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A new species of Achalinus Peters, 1869 (Squamata, Xenodermidae) from Hunan Province, China
expand article infoShun Ma‡§, Sheng-Chao Shi‡§, Sun-Jun Xiang|, Fu Shu, Jian-Ping Jiang‡§
‡ Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
§ University of Chinese Academy of Sciences, Beijing, China
| Huaihua University, Huaihua, China
¶ Central South Academy of Inventory and Planning of NFGA, Changsha, China

Corresponding author: Jian-Ping Jiang ( jiangjp@cib.ac.cn )

Academic editor: Robert Jadin
© 2023 Shun Ma, Sheng-Chao Shi, Sun-Jun Xiang, Fu Shu, Jian-Ping Jiang.
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: Ma S, Shi S-C, Xiang S-J, Shu F, Jiang J-P (2023) A new species of Achalinus Peters, 1869 (Squamata, Xenodermidae) from Hunan Province, China. ZooKeys 1166: 315-331. https://doi.org/10.3897/zookeys.1166.103055
ZooBank: urn:lsid:zoobank.org:pub:11887A71-8708-46AB-AB6D-B864779D5075
Open Access

Abstract

A new species, Achalinus hunanensis sp. nov., is described from middle and western Hunan Province based on the results of molecular systematics and morphological characters. It diverges from known congeners by a significant genetic divergence (p-distance 3.2%–16.9% based on CO1 mitochondrial gene), and it can be distinguished from all known congeners by the following morphological characters: (1) all dorsal scales strongly keeled, 23 rows throughout the body, the outmost one strongly keeled and enlarged; (2) tail relatively short, TaL/TL 0.221 ~ 0.225; (3) maxillary teeth 23; (4) the suture between internasals 2 × as long as that between prefrontals; (5) loreal one, subrectangular, LorH/LorL 0.62 ~ 0.70; (6) supralabials 6, the 4th and 5th touch the eye; (7) the two anterior temporals in contact with eye; (8) ventrals 163–165, subcaudals 69–72, not paired. This raises the number of known species of Achalinus to 24.

Key words

Achalinus hunanensis sp. nov., morphology, phylogeny, divergence time, taxonomy

Introduction

The odd-scaled snake genus Achalinus Peters, 1869, which is widely distributed in northern Vietnam, China, and Japan, is a group of small to medium-sized, nocturnal, fossorial, and non-venomous snakes (Zhao et al. 1998; Zhao 2006). It is the most diverse genus of six known genera of the family Xenodermidae: 23 species in Achalinus; two species in Fimbrios Smith, 1921; two species in Parafimbrios Teynié, David, Lottier, Le, Vidal & Nguyen, 2015; one species in Paraxenodermus Deepak, Lalronunga, Lalhmingliani, Das, Narayanan, Das & Gower, 2021; two species in Stoliczkia Jerdon, 1870; one species in Xenodermus Reinhardt, 1836 (Ha et al. 2022; Yang et al. 2022; Zhang et al. 2023). Among Achalinus species, more than half (14/23) have been described since 2019 (Wang et al. 2019; Ziegler et al. 2019; Li et al. 2020; Luu et al. 2020; Miller et al. 2020; Hou et al. 2021; Huang et al. 2021; Li et al. 2021; Ha et al. 2022; Yang et al. 2022; Zhang et al. 2023). Besides, previous studies revealed that A. ater Bourret, 1937, A. formosanus Boulenger, 1908, A. huangjietangi Huang, Peng & Huang, 2021, A. niger Maki, 1931, A. rufescens Boulenger, 1888, and A. spinalis Peters, 1869 required further studied, due to their distinct morphology variation, deep intraspecific divergence, or non-monophyletic relationship (Zhao et al. 1998; Miller et al. 2020; Huang et al. 2021; Zhang et al. 2023). However, because of poor sampling, morphological and molecular information of Achalinus were lacking, leading to unresolved taxonomic problems and poorly known distribution patterns. Therefore, the diversity of this genus is underestimated and further research is required.

During our field work, two specimens were collected from Hunan Province, China (Fig. 1). They could be assigned to Achalinus by body small, slender, and cylindrical; whole body scales strongly keeled, lanceolate-shaped, and metallic luster; and preocular and postocular absent, loreal and temporals contacting the eyes directly. However, further morphological and molecular analyses revealed that these specimens comprise a separate taxon from other known species. Thus, we described them as a new species herein.

Figure 1. 

Distribution of Achalinus hunanensis sp. nov. and its sister taxon A. ningshanensis. Blue pentacle: the type locality of A. ningshanensis: Xunyangba, Ningshan County, Shaanxi Province, China. Red triangle: the type locality of A. hunanensis sp. nov. (CIB 119039): Hecheng District, Huaihua City, Hunan Province, China. Red circle: A. hunanensis sp. nov. (CIB 119040): Wazizhai, Ningxiang County, Changsha City, Hunan Province, China.

