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Type: Article
Published: 2024-07-01
Page range: 375-411
Abstract views: 333
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A new species of green pitviper of the Trimeresurus macrops complex (Reptilia: Serpentes: Viperidae) from South Central Coastal Region of Vietnam

Department of Vertebrate Zoology; Lomonosov Moscow State University; Leninskiye Gory; GSP–1; Moscow 119991; Russia
Institute for Research and Training in Medicine; Biology and Pharmacy; Duy Tan University; Da Nang; 550000; Vietnam; College of Medicine and Pharmacy; Duy Tan University; 120 Hoang Minh Thao; Lien Chieu; Da Nang; 550000; Vietnam; Joint Vietnam – Russia Tropical Science and Technology Research Center; Nghia Do; Cau Giay; Hanoi; Vietnam
Department of Vertebrate Zoology; Lomonosov Moscow State University; Leninskiye Gory; GSP–1; Moscow 119991; Russia; Joint Vietnam – Russia Tropical Science and Technology Research Center; Nghia Do; Cau Giay; Hanoi; Vietnam
Rabbit in the Moon foundation; Suanphueng; Ratchaburi 70180; Thailand; Division of Fishery; School of Agriculture and Natural Resources; University of Phayao; Phayao; Thailand
Joint Vietnam – Russia Tropical Science and Technology Research Center; Nghia Do; Cau Giay; Hanoi; Vietnam
Society for South East Asian Herpetology; Im Sand-3; D-69115 Heidelberg; Germany
Reptiles & Amphibiens; UMR 7205 OSEB; Département évolution et Systématique; CP 30; Muséum National d’Histoire Naturelle. 57 rue Cuvier; F-75231 Paris Cedex 05; France
Department of Vertebrate Zoology; Lomonosov Moscow State University; Leninskiye Gory; GSP–1; Moscow 119991; Russia; Joint Vietnam – Russia Tropical Science and Technology Research Center; Nghia Do; Cau Giay; Hanoi; Vietnam
Reptilia Trimeresurus cyanolabris sp. nov. Vietnam new species morphology molecular phylogeny systematics

Abstract

We describe a new species of green pitviper from southern and central parts of coastal Vietnam based on morphological and molecular (2406 bp from cyt b, ND4, and 16S rRNA mitochondrial DNA genes) lines of evidence. Trimeresurus cyanolabris sp. nov. is distinguished from its congeners by the combination of the following morphological characters: small size, maximum known SVL of 638 mm; dorsal scales in 21 (rarely 23)–21–15 rows, moderately keeled except the outermost rows; ventral scales 166–178; subcaudal scales 52–75, all paired; hemipenis forked, calyculate, reaching the 8th subcaudal; eye bright yellow in both sexes; dorsal surface deep green lacking cross-bands; postocular white stripe missing in both sexes; ventrolateral stripe faintly present on the first few dorsal scale rows in males, absent in females; throat, chin, and lower labials in shades of blue. The new species forms a distinct clade on the phylogenetic tree of the genus Trimeresurus and differs from the morphologically similar T. rubeus by a significant divergence in cytochrome b mitochondrial DNA gene sequences (p = 6.0%). The new species is currently known from low- to mid-elevations (ca. 90–400 m a.s.l.) in tropical forests of central-southern Vietnam. This discovery further underlines the importance of this area as a local center of herpetofaunal diversity and endemism, which is under great threat of deforestation.

 

References

  1. Castoe, T.A. & Parkinson, C.L. (2006) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Molecular Phylogenetics and Evolution, 39, 91–110. https://doi.org/10.1016/j.ympev.2005.12.014
  2. Chan-ard, T., Nabhitabhata, J. & Parr, J.W. (2015) A field guide to the reptiles of Thailand. Oxford University Press, New York, New Yor,, 352 pp.
