Research Article |
Corresponding author: Jin-Long Ren ( renjl@cib.ac.cn ) Corresponding author: Jia-Tang Li ( lijt@cib.ac.cn ) Academic editor: Silke Schweiger
© 2022 Mao-Liang Li, Jin-Long Ren, Jun-Jie Huang, Zhi-Tong Lyu, Shuo Qi, Ke Jiang, Ying-Yong Wang, Jia-Tang Li.
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:
Li M-L, Ren J-L, Huang J-J, Lyu Z-T, Qi S, Jiang K, Wang Y-Y, Li J-T (2022) On the validity of Hebius sauteri maximus (Malnate, 1962) (Squamata, Natricidae), with the redescription of H. maximus comb. nov. and H. sauteri (Boulenger, 1909). Herpetozoa 35: 265-282. https://doi.org/10.3897/herpetozoa.35.e94920
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Hebius sauteri (Boulenger, 1909) has been long recognized as a widely distributed species with three subspecies, namely Hebius sauteri sauteri from Taiwan Island and southeastern China, Hebius sauteri bourreti (Malnate, 1962) from northern Vietnam, and Hebius sauteri maximus (Malnate, 1962) from Sichuan, southwestern China. However, the validity of these subspecies of the H. sauteri complex has not been evaluated. In the current study, we re-evaluate the taxonomic status of H. s. maximus based on morphological and molecular evidence. Molecular phylogenetic results indicate that H. s. maximus is a distantly diverged clade with respect to H. s. sauteri, and that H. s. maximus is morphologically distinguishable from the nominative subspecies. Therefore, our results support the validity of H. s. maximus and we elevate it to full species status, namely Hebius maximus comb. nov. The distribution range of H. sauteri is revised according to our proposed taxonomic change. Furthermore, detailed redescription, natural history, and coloration of both H. sauteri and H. maximus and comments on the validity of H. s. bourreti are also provided.
distribution, hemipenis, revision, subspecies, taxonomic confusion
Keelback snakes of the family Natricidae Bonaparte, 1840 represent a remarkable radiation of snakes in the world, which show unique adaptation to humid or riparian habitats (
Hebius sauteri (Boulenger, 1909) is a small to medium-sized snake inhabiting moist mountains and often found near water. Described based on two specimens from Taiwan Island, southeastern China, the species was subsequently reported across southern China and northern Vietnam (
Based on the examination of voucher specimens in natural history collection and individuals newly collected from the field, we re-evaluated the taxonomic status of H. s. sauteri and H. s. maximus by using morphological and molecular phylogenetic data, and discussed the taxonomic status of H. s. bourreti.
During field surveys conducted in the last five years, nine specimens of H. sauteri were collected in Sichuan, Guizhou, Guangdong, and Fujian, including one specimen near the type locality of H. s. maximus (
A total of 44 specimens of H. sauteri were examined in this study. The description and measurements of morphological characters were obtained according to
The hemipenes of one adult specimen of H. s. maximus near the type locality (
The following measurements were also used for hemipenial description: hemipenial total length (HTL): distance from the bottom of the truncus to the tip of the most distant point in the vertical direction; hemipenial truncus length (HCL): distance from the bottom of the truncus to the tip of crotch in the vertical direction; hemipenial total width (HTW): the widest distance of the hemipenis in the horizontal direction. The following ratios were also obtained from raw measurements, including HTL/HTW, HCL/HTL.
