Asian Herpetological Research 2013, 4(2): 109–115 DOI: 10.3724/SP.J.1245.2013.00109

A New Species of the Genus Protobothrops (: ) from Southern Tibet, China and Sikkim, India

Hujun PAN1, 5*, Basundhara CHETTRI2*, Daode YANG1, Ke JIANG3, Kai WANG4, Liang ZHANG5** and Gernot VOGEL6**

1 Institute of Wildlife Conservation, Central South University of Forestry and Technology, Changsha 410004, Hunan, China. 2 School of Policy Planning and Studies, Sikkim University, Gangtok 737102, Sikkim, India. 3 State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic , Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, Yunnan, China. 4 Washington State University, 99163 Pullman, Washington, USA 5 Guangdong Entomological Institute & South China Institute of Endangered Animals, Guangzhou 510260, Guangdong, China. 6 Society for Southeast Asian Herpetology, Im Sand 3, D-69115 Heidelberg, Germany.

Abstract A new species of the genus Protobothrops Hoge & Romano-Hoge, 1983, was described from Jilong County, southern Tibet, China, and Chungthang, northern Sikkim, India. It differs from congeners by the following characters: 1) relatively large body size (total length up to 1510 mm); 2) dorsal scale rows 25–25–19; 3) except for the smooth outermost row, dorsal scales are weakly keeled; 4) relatively high number of ventral (198–216) and subcaudal (65–76 pairs) scales; 5) 7–8 supralabials; 6) 11 to 13 infralabials; 7) dorsal head uniform dark brown, laterally a reddish-brown obscure postocular streak; 8) dorsum of trunk and tail olive, with distinct black edged red brown transverse bands across the body and tail; and 9) eye from bright brown and reddish brown to mildly brown. The new species was also observed from the Haa Valley in western Bhutan.

Keywords new species, Protobothrops, Viperidae, Squamata, Himalayan region

1. Introduction and Pauwels, 2000), although the generic positions of the last two species are still unclear. Subsequently, P. The genus Protobothrops was formally described in cornutus (Smith, 1930) was added to this genus as well 1983 by Hoge & Romano-Hoge for a group of slender, (Herrmann et al., 2004). Recently, three new species brownish, ground living pitvipers, and it was previously have been described from China and Vietnam, that is, included in the genus Lacépède, 1804. P. trungkhanhensis Orlov, Ryabov and Nguyen, 2009, When described, only 3 species were placed in the genus Protobothrops. Since then, some new species were P. maolanensis Yang, Orlov and Wang, 2011, and P. described, namely, Protobothrops xiangchengensis (Zhao dabieshanensis Huang, Pan, Han, Zhang, Hou, Yu, Zhang et al., 1978), P. mangshanensis (Zhao and Chen, 1987), and Zhang, 2012. Currently there are 12 valid species in and P. sieversorum (Ziegler, Herrmann, David, Orlov the genus, of which seven are known to inhabit China, and many of the species in China prefer mountain areas at * These authors contributed equally to this work. relatively high elevations. ** Corresponding authors: Gernot VOGEL from the Society for Southeast Asian Herpetology, Heidelberg, Germany; and Liang ZHANG Protobothrops kaulbacki (Smith, 1940) and P. jerdonii from South China Institute of Endangered Animals, Guangdong, China, (Günther, 1875) are known to inhabit the Himalayan with their research focusing on herpetofauna in southeastern Asian and southern China. Range. Herein, we report another species in the genus E-mail: [email protected] (Gernot VOGEL); vampire_cn@163. from the Himalayan region, which occurs in Tibet, China, com (Liang ZHANG) Received: 27 February 2013 Accepted: 11 May 2013 Sikkim, India and Bhutan. 110 Asian Herpetological Research Vol. 4

