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Larval Systematics of the Peninsular Malaysian Ranidae (Amphibia: Anura)

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Larval Systematics of the Peninsular Malaysian Ranidae (Amphibia: Anura) LARVAL SYSTEMATICS OF THE PENINSULAR MALAYSIAN RANIDAE (AMPHIBIA: ANURA) LEONG TZI MING NATIONAL UNIVERSITY OF SINGAPORE 2005 LARVAL SYSTEMATICS OF THE PENINSULAR MALAYSIAN RANIDAE (AMPHIBIA: ANURA) LEONG TZI MING B.Sc. (Hons.) A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES THE NATIONAL UNIVERSITY OF SINGAPORE 2005 This is dedicated to my dad, mum and brothers. i ACKNOWLEDGEMENTS I am grateful to the many individuals and teams from various institutions who have contributed to the completion of this thesis in various avenues, of which encouragement was the most appreciated. They are, not in any order of preference, from the National University of Singapore (NUS): A/P Peter Ng, Tan Heok Hui, Kelvin K. P. Lim, Darren C. J. Yeo, Tan Swee Hee, Daisy Wowor, Lim Cheng Puay, Malcolm Soh, Greasi Simon, C. M. Yang, H. K. Lua, Wang Luan Keng, C. F. Lim, Yong Ann Nee; from the National Parks Board (Singapore): Lena Chan, Sharon Chan; from the Nature Society (Singapore): Subaraj Rajathurai, Andrew Tay, Vilma D’Rozario, Celine Low, David Teo, Rachel Teo, Sutari Supari, Leong Kwok Peng, Nick Baker, Tony O’Dempsey, Linda Chan; from the Wildlife Department (Malaysia): Lim Boo Liat, Sahir bin Othman; from the Forest Research Institute of Malaysia (FRIM): Norsham Yaakob, Terry Ong, Gary Lim; from WWF (Malaysia): Jeet Sukumaran; from the Economic Planning Unit, Malaysia (EPU): Puan Munirah; from the University of Sarawak (UNIMAS): Indraneil Das; from the National Science Museum, Thailand: Jairujin Nabhitabhata, Tanya Chan-ard, Yodchaiy Chuaynkern; from the University of Kyoto: Masafumi Matsui; from the University of the Ryukyus: Hidetoshi Ota; from my Indonesian friends: Frank Bambang Yuwono, Ibu Mumpuni (MZB), Djoko Iskandar (ITB); from the Philippine National Museum (PNM): Arvin C. Diesmos; from the Wildlife Heritage Trust of Sri Lanka (WHT): Rohan Pethiyagoda, Kelum Manamendra-Arachchi, Mohamed Bahir; from the Senckenberg Museum: Gunther Köhler; from the Museum of Comparative Zoology (MCZ, Harvard): José Rosado; from the Field Museum of Natural History (FMNH, Chicago): Robert F. Inger, Tan Fui Lian, Harold K. Voris, Alan Resetar; from the La Sierra University, California: L. Lee Grismer, J. L. Grismer, Karen Crane; from the University of Texas, Austin: Rafe M. Brown; from the Museum of Vertebrate Zoology, University of California, Berkeley: Jimmy A. McGuire; from the Museum National d’Histoire Naturelle (Paris, France): Annemarie Ohler; and last but certainly not least, the Ford Motor Company Conservation and Environment Awards (2001). ii TABLE OF CONTENTS ACKNOWLEDGEMENTS ………………………………………………………….. ii TABLE OF CONTENTS ………………………………...……………………….…. iii LIST OF FIGURES ………………………………………………………………….. vi LIST OF TABLES ………………………………………………………………..… vii SUMMARY ……………………………………………………………………....... viii INTRODUCTION ……………………………………………………………..……... 1 OBJECTIVES …………………………………………………….…….……..…….... 6 MATERIALS & METHODS ………………………………………………….…...… 7 RESULTS …………………………………………………………………………..… 9 LIST OF GENERA AND SPECIES……………………….....