Additional morphological data were also obtained from published literature (
Sequences of 39 specimens of 20 species were obtained from GenBank (Table
Taxon | Voucher number | Locality | GenBank accession number | Reference | |||
---|---|---|---|---|---|---|---|
Cyt b | C-mos | NT3 | Rag1 | ||||
Hebius atemporalis | HS 11001 (CHS 153) | Mengzi, Yunnan, China | MK201299 | – | – | MK194367 |
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Hebius atemporalis | GP 1626 | Guangdong, China | KJ685680 | KJ685630 | KJ685732 | KJ685572 |
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Hebius boulengeri | SYS r001506 (CHS 757) | Dawuling, Guangdong, China | MK201509 | – | – | – |
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Hebius boulengeri | RE55 (CHS 291) | Chebaling, Guangdong, China | MK201380 | – | – | MK194448 |
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Hebius boulengeri | GP 1789 | Guangdong, China | KJ685684 | KJ685634 | KJ685736 | KJ685576 |
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Hebius clerki | CAS 215036 | Yunnan, China | KJ685666 | KJ685615 | KJ685716 | KJ685559 |
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Hebius concelarus | KUZ: R20253 (AB 989268) | Miyakojimashi, Japan | AB989268 | AB989271 | LC047778 | LC047774 |
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Hebius concelarus | KUZ: R20255 (AB 989272) | Miyakojimashi, Japan | AB989272 | – | – | – |
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Hebius craspedogaster | GP 139 | Sichuan, China | JQ687437 | JQ687429 | KJ685730 | KJ685569 |
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Hebius craspedogaster | HS 13020 (CHS 155) | Huangshan, Anhui, China | MK201301 | – | – | MK194369 |
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Hebius craspedogaster | SYS r000910 (CHS 602) | Huangshan, Anhui, China | MK201428 | – | – | MK194505 |
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Hebius igneus | AMNH 148575 | Ha Giang, Vietnam | KJ685665 | KJ685614 | KJ685715 | KJ685558 |
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Hebius ishigakiensis | KUZ: R33044 | Iriomotejima, Japan | AB989294 | – | – | – |
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Hebius ishigakiensis | KUZ: R33045 | Iriomotejima, Japan | AB989296 | – | – | – |
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Hebius johannis | GP 1569 | Yunnan, China | KJ685678 | KJ685628 | KJ685731 | KJ685571 |
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Hebius johannis | GP 897 | Yunnan, China | KJ685708 | KJ685658 | KJ685767 | KJ685605 |
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Hebius khasiensis | CAS 221504 | Kachin, Myanmar | KJ685668 | KJ685617 | KJ685718 | KJ685561 |
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Hebius khasiensis | CAS 221525 | Kachin, Myanmar | KJ685669 | KJ685618 | KJ685719 | KJ685562 |
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Hebius metusia | HS 11158 (CHS 152) | Pingshan, Yibin, Sichuan, China | MK201298 | – | – | MK194366 |
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Hebius metusia | GP 871 | Sichuan, China | KJ685707 | KJ685657 | KJ685766 | – |
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Hebius metusia | GP 1712 | Sichuan, China | KJ685682 | KJ685632 | KJ685734 | KJ685574 |
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Hebius modestus | CAS 234262 | Yunnan, China | KJ685671 | KJ685620 | KJ685721 | KJ685564 |
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Hebius optatus | HS 11143 (CHS 151) | Mangshan, Hunan, China | MK201297 | – | – | MK194365 |
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Hebius optatus | GP 1885 | Guizhou, China | KJ685687 | KJ685637 | KJ685739 | KJ685579 |
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Hebius optatus | AMNH 147155 | Vinh Phu, Vietnam | KJ685662 | KJ685611 | KJ685712 | KJ685555 |
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Hebius popei | GP 2169 | Hainan, China | KJ685692 | KJ685642 | KJ685744 | KJ685584 |
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Hebius popei | GP 2386 | Guizhou, China | KJ685697 | KJ685647 | KJ685749 | KJ685588 |
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Hebius pryeri | KUZ: R67983 | Amamioshima, Japan | AB989102 | AB989105 | LC047779 | LC047776 |
