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Research Article
First report of albinism for Achalinus sheni (Serpentes, Xenodermidae), with extended diagnosis of the species
expand article infoYu-Hao Xu‡, Shuai Wang‡, Shun Ma§|, Frank T. Burbrink, Li-Fang Peng‡, Song Huang#
‡ Qinghai University, Xining, China
§ Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
| University of Chinese Academy of Science, Beijing, China
¶ Department of Herpetology, The American Museum of Natural History, New York, United States of America
# Anhui Normal University, Wuhu, China

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

Academic editor: Robert Jadin
© 2024 Yu-Hao Xu, Shuai Wang, Shun Ma, Frank T. Burbrink, Li-Fang Peng, Song Huang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Xu Y-H, Wang S, Ma S, Burbrink FT, Peng L-F, Huang S (2024) First report of albinism for Achalinus sheni (Serpentes, Xenodermidae), with extended diagnosis of the species. ZooKeys 1209: 1-17. https://doi.org/10.3897/zookeys.1209.128944
ZooBank: urn:lsid:zoobank.org:pub:923C8E76-D352-42AC-A752-1257B7A562D1
Open Access

Abstract

Albinism is an uncommon phenomenon and inherited condition in animals characterized by a partial or complete lack of melanin. The family Xenodermidae Gray, 1849, is a group of caenophidian snakes widely distributed in South, East, and Southeast Asia, including five recognized genera and 36 species. However, there are currently no reports of albinism in any species in Xenodermidae. Achalinus sheni Ma, Xu, Qi, Wang, Tang, Huang & Jiang, 2023 was first described based on five male specimens from Loudi City and Nanyue District, Hunan Province, China. At the time, there were no descriptions on female individuals. In this study, we report in detail a collected albinistic specimen of A. sheni, which is the first discovery of wild albinism in the family Xenodermidae. We also provide photographs and descriptions of the first three female specimens of A. sheni and extend the diagnosis of this species.

Key words

Hunan Province, morphological characters, phylogeny, Shen’s Odd-scale Snake, Xenodermidae

Introduction

Coloration in most organisms evolved to respond to the background environment (Bechtel 1978; Krecsák 2008; Bruni 2017; Lu et al. 2024; Sun et al. 2024), and melanocytes that function to produce and store melanin play a crucial role in physiological color adaptations. However, the variation of melanocytes can also lead to corresponding chromatic anomalies, like the occurrence of albinism, which is usually characterized by a partial or complete lack of melanin. This condition is usually has been the result of tyrosinase inactivation caused by autosomal recessive mutations (Griffiths et al. 1998; Alberts et al. 2004; Krecsák 2008; Abegg et al. 2015).

In squamate reptiles, albinism is one of the most striking aberrations of body color pattern, which is usually divided into two types: 1) complete albinism showing the complete absence of melanin in the entire body with the red eyes and a pastel yellow, yellow, or white body coloration; and 2) partial albinism manifested as reduction in melanism across the whole body, rather than complete disappearance, resulting in a lighter body coloration (Sazima and Pombal 1986; Sazima and Di-Bernardo 1991; Hoshing and Mahabal 2013; Abegg et al. 2015). Often under artificial conditions, albino reptiles have been well documented, and many species with albino variants have been bred in large numbers for the pet market (Bechtel 1991; Bechtel 1995; Broghammer 2000). However, the wild albino phenomenon is usually extremely rare, due to the high probability of stillborns or malformations, such as linked anatomical abnormalities affecting eyesight, communications, and sexual selection, difficulty thermoregulating, and easy detection by prey and predators (Roulin and Bize 2007; Dutta et al. 2022).

The family Xenodermidae Gray, 1849 is a group of caenophidian snakes widely distributed in South, East, and Southeast Asia and including five recognized genera and 36 species (Deepak et al. 2021). Among them, Achalinus Peters, 1869 has the most species in this family, with 28 recognized species. Due to their cryptic lifestyle, small body size, and inconspicuous body color, they are hard to detect in the wild (Zhao et al. 1998; Zhao 2006; Ziegler et al. 2019). At present, there have been no cases of albinism in any species of Xenodermidae. Achalinus sheni was first described from Loudi City and Nanyue District, Hunan Province, China in 2023 based on five male specimens (Ma et al. 2023a). During a recent herpetological survey in Yangshi Town, Hunan Province, China in July 2023, we collected one male and three female specimens of A. sheni. However, one of the adult females displayed a distinct pastel-yellow body coloration and red eyes, which is considered to be a completely albino individual. In addition, the newly collected female specimens also showed certain sex differences in morphology. Herein, we first report details of the specimen displaying albinism, provide photographs of the first female specimens of A. sheni, and present an extended diagnosis of this species.

