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Ecosystems

, Volume 20, Issue 2, pp 340–353 | Cite as

Demographic Drivers of Aboveground Biomass Dynamics During Secondary Succession in Neotropical Dry and Wet Forests

  • Danaë M. A. Rozendaal
  • Robin L. Chazdon
  • Felipe Arreola-Villa
  • Patricia Balvanera
  • Tony V. Bentos
  • Juan M. Dupuy
  • J. Luis Hernández-Stefanoni
  • Catarina C. Jakovac
  • Edwin E. Lebrija-Trejos
  • Madelon Lohbeck
  • Miguel Martínez-Ramos
  • Paulo E. S. Massoca
  • Jorge A. Meave
  • Rita C. G. Mesquita
  • Francisco Mora
  • Eduardo A. Pérez-García
  • I. Eunice Romero-Pérez
  • Irving Saenz-Pedroza
  • Michiel van Breugel
  • G. Bruce Williamson
  • Frans Bongers
Article

Abstract

The magnitude of the carbon sink in second-growth forests is expected to vary with successional biomass dynamics resulting from tree growth, recruitment, and mortality, and with the effects of climate on these dynamics. We compare aboveground biomass dynamics of dry and wet Neotropical forests, based on monitoring data gathered over 3–16 years in forests covering the first 25 years of succession. We estimated standing biomass, annual biomass change, and contributions of tree growth, recruitment, and mortality. We also evaluated tree species’ contributions to biomass dynamics. Absolute rates of biomass change were lower in dry forests, 2.3 and 1.9 Mg ha−1 y−1, after 5–15 and 15–25 years after abandonment, respectively, than in wet forests, with 4.7 and 6.1 Mg ha−1 y−1, in the same age classes. Biomass change was largely driven by tree growth, accounting for at least 48% of biomass change across forest types and age classes. Mortality also contributed strongly to biomass change in wet forests of 5–15 years, whereas its contribution became important later in succession in dry forests. Biomass dynamics tended to be dominated by fewer species in early-successional dry than wet forests, but dominance was strong in both forest types. Overall, our results indicate that biomass dynamics during succession are faster in Neotropical wet than dry forests, with high tree mortality earlier in succession in the wet forests. Long-term monitoring of second-growth tropical forest plots is crucial for improving estimates of annual biomass change, and for enhancing understanding of the underlying mechanisms and demographic drivers.

Keywords

Biomass accumulation carbon sink forest dynamics Neotropics species’ dominance tree demography second-growth tropical forest 

Notes

Acknowledgements

We are grateful to numerous field assistants for their help with field work, local institutions for logistical support, and local communities for their hospitality. Funding was provided by the US National Science Foundation DEB-0639114, DEB-1147434, DEB-0424767, DEB-0639393, DEB-1147429; by the NASA Terrestrial Ecology Program, NASA LBA, the University of Connecticut Research Foundation, the Andrew W. Mellon Foundation; in Mexico by SEMARNAT-CONACYT 2002-C01-0597, 2002-C01-0267 and 2004-C01-227, SEP-CONACYT CB-2005-01-51043, 2009-129740, and CB-2009-01-128136, FOMIX Yucatán-CONACYT YUC2004-003-027, PAPIIT-DGAPA-UNAM IN218416, IN213714, and IN227210, CONACYT PhD scholarship, support of the Panamanian Sistema Nacional de Investigación-Secretaría Nacional de Ciencia, Tecnología e Innovación, by grant W85-326 from the Netherlands Organisation for Scientific Research, a PhD grant from Wageningen University, and the FOREFRONT-INREF program; and in Brazil by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM), the Instituto Nacional de Ciência e Tecnologia dos Serviços Ambientais da Amazônia (INCT/Servamb), and the Biological Dynamics of Forest Fragments Project (BDFFP). This is publication #701 in the Technical Series of the Biological Dynamics of Forest Fragments Project BDFFP-INPA-SI.

