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
Inter-specific interactions with eucalypts in mixed plantations increased N 2 fixation rate of acacia trees compared to monocultures. N 2 fixation was higher during the wet summer than during the dry winter both in acacia monocultures and in mixed plantations.
Introducing N-fixing trees in fast-growing tropical plantations may contribute to reducing the long-term requirements of N fertilizers. Management practices established in forest monocultures should be revisited in mixed-species plantations.
This field experiment aimed to compare N2 fixation rates of Acacia mangium Wild in monospecific stands and in mixed-species stands with Eucalyptus grandis W. Hill ex Maiden. A secondary objective was to gain insight into the seasonal variations of N2 fixation.
15N was applied to acacia and eucalypt monocultures and mixed-species with a 1:1 ratio at mid rotation. Leaves were collected in autumn, winter, spring, and summer to determine the foliar N concentrations and 15N atom fraction. The N content in the above-ground biomass was estimated as well as the percentage of N derived from atmospheric N2 (%Ndfa) using eucalypts in monoculture as reference plants.
%Ndfa values averaged over the year were 14% in monoculture and 44% in mixed-species stands. While the stocking density of acacia trees was twice as high in monoculture as in mixture, the amounts of N fixed in above-ground biomass of acacia trees were close (35–39 kg N ha−1) at 39 months after planting. %Ndfa values were higher during the wet summer than the dry winter both in acacia monocultures and in mixed plantations.
The stocking density of acacia trees can be reduced in mixed plantations with eucalypts in comparison to acacia monocultures with a low influence on the input of N to soil through biological fixation.
KeywordsSymbiotic N2 fixation Seasons Mixed-species plantations Competition Forest rotation
We should like to thank Rildo Moreira e Moreira (USP-Esalq), Eder Araújo da Silva (www.floragroapoio.com.br), the staff at the Itatinga experimental station, laboratory of stable isotope of CENA-USP, and the Applied Ecology Laboratory of ESALQ-USP for their technical support. We are also grateful Tony Tebby for the revision of the English.
We should like to thank the São Paulo Research Foundation-FAPESP (grant 2011/20510-8), FAPESP Thematic Project (grant 2010/16623-9), Intens & Fix project (ANR-2010-STRA-004-03), ANAEE, and ATP Neucapalm (CIRAD).
Compliance with ethical standards
Declaration on conflicts of interest
The authors declare no conflicts of interest.
- Balieiro FB, Alves BJR, Pereira MG, Faria SM, Franco AA, Campello EFC (2008) Biological nitrogen fixation and nutrient release from litter of the Guachapele leguminous tree under pure and mixed plantation with Eucalyptus. Cerne 14:185–193Google Scholar
- 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 297–337Google Scholar
- Bouillet J-P, Laclau J-P, 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. Forest Ecol Manag 255:3918–3930. https://doi.org/10.1016/j.foreco.2007.10.050 CrossRefGoogle Scholar
- Bouillet J-P, Laclau J-P, Gonçalves JLM, Voigtlaender M, Gava JL, Leite FP, Hakamada R, Mareschal L, Mabiala A, Tardy F, Levillain J, Deleporte P, Epron D, Nouvellon Y (2013) Eucalyptus and Acacia tree growth over entire rotation in single- and mixed-species plantations across five sites in Brazil and Congo. Forest Ecol Manag 301:89–101. https://doi.org/10.1016/j.foreco.2012.09.019 CrossRefGoogle Scholar
- Diagne N, Thioulouse J, Sanguin H, Prin Y, Krasova-Wade T, Sylla S, Galiana A, Baudoin E, Neyra M, Svistoonoff S, Lebrun M, Duponnois R (2013) Ectomycorrhizal diversity enhances growth and nitrogen fixation of Acacia mangium seedlings. Soil Biol Biochem 57:468–476. https://doi.org/10.1016/j.soilbio.2012.08.030 CrossRefGoogle Scholar
- Epron D, Laclau J-P, Almeida JCR, Gonçalves JLM, Ponton S, Sette C Jr, Delgado-Rojas J, Bouillet JP, Nouvellon Y (2012) Do changes in carbon allocation account for the growth response to potassium and sodium applications in tropical Eucalyptus plantations? Tree Physiol 32:667–679. https://doi.org/10.1093/treephys/tpr107 CrossRefPubMedGoogle Scholar
- Epron D, Nouvellon Y, Mareschal L, Moreira RM, Koutika L-S, Geneste B, Delgado-Rojas JS, Laclau J-P, Sola G, Gonçalves JLM, Bouillet J-P (2013) Partitioning of net primary production in Eucalyptus and Acacia stands and in mixed-species plantations: a comparison in two contrasting tropical environments. Forest Ecol Manag 301:102–111. https://doi.org/10.1016/j.foreco.2012.10.034 CrossRefGoogle Scholar
- FAO (2010) Global Forest Resources Assessment. Food and Agriculture Organization of the United Nations. http://www.fao.org/forestry/fra/fra2010/en/. Accessed 15 June 2016
- Galiana A, Balle P, N’Guessan Kanga A, 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 CrossRefGoogle Scholar