Materials and methods

Morphometrics

Four snake specimens were collected from Yangshi Town, Lianyuan City, Hunan Province, China (specimen vouchers LFR2023008–LFR2023010 and LFR2024015). Specimens were humanely euthanized using lethal injection with 0.7% tricaine methanesulfonate (MS222) solution, and liver tissues were taken and preserved in 95% alcohol. Then the specimens were directly preserved in 75% ethanol and deposited in Qinghai University Museum. Sampling procedures involving live snakes were in accordance with the Wild Animals Protection Law of China and approved by the Institutional Ethics Committee of Qinghai University (protocol code SL-2023028). The sex of all specimens was determined by tail dissection.

Measurements and scale counts followed Zhao (2006) and Ma et al. (2023a). Three measurement characters were measured with Deli Stainless Ruler (No. 8462) to the nearest 1 mm : snout–vent length (SVL) ,tail length (TAL) and total length (TL). All other measurements were performed using Deli digital calipers (DL312200) to the nearest 0.1 mm : loreal height (LorH): measured from the highest part to the lowest part of the loreal in lateral view ; loreal length (LorL): measured from the most anterior loreal to the most posterior loreal in lateral view ; length of the suture between internasals (LSBI) ; length of the suture between prefrontals (LSBP) ; head length (HL): taken from the tip of snout to the posterior margin of mandible ; head width (HW): measured around the widest part of the head in dorsal view ; eye diameter (ED): taken from the most anterior corner of the eye to the most posterior corner ; length of supraocular (SPOL): horizontal distance between anterior and posterior tip of supraocular , and length of upper anterior temporal (ATUL): horizontal distance between anterior and posterior tip of upper anterior temporal. The scale characters and their abbreviations are as follows : supralabials (SL) ; infralabials (IL) ; infralabials touching the first pair of chin shields (IL-1st Chin) ; loreals (Lor) ; preoculars (PRO) ; postoculars (PO) ; temporals (TEMP) ; supraoculars (SPO) ; dorsal scale rows (DSR) (counted at one-head-length behind the head, at midbody, at one-head-length before the cloacal plate ); ventral scales (VS) , cloacal plate (CP) , and subcaudals (SC).

Molecular phylogenetic analyses

Genomic DNA was extracted from liver tissue using a Qiagin DNEasy Blood and Tissue Extraction Kit (Qiagen Inc., Valencia, CA). The partial mitochondrial DNA gene encoding cytochrome c oxidase subunit 1 (CO1) was obtained by polymerase chain reaction (PCR) using primer Chmf4 (5′-TYT CWA CWA AYC AYA AAG AYA TCG G-3′) and Chmr4 (5′-ACY TCR GGR TGR CCR AAR AAT CA-3′) (Che et al. 2012). PCR products were sequenced by Shanghai Map Biotech Co., Ltd. The raw sequences were stitched using SeqMan in the DNASTAR software package (Burland 2000) and the newly generated sequences were submitted to GenBank (Table 1).

