Phylogeography and phylogenetic diversity of Amazon tree species and communities Eurídice Nora Honorio Coronado Submitted in accordance with the requirements for the degree of Doctor in Philosophy The University of Leeds School of Geography May, 2013 The candidate confirms that the work submitted is her own and that appropriate credit has been given where reference has been made to the work of others. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. © 2013 The University of Leeds and Eurídice Nora Honorio Coronado -ii- Acknowledgements This work was undertaken at the University of Leeds and at the Royal Botanic Garden Edinburgh (RBGE), and funded by a FINCyT studentship of the Peruvian Government (LASPAU student ID Number: 20090402), the School of Geography, University of Leeds and the Davis Expedition Fund. I am grateful to my supervisors Prof. Toby Pennington at Edinburgh and Prof. Oliver Phillips at Leeds who led me through the PhD, and for their comments and contributions to improve my research. Other external supervisors were Kyle Dexter from University of Edinburgh and Peter Hollingworth from RBGE who contributed with the discussion of my results. Thanks also to Simon Lewis and Manuel Gloor, who were part of my research support group at Leeds, for their questions about hypotheses, methods and analyses. This thesis was only possible because of the guidance of Prof. Toby Pennington and his team from RBGE who introduced me to the fascinating world of DNA extraction and sequencing and gave me assistance in using the molecular lab, library, computers and programmes. I am thankful to Alan Forrest, Michelle Hollingworth and Ruth McGregor for training and assistance during the molecular lab work. I would like to thank Dennis del Castillo from the Instituto de Investigaciones de la Amazonía Peruana (IIAP) who gave me his unconditional support in pursuing my studies abroad and for letting me spent this time in the UK. I am also thankful to Kyle Dexter and Nikée Groot for their patience to teach me useful tools in R Statistical Software. Fieldwork was a key component of chapter 2 and 3 and this was only possible thanks to all those people who worked with me in the forests of Ecuador, Peru and Bolivia. I am grateful to Pablo Alvez, Tim Baker, Aniceto Daza, Julio Irarica, Miguel Luza, Antonio Peña, Diego Rojas, Hugo Vasquez, Meison Vega, and J. Yalder for climbing nearly one thousand trees. Thanks also to Alejandro Araujo, Luzmila Arroyo, Stephan Beck, Roel Brienen, Abel Monteagudo, Carlos Reynel, and Guido Vasquez for helpful information in planning the fieldtrips and to the field stations and their station managers for logistical support. I am also thankful to Monica Poelchau, Kyle Dexter, Abel Monteagudo, Otilene dos Anjos, Ricardo Zárate, Jose Luis Marcelo, Chris Dick, William Farfán, Sanda Patiño, and Miguel -i- Luza for kindly sharing fresh leaves, herbarium specimens or sequences for some of the study species (see Appendix S2.1 and Appendix S3.2). During field work, I also collected soil samples for each of my tree species. Soil analysis was possible with the training received from Rachel Gasior at the laboratory of the School of Geography, University of Leeds. David Ashley kindly helped me running the analysis of concentration of cations using the ICP machine. In chapter 4, I analysed the floristic composition of a large number of permanent forest plots, a long-term dataset that was kindly shared by several collaborators of the Amazon Forest Inventory Network (RAINFOR). Fieldwork to support this network has been funded by the Gordon and Betty Moore Foundation and the Natural Environment Research Council. International and national organisations involved include University of Leeds, University of Oxford, University of Kent (UK), Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique (France), Naturalis Biodiversity Center Leiden, Wageningen University (Netherlands), James Cook University (Australia), Duke University, National Park Service Fredericksburg, Conservation International (USA), Herbario Universitario, Instituto de Investigaciones para el Desarrollo Forestal, Universidad de Los Andes (Venezuela), Jardín Botánico de Medellín, Universidad Nacional de Colombia (Colombia), Universidad Estatal Amazónica, Universidad Técnica del Norte (Ecuador), Andes Biodiversity and Ecosystem Research Group, Instituto de Investigaciones de la Amazonía Peruana, Jardín Botánico Missouri Oxapampa, Universidad de la Amazonía Peruana, Universidad Nacional San Antonio Abad del Cusco (Peru), Instituto Boliviano de Investigacion Forestal, Museo de Historia Natural Noel Kempff Mercado, Universidad Autónoma del Beni (Bolivia), Embrapa Amazonia