Legume abundance along successional and rainfall gradients in Neotropical forests

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.Data from 42 chronosequence sites show a geater abundance of legumes in seasonally dry forests than in wet forests, particularly during early secondary succession, probably owing to legumes’ nitrogen-fixing ability and reduced leaflet size.

José Luis Hernández-Stefanoni | Juan Manuel Dupuy | Arturo Sanchez-Azofeifa | Frans Bongers | Miguel Martínez-Ramos | Patricia Balvanera | Peter B Reich | Robert Muscarella | Julie S Denslow | José Luis Andrade | Daniel Piotto | Susan G. Letcher | Madelon Lohbeck | Michiel van Breugel | Marielos Peña-Claros | Lourens Poorter | W. Silver | J. Zimmerman | P. Balvanera | M. Uriarte | P. Reich | P. Brancalion | N. Swenson | F. Bongers | L. Poorter | J. Denslow | R. Chazdon | T. Aide | B. Finegan | Jefferson S. Hall | D. Kennard | G. Fernandes | Y. Nunes | D. Menge | J. Dupuy | J. Andrade | J. Hernández‐Stefanoni | I. Vieira | A. S. Almeida | M. Breugel | A. Sánchez-Azofeifa | D. Piotto | J. Powers | J. Sprent | D. Dent | E. Lebrija‐Trejos | J. Meave | E. A. Pérez-García | C. Reyes-García | J. Almeida-Cortez | Robert Muscarella | E. Marín-Spiotta | M. Peña-Claros | M. van Breugel | M. Martínez‐Ramos | J. Becknell | M. M. do Espírito Santo | S. Ochoa-Gaona | D. Rozendaal | George A. L. Cabral | Ben H. J. de Jong | S. DeWalt | Sandra M. Durán | R. César | A. B. Junqueira | Madelon Lohbeck | F. Mora | R. Muñoz | Edith Orihuela-Belmonte | J. Rodríguez-Velázquez | I. E. Romero-Pérez | N. Schwartz | Hans van der Wal | Maria D. M. Veloso | H. Vester | H. Wal | R. Ostertag | B. Sullivan | Susana Ochoa-Gaona | R. Cole | Nathan G Swenson | Robin L Chazdon | Susan G Letcher | Bryan Finegan | Jess K Zimmerman | T Mitchell Aide | Jefferson S Hall | Lucía Sanaphre-Villanueva | Maga Gei | Mira Garner | G. Colletta | V. G. Moser | A. S. de Almeida | Vanessa de Souza Moreno | Jennifer S Powers | Maria Uriarte | Francisco Mora | Maga Gei | Danaë M A Rozendaal | Janet I Sprent | Mira D Garner | Justin M Becknell | Pedro H S Brancalion | George A L Cabral | Ricardo Gomes César | Rebecca J Cole | Gabriel Dalla Colletta | Ben de Jong | Daisy H Dent | Saara J DeWalt | Sandra M Durán | Mário Marcos do Espírito Santo | G Wilson Fernandes | Yule Roberta Ferreira Nunes | Vanessa Granda Moser | André B Junqueira | Deborah Kennard | Edwin Lebrija-Trejos | Erika Marín-Spiotta | Jorge A Meave | Duncan N L Menge | Rodrigo Muñoz | Edith Orihuela-Belmonte | Rebecca Ostertag | Eduardo A Pérez-García | Casandra Reyes-García | Jorge Rodríguez-Velázquez | I Eunice Romero-Pérez | Lucía Sanaphre-Villanueva | Naomi B Schwartz | Arlete Silva de Almeida | Jarcilene S Almeida-Cortez | Whendee Silver | Vanessa de Souza Moreno | Benjamin W Sullivan | Hans van der Wal | Maria das Dores Magalhães Veloso | Hans F M Vester | Ima Célia Guimarães Vieira | Edwin Lebrija‐Trejos | H. van der Wal | M. D. E. Santo | Michiel van Breugel | S. Durán | Casandra Reyes-García | Jefferson S. Hall | E. A. PÉREZ-GARCÍA | Peter B. Reich | Ben de Jong | V. S. Moreno | Jennifer S. Powers | Lucía Sanaphre‐Villanueva | R. Muñoz | Vanessa S Moreno

[1]  C. Gehring,et al.  Leguminosae along 2–25 years of secondary forest succession after slash-and-burn agriculture and in mature rain forest of Central Amazonia1 , 2008 .

[2]  W. McDowell,et al.  The importance of nutrient pulses in tropical forests. , 1994, Trends in ecology & evolution.

[3]  S. Levin,et al.  Facultative versus Obligate Nitrogen Fixation Strategies and Their Ecosystem Consequences , 2009, The American Naturalist.

[4]  O. Loucks,et al.  Optimal leaf size in relation to environment , 1972 .

[5]  R. Chazdon,et al.  Nitrogen-fixing trees inhibit growth of regenerating Costa Rican rainforests , 2017, Proceedings of the National Academy of Sciences.

[6]  Erika Marin-Spiotta,et al.  Ecosystem Processes and Biogeochemical Cycles in Secondary Tropical Forest Succession , 2017 .

[7]  B. Houlton,et al.  Iron controls over di-nitrogen fixation in karst tropical forest. , 2017, Ecology.

[8]  N. Buchmann,et al.  Legumes are different: Leaf nitrogen, photosynthesis, and water use efficiency , 2016, Proceedings of the National Academy of Sciences.

[9]  F. Bongers,et al.  Environmental changes during secondary succession in a tropical dry forest in Mexico , 2011, Journal of Tropical Ecology.

[10]  Nitrogen cycling during secondary succession in Atlantic Forest of Bahia, Brazil , 2018, Scientific Reports.

