Importance of topography for tree species habitat distributions in a terra firme forest in the Colombian Amazon

  • Daniel ZuletaEmail author
  • Sabrina E. Russo
  • Andrés Barona
  • Juan S. Barreto-Silva
  • Dairon Cardenas
  • Nicolas Castaño
  • Stuart J. Davies
  • Matteo Detto
  • Sonia Sua
  • Benjamin L. Turner
  • Alvaro Duque
Regular Article



To test the relative importance of topography versus soil chemistry in defining tree species-habitat associations in a terra firme Amazonian forest.


We evaluated habitat associations for 612 woody species using alternative habitat maps generated from topography and soil chemistry in the 25-ha Amacayacu Forest Dynamics Plot, Colombian Amazon. We assessed the ability of each habitat map to explain the community-level patterns of species-habitat associations using two methods of habitat randomization and different sample size thresholds (i.e., species’ abundance).


The greatest proportion of species-habitat associations arose from topographically-defined habitats (55% to 63%) compared to soil chemistry-defined (19% to 40%) or topography plus soil chemistry-defined habitats (18% to 42%). Results were robust to the method of habitat randomization and to sample size threshold.


Our results demonstrate that certain environmental factors may be more influential than others in defining forest-level patterns of community assembly and that comparison of the ability of different environmental variables to explain habitat associations is a crucial step in testing hypotheses about the mechanisms underlying assembly. Our results point to topography-driven hydrological variation as a key factor structuring tree species distributions in what are commonly considered homogeneous Amazonian terra firme forests.


Amacayacu forest dynamics plot Forest global earth observatory (ForestGEO) Habitat filtering Hydrological niches Iterative amplitude adjusted Fourier transform Northwestern Amazon Torus translation test 



This study was partially supported by the Convocatoria Nacional para el Apoyo a Proyectos de Investigación y Creación Artística de la Universidad Nacional de Colombia 2017-2018 grant 38821 to A. Duque. We would like to thank Parques Nacionales Naturales de Colombia, in particular to Eliana Martínez and staff members of the Amacayacu Natural National Park. We are very grateful for the assistance of our coworkers in Comunidad de Palmeras and the students of forest engineering from the Universidad Nacional de Colombia in collecting the tree census data. We also thank the Center for Tropical Forest Science-Forest Global Earth Observatory (CTFS-Forest- GEO) of the Smithsonian Tropical Research Institute for partial support of the plot census. Many thanks are extended to J. Dalling and C. Baldeck for assistance with kriging, T. Romero and S. Ramirez for assistance with soil sampling, and D. Agudo, A. Bielnicka, and I. Torres for laboratory support. Analyses for this manuscript were first advanced and discussed at two CTFS-ForestGEO Workshops supported by the NSF grants 1545761 and 1354741 to S.J. Davies. D. Zuleta was supported by National Doctoral Scholarship COLCIENCIAS (647, 2015-II). Finally, we are very grateful to Rafael S. Oliveira and two anonymous referees for the comments made to this manuscript.

Supplementary material

11104_2018_3878_MOESM1_ESM.docx (2 mb)
ESM 1 (DOCX 2064 kb)


  1. Allié E, Pélissier R, Engel J, Petronelli P, Freycon V, Deblauwe V, Soucémarianadin L, Weigel J, Baraloto C (2015) Pervasive local-scale tree-soil habitat association in a tropical forest community. PLoS One 10:1–16. CrossRefGoogle Scholar
  2. Altman N, Krzywinski M (2017) Clustering. Nat Methods 14:545–546CrossRefGoogle Scholar
