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Qin Liu, Jiao-Wen Yan, Shao-Bing Hou, Ping Wang, Sang Ngoc Nguyen, Robert W. Murphy, Jing Che, Peng Guo. A new species of the genus Sinomicrurus (Serpentes: Elapidae) from China and Vietnam[J]. Zoological Research, 2020, 41(2): 194-198. doi: 10.24272/j.issn.2095-8137.2020.023
Citation: Qin Liu, Jiao-Wen Yan, Shao-Bing Hou, Ping Wang, Sang Ngoc Nguyen, Robert W. Murphy, Jing Che, Peng Guo. A new species of the genus Sinomicrurus (Serpentes: Elapidae) from China and Vietnam[J]. Zoological Research, 2020, 41(2): 194-198. doi: 10.24272/j.issn.2095-8137.2020.023

A new species of the genus Sinomicrurus (Serpentes: Elapidae) from China and Vietnam

doi: 10.24272/j.issn.2095-8137.2020.023
Funds:  This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA 20050201, XDA19050303), National Natural Science Foundation of China (NSFC31372152), Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (CAS) (Y4ZK111B01: 2017CASSEABRIQG002), International Partnership Program of CAS (152453KYSB20170033), and Animal Branch of the Germplasm Bank of Wild Species, CAS (Large Research Infrastructure Funding)
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    [2] Dowling HG. 1951. A proposed standard system of counting ventrals in snakes. British Journal of Herpetology, 1(5): 97−99.
    [3] Günther A. 1868. Sixth account of new species of snakes in the collection of the British Museum. Annals and Magazine of Natural History, 4(1): 413−429.
    [4] Kumar S, Nei M, Dudley J, Tamura K. 2008. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9(4): 299−306. doi:  10.1093/bib/bbn017
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    [6] Liu Q, Zhu F, Zhong GH, Wang YY, Fang M, Xiao R, Cai YS, Guo P. 2015. COI-based barcoding of Chinese vipers (Reptilia: Squamata: Viperidae). Amphibia-Reptilia, 36(4): 361−372. doi:  10.1163/15685381-00003012
    [7] Maki M. 1935. A new poisonous snake (Calliophis iwasakii) from Loo-Choo. Transactions of the Natural History Society of Formosa, Taihoku, 25: 216−219.
    [8] Peng LF, Wang LJ, Ding L, Zhu YW, Luo J, Yang DC, Huang RY, Lv SQ, Huang S. 2018. A new species of the genus Sinomicrurus Slowinski, Boundy and Lawson, 2001(Squamata: Elapidae) from Hainan Province, China. Asian Herpetological Research, 9(2): 65−73.
    [9] Pope CH. 1928. Seven new reptiles from Fukien Province, China. American Museum Novitates(320): 1−6.
    [10] Pope CH. 1935. The Reptiles of China: Turtles, Crocodilians, Snakes, Lizards. New York: American Museum of Natural History.
    [11] Pyron RA, Burbrink FT, Wiens JJ. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13(1): 93. doi:  10.1186/1471-2148-13-93
    [12] Rambaut A, Drummond AJ. 2007(2018-03-23). Tracer v 1.4. http://tree.bio.ed.ac.uk/software/tracer.
    [13] Reinhardt JT. 1844. Description of a new species of venomous snake, Elaps Macclellandi. Calcutta Journal of Natural History, 4: 532−534.
    [14] Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3): 539−542. doi:  10.1093/sysbio/sys029
    [15] Slowinski JB, Boundy J, Lawson R. 2001. The phylogenetic relationships of Asian coral snakes (Elapidae: Calliophis and Maticora) based on morphological and molecular characters. Herpetologica, 57(2): 233−245.
    [16] Smith MA. 1943. The Fauna of British India, Ceylon and Burma, Including the whole of the Indo-Chinese Sub-region. Reptilia and Amphibia, Vol. III, Serpentes. London: Taylor & Francis Ltd.
    [17] Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 75(5): 758−771.
    [18] Steindachner F. 1913. Über zwei neue Schlangenarten aus Formosa. Anzeiger der Kaiserlichen Akademie der Wissenschaften in Wien, Mathematisch-Naturwissenschaftliche Klasse, 50: 218−220.
    [19] Stejneger LH. 1907. Herpetology of Japan and Adjacent Territory. Washington: Bulletin of United States National Museum.
    [20] Takahashi S. 1930. Synopsis of the Terrestrial Snakes of JapanTokyo: Shunyo-do. (in Japanese)
    [21] 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. doi:  10.1093/molbev/mst197
    [22] van Denburgh J. 1912. Concerning certain species of reptiles and amphibians from China, Japan, the Loo Choo Islands, and Formosa. Proceedings of the California Academy of Sciences, 3(10): 187−258.
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    [27] Zhao EM. 2006. Snakes of China (I). Hefei: Anhui Sciences and Technology Publishing House. (in Chinese)
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A new species of the genus Sinomicrurus (Serpentes: Elapidae) from China and Vietnam

