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Research Article
A new species of the genus Hebius (Squamata, Natricidae) from Yunnan, China
expand article infoYu-Hao Xu‡, Dian-Cheng Yang§, Yan-An Gong§, Kai-Chen Ouyang‡, Shi-Yang Weng|, Jun-Dong Deng‡, Song Huang§, Li-Fang Peng‡
‡ Qinghai University, Xining, China
§ Anhui Normal University, Wuhu, China
| Tibet Plateau Institute of Biology, lhasa, China

Corresponding author: Song Huang ( snakeman@ahnu.edu.cn )

Corresponding author: Li-Fang Peng ( lifang@qhu.edu.cn )

Academic editor: Minh Duc Le
© 2024 Yu-Hao Xu, Dian-Cheng Yang, Yan-An Gong, Kai-Chen Ouyang, Shi-Yang Weng, Jun-Dong Deng, Song Huang, Li-Fang Peng.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Xu Y-H, Yang D-C, Gong Y-A, Ouyang K-C, Weng S-Y, Deng J-D, Huang S, Peng L-F (2024) A new species of the genus Hebius (Squamata, Natricidae) from Yunnan, China. ZooKeys 1206: 255-274. https://doi.org/10.3897/zookeys.1206.123841
ZooBank: urn:lsid:zoobank.org:pub:E5C4172E-FD09-48E2-A8EC-C5E109D9674D
Open Access

Abstract

A new species of the genus Hebius Thompson, 1913 is described from Yingjiang County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China, based on molecular and morphological evidence. It can be distinguished from its congeners by the following set of characters: (1) dorsal scale rows 19–17–17, feebly keeled; (2) ventrals 146–151; (3) nasal complete, nostril in the middle of the nasal; (4) supralabials 9, the fourth to sixth in contact with the eye; (5) infralabials 10–11, the first 5 touching the first pair of chin shields; (6) preoculars 2; (7) postoculars 3; (8) temporals 3, arranged in two rows (1+2); (9) maxillary teeth 31, the last 4 slightly enlarged, without diastema; (10) tail comparatively long, TAL/TL ratio 0.334 in the male; (11) dorsolateral series of irregular orange or ochre yellow blotches, extending from the neck to the posterior part of the tail; and (12) venter pale orange, tips of ventrals with subrectangular black blotches. All Hebius specimens were strongly recovered as monophyletic, in which Hebius taronensis (Smith, 1940) and Hebius venningi (Wall, 1910) were monophyletic as sister to the Yingjiang County specimens. According to the p‐distance of cytochrome b, the new species differs from its congeners by 9.7–15.4%.

Key words

Cyt b, Hebius citrinoventer sp. nov., keelback snake, molecular systematics, Natricinae, taxonomy, Yingjiang County

Introduction

The natricine snake genus Amphiesma Duméril, Bibron & Duméril, 1854 long represented a genus of small- to medium-sized, semi-aquatic species, widely distributed from South to Southeast Asia (Guo et al. 2014; Zhou et al. 2019; David et al. 2021). Because of interspecific morphological similarities and lack of broader genetic and morphological sampling, the systematic conflict of this group at the genus and species levels long persists. Based on molecular characteristics, Guo et al. (2014) split the genus Amphiesma into three genera: Amphiesma; Hebius Thompson, 1913, which accounts for most of the species; and Herpetoreas Günther, 1860. Kizirian et al. (2018) found that the genera Parahelicops Bourret, 1934 and Pararhabdophis Bourret, 1934 were junior synonyms of Hebius which was also supported by Ren et al. (2018). The molecular data presented by Patel et al. (2023) revealed a new genus, Sahyadriophis Patel, Thackeray, Campbell & Mirza, 2023, in which Hebius beddomei (Günther, 1864) was included. In addition, the generic assignments of some species have also changed. For example, Hebius xenura (Wall, 1907) and Hebius pealii (Sclater, 1891) have been assigned to Herpetoreas, and Hebius monticola (Jerdon, 1853) has been assigned to Amphiesma (Kizirian et al. 2018; Ren et al. 2018; Das et al. 2020; Lalronunga et al. 2020; Ren et al. 2022; Patel et al. 2023).

Currently, there are 51 valid species in the genus Hebius, of which 26 are known to occur in China (Hauser et al. 2022; Li et al. 2022; Ma et al. 2023; Xu et al. 2023; Uetz et al. 2024). Furthermore, recent morphological and molecular phylogenetic analyses of Hebius have shown that the weak species delimitation within this genus may be due to underestimated diversity (Guo et al. 2014; Kizirian et al. 2018; Liu et al. 2018; Zhou et al. 2019; Hou et al. 2021).

Our morphological and molecular results support the presence of a new snake species, based on two specimens collected from Yingjiang County, Yunnan Province, China (Fig. 1) during field surveys in July 2023 and February 2024. The specimens could be identified as members of Hebius by having the following combination of morphological characters: (1) 2 supralabials in contact with nasal; (2) maxillary teeth in a continuous series, gradually larger posteriorly in the series or the last two teeth abruptly enlarged, the diastema before the distinctly enlarged posterior maxillary teeth absent; (3) internasals broad anteriorly, nostrils lateral; and (4) color pattern usually comprising a dorsolateral series of dark dots, forming two longitudinal stripes. However, these specimens could not be assigned to any known species (Guo et al. 2014; Ren et al. 2018). Furthermore, molecular analyses also revealed that the Yingjiang County specimens differed from those of other congeners.

Figure 1. 

Distribution of selected species of the genus Hebius. Red star: Hebius citrinoventer sp. nov.; purple triangle: H. venningi; blue circle: H. taronensis.

Material and methods

Sampling

One drowned adult female and one road-killed subadult male specimens were collected from Yingjiang County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China. Sex was determined by tail dissection. Liver tissues were extracted and preserved in 95% ethanol. The specimens were preserved in 75% ethanol, and deposited in the Anhui Normal University Museum (ANU) and Qinghai University Museum (QHU). All sampling and procedures involving snake specimens were performed in accordance with the Wild Animals Protection Law of the People’s Republic of China and approved by the Institutional Ethics Committee of Anhui Normal University (protocol code AHNU-ET2021025) and Qinghai University (protocol code SL-2023028).