Supplementary material

10021_2016_29_MOESM1_ESM.docx (202 kb)
Supplementary material 1 (DOCX 201 kb)

References

  1. Anderson-Teixeira KJ, Miller AD, Mohan JE, Hudiburg TW, Duval BD, DeLucia EH. 2013. Altered dynamics of forest recovery under a changing climate. Glob Change Biol 19:2001–21.CrossRefGoogle Scholar
  2. Barajas-Morales J. 1987. Wood specific gravity in species from two tropical forests in Mexico. IAWA J 8:143–8.CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B. 2014. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-39.Google Scholar
  4. Bazzaz FA. 1979. Physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–71.CrossRefGoogle Scholar
  5. Becknell JM, Kucek LK, Powers JS. 2012. Aboveground biomass in mature and secondary seasonally dry tropical forests: a literature review and global synthesis. For Ecol Manag 276:88–95.CrossRefGoogle Scholar
  6. Bellingham PJ, Sparrow AD. 2009. Multi-stemmed trees in montane rain forests: their frequency and demography in relation to elevation, soil nutrients and disturbance. J Ecol 97:472–83.CrossRefGoogle Scholar
  7. Bongers F, Chazdon R, Poorter L, Peña-Claros M. 2015. The potential of secondary forests. Science 348:642–3.CrossRefPubMedGoogle Scholar
  8. Bonner MTL, Schmidt S, Shoo LP. 2013. A meta-analytical global comparison of aboveground biomass accumulation between tropical secondary forests and monoculture plantations. For Ecol Manag 291:73–86.CrossRefGoogle Scholar
  9. Brienen RJW, Lebrija-Trejos E, van Breugel M, Pérez-García EA, Bongers F, Meave JA, Martínez-Ramos M. 2009. The potential of tree rings for the study of forest succession in southern Mexico. Biotropica 41:186–95.CrossRefGoogle Scholar
  10. Brown S, Lugo AE. 1982. The storage and production of organic matter in tropical forests and their role in the global carbon cycle. Biotropica 14:161–87.CrossRefGoogle Scholar
  11. Brown S, Lugo AE. 1990. Tropical secondary forests. J Trop Ecol 6:1–32.CrossRefGoogle Scholar
  12. Burnham KP, Anderson DR. 2002. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer. 488 p.Google Scholar
  13. Busby PE, Vitousek P, Dirzo R. 2010. Prevalence of tree regeneration by sprouting and seeding along a rainfall gradient in Hawai’i. Biotropica 42:80–6.CrossRefGoogle Scholar
  14. Caspersen JP, Pacala SW, Jenkins JC, Hurtt GC, Moorcroft PR, Birdsey RA. 2000. Contributions of land-use history to carbon accumulation in US forests. Science 290:1148–51.CrossRefPubMedGoogle Scholar
  15. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. 2009. Towards a worldwide wood economics spectrum. Ecol Lett 12:351–66.CrossRefPubMedGoogle Scholar
  16. Chave J, Muller-Landau HC, Baker TR, Easdale TA, Ter Steege H, Webb CO. 2006. Regional and phylogenetic variation of wood density across 2456 neotropical tree species. Ecol Appl 16:2356–67.CrossRefPubMedGoogle Scholar
  17. Chave J, Réjou-Méchain M, Búrquez A, Chidumayo E, Colgan MS, Delitti WBC, Duque A, Eid T, Fearnside PM, Goodman RC, Henry M, Martínez-Yrízar A, Mugasha WA, Muller-Landau HC, Mencuccini M, Nelson BW, Ngomanda A, Nogueira EM, Ortiz-Malavassi E, Pélissier R, Ploton P, Ryan CM, Saldarriaga JG, Vieilledent G. 2014. Improved allometric models to estimate the aboveground biomass of tropical trees. Glob Change Biol 20:3177–90.CrossRefGoogle Scholar
  18. Chazdon RL. 2014. Second growth: The promise of tropical forest regeneration in an age of deforestation. Chicago: University of Chicago Press.CrossRefGoogle Scholar
  19. Chazdon RL, Brenes AR, Alvarado BV. 2005. Effects of climate and stand age on annual tree dynamics in tropical second-growth rain forests. Ecology 86:1808–15.CrossRefGoogle Scholar