doi: 10.24272/j.issn.2095-8137.2020.023
Funds:  This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA 20050201, XDA19050303), National Natural Science Foundation of China (NSFC31372152), Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (CAS) (Y4ZK111B01: 2017CASSEABRIQG002), International Partnership Program of CAS (152453KYSB20170033), and Animal Branch of the Germplasm Bank of Wild Species, CAS (Large Research Infrastructure Funding)
Qin Liu, Jiao-Wen Yan, Shao-Bing Hou, Ping Wang, Sang Ngoc Nguyen, Robert W. Murphy, Jing Che, Peng Guo. A new species of the genus Sinomicrurus (Serpentes: Elapidae) from China and Vietnam[J]. Zoological Research, 2020, 41(2): 194-198. doi: 10.24272/j.issn.2095-8137.2020.023
Citation: Qin Liu, Jiao-Wen Yan, Shao-Bing Hou, Ping Wang, Sang Ngoc Nguyen, Robert W. Murphy, Jing Che, Peng Guo. A new species of the genus Sinomicrurus (Serpentes: Elapidae) from China and Vietnam[J]. Zoological Research, 2020, 41(2): 194-198. doi: 10.24272/j.issn.2095-8137.2020.023
    • A new species of Sinomicrurus Slowinski, Boundy, and Lawson, 2001 is described herein based on a series of specimens. The new species, Sinomicrurus peinani sp. nov., occurs in southern China and northern Vietnam. Sinomicrurus peinani sp. nov. is distinguished from its congeners by the following combination of characters: (1) 30–35 black cross-bands on body and tail; (2) 13 dorsal scale rows throughout, all smooth; (3) white belly with black cross-bands or irregular spots; (4) broad white transverse bar on top of head with inverted V-shaped anterior margin, white bar wider than anterior black bar; and (5) frontal V-like, 1.3 times as long as wide. In addition, new occurrences of S. houi in Guangxi, China, and Vietnam are discussed.

      Sinomicrurus Slowinski, Boundy, and Lawson, is a group of small to medium-sized Asian coral snakes (Slowinski et al., 2001; Zhao, 2006). They are widely distributed in eastern and southeastern Asia, ranging from Nepal in the west to Japan in the east and from Hunan, China, in the north to Taiwan, China, in the south (Zhao, 2006).

      Previously, members of the genus Sinomicrurus were contained within Calliophis Gray (Slowinski et al., 2001; Zhao et al., 1998). However, phylogenetic analyses based on morphological characters and cytochrome b sequences suggested that the Asian coral snakes fell into three major clades (Slowinski et al., 2001). Thus, Slowinski et al. (2001) erected a new genus Sinomicrurus to accommodate the northern tropical/subtropical mainland species, including C. hatori (Takahashi, 1930), C. japonicas (Günther, 1868), C. kelloggi (Pope, 1928), C. macclellandi (Reinhardt, 1844), and C. sauteri (Steindachner, 1913). Recently, Peng et al. (2018) described a new species from Hainan Island, China. Thus, six species are recognized presently within this genus.

      In recent decades, a series of field surveys have been conducted in southern China (Guangxi) and Vietnam, involving the collection of several Sinomicrurus coral snakes. Further study based on morphological comparisons and genetic data indicated they were different from all putative species of this genus. Thus, we evaluated these specimens as a new species, which is described herein.

      Twenty-one specimens of Sinomicrurus collected from China were morphologically examined (Supplementary Appendix S1). Scalation, color pattern, and body proportions were recorded and measured. Measurements of body and tail lengths were taken with a ruler to the nearest 1 mm; other measurements were taken with a slide caliper to the nearest 0.1 mm. Meristic characters were recorded on both sides. Ventral scales were counted following Dowling (1951). For comparison, characters of other Sinomicrurus species were taken from previous publications (Peng et al., 2018; Pope, 1935; Stejneger, 1907; Zhao, 2006; Zhao et al., 1998).

