Another new species of karst-associated pitviper (Serpentes, Viperidae: Trimeresurus) from the Isthmus of Kra, Peninsular Thailand

Keywords: Crotalinae, T. kanburiensis complex, Peninsular Thailand, karst, taxonomy

Abstract

We describe a new species of karst-dwelling pitviper from Chumphon Province of Peninsular Thailand, in the Isthmus of Kra, based on morphological and molecular data (2427 bp from cyt b, ND4 and 16S rRNA mitochondrial DNA genes). Morphologically, Trimeresurus kraensis sp. nov. is distinguished from other congeners by the following combination of morphological characters: a dark/bottle-green dorsum with reddish-brown or purple crossbands; pale green venter lacking dark dots; stripes present on the lateral sides of the ventrals; internasals generally in contact; one large supraocular scale on each side of the head; iris pale copper; tail brown with dark purplish-brown crossbars; dorsal scales in 21–21–15 rows; ventral scales 167 in a single male, 169–171 in females; subcaudal scales 62 in a single male, 52–54 in females, all paired. White vertebral spots present in males, located on approximately every two or four dorsal scales; dark brown spots forming discontinuous pattern present on 1–3 lateral dorsal scale rows; males with reddish-brown postocular stripe with jagged edges. The new species differs from the morphologically similar species Trimeresurus venustus s. str. by a notable divergence in cytochrome b mitochondrial DNA gene sequences (p = 5.9%).

References

Captain A., Deepak V., Pandit R., Bhatt B. & Athreya R. 2019. A new species of pitviper (Serpentes: Viperidae: Trimeresurus Lacepède, 1804) from west Kameng District, Arunachal Pradesh, India. Russian Journal of Herpetology 26: 111–122. https://doi.org/10.30906/1026-2296-2019-26-2-111-122

Chan K.O., Sind L.I., Thong L.I., Ananthanarayanan S., Rasu S., Aowphol A., Rujirawan A., Anuar S., Mulcahy D., Grismer J.L. & Grismer L.L. 2022. Phylogeography of mangrove pit vipers (Viperidae, Trimeresurus erythrurus‐purpureomaculatus complex). Zoologica Scripta 51: 664–675. https://doi.org/10.1111/zsc.12562

Chan-ard T., Nabhitabhata J. & Parr J.W. 2015. A Field Guide to the Reptiles of Thailand. Oxford University Press, New York.

Chandramouli S.R., Campbell P.D. & Vogel G. 2020. A new species of green pit viper of the genus Trimeresurus Lacépède, 1804 (Reptilia: Serpentes: Viperidae) from the Nicobar Archipelago, Indian Ocean. Amphibian and Reptile Conservation 14: 169–176.

Chanhome L., Cox M.J., Vasaruchapong T., Chaiyabutr N. & Sitprija V. 2011 Characterization of venomous snakes of Thailand. Asian Biomedicine 5: 311–328.

Chen J.M., Poyarkov N.A., Suwannapoom C., Lathrop A., Wu Y.H., Zhou W.W., Yuan Z.Y., Jin J.Q., Chen H.M., Liu H.Q., Nguyen T.Q., Nguyen N.S., Duong T.V., Eto K., Nishikawa K., Matsui M., Orlov N.L., Stuart B.L., Brown R.M., Rowley J.J.L., Murphy R.W., Wang Y.Y. & Che J. 2018. Large-scale phylogenetic analyses provide insights into unrecognized diversity and historical biogeography of Asian leaf-litter frogs, genus Leptolalax (Anura: Megophryidae). Molecular Phylogenetics and Evolution 124: 162–171. https://doi.org/10.1016/j.ympev.2018.02.020

Chen Z., Yu J., Vogel G., Shi S., Song Z., Tang Y., Yang J., Ding L. & Chen C. 2020. A new pit viper of the genus Trimeresurus (Lacépède, 1804) (Squamata: Viperidae) from Southwest China. Zootaxa 4768 (1): 112–128. https://doi.org/10.11646/zootaxa.4768.1.7

Chen Z., Shi S., Gao J., Vogel G., Song Z., Ding L. & Dai R. 2021. A new species of Trimeresurus Lacépède, 1804 (Squamata: Viperidae) from Southwestern China, Vietnam, Thailand and Myanmar. Asian Herpetological Research 12: 167–177. https://doi.org/10.16373/j.cnki.ahr.200084

