Article | Published:

Legume abundance along successional and rainfall gradients in Neotropical forests

Nature Ecology & Evolutionvolume 2pages11041111 (2018) | Download Citation

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Global Forest Resources Assessment 2015: How Are the World’s Forests Changing? (FAO, Rome, 2015).

  2. 2.

    Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).

  3. 3.

    Chazdon, R. L. et al. Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Sci. Adv. 2, e1501639 (2017).

  4. 4.

    Davidson, E. A. et al. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol. Appl. 14, S150–S163 (2004).

  5. 5.

    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).

  6. 6.

    Batterman, S. A. et al. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227 (2013).

  7. 7.

    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).

  8. 8.

    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).

  9. 9.

    ter Steege, H. et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447 (2006).

  10. 10.

    DRYFLOR Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353, 1383–1387 (2016).

  11. 11.

    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).

  12. 12.

    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).

  13. 13.

    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).

  14. 14.

    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).

  15. 15.

    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).

  16. 16.

    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).

  17. 17.

    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).

  18. 18.

    Bastin, J.-F. et al. The extent of forest in dryland biomes. Science 356, 635–638 (2017).

  19. 19.

    Vitousek, P. M. et al. Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45 (2002).

  20. 20.

    Wurzburger, N. & Ford Miniat, C. Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174, 1117–1126 (2013).

  21. 21.

    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).

  22. 22.

    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).

  23. 23.

    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).

  24. 24.

    Poorter, L. et al. Biomass resilience of Neotropical secondary forests. Nature 530, 211–214 (2016).

  25. 25.

    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).

  26. 26.

    Chave, J. et al. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob. Change Biol. 20, 3177–3190 (2014).

  27. 27.

    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).

  28. 28.

    Slik, J. W. et al. Phylogenetic classification of the world’s tropical forests. Proc. Natl Acad. Sci. USA 115, 1837–1842 (2018).

  29. 29.

    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).

  30. 30.

    Hughes, C. E., Pennington, R. T. SpringerAmpamp; Antonelli, A. Neotropical plant evolution: assembling the big picture. Bot. J. Linn. Soc. 171, 1–18 (2013).

  31. 31.

    Sprent, J. I. Legume Nodulation: A Global Perspective (Wiley-Blackwell, Oxford, 2009).

  32. 32.

    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).

  33. 33.

    Parkhurst, D. F. & Loucks, O. L. Optimal leaf size in relation to environment. J. Ecol. 60, 505–537 (1972).

  34. 34.

    Wright, I. J. et al. Global climatic drivers of leaf size. Science 357, 917–921 (2017).

  35. 35.

    Givnish, T. J. in Tropical Trees as Living Systems (eds Tomlinson, P. B. & Zimmerman, M. H.) 351–380 (Cambridge Univ. Press, New York, 1978).

  36. 36.

    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).

  37. 37.

    Davidson, E. A. et al. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447, 995–998 (2007).

  38. 38.

    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).

  39. 39.

    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).

  40. 40.

    Lodge, M. M., McDowell, W. H. & McSwiney, C. P. The importance of nutrient pulses in tropical forests. Trends Ecol. Evol. 9, 384–387 (1994).

  41. 41.

    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).

  42. 42.

    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).

  43. 43.

    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).

  44. 44.

    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).

  45. 45.

    Legume Phylogeny Working Group A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66, 44–77 (2017).

  46. 46.

    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).

  47. 47.

    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).

  48. 48.

    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).

  49. 49.

    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).

  50. 50.

    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).

  51. 51.

    Barron, A. R. Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat. Geosci. 2, 42–45 (2008).

  52. 52.

    Winbourne, J. B., Brewer, S. W. & Houlton, B. Z. Iron controls over di-nitrogen fixation in karst tropical forest. Ecology 98, 773–781 (2017).

  53. 53.

    Feng, X., Porporato, A. & Rodriguez-Iturbe, I. Changes in rainfall seasonality in the tropics. Nat. Clim. Change 3, 811–815 (2013).

