New amphibian and reptile records from Ha Giang Province, northern Vietnam

Herpetology Notes, volume 7: 185-201 (2014) (published online on 16 April 2014) New amphibian and reptile records from Ha Giang Province, northern Vietnam Thomas Ziegler1,2, Dao Thi Anh Tran3,4, Truong Quang Nguyen2,5, Ronith Gila Bina Perl2,6 Lea Wirk2, Magdalena Kulisch2, Tanja Lehmann1,7, Anna Rauhaus1, Tao Thien Nguyen8, Quyet Khac Le9,10 and Thanh Ngoc Vu9 Abstract Based on herpetological surveys conducted between December 2006 and May 2008 in the Tung Vai forest, Quan Ba District, Ha Giang Province, northern Vietnam we recorded eight amphibian species (Hyla annectans, Babina chapaensis, Odorrana cf jingdongensis, O junlianensis, Gracixalus cf jinxiuensis, Rhacophorus duboisi, R feae, and R robertingeri) and twelve reptile species (Gekko cf palmatus, Sphenomorphus indicus, Cyclophiops major, C multicinctus, Euprepiophis mandarinus, Lycodon meridionalis, Oligodon chinensis, Oreocryptophis porphyraceus, Orthriophis taeniurus, Pseudoxenodon macrops, Rhabdophis subminiatus, and Sinomicrurus macclellandii) for the first time for that province Based on our recent findings together with literature surveys we provide an updated herpetofaunal list for Ha Giang Province, in total comprising 102 species (50 species of amphibians, and 52 species of reptiles) Keywords Herpetofauna, northern Vietnam, Ha Giang Province, morphology, taxonomy, distribution, first record Introduction Although Vietnam is in the focus of herpetological research since decades (e.g., Nguyen, 2006; Nguyen et al., 2009), there still remains a considerable number of new records and even species descriptions regularly being published from this country (e.g., Bain, Nguyen and Doan, 2007; Ziegler and Nguyen, 2010) Recent research in the Vietnamese-Chinese border region has revealed a number of species descriptions (e.g., David et al., 2012; Nguyen et al., 2010a, 2011b, 2012, 2013a, b) which clearly underlines the poor research state of these forested regions One of these poorly studied regions in northeastern Vietnam near the Vietnamese-Chinese border is Ha Giang Province Only a few studies have been conducted in this province so far Most important is the recent overview of Bain and Nguyen (2004), describing two new species from that province including a first provincial herpetofaunal list with 36 recorded species of amphibians (33 identified and unknown species) and 16 recorded species of reptiles Further new herpetofaunal records for Ha Giang Province were published by Ziegler et al (2006b), Le and Ziegler (2009), Nguyen, Ho and Nguyen (2009) and Nguyen et al (2010b) Most recently, Ohler et al (2011) described the megophryid anuran species Leptolalax nyx from Ha Cologne Zoo, Riehler Straße 173, 50735 Cologne, Germany Zoological Institute, University of Cologne, Zülpicher Str 47 b, 50674 Cologne, Germany University of Science, Vietnam National University, Ho Chi Minh City, 227 Nguyen Van Cu, District 5, Ho Chi Minh City, Vietnam Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam Zoological Institute, Technical University of Braunschweig, Mendelssohnstr 4, 38106 Braunschweig, Germany Rheinische Friedrich-Wilhelms-Universität Bonn, Germany Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam Faculty of Biology, University of Science, Vietnam National University, 334 Nguyen Trai Str., Thanh Xuan, Hanoi, Vietnam 10 University of Colorado Boulder, Colorado 80309, USA 186 Giang Province, and Nishikawa, Matsui and Nguyen (2013) described a new salamander species, Tylototriton ziegleri, from the northern provinces of Cao Bang and Ha Giang pointing again towards the necessity of ongoing research in these regions As a result of recent field work in the Tung Vai forest in Ha Giang between 2006 and 2008 we herein provide new records of amphibians and reptiles including an updated checklist of the herpetofauna known from Ha Giang Material and methods Field