Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-16T18:37:20.363Z Has data issue: false hasContentIssue false

A new species of Cuora (Testudines: Geoemydidae) from the Miocene of Thailand and its evolutionary significance

Published online by Cambridge University Press:  12 April 2013

WILAILUCK NAKSRI*
Affiliation:
Department of Biology, Faculty of Science, Mahasarakham University, Kantarawichai, Maha Sarakham, Thailand44150 Palaeontological Research and Education Centre, Mahasarakham University, Khamriang, Kantarawichai, Maha Sarakham, Thailand44150
HAIYAN TONG
Affiliation:
Palaeontological Research and Education Centre, Mahasarakham University, Khamriang, Kantarawichai, Maha Sarakham, Thailand44150
KOMSORN LAUPRASERT
Affiliation:
Department of Biology, Faculty of Science, Mahasarakham University, Kantarawichai, Maha Sarakham, Thailand44150
VARAVUDH SUTEETHORN
Affiliation:
Palaeontological Research and Education Centre, Mahasarakham University, Khamriang, Kantarawichai, Maha Sarakham, Thailand44150
JULIEN CLAUDE
Affiliation:
Institut des Sciences de l'évolution de Montpellier, UMR 5554 CNRS, Université de Montpellier 2, cc064, 2, place Eugène Bataillon, 34095, Montpellier, France
*
Author for correspondence: nwilailuck@gmail.com

Abstract

A new species of Cuora, Cuora chiangmuanensis sp. nov., is described on the basis of a nearly complete shell with limb bones from the late Middle – early Late Miocene Chiang Muan Mine, Phayao Province (Northern Thailand). C. chiangmuanensis is distinguished from other fossil and living Cuora species mainly on the basis of its plastral morphology. Among fossil and extant Cuora taxa, the new species appears to be a missing link between the taxa from Southeast Asia and those from East Asia. It represents the earliest record of the genus and demonstrates that by 11–12 Ma, Asian box turtles were already present in Southeast Asia.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Batsch, A. J. G. C. 1788. Versuch einer Anleitung zur Kenntniss und Geschichte der Thiere und Mineralien. Erster Theil. Allgemeine Geschichte der Natur; besondre der Säugthiere, Vögel, Amphibien und Fische. Jena: Akademischen Buchhandlung, 528 pp.Google Scholar
Bell, T. 1825. A monograph of the tortoise having a moveable sternum, with remarks on their arrangement and affinities. Zoological Journal 2, 299310.Google Scholar
Blanck, T. 2005. Cuora yunnanensis (Boulenger, 1906), the Yunnan box turtle, rediscovered after one-hundred years? Radiata 14, 1033.Google Scholar
Blanck, T., McCord, W. P. & Le, M. 2006. On the Variability of Cuora trifasciata (Bell, 1825). Frankfurt am Main: Edition Chimaira.Google Scholar
Bonin, F., Devaux, B. & Dupre, A. 2006. Turtles of the World. London: Johns Hopkins University Press.Google Scholar
Boulenger, G. A. 1906. Descriptions of new reptiles from Yunnan. Annals and Magazine of Natural History, Series 7 17, 567–8.Google Scholar
Bourret, R. 1939. Notes herpétologiques su l'Indochine française. XVIII. Reptiles et batraciens reçus au Laboratoire des Sciences Naturelles de l'Université au cours de l'année 1939. Descriptions de quatre espèces et d'une variété nouvelles. Bulletin Générale d'Instruction Publique 4 (annexe), 540.Google Scholar
Cantor, T. 1842. General features of Chusan, with remarks on the flora and fauna of that island. Annals and Magazine of Natural History, Series 1 9, 265–78, 361–70, 481–93.Google Scholar
Claude, J. & Tong, H. 2004. Early Eocene turtles from Saint Papoul, France, with the comments on the early evolution of modern Testudinoidea. Oryctos 5, 71113.Google Scholar
Cope, E. D. 1868. On the origin of genera. Proceedings of the Academy of Natural Sciences of Philadelphia 20, 242300.Google Scholar
Deng, T. 2006. Chinese Neogene mammal biochronology. Vertebrata Palasiatica 44, 143–63.Google Scholar
Deng, T. & Qi, G.-Q. 2009. Rhinocerotids (Mammalia, Perissodactyla) from Lufengpithecus site, Lufeng, Yunnan. Vertebrata PalAsiatica 47, 135–52.Google Scholar
