Research Article
Print
Research Article
Revalidated after having been described more than a century ago: Calamaria berezowskii Günther, 1896 (Squamata, Colubridae) from Sichuan, Southwestern China
expand article infoYa-Ting Liang‡, Zi-Dan Huang‡, Li Ding§, Gernot Vogel|, Natalia B. Ananjeva, Nikolai L. Orlov, Sheng-Chao Shi#, Zheng-Jun Wu‡, Ze-Ning Chen‡
‡ Guangxi Normal University, Guilin, China
§ Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China
| Society for Southeast Asian Herpetology, Heidelberg, Germany
¶ Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia
# Jianghan University, Wuhan, China

Corresponding author: Natalia B. Ananjeva ( nananjeva09@gmail.com )

Corresponding author: Ze-Ning Chen ( chenzn@gxnu.edu.cn )

Academic editor: Justin Bernstein
© 2024 Ya-Ting Liang, Zi-Dan Huang, Li Ding, Gernot Vogel, Natalia B. Ananjeva, Nikolai L. Orlov, Sheng-Chao Shi, Zheng-Jun Wu, Ze-Ning Chen.
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: Liang Y-T, Huang Z-D, Ding L, Vogel G, Ananjeva NB, Orlov NL, Shi S-C, Wu Z-J, Chen Z-N (2024) Revalidated after having been described more than a century ago: Calamaria berezowskii Günther, 1896 (Squamata, Colubridae) from Sichuan, Southwestern China. Zoosystematics and Evolution 100(3): 897-911. https://doi.org/10.3897/zse.100.125798
ZooBank: urn:lsid:zoobank.org:pub:453CA1DC-07E7-40E8-9979-243C9B948373
Open Access

Abstract

The reed snakes of the genus Calamaria Boie, 1827 are one of the largest groups of Asian snakes, distributed from northeast India to the Maluku Islands of east Indonesia. Recent research on the genus in China has revealed that the species diversity of the group was underestimated. In this study, morphological comparisons and mitochondrial DNA analysis revealed that a junior synonym of C. pavimentata Duméril, Bibron & Duméril, 1854 — Calamaria berezowskii Günther, 1896 is valid, hence we redescribed and recovered the validity of C. berezowskii. This species can be distinguished from other congeners by the combination of the following characters: four supralabials; one preocular; rostral shield width larger than height; mental not touching anterior chin shields; eye diameter less than the distance from eye to mouth edge; less than 1/2 of the posterior chin shield meets in the midline; dorsal scales reduced to six rows at tail; indistinct light ring present in the nuchal region or a more or less distinct yellowish collar. Phylogenetically, this species is sister to C. pavimentata, with significant genetic differences (0.190) on mitochondrial gene Cyt b.

Key Words

Calamaria berezowskii, Colubridae, morphology, phylogenetics, taxonomy

Introduction

Calamaria Boie, 1827 is the largest group of the colubrid subfamily Calamariinae (Reed Snakes), containing more than 68 species (Uetz et al. 2023). In mainland Southeast Asia and China, 20 species of Calamaria are known at present, including C. lumbricoidea Boie, 1827; C. albiventer (Gray, 1834); C. schlegeli Duméril, Bibron & Duméril, 1854; C. pavimentata Duméril, Bibron & Duméril, 1854; C. lovii Boulenger, 1887; C. septentrionalis Boulenger, 1890; C. prakkei Lidth De Jeude, 1893; C. buchi Marx & Inger, 1955; C. yunnanensis Chernov, 1962 (Yeung et al. 2022; Uetz et al. 2023); C. thanhi Ziegler & Quyet, 2005; C. gialaiensis Ziegler, Nguyen & Nguyen, 2009; C. sangi Nguyen, Koch et Ziegler, 2009; C. abramovi Orlov, 2009; C. concolor Orlov, Nguyen, Nguyen, Ananjeva & Ho, 2010; C. andersoni Yang & Zheng, 2018; C. dominici Ziegler, Tran & Nguyen, 2019; C. strigiventris Poyarkov, Nguyen, Orlov & Vogel, 2019; C. nebulosa Lee, 2021; C. arcana Yeung, Lau & Yang, 2022; C. jinggangensis Cai, Jiang, Wu, Huang, Fei & Ding, 2023.

There were only three species of genus Calamaria recorded in China 26 years ago: C. pavimentata, C. septentrionalis and C. yunnanensis (Zhao et al. 1998). Recently, three more species were described: C. andersoni, C. arcana, C. jinggangensis (Yang and Zheng 2018; Yeung et al. 2022; Cai et al. 2023; Uetz et al. 2023). The species diversity of the genus in China is suggested to be underestimated, and those widely distributed species should be re-evaluated. For example, the widely recorded species C. pavimentata has a synonym, C. berezowskii Günther 1896, which was described based on two specimens from Lun-ngan-fu (龙安府 Long’an Fu, now 龙安镇 Long’an Town of 平武县 Pingwu County) of Sze-chuen (Sichuan Province of China) (Günther 1896).

During the scientific expeditions in the Gongga Mountains, Luding County, Sichuan Province, between 2017 and 2022, we collected three Calamaria specimens. Morphological and molecular phylogenetic analyses showed that these specimens represent a species that differs from all currently recognized congeners of the genus. However, the morphology of these specimens matches the original description of C. berezowskii. Besides, Luding County and Pingwu County both are located on the eastern slope of Qinghai-Tibet Plateau bordering the Sichuan Basin. Therefore, we identify the specimens as C. berezowskii, and the species is revalidated and redescribed here.

Materials and methods

Sampling

Three specimens of Calamaria were collected from eastern slope of Mt. Gongga, Moxi Town, Luding County, Ganzi Tibetan Autonomous Prefecture, Sichuan Province, China during 2017 to 2022 (Fig. 1). One adult female GXNU DLR195 (29.645105°N, 102.111076°E, 1736 m a.s.l.), one adult male GXNU DLR194 (29.615872°N, 102.109208°E, 1680 m a.s.l.), one juvenile female GXNU 20221215002 (29.641749°N, 102.110340°E, 1827 m a.s.l.), collected by Xu Zhang on 31 August 2018, Li Ding on 21 August 2017 and Congcong Du on 15 December 2022. The three specimens were fixed and stored in 80% ethanol and deposited at the School of Life Sciences, Guangxi Normal University.

Figure 1. 

Distribution map of Calamaria berezowskii. Red star indicates the type locality, purple triangle indicates the distribution found in this study.

