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Issue: Vol. 5604 No. 4: 17 Mar. 2025
Type: Article
Published: 2025-03-17
DOI: 10.11646/zootaxa.5604.4.3
Page range: 465-504
Abstract views: 224
PDF downloaded: 4

Same but different: A systematic reassessment of the Hebius khasiensis Boulenger, 1890 (Reptilia: Squamata: Natricidae) species complex from the Indo-Burma biodiversity hotspot supports the revalidation of Natrix gilhodesi Wall, 1925 as a valid species

Help Earth; 16; Raghunath Choudhury Path; Lachitnagar; Guwahati; Assam; India.
College of Medicine and Pharmacy; Duy Tan University; 120 Hoang Minh Thao; Lien Chieu; Da Nang; 550000; Vietnam.
Society for South East Asian Herpetology; Im Sand-3; Heidelberg; Germany.
Developmental Biology and Herpetology Laboratory; Department of Zoology; Mizoram University; 796004 Tanhril; Mizoram; India.
Developmental Biology and Herpetology Laboratory; Department of Zoology; Mizoram University; 796004 Tanhril; Mizoram; India.
Help Earth; 16; Raghunath Choudhury Path; Lachitnagar; Guwahati; Assam; India.; Department of Zoology; Assam Don Bosco University; Sonapur; India.
Department of Zoology; Assam Don Bosco University; Sonapur; India.
Rohbah; South West Khasi Hills District; Mawkyrwat; Meghalaya 793114; India.
Department of Vertebrate Zoology; Lomonosov Moscow State University; Leninskiye Gory; GSP–1; Moscow 119991; Russia.; Joint Vietnam - Russia Tropical Science and Technology Research Centre; Nghia Do; Cau Giay; Hanoi; Vietnam.
Help Earth; 16; Raghunath Choudhury Path; Lachitnagar; Guwahati; Assam; India.; Department of Zoology; Assam Don Bosco University; Sonapur; India.
Reptilia cytochrome b keelback snake taxonomy north-east India

Abstract

This study provides new insights into the systematics of the natricid species Hebius khasiensis Boulenger sensu lato. Our findings are based on recent collections from northeast India, including the type locality in the Khasi Hills, Meghalaya, and the examination of its syntypes. There is a species named Natrix gilhodesi Wall from Kachin State, Myanmar, which is currently considered a subjective junior synonym of H. khasiensis, but molecular data based on the mitochondrial gene analysis show that populations from northeast India and Kachin, Myanmar are deeply divergent from each other. Here, we redescribe H. khasiensis and designate an adult female from its syntypes as the lectotype for the taxonomic stability of the given species. We also revalidate Natrix gilhodesi from Myanmar as a valid species of the genus Hebius based on molecular and morphological parameters.

 

References

  1. Ahmed, F., Das, A. & Dutta, S.K. (2009) Amphibians and Reptiles of Northeast India: A Photographic Guide. Aaranyak, Guwahati (Assam), xiv + 169 pp., map.
  2. Annandale, N. (1905) Additions to the collection of Oriental snakes in the Indian Museum. Part 3. Journal of the Asiatic Society of Bengal, 1905, 208–214.
  3. Annandale, N. (1912) Zoological results of the Abor Expedition. II. Reptilia. Records of the Indian Museum, 8, 37–55, pl. 5. https://doi.org/10.26515/rzsi/v8/i1/1912/163134
  4. Ao, J., David, P., Bordoloi, S. & Ohler, A. (2004) Notes on a collection of snakes from Nagaland, northeast India, with 19 new records for this state. Russian Journal of Herpetology, 11, 155–162. https://doi.org/10.30906/1026-2296-2004-11-2-155-162
  5. Boulenger, G.A. (1890) The Fauna of British India, including Ceylon and Burma: Reptilia and Batrachia. Taylor & Francis, London, xviii + 541 pp. https://doi.org/10.5962/bhl.title.100797
  6. Boulenger, G.A. (1893a) Viaggio di Leonardo Fea in Birmania e regioni vicine. LII. Concluding report on the Reptiles and Batrachians obtained in Burma by Signor L. Fea, dealing with the collection made in Pegu and the Karin Hills in 1887–1888. Annali del Museo Civico di Storia Naturale di Genova, Series 2, 13 (33), 304–347, pls. 7–12.