2. Material and Methods same locality as the holotype, a road killed specimen, collected by Hujun PAN on 23 May 2012, and deposited Two specimens of the new species were collected from in South China Institute of Endangered Animals, Jilong County of southern Tibet, China, and one specimen Guangzhou, China; ZSI 25990 (Figure 2), an adult male from Sikkim, India. All of them were designated as from Chungthang, northern Sikkim, India, collected by members of the type series. The specimens were fixed and Basundhara CHETTRI on 16 August 2008, and deposited deposited in 75% ethanol. in ZSI, Kolkata, India. All measurements were made with a slide-caliper to the Diagnosis: This new species is assigned to the genus nearest 0.1 mm, except for the snout-vent length (SVL) Protobothrops on the basis of the following characters: and tail length (TAL), which were made with a flexible 2 large solenoglyph teeth and a loreal pit; dorsal head ruler to the nearest 1 mm. The total length (TL) was covered with very small scales; body and tail elongated, obtained by summing the SVL and TAL. The following thin and cylindrical; DSR 25 at midbody, keeled except abbreviations for morphological characters are used: the outermost; and distinct transverse bands found across head length (HL, from the tip of snout to the posterior body and tail (Hoge and Romano-Hoge, 1983). margin of mandible); head width (HW, at the widest part Protobothrops himalayanus sp. nov. differs from other of head); eye horizontal diameter (ED); supralabials (SL); species of Protobothrops by the following characters: 1) infralabials (IL); dorsal scale rows (DSR); anterior part relatively large body size (TL up to 1510 mm ); 2) DSR of dorsal scale rows (ASR, about one head length behind 25–25–19; 3) with the exception of the smooth outermost the head); middle part of dorsal scale rows (MSR); row, dorsal scales are weakly keeled; 4) relatively high posterior part of dorsal scale rows (PSR, about one head number of ventral (198–216) and subcaudal scales (65–76 length before the vent); and ventral (VEN). The number pairs); 5) 7–8 supralabials; 6) 11 to 13 infralabials; 7) of ventralscales was counted according to Dowling dorsal head uniform dark brown, laterally a reddish- (1951a), scale reduction formula is done according to brown obscure postocular streak, starting behind the eye; Dowling (1951b). The dorsal scale rows were counted 8) dorsal body and tail olive, with distinct black edged red at one head length behind the head, at midbody, and at brown transverse bands across the body and tail; and 9) one head length anterior to the vent. The terminal scute eye found from bright brown and reddish brown to mildly was not included in the number of subcaudal scales brown. count. Values for paired head characters are given in left/ Etymology: The specific epithet is derived from the right order. Other abbreviations are also provided: CAS mountain range, the Himalayas. All of the current known (California Academy of Sciences, San Francisco, USA); distribution localities are on the southern slope of the KIZ (Kunming Institute of Zoology, Chinese Academy of Himalayas. The suggested English name is the Himalayan Sciences, Kunming, China); and ZSI (Zoological Survey Pitviper, and the Chinese name is Xi Shan Yuan Mao Tou of India, Kolkata, India). Additionally, two specimens Fu. of Protobothrops kaulbacki from KIZ (KIZ 011065) and Description of holotype: An adult female, with detailed CAS (CAS 224430) were examined, with the exception measurements listed in Table 1. Body size large (SVL 952 of P. kaulbacki, all the species for comparison are mainly mm, TAL 166 mm), elongated, thin and cylindrical; head based on the descriptions in literature (Gumprecht et al., triangular and elongated, 0.58 times wider than long, and 2004; Orlov et al., 2009; Yang et al., 2011; Zhao, 2006; distinct from the neck; dorsal head covered with very Zhao et al., 1998). small, convex and irregular shaped smooth scales; and eye convex, pupil vertical; rostral triangular and small, 3. Results slightly visible from above; internasal scales contact each other, and with the rostral; nasal trapezoidal, undivided, 3.1 Description with a large round nostril opening centrally; two canthal Protobothrops himalayanus sp. nov. scales between the supraocular and internasal, with the Holotype: KIZ 012736 (Figure 1), an adult female from posterior one being very small; one loreal present on the Jilong Valley, Jilong County, southern Tibet, China each side; supraocular large and elongate; two elongate (85.35360° E, 28.37996° N; elevation 2708 m), collected upper-preoculars present above the loreal pit, forming the by Kai WANG and Hujun PAN on 14 June 2012, and upper margin of the loreal pit, and the lower one wider deposited in KIZ. and slightly longer than the upper; one elongate lower- Paratypes: JL 20120614-001, an adult female from the preocular forming the lower margin of the loreal pit; 2/3 No. 2 Hujun PAN et al. New species of Protobothrops from China and India 111

Table 1 Variations in the type series of Protobothrops himalayanus sp. nov. (in mm).