  3. Anderson-Teixeira KJ, Davies SJ, Bennett AC, Gonzalez-Akre EB, Muller-Landau HC, Joseph Wright S, Abu Salim K, Almeyda Zambrano AM, Alonso A, Baltzer JL, Basset Y, Bourg NA, Broadbent EN, Brockelman WY, Bunyavejchewin S, Burslem DFRP, Butt N, Cao M, Cardenas D, Chuyong GB, Clay K, Cordell S, Dattaraja HS, Deng X, Detto M, du X, Duque A, Erikson DL, Ewango CEN, Fischer GA, Fletcher C, Foster RB, Giardina CP, Gilbert GS, Gunatilleke N, Gunatilleke S, Hao Z, Hargrove WW, Hart TB, Hau BCH, He F, Hoffman FM, Howe RW, Hubbell SP, Inman-Narahari FM, Jansen PA, Jiang M, Johnson DJ, Kanzaki M, Kassim AR, Kenfack D, Kibet S, Kinnaird MF, Korte L, Kral K, Kumar J, Larson AJ, Li Y, Li X, Liu S, Lum SKY, Lutz JA, Ma K, Maddalena DM, Makana JR, Malhi Y, Marthews T, Mat Serudin R, McMahon SM, McShea WJ, Memiaghe HR, Mi X, Mizuno T, Morecroft M, Myers JA, Novotny V, de Oliveira AA, Ong PS, Orwig DA, Ostertag R, den Ouden J, Parker GG, Phillips RP, Sack L, Sainge MN, Sang W, Sri-ngernyuang K, Sukumar R, Sun IF, Sungpalee W, Suresh HS, Tan S, Thomas SC, Thomas DW, Thompson J, Turner BL, Uriarte M, Valencia R, Vallejo MI, Vicentini A, Vrška T, Wang X, Wang X, Weiblen G, Wolf A, Xu H, Yap S, Zimmerman J (2015) CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob Chang Biol 21:528–549. CrossRefPubMedGoogle Scholar
  4. Baldeck CA, Harms KE, Yavitt JB, John R, Turner BL, Valencia R, Navarrete H, Davies SJ, Chuyong GB, Kenfack D, Thomas DW, Madawala S, Gunatilleke N, Gunatilleke S, Bunyavejchewin S, Kiratiprayoon S, Yaacob A, Supardi MNN, Dalling JW (2013) Soil resources and topography shape local tree community structure in tropical forests. Proc R Soc B Biol Sci 280:20122532. CrossRefGoogle Scholar
  5. Baltzer JL, Thomas SC, Nilus R, Burslem DFRP (2005) Edaphic specialization in tropical trees: physiological correlates and responses to reciprocal transplantation. Ecology 86:3063–3077CrossRefGoogle Scholar
  6. Brady NC, Weil RR (2002) The nature and properties of soils. Prentice Hall, Upper Saddle RiverGoogle Scholar
  7. Brum M, Vadeboncoeur MA, Ivanov V, Asbjornsen H, Saleska S, Alves LF, Penha D, Dias JD, Aragão LEOC, Barros F, Bittencourt P, Pereira L, Oliveira RS (2018) Hydrological niche segregation defines forest structure and drought tolerance strategies in a seasonal Amazon forest. J Ecol 00:1–16.
  8. Chamorro C (1989) Biología de los suelos del Parque Nacional Natural Amacayacu y zonas adyacentes (Amazonas, Colombia). Colomb Geográfica 15:45–63Google Scholar
  9. Chase JM (2014) Spatial scale resolves the niche versus neutral theory debate. J Veg Sci 25:319–322. CrossRefGoogle Scholar
  10. Chuyong GB, Kenfack D, Harms KE, Thomas DW, Condit R, Comita LS (2011) Habitat specificity and diversity of tree species in an African wet tropical forest. Plant Ecol 212:1363–1374. CrossRefGoogle Scholar
  11. Clark DB, Clark DA, Read JM (1998) Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. J Ecol 86:101–112. CrossRefGoogle Scholar
  12. Clifford P, Richardson S, Hémon D (1989) Assessing the significance of the correlation between two spatial processes. Biometrics 45:123–134CrossRefPubMedGoogle Scholar
  13. Condit R (1996) Defining and mapping vegetation in mega-diverse tropical forests. Tree 11:4–5PubMedGoogle Scholar
  14. Condit R (1998) Tropical forest census plots. Springer, TokyoCrossRefGoogle Scholar
  15. Condit R, Hubbell SP, Foster RB (1992) Recruitment near conspecific adults and the maintenance of tree and shrub diversity in a neotropical forest. Am Nat 140:261–286. CrossRefPubMedGoogle Scholar
  16. Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N, Hubbell SP, Foster RB, Itoh A, LaFrankie J, Lee HS, Losos E, Manokaran N, Sukumar R, Yamakura T (2000) Spatial patterns in the distribution of tropical tree species. Science 288:1414–1418. CrossRefPubMedGoogle Scholar
  17. Condit R, Pitman N, Leigh Jr EG, Chave J, Terborgh J, Foster RB, Núñez P, Aguilar S, Valencia R, Villa G, Muller-Landau HC, Losos E, Hubbell SP (2002) Beta-diversity in tropical forest trees. Science 295:666–669Google Scholar
  18. Condit R, Engelbrecht BMJ, Pino D, Perez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci U S A 110:5064–5068. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cosme LHM, Schietti J, Costa FRC, Oliveira RS (2017) The importance of hydraulic architecture to the distribution patterns of trees in a central Amazonian forest. New Phytol 215:113–125. CrossRefPubMedGoogle Scholar
