Open Access Open Access  Restricted Access Subscription or Fee Access

Unrealized diversity in an urban rainforest: A new species of Lygosoma (Squamata: Scincidae) from western Sarawak, Malaysia (Borneo)

BENJAMIN R. KARIN, ELYSE S. FREITAS, SAMUEL SHONLEBEN, L. LEE GRISMER, AARON M. BAUER, INDRANEIL DAS

Abstract


We collected two specimens of an undescribed species of Lygosoma from pitfall traps in an urban rainforest in Kuching and from the base of a forested hill in western Sarawak, East Malaysia. The new species is diagnosable from all south-east Asian congeners by morphological characters, and most closely resembles Lygosoma herberti from the Thai-Malay Peninsula. The new species shows substantial molecular divergence from its closest relatives in two protein-coding genes, one mitochondrial (ND1) and one nuclear (R35) that we sequenced for several south-east Asian congeners. We describe the new species on the basis of this distinct morphology and genetic divergence. It is the third species of Lygosoma known from Borneo, and highlights the continuing rise in lizard species diversity on the island. In addition, the discovery of this species from a small urban rainforest underscores the importance of preserving intact rainforest areas of any size in maintaining species diversity.

 


Keywords


Reptilia, Borneo; Sarawak; Scincidae; Lygosoma samajaya new species

Full Text:

PDF (26MB)

References


Bartlett, E. (1895) The crocodiles and lizards of Borneo in the Sarawak Museum, with descriptions of supposed new species, and the variation of colours in the several species during life. Journal of the Straits Branch of the Royal Asiatic Society, 28, 73–97.

Bourret, R. (2009) Les lezards de l’Indochine. Edition Chimaira, Frankfurt am Main / Reptiles et Amphibien, Muséum National d'Histoire Naturelle, Paris, 624 pp.

Brown, W.C. & Alcala, A.C. (1980) Philippine lizards of the family Scincidae (with a description of a new species of Trophidophorus by James P. Bacon). Silliman University. Natural Science Monograph Series 2. Silliman University Press, Dumaguete City, 264 pp.

de Bruyn, M., Stelbrink, B., Morley, R.J., Hall, R., Carvalho, G.R., Cannon, C.H., Van Den Bergh, G., Meijaard, E., Metcalfe, I., Boitani, L., Maiorano, L., Shoup, R. & Von Rintelen, T. (2014) Borneo and Indochina are major evolutionary hotspots for Southeast Asian biodiversity. Systematic Biology, 63, 879–901.
https://doi.org/10.1093/sysbio/syu047

Bryan, J.E., Shearman, P.L., Asner, G.P., Knapp, D.E., Aoro, G. & Lokes, B. (2013) Extreme differences in forest degradation in Borneo: comparing practices in Sarawak, Sabah, and Brunei. PLoS ONE, 8, e69679.
https://doi.org/10.1371/journal.pone.0069679

Cochran, D.M. (1927) New reptiles and batrachians collected by Dr. Hugh M. Smith in Siam. Proceedings of the Biological Society of Washington, 40, 179–192.

Cochran, D.M. (1930) The herpetological collections made by Dr. Hugh M. Smith in Siam from 1923 to 1929. Proceedings of the United States National Museum, 77, 1–39.
https://doi.org/10.5479/si.00963801.77-2834.1

Das, I. (2004a) Collecting in the “Land Below the Wind”, Herpetological Explorations of Borneo. In: Bauer, A.M. (Ed.), Herpetological expeditions and voyages. Bonner zoologische Beitrage, 52, pp. 231–243.

Das, I. (2004b) Lizards of Borneo: a pocket guide. Natural History Publications (Borneo), Sdn Bhd, Kota Kinabalu, 83 pp.

Das, I. (2010) A Field Guide to the Reptiles of South-east Asia. New Holland Publishers (UK), Ltd., London, 376 pp.

Das, I. & Austin, C.C. (2007) A new species of Lipinia (Squamata: Scincidae) from Borneo, revealed by molecular and morphological data. Journal of Herpetology, 41, 61–71.
https://doi.org/10.1670/0022-1511(2007)41[61:NSOLSS]2.0.CO;2

Das, I., Lakim, M. & Kandaung, P. (2008) New species of Luperosaurus (Squamata: Gekkonidae) from the Crocker Range Park, Sabah, Malaysia (Borneo). Zootaxa, 1719, 53–60.

Datta-Roy, A., Singh, M. & Karanth, K.P. (2014) Phylogeny of endemic skinks of the genus Lygosoma (Squamata: Scincidae) from India suggests an in situ radiation. Journal of Genetics, 93, 163–167.
https://doi.org/10.1007/s12041-014-0321-z

Fisher, R.N. & Rochester, C.J. (2012) Pitfall-trap Surveys. In: McDiarmid, R.W., Foster, M.S., Guyer, C., Gibbons, J.W. & Chernoff, N. (Eds.), Reptile biodiversity: standard methods for inventory and monitoring. University of California Press, Berkeley, CA, pp. 234–249.