Holotype Paratype Paratype KIZ 012736 JL 20120614-001 ZSI 25990 Sex Female Female Male SVL 952 904 1035 TAL 166 Incomplete 185 TAL/SVL 0.17 — 0.18 Rel TL 0.149 — 0.152 HL 38.0 45.1 43.6 HW 22.0 34.0 25.4 SL 7/7 8/8 8/8 IL 13/12 11 12/13 Loreal 1 2 2 PreO 2 2 2 3/2 and PostO 2/3 3 a granular One Figure 2 Protobothrops himalayanus sp. nov., ZSI 25990 (para- VEN 205 198 204 type), an adult male from Chungthang, northern Sikkim, India. SC 71 — 71 Photo by Basundhara CHETTRI. DSR 25-25-19 25-25-19 25-25-19 Body bands 48 50 47 infralabials, the first pair in contact with each other, the Tail bands 19 — 16 first two in contact with anterior chin shield; posterior small postocular scales; one elongate, thin, crescent- chin shield short, thinner and smaller than anterior chin shaped subocular separated from the lower preocular by shield. one small scale; temporals numerous, all smooth; 7/7 The dorsal scales narrow, in 25 rows at anterior supralabials, with the second one forming the anterior body, 25 rows at midbody, 19 rows at posterior body; at margin of the loreal pit and separated from the nasal by midbody, dorsal scales are weakly keeled, except for the one small scale, the third largest, the third and fourth lateralmost row which is smooth; ventral scales 205, plus separated from subocular by one row of scales; 13/12 2 preventrals; anal entire; and subcaudal scales divided, in 71 pairs. Scale reduction formula is given below:

5 + 6 → 5 (112) 5 + 6 → 5 (123) 4 + 5 → 4 (134) 25 —————— 23 —————— 21 ————— 19 4 + 5 → 4 (113) 6 + 7 → 6 (125) 5 + 6 → 5 (137)

Coloration in life: Dorsal body and tail is olive, with 48 and 19 black edged red-brown transverse bands across the body and tail, respectively. Each of the bands on body possesses a blotch with similar color on each side, which sometimes contacts the bands. The bands become gradually closer towards tail. Dorsal head is uniformly dark brown, and the lateral head is yellow, with a red brown stripe whose width is approximately that of one temporal scale, starting from the posterior margin of the eye, extending across the temporal region, and ending at the posterior margin of the mandible. Ventral sides of the head, body and tail are grayish white. Each ventral and subcaudal scale is found with irregular brownish gray blotches. Figure 1 Protobothrops himalayanus sp. nov., KIZ 012736 (holo- Variation: The type series is generally similar. Their type), an adult female from the Jilong Valley, Jilong County, southern measurements and scale characters are shown in Table 1. Tibet, China. A: Dorsal view in life; B: Head profile, photos by Kai WANG; C: Dorsal view of fixed specimen; D: Ventral view of fixed Distribution and ecology: Currently, P. himalayanus specimen, photos by Ke JIANG. sp. nov. is known from the Jilong Valley (Figure 3 A, B) 112 Asian Herpetological Research Vol. 4

2, the new species is mostly similar to P. kaulbacki. The main differences between the two species are found in head shape, eye color, and body coloration (Table 3, Figures 6, 7). Nevertheless these differences are significant enough to separate the two species. Protobothrops kaulbacki has a very sharp canthus rostralis, which is rounded in P. himalayanus sp. nov. (Figures 6, 7). The eye color of P. himalayanus sp. nov. is brown to copper, while that in P. kaulbacki it is nearly black. The eye color is lighter in juveniles of P. kaulbacki, but that in the juveniles of P. himalayanus sp. nov. is unknown. The dorsum of the head of P. himalayanus sp. nov. is uniformly brown without any marking, but with a visible postocular stripe, reddish brown in color; no marking presents on its neck. The dorsum of the head of