Molecular phylogenetic analysis

Genomic DNA was extracted from muscle or liver tissue taken from the collected specimens using the TIANamp Marine Animals DNA Kit (TIANGEN Biotech). We sequenced a fragment of the mitochondrial gene cytochrome b (Cyt b) using the primer pair L14910/H16064 (Burbrink et al. 2000). PCR amplification was performed in 25 μl reactions containing 12.5 μl 2× SanTaq PCR Master Mix (with Blue Dye), 10 μl ddH2O, 1 μl F-primers, 1 μl R-primers and 0.5 μl DNA template. The PCR conditions were an initial denaturing step at 94 °C for 5 min, followed by 35 cycles: denaturing at 94 °C for 30 s, annealing at 48.5 °C for 45 s, an extension step at 72 °C for 35 s; and a final extension of 72 °C for 10 min. Finally, the PCR products were sent to Sangon Biotechnologies Co., Ltd. (Shanghai, China), where the purified PCR products were sequenced using the same forward and reverse primers. Sequences for comparison of available species were downloaded from GenBank (Table 1).

Table 1.
Download as
CSV
XLSX

DNA sequences used in this study.

No. Taxa Voucher Locality Cyt b Reference
1 C. septentrionalis HSR19100 Mt. Huangshan, Anhui, China OQ354842 Cai et al. 2023
2 C. septentrionalis HS11145 Mt. Nanling, Guangdong, China OQ354840 Cai et al. 2023
3 C. septentrionalis DL2021610-1 Huangsha, Guangxi, China OQ354838 Cai et al. 2023
4 C. septentrionalis KFBG14506 Hainan Island, China MH445956 Yang and Zheng 2018
5 C. septentrionalis ROM35605 Nguyên Bình, CaoBang, Vietnam AF471081 Lawson et al. 2005
6 C. septentrionalis ROM35597 Cao Bang, Vietnam KX694890 Alencar et al. 2016
7 C. pavimentata KFBG14507 Ningming, Guangxi, China MH445957 Yang and Zheng 2018
8 C. andersoni HSR20101 Dehong, Yunnan, China OQ354844 Cai et al. 2023
9 C. andersoni HSR20181 Tengchong, Yunnan, China OQ354845 Cai et al. 2023
10 C. andersoni SYSr001699 Yingjiang, Yunnan, China MH445955 Yang and Zheng 2018
11 C. yunnanensis ROM41547 Simao, Yunnan, China KX694891 Zaher et al. 2009
12 C. yunnanensis YPx503 Unknown JQ598922 Grazziotin et al. 2012
13 C. arcana HS17082 Mt. Dawu, Guangdong, China OQ354835 Cai et al. 2023
14 C. arcana KFBG14611 Mt. Dadongshan, Guangdong, China ON482335 Yeung et al. 2022
15 C. arcana GP9975 Yongxing, Hunan, China OP980549 Cai et al. 2023
16 C. arcana DLR199 Mt. Wuyi, Fujian, China OQ354834 Cai et al. 2023
17 C. jinggangensis DL20200725 Mt. Jinggangshan, Jiangxi, China OQ354830 Cai et al. 2023
18 C. jinggangensis DL20200625-2 Mt. Jinggangshan, Jiangxi, China OQ354831 Cai et al. 2023
19 C. jinggangensis DL20200625-3 Mt. Jinggangshan, Jiangxi, China OQ354832 Cai et al. 2023
20 C. jinggangensis DL20200625-4 Mt. Jinggangshan, Jiangxi, China OQ354833 Cai et al. 2023
21 C. muelleri RMB1283 Gowa, South Sulawesi, Indonesia MT819391 Weinell et al. 2021
22 C. muelleri TNHC58955 Gowa, South Sulawesi, Indonesia MT819390 Weinell et al. 2021
23 C. lumbricoidea USMHC1560 Penang, Peninsular, Malaysia MN338526 Quah et al. 2019
24 C. palavanensis KU311411 Mt. Mantalingahan, Palawan, Philippine MT819387 Weinell et al. 2021
25 C. palavanensis KU309445 Barangay Irawan, Palawan, Philippine MT819386 Weinell et al. 2021
26 C. gervaisii KU334485 Municipality, Ilocos Sur, Philippines MT819385 Weinell et al. 2021
27 C. gervaisii KU324661 Puguis, Benguet, Philippines MT819384 Weinell et al. 2021
28 C. schlegeli LSUHC10278 Perak, Peninsular, Malaysia MN338525 Quah et al. 2019
29 C. nebulosa FMNH258666 Phongsaly, Laos MN338524 Quah et al. 2019
30 C. berezowskii GXNU DLR194 Mt. Gongga, Sichuan, China PP747047 This study
31 C. berezowskii GXNU DLR195 Mt. Gongga, Sichuan, China PP747048 This study
32 C. berezowskii GXNU 20221215002 Mt. Gongga, Sichuan, China PP747049 This study
33 Elaphe quatuorlineata LSUMZ40626 Turkey, European Turkey AY486931 Nagy et al. 2004
34 Lycodon rufozonatus LSUMZ44977 Unknown AF471063 Lawson et al. 2005
35 Orientocoluber spinalis MVZ211019 Yinnan, Ningxia, China AY486924 Nagy et al. 2004

We evaluated and manually corrected the sequencing peak maps of the three sequences obtained, downloaded 29 Cyt b sequences of 12 species of the genus Calamaria that have been reported in Southeast Asia and China in GenBank, and selected three species Elaphe quatuorlineata, Lycodon rufozonatus and Orientocoluber spinalis as outgroups (Yang and Zheng 2018; Yeung et al. 2022), for a total of 35 sequences to be used for multiple sequence comparisons. All sequences were aligned with other retrieved sequences in the same gene loci by using software MEGA 11 (Kumar et al. 2018). Phylogenetic trees were constructed based on mitochondrial gene Cyt b using maximum likelihood (ML) and Bayesian inference (BI). Maximum likelihood analysis was conducted in RAxML v8.2.4 (Stamatakis 2014). Confidence intervals were determined with 1000 bootstrap replicates utilizing the rapid bootstrap option under the GTR+GAMMA substitution model. Bayesian inference analysis was conducted in MrBayes 3.2 (Ronquist et al. 2012). PartitionFinder 2.1.1 software was used to select the most suitable nucleotide substitution models for Cyt b sequence data based on the Bayesian information criterion (BIC): GTR+G, HKY+G and GTR+G (Lanfear et al. 2012; Lanfear et al. 2017). We ran our analyses for 20 million generations with the chains, sampling every 1000 generations using the Markov Chain Monte Carlo (MCMC). After removing outgroup taxa, MEGA11 (Kumar et al. 2018) was used to calculate uncorrected pairwise sequence divergence between the Calamaria species.

Morphological analysis

Terminology and descriptions follow the views of Inger and Marx (1965) and Ziegler et al. (2008). Body and tail length were measured with a tape ruler to the nearest 1 mm: total length (TL), from the tip of snout to the tip of tail ; snout-vent length (SVL), from the tip of snout to posterior margin of cloaca ; tail length (TaL), from posterior margin of cloaca to the tip of tail. Other measurements were conducted with a digital caliper to the nearest 0.1 mm: head length (HL), from the snout tip to the posterior margin of the mandible ; head width (HW), measured at the widest part of the head on posterior side ; head height (HH), at the maximal highest part of the head ; the eye horizontal diameter (EyeD) ; and eye-mouth distance (Eye–Mouth D), measured from the anterior point of the eye to the mouth gap. Ventral scales (VEN) were counted according to Dowling (1951). The enlarged shield(s) anterior to the first ventral were regarded as preventral(s). The number of dorsal scale rows (DSR) are given at one head length behind head, at midbody, and at one head length before vent, respectively. The tail tip was not included in the number of subcaudal scales (SC). Sex was determined by examining the presence or absence of hemipenis.