  20. Chazdon RL, Broadbent EN, Rozendaal DMA, Bongers F, Zambrano AMA, Aide TM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Craven D, de Almeida-Cortez JS, Cabral GAL, de Jong B, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Durán SM, Espírito-Santo MM, Fandino MC, César RG, Hall JS, Hérnandez-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Lohbeck M, Martínez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Muñoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, Orihuela-Belmonte E, Peña-Claros M, Pérez-García EA, Piotto D, Powers JS, Rodríguez-Velazquez J, Romero-Pérez IE, Ruíz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Vester H, Vieira ICG, Vizcarra Bentos T, Williamson GB, Poorter L. 2016. Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Sci Adv 2:e1501639.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chazdon RL, Finegan B, Capers RS, Salgado-Negret B, Casanoves F, Boukili V, Norden N. 2010. Composition and dynamics of functional groups of trees during tropical forest succession in northeastern Costa Rica. Biotropica 42:31–40.CrossRefGoogle Scholar
  22. Condit R, Aguilar S, Hernandez A, Perez R, Lao S, Angehr G, Hubbell SP, Foster RB. 2004. Tropical forest dynamics across a rainfall gradient and the impact of an El Niño dry season. J Trop Ecol 20:51–72.CrossRefGoogle Scholar
  23. Dupuy JM, Hernández-Stefanoni JL, Hernández-Juárez RA, Tetetla-Rangel E, López-Martínez JO, Leyequién-Abarca E, Tun-Dzul FJ, May-Pat F. 2012. Patterns and correlates of tropical dry forest structure and composition in a highly replicated chronosequence in Yucatan, Mexico. Biotropica 44:151–62.CrossRefGoogle Scholar
  24. Etter A, McAlpine C, Pullar D, Possingham HP. 2005. Modeling the age of tropical moist forest fragments in heavily-cleared lowland landscapes of Colombia. For Ecol Manag 208:249–60.CrossRefGoogle Scholar
  25. Ewel JJ. 1977. Differences between wet and dry successional tropical ecosystems. Geo-Eco-Trop 1:103–17.Google Scholar
  26. FAO. 2010. Global forest resources assessment 2010. Rome: FAO Forestry Paper 163. Food and Agriculture Organization of the United Nations.Google Scholar
  27. Feldpausch TR, Prates-Clark CD, Fernandes ECM, Riha SJ. 2007. Secondary forest growth deviation from chronosequence predictions in central Amazonia. Glob Change Biol 13:967–79.CrossRefGoogle Scholar
  28. Finegan B. 1996. Pattern and process in neotropical secondary rain forests: The first 100 years of succession. Trends Ecol Evol 11:119–24.CrossRefPubMedGoogle Scholar
  29. Garnier E, Cortez J, Billes G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint JP. 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–7.CrossRefGoogle Scholar
  30. Gehring C, Denich M, Vlek PLG. 2005. Resilience of secondary forest regrowth after slash-and-burn agriculture in central Amazonia. J Trop Ecol 21:519–27.CrossRefGoogle Scholar
  31. Gómez-Pompa A, Vázquez-Yanes C. 1981. Successional studies of a rain forest in Mexico. In: Shugart HH, Botkin DB, Eds. West DC. Forest succession. Concepts and application. New York: Springer-Verlag. p 246–66.Google Scholar
  32. Grace J, Mitchard E, Gloor E. 2014. Perturbations in the carbon budget of the tropics. Glob Change Biol 20:3238–55.CrossRefGoogle Scholar
  33. Guariguata MR, Ostertag R. 2001. Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manag 148:185–206.CrossRefGoogle Scholar
  34. Hudiburg T, Law B, Turner DP, Campbell J, Donato DC, Duane M. 2009. Carbon dynamics of Oregon and Northern California forests and potential land-based carbon storage. Ecol Appl 19:163–80.CrossRefPubMedGoogle Scholar