Figure 3 Habitat of Protobothrops himalayanus sp. nov. A: Jilong Valley, Jilong County, southern Tibet, China; B: Collection locality of the paratype (JL 20120614-001), Jilong Valley, photos by Hujun PAN; C: Haa Valley, western Bhutan, photo by Jane HANCOCK. in southern Tibet, China (type locality), Sikkim, India Figure 4 Protobothrops himalayanus sp. nov., observed from Haa (Figure 3 C), and Bhutan (a specimen was photographed in the Haa Valley, western Bhutan. Living specimen, unpreserved, photo by Jane HANCOCK. on a road leading out of the town, Haa in the Haa Valley in western Bhutan, Figure 4). All of these localities are situated on the southern slope of the Himalayas (Figure 5) at elevations ranging from 1300 m to 2100 m. In Sikkim, P. himalayanus sp. nov. is commonly observed on the roads and moist litter of cardamom plantations at night from May to July, and is no longer active from mid September. Stone walls and tall grasses on the edge of agricultural fields provide refuge for the . During the day, the snakes hide themselves under boulders, among grasses or in the stone walls by agricultural fields, and they come out to feed at dawn. Several road killed specimens and direct field observations confirmed that rats and shrews are the main diets of this . 3.2 Comparison A comparison of the pholidosis of P. Figure 5 Map showing the three known localities of Protobothrops himalayanus sp. nov. Jilong Valley, Jilong County, southern Tibet, himalayanus sp. nov. with that of other species in this China (red dot); Chungthang, northern Sikkim, India (blue dot); and genus is shown in Table 2. As can be noticed from Table Haa in the Haa Valley, western Bhutan (purple dot). No. 2 Hujun PAN et al. New species of Protobothrops from China and India 113

Table 2 Comparison of pholidosis data of the species of the genus Protobothrops. P. mangshanensis and P. sieversorum are not included, which are very different and of which the generic membership is still under discussion (in mm). For abbreviations, see the “Material and Methods.”

TL TAL/TTL TAL/TTL VEN SC SC MSR PSR SL IL Outermost row max ♂ ♀ ♂ ♀ P. himalayanus sp. nov. 1510 0.148–0.171 0.149–0.180 198–216 71–75 65–76 25 19 7–8 11–13 Smooth (n = 6) (n = 12) P. kaulbacki‌① 1447⑧ 0.197⑧ 0.172⑩ 201–212 72–86 66–76 25–27 17–19 7–8 12–14 Smooth P. cornutus② 680 0.191–0.203 0.177–0.184 187–195 70–78 65–77 21 17 9 12–14 Smooth P. elegans③ 1287 0.199–0.229 0.179–0.193 179–192 69–79 63–72 23–25 19 7–8 10–12 Smooth P. flavoviridis 2315⑨ 0.153–0.176 0.142–0.169 220–239 79–94 73–86 33–39 23–25 7–9 14–17 Smooth P. jerdonii④ 1090 0.153–0.168 0.157–0.163 160–192 50–80 44–74 21–23 15–17 7–8 11–12 Smooth P. maolanensis⑤ 805 0.192–0.212 0.16 186–193 78–85 74 19–21 15–17 7–8 11–12 Keeled Smooth or P. mucrosquamatus 1280 0.160–0.240 0.110–0.190 193–233 78–100 70–87 23–27 17–25 9–11 11–17 obtusely keeled P. tokarensis 1500 0.183–0.222 0.169–0.200 179–192 75–84 72–79 23–25 19 7–9 12–16 Smooth P. trungkhanensis⑥ 733 0.194 0.176 188–194 75 76 19 17 8–9 11–12 Keeled P. xiangchengensis⑦ 1150 0.140–0.148 0.128–0.142 175–194 54–66 44–62 23–25 15–17 7–8 11–13 Smooth

① KIZ 011065, CAS 224430, Bhide et al., 2008 (source of counts unknown) and Smith (1940); ② David et al., 2008 and Gong et al., 2010; ③ Kikukawa, 1974; ④ Guo et al., 2011; ⑤ Yang et al., 2011; ⑥ Orlov et al., 2009; ⑦ Guo et al., 2006 and Zhao et al., 1998; ⑧ KIZ 011065 (as the data in the literature is inconsistent and contradictory, we decided to list here our own data only); ⑨ Mishima, 1980; ⑩ CAS 224430 (as the data in the literature is inconsistent and contradictory, we decided to list our own data only)

Table 3 Comparisons of the coloration of four selected species of the genus Protobothrops.

