Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2016-05-02
Page range: 101–140
Abstract views: 204
PDF downloaded: 1

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

Department of Wildlife, Faculty of Forest Resources and Environmental Management, Vietnam National University of Forestry, Xuan Mai, Chuong My, Hanoi, Vietnam. Institute of Zoology, Department of Terrestrial Ecology, University of Cologne, Zülpicher Street 47b, D–50674 Cologne, Germany. AG Zoologischer Garten Köln, Riehler Strasse 173, D–50735 Cologne, Germany.
Institute of Zoology, Department of Terrestrial Ecology, University of Cologne, Zülpicher Street 47b, D–50674 Cologne, Germany.
Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, Vietnam.
Faculty of Environmental Sciences/Biology, Hanoi University of Science, Vietnam National University, 334 Nguyen Trai Road, Hanoi, Vietnam. Centre for Natural Resources and Environmental Studies, Hanoi National University, 19 Le Thanh Tong, Hanoi, Vietnam Department of Herpetology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024
Institute of Zoology, Department of Terrestrial Ecology, University of Cologne, Zülpicher Street 47b, D–50674 Cologne, Germany. AG Zoologischer Garten Köln, Riehler Strasse 173, D–50735 Cologne, Germany.
Faculty of Environmental Sciences/Biology, Hanoi University of Science, Vietnam National University, 334 Nguyen Trai Road, Hanoi, Vietnam.
Institute of Zoology, Department of Terrestrial Ecology, University of Cologne, Zülpicher Street 47b, D–50674 Cologne, Germany. AG Zoologischer Garten Köln, Riehler Strasse 173, D–50735 Cologne, Germany.
Cryptic species karst forest morphology new species Truong Son Range phylogeny taxonomy Reptilia

Abstract

Species designated as ‘cryptic’ share a similar morphotype, and are often only clearly separable by molecular data. Cyrtodactylus, the most diverse gecko genus of the family Gekkonidae, is a prime example, because many morphologically similar taxa have only recently been identified as new species as a result of available genetic evidence. However, while cryptic diversity of Cyrtodactylus is already well documented on the Vietnamese side of the Truong Son range, only scarce data is available from central Laos. In this study, we address this issue by means of an integrative approach, which employs morphological, molecular, and ecological data to distinguish cryptic species of the Cyrtodacylus phongnhakebangensis species group primarily distributed along the northern Truong Son Range. Our analyses based on 12 selected morphological characters, a partial mitochondrial gene (COI), and five ecological parameters revealed three undescribed cryptic Cyrtodactylus species from Hin Nam No National Protected Area, which are described as Cyrtodactylus calamei sp. nov., Cyrtodactylus hinnamnoensis sp. nov., and Cyrtodactylus sommerladi sp. nov. A fourth discovered Cyrtodactylus population in Hin Nam No proved to be the first country record of C. cryptus for Laos. Our results highlight the importance of applying an integrative approach to resolving the taxonomy of complex and cryptic species groups, and the role of the Truong Son Range in maintaining the high level of biodiversity over time.

References

  1. Agarwal, I., Bauer, A.M., Jackman, T.R. & Karanth, K.P. (2014) Insights into Himalayan biogeography from geckos: A molecular phylogeny of Cyrtodactylus (Squamata: Gekkonidae). Molecular Phylogenetics and Evolution, 80, 145–155. http://dx.doi.org/10.1016/j.ympev.2014.07.018

    Ahmadzadeh, F., Fleck, M., Carretero, M.A., Mozaffari, O., Böhme, W., Harris, D.J., Freitas, S. & Rödder, D. (2013) Cryptic speciation patterns in Iranian rock lizards uncovered by integrative taxonomy. PLOS ONE, 8 (12), e80563.
    http://dx.doi.org/10.1371/journal.pone.0080563

    Aplin, K. & Lunde, D. (2008) Laonastes aenigmamus. The IUCN Red List of Threatened Species. Version 2015.2. Available from: http://www.iucnredlist.org (accessed 23 August 2015)

    Bain, R.H. & Hurley, M.M. (2011) A biogeographic synthesis of the amphibians and reptiles of Indochina. Bulletin of the American Museum of Natural History, 360, 1–138.
    http://dx.doi.org/10.1206/360.1

    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148–155.
    http://dx.doi.org/10.1016/j.tree.2006.11

    Clements, R., Sodhi, N.S., Schilthuizen, M. & Ng, P.K.L. (2006) Limestone karsts of Southeast Asia: imperiled arks of biodiversity. BioScience, 56, 733–742.