  20. Costa FRC, Magnusson WE, Luizao RC (2005) Mesoscale distribution patterns of Amazonian understorey herbs in relation to topography, soil and watersheds. J Ecol 93:863–878. CrossRefGoogle Scholar
  21. Dalling JW, Schnitzer SA, Baldeck C, Harms KE, John R, Mangan SA, Lobo E, Yavitt JB, Hubbell SP (2012) Resource-based habitat associations in a neotropical liana community. J Ecol 100:1174–1182. CrossRefGoogle Scholar
  22. Davies SJ, Tan S, LaFrankie JV, Potts MD (2005) Soil-related floristic variation in a hyperdiverse dipterocarp forest in Lambir Hills, Sarawak. In: Roubik DW, Sakai S, Hamid A (eds) Pollination ecology and the rain Forest diversity. Sarawak Studies. Springer-Verlag, New York, pp 22–34CrossRefGoogle Scholar
  23. Daws MI, Mullins CE, Burslem DFRP, Paton SR, Dalling JW (2002) Topographic position affects the water regime in a semideciduous tropical forest in Panamá. Plant Soil 238:79–90. CrossRefGoogle Scholar
  24. de Castilho CV, Magnusson WE, de Araújo RNO, Luizão RCC, Luizão FJ, Lima AP, Higuchi N (2006) Variation in aboveground tree live biomass in a central Amazonian Forest: effects of soil and topography. For Ecol Manag 234:85–96. CrossRefGoogle Scholar
  25. Deblauwe V, Kennel P, Couteron P (2012) Testing pairwise association between spatially autocorrelated variables: a new approach using surrogate lattice data. PLoS One 7:e48766. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Detto M, Muller-Landau HC, Mascaro J, Asner GP (2013) Hydrological networks and associated topographic variation as templates for the spatial organization of tropical forest vegetation. PLoS One 8:e76296. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Duffy PB, Brando P, Asner GP, Field CB (2015) Projections of future meteorological drought and wet periods in the Amazon. Proc Natl Acad Sci 112:13172–13177. CrossRefPubMedGoogle Scholar
  28. Duivenvoorden JF, Duque AJ (2010) Composition and diversity of northwestern Amazonian forests in a geoecological context. In: Hoorn C, Wesselingh F (eds) Amazonia landscape and species evolution: a look in the past. Wiley–Blackwell, Chichester, p 447Google Scholar
  29. Duivenvoorden J, Lips J (1995) A land-ecological study of soils, vegetation, and plant diversity in Colombian Amazonia, vol 12. Tropenbos Foundation, WageningenGoogle Scholar
  30. Duque A, Sánchez M, Cavelier J, Duivenvoorden JF (2002) Different floristic patterns of woody understorey and canopy plants in Colombian Amazonia. J Trop Ecol 18:499–525. CrossRefGoogle Scholar
  31. Duque A, Cavelier J, Posada A et al (2003) Strategies of tree occupation at a local scale in terra firme forests in the Colombian Amazon. Biotropica 35:20–27Google Scholar
  32. Duque A, Muller-Landau HC, Valencia R, Cardenas D, Davies S, de Oliveira A, Pérez ÁJ, Romero-Saltos H, Vicentini A (2017) Insights into regional patterns of Amazonian forest structure, diversity, and dominance from three large terra-firme forest dynamics plots. Biodivers Conserv 26:669–686. CrossRefGoogle Scholar
  33. Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82CrossRefPubMedGoogle Scholar
  34. Fraley C, Raftery AE (2007) Model-based methods of classification: using the mclust software in chemometrics. J Stat Softw 18:1–13. CrossRefGoogle Scholar
  35. Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution, Washington, D.C.Google Scholar
  36. Gunatilleke CVS, Gunatilleke IAUN, Esufali S, Harms KE, Ashton PMS, Burslem DFRP, Ashton PS (2006) Species–habitat associations in a Sri Lankan dipterocarp forest. J Trop Ecol 22:371–384. CrossRefGoogle Scholar
  37. Harms KE, Condit R, Hubbell SP, Foster RB (2001) Habitat associations of trees and shrubs in a 50-ha neotropical forest plot. J Ecol 89:947–959. CrossRefGoogle Scholar
  38. Hendershot WH, Lalande H, Duquette M (2008) Ion exchange and exchangeable cations. In: Carter MR, Gregorich EG (eds) Soil Sampling and Methods of Analysis, Second Edi. Canadian Society of Soil Science and CRC Press, Boca Raton, pp 197–206Google Scholar
