Habitat Endemism in White-sand Forests: Insights into the Mechanisms of Lineage Diversification and Community Assembly of the Neotropical Flora

Biotropica

Volumn 48, Issue 1, 2016, Pages 24-33

  Fine, Paul V A ^a   Baraloto, Christopher ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Campus Agronomique   (France)

^c FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

Amazon; Endemic; Functional traits; Habitat specialization; Niche conservatism; Speciation

Indexed keywords

ANGIOSPERM; ASSEMBLY RULE; BIODIVERSITY; DIVERSITY INDEX; ENDEMISM; EVOLUTIONARY BIOLOGY; FOREST ECOSYSTEM; FUNCTIONAL CHANGE; HABITAT SELECTION; NEOTROPIC ECOZONE; NICHE; PHYLOGENETICS; SPECIATION (BIOLOGY); SUBTROPICAL REGION;

AMAZONIA; GUYANA SHIELD;

ANIMALIA; BURSERACEAE; PAGAMEA; PROTIUM; RUBIACEAE;

EID: 84956639309     PISSN: 00063606     EISSN: 17447429     Source Type: Journal    
DOI: 10.1111/btp.12301     Document Type: Article

References (93)

1. Adeney, J. M., N. Christensen, A. Vincenti, and M. Cohn-Haft . 2016. White-sand ecosystems in Amazonia. Biotropica 48: 7-23.
2. Álvarez Alonso, J., M. R. Metz, and P. V. A. Fine . 2013. Habitat specialization by birds in western Amazonian white-sand forests. Biotropica 45: 365-372.
3. Álvarez Alonso, J., and B. M. Whitney . 2003. Eight new bird species for Peru and other distributional records from white-sand forests of northern Peruvian Amazon, with implications for biogeography of northern South America. Condor 105: 552-566.
4. Anderson, A. B. 1981. White-sand vegetation of Brazilian Amazonia. Biotropica 13: 199-210.
5. Banki, O. S. 2010. Does neutral theory explain community composition in the Guiana Shield forests? Ph.D. thesis. Utrecht University, The Netherlands.
6. Baraloto, C., D. Bonal, and D. E. Goldberg . 2006. Differential growth response to soil resource gradients among nine tropical tree species. J. Trop. Ecol. 22: 487-497.
7. Baraloto, C., S. Rabaud, Q. Molto, L. Blanc, C. Fortunel, B. Hérault, N. Dávila, I. Mesones, M. Ríos, E. Valderrama, and P. V. A. Fine . 2011. Disentangling stand and environmental correlates of aboveground biomass in Amazonian forests. Glob. Change Biol. 17: 2677-2688.
8. Barbosa, C. E. A., T. Misiewicz, P. V. A. Fine, and F. Costa . 2013. Plant ontogeny, spatial distance, and soil type influences negative density-dependent effects on a common Amazonian tree. PLoS One 8: e62639.
9. Borges, S. H., M. Moreira, C. Ribas, M. Cohn-Haft, J. M. Capurucho, C. Vargas, and R. Almeida . 2016. Bird communities in Amazonian white-sand vegetation patches: Effects of landscape structure and biogeographic context. Biotropica 48: 121-131.
10. Boubli, J. P. 2002. Lowland floristic assessment of Pico da Neblina National Park, Brazil. Plant Ecol. 160: 149-167.
11. Boyd, I. L., P. H. Freer-Smith, C. A. Gilligan, and H. C. J. Godfray . 2013. The consequence of tree pests and diseases for ecosystem services. Science 342: 1235773.
12. Brearley, F. Q., P. V. A. Fine, and K. Perreijn . 2011. Nitrogen isotope ratios suggest tropical heath forests are more limited by nitrogen than water availability. Acta Amazon 41: 409-412.
13. Chave, J., D. Navarrete, S. Almeida, E. Álvarez, L. E. O. C. Aragão, D. Bonal, P. Châtelet, J. E. Silva-Espejo, J.-Y. Goret, P. von Hildebrand, E. Jiménez, S. Patiño, M. C. Peñuela, O. L. Phillips, P. Stevenson, and Y. Malhi . 2010. Regional and seasonal patterns of litterfall in tropical South America. Biogeosciences 7: 43-55.
14. Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr. 53: 209-233.
15. Comita, L. S., H. C. Muller-Landau, S. Aguilar, and S. P. Hubbell . 2010. Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329: 330-332.
