TAXONOMY AND ECOLOGY OF AMPHIBIAN COMMUNITIES IN SOUTHERN VIETNAM: LINKING MORPHOLOGY AND BIOACOUSTICS TRAN, THI ANH DAO Taxonomy and ecology of amphibian communities in Southern Vietnam: Linking morphology and bioacoustics Dissertation zur Erlangung des Doktorgrades (Dr rer nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von TRAN, THI ANH DAO aus Ho Chi Minh City, Vietnam Bonn, 2013 Angefertigt mit Genehmigung der MathematischNaturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn Gutachter Prof Dr Wolfgang Böhme Gutachter Prof Dr Wolfgang Wägele Tag der Promotion:03/12/2013 Erscheinungsjahr: 2014 LIST OF CONTENTS LIST OF CONTENTS i LIST OF TABLES vi LIST OF FIGURES viii LIST OF PLATES xiv ABBREVIATIONS CHAPTER I INTRODUCTION Background Study area 2.1 Topography 2.2 Climate 10 2.3 Vegetation types 11 2.4 Vertebrate fauna in brief 11 2.5 Threats to the biodiversity 13 CHAPTER II METHODS AND MATERIALS 15 Sampling and field data collecting 15 1.1 Survey sites 15 1.2 Survey efforts 18 1.3 Sampling 19 1.4 Call recording 20 Analyses 20 2.1 Morphological analyses 20 2.2 Acoustic analyses 22 2.3 Statistical analyses 24 CHAPTER III RESULTS 25 i Bufonidae 26 Duttaphrynus melanostictus (Schneider, 1799) 26 Ingerophrynus galeatus (Günther, 1864) 27 Megophryidae 29 Brachytarsophrys intermedia (Smith, 1921) 29 Leptobrachium leucops Stuart, Rowley, Tran, Le, and Hoang, 2011 32 Leptobrachium pullum (Smith, 1921) 35 Leptolalax bidoupensis Rowley, Le, Tran, and Hoang, 2011 38 Ophryophryne hansi Ohler, 2003 41 Xenophrys major (Boulenger, 1908) 43 Microhylidae 46 Calluella guttulata (Blyth, 1856) 46 Kaloula pulchra Gray, 1831 47 Microhyla annamensis Smith, 1923 48 Microhyla berdmorei (Blyth, 1856) 50 Microhyla heymonsi Vogt, 1911 51 Microhyla pulchra (Hallowell, 1861) 53 Microhyla sp 54 Microhyla sp 56 Dicroglossidae 58 Occidozyga lima (Gravenhorst, 1829) 58 Occidozyga martensii (Peters, 1867) 60 Fejervarya limnocharis (Gravenhorst, 1829) 62 Limnonectes dabanus (Smith, 1922) 64 Limnonectes poilani (Bourret, 1942) 66 Ranidae 69 Hylarana attigua (Inger, Orlov, and Darevsky, 1999) 69 Hylarana milleti (Smith, 1921) 71 Hylarana montivaga (Smith, 1921) 74 Hylarana nigrovittata (Blyth, 1856) 77 Odorrana gigatympana (Orlov, Ananjeva, and Ho, 2006) 80 ii Odorrana graminea (Boulenger, 1900) 82 Rana johnsi Smith, 1921 84 Rhacophoridae 86 Chiromantis nongkhorensis (Cochran, 1927) 86 Feihyla palpebralis (Smith, 1924) 88 Kurixalus baliogaster (Inger, Orlov, and Darevsky, 1999) 90 Polypedates megacephalus Hallowell, 1861 92 Polypedates cf mutus (Smith, 1940) 94 Raorchestes gryllus (Smith, 1924) 95 Rhacophorus annamensis Smith, 1924 98 Rhacophorus calcaneus Smith, 1924 101 Rhacophorus robertingeri Orlov, Poyarkov, Vassilieva, Ananjeva, Nguyen, Nguyen, Geissler, 2012 103 Rhacophorus vampyrus Rowley, Le, Tran, Stuart, and Hoang, 2010 106 Theloderma asperum (Boulenger, 1886) 107 Theloderma bambusicolum Orlov, Poyarkov, Vassilieva, Ananjeva, Nguyen, Nguyen & Geissler, 2012 109 Theloderma gordoni Taylor, 1962 111 Theloderma palliatum Rowley, Le, Hoang, Dau & Cao 2011 113 Theloderma stellatum Taylor, 1962 115 Theloderma truongsonense (Orlov & Ho, 2005) 117 2.4 Ecological niche segregation of amphibians in the Langbian Plateau 123 Biogeographic relationships of the amphibian communities among forests within and neiboring the Langbian Plateau 128 3.1 Biogeographic relationships of the amphibian communities among the forests within the Langbian Plateau 128 Brachytarsophrys intermedia 130 Leptobrachium leucops 132 iii Leptobrachium pullum 134 Leptolalax bidoupensis 139 Xenophrys major 144 Hylarana attigua 146 Hylarana milleti 148 Hylarana nigrovittata 151 Chiromantis nongkhorensis 152 Kurixalus baliogaster 154 Raorchestes gryllus 156 Rhacophorus annamensis 158 Rhacophorus calcaneus 165 CHAPTER IV DISCUSSION 167 Taxonomic problems and species complexes 167 1.1 Brachytarsophrys intermedia 167 1.2 Hylarana nigrovittata complex 167 1.3 Polypedates leucomystax complex 168 1.4 Raorchestes gryllus 169 1.5 Rhacophorus calcaneus