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Hebius sangzhiensis | SYNU 08070350 | Sangzhi, Hunan, China | MK340763 | – | – | – |
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Hebius sauteri |
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Guangdong, China | OP937178 | OP965807 | OP965801 | OP965796 | This study |
Hebius sauteri | SYS r001766 | Hunan, China | OP937182 | OP965802 | OP965797 | OP965792 | This study |
Hebius sauteri | SYS r001258 | Jiangxi, China | OP937180 | OP965805 | OP965799 | OP965794 | This study |
Hebius sauteri | SYS r001266 | Jiangxi, China | OP937181 | OP965804 | OP965798 | OP965793 | This study |
Hebius sauteri | GP 1790 | Guangdong, China | KJ685685 | KJ685635 | KJ685737 | KJ685577 |
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Hebius sauteri | GP 2549 | Taiwan, China | KJ685701 | KJ685651 | KJ685754 | KJ685592 |
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Hebius sauteri |
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Fujian, China | OP937179 | OP965806 | OP965800 | OP965795 | This study |
Hebius sauteri | SYS r002087 | Hunan, China | OP937183 | OP965803 | – | – | This study |
Hebius maximus | HS 11157 (CHS 156) | Mianyang, Sichuan, China | MK201302 | – | – | MK194370 |
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Hebius maximus | GP 864 | Sichuan, China | KJ685706 | KJ685656 | KJ685765 | KJ685603 |
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Hebius maximus | GP 2382 | Sichuan, China | KJ685696 | KJ685646 | KJ685748 | – |
|
Hebius maximus |
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Dayi, Sichuan, China | OP937186 | OP937189 | OP937192 | OP965791 | This study |
Hebius maximus | SYS r002041 | Bijie, Guizhou, China | OP937184 | OP937190 | OP937191 | OP965790 | This study |
Hebius maximus |
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Bijie, Guizhou, China | OP937188 | – | – | – | This study |
Hebius maximus |
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Bijie, Guizhou, China | OP937187 | – | – | – | This study |
Hebius maximus |
|
Yibin, Sichuan, China | OP937185 | – | – | – | This study |
Hebius vibakari | KUZ: R21587 | Kyoto, Japan | AB989302 | AB989305 | – | – |
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Hebius vibakari | HS 14026 (CHS 149) | Harbin, China | MK201296 | – | – | MK194363 |
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Hebius vibakari | GP 1352 | Heilongjiang, China | KJ685677 | KJ685627 | KJ685729 | KJ685568 |
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Hebius yanbianensis | GP 4006 | Yanbian, Sichuan, China | MH532291 | – | – | – |
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Herpetoreas tpser | JK 201710 (CHS 849) | Mêdog, Tibet, China | MK201567 | – | – | – |
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A single mitochondrial gene (mitochondrial cytochrome b, Cyt b) and three nuclear genes (oocyte maturation factor mos, C-mos; recombination-activating gene 1, Rag1; neurotrophin 3, NT3) were amplified by using polymerase chain reaction (PCR), primers used in amplification are listed in Table
Gene | Primers | Primer sequences (from 5’ to 3’) | Reference |
---|---|---|---|
Cyt b | L14919 | AACCACCGTTGTTATTCA ACT |
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H16064 | CTTTGGTTTACAAGA ACAATGCTTTA | ||
C-mos | S77 | CATGGACTGGGATCAGTTATG |
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S78 | CCTTGGGTGTGATTTTCTCACCT | ||
Rag1 | R13 | TCTGAATGGAAATTCAAGCTGTT |
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R18 | GATGCTGCCTCGGTCGGCCACCT TT | ||
NT3 | NT3F | ATATTTCTGGCTTTTCTCTGTGGC |
|
NT3R | GCGTTTCATAAAAATATTGTTTGACCGG |
The best model of sequence evolution for Maximum Likelihood (ML) and Bayesian inference (BI) analysis were selected using PartitionFinder v2.1.1 (
Aligned sequences concatenation is 3,087 bp in length (Cyt b = 1,070 bp; C-mos = 587 bp; NT3 = 476 bp; Rag1 = 954 bp). The topological structure of the phylogenetic tree (Fig.
The uncorrected pairwise distance of Cyt b sequences between H. s. maximus and H. s. sauteri varies from 12.05 to 12.65% (Table
Uncorrected p-distance between Hebius species based on 1070 base pairs from the mitochondrial genes Cyt b.