Type specimen (lectotype ZISP 8823) was examined for morphological comparisons. Relevant morphological data of other Calamaria species were obtained from examined specimens (Appendix 1) and literatures.

Institution acronyms

FMNH: Field Museum of Natural History, Chicago. GXNU: Guangxi Normal University. KFBG: Kadoorie Farm and Botanic Garden. KU: University of Kansas Biodiversity Institute. LSUHC: La Sierra University Herpetological Collections. LSUMZ: Louisiana State University Museum of Natural Science. MVZ: Museum of Vertebrate Zoology. RMB: Rafe M. Brown field tag (specimen deposited in Museum Zoologicum Bogoriense, Indonesia). ROM: Royal Ontario Museum, Canada. SYS: BBiological Museum of Sun Yat-sen University, Guangzhou, China. TNHC: Texas Natural History Collections. USMHC: Universiti Sains Malaysia Herpetological Collection, Malaysia. ZFMK: Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany. ZISP: Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia.

Molecular results

The DNA dataset contains 35 samples with a total of 1105 base pairs. The phylogenetic topologies that resulted from Bayesian Inference (BI) and Maximum likelihood analysis (ML) are generally consistent in phylogenetic structure (Fig. 2). Phylogenetically, the species Calamaria from Mt. Gongga strongly clustered into a single lineage with high nodal support (Fig. 2, BPP 1.00 / UFB 100). Subsequently, it clustered with C. pavimentata KFBG14507 from Ningming, Guangxi (BPP 0.96 / UFB 94), and was clustered into the same clade with C. arcana, C. jinggangensis, C. septentrionalis, C. pavimentata, C. andersoni and C. yunnanensis.

Figure 2. 

Phylogenetic relationships of Calamaria species based on Cyt b. Bayesian posterior probabilities (BPP) and Ultrafast bootstrap approximation (UFB) were denoted beside each node (those lower than 75/0.7 were denoted as “-”).

The uncorrected pairwise p-distances of Cyt b sequences between the specimen of Mt. Gongga and the other 12 congeners included in the study were 17.1–31.2%, with the minimum value observed in the comparison with sequences of C. arcana (P = 17.1%) (Table 2). This divergence is clearly among interspecies level since these levels of divergences are distinctly higher than those observed between two other well distinguished species of C. andersoni and C. yunnanensis (P = 12.2–12.6%). The Calamaria specimens from Mt. Gongga, Luding, Sichuan represent an evolutionary distinct lineage.

Table 2.
Download as
CSV
XLSX

Uncorrected p-distances between Calamaria species based on 1105 base pairs from the mitochondrial genes Cyt b. The serial numbers in Table 2 are consistent with those in Table 1.

No. Taxa 1–6 7 8–10 11–12 13–16 17–20 21–22 23 24–25 26–27 28 29 30–32
1–6 C. septentrionalis 0.000–0.038
7 C. pavimentata 0.174–0.194
8–10 C. andersoni 0.130–0.148 0.246 0–0.019
11–12 C. yunnanensis 0.159–0.164 0.237 0.122–0.126 0.000
13–16 C. arcana 0.090–0.116 0.179–0.199 0.181–0.206 0.183–0.209 0.007–0.034
17–20 C. jinggangensis 0.095–0.103 0.180 0.161–0.171 0.158 0.062–0.074 0.000
21–22 C. muelleri 0.202–0.223 0.266 0.228–0.238 0.261–0.273 0.178–0.198 0.169–0.178 0.007
23 C. lumbricoidea 0.243–0.248 0.258 0.244–0.256 0.251 0.228–0.239 0.228 0.164
24–25 C. palavanensis 0.187–0.222 0.231–0.242 0.227–0.243 0.254–0.266 0.207–0.229 0.173–0.192 0.167–0.182 0.166–0.181 0.022
26–27 C. gervaisii 0.178–0.207 0.243–0.258 0.202–0.212 0.243–0.244 0.197–0.223 0.159–0.163 0.173–0.183 0.197–0.223 0.112–0.174 0.100
28 C. schlegeli 0.232–0.243 0.263 0.258 0.271 0.217–0.228 0.217 0.182–0.192 0.205 0.170–0.175 0.186–0.218
29 C. nebulosa 0.186–0.196 0.214 0.172 0.173 0.162–0.182 0.176 0.208–0.219 0.193 0.202–0.207 0.187–0.234 0.197
30–32 C. berezowskii 0.187–0.203 0.190 0.216–0.226 0.208 0.171–0.200 0.202 0.223–0.234 0.255 0.254–0.277 0.254–0.271 0.312 0.176 0.000

Morphological results

Morphology of the three Calamaria specimens from Luding County, Sichuan province matches the original description of C. berezowskii Günther 1896 and the morphological characters of lectotype ZISP 8823 (Figs 3, 4, 5, 6). They share the following characters: one preocular and one postocular; presence of a more or less distinct yellowish collar; similar number of ventral scales (149–165 vs 155–167) and subcaudal scales (16–25 vs 14–22); presence of a faint dark line on each side of the back; tail blunt and conical at the end. Besides, Luding County and the type locality Pingwu County are both located on the eastern slope of Qinghai-Tibet Plateau bordering the Sichuan Basin, with a geographic distance of about 350 km (Fig. 1). Hence, the Luding specimens were identified as conspecific with C. berezowskii.

Figure 3. 

Calamaria berezowskii (GNXU DLR195): A. Dorsal head; B. Ventral head; C. Right view of head; D. Left view of head; E. Dorsal middle body; F. Lateral middle body; G. Dorsal tail; H. Ventral tail; I. Dorsal view; J. Ventral view.

Figure 4. 

Calamaria berezowskii (GXNU DLR194) in life.

Figure 5. 

Lectotype ZISP 8823 of Calamaria berezowskii: A. Right view of head; B. Left view of head; C. Dorsal view; D. Ventral view.

Figure 6. 

Original description of Calamaria berezowskii Günther, 1896: A. Drawing; B. Description.

Morphological comparisons based on some characters between Calamaria berezowskii and other known species of the genus from mainland Southeast Asia and China were listed in Table 3. It can be distinguished by a combination of the following characters: four supralabials; preocular present; rostral shield width greater than height; mental not touching anterior chin shields; eye diameter less than distance from eye to mouth edge; less than 1/2 of the posterior chin shield meets in the midline; dorsal scales reduced to six rows at tail; presence of indistinct light rings in the nuchal region or a more or less distinct yellowish collar; and the two outermost dorsal scale rows light khaki, with upper margins partly dark pigmented.

