Abstract
Nitrogen-fixing legumes are widely used to improve ecosystems. However, N accumulation in biomass, N2 amounts biologically fixed, and the effects on soil N status are poorly understood for plantations with slow-growing N2-fixing legume trees in seasonally dry environments. In this study, we assessed these questions in monospecific stands of uninoculated Anadenanthera peregrina (L.) var. peregrina (angico) trees established in the Atlantic Forest biome. Nine experimental plots with a stand density of 1111 tree ha−1 were examined about five to six years after tree planting. N content in the leaves, branches, bark, and wood was estimated using allometric equations and N concentration in the tissues. To assess the N content, the topsoil layer was sampled in each plot and in one pasture area. The annual N2 fixation rate at the stand scale was estimated by the natural abundance of 15N, using leaves of angico and a mix of leaves of herbs and shrubs growing in the understory in each plot. N accumulation in aboveground biomass was estimated at 260 kg ha−1 and N allocated in the leaves and branches was four-fold that in the tree stem. N derived from biological N2 fixation was estimated at 50% on average, with an annual rate of N fixed in the aboveground biomass of 22 kg ha−1 year−1. Soil N storage was similar between A. peregrina stands and the pasture area at six years after planting. Long-term gains of N2 fixation may be greatly improved by the adoption of breeding programs for this slow-growing species and the use of an adequate rhizobium strain.
Similar content being viewed by others
References
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Koppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Amazonas NT, Forrester DI, Silva CC, Almeida DRA, Rodrigues RR, Brancalion PHS (2018) High diversity mixed plantations of Eucalyptus and native trees: an interface between production and restoration for the tropics. For Ecol Manag 417:247–256. https://doi.org/10.1016/j.foreco.2018.03.015
Andrade BG, Carneiro ACO, Vital BR, Souza AL, Coelho DJS (2013) Determinação do potencial tanífero em povoamento de angico. Braz J Wood Sci 4:139–151. https://doi.org/10.15210/cmad.v4i2.4059
Andrews M, James EK, Sprent JI, Boddey RM, Gross E, Dos Reis Jr FB (2011) Nitrogen fixation in legumes and actinorhizal plants in natural ecosystems: values obtained using 15N natural abundance. Plant Ecol Divers 4:131–140. https://doi.org/10.1080/17550874.2011.644343
Bala A, Murphy PJ, Osunde AO, Giller KE (2003) Nodulation of tree legumes and the ecology of their native rhizobial populations in tropical soils. Appl Soil Ecol 22:211–223. https://doi.org/10.1016/S0929-1393(02)00157-9
Balieiro FC, Franco AA, Fontes RLF, Dias LE, Campello EFC (2002) Accumulation and distribution of aboveground biomass and nutrients under pure and mixed stands of Guachapele and Eucalyptus. J Plant Nutr 25:2639–2654. https://doi.org/10.1081/PLN-120015528
Barron AR, Purves DW, Hedin LO (2011) Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165:511–520. https://doi.org/10.1007/s00442-010-1838-3
Bighi KN, Paula RR, Caldeira MVW, Burak DL, Mendonça EdS, de Souza PH, Delarmelina WM, Balieiro FdC (2021) Nitrogen pools in tropical plantations of N2-fixing and non-N2-fixing legume trees under different tree stand densities. Nitrogen 2:8698. https://doi.org/10.3390/nitrogen2010006
Binkley D, Giardina C (1997) Nitrogen fixation in tropical forest plantations. In: Nambiar EKS, Brown AG (eds) Management of soil: nutrients and water in tropical plantation forests. ACIAR Monograph, Canberra, pp 297–337
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 Agroecosys 57:235–270. https://doi.org/10.1023/A:1009890514844
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 Ecol Manag 255:3918–3930. https://doi.org/10.1016/j.foreco.2007.10.050