Materials and methods

Molecular phylogenetic analyses

Two specimens of the genus Achalinus were collected in Hunan Province, China: CIB 119039 was collected in Huaihua City, and CIB 119040 was collected in Ningxiang County, and they were deposited in Chengdu Institute of Biology (CIB) of Chinese Academy of Sciences (CAS). Genomic DNA were extracted from preserved muscle tissues of them using QIAamp DNA Mini Kit (QIAGEN, Changsheng Biotechnology Co. Ltd). A fragment of the mitochondrial cytochrome c oxidase subunit 1 (CO1) was amplified using the primer pairs dglco and dghco (Meyer et al. 2005). The polymerase chain reaction (PCR) was performed in 25 μL of reactant with the following cycling conditions: 95 °C for 4 min; 35 cycles of denaturing at 95 °C for 30 s, annealing at 48 °C for 30 s, and extending at 72 °C for 60 s; and a final extending step of 72 °C for 10 min (Wang et al. 2019). PCR products were sequenced by Beijing Qingke New Industry Biotechnology Co., Ltd.

For phylogenetic analysis, 25 sequences (Table 1) were selected, among which 23 sequences (NO. 3–25) were obtained from National Center for Biotechnology Information (NCBI) including 22 sequences from 19 species of Achalinus and three sequences of Fimbrios klossi Smith, 1921, Parafimbrios lao Teynié, David, Lottier, Le, Vidal & Nguyen, 2015 and Xenodermus javanicus Reinhardt, 1836, which were used as outgroups (Luu et al. 2020; Ha et al. 2022).

Table 1.
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Localities, voucher information, GenBank numbers, and references for all samples used in this study.

NO. Species Locality Voucher CO1 GenBank No. References
1 A. hunanensis sp. nov. Huaihua, Hunan, China CIB 119039 OQ848425 This study
2 A. hunanensis sp. nov. Ningxiang, Hunan, China CIB 119040 OQ848426 This study
3 A. ningshanensis Ningshan, Shaanxi, China ANU 20220006 ON548422 Yang et al. 2022
4 A. ningshanensis Ningshan, Shaanxi, China ANU 20220007 ON548423 Yang et al. 2022
5 A. ater Huaping Nature Reserve, Guangxi, China SYS r00852 MN380334 Wang et al. 2019
6 A. dehuaensis Dehua, Fujian, China YBU 13013 MZ442662 Li et al. 2021
7 A. emilyae Hoanh Bo, Quang Ninh, Vietnam IEBR 4465 MK330857 Ziegler et al. 2019
8 A. formosanus Taiwan, China RN2002 KU529452 Unpublished
9 A. huangjietangi Huangshan, Anhui, China HSR18030 MT380191 Huang et al. 2021
10 A. juliani Ha Lang, Cao Bang, Vietnam IEBR A.2018.8 MK330854 Ziegler et al. 2019
11 A. meiguensis Mianyang, Sichuan, China GP835 MZ442641 Li et al. 2021
12 A. niger Taiwan, China RN0667 KU529433 Unpublished
13 A. panzhihuaensis Yanbian, Sichuan, China KIZ 040189 MW664862 Hou et al. 2021
14 A. pingbianensis Honghe, Yunnan, China YBU 18273 MT365521 Li et al. 2020
15 A. rufescens Hongkong, China SYS r001866 MN380339 Wang et al. 2019
16 A. spinalis Badagong Mountains, Hunan, China SYS r001327 MN380340 Wang et al. 2019
17 A. timi Thuan Chau, Son La, Vietnam IEBR A.2018.10 MK330856 Ziegler et al. 2019
18 A. tranganensis Ninh Binh, Vietnam VNUF R.2018.21 MW023086 Luu et al. 2020
19 A. vanhoensis Van Ho, Son La, Vietnam VNUF R.2019.13 ON677935 Ha et al. 2022
20 A. yangdatongi Wenshan Nature Reserve, Yunnan, China KIZ 034327 MW664865 Hou et al. 2021
21 A. yunkaiensis Dawuling Forestry Station, Guangdong, China SYS r001443 MN380329 Wang et al. 2019
22 A. zugorum Bac Me, Ha Giang, Vietnam IEBR 4698 MT502775 Miller et al. 2020
23 Fimbrios klossi Quang Ngai, Vietnam IEBR 3275 KP410744 Teynié et al. 2015
24 Parafimbrios lao Louangphabang, Laos MNHN 2013.1002 KP410746 Teynié et al. 2015
25 Xenodermus javanicus Sumatera Barat, Indonesia: — KP410747 Teynié et al. 2015