- Germon A, Guerrini IA, Bordron B, Bouillet J-P, Nouvellon Y, Gonçalves JLM, Jourdan C, Paula RR, Laclau J-P (2017) Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m. Plant Soil doi: https://doi.org/10.1007/s11104-017-3428-1
- Gonçalves JLM, Stape JL, Laclau J-P, Bouillet J-P, Ranger J (2008) Assessing the effects of early management on long-term site productivity of fast-growing eucalypt plantations: the Brazilian experience. South Forests 70:105–118. https://doi.org/10.2989/SOUTH.FOR.2008.70.2.6.534 CrossRefGoogle Scholar
- Gonçalves JLM, Alvares CA, Higa AR, Silva LD, Alfenas AC, Stahl J, Ferraz SFB, Lima WP Brancalioni PHS, Hubner A, Bouillet J-P, Laclau J-P, Nouvellon Y, Epron D (2013) Integrating genetic and silvicultural strategies to minimize abiotic and biotic constraints in Brazilian eucalypt plantations. Forest Ecol Manag 301:6–27. https://doi.org/10.1016/j.foreco.2012.12.030 CrossRefGoogle Scholar
- Laclau J-P, Almeida JCR, Gonçalves JLM, Saint-André L, Ventura M, Ranger J, Moreira RM, Nouvellon Y (2009) Influence of nitrogen and potassium fertilization on leaf lifespan and allocation of above-ground growth in Eucalyptus plantations. Tree Physiol 29:111–124. https://doi.org/10.1093/treephys/tpn010 CrossRefPubMedGoogle Scholar
- Laclau J-P, Bouillet J-P, Gonçalves JLM, Silva EV, Jourdan C, Cunha MCS, Moreira RM, Saint-André L, Maquère V, Nouvellon Y, Ranger J (2008) Mixed-species plantations of Acacia mangium and Eucalyptus grandis in Brazil: 1. Growth dynamics and aboveground net primary production. Forest Ecol Manag 255:3905–3917. https://doi.org/10.1016/j.foreco.2007.10.049 CrossRefGoogle Scholar
- Laclau J-P, Nouvellon Y, Reine C, Gonçalves JLM, Krushe AV, Jourdan C, le Maire G, Bouillet J-P (2013) Mixing Eucalyptus and Acacia trees leads to fine root over-yielding and vertical segregation between species. Oecologia 172:903–913. https://doi.org/10.1007/s00442-012-2526-2 CrossRefPubMedGoogle Scholar
- le Maire G, Nouvellon Y, Christina M, Ponzoni FJ, Gonçalves JLM, Bouillet J-P, Laclau J-P (2013) Tree and stand light use efficiencies over a full rotation of single- and mixed-species Eucalyptus grandis and Acacia mangium plantations. Forest Ecol Manag 288:31–42. https://doi.org/10.1016/j.foreco.2012.03.005 CrossRefGoogle Scholar
- Li B, Li Y-Y, Wua H-M, Zhanga FF, Li CJ, Li X-X, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. PNAS 113:6496–6501. https://doi.org/10.1073/pnas.1523580113/-/DCSupplemental CrossRefPubMedPubMedCentralGoogle Scholar
- Lumley T using Fortran code by Alan Miller (2009) leaps: regression sub set selection. R package version 2.9.https://CRAN.R-project.org/package=leaps. Accessed 24 May 2016
- Maquère V (2008) Dynamics of mineral elements under a fast-growing eucalyptus plantation in Brazil. Implication for soil sustainability. Thesis, Agroparitech, ParisGoogle Scholar
- Nouvellon Y, Laclau J-P, Epron D, le Maire G, Bonnefond J-M, Gonçalves JLM, Bouillet J-P (2012) Production and carbon allocation in monocultures and mixed-species plantations of Eucalyptus grandis and Acacia mangium in Brazil. Tree Physiol 32:680–695. https://doi.org/10.1093/treephys/tps041 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- Prudent M, Vernoud V, Girodet S, Salon C (2016) How nitrogen fixation is modulated in response to different water availability levels and during recovery: a structural and functional study at the whole plant level. Plant Soil 399:1–12. https://doi.org/10.1007/s11104-015-2674-3 CrossRefGoogle Scholar
- Rachid CTCC, Balieiro FC, Peixoto RS, Pinheiro YAS, Piccolo MC, Chaer GM, Rosado AS (2013) Mixed plantations can promote microbial integration and soil nitrate increases with changes in the N cycling genes. Soil Biol Biochem 66:146–153. https://doi.org/10.1016/j.soilbio.2013.07.005 CrossRefGoogle Scholar
- R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/. Accessed 10 May 2016
- Santos FM, Balieiro FC, Ataíde DHS, Diniz AR, Chaer GM (2016) Dynamics of aboveground biomass accumulation in monospecific and mixed-species plantations of Eucalyptus and Acacia on a Brazilian sandy soil. Forest Ecol Manag 363:86–97. https://doi.org/10.1016/j.foreco.2015.12.028 CrossRefGoogle Scholar
- Silva EV, Gonçalves JLM, Coelho SRF, Moreira RM, Mello SLM, Bouillet J-P, Jourdan C, Laclau J-P (2009) Dynamics of fine root distribution after establishment of monospecific and mixed-species plantations of Eucalyptus grandis and Acacia mangium. Plant Soil 325:305–318. https://doi.org/10.1007/s11104-009-9980-6 CrossRefGoogle Scholar
- Voigtlaender M, Laclau J-P, Gonçalves JLM, Piccolo MC, Moreira MZ, Nouvellon Y, Ranger J, Bouillet J-P (2012) Introducing Acacia mangium trees in Eucalyptus grandis plantations: consequences for soil organic matter stocks and nitrogen mineralization. Plant Soil 352:99–111. https://doi.org/10.1007/s11104-011-0982-9 CrossRefGoogle Scholar
- Wickham H, Francois R (2015) dplyr: a grammar of data manipulation. R package version 0.4.3. https://CRAN.R-project.org/package=dplyr.Accessed: 15 May 2016