Stable Isotopes in Ecology and Environment Science. 2nd ed. Blackwell Publishing.CrossRefGoogle Scholar
Moyer, H.K., Burton, J., Israel, D. and Rufty, T. (2006). Nitrogen transfer between plants: a δ15N natural abundance study with crop and weed species. Plant and Soil 282, 7–20.CrossRefGoogle Scholar
Nair, P.K.R., Buresh, R.J., Mugendi, D.N. and Latt, C.R. (1999). Nutrient cycling in tropical agroforestry systems: myths and science. In: Buck L.E., Lassoie J.P. and Fernandes E.C.M. (eds), Agroforestry in Sustainable Agricultural Systems. Boca Raton, FL: CRC Press, pp. 1–31.Google Scholar
Nygren, P., Cruz, P., Domenach, A.M., Vaillant, V. and Sierra, J. (2000). Influence of forage harvesting regimes on dynamics of biological dinotrogen fixation of a tropical woody legume. Tree physiology 20, 41–48.CrossRefGoogle ScholarPubMed
Phillips, D.L. and Gregg, J.W. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.CrossRefGoogle ScholarPubMed
Rhoades, C.C. (1997). Single-tree influences on soil properties in agroforestry: lessons from natural forest and savanna ecosystems. Agroforest Systems 35, 71–94.CrossRefGoogle Scholar
Robinson, D. (2001). The δ15N as an integrator of the nitrogen cycle. Trends in Ecology Evolution 16, 153–162.CrossRefGoogle Scholar
Sanchez, P.A., Shepherd, K.D., Soule, M.J., Place, F.M., Buresh, R.J. and Izac, A.M. (1997). Soil fertility replenishment in Africa: An investiment in natural capital. In: Buresh et al. (eds), Replenishing soil fertility in Africa, Volume 51, USA: Soil Science Society of America, Inc., pp. 1–46.Google Scholar
Sanford, P., Pate, J.S., Unkovich, M.J. and Thompson, A.N. (1995). Nitrogen fixation in grazed and ungrazed subterranean clover pasture in south west Australia: assessment by the 15N natural abundance technique. Australian Journal of Agricultural Research 46, 1427–1443.CrossRefGoogle Scholar
Schroth, G. (1998). A review of belowground interactions in agroforestry, focusing on mechanisms and management options. Agroforest Systems 43, 5–34.CrossRefGoogle Scholar
Schulze, E.D., Chapin, F.S. and Gebauer, G. (1991). Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska. Oecologia 100, 406–412.CrossRefGoogle Scholar
Seiter, S., Ingham, E.R., William, R.D. and Hibbs, D.E. (1995). Increase in soil microbial biomass and transfer of nitrogen from alder to sweet corn in an alley cropping system. In Ehrenreich, J.H. et al. (ed.) Growing a Sustainable Future. Boise, ID: University of Idaho, pp. 56–158.Google Scholar
Sharifi, M.R., Nilsen, E.T. and Rundel, P.W. (1982). Biomass and net primary productivity of Prosopis glandulosa (Fabaceae) in the Sonoran Desert of California. American Journal of Botany 69, 760–767.CrossRefGoogle Scholar
Shearer, G., Virginia, R.A., Bryan, B.A., Skeeters, J.L., Nilsen, E.T., Sharifi, M.R. and Rundel, P.W. (1983). Estimates of N2-fixation from variation in the natural abundance of 15N in Sonoran desert ecosystems. Oecologia 56, 365–373.CrossRefGoogle ScholarPubMed
Sida, T.S., Baudron, F., Ndoli, A., Tirfessa, D. and Giller, K.E. et al. (2020). Should fertilizer recommendations be adapted to parkland agroforestry systems? Case studies from Ethiopia and Rwanda. Plant Soil. https://doi.org/10.1007/s11104-019-04271-y.CrossRefGoogle Scholar
Sierra, J. and Daudin, D. (2010). Limited 15N transfer from stem-labeled leguminous trees to associated grass in an agroforestry system. European Journal of Agronomy 32, 240–242.CrossRefGoogle Scholar
Sierra, J., Daudin, D., Domenach, A.M. and Nygren, P. (2007). Nitrogen transfer from a legume tree to associated grass estimated by the isotopic signature of tree root exudates: a comparison of the 15N leaf feeding and natural 15N abundance methods. European Journal of Agronomy 27, 178–186.CrossRefGoogle Scholar
Snoeck, D., Zapata, F. and Domenach, A.M. (2000). Isotopic evidence of the transfer of nitrogen fixed by legumes to coffee trees. Biotechnology, Agronomy, Society and Environoment 4, 95–100.Google Scholar
Stewart, G.R. (2001). What do δ15N signatures tell us about nitrogen relations in natural ecosystems? In: Unkovich, M. et al. (eds), Stable isotope techniques in the study of biological processes and functioning of ecosystems, The Netherlands: Kluwer Academic Publishers, pp. 91–101.CrossRefGoogle Scholar
Teste, F.P., Veneklaas, E.J., Dixon, K.W. and Lambers, H. (2014). Is nitrogen transfer among plants enhanced by contrasting nutrient acquisition strategies? Plant, Cell and Environment. doi: 10.1111/pce.12367.Google ScholarPubMed
Unkovich, M., Pate, J., McNeill, A. and Gibbs, D.J. (2001). Stable Isotope Techniques in the Study of Biological Processes and Functioning of Ecosystems. Kluwer Academic Publishers.CrossRefGoogle Scholar
Van Noordwijk, M., Barrios, E., Shepherd, K., Bayala, J. and Oborn, I. et al. (2019). Soil science as part of agroforestry. In: Sustainable Development Through Trees on Farms: Agroforestry in its Fifth Decade. Bogor, Indonesia: World Agroforestry (ICRAF) Southeast Asia Regional Program, pp 63–92.Google Scholar
Virgina, R. and Jarrell, W.M. (1983). Soil properties in a mesquite dominated Sonaran Desert ecosystem. Soil Science Society of America Journal 47, 138–144.CrossRefGoogle Scholar
Wichern, F., Eberhardt, E., Mayer, J., Joergensen, R.G. and Müller, T. (2008). Nitrogen rhizodeposition in agricultural crops: Methods, estimates and future prospects. Soil Biology and Biochemistry 40, 30–48.CrossRefGoogle Scholar
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