Table 3.
Download as
CSV
XLSX

Morphological comparisons of species of Calamaria from mainland Southeast Asia and China. “1+***” indicates preventrals + ventrals. Entries marked with ‘–’ are not available.

Species Comparison between rostral height and width Comparison between eye diameter and eye-mouth distance Number of scales surrounding paraparietal Preocular: present (1) or absent (0) Supralabials Mental touching (1) or separated from (0) anterior chin shields Posterior chin shields meeting in midline (1), diverging or meeting only in anteriorly (0) End of tail Modified maxillary teeth Ventrals Subcaudals Dorsal scales reducing to four rows above position of subcaudal on tail Total length TaL / TL ratio (given as %) Coloration of dorsum Coloration of venter Dorsal scales with light spots present (1) or absent (0) Dorsum with light nuchal collar (1) or absent (0) Tail with light rings: present (1) or absent (0) References
Male Female Male Female Male Female Male Female
C. berezowskii H < W < 6 1 4 0 1 Obtuse point – 2+149–155 153–2+165 22–25 16 Not reduced 248–290 123–305 6.6–10.5 5.6–6.5 Blackish-brown or brown Light khaki or white 0 1 0–1 Günther 1896; this study
C. pavimentata H ≥ W ≥ 5–6 1 – 0 1 Sharp point 8–9 125–168 137–206 3–33 8–20 Last–13th subcaudal 84–313 115–485 6.9–16.9 3.7–8.5 Brown Yellow 0 0–1 0–1 Inger and Marx 1965; Ziegler et al. 2008; Nguyen et al. 2009
C. septentrionalis H < W ≥ 6 1 – 1 1 Broadly rounded 8–9 148–166 168–188 15–19 6–11 Not reduced 111–344 117–384 6.3–8.6 2.6–4.3 Dark brown to black Yellow 1 1 1 Inger and Marx 1965; Ziegler et al. 2008; Poyarkov et al. 2019
C. yunnanensis H < W – 6 0 4 0 – Obtuse point 8–9 167–184 199 15–20 19 3rd–last subcaudal 245–300 516 5.4–8.2 5 Bluish-grey or olive-brown Red or yellow 0 0–1 1 Chernov 1962; Stuart and Heatwole 2008; Yang and Rao 2008; Lee 2021
C. andersoni H < W > 6 1 4 0 0 Obtuse point 9 171 – 23 – 2nd–last subcaudal 351.4 – 9.2 – Brownish Yellow 1 0 0 Yang and Zheng 2018
C. arcana H < W > 6 1 4 0 1 Obtuse point 10 170–176 192 20–22 12 Not reduced 144–303.2 36.5 7.2–11.8 4.7 Grey-brown with somewhat iridescent (in life) or caramel-brown (in alcohol) Orangish-red (in life) or light yellowish-beige (in alcohol) 0 0 1 Yeung et al. 2022; Zhang et al. 2023; Cai et al. 2023
C. jinggangensis H < W > 6 1 4 0 1 Obtuse point 9 159–160 179 20–22 12–14 Not reduced 314–353+ 329–364 7.1–10.1 3.6–4.6 Brownish black with iridescent (in life) or brownish black (in alcohol) Dark orange (in life) or light khaki (in alcohol) 0 0 0–1 Cai et al. 2023; this study
C. lumbricoidea H < W / H >W ≥ 4–5 1 5 1 1 Sharp point 9–11 144–196 137–229 17–27 13–21 Last–11th subcaudal 149–498 120–642 6.3–11.4 3.9–8.3 Dark brown to black Yellow 0–1 0 0–1 Inger and Marx 1965; Weinell et al. 2021; Lee 2021
C. albiventer H < W > 5 1 5 1 1 Sharp point 9 143–144 147–162 21–22 15–19 5th–8th subcaudal 205 170–361 8.8–9.3 4.7–8.8 Brown Red 1 1 0 Inger and Marx 1965; Wallach et al. 2014; Lee 2021
C. schlegeli – – 5–6 0–1 5 0 0–1 Blunt 9–10 129–161 136–180 25–44 19–37 3rd–25th subcaudal – 11.1–21.3 7.3–14.4 Dark brown to black White or yellow 0 0 0–1 Inger and Max 1965; Quah et al. 2018; Weinell et al. 2021
C. lovii gimletii – – 6 0 – 0 1 Blunt 8–9 161–202 215–249 14–20 10–12 Last–5th subcaudal – 6.2–8.4 3.0–3.7 Dark brown Yellow 0 0–1 0–1 Inger and Marx 1965; Quah et al. 2018; Grismer et al. 2004; Lee 2021
C. prakkei H = W > 5 1 5 1 1 Sharp point 7–8 126–132 142–144 31–32 24–25 7th–15th subcaudal 172–245 230–256 16.5–16.7 9.6–10.5 Brown Yellow 1 1 – Inger and Marx 1965; Wallach et al. 2014
C. buchi H > W ≤ 5 1 5 1 1 Obtuse point 9 – 221–236 – 13–14 3rd–4th subcaudal – 389–466 – 3.9–4.1 Black Yellow 1 0 0 Inger and Marx 1965; Ziegler er al. 2008; Nguyen et al. 2009
C. thanhi H < W > 6–7 0 4 0 0 Gradually to a point 9 184 198 28 21 Not reduced 461 455 9.9 6.8 Dark blue to grey Yellow 0 0 1 Ziegler and Quyet 2005; Ziegler et al. 2007; Ziegler et al. 2008; Nguyen et al. 2009; Wallach et al. 2014
C. gialaiensis H < W > 5 1 4 1 0 Rounded 9 3+191 – 23 – Last subcaudal 457 – 8.1 – Grey-brown Yellow 0 0 1 Ziegler et al. 2008; Wallach et al. 2014; Lee 2021
C. sangi H < W > 5–6 1 4 1 0 Obtuse point 9 2+190 19 Last–3rd subcaudal 373.3 6.2 Greyish-brown yellow 0 1 0 Nguyen et al. 2009; Wallach et al. 2014
C. abramovi H = W < 6 1 4 0 0 Sharp point 8 159 174 26 20 Last subcaudal – 482 13.3 7.1 Black Black and yellow 1 0 0 Orlov 2009; Wallach et al. 2014
C. concolor H < W < 5 1 5 1 1 Obtuse point 8 3+209 – 19 – Last subcaudal 578 – 7.3 – Brown Cream 0 0 0 Orlov et al. 2010; Wallach et al. 2014
C. dominici H < W > 6 1 4–5 1 0 Obtuse point 9 – 1+174 – 17–18 5th–6th subcaudal – _ 6.2 Black Yellow and black 0 0 0 Ziegler et al. 2019
C. strigiventris H < W < 6 1 4 0 0 Abruptly to point 9–11 130–157 158–180 29–33 20–30 Last–6th subcaudal – 13.8–17.9 8.4–11.5 Slate grey to grey-brown Yellow and black 0 0 0 Poyarkov et al. 2019
C. nebulosa H < W > 6 0 4 0 0 Obtuse point 9 – 3+179 – 22 Last subcaudal – 354 – 7.9 Bluish-grey Yellow 1 0 0 Lee 2021

Taxonomy

Calamaria berezowskii Günther, 1896

Figs 3, 4, 5, 6

Calamaria pavimentata — populations in Sichuan of Zhao et al. (1998) and Zhao (2006); Zhao (2003). Synonym.