Ernst, C. H. 1988. Cuora mccordi, a new Chinese box turtle from Guangxi Province. Proceedings of the Biological Society of Washington 101, 466–70.Google Scholar
Fritz, U. & Havas, P. 2007. Checklist of chelonians of the world. Vertebrate Zoology 57, 149368.Google Scholar
Fong, J., Parham, J. & Fu, J. 2002. A reassessment of the distribution of Cuora flavomarginata Gray, 1868 on mainland China. Russian Journal of Herpetology 9 (1), 914.Google Scholar
Gaffney, E. S. & Meylan, P. A. 1988. A phylogeny of turtles. In The Phylogeny and Classification of the Tetrapods, Vol. 1: Amphibians, Reptiles, Birds (ed. Benton, M. J.), pp. 157219. Oxford: Clarendon Press.Google Scholar
Gray, J. E. 1831. Synopsis Reptilium; or Short Descriptions of the Species of Reptiles. Part I. – Cataphracta. Tortoises, Crocodiles, and Enaliosaurians. London: Treuttel, Wurz and Co., 85 pp.CrossRefGoogle Scholar
Gray, J. E. 1855. On some new species of freshwater tortoises from North America, Ceylon and Australia, in the collection of the British Museum. Proceedings of the Zoological Society of London 23, 197202.Google Scholar
Gray, J. E. 1860. On some new species of Mammalia and tortoises from Cambojia. Annals and Magazine of Natural History, Series 3 6, 217–18.Google Scholar
Gray, J. E. 1862. Notice of a new species of Cyclemys from the Lao Mountains, in Siam. Annals and Magazine of Natural History, Series 3 10,157.Google Scholar
Gray, J. E. 1863. Observations on the box tortoises, with the descriptions of three new Asiatic species. Proceedings of the Zoological Society of London 1863, 173–8.Google Scholar
Hasegawa, Y. & Ota, M. 1980. Report on a Pleistocene terrapin, Cyclemys from Katayama Marble Quarry, Mine City, Japan. Science Reports of the Yokohama National University, Section II 27, 4752.Google Scholar
He, T., Zhou, T., Rao, T.-Q. & Zhang, Y.-P. 2007. Molecular identification and phylogenetic position of Cuora yunnanensis . Chinese Science Bulletin 52 (23), 3305–9.Google Scholar
Hirayama, R. 1985. Cladistic analysis of batagurine turtles (Batagurinae: Emydidae: Testudinoidea); a preliminary result. In Studio Palaeocheloniologica 1. Stvdia Geølogica Salmanticensia Volumen Especial 1 (eds. de Broin, F. & Jiménez-Fuentes, E.), pp. 141–57.Google Scholar
Hirayama, R. 2007. Revision of the systematics of the fossil turtles from Japan. Jubilee Publication in Commemoration of Professor Kamei Tadao's 80th Birthday, 145–53.Google Scholar
Honda, M., Yasukawa, Y., Hirayama, R. & Ota, H. 2002. Phylogenetic relationships of the Asian box turtles of the genus Cuora sensu lato (Reptilia: Bataguridae) inferred from mitochondrial DNA sequences. Zoological Science 19, 1305–12.CrossRefGoogle ScholarPubMed
Iverson, J. B. 2008. A checklist of the turtles of the world. http://www.earlham.edu/biology/documents/TurtleNamesOct07.Google Scholar
Iverson, J. B. 1992. A Revised Checklist with Distribution Maps of the Turtles of the World. Richmond, Indiana: Privately Printed.Google Scholar
Iverson, J. B., Brown, R. M., Akre, T. S., Near, T. J., Le, M., Thomson, R. C. & Starkey, D. E. 2007. In search of the tree of life for turtles. In Defining Turtle Diversity: Proceedings of a Workshop on Genetics, Ethics, and Taxonomy of Freshwater Turtles and Tortoises (eds Shaffer, H. B., Fitz Simmons, N. N., Georges, A. & Rhodin, A. G. J.). Chelonian Research Monographs 4, 85106.Google Scholar
Iverson, J. B. & McCord, W. P. 1992. A new subspecies of Cuora galbinifrons (Testudines: Batagurinae) from Hainan Island, China. Proceedings of the Biological Society of Washington 105, 433–9.Google Scholar
Kunimatsu, Y., Ratanasthien, B., Nakaya, H., Saegusa, H. & Nagaoka, S. 2004. Earliest Miocene hominoid from Southeast Asia. American Journal of Physical Anthropology 124, 99108.Google Scholar
Lehr, E., Fritz, U. & Obst, F. J. 1998. Cuora galbinifrons picturata subsp. nov., eine neue Unterart der Hinterindischen Scharnierschildkröte. Herpetofauna 20 (113), 511.Google Scholar