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

NO. Species name Locality Voucher NO. Genbank No. References
1 Achalinus sheni Lianyuan, Hunan, China LFR2023008 PP725554 This study
2 A. sheni Lianyuan, Hunan, China LFR2023009 PP725555 This study
3 A. sheni Lianyuan, Hunan, China LFR2023010 PP725556 This study
4 A. sheni Lianyuan, Hunan, China LFR2024015 PP725559 This study
5 A. sheni Lianyuan, Hunan, China ANU20230012 OR178145 Ma et al. 2023a
6 A. sheni Lianyuan, Hunan, China ANU20230013 OR178146 Ma et al. 2023a
7 A. yunkaiensis Dawuling Forestry Station, Guangdong, China SYS r001443 MN380329 Wang et al. 2019
8 A. yunkaiensis Dawuling Forestry Station, Guangdong, China SYS r001502 MN380330 Wang et al. 2019
9 A. yunkaiensis Maoershan Nature Reserve, Guangxi, China YBU 14612 MT365525 Yu et al. 2020
10 A. yunkaiensis Xinning, Hunan, China CIB 119041 OQ978852 Ma et al. 2023b
11 A. ater Huaping Nature Reserve, Guangxi, China SYS r00852 MN380334 Wang et al. 2019
12 A. dabieshanensis Yaoluoping Nature Reserve, Anhui, China AHU2018EE0710 MW316598 Zhang et al. 2023
13 A. damingensis Nanning, Guangxi, China ANU20220009 OP644487 Yang et al. 2023
14 A. dehuaensis Dehua, Fujian, China YBU 13013 MZ442662 Li et al. 2021
15 A. emilyae Hoanh Bo, Vietnam IEBR 4465 MK330857 Ziegler et al. 2019
16 A. formosanus Taiwan, China RN2002 KU529452 Unpublished
17 A. hunanensis Huaihua, Hunan, China CIB 119039 OQ848425 Ma et al. 2023c
18 A. huangjietangi Huangshan, Anhui, China HSR18030 MT380191 Huang et al. 2020
19 A. juliani Ha Lang, Cao Bang, Vietnam IEBR A.2018.8 MK330854 Ziegler et al. 2019
20 A. meiguensis Mianyang, Sichuan, China GP835 MZ442641 Li et al, 2021
21 A. nanshanensis Huaihua, Hunan Province, China HNNU230901 OR523368 Li et al. 2024
22 A. niger Taiwan, China RN0667 KU529433 Unpublished
23 A. ningshanensis Ningshan, Shaanxi, China ANU 20220006 ON548422 Yang et al. 2022
24 A. panzhihuaensis Yanbian, Sichuan, China KIZ 040189 MW664862 Hou et al. 2021
25 A. pingbianensis Honghe, Yunnan, China YBU 18273 MT365521 Li et al. 2020b
26 A. quangi Phu Yen, Son La, Vietnam ZVNU.2022.08 OQ197471 Pham et al. 2023
27 A. rufescens Hongkong, China SYS r001866 MN380339 Wang et al. 2019
28 A. sp1 Ningshan, Shaanxi, China LFR2023038 PP725557 This study
29 A. sp1 Ningshan, Shaanxi, China LFR2023039 PP725558 This study
30 A. sp2 Taibai, Shaanxi, China CHS007 MK064591 Li et al. 2020a
31 A. spinalis Badagong Mountains, Hunan, China SYS r001327 MN380340 Wang et al. 2019
32 A. timi Thuan Chau, Son La, Vietnam IEBR A.2018.10 MK330856 Ziegler et al. 2019
33 A. tranganensis Ninh Binh, Vietnam VNUF R.2018.21 MW023086 Luu et al. 2020
34 A. vanhoensis Van Ho, Son La, Vietnam VNUF R.2019.13 ON677935 Ha et al. 2022
35 A. yangdatongi Wenshan Nature Reserve, Yunnan, China KIZ 034327 MW664865 Hou et al. 2021
36 A. zugorum Bac Me, Ha Giang, Vietnam IEBR 4698 MT502775 Miller et al. 2020
Out group
37 Fimbrios klossi Quang Ngai, Vietnam IEBR 3275 KP410744 Teynié et al. 2015
38 Parafimbrios lao Louangphabang, Laos MNHN 2013.1002 KP410746 Teynié et al. 2015
39 Stoliczkia vanhnuailianai Mizoram, India BNHS 3656 OL422476 Deepak et al. 2021

Except for the newly generated sequence, 32 sequences of 25 recognized species and one unnamed of genus Achalinus, and three outgroups (selected as Ma et al. 2023a): Fimbrios klossi Smith, 1921, Parafimbrios lao Teynié, David, Lottier, Le, Vidal & Nguyen, 2015, and Stoliczkia vanhnuailianai Lalronunga, Lalhmangaiha, Zosangliana, Lalhmingliani, Gower, Das & Deepak, 2021 were downloaded from the National Center for Biotechnology Information (NCBI) (Accession numbers listed in Table 1). The CO1 sequences (624 bp) were input in MEGA X software (Kumar et al. 2018) and aligned by MUSCLE (Edgar 2004). Maximum likelihood (ML) was used to infer tree structure with IQ-TREE v. 1.6.12 (Nguyen et al. 2015). The best-fit model, TN+F+I+G4, was inferred using a Bayesian Information Criterion (BIC) with the program ModelFinder (Kalyaanamoorthy et al. 2017). Ultrafast Bootstrap Approximation (UFB) node support was assessed by using 5000 ultrafast bootstrap replicates, and SH-like approximate likelihood ratio test (SH-aLRT) was conducted to the single branch tests by 1000 replicates. In addition, we calculated the uncorrected pairwise distances (p-distances) using the MEGA X software (Kumar et al. 2018).

Results

The phylogeny inferred using the mitochondrial fragment CO1 (624 bp) demonstrated that the newly collected specimens from Yangshi Town, Hunan Province, China were clustered together with selected A. sheni type series (SH 100 / UFB 100) (Fig. 1). We also show that intraspecific generic divergence ranged from 0.0%–0.8% was detected (Table 2), which is less than the minimum interspecific uncorrected p-distance among other recognized species of Achalinus, indicating that the newly collected Achalinus specimens should be identified as A. sheni.

Table 2.
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Uncorrected p-distances (%) among the Achalinus species based on partial mitochondrial CO1 gene for species compared in this study.

ID Species 1–6 7 8 9 10 11 12 13 14 15 16 17 18 19–20 21 22 23 24 25 26 27 28 29 30 31 32–35
1–6 A. sheni 0–0.8
7 A. ater 13.1–13.4 –
8 A. dabieshanensis 15.3–15.9 14.8 –
9 A. damingensis 13.3–13.6 7.4 15.9 –
10 A. dehuaensis 13.8 16.1 18.6 15.2 –
11 A. emilyae 13.6–14.2 11.2 18.0 12.9 15.3 –
12 A. formosanus 12.7–12.9 13.3 18.8 14.2 15.7 13.6 –
13 A. huangjietangi 12.9 13.1 11.0 15.2 15.3 15.5 16.1 –
14 A. hunanensis 12.7–13.1 7.6 17.0 5.7 15.3 13.8 13.6 15.0 –
15 A. juliani 13.6–14.0 6.6 15.9 8.3 14.8 12.9 11.4 14.4 9.1 –
16 A. meiguensis 14.2–14.8 15.3 18.0 16.5 18.4 15.3 15.5 16.9 16.3 16.7 –
17 A. niger 12.9–13.1 12.9 16.1 13.3 16.3 12.7 8.5 15.7 13.3 11.7 13.8 –
18 A. ningshanensis 13.6–14.0 7.4 17.2 7.4 15.5 13.8 14.2 15.5 3.4 9.5 16.9 14.0 –
19–20 A. sp1 9.8–10.4 12.7–12.9 14.4–14.6 11.9–12.1 13.8–14.0 12.9–13.1 12.7–12.9 13.6–13.8 13.1–13.3 12.1–12.3 15.0–15.2 9.8–10.0 13.8–14.0 0.2
21 A. nanshanensis 13.6–14.0 6.8 16.1 5.1 13.4 13.3 13.6 14.6 4.9 8.1 17.6 12.1 5.7 12.5–12.7 –
22 A. panzhihuaensis 14.8 16.5 16.5 15.5 15.5 16.5 16.1 15.7 16.5 15.7 11.4 14.0 17.4 14.4–14.6 15.3 –
23 A. pingbianensis 11.2 11.0 15.3 10.2 14.6 13.1 14.2 14.0 11.0 11.6 16.7 11.9 11.6 10.0–10.2 11.0 14.8 –
24 A. quangi 14.2–14.8 11.4 18.4 12.7 15.5 2.8 13.6 15.9 13.6 12.5 15.2 12.1 13.1 12.3–12.5 12.7 16.9 13.6 –
25 A. rufescens 13.1 11.7 15.9 12.1 12.9 9.7 13.8 14.6 11.7 11.2 18.6 13.8 11.9 13.4–13.6 11.4 15.9 12.7 10.0 –
26 A. spinalis 11.7–12.3 14.6 16.5 14.6 14.2 14.4 14.2 14.4 14.0 14.0 15.9 13.8 15.2 8.9–9.1 14.4 16.1 13.3 13.6 12.7 –
27 A. sp2 11.0 14.0 14.8 13.4 15.3 13.3 14.2 13.6 15.0 13.8 15.7 11.9 15.7 3.2–3.4 13.8 15.5 12.3 13.1 14.8 10.4 –
28 A. timi 13.3–13.6 12.7 16.5 12.5 15.0 12.9 13.3 15.9 12.1 13.4 15.9 11.6 12.9 11.4–11.6 13.1 15.3 11.9 12.5 14.0 14.0 12.9 –
29 A. tranganensis 14.2–14.6 12.5 15.3 13.8 14.0 12.3 16.9 13.4 14.8 14.2 16.3 14.6 15.0 13.1–13.3 13.4 16.5 13.4 11.7 12.7 15.5 13.6 13.4 –
30 A. vanhoensis 12.7–13.1 11.9 15.5 11.7 14.8 11.7 13.6 15.2 11.4 12.7 15.7 11.7 11.7 11.2–11.4 11.9 15.3 10.6 11.6 12.9 12.3 12.7 4.5 11.9 –
31 A. yangdatongi 14.0–14.4 6.4 16.7 5.7 14.4 12.7 14.2 14.8 5.1 7.6 17.2 13.4 5.9 12.1–12.3 4.5 15.7 10.8 12.5 11.6 14.2 13.6 12.7 12.9 10.8 –
32–35 A. yunkaiensis 6.4–7.2 11.9–12.9 15.0–15.9 12.3–12.9 14.4–14.8 12.7–13.1 11.9–12.5 14.0–14.2 11.7–12.3 12.3–12.9 15.3–15.9 10.4–11.9 12.7–13.3 9.3–10.0 11.6–12.5 15.7–16.1 10.8–11.4 12.7–13.6 12.1–13.4 11.7–11.9 10.0–11.0 12.7–13.3 13.1–14.0 11.7–12.3 12.3–12.5 0.0–3.0
36 A. zugorum 10.4 13.3 15.3 12.3 14.2 12.9 13.4 15.0 12.1 13.3 15.0 13.1 12.5 11.6–11.7 12.7 15.2 10.2 13.1 13.8 13.4 13.6 13.4 11.7 11.7 12.1 10.4–11.9
Figure 1. 

