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Herpetology Notes, volume 7: 771-777 (2014) (published online on 21 December 2014). New records of snakes (Squamata: Serpentes) from. Son La Province ...
Herpetology Notes, volume 7: 771-777 (2014) (published online on 21 December 2014)

New records of snakes (Squamata: Serpentes) from Son La Province, Vietnam Anh Van Pham1,2, Son Lan Hung Nguyen2 and Truong Quang Nguyen3,*

Abstract. We report seven new records of snake species from Son La Province, northwestern Vietnam on the basis of a new reptile collection from Copia Nature Reserve (Thuan Chau District) and Son La City, comprising six species of Colubridae (Cyclophiops multicinctus, Gonyosoma frenatum, G. prasinum, Liopeltis frenatus, Oligodon catenatus, and O. chinensis) and one species of Pseudoxenodontidae (Pseudoxenodon macrops). Our findings bring the species number of snakes to 51 in Son La Province. Keywords. Colubridae, Pseudoxenodontidae, distribution, taxonomy, Copia Nature Reserve, Son La City.

Introduction In the recent checklist of the herpetofauna of Vietnam, Nguyen, Ho and Nguyen (2009) listed 192 species of snakes. Since then one new genus (Colubroelaps Orlov, Kharin, Ananjeva, Nguyen and Nguyen, 2009), 13 new species and one new subspecies of snakes have been described in Vietnam, viz. Calamaria gialaiensis Ziegler, Nguyen and Nguyen, 2008; Calamaria abramovi Orlov, 2009; Colubroelaps nguyenvansangi Orlov, Kharin, Ananjeva, Nguyen and Nguyen, 2009; Lycodon ruhstrati abditus Vogel, David, Pauwels, Sumonth, Norval, Hendrix, Vu and Ziegler, 2009; Protobothrops trungkhanhensis Orlov, Ryabov and Nguyen, 2009; Calamaria concolor Orlov, Nguyen, Nguyen, Ananjeva and Ho, 2010, Calamaria sangi Nguyen, Koch and Ziegler, 2010, Emydocephalus szczerbaki Dotsenko, 2010; Opisthotropis cucae David, Pham, Nguyen and Ziegler, 2011; Trimeresurus rubeus (Malhotra, Thorpe, Mrinalini and Stuart, 2011); Homalopsis mereljcoxi

Murphy, Voris, Murthy, Traub and Cumberbatch, 2012; Oligodon nagao David, Nguyen, Nguyen, Jiang, Chen, Teynié and Ziegler, 2012; Oligodon cattienensis Vassilieva, Geissler, Galoyan, Poyarkov, Van Devender and Böhme, 2013; and Azemiops kharini Orlov, Ryabov & Nguyen, 2013. In addition, nine new country records of snakes have reported from the country, comprising two species of Colubridae, one species of Homalopsidae, and six species of Elapidae (Vogel et al., 2009; Nguyen et al., 2010; Rasmussen et al., 2011; Murphy et al., 2012a). In Son La Province, Nguyen, Ho and Nguyen (2009) documented a total of 38 species of snakes. Pham et al. (2013) recently recorded five species of colubrids and one species of viper for the first time from Son La Province. In this paper, we report seven new records of snakes for Son La Province based on newly collected materials from Copia Nature Reserve (Thuan Chau District) and Son La City. Material and Methods

Faculty of Biology and Chemistry, Tay Bac University, Quyet Tam Ward, Son La City, Son La Province, Vietnam. E-mail: [email protected] 2 Faculty of Biology, Hanoi National University of Education, 136 Xuan Thuy Street, Cau Giay District, Hanoi, Vietnam. E-mail: [email protected]­ 3 Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, Vietnam. E-mail: [email protected] * Corresponding author 1

Field surveys were conducted in the Copia Nature Reserve (NR), Thuan Chau District and on the outskirts of Son La City, Son La Province, northwestern Vietnam (Fig. 1) by Anh Van Pham, Tan Van Nguyen, Ngoc Thi Bich Nguyen, Men Thi Nguyen, and Hoang Van Tu (hereafter AVP et al.) between June 2013 and August 2014. Specimens were collected by hand or snake hook between 9:00–23:00. After taking photographs, specimens were anaesthetized in a closed vessel with a piece of cotton wool containing ethyl acetate, fixed in 85% ethanol and subsequently stored in 70% ethanol.

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Figure 1. Map showing the survey site (black square) in Son La Province, northwestern Vietnam.