[11]  A. Antonelli,et al.  Neotropical Plant Evolution: Assembling the Big Picture , 2013 .

[12]  I. C. Prentice,et al.  Global climatic drivers of leaf size , 2017, Science.

[13]  J. Downie Legume nodulation , 2014, Current Biology.

[14]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[15]  Sarah J. Graves,et al.  A new urban landscape in East–Southeast Asia, 2000–2010 , 2015 .

[16]  N. Wurzburger,et al.  Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree , 2014, Oecologia.

[17]  Kalle Ruokolainen,et al.  Phylogenetic classification of the world’s tropical forests , 2018, Proceedings of the National Academy of Sciences.

[18]  W. Parton,et al.  Patterns of new versus recycled primary production in the terrestrial biosphere , 2013, Proceedings of the National Academy of Sciences.

[19]  K. Macdicken,et al.  Global Forest Resources Assessment 2015: how are the world's forests changing? , 2015 .

[20]  A. Staver,et al.  Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes. , 2016, Ecology.

[21]  R. B. Jackson,et al.  A Large and Persistent Carbon Sink in the World’s Forests , 2011, Science.

[22]  R. Pennington,et al.  Stability structures tropical woody plant diversity more than seasonality: Insights into the ecology of high legume-succulent-plant biodiversity , 2013 .

[23]  P. Boeckx,et al.  Facultative nitrogen fixation by legumes in the central Congo basin is downregulated during late successional stages , 2016 .

[24]  P. B. Tomlinson,et al.  Tropical Trees as Living Systems. , 1980 .

[25]  Susan G. Letcher,et al.  Biomass resilience of Neotropical secondary forests , 2016, Nature.

[26]  J. Janssen,et al.  On the Relevance and Control of Leaf Angle , 2010 .

[27]  Alexander R. Barron,et al.  Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils , 2009 .

[28]  Alan Grainger,et al.  The extent of forest in dryland biomes , 2017, Science.

[29]  O. Phillips,et al.  Continental-scale patterns of canopy tree composition and function across Amazonia , 2006, Nature.

[30]  R. Pennington,et al.  Woody Plant Diversity, Evolution, and Ecology in the Tropics: Perspectives from Seasonally Dry Tropical Forests , 2009 .

[31]  Amilcare Porporato,et al.  Changes in rainfall seasonality in the tropics , 2012 .

[32]  S. Manzoni,et al.  How competitive is drought deciduousness in tropical forests? A combined eco-hydrological and eco-evolutionary approach , 2017 .

[33]  R. Chazdon,et al.  Higher survival drives the success of nitrogen-fixing trees through succession in Costa Rican rainforests. , 2016, The New phytologist.

[34]  D. Menge,et al.  Global climate change will increase the abundance of symbiotic nitrogen‐fixing trees in much of North America , 2017, Global change biology.

[35]  J. Sprent Legume Nodulation: A Global Perspective , 2009 .

[36]  M. Tigabu,et al.  The Effects of Established Trees on Woody Regeneration during Secondary Succession in Tropical Dry Forests , 2016 .

[37]  N. Grimm,et al.  Towards an ecological understanding of biological nitrogen fixation , 2002 .

[38]  Jefferson S. Hall,et al.  Key role of symbiotic dinitrogen fixation in tropical forest secondary succession , 2013, Nature.

[39]  Susan G. Letcher,et al.  Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics , 2016, Science Advances.

[40]  A. Townsend,et al.  Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. , 2014, Ecology letters.

[41]  P. Reich,et al.  Strategy shifts in leaf physiology, structure and nutrient content between species of high‐ and low‐rainfall and high‐ and low‐nutrient habitats , 2001 .

[42]  E. Davidson,et al.  NITROGEN AND PHOSPHORUS LIMITATION OF BIOMASS GROWTH IN A TROPICAL SECONDARY FOREST , 2004 .

[43]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[44]  S. Reed,et al.  Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle , 2014, Proceedings of the National Academy of Sciences.

[45]  B. Nelson,et al.  Improved allometric models to estimate the aboveground biomass of tropical trees , 2014, Global change biology.

[46]  Efrat Sheffer,et al.  Biome-scale nitrogen fixation strategies selected by climatic constraints on nitrogen cycle , 2015, Nature Plants.

[47]  Alexander R. Barron,et al.  Facultative nitrogen fixation by canopy legumes in a lowland tropical forest , 2011, Oecologia.

[48]  Frans Bongers,et al.  Functional traits and environmental filtering drive community assembly in a species-rich tropical system. , 2010, Ecology.

[49]  Rafael Barbosa Pinto,et al.  A new subfamily classification of the leguminosae based on a taxonomically comprehensive phylogeny , 2017 .

[50]  Jeffrey M. Minucci,et al.  Tolerance or avoidance: drought frequency determines the response of an N2 -fixing tree. , 2017, The New phytologist.

[51]  L. Poorter,et al.  Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. , 2006 .

[52]  F. Bongers,et al.  Light-dependent leaf trait variation in 43 tropical dry forest tree species. , 2007, American journal of botany.

[53]  Eric A. Davidson,et al.  Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment , 2007, Nature.

[54]  D. Lawrence,et al.  Effects of model structural uncertainty on carbon cycle projections: biological nitrogen fixation as a case study , 2015 .

[55]  J. Franklin,et al.  Plant diversity patterns in neotropical dry forests and their conservation implications , 2016, Science.

[56]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[57]  Daniel J. Murphy,et al.  Legume phylogeny and classification in the 21st century: Progress, prospects and lessons for other species-rich clades , 2013 .

[58]  A. Nicotra,et al.  The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? , 2017, Plant, cell & environment.