Number | Species | Voucher | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | 13 | 14 | 15 |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | Hebius atemporalis | GP 1626 | |||||||||||||||
2 | Hebius concelarus | KUZ: R20255 | 0.174 | ||||||||||||||
3 | Hebius craspedogaster | GP 139 | 0.152 | 0.164 | |||||||||||||
4 | Hebius igneus | AMNH 148575 | 0.155 | 0.174 | 0.168 | ||||||||||||
5 | Hebius ishigakiensis | KUZ: R33044 | 0.136 | 0.133 | 0.159 | 0.159 | |||||||||||
6 | Hebius metusia | GP 871 | 0.131 | 0.150 | 0.131 | 0.143 | 0.136 | ||||||||||
7 | Hebius optatus | AMNH 147155 | 0.145 | 0.144 | 0.157 | 0.163 | 0.131 | 0.136 | |||||||||
8 | Hebius pryeri | KUZ: R67983 | 0.153 | 0.093 | 0.171 | 0.176 | 0.117 | 0.139 | 0.151 | ||||||||
9 | Hebius sangzhiensis | SYNU 08070350 | 0.151 | 0.132 | 0.152 | 0.162 | 0.123 | 0.139 | 0.139 | 0.120 | |||||||
10 | Hebius sauteri |
|
0.138 | 0.151 | 0.143 | 0.162 | 0.123 | 0.119 | 0.120 | 0.141 | 0.132 | ||||||
11 | Hebius sauteri | SYS r001258 | 0.136 | 0.151 | 0.139 | 0.162 | 0.125 | 0.117 | 0.120 | 0.137 | 0.133 | 0.009 | |||||
12 | Hebius sauteri |
|
0.124 | 0.139 | 0.138 | 0.158 | 0.115 | 0.110 | 0.112 | 0.132 | 0.126 | 0.030 | 0.029 | ||||
13 | Hebius maximus |
|
0.133 | 0.157 | 0.133 | 0.144 | 0.125 | 0.124 | 0.124 | 0.139 | 0.082 | 0.125 | 0.126 | 0.116 | |||
14 | Hebius maximus |
|
0.133 | 0.154 | 0.136 | 0.150 | 0.122 | 0.134 | 0.122 | 0.139 | 0.084 | 0.123 | 0.124 | 0.116 | 0.007 | ||
15 | Hebius maximus |
|
0.139 | 0.151 | 0.137 | 0.150 | 0.128 | 0.136 | 0.125 | 0.136 | 0.085 | 0.124 | 0.125 | 0.117 | 0.007 | 0.007 | |
16 | Hebius yanbianensis | GP 4006 | 0.130 | 0.152 | 0.139 | 0.150 | 0.134 | 0.057 | 0.141 | 0.135 | 0.126 | 0.126 | 0.124 | 0.120 | 0.119 | 0.125 | 0.129 |
Specimens of H. s. maximus from Sichuan and Guizhou Provinces in southwestern China largely agree with the original description of H. s. maximus as follows (data from the original description in parenthesis): ventrals 132–143 (vs. 137–141); SpL 7–8 (vs. 7); IfL 7–9 on both sides of the head, IfL 1–3, 1–4, or 1–5 border the anterior chin-shields (vs. IfL 8/9, IfL 1–4 in contact with the anterior chin-shields); 2 preoculars in two specimens, on both sides in
Although superficially similar to H. s. sauteri, H. s. maximus can be distinguished from H. s. sauteri by having a higher number of ventrals (132–138 in males, 135–143 in females in H. s. maximus vs. 125–130 in males, 116–133 in females in H. s. sauteri), a higher number of ventrals + subcaudals (207–225 in H. s. maximus vs. 187–212 in H. s. sauteri), and a different coloration of infralabials (usually white with black edge on the posterior part of 1st–3rd IfL only in H. s. maximus vs. white with black edge between each IfL in H. s. sauteri) (Table
Morphological characters of H. maximus and H. sauteri. For specimens with asymmetrical cephalic scales, the scale count was given as “left/right”, “–” indicates missing data.