CO1 sequences (681 bp) were input in MEGA11 (Tamura et al. 2021) and aligned by MUSCLE (Edgar 2004), and then the uncorrected pairwise distances (p-distance) were calculated in MEGA11. IQ-TREE 1.6.12 was used to conduct the maximum likelihood (ML) analysis (Nguyen et al. 2015) under the best-fit model TN+F+I+G4 selected by Modelfinder according to BIC (Kalyaanamoorthy et al. 2017). Ultrafast Bootstrap Approximation (UFB) node support as assessed by using 5000 ultrafast bootstrap replicates and the UFB ≥ 95 was considered significantly supported (Hoang et al. 2018). The single branch tests were made using SH-like approximate likelihood ratio test (SH-aLRT) via 1000 replicates, and the SH ≥ 80 was also considered supported well (Stephane et al. 2010). For Bayesian inference (BI), the best-fitting model HKY+I+G was selected by jModelTest 2.1.10 identified via BIC (Darriba et al. 2012) on CIPRES (Miller et al. 2010). The Bayesian inference analysis was conducted using MrBayes v. 3.2.1 (Ronquist et al. 2012) under HKY+I+G this model, and four chains run was calculated for 10 million generations, sampled every 1000 with the first 25% of samples discarded as burn-in, resulting in a potential scale reduction factor (PSRF) of ≤ 0.005. Bayesian posterior probabilities (BI) ≥ 0.95 were considered supported well.

We also estimated divergence time by BEAST v. 2.6.7 using CO1 sequences dataset (Bouckaert et al. 2019). Three calibration constraints were used: the divergence time between Achalinus and other Xenodermatidae: 38.6 Mya; the divergence time between Xenodermus and Fimbrios + Parafimbrios: 29.67 Mya; and the divergence time between Fimbrios and Parafimbrios: 17.66 Mya (Kumar et al. 2022). Two independent searches of 20 million generations were conducted, sampling every 1000 iterations with 25% of the initial samples discarded as burn-in. Tracer v. 1.7.2 was used to evaluate estimate ESS for all parameters (Rambaut et al. 2018).

Morphological examination

Morphological data of known species of Achalinus were obtained from the two newly collected specimens, examination of museum specimens (A. ater: n = 1; A. rufescens: n = 1; A. yunkaiensis: n = 1) (Appendix 1) and many key references (Boulenger 1888, 1893, 1896; Denburgh 1912; Bourret 1935, 1937; Hu and Zhao 1966; Hu et al. 1973; Koshikawa 1982; Zong and Ma 1983; Ota and Toyama 1989; Zhao et al. 1998; Zhao 2006; Wang et al. 2019; Ziegler et al. 2019; Li et al. 2020; Luu et al. 2020; Miller et al. 2020; Yu et al. 2020; Hou et al. 2021; Huang et al. 2021; Li et al. 2021; Chen et al. 2022; Ha et al. 2022; Xu et al. 2023; Yang et al. 2022; Zhang et al. 2023).

Morphological descriptions followed Zhao (2006) and Yang et al. (2022). Three characters were measured to the nearest 1 mm by Deli Stainless Ruler (No. 8460): snout-vent length (SVL), tail length (TaL) and total length (TL); the other characters were measured to the nearest 0.01 mm by Deli Digital Vernier Caliper (DL91150): head length (HL), head width (HW), eye horizontal diameter (ED), loreal height (LorH), loreal length (LorL), length of the suture between internasals (LSBI), length of the suture between prefrontals (LSBP). We counted the following ratios: TaL/TL: tail length/total length, LorH/LorL: loreal height/loreal length, LSBI/LSBP: length of the suture between internasals/length of the suture between prefrontals, HL/HW: ratio head length/head width. We also directly compared the length of the sutures between internasals and prefrontals (LSBI vs. LSBP).

Scalation features and their abbreviations are as follows: loreals (Loreal), supralabials (SPL), infralabials (IFL), the number of chin shield pairs (Chins), the number of infralabials touch the first pair of chin shields (IFL-1st Chin), supraoculars (SPO), temporals (TEM), the number of anterior temporals touch the eye (aTEM-Eye) (those head bilateral scale counts were given as left/right), pre-ventral scales (PrV), ventral scales (VEN), subcaudal (SC), entire or divided of the anal (Anal), dorsal scale rows (DSR) (counted at one-head-length behind the head, at midbody, at one-head-length before the anal). We also counted the number of maxillary teeth (MT) under the microscope.

Results

Molecular systematics

All Achalinus samples cluster in a monophyletic group with high supporting values (SH 100/ UFB 100/ BI 1), and they can be divided into six clades, although the relationships among these clades are still unresolved (Fig. 2). Clade A contains A. dehuaensis Li, Wu, Xu. Zhu, Ren, Guo & Dong, 2021; clade B contains A. emilyae Ziegler, Nguyen, Pham, Nguyen, Pham, Van Schingen, Nguyen & Le, 2019, A. rufescens and A. tranganensis Luu, Ziegler, Ha, Lo, Hoang, Ngo, Le, Tran & Nguyen, 2020; clade C A. zugorum Miller, Davis, Luong, Do, Pham, Ziegler, Lee, De Queiroz, Reynolds & Nguyen, 2020, A. huangjietangi, A. panzhihuaensis Hou, Wang, Guo, Chen, Yuan & Che, 2021, A. meiguensis Hu & Zhao, 1966, A. spinalis, A yunkaiensis Wang, Li & Wang, 2019, A. niger and A. formosanus; Clade D includes A. timi Ziegler, Nguyen, Pham, Nguyen, Pham, Van Schingen, Nguyen & Le, 2019 and A. vanhoensis Van Ha, Ziegler, Sy, Le, Nguyen & Luu, 2022, and Clade E contains A. pingbianensis Li, Yu, Wu, Liao, Tang, Liu & Guo, 2020, respectively. Clade F consists five species with a significantly high nodal support (SH 100/ UFB 100/ BI 1; divergence time: 1.76 Mya, 95% highest posterior density interval (HPD): 2.473 ~ 0.988 Mya), of which, the two specimens newly collected in this work are firstly clustered together as a lineage with well support (SH 88/UFB 96/BI 0.98; divergence time: 0.21 Mya, 95% HPD: 0.534 ~ 0.003 Mya), and then clustered with A. ningshanensis Yang, Huang, Jiang, Burbrink, Gong, Yu, Zhang, Huang & Huang, 2022 (SH 98/UFB 100/BI 1; divergence time: 0.48 Mya, 95% HPD: 0.914 ~ 0.120 Mya), forming a sister group of A. yangdatongi Hou, Wang, Guo, Chen, Yuan & Che, 2021 diverged at 0.83 Mya (95% HPD: 1.418 ~ 0.279 Mya), and then they form a sister group of the lineage which contains the A. ater and A. juliani Ziegler, Nguyen, Pham, Nguyen, Pham, Van Schingen, Nguyen & Le, 2019 (divergence time: 1.27 Mya, 95% HPD: 1.930 ~ 0.602 Mya) (Fig. 3).

Figure 2. 

Phylogenetic tree of the genus Achalinus inferred from CO1 gene fragment (681 bp) using Maximum Likelihood. The tree nodes present the supporting values: SH-like approximate likelihood ratio test, Ultrafast Bootstrap Approximation and Bayesian posterior probabilities, respectively (SH, %/UFB, %/BI) (the ones lower than 50 are displayed as “-”). Achalinus ningshanensis is noted in blue and A. hunanensis sp. nov. is noted in red.

Figure 3. 

Divergence date estimation (Mya) and 95% HPD (in square bracket) of Clade F. Achalinus ningshanensis is in blue and A. hunanensis sp. nov. is in red.

The genetic distances range from 5.0% (A. timi and A. vanhoensis) to 18.1% (A. dehuaensis and A. meiguensis) among the known Achalinus species studied in this work (Table 2), of which, within the Clade F, the genetic distances among the four known species range from 5.8% (A. ningshanensis and A. yangdatongi) to 9.6% (A. juliani and A. ningshanensis), while the lineage composed by those two newly collected specimens range from 3.2% to 8.8% divergent from congeners.

Table 2.
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Uncorrected p-distances (%) among Achalinus species inferred from mitochondrial CO1 gene.

1–2 3–4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
1–2 A. hunanensis sp. nov. 0.5
3–4 A. ningshanensis 3.2–3.3 0.7
5 A. ater 7.1–7.3 7.6–7.7
6 A. dehuaensis 15.1–15.2 16.3–16.5 16.5
7 A. emilyae 12.9–13.3 13.5–14.1 11.7 15.7
8 A. formosanus 13.8–13.9 14.8–15.1 14.1 15.7 14.6
9 A. huangjietangi 16.8–16.9 17.2 15.0 16.8 14.8 16.2
10 A. juliani 8.7–8.8 9.1–9.6 7.1 15.2 11.5 13.4 14.8
11 A. meiguensis 16.4 17.0 15.4 18.1 15.4 15.6 15.2 16.8
12 A. niger 13.2–13.3 14.6 13.5 15.7 12.9 9.0 14.6 12.9 13.9
13 A. panzhihuaensis 16.2 17.1–17.4 16.2 15.3 16.6 16.0 15.2 15.5 11.6 14.4
14 A. pingbianensis 11.1–11.2 11.7–12.4 11.8 14.8 13.0 14.5 13.0 12.2 16.8 11.7 14.9
15 A. rufescens 12.1–12.2 12.3–12.7 12.7 14.3 8.0 14.1 14.3 12.3 17.3 12.7 16.0 12.9
16 A. spinalis 14.0–14.3 15.1–15.6 15.2 14.3 13.9 13.9 13.4 13.9 16.0 13.5 15.8 13.3 13.0
17 A. timi 12.1 13.6 13.3 15.8 12.9 14.0 14.8 13.7 15.8 12.0 15.5 12.2 13.9 14.3
18 A. tranganensis 13.7–14.2 14.3–15.2 12.7 14.2 10.6 17.3 13.7 12.3 16.4 14.9 16.4 13.3 11.5 14.6 13.5
19 A. vanhoensis 11.3–11.7 12.1–12.4 13.1 15.8 12.3 14.1 14.8 13.5 15.6 12.6 15.5 10.8 13.8 12.9 5.0 13.3
20 A. yangdatongi 5.1 5.8–5.9 6.2 14.0 12.8 14.4 14.6 7.3 17.1 13.7 15.5 11.3 11.5 14.2 13.1 12.8 11.3
21 A. yunkaiensis 11.7–12.1 13.0–13.7 12.8 14.7 13.1 12.3 12.5 12.5 15.8 12.2 15.7 11.6 13.3 12.0 14.1 13.5 13.6 12.0
22 A. zugorum 11.6–11.9 12.8 13.1 14.3 12.9 13.7 14.4 13.5 15.0 13.4 15.3 10.9 13.5 13.3 13.4 12.5 12.0 12.2 10.9

The results above indicate that the Hunan samples are close to the species A. ningshanensis but consist independent evolution lineage.

Morphological systematics

The two specimens of the genus Achalinus newly collected from Hunan Province can be easily distinguished from all other known congeners (Tables 3, 4). By having 23-23-23 dorsal scale rows, the two specimens can be distinguished from these species including A. formosanus formosanus Boulenger, 1908 (vs. 29-27-25), A. f. chigirai Ota & Toyama, 1989 (vs. (25–27)-(25–27)-25), A. meiguensis (vs. (21–23)-(19–21)-(19–21)), A. niger (vs. 25-25-23), A. panzhihuaensis (vs. 23-23-19), A. timi (vs. 25-25-23), A. tranganensis (vs. 25-23-23), A. vanhoensis (vs. 25-23-23), A. zugorum (vs. 25-23-23). By having loreal separated from prefrontal, they are different from A. jinggangensis and A. pingbianensis (vs. loreal fused with prefrontal). By having LSBI vs. LSBP > 1, they differ from A. dabieshanensis Zhang, Liu, Huang, Hu, Yu, Sun, Zhang, Wen & Zhang, 2023 (vs. < 1), A. hainanus Huang, 1975 (vs. = 1), A. huangjietangi (vs. < 1), A. spinalis (vs. < 1), A. werneri Van Denburgh, 1912 (vs. = 1) and A. yunkaiensis (vs. = 1). By having more ventrals (163–165), they can be distinguished from A. dehuaensis (vs. 142–154), A. emilyae (157–161), and A. rufescens (vs. 132–156).

Table 3.
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Main morphological characters of Achalinus hunanensis sp. nov.

Voucher Number CIB 119039 CIB 119040
Holotype Paratype
Sex Male Male
SVL 255 204
TaL 74 58
TL 329 262
TaL/TL 0.225 0.221
Loreal 1/1 1/1
LorH 1.03/1.04 0.91/0.93
LorL 1.54/1.58 1.46/1.49
LorH/LorL 0.70/0.66 0.62/0.62
LSBI 1.78 1.52
LSBP 0.88 0.76
LSBI/LSBP 2.02 2.00
LSBI vs. LSBP > 1 > 1
HL 7.91 6.33
HW 4.80 3.38
HL/HW 1.65 1.87
ED 1.42/1.41 1.37/1.36
MT 23 23
SPL 3-2-1/3-2-1 3-2-1/3-2-1
IFL 5/6 5/5
IFL-1st Chin 3/4 3/3
SPO 1/1 1/1
TEM 2+2+4/2+2+4 2+2+4/2+2+4
aTEM-Eye 2/2 2/2
PrV 2 2
VEN 163 165
SC 69 72
Anal Entire Entire
DSR 23-23-23 23-23-23
Table 4.
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Morphological characters of Achalinus obtained from specimens examined in this study and literatures (Boulenger 1888, 1893, 1896; Denburgh 1912; Bourret 1935, 1937; Hu and Zhao 1966; Hu et al. 1973; Koshikawa 1982; Zong and Ma 1983; Ota and Toyama 1989; Zhao et al. 1998; Zhao 2006; Wang et al. 2019; Ziegler et al. 2019; Li et al. 2020; Luu et al. 2020; Miller et al. 2020; Yu et al. 2020; Hou et al. 2021; Huang et al. 2021; Li et al. 2021; Chen et al. 2022; Ha et al. 2022; Yang et al. 2022; Zhang et al. 2023; Xu et al. 2023). Int. fus.: internasal fused to prefrontal; Pre fus.: prefrontal fused to loreal; PtO: postoculars.

