A Systematic Review of Kerivoula Gray, 1842 (Chiroptera: Vespertilionidae: Kerivoulinae) from Thailand Bounsavane Douangboubpha A Thesis Submitted in Fulfillment of the Requirement for the Degree of Doctor of Philosophy in Biology Prince of Songkla University 2014 Copyright of Prince of Songkla University i A Systematic Review of Kerivoula Gray, 1842 (Chiroptera: Vespertilionidae: Kerivoulinae) from Thailand Bounsavane Douangboubpha A Thesis Submitted in Fulfillment of the Requirement for the Degree of Doctor of Philosophy in Biology Prince of Songkla University 2014 Copyright of Prince of Songkla University ii Thesis Title A Systematic Review of Kerivoula Gray, 1842 (Chiroptera: Vespertilionidae: Kerivoulinae) from Thailand Author Mr. Bounsavane Douangboubpha Major Program Doctor of Philosophy in Biology Major Advisor Examining Committee …………………………………… …………………………………… (Assist. Prof. Dr. Sara Bumrungsri) (Dr. Yodchaiy Chuaynkern) …………………………………… Co-advisor (Assist. Prof. Dr. Sara Bumrungsri) …………………………………… …………………………………… (Dr. Paul J. J. Bates) (Dr. Paul J. J. Bates) …………………………………… …………………………………… (Assoc. Prof. Dr. Chutamas Satasook) (Assist. Prof. Dr. Warapond Wanna) …………………………………… …………………………………… (Assist. Prof. Dr. Warapond Wanna) (Assist. Prof. Dr. Supiyanit Maiphae) The Graduate School, Prince of Songkla University, has approved this thesis as fulfillment of the requirements for the Doctor of Philosophy Degree in Biology. ………………………………… (Assoc. Prof. Dr. Teerapol Srichana) Dean of Graduate School iii This is to certify that the work here submitted is the result of the candidate’s own investigations. Due acknowledgement has been made of any assistance received. …………………………………… (Assist. Prof. Dr. Sara Bumrungsri) Major Advisor …………………………………… (Mr. Bounsavane Douangboubpha) Candidate iv I hereby certify that this work has not already been accepted in substance for any degree, and is not being concurrently submitted in candidature for any degree. …………………………………… (Mr. Bounsavane Douangboubpha) Candidate v Thesis Title A Systematic Review of Kerivoula Gray, 1842 (Chiroptera: Vespertilionidae: Kerivoulinae) from Thailand Author Mr. Bounsavane Douangboubpha Major Program Doctor of Philosophy in Biology Academic Year 2014 ABSTRACT A systematic study of the genus Kerivoula Gray, 1842 from Thailand was undertaken based on morphology, acoustics and genetics. Seven species, K. papillosa, K. kachinensis, K. hardwickii, K. titania, K. pellucida, K. krauensis and K. minuta, were included in the study. One, K. krauensis, is recorded for the first time from the country. Two other species, K. picta and K. whiteheadi, which had been recorded previously from the country were not available to examine for the present study. The results of morphological and genetic analyses show that the bats in this genus consist of several species complexes, including the K. papillosa complex, the K. hardwickii complex and the K. titania complex. Acoustic analysis indicates that echolocation call characters are significantly different between species, although, there is considerably overlap in each parameter among species. A detailed study of the K. papillosa species complex, based on data from throughout South-east Asia, indicated that it includes three distinct species, of which one is referable to an undescribed species, Kerivoula spA. The other two are K. papillosa and K. malayana respectively The results also show that specimens previously referred to K. lenis from the Sundaic Subregion are discrete from those from India and are here considered as an undescribed species, Kerivoula spB. In case of the K. hardwickii species complex, both morphological and genetic analysis show that the bats previously referred to K. hardwickii consist of several cryptic species, which are divided into two type, ‘domed-skull’ type and ‘flat-skull type. The specimens with a ‘domed-skull’ type are here considered referable to K. hardwickii, which is itself an apparant species complex. Those with the ‘flat-skull’ type are referred to the K. depressa complex, which also appears to include several cryptic species. More data are required to analyse these latter two complexes in detail. vi ACKNOWLEDGEMENTS First, I would like to thank all of my advisor and co-advisor Assist. Prof. Dr. Sara Bumrungsri, Dr. Paul J. J. Bates, Assoc. Prof. Dr. Chutamas Satasook, Dr. Warapond Wanna, for their help, suggestion and encouragement during the study. Thanks are due to Thesis Examining Committee, including Assist. Prof. Dr. Supiyanit Maiphae of Department of Biology, Faculty of Science, Prince of Songkla University, and Dr. Yodchaiy Chuaynkern of Department of Biology, Faculty of Science, Khon Kaen University help, correction and valuable suggestion. I am grateful to all students