Species | Voucher number | Locality | Sex | ToL (mm) | TL (mm) | SpL | IfL | PtO | DSR | V | SC | V+SC | MT |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
H. maximus |
|
Sichuan, China | M | 470 | 141 | 3-2-3 | 8 | 3 | 17-17-17 | 138 | 87+1 | 225 | 22+2 |
H. maximus |
|
Sichuan, China | M | 433 | 137+? | – | – | 2 | 17-17-17 | 137 | 74+? | – | – |
H. maximus |
|
Guizhou, China | M | 352 | 117 | 3/2-2-2 | 7/8 | 2 | 17-17-17 | 136 | 83+1 | 219 | – |
H. maximus | YBU 18170 | Sichuan, China | M | 260 | 66 | 2-2-3 | 9 | 3/2 | 17-17-17 | 137 | 72+1 | 209 | 22+2 |
H. maximus | YBU 11258 | Chongqing, China | M | 365 | 111 | 2-2-3 | 7 | 2/3 | 17-17-17 | 133 | 92+1 | 225 | 22+2 |
H. maximus |
|
Guizhou, China | F | 384 | 106 | 3/2-2-3 | 7/8 | 3 | 17-17-17 | 141 | 73+1 | 214 | – |
H. maximus |
|
Sichuan, China | F | 496 | 131 | 2-2-3 | 8 | 2/3 | 17-17-17 | 135 | 73+1 | 208 | – |
H. maximus |
|
Guizhou, China | F | 300 | 70 | 2-2-3 | 8 | 3/2 | 17-17-17 | 143 | 64+1 | 207 | – |
H. maximus |
|
Sichuan, China | F | 333 | 93 | 2/3-3/2-3 | 7 | 2 | 17-17-17 | 135 | 72+1 | 207 | – |
H. maximus |
|
Sichuan, China | F | 523 | 162 | 3-2-3 | 8 | 2/3 | 17-17-17 | 135 | 82+1 | 217 | – |
H. sauteri | SYS r001766 | Hunan, China | M | 320 | 96 | 2-2-3 | 7/8 | 3/2 | 17-17-17 | 128 | 76+1 | 204 | 24+2 |
H. sauteri | SYS r001266 | Jiangxi, China | M | 282 | 88 | 2-2-3 | 8 | 2/3 | 17-17-17 | 129 | 84+1 | 213 | 23+2 |
H. sauteri |
|
Hainan, China | M | 347 | 95 | 3/2-2-? /2 | -/8 | 3 | 17-17-17 | 125 | 74+1 | 199 | – |
H. sauteri |
|
Taiwan, China | F | 303 | 99 | 2-2-3 | 7 | 3 | 17-17-17 | 116 | 71+1 | 187 | – |
H. sauteri |
|
Taiwan, China | – | 299 | 83 | 2-2-3 | 7 | 3 | 17-17-17 | 128 | 77+1 | 205 | – |
H. sauteri | YBU 17001 | Hainan, China | F | 225 | 58 | 2-2-3 | 7 | 3 | 17-17-17 | 126 | 76+1 | 202 | 25+2 |
H. sauteri |
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Fujian, China | F | 412 | 120 | 2-2-3 | 8 | 2/3 | 17-17-17 | 133 | 79+1 | 212 | 24+3 |
H. sauteri |
|
Guangdong, China | F | 324 | 88 | 2-2-3 | 7 | 3 | 17-17-17 | 129 | 69+1 | 198 | – |
H. sauteri | SYS r001150 | Guangdong, China | F | 145 | 38 | 2-2-3 | 7 | 3 | 17-17-17 | 129 | 70+1 | 199 | 21+2 |
H. sauteri | SYS r000275 | Guizhou, China | F | 306 | 77 | 2-2-3 | 7 | 3/2 | 17-17-17 | 132 | 66+? | – | – |
Comparison of main morphological characters of H. maximus, H. s. sauteri, “–” indicates missing data.
Species | TL/ToL | V | SC | V + SC | MT | |||||
---|---|---|---|---|---|---|---|---|---|---|
Male | Female | Male | Female | Male | Female | Male | Female | Male | Female | |
H. maximus | 0.25–0.33 (0.29 ± 0.02) | 0.25–0.31 (0.27 ± 0.02) | 132–138 (136 ± 2) | 135–143 (138 ± 3) | 72–92 (81 ± 6) | 64–82 (72 ± 5) | 209–225 (216 ± 6) | 207–217 (210 ± 3) | 24 | – |
H. s. sauteri | 0.27–0.31 (0.30 ± 0.02) | 0.24–0.33 (0.28 ± 0.02) | 125–130 (128 ± 2) | 116–133 (129 ± 4) | 74–84 (78 ± 4) | 69–86 (74 ± 5) | 199–213 (205 ± 6) | 187–215 (203 ± 7) | 25–27 | 23–27 |
Consequently, all available data support the recognition of H. s. maximus as a distinct species rather than a subspecies of H. sauteri. Herein, we elevate the subspecies H. s. maximus to a full species status, i.e., Hebius maximus (
Tropidonotus sauteri Boulenger, 1909, Ann. Mag. Nat. Hist., London. ser.8, 4, 495. Type locality: Kosempo (= Chiahsien, Kaohsiung County), Taiwan, China.