Campanharo IF (2017) Mudanças edáficas após plantio de leguminosas arbóreas em pastagem no sul do Espírito Santo. Federal University of Espírito Santo, Jerônimo Monteiro, Monograph
Carlsson G, Huss-Danell K (2014) Does nitrogen transfer between plants confound 15N-based quantifications of N2 fixation? Plant Soil 374:345–358. https://doi.org/10.1007/s11104-013-1802-1
Castro D, Urzúa J, Rodriguez-Malebran M, Inostroza-Blancheteau C, Ibáñez C (2017) Woody leguminous trees: new uses for sustainable development of drylands. J Sustain For 36:764–786. https://doi.org/10.1080/10549811.2017.1359098
Chaer GM, Resende AS, Campello EFC, Faria SM, Boddey RM (2011) Nitrogen-fixing legume tree species for the reclamation of severely degraded lands in Brazil. Tree Physiol 31:139–149. https://doi.org/10.1093/treephys/tpq116
Chalk PM, Inácio CT, Balieiro FC, Rouws JRC (2016) Do techniques based on 15N enrichment and 15N natural abundance give consistent estimates of the symbiotic dependence of N2-fixing plants? Plant Soil 399:415–426. https://doi.org/10.1007/s11104-015-2689-9
Coelho SRF, Gonçalves JLM, Laclau JP, Mello SLM, Moreira RM, Silva EV (2007) Crescimento, nutrição e fixação biológica de nitrogênio em plantios mistos de eucalipto e leguminosas arbóreas. Pesqui Agropec Bras 42:759–768. https://doi.org/10.1590/S0100-204X2007000600001
Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560. https://doi.org/10.1002/rcm.5129
Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L (2015) Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26. https://doi.org/10.1007/s11104-015-2542-1
Cramer MD, Chimpahango SBM, Van Cauter A, Waldram MS, Bond WJ (2007) Grass competition induces N2 fixation in some species African Acacia. J Ecol 95:1123–1133. https://doi.org/10.1111/j.1365-2745.2007.01285.x
Faria SM, Moraes LFD, Lima HC, Ribeiro RD, Mattos CMJ, Rodrigues TM, Castilho AF, Canosa GA, Silva MP (2011) Composição florística de leguminosas com potencial para fixação biológica de nitrogênio em áreas de vegetação de Canga (savana metalófita) do entorno do complexo minerador de Carajás. Comunicado Técnico 140 Embrapa, Seropédica
Forrester DI, Schortemeyer M, Stock WD, Bauhus J, Khanna PK, Cowie AL (2007) Assessing nitrogen fixation in mixed-and single-species plantations of Eucalyptus globulus and Acacia mearnsii. Tree physiol 27:1319–1328. https://doi.org/10.1093/treephys/27.9.1319
Franco AA, Faria SM (1997) The contribution of N2-fixing tree legumes to land reclamation and sustainability in the tropics. Soil Biol Biochem 29:897–903. https://doi.org/10.1016/S0038-0717(96)00229-5
Galiana A, Balle P, Kanga AG, Domenach AM (2002) Nitrogen fixation estimated by the 15N natural abundance method in Acacia mangium Willd. inoculated with Bradyrhizobium sp. and grown in silvicultural conditions. Soil Biol Biochem 34:251–262. https://doi.org/10.1016/S0038-0717(01)00179-1
Gehring C, Vlek PLG (2005) Limitations of the 15N natural abundance method for estimating biological nitrogen fixation in Amazonian forest legumes. Basic Appl Ecol 5:567–580. https://doi.org/10.1016/j.baae.2004.09.005
Gross E, Cordeiro L, Caetano FH (2002) Nodule ultrastructure and initial growth of Anadenanthera peregrina (L.) Speg. var. falcata (Benth.) Altschul plants infected with Rhizobia. Ann Bot 90:175–183. https://doi.org/10.1093/aob/mcf184
Högberg P (1997) 15N natural abundance in soil–plant systems. New Phytol 137:179–203. https://doi.org/10.1046/j.1469-8137.1997.00808.x
Instituto Brasileiro de Geografia e Estatística (IBGE) (1987) Projeto RADAM, Folha SE 24 Rio Doce, Rio de Janeiro
Lorenzi H (2014) Árvores Brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, 1st edn. Nova Odessa
Malavolta E, Vitti GC, Oliveira AS (1989) Avaliação do estado nutricional das plantas: princípios e aplicações. Associação Brasileira para Pesquisa da Potassa e do Fosfato, Piracicaba