and Rhacophorus robertingeri 170 Bioacoustics 171 2.1 Vocal property and behavior similarities within the anuran families 171 Megophryidae 171 Ranidae 173 Rhacophoridae 178 2.2 Multiple call types 182 2.3 Chorus behavior 182 Diversity and biogeography of the amphibian fauna of the Langbian Plateau 186 3.1 Diversity 186 3.2 Biogeographic relationships of the amphibian communities among the forests within and adjacent the Langbian Plateau 188 iv Plate Genera Calluella, Kaloula pulchra, and Microhyla A-B: Calluella guttulata; C: Kaloula pulchra; D: Microhyla annamensis; E: M heymonsi; F: M pulchra; G: M sp1; H: M sp.2 223 Plate Genera Occidozyga, Fejervarya, and Limnonectes A: Occidozyga lima; B: O martensii; C-D & G: Fejervarya limnocharis; E-F, & H: Limnonectes poilani; J-K, & I: Limnonectes dabanus 224 Plate Genus Hylarana A-C: Hylarana attigua; D-F: H milleti; G-I: H montivaga; J-L: H nigrovittata 225 Plate Genera Rana, Odorrana, Chiromantis, Feihyla, and Kurixalus A: Rana johnsi; B-C: Odorrana gigatympana; D-G: O Graminea (D, E: males; G: female); G-H: Chiromantis nongkhorensis; I-L: Feihyla palpebralis; M-O: Kurixalus baliogaster 226 Plate Genera Polypedates, Raorchestes, and Rhacophorus A: Polypedates cf mutus; B-C: P megacephalus; D-F: Raorchestes gryllus; G-I: Rhacophorus annamensis; J-L: R vampyrus (J: adult male; K: juvenile) 227 Plate Genera Rhacophorus and Theloderma A-G: Rhacophorus calcaneus (A-C, E-F: males; D: female; G: metamorph, H: juvenile); H-I: R robertingeri; J-K: Theloderma asperum 228 Plate Genus Theloderma A-B: T bambusicolum; C-E: T gordoni; F-H: T palliatum; I-K: T stellatum; L-M: T truongsonense 229 Plate 10 Types of forests in the Langbian Plateau A: Cloud forest in TD NR; B: Cloud forest in BDNB NP; C: evergreen forest in BDNB NP (1500 m elev.); D: Stream in evergreen forest in BDNB NP (1800 m elev.); E Stream in mixed forest of hard wood and bamboo in CYS NP (900 m elev.); F: Stream in mixed forest of hard wood and bamboo in PB NP (700 m elve.); G: Stream in mixed forest of small hard wood and bamboo in SLSM; H: A channel in mixed forest of small hard wood and bamboo in SLSM; I & J: cultivated areas in TD NR 230 Plate 11 Microhabitats using by anurans in the Langbian Plateau A: Shallow water in CYS NP; B: A rain puddle in TD NR; C: Leaf litter and fallen trees on the ground; D: Small shrubs nearby a swallow water in CYS NP; E & F: Vegetation and grass near to corn farm in SLSM; G–I: Small streams with grass, small trees and shrubs along the banks in BDNB NP; J & K: Rocks along banks of stream in PB NP & SLSM; L: Rocky crevice in SLSM (above) and hole in bank along stream in BDNB NP (below) 231 Plate 12 Amplexus ativities in amphibans from the Langbian Plateau A: Leptobrachium leucops; B: Leptobrachium pullum; C: Limnonectes poilani; D: Calluella guttulata; E & F: Polypedates megacephalus; G– I: Rhacophorus annamensis; J: Raorchestes gryllus 232 Plate 13 Color pattern in Raorchestes gryllus 233 APPENDIX PUBLICATIONS OF KEY PART OF THE DISSERTATION Rowley JJL, Le DTT, Tran DTA, Stuart BL, Hoang HD 2010 A new tree frog of the genus Rhacophorus (Anura: Rhacophoridae) from southern Vietnam Zootaxa 2727:45−55 Rowley JJL, Le DTT, Tran DTA, Hoang HD 2011 A new species of Leptolalax (Anura: Megophryidae) from southern Vietnam Zootaxa 2796:15−28 Stuart BL, Rowley JJL, Tran DTA, Le DTT, Hoang HD 2011 The Leptobrachium (Anura: Megophryidae) of the Langbian Plateau, southern Vietnam, with description of a new species Zootaxa 2804:25−40 Tran, D T A., Nguyen, T T., Phung, T M., Ly, T., Boehme, W & Ziegler, T (2011) Redescription of Rhacophorus chuyangsinensis Orlov, Nguyen & Ho, 2008 (Anura: Rhacophoridae) based on new collections from new south Vietnamese provincial records: Lam Dong and Khanh Hoa Revue suisse de Zoologie 118, 1−9 Rowley, J J L., D T A Tran, D T T Le, H D Hoang and R Altig 2012 The strangest tadpole: the oophagous, tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam Journal of Natural History 46 (47−48): 2969−2978 APPENDIX CURRICULUM VITAE Name: Tran, Thi Anh Dao Date of birth: 13.03.1974 Place of birth: Sai Gon (now Ho Chi Minh City), Vietnam Nationality: Vietnamese Address in Vietnam: The University of Science, Ho Chi Minh City, Vietnam Faculty of Biology 227 Nguyen Van Cu, District 5, Ho Chi Minh City, Vietnam Address in Germany: The Zoologisches Forschungsmuseum Alexander Koenig Herpetology Section Adenaueralle 160, 53113 Bonn Email: ttadao.hcmuns@gmail.com Education and Training 1992 - 1994 Studied at Forestry and Aquaculture University, Vietnam 1994−1997 Studied at University of Natural Science Ho Chi Minh City, Vietnam (Bachelor of Science) 1999−2002 Studied at University of Natural Science Ho Chi Minh City, Vietnam (M Sc Animal Physiology) Thesis title: “Efficiency of using the CMS (Concentrate Molasses Solution) as a material of artificial food for freshwater fish in aquaculture” 2004 Training course on Wetland Ecology and management in the Lower Mekong Basin (at Mahidol University, Thailand) 10/2009−2013 Study at University of Bonn, Germany (Faculty of Mathematic and Natural Science) Employment 1998−2003 Lecturer assistant at Department of Zoology and Animal Physiology, Faculty of Biology, University of Natural Science Ho Chi Minh City, Vietnam 2003−2013 Lecturer at Department of Zoology and Animal Physiology, Faculty of Biology, University of Natural Science Ho Chi Minh City, Vietnam Resposibility in subjects: “Labwork of General Biology” (for the first class students) and “Labwork of Vertebrates” (for the second class students) Publications and presentation Tran DTA, Le QK, Le KV, Vu TN, Nguyen TQ, Böhme W, Ziegler T 2010 First and preliminary frog records (Amphibian: Anura) from Quang Ngai Province, Vietnam Herpetology Notes 3:111−119 Rowley JJL, Le DTT, Tran DTA, Stuart BL, Hoang HD 2010 A new tree frog of the genus Rhacophorus (Anura: Rhacophoridae) from southern Vietnam Zootaxa 2727:45−55 Rowley JJL, Le DTT, Tran DTA, Hoang HD 2011 A new species of Leptolalax (Anura: Megophryidae) from southern Vietnam Zootaxa 2796:15−28 Stuart BL, Rowley JJL, Tran DTA, Le DTT, Hoang HD 2011 The Leptobrachium (Anura: Megophryidae) of the Langbian Plateau, southern Vietnam, with description of a new species Zootaxa 2804:25−40 Tran, D T A., Nguyen, T T., Phung, T M., Ly, T., Boehme, W & Ziegler, T (2011) Redescription of Rhacophorus chuyangsinensis Orlov, Nguyen & Ho, 2008 (Anura: Rhacophoridae) based on new collections from south Vietnamese provincial records: Lam Dong and Khanh Hoa Revue suisse de Zoologie 118, 1−9 Wildenhues, M J., Bagaturov, M F., Schmitz, A., Tran, D T A., Hendrix, R & Ziegler, T (2011) Captive management and reproductive biology of Orlov’s Treefrog, Rhacophorus orlovi Ziegler & Köhler, 2001 (Amphibia: Anura: Rhacophoridae), including larval description, colour pattern variation and advertisement call Zool Garten N.F 80, 287−303 Rowley, J J L., D T A Tran, D T T Le, H D Hoang and R Altig 2012 The strangest tadpole: the oophagous, tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam Journal of Natural History 46 (47−48): 2969−2978 Rowley, J J L., D T A Tran, H D Hoang and D T T Le 2012 A new species of large flying frog (Rhacophoridae: Rhacophorus) from lowland forest in southern Vietnam Jouranal of Herpetology 46 (4): 480−487 Participate the 5th Asia Herpetological Conference in Chengdu, Sichuan, China (2−4 June 2012): “Amphibian communities in Langbian Plateau, southern Vietnam” (Oral presentation) [...]... Plateau and provided accounts for four other anurans The second paper was published in 1924 and Smith reported 11 species of Rhacophoridae from Indochina and Malaysia, including seven new species, six of them being discovered from the Langbian Plateau and neighboring areas (Smith, 1924) The comprehensive book of Bourret, published in 1942, provided accounts and descriptions of amphibians in Indochina (Cambodia,... forests, in Binh Thuan Province, Vietnam TD NR Ta Dung Nature Reserve, Dak Nong Province, Vietnam 1 2 CHAPTER I INTRODUCTION 1 Background 1.1 Amphibian communities in Vietnam: divers but poorly