16. Connell, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In P. J. den Boer, and G. R. Gradwell (Eds.). Dynamics of populations, pp. 298-312. Centre for Agricultural Publication and Documentation, Wageningen, The Netherlands.
17. Coomes, D. A., and P. J. Grubb . 1996. Amazonian caatinga and related communities at La Esmeralda, Venezuela: Forest structure, physiognomy and floristics, and control by soil factors. Vegetatio 122: 167-191.
18. Coomes, D. A., and P. J. Grubb . 1998. Responses of juvenile trees to above- and belowground competition in nutrient-starved Amazonian rain forest. Ecology 79: 768-782.
19. Daly, D. C., and P. V. A. Fine . 2011. A new Amazonian section of Protium (Burseraceae) including both edaphic specialist and generalist taxa. Studies in Neotropical Burseraceae XVI. Syst. Bot. 36: 939-949.
20. Damasco, G., A. Vicentini, C. V. Castilho, T. P. Pimentel, and H. E. M. Nascimento . 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. J. Veg. Sci. 24: 384-394.
21. De Caceres, M., P. Legendre, and M. Moretti . 2010. Improving indicator species analysis by combining groups of sites. Oikos 119: 1674-1684.
22. Dufrene, M., and P. Legendre . 1997. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol. Monogr. 67: 345-366.
23. Duivenvoorden, J. F., and J. M. Lips . 1995. A land-ecological study of soils, vegetation, and plant diversity in Colombian Amazonia. Tropenbos, Wageningen, The Netherlands.
24. Endler, J. A. 1982. Pleistocene refuges, fact or fancy? In G. T. Prance (Ed.). Biological diversification in the tropics, pp. 641-657. Columbia University Press, New York.
25. Fine, P. V. A., D. C. Daly, F. G. Villa, I. Mesones, and K. Cameron . 2005. The contribution of edaphic heterogeneity to the evolution and diversity of Burseraceae trees in the Western Amazon. Evolution 59: 1464-1478.
26. Fine, P. V. A., R. García-Villacorta, N. C. A. Pitman, I. Mesones, and S. W. Kembel . 2010. A floristic study of the white-sand forests of Peru. Ann. MO. Bot. 97: 283-305.
27. Fine, P. V. A., and S. W. Kembel . 2011. Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34: 552-565.
28. Fine, P. V. A., and I. Mesones . 2011. The role of natural enemies in the germination and establishment of Pachira (Malvaceae) trees in the Peruvian Amazon. Biotropica 43: 265-269.
29. Fine, P. V. A., I. Mesones, and P. D. Coley . 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305: 663-665.
30. Fine, P. V. A., M. R. Metz, J. Lokvam, I. Mesones, J. M. Ayarza Zuñiga, G. P. A. Lamarre, M. Vasquez Pilco, and C. Baraloto . 2013b. Insect herbivores, chemical innovation and the evolution of habitat specialization in Amazonian trees. Ecology 94: 1764-1775.
31. Fine, P. V. A., Z. J. Miller, I. Mesones, S. Irazuzta, H. M. Appel, M. H. H. Stevens, I. Sääksjärvi, J. C. Schultz, and P. D. Coley . 2006. The growth-defense tradeoff and habitat specialization by plants in Amazonian forests. Ecology 87: S150-S162.
32. Fine, P. V. A., F. Zapata, and D. C. Daly . 2014. Investigating processes of Neotropical rain forest tree diversification by examining the evolution and historical biogeography of Protieae (Burseraceae). Evolution 68: 1988-2004.
33. Fine, P. V. A., F. Zapata, D. C. Daly, I. Mesones, T. M. Misiewicz, H. F. Cooper, and C. E. A. Barbosa . 2013a. The importance of environmental heterogeneity and spatial distance in generating phylogeographic structure in edaphic specialist and generalist species of Protium (Burseraceae) across the Amazon basin. J. Biogeogr. 60: 646-661.