Oriental, Instituto Nacional de Pesquisas da Amazônia, Museu Paraense Emílio Goeldi, Tropical Ecology Assessment and Monitoring Network, CNPq/PELD 558069/2009-6/Universidade do Estado de Mato Grosso, Universidade Federal do Acre (Brazil). Thanks also to Gabriela López-Gonzalez for her work curating and managing the ForestPlots database and for helping me with the queries to access the floristic data. Research permits for the molecular work were provided by the Ministerio de Medio Ambiente y Agua in Bolivia (SERNAP-DMA-CAR-1232/10) and the Direccion General Forestal y de Fauna Silvestre in Peru (Resolucion Directorial № 281-2010-AG-DGFFS- -ii- DGEFFS). Several other research permits have been granted to national and international collaborators in different Amazonian countries for fieldwork in RAINFOR plots. During my lab work at the RBGE, I spent great moments with my friends in Edinburgh. I would like to thank Boni, Rocio, Maca, Natalia, Nikki, Tony, Jal, Andreas, and Kyle for sharing with me so many wonderful moments, trips, parties and pub times. At Leeds, I am grateful to my friend Lina who has always been so positive about this project and for understanding my busy days and for sharing so many nice moments. I would also like to thanks the researchers and students at the University of Leeds who were also interested in my project. I want also to thank Tim Baker, my husband, who gave me support and took care of me during my PhD, and for listening so many times to my results and interpretation of the data. Finally, I thank my mother who believed I was able to complete this project, and all my family in Peru who have always encouraged my professional development. -iii- -iv- Abstract The Amazon rain forest is the most diverse ecosystem on Earth, harbouring more than ten thousand tree species. In this project, I used ecological and molecular information to explore how ecological factors and historical events have determined the species distributions and population genetic structure of tree species and the phylogenetic diversity of tree communities in the Amazon rain forest. Chapter 2 indicates that seasonally dry vegetation in northern South America represents a barrier to migration for Ficus insipida (Moraceae) and other wet-adapted Amazonian tree species as they have different plastid haplotypes restricted to Mesoamerica and Amazonia. Conversely, the ability of some pioneer species to survive seasonal drought may explain the weakly differentiated phylogeographic structure within these species, with some haplotypes occurring on both sides of this barrier. Chapter 3 explores whether patterns of population genetic structure in five widespread western Amazonian tree species are consistent with historical explanations. My results show that the genetic patterns among species are not entirely congruent suggesting that tropical rain forest species respond differently to long-term geological and climatic changes. Despite this, some tentative generalisations emerge, notably high genetic diversity and a strong geographic structure for plastid sequences suggesting long-term population stability across western Amazonia, and recent population expansions in the south-western Amazon. Chapter 4 uses 283 floristic inventories from the RAINFOR plot network to explore patterns of phylogenetic diversity across Amazonia. This study reveals that the species-rich communities of central Amazonia are dominated by phylogenetic close relatives compared to the equally species- rich communities of the north-west that tend to contain more distantly related species. Across Amazonia, an east-west gradient of the abundance of early divergent angiosperm clades was found, with the greatest percentage of tree species of Magnoliids and Monocots in the west. As these early diverging clades are also characteristic of pre- montane habitats, these results suggest that migration events from cooler environments at different geological times has played an important role in the assemblage of the most phylogenetically diverse communities in Amazonia. -v- The findings from these three chapters corroborate the notion that both ecological factors and historical events have been important in determining species distributions and the phylogenetic diversity of tropical tree communities in Amazonia. Regional differences in genetic structure among populations, and phylogenetic diversity among communities, should both be taken into account in forest conservation planning and management. -vi- Table of Contents ACKNOWLEDGEMENTS .................................................................................................................... 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