Specimens were deposited in the collections of the Faculty of Biology and Chemistry, Tay Bac University (TBU), Son La Province, Vietnam. Abbreviation are as follows: SVL (snout-vent length): from tip of snout to anterior margin of cloaca; TaL (Tail length): from posterior margin of cloaca to tip of tail; a.s.l.: above sea level. Bilateral scale counts were given as left/right.

Anh Van Pham et al. Bom Commune, Copia NR, Thuan Chau District, Son La Province (21°23.460’N, 103°37.732’E, elevation 1260 m a.s.l.). Morphological characters. Body cylindrical; head moderately distinct from neck; eye large, pupil round; rostral as broad as high, partly visible from above; internasal not in contact with loreal; prefrontal as long as half of frontal; parietals longer than wide; nasal undivided; loreal 1/1, not contact with orbit; preocular 1/1; postoculars 2/2, bodering anterior temporals; anterior temporal 1/1, posterior temporals 2/2; subpralabials 7/7, fourth and fifth touching the eye, sixth largest; infralabials 6/6, first to fourth bordering chin shields; dorsal scale rows 15–15–15, smooth; ventrals 180; cloacal scale paired; subcaudals 93, paired. Coloration in preservative. Dorsal surface green anteriorly, grey posteriorly, with whitish cross–bars on the posterior half of the body and tail; belly whitish green anteriorly, grey posteriorly (determination after Smith 1943). Ecological notes. The adult female was collected at 20:00 on tree branch, ca. 1.2 m above on the forest floor, near a stream. The surrounding habitat was evergreen secondary forest. Distribution. In Vietnam, this species has been recorded from Lai Chau and Lao Cai provinces in the North southwards to Kon Tum and Lam Dong provinces (Nguyen et al., 2009). Elsewhere, this species is known from China and Laos (Nguyen et al., 2009). Remarks. The specimen from Son La differs from the description of Smith (1943) in having more ventrals (180 versus 164–177).

Results Taxonomic accounts Family Colubridae Cyclophiops multicinctus (Roux, 1907) Many-banded Green Snake / Ran nhieu dai (Fig. 2) Specimen examined (n = 1). One adult female TBU PAR.183 (SVL 845 mm, TaL 260 mm) collected by AVP et al., 19 June 2014, near Huoi Pu Village, Chieng

Figure 2. Cyclophiops multicinctus (TBU PAR.183, adult female) from Son La Province.

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New records of snakes from Son La Province, Vietnam

Figure 3. Gonyosoma frenatum (TBU PAR.154, adult female) from Son La Province, Vietnam.

Figure 4. Gonyosoma prasinum (TBU PAR.86, adult female) from Son La Province, Vietnam.

Gonyosoma frenatum (Gray, 1853) Khasi Rat Snake / Ran soc ma (Fig. 3)

The surrounding habitat was evergreen secondary forest. Distribution. In Vietnam, this species has been recorded from Lao Cai, Lang Son, Vinh Phuc and Quang Binh provinces (Nguyen et al., 2009). This species is also known from China and India (Nguyen et al., 2009).

Specimens examined (n = 3). Three specimens collected by AVP et al. near Nong Vai Village (21°19.953’N, 103°35.283’E, elevation 1470 m a.s.l.), Co Ma Commune, Copia NR, Thuan Chau District, Son La Province: TBU PAR.114 (SVL: 234 mm, TaL: 90 mm), subadult female, 17 August 2013 and TBU PAR.133 (SVL: 275 mm, TaL: 117 mm), subadult female, 15 September 2013; TBU PAR.154 (SVL: 860 mm, TaL: 298+ mm, tail tip lost), adult female, 17 April 2014. Morphological characters. Body subcylindrical; head distinguished from neck, rather flattened; snout elongate; pupil rounded; rostral broader than high, partly visible from above; internasals wider than long, as long as prefrontal; prefrontal approximately half length of frontal, in contact with second to third supralabials; frontal hexagonal; parietals longer than wide; nasal paired; loreal absent; supralabials 9/9, fourth to sixth touching the eye, eighth largest; infralabials 9/9 or 10/10, first to fifth bordering chin shields; preocular 1/1; postoculars 2/2, bodering anterior temporals; anterior temporals 2/2, posterior temporals 3/3; dorsal scale rows 19–19–15, smooth; ventrals 205–206; cloacal scale paired; subcaudals 133–143, paired. Coloration in preservative. Dorsal surface green or greenish grey; lateral head with a black stripe, from nasal across the eye to the neck; chin and belly white (determination after Smith, 1943). Ecological notes. The specimens were collected between 9:00 and 10:00 while moving across the road.

