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Type: Article
Published: 2018-09-26
Page range: 31–56
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Taxonomic re-evaluation of the monotypic genus Pararhabdophis Bourret, 1934 (Squamata: Colubridae: Natricinae) with discovery of its type species, P. chapaensis, from China

CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, China. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, Nay Pyi Taw, Myanmar University of Chinese Academy of Sciences, Beijing, China
Sam Noble Oklahoma Museum of Natural History & Department of Biology, University of Oklahoma, Norman, Oklahoma, USA.
Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, Hanoi, Vietnam. Graduate University of Science and Technology, Vietnam Academy of Science and Technology, Hanoi, Vietnam
Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, Hanoi, Vietnam.
College of Life Sciences and Food Engineering, Yibin University, Yibin, Sichuan, China. E-mail: ybguop@163.com
CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, China.
College of Life Sciences and Food Engineering, Yibin University, Yibin, Sichuan, China.
CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, China. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, Nay Pyi Taw, Myanmar University of Chinese Academy of Sciences, Beijing, China
Reptilia Amphiesma Hebius Parahelicops cryptic diversity distribution misidentification new record

Abstract

The Asian monotypic genus Pararhabdophis Bourret, 1934 has long been known from a single holotype of the type species Pararhabdophis chapaensis Bourret, 1934 only. The limited available information hampered the identification of the natricine species. On the basis of eight newly collected specimens of P. chapaensis from the type locality in Sa Pa, Lao Cai Province, Vietnam and from Pingbian, Yunnan Province in southwestern China, the taxonomic position of the genus Pararhabdophis was re-evaluated using both morphological and molecular datasets for the first time. Pararhabdophis chapaensis is nested within the genus Hebius Thompson, 1913 with strong support, and morphologically indistinguishable from the latter genus. As a consequence, we herein synonymize the genus Pararhabdophis with Hebius and discuss about the existing paraphyly of some Hebius species. In addition we report Hebius chapaensis for the first time from China and provide redescription and natural history data of this poorly known species. To facilitate future taxonomic work, an identification key to all known natricine genera from China and Vietnam is also provided.

 

References

  1. Alfaro, M.E. & Arnold, S.J. (2001) Molecular systematics and evolution of Regina and the thamnophiine snakes. Molecular Phylogenetics and Evolution, 21 (3), 408–423.
    https://doi.org/10.1006/mpev.2001.1024

    Bain, R.H., Stuart, B.L., Nguyen, T.Q., Che, J. & Rao, D.Q. (2009) A new Odorrana (Amphibia: Ranidae) from Vietnam and China. Copeia, 2009 (2), 348–362.
    https://doi.org/10.1643/ch-07-195

    Boulenger, G.A. (1893) Catalogue of the Snakes in the British Museum (Natural History). Vol. I. containing the families Typhlopidae, Glauconiidae, Boidae, Ilysiidae, Uropeltidae, Xenopeltidae, and Colubridae Aglyphae, part. British Museum of Natural History, London, xiii + 448 pp., 28 pls.
    https://doi.org/10.5962/bhl.title.54273

    Bourret, R. (1934a) Notes herpétologiques sur l'Indochine française. I. Ophidiens de Chapa. Bulletin général de l'instruction Publique, 13e Année (7 March), 129–138. [in French, separate reprint: 1–10]

    Bourret, R. (1934b) Notes herpétologiques sur l'Indochine française. III. Ophidiens d'Annam et du Moyen Laos. Bulletin général de l'instruction Publique, 13e Année (9 May), 167–176. [in French, separate reprint: 3–12]

    Bourret, R. (1936) Les serpents de l'Indochine. Tome II. Catalogue systématique descriptif. Henri Basuyau et Cie, Toulouse, 505 pp. [in French]

    Burbrink, F.T. & Myers, E.A. (2015) Both traits and phylogenetic history influence community structure in snakes over steep environmental gradients. Ecography, 38 (10), 1036–1048.
    https://doi.org/10.1111/ecog.01148

    Cai, B., Wang, Y.Z., Chen, Y.Y. & Li, J.T. (2015) A revised taxonomy for Chinese reptiles. Biodiversity Science, 23 (3), 365–382. [in Chinese]
    https://doi.org/10.17520/biods.2015037

    Chen, X., Huang, S., Guo, P., Colli, G.R., Nieto Montes de Oca, A., Vitt, L.J., Pyron, R.A. & Burbrink, F.T. (2013) Understanding the formation of ancient intertropical disjunct distributions using Asian and Neotropical hinged-teeth snakes (Sibynophis and Scaphiodontophis: Serpentes: Colubridae). Molecular Phylogenetics and Evolution, 66 (1), 254–261.
    https://doi.org/10.1016/j.ympev.2012.09.032

    Cogger, H.G. (2014) Reptiles and Amphibians of Australia, 7th edition. CSIRO Publishing, Collingwood, xxx + 1033 pp.

