Skip to main content
NCBI home page
Animals : an Open Access Journal from MDPI logoLink to Animals : an Open Access Journal from MDPI
. 2023 Feb 17;13(4):708. doi: 10.3390/ani13040708

A New Species of the Genus Achalinus (Squamata: Xenodermidae) from the Dabie Mountains, Anhui, China

Caiwen Zhang 1, Kai Liu 1,†, Ruyi Huang 2,†, Tingli Hu 1, Lei Yu 1, Ruolei Sun 1, Yucai Zhang 3, Jing Wen 4, Baowei Zhang 1,*
Editor: Franco Andreone
PMCID: PMC9952718  PMID: 36830495

Abstract

Simple Summary

A new species of odd-scaled snake in the genus Achalinus is described from Dabie Mountains Luan City, Anhui Province, China, based on one male and two female specimens. Bayesian inference and maximum likelihood analyses based on a mitochondrial DNA fragment (CO1) indicated the new taxon is different from its congeners (p–distance ≥ 9.4%). Morphologically, the new species can be diagnosed from the other species by a combination of 12 characters. The recognition of the new species brings the number of described Achalinus species to 22.

Abstract

A new species of Xenodermid snake, Achalinus dabieshanensis sp. nov., was described based on three specimens (two female and one male) collected from the Dabie Mountains of western Anhui Province. It can be distinguished from known congeners by a significant genetic divergence in the mitochondrial gene fragment COI (p-distance ≥ 9.4%) and the following combination of characteristics: (1) length of the suture between the internasals being distinctly shorter than between the prefrontals; (2) a single loreal; (3) dorsal scales strongly keeled, in 23 rows throughout the body; (4) two pairs of prefrontals; (5) six supralabials; (6) five infralabials; (7) temporals 2 + 2 + 3 (or 2 + 2 + 4); (8) 141–155 ventrals; (9) 45–55 subcaudals, unpaired; (10) anal entire; (11) weakly iridescent tinged, uniform, brown to black dorsum with vertebral scales and about three adjacent dorsal scales dark brown forming a longitudinal vertebral line from posterior margin of parietals to tail tip; (12) light brown venter, ventral shields wide, visible on both sides, light brown flanks, giving the appearance of a black subcaudal streak. The recognition of the new species increases the number of described Achalinus species to 22.

Keywords: Achalinus dabieshanensis sp. nov., morphology, phylogenetics, taxonomy

1. Introduction

The odd-scaled snakes (also known as burrowing snakes) of the genus Achalinus Peters, 1869 belong to the family Xenodermidae and currently include 21 species: A. spinalis (Peters, 1869), A. rufescens (Boulenger, 1888), A. formosanus (Boulenger, 1908), A. werneri (Van Denburgh, 1912), A. niger (Maki, 1931), A. ater (Bourret, 1937), A. meiguensis (Hu and Zhao, 1966), A. hainanus (Huang, 1975), A. jinggangensis (Zong and Ma, 1983), A. juliani (Ziegler et al., 2019), A. emilyae (Ziegler et al., 2019), A. timi A. timi (Ziegler et al., 2019), A. yunkaiensis (Wang et al., 2019), A. pingbianensis (Li et al., 2020), A. tranganensis (Luu et al., 2020), A. zugorum (Miller et al., 2020), A. panzhihuaensis (Hou et al., 2021), A. yangdatongi (Hou et al., 2021), A. dehuaensis (Hou et al., 2021) and A. ningshanensis (Yang et al. 2022) [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17]. Morphologically, all species of the genus Achalinus have conservative morphological characters, including a slender, cylindrical body, a head that is slightly distinct from the neck, small eyes, and an entire anal [18,19]. Although most of their morphological characteristics overlap between species [20], some significant differences in color patterns and squam characteristics have been recognized. The presence of a longitudinal vertebral line from the posterior margin of the parietal to the tail tip, the numbers of infralabials and supralabials, and the lengths of the sutures between the internasals and the prefrontals differ. Recent phylogenetic studies have also supported the species divisions within the genus Achalinus [21,22]. The genus Achalinus is widely distributed in eastern and southeastern Asia, ranging from northern Vietnam to southwestern China, and partly into Japan. Presently, 16 species occur in China, of which ten are endemic to the country [14,15,17].

During recent herpetological surveys of the Dabie Mountains, we collected three odd-scaled snake specimens that differed from all other species of known snakes in their morphology and color pattern characteristics. According to the diagnostic characteristics of the genus Achalinus, as indicated by Smith and Zhao et al. [18,19], the specimens could be assigned to this genus. Further morphological examinations and molecular analyses showed that these specimens represent a separate evolutionary lineage that can be distinguished from all recognized species. Herein, we describe these specimens as a new species of the genus Achalinus.

2. Materials and Methods

2.1. Sampling

We obtained three odd-scaled snake samples from the Yaoluoping Nature Reserve and Fuziling Provincial Reserve in the Dabie Mountains, Anhui Province, China. The specimens were collected in the field and fixed in 75% ethanol. Liver tissue samples were separately transferred to 95% ethanol. The specimens have been deposited in the Biological Museum of Anhui University, Anhui, China. Permission for the field surveys in the Dabie Mountains was granted by the Huoshan Forestry Bureau (No. HFB20180801) and Management Office of the Yaoluoping National Reserve (No. YNR 20190503).

2.2. DNA Sequencing

Tissue samples from three individuals of the new specimens were used for the phylogenetic analyses. DNA was extracted from the liver samples using phenol/chloroform extraction [23]. The partial mitochondrial gene fragment of the cytochrome c oxidase 1 gene (COI) was amplified using the primer pair RepCOIF (5′-TNT TMT CAA I ACC ACA AAG A-3′) and RepCOIR (5′-ACT TCT GGR TGK CCA AAR AAT CA-3′) [24]. Experimental primer pairs were synthesized and provided by General Biosystems (Anhui) Co., Ltd. (Chuzhou, China). The PCR conditions followed those described by Nagy et al. (2012) [24]. The PCR products were sequenced by General Biosystems (Anhui) Co., Ltd. The sequences were edited and assembled using SeqMan (DNASTAR, Lasergene v7.1) and then aligned using Clustal X 1.8 [25] in MEGA6 [26]. Sequences with insertions or deletions (indels) were sequenced at least twice with both the forward and reverse primers to confirm the variations. All sequences were deposited in GenBank (Table 1).

Table 1.

Samples used for molecular phylogenetic analysis in this study.

ID Species Specimen Voucher Locality GenBank Number
1 Achalinus dabieshanensis sp. nov. AHU2016EE0615 Yaoluoping Nature Reserve, Anhui, China MW316597
2 Achalinus dabieshanensis sp. nov. AHU2018EE0710 Fuziling Provincial Reserve, Anhui, China MW316598
3 Achalinus dabieshanensis sp. nov. AHU2019EE0813 Yaoluoping Nature Reserve, Anhui, China MW316596
4 Achalinus ater SYS r000852 Anjiangping, Guangxi, China MK064760
5 Achalinus dehuaensis YBU 13013 Dehua, Fujian, China MZ442642
6 Achalinus emilyae IEBR 4465 Hoanh Bo District, Quang Ninh, Vietnam MK330857
7 Achalinus formosanus RN 2004 Taiwan Province, China KU529454
8 Achalinus huangjietangi HSR18030 Huangjialing Village, Anhui, China MT380191
9 Achalinus juliani IEBR A.2018.9 Ha Lang District, Cao Bang, Vietnam MK330855
10 Achalinus meiguensis GP836 Mianyang, Sichuan, China MT365518
11 Achalinus niger RN 1159 Taiwan Province, China KU529435
12 Achalinus ningshanensis HSR19232 Ningshan County, Shaanxi Province, China ON548423
13 Achalinus panzhihuaensis KIZ 040189 Hongbao, Yanbian, Sichuan, China MW664862
14 Achalinus pingbianensis YBU 18273 Honghe, Yunnan, China MT365521
15 Achalinus rufescens SYS r001527 Heishiding, Guangdong, China MK064864
16 Achalinus spinalis SYS r001327 Mt. Badagong, Hunan, China MN380340
17 Achalinus timi IEBR A.2018.10 Thuan Chau District, Son La, Vietnam MK330856
18 Achalinus tranganensis VNUF R.2018.21 Ninh Binh Province, Vietnam MW023086
19 Achalinus yangdatongi KIZ 034327 Wenshan Nature Reserve, Yunnan, China MW664865
20 Achalinus yunkaiensis SYS r001443 Guangdong, China MN380329
21 Achalinus zugorum IEBR 4698 Ha Giang Province, Vietnam MT502775
Out group
22 Fimbrios klossi IEBR A.2013.56 Gia La, Vietnam KP410745
23 Parafimbrios lao MNHN 2013.1002 Louangphabang, Laos KP410746
24 Parafimbrios vietnamensis IEBR A.2018.7 Lai Chau, Vietnam MH884515
Open in a new tab

2.3. Phylogenetic Analyses

To explore the phylogenetic position of the samples in the genus Achalinus, COI sequences from 21 snakes, including three outgroups, Fimbrios klossi, Parafimbrios lao, and P. vietnamensis, were retrieved from GenBank for our analyses (Accession number listed in Table 1) [16,17]. The nucleotide substitution models were tested in MrModeltest 2.3 using Akaike information criteria [27], and the GTR + G + I model was found to be the best fit. Bayesian analyses were conducted using MrBayes 3.2.4 [28]. Three independent runs with four Markov Chain Monte Carlo were performed based on the models selected, starting from a random tree; each run consisted of a total of 3 × 106 generations, sampled every 2000 generations. The first 25% of the samples were discarded as burn-in. The remaining trees were used to construct a 50% majority rule consensus tree. The results were analyzed in Tracer v1.7 to assess convergence and ensure effective sample sizes (≥200) for all parameters [29]. Maximum likelihood analyses were executed using IQ-TREE 2 (Minh et al., 2020), and the support of the tree was by bootstrap resampling with 1000 nonparametric bootstrap replicates. Phylogenetic trees were visualized and edited using FigTree v1.4.2 [30]. We also calculated the uncorrected pairwise genetic distances (p-distance) using MEGA 6 [25].

2.4. Morphometric Measurements

Morphometric measurements to the nearest 0.1 mm were taken using dial calipers, following Zhao et al. (1998) [19]. The abbreviations of morphological characteristics used in the text are as follows: total length (TL, from snout tip to tail end); snout-vent length (SVL, from cusp of snout to anterior margin of cloacae opening); tail length (TaL, from posterior margin of cloacae opening to tip of tail); head length (HL, from snout tip to posterior margin of mandible); head width (HW, at the widest part of the head); head height (HH, at the highest part of the head); length of loreal (LeL, at the longest part of the loreal); height of loreal (HiL, at the highest part of the loreal); length of anterior section of nasal (LaSN); length of posterior section of nasal (LpSN); length of suture between prefrontals (LSBP); length of suture between internasals (LSBI); preoculars (PrO); postoculars (PtO); supraoculars (SpO); supralabials (SPL); infralabials (IFL); anterior temporals (aTMP); middle temporals (mTMP); posterior temporals (pTMP); ventral scales (V); and subcaudals (SC). Dorsal scale rows (DSR) were counted at two head lengths behind the head, mid-body, and two head lengths before the vent. Bilateral scale counts are given as left/right. Sex identification was performed by inspecting the presence or absence of hemipenes. In this study, while comparing the undescribed species with A. rufescens, the most widespread species, we used its latest description of A. rufescens rather than descriptions in the early literature, because it was very likely that multiple cryptic species will be involved in them [10]. In the morphometric analysis, we focused on the species that clustered most closely with the new specimen in the phylogenetic trees. Morphological data for the Achalinus species were obtained from the relevant literature sources [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17].

The electronic version of this articIe in Portable Document Format (PDF) will represent 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. 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 prefix http://zoobank.org/ (accessed on 22 October 2022). The LSID for this publication is urn:lsid:zoobank.org:pub: 1E1842EA-CB20-46FA-AA0D-3D35017814D4.