  3. Creer, S., Malhotra, A. & Thorpe, R.S. (2003) Assessing the phylogenetic utility of four mitochondrial genes and a nuclear intron in the Asian pit viper genus, Trimeresurus: separate, simultaneous, and conditional data combination analyses. Molecular Biology and Evolution, 20, 1240–1251. https://doi.org/10.1093/molbev/msg136
  4. Dahn, H.A., Strickland, J.L., Osorio, A., Colston, T.J. & Parkinson, C.L. (2018) Hidden diversity within the depauperate genera of the snake tribe Lampropeltini (Serpentes, Colubridae). Molecular Phylogenetics and Evolution, 129, 214–225. https://doi.org/10.1016/j.ympev.2018.08.018
  5. David, P., Vogel, G. & Dubois, A. (2011) On the need to follow rigorously the rules of the code for the subsequent designation of a nucleospecies (type species) for a nominal genus which lacked one: the case of the nominal genus Trimeresurus Lacépède, 1804 (Reptilia: Squamata: Viperidae). Zootaxa, 2992 (1), 1–51. https://doi.org/10.11646/zootaxa.2992.1.1
  6. Dawson, K., Malhotra, A., Thorpe, R.S., Guo, P., Mrinalini & Ziegler, T. (2008) Mitochondrial DNA analysis reveals a new member of the Asian pitviper genus Viridovipera (Serpentes: Viperidae: Crotalinae). Molecular Phylogenetics and Evolution, 49, 356–361. https://doi.org/10.1016/j.ympev.2008.05.044
  7. De Koninck, R. (1999) Deforestation in Viet Nam. International Research Centre, Ottawa, Ontario, 100 pp.
  8. Dowling, H. (1951) A proposed standard system of counting ventrals in snakes. British Journal of Herpetology, 11, 97–99.
  9. Duong, T.V., Do, D.T., Ngo, C.D., Nguyen, T.Q. & Poyarkov, N.A. (2018) A new species of the genus Leptolalax (Anura: Megophryidae) from southern Vietnam. Zoological Research, 39 (3), 185–201. https://doi.org/10.24272/j.issn.2095-8137.2018.009
  10. 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, e0161070. https://doi.org/10.1371/journal.pone.0161070
  11. Golay, P., Smith, H.M., Broadley, D.G., Dixon, J.R., McCarthy, C., Rage, J.-C., Schätti, B., & Toriba, M. (1993) Endoglyphs and other major venomous snakes of the world. A checklist. Azemiops Herpetological Data Center, Aïre, xv + 478 pp.
  12. Gorin, V.A., Trofimets, A.V., Gogoleva, S.S., Le, D.X. & Poyarkov, N.A. (2023) A new species of Nanohyla (Anura: Microhylidae) from the lowland forests of southern Vietnam. Zoological Research, 44, 732–736. https://doi.org/10.24272/j.issn.2095-8137.2023.029
  13. Green, M.D., Orlov, N.L. & Murphy, R.W. (2010) Toward a phylogeny of the Kukri snakes, genus Oligodon. Asian Herpetological Research, 1, 1–21. https://doi.org/10.3724/SP.J.1245.2010.00001
  14. Gumprecht, A., Tillack, F., Orlov, N.L., Captain, A. & Raybov, S. (2004) Asian Pitvipers. GeitjeBooks, Berlin, 368 pp.
  15. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series, 41, 95–98.