  35. Hughes RF, Kauffman JB, Jaramillo VJ. 1999. Biomass, carbon, and nutrient dynamics of secondary forests in a humid tropical region of Mexico. Ecology 80:1892–907.Google Scholar
  36. IPCC. 2006. 2006 IPCC Guidelines for national greenhouse gas inventories. In: Eggleston HS, Buendia L, Miwa K, Ngara T, Tanabe K, Eds. National Greenhouse Gas Inventories Programme. IGES: Hayama. Google Scholar
  37. Jakovac CC, Peña-Claros M, Kuyper TW, Bongers F. 2015. Loss of secondary-forest resilience by land-use intensification in the Amazon. J Ecol 103:67–77.CrossRefGoogle Scholar
  38. Kobe RK. 1999. Light gradient partitioning among tropical tree species through differential seedling mortality and growth. Ecology 80:187–201.CrossRefGoogle Scholar
  39. Laliberté E, Legendre P, Shipley B. 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12.Google Scholar
  40. Lebrija-Trejos E, Bongers F, Pérez-García EA, Meave JA. 2008. Successional change and resilience of a very dry tropical deciduous forest following shifting agriculture. Biotropica 40:422–31.CrossRefGoogle Scholar
  41. Lebrija-Trejos E, Meave JA, Poorter L, Pérez-García EA, Bongers F. 2010a. Pathways, mechanisms and predictability of vegetation change during tropical dry forest succession. Perspect Plant Ecol Evol Systematics 12:267–75.CrossRefGoogle Scholar
  42. Lebrija-Trejos E, Pérez-García EA, Meave JA, Bongers F, Poorter L. 2010b. Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology 91:386–98.CrossRefPubMedGoogle Scholar
  43. Lebrija-Trejos E, Pérez-García EA, Meave JA, Poorter L, Bongers F. 2011. Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477–89.CrossRefGoogle Scholar
  44. Lewis SL, Sonké B, Sunderland T, Begne SK, Lopez-Gonzalez G, van der Heijden GMF, Phillips OL, Affum-Baffoe K, Baker TR, Banin L, Bastin JF, Beeckman H, Boeckx P, Bogaert J, De Cannière C, Chezeaux E, Clark CJ, Collins M, Djagbletey G, Djuikouo MNK, Droissart V, Doucet JL, Ewango CEN, Fauset S, Feldpausch TR, Foli EG, Gillet JF, Hamilton AC, Harris DJ, Hart TB, de Haulleville T, Hladik A, Hufkens K, Huygens D, Jeanmart P, Jeffery KJ, Kearsley E, Leal ME, Lloyd J, Lovett JC, Makana JR, Malhi Y, Marshall AR, Ojo L, Peh KSH, Pickavance G, Poulsen JR, Reitsma JM, Sheil D, Simo M, Steppe K, Taedoumg HE, Talbot J, Taplin JRD, Taylor D, Thomas SC, Toirambe B, Verbeeck H, Vleminckx J, White LJT, Willcock S, Woell H, Zemagho L. 2013. Above-ground biomass and structure of 260 African tropical forests. Philos Trans R Soc B 368:20120295.CrossRefGoogle Scholar
  45. Lohbeck M, Poorter L, Lebrija-Trejos E, Martínez-Ramos M, Meave JA, Paz H, Pérez-García EA, Romero-Pérez IE, Tauro A, Bongers F. 2013. Successional changes in functional composition contrast for dry and wet tropical forest. Ecology 94:1211–16.CrossRefPubMedGoogle Scholar
  46. Lohbeck M, Poorter L, Martínez-Ramos M, Rodriguez-Velázquez J, van Breugel M, Bongers F. 2014. Changing drivers of species dominance during tropical forest succession. Funct Ecol 28:1052–8.CrossRefGoogle Scholar
  47. Lohbeck M, Poorter L, Paz H, Pla L, van Breugel M, Martínez-Ramos M, Bongers F. 2012. Functional diversity changes during tropical forest succession. Perspect Plant Ecol Evol Systematics 14:89–96.CrossRefGoogle Scholar
  48. Longworth JB, Mesquita RC, Bentos TV, Moreira MP, Massoca PE, Williamson GB. 2014. Shifts in dominance and species assemblages over two decades in alternative successions in central Amazonia. Biotropica 46:529–37.CrossRefGoogle Scholar
  49. Marín-Spiotta E, Cusack DF, Ostertag R, Silver WL. 2008. Trends in above and belowground carbon with forest regrowth after agricultural abandonment in the Neotropics. In: Myster RW, Ed. Post-agricultural succession in the Neotropics. New York: Springer. p 22–72.CrossRefGoogle Scholar
