Abstract
The nutrient demands of regrowing tropical forests are partly satisfied by nitrogen-fixing legume trees, but our understanding of the abundance of those species is biased towards wet tropical regions. Here we show how the abundance of Leguminosae is affected by both recovery from disturbance and large-scale rainfall gradients through a synthesis of forest inventory plots from a network of 42 Neotropical forest chronosequences. During the first three decades of natural forest regeneration, legume basal area is twice as high in dry compared with wet secondary forests. The tremendous ecological success of legumes in recently disturbed, water-limited forests is likely to be related to both their reduced leaflet size and ability to fix N2, which together enhance legume drought tolerance and water-use efficiency. Earth system models should incorporate these large-scale successional and climatic patterns of legume dominance to provide more accurate estimates of the maximum potential for natural nitrogen fixation across tropical forests.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Global Forest Resources Assessment 2015: How Are the World’s Forests Changing? (FAO, Rome, 2015).
Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).
Chazdon, R. L. et al. Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Sci. Adv. 2, e1501639 (2017).
Davidson, E. A. et al. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol. Appl. 14, S150–S163 (2004).
Cleveland, C. C. et al. Patterns of new versus recycled primary production in the terrestrial biosphere. Proc. Natl Acad. Sci. USA 110, 12733–12737 (2013).
Batterman, S. A. et al. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227 (2013).
Barron, A. R., Purves, D. W. & Hedin, L. O. Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165, 511–520 (2010).
Wieder, W. R., Cleveland, C. C., Lawrence, D. M. & Bonan, G. B. Effects of model structural uncertainty on carbon cycle projections: biological nitrogen fixation as a case study. Environ. Res. Lett. 10, 1–9 (2015).
ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).
DRYFLOR Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353, 1383–1387 (2016).
Oliveira-Filho, A. T. et al. Stability structures tropical woody plant diversity more than seasonality: insights into the ecology of high legume-succulent-plant biodiversity. S. Afr. J. Bot. 89, 42–57 (2013).
Pellegrini, A. F. A., Staver, A. C., Hedin, L. O., Charles-Dominique, T. & Tourgee, A. Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes. Ecology 97, 2177–2183 (2016).
Gehring, C., Muniz, F. H., & Gomes de Souza, L. A. Leguminosae along 2–25 years of secondary forest succession after slash-and-burn agriculture and in mature rain forest of central Amazonia. J. Torre. Bot. Soc. 135, 388–400 (2008).
Sullivan, B. W. et al. Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc. Natl Acad. Sci. USA 111, 8101–8106 (2014).
Menge, D. N. L. & Chazdon, R. L. Higher survival drives the success of nitrogen-fixing trees through succession in Costa Rican rainforests. New Phytol. 209, 965–977 (2015).
Bauters, M., Mapenzi, N., Kearsley, E., Vanlauwe, B. & Boeckx, P. Facultative nitrogen fixation by legumes in the central Congo Basin is downregulated during late successional stages. Biotropica 48, 281–284 (2016).
Lebrija-Trejos, E., Pérez-García, E. A., Meave, J. A., Bongers, F. & Poorter, L. Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology 91, 386–398 (2010).
Bastin, J.-F. et al. The extent of forest in dryland biomes. Science 356, 635–638 (2017).
Vitousek, P. M. et al. Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45 (2002).
Wurzburger, N. & Ford Miniat, C. Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174, 1117–1126 (2013).
Adams, M. A., Turnbull, T. L., Sprent, J. I. & Buchmann, N. Legumes are different: leaf nitrogen, photosynthesis, and water use efficiency. Proc. Natl Acad. Sci. USA 113, 4098–4103 (2016).
Menge, D. N. L., Levin, S. A. & Hedin, L. O. Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am. Nat. 174, 465–477 (2009).
Sheffer, E., Batterman, S. A., Levin, S. A. & Hedin, L. O. Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle. Nat. Plants 1, 15182 (2015).
Poorter, L. et al. Biomass resilience of Neotropical secondary forests. Nature 530, 211–214 (2016).
Hijmans, R. J., Cameron, S. E., Parra, J. L., P. Jones, G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Chave, J. et al. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob. Change Biol. 20, 3177–3190 (2014).
Vico, G., Dralle, D., Feng, X., Thompson, S., & Manzoni, S. How competitive is drought deciduousness in tropical forests? A combined eco-hydrological and eco-evolutionary approach. Environ. Res. Lett. 12, 065006 (2017).
Slik, J. W. et al. Phylogenetic classification of the world’s tropical forests. Proc. Natl Acad. Sci. USA 115, 1837–1842 (2018).
Pennington, R. T., Lavin, M. & Oliveira-Filho, A. Woody plant diversity, evolution, and ecology in the tropics: perspectives from seasonally dry tropical forests. Annu. Rev. Ecol. Evol. Syst. 40, 437–457 (2009).
Hughes, C. E., Pennington, R. T. SpringerAmpamp; Antonelli, A. Neotropical plant evolution: assembling the big picture. Bot. J. Linn. Soc. 171, 1–18 (2013).