  7. Boulenger, G.A. (1893b). 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.
  8. Bourret, R. (1936a) Les Serpents de l’Indochine. Tome I. Études sur la faune. Henri Basuyau et Cie, Toulouse, 141 pp.
  9. Bourret, R. (1936b) Les Serpents de l’Indochine. Tome II. Catalogue systématique descriptif. Henri Basuyau et Cie, Toulouse, 505 pp.
  10. Burbrink, F.T., Lawson, R. & Slowinski, J.B. (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution, 54, 2107–2118. https://doi.org/10.1111/j.0014-3820.2000.tb01253.x
  11. Chan-ard, T., Parr, J.W.K. & Nabhitabhata, J. (2015) A Field Guide to the Reptiles of Thailand. Oxford University Press, New York, New York, 352 pp.
  12. Chan, K.O. & Grismer, L.L. (2022) GroupStruct: An R package for allometric size correction. Zootaxa, 5124 (4), 471–482. https://doi.org/10.11646/zootaxa.5124.4.4
  13. Das, I. (1996) Biogeography of the Reptiles of South Asia. Krieger Publishing Company, Malabar, Florida, vii + 87 pp.
  14. David, P. & Das, I. (2003) A new species of the snake genus Amphiesma (Serpentes: Colubridae: Natricinae) from western Sumatra, Indonesia. Raffles Bulletin of Zoology, 51, 413–420.
  15. David, P. & Vogel, G. (2010) A new species of the natricine snake genus Amphiesma from Borneo (Squamata: Natricidae). Russian Journal of Herpetology, 17, 121–127. https://doi.org/10.30906/1026-2296-2010-17-2-121-127
  16. David, P., Agarwal, I., Athreya, R., Mathew, R., Vogel, G. & Mistry, V.K. (2015) 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/10.11646/zootaxa.3919.2.9
  17. David, P., Bain, R.H., Nguyen, Q.T., Orlov, N.L., Vogel, G., Vu, N.T. & Ziegler, T. (2007) A new species of the natricine snake genus Amphiesma from the Indochinese Region (Squamata: Colubridae: Natricinae). Zootaxa, 1462 (1), 41–60. https://doi.org/10.11646/zootaxa.1462.1.2
  18. David, P., Vogel, G. & Van Rooijen, J. (2013) On some taxonomically confused species of the genus Amphiesma Duméril, Bibron & Duméril, 1854 related to Amphiesma khasiense (Boulenger, 1890) (Squamata, Natricidae). Zootaxa, 3694 (4), 301–335. https://doi.org/10.11646/zootaxa.3694.4.1
  19. David, P., Vogel, G., Nguyen, T.Q., Orlov, N.L., Pauwels, O.S.G., Teynié, A. & Ziegler, T. (2021) A revision of the dark-bellied, stream-dwelling snakes of the genus Hebius (Reptilia: Squamata: Natricidae) with the description of a new species from China, Vietnam and Thailand. Zootaxa, 4911 (1), 1–61. https://doi.org/10.11646/zootaxa.4911.1.1
  20. Deepak, V., Cooper, N., Poyarkov, N.A., Kraus, F., Burin, G., Das, A., Narayanan, S., Streicher, J.W., Smith, S.J. & Gower, D.J. (2022) Multilocus phylogeny, natural history traits and classification of natricine snakes (Serpentes: Natricinae). Zoological Journal of the Linnean Society, 195 (1), 279–298. https://doi.org/10.1093/zoolinnean/zlab099
  21. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
  22. Gao, Z.Y., Huang, J.J., Ding, L., Jiang, K. & Mao, J. (2024) Taxonomic re-evaluation of the subspecies of Hebius vibakari (Boie, 1826) (Reptilia: Serpentes: Natricidae), with new evidence from central and northern China. Zootaxa, 5474 (5), 503–521. https://doi.org/10.11646/zootaxa.5474.5.3
  23. Grismer, L.L., Chav, T., Neang, T., Wood, P.L. Jr., Grismer, J.L., Youmans, T.M., Ponce, A., Daltry, J.C. & Kaiser, H. (2007) The herpetofauna of the Phnom Aural Wildlife Sanctuary and checklist of the herpetofauna of the Cardamom Mountains, Cambodia. Hamadryad, 31, 216–241.