Linnaeus, C. 1758. Systema Naturae, per Regna Tria Naturae, secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Tomus I. Editio Decima, Reformata. [10th ed.]. Holmiae [Stockholm]: Laurentii Salvii, 824 pp.Google Scholar
Luo, B. & Zong, Y. 1988. A new species of CuoraCuora aurocapitata . Acta Herpetologica Sinica 3, 1315.Google Scholar
McCord, W. P. & Iverson, J. B. 1991. A new box turtle of the genus Cuora Testudines Emydidae with taxonomic notes and a key to the species. Herpetologica 47, 407–20.Google Scholar
Nakaya, H., Saegusa, H., Kunimatsu, Y. & Ratanasthien, B. 2002. Miocene mammalian faunas of Northern Thailand and their geological age. Primate Research 18, 131–41 (in Japanese with English abstract).CrossRefGoogle Scholar
Nutaphand, V. 1979. The Turtles of Thailand. Bangkok: Siamfarm Zoological Garden, 222 pp.Google Scholar
Obst, F. J. & Reimann, M. 1994. Bemerkenswerte Variabilität bei Cuora galbinifrons Bourret, 1939, mit Beschreibung einer neuen geographischen Unterart: Cuora galbinifrons bourreti subsp. nov. (Reptilia: Testudines: Criptodira: Bataguridae). Zoologische Abhandlungen, Staatliches Museum für Tierkunde Dresden 48, 125–39.Google Scholar
Parham, J. F. & Li, D. 1999. A new locality for Cuora pani Song 1984 with comments on its known range. Asiatic Herpetological Research 8, 111–13.Google Scholar
Parham, J. F., Simison, W. B., Kozak, K. H., Feldman, C. R. & Shi, H. 2001. New Chinese turtles: endangered or invalid. A reassessment of two species using mitochondrial DNA, allozyme electrophoresis and known-locality specimens. Animal Conservation 4, 357–67.Google Scholar
Parham, J. F., Stuart, B. L., Bour, R. & Fritz, U. 2004. Evolutionary distinctiveness of the extinct Yunnan box turtle (Cuora yunnanensis) revealed by DNA from an old museum specimen. Proceedings of the Royal Society Biological Sciences Series B 271, S391S394.Google Scholar
Pickford, M., Nakaya, H., Kunimatsu, Y., Saegusa, H., Fukuchi, A. & Ratanasthien, B. 2004. Age and taxonomic status of the Chiang Muan (Thailand) hominoids. Comptes Rendus Palevol 3, 6575.Google Scholar
Riche, M. 1801. Testudo amboinensis . In Histoire Naturelle, á Générale et Particulière, des Reptiles. Tome Second (ed. Daudin, F. M.), pp. 309–12. Paris: Dufart.Google Scholar
Schweigger, A. F. 1812. Prodromus monographiae Cheloniorum. Königsberger Archive für Naturwissenschaftliche und Mathematik 1, 271368, 406–58.Google Scholar
Shi, H. 2008. Identification Manual for Trade Turtles in China. Beijing: Encyclopedia of China Publishing House.Google Scholar
Shi, H., Parham, J. F., Simison, W. B., Wang, J., Gong, S. & Fu, B. 2005. A report on the hybridization between two species of threatened Asian box turtles (Testudines: Cuora) in the wild on Hainan Island (China) with comments on the origin of ‘serrata’-like turtles. Amphibia-Reptilia 26 (3): 377–81.Google Scholar
Shikama, T. 1949. The Kuzuü Ossuaries: geological and palaeontological studies of the limestone fissure deposits, in Kuzuü, Totigi Prefecture. Science Report of Tohoku University, 2nd Series (Geology) 23, 1201.Google Scholar
Silaratana, T., Ratanasthien, B., Takayasu, K., Fyfe, W. S., Asnachinda, P., Kandharosa, W. & Kusakabe, M. 2004. Sulfur isotopic implication of Middle Miocene marine incursion in Northern Thailand. Science Asia 30, 4358.Google Scholar
Song, M. T. 1984. A new species of the turtle genus Cuora (Testudoformes: Testudinidae). Acta Zootaxonomica Sinica 9 (3), 330–32.Google Scholar
Spinks, P. Q. & Shaffer, H. B. 2007. Conservation phylogenetics of the Asian box turtles (Geoemydidae, Cuora): mitochondrial introgression, numts, and inferences from multiple nuclear loci. Conservation Genetics 8, 641–57.Google Scholar
Spinks, P. Q., Thomson, R. C., Shaffer, H. B. 2009. A reassessment of Cuora cyclornata Blanck, McCord and Le, 2006 (Testudines, Geoemydidae) and a plea for taxonomic stability. Zootaxa 2018, 5868.Google Scholar
Spinks, P. Q., Thomson, R. C., Zhang, Y., Che, J., Wu, Y. & Shaffer, H. B. 2012. Species boundaries and phylogenetic relationships in the critically endangered Asian box turtle genus Cuora . Molecular Phylogenetics and Evolution 63, 656–67.Google Scholar