Mariotti A, Sougoufara B, Dommergues YR (1992) Estimation de la fixation d’azote atmospherique par le tracage isotopique naturel dans une plantation de Casuarina equisetifolia. Soil Biol Biochem 24:647–653. https://doi.org/10.1016/0038-0717(92)90043-W
McFarland JW, Ruess RW, Kielland K, Pregitzer K, Hendrick R, Allen M (2010) Cross-ecosystem comparisons of in situ plant uptake of amino acid-N and NH4+. Ecosyst 13:177–193. https://doi.org/10.1007/s10021-009-9309-6
Mendonça ES, Matos ES (2005) Matéria orgânica do solo: métodos de análises. Federal University of Viçosa, Viçosa
Morin MP (2018) Anadenanthera in lista de espécies da flora do Brasil. Jardim Botânico do Rio de Janeiro. http://reflora.jbrj.gov.br/jabot/floradobrasil/FB22783. Accessed 15 Sept 2018
Munroe JW, Isaac ME (2014) N2-fixing trees and the transfer of fixed-N for sustainable agroforestry: a review. Agron Sustain Dev 34:417–427. https://doi.org/10.1007/s13593-013-0190-5
Nascimento GA, Pifano DS, Lima MP, Calegário N (2009) Foristic aspects and diversity of regenerated arboreal species under a stand of Anadenanthera peregrina SPEG. Cerne 15:187–195
Nogueira SX, Paula RR, Souza ND, Dias AF Jr, Mendonça ES (2018) Investigando a química de folhas verdes e lixiviados de espécies florestais de rápido crescimento que afetam a germinação de braquiária. Anais do Simpósio IPEF 50 anos. IPEF, Piracicaba, pp 163–167
Parrotta JA, Baker DD, Fried M (1996) Changes in dinitrogen fixation in maturing stands of Casuarina equisetifolia and Leucaena leucocephala. Can J For Res 26:1684–1691. https://doi.org/10.1139/x26-190
Paula RR, Bouillet J-P, Gonçalves JLM, Trivelin PCO, Balieiro FC, Nouvellon Y, Oliveira JC, Deus JC Jr, Bordron B, Laclau J-P (2018) Nitrogen fixation rate of Acacia mangium Wild at mid rotation in Brazil is higher in mixed plantations with Eucalyptus grandis Hill ex Maiden than in monocultures. Ann For Sci 75:2–14. https://doi.org/10.1007/s13595-018-0695-9
Paula RR, Bouillet J-P, Trivelin PCO, Zeller B, Gonçalves JLM, Nouvellon Y, Bouvet J-M, Plassard C, Laclau J-P (2015) Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest. Soil Biol Biochem 91:99–108. https://doi.org/10.1016/j.soilbio.2015.08.017
Peoples MB, Chalk PM, Unkovich MJ, Boddey RM (2015) Can Differences in 15N natural abundance be used to quantify the transfer of nitrogen from legumes to neighbouring non-legume plant species? Soil Biol Biochem 87:97–109. https://doi.org/10.1016/j.soilbio.2015.04.010
Portillo-Quintero CA, Sánchez-Azofeifa GA (2010) Extent and conservation of tropical dry forest in the Americas. Biol Conserv 143:144–155. https://doi.org/10.1016/j.biocon.2009.09.020
Raddad AY, Salih AA, El Fadl MA, Kaarakka V, Luukkanen O (2005) Symbiotic nitrogen fixation in eight Acacia senegal provenances in dryland clays of the Blue Nile Sudan estimated by the 15N natural abundance method. Plant Soil 275:261–269. https://doi.org/10.1007/s11104-005-2152-4
Reich PB (2014) The world-wide “fast-slow” plant economics spectrum: a traits manifesto. J Ecol 102:275–301. https://doi.org/10.1111/1365-2745.12211
Reis FB Jr, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, Loureiro MF, Queiroz LP, Scotti MR, Chen WM, Norén A, Rubio MC, Faria SM, Bontemps C, Goi SR, Young JP, Sprent JI, James EK (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946. https://doi.org/10.1111/j.1469-8137.2010.03267.x
Schubert KR (1986) Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Annu Rev Plant Physiol 37:539–574. https://doi.org/10.1146/annurev.pp.37.060186.002543
Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756. https://doi.org/10.1071/PP9860699
Shi S, Peng C, Wang M, Zhu Q, Yang G, Yang Y, ** T, Zhang T (2016) A global meta-analysis of changes in soil carbon, nitrogen, phosphorus and sulfur, and stoichiometric shifts after forestation. Plant Soil 407:323–340. https://doi.org/10.1007/s11104-016-2889-y