  24. Günther, A. (1875) Second report on collections of Indian Reptiles obtained by the British Museum. Proceedings of the Zoological Society of London, 1875, 224–234.
  25. 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
  26. Hauser, S., Smits, T. & David, P. (2022) On the distribution of the species of the genus Hebius Thompson, 1913 (Squamata: Natricidae) in northern Thailand, including the description of a new species and a discussion on snake diversity of this region. Zootaxa, 5116 (1), 1–39. https://doi.org/10.11646/zootaxa.5116.1.1
  27. Hou, S.B., Yuan, Z.Y., Wei, P.F., Zhao, G.G., Liu, G.H., Wu, Y.H., Shen, W.J., Chen, J.M., Guo, P. & Che, J. (2021) Molecular phylogeny and morphological comparisons of the genus Hebius Thompson, 1913 (Reptilia: Squamata: Colubridae) uncover a new taxon from Yunnan Province, China, and support revalidation of Hebius septemlineatus (Schmidt, 1925). Zoological Research, 42, 620–625. https://doi.org/10.24272/j.issn.2095-8137.2021.093
  28. Jeong, T.J., Jun, J., Han, S., Kim, H.T., Oh, K. & Kwak, M. (2013) DNA barcode reference data for the Korean herpetofauna and their applications. Molecular Ecology Resources, 13 (6), 1019–1032. https://doi.org/10.1111/1755-0998.12055
  29. Kaito, T. & Mamoru, T. (2016) The biogeographical history of Asian keelback snakes of the genus Hebius (Squamata: Colubridae: Natricinae) in the Ryukyu Archipelago, Japan. Biological Journal of the Linnean Society, 118 (2), 187–199. https://doi.org/10.1111/bij.12726
  30. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  31. Kambayashi, C., Kakehashi, R., Sato, Y., Mizuno, H., Tanabe, H., Rakotoarison, A., Künzel, S., Furuno, N., Ohshima, K., Kumazawa, Y. & Nagy, Z.T. (2022) Geography-dependent horizontal gene transfer from vertebrate predators to their prey. Molecular Biology and Evolution, 39 (4), msac052. https://doi.org/10.1093/molbev/msac052
  32. Kizirian, D., Nguyen, T.Q., Ngo, T.H. & Le, D.M. (2018) Parahelicops, Pararhabdophis, paraphyly: phylogenetic relationships among certain Southeast Asian natricine snakes (Hebius). American Museum Novitates, 3906, 1–7. https://doi.org/10.1206/3906.1
  33. Koch, A. (2008) Discovery of new specimens of Sarasin’s Keelback, Amphiesma sarasinorum (Boulenger, 1896), endemic to Southwest Sulawesi, Indonesia. Herpetozoa, 20, 178–182.
  34. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  35. 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, 772–773. https://doi.org/10.1093/molbev/msw260
  36. Li, J.N., Liang, D., Wang, Y.Y., Guo, P., Huang, S. & Zhang, P. (2020) A large-scale systematic framework of Chinese snakes based on a unified multilocus marker system. Molecular Phylogenetics and Evolution, 148, 106807. https://doi.org/10.1016/j.ympev.2020.106807
  37. Li, M.L., Ren, J.L., Huang, J.J., Lyu, Z.T., Qi, S., Jiang, K. & Wang, Y.Y. (2022) On the validity of Hebius sauteri maximus (Malnate, 1962) (Squamata, Natricidae), with the redescription of H. maximus comb. nov. and H. sauteri (Boulenger, 1909). Herpetozoa, 35, 265–282. https://doi.org/10.3897/herpetozoa.35.e94920
  38. Liu, Q., Zhong, G.H., Wang, P., Liu, Y. & Guo, P. (2018) A new species of the genus Hebius (Squamata: Colubridae) from Sichuan, China. Zootaxa, 4483 (2), 385–394. https://doi.org/10.11646/zootaxa.4483.2.10
  39. Ma, S., Shi, S., Ayi, B. & Jiang, J. (2023) A new species of the genus Hebius Thompson, 1913 (Serpentes: Natricidae) from Yunnan, China. Asian Herpetological Research, 14, 212–226. https://doi.org/10.3724/ahr.2095-0357.2023.0008
  40. Mahendra, B.C. (1984) Handbook of the Snakes of India, Ceylon, Burma, Bangladesh and Pakistan. Annals of Zoology, Agra (B), 22, i–xvi + 1–412.