Maximum-likelihood tree of the genus Achalinus inferred from the CO1 gene fragment. The nodes supporting values on branches are presented as SH-like approximate likelihood ratio test (SH) / Ultrafast Bootstrap Approximation (UFB), the ones lower than 50 are displayed as “–”.

Taxonomic account

Reptilia

Serpentes

Xenodermidae

Achalinus

Achalinus sheni Ma, Xu, Qi, Wang, Tang, Huang & Jiang, 2023

Figs 2, 3, 4, 5, 6 Common name: Shen’s Odd-scale Snake / Shěn Shì Jǐ Shé (沈氏脊蛇)

Specimens examined

Three typical specimens: LFR2023008 (adult female), LFR2023009 (adult male), LFR2023010 (adult female); and one albinistic specimen: LFR2024015 (adult female), collected in July, 2023 from Yangshi Town, Lianyuan City, Loudi City, Hunan Province (27°32'07.08"N, 111°48'31.68"W, 370 m a. s. l.) ; coll. by Shu Li and Ziyuan Feng.

Description of the albinistic specimen

Measurements and scalation. An adult female specimen (field number LFR2024015) with SVL 354 mm (TL 416 mm and TAL 62 mm); tail relatively short, TAl/TL ratio 0.149; body slender and cylindrical; head slightly distinct from the neck; HW 5.8 mm; HL 10.8 mm; eye small; ED 1.1 mm; rostrum small, triangular, slightly visible from above; length of the suture between the internasals (LSBI 1.25 mm) subequal to the length of the suture between the prefrontals (LSBP 1.32 mm), LSBI/LSBP ratio 0.95; nostril in the anterior part of the nasal; prefrontals paired; frontal single, pentagonal, pointing to the rear, the width and length close; loreal one, subrectangular, LorL 1.6 mm, LorH 0.9 mm, LorH/LorL ratio 0.56; supraocular one, pentagonal, SPOL 1.9 mm; TEMP 7/8, arranged in three rows (2+1+4 in left and 2+2+4 in right), the anterior two contact the eye, ATUL 1.7 mm, SPOL/ATUL ratio 1.1; SL 6, the 4th–5th contact the eye, the last one much elongated; two pairs of chin shields, the anterior pairs longer than the posterior pairs, followed by preventrals; one mental; IL 5, the first one contact with each other after the mental and before the 1st chin-shields, 1st–3rd touch the first pair of chin-shields.

