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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Integrating molecular biogeography and community ecology to understand the evolution of habitat specialization in Amazonian forests Roosevelt García-Villacorta PhD thesis Doctor of Philosophy The University of Edinburgh Royal Botanic Garden of Edinburgh 2015 Declaration I hereby declare that the work contained in this thesis is my own, unless otherwise acknowledged and cited. This thesis has not in whole or in part been previously presented for any degree. Roosevelt García-Villacorta 16th March, 2015 i Abstract I investigated the origin of western Amazonian white-sand vegetation and the evolution of plant habitat specialization to different edaphic conditions in Neotropical lowland forests. In order to address these goals I used complementary ecological as well as molecular phylogenetic approaches. Amazonian white-sand forests harbour a flora specialized to nutrient-poor sandy soils, which is distributed as habitat-islands across the Amazon and Guiana Shield regions. This flora has been suggested to have many local and regional endemics, therefore making an important contribution to overall Neotropical plant diversity. The role of habitat specialization in the origin of this flora and its relationships with other floras within the Amazon- Guiana regions is not well understood. To shed light onto these questions, this thesis studies the floristic composition of these forests as well as molecular phylogenetic patterns of selected plant lineages containing white-sand species. The floristic study focused on the white-sand forests of the western Amazon region, which contained 1180 species of vascular plants whereas the non-white-sand Amazon and Guiana Shield dataset consisted of 26,887 vascular plant species. 77% of these species occurred outside white-sand habitats, in other habitat types of the Amazon region, while 23% were white-sand specialists. This demonstrates lower endemism in western Amazonian white-sand forests than previously estimated. 88% of the total westen Amazon white-sand specialist occur within the limits of the Guiana Shield region with the remaining 12% being endemics to the white-sand forests of the western Amazon. Within the Guiana-Shield region, Caquetá Moist Forests (56%), Guayanan Highlands (55%), and Negro-Branco Moist Forests (53%) were the biogeographic regions with the highest proportions of western Amazonian white- sand specialists. Cluster analysis of province level floristic checklists across the Amazon and Guiana regions showed that western Amazonian white-sand forests are nested within floras of the western Guiana-Shield region compared to other floras in the Amazon. Molecular phylogenetic analyses were carried out for the widespread and species-rich families Sapotaceae and Chrysobalanaceae, which display an uneven number of white-sand specialists. Sapotaceae had only three white-sand specialists but Chrysobalanaceae had a larger number of white-sand specialists (14 species). Phylogenetic analysis showed that white-sand specialist species in both ii studied families were scattered across the phylogenies. Both families show a marked absence of edaphic niche conservatism, suggesting that evolutionary switching amongst habitat types has been frequent. Ancestral state reconstruction of habitat specialization under a maximum likelihood approach suggests that preference for poor soils may be ancestral in these clades, especially in Chrysobalanaceae, but that the evolution of species entirely restricted to white-sand soils is in general much more recent and has multiple origins. For the white-sand flora of the western Amazon in particular, there is little evidence that it comprises ancient lineages as previously hypothesized. The historical construction of the Amazonian white sand flora is more likely to be the result of a gradual accumulation of species with different degrees of edaphic specialization, both by on-going speciation driven via habitat switching from non-white-sand specialists and via regional dispersal events after these habitats became available in regions such as the western Amazon. Edaphic transitions between different habitat types were not evolutionary constrained, which may have favoured edaphic niche evolution and the accumulation of plant species diversity in Neotropical lowland forests. iii Acknowledgments First of all, I