Description of lectotype ZISP 8823

Adult male, collected from Lun-ngan-fu (龙安府 Long’an Fu, now 龙安镇 Long’an Town of 平武县 Pingwu County) of Sze-chuen (Sichuan Province of China) (Günther 1896).

HL: 8.0 mm, 3.0% of SVL; HW: 5.0 mm, HW/HL: 62.5%; HH: 4.0 mm, HH/HL: 50.0%; EyeD: 0.7 mm, larger than eye-mouth distance 1.0 mm; EyeD 8.8% of HL.

SVL: 271 mm; TaL: 19 mm; TL: 290 mm; Tal/TL: 6.6%.

DSR: 13–13–13 scales; VEN: 155; SC: 22, divided, followed by a shield covering tail tip; anal scale single.

Rostral as broad as high; pupil rounded; preocular 1/1 (left/right, hereafter); postocular 1/1; supralabials 4/4, the second and third supralabials entering orbit, the fourth longest; infralabials 5/5. Visible yellowish collar on left and right sides of the neck present. Dorsal color brown, with a faint dark line along each side of the back; ventral surface uniform white. Tail rather obtuse, with a conical end. 2–3 pairs light color spots at the base of the tail.

Description of referred specimen GXNU DLR195

Adult female, collected from Mt. Gongga, Moxi Town, Luding County, Ganzi Tibetan Autonomous Prefecture, Sichuan Province, China (29.645105°N, 102.111076°E, 1736 m a.s.l.) collected by Xu Zhang on 31 August 2018.

Body elongated, cylindrical; head small, not distinct from nape; tail short, similar in form to head; tail not flattened, tapering and bluntly pointed at tip.

HL: 8.3 mm, 2.9% of SVL; HW: 3.9 mm, HW/HL: 47.0%; HH: 4.0 mm, HH/HL: 48.2%; EyeD: 0.7 mm, larger than eye-mouth distance 1.1 mm; EyeD 8.4% of HL.

SVL: 288 mm; TaL: 17 mm; TL: 305 mm; Tal/TL: 5.6%. Body thickness about 4.70 to 6.71 mm; base of tail 3.18 mm thick.

VEN: 165 (+2 preventrals); SC: 16, all paired; anal shield entire, ventral scales immaculate.

DSR: 13–13–13 scales, dorsal scales smooth and immaculate.

Rostral shield width (2.22 mm) is larger than height (1.62 mm), internasals and prefrontals fused 2 scales; prefrontal length (2.28 mm) is less than frontal length (2.61 mm), not entering orbit, and touching first two supralabials; frontal hexagonal, longer (2.61 mm) than wide (2.50 mm); six paraparietals; parietal scales long, tangent to supraocular, postocular scales, supralabials; one preocular present; parietal broadly in contact with the last supralabials; pupil rounded; supralabials 4/4, second and third entering orbit, the fourth largest (length 2.34/2.32 mm) and tangent to the postoculars; mental not touching anterior chin shields; infralabials 5/5, first three touching anterior chin shields; anterior chin shields are slightly longer than posterior chin shields, presence of mental groove; less than 1/2 of the posterior chin shield meets in the midline; dorsal scales reduced to 6 rows above last subcaudal at tail; anal scale is complete and single.

Coloration in life. The dorsal color was blackish brown, with a faint dark line along each side of the back which is about 3 scales wide apart; the outermost corners of the ventral scales were brownish, and the ventral surface was lighter; presence of distinct yellowish collar; absence of light ring at the base of the tail.

Coloration in preservative. The specimen was preserved in alcohol. Dorsal body blackish brown, ventral surface light khaki. Dorsal head and neck coincide with the dorsal body, with a pair of light spots on each side of the neck and on the back of head; dorsum without distinct blotches; venter immaculate, without any dark stripes or scattered spots; ventral surface of tail with a dark longitudinal stripe and blotches; ventral scales with dark outermost corners.

Variations for population from Mt. Gongga, Luding County

Measurements of other specimens are given in Table 4. Male with relatively longer tail (TaL/TL are distinctly larger in the adult male). Adult female GXNU DLR194 displays many scattered brown spots on the venter, and with distinct light-yellow blotches on the left and right sides of the neck, but in adult male GXNU DLR195 the venter is immaculate without any dark spots. The population of Mt. Gongga, Luding County differs slightly from the type specimen in dorsal and ventral coloration (dorsal body blackish brown vs brown, ventral surface light khaki vs white), and differs from the lectotype ZISP 8823 in color spots at the base of the tail (absent vs present) (Figs 3, 4, 5).

Table 4.
Download as
CSV
XLSX

Main morphological characters of Calamaria berezowskii. Abbreviations are listed in the Materials and Methods. “–” indicates missing data. Data of lectotype and syntype of C. berezowskii by Günther 1896 and Nikolai Orlov.

Voucher No. ZISP 8823 – GXNU DLR194 GXNU DLR195 GXNU 20221215002
Type of specimen Lectotype Syntype – – –
Sex ♂ – ♂ ♀ ♀
Ontogenetic Adult Adult Adult Adult Juvenile
Preocular 1/1 1 1/1 1/1 –
Postocular 1/1 1 1/1 1/1 –
Supralabials 4/4 4 4/4 4/4 4/4
Infralabials 5/5 – 5/5 5/5 5/5
Dorsals 13–13–13 – 13–13–13 13–13–13 13–13–13
Ventrals 155 167 2+149 2+165 153
Subcaudals 22 14 25 16 16
Tailspot 2+1 – Absent Absent Absent
TL (mm) 290 245 248 305 123
SVL (mm) 271 220 222 288 115
TaL (mm) 19 25 26 17 8
TaL/TL 0.066 0.102 0.105 0.056 0.065
HL (mm) 8.0 7.0 8.1 8.3 –
HW (mm) 5.0 – 4.1 3.9 –
HH (mm) 4.0 – 3.5 4.0 –
HW/HL 0.625 – 0.506 0.470 –
HH/HL 0.500 – 0.432 0.482 –
EyeD (mm) 0.7 – 0.6 0.7 –
Eye-MouthD (mm) 1.0 – 0.9 1.1 –

Detailed morphological comparisons

Detailed morphological comparisons between Calamaria berezowskii and 20 congeners of the genus from China and mainland Southeast Asia are:

Calamaria berezowskii is distinguished from C. albiventer, C. lumbricoidea, C. prakkei, C. schlegeli, and C. concolor by having fewer supralabials (4 vs 5–6), and the 2nd and 3rd supralabials shields touching the orbit (vs. 3rd and 4th supralabials touching orbit), mental not touching anterior chin shields (vs. touching in C. albiventer, C. lumbricoidea, C. prakkei and C. concolor).