Molecular phylogeny

Total genomic DNA was extracted from ethanol-preserved liver tissues using the QIAamp DNA Mini Kit (QIAGEN, Changsheng Biotechnology Co. Ltd., Changchun, China). We amplified the fragments of cytochrome b (Cyt b) by the Polymerase Chain Reaction (PCR), using the primers L14910 (5’-GAC CTG TGA TMT GAA AAC CAY CGT TGT-3’) and H16064 (5’-CTT TGG TTT ACA AGA ACA ATG CTT TA-3’) (Burbrink et al. 2000). The PCR products were sequenced by Shanghai Map Biotech Co., Ltd. (Shanghai, China). The raw sequences were stitched using SeqMan in the DNASTAR software package (Burland 2000) and the newly generated sequences were submitted to GenBank (accession numbers: PP472750, ANU20230016; PP429724, QHU2024005).

For phylogenetic analysis, 56 sequences were selected (Table 1), among which 54 (No. 3–56) were obtained from the National Center for Biotechnology Information (NCBI), including 51 sequences from 31 Hebius species and three outgroups: Trachischium monticola (Cantor, 1839), Herpetoreas platyceps (Blyth, 1854), and Herpetoreas burbrinki Guo, Zhu, Liu, Zhang, Li, Huang & Pyron, 2014, and aligned using MEGA X software (Kumar et al. 2018). Tree inference was performed in IQ-TREE v. 1.6.12 (Nguyen et al. 2015) under the maximum likelihood (ML) model, and 5000 replicates of ultrafast bootstrap were used to estimate the Ultrafast Bootstrap Approximation (UFB) node support. The SH-like approximate likelihood ratio test (SH-aLRT) was conducted with 1000 replicates. In addition, we calculated the uncorrected pairwise distances (p-distances) using the MEGA X software (Kumar et al. 2018).

Table 1.
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GenBank accession numbers, localities, and voucher information for all specimens used in this study.

ID Species name Locality Voucher Cyt b Reference
1 Hebius citrinoventer sp. nov. Yingjiang, Yunnan, China ANU20230016 PP472750 This study
2 H. citrinoventer sp. nov. Yingjiang, Yunnan, China QHU2024005 PP429724 This study
3 H. andreae Khammouane, Laos VNUF R.2017.25 MK253674 Ziegler et al. 2019
4 H. annamensis Laos FMNH 258637 OK315812 Deepak et al. 2022
5 H. atemporalis Vietnam ZMMU NAP-07877 OK315813 Deepak et al. 2022
6 H. atemporalis Guangdong, China GP 1626 KJ685680 Guo et al. 2014
7 H. bitaeniatus 1 Guangxi, China GP 1940 KJ685688 Guo et al. 2014
8 H. bitaeniatus 2 Thailand AUP-00062 OK315816 Deepak et al. 2022
9 H. boulengeri Fujian, China GP 2433 KJ685699 Guo et al. 2014
10 H. boulengeri Guangdong, China GP 1789 KJ685684 Guo et al. 2014
11 H. chapaensis Lao Cai, Vietnam VNMN 06102 MH778702 Ren et al. 2018
12 H. chapaensis Lao Cai, Vietnam VNMN 06103 MH778700 Ren et al. 2018
13 H. clerki Pianma, Lushui, Yunnan, China KIZ037714 MZ570478 Hou et al. 2021
14 H. concelarus Miyakojimashi, Ryukyu, Japan KUZ R18555 AB989258 Takuma and Toda 2016
15 H. concelarus Miyakojimashi, Ryukyu, Japan KUZ R20253 AB989268 Takuma and Toda 2016
16 H. craspedogaster Guizhou, China GP 1240 KJ685672 Guo et al. 2014
17 H. deschauenseei Thailand AUP-00182 OK315827 Deepak et al. 2022
18 H. igneus Ha Giang, Vietnam AMNH 148575 KJ685665 Guo et al. 2014
19 H. ishigakiensis Ishigakishi, Ryukyu, Japan KUZ R19251 AB989282 Takuma and Toda 2016
20 H. ishigakiensis Taketomityo, Ryukyu, Japan KUZ R33043 AB989292 Takuma and Toda 2016
21 H. jingdongensis Jingdong, Yunnan, China CIB 119044 OR285310 Ma et al. 2023
22 H. johannis Yunnan, China KIZ014484 MZ570479 Hou et al. 2021
23 H. khasiensis Kachin state, Myanmar CAS 221504 KJ685668 Guo et al. 2014
24 H. khasiensis Kachin state, Myanmar CAS 221525 KJ685669 Guo et al. 2014
25 H. maximus Sichuan, China GP 864 KJ685706 Guo et al. 2014
26 H. maximus Sichuan, China GP 2382 KJ685696 Guo et al. 2014
27 H. metusia Shimian, Sichuan, China KIZ05178 MZ570480 Hou et al. 2021
28 H. metusia Sichuan, China GP 871 KJ685707 Guo et al. 2014
29 H. modestus Yunnan, China CAS 234262 KJ685671 Guo et al. 2014
30 H. modestus Diantan, Tengchong, Yunnan, China KIZ037715 MZ570481 Hou et al. 2021
31 H. octolineatus Kunming, Yunnan, China KIZ026445 MZ570484 Hou et al. 2021
32 H. octolineatus Kunming, Yunnan, China KIZ03204 MZ570483 Hou et al. 2021
33 H. optatus Guizhou, China GP 1885 KJ685687 Guo et al. 2014
34 H. cf. optatus Vinh Phuc, Vietnam AMNH 147155 KJ685662 Guo et al. 2014
35 H. popei Hainan, China GP 2169 KJ685692 Guo et al. 2014
36 H. popei Guizhou, China GP 2386 KJ685697 Guo et al. 2014
37 H. pryeri Tokunoshimacho, Ryukyu, Japan KUZ R34044 AB989124 Takuma and Toda 2016
38 H. pryeri Ryukyu, Japan KUZ R34062 AB989126 Takuma and Toda 2016
39 H. sangzhiensis Hunan, China SYNU08070350 MK340763 Zhou et al. 2019
40 H. sauteri Taiwan, China GP 2549 KJ685701 Guo et al. 2014
41 H. sauteri Guangdong, China CIB 118516 OP937178 Li et al. 2022
42 H. septemlineatus Diantan, Tengchong, Yunnan, China KIZ037706 MZ570485 Hou et al. 2021
43 H. septemlineatus Zizhi, Tengchong, Yunnan, China KIZ037720 MZ570486 Hou et al. 2021
44 H. taronensis Myanmar GP 1618 KJ685679 Guo et al. 2014
45 H. taronensis Myanmar CAS 224426 OK315828 Deepak et al. 2022
46 H. venningi KaChin state, Myanmar CAS 233206 KJ685670 Guo et al. 2014
47 H. vibakari Liaoning, China GP 1345 KJ685676 Guo et al. 2014
48 H. vibakari Heilongjiang, China GP 1352 KJ685677 Guo et al. 2014
49 H. weixiensis Weixi, Yunnan, China KIZ035740 MZ570488 Hou et al. 2021
50 H. weixiensis Lijiang, Yunnan, China HSR19088 OQ085074 Xu et al. 2023
51 H. yanbianensis Yanbian, Sichuan, China GP 4006 MH532291 Liu et al. 2018
52 H. yanbianensis Binchuan, Yunnan, China CIB5334220120 OR215499 Ma et al. 2023
53 H. youjiangensis Baise, Guangxi, China ANU20220010 OQ085073 Xu et al. 2023
Out group
54 Herpetoreas burbrinki Tibet, China YBU 071128 GQ281781 Guo et al. 2014
55 H. platyceps Tibet, China GP 2096 KJ685690 Guo et al. 2014
56 Trachischium monticola Tibet, China GP 1487 JQ687435 Guo et al. 2014