Gonyosoma prasinum (Blyth, 1854) Green Bush Rat Snake / Ran soc xanh (Fig. 4) Specimens examined (n = 3). Three specimens collected by AVP et al. in Copia NR, Thuan Chau Distric, Son La Province: TBU PAR.86 (SVL: 613 mm, TaL: 216 mm), adult female, 25 July 2013, near Hua Ty Village, Co Ma Commune (21°20.923’N, 103°34.834’E, elevation 1400 m a.s.l.); TBU PAR.135 (SVL: 676 mm, TaL: 253 mm), adult male, 12 October 2013, near Hua Ty B Village, Chieng Bom Commune (21°22.952’N, 103°37.986’E, elevation 1370 m a.s.l.), and TBU PAR.182 (SVL: 773 mm, TaL: 267 mm), adult male, 10 May 2014, near Nong Vai Village, Co Ma Commune (21°19.510’N, 103°35.387’E, elevation 1510 m a.s.l.). Morphological characters. Body subcylindrical; head distinguished from neck, rather flattened; snout elongate; pupil rounded; rostral broader than high, partly visible from above; internasals as wide as long, not in contact with loreal; prefrontal as long as half length of frontal; frontal pentagonal; parietals longer than wide; nasal paired; loreal 1/1; supralabials 9/9, fourth to sixth entering orbit, eighth largest; infralabials 10/10, first to fifth bordering chin shields; preocular 1/1; postoculars 2/2, bodering anterior temporals; anterior temporals

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Figure 5. Liopeltis frenatus (TBU PAR.109, adult male) from Son La Province, Vietnam.

Figure 6. Oligodon catenatus (TBU PAR.100, adult male) from Son La Province, Vietnam.

2/2, posterior temporals 2/3; dorsal scale rows 19–19– 15, keeled; ventrals 193–198 in males, 193 in female; cloacal scale paired; subcaudals 102–103 in males, 96 in the female, paired. Coloration in preservative. Dorsal surface green; upper lip and lower parts greenish white, chin and belly greenish (determination after Smith, 1943). Ecological notes. Two adult males were collected between 8:00 and 9:00 while moving across the road; one adult female were collected at ca. 21:00 on the tree, 1 m above the forest floor. The surrounding habitat was evergreen secondary forest. Distribution. In Vietnam, this species has been recorded from Lao Cai, Bac Kan, Thai Nguyen, Vinh Phuc, Nghe An, Quang Binh, and Gia Lai provinces (Nguyen et al., 2009). Elsewhere, this species is known from China, India, Myanmar, Malaysia, Thailand and Laos (Nguyen et al., 2009).

rostral distinctly broader than high, partly visible from above; internasals broader than long, not in contact with loreal; prefrontal less than half length of frontal; parietals longer than wide; nasal undivided; loreal 1/1, not contact with orbit; preocular 1/1; postoculars 2/2, bodering anterior temporals; anterior temporal 1/1, posterior temporals 2/2; subpralabials 7/7, third and fourth entering orbit, sixth largest; infralabials 8/8, first to fourth bordering chin shields; dorsal scale rows 15– 15–15, smooth; ventrals 149 in the male and 144 in the female; cloacal scale paired; subcaudals 100 in the male and 94 in the female, paired. Coloration in preservative. Dorsal surface yellowish brown with longitudinal lines on the anterior half of the body; lateral side of head with a broad black stripe, from behind the eye to the neck; upper jaw, chin and belly white (determination after Smith, 1943). Ecological notes. The adult male was collected at ca. 9:00 while moving across the road and the adult female was collected at ca. 16:00 on forest path. The surrounding habitat was evergreen secondary forest. Distribution. Liopeltis frenatus is a rare snake species in Vietnam. This species has been recorded from Lao Cai, Quang Binh, Da Nang, Gia Lai and Dong Nai provinces (Orlov et al., 2003; Nguyen et al., 2009). Elsewhere, this species is known from China, India, Myanmar, and Laos (Nguyen et al., 2009).

