Volume 43 Issue 5
Sep.  2022
Turn off MathJax
Article Contents
Ade Prasetyo Agung, Ada Chornelia, L. Lee Grismer, Jesse L. Grismer, Evan S. H. Quah, Jian-Mei Lu, Kyle W. Tomlinson, Alice C. Hughes. Description of two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from karst landscapes in Yunnan, China, highlights complex conservation needs. Zoological Research, 2022, 43(5): 767-786. doi: 10.24272/j.issn.2095-8137.2022.105
Citation: Ade Prasetyo Agung, Ada Chornelia, L. Lee Grismer, Jesse L. Grismer, Evan S. H. Quah, Jian-Mei Lu, Kyle W. Tomlinson, Alice C. Hughes. Description of two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from karst landscapes in Yunnan, China, highlights complex conservation needs. Zoological Research, 2022, 43(5): 767-786. doi: 10.24272/j.issn.2095-8137.2022.105

Description of two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from karst landscapes in Yunnan, China, highlights complex conservation needs

doi: 10.24272/j.issn.2095-8137.2022.105
Funds:  This study was supported by the National Natural Science Foundation of China (U1602265, Mapping Karst Biodiversity in Yunnan), Strategic Priority Research Program of the Chinese Academy of Sciences (CAS) (XDA20050202), High-End Foreign Experts Program of Yunnan Province (Y9YN021B01, Yunnan Bioacoustic Monitoring Program), CAS 135 Program (2017XTBG-T03), and Chinese Academy of Sciences Southeast Asia Biodiversity Research Center Fund (Y4ZK111B01).
More Information
  • Karst habitats are hotspots of diversity and endemism. Their naturally fragmented distributions across broad geographic landscapes have led to the complex array of smaller evolutionary ecosystems that present unique challenges from a conservation perspective. Comprehensive biodiversity assessments of karst habitats have revealed that these ecosystems contain an almost unparalleled level of endemism, and many site-restricted species remain undescribed, thus posing considerable challenges for effective conservation management. Small rock-dwelling species, such as geckos, may be particularly prone to such isolation. In this paper, we discuss one such genus, i.e., Hemiphyllodactylus, and explore its diversity across karst landforms in Yunnan Province, southwestern China. Based on morphological and genetic data, we describe two new species of Hemiphyllodactylus from karst habitats in Simao District and Yanshan County. A phylogenetic tree for Hemiphyllodactylus was constructed using 1 039 base pairs (bp) of the mitochondrial NADH dehydrogenase subunit 2 gene (ND2). The Simao and Yanshan specimens can be distinguished from all other congeners within their respective subclades based on uncorrected genetic pairwise distances greater than 6.3% and 4.3% respectively, as well as significant morphological differences. The discovery and description of these two new species brings the total number of described Hemiphyllodactylus species in China to 14 and indicates many more undescribed species from unsurveyed karst regions await discovery. Our findings suggest that karst ecosystems in Yunnan support a higher diversity of Hemiphyllodactylus than previously known. This study also highlights the importance of karst ecosystems as refugia for site-specific endemic species and the need for heightened conservation efforts.
  • loading
  • [1]
    Agarwal I, Khandekar A, Giri VB, Ramakrishnan U, Karanth KP. 2019. The hills are alive with geckos! A radiation of a dozen species on sky islands across peninsular India (Squamata: Gekkonidae, Hemiphyllodactylus) with the description of three new species. Organisms Diversity & Evolution, 19(2): 341−361.
    Agung AP, Grismer LL, Grismer JL, Quah ESH, Chornelia A, Lu JM, et al. 2021. A new species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from Yunnan, China and its phylogenetic relationship to other congeners. Zootaxa, 4980(1): 1−27. doi: 10.11646/zootaxa.4980.1.1
    Chai J, Lu CQ, Yi MR, Dai NH, Weng XD, Di MX, et al. 2022. Discovery of a wild, genetically pure Chinese giant salamander creates new conservation opportunities. Zoological Research, 43(3): 469−480. doi: 10.24272/j.issn.2095-8137.2022.101
    Che J, Jiang K, Yan F, Zhang YP. 2020. Amphibians and Reptiles in Tibet: Diversity and Evolution. Beijing: Science Press, 803.
    Clements GR, Sodhi NS, Schilthuizen M, Ng PKL. 2006. Limestone karsts of Southeast Asia: imperiled arks of biodiversity. BioScience, 56(9): 733−742. doi: 10.1641/0006-3568(2006)56[733:LKOSAI]2.0.CO;2
    Cobos A, Grismer LL, Wood Jr PL, Quah ESH, Anuar S, Muin MA. 2016. Phylogenetic relationships of geckos of the Hemiphyllodactylus harterti group, a new species from Penang Island, Peninsular Malaysia, and a likely case of true cryptic speciation. Zootaxa, 4107(3): 367−380. doi: 10.11646/zootaxa.4107.3.5
    Conroy CJ, Papenfuss T, Parker J, Hahn NE. 2009. Use of Tricaine Methanesulfonate (MS222) for Euthanasia of Reptiles. Journal of the American Association for Laboratory Animal Science, 48(1): 28−32.
