Plant Ecology

, Volume 218, Issue 9, pp 1047–1062 | Cite as

Does soil pyrogenic carbon determine plant functional traits in Amazon Basin forests?

  • Klécia G. MassiEmail author
  • Michael Bird
  • Beatriz S. Marimon
  • Ben Hur MarimonJr.
  • Denis S. Nogueira
  • Edmar A. Oliveira
  • Oliver L. Phillips
  • Carlos A. Quesada
  • Ana S. Andrade
  • Roel J. W. Brienen
  • José L. C. Camargo
  • Jerome Chave
  • Eurídice N. Honorio Coronado
  • Leandro V. Ferreira
  • Niro Higuchi
  • Susan G. Laurance
  • William F. Laurance
  • Thomas Lovejoy
  • Yadvinder Malhi
  • Rodolfo V. Martínez
  • Abel Monteagudo
  • David Neill
  • Adriana Prieto
  • Hirma Ramírez-Angulo
  • Hans ter Steege
  • Emilio Vilanova
  • Ted R. FeldpauschEmail author


Amazon forests are fire-sensitive ecosystems and consequently fires affect forest structure and composition. For instance, the legacy of past fire regimes may persist through some species and traits that are found due to past fires. In this study, we tested for relationships between functional traits that are classically presented as the main components of plant ecological strategies and environmental filters related to climate and historical fires among permanent mature forest plots across the range of local and regional environmental gradients that occur in Amazonia. We used percentage surface soil pyrogenic carbon (PyC), a recalcitrant form of carbon that can persist for millennia in soils, as a novel indicator of historical fire in old-growth forests. Five out of the nine functional traits evaluated across all 378 species were correlated with some environmental variables. Although there is more PyC in Amazonian soils than previously reported, the percentage soil PyC indicated no detectable legacy effect of past fires on contemporary functional composition. More species with dry diaspores were found in drier and hotter environments. We also found higher wood density in trees from higher temperature sites. If Amazon forest past burnings were local and without distinguishable attributes of a widespread fire regime, then impacts on biodiversity would have been small and heterogeneous. Alternatively, sufficient time may have passed since the last fire to allow for species replacement. Regardless, as we failed to detect any impact of past fire on present forest functional composition, if our plots are representative then it suggests that mature Amazon forests lack a compositional legacy of past fire.


Fruit type Wood density Fire Soil charcoal Climatological water deficit Temperature Elevation 



We gratefully acknowledge the financial support provided to KGM, BSM, BHMJ, EAO and TRF by the Coordination of Improvement of Personnel in Higher Education, Brazil (CAPES) through a Science without Borders grant to TRF (PVE 177/2012). Sample analysis was supported by a grant from the University of Exeter to TRF. The National Council of Science and Technology, Brazil (CNPq) is acknowledged for a productivity grant (bolsa produtividade PQ) to BHMJ and BSM, for a Postdoctoral fellowship to DSN, and the financial support to the projects PELD (403725/2012-7) and PPBio (457602/2012-0). We acknowledge the financial support provided to DSN, OLP, and BSM by CNPq through a Science without Borders grant to OLP (PVE 401279/2014-6). OLP is also supported by an ERC Advanced Grant (T-FORCES) and is a Royal Society-Wolfson Research Merit Award Holder. Tree data used in this analysis are available online at the Tropical Ecology Assessment and Monitoring (TEAM) Network of Conservation International, funded by the Gordon and Betty Moore Foundation, and database. The RAINFOR forest monitoring network has been supported principally by the Natural Environment Research Council (Grants NE/B503384/1, NE/D01025X/1, NE/I02982X/1, NE/F005806/1, NE/D005590/1, and NE/I028122/1), the Gordon and Betty Moore Foundation, and by the EU Seventh Framework Programme (GEOCARBON-283080 and AMAZALERT-282664). The field data summarized here involve vital contributions from many field assistants and rural communities, specifically acknowledged elsewhere (Phillips et al. 2009; Brienen et al. 2015). This is the number 719 of the Technical Series of the BDFFP. We also thank Jon Lloyd and Timothy Baker for permission to use their data. Finally, we wish to thank the referees for the thoughtful reviews and Diogo B. Provete for his precious help.