Natrix sauteri
—
Amphiesma sauteri
—
Amphiesma sauteri sauteri
—
Amphiesma sauteri bourreti
—
Natrix copei
Syntypes
.
19 specimens of H. s. sauteri were examined in this study: CHINA (n = 19) – Taiwan Prov.
Hebius sauteri can be distinguished from its congeners by the following features: (1) body size small to medium, maximum ToL 455 mm; (2) dorsal scales rows 17-17-17, all weekly keeled or smooth on outmost one or two rows; (3) ventral scales 116–133, subcaudals 60–86, paired; (4) maxillary teeth 23–27, last two or three distinctly enlarged teeth, without diastema; (5) preocular single, occasionally two; (6) supralabials 6–8, 2nd or 2nd–3rd border the loreal; (7) infralabials 6–9, mostly edged with black on their posterior border; (8) single white to orange stripe extends from angulus oris to neck; (9) dorsal body brown to reddish brown, with or without single series of white spots or short band on lateral.
Head moderately distinct from neck; body size small to medium, ToL 145–455 mm (282–370 mm in males, 145–455 mm in females), TL/ToL 0.24–0.33 (0.27–0.31 in males, 0.24–0.33 in females). Eye large, pupil round.
Dentition. Maxillary teeth 23–27 without diastema, gradually enlarged posteriorly, last two or three distinctly enlarged.
Body scalation. Body scale in 17-17-17 rows, weekly keeled except outer 1–4 rows smooth anteriorly, outer 0–2 rows smooth at midbody and outer 0–1 row smooth posteriorly; ventrals 116–133 (125–130 in males, 116–133 in females); subcaudals 60–86 (60–86 in females, 65–84 in males), paired.
Head scalation. Rostral broad, visible from above; internasals paired, nearly triangular, curved outwards, not in contact with loreal; prefrontals paired, nearly in a diamond shape, wider than long, border on loreal laterally, preocular and supraocular posteriorly; frontal hexagonal, longer than wide, embedded into parietal posteriorly; parietal paired, much longer than wide; nasals wider than high, divided below nostril, borders 1st–2nd supralabials; loreal single, rarely divided (right side of
Hemipenis. The description of the hemipenis is based on an adult specimen (SYS r000323) from Mt. Jinggang, Jiangxi, southeastern China. Left side of hemipenis fully everted, right side remained in situ for description of retracted condition.
The everted hemipenis is thin and short, Y-shaped, shallowly bilobed. Both sulcate and asulcate surfaces densely ornamented with spinules, a large basal hook present at proximal part. Sulcus spermaticus single, extending to base of inner right lobe where it takes a centripetal position. Sulcus lip highly developed and raised, walls covered with spinules (Fig.
In situ hemipenis extends to 7th SC with its crotch extending to 6th SC; crotch of m. retractor penis magnus extending to 8th SC, origin of m. retractor penis magnus at level of 20th SC.
Based on two adult female specimens from Guangdong (
Dorsal (left), lateral (middle) and ventral (right) of the head comparisons between Hebius sauteri and Hebius maximus comb. nov. Row D photographed by Kai Wang, others were photographed by Jun-Jie Huang. A–C. Hebius maximus comb. nov. (A.