    Davis HR, Bauer AM, Jackman TR, Nashriq I, Das I. 2019. Uncovering karst endemism within Borneo: two new Cyrtodactylus species from Sarawak, Malaysia. Zootaxa, 4614(2): 331−352. doi: 10.11646/zootaxa.4614.2.4
    De Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology, 56(6): 879−886. doi: 10.1080/10635150701701083
    Dittmar K, Porter M, Price L, Svenson GJ, Whiting MF. 2005. A brief survey of invertebrates in caves of Peninsular Malaysia. Malayan Nature Journal, 57(2): 221−233.
    Do QH, Pham CT, Phan TQ, Le MD, Ziegler T, Nguyen TQ. 2020. A new species of Hemiphyllodactylus (Squamata: Gekkonidae) from Tuyen Quang Province, Vietnam. Zootaxa, 4821(3): 511−532. doi: 10.11646/zootaxa.4821.3.5
    Eliades SJ, Phimmachak S, Sivongxay N, Siler CD, Stuart BL. 2019. Two new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from Laos. Zootaxa, 4577(1): 131−147. doi: 10.11646/zootaxa.4577.1.8
    Grismer LL. 1999. An evolutionary classification of reptiles on islands in The Gulf of California, Mexico. Herpetologica, 55(4): 446−469.
    Grismer LL, Wood Jr PL, Anuar S, Muin MA, Quah ESH, Mcguire JA, et al. 2013. Integrative taxonomy uncovers high levels of cryptic species diversity in Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) and the description of a new species from Peninsular Malaysia. Zoological Journal of the Linnean Society, 169(4): 849−880. doi: 10.1111/zoj.12064
    Grismer LL, Wood Jr PL, Anuar S, Quah ESH, Muin MA, Onn CK, et al. 2015. Repeated evolution of sympatric, palaeoendemic species in closely related, co-distributed lineages of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) across a sky-island archipelago in Peninsular Malaysia. Zoological Journal of the Linnean Society, 174(4): 859−876. doi: 10.1111/zoj.12254
    Grismer LL, Wood Jr PL, Anuar S, Riyanto A, Ahmad N, Muin MA, et al. 2014. Systematics and natural history of Southeast Asian Rock Geckos (genus Cnemaspis Strauch, 1887) with descriptions of eight new species from Malaysia, Thailand, and Indonesia. Zootaxa, 3880(1): 1−147. doi: 10.11646/zootaxa.3880.1.1
    Grismer LL, Wood Jr PL, Poyarkov NA, Le MD, Karunarathna S, Chomdej S, et al. 2021. Karstic landscapes are foci of species diversity in the world’s third-largest vertebrate genus Cyrtodactylus Gray, 1827 (Reptilia: Squamata; Gekkonidae). Diversity, 13(5): 183. doi: 10.3390/d13050183
    Grismer LL, Wood Jr PL, Quah ESH, Thura MK, Oaks JR, Lin A. 2020a. Four new Burmese species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from distantly related parapatric clades from the Shan Plateau and Salween Basin. Zootaxa, 4758(1): 45−82. doi: 10.11646/zootaxa.4758.1.2
    Grismer LL, Wood Jr PL, Thura MK, Zin T, Quah ESH, Murdoch ML, et al. 2018a. Twelve new species of Cyrtodactylus Gray (Squamata: Gekkonidae) from isolated limestone habitats in east-central and southern Myanmar demonstrate high localized diversity and unprecedented microendemism. Zoological Journal of the Linnean Society, 182(4): 862−959. doi: 10.1093/zoolinnean/zlx057
    Grismer LL, Wood Jr PL, Thura MK, Zin T, Quah ESH, Murdoch ML, et al. 2018b. Phylogenetic taxonomy of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) with descriptions of three new species from Myanmar. Journal of Natural History, 52(13–16): 881–915.