  16. Hoang, M.D., Luu, H.T., Tran, B.V., Le, D., To, V.Q., Dang, V.D. & Nguyen, H.N. (2019) Forest biodiversity in Khanh Hoa province—Part 2 Animals. Publishing House for Science and Technology, 215 pp. [in Vietnamese]
  17. Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. Systematic Biology 42: 247–264. https://doi.org/10.1093/sysbio/42.3.247
  18. Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
  19. Idiiatullina, S.S., Pawangkhanant, P., Tawan, T., Worranuch, T., Dechochai, B., Suwannapoom, C., Nguyen, T.V., Chanhome, L. & Poyarkov, N.A. (2023) Limestone jewel: A new colourful karst-dwelling pitviper (Serpentes: Viperidae: Trimeresurus) from the poorly explored borderlands of southern peninsular Thailand. Vertebrate Zoology, 73, 697–716. https://doi.org/10.3897/vz.73.e109854
  20. Idiiatullina, S.S., Pawangkhanant, P., Suwannapoom, C., Tawan, T., Chanhome, L., Nguyen, T.V., David, P., Vogel, G. & Poyarkov, N.A. (2024a) Another new species of karst-associated pitviper (Serpentes, Viperidae: Trimeresurus) from the Isthmus of Kra, Peninsular Thailand. European Journal of Taxonomy, 930, 20–52. https://doi.org/10.5852/ejt.2024.930.2489
  21. Idiiatullina, S.S., Nguyen, T.V., Pawangkhanant, P., Suwannapoom, C., Chanhome, L., Mirza, Z.A., David, P., Vogel, G. & Poyarkov, N.A. (2024b) An integrative taxonomic revision of the Trimeresurus popeiorum species complex (Reptilia: Serpentes: Viperidae), with descriptions of two new species from the Indo-Burma biodiversity hotspot. Vertebrate Zoology, 74, 303–342. https://doi.org/10.3897/vz.74.e113347
  22. IUCN Standards and Petitions Subcommittee (2019) Guidelines for Using the IUCN Red List Categories and Criteria. Version 14. Prepared by the Standards and Petitions Subcommittee, IUCN, Cambridge and Gland 113pp.
  23. Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. https://doi.org/10.1093/bib/bbx108
  24. Klemmer, K. (1963) Liste der rezenten Giftschlangen: Elapidae, Hydropheidae, Viperidae und Crotalidae. In: Die Giftschlangen der Erde: Wirkungen und Antigenität der Gifte Therapie von Giftschlangenbissen. N.G. Elwert Universitäts- und VerlagsBuchhandlung, Marburg, pp. 255–464, 37 col. pls. [in German]
  25. Kliukin, N.S., Nguyen, T.V., Le, S.X., Bragin, A.M., Tran, T.T.V., Gorin, V.A. & Poyarkov, N.A. (2023) A new species of the genus Dibamus Duméril & Bibron, 1839 (Squamata: Dibamidae) from the driest and hottest place of Vietnam. Zootaxa, 5380 (4), 301–320. https://doi.org/10.11646/zootaxa.5380.4.1
  26. Kliukin, N.S., Bragin, A.M., Nguyen, T.V., Le, S.X., Tran, T.T.V., Gorin, V.A. & Poyarkov, N.A. (2024) Another new species of Dibamus Duméril & Bibron, 1839 (Squamata: Dibamidae) from Nui Chua National Park, Ninh Thuan Province, Vietnam. Zootaxa, 5406 (1), 87–104. https://doi.org/10.11646/zootaxa.5406.1.4
  27. Kramer, E. (1977) Zur Schlangenfauna Nepals. Revue Suisse de Zoologie, 84 (3), 721–761, 5 figs. [in German] https://doi.org/10.5962/bhl.part.91420
  28. Kraus, F., Mink, D.G. & Brown, W.M. (1996) Crotaline Intergeneric Relationships Based on Mitochondrial DNA Sequence. Copeia, 1996, 763–773. https://doi.org/10.2307/1447637
  29. Kuznetsov, A. & Kuznetsova, S. (2011) Botany of Bidoup-Nui Ba National Park. In: Nguyen, D.H. & Kuznetsov, A. (Eds.), Biodiversity and ecological characteristics of Bidoup-Nui Ba National Park. Vietnam Academy of Science and Technology Publishing House for Science and Technology, Hanoi, pp. 37–105. [in Vietnamese]
  30. Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701. https://doi.org/10.1093/molbev/mss020
  31. Laopichienpong, N., Muangmai, N., Supikamolseni, A., Twilprawat, P., Chanhome, L., Suntrarachun, S., Peyachoknagul, S. & Srikulnath, K. (2016) Assessment of snake DNA barcodes based on mitochondrial COI and Cytb genes revealed multiple putative cryptic species in Thailand. Gene, 594, 238–247. https://doi.org/10.1016/j.gene.2016.09.017