Souza LQ, Freitas ADS, Sampaio EVDSB, Moura PM, Menezes RSC (2012a) How much nitrogen is fixed by biological symbiosis in tropical dry forests? 1. Trees Shrubs Nutr Cycl Agroecosys 94:171–179. https://doi.org/10.1007/s10705-012-9531-z
Souza PB, Souza AL, Costa WS, Peloso RV, Lana JM (2012b) Florística e diversidade das espécies arbustivo-arbóreas regeneradas no sub-bosque de Anadenanthera peregrina (L.) Speg. Cerne 18:413–421
Souza PH (2018) Biomassa e estoque de carbono em povoamento de Anadenanthera peregrina (L.) Speg sob diferentes espaçamentos. Dissertation, Federal University of Espírito Santo, Jerônimo Monteiro
Sprent JI, Odee DW, Dakota FD (2010) African legumes: a virtual but under-utilized resource. J Exp Bot 61:1257–1265. https://doi.org/10.1093/jxb/erp342
Spriggs AC, Dakota FD (2009) Field assessment of symbiotic N2 fixation in wild and cultivated Cyclopia species in the South African fynbos by 15N natural abundance. Tree Physiol 29:239–247. https://doi.org/10.1093/treephys/tpn021
Systat Software Inc. (2014) SigmaPlot for windows, Version 13.0. Registration number: 775302386
Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. Canberra, ACIAR Monograph, p 258
Voigtlaender M, Brandani CB, Caldeira DRM, Tardy F, Bouillet J-P, Goncalves JLM, Moreira MZ, Leite FP, Brunet D, Paula RR, Laclau J-P (2019) Nitrogen cycling in monospecific and mixed-species plantations of Acacia mangium and Eucalyptus at 4 sites in Brazil. For Ecol Manag 436:56–67. https://doi.org/10.1016/j.foreco.2018.12.055
Wang F, Li Z, **a H, Zou B, Li N, Liu J, Zhu W (2010) Effects of nitrogen-fixing and non-nitrogen-fixing tree species on soil properties and nitrogen transformation during forest restoration in southern China. Soil Sci Plant Nutr 56:297–306. https://doi.org/10.1111/j.1747-0765.2010.00454.x
Acknowledgments
The authors wish to thank the Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (Grants 71416382/2016 and 64946088/2013) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico for the financial support. We are also grateful to the Laboratório de Isótopos Estáveis of CENA/USP, the Laboratório de Ecologia Aplicada of ESALQ/USP, and the Laboratório de Recursos Hídricos e Solos of DCFM/UFES for their technical support. We would like to thank the Instituto Federal de Ciência e Tecnologia do Espírito Santo Campus de Alegre and the partners, for the available study area formally called the “Floresta Piloto.”, and the Instituto Federal de Ciência e Tecnologia do Espírito Santo for the financial contribution to review the article through PRODIF—Edital PRPPG 07/2020. We are also grateful to J-P. Bouillet, F.C. Balieiro, E.S. Mendonça and the anonymous reviewers who contributed to improving the manuscript.
Author information
Authors and Affiliations
Contributions
Conceptualization: RRP; Data curation: RRP, PHZ, MVWC; Formal analysis: RRP, PHZ, LJM; Funding acquisition: RRP, MVWC, WMD; Investigation: LJM, IFC, PHZ, WMD, RRP; Isotopic analysis: PCO; Writing original draft: RRP, LJM. Review and Edition: RRP, LJM. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Table 1. Mean values of soil attribute at 0–20 cm of depth in experimental plots about six years after planting of A. peregrina trees
Table 2. Equations used to estimate aboveground biomass compartments of A. peregrina trees and respective statistical information. Dbh is expressed in centimeters and Ht is meters.
Fig. 1. Relationship between diameter at breast height and total height of 270 A. peregrina trees about six years after planting. SEE = standard error of the estimate
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mendes, L.J., Paula, R.R., de Souza, P.H. et al. Nitrogen accumulated and biologically fixed by uninoculated Anadenanthera peregrina (L.) Speg trees under monospecific stands in the Atlantic Forest biome. Braz. J. Bot 44, 503–512 (2021). https://doi.org/10.1007/s40415-021-00713-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-021-00713-z