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A New Moth-Preying Alpine Pit Viper Species from Qinghai-Tibetan Plateau (Viperidae, Crotalinae)

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Amphibia-Reptilia 38 (2017): 517-532 A new moth-preying alpine pit viper species from Qinghai-Tibetan Plateau (Viperidae, Crotalinae) Jingsong Shi1,2,∗, Gang Wang3, Xi’er Chen4, Yihao Fang5,LiDing6, Song Huang7,MianHou8,9, Jun Liu1,2, Pipeng Li9 Abstract. The Sanjiangyuan region of Qinghai-Tibetan Plateau is recognized as a biodiversity hotspot of alpine mammals but a barren area in terms of amphibians and reptiles. Here, we describe a new pit viper species, Gloydius rubromaculatus sp. n. Shi, Li and Liu, 2017 that was discovered in this region, with a brief taxonomic revision of the genus Gloydius.The new species can be distinguished from the other congeneric species by the following characteristics: cardinal crossbands on the back, indistinct canthus rostralis, glossy dorsal scales, colubrid-like oval head shape, irregular small black spots on the head scales, black eyes and high altitude distribution (3300-4770 m above sea level). The mitochondrial phylogenetic reconstruction supported the validity of the new species and furthermore reaffirms that G. intermedius changdaoensis, G. halys cognatus, G. h. caraganus and G. h. stejnegeri should be elevated as full species. Gloydius rubromaculatus sp. n. was found to be insectivorous: preying on moths (Lepidoptera, Noctuidae, Sideridis sp.) in the wild. This unusual diet may be one of the key factors to the survival of this species in such a harsh alpine environment. Keywords: Gloydius rubromaculatus sp. n., insectivorous, new species, Sanjiangyuan region. Introduction leopards (Uncia uncia), wild yaks (Bos grun- niens) and Tibetan antelopes (Pantholops hodg- The Sanjiangyuan region (the Source of Three sonii) (Shen and Tan, 2012). However, the her- Rivers region) lies in the southern part of Qing- petological diversity here is quite low due to hai Province, along the eastern part of Qinghai- the harsh conditions for sustaining life (e.g. Tibetan Plateau with an area covering 0.36 mil- low temperatures, low oxygen levels, and in- lion km2. It encompasses the headwaters of tense solar radiation). To date, only ten rep- the Yellow River, the Yangtze River, and the tile species have been recorded (Li et al., 1989; Mekong River. The Sanjiangyuan region is rich Zhao et al., 1998), within which are three snake in biodiversity of alpine mammals, such as snow species (Gloydius strauchi, Gloydius cognatus and Elaphe dione). In this study, a new species 1 - Key Laboratory of Vertebrate Evolution and Human of Asian pit viper (Gloydius) has been discov- Origins of Chinese Academy of Sciences, Institute of ered along the Tongtianhe River at the elevation Vertebrate Paleontology and Paleoanthropology, Chi- up to 4770 m. nese Academy of Science, 100044 Beijing, China Asian pit vipers are small venomous snakes 2 - University of Chinese Academy of Sciences, 100044 Beijing, China distributed mainly in Asia. They are widely 3 - Chengdu Normal University, 611130 Chengdu, China recognized to be one of the most successfully 4 - College of Life Sciences, Peking University. 100871 evolved snake groups, which radiated into vari- Beijing, China ous habitats, such as subfrigid forests (G. halys), 5 - Institute of Eastern-Himalaya Biodiversity Research, Dali University, 671003 Dali, China alps or plateaus (G. strauchi, G. himalayanus 6 - Chengdu Institute of Biology, Chinese Academy of Sci- and G. monticola), islands (G. shedaoensis ences. 