      Abbreviations used for measurements and meristic characters are as follows: SVL (snout-vent length): distance between tip of snout and cloaca; TaL (tail length): distance between cloaca and tip of tail; DS: dorsal scales; VS: ventral scales; SC: subcaudal scales; IL: infralabials; SL: supralabials; Tem: temporals; Lo; Loreals; Poo: postoculars; Pro: preoculars; CB: number of cross-bands on body. All specimens are deposited in Yibin University (YBU), Sichuan, China.

      In total, 25 individuals representing three Chinese species and one unidentified taxon were sequenced and analyzed (Supplementary Appendix S2). Genomic DNA was extracted from liver samples preserved in 85% alcohol using Tissue DNA kits (Omega Bio-Tek, Inc., USA). A partial sequence for the mitochondrial cytochrome c oxidase I (COI) was amplified using the primer chmf/chmr and cycling parameters provided in Che et al. (2012). The double-stranded products were sequenced by a commercial company (Genewiz, China), with the sequences then edited manually using SeqMan in Lasergene v15.1 (DNASTAR Inc., USA) (GenBank accession Nos.: MN 685872–MN685896). An additional nine sequences representing S. sauteri, S. hatori, S. macclellandi, and S. kelloggi were retried from GenBank and added to the dataset for subsequent analyses (Supplementary Appendix S2). Micrurus nigrocinctus and M. lemniscatus were chosen as outgroups based on previous work (Pyron et al., 2013).

      We reconstructed phylogenetic relationships using Bayesian inference (BI) and Maximum likelihood (ML) methods. Prior to analyses, the optimal evolutionary models for each codon position were selected using PartitionFinder under Bayesian Information Criterion (BIC) (Lanfear et al., 2012). BI analysis was performed using MrBayes v3.2.2 (Ronquist et al., 2012). All searches were performed with two independent runs, with each initiating a random tree. Each run consisted of four Markov chains (three heated and one cold chain) estimated for 5×106 million generations and sampled every 2 000 generations, with 25% of initial samples discarded as burn-in. Convergence was assessed by examining effective sample sizes (ESS) (ESS>200) and likelihood plots through time in TRACER v1.4 (Rambaut & Drummond, 2007). The resulting trees were combined to calculate posterior probabilities (PP) for each node in a 50% majority-rule consensus tree. The ML trees were constructed using RaxML v7.2.6 (Stamatakis, 2008) with the GTRCAT model under the same partitioning scheme as Bayesian analysis. Branch support was assessed using 1 000 non-parametric bootstrap (BS) topological replicates. Pairwise distances (P-distances) between in-group taxa were calculated in Mega 6.0 (Kumar et al., 2008; Tamura et al., 2013).

    • Sinomicrurus peinani sp. nov. (Figure 1AD; Table 1)

      Figure 1.  Holotype and phylogenetic position of Sinomicrurus peinani sp. nov.

      SpecimensSexSVL (mm)TaL (mm)DSVSSCILSLTemLoPooProCB
      YBU16086F5504513-13-13210287/76/61+1/1+102/21/127+3
      YBU16054F5754513-13-13208277/76/61+1/1+102/21/126+3
      YBU16066M3353313-13-13217287/76/61+1/1+102/21/131+4
      YBU16067F5004913-13-13225287/76/61+1/1+102/21/132+4
      For abbreviations, see text. F: Female; M: Male.

      Table 1.  Morphological characters of the type specimens of Sinomcrurus peinani sp. nov.

      Holotype: YBU 16086, adult female, from Cangwu County (N23.65°, E111.56°), Guangxi, China, elevation of ~30 m a.s.l.; collected on 05 June 2016.

      Paratypes (three specimens): YBU 16054, female; YBU 16066, male; YBU 16067, female. Same locality and date as holotype.

      Diagnosis: All examined specimens possessed a small to medium-sized body, varying from 368 mm to 620 mm, as well as: (1) 30–35 black cross-bands on body and tail; (2) 13 dorsal scale rows throughout, all smooth; (3) white belly with black speckles or bands; (4) broad white transverse bar on top of head with inverted V-shaped anterior margin, white bar wider than anterior black bar; and (5) frontal V-like, 1.3 times as long as wide.