    Grismer LL, Wood Jr PL, Zug GR, Thura MK, Grismer MS, Murdoch ML, et al. 2018c. Two more new species of Hemiphyllodactylus Bleeker (Squamata: Gekkonidae) from the Shan Hills of eastern Myanmar (Burma). Zootaxa, 4483(2): 295−316. doi: 10.11646/zootaxa.4483.2.4
    Grismer LL, Yushchenko PV, Pawangkhanant P, Naiduangchan M, Nazarov RA, Orlova VF, et al. 2020b. A new species of Hemiphyllodactylus Bleeker (Squamata; Gekkonidae) from Peninsular Thailand that converges in morphology and color pattern on Pseudogekko smaragdinus (Taylor) from the Philippines. Zootaxa, 4816(2): 171−190. doi: 10.11646/zootaxa.4816.2.2
    Guo WB, Zhou KY, Yan J, Li P. 2015. A new species of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from western Yunnan, China. Zootaxa, 3974(3): 377−390. doi: 10.11646/zootaxa.3974.3.5
    Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35(2): 518−522. doi: 10.1093/molbev/msx281
    Huang TF, Zhang PL, Huang XL, Wu T, Gong XY, Zhang YX, et al. 2019. A new cave-dwelling blind loach, Triplophysa erythraea sp. nov. (Cypriniformes: Nemacheilidae), from Hunan Province, China. Zoological Research, 40(4): 331−336. doi: 10.24272/j.issn.2095-8137.2019.049
    Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294(5550): 2310−2314. doi: 10.1126/science.1065889
    Hughes AC. 2017. Understanding the drivers of Southeast Asian biodiversity loss. Ecosphere, 8(1): e01624. doi: 10.1002/ecs2.1624
    Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587−589. doi: 10.1038/nmeth.4285
    Kleiber C, Zeileis A. 2008. Applied Econometrics with R. New York: Springer.
    Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7): 1870−1874. doi: 10.1093/molbev/msw054
    Lenth RV. 2021[2021-07-03]. Emmeans: estimated marginal means, aka least-squares means. R package version 1.7. 5.https://CRAN.R-project.org/package=emmeans/.
    Lleonart J, Salat J, Torres GJ. 2000. Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205(1): 85−93. doi: 10.1006/jtbi.2000.2043
    Luu VQ, Bonkowski M, Nguyen TQ, Le MD, Schneider N, Ngo HT, et al. 2016. Evolution in karst massifs: cryptic diversity among bent-toed geckos along the Truong Son Range with descriptions of three new species and one new country record from Laos. Zootaxa, 4107(2): 101−140. doi: 10.11646/zootaxa.4107.2.1
    Mace GM. 2004. The role of taxonomy in species conservation. Philosophical Transaction of the Royal Society B, 359(1444): 711−719. doi: 10.1098/rstb.2003.1454
    Macey JR, Larson A, Ananjeva NB, Fang Z, Papenfuss TJ. 1997. Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Molecular Biology and Evolution, 14(1): 91−104. doi: 10.1093/oxfordjournals.molbev.a025706
    Marzuki MEB, Liew TS, Mohd-Azlan J. 2021. Land snails and slugs of Bau limestone hills, Sarawak (Malaysia, Borneo), with the descriptions of 13 new species. ZooKeys, 1035(7): 1−113.
    Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the 2010 Gateway Computing Environments Workshop (GCE). New Orleans: IEEE, 1–8.
    Minh BQ, Nguyen MAT, von Haeseler A. 2013. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30(5): 1188−1195. doi: 10.1093/molbev/mst024
    Nazarov RA, Pauwels OSG, Konstantinov EL, Chulisov AS, Orlov NL, Poyarkov Jr NA. 2018. A new karst-dwelling bent-toed gecko (Squamata: Gekkonidae: Cyrtodactylus) from Xiangkhoang Province, northeastern Laos. Zoological Research, 39(3): 202−219. doi: 10.24272/j.issn.2095-8137.2018.010
    Nester H. 2021[2021-09-15]. China’s karst region: infographics. Circle of Blue,https://www.circleofblue.org/2010/world/chinas-karst-region-infographics/.
    Nguyen CH, Van Nguyen L, Nguyen KS, Egorov AA, Averyanov LV. 2021. Hemiboea chanii (Gesneriaceae), a new species from limestone areas of northern Vietnam. PhytoKeys, 183(1): 108−114.
    Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1): 268−274. doi: 10.1093/molbev/msu300
    Nguyen TQ, Do QH, Ngo HT, Van Pham A, Pham CT, Le MD, et al. 2020. Two new species of Hemiphyllodactylus (Squamata: Gekkonidae) from Hoa Binh Province, Vietnam. Zootaxa, 4801(3): 513−536. doi: 10.11646/zootaxa.4801.3.5
    Nguyen TQ, Lehmann T, Le MD, Duong HT, Bonkowski M, Ziegler T. 2013. A new species of Hemiphyllodactylus (Reptilia: Gekkonidae) from northern Vietnam. Zootaxa, 3736(1): 89−98. doi: 10.11646/zootaxa.3736.1.5
    Nguyen TQ, Van Pham A, Ziegler T, Ngo HT, Le MD. 2017. A new species of Cyrtodactylus (Squamata: Gekkonidae) and the first record of C. otai from Son La Province, Vietnam. Zootaxa, 4341(1): 25−40. doi: 10.11646/zootaxa.4341.1.2
    Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. 2020[2020-09-20]. Vegan: community ecology package. R package version 2.6–2.https://CRAN.R-project.org/package=vegan/.