  39. Higgins MA, Ruokolainen K, Tuomisto H, Llerena N, Cardenas G, Phillips OL, Vásquez R, Räsänen M (2011) Geological control of floristic composition in Amazonian forests. J Biogeogr 38:2136–2149. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hogan JA, Zimmerman JK, Uriarte M, Turner BL, Thompson J (2016) Land-use history augments environment–plant community relationship strength in a Puerto Rican wet forest. J Ecol 104:1466–1477. CrossRefGoogle Scholar
  41. Holdridge LR (1978) Ecología basada en zonas de vida. IICA, San José, pp 1978–1982Google Scholar
  42. Honorio EN, Baker TR, Phillips OL et al (2009) Multi-scale comparisons of tree composition in Amazonian terra firme forests. Biogeosciences 6:2719–2731. CrossRefGoogle Scholar
  43. Hoorn C (1994) An environmental reconstruction of the paleo-Amazon river system (Midle-Late Miocene, NW, Amazonia). Palaeogeogr Palaeoclimatol Palaeoecol 112:187–238CrossRefGoogle Scholar
  44. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University press, PrincetonGoogle Scholar
  45. Hubbell SP, Foster RB (1986) Commonness and rarity in a Neotropical forest: implications for tropical tree conservation. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer associates, Sunderland, Mass., pp 205–231Google Scholar
  46. Hubbell SP, Foster RB, O’Brien ST, Harms KE, Condit R, Wechsler B, Wright SJ, Loo de Lao S (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a Neotropical Forest. Science 283:554–557Google Scholar
  47. Itoh A, Yamakura T, Ohkubo T, Kanzaki M, Palmiotto PA, LaFrankie JV, Ashton PS, Lee HS (2003) Importance of topography and soil texture in the spatial distribution of two sympatric dipterocarp trees in a Bornean rainforest. Ecol Res 18:307–320. CrossRefGoogle Scholar
  48. Itoh A, Ohkubo T, Nanami S, Tan S, Yamakura T (2010) Comparison of statistical tests for habitat associations in tropical forests: a case study of sympatric dipterocarp trees in a Bornean forest. For Ecol Manag 259:323–332. CrossRefGoogle Scholar
  49. John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M, Foster RB (2007) Soil nutrients influence spatial distributions of tropical tree species. Proc Natl Acad Sci U S A 104:864–869. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Jucker T, Bongalov B, Burslem DFRP, Nilus R, Dalponte M, Lewis SL, Phillips OL, Qie L, Coomes DA (2018) Topography shapes the structure, composition and function of tropical forest landscapes. Ecol Lett 21:989–1000. CrossRefPubMedGoogle Scholar
  51. Kenfack D, Chuyong GB, Condit R, Russo SE, Thomas DW (2014) Demographic variation and habitat specialization of tree species in a diverse tropical forest of Cameroon. For Ecosyst 1:22. CrossRefGoogle Scholar
  52. Laurance WF, Fearnside PM, Laurance SG, Delamonica P, Lovejoy TE, Rankin-de Merona JM, Chambers JQ, Gascon C (1999) Relationship between soils and Amazon forest biomass: a landscape scale study. For Ecol Manag 118:127–138. CrossRefGoogle Scholar
  53. Law R, Illian J, Burslem DFRP, Gratzer G, Gunatilleke CVS, Gunatilleke IAUN (2009) Ecological information from satial patterns of plants: insights from point process theory. J Ecol 97:616–628. CrossRefGoogle Scholar
  54. Legendre P, Legendre LFJ (2012) Numerical Ecology. ElsevierGoogle Scholar
  55. Lloyd J, Domingues TF, Schrodt F, Ishida FY, Feldpausch TR, Saiz G, Quesada CA, Schwarz M, Torello-Raventos M, Gilpin M, Marimon BS, Marimon-Junior BH, Ratter JA, Grace J, Nardoto GB, Veenendaal E, Arroyo L, Villarroel D, Killeen TJ, Steininger M, Phillips OL (2015) Edaphic, structural and physiological contrasts across Amazon Basin forest-savanna ecotones suggest a role for potassium as a key modulator of tropical woody vegetation structure and function. Biogeosciences 12(22):6529–6571CrossRefGoogle Scholar
  56. Oksanen J, Blanchet FG, Kindt R, et al (2016) vegan: Community Ecology PackageGoogle Scholar
  57. Oliveira RS, Costa FRC, Baalen E, Jonge A, Bittencourt PR, Almanza Y, Barros Fd, Cordoba EC, Fagundes MV, Garcia S, Guimaraes Z, Hertel M, Schietti J, Rodrigues‐Souza J, Poorter L (2018) Embolism resistance drives the distribution of Amazonian rainforest tree species along hydro-topographic gradients. New Phytol.
