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A New Species of the Endemic Himalayan Genus Liurana (Anura

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A New Species of the Endemic Himalayan Genus Liurana (Anura ZOOLOGICAL RESEARCH A new species of the endemic Himalayan genus Liurana (Anura, Ceratobatrachidae) from southeastern Tibet, China, with comments on the distribution, reproductive biology, and conservation of the genus Ke Jiang1,#, Kai Wang1,2,#, Yu-Fan Wang3, Cheng Li4, Jing Che1,5,* 1 State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming Yunnan 650223, China 2 Sam Noble Oklahoma Museum of Natural History and Department of Biology, University of Oklahoma, Norman OK 73072-7029, USA 3 Zhejiang Forest Resource Monitoring Center, Hangzhou Zhejiang 310020, China 4 Funsome Nature Center, Shenzhen Guangdong 518067, China 5 Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin Nay Pyi Taw 05282, Myanmar ABSTRACT specialists, with many species undergoing direct development A new species of the genus Liurana Dubois, 1986 is without reliance on standing water bodies for breeding (Brown & Alcala, 1982; Brown et al., 2015). Within this family, frogs described from Medog County, Tibet, China, based on of the genus Liurana represent an understudied yet fascinating morphological and molecular data. The new species endemic group from the East Himalaya region. can be differentiated from all other congeners by the First considered as a subgenus of Ingerana by Dubois following combination of characters: (1) head wider (1986), Liurana was established based on the type species than long; (2) tympanum distinct and large; (3) hindlimb Cornufer xizangensis Hu, 1987, with the subgenus later long, tibiotarsal articulation beyond tip of snout when elevated to full genus based on morphological evidence (Fei et al., 1997). This taxonomic elevation is supported by adpressed; (4) belly with flat tubercles, cloacal region recent phylogenetic studies, where Liurana was recovered as with small tubercles; (5) transverse bands distinctly on a distinct monophyletic clade from Ingerana, Platymantis, and dorsal limbs, four bands on thigh and three on tibia; Cornufer (Yan et al., 2016). However, despite research efforts and, (6) dark brown marbled patterns or speckles on on the higher-level systematic relationships of the genus Liurana, white belly. Here, we also discuss the distribution pattern of Liurana in the East Himalaya region, the role of the Yarlung Tsangpo River in the speciation and genetic Received: 12 October 2018; Accepted: 24 October 2018; Online: 20 isolation of congeners, the direct developmental mode of March 2019 reproduction, and the two different ecotypes of the genus. Foundation items: This project was supported by the Strategic Lastly, we provide conservation recommendations for the Priority Research Program (A) Grant XDB13020200 of the Chinese genus in southeastern Tibet. Academy of Sciences (CAS), Ministry of Science and Technology of China (2014FY210200), China’s Biodiversity Observation Network Keywords: Advertisement call; Biogeography; Ecology; Natural history; Tibet; Taxonomy (Sino-BON), Nanjing Institute of Environmental Sciences, Ministry of Environmental Protection of China, and Animal Branch of INTRODUCTION the Germplasm Bank of Wild Species of CAS (Large Research Infrastructure Funding) As a wide-spread amphibian family in Southeast Asia, species # of the family Ceratobatrachidae are distributed from the southern Authors contributed equally to this work foothills of the Himalaya to the tropics of Southeast Asia (Yan et *Corresponding author, E-mail: [email protected] al., 2016). Members of the family are characterized as tropical DOI: 10.24272/j.issn.2095-8137.2019.025 Science Press Zoological Research 40(3): 175–184, 2019 175 little attention has been given to the species level taxonomy of the and preserved in 95% ethanol, with the specimens then fixed in group in the Himalaya. To date, only a few studies have focused 10% buffered formalin solution and transferred to 75% ethanol on species level taxonomy of the genus, with just a single study after fieldwork. All specimens were deposited in the Museum conducted in the last decade (Borah et al., 2013; Fei et al., 1997; of the Kunming Institute of Zoology, Chinese Academy of Huang & Ye, 1997; Sichuan Biological Research Institute, 1977). Sciences (KIZ) (Appendix II). As a result, all recognized species of Liurana are known from Morphological data only a few vouchered specimens, and little is understood about their morphological variation and population structure. Based on We confirmed the sex of each specimen by anatomical limited studies, three species have been recognized in the genus observation, with an incision made on the left side. All to date, including L. alpina Huang, Ye, 1997, L. medogensis Fei, measurements were carried out by Ke Jiang using a digital Ye, Huang, 1997, and L. xizangensis (Hu, 1987). caliper to the nearest 0.1 mm. Morphological characters and their measurement followed Fei et al.