    Corlett, R.T. (2014) The ecology of tropical east asia. Oxford University Press, Oxford, 283 pp.

    Crowther, T.W., Glick, H.B., Covey, K.R., Bettigole, C., Maynard, D.S., Thomas, S.M., Smith, J.R., Hintler, G., Duguid, M.C., Amatulli, G., Tuanmu, M.N., Jetz, W., Salas, C., Stam, C., Piotto, D., Tavani, R., Green, S., Bruce, G., Williams, S.J., Wiser, S.K., Huber, M.O., Hengeveld, G.M., Nabuurs, G.J., Tikhonova, E., Borchardt, P., Li, C.F., Powrie, L.W., Fischer, M., Hemp, A., Homeier, J., Cho, P., Vibrans, A.C., Umunay, P.M., Piao, S.L., Rowe, C.W., Ashton, M.S., Crane, P.R. & Bradford, M.A. (2015) Mapping tree density at a global scale. Nature, 525 (7568), 201–205.
    http://dx.doi.org/10.1038/nature14967

    Dayrat, B. (2005) Toward integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
    http://dx.doi.org/10.1111/j.1095-8312.2005.00503.x.

    Donihue, C.M., Brock, K.M., Foufopoulos, J. & Herrel, A. (2015) Feed or fight: Testing the impact of food availability and intraspecific aggression on the functional ecology of an island lizard. Functional Ecology. [online in advance of print]
    http://dx.doi.org/10.1111/1365-2435.12550

    Dring, J.C.M. (1979) Amphibians and reptiles from northern Trengganau, Malaysia, with descriptions of two new geckos: Cnemaspis and Cyrtodactylus. Bulletin of the British Museum (Natural History), 34, 181–241.

    Ellis, M. & Pauwels, O.S.G. (2012) The bent-toed geckos (Cyrtodactylus) of the caves and karst of Thailand. Cave and Karst Science, 39 (1), 16–22.

    Grace, J., Mitchard, E. & Gloor, E. (2014) Perturbations in the carbon budget of the tropics. Global Change Biology, 20, 3238–3255.

    Grismer, L.L., Wood, P.L. Jr., Anuar, S., Davis, H.R., Burch, B.T., Cobos, A.J. & Murdoch, M.L. (2016) A new species of karst forest Bent-toed Gecko (genus Cyrtodactylus Gray) not yet threatened by foreign cement companies and a summary of Peninsular Malaysia’sendemic karst forest herpetofauna and the need for its conservation, Zootaxa, 4061 (1), 1–17.
    http://doi.org/10.11646/zootaxa.4061.1.1

    Grismer, L.L., Wood, P.L. Jr., Ngo, T.V. & Murdoch, M.L. (2015) The systematics and independent evolution of cave ecomorphology in distantly related clades of Bent-toed Geckos (Genus Cyrtodactylus Gray, 1827) from the Mekong Delta and islands in the Gulf of Thailand. Zootaxa, 3980 (1), 106–126.
    http://dx.doi.org/10.11646/zootaxa.3980.1.6

    Groves, C.P. & Schaller, G.B. (2000) The phylogeny and biogeography of the newly discovered Annamite Artiodactyls. In: Vrba, E.S. & Schaller, G.B. (Eds.), Antelops, deer, and relatives. Fossil record, behavioural ecology, systematic, and conservation. Yale University Press, New Haven, pp. 261–282.

    Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4 (1), 1–9. Available from: http://palaeo-electronica.org/2001_1/past/issue1_01.htm

    Heidrich, A., Rösler, H., Vu, N.T., Böhme, W. & Ziegler, T. (2007) Another new Cyrtodactylus (Squamata: Gekkonidae) from Phong Nha-Ke Bang National Park, central Truong Son, Vietnam. Zootaxa, 1445, 35–48.