34. Fortunel, C., P. V. A. Fine, and C. Baraloto . 2012. Leaf, stem and root tissue strategies across 758 Neotropical tree species. Funct. Ecol. 26: 1153-1161.
35. Fortunel, C., C. T. E. Paine, P. V. A. Fine, N. J. B. Kraft, and C. Baraloto . 2014a. Environmental factors predict community functional composition in forests across Amazonia. J. Ecol. 102: 145-155.
36. Fortunel, C., J. Ruelle, J. Beuchene, P. V. A. Fine, and C. Baraloto . 2014b. Wood specific gravity and anatomy of branches and roots in 113 Amazonian rainforest tree species across environmental gradients. New Phytol. 202: 79-94.
37. Frasier, C. L., V. A. Albert, and L. Struwe . 2008. Amazonian lowland, white sand areas as ancestral regions for South American biodiversity: Biogeographic and phylogenetic patterns in Potalia (Angiospermae: Gentianaceae). Org. Divers. Evol. 8: 44-57.
38. Fyllas, N. M., S. Patino, T. R. Baker, G. Bielefeld Nardoto, L. A. Martinelli, C. A. Quesada, R. Paiva, M. Schwarz, V. Horna, L. M. Mercado, A. Santos, L. Arroyo, E. M. Jimenez, F. J. Luizao, D. A. Neill, N. Silva, A. Prieto, A. Rudas, M. Silviera, I. C. G. Vieira, G. Lopez-Gonzalez, Y. Malhi, O. L. Phillips, and J. Lloyd . 2009. Basin-wide variations in foliar properties of Amazonian forest: Phylogeny, soils and climate. Biogeosciences 6: 2677-2708.
39. García Villacorta, R., M. Ahuite, and M. Olórtegui . 2003. Clasificación de bosques sobre arena blanca de la zona reservada Allpahuayo-Mishana. Folia Amaz. 14: 11-31.
40. Gentry, A. H. 1981. Distributional patterns and an additional species of the Passiflora vitifolia complex: Amazonian species diversity due to edaphically differentiated communities. Plant Syst. Evol. 137: 95-105.
41. Gentry, A. H. 1986. Endemism in tropical versus temperate plant communities. In M. E. Soulé (Ed.). Conservation biology: The science of scarcity and diversity, pp. 153-181. Sinauer, Sunderland, Massachusetts.
42. Givnish, T. J. 1979. On the adaptive significance of leaf form. In O. T. Solbrig, S. Jain, G. B. Johnson, and P. H. Raven (Eds.). Topics in plant population biology, pp. 375-407. Columbia University Press, New York.
43. Givnish, T. J. 1999. On the causes of gradients in tropical tree diversity. J. Ecol. 87: 193-210.
44. Glennon, K. L., L. J. Rissler, and S. A. Church . 2012. Ecogeographic isolation: A reproductive barrier between species and between cytotypes in Houstonia (Rubiaceae). Evol. Ecol. 26: 909-926.
45. Grubb, P. J., and D. A. Coomes . 1997. Seed mass and nutrient content in nutrient-starved tropical rainforest in Venezuela. Seed Sci. Res. 7: 269-280.
46. Guevara, J. E., G. Damasco, C. Baraloto, P. V. A. Fine, M. C. Peñuela-Mora, C. Castilho, A. Vincentini, D. Cárdenas, F. Wittmann, N. Targhetta, O. L. Phillips, J. Stropp, I. Amaral, P. Maas, A. Monteagudo, E. M. Jimenez, R. Thomas, R. Brienen, A. Duque, W. Magnusson, J. Ferreira, E. Honorio, F. de Almeida Matos, F. Ramírez Arevalo, J. Engel, P. Petronelli, R. Vasquez, and H. ter Steege . 2016. Low phylogenetic beta diversity and geographic neo-endemism in Amazonian white-sand forests. Biotropica 48: 34-46.
47. Hammond, D. S. 2005. Ancient land in a modern world. In D. S. Hammond (Ed.). Tropical forests of the Guiana Shield: Ancient forests in a modern world, pp. 1-14. CABI publishing, Wallingford, U.K.
48. Hoorn, C. 1993. Marine incursions and the influence of Andean tectonics on the Miocene depositional history of northwestern Amazonia: Results of a palynostratigraphic study. Palaeogeogr. Palaeoclimatol. Palaeoecol. 105: 267-309.