(2009) and included: During herpetological surveys in southeastern Tibet from snout–vent length (SVL); head length (HL), measured from 2012 to 2016, 20 specimens of the genus Liurana were posterior corner of mandible to tip of snout; head width (HW), collected from Bomê and Medog Counties of the Nyingchi measured at the angle of the jaw; snout length (SL), measured Prefecture, Tibet, China. Combining phylogenetic and from tip of snout to anterior corner of eye; internarial distance morphological datasets, we describe here a new species of the (IND); interorbital distance (IOD), measured at the shortest genus from the tropical rainforest of Medog County, Nyingchi distance between upper eyelid; maximum width of upper Prefecture, Tibet, China. Furthermore, we comment on the eyelid (UEW); eye diameter (ED), measured as the horizontal evolution, ecology, natural history, and conservation of the diameter of eye); tympanum diameter (TD), measured as the genus Liurana in China. maximum horizontal diameter of tympanum); length of lower MATERIALS AND METHODS arm and hand (LAHL), measured from the elbow joint to the tip of the longest finger; largest diameter of lower arm (LAD); hand Taxon sampling length (HAL), measured from the base of the outer metacarpal A total of 20 individuals of the recognized species of the genus tubercle to the tip of finger III; femur length (FML), measured as Liurana were collected from different localities in the Bomê the linear distance between the insertion of the leg to the knee and Medog Counties, Nyingchi Prefecture, southeastern Tibet, joint; tibia length (TL), measured as the linear distance between China, and were comprised of 18 individuals of L. alpina, L. the knee joint and tibiotarsal articulation; length of tarsus and medogensis, and L. xizangensis and two individuals (one adult foot (TFL), measured from the tibiotarsal articulation to the tip male and one adult female) of the new species (Figure1; of toe IV; and foot length (FL), measured from the base of the Appendix I). Following euthanasia, tissue samples were taken inner metatarsal tubercle to the tip of toe IV. Figure 1 Distribution of LiuranaFigure 1species Distribution in the of East Liurana Himalaya species in East Himalaya Blue star represents type locality of the new species, Liurana vallecula sp. nov. Rectangles represent type localities of recognized species and circles represent additional known localities of recognizedBlue star represents species. Different type locality species areof the color-coded new species, as follows: LiuranaL. alpina vallecula(red), L.sp. medogensis nov. (purple), and L. xizangensis (yellow). For L. xizangensis, the two additional localities are (1) Tongmai, Bomê County, Tibet, China; and (2) 62K, Medog County, Tibet, China. The two light blue localities represent reportedRectangles records of representLiurana cf. medogensistype localitiesfrom of Southern recognized Tibet (seespecies discussion and circles for details). represent additional known localities of recognized species. Different species are color-coded as follows: L. alpina (red), L. medogensis (purple), and L. xizangensis (yellow). For L. 176 www.zoores.ac.cn xizangensis, the two additional localities are (1) Tongmai, Bomê County, Tibet, China; and (2) 62K, Medog County, Tibet, China. The two light blue localities represent reported records of Liurana cf. medogensis from Southern Tibet (see discussion for details). In addition to the newly obtained data, morphological data on phylogenetic relationships of the focal group (Yan et al., 2016). of congeners were also obtained from published literature for comparison (Borah et al., 2013; Fei et al., 1997, 2009; Huang Table 1 Partition strategies and best evolutionary models & Ye, 1997). selected for each partition Molecular analysis Gene Codon Fragment length (bp) Model selected Genomic DNA was extracted from tissue samples using COI 1st 190 GTR standard phenol-chloroform protocols (Sambrook et al., 1989). 2nd 190 HKY+G Fragments of a single mitochondrial DNA locus (cytochrome c oxidase subunit I, COI) and three nuclear loci, including 3rd 190 HKY recombination activating protein 1 (Rag1), tyrosinase (Tyr), Rag1 1st 184 F81 and rhodopsin (Rhod), were targeted and amplified following 2nd 184 HKY published primers and protocols (Che et al., 2011; Yan et 3rd 184 HKY al., 2016). The products were purified with a Gel Extraction Rod 1st 105 JC Mini Kit (Watson Biotechnologies, Shanghai, China) and 2nd 105 F81 sequenced on an ABI 3730xI DNA automated sequencer 3rd 105 GTR (Applied Biosystems, UK). Tyr 1st 177 GTR+G Additional sequences of congeners and closely
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