    Pauwels OSG, Sumontha M, Bauer AM. 2016. A new bent-toed gecko (Squamata: Gekkonidae: Cyrtodactylus) from Phetchaburi Province, Thailand. Zootaxa, 4088(3): 409−419. doi: 10.11646/zootaxa.4088.3.6
    Pinheiro J, Bates D, DebRoy S, Sarkar D, EISPACK Authors, Siem Heisterkamp, et al. 2020[2020-09-20]. Nlme: linear and nonlinear mixed effects models. R package version 3.1–158.https://CRAN.R-project.org/package=nlme/.
    Quah ESH, Grismer LL, Anuar MSS. 2021. Conservation of Peninsular Malaysia’s Karst Herpetofauna: a review of herpetological discoveries, research trends, and challenges. Raffles Bulletin of Zoology, 69: 235−252.
    R Core Team. 2020. R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria.https://www.R-project.org/.
    Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5): 901−904. doi: 10.1093/sysbio/syy032
    Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna B, et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3): 539−542. doi: 10.1093/sysbio/sys029
    Sung YH, Lee WH, Ng HN, Zhang YJ, Yang JH. 2018. A new species of Hemiphyllodactylus (Squamata: Gekkonidae) from Hong Kong. Zootaxa, 4392(2): 361−373. doi: 10.11646/zootaxa.4392.2.8
    Thorpe RS. 1975. Quantitative handling of characters useful in snake systematics with particular reference to intraspecific variation in the Ringed Snake Natrix natrix (L. ). Biological Journal of the Linnean Society, 7(1): 27−43. doi: 10.1111/j.1095-8312.1975.tb00732.x
    Thorpe RS. 1983. A review of the numerical methods for recognising and analysing racial differentiation. In: Felsenstein J. Numerical Taxonomy. Berlin: Springer, 404–423.
    Tian MY, Huang S. 2015. Two new species of cavernicolous trechines from southern China karst (Coleoptera: Carabidae: Trechinae). Journal of cave and Karst Studies, 77(3): 152−159.
    Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44(W1): W232−W235. doi: 10.1093/nar/gkw256
    Turan C. 1999. A note on the examination of morphometric differentiation among fish populations: the Truss System. Turkish Journal of Zoology, 23(3): 259−263.
    Uetz P, Freed P, Aguilar R, Hošek J. 2021[2021-11-10]. The reptile database. http://www.reptile-database.org.
    Vieites DR, Wollenberg KC, Andreone F, Köhler J, Glaw F, Vences M. 2009. Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the United States of America, 106(20): 8267−8272. doi: 10.1073/pnas.0810821106
    Whitten T. 2009. Applying ecology for cave management in China and neighbouring countries. Journal of Applied Ecology, 46(3): 520−523. doi: 10.1111/j.1365-2664.2009.01630.x
    Wilcox TP, Zwickl DJ, Heath TA, Hillis DM. 2002. Phylogenetic relationships of the Dwarf Boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution, 25(2): 361−371. doi: 10.1016/S1055-7903(02)00244-0
    Wood PL Jr, Grismer LL, Aowphol A, Aguilar CA, Cota M, Grismer MS, et al. 2017. Three new karst-dwelling Cnemaspis Strauch, 1887 (Squamata; Gekkoniade) from Peninsular Thailand and the phylogenetic placement of C. punctatonuchalis and C. vandeventeri. PeerJ, 5: e2884.
    Yan J, Lin YB, Guo WB, Li P, Zhou KY. 2016. A new species of Hemiphyllodactylus Bleeker, 1860 (Squamata: Gekkonidae) from Guizhou, China. Zootaxa, 4117(4): 543−554. doi: 10.11646/zootaxa.4117.4.6
    Zhang B, Qian TY, Jiang XJ, Cai B, Deng XJ, Yang DD. 2020. A new species of Hemiphyllodactylus Bleeker, 1860 (Reptilia: Squamata) from Hunan Province, China. Asian Herpetological Research, 11(3): 183−193.
    Zhou KY, Liu YZ, Yang GP. 1981. Three new subspecies of Hemiphyllodactylus yunnanensis (Boulenger) from China (Lacertiformes: Gekkonidae). Acta Zootaxonomica Sinica, 6(2): 202−209.
    Zug GR. 2010. Speciation and dispersal in a low diversity taxon: the Slender geckos Hemiphyllodactylus (Reptilia, Gekkonidae). Smithsonian Contributions to Zoology, 631: 1−70.
  • ZR-2022-105 Supplementary Materials.zip
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(10)  / Tables(11)

    Article Metrics

    Article views (2226) PDF downloads(378) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint