Population Genetics and Structure of the Sumatran Tiger
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Population Genetics and Structure of the Sumatran tiger Olutolani Smith A thesis submitted for the degree of Doctor of Philosophy Division of Biology, Imperial College London May 2012 Declaration I confirm that the work presented in this thesis is my own. Where information has been derived from other sources I confirm that this has been appropriately referenced. © The copyright of this thesis rests with the author. No quotation from it should be published without her prior written consent and information derived from it should be acknowledged. - 2 - Abstract The two key determinants of population persistence in fragmented landscapes are population size and connectivity. Populations with high levels of genetic variation and large population size are expected to have a lower risk of extinction. Similarly, populations with high rates of connectivity are expected to persist long-term. For many elusive landscape species it is difficult to obtain direct estimates of these parameters, but genetic sampling can offer powerful indirect assessments. Whilst these techniques have been applied to the study of many wide-ranging carnivores, this study represents the first example in the Sumatran tiger (Panthera tigris sumatrae). Extensive field surveys were conducted to collect faecal samples from several Tiger Conservation Landscapes and protected areas on Sumatra. Samples were then processed according to optimised protocols to obtain reliable results. In order to quantify extinction risk I first estimated genetic variation and effective population size using microsatellite loci. I also determined relative levels of connectivity using estimates of differentiation (FST), gene flow and genetic clustering. Results indicate that Sumatran tigers have high levels of genetic variation and that their effective population size is within the expected range. There is very little population structure and there is no obvious evidence for barriers to dispersal. The Batang Hari/Kerinci Seblat ecosystem emerged as a potential source population and in contrast there was some evidence of isolation affecting the population of Way Kambas NP in the extreme south of the island. Overall, despite high levels of human land cover conversion over the past 20-30 years, few genetic changes have been expressed in the Sumatran tiger. The immediate threat to tigers is not the loss of genetic diversity, but the rapidly declining area of suitable habitat in which they can survive. - 3 - Acknowledgements This project would not have been possible without the help and support of a huge number of people both in Indonesia and the UK. My supervisors Tim Coulson, Jinliang Wang and Chris Carbone deserve special mention for believing that a shy, small animal vet could sample one of the world's most elusive cats on the sixth largest island in the world. Their knowledge, expertise and guidance has been invaluable. Special thanks must also go to Dada Gottelli whose yoda-like advice has proved that when the force is with you the scat is not your enemy. Thanks also to the IOZ genetics theme and the lab gurus Rob Pickles, Patricia Brekke, Kate Ciborowski and Geoff Hobbs whose lab advice got me through the early days of trying to appease the PCR gods. UK support was also provided by Sarah Christie, Malcolm Fitzpatrick and BIAZA who were instrumental in encouraging zoos to provide samples for an initial pilot study. Samples were donated by Howletts Wild Animal Park, Wildlife Heritage Foundation, Dublin zoo, Dudley zoo, London zoo, Paignton zoo and Thrigby Hall Wildlife Gardens. Tiger samples from Sumatra were kindly sent to the Eijkman lab by the following people: Tom Maddox, Dolly Priatna and Citra Novalina (ZSL Indonesia Program), Karmila Parakkasi, Wishnu Sukmantoro and Sunarto (WWF Riau), Matt Linkie, Elva Gemita and Yoan Dinata (FFI Batang Hari), Agung Nugroho (FFI Kerinci), Tony Sumampau, Retno Sudarwati and Hariyo Wibisono (HarimauKita and Taman Safari Indonesia), Iding Haidir and Rahmad Simbolon (Sembilang NP), Matt Linkie and Dolly Priatna (FFI Aceh). I am also grateful to the staff at Way Kambas NP, Kerinci Seblat NP and PT Andalas Merapi Timber for being adventurous enough to participate in the detection dog surveys. Sumianto, Ali Mashuri, Sunarwanto and Nur Alim (Way Kambas NP), Rika Putra Abbas and Hambali (Kerinci Seblat NP), Dwi Adhiasto and Lilik Prastowo (Bukit Barisan Selatan NP) all provided welcome assistance in the field. I also received great support from office and field staff in the Wildlife Conservation Society Indonesia Program. In particular, I am grateful to Nick - 4 - Brickle, Noviar Andayani and Minda Saanin for readily providing introductions and support letters for numerous permits and visas. Ibu Yani, I hope this project serves as the spark you needed to fire up the genetics revolution in Indonesia! Elva Gemita, Gigih Suparmano and Jasman were core members of the scat collection A-team. Elva as always had boundless energy and an infectious spirit that was wonderful to work