Chomdej S., Pradit W., Suwannapoom C., Pawangkhanant P., Nganvongpanit K., Poyarkov N.A., Che J., Gao Y. & Gong S. 2021. Phylogenetic analyses of distantly related clades of bent-toed geckos (genus Cyrtodactylus) reveal an unprecedented amount of cryptic diversity in northern and western Thailand. Scientific Reports 11: 2328. https://doi.org/10.1038/s41598-020-70640-8

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

David P., Vogel G., Sumontha M., Pauwels O.S.G. & Chanhome L. 2004. Expanded description of the poorly known pitviper Trimeresurus kanburiensis Smith, 1943, with confirmation of the validity of Trimeresurus venustus Vogel, 1991 (Reptilia: Serpentes: Crotalidae). Russian Journal of Herpetology 11: 81–90.

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

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

Dowling H.G. 1951a. A proposed method of expressing scale reductions in snakes. Copeia 1951: 131. https://doi.org/10.2307/1437542

Dowling H.G. 1951b. A proposed standard system of counting ventrals in snakes. British Journal of Herpetology 1: 97–99.

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

Gorin V.A., Solovyeva E.N., Hasan M., Okamiya H., Karunarathna D.M.S.S., Pawangkhanant P., de Silva A., Juthong W., Milto K.D., Nguyen L.T., Suwannapoom C., Haas A., Bickford D.P., Das I. & Poyarkov N.A. 2020. A little frog leaps a long way: compounded colonizations of the Indian Subcontinent discovered in the tiny Oriental frog genus Microhyla (Amphibia: Microhylidae). PeerJ 8: e9411. https://doi.org/10.7717/peerj.9411

Grismer L.L., Yushchenko P.V., Pawangkhanant P., Naiduangchan M., Nazarov R.A., Orlova V.F., Suwannapoom C., Poyarkov N.A. 2020a. A new species of Hemiphyllodactylus Bleeker (Squamata; Gekkonidae) from Peninsular Thailand that converges in morphology and color pattern on Pseudogekko smaragdinus (Taylor) from the Philippines. Zootaxa 4816 (2): 171–190. https://doi.org/10.11646/zootaxa.4816.2.2

Grismer L.L., Yushchenko P.V., Pawangkhanant P., Nazarov R.A., Naiduangchan M., Suwannapoom C. & Poyarkov N.A. 2020b. A new species of Cnemaspis Strauch (Squamata: Gekkonidae) of the C. siamensis group from Tenasserim Mountains, Thailand. Zootaxa 4852 (5): 547–564. https://doi.org/10.11646/zootaxa.4852.5.3

Grismer L.L., Youmans T.M., Wood P.L., Ponce A., Wright S.B., Jones B.S., Johnson R., Sanders K.L., Gower D.J., Yaakob N.S. & Lim K.K.P. 2006. Checklist of the herpetofauna of Pulau Langkawi, Malaysia with comments on taxonomy. Hamadryad 30: 61–75.

Grismer L.L., Ngo T.V. & Grismer J.L. 2008. A new species of insular pitviper of the genus Cryptelytrops (Squamaa: Viperidae) from southern Vietnam. Zootaxa 1715 (1): 57–68. https://doi.org/10.11646/zootaxa.1715.1.4

Grismer L.L., Wood P.L., Poyarkov N.A., Le M.D., Karunarathna S., Chomdej S., Suwannapoom C., Qi S., Liu S., Che J., Quah E.S.H., Kraus F., Oliver P.M., Riyanto A., Pauwels O.S.G. & Grismer J.L. 2021. Karstic landscapes are foci of species diversity in the World’s third-largest vertebrate genus Cyrtodactylus Gray, 1827 (Reptilia: Squamata; Gekkonidae). Diversity 13 (183): 1–15. https://doi.org/10.3390/d13050183

Grismer L.L., Poyarkov N.A., Quah E.S.H., Grismer J.L. & Wood P.L. 2022. The biogeography of bent-toed geckos, Cyrtodactylus (Squamata: Gekkonidae). PeerJ 10: e13153. http:/doi.org/10.7717/peerj.13153

Gumprecht A., Tillack F., Orlov N.L., Captain A. & Ryabov S. 2004. Asian Pit Vipers. GeitjeBooks Berlin, Berlin.