known The knowledge about the actual diversity of amphibians in Vietnam is still imperfect although many researches that focus on the herpetofauna of this country have been intensive in recent years The number of. .. calling neighbors in anurans is a rising in duration or rate of call in comparison with single calling (Gerhardt & Huber, 2002) The calling males also change in other characteristics of the calls such as dominant frequency and intensity (Narins et al., 2007; Wells, 2007) Vocalization provides efficient approaches for studies on biology of anurans Many behavioral activities in mating and reproduction in. .. level, in the Southeast Central Vietnam has features of Truong Son Range and coastal lowlands The southern part of the country is well known with the lowland of Mekong Delta, with an average elevation at under ten meters above sea level (Averyanov et al., 2003; Sterling et al., 2007) Truong Son Mountains is the Vietnamese part of Annamite Range, the main uplands in Indochina, spreading over Laos, Vietnam, ... for paying their debts not for current daily needs as before and level of wildlife and timber trades in and near to buffer zone of the Park was rapidly raised up (Birdlife, 2010) Other factors that caused raising of overexploiting the natural resources in the Langbian Plateau were developing of hunting and harvest techniques and influx of ethnic immigrants from other regions into buffer zones of protected... districts, Dak Lak Province Topography of the Park is mountainous with elevations 600−2440 m and dominated by Chu Yang Sin Peak, at 2442 m Main streams in the forest are Ea K’Tuar and Ea Krong Kmar, which joint to Ea Krong Ana River in the North and streams in the South of the forest 15 drain into the Krong No River Both the Ea Krong Ana and Krong No rivers flow west and north before joining Serepok River... solangiae, and Carduelis monguilloti), including six Important Bird Areas namely Chu Yang Sin, Bidoup, Lang Bian, Cong Troi, Tuyen Lam, and Phuoc Binh Mountains (Birdlife, 2001b) According to Bain and Hurley (2011), in herpetological respect, the Langbian Plateau is within the subregion Southern Annamites of Indochina This subregion ranks eighth in Indochina for species richness and second for endemic species,... Reasons of the decline status were mainly overexploiting natural resources, habitat loss and fragmentation that are associated with alternating of land use (Sterling et al., 2007) Hunting, fishing, logging, and collecting of plants and animals were routine activities of local ethnic people for long time ago These activities did not threat to natural resource until recent years, when the use of wildlife... sub-regions in Vietnam (Modified after Bain & Hurley, 2011; Map: Kevin Koy) 9 in Vietnam (Birdlife, 2001a; Averyanov et al., 2003; Sterling et al., 2007; Bain & Hurley, 2011) Separated from south of the Kon Tum Massif by Pleiku and Dak Lak highlands, Dak Lak Province, the Langbian Plateau extends southwestward and connects to Di Linh Plateau, Lam Dong Province, slopes eastward into coastal lowlands in Ninh... temperatures of these regions range between 22−25oC The lowland areas surrounding the Langbian Plateau have an annual average rainfall of 1500−3000 mm (Sterling et al., 2007) 2.3 Vegetation types Vegetation of Vietnam is belonging to the Indochinese Floristic Region, including six zones: Sikang-Yunnan, South Chinese, North Indochinese, Central Annamese, South Annamese, and South Indochinese (Averyanov ... Taxonomy and ecology of amphibian communities in Southern Vietnam: Linking morphology and bioacoustics Dissertation zur Erlangung des Doktorgrades... elbow and base of inner palmar tubercle; (12) Length of hand (HAL): distance between base of inner palmar tubercle and tip of the longest finger; (13) Length of finger: distance between tip of finger... calls−1)/ duration of time between beginning of the first call and end of the last call; (3) Inter-call interval (s): duration of time between end of the first call and beginning of the second call;