Calamaria berezowskii is distinguished with C. lovii, C. nebulosa, C. thanhi and C. yunnanensis by having presence of preocular scale (vs. absence of preocular scale), eye diameter less than distance from eye to mouth edge (vs. reverse condition in C. thanhi and C. nebulosa), fewer ventral scales in males (149–155 vs 161–202 in C. lovii, 149–155 vs 184 in C. thanhi and 149–155 vs 167–184 in C. yunnanensis), more subcaudal scale in males (22–25 vs 14–20 in C. lovii, 22–25 vs 15–20 in C. yunnanensis).

Calamaria berezowskii differs from C. sangi, C. gialaiensis and C. buchi by having mental not touching anterior chin shields (vs. touching), dorsal scales reduced to six rows at tail (vs. reduced to four rows), fewer ventral scales (149–167 vs 190 in C. sangi, 149–167 vs 191 in C. gialaiensis, 149–167 vs 221–236 in C. buchi).

Calamaria berezowskii is distinct from C. arcana and C. jinggangensis by having the eye diameter less than the distance from the eye to mouth edge (vs. reverse condition in C. arcana and C. jinggangensis), fewer ventral scales (149–167 vs 170–192 in C. arcana and C. jinggangensis), more subcaudals in females (16 vs 12–14 in C. arcana and C. jinggangensis), a distinctly different coloration (dark orange or orangish-red in fresh specimens in C. arcana and C. jinggangensis), presence of dark outermost corners on ventral scales (vs. absence in C. arcana and C. jinggangensis), a faint dark line along each side of the back present (vs. opposite condition in C. arcana and C. jinggangensis), a dark longitudinal line or scattered spots on the underside of tail present (vs. absent in C. arcana and C. jinggangensis).

Calamaria berezowskii differs from C. abramovi by having the rostral wider than high (vs. width equal to high in C. abramovi), fewer ventral scales in males (149–155 vs 159 in C. abramovi), dorsal scales reduced to six rows at tail (vs. reduced to four rows in C. abramovi), tail ends in obtuse point (vs. sharp point in the end of tail in C. abramovi), and a distinctly different coloration (body black with yellow-orange spots on venter in C. abramovi).

Calamaria berezowskii differs from C. andersoni by having eye diameter smaller than distance from eye to mouth edge (vs. reverse condition in C. andersoni), fewer ventral scales in males (149–155 vs 171 in C. andersoni), dorsal scales reduced to six rows at tail (vs. reduced to four rows in C. andersoni), light blotches on neck present (vs. absent in C. andersoni).

Calamaria berezowskii differs from C. septentrionalis by having eye diameter less than distance from eye to mouth edge (vs. reverse condition in C. septentrionalis), mental separated from anterior chin shields (vs. reverse condition in C. septentrionalis), not gradually tapering at tip (vs. tail tip broadly rounded in C. septentrionalis), higher number of subcaudals (22–25 vs 15–19 in males and 16 vs 6–11 in females), absence of black stripe on venter of tail (vs. venter of tail with broad and distinct median black stripe in C. septentrionalis).

Calamaria berezowskii differs from C. pavimentata by having the rostral shield width larger than high (vs. reverse condition in C. pavimentata), the eye diameter less than the distance from eye to mouth edge (vs. reverse condition in C. pavimentata), tail not tapering anteriorly and abruptly pointed at tip (vs. tail tapering gradually to a point in C. pavimentata), dorsal scales reduced to six rows at tail (vs. reduced to four rows in C. pavimentata), dorsum of body with two faint dark lines (vs. distinct narrow and dark longitudinal lines on dorsum in C. pavimentata).

Calamaria berezowskii differs from C. dominici by having eye diameter less than eye-mouth distance (vs. opposite situation in C. dominici), mental separated from anterior chin shields (vs. mental touching tip of right anterior chin shield in C. dominici), dorsal scales reduced to six rows at tail (vs. reduced to four rows in C. dominici), fewer ventral scales in females (153–165 vs 174 in C. dominici), absence of blotches on dorsum (vs. present irregular yellow blotches on dorsum in C. dominici), venter immaculate without dark stripes (vs. ventral side dark with yellow blotches and bands).

Calamaria berezowskii differs from C. strigiventris by having posterior chin shields meeting in midline (vs. diverging or meeting only in anteriorly in C. strigiventris), dorsal scales reduced to six rows at tail (vs. reduced to four rows in C. strigiventris), lower number of subcaudals (22–25 vs 29–33 in males and 16 vs 20–30 in females in C. strigiventris), venter immaculate (vs. presence of three interrupted longitudinal black stripes in C. strigiventris), tail not flattened, tapering and bluntly pointed at tip (vs. slowly tapering anteriorly, then abruptly tapering to a point in C. strigiventris).

Diagnosis

Calamaria berezowskii can be distinguished from all other congeneric species by having the following combination of morphological characters: 1) rostral shield width larger than high; 2) prefrontal shorter than frontal, touching the first and second supralabials; 3) frontal hexagonal, length longer than width; 4) mental not touching anterior chin shields; 5) two pairs of chin-shields, the anterior not much longer than the posterior, less than 1/2 of the posterior chin shield meets in the midline; 6) eye diameter less than eye-mouth distance; 7) single preocular, single postocular; 8) four supralabials, second and third supralabials entering orbit; 9) five infralabials, first three touching anterior chin shields, first pair of supralabials touching each other; 10) six scales and shields surrounding the paraparietals; 11) dorsal scales smooth, DSR 13–13–13 (n = 4); 12) dorsal scales reduced to six rows above last subcaudal at tail; 13) 149 (+2 preventrals)–155 ventrals in the males (n = 2), 153–165 (+2 preventrals) in the females (n = 2); 14) 22–25 subcaudals in the males (n = 2), 16 in the females (n = 2), all paired; 15) anal plate single and intact; 16) dorsum of body and tail blackish-brown or brown, with a faint dark line along each side of the back; 17) a more or less distinct yellowish collar; 18) 2–3 pairs of small white spots may be present or absent on the tail; 19) ventral scales of body light khaki or white, with a dark longitudinal line or scattered spots on the underside of tail; 20) two outermost dorsal scale rows light khaki with upper margins partly dark pigmented; 21) tail relatively short (5.6–10.5% of the total length), not flattened, slowly tapering to obtuse, with a conical end.

Etymology

Named after collector of type specimen, Russian traveler and zoologist. Michael Berezowski. For common name, we suggest “川西两头蛇” (Chinese), “Berezowski’s Reed Snake” (English).