Author contributions

KGM, DSN, and TRF wrote the paper; KGM, TRF, BSM, and BHMJ designed the study; MB carried out the pyrogenic carbon analysis; TRF, BSM, and BHMJ received funding in support of the research; and AP, DN, EV, EO, OLP, HS, HR-A, JC, LVF, NH, RVM, RB, SLL, WL, and YM coordinated data collection with the help of most co-authors. Most co-authors collected field data and all of them commented on the manuscript.

Supplementary material

11258_2017_751_MOESM1_ESM.docx (107 kb)
Supplementary material 1 (DOCX 106 kb)


  1. Ackerly DD, Thomas WW, Ferreira CAC, Pirani JR (1989) The forest-cerrado transition zone in southern Amazonia: results of the 1985 Projecto Flora Amazônica expedition to Mato Grosso. Brittonia 41:113–128CrossRefGoogle Scholar
  2. Alencar AA, Brando PM, Asner GP, Putz FE (2015) Landscape fragmentation, severe drought, and the new Amazon forest fire regime. Ecol Appl 25:1493–1505CrossRefPubMedGoogle Scholar
  3. Almeida DRA, Nelson BW, Schietti J et al (2016) Contrasting fire damage and fire susceptibility between seasonally flooded forest and upland forest in the Central Amazon using portable profiling LiDAR. Remote Sens Environ 184:153–160CrossRefGoogle Scholar
  4. Amaral DD, Vieira ICG, Almeida SS et al (2009) Checklist da flora arbórea de remanescentes florestais da região metropolitana de Belém e valor histórico dos fragmentos, Pará, Brasil. Bol Mus Para Emílio Goeldi Cienc Nat 4:231–289CrossRefGoogle Scholar
  5. Amaral S, Costa CB, Arasato LS, Ximenes AC, Rennó CD (2013) AMBDATA: Variáveis ambientais para Modelos de Distribuição de Espécies (MDEs). In: Ribeiro ML, Santos TG, Sant’Anna SJ (eds) Anais XV Simpósio Brasileiro de Sensoriamento Remoto. Instituto Nacional de Pesquisas Espaciais, São José dos Campos, pp 6930–6937Google Scholar
  6. Ames GM, Anderson SM, Wright JP (2015) Multiple environmental drivers structure plant traits at the community level in a pyrogenic ecosystem. Funct Ecol 30:789–798CrossRefGoogle Scholar
  7. Aragão LEOC, Malhi Y, Roman-Cuesta RM et al (2007) Spatial patterns and fire response of recent Amazonian droughts. Geophys Res Lett 34:L07701CrossRefGoogle Scholar
  8. Barlow J, Peres CA (2008) Fire-mediated dieback and compositional cascade in an Amazonian forest. Philos Trans R Soc Lond B Biol Sci 363:1787–1794CrossRefPubMedPubMedCentralGoogle Scholar
  9. Barton H, Denham T, Neumann K, Arroyo-Kalin M (2012) Long-term perspectives on human occupation of tropical rainforests: an introductory overview. Quat Int 249:1–3CrossRefGoogle Scholar
  10. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377CrossRefPubMedPubMedCentralGoogle Scholar
  11. Benavides R, Escudero A, Coll L et al (2016) Recruitment patterns of four tree species along elevation gradients in Mediterranean mountains: not only climate matters. For Ecol Manage 360:287–296CrossRefGoogle Scholar
  12. Bennett JM, Cunningham SC, Connelly CA, Clarke RH, Thomson JR, Mac Nally R (2013) The interaction between a drying climate and land use affects forest structure and above-ground carbon storage. Global Ecol Biogeogr 22:1238–1247CrossRefGoogle Scholar
  13. Bird MI, Wynn JG, Saiz G, Wurster CM, McBeath A (2015) The pyrogenic carbon cycle. Annu Rev Earth Planet Sci 43:273–298CrossRefGoogle Scholar
  14. Bowman DMJS, Balch JK, Artaxo P et al (2009) Fire in the earth system. Science 324:481–484CrossRefPubMedGoogle Scholar
  15. Bradshaw SD, Dixon KW, Hopper SD, Lambers H, Turner SR (2011) Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci 16:1365–1380Google Scholar
  16. Brando PM, Nepstad DC, Balch JK et al (2012) Fire-induced tree mortality in a neotropical forest: the roles of bark traits, tree size, wood density and fire behavior. Glob Change Biol 18:630–641CrossRefGoogle Scholar
  17. Brando PM, Balch JK, Nepstad D et al (2014) Abrupt increases in Amazonian tree mortality due to drought-fire interactions. Proc Natl Acad Sci 111:6347–6352CrossRefPubMedPubMedCentralGoogle Scholar
  18. Brewer N, Smith AMS, Hatten JA et al (2013) Fuel moisture influences on fire-altered carbon in masticated fuels: an experimental study. J Geophys Res-Biogeo 118:30–40CrossRefGoogle Scholar
  19. Brienen RJW, Phillips OL, Feldpausch TR et al (2015) Long-term decline of the Amazon carbon sink. Nature 519:344–348CrossRefPubMedGoogle Scholar
  20. Bush MB, Silman MR, de Toledo MB et al (2007) Holocene fire and occupation in Amazonia: records from two lake districts. Phil Trans R Soc B 362:209–218CrossRefPubMedPubMedCentralGoogle Scholar
  21. Bush MB, Silman MR, McMichael C, Saatchi S (2008) Fire, climate change and biodiversity in Amazonia: a Late-Holocene perspective. Phil Trans R Soc B 363:1795–1802CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cadotte MW, Arnillas CA, Livingstone SW, Yasui SL (2015) Predicting communities from functional traits. Trends Ecol Evol 30:510–511CrossRefPubMedGoogle Scholar
  23. Chazdon RL, Careaga S, Webb C, Vargas O (2003) Community and phylogenetic structures of reproductive traits of woody species in wet tropical forests. Ecol Monogr 73(3):331–348CrossRefGoogle Scholar
  24. Chuine I (2010) Why does phenology drive species distribution? Phil Trans R Soc B B 365:3149–3160CrossRefGoogle Scholar
  25. Cianciaruso MV, Silva IA, Batalha MA, Gastonc KJ, Petchey OL (2012) The influence of fire on phylogenetic and functional structure of woody savannas: moving from species to individuals. Perspect Plant Ecol 14:205–216CrossRefGoogle Scholar
  26. Clarke PJ, Lawes MJ, Midgley JJ, Atri M (2016) Fire regime, soil fertility and growth form interact to shape fire and growth traits in two co-occurring Banksia species. Evolut Ecol 30:35–45CrossRefGoogle Scholar
  27. Cochrane MA, Alencar A, Schulze MD et al (1999) Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284:1832–1835CrossRefPubMedGoogle Scholar
  28. Correa DF, Álvarez E, Stevenson PR (2015) Plant dispersal systems in Neotropical forests: availability of dispersal agents or availability of resources for constructing zoochorous fruits? Global Ecol Biogeogr 24:203–214CrossRefGoogle Scholar
  29. Dantas VL, Batalha MA, Pausas JG (2013) Fire drives functional thresholds on the savanna–forest transition. Ecology 94:2454–2463CrossRefGoogle Scholar
  30. Davidson EA, Araújo AC, Artaxo P et al (2012) The Amazon basin in transition. Nature 481:321–328CrossRefPubMedGoogle Scholar
  31. Dray S, Choler P, Doledéc S et al (2014) Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology 95:14–21CrossRefPubMedGoogle Scholar
  32. Erickson CL (2008) Amazonia: The Historical Ecology of a Domesticated Landscape. In: Silverman H, Isbell W (eds) The handbook of South American archaeology. Springer, New York, pp 157–183CrossRefGoogle Scholar
  33. Esquivel Muelbert A, Baker TR, Dexter K et al (2016) Seasonal drought limits tree species across the Neotropics. Ecography 39:1–12CrossRefGoogle Scholar
  34. Feldpausch TR, Banin L, Phillips OL et al (2011) Height- diameter allometry of tropical forest trees. Biogeosciences 8:1081–1106CrossRefGoogle Scholar
  35. Feldpausch TR, Phillips OL, Brienen RJW et al (2016) Amazon forest response to repeated droughts. Global Biogeochem Cycle 30:964–982CrossRefGoogle Scholar
  36. Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. Disponível em: Accessed October 2015
  37. Flores BM, Piedade M-TF, Nelson BW (2012) Fire disturbance in Amazonian blackwater floodplain forests. Plant Ecol Divers 7:319–327CrossRefGoogle Scholar