  54. 54.

    Kew Herbarium Catalogue (Royal Botanic Gardens Kew, accessed 2016); http://apps.kew.org/herbcat/

  55. 55.

    Tropicos (Missouri Botanical Garden, accessed 2016); http://www.tropicos.org/

  56. 56.

    Neotropical Herbarium Specimens (The Field Museum, accessed 2016); http://fm1.fieldmuseum.org/vrrc/

  57. 57.

    OTS Plant Database (Organization for Tropical Studies, accessed 2016); https://tropicalstudies.org/index.php?option=com_wrapper&Itemid=497

  58. 58.

    The Arizona–New Mexico Chapter of the Southwest Environmental Information Network (SEINet, accessed 2016); http://swbiodiversity.org/seinet/

  59. 59.

    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).

  60. 60.

    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).

  61. 61.

    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).

  62. 62.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2015).

Download references

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

Affiliations

  1. Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN, USA

    • Maga Gei
    •  & Jennifer S. Powers
  2. Department of Biology, University of Regina, Regina, Saskatchewan, Canada

    • Danaë M. A. Rozendaal
  3. Forest Ecology and Forest Management Group, Wageningen University and Research, Wageningen, The Netherlands

    • Danaë M. A. Rozendaal
    • , Lourens Poorter
    • , Frans Bongers
    • , Madelon Lohbeck
    •  & Marielos Peña-Claros
  4. Laboratory of Geo-Information Science and Remote Sensing, Wageningen University and Research, Wageningen, The Netherlands

    • Danaë M. A. Rozendaal
  5. Royal Botanic Gardens Edinburgh, Edinburgh, UK

    • Janet I. Sprent
  6. College of Biological Sciences, University of Minnesota, St. Paul, MN, USA

    • Mira D. Garner
  7. Department of Biology, University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico

    • T. Mitchell Aide
  8. Centro de Investigación Científica de Yucatán, Unidad de Recursos Naturales, Mérida, Yucatán, Mexico

    • José Luis Andrade
    • , Juan Manuel Dupuy
    • , José Luis Hernández-Stefanoni
    • , Casandra Reyes-García
    •  & Lucía Sanaphre-Villanueva
  9. Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Mexico

    • Patricia Balvanera
    • , Miguel Martínez-Ramos
    • , Francisco Mora
    • , Jorge Rodríguez-Velázquez
    •  & Lucía Sanaphre-Villanueva
  10. Environmental Studies Program, Colby College, Waterville, ME, USA

    • Justin M. Becknell
  11. Department of Forest Sciences, Luiz de Queiroz College of Agriculture, University of São Paulo, Piracicaba, Brazil

    • Pedro H. S. Brancalion
    • , Ricardo Gomes César
    •  & Vanessa de Souza Moreno
  12. Departamento de Genética, Universidade Federal de Pernambuco, Recife, Brazil

    • George A. L. Cabral
  13. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA

    • Robin L. Chazdon
  14. International Institute for Sustainability, Rio de Janeiro, Brazil

    • Robin L. Chazdon
    •  & André B. Junqueira
  15. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA

    • Robin L. Chazdon
  16. Tropical Forests and People Research Centre, University of the Sunshine Coast, Sippy Downs, Queensland, Australia

    • Robin L. Chazdon
  17. Department of Natural Resources and Environmental Management, University of Hawaii at Manoa, Honolulu, HI, USA

    • Rebecca J. Cole
  18. Programa de Pós-graduação em Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, Brazil

    • Gabriel Dalla Colletta
  19. Department of Sustainability Science, El Colegio de la Frontera Sur, Campeche, Mexico

    • Ben de Jong
    •  & Susana Ochoa-Gaona
  20. Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA, USA

    • Julie S. Denslow
  21. Smithsonian Tropical Research Institute, Panamá, Republic of Panama

    • Daisy H. Dent
    •  & Jennifer S. Powers
  22. Biological and Environmental Sciences, University of Stirling, Stirling, UK