    Ivanova, N.V., de Waard, J. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002.

    Jenkins, P.D., Kilpatrick, C.W., Robinson, M.F. & Timmins, R.J. (2005) Morphological and molecular investigations of a new family, genus and species of rodent (Mammalia: Rodentia: Hystricognatha) from Lao PDR. Systematics and Biodiversity, 2, 419–454.
    http://dx.doi.org/10.1017/S1477200004001549

    Le, M., Nguyen, H.M., Duong, H.T., Nguyen, T.V., Dinh, L.D., Nguyen, N.X., Nguyen, L.D., Dinh, T.H. & Nguyen, D.X. (2015) Phylogeography of the Laotian rock rat (Diatomyidae: Laonastes): implications for Lazarus taxa. Mammal Study, 40, 109–114.
    http://dx.doi.org/10.3106/041.040.0206

    Le, M., Raxworthy, C.J., McCord, W.P. & Mertz, L. (2006) A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 40, 517−531.
    http://dx.doi.org/10.1016/j.ympev.2006.03.003

    Li, B., Pan, R. & Oxnard, C.E. (2002) Extinction of snub-nosed monkeys in China during the past 400 years. International Journal of Primatology, 23, 1227–1244.
    http://dx.doi.org/10.1023/A:1021122819845

    Loos, J., Wehrden, H.V., Dang, K.N. & Ziegler, T. (2012) Niche segregation in Microhabitat use of three sympatric Cyrtodactylus in the Phong Nha-Ke Bang National Park, Central Vietnam. Herpetological Conservation and Biology, 7 (1), 101–108.

    Luu, V.Q., Calame, T., Bonkowski, M., Nguyen, T.Q. & Ziegler, T. (2014a) A new species of Cyrtodactylus (Squamata: Gekkonidae) from Khammouane Province, Laos. Zootaxa, 3760 (1), 54−66.
    http://dx.doi.org/10.11646/zootaxa.3760.1.3

    Luu, V.Q., Calame, T., Nguyen, T.Q., Bonkowski, M. & Ziegler, T. (2015a) A new species of Cyrtodactylus (Squamata: Gekkonidae) from limestone forest, Khammouane Province, central Laos. Zootaxa, 4058 (3), 388–402.
    http://dx.doi.org/10.11646/zootaxa.4058.3.6

    Luu, V.Q., Calame, T., Nguyen, T.Q., Le, M.D., Bonkowski, M. & Ziegler, T. (2014b) A new species of the Gekko japonicus group (Squamata: Gekkonidae) from central Laos. Zootaxa, 3895 (1), 73–88.
    http://doi.org/10.11646/zootaxa.3895.1.4

    Luu, V.Q., Calame, T., Nguyen, T.Q., Le, M.D., Bonkowski, M. & Ziegler, T. (2016a) Cyrtodactylus rufford, a new cave-dwelling bent-toed gecko (Squamata: Gekkonidae) from Khammouane Province, central Laos. Zootaxa, 4067 (2), 185–199.
    http://doi.org/10.11646/zootaxa.4067.2.4

    Luu, V.Q., Calame, T., Nguyen, T.Q., Le, M.D. & Ziegler, T. (2015b) Morphological and molecular review of the Gekko diversity of Laos with descriptions of three new species. Zootaxa, 3986 (3), 279–306.
    http://dx.doi.org/10.11646/zootaxa.3986.3.2.

    Luu, V.Q., Nguyen, T.Q., Calame, T., Hoang, T.T., Southichack, S., Bonkowski, M. & Ziegler, T. (2013) New country records of reptiles from Laos. Biodiversity Data Journal, 1, 1–14.
    http://dx.doi.org/10.3897/BDJ.1.e1015

    Luu, V.Q., Nguyen, T.Q., Le, M.D., Bonkowski, M. & Ziegler, T. (2016b) A new species of karst-dwelling bent-toed gecko (Squamata: Gekkonidae) from Khammouane Province, central Laos. Zootaxa, 4079 (1), 087–102.
    http://doi.org/10.11646/zootaxa.4079.1.6

    Nazarov, R.A., Poyarkov, N.A., Orlov, N.L., Nguyen, S.N., Milto, K.D., Martynov, A.A., Konstantinov, E.L. & Chulisov, A.S. (2014) A review of genus Cyrtodactylus (Reptilia: Sauria: Gekkonidae) in fauna of Laos with description of four new species. Proceedings of the Zoological Institute RAS, 318, 391–423.

    Nazarov, R.A., Poyarkov, N.A., Orlov, N.L., Phung, T.M., Nguyen, T.T., Hoang, D.M. & Ziegler, T. (2012) Two new cryptic species of the Cyrtodactylus irregularis complex (Squamata: Gekkonidae) from southern Vietnam. Zootaxa, 3302, 1–24.

    Nevo, E. (2001) Evolution of genome-phenome diversity under environmental stress. Proceeding of the National Academy of Sciences, USA, 98, 6233–6240.
    http://dx.doi.org/10.1073/pnas.101109298

    Nguyen, S.N., Yang, J.-X., Le, T.-N.T., Nguyen, L.T., Orlov, N.L., Hoang, C.V., Nguyen, T.Q., Jin, J.-Q., Rao, D.-Q., Hoang, T.N., Che, J., Murphy, R.W. & Zhang, Y.-P. (2014) DNA barcoding of Vietnamese bent-toed geckos (Squamata: Gekkonidae: Cyrtodactylus) and the description of a new species. Zootaxa, 3784 (1), 48–66.

    http://dx.doi.org/10.11646/zootaxa.3784.1.2

    Nguyen, T.Q., Le, M.D., Pham, A.V., Ngo, H.N., Hoang, C.V., Pham, C.T. & Ziegler, T. (2015) Two new species of Cyrtodactylus (Squamata: Gekkonidae) from the karst forest of Hoa Binh Province, Vietnam. Zootaxa, 3985 (3), 375–390.
    http://dx.doi.org/10.11646/zootaxa.3985.3.3

    Nicolas, V., Herbreteau, V., Couloux, A., Keovichit, K., Douangboupha, B. & Hugot, J.-P. (2012) A remarkable case of micro-endemism in Laonastes aenigmamus (Diatomyidae, Rodentia) revealed by nuclear and mitochondrial DNA sequence data. PLOS ONE, 7, e48145.

    Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16.

    http://dx.doi.org/10.1186/1742-9994-7-16

    Panitvong, N., Sumontha, M., Tunprasert, J. & Pauwels, O.S.G. (2014) Cyrtodactylus saiyok sp. nov., a new dry evergreen forest-dwelling Bent-toed Gecko (Squamata: Gekkonidae) from Kanchanaburi Province, western Thailand. Zootaxa, 3869 (1), 064–074.

    http://dx.doi.org/10.11646/zootaxa.3869.1.6

    Pauwels, O.S.G. & Sumontha, M. (2014) Cyrtodactylus samroiyot, a new limestone-dwelling Bent-toed Gecko (Squamata: Gekkonidae) from Prachuap Khiri Khan Province, peninsular Thailand. Zootaxa, 3755 (6), 573–583.
    http://dx.doi.org/10.11646/zootaxa.3755.6.4

    Pauwels, O.S.G., Sumontha, M., Panitvong, N. & Varaguttanonda, V. (2014) Cyrtodactylus khelangensis, a new cave-dwelling Bent-toed Gecko (Squamata: Gekkonidae) from Lampang Province, northern Thailand. Zootaxa, 3755 (6), 584–594.

    http://dx.doi.org/10.11646/zootaxa.3755.6.5

    Pham, G.M., Do, T., Vu, D.V., Wikramanayake, E.D., Amato, G., Arctander, P. & MacKinnon, J.R. (1998) Description of Muntiacus truongsonensis, a new species of muntjac (Artiodactyla: Muntiacidae) from Central Vietnam, and implications for conservation. Animal Conservation, (1), 61–68.
    http://dx.doi.org/10.1111/j.1469-1795.1998.tb00227.x

    Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817−818.
    http://dx.doi.org/10.1093/bioinformatics/14.9.817

    Qiu, Y.-X., Fu, C.-X. & Comes, H.P. (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Molecular Phylogenetics and Evolution, 59, 225–244.
    http://dx.doi.org/10.1016/j.ympev.2011.01.012

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539−542.