Species TaL/TL MT Int fus. Pre fus. LorH/LorL LSBI vs. LSBP DSR PtO SPL SPL-Eye IFL IFL-1st Chin TEM aTEM-Eye VEN SC
A. ater 0.190 ~ 0.220 – 0 0 0.40 > 1 (21–23)-(21–25)-(21–25) 0 6 4–5 5–6 1–3 2+2+3 2 160–170 47–70
A. dabieshanensis 0.168 ~ 0.223 – 0 0 0.73 ~ 0.83 < 1 23-23-23 0 6 4–5 5 1–3 2+2+3(4) 2 141–155 45–55
A. dehuaensis 0.206 ~ 0.286 31–33 0 0 – > 1 23-23-23 0 6 4–5 5 1–3 2+2(3)+3(4) 1–2 142–154 63–81
A. emilyae 0.183 ~ 0.203 27–28 0 0 – > 1 23-23-23 0 6 4–5 5 1–3 2+2+3 1 157–161 56–63
A. formosanus chigirai 0.317 14 0 1 – = 1 (25–27)-(25–27)-25 0 6 4–5 5–6 – 2+2 2 161–167 96–97
A. f. formosanus 0.159 17 0 1(usually) – = 1 29-27-25 0 6 4–5 6–7 – 2+2 1 158–184 61–83
A. hainanus 0.258 ~ 0.266 – 0 0 – = 1 23-23-23 0 6 4–5 5 1–3 1+2+3(4) 1 165–168 67–69
A. huangjietangi 0.152 ~ 0.232 – 0 0 0.70 ~ 0.74 < 1 23-23-23 0 6 4–5 5–6 1–3(4) 2+2+3(4) 2 157–170 40–67
A. hunanensis sp. nov. 0.221 ~ 0.225 23 0 0 0.62 ~ 0.70 > 1 23-23-23 0 6 4–5 5–6 1–3(4) 2+2+4 2 163–165 69–72
A. jinggangensis 0.174 ~ 0.217 – 0 1 – > 1 23-23-23 0 6 4–5 6 1–4 2(1)+2+3(4) 2 156–164 51–64
A. juliani 0.224 ~ 0.268 28 0 0 – > 1 25-23-23 0 6(7) 4–5(5–6) 6 1–3(4) 2+2+4 2 163–179 77–91
A. meiguensis 0.142 ~ 0.238 17 1 0 – – (21–23)-(19–21)-(19–21) 1 6 4–5 6 1–3 2(3)+2(3) 1 146–173 39–60
A. niger 0.151 ~ 0.179 – 0 0 0.67 < 1 25-25-23 0 6 4–5 6 1–3(4) 2+2(3) 2 169–185 52–72
A. ningshanensis 0.121 ~ 0.161 – 0 0 0.45 ~ 0.58 = 1 23-23-23(21) 0 6 4–5 5 1–2(3) 2+2(3)+3(4) 1–2 159–174 41–46
A. panzhihuaensis 0.246 28 1 0 0.67 – 23-23-19 1 6 4–5 6 1–3 2+2+3 1 160 73
A. pingbianensis 0.243 – 0 1 – = 1 23-23-23 0 7 5–6 6 1–3 2+2+3 1 164 56
A. rufescens 0.191 ~ 0.276 23 0 0 0.80 ~ 1.00 > 1 23-(23–25)-23 0 6 4–5 5 1–3 2(1)+2+3(4) 1–2 132–156 58–82
A. spinalis 0.150 ~ 0.250 16–20 0 0 – < 1 (23–25)-(23–25)-(23–25) 0 6 4–5 5–6 1–3 2+2(3) 1–2 138–175 48–67
A. timi 0.213 27 0 1 – > 1 25-25-23 0 6 4–5 6 1–3 2+2+3 1 170 72
A. tranganensis 0.254(+) 29 0 0 – > 1 25-23-23 0 6 4–5 6 1–3 2+2+3 2 171 73(+)
A. werneri 0.250 ~ 0.300 – 0 0 – = 1 ?-(21–23)-? 0 6 4–5 6 – 2+3(4) – 157–191 67–98
A. yangdatongi 0.180 ~ 0.262 24–26 0 0 0.57 > 1 23-23-23 0 6 4–5 5–6 1–3 2+2/3+2/3 2 155–171 59–76
A. yunkaiensis 0.156 ~ 0.203 20–24 0 0 0.49 ~ 0.64 = 1 23-23-23 0 6 4–5 6 1–3(4) 2+2+3(4) 2 150–162 49–56
A. vanhoensis 0.264 32 0 1 – > 1 25-23-23 0 6/7 4–5/5–6 6 1–4 2+2+3 2 176 84
A. zugorum 0.229 28 0 1 – > 1 25-23-23 0 6 4–5 7 1–3 2+2+3 2 173 70

Within the clade F, the two newly collected specimens from Hunan can be identified from A. ater by having nostril in the anterior part of the nasal (vs. nostril in the posterior part of the nasal), loreal length ~ 1.5 × than loreal height (vs. loreal length > 2 × than loreal height), and more subcaudals (69–72 vs. 47–70). They are different from A. juliani by having different dorsal scale rows (23-23-23 vs. 25-23-23), less maxillary teeth (23 vs. 28), and less subcaudals (69–72 vs. 77–91). They differ from A. yangdatongi by having relatively shorter tail length in males (0.221 ~ 0.225 vs. 0.261 ~ 0.262), more ventrals in males (163–165 vs. 155), and fewer subcaudals in males (69–72 vs. 76) fewer maxillary teeth (23 vs. 24–26). They also can be easily distinguished from its sister group A. ningshanensis by the following morphological characters: (1) the suture between the internasals 2 × as long as the suture between the prefrontals vs. the suture between the internasals subequal to the suture between the prefrontals; (2) relatively longer tail (TaL/TL: 0.221 ~ 0.225 vs. 0.121 ~ 0.161); (3) more subcaudals: 69–72 vs. 41–46; (4) two chin pairs vs. three chin pairs; (5) relatively narrow and long loreals (0.62 ~ 0.70 vs. 0.45 ~ 0.58) (more details are presented in Table 5).

