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Understanding Anuran Responses to Rainforest Fragmentation and Oil Palm Agriculture in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysia

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Understanding Anuran Responses to Rainforest Fragmentation and Oil Palm Agriculture in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysia Understanding anuran responses to rainforest fragmentation and oil palm agriculture in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysia. Juan Manuel Aguilar-León (MSc) January 2020 Organism and the Environment Division, School of Biosciences, Cardiff University This thesis is submitted to Cardiff University in candidature for the degree of Doctor of Philosophy Primary supervisor: Prof. Michael W. Bruford Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK Secondary supervisor: Dr. Benoît Goossens Danau Girang Field Centre, c/o Sabah Wildlife Department, Wisma Muis, 88100 Kota Kinabalu, Sabah, Malaysia. Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK Third supervisor: Dr. Pablo Orozco ter Wengel Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK This project was funded by a scholarship from CONCyTEC and grant from The Rufford Foundation. The local counterpart was Dr. Senthivel K.S.S Nathan of the Sabah Wildlife Department (research permit: number: JHL(PB)600-3/18/1/1 Jld.23) I Declaration This thesis is the result of my own independent work, except where otherwise stated, and the views expressed are my own. Other sources are acknowledged by explicit references. The thesis has not been edited by a third party beyond what is permitted by Cardiff University's Use of Third Party Editors by Research Degree Students Procedure. Signed................................................(Candidate) Date.......................... STATEMENT 1 This thesis is being submitted in partial fulfilment of the requirements for the degree of.............................(insert MCh, MD, Mphil, PhD etc, as appropriate) STATEMENT 2 This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is it being submitted concurrently for any other degree or award (outside of any formal collaboration agreement between the University and a partner organisation). Signed................................................(Candidate) Date.......................... STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available in the University’s Open Access repository (or, where approved, to be available in the University's library and for inter-library loan), and for the title and summary to be made available to outside organisations, subject to the expiry of a University-approved bar on access if applicable. Signed................................................(Candidate) Date.......................... II Acknowledgments There are many people I woul like to thanks for all the support they gave it to me during the last 4 years of my PhD. It has been a great pleasure and a great opportunity to do my PhD in the University of Cardiff, UK. It has been a privilege to have been supervised by Mike Bruford, Pablo Orozco ter Wengel and Benoit Gossens whom are truly inspirational: sincere thanks for your patience (specially correcting my grammar Mike!), guidance and enthusiasm. I would like to thank my beautiful family for all their support and love during these time. To my parents, thank you for been an example of hard work but mostly to teach me how to be a good person and always try to give 100%. My father, who left me in the middle of this PhD, this thesis is for you! miss you every day. My brother and sister for always be there for me. I am very gratefull with all the people who have contributed to this thesis in one way or another. Thank you Jordan Cuff for being the driving force behind the statistic, and for your positivity and friendship. Mafalda Costa, Isa-Rita Russo, Nia, Ian , Ewan and Frank thank you for been amazing human beings. This project would not have been possible without the financial support provided from the Peruvian Government, through CONCyTEC, and the Rufford Small Grants for Nature Conservation. To my counterpart and friend Dr. Sen Nathan of the Sabah Wildlife Department for his support in this project. To the Sabah Biodiversity Centre (SaBC) for permission to conduct this research and export permits. I am enormously thankful with my DGFC family. Specialy with Samsir and Koko, with out them nothing of this could have been possible. Last but not least, a very special thanks to my beautiful wife for all her support and constant encouragement. You are my best friend. Love you 3000. III TABLE OF CONTENTS Declaration…………………………………………………………………...……..II Acknowledgments.....…………………………………………………………......III List of Contents……………...……………………………………………..…......IV List of Figures…………………………………………………………………….VIII List of Tables.……………………………………………………………………....X Summary……………………………………………………………………..…..XIII CHAPTER 1. GENERAL INTRODUCTION………………………………………………...…...1 1.1 Foreword and justification………………………………………………...…..2 1.2 Global deforestation and degradation of tropical forest……………………3 1.2.1 Oil Palm agriculture……………………………………………………..5 1.2.2 Deforestation in South East Asia…………………...…………………8 1.3 Borneo…………………………………………………………………………..9 1.3.1 The Lower Kinabatangan Wildlife Sanctuary………………...………9 1.3.2 Kabili-Sepilok Forest Reserve………………………………………..10 1.4 An introduction to the amphibians…...……………………………………..12 1.5 Fragmentation effects on amphibians…………………...…………………13 1.5.1 Amphibian declines……………………………………………………15 1.6 Phylogenetic diversity………………………………………………………..17 1.6.1 Phylogenetic diversity and conservation……...…………………….18 1.7 Fragmentation effects in tropical forest on genetic diversity………...…..19 1.8 Project aims and hypotheses…………………………...…………………..20 1.9 Bibliography…………………………………………………………………...22 CHAPTER 2. DE NOVO NUCLEAR MARKER DEVELOPMENT FROM ILLUMINA – PAIRED-END DATA FROM FOUR SPECIES OF BORNEAN FROGS..….32 2.1 Introduction……………………………………....……………………………33 IV 2.2 Materials and Methods………………………………...…………………….34 2.2.1 Sample collection and DNA extraction………………………………34 2.2.2 Library preparation…………………………………………………….36 2.2.3 Contig assembly and microsatellite detection…..…………............37 2.2.4 Amplification conditions and validation of primers.........................38 2.2.5 Data analysis..................................................................................39 2.3 Results....................................................................................................39 2.3.1 Sequence assembly.......................................................................39 2.3.2 Microsatellite screening and quality evaluation..............................43 2.4 Discussion and conclusions....................................................................48 2.5 Bibliography.............................................................................................50 CHAPTER 3. AMPHIBIAN POPULATION GENETICS IN A FRAGMENTED LANDSCAPE: DO OIL PALM PLANTATIONS DRIVE POPULATION STRUCTURE?..............................................................................................55 3.1 Introduction..............................................................................................56 3.2 Materials and Methods............................................................................60 3.2.1 Lower Kinabatangan Wildlife Sanctuary (LKWS)...........................60 3.2.2 Kabili-Sepilok Forest Reserve........................................................61 3.2.3 Sampling and DNA extraction........................................................61 3.2.4 Microsatellite genotyping and population genetics parameters.....65 3.2.5 Population structure analysis.........................................................71 3.2.6 Structure analysis of LKWS lots and inferred gene flow clusters..........................................................................................................72 3.3 Results....................................................................................................73 3.3.1 Genetic diversity.............................................................................73 3.3.2 Population structure.......................................................................78 3.3.3 Immigration....................................................................................87 3.4 Discussion...............................................................................................90 3.4.1 Genetic Diversity............................................................................91 3.4.2 Population Structure......................................................................94 V 3.4.3 Migration rates...............................................................................95 3.4.4 Conservation implications..............................................................96 3.5 Bibliography.............................................................................................98 CHAPTER 4. THE VALUE OF SECONDARY FOREST FOR TROPICAL ANURAN COMMUNITIES: DNA BARCODING, AND PHYLOGENETIC DIVERSITY OF THE LOWER KINABATANGAN WILDLIFE SANCTUARY AND SEPILOK FOREST RESERVE...................................................................107 4.1 Introduction............................................................................................108 4.2 Materials and Methods..........................................................................112 4.2.1 Study area....................................................................................112 4.2.2 Anuran survey and habitat parameters........................................113 4.2.3 DNA
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