    • Daisy H. Dent
  23. Department of Biological Sciences, Clemson University, Clemson, SC, USA

    • Saara J. DeWalt
  24. Earth and Atmospheric Sciences Department, University of Alberta, Edmonton, Alberta, Canada

    • Sandra M. Durán
    •  & Arturo Sanchez-Azofeifa
  25. Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, Brazil

    • Mário Marcos do Espírito Santo
    • , Yule Roberta Ferreira Nunes
    •  & Maria das Dores Magalhães Veloso
  26. Ecologia Evolutiva and Biodiversidade/DBG, ICB/Universidade Federal de Minas Gerais, Belo Horizonte, Brazil

    • G. Wilson Fernandes
  27. Forests, Biodiversity and Climate Change Programme, Tropical Agricultural Centre for Research and Higher Education (CATIE), Turrialba, Costa Rica

    • Bryan Finegan
  28. Graduate School, Tropical Agricultural Centre for Research and Higher Education (CATIE), Turrialba, Costa Rica

    • Vanessa Granda Moser
  29. ForestGEO, Smithsonian Tropical Research Institute, Panamá, Republic of Panama

    • Jefferson S. Hall
    •  & Michiel van Breugel
  30. Department of Soil Quality, Wageningen University, Wageningen, The Netherlands

    • André B. Junqueira
  31. Centre for Conservation and Sustainability Science (CSRio), Department of Geography and the Environment, Pontifical Catholic University of Rio de Janeiro, Rio de Janeiro, Brazil

    • André B. Junqueira
  32. Department of Physical and Environmental Sciences, Colorado Mesa University, Grand Junction, CO, USA

    • Deborah Kennard
  33. Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa-Oranim, Tivon, Israel

    • Edwin Lebrija-Trejos
  34. Department of Plant Biology, College of the Atlantic, Bar Harbor, ME, USA

    • Susan G. Letcher
  35. World Agroforestry Centre (ICRAF), Nairobi, Kenya

    • Madelon Lohbeck
  36. Department of Geography, University of Wisconsin–Madison, Madison, WI, USA

    • Erika Marín-Spiotta
  37. Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico

    • Jorge A. Meave
    • , Rodrigo Muñoz
    • , Eduardo A. Pérez-García
    •  & I. Eunice Romero-Pérez
  38. Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, NY, USA

    • Duncan N. L. Menge
    • , Naomi B. Schwartz
    •  & Maria Uriarte
  39. Section for Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, Aarhus, Denmark

    • Robert Muscarella
  40. National Institute of Ecology and Climate Change, Delegación Coyoacán, Mexico

    • Edith Orihuela-Belmonte
  41. Department of Biology, University of Hawaii at Hilo, Hilo, HI, USA

    • Rebecca Ostertag
  42. Centro de Formação em Ciências Agroflorestais, Universidade Federal do Sul da Bahia, Itabuna, Brazil

    • Daniel Piotto
  43. Department of Forest Resources, University of Minnesota, St. Paul, MN, USA

    • Peter B. Reich
  44. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia

    • Peter B. Reich
  45. Museu Paraense Emilio Goeldi, Belém, Brazil

    • Arlete Silva de Almeida
    •  & Ima Célia Guimarães Vieira
  46. Departamento de Botânica, Universidade Federal de Pernambuco, Recife, Brazil

    • Jarcilene S. Almeida-Cortez
  47. Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA

    • Whendee Silver
  48. Department of Natural Resources and Environmental Science, University of Nevada, Reno, NV, USA

    • Benjamin W. Sullivan
  49. Department of Biology, University of Maryland, College Park, MD, USA

    • Nathan G. Swenson
  50. Yale-NUS College, Singapore and Department of Biological Sciences, National University of Singapore, Singapore, Singapore

    • Michiel van Breugel
  51. Grupo Académico de Agroecología, Departamento de Agricultura, Sociedad y Ambiente, El Colegio de la Frontera Sur, Tabasco, Mexico

    • Hans van der Wal
  52. Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, Amsterdam, The Netherlands