Guo P. & Wang Y.Z. 2011. A new genus and species of cryptic Asian green pitviper (Serpentes: Viperidae: Crotalinae) from southwest China. Zootaxa 2918 (1): 1–14. https://doi.org/10.11646/zootaxa.2918.1.1

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.

Huelsenbeck J.P. & Hillis D.M. 1993. Success of phylogenetic methods in the four-taxon case. Systematic Biology 42: 247–264. https://doi.org/10.1093/sysbio/42.3.247

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

Idiiatullina S., Pawangkhanant P., Tawan T., Worranuch T., Dechochai B., Suwannapoom C., Nguyen T.V., Chanhome K. & 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

IUCN Standards and Petitions Committee. 2019. Guidelines for Using the IUCN Red List Categories and Criteria. Version 14. Prepared by the Standards and Petitions Committee.

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

Kraus F., Mink D.G. & Brown W.M. 1996. Crotaline intergeneric relationships based on mitochondrial DNA sequence. Copeia 763–773. https://doi.org/10.2307/1447637

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

Malhotra A. & Thorpe R.S. 2004a. 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

Malhotra A. & Thorpe R.S. 2004b. Reassessment of the validity and diagnosis of the pitviper Trimeresurus venustus Vogel, 1991. Herpetological Journal 14: 21–33.

Malhotra A. & Thorpe R.S. 2004c. Maximizing information in systematic revisions: A combined molecular and morphological analysis of a cryptic green pitviper complex (Trimeresurus stejnegeri). Biological Journal of the Linnean Society 82: 219–235. https://doi.org/10.1111/j.1095-8312.2004.00354.x

Malhotra A., Thorpe R.S. & 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

Matsui M., Khonsue W. & Nabhitabhata J. 2005. A new Ansonia from the Isthmus of Kra, Thailand (Amphibia, Anura, Bufonidae). Zoological Science 22: 809–814. https://doi.org/10.2108/zsj.22.809

Mirza Z.A., Bhosale H.S., Phansalkar P.U., Sawant M., Gowande G.G. & Patel H. 2020. A new species of green pit vipers of the genus Trimeresurus Lacépède, 1804 (Reptilia, Serpentes, Viperidae) from western Arunachal Pradesh, India. Zoosystematics and Evolution 96: 123–138. https://doi.org/10.3897/zse.96.48431

Mirza Z.A., Lalremsanga H.T., Bhosale H., Gowande G., Patel H., Idiiatullina S. & Poyarkov N.A. 2023. Systematics of Trimeresurus popeiorum Smith, 1937 with a revised molecular phylogeny of Asian pitvipers of the genus Trimeresurus Lacépède, 1804 sensu lato. Evolutionary Systematics 7: 91–104. https://doi.org/10.3897/evolsyst.7.97026

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

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

Pauwels O.S.G., Sumontha M., Latinne A. & Grismer L.L. 2013. Cyrtodactylus sanook (Squamata: Gekkonidae), a new cave-dwelling gecko from Chumphon Province, southern Thailand. Zootaxa 3635 (3): 275–285. https://doi.org/10.11646/zootaxa.3635.3.7

Pawangkhanant P., Poyarkov N.A., Duong T.V., Naiduangchan M. & Suwannapoom C. 2018. A new species of Leptobrachium (Anura, Megophryidae) from western Thailand. PeerJ 6: e5584. https://doi.org/10.7717/peerj.5584

Poyarkov N.A., Geissler P., Gorin V.A., Dunayev E.A., Hartmann T. & Suwannapoom C. 2019. Counting stripes: revision of the Lipinia vittigera complex (Reptilia, Squamata, Scincidae) with description of two new species from Indochina. Zoological Research 40 (5): 358–393. https://doi.org/10.24272/j.issn.2095-8137.2019.052

Poyarkov N.A., Pawangkhanant P., Gorin V.A., Juthong W. & Suwannapoom C. 2020. A new species of miniaturized narrow-mouth frog of the genus Microhyla Tschudi, 1838 (Amphibia: Anura: Microhylidae) from northern Tenasserim, Thailand. Journal of Natural History 54 (23–24): 1525–1558. https://doi.org/10.1080/00222933.2020.1804005