49. Hoorn, C., F. P. Wesselingh, H. ter Steege, M. A. Bermudez, A. Mora, J. Sevink, I. Sanmartín, A. Sanchez-Meseguer, C. L. Anderson, J. P. Figueiredo, C. Jaramillo, D. Riff, F. R. Negri, H. Hooghiemstra, J. Lundberg, T. Stadler, T. Särkinen, and A. Antonelli . 2010. Amazonia through time: Andean uplift, climate change, landscape evolution and biodiversity. Science 330: 927-931.
50. Janzen, D. H. 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104: 501-528.
51. Janzen, D. H. 1974. Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6: 69-103.
52. Jørgensen, P., and S. Léon-Yánez . 1999. Catalogue of the vascular plants of Ecuador, Missouri Botanical Garden Press, Monogr. Syst. Bot. MO Bot. Gard. 75.
53. Kay, K. M., K. L. Ward, L. R. Watt, and D. W. Schemske . 2011. Plant speciation. In S. P. Harrison, and N. Rajakaruna (Eds.). Serpentine: The evolution and ecology of a model system, pp. 71-95. University of California Press, Berkeley, California.
54. Kelloff, C. L., and V. A. Funk . 2004. Phytogeography of the Kaieteur Falls, Potaro Plateau, Guyana: Floral distributions and affinities. J. Biogeogr. 31: 501-513.
55. Konno, K. 2011. Plant latex and other exudates as plant defense systems: Roles of various defense chemicals and proteins contained therein. Phytochemistry 72: 1510-1530.
56. Lamarre, G. P. A., C. Baraloto, C. Fortunel, N. Dávila, I. Mesones, J. Grandez Ríos, M. Ríos, E. Valderrama, M. Vasquez, and P. V. A. Fine . 2012. Herbivory, growth rates, and habitat specialization in tropical tree lineages: Implications for Amazonian beta-diversity. Ecology 93: S195-S210.
57. Lamarre, G. P. A., B. Hérault, I. Mesones, P. V. A. Fine, and C. Baraloto . In press. Taxonomic and functional composition of arthropod assemblages across Amazonian forests. J. Anim. Ecol. doi: 10.1111/1365-2656.12445.
58. Latrubesse, E. M., M. Cozzuol, S. A. F. da Silva-Caminha, C. A. Rigsby, M. L. Absy, and C. Jaramillo . 2010. The late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system. Earth Sci. Rev. 99: 99-124.
59. Liang, M., X. Liu, R. S. Etienne, F. Huang, Y. Wang, and S. Yu . 2015. Arbuscular mycorrhizal fungi counteract the Janzen-Connell effect of soil pathogens. Ecology 96: 562-574.
60. Lokvam, J., and P. V. A. Fine . 2012. An oxidized squalene derivative from Protium subserratum (Engl.) Engl. growing in Peru. Molecules 17: 7451-7457.
61. Lokvam, J., M. R. Metz, G. R. Takeoka, L. Nguyen, and P. V. A. Fine . 2015. Habitat-specific divergence of procyanidins in Protium subserratum (Burseraceae). Chemoecology 25: 293-302.
62. Mangan, S. A., S. A. Schnitzer, E. A. Herre, K. M. L. Mack, M. C. Valencia, E. I. Sanchez, and J. D. Bever . 2010. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466: 752-755.
63. Medina, E., and E. Cuevas . 1989. Patterns of nutrient accumulation and release in Amazonian forests of the upper Rio Negro basin. In J. Proctor (Ed.). Mineral nutrients in tropical forest and savanna ecosystems, pp. 217-240. Blackwell Scientific, Oxford.
64. Misiewicz, T. M. 2014. Ecological divergence and reproductive isolation in an Amazonian tropical tree: Protium subserratum (Burseraceae). PhD dissertation, University of California, Berkeley.
65. Misiewicz, T. M., and P. V. A. Fine . 2014. Evidence for ecological divergence across a mosaic of soil types in an Amazonian tropical tree: Protium subserratum (Burseraceae). Mol. Ecol. 23: 2543-2558.
66. Misiewicz, T. M., E. Kraichak, and C. Rasmussen . 2014. Distance and habitat drive fine scale stingless bee (Hymenoptera: Apidae) community turnover across naturally heterogeneous forests in the western Amazon. Sociobiology 61: 407-414.
67. Neill, D. A., and M. Asanza . 2012. Lozania nunkui (Lacistemataceae), a new species from the sandstone plateaus of the Cordillera del Condor in Ecuador and Peru. Novon 22: 207-211.
68. de Oliveira, A. A., A. Vicentini, J. Chave, C. D. T. Castanho, S. J. Davies, A. M. Z. Martini, R. A. F. Lima, R. R. Ribeiro, A. Iribar, and V. C. Souza . 2014. Habitat specialization and phylogenetic structure of tree species in a coastal Brazilian white-sand forest. J. Plant Ecol. 7: 134-144.
69. Paine, C. E. T., N. Norden, J. Chave, C. Fortunel, P.-M. Forget, and C. Baraloto . 2012. Phylogenetic density dependence and environmental filtering predict seedling survival in a tropical forest. Ecol. Lett. 15: 34-41.
70. Patiño, S., J. Lloyd, R. Paiva, T. R. Baker, C. A. Quesada, L. M. Mercado, J. Schmerler, M. Schwarz, A. J. B. Santos, A. Aguilar, C. I. Czimczik, J. Gallo, V. Horna, E. J. Hoyos, E. M. Jimenez, W. Palomino, J. Peacock, A. Peña-Cruz, C. Sarmiento, A. Sota, J. D. Turriago, B. Villanueva, P. Vitzthum, E. Alvarez, L. Arroyo, C. Baraloto, D. Bonal, J. Chave, A. C. L. Costa, R. Herrera, N. Higuchi, T. Killeen, E. Leal, F. Luizão, P. Meir, A. Monteagudo, D. Neil, P. Nuñez-Vargas, M. C. Peñuela, N. Pitman, N. Priante Filho, A. Prieto, S. N. Panfil, A. Rudas, R. Salomão, N. Silva, M. Silveira, S. Soares deAlmeida, A. Torres-Lezama, R. Vasquez-Martinez, I. Vieira, Y. Malhi, and O. L. Phillips . 2009. Branch xylem density variations across the Amazon Basin. Biogeosciences 6: 545-568.
71. Peay, K. G., C. Baraloto, and P. V. A. Fine . 2013. Strong coupling of plant and fungal community structure across Amazonian rainforests. ISME J. 7: 1852-1861.
72. Peñuela-Mora, M. C. 2014. Understanding Colombian Amazonian white sand forests. Ph.D. thesis. Utrecht University, The Netherlands.
73. Proctor, J. 1999. Heath forests and acid soils. Bot. J. Scot. 51: 1-14.
74. Quesada, C. A., J. Lloyd, L. O. Anderson, N. M. Fyllas, M. Schwarz, and C. I. Czimczik . 2011. Soils of Amazonia with particular reference to the RAINFOR sites. Biogeosciences 8: 1415-1440.
75. Rossetti, D. F., T. C. Bertani, H. Zani, E. H. Cremon, and E. H. Hayakawa . 2012. Late quaternary sedimentary dynamics in Western Amazonia: Implications for the origin of open vegetation/forest contrasts. Geomorphology 177: 74-92.
76. Roy, M., H. Schimann, R. Braga-Neto, R. A. E. Da Silva, J. Duque, D. Frame, F. Wartchow, and M.-A. Neves . 2016. Diversity and distribution of ectomycorrhizal fungi in Amazonian lowland white-sand forests. Biotropica 48: 90-100.
77. Ruokolainen, K., A. Linna, and H. Tuomisto . 1997. Use of Melastomataceae and pteridophytes for revealing phytogeographical patterns in Amazonian rain forests. J. Trop. Ecol. 13: 243-256.
78. Schulman, L. 2003. A geo-ecologically specialised new species of Adelobotrys (Melastomataceae: Merianieae) from Peruvian Amazonia. Kew. Bull. 58: 459-466.
79. Silver, W. L., J. Neff, M. Mcgroddy, E. Veldkamp, M. Keller, and R. Cosme . 2000. Effects of soil texture on belowground carbon and nutrient storage in a lowland Amazonian forest ecosystem. Ecosystems 3: 193-209.
80. ter Steege, H., V. G. Jetten, A. M. Polak, and M. J. A. Werger . 1993. Tropical rain-forest types and soil factors in a watershed area in Guyana. J. Veg. Sci. 4: 705-716.
81. ter Steege, H., D. Sabatier, H. Castellanos, T. Van Andel, J. Duivenvoorden, A. A. de Oliveira, R. Ek, R. Lilwah, P. Maas, and S. Mori . 2000. An analysis of the floristic composition and diversity of Amazonian forests including those of the Guiana Shield. J. Trop. Ecol. 16: 801-828.