………….………. 10 KEY TO THE KNOWN LARVAE ………...……………………...……………. 12 SYSTEMATIC ACCOUNT & LARVAL DESCRIPTIONS ….………….....….. 14 GENUS AMOLOPS COPE, 1865 …………………………………………… 15 A. larutensis (Boulenger, 1899) ……………………………………... 16 GENUS FEJERVARYA BOLKAY, 1915 …………………………………… 21 F. cancrivora (Gravenhorst, 1829) ………………………………….. 21 F. limnocharis (Gravenhorst, 1829) ………………………………… 24 GENUS HOPLOBATRACHUS PETERS, 1863 …………………………….. 28 H. rugulosus (Wiegmann, 1834) ……………………………………. 29 GENUS INGERANA DUBOIS, 1986 ……………………………………….. 33 I. tennasserimensis (Sclater, 1892) ………………………………….. 33 GENUS LIMNONECTES FITZINGER, 1843 …………………………….... 35 L. blythii (Boulenger, 1920) …………………………………………. 36 L. doriae (Boulenger, 1890) ……………………………………….... 38 L. hascheanus (Stoliczka, 1870) …………………………..………… 39 L. kuhlii (Tschudi, 1838) ……………………………………………. 40 L. laticeps (Boulenger, 1882) ……………………………………….. 43 L. macrognathus (Boulenger, 1917) ……………………………….... 46 L. malesianus (Kiew, 1984) …………………………………………. 46 L. nitidus (Smedley, 1931) …………………………………………... 48 L. paramacrodon (Inger, 1966) …………………………………...… 52 iii L. plicatellus (Stoliczka, 1873) ……………………………………… 52 L. tweediei (Smith, 1935) ……………………………………………. 54 GENUS OCCIDOZYGA KUHL & VAN HASSELT, 1822 ………………... 58 O. laevis Günther, 1858 …..………...………………………………. 59 O. lima (Gravenhorst, 1829) ………………………………………… 63 O. martensii (Peters, 1867) ………………………………………….. 65 GENUS RANA LINNAEUS, 1758 ………………………………………….. 68 R. alticola Boulenger, 1882 …………………………………………. 70 R. banjarana Leong & Lim, 2003 ……………………………………72 R. baramica Boettger, 1901 …………………………………………. 75 R. chalconota (Schlegel, 1837) ……………………………………… 76 R. erythraea (Schlegel, 1837) ……………………………………….. 80 R. glandulosa Boulenger, 1882 ……………………………………... 83 R. hosii Boulenger, 1891 ……………………………………………. 85 R. laterimaculata Barbour & Noble, 1916 ………………………….. 88 R. luctuosa (Peters, 1871) ……………………………………..…….. 90 R. macrodactyla (Günther, 1859) ……………..…………………….. 93 R. miopus Boulenger, 1918 …………………..…………………….... 96 R. nicobariensis (Stoliczka, 1870) …………..………………………. 98 R. nigrovittata (Blyth, 1856) …………………………………….… 101 R. siberu Dring, McCarthy & Whitten, 1990 …………………….... 104 R. signata (Günther, 1872) ………………………………………… 105 CLADISTIC ANALYSIS ………………………………………………………. 109 ECOLOGICAL OBSERVATIONS …………………………………...…….… 110 DISCUSSION …………………………………………………………………….... 113 1 SYSTEMATICS ………………………………………………….…………. 114 1.1 Subgeneric Assignments ………………………………………...………. 114 1.2 Intergeneric Comparisons …………………………………………..…… 114 1.2.1 Genera Fejervarya vs. Limnonectes ……………………………...….. 115 1.2.2 Genus Limnonectes (a) Morphological Analysis ……………………………………….…. 117 (b) Cladistic Analysis …………………………………………….….. 120 1.2.3 Genus Rana (a) Morphological Analysis ………………………………………..… 121 iv (b) Cladistic Analysis ……………………………………………..…. 122 1.3 Revalidation of synonyms ……………………………………………….. 123 2 BIOGEOGRAPHY ……………………………………………..………. 123 3 FUTURE DIRECTIONS ……………………………………………….. 125 REFERENCES …………………………………………………………………….. 127 APPENDICES ……………………………………………………………….…….. 143 1. Updated checklist of Peninsular Malaysian anura ………………………...… 144 2. Comparisons of generic/subgeneric assignments ………………………….... 148 3. Adult specimens examined at ZRC ………………………………….........… 153 4. Data matrices of Limnonectes and Rana ……………………………..