Largely the same as in life except dorsal side of head brown to dark brown, scattered with small black spots; ventral side of head cream white; a pale yellow stripe extends from angulus oris to dorsal side of neck, 1–2 scales wide; dorsal of body and tail brown to dark brown, a lighter lateral streak on 4th–6th body scale rows presents or not, covered with series of cream white spots separated by 2–3 scales; ventral and subcaudal sides cream to pale white; sclera black (Figs
Hebius sauteri was named after the collector of the type specimens, Hans Sauter (1871–1943), a German naturalist (
This species inhabits flatlands and mountain regions up to 1,500 m and prefers terrestrial microhabitat such as grassland, woodland, and bushes near water bodies; diurnal, occasionally found at night, preys include earthworms, slugs, snails and tadpoles; oviparous (this study;
Hebius sauteri is currently known to be reported in Vietnam (Ngan Son, Lang Son, Tam Dao and Ba Vi), and China, including Taiwan (Kaohsiung County [type locality]), Fujian (Dehua County), Anhui (Huangshan County), Jiangxi (Jinggangshan City, Longnan County), Hunan (Yizhang County), Guangdong (Lianping County, Xinyi County, Deqing County, Ruyuan County, Dongguan City), Guangxi (Jinxiu County, Quanzhou County, Rongxian County, Beiliu County, Long’an County), Guizhou (Libo County, Leishan County), Yunnan (Jinping County), Hainan (Qiongzhong County, Wuzhishan County, Baisha County, Lingshui County) (
Natrix copei (Van Denburgh, 1909) was described by
Amphiesma sauteri maximus Malnate, 1962, Proc. Acad. Nat. Sci. Philadelphia, 114, 251–299. Type locality: “Hsaioyangchi, Szechwan, China.” (= Xiaoyangxi, Mabian Yi Autonomous County, Leshan City, Sichuan Province, China)
Natrix sauteri
—
Amphiesma sauteri maximus
—
Amphiesma sauteri
—
Hebius sauteri
—
Holotype.
Holotype of Hebius maximus comb. nov. (
25 specimens of H. maximus were examined in this study: CHINA (n = 25) – Sichuan Prov.
Hebius maximus comb. nov. can be distinguished from its congeners by the following morphological characters: (1) body size small to medium, maximum ToL 597 mm; (2) dorsal scales rows 17-17-17, all weekly keeled or smooth at outmost one or two rows; (3) ventral scales 132–143, cloacal plates divided, subcaudals 64–92, paired; (4) maxillary teeth 24, last two distinctly enlarged, without diastema; (5) supralabials 7–8; (6) infralabials 7–9, generally edged with black at posterior border on 1st–3rd scales only; (7) a light orange stripe extends from angulus oris to the neck; (8) dorsal body reddish brown or grayish brown, with an ill-defined dark olive streak scattered with black spots extending from neck to end at medium of the dorsal.
Body elongated, small to medium-sized, ToL 175–597 mm (260–470 mm in males, 175–597 mm in females); tail relatively long, TL/ToL 0.25–0.33 (0.25–0.33 in males, 0.25–0.31 in females). Eye large, pupil round.
Dentition. Maxillary teeth 24, without diastema, gradually enlarged posteriorly, last two distinctly enlarged.
Body scalation. Dorsal scales in 17-17-17 rows, weekly keeled except outer 1–4 rows at anterior body, outer 0–2 rows smooth at midbody and outer 0–1 row smooth posteriorly; ventrals 132–143 (132–138 in males, 135–143 in females); cloacal plates divided; subcaudals 64–92 (72–92 in males, 64–82 in females), paired.
Head scalation. Rostral broad, visible from above; internasals paired, nearly triangular, curved outwards, not bordering loreal; prefrontals paired, nearly in a diamond shape, wider than long, borders the loreal, preocular, and supraocular; frontal hexagonal, longer than wide, embedded into parietals posteriorly; parietals paired, not bordering preocular; nasals wider than high, divided at lower half, borders 1st–2nd supralabials; loreal single, borders 2nd or 2nd–3rd supralabials, not entering orbit; preocular single, higher than wide, rarely divided (
Hemipenis. The description of hemipenis based on an adult specimen (
Hemipenis thin and short, hemipenial total length (HTL) 7.14 mm, hemipenial total width (HTW) 1.57 mm. HTL/HTW 4.55; Y-shaped, shallowly bilobed, hemipenial truncus length (HCL): 5.75 mm, HCL/HTL 0.81. Both sulcate and asulcate surfaces densely ornamented with spinules, a large basal hook present at the proximal part. Sulcus spermaticus single, extending to base of inner right lobe where it takes a centripetal position. Sulcus lip highly developed and raised, walls covered with spinules (Fig.
In situ hemipenis extends up to 5th SC with its crotch extending to 4th SC; crotch of m. retractor penis magnus extending to 6th SC, origin of m. retractor penis magnus invariably at level of 20th SC.
Based on one male adult specimen near the type locality (
Largely the same as in life except dorsal head brown to seal brown, with or without irregular dark spots; supralabials cream white to pale gray, 1st–6th supralabials with black edge or spots posteriorly, upper half of the highest supralabial brown to black; a pale orange to yellow short stripe extends from angulus oris to neck; dorsal of body and tail brown to seal brown, slightly darker posteriorly, with or without a series of white spots or short band separated by 2–3 scales on 4–6 body scale rows; ventral and subcaudal cream white to pale grey; sclera black (Fig.