3. Results

3.1. Phylogenetic Relationship

The alignment contained 657 nucleotide base pairs (bp) sequences. The Bayesian inference (BI) and Maximum likelihood (ML) phylogenetic results (Figure 1) were largely concordant concerning the relationships among species within the major clades of Achalinus. The Achalinus lineages formed a monophyletic group with high support values (BI, PP = 1.00; ML, BS = 100%). These three specimens from the Dabie mountain were nested within the Achalinus genus and the independence of our collections and their affinity to A. huangjietangi were also strongly supported (BI, PP = 1.00; ML, BS = 82%). In addition, these new samples have distinct branch lengths compared with the adjacent clade of A. huangjietangi (HSR18030 collection number).

Figure 1.

Figure 1

Open in a new tab

Maximum likelihood (ML) tree of the genus Achalinus reconstructed based on DNA sequences of segments of the COI genes. ML bootstrap support/Bayesian posterior probability is denoted beside each node, and the symbol “-” indicates values below 50%. Sample information is provided in Table 1.

The uncorrected p-distance among all species within the genus Achalinus ranged from 6.1% to 21.7% (Table 2). The maximum genetic distance was found between the new species and A. formosanus (21.7%), and the minimum one was found between the new species and A. huangjietangi (9.4%) (Table 2). The genetic distance between the new samples and A. huangjietangi (9.4%) is greater than the lowest three ones: (7.5% between A. ater and A. juliani, 6.5% between A. yangdatongi and A. juliani, and 6.1% between A. ningshanensis and A. yangdatongi).

Table 2.

Uncorrected p-distances among the Achalinus species based on partial mitochondria COI gene.

ID Species 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
1 A. dabieshanensis sp. nov.
2 A. huangjietangi 0.094
3 A. juliani 0.185 0.169
4 A. ater 0.174 0.171 0.068
5 A. yangdatongi 0.191 0.165 0.075 0.065
6 A. rufescens 0.185 0.172 0.129 0.140 0.127
7 A. emilyae 0.209 0.168 0.159 0.132 0.147 0.112
8 A. spinalis 0.186 0.150 0.161 0.172 0.160 0.141 0.173
9 A. yunkaiensis 0.168 0.138 0.149 0.142 0.132 0.154 0.147 0.134
10 A. formosanus 0.217 0.179 0.144 0.161 0.163 0.163 0.158 0.160 0.139
11 A. niger 0.196 0.156 0.130 0.131 0.147 0.145 0.149 0.143 0.134 0.080
12 A. pingbianensis 0.173 0.144 0.133 0.127 0.124 0.143 0.154 0.148 0.125 0.164 0.139
13 A. zugorum 0.171 0.162 0.154 0.154 0.136 0.160 0.149 0.152 0.123 0.151 0.151 0.117
14 A. timi 0.186 0.168 0.167 0.149 0.146 0.168 0.142 0.161 0.157 0.151 0.134 0.131 0.152
15 A. tranganensis 0.175 0.149 0.156 0.146 0.143 0.139 0.143 0.170 0.153 0.196 0.164 0.148 0.134 0.160
16 A. meiguensis 0.196 0.173 0.187 0.167 0.194 0.208 0.175 0.175 0.170 0.173 0.149 0.191 0.162 0.174 0.174
17 A. panzhihuaensis 0.191 0.173 0.183 0.187 0.178 0.180 0.197 0.182 0.178 0.186 0.173 0.170 0.174 0.177 0.187 0.123
18 A. ningshanensis 0.211 0.199 0.096 0.080 0.061 0.137 0.159 0.176 0.154 0.168 0.147 0.128 0.144 0.151 0.173 0.195 0.204
19 A. dehuaensis 0.211 0.189 0.165 0.191 0.158 0.144 0.178 0.162 0.168 0.187 0.175 0.168 0.164 0.176 0.152 0.201 0.174 0.189
Open in a new tab

Given that these specimens possess obvious monophyletic structures in the molecular phylogenetic tree, adding the significant molecular distance, unique geographical distribution, and prominent morphological differences from congenetic species, they are described as a new species below.

3.2. Taxonomic Account

Achalinus dabieshanensis sp. nov. Zhang, Liu, Huang and Zhang (Figure 2 and Figure 3A–F; and Table 3).

Figure 2.

Figure 2

Open in a new tab

General view of the holotype of Achalinus dabieshanensis sp. nov. in life (Photography by Kai Zhao).

Figure 3.

Figure 3

Open in a new tab

The general aspect of the adult female holotype (AHU 2018-EE-0710) and the adult male paratype (AHU 2016-EE-0615) of Achalinus dabieshanensis sp. nov. (A–D) the holotype left and right and dorsal and ventral view of head (showing length of the suture between internasals shorter than it between prefrontals, a single loreal, six supralabials, five infralabials and temporals 2 + 2 + 3); (E–H) the paratype left and right and dorsal and ventral view of head; (I) Overall view of the preserved holotype; (J) the holotype dorsal view of midbody (showing dorsum iridescent brown with three scales wide dorsal black line). Photos by Lihua Huang and Caiwen Zhang.

Table 3.

Measurements, scale counts, body proportions, and squamae characters of the sample of Achalinus dabieshanensis sp. nov.

Voucher AHU 2016-EE-0615 AHU 2018-EE-0710 AHU 2019-EE-0813
Sex male female Male
TL 376 316 266
SVL 287 263 217
TaL 84 53 47
TaL/TL 22.3% 16.8% 17.7%
HW 5.6 5.3 4.8
HL 11.2 9.5 8.7
HH 4.5 3.5 3.1
HW/HL 0.5 0.6 0.6
SPL 6 6 6
SPL–Lorea 3rd–4th 3rd–4th 3rd–4th
IFL 5 5 5
Loreal 1 1 1
HiL 1.1 1.0 0.9
LeL 1.5 1.2 1.1
HiL/LeL 0.7 0.8 0.8
LSBP 1.2 0.8 0.9
LSBI 1.8 1.2 1.1
LSBP/LSBI 0.7 0.7 0.8
LaSN 0.3 0.3 0.3
LpSN 0.8 0.7 0.5
LaSN/LpSN 0.4 0.4 0.6
SpO 1 1 1
TMP 2 + 2 + 4/2 + 2 + 4 2 + 2 + 3/2 + 2 + 3 2 + 2 + 4/2 + 2 + 4
Elogate aTMP 2nd 2nd 2nd
Elogate mTMP 1st 1st 1st
Elogate pTMP 1st 1st 1st
DSR 23 + 23 + 23 23 + 23 + 23 23 + 23 + 23
V 141 155 151
SC 55 45 46
Open in a new tab

Holotype: AHU 2018-EE-0710 (Figure 2 and Figure 3A–F), an adult female, collected by Tingli Hu, Zhen Xu, Ruolei Sun, and Guotao Chen on 10 July 2018 from Fuziling Provincial Reserve in the Dabie Mountains (30°57′47.88″ N, 116°04′37.20″ E; 1361 m a.s.l.), Huoshan County, Luan City, Anhui Province, China.