Table 5.
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Main morphological characters of Achalinus hunanensis sp. nov. and A. ningshanensis.

Species Achalinus hunanensis sp. nov. A. ningshanensis
Sex Males (n = 2) Females (n = 5)
SVL 204–255 334–463
TaL 58–74 62–72
TL 262–329 398–527
TaL/TL 0.221 ~ 0.225 0.121 ~ 0.161
Loreal 1/1 1/1
LorH/LorL 0.62 ~ 0.70 0.45 ~ 0.58
LSBI/LSBP 2.00 ~ 2.02 0.95 ~ 1.11
LSBI vs. LSBP > 1 = 1
HL 6.33–7.91 11.17–13.72
HW 3.38–4.80 4.75–7.48
HL/HW 1.65–1.87 1.78–2.67
MT 23 —
SPL 3-2-1 3-2-1
IFL 5–6 5
Chins 2 3
IFL-1st Chin 3–4 2–3
SPO 1 1
TEM 2+2+4 2+2+3/2+2+4/2+3+4
aTEM-Eye 2 1–2
VEN 163–165 159–174
SC 69–72 41–46
Anal Entire Entire
DSR 23-23-23 23-23-23 (rarely 21)
References This study Yang et al. 2022

Combined the results of molecular systematics and morphological characters above, the specimens newly collected in this work represent a new species, and we describe it herein.

Taxonomic account

Achalinus hunanensis sp. nov.

https://zoobank.org/05012A7E-84CE-4C6D-A915-51FCF365DFFE
Figs 4, 5

Chresonymy

Achalinus ater: Shu et al. 2014; Shen et al. 2014; Gao et al. 2022.

Material examined

Holotype. CIB 119039 (Collection No. 20130505001), subadult male (Fig. 4), collected in early May 2013, by Sheng-Chao Shi and Sun-Jun Xiang from Huangyan Village, Hecheng District, Huaihua City, Hunan Province, China (27°28′N, 110°02′E; ca. 880 m a.s.l.).

Figure 4. 

The holotype (CIB 119039, subadult male) of Achalinus hunanensis sp. nov. A dorsolateral view B ventral view C right side of middle body view D dorsal head view E left side of head view F right side of head view G ventral head view. Photographs by SCS.

Paratype. CIB 119040, subadult male (Fig. 5), collected on 16 June 2022, by Sheng-Qiang Liu from Wazizhai, Ningxiang County, Changsha City, Hunan Province, China (28°00′N, 111°53′E; ca. 1020 m a.s.l.).

Figure 5. 

The paratype (CIB 119040, subadult male) of the Achalinus hunanensis sp. nov. A dorsolateral view B ventral view C dorsal head view D right side of head view E ventral head view. Photographs by SCS.

Etymology

This new species is named after its known distribution range, which is endemic to Hunan Province. The Chinese name is suggested as “湖南脊蛇” (Hú Nán Jǐ Shé) and the English name “Hunan Odd-scale Snake” or “Hunan Burrowing Snake” is suggested.

Diagnosis

(1) 23 rows of dorsal scales throughout the body, all dorsal scales strongly keeled, and the outmost one strongly keeled and enlarged; (2) tail relatively short, TaL/TL 0.221 ~ 0.225; (3) maxillary teeth 23; (4) the suture between internasals 2 × as long as that between prefrontals; (5) loreal one, subrectangular, LorH/LorL 0.62 ~ 0.70; (6) supralabials six, the 4th and 5th touch the eye; (7) the two anterior temporals in contact with eye; (8) ventrals 163–165, subcaudals 69–72, not paired.

Description of holotype

A subadult male with a total length of 329 mm (SVL 255 mm and TaL 74 mm); tail relatively short, Tal/TL 0.225; body slender, cylindrical; head length (HL) 7.91 mm, head width 4.80 mm, HL/HW 1.65, slightly distinct from neck; eye small, ED 1.42/1.41 mm; maxillary teeth 23, small, equally sized and curved. Rostral small, triangular, only the upper tip visible from above. Length of the suture between the internasals (LSBI 1.78 mm) ~ 2 × as long as length of the suture between the prefrontals (LSBP 0.88 mm). Nostril in the anterior part of the nasal. Loreal one, subrectangular, loreal height (LorH) 1.03/1.04 mm, loreal length (LorL) 0.70/0.66 mm, LorH/LorL 0.62 ~ 0.70. Supraocular one. Frontal one, pentagonal, pointed backwards, much shorter than the parietals. Parietals paired and elongated. No preoculars and postoculars. Temporals 2+2+4, the anterior two contact the eye, the lower anterior temporal much larger, the upper medium temporal much larger, the upper posterior temporal much larger and separated from the other side one by two small scales which contact the parietals. Supralabials 6, 4th and 5th contact the eye, the last one much elongated. One mental. Two chin shields, similar length. Infralabials 5/6, the first one contact with each other after the mental and before the 1st chin shields, 1st–3rd/1st–4th touch the 1st chin shields.

Dorsal scales lanceolate and strongly keeled; 23 rows throughout the body; those of the outmost rows on both sides significantly enlarged and strongly keeled. Ventrals 163, with two preventrals; anal entire; subcaudals 69, not paired.

Coloration of holotype

In life, dorsum dark, slightly metallic, vent black-brown, dark brown near the margin, grey in the margin. A yellowish brown patch on the head occipital. The head ventral anterior part dark brown and posterior part yellowish white (Shu et al. 2014). In preservation, dorsum brown, vent anterior part grey and posterior part light brown. Ventral side of tail brown. The head ventral anterior part brown and posterior part grey.

Variations

Main morphological characters were listed in Table 3. The other sample are very similar to the holotype except that: (1) more ventrals: CIB 119040: 165; (2) more subcaudals: CIB 119040: 72; (3) vent coloration: CIB 119040: dark brown throughout the vent.

Distribution and habits

Achalinus hunanensis sp. nov. is currently only known from Hunan Province, China: Hecheng District, Huaihua City and Ningxiang County, Changsha City (880–1020 m a.s.l.). The holotype was found at night, near a mountain stream (AT 24 °C, RH 80%) with shrubs under subtropical evergreen broadleaves forest. It was moving from leaf litter to the stream. Earthworms were found at the same place, which we speculated as its prey (Shu et al. 2014).

Discussion

Based on molecular evidence, the newly collected Achalinus specimens in this study are most closely to A. ningshanensis but a genetic differentiation (p-distance 3.2%) already exists between these two groups (Fig. 2, Table 2). The newly collected Achalinus specimens and its sister group A. ningshanensis have separate distribution ranges at south of Yangtze River and north of Yangtze River, respectively, isolated by Three Gorges (Fig. 1). In addition, their estimated divergence time was at 0.48 Mya (Fig. 3), which broadly coincides with the formation of Three Gorges of the Yangtze River (0.30 ~ 0.12 Mya) (Zhang et al. 2018), hindering their communication and driving allopatric speciation. Moreover, combining their distinct morphological differences (Table 5), we describe them as a new species. Currently, 24 Achalinus species are reported.

Achalinus ater was first recorded in Hunan Province only based one specimen (Shen et al. 2014; Shu et al. 2014; Gao et al. 2022). However, this study found that this record was a misidentification and this specimen was designed as the new species holotype. Therefore, A. ater recorded on Hunan reptile check list should be transferred as A. hunanensis.

Due to the secretive life history and morphological similarities, many cryptic species may be “hidden” within known widely distributed species, such as A. spinalis, A. rufescens, and A. ater (Wang et al. 2019; Yang et al. 2022), and the description of A. hunanensis sp. nov. indicated that further study is necessary to conduct by using different Achalinus species and geographic populations to revise the mystery snakes and reveal their evolutionary history.

Acknowledgements

The study was supported by the National Key Programme of Research and Development, Ministry of Science and Technology (2022YFF1301401). We thank the support of CIB Herpetological Museum, and sincerely express our thanks to Mr. Sheng-Qiang Liu for his kind and careful work in the field survey. We also thank Qi-Heng Chen for his help in molecular phylogenetic analyses.

Additional information

Conflict of interest

No conflict of interest was declared.

Ethical statement

No ethical statement was reported.

Funding

National Key Programme of Research and Development, Ministry of Science and Technology (2022YFF1301401).

Author contributions

Shun Ma: Laboratory work, methodology, data analysis, validation, writing: orgination and draft, writing: review and editing; Sheng-Chao Shi: methodology, investigation and resources, writing: orgination and draft, writing: review and editing; Sun-Jun Xiang: investigation and resources, writing: review and editing; Fu Shu: investigation and resources, writing: review and editing; Jian-Ping Jiang: conceptualization, data curation, project administrition, resources, supervision, writing: review and editing.

Author ORCIDs

Shun Ma https://orcid.org/0009-0003-8611-4550

Sheng-Chao Shi https://orcid.org/0000-0003-2337-6572

Sun-Jun Xiang https://orcid.org/0009-0003-6692-7087

Fu Shu https://orcid.org/0000-0002-6082-8112

Jian-Ping Jiang https://orcid.org/0000-0002-1051-7797

Data availability

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

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Appendix 1

Examined Achalinus specimens

A. ater (n = 1): China, Guizhou Province, Xingyi County: CIB 63III5243.

A. rufescens (n = 1): China, Hong Kong: CIB 119042.

A. yunkaiensis (n = 1): China, Hunan Province, Xinning County: CIB 119041.

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