surveys were conducted by Quyet Khac Le and Thanh Ngoc Vu in the Tung Vai forest, Quan Ba District, Ha Giang Province (Fig 1), northern Vietnam between December 2006 and May 2008 The typical habitat consisted of evergreen broad-leaved forest on limestone affected by cultivation of cardamom (Amomum tsaoko) Surveys were taken place along forest paths and streams Specimens were photographed in the field and Thomas Ziegler et al subsequently released, or collected and photographed prior to preservation Specimens were fixed in 4% formalin or in 40-60% ethanol (amphibians) and 90% ethanol (reptiles) and subsequently transferred in 70 % ethanol for permanent storage Specimens referred to in this paper were deposited in the following collections: Institute of Ecology and Biological Resources (IEBR), Hanoi, Vietnam; Zoological Museum, Vietnam National University Hanoi (VNUH), Vietnam; Vietnam National Museum of Nature (VNMN), Hanoi, Vietnam; and Zoologisches Forschungsmuseum Alexander Koenig, Bonn (ZFMK), Germany A total of 25 specimens of amphibians were collected (Leptobrachium chapaense IEBR A.2013.94, ZFMK 95471; Xenophrys major ZFMK 95472; Hyla annectans IEBR A.2013.93, ZFMK 95473; Limnonectes cf bannaensis IEBR A.2013.95, A.2013.96, VNUH 19.11.04-1, ZFMK 95474; Quasipaa spinosa IEBR A.2013.97, VNUH 19.11.04-2, ZFMK 95475; Babina chapaensis IEBR A.2013.98, ZFMK 95476; Odorrana Figure (A) Map showing the location of Ha Giang Province in northern Vietnam; (B, C) Tung Vai forest, Quan Ba District, Ha Giang Province, where surveys were conducted 187 New amphibian and reptile records from Ha Giang Province, northern Vietnam chloronota ZFMK 95477; Odorrana cf jingdongensis ZFMK 95478; Odorrana junlianensis ZFMK 95479; Gracixalus gracilipes ZFMK 93670; G cf jinxiuensis IEBR A.2013.99, ZFMK 93668-9; Rhacophorus duboisi IEBR A.2013.100, ZFMK 95481; R robertingeri ZFMK 95480; Theloderma asperum IEBR A.2013.101, ZFMK 95482) and 10 specimens of reptiles (Acanthosaura lepidogaster ZFMK 95483; Sphenomorphus indicus ZFMK 95484; Cyclophiops major ZFMK 95485; Oligodon chinensis ZFMK 95486; Pseudoxenodon macrops IEBR A.2013.102, ZFMK 95487; Rhabdophis subminiatus ZFMK 95488; Ovophis tonkinensis ZFMK 95489-95490; Sinomicrurus macclellandii VNMN 899) (see Tables 1-3) Taxonomic identifications were based on Boulenger (1893), Smith (1943), Bourret (1936, 1942, 2009), Liu (1950), Taylor (1962), Schulz (1996), Ohler et al (2000), Ziegler (2002), Bain et al (2003), Bain and Stuart (2006), Ziegler et al (2006a, 2007), Bourret (2009), Chuaynkern et al (2010), Nguyen et al (2011a), and Orlov et al (2012) Nomenclature for amphibians followed Bain et al (2009), McLeod (2010), Yu, Zhang and Yang (2010), Ohler et al (2011), Frost (2013), and Nishikawa et al (2013); for reptiles Nguyen et al (2009), Rösler et al (2011), and Luu et al (2013) Systematics and common names followed Nguyen et al (2009) and Tran et al (2010) unless otherwise stated For amphibians, all measurements for morphological analyses were taken with a digital caliper to the nearest 0.1 mm Measurements of anurans were performed as follows: snout-vent length (SVL), from tip of snout to urostyle; head length (HL); head width (HW); snout length (SNL); horizontal eye diameter (ED); horizontal tympanum diameter (TD); interorbital distance (IO); width of upper eyelid (UEW); thigh length (THL); tibia length (TBL); webbing formula followed Myers and Duellman (1982) For reptiles, all measurements except for body and tail lengths were taken with a caliper to the nearest 0.1 mm Body and tail lengths were measured with a caliper to the nearest 1.0 mm Abbreviations are as follows: snout-vent length (SVL), from tip of snout to vent; tail length (TaL), from vent to tip of tail; dorsal scale formula (DSF): dorsal scale rows one head length behind the head : at midbody : one head length anterior to the vent The number of ventral scales was counted according to Dowling (1951) Bilateral scales counts are given as right/left Scale counts and measurements are lacking for those specimens which were photographed and directly released into the field afterwards Sex was determined by examination of secondary sexual characters and sex of collected specimens lacking distinct secondary sexual characters was determined by gonad inspection Table Measurements (in mm) of newly recorded anuran species from Ha Giang Province, northern Vietnam (n: number of investigated specimens) SVL Hyla annectans HL HW SNL ED TD IO/UEW THL TBL 35.4–38.2 11.2–11.6 12.0–13.3 4.9–5.1 4.0–4.4 2.3–2.3 1.1–1.2 17.1–18.3 19.2–18.44 42.1–48.8 19.7–21.0 15.2–17.6 6.9–8.6 5.7–5.9 4.6–4.8 1.2–1.4 18.3–21.1 20.5–25.4 (n = 2) Babina chapaensis (n = 2) Odorrana cf jingdongensis 38.6 15.4 13.4 6.3 5.8 2.4 0.9 20.2 23.1 70.4 28.3 26.1 11.6 10.1 3.8 1.1 42 47.455 30.9–32.0 11.1–11.5 11.7–12.6 5.4 4.4 1.8–1.9 1.2–1.3 13.3–14.5 15.2–15.7 60.3–61.5 21.9–23.4 20.8–21.8 9.2–10.7 7.1–8.3 4.9–5.1 1.2–1.3 30.8–30.9 29.6–29.8 7.4 5.6 2.7 1.5 (n = 1) O junlianensis (n = 1) Gracixalus cf jinxiuensis (n = 2) Rhacophorus duboisi (n = 2) R robertingeri (n = 1) 40.3 16.5 16.8 22.22 22.57 188 Thomas Ziegler et al Table List of amphibian species recorded from Ha Giang Province, Vietnam (new provincial records in bold Data sources: 1: Bain and Nguyen (2004), 2: Nguyen et al (2009), 3: This study, 4: Nishikawa et al (2013), 5: Ohler et al (2011),*: species considered as complex of cryptic species; IUCN categories: EN: Endangered; NT: Near Threatened; VU: Vulnerable); **: R calcaneus (see chapter of R robertingeri) was listed as NT; nomenclature followed Bain et al (2009), McLeod (2010), Yu et al (2010), Ohler et al (2011), Frost (2013), Luu et al (2013) and Nishikawa et al (2013) 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 Taxon Order Caudata Salamandridae Tylototriton ziegleri Nishikawa, Matsui & Nguyen, 2013 Order Anura Bombinatoridae Bombina maxima (Boulenger, 1905) Bufonidae Duttaphrynus melanostictus (Schneider, 1799) Megophryidae Brachytarsophrys cf feae (Boulenger, 1887) Leptobrachium chapaense (Bourret, 1937)* Leptolalax nyx Ohler, Wollenberg, Grosjean, Hendrix, Vences, Ziegler & Dubois, 2011 Leptolalax sp Xenophrys major (Boulenger, 1908) Xenophrys palpebralespinosa (Bourret, 1947) Xenophrys parva (Boulenger, 1894) Ophryophryne microstoma Boulenger, 1904 Microhylidae Microhyla butleri Boulenger, 1900 Microhyla heymonsi Vogt, 1911 Microhyla pulchra (Hallowell, 1861) Microhyla sp Hylidae Hyla annectans (Jerdon, 1870) Dicroglossidae Fejervarya limnocharis (Gravenhorst, 1829) * Hoplobatrachus rugulosus (Wiegmann, 1834) Limnonectes cf.bannaensis Je, Fei & Jiang, 2007 * Nanorana delacouri (Angel, 1918) Quasipaa boulengeri (Günther, 1889) Quasipaa spinosa (David, 1875) Quasipaa verrucospinosa (Bourret, 1947) Ranidae Amolops iriodes (Bain & Nguyen, 2004) Amolops ricketti (Boulenger, 1899) Babina chapaensis (Bourret, 1937) Hylarana guentheri (Boulenger, 1882) Hylarana macrodactyla Günther, 1858 Hylarana maosonensis Bourret, 1937 Hylarana taipehensis (Van Denburgh, 1909) Odorrana geminata Bain, Stuart, Nguyen, Che & Rao, 2009 Odorrana chloronota (Günther, 1876) * Odorrana cf jingdongensis Fei, Ye & Li, 2001 Odorrana junlianensis Huang, Fei & Ye, 2001 Odorrana tiannanensis (Yang & Li, 1980) * Rana johnsi Smith, 1921 Rhacophoridae Gracixalus gracilipes (Bourret, 1947) Gracixalus cf jinxiuensis (Hu, 1978)* Kurixaluscf bisacculus (Taylor, 1962)* Philautus maosonensis Bourret, 1947* Polypedates megacephalus Hallowell 1861* Raorchestes parvulus (Boulenger, 1894) Rhacophorus duboisi Ohler, Marquis, Swan & Grosjean, 2000 Rhacophorus feae Boulenger, 1894 Rhacophorus hoanglienensis Orlov, Lathrop, Murphy & Ho, 2001 Rhacophorus puerensis (He, 1999) * Rhacophorus robertingeri Orlov, Poyarkov, Vassilieva, Ananjeva, Nguyen, Nguyen & Geissler, 2012** Theloderma asperum (Boulenger, 1886) Theloderma cf corticale (Boulenger, 1903) Theloderma rhododiscus (Liu& Hu, 1962) Status Data source 1, 3, 1, 1, 2, 1, 2, 1, 2 1, 2, 1, 1, 1, 2 1,2, 1, EN VU NT VU VU 1, 1, 1, 2, 1, 1, 2, 1, 1, 1, 2 1, 1, 1, 2, 3 1, 2 1, 2, 3 2, 1, 1, 1, 3 1, NT 1, 2, 2, 1, 189 New amphibian and reptile records from Ha Giang Province, northern Vietnam Table List of reptile species recorded from Ha Giang Province, Vietnam (new provincial records in bold Data sources: 1: Bain and Nguyen (2004), 2: Nguyen et al (2009), 3: This study, 4: Ziegler et al (2006b), 5: Le and Ziegler (2009), 6: Nguyen et al (2010b), *: species considered as complex of cryptic species; IUCN categories: EN: Endangered; NT: Near Threatened; VU: Vulnerable); nomenclature followed Nguyen et al (2009, 2011a), Rösler et al (2011), and Luu et al (2013) 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 Taxon Order Squamata Gekkonidae Gekko gecko Linnaeus, 1758* Gekko cf palmatus Boulenger, 1907 Hemidactylus frenatus Duméril & Bibron, 1836 Agamidae Acanthosaura lepidogaster (Cuvier, 1829)* Physignathus cocincinus Cuvier, 1829 Lacertidae Takydromus sexlineatus Daudin, 1802 Scincidae Ateuchosaurus chinensis Gray, 1845 Eutropis longicaudatus (Hallowell, 1856) Eutropis multifasciatus (Kuhl, 1820) Plestiodon chinensis (Gray, 1838) Plestiodon tamdaoensis (Bourret, 1937) Scincella reevesii (Gray, 1838) Sphenomorphus indicus (Gray, 1853) Tropidophorus hainanus Smith, 1923 Anguidae Dopasia harti (Boulenger, 1899) Order Serpentes Colubridae Ahaetulla prasina (Boie, 1827) Amphiesma modestum (Günther, 1875) Amphiesma khasiense (Boulenger, 1890) Calamaria septentrionalis Boulenger, 1890 Coelognathus radiatus Boie, 1827 Cyclophiops major (Günther, 1858) Cyclophiops multicinctus (Roux, 1907) Dendrelaphis ngansonensis (Bourret, 1935) Dendrelaphis pictus (Gmelin, 1789) Enhydris plumbea (Boie, 1827) Euprepiophis mandarinus (Cantor, 1842) Lycodon meridionalis (Bourret, 1935) Oligodon chinensis (Günther, 1888) Oligodon taeniatus (Günther, 1861) Oreocryptophis porphyraceus (Cantor, 1839) Orthriophis taeniurus (Cope, 1861) Pareas hamptoni (Boulenger, 1905) Pseudoxenodon bambusicola Vogt, 1922 Pseudoxenodon karlschmidti Pope, 1928 Pseudoxenodon macrops (Blyth, 1854) Ptyas korros (Schlegel, 1837) Rhabdophis subminiatus (Schlegel, 1837) Sinonatrix aequifasciata (Barbour, 1908) Sinonatrix percarinata (Boulenger, 1899) Xenochrophis flavipunctatus (Hallowell, 1860) Elapidae Sinomicrurus macclellandii (Reinhardt, 1844) Viperidae Ovophis tonkinensis (Bourret 1934) Protobothrops cornutus (Smith, 1930) Protobothrops mucrosquamatus (Cantor, 1839) Trimeresurus stejnegeri Schmidt, 1925 Order Testudines Platysternidae Platysternon megacephalum Gray, 1831 Geoemydidae Cuora mouhotii (Gray, 1862) Mauremys mutica (Cantor, 1842) Sacalia quadriocellata (Siebenrock, 1903) Testudinidae Manouria impressa (Günther, 1882) Trionychidae Palea steindachneri (Siebenrock, 1906) Status Data source 1, 1, 2 2 2 2, 1, 1, 1, 1, 1, 1, 2 3 2 2, 3 1, 3 1, 2, 2, 1, 1, 1, 1, 2 NT 2, 2, 3, EN EN EN EN 2 VU EN 190 Results Anura Hylidae Hyla annectans (Jerdon, 1870) Assam Treefrog / Nhai ben dinh (Fig 2) Specimens examined (n = 2): adult females (IEBR A.2013.93, ZFMK 95473) Distribution: Vietnam: Lao Cai, Vinh Phuc, and Thua Thien-Hue provinces Elsewhere: India, China, Myanmar, and Thailand (Nguyen et al., 2009) Morphological features of examined specimens: SVL 35.4–38.2 mm; head broader than long; snout rounded anteriorly, its length longer than eye diameter; interorbital space broader than upper eyelid width; tympanum distinct, half the diameter of the eye, but larger than the interorbital distance; supratympanic fold distinct, granular; tongue slightly notched posteriorly; Thomas Ziegler et al tips of fingers and toes with discs; fingers webbed at base and bearing lateral fringes, formula: I2–2½II2–3III2½–2IV; webbing between toes more developed than between fingers, formula: I22ẳII1ẵ3III23IV2ắ2V; relative lengths of fingers: I=II