Males H. maximus comb. nov. exhibit a lower number of ventral scales [132–138 (136 ± 2) in male vs. 135–143 (138 ± 3) in female] and a higher number of subcaudal scale counts [72–92 (81 ± 6) in male vs. 64–82 (72 ± 5) in female] than female (n = 13 male and 12 female) (Tables
Hebius maximus comb. nov. differs from H. andreae, H. annamensis, H. arquus, H. beddomei, H. bitaeniatus, H. boulengeri, H. celebicus, H. clerki, H. concelarus, H. craspedogaster, H. deschauenseei, H. flavifrons, H. groundwateri, H. igneus, H. inas, H. ishigakiensis, H. johannis, H. kerinciensis, H. khasiensis, H. lacrima, H. leucomystax, H. metusia, H. miyajimae, H. modestus, H. monticola, H. nicobariensis, H. octolineatus, H. optatus, H. parallelus, H. petersii, H. popei, H. pryeri, H. sangzhiensis, H. sanguineus, H. sarasinorum, H. septemlineatus, H. vibakari, H. viperinus, H. weixiensis, H. xenura and H. yanbianensis by having 17-17-17 dorsal scale rows vs. 19-19-17 rows.
Hebius maximus comb. nov. differs from H. chapaensis, H. frenatus, H. nigriventer, H. sarawacensis and H. taronensis by (1) maxillary teeth 24 vs. 29–34 in H. chapaensis, 28–33 in H. nigriventer, 28–32 in H. taronensis; (2) ventrals 132–143 vs. 159–177 in H. chapaensis, 164–166 in H. frenatus, 155–168 in H. nigriventer, 145–150 in H. sarawacensis, 158–176 in H. taronensis (
Hebius maximus comb. nov. differs from H. atemporalis by (1) temporals present, supralabial not in contact with parietal vs. usually absent or a small triangular temporal between postocular and supralabial, supralabial in contact with parietal; (2) maxillary teeth 24 vs. 27–32 (
Lastly, H. maximus comb. nov. was previously confused with H. sauteri, H. maximus differs from the latter species in having (1) more ventrals, 132–138 in male, 135–143 in female vs. 125–130 in male, 116–133 in female; (2) more ventrals + subcaudals counts, 207–225 vs. 187–215 (3) fewer maxillary teeth 24 vs. 23–27 (
Hebius maximus comb. nov. is named for its highest count of ventral scales among three previous subspecies of H. sauteri (
Hebius maximus comb. nov. inhabits subtropical mountain regions around 812–1,200 m above sea level, including coniferous forest and large forest clearings (
Hebius maximus comb. nov. is currently known to be distributed in southwestern China, including Chongqing (Youyang Tujia & Miao Autonomous County, Xiushan Tujia & Miao Autonomous County), Sichuan (Mabian County, Pingshan County, Yingjing County, Hongya County, Dujiangyan City, Mianyang City, Leshan City) and Guizhou (Qixingguan District, Bijie City) (this study; Wu 1985) (Fig.
The Asian keelback snakes, genus Hebius, has long been considered difficult to identify due to the morphological resemblance among species, and H. maximus and H. sauteri were confused in the past six decades (
Despite the high resemblance between H. maximus and H. sauteri, which leads to great difficulty in species identification, H. sauteri and H. maximus are shown to be two distantly related clades (Fig.
Three subspecies of Hebius sauteri were previously recognized based on the counts of ventral and subcaudal scales, i.e., H. s. sauteri, H. s. bourreti, and H. s. maximus. In the current study, H. s. maximus is recognized as a distinct species, i.e. Hebius maximus (see above). However, the taxonomic identity of the subspecies H. s. bourreti still remained elusive. The taxa H. s. bourreti was originally described by
Yang et al. (2008: 266) reported one specimen of H. s. bourreti from Adebo Town, Jinping County, Yunnan China (Fig.
We thank Dr. Kai Wang (KIZ) for providing photos and morphological data. We thank Mr. Dihao Wu (