  58. Peay KG, Russo SE, Mcguire KL et al (2015) Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient. Ecol Lett 18:807–816. CrossRefPubMedGoogle Scholar
  59. Phillips OL, Núñez Vargas P, Monteagudo AL et al (2003) Habitat association among Amazonian tree species: a landscape-scale approach. J Ecol 91:757–775. CrossRefGoogle Scholar
  60. Phillips OL, Baker TR, Arroyo L, Higuchi N, Killeen TJ, Laurance WF, Lewis SL, Lloyd J, Malhi Y, Monteagudo A, Neill DA, Nunez Vargas P, Silva JNM, Terborgh J, Vasquez Martinez R, Alexiades M, Almeida S, Brown S, Chave J, Comiskey JA, Czimczik CI, di Fiore A, Erwin T, Kuebler C, Laurance SG, Nascimento HEM, Olivier J, Palacios W, Patino S, Pitman NCA, Quesada CA, Saldias M, Torres Lezama A, Vinceti B (2004) Pattern and process in Amazon tree turnover, 1976-2001. Philos Trans R Soc B Biol Sci 359:381–407. CrossRefGoogle Scholar
  61. Pitman NCA, Terborgh J, Silman MR, Nunez PV (1999) Tree species distributions in an upper Amazonian forest. Ecology 80:2651–2661CrossRefGoogle Scholar
  62. Pitman NCA, Terborgh JW, Silman MR, Núñez V P, Neill DA, Cerón CE, Palacios WA, Aulestia M (2001) Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology 82:2101–2117.[2101:DADOTS]2.0.CO;2Google Scholar
  63. Poulsen DA, Balslev H (1991) Abundance and cover of ground herbs in an Amazonian rain forest. J Veg Sci 2:315–322. CrossRefGoogle Scholar
  64. Prieto A (1994) Análisis estructural y florístico de la vegetación de la isla Mocagua, río Amazonas (Amazonas, Colombia). Universidad Nacional de Colombia, BogotáGoogle Scholar
  65. Quesada CA, Lloyd J (2016) Soil–vegetation interactions in Amazonia. In: Nagy L, Forsberg BR, Artaxo P (eds) Interactions between biosphere. Atmosphere and Human Land Use in the Amazon Basin. Springer, Berlin, Heidelberg, pp 267–299Google Scholar
  66. Quesada CA, Lloyd J, Schwarz M, Baker TR, Phillips OL, Patiño S, Czimczik C, Hodnett MG, Herrera R, Arneth A, Lloyd G, Malhi Y, Dezzeo N, Luizão FJ, Santos AJB, Schmerler J, Arroyo L, Silveira M, Priante Filho N, Jimenez EM, Paiva R, Vieira I, Neill DA, Silva N, Peñuela MC, Monteagudo A, Vásquez R, Prieto A, Rudas A, Almeida S, Higuchi N, Lezama AT, López-González G, Peacock J, Fyllas NM, Alvarez Dávila E, Erwin T, di Fiore A, Chao KJ, Honorio E, Killeen T, Peña Cruz A, Pitman N, Núñez Vargas P, Salomão R, Terborgh J, Ramírez H (2009a) Regional and large-scale patterns in Amazon forest structure and function are mediated by variations in soil physical and chemical properties. Biogeosci Discuss 6:3993–4057. CrossRefGoogle Scholar
  67. Quesada CA, Lloyd J, Schwarz M, Patiño S, Baker TR, Czimczik C, Fyllas NM, Martinelli L, Nardoto GB, Schmerler J, Santos AJB, Hodnett MG, Herrera R, Luizão FJ, Arneth A, Lloyd G, Dezzeo N, Hilke I, Kuhlmann I, Raessler M, Brand WA, Geilmann H, Moraes Filho JO, Carvalho FP, Araujo Filho RN, Chaves JE, Cruz Junior OF, Pimentel TP, Paiva R (2009b) Chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosci Discuss 6:3923–3992. CrossRefGoogle Scholar
  68. Quesada CA, Lloyd J, Anderson LO, Fyllas NM, Schwarz M, Czimczik CI (2011) Soils of Amazonia with particular reference to the RAINFOR sites. Biogeosciences 8:1415–1440. CrossRefGoogle Scholar