  38. Girardin CAJ, Malhi Y, Doughty CE et al (2016) Seasonal trends of Amazonian rainforest phenology, net primary productivity, and carbon allocation. Global Biogeochem Cycle 30(5):700–715CrossRefGoogle Scholar
  39. Goulart AC, Macario KD, Scheel-Ybert R et al (2017) Charcoal chronology of the Amazon forest: a record of biodiversity preserved by ancient fires. Quat Geochronol. doi: 10.1016/j.quageo.2017.04.005 Google Scholar
  40. Hardesty J, Myers RL, Fulks W (2005) Fire, ecosystems, and people: a preliminary assessment of fire as a global conservation issue. George Wright Forum 22:78–87Google Scholar
  41. Heckenberger MJ, Russell JC, Toney JR, Schmidt MJ (2007) The legacy of cultural landscapes in the Brazilian Amazon: implications for biodiversity. Phil Trans R Soc B 362:197–208CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  43. Hoffmann WA, Orthen B, Nascimento PKV (2003) Comparative fire ecology of tropical Savanna and forest trees. Funct Ecol 17:720–726CrossRefGoogle Scholar
  44. Hoffmann WA, Geiger EL, Gotsch CG et al (2012) Ecological thresholds at the savanna-forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes. Ecol Lett 15:759–768CrossRefPubMedGoogle Scholar
  45. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228CrossRefGoogle Scholar
  46. Huete AR, Didan K, Shimabukuro YE (2006) Amazon rainforests green-up with sunlight in dry season. Geophys Res Lett 33:L06405CrossRefGoogle Scholar
  47. Intergovernmental Panel on Climate Change (2013) Climate change 2013: the physical science basis. In: Stocker TF et al. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, CambridgeGoogle Scholar
  48. Keeley JE, Pausas JG, Rundel PW, Bond WJ, Bradstock RA (2011) Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci 16:406–411CrossRefPubMedGoogle Scholar
  49. Ketterings QM, Coe R, van Noordwijk M, Ambagau Y, Palm CA (2001) Reducing uncertainty in the use of allometric biomass equations for predicting above-ground tree biomass in mixed secondary forests. Forest Ecol Manag 146:199–209CrossRefGoogle Scholar
  50. Kleyer M, Dray S, Bello F et al (2012) Assessing species and community functional responses to environmental gradients: which multivariate methods? J Veg Sci 23:805–821CrossRefGoogle Scholar
  51. Koele N, Bird MI, Haig J et al (2017) First estimate of soil pyrogenic carbon stocks to 2 m in the Amazon Basin. Geoderma.Google Scholar
  52. Kraft NJB, Valencia R, Ackerly D (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322:580–582CrossRefPubMedGoogle Scholar
  53. Lopez-Gonzalez G, Lewis SL, Burkitt M, Baker TR, Phillips OL (2009) Database. Accessed 05–30 Oct, 2015
  54. Lopez-Gonzalez G, Lewis SL, Burkitt M, Baker TR, Phillips OL (2011) a web application and research tool to manage and analyse tropical forest plot data. J Veg Sci 22:610–613CrossRefGoogle Scholar
  55. Lucena IC, Leite MB, Matos DMS (2015) A deciduidade foliar indica a vulnerabilidade de espécies lenhosas ao fogo. Rev Árvore 39:59–68CrossRefGoogle Scholar
  56. Malhado ACM, Malhi Y, Whittaker RJ et al (2009) Spatial trends in leaf size of Amazonian rainforest trees. Biogeosciences 6:1563–1576CrossRefGoogle Scholar
  57. Malhado ACM, Oliveira-neto JA, Stropp J et al (2015) Climatological correlates of seed size in Amazonian forest trees. J Veg Sci 26:956–963CrossRefGoogle Scholar
  58. Marimon BS, Lima ES, Duarte TG, Chieregatto LC, Ratter JA (2006) Observations on the vegetation of northeastern Mato Grosso, Brazil. IV. An analysis of the Cerrado-Amazonian Forest ecotone. Edinb J Bot 63:323–341CrossRefGoogle Scholar
  59. Marimon BS, Marimon-Junior BH, Feldpausch TR et al (2014) Disequilibrium and hyperdynamic tree turnover at the forest–cerrado transition zone in southern Amazonia. Plant Ecol Div 7:281–292CrossRefGoogle Scholar
  60. McMichael CH, Piperno DR, Bush MB et al (2012) Sparse pre-columbian human habitation in Western Amazonia. Science 336:1429–1431CrossRefPubMedGoogle Scholar
  61. McMichael CNH, Matthews-Bird F, Farfan-Rios W, Feeley KJ (2017) Ancient human disturbances may be skewing our understanding of Amazonian forests. Proceed Natl Acad Sci 114:522–527CrossRefGoogle Scholar
  62. Meredith W, Ascough PL, Bird MI et al (2012) Assessment of hydropyrolysis as a method for the quantification of black carbon using standard reference materials. Geochim Cosmochim Acta 97:131–147CrossRefGoogle Scholar
  63. Mews HA, Marimon BS, Maracahipes L, Franczak DD, Marimon-Junior BH (2011) Dinâmica da comunidade lenhosa de um Cerrado Típico na região Nordeste do Estado de Mato Grosso, Brasil. Biota Neotrop 11:73–82CrossRefGoogle Scholar
  64. Mittelbach GG, Schemske DW (2015) Ecological and evolutionary perspectives on community assembly. Trends Ecol Evol 30:241–247CrossRefPubMedGoogle Scholar
  65. Morandi PS, Marimon BS, Eisenlohr PV et al (2016) Patterns of tree species composition at watershed-scale in the Amazon ‘arc of deforestation’: implications for conservation. Environ Conserv 43:317–326CrossRefGoogle Scholar
  66. Moy CM, Seltzer GO, Rodbell DT, Anderson DM (2002) Variability of El Niño/southern oscillation activity at millennial timescales during the Holocene epoch. Nature 420:162–165CrossRefPubMedGoogle Scholar
  67. Muniz FH (2008) Padrões de floração e frutificação de árvores da Amazônia Maranhense. Acta Amaz 38:617–626CrossRefGoogle Scholar
  68. (MPEG) Museu Paraense Emilio Goeldi (2014). Vegetation—trees & lianas 1.4, CAX1Google Scholar
  69. Nogueira EM, Nelson BW, Fearnside PM, França MB, Oliveira ACA (2008) Tree height in Brazil’s ‘arc of deforestation’: shorter trees in south and southwest Amazonia imply lower biomass. For Ecol Manag 225:2963–2972CrossRefGoogle Scholar
  70. O’Brien MJ, Engelbrecht BMJ, Joswig J et al (2017) A synthesis of tree functional traits related to drought-induced mortality in forests across climatic zones. J Appl Ecol. doi: 10.1111/1365-2664.12874 Google Scholar
  71. Pausas JG, Lavorel S (2003) A hierarchical deductive approach for functional types in disturbed ecosystems. J Veg Sci 14:409–416CrossRefGoogle Scholar
  72. Phillips OL, Aragao LE, Lewis SL et al (2009) Drought sensitivity of the Amazon rainforest. Science 323:1344–1347CrossRefPubMedGoogle Scholar
  73. Pinter N, Fiedel S, Keely JE (2011) Fire and vegetation shifts in the Americas at the vanguard of Paleoindian migration. Quat Sci Rev 30:269–272CrossRefGoogle Scholar
  74. Piperno DR, Becker P (1996) Vegetational history of a site in the Central Amazon basin derived from phytolith and charcoal records from natural soils. Quat Res 45:202–209CrossRefGoogle Scholar
  75. Quesada CA, Phillips OL, Schwarz M et al (2012) Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9:2203–2246CrossRefGoogle Scholar
  76. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  77. Reich PB, Wright IJ, Cavendar-Bares J, Craine JM et al (2003) The evolution of plant functional variation: traits, Spectra, and strategies. Int J Plant Sci 164:143–164CrossRefGoogle Scholar
  78. Roosevelt AC (2013) The Amazon and the Anthropocene: 13,000 years of human influence in a tropical rainforest. Anthropocene 4:69–87CrossRefGoogle Scholar
  79. Rowland L, Malhi Y, Silva-Espejo JE et al (2014) The sensitivity of wood production to seasonal and interannual variations in climate in a lowland Amazonian rainforest. Oecologia 174:295–306CrossRefPubMedGoogle Scholar
  80. Sanford RL, Saldarriaga J, Clark KE, Uhl C, Herrera R (1985) Amazon rain-forest fires. Science 227:53–55CrossRefPubMedGoogle Scholar