    Das, I. (2010) A field guide to the reptiles of South-East Asia. New Holland Publishers, London, 376 pp.
    https://doi.org/10.1108/rr-08-2016-0210

    Das, I. (2012) A naturalist's guide to the snakes of South-East Asia: Malaysia, Singapore, Thailand, Myanmar, Borneo, Sumatra, Java and Bali. John Beaufoy Publishing, Oxford, 160 pp.
    https://doi.org/10.1644/1545-1542(2002)083<0633:>2.0.co;2

    David, P., Agarwal, I., Athreya, R., Mathew, R., Vogel, G. & Mistry, V.K. (2015a) Revalidation of Natrix clerki Wall, 1925, an overlooked species in the genus Amphiesma Duméril, Bibron & Duméril, 1854 (Squamata: Natricidae). Zootaxa, 3919 (2), 375–395.
    https://doi.org/http://dx.doi.org/10.11646/zootaxa.3919.2.9

    David, P., Bain, R.H., Nguyen, T.Q., Orlov, N.L., Vogel, G., Vu, T.N. & Ziegler, T. (2007) A new species of the natricine snake genus Amphiesma from the Indochinese Region (Squamata: Colubridae: Natricinae). Zootaxa, 1462, 41–60.

    David, P., Pauwels, O.S., Nguyen, T.Q. & Vogel, G. (2015b) On the taxonomic status of the Thai endemic freshwater snake Parahelicops boonsongi, with the erection of a new genus (Squamata: Natricidae). Zootaxa, 3948 (2), 203–217.
    https://doi.org/10.11646/zootaxa.3948.2.3

    de Queiroz, A. & Lawson, R. (2008) A peninsula as an island: multiple forms of evidence for overwater colonization of Baja California by the gartersnake Thamnophis validus. Biological Journal of the Linnean Society, 95 (2), 409–424.
    https://doi.org/10.1111/j.1095-8312.2008.01049.x

    de Queiroz, A., Lawson, R. & Lemos-Espinal, J.A. (2002) Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: how much DNA sequence is enough? Molecular Phylogenetics and Evolution, 22 (2), 315–329.
    https://doi.org/10.1006/mpev.2001.1074

    Figueroa, A., McKelvy, A.D., Grismer, L.L., Bell, C.D. & Lailvaux, S.P. (2016) A species-level phylogeny of extant snakes with description of a new colubrid subfamily and genus. PLoS ONE, 11 (9), e0161070.
    https://doi.org/10.1371/journal.pone.0161070

    Fontenot, C.L. (2008) Variation in pupil diameter in North American Gartersnakes (Thamnophis) is regulated by immersion in water, not by light intensity. Vision Research, 48 (15), 1663–1669.
    https://doi.org/10.1016/j.visres.2008.01.006

    Günther, A. (1860) Contributions to a knowledge of the reptiles of the Himalaya mountains. -I. Descriptions of the new species. II. List of Himalayan reptiles, with remarks on their horizontal distribution. Proceedings of the Zoological Society of London, 1860, 148–175.

    Giri, V.B., Deepak, V., Captain, A., Das, A., Das, S., Rajkumar, K.P., Rathish, R.L. & Gower, D.J. (2017) A new species of Rhabdops Boulenger, 1893 (Serpentes: Natricinae) from the northern Western Ghats region of India. Zootaxa, 4319 (1), 27–52.
    https://doi.org/10.11646/zootaxa.4319.1.2

    Guicking, D., Lawson, R., Joger, U. & Wink, M. (2006) Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). Biological Journal of the Linnean Society, 87 (1), 127–143.
    https://doi.org/10.1111/j.1095-8312.2006.00561.x

    Guo, P., Liu, Q., Xu, Y., Jiang, K., Hou, M., Ding, L., Pyron, R.A. & Burbrink, F.T. (2012) Out of Asia: natricine snakes support the Cenozoic Beringian Dispersal Hypothesis. Molecular Phylogenetics and Evolution, 63 (3), 825–833.
    https://doi.org/10.1016/j.ympev.2012.02.021

    Guo, P., Zhu, F., Liu, Q., Zhang, L., Li, J.X., Huang, Y.Y. & Pyron, R.A. (2014) A taxonomic revision of the Asian keelback snakes, genus Amphiesma (Serpentes: Colubridae: Natricinae), with description of a new species. Zootaxa, 3873 (4), 425–440.
    https://doi.org/10.11646/zootaxa.3873.4.5

    Koch, A. (2008) Discovery of new specimens of Sarasin's Keelback, Amphiesma sarasinorum (Boulenger, 1896), endemic to Southwest Sulawesi, Indonesia. Herpetozoa, 20 (3–4), 178–182.

    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34 (3), 772–773.
    https://doi.org/10.1093/molbev/msw260

    Lawson, R., Slowinski, J.B., Crother, B.I. & Burbrink, F.T. (2005) Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 37 (2), 581–601.
    https://doi.org/10.1016/j.ympev.2005.07.016

    Le, T.D., Dao, N.A., Pham, T.D., Ziegler, T. & Nguyen, Q.T. (2018) New records and an updated list of snakes from Yen Bai Province, Vietnam. Herpetology Notes, 11 (2018), 101–108.

    Malnate, E.V. (1961) Amphiesmoides, a new genus for Tropidonotus ornaticeps Werner (Serpentes: Colubridae). Proceedings of the Academy of Natural Sciences of Philadelphia, 341, 1–7.

    Murphy, J.C., Chan-ard, T., Mekchai, S., Cota, M. & Voris, H.K. (2008) The Rediscovery of Angel's Stream Snake, Paratapinophis praemaxillaris Angel, 1929 (Reptilia: Serpentes: Natricidae). The Natural History Journal of Chulalongkorn University, 8 (2), 169–183.

    Myers, C.W. (1984) Subcircular pupil shape in the snake Tantalophis (Colubridae). Copeia, 1984 (1), 215–216.
    https://doi.org/10.2307/1445058

    Nguyen, S.V. & Ho, C.T. (1996) A checklist of reptiles and amphibians in Vietnam. Science and Technology Publishing House, Hanoi, 264 pp. [in Vietnamese]

    Nguyen, S.V., Ho, C.T. & Nguyen, T.Q. (2009) Herpetofauna of Vietnam. Edition Chimaira, Frankfurt am Main, 768 pp.

    Nguyen, T.Q., David, P., Tran, T.T., Luu, V.Q., Le, Q.K. & Ziegler, T. (2010) Amphiesmoides ornaticeps (Werner, 1924), an addition to the snake fauna of Vietnam, with a redescription and comments on the genus Amphiesmoides Malnate, 1961 (Squamata: Natricidae). Revue Suisse de Zoologie, 117 (1), 45–56.
    https://doi.org/10.5962/bhl.part.117587

    Nguyen, T.V., Nguyen, T.Q., Pham, C.T. & Ziegler, T. (2018) First country record of Opisthotropis maculosa Stuart & Chuaynkern, 2007 from Vietnam. Russian Journal of Herpetology. 25 (1), 74–78.

    Orlov, N.L., Ryabov, S.A., Nguyen, V.S. & Nguyen, Q.T. (2003) New records and data on the poorly known snakes of Vietnam. Russian Journal of Herpetology, 10 (3), 217–240.

    Pham, A.V., Nguyen, N.T.B., Nguyen, M.T., Nguyen, S.L.H. & Nguyen, T.Q. (2013) New records of snakes (Reptilia: Squamata: Serpentes) from Son La Province. In: Proceedings of the 5th National Scientific Conference on Ecology and Biological Resources. Hanoi Agricultural Publisher, Hanoi, pp. 16–22. [in Vietnamese]

    Pope, C.H. (1935) The reptiles of China. Turtles, crocodilians, snakes, lizards. American Museum of Natural History, New York, xlii + 604 pp., 27 pls.

    Pyron, R.A., Kandambi, H.K., Hendry, C.R., Pushpamal, V., Burbrink, F.T. & Somaweera, R. (2013) Genus-level phylogeny of snakes reveals the origins of species richness in Sri Lanka. Molecular Phylogenetics and Evolution, 66 (3), 969–978.
    https://doi.org/10.1016/j.ympev.2012.12.004

    Rambaut, A., Suchard, M., Xie, D. & Drummond, A. (2013) Tracer, version 1.6, MCMC trace analysis package. Available from: http://tree.bio.ed.ac.uk/software/tracer/ (accessed 7 March 2018)

    Ren, J.-L., Wang, K., Jiang, K., Guo, P. & Li, J.-T. (2017) A new species of the Southeast Asian genus Opisthotropis (Serpentes: Colubridae: Natricinae) from western Hunan, China. Zoological Research, 38 (5), 251–263.
    https://doi.org/10.24272/j.issn.2095-8137.2017.068

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574.
    https://doi.org/10.1093/bioinformatics/btg180

    Smith, M.A. (1943) The fauna of British India, Ceylon and Burma, including the whole of the Indo-chinese subregion. Reptilia and Amphibia. Vol. III. Serpentes. Taylor & Francis, London, xii + 583 pp.

    Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313.

    https://doi.org/10.1093/bioinformatics/btu033

    Stuart, B.L. (2006) A second specimen of Parahelicops annamensis Bourret, 1934 (Serpentes: Colubridae: Natricinae). Hamadryad, 30 (1–2), 167–171.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Thompson, J.C. (1913) Contributions to the anatomy of the Ophidia. Proceedings of the Zoological Society of London, 414–425.
    https://doi.org/10.1111/j.1469-7998.1913.tb06139.x

    Wall, F. (1910) A new Tropidonotus from the Chin Hills. The Journal of the Bombay Natural History Society, 20, 345–346.

    Wallach, V., Williams, K.L. & Boundy, J. (2014) Snakes of the world. A catalogue of living and extinct species. CRC Press, Boca Raton, xxvii + 1209 pp.
    https://doi.org/10.1201/b16901

    Wang, K., Jiang, K., Wang, Y.F., Poyarkov, N.A.J., Che, J. & Siler, C.D. (2018) Rediscovery of Japalura chapaensis Bourret, 1937 (Reptilia: Squamata: Agamidae) from Southeast Yunnan Province, China. Zoological Research, 39 (2), 105–113.

    https://doi.org/10.24272/j.issn.2095-8137.2017.064

    Wang, K., Ren, J.L., Jiang, K., Yuan, Z.Y., Che, J. & Siler, C.D. (2017a) Rediscovery of the enigmatic Mountain Dragon, Japalura yulongensis (Reptilia: Sauria: Agamidae), with notes on its natural history and conservation. Zootaxa, 4318 (2), 351–363.
    https://doi.org/10.11646/zootaxa.4318.2.8

    Wang, Y.Y., Guo, Q., Liu, Z.Y., Lyu, Z.T., Wang, J., Luo, L., Sun, Y.J. & Zhang, Y.W. (2017b) Revisions of two poorly known species of Opisthotropis Günther, 1872 (Squamata: Colubridae: Natricinae) with description of a new species from China. Zootaxa, 4247 (4), 391–412.
    https://doi.org/10.11646/zootaxa.4247.4.3

    Werner, Y.L. (1967) Dark adaptation of the vertical pupil in a snake. Herpetologica, 23 (1), 62–63.

    Werner, Y.L. (1970) Extreme adaptability to light, in the round pupil of the snake Spalerosophis. Vision Research, 10 (11), 1159–1164.
    https://doi.org/10.1016/0042-6989(70)90033-7

    Zaher, H., Grazziotin, F.G., Cadle, J.E., Murphy, R.W., Moura-Leite, J.C.D. & Bonatto, S.L. (2009) Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia, 49 (11), 115–153.
    https://doi.org/10.1590/s0031-10492009001100001

    Zhao, E.M. (2006) Snakes of China. I. Anhui Science and Technology Publishing House, Hefei, 372 pp. [in Chinese]

    Zhao, E.M. & Adler, K. (1993) Herpetology of China. Society for the Study of Amphibians and Reptiles: Contribution to Herpetology. No. 10. SSAR, Oxford/Ohio, 522 pp., 48 pls.

    Zhao, E.M., Huang, M.H. & Zong, Y. (1998) Fauna Sinica Reptilia, Vol. 3: Squamata, Serpentes. Science Press, Beijing, xvii + 522 pp., 4 pls. [in Chinese]

    Zhu, G.X., Wang, Y.Y., Takeuchi, H. & Zhao, E.M. (2014) A new species of the genus Rhabdophis Fitzinger, 1843 (Squamata: Colubridae) from Guangdong Province, southern China. Zootaxa, 3765 (5), 469–480.
    https://doi.org/10.11646/zootaxa.3765.5.5

    Ziegler, T., David, P., Ziegler, T.N., Pham, C.T., Nguyen, T.Q. & Le, M.D. (2018) Morphological and molecular review of Jacob’s Mountain Stream Keelback Opisthotropis jacobi Angel & Bourret, 1933 (Squamata: Natricidae) with description of a sibling species from northern Vietnam. Zootaxa, 4374 (4), 476–496.
    https://doi.org/10.11646/zootaxa.4374.4.2

    Ziegler, T. & Le, Q.K. (2006) A new natricine snake of the genus Amphiesma (Squamata: Colubridae: Natricinae) from the central Truong Son, Vietnam. Zootaxa, 1225, 39–56.