      Description of holotype: Adult female. Total length 550 mm, tail length 45 mm. Body rather slender; head short, broad, and rounded with obtuse muzzle. Rostral trapezoidal, 1.5 times as broad as deep. Internasals large and square, slightly wider than long, in contact with each other and with rostral. Prefrontals pentagonal, length equal to width. Frontal V-shaped, nearly 1.3 times as long as wide. Supraoculars large, twice as long as broad, shorter than frontals. Parietals large, 1.6 times as long as broad. Single loreal, large; one preocular, longer than wide; two postoculars, one below other. Two temporals, one behind other, in contact with supralabials. Seven supralabials on each side, third and fourth bordering eye. Six infralabials, second smallest, first four touching chin-shield; two pairs of chin-shields, in contact with each other.

      Dorsal scales in 13 rows throughout, all smooth. Ventrals 219+4, cloaca scale divided. Subcaudals 28, paired; dorsal tail scale rows reduced from six to four at sixth subcaudal. Tail short and tip pointed.

      Dorsal surface brownish, with 27+3 regular, narrow, black transverse bands edged with yellow, each band in contact with cross-band on belly, forming closed ring. Quadrangular spots or irregular short bands between rings on belly. Black rings occasionally not reaching abdomen, forming half rings. Head black above with very broad white transverse bar behind eyes. Anterior margin inverted V-shaped white band, extending to prefrontals; posterior margin nearly straight, exceeding end of frontals; white bar wider than anterior black bar, yellowish white below, with 47+5 cross-bars or quadrangular spots.

      Ecological notes: The specimens were found in meadowland in bamboo forest (Figure 1A). An individual of Achalinus sp. was found in the stomach of Sinomicrurus peinani sp. nov. No data on diet or reproduction are available.

      Etymology: The species is named after Professor Pei-Nan Yu, a distinguished doctor in China, in recognition of his great contribution to the treatment of snakebite. We suggest the following common names for this species: “广西华珊瑚蛇” (Chinese) and Guangxi coral snake (English).

      Description of paratypes: The three paratypes are similar to the holotype in body color and pattern. A summary of the morphological and meristic data of the three paratypes is given in Table 1.

      Distribution: This species is currently known from China (Cangwu, Guangxi) and Vietnam (Cao Bằng and Vinh Phuc). The speciemens from Vietnam were unavailable for examination, but molecular phylogeney indicated that they should be conspecific with those from Cangwu, Guangxi, China (Supplementary Appendix S3).

      Phylogenetic position: Both BI and ML analyses recovered a consistent topology, with slight disagreement in support values in some nodes (Figure 1C). In the BI tree, all individuals of Sinomicrurus formed a monophyly with high support (1.00 PP and 100% BS). Within Sinomicrurus, the two species (S. sauteri and S. hatori) endemic to Taiwan, China formed the basal lineage. Sinomicrurus kelloggi and the recently described S. houi Peng, Wang, Ding, Zhu, Luo, Yang, Huang, Lv, & Huang, 2017, formed a highly supported lineage (1.00 PP and 100% BS). All putative individuals of S. macclellandi formed a monophyly with high support indices (1.00 PP and 97% BS), which was sister to a well-supported monophyly consisting of several individuals from Wuzhou and Guangxi, China and from Vietnam with poor support (0.60 PP and 57% BS). However, unexpectedly, all samples of S. m. swinhoei (Denburgh) were nested within the nominated subspecies (Figure 1C). In addition, two specimens from Guangxi, China and Vietnam formed a well-supported clade (97% BS) with all samples of S. houi from Hainan, China.

      Uncorrected P-distances between each in-group taxa/lineage of Sinomicrurus ranged from 1.3% (between S. sauteri and S. hatori) to 14.6% (between S. houi and S. macclellandi) (Supplementary Appendix S4).

      Based on a combination of morphological comparisons and molecular phylogenies, we deemed these specimens to represent an undescribed species, which we described herein.

    • DNA barcoding based on COI is widely applied for rapid and unambiguous identification of species and can be used to screen for potentially cryptic species (Che et al., 2012; Liu et al., 2015). Our results indicated that the genetic distances between the new species and its congeners were much higher than that between other congeners (Supplementary Appendix S4), as well as that between other snakes (Liu et al., 2015), indicating that Sinomicrurus peinani sp. nov. should sever as a specific rank.