  81. Santín C, Doerr SH, Preston CM, González-Rodríguez G (2015) Pyrogenic organic matter production from wildfires: a missing sink in the global carbon cycle. Glob Change Biol 21:1621–1633CrossRefGoogle Scholar
  82. Säumel I, Kowarik I (2013) Propagule morphology and river characteristics shape secondary water dispersal in tree species. Plant Ecol 214:1257–1272CrossRefGoogle Scholar
  83. Sfair JC, Rosado BHP, Tabarelli M (2016) The effects of environmental constraints on plant community organization depend on which traits are measured. J Veg Sci 27:1264–1274CrossRefGoogle Scholar
  84. Silva KE, Martins SV, Fortin M-J et al (2014) Tree species community spatial structure in a terra firme Amazon forest, Brazil. Bosque 35:347–355CrossRefGoogle Scholar
  85. Sombroek W (2001) Spatial and temporal patterns of Amazon rainfall. Consequences for the planning of agricultural occupation and the protection of primary forests. Ambio 30:388–396CrossRefPubMedGoogle Scholar
  86. Stefanello D, Fernandes-Bulhão C, Martins SV (2009) Síndromes de dispersão de sementes em três trechos de vegetação ciliar (nascente, meio e foz) ao longo do rio Pindaíba, MT. Revta Árvore 33:1051–1061CrossRefGoogle Scholar
  87. Swenson NG, Enquist BJ (2007) Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation. Am J Bot 94:451–459CrossRefPubMedGoogle Scholar
  88. ter Braak CJF, Peres-Neto PR, Dray S (2016) A critical issue in model-based inference for studying trait-based community assembly and a solution. PeerJ 5:e2885CrossRefGoogle Scholar
  89. ter Steege H, Pitman NCA, Sabatier D et al (2013) Hyperdominance in the Amazonian Tree Flora. Science 342:325–334Google Scholar
  90. Toledo JJ, Castilho CV, Magnusson WE, Nascimento HEM (2016) Soil controls biomass and dynamics of an Amazonian forest through the shifting of species and traits. Braz J Bot 39:1–11CrossRefGoogle Scholar
  91. Turcq B, Sifeddine A, Martin L et al (1998) Amazonia rainforest fires: a lacustrine record of 7000 Years. Ambio 27:139–142Google Scholar
  92. Uhl C, Kauffman JB, Cummings DL (1998) Fire in the Venezuelan Amazon 2: environmental conditions necessary for forest fires in the evergreen rainforest of Venezuela. Oikos 53:176–184CrossRefGoogle Scholar
  93. Urrego DH, Bush MB, Silman MR, Vetaas OR (2013) Holocene fires, forest stability and human occupation in south-western Amazonia. J Biogeogr 40:521–533CrossRefGoogle Scholar
  94. van der Pijl L (1972) Principles of dispersal in higher plants. Springer, New YorkCrossRefGoogle Scholar
  95. van der Sande MT, Arets EJMM, Peña-Claros M et al (2016) Old-growth neotropical forests are shifting in species and trait composition. Ecol Monogr 86:228–243CrossRefGoogle Scholar
  96. Vieira DLM, Scariot A (2006) Principles of natural regeneration of tropical dry forest for restoration. Restor Ecol 14:11–20CrossRefGoogle Scholar
  97. Watling J, Iriarte J, Mayle FE et al (2017) Impact of pre-columbian “geoglyph” builders on Amazonian forests. Proceed Natl Acad Sci 114:1868–1873CrossRefGoogle Scholar
  98. Whitlock C, Larsen C (2001) Charcoal as a Fire Proxy. In: Smol JP, Birks HJB, Last HM et al (eds) Tracking environmental change using lake sediments, vol 3. The series developments in paleoenvironmental research. Springer, Netherlands, pp 75–97CrossRefGoogle Scholar
  99. Woodward FI (1987) Climate and plant distribution. Cambridge University Press, CambridgeGoogle Scholar
  100. Yamamoto LF, Kinoshita LS, Martins FR (2007) Síndromes de polinização e de dispersão em fragmentos da Floresta Estacional Semidecídua Montana, SP, Brasil. Acta Bot Bras 21:553–573CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Klécia G. Massi
    • 1
    • 2
    Email author
  • Michael Bird
    • 3
  • Beatriz S. Marimon
    • 1
  • Ben Hur MarimonJr.