  50. Markesteijn L, Poorter L, Bongers F, Paz H, Sack L. 2011. Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance. New Phytol 191:480–95.CrossRefPubMedGoogle Scholar
  51. Martin PA, Newton AC, Bullock JM. 2013. Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proc R Soc B 280:20132236.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Martínez-Ramos M, Alvarez-Buylla ER. 1998. How old are tropical rain forest trees? Trends Plant Sci 3:400–5.CrossRefGoogle Scholar
  53. Martínez-Yrízar A, Sarukhan J, Pérez-Jiménez A, Rincón E, Maass JM, Solis-Magallanes A, Cervantes L. 1992. Above-ground phytomass of a tropical deciduous forest on the coast of Jalisco, México. J Trop Ecol 8:87–96.CrossRefGoogle Scholar
  54. Maza-Villalobos S, Poorter L, Martínez-Ramos M. 2013. Effects of ENSO and temporal rainfall variation on the dynamics of successional communities in old-field succession of a tropical dry forest. PloS One 8:e82040.CrossRefPubMedPubMedCentralGoogle Scholar
  55. McLaren KP, McDonald MA. 2003. Seedling dynamics after different intensities of human disturbance in a tropical dry limestone forest in Jamaica. J Trop Ecol 19:567–78.CrossRefGoogle Scholar
  56. McMahon SM, Parker GG, Miller DR. 2010. Evidence for a recent increase in forest growth. Proc Natl Acad Sci USA 107:3611–15.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Mesquita RCG, Ickes K, Ganade G, Williamson GB. 2001. Alternative successional pathways in the Amazon Basin. J Ecol 89:528–37.CrossRefGoogle Scholar
  58. Mesquita RCG, Massoca PES, Jakovac CC, Bentos TV, Williamson GB. 2015. Amazon rain forest succession: stochasticity or land-use legacy? Bioscience 65:849–61.CrossRefGoogle Scholar
  59. Mora F, Martínez-Ramos M, Ibarra-Manríquez G, Pérez-Jiménez A, Trilleras J, Balvanera P. 2015. Testing chronosequences through dynamic approaches: time and site effects on tropical dry forest succession. Biotropica 47:38–48.CrossRefGoogle Scholar
  60. Murphy PG, Lugo AE. 1986. Ecology of tropical dry forest. Annu Rev Ecol Syst 17:67–88.CrossRefGoogle Scholar
  61. Nakagawa S, Schielzeth H. 2013. A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–42.CrossRefGoogle Scholar
  62. Neeff T, Lucas RM, dos Santos JR, Brondizio ES, Freitas CC. 2006. Area and age of secondary forests in Brazilian Amazonia 1978–2002: an empirical estimate. Ecosystems 9:609–23.CrossRefGoogle Scholar
  63. Nogueira EM, Nelson BW, Fearnside PM. 2005. Wood density in dense forest in central Amazonia, Brazil. For Ecol Manag 208:261–86.CrossRefGoogle Scholar
  64. Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao SL, Rautiainen A, Sitch S, Hayes D. 2011. A large and persistent carbon sink in the world’s forests. Science 333:988–93.CrossRefPubMedGoogle Scholar
  65. Peet RK, Christensen NL. 1987. Competition and tree death. Bioscience 37:586–95.CrossRefGoogle Scholar
  66. Peña-Claros M. 2003. Changes in forest structure and species composition during secondary forest succession in the Bolivian Amazon. Biotropica 35:450–61.CrossRefGoogle Scholar
  67. Pineda-García F, Paz H, Meinzer FC. 2013. Drought resistance in early and late secondary successional species from a tropical dry forest: the interplay between xylem resistance to embolism, sapwood water storage and leaf shedding. Plant Cell Environ 36:405–18.CrossRefPubMedGoogle Scholar
  68. Plourde BT, Boukili VK, Chazdon RL. 2015. Radial changes in wood specific gravity of tropical trees: inter- and intra-specific variation during secondary succession. Funct Ecol 29:111–20.CrossRefGoogle Scholar
  69. Poorter L, Bongers F, Aide TM, Almeyda Zambrano AM, Balvanera P, Becknell JM, Bentos TV, Boukili VK, Broadbent EN, Chazdon RL, Craven D, Cabral GAL, de Almeida-Cortez JS, de Jong B, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Durán SM, Espírito-Santo MM, Fandino MC, Hall JS, Hernández-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard DK, Letcher SG, Lohbeck M, Marín-Spiotta E, Martínez-Ramos M, Massoca PES, Meave JA, Mesquita RCG, Mora F, Muñoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, Orihuela-Belmonte E, Peña-Claros M, Pérez-García EA, Piotto D, Powers JS, Rodríguez-Velazquez J, Romero-Pérez IE, Ruíz J, Sanchez-Azofeifa GA, Swenson N, Toledo M, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Williamson GB, Rozendaal DMA. 2016. Biomass resilience of Neotropical secondary forests. Nature 530:211–14.CrossRefPubMedGoogle Scholar
  70. Poorter L, van der Sande MT, Thompson J, Arets E, Alarcón A, Álvarez-Sánchez J, Ascarrunz N, Balvanera P, Barajas-Guzman G, Boit A, Bongers F, Carvalho FA, Casanoves F, Cornejo-Tenorio G, Costa FRC, de Castilho CV, Duivenvoorden JF, Dutrieux LP, Enquist BJ, Fernández-Méndez F, Finegan B, Gormley LHL, Healey JR, Hoosbeek MR, Ibarra-Manríquez G, Junqueira AB, Levis C, Licona JC, Lisboa LS, Magnusson WE, Martínez-Ramos M, Martínez-Yrizar A, Martorano LG, Maskell LC, Mazzei L, Meave JA, Mora F, Muñoz R, Nytch C, Pansonato MP, Parr TW, Paz H, Pérez-García EA, Rentería LY, Rodríguez-Velazquez J, Rozendaal DMA, Ruschel AR, Sakschewski B, Salgado-Negret B, Schietti J, Simões M, Sinclair FL, Souza PF, Souza FC, Stropp J, ter Steege H, Swenson NG, Thonicke K, Toledo M, Uriarte M, van der Hout P, Walker P, Zamora N, Peña-Claros M. 2015. Diversity enhances carbon storage in tropical forests. Glob Ecol Biogeogr 24:1314–28.CrossRefGoogle Scholar
  71. Powers JS, Becknell JM, Irving J, Pérez-Aviles D. 2009. Diversity and structure of regenerating tropical dry forests in Costa Rica: Geographic patterns and environmental drivers. For Ecol Manag 258:959–70.CrossRefGoogle Scholar
  72. R Core Team. 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  73. Read L, Lawrence D. 2003. Recovery of biomass following shifting cultivation in dry tropical forests of the Yucatan. Ecol Appl 13:85–97.CrossRefGoogle Scholar
  74. Reyes-García C, Andrade JL, Sima JL, Us-Santamaria R, Jackson PC. 2012. Sapwood to heartwood ratio affects whole-tree water use in dry forest legume and non-legume trees. Trees Struct Funct 26:1317–30.CrossRefGoogle Scholar
  75. Rozendaal DMA, Chazdon RL. 2015. Demographic drivers of tree biomass change during secondary succession in northeastern Costa Rica. Ecol Appl 25:506–16.CrossRefPubMedGoogle Scholar
  76. Silver WL, Ostertag R, Lugo AE. 2000. The potential for carbon sequestration through reforestation of abandoned tropical agricultural and pasture lands. Restor Ecol 8:394–407.CrossRefGoogle Scholar
  77. Tanentzap AJ, Mountford EP, Cooke AS, Coomes DA. 2012. The more stems the merrier: advantages of multi-stemmed architecture for the demography of understorey trees in a temperate broadleaf woodland. J Ecol 100:171–83.CrossRefGoogle Scholar
  78. Toledo M, Poorter L, Peña-Claros M, Alarcón A, Balcázar J, Leaño C, Licona JC, Llanque O, Vroomans V, Zuidema P, Bongers F. 2011. Climate is a stronger driver of tree and forest growth rates than soil and disturbance. J Ecol 99:254–64.CrossRefGoogle Scholar
  79. van Breugel M, Bongers F, Martínez-Ramos M. 2007. Species dynamics during early secondary forest succession: Recruitment, mortality and species turnover. Biotropica 39:610–19.CrossRefGoogle Scholar