Paratypes: AHU 2016-EE-0615 (Figure 3A–D), an adult male, collected by Lei Yu and Tao Pan on 15 June 2016 from the Yaoluoping Nature Reserve in the Dabie Mountains (30°59′05.99″ N, 116°04′45.20″ E; 1051 m a.s.l.), Yuexi County, Anqing City, Anhui Province, China. AHU 2019-EE-0813, a female collected by Caiwen Zhang and Haohao Ma on13 August 2019 from the same locality as the holotype (31°11′6.72″ N, 116°04′38.28″ E; 635 m a.s.l).

3.3. Diagnosis

A new species of Achalinus with: (1) weakly iridescent tinged, uniform brown dorsum with vertebral scales and about three adjacent dorsal scales dark brown, forming longitudinal vertebral line from posterior margin of parietals to tail tip; (2) light brown venter; (3) relatively short tail, TaL/TL ratio 16.8–22.3%; (4) suture length between internasals distinctly shorter than between prefrontals; (5) one loreal (height/length ratio 0.79–0.89); (6) six supralabials, 4th and 5th widely in contact with eye; (7) temporals 2 + 2 + 3 (or 2 + 2 + 4), two elongated anterior temporals in contact with eye; (8) five infralabials, two pairs of chin shields, first three infralabials touching first pair of chin shields; (9) 141–155 ventrals, 45–55 subcaudals, not paired; (10) dorsal scales in 23 rows throughout, strongly keeled, but outermost rows on both sides smooth and significantly enlarged; (11) anal entire.

3.4. Comparisons

Achalinus dabieshanensis sp. nov. differs from all other species of Achalinus, except A. formosanus, A. huangjietangi, A. niger, and A. spinalis by having internasal suture lengths distinctly shorter than the lengths of the suture between the prefrontals (vs. other species of Achalinus, length of suture between the internasals distinctly longer than or equal to that between the prefrontals). In addition, it differs from all other species of Achalinus, except A. dehuaensis, A. emilyae, A. hainanus, A. huangjietangi, A. rufescens, A. meiguensis, and A. ningshanensis, by having five infralabials (other species of Achalinus have six or seven). Thus, these characteristics are not repeated in the detailed comparisons that follow. At first glance, the color pattern and dorsal scale-row formula of A. dabieshanensis sp. nov. are most similar to those of A. huangjietangi, A. rufescens, and A. yunkaiensis. However, Achalinus dabieshanensis sp. nov. can be easily distinguished from A. huangjietangi by having fewer ventral scales (141–155 vs. 157–170 in A. huangjietangi) and the absence of a dark streak in the middle of caudal ventral (Figure 4). The new species can be distinguished from A. rufescens by two anterior pairs of chin shields (vs. three pairs of chin shields in A. rufescens) and two anterior temporals in contact with the eye (vs. only the upper anterior temporal in contact with the eye in A. rufescens), from A. yunkaiensis by having fewer ventral scales (45–55 vs. 56–59 in A. yunkaiensis) and the obvious three-scale-wide mid-dorsal dark longitudinal line.

Figure 4.

Figure 4

Open in a new tab

Ventral of the adult female holotype (AHU 2018-EE-0710). (A) ventral; (B) close-up of caudal ventral (showing absence of a dark streak in the middle of caudal ventral).

Achalinus dabieshanensis sp. nov. can be differentiated from A. ater by having fewer ventral scales (141–155 vs. 160–170); from A. dehuaensis by having two anterior temporals (vs. only one), fewer subcaudals (45–55 vs. 63–81); from A. emilyae by having fewer subcaudals (45–55 vs. 60–65) and fewer ventral scales (141–155 vs. 157–166); from A. formosanus by having fewer DSR (23//23//23 vs. 27–29//25–27//25), fewer subcaudals (45–55 vs. 61–83), and fewer ventral scales (141–155 vs. 158–169); from A. hainanus by having two anterior temporals (vs. only one), fewer subcaudals (45–55 vs. 67–69), fewer ventral scales (141–155 vs. 165–168), and a relatively short tail (TaL/TL 16.8–22.3% vs. 26–27%); from A. jinggangensis by having the loreal not being fused with the prefrontal (vs. loreal fused with the prefrontal) and fewer ventral scales (141–155 vs. 156–164); from A. juliani by having fewer subcaudals (45–55 vs. 77–91) and fewer ventral scales (141–155 vs. 163–179); from A. meiguensis by having internasals (vs. lacking internasals), lacking postocular (vs. having postocular), and more DSR both anteriorly and posteriorly (23 vs. 21 or 23 and 23 vs. 19, respectively); from A. niger by having fewer ventral scales (141–155 vs. 169–185), fewer DSR anteriorly (23 vs. 25), and fewer middle temporals (23 vs. 25); from A. ningshanensis by having a relatively long tail (TaL/TL 16.8–22.3% vs. 12–16%) and fewer ventral scales (141–155 vs. 171); from A. pangzhihuaensi by having internasals (vs. lacking internasals), lacking postocular (vs. having postocular), and more DSR posteriorly (23 vs. 19), fewer ventral scales (141–155 vs. 160), a relatively short tail (TaL/TL 16.8–22.3% vs. 24.6%), and fewer subcaudals (45–55 vs. 73); from A. pingbianensis by having fewer supralabials (six vs. seven), fewer subcaudals (45–55 vs. 56), and fewer ventral scales (141–155 vs. 160); from A. spinalis by having two anterior temporals in contact with eye (vs. upper anterior anterior broadly in contact with eye) and fewer infralabials (five vs. six); from A. tranganensis by having fewer DSR anteriorly (23 vs. 25), a relatively short tail (TaL/TL 16.8–22.3% vs. 25%), fewer subcaudals (45–55 vs. 73+), and fewer ventral scales (141–155 vs. 171); from A. werner by having a relatively short tail (TaL/TL 16.8–22.3% vs. 25%), fewer subcaudals (45–55 vs. 67–98), and fewer ventral scales (141–155 vs. 157–191); from A. yangdatongi by having more DSR posteriorly (23 vs. 19), fewer vetral scales (141–155 vs. 161), a relatively short tail (TaL/TL 16.8–22.3% vs. 26.2%), and fewer subcaudals (45–55 vs. 82); and from A. zugorum by having fewer infralabials (five vs. seven), fewer DSR anteriorly (23 vs. 25), fewer subcaudals (45–55 vs. 70), and fewer ventral scales (141–155 vs. 173). Comparisons between the new species and its congeners are summarized in Table 4.