Morphological examination

Morphological characters were described for the newly collected specimen and compared with other key references (Günther 1875; Wall 1910; Wall 1925; Bourret 1934; Taylor 1934; Gressitt 1937; Smith 1940; Dowling 1951a, 1951b; David and Das 2003; Zhao 2006; David and Vogel 2010; Guo et al. 2014; Liu et al. 2018; Ren et al. 2018; Purkayastha and David 2019; Zhou et al. 2019; Ziegler et al. 2019; David et al. 2021; Huang 2021; Hou et al. 2021; Hauser et al. 2022; Li et al. 2022; Ma et al. 2023; Xu et al. 2023). The measurements and scale counts followed those of Dowling (1951a, 1951b), Zhao (2006), and Huang (2021). A ruler with 1 mm accuracy was used to measure the snout-vent length (SVL), measured from the tip of the snout to the anterior edge of the vent ;tail length (TAL), measured from the anterior edge of the vent to the tip of the tail ; and total length (TL), defined as the sum of the SVL and TAL. All other measurement characteristics were measured to the nearest 0.01 mm using digital calipers ; head length (HL), measured from the tip of the snout to the posterior margin of the mandible : head width (HW), measured from the widest part of the head in dorsal view ; and eye diameter (ED), measured from the most anterior corner of the eye to the most posterior corner. Scalation features and their abbreviations are as follows : supralabials (SL) ; infralabials (IL) ; loreals (LOR) ; preoculars (PRO) ; postoculars (PO); Chin : infralabials touching the first pair of chin shields (IFL-1st Chin) ; temporals (TEMP) ; supraoculars (SPO); and three dorsal scale row (DSR) counts: 1) counting from one head length behind the head, 2) at midbody (namely at SVL/2), and 3) at one head length before the vent ; ventral scales (VS) ; cloacal plate (CP); and subcaudal (SC). In addition, we also examined the number of maxillary teeth (MT).

Results

Phylogenetic relationships

The ML tree was reconstructed from a fragment of the mitochondrial Cyt b gene (Fig. 2). Due to the poor quality at both ends of the newly generated sequences, we cut the sequences to obtain a final length of 725 base pairs (bp). All Hebius specimens clustered into one monophyletic group with strong supports (SH 97 / UFB 100). Hebius taronensis (Smith, 1940) and H. venningi (Wall, 1910) were grouped together (SH 100 / UFB 100), forming a sister clade to specimens from Yingjiang County (SH 82 / UFB 93), then clustering with H. septemlineatus (Schmidt, 1925), H. weixiensis Hou, Yuan, Wei, Zhao, Liu, Wu, Shen, Chen, Guo & Che, 2021, and the specimen AUP-00062 that was once identified as H. bitaeniatus (Wall, 1925). Regarding p-distance, the new species differed from its congeners by 9.7% (with H. venningi) to 15.4% (with H. popei (Schmidt, 1925)) (Table 2), which strongly suggests that the newly collected specimens have distinct genetic differentiation from their congeners. Moreover, morphological data supported the recognition of specimens from Yingjiang County as distinct from all other described species of Hebius. Thus, we describe the unnamed specimens as a new species.

Table 2.
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Uncorrected p-distances (%) among the Hebius species based on partial mitochondrial Cyt b gene.