      In addition to the large genetic distances between the new species and its congeners, Sinomicrurus peinani sp. nov. can also be differentiated by various phenotypic characters. The new species differs from S. sauteri, S. hatori, and S. japonicus by black longitudinal stripes on body absent (vs. present) (Günther, 1868; Steindachner, 1913; Takahashi, 1930). Sinomicrurus peinani sp. nov. is distinct from S. houi and S. kelloggi by 13 rows of dorsal scales throughout (vs. 15) and broad white band on top of head (vs. two narrow white bands) (Peng et al., 2018; Pope, 1928; Smith, 1943).

      Sinomicrurus macclellandi currently contains four subspecies (Vogel, 2006). Besides the nominate form, which is mainly found in mainland China (Zhao, 2006), S. m. swinhoei (van Denburgh, 1912) is endemic to Taiwan, China, S. m. iwasakii (Maki, 1935) is endemic to Japan, and S. m. univirgatus (Günther, 1868) occurs in India and Nepal. Sinomicrurus peinani sp. nov. differs from S. m. univirgatus by its different body pattern, with the latter having black vertebral strip and transverse bars restricted to sides of body, or absent altogether (Günther, 1868). Sinomicrurus peinani sp. nov. can be distinguished from the other three subspecies by broad white transverse band with inverted V-shaped anterior margin on top of head (vs. two white bands with straight margin) and V-shaped frontal (vs. spindle-shaped frontal), small and not closely arranged cross-bands and spots (Figure 1D) (vs. more closely arranged black cross-bands and spots on belly, such that abdomen appears dark black, Figure 1E) (Reinhardt, 1844; Maki, 1935; van Denburgh, 1912; Zhao, 2006). Sinomicrurus peinani sp. nov. can be distinguished from S. macclellandi by white band on top of head wider than anterior black band vs. white band generally as wide as anterior black band. Historically, several other names have been allied to S. macclellandi, e.g., Calliophis macclellandi gorei Wall, 1910 and Calliophis macclellandi concolor Wall, 1925, with the first described from India and the latter described from Myanmar. Nevertheless, the new species differs from both by having black transverse bars on body (vs. without) (Wall, 1910, 1925).

      Sinomicrurus houi Peng, Wang, Ding, Zhu, Luo, Yang, Huang, Lv, & Huang was originally described only from Hainan, China and was thus regarded as endemic to that area (Peng et al., 2018). However, our molecular phylogenetic results suggested that several closely situated specimens from Guangxi, China and Vietnam formed a monophyly with S. houi from Hainan, China indicating that S. houi may occur on the Asian mainland and may not be endemic to Hainan, China alone. Unexpectedly, the S. m. swinhoei samples were nested within those from mainland China (S. m. macclellandi), indicating that the intraspecific relationship and taxonomy of S. macclellandi need to be further studied.

    • The electronic version of this article in portable document format represents a published work according to the International Commission on Zoological Nomenclature (ICZN), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone (see Articles 8.5–8.6 of the Code). This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information can be viewed through any standard web browser by appending the LSID to the prefixhttp://zoobank.org/.

      Publication LSID:

      urn:lsid:zoobank.org:pub:DB71DFD6-4CE8-448C-8217-926E055D626E.

      Sinomicrurus peinani LSID:

      urn:lsid:zoobank.org:act:8FF100CF-421D-4769-A343-D7B93B02DACC.

    • This field survey was approved by the Department of Forestry of Guangxi Zhuang Autonomous Region, China and Vietnam Adiministration of Forestry (982/TCLN-BTTN).

    • Supplementary data to this article can be found online.

    • The authors declare that they have no competing interests.

    • Q.L., P.G., and J.C. designed the study; P.G., J.W.Y., P.W., S.N.N., and R.W.M. collected specimens; P.G. collected morphological data; Q.L. and S.B.H. collected genetic data; Q.L. performed molecular and phylogenetic analyses and prepared the manuscript; P.G. and J.C. revised the manuscript. All authors read and approved the final version of the manuscript.

    • We appreciate P.L. Yu, Y.L. Xie, J.X. Yang, Z.J. Zhang, K. Jiang, N. Orlov, and K. Li for assistance in field work; M. Yu, D. Wang, J.Q. Jin, and H.M. Chen for assistance in lab work; G.H. Zhong for drawing the map; and K. Jiang for providing references. We thank the Department of Forestry of Guangxi for permission to undertake field survey. We would like to thank Vietnam Administration of Forestry issued the permit and provided local helps during the fieldwork. We extend our sincere gratitude to Amy Lathrop (Royal Ontario Museum, Canada) for the help during the tissue loan.

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