Table 4.

Comparisons of main morphological characters among Achalinu dabieshanensis sp. nov. species.

Species TL Max. SVL Max. TaL Max. TaL/TL Int. Fus. SPL TMP Loreal IFL aTMP [Eye Contact] LSBI vs. LSBP Ant DSR Mid DSR Post DSR V Post DSR
Achalinus dabieshanensis sp. nov 376 287 84 16.8–22.3% no 6 2 + 2 + 3 (4) 1 5 2 < 23 23 23 141–155 45–55
A. ater 401 - 70 19–22% no 6 2 + 2 1 6 2 > 23 (21) 23 (21) 23 (21) 160–170 47–70
A. dehuaensis 343 253 90 21–29% no 6 2 + 2 (3) + 3 (4) 1 5 (6) 1 > 23 23 23 142–153 63–81
A.emilyae 519.5 424.4 95.1 18–20.3% no 6 2 + 2 1 5 2 (1) > 23 23 23 157–166 60–65
A. formosanus 853 717 136 16% no 6 2 + 2 0 6–7 2 (1 or 2) < 27 (29) 25–27 25 158–169 61–83
A. hainanus 310 - 80 26–27% no 6 1 + 2 + 3 1 5 1 ≥ 23 23 23 165–168 67–69
A. huangjietangi 404 340 64 15–23% no 6 2 + 2 + 3 1 5–6 2 < 23 23 23 157–170 47–67
A. spinalis 600 345 83 15–25% no 6–7 2 + 2 (3) 1 6 1 ≤ 23 (25) 23 (25) 23 (25) 138–175 39–69
A. timi 177.9 140 37.9 21% no 6 2 + 2 0 6 2 (1) > 25 25 25 170 72
A. tranganensis 448 334 114 25% no 6 2 + 3 1 6 2 > 25 23 23 171 73+
A. werner 550 - - 25–30% no 6 2 + ? 1 6 2 = 23 (21) 23 (21) 23 (21) 157–191 67–98
A. yangdatongi 397 293 104 26.20% no 6 2 + 2 + 3 1 6 2 > 23 23 19 161 82
A. yunkaiensis 448.1 386.3 63.3 18.5–20.0% no 6 2 + 2 + 3 (4) 1 6 2 > 23 23 23 151–162 56–79
A. zugorum 458 353 105 23% no 6 2 + 2 0 7 2 > 25 23 23 173 70
A. jinggangensis 460 - 80 17–22% no 6 2 (1) + 2 + 3 (4) 0 6 2 (1) > 23 23 23 156–164 51–64
A. juliani 413 304 109 22–37% no 6(7) 2 + 2 1 6 2 (2) > 25 23 23 173–179 77–91
A. meiguensis 555 - 81 15–25% yes 6 2 (3) + 2 (3) 1 6(5) 2 (3) no suture 21 (23) 19–21 (23) 19 146–173 39–60
A. niger 730 - 110 15–18% no 6 2 + 2 1 6 2 ≤ 25 25 23 169–185 52–72
A. ningshanensis 527 463 72 12–16% no 6 2 + 2 + 3 (4) 1 5 2 = 23 23 23 (21) 159–174 41–46
A. panzhihuaensis 257 194 63 24.60% Yes 6 2 + 2 1 6 2 no suture 23 23 19 160 73
A. pingbianensis 429 345 84 24% no 7 2 + 2 (+3) 0 7 2 (1) = 23 23 23 160 56
A. rufescens 450 210 80 17–28% no 6 2 + 2 (3) 1 5 1 > 23 23–25 23 138–165 48–75
Open in a new tab

Note: Values given in brackets indicate infrequent conditions, TL max. = maximum total length, SVL max. = maximum snout-vent length, TaL max. = maximum tail length, Int. fus.: internasal fused to prefrontal, SPL = supralabials, IFL = infralabials, aTMP [eye contact] = anterior temporals contact eye, LSBI vs. LSBP = length of suture between internasals vs. length of suture between the prefrontals, DSR = dorsal scale rows, V = ventral scales, SC = subcaudals.

3.5. Description of Holotype

Adult female with total length 316 mm (SVL 263 mm, TaL 53 mm); tail relatively short, TaL/TL ratio 16.8%; body slender, cylindrical; HL 9.5 mm, HW 7.2 mm, HH 3.5 mm; head indistinct from neck; eye small with the vertically elliptical pupil; rostral small, triangular, scarcely visible from above; HL/RW ratio 0.7; internasal suture (0.7 mm) about half length of prefrontal suture (1.2 mm).