610041 Chengdu, China and G. changdaoensis) and deserts (G. cogna- 7 - Huangshan University, 245000 Huangshan, China tus) (Hoge and Romano-Hoge, 1981). Asian 8 - Sichuan Normal University, 610101 Chengdu, China 9 - Institute of Herpetology, Shenyang Normal University, pit vipers hold the record for the highest alti- 110034 Shenyang, China tude distribution within venomous snakes (G. ∗Corresponding author; e-mail: [email protected] himalayanus, above 4880 m; Sharma et al., Downloaded from Brill.com10/07/2021 08:28:56AM via free access © Koninklijke Brill NV, Leiden, 2017. DOI:10.1163/15685381-00003134 518 J. Shi et al. 2013) and the highest population density within and G. liupanensis. Thus, a further investigation the suborder of Serpentes (G. shedaoensis, is required to clarify the taxonomic relationship 20 281 snakes within 0.73 km2, express as about between the different taxa of this complex. 0.028/m2, based on the pit viper population sur- vey conducted by the Snake Island National Na- ture Reserve; Li et al., 2007). Taking advan- Material and methods tage of their heat sensitive pits, most Asian pit We examined preserved specimens from Chengdu Insti- vipers tend to prey on small endotherms. As tute of Biology (CIB), Northwest Institute of Plateau Bi- well, some of them are reported to be insectivo- ology (NWIPB) and Kunming Institute of Zoology (KIZ). Newly obtained specimens collected were preserved in 75% rous (Gloyd and Conant, 1990; Zhao, 2006). ethanol and deposited at Institute of Zoology (IOZ), North- Based on previous taxonomy (Orlov and west Institute of Plateau Biology (NWIPB) (table 1). Barabanov 1999; Xu et al., 2012; Shi et al., 2016; Wagner et al., 2016), the genus Gloydius Institutional abbreviations could be preliminarily divided into the follow- IVPP: Institute of Vertebrate Paleontology and Paleoanthro- ing complexes (groups): pology; CIB: Chengdu Institute of Biology; IOZ: Institute 1. Gloydius halys-intermedius complex (G. of Zoology; NWIPB: Northwest Institute of Plateau Biol- ogy; SYNU: Shenyang Normal University; KIZ: Kunming halys, G. intermedius, G. changdaoensis, Institute of Zoology. (IVPP, CIB, IOZ and NWIPB are be- G. rickmersi, G. cognatus, G. stejnegeri longing to Chinese Academy of Science.) and G. shedaoensis). 2. Gloydius blomhoffii complex (G. blomhof- Morphology fii, G. brevicaudus, G. tsushimaensis and Measurements were taken with vernier calliper (Guanglu, G. ussuriensis). 0-200 mm, Made in China). Snout-vent length (SVL), tail length (TL) and total length (TTL = SVL + TL) are 3. Gloydius strauchi complex (G. strauchi, measured to the nearest 0.1 mm; head length (HL, from the G. monticola, G. qinlingensis G. liupanen- tip of snout to the posterior margin of mandible), head width sis and G. himalayanus). (HW, from the posterior jaw, which is the widest part of the head), head height (HH, the highest part of the head), eye The members of Gloydius strauchi complex diametre (ED, horizontal distance), interorbital space (IOS), are generally described as an alpine group with and internasal space (INS). We took counts of supralabials 21 dorsal scale rows (except for 19 rows in G. (SPL), infralabials (IFL), dorsal scales (DS), ventral scales (V) and subcaudal scales (Sc). Dimensions and scale data monticola) and three palatine teeth, distributed are listed in table 2. along the north of the Hengduanshan Moun- tains (Zhao and Yang, 1997). The taxonomy on X-ray micro-computerized tomography this group is still controversial: some regard G. The scanning was carried out with the 225 kV micro- monticola as a full species (Gloyd and Conant, computerized tomography (developed by the Institute of 1990; Wagner et al., 2016), while others suggest High Energy Physics (IHEP), Chinese Academy of Sciences that G. monticola should be attributed to one (CAS)) at the Key Laboratory of Vertebrate Evolution and Human Origins, CAS. Specimens were scanned at 140 kV of the subspecies of G. strauchi and deny the with a flux of 100 μA at a resolution of 42.3 μmperpixel validity of qinlingensis and liupanensis (Zhao, using a 360° rotation with a step size of 0.5° and an unfil- 1998; Zhao, 2006). Xu et al. (2012) conducted tered aluminium reflection target. A total of 720 transmis- sion images