ID Species 1–2 3 4 5–6 7 8 9–10 11–12 13 14–15 16 17 18 19–20 21 22 23–24 25–26 27–28 29–30 31–32 33 34 35–36 37–38 39 40–41 42–43 44–45 46 47–48 49–50 51–52
1–2 H. citrinoventer sp. nov. 1.3
3 H. andreae 16.5–16.9 –
4 H. annamensis 14.2–14.5 12.7 –
5–6 H. atemporalis 12.5–13.7 14.2–15.2 12.5–12.7 6.1
7 H. bitaeniatus 2 10.0 15.9 12.7 10.7–11.0 –
8 H. bitaeniatus1 11.0–11.4 13.7 10.9 9.4–10.5 10.2 –
9– 10 H. boulengeri 13.7–14.5 16.2–16.4 12.2–12.4 11.7–12.2 10.4–10.7 10.4–10.5 1.2
11–12 H. chapaensis 12.9–13.2 12.7 5.7 11.0–11.4 12.2 10.5 12.0–12.2 0
13 H. clerki 13.7–14.0 15.5 12.2 10.4–12.2 12.7 11.5 10.5–10.7 11.0 –
14–15 H. concelarum 14.7–15.0 18.5 14.5 14.0–14.7 13.9 12.9 13.4–13.9 14.0 15.0 0
16 H. craspedogaster 11.4–11.7 14.7 11.0 9.4–11.2 11.5 3.5 11.2–11.4 10.9 12.0 14.4 –
17 H. deschauenseei 12.9–13.0 13.4 7.9 12.2–12.5 13.4 11.0 13.2–13.4 6.0 12.4 14.7 11.5 –
18 H. igneus 13.2–13.4 12.5 5.7 11.4–11.5 12.5 10.9 12.9–13.0 .9 11.5 14.5 11.2 5.7 –
19–20 H. ishigakiensis 12.9–13.2 17.0 12.4 12.0–12.2 12.4 12.2 11.9–12.0 12.5 11.9 12.5 13.2 13.5 12.9 0
21 H. jingdongensis 11.2–11.5 13.0 10.9 9.9–10.2 10.5 7.4 9.2–9.7 10.5 11.4 13.9 8.5 10.5 10.5 12.2 –
22 H. johannis 10.4–10.7 14.2 9.7 10.4–10.5 11.0 4.8 10.5–10.7 9.7 11.4 12.9 5.3 11.5 10.2 12.9 9.9 –
23–24 H. khasiensis 14.9–15.2 15.7–16.5 12.4–12.9 11.4–12.7 12.2–12.4 10.7–11.2 7.5–8.0 12.0–12.2 12.2–12.4 14.0–14.4 11.2–11.5 13.0 12.7–13.0 12.9–13.4 9.5–10.7 11.7 2.8
25–26 H. maximus 13.9–14.4 13.0–13.2 12.7–13.4 11.2–13.2 12.0–12.2 10.4–10.7 13.2–13.7 11.9 13.0–13.4 14.5–14.9 11.0–11.4 11.7–11.9 11.9–12.0 12.0–12.7 11.9–12.2 12.5–12.7 13.7–14.4 0.7
27–28 H. metusia 10.9–11.4 13.5–13.7 10.2–10.7 9.7–9.9 9.7–10.0 2.8–3.5 10.5–11.2 10.2 11.5–11.7 13.2–16.0 4.7 10.5–10.7 10.4–10.5 12.5–12.7 7.5–8.4 4.5–4.8 10.9–11.4 10.4–10.9 1.0
29–30 H. modestus 14.2–15.2 13.4–14.2 6.7–7.0 12.0–13.5 13.4–13.7 12.5–12.9 13.5–14.2 5.0–5.3 12.2–12.9 15.7 13.0–13.2 6.2–6.8 4.8 12.4–12.7 11.7–12.0 12.5 13.9–14.2 12.5–13.2 12.4–12.9 2.3
31–32 H. octolineatus 11.2–11.5 12.7–12.9 10.5–10.7 9.7–11.0 11.4 4.2–4.3 10.0–10.7 10.5–10.7 11.9–12.0 12.5–13.0 4.7–4.8 11.0–11.4 11.0 12.0–12.2 8.2–8.4 5.2–5.3 10.7–11.9 10.5–10.9 4.7–4.8 12.2–12.7 0.5
33 H. cf. optatus 12.9 15.9 13.5 11.9–12.2 11.5 10.0 10.7–10.9 12.5 12.2 13.5 11.0 12.7 12.5 11.7 11.2 10.5 13.5 10.9–11.0 10.9–11.0 13.9–14.0 10.4 –
34 H. optatus 12.7 17.0 13.0 11.5–11.7 11.2 10.4 12.5–12.7 11.2 13.2 13.4 11.0 12.9 11.9 11.7 11.7 11.4 13.4 10.0–10.4 10.0–10.5 13.7–14.7 10.9–11.4 9.9 –
35–36 H. popei 14.2–15.4 15.9–16.5 13.2–13.5 11.0–12.9 13.0–13.4 10.7–11.4 13.5–13.9 13.2–13.5 12.7 15.4–15.7 11.5–12.5 13.2–13.5 13.5–13.9 12.4–13.4 11.4–11.7 12.4–12.5 12.9–14.0 11.2–12.2 11.2–11.9 13.0–13.9 11.9–12.0 11.4–13.2 10.7–11.2 4.0
37–38 H. pryeri 14.4–14.7 18.2 14.7 13.5–13.9 13.5 12.5 12.9–13.0 14.5 13.7 9.0 14.2 15.0 15.0 11.5 13.7 13.4 14.7 12.9–13.0 12.7–12.9 15.4–16.7 12.4–12.5 14.0 13.5 14.4–14.5 0
39 H. sangzhiensis 13.0–13.4 14.2 13.0 11.5–12.5 11.5 9.0 12.4–12.5 11.9 13.0 11.7 11.4 12.0 12.2 11.9 11.5 11.0 12.5–13.0 6.7–7.0 10.7–11.0 12.5–12.9 9.9–10.0 12.0 12.0 11.4 11.5 –
40–41 H. sauteri 12.0–13.0 14.5–15.5 13.4–13.7 10.9–13.2 11.9–12.4 10.4–11.0 11.9–13.2 12.2–12.5 12.0 14.0 10.4–11.5 12.7–12.9 12.7–12.9 11.4–11.5 9.7–10.7 11.7 11.9–13.0 11.2–12.0 10.4–10.7 13.9–14.2 9.7–10.9 11.0–11.7 10.4–10.7 11.2–12.0 13.5–13.9 12.4–13.0 2.3
42–43 H. septemlineatus 10.0–10.2 15.2–15.5 12.2–12.4 11.0–11.7 4.2 10.0–10.2 10.5–11.4 12.0–12.2 12.4–12.7 13.4–13.5 10.5–10.7 12.4–12.7 12.4–12.7 11.7–12.5 9.5–9.7 10.2–10.7 11.7–12.5 11.0–11.5 9.7–9.9 13.0–14.2 10.0–10.2 12.0–12.4 11.4–11.5 12.5–13.7 13.0 10.4–10.7 10.7–11.5 1.0
44–45 H. taronensis 10.7–11.2 14.4–14.5 12.2–12.5 12.2–13.5 10.5–11.0 10.7–11.2 12.7–13.4 11.4–11.7 13.0–13.2 14.4–14.9 10.5–11.0 11.9–12.2 11.7–12.0 12.7–12.9 10.7–11.2 11.0–11.5 13.2–14.0 11.7–12.2 10.0–10.9 12.4–13.0 10.0–10.5 12.4–12.9 12.5–13.0 10.9–11.5 13.0–13.4 10.9–11.4 12.5–13.5 9.7–10.2 0.5
46 H. venningi 9.7–10.0 13.2 11.4 11.0–11.2 8.7 9.0 12.7–12.9 10.2 12.5 13.9 10.5 11.7 10.5 12.2 10.2 9.4 13.0–13.4 12.4–12.7 9.4–9.7 11.4–11.7 9.5–9.9 11.5 12.0 11.4 12.7 10.9 11.7–12.4 8.5–8.8 5.8–6.0 –
47–48 H. vibakari 12.4–12.7 14.4 13.0 10.2–12.5 11.7 9.7 12.7–12.9 11.4 11.7 13.4 11.0 11.9 11.7 12.0 10.0 11.0 12.5 7.9–8.2 10.4–10.5 12.9–13.7 10.4–10.5 12.9 10.4 12.5 13.0 7.2 12.0–12.4 10.2–10.7 11.5–12.0 11.2 0
49–50 H. weixiensis 11.0–11.5 14.9–15.4 12.2 11.4–12.2 5.7–5.8 9.9–10.2 10.9–11.5 11.5–11.9 12.2–12.7 12.9–13.0 10.2–10.5 12.5–12.9 11.9–12.2 12.2–12.4 9.7–10.2 10.5–10.9 12.2–13.0 11.4–11.9 9.9–10.2 12.9–13.5 10.7–11.4 11.7–12.2 10.9–11.0 13.4–13.7 13.4–13.9 10.4–10.9 11.5–12.2 5.0–5.7 9.8–10.9 8.3–8.5 10.4–10.5 0.5
51–52 H. yanbianensis 11.9–12.2 13.7–14.2 11.7–11.9 10.0–10.7 10.7–11.2 3.7–4.2 10.7–11.4 11.0–11.5 12.4–12.7 13.0–13.4 4.8–5.3 11.5–11.7 11.5–11.7 12.4–13.5 9.0–9.5 6.3–6.5 11.2–12.5 11.2–11.4 4.5–4.8 13.0–14.0 5.5–6.0 12.2–12.4 11.5 11.7–12.4 12.5–13.5 10.0–10.5 11.2–12.2 9.5–10.4 10.7–11.4 9.8–10.4 10.7–10.9 9.5–10.4 1.8
53 H. youjiangensis 14.0–14.2 13.9 6.7 11.7–12.7 13.4 11.5 13.2–13.4 5.2 11.5 15.4 12.2 5.5 4.7 13.0 10.2 12.0 13.2–13.9 12.7–12.9 11.2–11.4 3.7 11.5–11.9 13.5 14.0 13.5 15.4 12.2 12.9–13.2 13.0–13.4 12.4–12.7 12.0 12.5 12.9–13.2 12.7–13.0
Figure 2. 

Maximum likelihood tree of the genus Hebius inferred from Cyt b. The nodes supporting values on branches are presented as SH-like approximate likelihood ratio test (SH) / Ultrafast Bootstrap Approximation (UFB); ones under 50% are omitted. Tips for the new species in the present study are shown in red.

Taxonomic account

Natricinae Bonaparte, 1838

Hebius Thompson, 1913

Hebius citrinoventer Xu, Yang, Ouyang, Huang & Peng, sp. nov.

https://zoobank.org/EFBD9EA8-897A-46F4-91AD-12E03C26E7F5
Figs 3, 4, 5

Material examined

Holotype. ANU20230016 (field number: HSR23030, Figs 3, 4), an adult female, collected by Diancheng Yang and Jundong Deng on July 18, 2023, in Tongbiguan Town, Yingjiang County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China (24°36′30.60″N, 97°39′27.00″E, 1300 m a.s.l.). Paratype. QHU2024005 (field number: LFR2024007, Fig. 5), a subadult male, had been crushed to death on the side of the road, collected by Kaichen Ouyang and Lifang Peng on February 5, 2024, in Tongbiguan Town, Yingjiang County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China (24°36′03.60″N, 97°39′05.76″E, 1300 m a.s.l.).

Figure 3. 

Fresh specimen of the holotype (ANU20230016) of Hebius citrinoventer sp. nov.: dorsal (A), and ventral views (B). Photos by Kai-Chen Ouyang. Scale bars are not shown.

Figure 4. 

Preserved specimen of the holotype (ANU20230016) of Hebius citrinoventer sp. nov. Photos by Yu-Hao Xu. Scale bars: 10 mm.

Figure 5. 

Preserved specimen of the paratype (QHU2024005) of Hebius citrinoventer sp. nov. Photos by Yu-Hao Xu. Scale bars: 5 mm.

Etymology

The specific name citrinoventer comprises the Latin words “citrinus” (yellowish-orange or orange) and “venter” (the belly or underside), based on the pale orange venter of the new species. According to its type locality Yingjiang County, Yunnan Province, China, the name we suggest is Yíng Jiāng Fù Liàn Shé (盈江腹链蛇) in Chinese and Yingjiang Keelback Snake in English.

Diagnosis

Hebius citrinoventer sp. nov. can be distinguished from its congeners by the following set of characters: (1) DSR 19–17–17, feebly keeled; (2) ventrals 146–151; (3) nasal complete, nostril in the middle of the nasal; (4) supralabials 9, the fourth to sixth in contact with the eye; (5) infralabials 10–11, the first 5 touching the first pair of chin shields; (6) preoculars 2; (7) postoculars 3; (8) temporals 3, arranged in two rows (1+2); (9) maxillary teeth 31, the last 4 slightly enlarged, without diastema; (10) tail comparatively long, TAL/TL ratio 0.334 in male; (11) dorsolateral series of irregular orange or ochre yellow blotches, extending from the neck to the posterior part of the tail; and (12) venter pale orange, tips of ventrals with subrectangular black blotches.

Comparisons

In many characters, Hebius citrinoventer sp. nov. is similar to H. venningi (Wall, 1910) and H. taronensis (Smith, 1940). However, the new species can be distinguished from H. venningi by (1) 19 DSR on the anterior part of the body (vs. 17), (2) VS 146–151 (vs. 155–172), (3) TEMP 1+2 (vs. 1 or 1+1); (4) maxillary teeth 31 (vs. 28–30), (5) venter pale orange, tips of ventrals with subrectangular black blotches (vs. venter pink or bright coral red, sometimes yellow). It can be distinguished from H. taronensis by (1) 17 DSR at midbody (vs. 19); (2) VS 146–151 (vs. 158–176); (3) TEMP 1+2 (vs. 1 or 1+1); (4) SC 113 (vs. 92–104); (5) tail comparatively longer, TAL/TL ratio 0.334 (vs. TAL/TL ratio 0.254–0.288); and (6) venter pale orange, tips of ventrals with subrectangular black blotches (vs. pale areas of the venter are yellowish-ochre or yellowish-brown). For more detailed information and visual comparisons, please refer to Table 3 and Fig. 6.

Table 3.
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Comparisons of main morphological characters between H. citrinoventer sp. nov., H. taronensis and H. venningi. Abbreviations as per Material and methods.

Species TAL/TL SL IL TEMP DSR VEN SC MT Venter background coloration
H. citrinoventer sp. nov. 0.334 9 10–11 1+2 19–17–17 146–151 113 31 pale orange
H. taronensis 0.254–0.288 9 (rarely 8) 10 1 or 1+1 19–19–17 158–176 92–104 28–32 yellowish-ochre or yellowish-brown
H. venningi 0.295–0.347 9 9–10 1+1 17–17–17 155–172 115–129 28–30 pink or bright coral red, sometimes yellow
Figure 6. 

Comparisons of the lateral head (A), dorsal head (B), dorsal overview (C), and ventral overview (D) among the holotypes of H. citrinoventer sp. nov. (ANU20230016; A1–D1), H. venningi (BMNH 1946.1.21.86; A2–D2), and H. taronensis (BMNH 1946.1.13.55; A3–D3). Photos of H. venningi and H. taronensis were obtained from David et al. (2021), remaining photos by Yu-Hao Xu. Scale bars are not shown.

Due to the absence of a dark belly, Hebius citrinoventer sp. nov. can be distinguished from H. annamensis (Bourret, 1934), H. chapaensis (Bourret, 1934), H. deschauenseei (Taylor, 1934), H. nigriventer (Wall, 1925), H. igneus David, Vogel, Nguyen, Orlov, Pauwels, Teynié & Ziegler, 2021, and H. youjiangensis Yang, Xu, Wu, Gong, Huang & Huang, 2023 (vs. the dark belly present). Moreover, it can be distinguished from H. deschauenseei and H. igneus by having 17 DSR at midbody (vs. 19); from H. chapaensis and H. nigriventer by having 19 DSR on the anterior part of the body (vs. 17); from H. annamensis by having prefrontals 2 (vs. prefrontal single), VS 146–151 (vs. 158–172), IL 10–11 (vs. up to 10); and from H. youjiangensis by having TEMP 1+2 (vs. 1+1), PRO 2 (vs. 1), PO 3 (vs. 2), and dorsolateral series of irregular blotches (vs. a continuous stripe on dorsolateral).

By having 17 DSR at midbody, Hebius citrinoventer sp. nov. can be easily distinguished from the other 35 known species in the genus, which have 19 or 15 rows: H. andreae (Ziegler & Le Khac Quyet, 2006), H. beddomei (Günther, 1864), H. bitaeniatus (Wall, 1925), H. boulengeri (Gressitt, 1937), H. celebicus (Peters & Doris, 1878), H. clerki (Wall, 1925), H. concelarus (Malnate, 1963), H. craspedogaster (Boulenger, 1899), H. flavifrons (Boulenger, 1887), H. inas (Laidlaw, 1901), H. ishigakiensis (Malnate & Munsterman, 1960), H. johannis (Boulenger, 1908), H. kerinciensis (David & Das, 2003), H. khasiensis (Boulenger, 1890), H. lacrima Purkayastha & David, 2019, H. leucomystax (David, Bain, Quang Truong, Orlov, Vogel, Ngoc Thanh & Ziegler, 2007), H. metusia (Inger, Zhao, Shaffer & Wu, 1990), H. modestus (Günther, 1875), H. miyajimae (Maki, 1931), H. nicobariensis (Sclater, 1891), H. octolineatus (Boulenger, 1904), H. optatus (Hu & Zhao, 1966), H. parallelus (Boulenger, 1890), H. petersii (Boulenger, 1893), H. popei (Schmidt, 1925), H. pryeri (Boulenger, 1887), H. sanguineus (Smedley, 1932), H. sangzhiensis Zhou, Qi, Lu, Lyu & Li, 2019, H. sarasinorum (Boulenger, 1896), H. septemlineatus (Schmidt, 1925), H. terrakarenorum Hauser, Smits & David, 2022, H. vibakari (Boie, 1826), H. viperinus (Schenkel, 1901), H. weixiensis Hou, Yuan, Wei, Zhao, Liu, Wu, Shen, Chen, Guo & Che, 2021 and H. yanbianensis Liu, Zhong, Wang, Liu & Guo, 2018.