…...… 164 5. Text figures ……………………………………………………………..…… 169 v LIST OF FIGURES Fig. 1. Schematic map of Peninsular Malaysia ………………………………..………..………..…… 170 Fig. 2. Schematic diagram of a generalized anuran larva ……………………………...…………..…. 171 Fig. 3. Schematic diagram of a typical tadpole oral disc ……………………………………….…..… 171 Fig. 4. Dorsal and ventral aspects of larval Amolops larutensis (Stage 41) ……………………..…… 172 Fig. 5. Dorsal and ventral aspects of larval Amolops larutensis (Stage 42) ….…………………...….. 173 Fig. 6. Dorsal, lateral aspects, and oral disc of larval Fejervarya cancrivora (Stage 41) ………….… 174 Fig. 7. Dorsal, lateral aspects, and oral disc of larval Fejervarya limnocharis (Stage 41) …………... 175 Fig. 8. Dorsal, lateral aspects, and oral disc of larval Hoplobatrachus rugulosus (Stage 37) …...…… 176 Fig. 9. Jaw musculature of larval Hoplobatrachus rugulosus (Stage 38) ……………………….…… 177 Fig. 10. Dorsal, lateral aspects, and oral disc of larval Limnonectes blythii (Stage 36) …………...…. 178 Fig. 11. Dorsal, lateral aspects, and oral disc of larval Limnonectes kuhlii (Stage 41) ……................ 179 Fig. 12. Dorsal, lateral, and ventral aspects of larval Limnonectes laticeps (Stage 37) …………...…. 180 Fig. 13. Dorsal, lateral aspects, and oral disc of larval Limnonectes malesianus (Stage 39) ……...…. 181 Fig. 14. Dorsal, lateral aspects, and oral disc of larval Limnonectes nitidus (Stage 40) …………...… 182 Fig. 15. Dorsal, lateral aspects, and oral disc of larval Limnonectes plicatellus (Stage 38) ………..... 183 Fig. 16. Dorsal, lateral aspects, and oral disc of larval Limnonectes tweediei (Stage 26) ………..…... 184 Fig. 17. Dorsal and lateral aspects of larval Occidozyga laevis (Stage 26) ………………………...… 185 Fig. 18. Dorsal and lateral aspects of larval Occidozyga lima (Stage 36) ……………...…………….. 186 Fig. 19. Dorsal and lateral aspects of larval Occidozyga martensii .……………………...................... 187 Fig. 20. Lateral, dorsal aspects, and oral disc of larval Rana alticola (Stage 39) ………………….… 188 Fig. 21. Dorsal, lateral aspects, and oral disc of larval Rana banjarana (Stage 27) ……………...….. 189 Fig. 22. Dorsal, lateral, ventral aspects, and oral disc of larval Rana chalconota (Stage 28) ………... 190 Fig. 23. Dorsal, lateral aspects and oral disc of larval Rana erythraea (Stage 37) ………………....... 191 Fig. 24. Dorsal, lateral & ventral aspects, and oral disc of larval Rana glandulosa (Stage 36) ....…… 192 Fig. 25. Dorsal, lateral aspects and oral disc of larval Rana hosii (Stage 26) …………………...…… 193 Fig. 26. Dorsal, lateral aspects and oral disc of larval Rana laterimaculata (Stage 37)…………….... 194 Fig. 27. Dorsal, lateral aspects and oral disc of larval Rana luctuosa (Stage 41) ………………...….. 195 Fig. 28. Lateral, dorsal aspects, and oral disc of larval Rana macrodactyla ……………………...….. 196 Fig. 29. Lateral, dorsal, ventral aspects, and oral disc of larval Rana miopus (Stage 40) ..…………... 197 Fig. 30. Dorsal, lateral aspects, and oral disc of larval Rana nicobariensis (Stage 38) …………….... 198 Fig. 31. Lateral aspects and oral disc of larval Rana nigrovittata (Stages 39 and 42) ……………….. 199 Fig. 32. Dorsal, lateral aspects, and oral disc of larval Rana signata (Stage 31) ………………...…..
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