82. ter Steege, H., N. C. A. Pitman, D. Sabatier, C. Baraloto, R. P. Salomão, J. E. Guevara, O. L. Phillips, C. V. Castilho, W. E. Magnusson, J.-F. Molino, A. Monteagudo, P. Núñez Vargas, J. C. Montero, T. R. Feldpausch, E. N. H. Coronado, T. J. Killeen, B. Mostacedo, R. Vasquez, R. L. Assis, J. Terborgh, F. Wittmann, A. Andrade, W. F. Laurance, S. G. W. Laurance, B. S. Marimon, B.-H. Marimon, I. C. Guimarães Vieira, I. L. Amaral, R. Brienen, H. Castellanos, D. Cárdenas López, J. F. Duivenvoorden, H. F. Mogollón, F. D. D. A. Matos, N. Dávila, R. García-Villacorta, P. R. Stevenson Diaz, F. Costa, T. Emilio, C. Levis, J. Schietti, P. Souza, A. Alonso, F. Dallmeier, A. J. D. Montoya, M. T. Fernandez Piedade, A. Araujo-Murakami, L. Arroyo, R. Gribel, P. V. A. Fine, C. A. Peres, M. Toledo, C. G. A. Aymard, T. R. Baker, C. Cerón, J. Engel, T. W. Henkel, P. Maas, P. Petronelli, J. Stropp, C. E. Zartman, D. Daly, D. Neill, M. Silveira, M. R. Paredes, J. Chave, D. D. A. Lima Filho, P. M. Jørgensen, A. Fuentes, J. Schöngart, F. Cornejo Valverde, A. Di Fiore, E. M. Jimenez, M. C. Peñuela Mora, J. F. Phillips, G. Rivas, T. R. van Andel, P. von Hildebrand, B. Hoffman, E. L. Zent, Y. Malhi, A. Prieto, A. Rudas, A. R. Ruschell, N. Silva, V. Vos, S. Zent, A. A. Oliveira, A. C. Schutz, T. Gonzales, M. Trindade Nascimento, H. Ramirez-Angulo, R. Sierra, M. Tirado, M. N. Umaña Medina, G. van der Heijden, C. I. A. Vela, E. Vilanova Torre, C. Vriesendorp, O. Wang, K. R. Young, C. Baider, H. Balslev, C. Ferreira, I. Mesones, A. Torres-Lezama, L. E. Urrego Giraldo, R. Zagt, M. N. Alexiades, L. Hernandez, I. Huamantupa-Chuquimaco, W. Milliken, W. Palacios Cuenca, D. Pauletto, E. Valderrama Sandoval, L. Valenzuela Gamarra, K. G. Dexter, K. Feeley, G. Lopez-Gonzalez, and M. R. Silman . 2013. Hyperdominance in the Amazonian tree flora. Science 342: 1243092.
83. Stropp, J., P. van der Sleen, P. A. Assunçao, A. L. da Silva, and H. ter Steege . 2011. Tree communities of white-sand and terra-firme forests of the upper Rio Negro. Acta Amazon 41: 521-543.
84. Stropp, J., P. van der Sleen, C. A. Quesada, and H. ter Steege . 2013. Herbivory and habitat association of tree seedlings in lowland evergreen rainforest on white-sand and terra-firme in the upper Rio Negro. Plant Ecol. Div. 7: 255-265.
85. Tabarelli, M., C. A. Peres, and F. P. Melo . 2012. The 'few winners and many losers' paradigm revisited: Emerging prospects for tropical forest biodiversity. Biol. Conserv. 155: 136-140.
86. Terborgh, J. 2012. Enemies maintain hyperdiverse tropical forests. Am. Nat. 179: 303-314.
87. Tuomisto, H., K. Ruokolainen, R. Kalliola, A. Linna, W. Danjoy, and Z. Rodriguez . 1995. Dissecting Amazonian biodiversity. Science 269: 63-66.
88. Tuomisto, H., K. Ruokolainen, and M. Yli-Halla . 2003. Dispersal, environment, and floristic variation of Western Amazonian forests. Science 299: 241-244.
89. Vanzolini, P. E., and E. E. Williams . 1981. The vanishing refuge: A mechanism for ecogeographic speciation. Pap. Avulsos Zool. 34: 251-255.
90. Vicentini, A. 2016. The evolutionary history of Pagamea (Rubiaceae), a white-sand specialist lineage in tropical South America. Biotropica 48: 58-69.
91. Vormisto, J., O. L. Phillips, K. Ruokolainen, H. Tuomisto, and R. Vásquez . 2000. A comparison of fine-scale distribution patterns of four plant groups in an Amazonian forest. Ecography 23: 349-359.
92. Vriesendorp, C. M., N. C. A. Pitman, J. Rojas, B. Pawlak, L. Rivera, L. Calixto, M. Vela, and P. Fasabi (Eds.). 2006. Perú: Matsés. Rapid Biological Inventories Report 16. The Field Museum of Natural History, Chicago.
93. Wiens, J. J., D. D. Ackerly, A. P. Allen, B. L. Anacker, L. B. Buckley, H. V. Cornell, E. I. Damschen, T. J. Davies, J. A. Grytnes, and S. P. Harrison . 2010. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol. Lett. 10: 1310-1324.