Sprent, J. I. Legume Nodulation: A Global Perspective (Wiley-Blackwell, Oxford, 2009).
Leigh, A., Sevanto, S., Close, J. D. & Nicotra, A. B. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant Cell Environ. 40, 237–248 (2017).
Parkhurst, D. F. & Loucks, O. L. Optimal leaf size in relation to environment. J. Ecol. 60, 505–537 (1972).
Wright, I. J. et al. Global climatic drivers of leaf size. Science 357, 917–921 (2017).
Givnish, T. J. in Tropical Trees as Living Systems (eds Tomlinson, P. B. & Zimmerman, M. H.) 351–380 (Cambridge Univ. Press, New York, 1978).
Liao, W., Menge, D. N. L., Lichstein, J. W., & Ángeles-Pérez, G. Global climate change will increase the abundance of symbiotic nitrogen-fixing trees in much of North America. Glob. Change Biol. 23, 4777–4787 (2017).
Davidson, E. A. et al. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447, 995–998 (2007).
Powers, J. S. & Marín-Spiotta, E. Ecosystem processes and biogeochemical cycles in secondary tropical forest succession. Annu. Rev. Ecol. Evol. Syst. 48, 497–519 (2017).
Winbourne, J. B., Feng, A., Reynolds, L., Piotto, D., Hastings, M. G. & Porder, S. Nitrogen cycling during secondary succession in Atlantic Forest of Bahia, Brazil. Sci. Rep. 8, 1377 (2018).
Lodge, M. M., McDowell, W. H. & McSwiney, C. P. The importance of nutrient pulses in tropical forests. Trends Ecol. Evol. 9, 384–387 (1994).
Minucci, J. M., Miniat, C. F., Teskey, R. O. & Wurzburger, N. Tolerance or avoidance: drought frequency determines the response of an N2-fixing tree. New Phytol. 215, 434–442 (2017).
Lebrija-Trejos, E., Pérez-García, E. A., Meave, J. A., Poorter, L. & Bongers, F. Environmental changes during secondary succession in a tropical dry forest in Mexico. J. Trop. Ecol. 27, 477–489 (2011).
Wright, I. J., Reich, P. B. & Westoby, M. Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct. Ecol. 15, 423–434 (2001).
van Zanten, M., Pons, T. L., Janssen, J. A. M., Voesenek, L. A. C. J. & Peeters, A. J. M. On the relevance and control of leaf angle. Crit. Rev. Plant Sci. 29, 300–316 (2010).
Legume Phylogeny Working Group A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66, 44–77 (2017).
Legume Phylogeny Working Group Legume phylogeny and classification in the 21st century: progress, prospects and lessons for other species-rich clades. Taxon 62, 217–248 (2013).
Schrire, B. D., Lavin, M. & Lewis, G.P. in Plant Diversity and Complexity Patterns: Local, Regional and Global Dimensions Biologiske Skrifter Vol. 55 (eds Friis, I. & Balslev, H.) 375–422 (The Royal Danish Academy of Sciences and Letters, Copenhagen, 2005).
Derroire, G., Tigabu, M., Odén, P. C. & Healey, J. R. The effects of established trees on woody regeneration during secondary succession in tropical dry forests. Biotropica 48, 290–300 (2016).
Taylor, B. N., Chazdon, R. L., Bachelot, B. & Menge, D. N. Nitrogen-fixing trees inhibit growth of regenerating Costa Rican rainforests. Proc. Natl Acad. Sci. USA 114, 8817–8822 (2017).
Nasto, M. K. et al. Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol. Lett. 17, 1282–1289 (2014).
Barron, A. R. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat. Geosci. 2, 42–45 (2008).
Winbourne, J. B., Brewer, S. W. & Houlton, B. Z. Iron controls over di-nitrogen fixation in karst tropical forest. Ecology 98, 773–781 (2017).
Feng, X., Porporato, A. & Rodriguez-Iturbe, I. Changes in rainfall seasonality in the tropics. Nat. Clim. Change 3, 811–815 (2013).
Kew Herbarium Catalogue (Royal Botanic Gardens Kew, accessed 2016); http://apps.kew.org/herbcat/
Tropicos (Missouri Botanical Garden, accessed 2016); http://www.tropicos.org/
Neotropical Herbarium Specimens (The Field Museum, accessed 2016); http://fm1.fieldmuseum.org/vrrc/
OTS Plant Database (Organization for Tropical Studies, accessed 2016); https://tropicalstudies.org/index.php?option=com_wrapper&Itemid=497
The Arizona–New Mexico Chapter of the Southwest Environmental Information Network (SEINet, accessed 2016); http://swbiodiversity.org/seinet/
Rozendaal, D. M. A., Hurtado, V. H. & Poorter, L. Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Funct. Ecol. 20, 207–216 (2006).
Markesteijn, L., Poorter, L. & Bongers, F. Light-dependent leaf trait variation in 43 tropical dry forest tree species. Am. J. Bot. 94, 515–525 (2007).
Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2012).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2015).