Dorsal scales strongly keeled, lanceolate, 23 rows throughout the body, the outmost row smooth and significantly enlarged. VS 164; anal entire; SC 46, not paired.

Coloration. The comparison of color pattern between the albinistic specimen and the typical specimen are shown in Fig. 4. In life, dorsum (head, body, and tail) predominantly pastel yellow or paster orange owning to the lack of melanophoric pigments, and the iridescence on the body surface also disappears. Head scales in dorsal view same as dorsum, interstitial skin of dorsal and sutures of head scales milk star white. The iris was blood-red, with a reddish pupil. Supralabials, mental, and infralabials were pastel orange. The ventral ground color of body and tail were milk star white, darker on both sides than in the middle, and with free margins of ventral scales and subcaudals almost transparent with a slight hint of pastel orange (Figs 2, 3).

Figure 2. 

Adult female albinistic specimen of Achalinus sheni in life (LFR2024015) A dorsal view B ventral view. Photos by Yu-Hao Xu.

Figure 3. 

Close-up view of the adult female albinistic specimen of Achalinus sheni in life (LFR2024015) A dorsal view of the head B ventral view of the head C right view of the head D left view of the head E lateral view of the middle body F venter view of the middle body. Photos by Yu-Hao Xu.

Figure 4. 

Comparisons between the albinistic specimen and typical specimen of Achalinus sheni in life A1–A2 LFR2024015 B1–B2 LFR2023010 A1, B1 dorsal view A2, B2 ventral view. Photos by Yu-Hao Xu.

Expanded description of the females

Measurements and scalation data of the newly collected specimens (1 male and 3 females) are presented in Table 3. Based on three newly collected female specimens (field number: LFR2023008, LFR2023010, LFR2024015), an expanded description of the females is provided as below.

Table 3.
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Morphological variation characters in the newly collected Achalinus sheni specimens.

Voucher number LFR2023008 LFR2023009 LFR2023010 LFR2024015
Sex ♀ ♂ ♀ ♀
SVL 341 257 298 354
TL 408 324 355 416
TAL 67 67 57 62
TAL/TL 0.164 0.207 0.160 0.149
HL 11.4 9.6 11.5 10.8
HW 6.6 5.1 5.5 5.8
SL 3+2+1 3+2+1 3+2+1 3+2+1
IL 5/5 5/5 5/5 5/5
Chin 2 2 2 2
IFL–1stChin 1th–3rd 1th–3rd 1th–3rd 1th–3rd
Lor 1 1 1 1
LorH 1.2 1.0 1.3 0.9
LorL 1.7 1.6 1.7 1.6
LorH/LorL 0.71 0.63 0.76 0.56
LSBI 1.8 1.3 1.5 1.23
LSBP 1.6 1.1 1.6 1.32
LSBI/LSBP = = = =
ED 1.1 0.9 1.1 1.1
PrO 0 0 0 0
PO 0 0 0 0
TEMP 2+2+3/2+2+3 2+2+3/2+2+4 2+2+3/2+2+3 2+1+4/2+2+4
ATUL 1.7 1.3 1.7 1.7
SPO 1 1 1 1
SPOL 1.6 1.3 1.6 1.9
SPOL/ATUL 0.94 1.00 0.94 1.12
DSR 23-23-23 23-23-23 23-23-23 23-23-23
VS 172 167 172 174
CP entire entire entire entire
SC 49 59 47 46

Measurements and scalation. Tail relatively short, TAL/TL ratio 0.149–0.164; body slender and cylindrical, the maximal TL 416 mm with SVL 354 mm and TAL 62 mm; head relatively narrow, slightly distinct from the neck, HL 10.8–11.5 mm; HW 5.5–6.6 mm; rostrum small, triangular, slightly visible from above; eye small, pupil round, ED 1.1 mm; LSBI subequal to LSBP; nostril in the anterior part of the nasal; prefrontals 2, elongated; frontal 1, pentagonal, pointing to the rear, the width and length close; loreal one, subrectangular, LorL 1.6–1.7 mm, LorH 0.9–1.3 mm, LorH/LorL ratio 0.56–0.76; supraocular one, pentagonal, SPOL 1.6–1.9 mm; temporals long, arranged in three rows, TEMP 2+1+4, 2+2+3 or 2+2+4, the anterior two contact the eye, ATUL 1.7 mm, SPOL/ATUL ratio 0.94–1.12; SL 6, the 4th–5th contact the eye, the last one much elongated; two pairs of chin shields, the anterior pairs longer than the posterior pairs, followed by preventrals; one mental; IL 5, the first one contact with each other after the mental and before the 1st chin-shields, 1st–3rd touch the first pair of chin-shields.

Dorsal scales 23-23-23, lanceolate and strongly keeled, the outmost row smooth and significantly enlarged. VS 172–174; CP entire; SC 46–49, unpaired.

Coloration in life. In life, the dorsum (head, body, and tail) is predominantly brownish black and slightly tinged with iridescence. Head scales in dorsal view are the same as the dorsum, and with the middle darker than the sides. Dorsum brownish black and the five innermost dorsal scale rows a little darker, forming an inconspicuous longitudinal vertebral line. Eyes pure black. Mental, infralabials, and chin shields light grayish brown. Ventral ground color of body and tail generally light grey or light taupe and darker on the sides. The free margins of ventral scales are greyish white (Fig. 4).

Coloration in preservation. In preservation, coloration still resembles the specimen in life, except that the coloration of dorsum further deepening, and the background color of the venter becomes light brownish grey (Fig. 5).

Figure 5. 

Preserved specimen of the typical female specimen of A. sheni (LFR2023008). Photos by Yu-Hao Xu.

Variation

The female specimens have a similar color pattern as male specimens, but in measurement and scalation features, there is variation by sex: females have a relatively large body size (TL 355–408 mm vs 149–371 mm in male); a significantly short tail, TAL/TL ratio 0.149–0.164 (vs 0.183–0.224 in male) (Fig. 6); more ventral scales (172–174 vs 161–170 in male); and fewer subcaudals (46–49 vs 55–61 in male) (Table 4).

Table 4.
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Comparison of the key morphological characters between Achalinus sheni and A. yunkaiensis obtained from specimens examined in this study, Wang et al. (2019), and Ma et al. (2023a).

Sex A. sheni A. yunkaiensis
♂ ♀ ♂ ♀
N 6 3 4 3
SVL 122–292 298–354 189–359 204–386
TL 149–371 355–416 232–418 256–488(+)
TAL 27–80 57–67 43–63 52–73
TAL/TL 0.183–0.224 0.149–0.164 0.185–0.200 0.156–0.204
SL 3+2+1 3+2+1 3+2+1 3+2+1
IL 5 (rarely 6) 5 6 6
Chin 2 2 2 2
IFL–1stChin 1th–3rd 1th–3rd 1th–3rd 1th–3rd
Lor 1 1 1 1
LorH 0.7–1 0.9–1.3 0.8–1.3 0.7–1.2
LorL 1.3–1.7 1.6–1.7 1.3–2.2 1.5–2.2
LorH/LorL 0.53–0.93 0.56–0.76 0.56–0.64 0.49–0.55
LSBI vs LSBP = = = =
TEMP 2+2+3 2+2+3 or 2+2+4 or 2+1+4 2+2+3 or 2+2+4 2+2+3 or 2+2+4
ATUL 1.3–1.5 1.7 1.2–2.2 1.9–2.9
SPO 1 1 1 1
SPOL 1.1–1.6 1.6–1.9 1–1.6 1.3–1.6
SPOL/ATUL 0.99–1.16 0.94–1.12 0.66–0.83 0.55–0.65
DSR 23-23-23 23-23-23 23-23-23 23-23-23
VS 161–170 172–174 151–162 144–156
CP 1 1 1 1
SC 55–61 46–49 49–56 51–55
VS+SC 220–226 219–221 200–212 195–205
Figure 6. 