Compared with the other seven congeners that have 17 DSR at the midbody, Hebius citrinoventer sp. nov. can be distinguished from H. arquus (David & Vogel, 2010), H. atemporalis (Bourret, 1934), H. frenatus (Dunn, 1923), H. sarwacensis (Günther, 1872), H. sauteri (Boulenger, 1909), and H. maximus (Malnate, 1962) by the 19–17–17 DSR counts (vs. 17–17–15 in H. arquus and H. frenatus; and 17–17–17 in H. atemporalis, H. sarwacensis H. sauteri and H. maximus), from H. groundwateri (Smith, 1922) by the divided cloacal plate (vs. CP entire). Furthermore, this new species differs from H. arquus by having a single loreal (vs. the absence of loreal). It differs from H. atemporalis, H. frenatus and H. sarwacensis in terms of SL, namely (9 vs. 6 in H. atemporalis, 5–8 in H. sauteri, and 8 in H. frenatus and H. sarwacensis).

Description of holotype

An adult female specimen with SVL 583 mm and incomplete tail (TAL 198+ mm). Body slightly stout and cylindrical; head flattened anteriorly, distinct from the neck, HL 26.1 mm, HW 15.6 mm. Nostril: lateral, round, piercing in the middle of the nasal. Eye large, ED 3.5 mm, pupil round.

Body scalation : DSR 19–17–17, feebly keeled, including the outermost DSR on both sides, not notched at the posterior extremity. VEN 144 (+2 preventrals); SC 80+, all paired; CP divided.

DSR reduction:

3+4→3 (79–80) (right)

19———————————17

3+4→3 (78–79) (left)

Dentition : Maxillary teeth 31, gradually enlarged, the last four slightly enlarged, without diastema between last four and anterior teeth.

Head scalation : Rostral pentagonal, wider than high, visible from above; nasal entire, subpentagonal, about twice as wide as high; internasals 2, trapezoidal, in broad contact with each other, narrowing anteriorly; prefrontals 2, pentagonal, wider than long, in contact with loreal; frontal narrow, pentagonal, longer than wide, shield-like, slightly concave in the middle on both sides; SPO 1 on each side, hexagonal, much longer than wide; LOR 1/1, subrectangular, wider than long; PRO 2/2, upper one larger than lower one; PO 3/3; SL 9/9, the first 2 in contact with nasal, the 2nd to 4th in contact with the loreal, 4th to 6th entering orbit, the 7th and 8th largest; TEMP 3/3, arranged in two rows (1+2), the anterior temporal long and trapezoidal; chin shields in 2 pairs, the posterior pair longer than anterior one and separated by several small scales; IL 11/11, first pair in contact behind the mental, 1st to 5th touching the first pair of chin shields, the 5th and 7th largest.

Coloration of the fresh specimen : Dorsal surface of the head is olive-brown and scattered with pale-brown vermiculate stripes or irregular blotches. A pale, irregular yellow-ochre oblique streak is directed upward on both sides of the head, extending from the temporal region to the nape. The upper half of the 1st to 8th SL is olive-brown, the lower half is pale brown, and the 9th is completely olive-brown. Ventral surface of head creamy yellow, the edges of partial scales have irregular black-gray patches.

Body olive-brown, darker on the top than on the sides. A faint, yellow-ochre or rusted dorsolateral stripe extends from the neck to the end of the tail, on the upper part of the 5th to the lower part of the 7th scale rows in the anterior part of the body, and the upper part of the 4th to 6th in the middle and posterior parts of the body, accompanied by a series of conspicuous, pale orange or ochre yellow irregular blotches, about two scales in diameter. The orange or ochre yellow blotches are not symmetrically distributed on both sides of the body but are arranged in a staggered manner, that is, the blotch on the left side of the body corresponds to the area between the two blotches on the right side of the body, and vice versa. Above and below the orange blotch, there is a slightly smaller, dull blackish-brown irregular blotch. The blackish-brown blotches above are arranged in a staggered pattern in the middle of the body, forming a checkered pattern with the background color.

Ventral anterior pale orange, darker toward the rear, and scattered with a few small black spots. The outermost edge of the ventral is black. Outer one-sixth of the ventrals with subrectangular black blotches on each side, producing an irregular, continuous ventrolateral stripe, which merges with the dark ventral edge in the posterior part of the body. The ventral surface of the tail is uniform pale orange with black-brown edge; a thin, brown-black stripe extends on the ventral part of the tail, formed by the inner margins of the SC, extending from the 1st SC to the end of the tail.

Coloration in preservation : In preservation, the background color of the dorsal body changed to brownish-black, and the checkered pattern on dorsal surface has disappeared or faded. An indistinct pale-brown dorsolateral stripe extends from the neck to the end of the tail and is accompanied by a series of ochre yellow, irregular blotches. Head brownish-black, upper half of the 1st to 8th supralabials brownish-black, lower half gray white, the 9th completely brownish-black. The infralabials mainly black-gray, the left half of the 5th to 11th pale gray, and the right half very dark gray. Ventral surface of the head cream, the edges of the partial scales had irregular very dark gray patches. The ventral surface of the body cream anteriorly, darker toward the rear, and the posterior part is light creamy yellow. In addition, the rest of the color pattern is similar to that seen in life.

Variation

The paratype has a similar coloration in preservation as the holotype, but the subcaudals are almost completely black, with only the inner margins being creamy yellow. In scalation features, there is the following variation: the paratype has fewer infralabials (10 vs. 11) and more ventrals (151 vs. 146). The measurements and scalation features of the series (N = 2) are listed in Table 4.

Table 4.
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Main morphological characters of Hebius citrinoventer sp. nov. Abbreviations as per Material and methods.