  41. Malnate, E.V. (1960) Systematic division and evolution of the colubrid snake genus Natrix, with comments on the subfamily Natricinae. Proceedings of the Academy of Natural Sciences of Philadelphia, 112, 41–71. https://doi.org/10.2307/1439618
  42. Malsawmdawngliana, B., Boruah, N.G., Patel, S., Lalronunga, I., Zosangliana, K., Lalhmangaiha & Das, A. (2022) An updated checklist of reptiles from Dampa Tiger Reserve, Mizoram, India, with sixteen new distribution records. Journal of Threatened Taxa, 14, 21946–21960. https://doi.org/10.11609/jott.8004.14.10.21946-21960
  43. Maury, N., David, P. & Sudavanh, S. (2022) The snake fauna of Laos with new provincial records. Taprobanica, 11, 84–93. https://doi.org/10.47605/tapro.v11i2.284
  44. Minh, B.Q., Nguyen, M.A.T. & Von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188–1195. https://doi.org/10.1093/molbev/mst024
  45. Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
  46. Ota, H. & Iwanaga, S. (1997) A systematic review of the snakes allied to Amphiesma pryeri (Boulenger) (Squamata: Colubridae) in the Ryukyu Archipelago, Japan. Zoological Journal of the Linnean Society, 121, 339–360. https://doi.org/10.1111/j.1096-3642.1997.tb00341.x
  47. Pauwels, O.S.G., Kunya, K., David, P., Waengsothorn, S. & Sumontha, S. (2009) On the occurrence of Amphiesma khasiense (Serpentes: Natricidae) in Thailand. Hamadryad, 34, 75–79.
  48. Purkayastha, J. & David, P. (2019) A new species of the snake genus Hebius Thompson from Northeast India (Squamata: Natricidae). Zootaxa, 4555 (1), 79–90. https://doi.org/10.11646/zootaxa.4555.1.6
  49. Ren, J., Wang, K., Nguyen, T.T., Hoang, C.V., Zhong, G., Jiang, K., Guo, P. & Li, J. (2018) Taxonomic re-evaluation of the monotypic genus Pararhabdophis Bourret, 1934 (Squamata: Colubridae: Natricinae) with discovery of its type species, P. chapaensis, from China. Zootaxa, 4486 (1), 31–56. https://doi.org/10.11646/zootaxa.4486.1.2
  50. Sharma, R.C. (2004) Handbook—Indian Snakes. Zoological Survey of India, Kolkata, vi + 292 pp., 69 pls.
  51. Smith, M.A. (1940) The amphibians and reptiles obtained by Mr. Ronald Kaulback in Upper Burma. Records of the Indian Museum, 43, 465–486.
  52. Smith, M.A. (1943) The Fauna of British India, Ceylon and Burma, including the whole of the Indo-Chinese Sub-region: Reptilia and Amphibia. Vol. III. Serpentes. Taylor & Francis, London, xii + 583 pp.
  53. Stuart, B.L., Sok, K. & Neang, T. (2006). A collection of amphibians and reptiles from hilly eastern Cambodia. The Raffles Bulletin of Zoology, 54 (1), 129–155.