    • 1
  • Denis S. Nogueira
    • 1
  • Edmar A. Oliveira
    • 1
  • Oliver L. Phillips
    • 4
  • Carlos A. Quesada
    • 5
  • Ana S. Andrade
    • 5
  • Roel J. W. Brienen
    • 4
  • José L. C. Camargo
    • 5
  • Jerome Chave
    • 6
  • Eurídice N. Honorio Coronado
    • 7
  • Leandro V. Ferreira
    • 8
  • Niro Higuchi
    • 9
  • Susan G. Laurance
    • 3
  • William F. Laurance
    • 3
  • Thomas Lovejoy
    • 5
    • 10
  • Yadvinder Malhi
    • 11
  • Rodolfo V. Martínez
    • 12
  • Abel Monteagudo
    • 12
  • David Neill
    • 13
  • Adriana Prieto
    • 14
  • Hirma Ramírez-Angulo
    • 15
  • Hans ter Steege
    • 16
    • 17
  • Emilio Vilanova
    • 18
  • Ted R. Feldpausch
    • 19
    Email author
  1. 1.Laboratório de Ecologia VegetalUniversidade do Estado de Mato Grosso (UNEMAT)Nova XavantinaBrazil
  2. 2.Instituto de Ciência e TecnologiaUniversidade Estadual Paulista (Unesp)São José dos CamposBrazil
  3. 3.College of Science and Engineering and Centre for Tropical Environmental and Sustainability Science (TESS)James Cook UniversityCairnsAustralia
  4. 4.School of GeographyUniversity of LeedsLeedsUK
  5. 5.Biological Dynamics of Forest Fragments ProjectNational Institute for Amazonian Research (INPA) and Smithsonian Tropical Research InstituteManausBrazil
  6. 6.Laboratoire EDB, Université Paul SabatierToulouseFrance
  7. 7.Instituto de Investigaciones de la Amazonía PeruanaIquitosPeru
  8. 8.Coordenação de Botânica, Museu Paraense Emilio GoeldiBelémBrazil
  9. 9.National Institute for Amazonian Research (INPA)ManausBrazil
  10. 10.Department of Environmental Science and PolicyGeorge Mason UniversityFairfaxUSA
  11. 11.Environmental Change Institute, School of Geography and the EnvironmentUniversity of OxfordOxfordUK
  12. 12.Proyecto Flora del Peru, Jardin Botanico de MissouriOxapampaPeru
  13. 13.Puyo, Universidad Estatal AmazónicaPastazaEcuador
  14. 14.Instituto de Ciencias NaturalesUniversidad Nacional de ColombiaBogotaColombia
  15. 15.Universidad de Los AndesMéridaVenezuela
  16. 16.Naturalis Biodiversity CenterLeidenThe Netherlands
  17. 17.Systems EcologyFree UniversityAmsterdamThe Netherlands
  18. 18.University of WashingtonSeattleUSA
  19. 19.Geography, College of Life and Environmental SciencesUniversity of ExeterExeterUK

Personalised recommendations