Nostril in anterior part of nasal, posterior margin of nostril with distinct nostril cleft, posterior section of nasal vertically rectangular, posterior section nearly half as long as anterior section, LaSN/LpSN 0.4; single pentagonal frontal, nearly straight anteriorly, slightly broader than long, pointed backwards, much shorter than parietals; single loreal, HiL/LeL ratio 0.8, extending from nasal to eye; single supraocular, elongated, twice as wide as high; two anterior temporals, elongated, upper one smaller, widely in contact with eye, lower one narrowly in contact with eye; two elongated middle temporals, upper one much larger, lower one in contact with 6th supralabial, not in contact with elongated anterior temporals on left, only tip in contact with anterior temporals on right; three elongated posterior temporals, uppermost one significantly enlarged (super-temporal), surrounding the parietal; each parietal bordered by elongated nuchal; nuchals separated from each other behind super-temporals by one small intertemporal nuchal scale; 2nd nuchal about twice size of 1st; six supralabials, 1st smallest, 4th and 5th widely in contact with eye, 6th longest and largest; 3rd and 4th in broad contact with loreal; one mental, followed by five infralabials with first pair in contact with each other; two pairs anterior and posterior chin shields in contact with 3rd infralabial; posterior pair of chin shields smaller, length of suture between 1st pair twice that between 2nd pair; dorsal scales lanceolate and feebly keeled; dorsal scales in 23 rows throughout body, outermost rows on both sides smooth and significantly enlarged; 155 ventrals, distinctly rounded laterally; 45 subcaudals, not paired; anal entire.

The coloration of the holotype in life Dorsal surface is uniform iridescent brown, with a longitudinal dark brown vertebral line, a width of about 3 DSR, from posterior margin of parietals to tail tip, ventrals light brown; margins of all scales grayish white; coloration of supralabials and temporal regions much lighter; iris dark brown, pupil black.

3.6. Intraspecific Morphological Variations

The measurements, scale counts, body proportions, and squamae details are listed in Table 3. All paratypes are morphologically very similar to the holotype except that: (1) The adult male (AHU 2016-EE-0615) possessed a significantly larger body size, TL 376.2 mm, TaL 84 mm, TaL/TL radio 22.3% (vs. TL 316 mm, TaL 53 mm, TaL/TL radio 16.8 % in female holotype; TL 226 mm, TaL 47 mm, TaL/TL radio 17.7% in female paratype); (2) the adult male (AHU 2016-EE-0615) and second female (AHU 2019-EE-0813) had TMP 2 + 2 + 4/2 + 2 + 4 (vs. TMP 2 + 2 + 3/2 + 2 + 3 in holotype); and (3) the LSBI/LSBP radio was 0.8 in AHU 2019-EE-0813 (vs. an LSBI/LSBP ratio of 0.7 in the holotype and paratype AHU 2019-EE-0615).

3.7. Etymology

The specific epithet, Achalinus dabieshanensis sp. nov., refers to the distribution of the new species in the Dabie Mountains in Anhui, China. We suggest the English name would be the “Dabie Mountains Odd-scaled Snake” or “Dabie Mountain Burrowing Snake” and the Chinese name “大别山脊蛇 (Dà Bié Shān Jǐ Shé)”.

3.8. Distribution and Habitat

Currently, Achalinus dabieshanensis sp. nov. is only known from its type-locality, Fuziling Provision Reserve, Yaoluoping Nature Reserve, and an adjacent area in the Dabie Mountains, Anhui, China (Figure 5). The new species was discovered in the leaf litter of a well-preserved montane evergreen deciduous broad-leaved mixed forest (635–1361 m a.s.l.).

Figure 5.

Figure 5

Open in a new tab

Habitat of Achalinus dabieshanensis sp. nov. in its type locality in the Dabie Mountains, Anhui, China (Photography by Baowei Zhang).

4. Discussion

Achalinus is an ancient group, which diverged from its closest related genus approximately 77.4 million years ago, and is widely distributed in China, Vietnam, and Japan now [4,18,19,31]. However, the morphological characteristics of the genus Achalinus are relatively conservative, such as its color, number of scales, etc. [20], which require detailed morphological differences comparison and more molecular evidence to distinguish species [14,20]. Thus, for Achalinus, slight morphological differences often play key roles in species delimitation. For example, in 2019, A. yunkaiensis was discovered in Guangdong; it only differs from A. spinalis by comparing the length of suture between the internasals and that between the prefrontals [10]. Another example is that A. huangjietangi only differs from A. yunkaiensis by a dark streak in the middle of the caudal ventral [14]. In addition, A. huangjietangi differs from A. spinalis by the number of anterior temporals in contact with the eye and a dark streak in the middle of the caudal ventral [14]. In contrast, there are often very substantial genetic differentiations between these species. Given the significant molecular distance within the specimens of A. huangjietangi, we suspect that there are one or more cryptic species to be further investigated; because of the lack of the morphological data, we could not further investigate the taxonomic relationship within those specimens [14]. Temporarily in this study, they are labeled as sp. 1 and sp. 2 (Figure 1).

In this study, ML and BI trees showed that A. dabieshanensis sp. nov. is the sister to A. huangjietangi (Figure 1), and these two lineages have distinct morphologies (Figure 3, Table 4). Moreover, the difference between A. dabieshanensis and A. huangjietangi is also reflected in their significant genetic divergences (p-distance = 9.4%, Table 2); their genetic distance is higher than that among many species in the genus. In general, Achalinus species tend to inhabit wetter, more mountainous areas with low dispersal ability [9], so large rivers may form insurmountable geographical barriers [13]. In this study, the Yangtze River acted as the geographical barrier separating A. huangjietangi from the A. dabieshanensis sp. nov.. Similar situations have been reported in adjacent species, such as A. timi and A. zugorum; they were separated by the Red River [13]. Therefore, the limited dispersal ability and geographical barriers may have probably led to species divergence between A. huangjietangi and A. dabieshanensis sp. nov. Based on the molecular and morphological evidence, we think that A. dabieshanensis sp. nov. should be considered a valid species.

The discovery of A. dabieshanensis sp. nov. extends the distribution of the genus northward to Dabie Mountain in the lower reaches of the Yangtze River. To date, many new vertebrate species have been discovered in the Dabie Mountains [32,33,34,35,36,37]; the discovery of the A. dabieshanensis sp. nov. further suggests that species diversity in the Dabie Mountains remains underestimated to some extent. At present, based on the collection sites of the three new specimens, it is speculated that A. dabieshanensis sp. nov. may be distributed throughout the Dabie Mountains. Given that the secretive nature of odd-scaled snakes makes their discovery largely serendipitous [10], we cannot make exact judgments about the abundance and population status of the new species in the Dabie Mountain area. Therefore, it is difficult to assess the risk of extinction of this species for the time being. We recommend classifying A. dabieshanensis sp. nov. as Data Deficient (DD) on the IUCN Red List. It is worth noting that human activities in the Dabie Mountains in recent years, including vegetation destruction, road construction, and artificial surface expansion [38], may threaten this species.