  69. Quesada CA, Phillips OL, Schwarz M, Czimczik CI, Baker TR, Patiño S, Fyllas NM, Hodnett MG, Herrera R, Almeida S, Alvarez Dávila E, Arneth A, Arroyo L, Chao KJ, Dezzeo N, Erwin T, di Fiore A, Higuchi N, Honorio Coronado E, Jimenez EM, Killeen T, Lezama AT, Lloyd G, López-González G, Luizão FJ, Malhi Y, Monteagudo A, Neill DA, Núñez Vargas P, Paiva R, Peacock J, Peñuela MC, Peña Cruz A, Pitman N, Priante Filho N, Prieto A, Ramírez H, Rudas A, Salomão R, Santos AJB, Schmerler J, Silva N, Silveira M, Vásquez R, Vieira I, Terborgh J, Lloyd J (2012) Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9:2203–2246. CrossRefGoogle Scholar
  70. R Core Team (2017) R: A language and environment for statistical computingGoogle Scholar
  71. Reynolds AP, Richards G, De La Iglesia B, Rayward-Smith VJ (2006) Clustering rules: a comparison of partitioning and hierarchical clustering algorithms. J Math Model Algorithms 5:475–504. CrossRefGoogle Scholar
  72. Ricklefs RE (1977) Environmental heterogeneity and plant species diversity: a hypothesis. Am Nat 111:376–381CrossRefGoogle Scholar
  73. Russo SE, Augspurger CK (2004) Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol Lett 7:1058–1067. CrossRefGoogle Scholar
  74. Russo SE, Davies SJ, King DA, Tan S (2005) Soil-related performance variation and distributions of tree species in a Bornean rain forest. J Ecol 93:879–889. CrossRefGoogle Scholar
  75. Russo SE, Potts MD, Davies S, Tan S (2007) Determinants of tree species distributions: comparing the roles of dispersal, seed size, and soil specialization in a Bornean rain forest. In: Dennis A, Green R, Schupp EW, Wescott D (eds) Seed dispersal: theory and its application in a changing world. CAB International, Wallingford, pp 499–518CrossRefGoogle Scholar
  76. Russo SE, Cannon WL, Elowsky C, Tan S, Davies SJ (2010) Variation in leaf stomatal traits of 28 tree species in relation to gas exchange along an edaphic gradient in a Bornean rain forest. Am J Bot 97:1109–1120. CrossRefPubMedGoogle Scholar
  77. Schietti J, Emilio T, Rennó CD, Drucker DP, Costa FRC, Nogueira A, Baccaro FB, Figueiredo F, Castilho CV, Kinupp V, Guillaumet JL, Garcia ARM, Lima AP, Magnusson WE (2014) Vertical distance from drainage drives floristic composition changes in an Amazonian rainforest. Plant Ecol Divers 7:241–253. CrossRefGoogle Scholar
  78. Schreiber T, Schmitz A (2000) Surrogate time series. Phys D Nonlinear Phenom 142:346–382CrossRefGoogle Scholar
  79. Schupp EW, Milleron T, Russo S (2002) Dissemination limitation and the origin and maintenance of species-rich tropical forests. In: Seed dispersal and frugivory: Ecology, evolution and conservation, pp 19–33Google Scholar
  80. Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys, 2nd edn. Natural Resources Conservation Service, U.S Department of Agriculture HandbookGoogle Scholar
  81. Sombroek W (2000) Amazon landforms and soils in relation to biological diversity. Acta Amaz 30:81–81. CrossRefGoogle Scholar
  82. Svenning J-C (1999) Microhabitat specialization in a species-rich palm community in Amazonian Ecuador. J Ecol 87:55–65. CrossRefGoogle Scholar