Stuart, B. & Parham, J. F. 2004. Molecular phylogeny of the critically endangered Indochinese box turtle (Cuora galbinifrons). Molecular Phylogenetics and Evolution 31, 164–77.Google Scholar
Stuart, B. & Parham, J. F. 2007. Recent hybrid origin of three rare Chinese turtles. Conservation Genetics 8, 169–75.Google Scholar
Suganuma, Y., Hamada, T., Tanaka, S., Okada, M., Nakaya, H., Kunimatsu, Y., Saegusa, H., Nagaoka, S., & Ratanasthien, B. 2006. Magnetostratigraphy of the Miocene Chiang Muan Formation, Northern Thailand: implication for revised chronology of the earliest Miocene hominoid in Southeast Asia. Palaeogeography, Palaeoclimatology, Palaeoecology 239, 7586.Google Scholar
Swofford, D. L. 1998. PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MA.Google Scholar
Takahashi, A., Otsuka, H. & Ota, H. 2008. Systematic review of Late Pleistocene turtles (Reptilia: Chelonii) from the Ryukyu Archipelago, Japan, with special reference to paleogeographical implication. Pacific Science 62 (3), 395402.Google Scholar
Theobald, W. Jr. 1868. Catalogue of Reptiles in the Museum of the Asiatic Society of Bengal. Journal of the Asiatic Society, Extra Number. Calcutta: Printed at the Baptist Mission Press, 88 pp.Google Scholar
Turtle Taxonomy Working Group [Van Dijk, P. P., Iverson, J. B., Shaffer, H. B., Bour, R. & Rhodin, A. G. J.]. 2011. Turtles of the World, 2011 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. In Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group (eds A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, J. B. Iverson & R. A. Mittermeier). Chelonian Research Monographs 5, pp. 000.165–000.242, doi:10.3854/crm.5.000.checklist. v4.2011, http://www.iucn-tftsg.org/cbftt/.Google Scholar
Wang, B.-Y. & Qi, G.-Q. 2005. A procupine (Rodentia, Mammalia) from Lufengpithecus site, Lufeng, Yunnan. Vertebrata PalAsiatica 43, 1123.Google Scholar
Yasukawa, Y., Hirayama, R. & Kikida, T. 2001. Phylogenetic relationships of Geoemydine turtles (Reptilia: Bataguridae). Current Herpetology 20, 105–33.CrossRefGoogle Scholar
Yeh, H.-K. 1961. The first discovery of a box-turtle in China. Vertebrata PalAsiatica 3, 5864.Google Scholar
Yeh, H.-K. 1981. New fossil Cuora (Emydidae) from Early Pliocene of Yunnan. Vertebrata PalAsiatica 19, 239–46.Google Scholar
Yeh, H.-K. 1983. New remains of Cuora from Zhejiang. Vertebrata PalAsiatica 21: 4953.Google Scholar
Yeh, H.-K. 1985 a. Studies on fossils of Cuora of China and Japan. Acta Hepetologica Sinica 4, 81–7.Google Scholar
Yeh, H.-K. 1985 b. New materials of Cuora pitheca and its generic history. Acta Anthropologiga Sinica 6, 113–17.Google Scholar
Yeh, H.-K. 1994 a. Notes on a fossil Cuora (Testudines) from Tongshan, Anhui. Vertebrata PalAsiatica 32, 66–8.Google Scholar
Yeh, H.-K. 1994 b. Fossil and Recent Turtles of China. Beijing: Science Press.Google Scholar
Yeh, H.-K. & Zhang, J. 1994. Turtle remains from Jiahu site at Wuyang, Henan. Acta Anthropologiga Sinica 13, 32–9.Google Scholar
Zhang, L., Nie, L. W., Cao, C. H. & Zhang, Y. 2008. The complete mitochondrial genome of the keeled box turtle Pyxidea mouhotii and phylogenetic analysis of major turtle groups. Journal of Genetics and Genomics 35, 3340.Google Scholar
Zhao, E. 1990. Cuora zhoui . In A new Chinese box turtle (Testudinata: Emydidae) – Cuora zhoui (eds Zhao, E., Zhou, T. & Ye, P.), pp. 213–16. In From Water Onto Land (ed. E. Zhao). Beijing: Chinese Society for the Study of Amphibians and Reptiles (in Chinese).Google Scholar
Zhou, T., Blanck, T., McCord, W. P. & Li, P.-P. 2008. Tracking Cuora mccordi Ernst, 1988: the first record of its natural habitat; a re-description; with data on captive populations and its vulnerability. Hamadryad 32, 5769.Google Scholar
Zhou, T. & Zhao, E. 2004. On the occurrence of living Cuora yunnanensis since fifty-eight years, and its description. Sichuan Journal of Zoology 23, 325–6.Google Scholar