    Rowley, J.J.L., Tran, D.T.A., Frankham, G.J., Dekker, A.H., Le, D.T.T., Nguyen, T.Q., Dau, V.Q. & Hoang, H.D. (2015) Undiagnosed Cryptic Diversity in Small, Microendemic Frogs (Leptolalax) from the Central Highlands of Vietnam. PLOS ONE, 10 (5), e0128382.
    http://dx.doi.org/10.1371/journal.pone.0128382

    Rundel, P.W. (1999) Conservation Priorities in Indochina. WWF Desk Study: Forest habitats and flora in Lao PDR, Cambodia and Vietnam. Prepared for World Wide Fund for Nature, Indochina Programme Office, Hanoi, 197 pp. [Department of Ecology and Evolutionary Biology University of California Los Angeles, California]

    Schlick-Steiner, B.C., Steiner, F. M., Seifert, B., Stauffer,C., Christian, E. & Crozier R.H. (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology, 55, 421–438.
    http://dx.doi.org/10.1146/annurev-ento-112408-085432

    Schneider, N., Nguyen, T.Q., Le, M.D., Nophaseud, L., Bonkowski, M. & Ziegler, T. (2014) A new species of Cyrtodactylus (Squamata: Gekkonidae) from the karst forest of northern Laos. Zootaxa, 3835 (1), 080–096.
    http://dx.doi.org/10.11646/zootaxa.3835.1.4

    Schneider, N., Nguyen, T.Q., Schmitz, A., Kingsada, P., Auer, M. & Ziegler, T. (2011) A new species of karst dwelling Cyrtodactylus (Squamata: Gekkonidae) from northwestern Laos. Zootaxa, 2930, 1–21.

    Sterling, E.J., Hurley, M.M. & Le, M.D. (2006) Vietnam: A Natural History. Yale University Press, New Haven, 448 pp.

    Sumontha, M., Pauwels, O.S.G., Panitvong, N., Kunya, K. & Grismer, J.L. (2015) A new lowland forest Bent-toed Gecko (Squamata: Gekkonidae: Cyrtodactylus) from Ranong Province, peninsular Thailand. Zootaxa, 3911 (1), 106–118.

    http://dx.doi.org/10.11646/zootaxa.3911.1.6

    Swofford, D.L. (2001) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), version 4. Sinauer Associates, Sunderland, Massachusetts.

    Teynié, A. & David, P. (2010) Voyages naturalistes au Laos. Les Reptiles. Editions Revoir, Nohanent, 315 pp.

    Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876−4882.

    http://dx.doi.org/10.1093/nar/25.24.4876

    Vu, V.D, Pham, M.G, Nguyen, N.C., Do, T., Arctander, P. & MacKinnon, J. (1993) A new species of living bovid from Vietnam. Nature, 363, 443−445.
    http://dx.doi.org/10.1038/363443a0

    Ziegler, T., Nazarov, R., Orlov, N., Nguyen, T.Q., Vu, T.N., Dang, K.N., Dinh, T.H. & Schmitz, A. (2010) A third new Cyrtodactylus (Squamata: Gekkonidae) from Phong Nha-Ke Bang National Park, Vietnam. Zootaxa, 2413, 20–36.

    Ziegler, T. & Vu, N.T. (2009) Ten years of herpetodiversity research in Phong Nha-Ke Bang National Park, central Vietnam. In: Vo, V.T., Nguyen, T.D., Dang, N.K. & Pham, T.H.Y. (Eds.), Phong Nha-Ke Bang National Park and Cologne Zoo, 10 year of cooperation. Quang Binh, pp. 103–124.