Fry, B.G., Vidal, N., Norman, J.A., Vonk, F.J., Scheib, H., Ramjan, S.F.R., Kuruppu, S., Fung, K., Hedges, B.S., Richardson, M.K., Hodgson, W.C., Ignjatovic, V., Summerhayes, R. & Kochva, E. (2006) Early evolution of the venom system in lizards and snakes. Nature, 439, 584–588.
https://doi.org/10.1038/nature04328

Gadgil, M., Berkes, F. & Folke, C. (1993) Indigenous knowledge for biodiversity conservation. Ambio, 22, 151–156.

Gaveau, D.L.A., Sloan, S., Molidena, E., Yaen, H., Sheil, D., Abram, N.K., Ancrenaz, M., Nasi, R., Quinones, M., Wielaard, N. & Meijaard, E. (2014) Four decades of forest persistence, clearance and logging on Borneo. PLoS ONE, 9, 1–11.
https://doi.org/10.1371/journal.pone.0101654

Geissler, P., Harmann, T. & Neang, T. (2012) A new species of the genus Lygosoma Hardwicke & Gray, 1827 (Squamata: Scincidae) from northeastern Cambodia, with an updated identification key to the genus Lygosoma in mainland Southeast Asia. Zootaxa, 3190, 56–68.

Gibson, L., Lee, T.M., Koh, L.P., Brook, B.W., Gardner, T.A., Barlow, J., Peres, C.A., Bradshaw, C.J.A., Laurance, W.F., Lovejoy, T.E. & Sodhi, N.S. (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature, 478, 378–383.
https://doi.org/10.1038/nature10425

Greer, A.E. (1977) The systematics and evolutionary relationships of the scincid lizard genus Lygosoma. Journal of Natural History, 11, 515–540.
https://doi.org/10.1080/00222937700770451

Grismer, L. L. (2011) Lizards of Peninsular Malaysia, Singapore, and their adjacent archipelagos: their description, distribution, and natural history. Edition Chimaira, Frankfurt am Main, 728 pp.

Grismer, L.L. & Onn, C.K. (2009) A new species of karst dwelling Cnemaspis Strauch 1887 (Squamata: Gekkonidae) from Sarawak, Borneo. Zootaxa, 31, 21–31.

Grismer, L.L., Muin, M.A., Wood, P.L., Anuar, S. & Linkem, C.W. (2016) The transfer of two clades of Malaysian Sphenomorphus Fitzinger (Squamata: Scincidae) into the genus Tytthoscincus Linkem, Diesmos, & Brown and the description of a new Malaysian swamp-dwelling species. Zootaxa, 4092 (2), 231–242.
https://doi.org/10.11646/zootaxa.4092.2.6

Günther, A.C.L.G. (1864) The reptiles of British India. Ray Society, London, xxvii + 452 pp.

Hardwicke, T. & Gray, J.E. (1827) A synopsis of the species of saurian reptiles collected in India by Major-General Hardwicke. Zoological Journal, London, 3, 213–229.

Heitz, B.B., Diesmos, A.C., Freitas, E.S., Ellsworth, E.D., Grismer, L.L., Aowphol, A., Brown, R.M. & Siler, C.D. (2016) A new Supple Skink, genus Lygosoma (Reptilia: Squamata: Scincidae), from the western Philippines. Herpetologica, 72, 352–361.
https://doi.org/10.1655/Herpetologica-D-16-00023.1

Honda, M., Ota, H., Kohler, G., Eneich, I., Chirio, L., Chen, S. & Hikida, T. (2003) Phylogeny of lizard subfamily Lygosominae (Reptilia: Scincidae), with special reference to the origin of new world taxa. Genes & Genetic Systems, 78, 71–80.
https://doi.org/10.1266/ggs.78.71

Inger, R.F. (1966) Systematics and zoogeography of the Amphibia of Borneo. Fieldiana Zoology, 52, 1–402.

Inger, R.F., Lian, T.F., Lakim, M. & Yambun, P. (2001) New species of the lizard genus Sphenomorphus (Lacertilia: Scincidae), with notes on ecological and geographic distribution of species in Sabah, Malaysia. The Raffles Bulletin of Zoology, 49, 181–189.

Karin, B.R., Das, I. & Bauer, A.M. (2016) Two new species of diminutive leaf-litter skinks (Squamata: Scincidae: Tytthoscincus) from Gunung Penrissen, Sarawak, Malaysia (northern Borneo). Zootaxa, 4093 (3), 407–423.
https://doi.org/10.11646/zootaxa.4093.3.7

Kurita, T., Nishikawa, K., Matsui, M. & Hikida, T. (2017) A new species of Rock Gecko genus Cnemaspis (Squamata: Gekkonidae) from Western Sarawak, Malaysia. Zootaxa, 4258 (6), 525–538.
https://doi.org/10.11646/zootaxa.4258.6.2

Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://doi.org/10.1093/molbev/mss020

Leaché, A.D. & Reeder, T.W. (2002) Molecular systematics of the Eastern Fence Lizard (Sceloporus undulatus): A comparison of parsimony, likelihood, and Bayesian approaches. Systematic Biology, 51, 44–68.
https://doi.org/10.1080/106351502753475871

Linnaeus, C. (1766) Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio duodecima, reformata. Laurentii Salvii, Holmiae [= Stockholm], 532 pp.

Lourenço, A., Álvarez, D., Wang, I.J. & Velo-Antón, G. (2017) Trapped within the city: integrating demography, time since isolation and population-specific traits to assess the genetic effects of urbanization. Molecular Ecology, 26, 1498–1514. https://doi.org/10.1111/mec.14019

Malkmus, R., Ulrich, M., Vogel, G., Hoffmann, P. & Kosuch, J. (2002) Amphibians and reptiles of Mount Kinabalu (North Borneo). Koeltz Scientific Books, Königstein, 424 pp.

Manthey, U. & Grossmann, W. (1997) Amphibien und Reptilien Südostasiens. Natur und Tier Verlag, Münster, 512 pp.

Mitchell, J.C. & Jung Brown, R.E. (2008) Urban herpetology: Global overview, synthesis, and future directions. In: Mitchell, J.C., Jung Brown, R.E. & Bartholomew, B. (Eds.), Urban Herpetology. Society for the Study of Amphibians and Reptiles, Salt Lake city, UT, pp. 1–30.

Mittermeier, R.A., Myers, N., Thomsen, J.B., da Fonseca, G.A.B. & Olivieri, S. (1998) Biodiversity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conservation Biology, 12, 516–520.
https://doi.org/10.1046/j.1523-1739.1998.012003516.x

Munshi-South, J., Zak, Y. & Pehek, E. (2013) Conservation genetics of extremely isolated urban populations of the northern dusky salamander (Desmognathus fuscus) in New York City. PeerJ, 1, e64.
https://doi.org/10.7717/peerj.64

Myers, N., Mittermeier, R., Mittermeier, C.G., Fonseca, G.A.B. da & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.
https://doi.org/10.1038/35002501

Palumbi, S. (1991) Simple Fool’s Guide to PCR. Dept. of Zoology and kewalo Marine Laboratory, University of Hawaii, Honolulu, 45 pp.

Pui, Y.M., Karin, B.R., Bauer, A.M. & Das, I. (2017) A new species of Tropidophorus Duméril & Bibron, 1839 (Squamata: Sauria: Scincidae) from Sarawak, East Malaysia (Borneo). Zootaxa, 4258 (6), 539–550.
https://doi.org/10.11646/zootaxa.4258.6.3

Pyron, R.A., Burbrink, F.T. & Wiens, J.J. (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 1–53.
https://doi.org/10.1186/1471-2148-13-93

de Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless forms: species and speciation. Oxford University Press, New York, pp. 57–75.

de Queiroz, K. (1999) The general lineage concept of species and the defining properties of the species category. In: Wilson, R.A. (Eds.), Species: new interdisciplinary essays. Massachusetts Institute of Technology Press, Cambridge, Massachusetts, USA, pp. 49–89.

Radespiel, U. & Bruford, M.W. (2014) Fragmentation genetics of rainforest animals: Insights from recent studies. Conservation Genetics, 15, 245–260.
https://doi.org/10.1007/s10592-013-0550-3

Rogers, R.L. & Slatkin, M. (2017) Excess of genomic defects in a woolly mammoth on Wrangel island. PLoS Genetics, 13, 1–16.
https://doi.org/10.1371/journal.pgen.1006601

Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180

de Rooij, N. (1915) The Reptiles of the Indo-Australian Archipelago. Vol. I. Lacertilia, Chelonia, Emydosauria. E. J. Brill, Leiden, xiv + 384 pp.
https://doi.org/10.5962/bhl.title.24239

Sabaj Pérez, M.H. (2016) Standard Symbolic Codes for Institutional Resource Collections in Herpetology and Ichthyology: An Online Reference. Version 6.5 (16 August 2016). American Society of Ichthyologists and Herpetologists, Washington, D.C. Available from: http://www.asih.org (accessed 6 September 2016)

Shreve, B. (1940) Reptiles and amphibians from Burma with descriptions of three new skincs (sic). Proceedings of the New England Zoölogy Club, 18, 17–26.

