Incorporating phylogenetic information for the definition of floristic districts in hyperdiverse Amazon forests: Implications for conservation

Abstract

Using complementary metrics to evaluate phylogenetic diversity can facilitate the delimitation of floristic units and conservation priority areas. In this study, we describe the spatial patterns of phylogenetic alpha and beta diversity, phylogenetic endemism, and evolutionary distinctiveness of the hyperdiverse Ecuador Amazon forests and define priority areas for conservation. We established a network of 62 one-hectare plots in terra firme forests of Ecuadorian Amazon. In these plots, we tagged, collected, and identified every single adult tree with dbh ≥10 cm. These data were combined with a regional community phylogenetic tree to calculate different phylogenetic diversity (PD) metrics in order to create spatial models. We used Loess regression to estimate the spatial variation of taxonomic and phylogenetic beta diversity as well as phylogenetic endemism and evolutionary distinctiveness. We found evidence for the definition of three floristic districts in the Ecuadorian Amazon, supported by both taxonomic and phylogenetic diversity data. Areas with high levels of phylogenetic endemism and evolutionary distinctiveness in Ecuadorian Amazon forests are unprotected. Furthermore, these areas are severely threatened by proposed plans of oil and mining extraction at large scales and should be prioritized in conservation planning for this region.

REFERENCES APG III (2009). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society, 161, 105–121. Bass, S. M., Finner, M., Jenkins, C. N., Kreft, H., Cisneros-Heredia, D. F., McCraken, S., … Kunz, T. H. (2010). Global conservation significance of Ecuador's Yasunı′ National Park. PLoS One, 5(1), 1–22. Bernal, C., Christophoul, F., Darrozes, J., Soula, J.-C., Baby, P., & Burgos, J. (2011). Late Glacial and Holocene avulsions of the Rio Pastaza Megafan (Ecuador–Peru): frequency and controlling factors. International Journal of Earth Sciences, 100, 1759–1782. Bryant, J. A., Lamanna, C., Morlon, H., Kerkhoff, A. J., Enquist, B., & Green, J. (2008). Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity. Proceedings of the National Academy of Science of the USA, 105, 11505–11511. Cadotte, M. W., & Davies, T. J. (2010). Rarest of the rare: Advances in combining evolutionary distinctiveness and scarcity to inform conservation at biogeographical scales. Diversity and Distributions, 16, 376–385. Cadotte, M. W., Davies, T. J., Regetz, J., Kembel, S. W., Cleland, E., & Oakley, T. H. (2010). Phylogenetic diversity metrics for ecological communities: Integrating species richness, abundance and evolutionary history. Ecology Letters, 13, 96–105. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates. Dexter, K., Lavin, M., Torke, B. M., Twyford, A. D., Kursar, T. A., Coley, P. D., … Pennington, T. R. (2017). Dispersal of rain forest tree communities across the Amazon basin. Proceedings of the National Academy of Sciences of the USA, 114, 2645–2650. De Oliveira, A., & Daly, D. (1999). Geographic distribution of tree species occurring in the region of Manaus, Brazil: implications for regional diversity and conservation. Biodiversity & Conservation, 8(9), 1245–1259. De Oliveira, A., & Mori, S. (1999). A central Amazonia terra firme forest. I. High tree species richness on poor soils. Biodiversity & Conservation, 8, 1219–1244. Duque, A., Sánchez, M., Cavelier, J., & Duivenvoorden, J. F. (2002). Different floristic patterns of woody understorey and canopy plants in Colombian Amazonia. Journal of Tropical Ecology, 18, 499–525. Faith, D. P. (1992). Conservation evaluation and phylogenetic diversity. Biological Conservation, 61, 1–10. Ferrier, S., Manion, G., Elith, J., & Richardson, K. (2007). Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Diversity and Distributions, 13, 252–264. https://doi.org/10.1111/j.1472-4642.2007.00341 Fine, P. V. A., & Baraloto, C. (2016). Habitat Endemism in white-sand forests: Insights into the mechanisms of lineage diversification and community assembly of the Neotropical Flora. Biotropica, 48, 24–33. Fine, P. V. A., Garcia Villacorta, R., Pitman, N. C. A., Mesones, I., & Kembel, S. (2010). A floristic study of the white sand forests of Peru. Annals of the Missouri Botanical Garden, 97, 283–305. Fine, P. V. A., Zapata, F., Daly, D., Mesones, I., Misiewicz, T., Cooper, H., & Barbosa, C. E. (2013). The importance of environmental heterogeneity and spatial distance in generating phylogeographic structure in edaphic specialist and generalist tree species of Protium (Burseraceae) across the Amazon Basin. Journal of Biogeography, 40, 646–661. https://doi.org/10.1111/j.1365-2699.2011.02645 Finer, M., & Jenkins, C. (2012). Proliferation of hydroelectric dams in the Andean Amazon and implications for Andes-Amazon connectivity. PLoS One, 7(4), e35126. Finer, M., Jenkins, C. N., Pimm, S. L., Keane, B., & Ross, C. (2008). Oil and gas projects in the western Amazon: Threats to wilderness, biodiversity, and indigenous peoples. PLoS One, 3, e2932. Forest, F., Grenyer, R., Rouget, M., Davies, T. J., Cowling, R. M., Faith, D. P., … Savolainen, V. (2007). Preserving the evolutionary potential of floras in biodiversity hotspots. Nature, 445, 757–760. Funk, W. C., Caminer, M., & Ron, S. (2012). High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society of London, B, Biological Sciences, 279, 1806–1814. Gotelli, N. (2000). Null model analysis of species co-occurrence patterns. Ecology, 81(9), 2606–2621. Graham, C. H., & Fine, P. V. A. (2008). Phylogenetic beta diversity: Linking ecological and evolutionary processes across space in time. Ecology Letters, 11, 1265–1277. Graham, C. H., Parra, J. L., Rahbeck, C., & Mcguire, J. A. (2009). Phylogenetic structure in tropical hummingbird communities. Proceedings of the National Academy of Sciences of the USA, 106, 19673–19678. Guevara, J. E., Mogollon, H., Pitman, N. C. A., Ceron, C., Palacios, W., & Neill, D. (2016a). In press. A floristic assessment of the Ecuador Amazon tree flora. In R. W. Myster (Ed.), Forest structure, function and dynamics in Western Amazonia (pp. 27–52). Chichester, UK: John Wiley & Sons Limited. Guevara, J. E., Damasco, G., Baraloto, C., Fine, P. V. A., Peñuela, M. C., Castilho, C., … ter Steege, H. (2016). Low phylogenetic beta diversity and geographic neo-endemism in Amazonian white-sand forests. Biotropica, 48, 34–46. Higgins, M., Ruokolainen, K., Tuomisto, H., Llerena, N., Cardenas, G., Phillips, O., … Rassanen, M. (2011). Geological control of floristic composition in Amazonian forests. Journal of Biogeography, 38, 2136–2149. Honorio Coronado, E., Dexter, K. G., Pennington, R. T., Chave, J., Lewis, S. L., Alexiades, M., … Phillips, O. L. (2015). Phylogenetic diversity of Amazonian tree communities. Diversity and Distribution, 21, 1295–1307. Jetz, W., Thomas, G., Joy, J. B., Redding, D. W., Hartmann, K., & Mooers, A. O. (2014). Global distribution and conservation of evolutionary distinctness in birds. Current Biology, 24, 919–930. Keil, P., Schweiger, O., Kuhn, I., Kuussaari, M., Kunin, W. E., Settele, J., … Storch, D. (2012). Patterns of beta diversity in Europe: the role of climate, land cover and distance across scales. Journal of Biogeography, 39, 1473–1486. Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., … Webb, C. O. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463–1464. Kraft, N. J. B., Baldwin, B. G., & Ackerly, D. (2010). Range size, taxon age and hotspots of neoendemism in the California flora. Diversity and Distribution, 16, 403–413. Kreft, H., & Jetz, W. (2010). A framework for delineating biogeographical regions based on species distributions. Journal of Biogeography, 37, 2029–2053. Laffan, S. W., Lubarsky, E., & Rosauer, D. F. (2010). Biodiverse, a tool for the spatial analysis of biological and related diversity. Ecography, 33, 643–647. Legendre, P., & Legendre, L. (2012). Numerical ecology (3rd ed.). Amsterdam: Elsevier Scientific Publishing Company. Lennon, J. J., Koleff, P., Grenwood, J. J. D., & Gaston, K. J. (2001). The geographical structure of British bird distributions: Diversity, spatial turnover and scale. Journal of Animal Ecology, 70, 966–979. Lennon, J. J., Koleff, P., Grenwoow, J. D., & Gaston, K. J. (2004). Contribution of rarity and commonness to patterns of species richness. Ecology Letters, 7, 81–87. Lessmann, J., Fajardo, K., Munoz, J., & Bonaccorso, E. (2016). Large expansion of oil industry in the Ecuadorian Amazon: Biodiversity vulnerability and conservation alternatives. Ecology and Evolution, 6(14), 4997–5012. Lessmann, J., Munoz, J., & Bonaccorso, E. (2014). Maximizing species conservation in continental Ecuador: A case of systematic conservation planning for biodiverse regions. Ecology and Evolution, 4(12), 2410–2422. Li, R., Kraft, N. J. B., Yang, J., & Wang, Y. (2015). A phylogenetically informed delineation of floristic regions within a biodiversity hotspot in Yunnan, China. Scientific Reports, 5, 9396. Macía, J. M., & Svenning, J. C. (2005). Oligarchic dominance in western Amazonian plant communities. Journal of Tropical Ecology, 21, 613–626. Mielke, P. W. Jr (1991). The application of multivariate permutation methods based on distance functions in the earth sciences. Earth-Science Reviews, 31, 55–71. Ministerio del Ambiente del Ecuador. (2013). Sistema de Clasificación de los Ecosistemas del Ecuador Continental. Quito: Subsecretaría de Patrimonio Natural. Mishler, B. D., Knerr, N., Gonzalez-Orozco, C. E., Thornhill, A., Laffan, S. W., & Miller, J. T. (2014). Phylogenetic measures of biodiversity and neo- and paleo-endemism in Australian Acacia. Nature Communications, 5, 4473. Misiewicz, T., & Fine, P. V. A. (2014). Evidence for ecological divergence across a mosaic of soil types in an Amazonian tropical tree: Protium subserratum (Burseraceae). Molecular Ecology, 23, 2543–2558. Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., … Wagner, H. (2015). vegan: Community Ecology Package. R package version 2.3-0. Orme, C. D. L., Davies, R. G., Burgess, M., Eigenbrod, F., Pickup, N., Olson, V. A., … Owens, I. P. F. (2005). Global hotspots of species richness are not congruent with endemism or threat. Nature, 436, 1016–1019. Pitman, N. C. A. (2000). A large-scale inventory of two Amazonian tree communities. PhD. Thesis. Universidad de Duke, Durham, North Carolina, USA. Pitman, N. C. A., Jorgensen, P. M., Williams, R. S. R., Leon-Yanez, S., & Valencia, R. (2002). Extinction-rate estimates for a modern neotropical flora. Conservation Biology, 16(5), 1427–1431. Pitman, N. C. A., Beltrán, H., Foster, R., García, R., Vriesendorp, C., & Ahuite, M. (2003). Flora y vegetación del valle del río Yavarí. En N. C. Pitman, D. Vriesendorp, & D. Moskovits (Eds.), Perú: Yavarí. Rapid biological inventories report 11 (pp. 52–59). Chicago, IL: The Field Museum press. Pitman, N. C. A., Terborgh, J., Silman, M. R., Nuñez, P. V., Neill, D. A., Cerón, C., … Aulestia, M. (2001). Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology, 82, 2101–2117. Pitman, N. C. A., Mogollón, H., Dávila, N., Ríos, M., García-Villacorta, R., Guevara, J., … Vásquez-Martínez, R. (2008). Tree community change across 700 km of lowland Amazonian forest from the Andean foothills to Brazil. Biotropica, 40(5), 525–654. Pos, E., Guevara Andino, J. E., Sabatier, D., Molino, J.-F., Pitman, N., Mogollón, H., … ter Steege, H. (2014). Are all species necessary to reveal ecologically important patterns? Ecology and Evolution, 4(24), 4626–4636. Qian, H., Swenson, N. G., & Zhan, J. (2013). Phylogenetic beta diversity of angiosperms in North America. Global Ecology and Biogeography, 22, 1152–1161. Räsänen, M. E., Salo, J. E., & Kalliola, R. J. (1987). Fluvial perturbance in the Western Amazon Basin: Regulation by long-term sub-Andean tectonics. Science, 238, 1398–1401. Redding, D. W., & Moers, A. (2006). Incorporating evolutionary measures into conservation prioritization. Conservation Biology, 20(6), 1670–1678. Rosauer, D. F., Laffan, S. W., Crisp, D. M., Donnellan, S. C., & Cook, L. G. (2009). Phylogenetic endemism: A new approach to identifying geographical concentrations of evolutionary history. Molecular Ecology, 18, 4061–4072. Sandel, B., Arge, L., Dalsgaard, B., Davies, R. G., Gaston, K. J., Sutherland, W. J., & Svenning, J.-C. (2011). The influence of late quaternary climate-change velocity on species endemism. Science, 334, 660–664. ter Steege, H., Pitman, N. C. A., Sabatier, D., Baraloto, C., De Paiva Salomao, R., Guevara, J. E., … Silman, M. R. (2013). Hyper dominance in Amazonian tree flora. Science, 342, 1243092. ter Steege, H., Vaessen, R. W., Cárdenas-López, D., Sabatier, D., Antonelli, A., de Oliveira, S. M., … Salomão, R. P. (2016). The discovery of the Amazonian tree flora with an updated checklist of all known tree taxa. Scientific Reports, 6, 29549. Schulte, R. P. O., Lantinga, E. A., & Hawkins, M. J. (2005). A new family of Fisher-curves estimates Fisher's alpha more accurately. Journal of Theoretical Biology, 232, 305–313. Swenson, N. G. (2009). Phylogenetic resolution and quantifying the phylogenetic diversity and dispersion of communities. PLoS One, 4, e4390. Valencia, R., Foster, R. B., Villa, G., Condit, R., Hernández, C., Romoleroux, K., … Balslev, H. (2004). Tree diversity in the Amazon and the contribution of local habitat variation: A large forest plot in eastern Ecuador. Journal of Ecology, 92, 214–229. Webb, C. O. (2000). Exploring the phylogenetic structure of ecological communities: An example for rain forest trees. American Naturalist, 156(145), 155. Webb, C. O., Ackerly, D. D., & Kembel, S. W. (2008). Phylocom: Software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics, 24, 2098–2100. Webb, C. O., & Donoghue, M. J. (2005). Phylomatic: Tree assembly for applied phylogenetics. Molecular Ecology Notes, 5, 181–183. Whittaker, R. J., Araujo, M. B., Paul, J., Ladle, R. J., Watson, J. E. M., & Willis, K. J. (2005). Conservation biogeography: Assessment and prospect. Diversity and Distributions, 11, 3–23. Wikström, N., Savolainen, V., & Chase, M. W. (2001). Evolution of the angiosperms: Calibrating the family tree. Proceedings of the Royal Society of London, B, Biological Sciences, 268, 2211–2220.