  80. van Breugel M, Hall JS, Craven D, Bailon M, Hernandez A, Abbene M, van Breugel P. 2013. Succession of ephemeral secondary forests and their limited role for the conservation of floristic diversity in a human-modified tropical landscape. PLoS One 8:e82433.CrossRefPubMedPubMedCentralGoogle Scholar
  81. van Breugel M, Hall JS, Craven DJ, Gregoire TG, Park A, Dent DH, Wishnie MH, Mariscal E, Deago J, Ibarra D, Cedeño N, Ashton MS. 2011. Early growth and survival of 49 tropical tree species across sites differing in soil fertility and rainfall in Panama. For Ecol Manag 261:1580–9.CrossRefGoogle Scholar
  82. van Breugel M, Martínez-Ramos M, Bongers F. 2006. Community dynamics during early secondary succession in Mexican tropical rain forests. J Trop Ecol 22:663–74.CrossRefGoogle Scholar
  83. van Breugel M, van Breugel P, Jansen PA, Martínez-Ramos M, Bongers F. 2012. The relative importance of above- versus belowground competition for tree growth during early succession of a tropical moist forest. Plant Ecol 213:25–34.CrossRefGoogle Scholar
  84. Williamson GB, Bentos TV, Longworth JB, Mesquita RCG. 2014. Convergence and divergence in alternative successional pathways in Central Amazonia. Plant Ecol Divers 7:341–8.CrossRefGoogle Scholar
  85. Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Diaz S, Engelbrecht BMJ, Harms KE, Hubbell SP, Marks CO, Ruiz-Jaen MC, Salvador CM, Zanne AE. 2010. Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91:3664–74.CrossRefPubMedGoogle Scholar
  86. Zanne AE, López-González G, Coomes DA, Illic J, Jansen S, Lewis SL, Miller RB, Swenson NG, Wiemann MC, Chave J. 2009. Data from: Towards a worldwide wood economics spectrum. Dryad Digit Repos. doi: 10.5061/dryad.234.Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Danaë M. A. Rozendaal
    • 1
    • 2
    • 15
  • Robin L. Chazdon
    • 1
    • 3
    • 4
  • Felipe Arreola-Villa
    • 5
  • Patricia Balvanera
    • 5
  • Tony V. Bentos
    • 6
  • Juan M. Dupuy
    • 7
  • J. Luis Hernández-Stefanoni
    • 7
  • Catarina C. Jakovac
    • 2
    • 6
  • Edwin E. Lebrija-Trejos
    • 8
    • 9
  • Madelon Lohbeck
    • 2
    • 5
    • 10
  • Miguel Martínez-Ramos
    • 5
  • Paulo E. S. Massoca
    • 6
  • Jorge A. Meave
    • 11
  • Rita C. G. Mesquita
    • 6
  • Francisco Mora
    • 5
    • 11
  • Eduardo A. Pérez-García
    • 11
  • I. Eunice Romero-Pérez
    • 11
  • Irving Saenz-Pedroza
    • 7
  • Michiel van Breugel
    • 8
    • 12
    • 13
  • G. Bruce Williamson
    • 6
    • 14
  • Frans Bongers
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA
  2. 2.Forest Ecology and Forest Management GroupWageningen UniversityWageningenThe Netherlands
  3. 3.International Institute for SustainabilityRio de JaneiroBrazil
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  5. 5.Instituto de Investigaciones en Ecosistemas y SustentabilidadUniversidad Nacional Autónoma de MéxicoMoreliaMexico
  6. 6.Biological Dynamics of Forest Fragments Project, Coordenação de Dinâmica AmbientalInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  7. 7.Unidad de Recursos NaturalesCentro de Investigación Científica de Yucatán (CICY)MéridaMexico
  8. 8.Smithsonian ForestGEOSmithsonian Tropical Research InstituteBalboaPanama
  9. 9.Department of Biology and the Environment, Faculty of Natural SciencesUniversity of Haifa-OranimTivonIsrael
  10. 10.World Agroforestry CentreNairobiKenya
  11. 11.Departamento de Ecología y Recursos Naturales, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico
  12. 12.Yale-NUS CollegeSingaporeSingapore
  13. 13.Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  14. 14.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  15. 15.Department of BiologyUniversity of ReginaReginaCanada

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