    • Hans F. M. Vester
  53. Department of Environmental Sciences, University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico

    • Jess K. Zimmerman
  54. Department of Plant Biology and Microbial Biology, University of Minnesota, St. Paul, MN, USA

    • Jennifer S. Powers

Authors

  1. Search for Maga Gei in:

  2. Search for Danaë M. A. Rozendaal in:

  3. Search for Lourens Poorter in:

  4. Search for Frans Bongers in:

  5. Search for Janet I. Sprent in:

  6. Search for Mira D. Garner in:

  7. Search for T. Mitchell Aide in:

  8. Search for José Luis Andrade in:

  9. Search for Patricia Balvanera in:

  10. Search for Justin M. Becknell in:

  11. Search for Pedro H. S. Brancalion in:

  12. Search for George A. L. Cabral in:

  13. Search for Ricardo Gomes César in:

  14. Search for Robin L. Chazdon in:

  15. Search for Rebecca J. Cole in:

  16. Search for Gabriel Dalla Colletta in:

  17. Search for Ben de Jong in:

  18. Search for Julie S. Denslow in:

  19. Search for Daisy H. Dent in:

  20. Search for Saara J. DeWalt in:

  21. Search for Juan Manuel Dupuy in:

  22. Search for Sandra M. Durán in:

  23. Search for Mário Marcos do Espírito Santo in:

  24. Search for G. Wilson Fernandes in:

  25. Search for Yule Roberta Ferreira Nunes in:

  26. Search for Bryan Finegan in:

  27. Search for Vanessa Granda Moser in:

  28. Search for Jefferson S. Hall in:

  29. Search for José Luis Hernández-Stefanoni in:

  30. Search for André B. Junqueira in:

  31. Search for Deborah Kennard in:

  32. Search for Edwin Lebrija-Trejos in:

  33. Search for Susan G. Letcher in:

  34. Search for Madelon Lohbeck in:

  35. Search for Erika Marín-Spiotta in:

  36. Search for Miguel Martínez-Ramos in:

  37. Search for Jorge A. Meave in:

  38. Search for Duncan N. L. Menge in:

  39. Search for Francisco Mora in:

  40. Search for Rodrigo Muñoz in:

  41. Search for Robert Muscarella in:

  42. Search for Susana Ochoa-Gaona in:

  43. Search for Edith Orihuela-Belmonte in:

  44. Search for Rebecca Ostertag in:

  45. Search for Marielos Peña-Claros in:

  46. Search for Eduardo A. Pérez-García in:

  47. Search for Daniel Piotto in:

  48. Search for Peter B. Reich in:

  49. Search for Casandra Reyes-García in:

  50. Search for Jorge Rodríguez-Velázquez in:

  51. Search for I. Eunice Romero-Pérez in:

  52. Search for Lucía Sanaphre-Villanueva in:

  53. Search for Arturo Sanchez-Azofeifa in:

  54. Search for Naomi B. Schwartz in:

  55. Search for Arlete Silva de Almeida in:

  56. Search for Jarcilene S. Almeida-Cortez in:

  57. Search for Whendee Silver in:

  58. Search for Vanessa de Souza Moreno in:

  59. Search for Benjamin W. Sullivan in:

  60. Search for Nathan G. Swenson in:

  61. Search for Maria Uriarte in:

  62. Search for Michiel van Breugel in:

  63. Search for Hans van der Wal in:

  64. Search for Maria das Dores Magalhães Veloso in:

  65. Search for Hans F. M. Vester in:

  66. Search for Ima Célia Guimarães Vieira in:

  67. Search for Jess K. Zimmerman in:

  68. Search for Jennifer S. Powers in:

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.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Jennifer S. Powers.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–7, Supplementary Tables 2, 4, 5 and 6, Supplementary References

  2. Reporting Summary

  3. Supplementary Table 1

    Metadata associated with 2ndFOR sites in the neotropics

  4. 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)

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41559-018-0559-6

Further reading