  32. Laurance, W.F. (2007) Forest destruction in tropical Asia. Current Science, 93 (11), 1544–1550.
  33. Malhotra, A. & Thorpe, R.S. (2000) A phylogeny of the Trimeresurus group of pitvipers: new evidence from a mitochondrial gene tree. Molecular Phylogenetics and Evolution, 16, 199–211. https://doi.org/10.1006/mpev.2000.0779
  34. Malhotra, A. & Thorpe, R.S. (2004) A phylogeny of four mitochondrial gene regions suggests a revised taxonomy for Asian pitvipers (Trimeresurus and Ovophis). Molecular Phylogenetics and Evolution, 32, 83–100. https://doi.org/10.1016/j.ympev.2004.02.008
  35. Malhotra, A., Thorpe, R.S., Mrinalini & Stuart, B.L. (2011) Two new species of pitviper of the genus Cryptelytrops Cope 1860 (Squamata: Viperidae: Crotalinae) from Southeast Asia. Zootaxa, 2757 (1), 1–23. https://doi.org/10.11646/zootaxa.2757.1.1
  36. Mallik, A.K., Srikanthan, A.N., Ganesh, S.R., Vijayakumar, S.P., Campbell, P.D., Malhotra, A. & Shanker, K. (2021) Resolving pitfalls in pit viper systematics–A multi-criteria approach to species delimitation in pit vipers (Reptilia, Viperidae, Craspedocephalus) of Peninsular India reveals cryptic diversity. Vertebrate Zoology, 71, 577–619. https://doi.org 10.3897/vz.71.e66239
  37. Meijer, W. (1973) Devastation and regeneration of lowland dipterocarp forests in Southeast Asia. BioScience, 23 (9), 528–533. https://doi.org/10.2307/1296481
  38. Meyfroidt, P. & Lambin, E.F. (2008) Forest transition in Vietnam and its environmental impacts. Global Change Biology, 14(6), 1319–1336. https://doi.org/10.1111/j.1365-2486.2008.01575.x
  39. Minh, 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
  40. Mrinalini, Thorpe, R.S., Creer, S., Lallias, D., Dawnay, L., Stuart, B.L. & Malhotra, A. (2015) Convergence of multiple markers and analysis methods defines the genetic distinctiveness of cryptic pitvipers. Molecular Phylogenetics and Evolution, 92, 266–279. https://doi.org/10.1016/j.ympev.2015.06.001
  41. Nemes, L., Babb, R., Devender, W.V., Nguyen, K.V., Le, Q.K., Vu, T.N., Rauhaus, A., Nguyen, T.Q. & Ziegler, T. (2013) First contribution to the reptile fauna of Quang Ngai province, central Vietnam. Biodiversity Journal, 4 (2), 301–326.
  42. Ngo, H.T., Nguyen, T.Q., Nguyen, H.V.M., Luu, V.Q., Phimphasone, V., Ha, N.V., Ziegler, T. & Le, M.D. (2022) Molecular assessement of Pitviper populations (genus Trimeresurus) in Laos and Vietnam reveals new country record and overlooked diversity. Vietnam Journal of Biotechnology, 20 (4), 589–598. https://doi.org/10.15625/1811-4989/16863