5. Conclusions

A new species of Achalinus, Achalinus dabieshanensis sp. nov., is described based on three specimens collected from the Dabie Mountains of western Anhui Province. It appears to be widespread in the Dabie Mountains. The discovery of new species made the members of the genus Achalinus distribution area extend northward to the Dabie Mountain in the lower reaches of the Yangtze River. However, their discovery is largely accidental, which makes it difficult for us to make accurate judgments on the abundance and population status of this new species in the Dabie Mountains. Further investigations will be necessary to assess the risk of extinction of this species.

Acknowledgments

We are grateful to Lihua Huang, Peng Guo, Vinh Quang Luu, and Tao Pan for their help in the study. We thank Zhen Xu and Guotao Chen for their assistance in the fieldwork and manuscript preparation, Na Xu for making a map of the collection location, and Kai Zhao for photographing the holotype. We are also grateful to the anonymous reviewers’ useful and constructive comments on our manuscript.

Author Contributions

Conceptualization, C.Z., K.L. and R.H.; methodology, all authors; data curation, C.Z., R.H. and K.L.; writing—original draft preparation, C.Z. and T.H.; writing—review and editing, C.Z., K.L. and R.H.; visualization, T.H., L.Y., R.S., Y.Z. and J.W.; supervision, B.Z. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

The study received ethical review and approval from the Institutional Animal Care and Use Committee of School of Life Sciences, Anhui University (project number IACUC(AHU)-2022-050).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

Funding Statement

Comprehensive Scientific Investigation of Biodiversity in the Dabie Mountains (2019FY101803), the Biodiversity Survey, Monitoring, and Assessment Project of Ministry of Ecology and Environment, China (Grant No. 2019HB2096001006).