  83. ter Steege H, Pitman N, Sabatier D, Castellanos H, van der Hout P, Daly DC, Silveira M, Phillips O, Vasquez R, van Andel T, Duivenvoorden J, de Oliveira AA, Ek R, Lilwah R, Thomas R, van Essen J, Baider C, Maas P, Mori S, Terborgh J, NúÑez Vargas P, Mogollón H, Morawetz W (2003) A spatial model of tree alfa-diversity and tree density for the Amazon. Biodivers Conserv 12:2255–2277CrossRefGoogle Scholar
  84. ter Steege H, Pitman NCA, Phillips OL, Chave J, Sabatier D, Duque A, Molino JF, Prévost MF, Spichiger R, Castellanos H, von Hildebrand P, Vásquez R (2006) Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443:444–447CrossRefPubMedGoogle Scholar
  85. Thessler S, Ruokolainen K, Tuomisto H, Tomppo E (2005) Mapping gradual landscape-scale floristic changes in Amazonian primary rain forests by combining ordination and remote sensing. Glob Ecol Biogeogr 14:315–325. CrossRefGoogle Scholar
  86. Tilman D (1982) Resource competition and community structure. Princeton university pressGoogle Scholar
  87. Tuomisto H, Ruokolainen K, Aguilar M, Sarmiento A (2003a) Floristic patterns along a 43 km long transect in an Amazonian rain forest. J Ecol 91:743–756. CrossRefGoogle Scholar
  88. Tuomisto H, Ruokolainen K, Yli-Halla M (2003b) Dispersal, environment, and floristic variation of western Amazonian forests. Science 299:241–244. CrossRefPubMedGoogle Scholar
  89. Valencia R, Foster RB, Villa G, Condit R, Svenning JC, Hernandez C, Romoleroux K, Losos E, Magard E, Balslev H (2004) Tree species distributions and local habitat variation in the Amazon: large forest plot in eastern Ecuador. J Ecol 92:214–229. CrossRefGoogle Scholar
  90. Venema V, Meyer S, Garcìa SG, Kniffka A, Simmer C, Crewell S, Löhnert U, Trautmann T, Macke A (2006) Surrogate cloud fields generated with the iterative amplitude adapted Fourier transform algorithm. Tellus 58A:104–120. CrossRefGoogle Scholar
  91. Vincent JB, Turner BL, Alok C, Novotny V, Weiblen GD, Whitfeld TJS (2018) Tropical forest dynamics in unstable terrain : a case study from New Guinea. J Trop Ecol 34:1–19. CrossRefGoogle Scholar
  92. Zhang T, Niinemets Ü, Sheffield J, Lichstein JW (2018) Shifts in tree functional composition amplify the response of forest biomass to climate. Nature 556:99–102. CrossRefPubMedGoogle Scholar
  93. Zuleta D, Duque A, Cardenas D, Muller-Landau HC, Davies SJ (2017) Drought-induced mortality patterns and rapid biomass recovery in a terra firme forest in the Colombian Amazon. Ecology 98:2538–2546. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Daniel Zuleta
    • 1
    Email author
  • Sabrina E. Russo
    • 2
  • Andrés Barona
    • 3
  • Juan S. Barreto-Silva
    • 3
  • Dairon Cardenas
    • 3
  • Nicolas Castaño
    • 3
  • Stuart J. Davies
    • 4
  • Matteo Detto
    • 5
  • Sonia Sua
    • 3
  • Benjamin L. Turner
    • 6
  • Alvaro Duque
    • 1
  1. 1.Departamento de Ciencias ForestalesUniversidad Nacional de Colombia Sede MedellínMedellínColombia
  2. 2.School of Biological SciencesUniversity of NebraskaLincolnUSA
  3. 3.Herbario Amazónico ColombianoInstituto Amazónico de Investigaciones Científicas SinchiBogotáColombia
  4. 4.Center for Tropical Forest Science-Forest Global Earth ObservatorySmithsonian Tropical Research InstituteWashingtonUSA
  5. 5.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA
  6. 6.Smithsonian Tropical Research InstituteAnconRepublic of Panama

Personalised recommendations