  43. 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
  44. Nguyen, S.V., Ho, C.T. & Nguyen, T.Q. (2009) Herpetofauna of Vietnam. Chimaira, Frankfurt, 768 pp.
  45. Nguyen, T.V., Duong, L.D. & Duong, T.T.A. (2019) New records and an updated list of snakes (Squamata: Serpentes) from Binh Dinh Province, Central-Southern Vietnam. Hue University Journal of Science: Natural Science, 128 (1B), 35–41. https://doi.org/10.26459/hueuni-jns.v128i1B.5203
  46. Orlov, N.L., Ryabov, S.A., Nguyen, S.V. & Nguyen, T.Q. (2003) New records and data on the poorly known snakes of Vietnam. Russian Journal of Herpetology, 10 (3), 217–240. https://doi.org/10.30906/1026-2296-2003-10-3-217-240
  47. Pauwels, O.S.G., Nazarov, R.A., Bobrov, V.V. & Poyarkov, N.A. (2018) Taxonomic status of two populations of Bent-toed Geckos of the Cyrtodactylus irregularis complex (Squamata, Gekkonidae) with description of a new species from Nui Chua National Park, southern Vietnam. Zootaxa, 4403 (2), 307–335. https://doi.org/10.11646/zootaxa.4403.2.5
  48. Poyarkov, N.A., Nguyen, T.V., Popov, E.S., Geissler, P., Pawangkhanant, P., Neang, T., Suwannapoom, C., Ananjeva, N.B. & Orlov, N.L. (2023) Recent progress in taxonomic studies, biogeographic analysis and revised checklist of Reptilians in Indochina. Russian Journal of Herpetology, 30 (5), 255–476. https://doi.org/10.30906/1026-2296-2023-30-5-255-476
  49. Poyarkov, N.A., Nguyen, T.V., Popov, E.S., Geissler, P., Pawangkhanant, P., Neang, T., Suwannapoom, C. & Orlov, N.L. (2021) Recent progress in taxonomic studies, biogeographic analysis and revised checklist of Amphibians in Indochina. Russian Journal of Herpetology, 28 (3A), 1–110. https://doi.org/10.30906/1026-2296-2021-28-3A-1-110
  50. Pyron, R.A., Kandambi, H.K.D., 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, 969–978. https://doi.org/10.1016/j.ympev.2012.12.004
  51. Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in bayesian phylogenetics using tracer 1.7. Susko E (Ed.). Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
  52. Rathee, Y.S., Purkayastha, J., Lalremsanga, H.T., Dalal, S., Biakzuala, L., Muansanga, L. & Mirza, Z.A. (2022) A new cryptic species of green pit viper of the genus Trimeresurus Lacépède, 1804 (Serpentes, Viperidae) from northeast India. Plos One, 17, 1–17. https://doi.org/10.1371/journal.pone.0268402
  53. Regenass, U. & Kramer, E. (1981) Zur Systematik der grünen Grubenottern der Gattung Trimeresurus (Serpentes, Crotalidae). Revue suisse de Zoologie, 88 (1), 163–205. [in German] https://doi.org/10.5962/bhl.part.82363
  54. Salvi, D., Harris, D.J., Kaliontzopoulou, A., Carretero, M.A. & Pinho, C. (2013) Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard. BMC Evolutionary Biology, 13, 1–18. https://doi.org/10.1186/1471-2148-13-147
  55. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, 473 pp.
  56. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729. https://doi.org/10.1093/molbev/mst197
  57. Uetz, P., Freed, P. & Hošek, J. (2024) The Reptile Database. Available at http://www.reptile-database.org/ (accessed 1 March 2024)
  58. Vassilieva, A.B., Galoyan, E.A., Poyarkov, N.A. & Geissler, P. (2016) A Photographic Field Guide to the Amphibians and Reptiles of the Lowland Monsoon Forests of Southern Vietnam. Edition Chimaira, Frankfurt am Main, 324 pp.
  59. Vogel, G., Nguyen, T.V. & David, P. (2023) A new green pitviper of the complex of Trimeresurus albolabris complex (Reptilia, Serpentes, Viperidae) from central and southern Myanmar. Zootaxa, 5357 (4), 515–554. https://doi.org/10.11646/zootaxa.5357.4.3
  60. Zhu, F., Liu, Q., Che, J., Zhang, L., Chen, X., Yan, F., Murphy, R., Guo, C. & Guo, P. (2016) Molecular phylogeography of white-lipped tree viper (Trimeresurus; Viperidae). Zoologica Scripta, 45 (3), 252–262. https://doi.org/10.1111/zsc.12156
  61. Ziegler, T., Pham, C.T., Nguyen, T.Q., Berger, M., Ngo, H.T. & Le, M.D. (2018) First record of the White-lipped Pitviper (Trimeresurus albolabris) from Hai Phong City, report of an unusual colour morph from Bach Long Vy Island in the Gulf of Tonkin, northern Vietnam and identification of previously erroneously determined T. rubeus. Sauria, 40 (2), 1–24.