alongside. We had many giggles and bonded over a shared love of Green & Blacks chocolate. Gigih willingly ferried people, equipment and dogs through most of west Sumatra, and Jasman excelled as the master scat spotter. Although not officially part of the field team, Pak Heri and Pak Wawan drove for 18 hours from Java to Sumatra and back again to transport me, Rudi and all our equipment to base camp. Pak Heri also waited patiently in many car parks while I pursued dogs, scats and permits all over Java and south Sumatra. Karmele, Magda and Lia also helped to organise the paperwork and logistics involved with moving Rudi between Java and Sumatra. The detection dog surveys benefitted from the initial guidance of Amy Dickman, and later from the teaching of Richard Clarke and Stanley the wonder dog. I am particularly grateful to Richard for handler training in the UK and for his willingness to come to Indonesia to train Rudi. I'm sure that is something the residents of Bogor will never forget! And of course I must thank Rudi himself for keeping his spirit despite the many trials we put him through. The Eijkman laboratory were kind enough to let me bring smelly samples into their wonderful facility. Prof Sankot Marzuki, Dr Herawati Sudoyo and Dr Helena Surjadi were supportive from the very beginning and now have a growing wildlife forensics service. Thank you also to Dr Safarina Malik for giving up her lab space and for her unfailing positive energy, Eva for her calm acceptance of my endless sequencer runs and Wulan for her support and friendship. During my time in Indonesia the 'Bogor massive' made me feel very welcome as the newbie on the block and introduced me to the joys of Bintang, G&Ts and pot luck. In particular, heartfelt thanks go to Nick, Anna, Robbie and Alex for welcoming such a - 5 - bewildered ex-pat into their home. Thank you to my friends and family who have been wonderful over the past few years, even though I'm sure they still don't understand what it is I've been doing. Watch this space - there are more adventures to come! At the IOZ my office mates Lisa Signorile, Martina di Fonzo and Farid Belbachir have had to endure many months of grumbling but we have also had some great conversations about food and the meaning of life. I know that you will do well in your PhDs and go on to great things. And last but not least, thank you to Joe for being a source of inspiration and encouragement since the day we met. I wouldn't be on this crazy journey if it wasn't for you. I have been helped along the way and have been given advice by so many people that I may have missed one or two. My sincerest apologies if that happens to be you. This study was funded by a National Environment Research Council (NERC)/CASE Studentship and I also received valuable support from the Panthera-Kaplan Graduate Award scheme and the Zoological Society of London. Indonesian research permits were provided by the Ministry of Research & Technology (Ristek), the Department of Forestry, and the Department for Forest Protection and Nature Conservation (PHKA). - 6 - Contents Declaration 2 Abstract 3 Acknowledgements 4 Contents 7 List of Tables 15 List of Figures 16 1. Research Background 18 1.1 Introduction ………………………………………………………………19 1.2 Metapopulation dynamics ………………………………………………20 1.2.1. Patch size & isolation ………………………………………………21 1.2.2. Extinction threshold ………………………………………………23 1.2.3. Time lag ……………………………………………………………23 1.2.4. Stochasticity…………………………………………………………24 1.2.5. Source-sink dynamics ……………………………………………24 1.2.6. Extinction risk ………………………………………………………25 1.3 Landscape ecology ……………………………………………………25 - 7 - 1.3.1. Population viability …………………………………………………26 1.3.2. Matrix quality & patch boundaries ………………………………27 1.3.3. Connectivity & corridors ……………………………………………29 1.3.4. Population persistence ……………………………………………30 1.4 Population genetics ……………………………………………………30 1.4.1. Population size ……………………………………………………31 1.4.2. Isolation ……………………………………………………………33 1.4.3. Extinction risk ………………………………………………………35 1.5 Landscape genetics ……………………………………………………35 1.5.1. Isolation by distance ………………………………………………36 1.5.2. Barriers to dispersal ………………………………………………37 1.5.3. Functional connectivity ……………………………………………38 1.5.4. Population persistence & connectivity……………………………39 1.6 Overall summary ………………………………………………………40 1.7 Case study - the Sumatran tiger (Panthera tigris sumatrae) ………41 1.7.1. Sumatra ……………………………………………………………41 1.7.2. Sumatran tigers ……………………………………………………42 1.7.3. Threats ………………………………………………………………43 1.7.4. Population viability …………………………………………………45 1.7.5. Genetics ……………………………………………………………47 1.7.6. Further study ………………………………………………………50 Thesis outline 51 - 8 - 2. Sampling effects in Conservation Genetics Studies 52 2.1 Abstract 53 2.2 Introduction ………………………………………………………………53 2.3 Methods …………………………………………………………………56 2.3.1. Simulated data………………………………………………………56 2.3.2. Genetic parameters ………………………………………………56 2.4 Results ……………………………………………………………………59 2.4.1. Genetic diversity and sample size ………………………………59 2.4.2. Population structure and sample size ……………………………60 2.5 Discussion ………………………………………………………………63 3.