Comparisons of the tails between males and females of Achalinus sheni A1 specimen ANU20230013, paratype, adult male A2 specimen ANU20230012, paratype, adult male A3 specimen LFR2023009, adult male B1 specimen LFR2023010, adult female B2 specimen LFR2024015, adult female B3 specimen LFR2023008, adult female. Photos by Yu-Hao Xu.

Revision of diagnostic characters

(1) dorsal scales strongly keeled, 23 rows throughout the body, the outmost row smooth and significantly enlarged; (2) tail relatively short, TAL/TL ratio 0.183–0.224 in males, and 0.140–0.164 in females; (3) the suture between internasals subequal to the suture between prefrontals; (4) loreal one, subrectangular, LorH/LorL 0.53–0.76; (5) ventrals 161–170 in males and 172–174 in females; (6) cloacal plate entire; (7) subcaudals 55–61 in males and 46–49 in females, not paired; (8) the length of supraocular almost equal to the length of upper anterior temporal; (9) vertebral line inconspicuous and subcaudal streak absent.

Natural history notes

Achalinus sheni is currently known from Hunan Province, China: Lianyuan City, Nanyue District and Nanshan National Park, Shaoyang City (350–410 m a.s.l.). The known activity period of A. sheni is from March to October but activity peaks in early summer. The species usually prefers to hide under rocks, decaying wood, or fallen leaves, but it has sometimes been found on cement roads in the mountains after rain or on high-humidity nights. Through dissection, it was found that there were undigested earthworms in the intestine of specimen LFR2023009. Therefore, we speculate that A. sheni feeds mainlyon worms in the wild.

Discussion

The genus Achalinus is widely distributed in Vietnam, China, and Japan (Zhao et al. 1998; Zhao 2006), with 28 currently recognized species, and lately it has attracted much attention in scientific literature (Wang et al. 2019; Ziegler et al. 2019; Li et al. 2020b; Luu et al. 2020; Hou et al. 2021; Huang et al. 2021; Li et al. 2021; Ha et al. 2022; Yang et al. 2022; Ma et al. 2023a, 2023b, 2023c; Pham et al. 2023; Yang et al. 2023; Zhang et al. 2023; Li et al. 2024). However, no cases of albinism have been described to our knowledge. Therefore, this first report of albinism in A. sheni sheds light on this rare phenomenon in the genus and family.

Species of Achalinus typically exhibit a rainbow-colored iridescence on their body surface especially when exposed to sunlight or camera flash. However, when observing the albino individual, we found that the rainbow color on their body surface almost completely disappeared. It is currently unclear whether the lack of iridescence is entirely caused by the disappearance of melanin. In the future, we will further examine microstructure of albinism and examine the genetic underpinnings of this phenomenon.

In this study, we provide the first detailed description and photographs of the female of A. sheni and compare the morphological differences between males and females. We demonstrate intersexual differences such as the total length, the tail length, and the number of venter scales and subcaudals, which will help distinguish this species from other closely related species, especially its sister species A. yunkaiensis (Table 4), which is sympatric in distribution with A. sheni in the Nanshan National Park (Li et al. 2024).

Moreover, in this study, we provide two partial CO1 sequences of two Achalinus specimens from Ningshan County, Shaanxi Province, China, which cluster with the Taibai specimen (considered as Achalinus sp. by Yang et al. (2023)) (Table 1) with high support values (SH 97 / UFB 99) (Fig. 1). Interestingly, the uncorrected p-distance was 3.2–3.4%, indicating substantial genetic differences between the two populations, but further population genomic investigation is needed to properly understand biogeographic causes of this putative population structure. However, the morphological examination indicated that these two specimens from Ningshan County are consistent with the original descriptions of A. ningshanensis. Therefore, broad sampling of morphological and genomic data is required to better understand population or species structuring within A. ningshanensis.

Acknowledgements

We are very grateful to Shu Li and Ziyuan Feng for their help fieldwork.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

All sampling and procedures involving live snakes were performed in accordance with the Wild Animals Protection Law of the People’s Republic of China, approved by the Institutional Ethics Committee of Qinghai University (protocol code SL-2023028 and date of approval 15 March 2023).

Funding

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

Author contributions

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

Author ORCIDs

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

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

Data availability

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

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