Distribution and ecology

Terra typica of Calamaria berezowskii is Lun-ngan-fu (now Long’an Town of Pingwu County) (Günther 1896). It is known from western Sichuan Province, China, including Pingwu County, Shimian County, Baoxing County, Luding County, Mt. Emei and Pingshan County (Zhao et al. 1998; Zhao 2003; this study). These localities are all on the eastern edge of the Qinghai-Tibet Plateau bordering Sichuan Basin. In Luding County, it was found at an elevation of 1680–1827 meters, surrounded by mountainous evergreen broad-leaved forest belt and evergreen broad-leaved deciduous broad-leaved mixed forest belt (Fig. 7). It has a typical subtropical-based vertical natural belt spectrum, with big altitude differences, and abundant rare plant and animal resources (Wang et al. 2023).

Figure 7. 

Macrohabitat of Calamaria berezowskii in Luding County, Sichuan Province, China.

Discussion

Morphologically, specimens of C. berezowskii collected in Luding County, Sichuan Province are a close match to the type specimens collected in Pingwu County, Mianyang City of Sichuan Province (Günther 1896). For example, there was no significant difference in the number of ventral and subcaudal scales; presence of a more or less distinct yellowish collar; one preocular and one postocular; presence of faint dark line along each side of the dorsum. Geographically, Luding County and Pingwu County are both located in the western region of the Sichuan Province, which lies on the eastern slope of the Qinghai-Tibet Plateau bordering the Sichuan Basin. Even though the samples of Calamaria used by this study do not originate from the type locality, the morphology of the voucher specimens matches the original description by Günther (1896), so we confirm that the Calamaria specimens collected in Luding County, Sichuan Province are C. berezowskii and recover the validity of C. berezowskii.

Due to their subterranean mode of life, digging behavior and mysterious habits, Calamaria species are not often encountered in the wild. However, in the last five years, five species of Calamaria were described, which once more shows that the diversity of the genus Calamaria is still highly underestimated. In addition, the formal redescription of C. berezowskii brings the total number of species of the genus Calamaria in China to seven, namely C. pavimentata, C. septentrionalis, C. yunnanensis, C. andersoni, C. arcana, C. jinggangensis, and C. berezowskii (Cai et al. 2023; Uetz et al. 2023). At the same time, finding additional specimens of C. berezowskii from the type locality and surrounding areas would allow for a greater understanding of its intraspecific variation.

C. berezowskii was found at an elevation of 1680–1827 meters, which is higher than the altitude of all previously known Calamaria in China (vs.175–1520 m a.s.l.). The discovery of this new species increases the elevation of all known Calamaria species in China and suggests that the actual habitat of Calamaria species may span a greater range of elevations. The Hengduan Mountains in southwest China are a biodiversity hot spot, harboring a high percentage of endemic biota (Hu et al. 2012; Wu et al. 2013; Sun et al. 2017; Qiao et al. 2022). For snakes, the high altitude, steep terrain and varying climatic conditions of the Hengduan Mountains are important factors limiting their distribution and are conducive to species migration and isolation, accelerating gene flow and promoting species adaptation to the environment and species formation. Therefore, studying this species is beneficial for understanding the influence of geographical factors and the ecological environment on species formation and evolution.

We update the key to Calamaria in China, which is based on Zhao (2006), Yeung et al. (2022) and Cai et al. (2023). The identification of this key is only for reference. Species should be identified by comparing more morphological characteristics or molecular sequences.

Key to the identification of the genus Calamaria from China

1 Preocular absent Calamaria yunnanensis
– Preocular present 2
2 Dorsal scales reduced to four rows on tail at last subcaudals 3
– Dorsal scales reduced to more than four rows on tail at last subcaudals 5
3 Light rings/blotches on neck and tail absent Calamaria andersoni
– Presence of light rings/blotches on neck or tail 4
4 Tail tapering gradually to a point Calamaria pavimentata
– Tail not tapering, broadly rounded on tip Calamaria septentrionalis
5 Most of the posterior chin shield meets in the midline, absence of collar or spots in nuchal region Calamaria jinggangensis
– Less than 1/2 of the posterior chin shield meets in the midline, present indistinct light ring or one pair of spots in nuchal region 6
6 Ventral scales immaculate, without dark outermost corners and pigmentation anteriorly Calamaria arcana
– Two outermost dorsal scale rows light khaki, with upper margins partly dark pigmented Calamaria berezowskii

Acknowledgements

This study was supported by Science and Technology Programme Project of Guangxi, China (AD21220058), the National Natural Science Foundation of China (NSFC 32200379), the Natural Science Foundation of Guangxi, China (2023GXNSFBA026309), and Survey and Assessment of Priority Areas for Biodiversity Conservation in the Terrestrial Area of Guangxi, China (2022–2023). It is partly supported by the State Themes of ZISP 122031100282-2 and grant no.075-15-2021-1069 by the Ministry of Science and Higher Education of the Russian Federation.

We thank Xu Zhang and Congcong Du for providing specimens, and thanks to Konstantin Milto for the help with photographs of type specimens. We would also like to thank Xin Wang and the reviewers for their valuable comments on the manuscript.