would like to thank my supervisors, Dr. Toby Pennington, Dr. James Richardson, and Dr. Kyle Dexter, for giving me their valuable time and providing me with insightful feedback, advice, and support all along my studies. Their scientific guidance has been fundamental for finishing this work. Many other scientists have influenced my professional development and I would like to thank in particular to Dr. Chris Dick, Dr. Paul Fine, Dr. Nigel Pitman, Dr. Robert Ricklefs, and Dr. Kalle Ruokolainen, for providing me with advice, inspiration, and help in many ways before my studies in Edinburgh. My field work in Peru and Guyana was only possible with the collaboration of a cadre of wonderful people, and friends. In particular, I want to thank to Luis Torres Montenegro, Julio Irarica, Erika Ortiz, Robert Rodriguez, Jarlis Isuiza, Huber Barriga, Nicole Mitidieri, Jonehi da Silva, Jhonatan Matute, Claus Koo, Guillisa Flores, Betsy Alva, Luis Valles, Julian del Aguila, and Alberto Alva for all their effort during our collection trips in the Peruvian Amazon. Many thanks to Nállarett Davila, Fernanda Cabral, and Marcos Ríos for their help collecting targeted plant species. Thanks to Dr. Euridice Honorio for providing important help when planning my field work in Jenaro Herrera. Thanks to Dr. Kember Mejia, Alfonso Arévalo, and Carlos Rivera for their valuable help while conducting my field work in the Allpahuayo-Mishana National Reserve. Dr. Hans ter Steege, Dr. Karen Redden, and Dr. Kyle Dexter gave me valuable suggestions when planning my field work in Guyana. Ria Bisnauth, Leanna Kalicharan, Calvin Bernard, Hemchandranauth Sambhu, and Kaslyn Holder-Collins helped me enormously with field work logistics while in Guyana, and gave me critical support when exporting my collection samples to the UK. Many thanks to Dr. Carlos Reynel, and Aniceto Daza for their valuable assistance while in the process of obtaining my plant export permits in Peru. Thanks to Dr. Liana Anderson, and Dr. Alberto Quesada for their help in locating Amazon region’s soil spatial data. Dr. Robert Stallard, Dr. Martin Roddaz, Dr. Vincent Regard, and Dr. Matti Räsänen provided valuable discussion on Amazonian geology related to white-sand soils. Thanks to Dr. Jérôme Chave, and Léa Bardon for their iv willingness to collaborate studying Chrysobalanceae. Dr. Rosabelle Samuel, and Dr. Barbara Turner provided access to Lissocarpa (Ebenaceae) samples and I am thankful for that. I would like to also thank the helpful support of the researchers at the molecular lab facilities of the Royal Botanic Garden of Edinburgh, especially to Dr. Laura Forrest, Dr. Michelle Hollingsworth, Ruth Hollands, and Dr. Markus Ruhsam for kindly answering my questions while working in the lab. My time in Edinburgh has been enriched by interacting with all other PhD students, visitors, and researchers of the Royal Botanic Garden of Edinburgh. I have shared great memories with many friends including: Dr. Lidiany Carvalho, Tony Colon, Dr. Liliane Dantas, Katie Emelianova, Renata Françoso, Karina Banda, Alan Eliott, Dr. Faten Filimban, Dr. Maca Gomez, Dr. Emma Goodyear, Dr. Mark Hughes, Adolfo Jara, Lakmini Kumarage, Javier Luna-Castro, Peter Moonlight, Dr. Danilo Neves, Dr. Carmen Puglisi, Subhani Ranasinghe, Dr. Tiina Särkinen, Nicky Sharp, Julieth Serrano, Dr. Alex Twyford, Eugenio Valderrama, and many others. The Missouri Botanical Garden’s A. H. Gentry Fellowship provided financial support for visiting its herbarium to study Amazonian white-sand specimen collections. My PhD studies were funded through a Principal Career Scholarship of the University of Edinburgh, Scotland, UK. I am more than grateful for their support. Most of all I would like to thank my parents and family in Peru for their never ending encouragement and support which has been essential during my studies in Edinburgh. v Table of Contents Chapter 1: Introduction .................................................................................. 1 1.1. Overview ............................................................................................ 1 1.2. Aims and structure of the doctoral thesis ........................................... 5 Chapter 2: Edaphic heterogeneity and the origin of white-sand soils in Amazonia ......................................................................................................
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