Liopeltis frenatus (Günther, 1858) Frenated Ringneck / Ran dai ma (Fig. 5) Specimens examined (n = 2). Two specimens collected by AVP et al. in Copia NR, Thuan Chau District, Son La Province: TBU PAR.109 (SVL 335 mm, TaL 160 mm), adult male, 16 August 2013, near Hua Ty Village, Co Ma Commune (21°20.234’N, 103°35.194’E, elevation 1460 m a.s.l.) and TBU PAR.116 (SVL 255 mm, TaL 116 mm), adult female, 29 August 2013, near Hua Ty B Village, Chieng Bom (21°21.667’N, 103°36.529’E, elevation 1510 m a.s.l.). Morphological characters. Body cylindrical; head moderately distinct from neck; eye large, pupil round;

Oligodon catenatus (Blyth, 1854) Assam Kukri Snake / Ran khiem a-sam (Fig. 6) Specimens examined (n = 4). Four specimens collected by AVP et al. in Co Ma Commune, Copia NR, Thuan

New records of snakes from Son La Province, Vietnam

Figure 7. Oligodon chinensis (TBU PAR.191, adult female) from Son La Province, Vietnam.

775 Ecological notes. Two adult males were collected between 8:00 and 9:00 while moving across the road and two adult females were collected between 9:00 and 9:30 on forest path. The surrounding habitat was evergreen secondary forest. Distribution. Oligodon catenatus is a poorly known species in Vietnam. This species has been recorded from Lao Cai and Vinh Phuc provinces (Nguyen et al., 2009). Elsewhere, this species is known from China, India, Myanmar and Cambodia (Nguyen et al., 2009). Remarks. O. catenatus is morphologically similar to O. eberharti but they can be distinguished from each other by the presence of a loreal in the latter. Oligodon chinensis (Günther, 1888) Chinese Kukri Snake / Ran khiem trung quoc (Fig. 7)

Chau District, Son La Province: TBU PAR.100 (SVL 525 mm, TaL 75 mm), adult male, 15 August 2013, and TBU PAR.117 (SVL 517 mm, TaL 61.5 mm), adult female, 30 August 2013, near Nong Vai Village (21°19.675’N, 103°33.969’E, elevation 1570 m a.s.l.); TBU PAR 120 (SVL 483 mm, TaL 55 mm), adult female, 13 September 2013, and TBU PAR.172 (SVL 527 mm, TaL 72 mm), adult male, 19 April 2014, near Co Ma Village (21°22.005’N, 103°29.596’E, elevation 1360 m a.s.l.). Morphological characters. Body cylindrical; head indistinct from neck; eye small, pupil round; rostral distinctly broader than high, visible from above; internasals absent; prefrontal shorter than frontal, in contact with the second labial; parietals longer than wide; nasal undivided; loreal absent; preocular 1/1; postoculars 1/1, bodering anterior temporals; anterior temporal 1/1; posterior temporals 2/2; supralabials 6/6, third and fourth touching the eye, fifth largest; infralabials 6/6, first to fourth bordering chin shields; dorsal scale rows 13–13–13, smooth; ventrals 179– 184 in males and 190–193 in females; cloacal scale undivided; subcaudals 31–36 in males and 30–35 in females, paired. Coloration in life. Dorsal head dark brown, dorsal surface of body greyish brown with an yellow vertebral stripe formed by a concatenation of lozenge-shaped spots, edged in black, from the neck to the end of tail; lateral side of head with three yellow oblique streaks: one in loreal region, one behind the eye and one on neck; venter red, each ventral with a black square spot at the outer end and a white spot (determination after Smith, 1943; Vassilieva et al., 2013).

Specimen examined (n = 1). One adult female TBU PAR.191 (SVL 580 mm, TaL 103 mm) collected by AVP et al., 1 August 2014, near Khoang Village, Chieng Ngan Commune, Son La City, Son La Province (21°18.540’N, 103°56.578’E, elevation 690 m a.s.l.). Morphological characters. Body cylindrical; head moderately distinct from neck; eye large, pupil round; rostral as broad as high, visible from above; internasals as broad as long; prefrontal about one-third of frontal; parietals as long as wide; nasal undivided; loreal 1/1; preocular 1/1; postoculars 1/1, bodering anterior temporals; anterior temporal 1/1; posterior temporals 2/2; subpralabials 7/8, third and fourth or fourth and fifth touching the eye, fifth or sixth largest; infralabials 7/7, first to fourth bordering chin shields; dorsal scale rows 17–17–15, smooth; ventrals 193; cloacal scale undivided; subcaudals 50, paired. Coloration in preservative. Dorsal surface of head and body yellowish brown with dark brown blotches, edged in black; dorsal head with two dark marking in ˄-shape, edged in black: a narrow one between the eyes and another one on the nape; venter cream anteriorly and pinkish posteriorly with black square spots (determination after Smith, 1943; David et al., 2008). Ecological notes. The adult female was collected at ca. 20:30 while moving on the forest floor. The surrounding habitat was secondary karst forest. Distribution. In Vietnam, this is a widespread species known from Lao Cai and Lang Son in the North southwards to Quang Binh and Gia Lai provinces (Nguyen et al., 2009). This species is also known from China (Nguyen et al., 2009).