P. himalayanus sp. nov. P. kaulbacki P. jerdonii P. mucrosquamatus

Eye color (adults only) Brown Black Black or nearly black Brown or copper Blackish, with vivid Blackish, with vivid Dorsal head color Brown, uniform Brown, uniform markings ornamentations “V” on head No Yes Yes No Postocular stripe color Red brown Light yellow Yellow or white Dark brown Postocular stripe Obscure Sharp Sharp Sharp specificity Postocular stripe Behind eye Before eye Before eye Behind eye starting Creamy yellow, with faint orange Light brown, more or less in the Color of the upper White to yellow, some or all markings on the margins of the Light yellow, uniform same color as the dorsal head, labials with black margins. upper labials uniform

P. kaulbacki is nearly black, with a very sharp “Y-shaped” sp. nov. differs in the number of upper labials (7–8 vs. marking, opening posteriorly; a yellow stripe starting 9–11), in coloration (Table 3), and having a larger body from the loreal region, extending across the temporal size (TL max 1510 mm in P. himalayanus sp. nov. vs. TL region, ending at the posterior margin of the mandible, max 1280 mm in P. mucrosquamatus). and an inverted yellow “Y-shaped” marking occurs on the neck. Some faint orange or red brown markings present 4. Discussion on the margins of the upper labials of P. himalayanus sp. nov., while the margins of the upper labials of P. The continuous discovery of new species in the Himalayas kaulbacki are uniformly bright yellow. shows a strong need for further exploration in the region. Protobothrop himalayanus sp. nov. differs from P. It is astonishing that three distinct species of the same jerdonii in the number of dorsal scale rows (25 MSR and genus are distributed in such close proximity in the 19 PSR in P. himalayanus sp. nov. vs. 21–23 MSR and Himalayan mountain range. Obviously here are several 15–17 PSR in P. jerdonii), in the number of ventral scales centers of endemisms which were not detected so far. One (198–216 vs. 160–192), in an overall larger size (TL max reason for this is the fact that the Himalayan region is 1510 mm vs. TL max 1090 mm) and in coloration (Table partitioned by political borders, which make field surveys 3). As compared to P. mucrosquamatus, P. himalayanus much more difficult to conduct. Thus, collaboration 114 Asian Herpetological Research Vol. 4

Figure 6 Comparison of the heads of Protobothrops himalayanus sp. nov. (A: ZSI 25990, adult male from Chungthang, northern Sikkim, India, photo by Basundhara CHETTRI) and Protobothrops kaulbacki (B: KIZ 011065, adult male from Medog, southeastern Tibet, China, photo by Ke JIANG). between scientists from different neighboring countries is distribution range. essential for a successful inventory of the herpetofauna of this huge region. Acknowledgements We are grateful to Yaping This newly described species may not be uncommon ZHANG (KIZ) and Huijian HU (South China Institute along its range, but it is restricted to a narrow elevation of Endangered , China), for their support to range between 1300 m to 2100 m. Unfortunately, within this research, and Patrick DAVID (Muséum National its distribution area in India, the active period of P. d’Histoire Naturelle, Paris, France) for his help in many himalayanus sp. nov. coincides with the peak tourist ways for this research. We thank Junxiao YANG (KIZ), season (Government of Sikkim, 2012), resulting a high Haihua QIN, Youling BAO (South China Institute of route-killing rate. Two to three snakes on average are Endangered Animal, China), Jingjing LI (Southwest killed per night in the vicinity of Chungthang, northern Forestry University, China) and all the other people Sikkim. In addition, expanding habitat destruction around who assisted with our fieldwork. We also thank Yunke agricultural land reduces the natural shelters of snakes, WU (Harvard University, USA.) and Mian HOU making snakes more vulnerable to human activities. (Sichuan Normal University, China) for providing Habitat conservation and public educational programs literatures; we thank S. Bhupathy (Principal Scientist of should be conducted to protect the restricted habitats for Sálim Ali Centre for Ornithology and Natural History, the new species, and continuing field surveys are needed Coimbatore, India) for guidance and B. K. Acharya to obtain more accurate data for its population size and (Sikkim Government College, Tadong, Gangtok, India) for constant support and encouragement. Jigme Tshelthrim WANGYAL (District Forest Office, District Administration, Trashigang, Bhutan) supported us with data from Bhutan. Jane HANCOCK was so kind to contribute pictures of a specimen of the new species from Bhutan. We are grateful to the Forests, Environment and Wildlife Management Department, and Government of Sikkim, India, for the necessary permission to carry out this research. Assistance and cooperation rendered by the residents of northern Sikkim are acknowledged. Jens V. VINDUM and Alan E. LEVITON (CAS) were so kind to let us examine specimens under their care. Gerrut NORVAL (Department of Environmental Sciences, UNISA, Republic of South Africa) and Theodore J. Figure 7 Protobothrops kaulbacki in life (KIZ 011065, adult male PAPENFUSS (Museum of Vertebrate Zoology, University from Medog, southeastern Tibet, China. 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