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

References

  • 1.Goris R.C., Maeda N. Guide to the Amphibians and Reptiles of Japan. Krieger Publishing Company; Malabar, FL, USA: 2004. [Google Scholar]
  • 2.Karsen S.J., Lau M.W., Bogadek A. Hong Kong Amphibians and Reptiles. Urban Council; Hong Kong, China: 1986. p. 136. [Google Scholar]
  • 3.Koshikawa A. Three new species of reptiles from Hainan Island, Guangdong Province. Smithson. Herpetol. Inf. Serv. 1982;53:1–10. doi: 10.5479/si.23317515.53.1. [DOI] [Google Scholar]
  • 4.Ota H., Toyama M. Taxonomic re-definition of Achalinus formosanus Boulenger (Xenoderminae: Colubridae: Ophidia), with description of a new subspecies. Copeia. 1989;8:597–602. doi: 10.2307/1445485. [DOI] [Google Scholar]
  • 5.Van D.J. Concerning certain species of reptiles and amphibians from China, Japan, the Loo Choo Islands, and Formosa. Proc. Calif. Acad. Sci. 1912;3:187–258. [Google Scholar]
  • 6.Wang Y.Y., Chen C.Q., Zhao J., Wu Y., Liu Z.T., Yang J.H., Yu W.H., Lin J.S., Liu Z.Y., Wang J., et al. Color atlers of terrestrial vertebrates of the Jinggangshan region in China. Beijing Sci. Press. 2017;25:1321–1330. [Google Scholar]
  • 7.Ziegler T. Die Amphibien und Reptilien eines Tieflandfeuchtwald-Schutzgebietes in Vietnam. Natur & Tier Verlag; Münster, Germany: 2002. [Google Scholar]
  • 8.Zhao E.M. Snakes of China. Anhui Science and Technology Publishing House; Hefei, China: 2006. [Google Scholar]
  • 9.Ziegler T., Nguyen T.Q., Pham C.T., Nguyen T.T., Pham A.V., Schingen V.S., Nguyen T.T., Le M.D. Three new species of the snake genus Achalinus from Vietnam (Squamata: Xenodermatidae) Zootaxa. 2019;4590:249–269. doi: 10.11646/zootaxa.4590.2.3. [DOI] [PubMed] [Google Scholar]
  • 10.Wang J., Li Y., Zeng Z.C., Lyu Z.T., Sung Y.H., Li Y.Y., Yu C.L., Wang Y.Y. A new species of the genus Achalinus from southwestern Guangdong Province, China (Squamata: Xenodermatidae) Zootaxa. 2019;4674:471–481. doi: 10.11646/zootaxa.4674.4.6. [DOI] [PubMed] [Google Scholar]
  • 11.Li K., Yu M., Wu Y.Y., Liao L.H., Tang K., Liu Q., Guo P. A new species of the genus Achalinus (Squamata: Xenodermatidae) from southeastern Yunnan Province, China. Zootaxa. 2020;4860:116–128. doi: 10.11646/zootaxa.4860.1.6. [DOI] [PubMed] [Google Scholar]
  • 12.Luu Q.V., Ziegler T., Ha V.N., Lo O.V., Hong T.T., Ngo T.H., Le M.D., Tran D.H., Nguyen T.Q. A new species of Achalinus (Squamata: Xenodermidae) from Trang An Landscape Complex, Ninh Binh Province, Vietnam. Zootaxa. 2020;4877:174–184. doi: 10.11646/zootaxa.4877.1.8. [DOI] [PubMed] [Google Scholar]
  • 13.Miller A.H., Davis H.R., Luong A.M., Do Q.H., Pham C.T., Ziegler T., Lee J.L., De-Queiroz K., Reynolds R.G. Discovery of a new species of enigmatic Odd-Scaled snake (Serpentes: Xenodermidae: Achalinus) from Ha Giang Province, Vietnam. Copeia. 2020;108:796–808. doi: 10.1643/CH2020060. [DOI] [Google Scholar]
  • 14.Huang R.Y., Peng L.F., Yu L., Huang T.Q., Jiang K., Chang J.K., Yang D.C., Xu Y.H., Huang S. A new species of the genus Achalinus from Huangshan, Anhui, China (Squamata: Xenodermidae) Asian Herpetol. Res. 2021;12:1–10. [Google Scholar]
  • 15.Hou S.B., Wang K., Gou P., Chen J.M., Yuan Z.Y., Che J. Two new species and a new country record of the genus Achalinus (Reptilia: Squamata: Xenodermidae) from China. Zootaxa. 2021;4950:528–546. doi: 10.11646/zootaxa.4950.3.6. [DOI] [PubMed] [Google Scholar]
  • 16.Li K., Wu Y.Y., Xu R.Y., Zhu F., Ren J.L., Guo P., Dong B.J. A new species of the Achalinus rufescens complex (Xenodermidae: Achalinus) from Fujian Province, China. Zootaxa. 2021;5026:239–254. doi: 10.11646/zootaxa.5026.2.5. [DOI] [PubMed] [Google Scholar]
  • 17.Yang D.C., Huang R.Y., Jiang K., Burbrink F.T., Gong Y.A., Yu J., Zhang Y., Huang T.Q., Huang S. A new species of the genus Achalinus (Squamata: Xenodermidae) from Ningshan County, Shaanxi Province, China. Zootaxa. 2022;5190:127–140. doi: 10.11646/zootaxa.5190.1.5. [DOI] [PubMed] [Google Scholar]
  • 18.Smith M.A. Reptilia and Amphibia. Taylor & Francis Ltd.; London, UK: 1943. [Google Scholar]
  • 19.Zhao E.M., Huang M.H., Zong Y. Fauna Sinica: Reptilia, Vol. 3, Squamata, Serpentes. Science Press; Beijing, China: 1998. [Google Scholar]
  • 20.Guo P., Liu Q., Li J.T., Zhong G.H., Chen Y.Y., Wang Y.Z. Catalogue of the type specimens of amphibians and reptiles in the herpetological museum of the Chengdu institute of biology, Chinese Academy of Sciences: III. snakes excluding Viperids (Reptilia, Serpentes) Asian Herpetol. Res. 2012;3:334–339. [Google Scholar]
  • 21.Peng L.F., Yang D.C., Duang S.Q., Huang S. Mitochondrial genome of the common burrowing snake Achalinus spinalis (Reptilia: Xenodermatidae) Mitochondrial DNA Part B. 2017;2:571–572. doi: 10.1080/23802359.2017.1365643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Zhang B.W., Huang X., Pan T., Zhang L., Zhou W.L., Song T., Han D.M. Systematics and species validity of the Dabieshan Pit Viper Protobothrops dabieshanensis. Asian Herpetol. Res. 2013;4:282–287. [Google Scholar]
  • 23.Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor Laboratory Press; Cold Spring Harbor, NY, USA: 1989. [Google Scholar]
  • 24.Nagy Z.T., Sonet G., Glaw F., Vences M. First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. PLoS ONE. 2012;7:e34506. doi: 10.1371/journal.pone.0034506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Nylander J.A.A. MrModeltest v2. Program Distributed by the Author. Evolutionary Biology Centre; Uppsala, Sweden: 2004. [Google Scholar]
  • 28.Ronquist F., Teslenko M., Van D.M.P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Soc. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. Posterior summarization in bayesian phylogenetics using tracer 1.7. Syst. Biol. 2018;67:901–904. doi: 10.1093/sysbio/syy032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Rambaut A. FigTree version 1.4.2. 2014. [(accessed on 22 October 2022)]. Available online: http://tree.bio.ed.ac.uk/
  • 31.Li J.N., Liang D., Wang Y.Y., Guo P., Huang S., Zhang P. A large-scale systematic framework of Chinese snakes based on a unified multilocus marker system. Mol. Phylogenetics Evol. 2020;148:106807. doi: 10.1016/j.ympev.2020.106807. [DOI] [PubMed] [Google Scholar]
  • 32.Zhang C.W., Chen C., Zhang M.H., Wang Z.Y., Ma H.H., Sun R.L., Jiang J.P., Zhang B.W. A New Species of the Genus Microhyla (Amphibia: Anura: Microhylidae) from the Dabie Mountains, China. Animals. 2022;12(21):2894. doi: 10.3390/ani12212894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Hu T.L., Xu Z., Zhang H., Liu Y.X., Liao R., Yang G.D., Sun R.L., Shi J., Ban Q., Li C.L., et al. Description of a new species of the genus Uropsilus (Eulipotyphla: Talpidae: Uropsilinae) from Dabie Mountains, Anhui, Eastern China. Zool. Res. 2021;42:294–299. doi: 10.24272/j.issn.2095-8137.2020.266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Huang X., Pan T., Han D., Zhang L., Hou Y.X., Yu L., Zheng H., Zhang B.W. A new species of the genus Protobothrops (Squamata: Viperidae: Crotalinae) from the Dabie Mountains, Anhui, China. Asian Herpetol. Res. 2012;3:213–218. [Google Scholar]
  • 35.Pan T., Zhang Y.N., Wang H., Wu J., Kang X., Qian L.F., Li K., Zhang Y., Chen J.Y., Rao D.Q., et al. A new species of the genus Rhacophorus (Anura: Rhacophoridae) from Dabie Mountains in east China. Asian Herpetol. Res. 2017;8:1–13. [Google Scholar]
  • 36.Qian L.F., Sun X.N., Li J.Q., Guo W.B., Pan T., Kang X., Wang H., Jiang J.P., Wu J., Zhang B.W. A new species of the genus Tylototriton (Amphibia: Urodela: Salamandridae) from the southern Dabie Mountains in Anhui Province. Asian Herpetol. Res. 2017;8:151–164. [Google Scholar]
  • 37.Wang C.C., Qian L.F., Zhang C.L., Guo W.B., Pan T., Wu J., Wang H., Zhang B.W. A new species of Rana from the Dabie Mountains in eastern China (Anura, Ranidae) Zookeys. 2017;724:135–153. doi: 10.3897/zookeys.724.19383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Tian S., Xu J.L., Wang Y. Human infrastructure development drives decline in suitable habitat for Reeves’s pheasant in the Dabie Mountains in the last 20 years. Glob. Ecol. Conserv. 2020;22:e00940. doi: 10.1016/j.gecco.2020.e00940. [DOI] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Articles from Animals : an Open Access Journal from MDPI are provided here courtesy of Multidisciplinary Digital Publishing Institute (MDPI)

RESOURCES