Siler, C.D., Diesmos, A.C., Alcala, A.C. & Brown, R.M. (2011) Phylogeny of Philippine slender skinks (Scincidae: Brachymeles) reveals underestimated species diversity, complex biogeographical relationships, and cryptic patterns of lineage diversification. Molecular Phylogenetics and Evolution, 59, 53–65.
https://doi.org/10.1016/j.ympev.2010.12.019

Skinner, A., Hugall A.F., and Hutchinson, M.N. (2011) Lygosomine phylogeny and the origins of Australian scincid lizards. Journal of Biogeography, 38, 1044–1058.
https://doi.org/10.1111/j.1365-2699.2010.02471.x

Smith, M.A. (1916) Descriptions of three new lizards and a new snake from Siam. The journal of the Natural History Society of Siam, 2, 44–47.

Smith, M.A. (1921) New or little-known reptiles and batrachians from southern Annam (Indo-China). Proceedings of the Zoological Society of London, 91, 423–440.
https://doi.org/10.1111/j.1096-3642.1921.tb03271.x

Smith, M.A. (1935) The fauna of British India, including Ceylon and Burma. Reptilia and Amphibia. Vol. II. Sauria. Taylor And Francis, London, xiii + 440 pp., 1 pl. [reprinted 1970 Ralph Curtis Books, Hollywood, Florida and 1980 Today and Tomorrow’s Publishers, Dehradun]

Smith, M.A. (1937) A review of the genus Lygosoma (Scincidae: Reptilia) and its allies. Records of the Indian Museum, 39, 213–234.
https://doi.org/10.3853/j.0067-1975.2.1893.1196

Sodhi, N.S., Koh, L.P., Brook, B.W. & Ng, P.K.L. (2004) Southeast Asian biodiversity: an impending disaster. Trends in Ecology and Evolution, 19, 654–660.
https://doi.org/10.1016/j.tree.2004.09.006

Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.
https://doi.org/10.1093/bioinformatics/btu033

Stoliczka, F. (1870) Observations on some Indian and Malayan Amphibia and Reptilia. The journal of the Asiatic Society of Bengal, 6, 134–228.
https://doi.org/10.1080/00222937008696209

Sumner, J., Jessop, T., Paetkau, D. & Moritz, C. (2004) Limited effect of anthropogenic habitat fragmentation on molecular diversity in a rain forest skink, Gnypetoscincus queenslandiae. Molecular Ecology, 13, 259–269.
https://doi.org/10.1046/j.1365-294X.2003.02056.x

Sumner, J., Rousset, F., Estoup, A. & Moritz, C. (2001) ‘Neighbourhood’ size, dispersal and density estimates in the prickly forest skink (Gnypetoscincus queenslandiae) using individual genetic and demographic methods. Molecular Ecology, 10, 1917–1927.
https://doi.org/10.1046/j.0962-1083.2001.01337.x

Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4. Sinauer Associates, Sunderland, MA. [software]

Taylor, E.H. (1962) New Oriental reptiles. University of Kansas Science Bulletin, 43, 209–263.
https://doi.org/10.5962/bhl.part.13346

Taylor, E.H. (1963) The lizards of Thailand. University of Kansas Science Bulletin, 44, 687–1077.

Theobald, W. (1868) Catalogue of the reptiles of British Birma, embracing the provinces of Pegu, Martaban, and Tenasserim; with descriptions of new or little-known species. Zoological Journal of the Linnean Society, 10, 4–67.
https://doi.org/10.1111/j.1096-3642.1868.tb02007.x

Uetz, P. & Hošek, J. (2017) The reptile database. Available from: http://reptile-database.reptarium.cz/ (accessed 29 May 2017)

Wallace, A.R. (1869) The Malay Archipelago: the land of the orang-utan and the bird of paradise; a narrative of travel, with studies of man and nature. Macmillan, London, 512 pp.
https://doi.org/10.5962/bhl.title.131886

Werner, F. (1910) Über neue oder seltene Reptilien des Naturhistorischen Museums in Hamburg: II. Eidechsen. Jahrbuch der Hamburgischen Wissenschaftliche Anstalten, 27, 1–46.

Woodruff, D.S. (2001) Declines of biomes and biotas and the future of evolution. Proceedings of the National Academy of Sciences of the United States of America, 98, 5471–5476.
https://doi.org/10.1073/pnas.101093798

Ziegler, T., Schmitz, A. & Heidrich, A. (2007) A new species of Lygosoma (Squamata: Sauria: Scincidae) from the Central Truong Son, Vietnam, with notes on its molecular phylogenetic position. Revue Suisse de Zoologie, 114, 397–415.
https://doi.org/10.5962/bhl.part.80396




DOI: http://dx.doi.org/10.11646/zootaxa.4370.4.2

Refbacks

  • There are currently no refbacks.


 
ISSN 1175-5326 (Print Edition) & ISSN 1175-5334 (Online Edition)
Published by Magnolia Press, Auckland, New Zealand