Voucher Number ANU20230016 QHU2024005
Holotype Paratype
Sex Adult female Subadult male
SVL 583 267
TAL 198+ 134
TL 781+ 401
TAL/TL – 0.334
HW 15.6 6.7
HL 26.1 12.6
ED 3.5 1.9
MT 31 –
SL 9/9 9/9
SL-Eye 4th–6th 4th–6th
IL 11/11 10/10
Chin 2 2
IL-1st Chin 1st–5th 1st–5th
LOR 1 1
PRO 2 2
PO 3 3
TEMP 1+2 1+2
DSR 19–17–17 19–17–17
VS 146 151
SC 80+ 113
CP 2 2

Distribution and habitat

Hebius citrinoventer sp. nov. is currently only known from Yingjiang County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China: Tongbiguan Town (1300 m a.s.l.) (Fig. 7). The holotype (ANU20230016) was found drowned in a fish-catching cage placed by local residents in a wide stream at approximately 7:00 am, and we presume that it may have fallen into the trap the preceding night while attempting to catch fish in the cage. The paratype (QHU2024005) was found road-killed on the side of the road next to a stream after a light rain between 21:00 and 22:00. Both specimens were found in a well-preserved monsoon forest habitat.

Figure 7. 

Habitat of Hebius citrinoventer sp. nov., Tongbiguan Town, Yingjiang County, Yunnan Province. Photos by Kai-Chen Ouyang.

Discussion

In this study, we combined morphological and molecular analyses of specimens in the genus Hebius to provide robust evidence for the identification of new species. Based on molecular phylogenetic analysis, we found that the sequence KJ685679 (voucher number: GP 1618) from Myanmar clustered together with H. taronensis and had a very low p-distance of approximately 0.3% in Cyt b. However, it was referred to as Hebius sp. in Guo et al. (2014) but tentatively as H. venningi in David et al. (2021). Because the specimen was not examined, we conservatively assigned it to H. taronensis. Additionally, the uncorrected p-distance between specimen AMNH 147155 from Vietnam and H. optatus was 9.8%, which clearly reached the inter-species level; therefore, we proposed the specimen as H. cf. optatus. Likewise, the phylogenetic structure showed that the specimens (GP 1940 and AUP-00062), which were once considered Hebius bitaeniatus, clustered in different clades: H. craspedogaster, H. johannis, H. metusia and H. octolineatus were clustered together with low support and formed a sister group with specimen GP 1940; the specimen AUP-00062 was clustered with H. septemlineatus with high support (SH 93 / UFB 99), and the uncorrected p-distance was 4.2%. However, due to the lack of morphological and molecular data on the topotype, the classification status of these two specimens requires further study.

The new species, Hebius citrinoventer sp. nov., has some morphological features common to H. venningi and H. taronensis, but can still be distinguished from them in the following characters: dorsal scale rows, number of temporal and ventral scales, and venter color pattern. Molecular phylogenetic analysis also separated the new species H. citrinoventer sp. nov. and provided strong support for its placement as a sister taxon. Moreover, the new species also possessed a considerable level of genetic divergence from 9.7–10.0% for H. venningi and 10.9–11.2% for H. taronensis in Cyt b. In addition, the new species is geographically isolated by the Hengduan Mountains, which plays an important role as a geographical barrier in speciation.

The genus Hebius is a highly diverse group distributed throughout eastern and southern Asia. Owing to the semi-aquatic habitats of this genus, specimen collection is relatively difficult, and the population and distribution data for many species is insufficient, which poses obstacles to conservation. Yingjiang County, where the new species was found, lies in the southwest Yunnan Province and is one of the most biodiverse regions in China. Although the discovery site of this new species is legally protected, the holotype derived from the fish trap and the road-killed paratype clearly indicates that this species is still influenced by human activities. Further surveys and evaluation of the population of the new species should be performed, and further consideration should be given to incorporating it in the local protected animal lists for protection.

In China, most species of Hebius are known from Yunnan Province, and the identification of Hebius citrinoventer sp. nov. brings the total number of Hebius species in China to 27, of which 20 are reported in Yunnan Province. This result further illustrates that reptile diversity in Yunnan is still underestimated. Therefore, more specific surveys may help to better understand the biodiversity in southwest China.

Conclusion

Here, we describe a new species of the genus Hebius, Hebius citrinoventer sp. nov., based on two specimens collected from Yingjiang County, Dehong Dai and Jingpo Autonomous Prefecture, Yunnan Province, China. The discovery of this new species has brought the total number of known species in the genus Hebius to 52. Currently, Hebius citrinoventer sp. nov. is only known to be distributed in southwest Yunnan Province, China. Since Yingjiang County is close to the borders of Myanmar, this species also probably occurs in the adjacent area of this country. However, the detailed distribution range, population size, and feeding habits of the new species have not yet been elucidated, and further research and evaluation of the population of the new species should be conducted.

Acknowledgements

We are grateful to Dr Christopher Glasby, Jun-Man Huang (Southern Illinois University), and Editage (www.editage.cn) for English language editing. We thank the reviewers Dr Patrick David and Dr Vinh Quang Luu for valuable and helpful comments.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

All sampling and procedures involving snake specimens were performed in accordance with the Wild Animals Protection Law of the People’s Republic of China, approved by the Institutional Ethics Committee of Anhui Normal University (protocol code AHNU-ET2021025 and date of approval 7 May 2021) and Qinghai University (protocol code SL-2023028 and date of approval 15 March 2023).

Funding

This research was funded by the National Natural Science Foundation of China (32301325; 31471968), the Project of Qinghai Science & Technology Department (2024‐ZJ‐965), and the Open Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (2023‐ZZ‐08).

Author contributions

YHX, DCY, YAG, HCOY and SYW measured the specimens, analyzed the data, constructed the phylogenetic tree, and prepared the manuscript; LFP and SH provided the funding for the field survey; LFP, JDD and SH conceived and designed the study and reviewed the manuscript before submission. All authors have read and agreed to the published version of the manuscript.

Author ORCIDs

Yu-Hao Xu https://orcid.org/0000-0001-6094-6680

Dian-Cheng Yang https://orcid.org/0000-0001-6390-5251

Yan-An Gong https://orcid.org/0000-0002-8155-7024

Kai-Chen Ouyang https://orcid.org/0009-0003-6876-4699

Song Huang https://orcid.org/0000-0001-6786-8523

Li-Fang Peng https://orcid.org/0000-0001-9325-7048

Data availability

All of the data that support the findings of this study are available in the main text.

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1Yu-Hao Xu1 and Dian-Cheng Yang have contributed equally to this work.
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