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

Poyarkov N.A., Nguyen T.V., Pawangkhanant P., Yushchenko P.V., Brakels P., Nguyen L.H., Nguyen H.N., Suwannapoom C., Orlov N.L. & Vogel G. 2022. An integrative taxonomic revision of slug-eating snakes (Squamata: Pareidae: Pareineae) reveals unprecedented diversity in Indochina. PeerJ 10: e12713. https://doi.org/10.7717/peerj.12713

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

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

Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032

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

Sambrook J., Fritsch E.F. & Maniatis T. 1989. Molecular Cloning: A Laboratory Manual. 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

Sanders K.L., Malhotra A. & Thorpe R.S. 2004. Ecological diversification in a group of Indomalayan pitvipers (Trimeresurus): convergence in taxonomically important traits has implications for species identification. Journal of Evolutionary Biology 17: 721–731. https://doi.org/10.1111/j.1420-9101.2004.00735.x

Sanders K.L., Malhotra A. & Thorpe R.S. 2006. Evidence for a Müllerian mimetic radiation in Asian pitvipers. Proceedings of the Royal Society B: Biological Sciences 273 (1590): 1135–1141. https://doi.org/10.1098/rspb.2005.3418

Sumontha M., Suntrarachun S., Pauwels O.S.G., Pawangkhanant P., Chomngam N., Iamwiriyakul P. & Chanhome L. 2021. A new karst-dwelling, colorful pitviper (Viperidae: Trimeresurus) from northern Peninsular Thailand. Zootaxa 4974 (2): 307–332. https://doi.org/10.11646/zootaxa.4974.2.4

Suwannapoom C., Sumontha M., Tunprasert J., Ruangsuwan T., Pawangkhanant P., Korost D.V. & Poyarkov N.A. 2018. A striking new genus and species of cave-dwelling frog (Amphibia: Anura: Microhylidae: Asterophryinae) from Thailand. PeerJ 6: e4422. https://doi.org/10.7717/peerj.4422

Suwannapoom C., Nguyen T.V., Pawangkhanant P., Gorin V.A., Chomdej S., Che J. & Poyarkov N.A. 2020. A new species of Micryletta (Amphibia: Microhylidae) from southern Thailand. Zoological Research 41 (5): 581–588. https://doi.org/10.24272/j.issn.2095-8137.2020.139

Suwannapoom C., Grismer L.L., Pawangkhanant P., Naiduangchan M., Yushchenko P.V., Arkhipov D.V., Wilkinson J.A. & Poyarkov N.A. 2021. Hidden tribe: a new species of Stream Toad of the genus Ansonia Stoliczka, 1870 (Anura: Bufonidae) from the poorly explored mountainous borderlands of western Thailand. Vertebrate Zoology 71: 763–779. https://doi.org/10.3897/vz.71.e73529

Suwannapoom C., Grismer L.L., Pawangkhanant P. & Poyarkov N.A. 2022. A new species of stream toad of the genus Ansonia Stoliczka, 1870 (Anura: Bufonidae) from Nakhon Si Thammarat Range in southern Thailand. Zootaxa 5168 (2): 119–136. https://doi.org/10.11646/zootaxa.5168.2.2

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

Vogel G. 1991. Eine neue Trimeresurus-Art aus Thailand, Trimeresurus venustus sp. nov. (Reptilia: Serpentes: Crotalidae). Sauria 13 (1): 23–28. [In German.]

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

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: 252–262. https://doi.org/10.1111/zsc.12156

Zimmerer J. 2004. Nature Guide, Langkawi. Sakti Mega Enterprise, Penang.

Published
2024-03-27
How to Cite
Idiiatullina, S. S., Pawangkhanant, P., Suwannapoom, C., Tawan, T., Chanhome, L., Nguyen, T. V., David, P., Vogel, G., & Poyarkov, N. A. (2024). Another new species of karst-associated pitviper (Serpentes, Viperidae: Trimeresurus) from the Isthmus of Kra, Peninsular Thailand. European Journal of Taxonomy, 930(1), 20–52. https://doi.org/10.5852/ejt.2024.930.2489
Section
Research article