Acknowledgements
This paper is a product of the 2ndFOR collaborative research network on secondary forests. We thank the owners of the sites for access to their forests, the people who have established and measured the plots, and the institutions and funding agencies that supported them. This study was partly funded by a University of Minnesota Grant-in-Aid to J.S.P. that supported M.G. We thank the University of Minnesota Herbarium and A. Cholewa for access to herbarium collections, and S. St. George, C. Cleveland and P. Tiffin for comments. Additional funding was provided by Secretaría de Educación Pública-Consejo Nacional de Ciencia y Tecnología, Ciencia Básica (SEP-CONACYT: CB-2009-128136, CB-2015-255544), Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, Universidad Nacional Autónoma de México (PAPIIT-UNAM: 218416, 211114, IN212617), United States Agency for International Development BOLFOR Project, Andrew Mellon Foundation, United States National Science Foundation (Division of Environmental Biology: DEB-0129104, DEB-1050957, DEB-1053237, DEB-9208031, DEB-0424767, DEB-0639393, DEB-1147429, DEB-0129104, 10-02586, DEB-1313788), National Science Foundation CAREER Behavioral and Cognitive Sciences 1349952, National Science Foundation Geosciences GEO-1128040, United States Department of Energy (Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Science Program award number DE-SC0014363), United States National Aeronautics and Space Agency Terrestrial Ecology Program, the University of Connecticut Research Foundation, Tropi-Dry - a collaborative Research Network funded by the Inter-American Institute for Global Change Research (IAI CRN3-025, IAI CRN3035) under the US National Sciences Foundation, the National Science and Research Council of Canada (NSERC) Discovery Grant Program, Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG), Instituto Internacional de Educação do Brasil, Netherlands Organization for Cooperation in Higher Education, Interdisciplinary Research and Education Fund (Wageningen University) Terra Preta and FOREFRONT Programmes, Secretaria Nacional de Ciencia, Tecnologia e Innovacion, Panama (SENACYT: International Collaboration grant, COL10-052), Fondo Mixto Consejo Nacional de Ciencia y Tecnología - Gobierno del Estado de Yucatán (Yuc-2008-C06-108863), El Consejo de Ciencia y Technologia Grant 33851-B, São Paulo Research Foundation (FAPESP; grants #2013/50718-5, #2011/14517-0, #2014/14503-7, 2011/06782-5 and 2014/14503-7), Coordination for the Improvement of Higher Education Personnel of Brazil (CAPES; grant #88881.064976/2014-01), the National Council for Scientific and Technological Development of Brazil (CNPq; grant #304817/2015-5, 306375/2016-8, 563304/2010-3, 308471/2017-2), El Consejo de Ciencia y Technologia Grant 33851-B, Stichting Het Kronendak, Stichting Tropenbos, Center for International Forestry Research, Norwegian Agency for Development Cooperation (Norad), International Climate Initiative (IKI) of the German Federal Ministry for the Environment, Nature Conservation, and Building and Nuclear Safety (BMUB), Yale-NUS College grant R-607-265-054-121, Heising-Simons Foundation, Hoch Family, Silicon Valley Foundation, Stanley Motta, Smithsonian Tropical Research Institute and the Grantham Foundation for the Environment.
Author information
Authors and Affiliations
Contributions
M.G. and J.S.P. conceived the idea, all co-authors coordinated the data compilations, M.G. and M.D.G. collected leaf traits data, M.G. analysed the data, D.M.A.R. contributed to the analytical approach, M.G. and J.S.P. wrote the paper, and all co-authors collected field data, discussed the results, gave suggestions for further analyses and commented on the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Figures 1–7, Supplementary Tables 2, 4, 5 and 6, Supplementary References
Supplementary Table 1
Metadata associated with 2ndFOR sites in the neotropics
Supplementary Table 3
List of 398 Leguminosae species present in 42 neotropical chronosequences, their current (and previous) subfamily classification, their potential to form symbioses with N-fixing bacteria, leaf type, and average (and standard deviation) leaflet length and width (cm)
Rights and permissions
About this article
Cite this article
Gei, M., Rozendaal, D.M.A., Poorter, L. et al. Legume abundance along successional and rainfall gradients in Neotropical forests. Nat Ecol Evol 2, 1104–1111 (2018). https://doi.org/10.1038/s41559-018-0559-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-018-0559-6
This article is cited by
-
Biological nitrogen fixation in young and old tropical forests under five contrasting edaphoclimatic conditions
Nutrient Cycling in Agroecosystems (2024)
-
Symbiotic bacteria associated with legume tree species in a Mexican tropical dry forest
Brazilian Journal of Botany (2023)
-
Enhanced carbon, nitrogen and associated bacterial community compositional complexity, stability, evenness, and differences within the tree-soils of Inga punctata along an age gradient of planted trees in reforestation plots
Plant and Soil (2023)
-
Can we see the nitrate from the trees? Long-term linkages between tropical forest productivity and stream nitrogen concentrations
Biogeochemistry (2023)
-
Nitrogen and light regulate symbiotic nitrogen fixation by a temperate forest tree
Oecologia (2023)