  54. Takeuchi, H., Savitzky, A.H., Ding, L., de Silva, A., Das, I., Nguyen, T.T., Tsai, T.S., Jono, T., Zhu, G.X., Mahaulpatha, D. & Tang, Y. (2018) Evolution of nuchal glands, unusual defensive organs of Asian natricine snakes (Serpentes: Colubridae), inferred from a molecular phylogeny. Ecology and evolution, 8 (20), 10219–10232. https://doi.org/10.1002/ece3.4497
  55. Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
  56. Thompson, J.C. (1913) Contributions to the anatomy of the Ophidia. Proceedings of the Zoological Society of London, Pt. 3–4, 414–425. https://doi.org/10.1111/j.1469-7998.1913.tb06139.x
  57. Thorpe, R.S. (1975) Quantitative handling of characters useful in snake systematics withparticular reference to intraspecific variation in the Ringed Snake Natrix natrix. Biological Journal of the Linnean Society, 7, 27–43. https://doi.org/10.1111/j.1095-8312.1975.tb00732.x.
  58. Van Nguyen, T., Lalremsanga, H.T., Biakzuala, L. & Vogel, G. (2024) Taxonomic reassessment of the Herpetoreas xenura (Wall, 1907) (Squamata: Serpentes: Natricidae) from Myanmar with description of a new species. European Journal of Taxonomy, 932, 158–203. https://doi.org/10.5852/ejt.2024.932.2519
  59. Wall, F. (1908) Notes on a collection of snakes from the Khasi Hills, Assam. Journal of the Bombay Natural History Society, 18, 312–337.
  60. Wall, F. (1923) A hand-list of the snakes of the Indian Empire. Journal of the Bombay Natural History Society, 29, 598–632.
  61. Wall, F. (1925a) Two new Burmese snakes. Journal of the Bombay Natural History Society, 30, 587–588.
  62. Wall, F. (1925b) Notes on snakes collected in Burma in 1924. Journal of the Bombay Natural History Society, 30, 805–821.
  63. Wall, F. (1926) Snakes collected in Burma in 1925. Journal of the Bombay Natural History Society, 31, 558–566.
  64. Wallach, V., Williams, K.L. & Boundy, J. (2014) Snakes of the World: A Catalogue of Living and Extinct Species. CRC Press, Boca Raton, Florida, 1237 pp. https://doi.org/10.1201/b16901
  65. Wang, K., Yu, Z.B., Wu, Y.H., Hou, S.B., Gao, W., Duan, S.H., Xiong, Y., Jiang, Y.F., Liu, K.C., Li, J.H. & Yang, Q. (2024) Herpetofauna diversity of the Gaoligong Mountain in China: Checklist, zoogeography, and conservation. Zoological Research: Diversity and Conservation, 1 (3), 169–179. https://doi.org/10.24272/j.issn.2097-3772.2024.003
  66. Whitaker, R. & Captain, A. (2004) Snakes of India: The Field Guide. Draco Books, Chennai, xiv + 479 pp.
  67. Xu, Y.H., Yang, D.C., Gong, Y.A., Ouyang, K.C., Weng, S.Y., Deng, J.D. & Huang, S. (2024) A new species of the genus Hebius (Squamata, Natricidae) from Yunnan, China. ZooKeys, 1206, 255–266. https://doi.org/10.3897/zookeys.1206.123841
  68. Xu, Y.H., Yang, D.C., Gong, Y.A., Wu, J.X., Huang, R.Y., Liu, Y.J., Liang, S.M., Huang, T.Q. & Huang, S. (2023) A new species of the genus Hebius Thompson, 1913 (Squamata: Colubridae) from Baise, Guangxi, China. Zootaxa, 5319 (1), 76–90. https://doi.org/10.11646/zootaxa.5319.1.5
  69. Zhou, Z., Sun, Z., Qi, S., Lu, Y., Lyu, Z., Wang, Y. & Li, P. (2019) A new species of the genus Hebius (Squamata: Colubridae: Natricinae) from Hunan Province, China. Zootaxa, 4674 (1), 68–82. https://doi.org/10.11646/zootaxa.4674.1.3
  70. Ziegler, T. & Le Khac, Q. (2006) A new natricine snake of the genus Amphiesma (Squamata: Colubridae: Natricinae) from the central Truong Son, Vietnam. Zootaxa, 1225, 39–56. https://doi.org/10.11646/zootaxa.1225.1.4