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Figure 8. Pseudoxenodon macrops (TBU PAR.119, adult male) from Son La Province, Vietnam.

Anh Van Pham et al. Coloration in preservative. Dorsal surface brownish grey or brownish red with dark or reddish spots or short greyish cross-bars; chin and venter yellowish cream, with large black spots anteriorly (determination after Smith, 1943). Ecological notes. Two adult females were collected between 9:00 and 10:00 on the forest path; one adult female was collected at ca. 9:00 while moving across the road and another male was collected at ca. 20:00 on forest path, near a slow flowing stream. The surrounding habitat was evergreen secondary forest. Distribution. In Vietnam, this species has been recorded from Lai Chau, Lao Cai, Vinh Phuc, Nghe An, Ha Tinh, Quang Binh, Da Nang and Lam Dong provinces (Nguyen et al., 2009). This species is also known from India, Nepal, China, Myanmar, Malaysia, Thailand and Laos (Nguyen et al., 2009). Discussion

Family Pseudoxenodontiae Pseudoxenodon macrops (Blyth, 1854) Big-eyed Bamboo Snake / Ran ho xien mat to (Fig. 8) Specimens examined (n = 4). Four specimens collected by AVP et al. in Co Ma Commune, Copia NR, Thuan Chau District, Son La Province: three adult females: TBU PAR.71 (SVL: 520 mm, TaL: 116 mm), 9 June 2013; TBU PAR.89 (SVL: 480 mm, TaL: 105 mm), 1 August 2013, near Hua Ty Village (21°20.497’N, 103°35.215’E, elevation 1470 m a.s.l.); TBU PAR.103 (SVL: 540 mm, TaL: 116 mm), 15 August 2013, near Pha Khuong Village (21°21.009’N, 103°32.467’E, elevation 1370 m a.s.l.); and one adult male TBU PAR.119 (SVL: 555 mm, TaL: 135 mm), 2 September 2013, near Pha Khuong Village (21°21.296’N, 103°32.145’E, elevation 1360 m a.s.l.). Morphological characters. Body cylindrical; head distinct from neck; snout elongate; eye large, pupil rounded; rostral as broad as high, partly visible from above; internasals as wide as long, not in contact with loreal; prefrontal about a half length of frontal; frontal pentagonal; parietals longer than wide; nasal paired; loreal 1/1; supralabials 8/8, fourth to fifth entering orbit, 7 largest; infralabials 10/10, first to fifth or first to fourth bordering chin shields; preocular 1/1; postoculars 3/3, bordering anterior temporals; anterior temporals 2/2; posterior temporals 2/2; dorsal scale rows 19–17–15, keeled; ventrals 165 in the male, 155–168 in females; cloacal scale paired; subcaudals 66 in the male, 60–62 in females, paired.

Son La Province is located in the northwestern region, one of four biodiversity centres of Vietnam (Tordoff et al., 2004). Sterling et al. (2006) indicated that a wild range of elevations and the complexity of landforms have given the northwestern region of Vietnam a great diversity of natural habitats and a high level of biodiversity potential. For instance, north of the Son La Province, the Hoang Lien National Park in Lao Cai Province harbours a total of 57 species of snakes (Nguyen et al., 2009). The new records bring the total number of snake species to 51 in Son La Province and it is expected that further new records of reptiles and amphibians will be made from this province in further studies. Acknowledgements. We are grateful to the directorate of Copia Nature Reserve for support of our field work. We thank T. V. Nguyen, N. B. T. Nguyen, M. T. Nguyen, H. V. Tu (Tay Bac University) and M. A. Lau, T. A. Sung (Son La) for their assistance in the field. We thank T. Ziegler (Cologne) and two anonymous reviewers for their helpful comments. Many thanks to E. Sterling (New York) and K. Koy (Berkeley) for providing the map. Field equipment was supported by the Ideal Wild to A. V. Pham. Research of T. Q. Nguyen is funded by the National Geographic Society (Grant No. 9492–14) and the Alexander von Humboldt Foundation (VIE 114344).

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Accepted by Cynthia Prado; Managing Editor: Alessandro Morais