References

  • Alencar LRV, Quental TB, Grazziotin FG, Alfaro ML, Martins M, Venzon M, Zaher H (2016) Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Molecular Phylogenetics and Evolution 105: 50–62. https://doi.org/10.1016/j.ympev.2016.07.029
  • Burbrink FT, Lawson R, Slowinski JB (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): A critique of the subspecies concept. Evolution 54(6): 2107–2118. https://doi.org/10.1111/j.0014-3820.2000.tb01253.x
  • Dowling HG (1951) A proposed standard system of counting ventrals in snakes. British Journal of Herpetology 1: 97–99.
  • Grazziotin FG, Zaher H, Murphy RW, Scrocchi G, Benavides MA, Zhang YP, Bonatto SL (2012) Molecular phylogeny of the new world Dipsadidae (Serpentes: Colubroidea): a reappraisal. Cladistics 28(5): 437–459. https://doi.org/10.1111/j.1096-0031.2012.00393.x
  • Grismer LL, Kaiser H, Yaakob NS (2004) A new species of reed snake of the genus Calamaria H. Boie, 1827, from Pulau Tioman, Pahang, West Malaysia. Hamadryad 28: 1–6.
  • Günther A (1896) Report on the collections of reptiles, batrachians and fishes made by Messrs Potanin and Berezowski in the Chinese provinces Kansu and Sze-chuen. Ezhegodnik. Zoologicheskogo Muzeya Akademii Nauk SSSR 1896: 199–219.
  • Inger RF, Marx H (1965) The systematics and evolution of the oriental colubrid snakes of the genus Calamaria. Fieldiana. Zoology 49: 1–304.
  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549. https://doi.org/10.1093/molbev/msy096
  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29(6): 1695–1701. https://doi.org/10.1093/molbev/mss020
  • Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34(3): 772–773. https://doi.org/10.1093/molbev/msw260
  • Lawson R, Slowinski JB, Crother BI, Burbrink FT (2005) Phylogeny of the Colubroidea (Serpentes): New evidence from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 37(2): 581–601. https://doi.org/10.1016/j.ympev.2005.07.016
  • Lee JL (2021) Description of a new species of Southeast Asian reed snake from northern Laos (Squamata: Colubridae: Genus Calamaria F. Boie, 1827) with a revised diagnosis of Calamaria yunnanensis Chernov, 1962. Journal of Natural History 55(9–10): 531–560. https://doi.org/10.1080/00222933.2021.1909165
  • Nagy ZT, Lawson R, Joger U, Wink M (2004) Molecular systematics of racers, whipsnakes and relatives (Reptilia: Colubridae) using mitochondrial and nuclear markers. Journal of Zoological Systematics and Evolutionary Research 42(3): 223–233. https://doi.org/10.1111/j.1439-0469.2004.00249.x
  • Nguyen TQ, Koch A, Ziegler T (2009) A new species of reed snake, Calamaria Boie, 1827 (Squamata: Colubridae), from central Vietnam. Hamadryad 34(1): 1–8.
  • Orlov NL (2009) A new species of the genus Calamaria (Squamata: Ophidia: Colubridae) from the Central Highlands (Ngoc Linh Nature Reserve, Ngoc Linh Mountain, Kon Tum Province), Vietnam. Russian Journal of Herpetology 16(2): 146–154. https://doi.org/10.30906/1026-2296-2009-16-2-146-154
  • Orlov NL, Nguyen QT, Nguyen TT, Ananjeva NB, Ho TC (2010) A new species of the genus Calamaria (Squamata: Ophidia: Colubridae) from Thua Thien-Hue Province, Vietnam. Russian Journal of Herpetology 17(3): 236–242. https://doi.org/10.30906/1026-2296-2010-17-3-236-242
  • Poyarkov NA, Van Nguyen T, Orlov NL, Vogel G (2019) A new species of the genus Calamaria Boie, 1827 from the highlands of the Langbian Plateau, Southern Vietnam (Squamata: Colubridae). Russian Journal of Herpetology 26(6): 335–348. https://doi.org/10.30906/1026-2296-2019-26-6-335-348
  • Qiao J, Jia GQ, Zhou HM, Gong L, Jiang Y, Xiao NW, Gao XQ, Wen AX, Wang J (2022) Mammal and bird diversity recorded with camera traps in Gongga Mountain National Nature Reserve, Sichuan, China. Shengwu Duoyangxing 30(2): 20395. https://doi.org/10.17520/biods.2020395
  • Quah RV, Tan YH, Mubarak NM, Khalid M, Abdullah EC, Nolasco-Hipolito C (2019) An overview of biodiesel production using recyclable biomass and non-biomass derived magnetic catalysts. Journal of Environmental Chemical Engineering 7(4): 103219. https://doi.org/10.1016/j.jece.2019.103219
  • Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Stuart BL, Heatwole H (2008) Country records of snakes from Laos. Hamadryad 33(1): 97–106.
  • Wallach V, Williams KL, Boundy J (2014) Snakes of the World: A Catalogue of Living and Extinct Species. CRC press, 1st edn., 1237. https://doi.org/10.1201/b16901
  • Wang XM, Li Y, Liao R, Liu YX, Zhang XA, Qiao J, Wang Y, Wang X, Liu SY (2023) Species diversity of small mammals on the north and south slopes of Gongga Mountain National Nature Reserve. Sichuan Linye Keji 44(6): 1–8. https://doi.org/10.12172/202307240001
  • Weinell J, Leviton AE, Brown RM (2021) A new species of reed snake, genus Calamaria (Colubridae: Calamariinae), from Mindoro Island, Philippines. Philippine Journal of Systematic Biology 14(2): 1–14. https://doi.org/10.26757/pjsb2020b14006
  • Wu YJ, Colwell RK, Rahbek C, Zhang CL, Quan Q, Wang CK, Lei FM (2013) Explaining the species richness of birds along a subtropical elevational gradient in the Hengduan Mountains. Journal of Biogeography 40(12): 2310–2323. https://doi.org/10.1111/jbi.12177
  • Yang DT, Rao DQ (2008) Amphibia and Reptilia of Yunnan. Kunming: Yunnan Science and Technology Press.
  • Yang JH, Zheng X (2018) A new species of the genus Calamaria (Squamata: Colubridae) from Yunnan Province, China. Copeia 106(3): 485–491. https://doi.org/10.1643/CH-17-663
  • Yeung HY, Lau MWN, Yang JH (2022) A new species of Calamaria (Squamata: Colubridae) from Guangdong Province, southern China. Vertebrate Zoology 72: 433–444. https://doi.org/10.3897/vz.72.e84516
  • Zaher H, Grazziotin FG, Cadle JE, Murphy RW, Moura-Leite JCD, Bonatto SL (2009) Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: A revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia 49(11): 115–153. https://doi.org/10.1590/S0031-10492009001100001
  • Zhao EM (2003) Coloured Atlas of Reptiles of Sichuan. China Forestry Press: Beijing, China.
  • Zhao EM (2006) Snakes of China. Hefei, China: Anhui Science and Technology Press.
  • Zhao EM, Huang MH, Zong Y (1998) Fauna Sinica Reptilia, Vol. 3: Squamata: Serpentes. Beijing. Science Press 1998(522): 1–8.
  • Ziegler T, Quyet LK (2005) A new species of reed snake, Calamaria (Squamata: Colubridae), from the Central Truong Son (Annamite Mountain range), Vietnam. Zootaxa 1042(1): 27–38. https://doi.org/10.11646/zootaxa.1042.1.2
  • Ziegler T, Hendrix R, Vu NT, Vogt M, Forster B, Dang NK (2007) The diversity of a snake community in a karst forest ecosystem in the central Truong Son, Vietnam, with an identification key. Zootaxa 1493(1): 1–40. https://doi.org/10.11646/zootaxa.1493.1.1
  • Ziegler T, Tran VA, Babb RD, Jones TR, Moler PE, Van Devender RW, Nguyen TQ (2019) A new species of reed snake, Calamaria Boie, 1827 from the Central Highlands of Vietnam (Squamata: Colubridae). Revue Suisse de Zoologie 126(1): 17–26. https://doi.org/10.5281/zenodo.2619512

Appendix 1

Examined specimens (n = 6)

Calamaria berezowskii (n = 4). China: Sze-chuen (now Sichuan Province): Lun-ngan-fu (Long’an Fu, now Long’an Town of Pingwu County): ZISP 8823 (lectotype, adult male); Sichuan: Mt. Gongga, Moxi Town, Luding County, Ganzi Tibetan Autonomous Prefecture: GXNU DLR195 (adult female); GXNU DLR194 (adult male); GXNU 20221215002 (juvenile female).

Calamaria jinggangensis (n = 2). China: Guangxi: Quanzhou County, Guilin: GXNU 20210909007 (adult male); Longsheng County, Guilin: GXNU 20220613012 (adult male).

login to comment