were reconstructed into the 2048 × 2048 ma- the molecular phylogeny of the genus Gloydius trix of 1536 slices using a two-dimensional reconstruction and suggested that G. qinlingensis and G. li- software developed by IHEP, CAS. upanensis should be regarded as full species. However, the topological structures of the max- Laboratory protocols imum likelihood (ML), maximum parsimony Specimens were fixed in 95% ethanol or 10% formalin. (MP) and Bayesian inference (BI) trees differ Shed skin and scale tissues were preserved in 98% ethanol for molecular study. Genomic DNA was extracted with significantly, with primary differences indicated Miniprep Kit (Axygen). Samples included in this study are by the positions of G. qinlingensis, G. strauchi listed in table 1. Downloaded from Brill.com10/07/2021 08:28:56AM via free access A new alpine pit viper species Table 1. Details of the molecular samples for this study. Museum voucher Code Taxa Locality GenBank Accession Numbers Reference 12s 16s Cytb ND4 JSSD1408Z1 Z1 G. changdaoensis Lianyungang, Jiangsu KY040521 KY040553 KX063821 KX063794 this study JSSD1510C1 C1 G. changdaoensis Changdao, Shandong KY040522 KY040554 KX063823 KX063796 this study JSSD11110D2 D2 G. shedaoensis Lvshun, Liaoning KY040523 KY040555 KX063819 KX063792 this study JS150622 22 G. intermedius Zhuanghe, Liaoning KY040524 KY040556 KY040617 KY040638 this study JSSD1110Q4 Q4 G. intermedius Wafangdian, Liaoning KY040525 KY040557 KX063793 KX063820 this study QS002 QS002 G. intermedius Anshan, Liaoning JX661216 / JX661205 JX661228 Wu et al. (2015) –SX1G. intermedius Heilongjiang KM434236 KM434236 KM434236 KM434236 Xu et al. (2012) SYNU1301908 46 G. h. halys Lingyuan, Liaoning KY040526 KY040558 KX063802 KX063775 this study JSSD1508X3 X3 G. h. halys Xilinhot, Inner KY040527 KY040559 KX063803 KX063776 this study Mongolia JS1407H9 H9 G. h. halys Greater Hinggan Mts., KY040528
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    Sacred Heart University DigitalCommons@SHU Biology Faculty Publications Biology 9-2007 Eleutherodactylus ridens (Pygmy Rainfrog) Predation Tobias Eisenberg Twan Leenders Sacred Heart University Follow this and additional works at: https://digitalcommons.sacredheart.edu/bio_fac Part of the Population Biology Commons, and the Zoology Commons Recommended Citation Eisenberg, T. & Leenders, T. (2007). Eleutherodactylus ridens (Pygmy Rainfrog) predation. Herpetological Review, 38(3), 323. This Article is brought to you for free and open access by the Biology at DigitalCommons@SHU. It has been accepted for inclusion in Biology Faculty Publications by an authorized administrator of DigitalCommons@SHU. For more information, please contact [email protected], [email protected]. SSAR Officers (2007) HERPETOLOGICAL REVIEW President The Quarterly News-Journal of the Society for the Study of Amphibians and Reptiles ROY MCDIARMID USGS Patuxent Wildlife Research Center Editor Managing Editor National Museum of Natural History ROBERT W. HANSEN THOMAS F. TYNING Washington, DC 20560, USA 16333 Deer Path Lane Berkshire Community College Clovis, California 93619-9735, USA 1350 West Street President-elect [email protected] Pittsfield, Massachusetts 01201, USA BRIAN CROTHER [email protected] Department of Biological Sciences Southeastern Louisiana University Associate Editors Hammond, Louisiana 70402, USA ROBERT E. ESPINOZA CHRISTOPHER A. PHILLIPS DEANNA H. OLSON California State University, Northridge Illinois Natural History Survey USDA Forestry Science Lab Secretary MARION R. PREEST ROBERT N. REED MICHAEL S. GRACE R. BRENT THOMAS Joint Science Department USGS Fort Collins Science Center Florida Institute of Technology Emporia State University The Claremont Colleges Claremont, California 91711, USA EMILY N. TAYLOR GUNTHER KÖHLER MEREDITH J. MAHONEY California Polytechnic State University Forschungsinstitut und Illinois State Museum Naturmuseum Senckenberg Treasurer KIRSTEN E.