of the Mammal and Bird Research Unit, Department of Biology, students of Department of Molecular Biotechnology and Bioinformatics, Faculty of Science, and the staff of Princess Maha Chakri Sirindhorn Natural History Museum, Prince of Songkla University for their help and encouragement. I also thank the staff of Hala-Bala Wildlife Research Station, especially Mr. Sunate Karapan, for their help in organizing and participating in a range of the field surveys. Thanks also due to all lecturer and staff of Department of Biology and Department of Molecular Biotechnology and Bioinformatics, Faculty of Science, Prince of Songkla University for their help and suggestion. I would like to thank the staff of Faculty of Environmental Sciences, National University of Laos, Lao PDR, especially Assoc. Prof. Souphab Khouangvichit, Oley Phearkeo, Daosavanh Sanamxay, Vilakhan Xayaphet, for their help, support, loaning specimens and encouragements. Thanks also due to Mr. Ith Saveng and Dr. Neil M. Furey of Centre for Biodiversity Conservation, Faculty of Science, Royal University of Phnom Penh, Cambodia; Dr. Vu Dinh Thong of Institute of Ecology and Biological Resource, Vietnam Academy of Science and Technology, Vietnam; Dr. Faisal Ali Anwarali Khan of Department of Zoology, Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, Malaysia; Mr. Joe Chun-chia Huang of Department of Biological Sciences and the Museum, Texas Tech University, USA; and Dr. Ibnu Maryanto of Museum Zoologicum Bogoriense, Research Center for Biology-Indonesian Institute of Sciences, Indonesia, for their collaboration and loaning specimens for the present study. vii In addition, I would like to thank the staff of Harrison Institute, UK, especially Malcolm J. Pearch, Nikky M. Thomas, David L. Harrison and Beatrix Lanzinger, for their help, suggestion, support, providing literature and loaning specimens for the present study. Thanks also due to Dr. Tigga Kingston of the Department of Biological Sciences and the Museum, Texas Tech University, USA and South-east Asian Bat Conservation and Research Unit (SEABCRU) for help co-ordinating the loaning of specimens and promoting networking amongst bat taxonomists in South-east Asia. Finally, I would like to thank the National Research University Project of Thailand’s Office of the Higher Education Commission and Graduate School, Prince of Songkla University, Thailand, and the Darwin Initiative of the UK Government for their financial support. I am also grateful to my family for their support and encouragement during study. Without all of the above and the collaboration of many others, this project would not have been possible. Bounsavane Douangboubpha viii Contents Abstract ……………………………………………………………………………… v Acknowledgements …………………………………………………………………. vi Contents …………………………………………………………………………… viii List of Tables ………………………………………………………………………... xi List of Figures ……………………………………………………………………... xiii Chapter 1: General Introduction.………………………………………………………1 1.1. Order Chiroptera………………………………………………………………….1 1.1.1. Systematics...……………………………………………………………………1 1.2. Family Vespertilionidae…………………………………………………………..2 1.3. Genus Kerivoula…………………………………………………………………..4 1.3.1. Research on genus Kerivoula in Thailand………………………………………5 1.4. Objectives…………………………………………………………………………8 Chapter 2: Morphology, acoustics and genetics of the genus Kerivoula (Chiroptera: Vespertilionidae: Kerivoulinae) in Thailand…………………………………………..9 Abstract ……………………………………………………………………………….9 2.1. Introduction……………………………………………………………………….9 2.2. Material and Methods……………………………………………………………11 2.2.1. Field work……………………………………………………………………..12 2.2.2. Sound records and analysis……………………………………………………14 2.2.3. Measurements…………………………………………………………………16 2.2.4. Morphological analysis………………………………………………………..19 2.2.5. Genetic analysis………………………………………………………………..20 2.3. Results…………………………………………………………………………...21 2.3.1. Morphometrics………………………………………………………………...21 2.3.2. Acoustics………………………………………………………………………30 2.3.3. Genetics………………………………………………………………………..31 2.4. Discussion……………………………………………………………………….40 Chapter 3: A Review of the Kerivoula papillosa Species Complex and K. lenis (Chiroptera: Vespertilionidae: Kerivoulinae) from South-east Asia…………………47 ix Abstract ……………………………………………………………………………...47 3.1. Introduction……………………………………………………………………...47 3.2. Material and Methods..…………………………………………………………..49 3.2.1. Measurements………………………………………………………………….49 3.2.2. Morphometric analysis………………………………………………………...51 3.2.3. Genetic analysis………………………………………………………………..51 3.3. Results…………………………………………………………………………...52 3.3.1. Morphometrics………………………………………………………………...52 3.3.2. Genetics………………………………………………………………………..72 3.4. Systematic Descriptions…………………………………………………………73 Kerivoula malayana Chasen, 1940…………………………………………………..77 Kerivoula