Open Access Open Access  Restricted Access Subscription or Fee Access


DOI: http://dx.doi.org/10.11646/zootaxa.3835.1.3

Description of the tadpoles of three rare species of megophryid frogs (Amphibia: Anura: Megophryidae) from Gunung Mulu, Sarawak, Malaysia

EVELYNE OBERHUMMER, CATHERIN BARTEN, MANUEL SCHWEIZER, INDRANEIL DAS, ALEXANDER HAAS

Abstract


The megophryid frogs Leptobrachella brevicrus, Leptolalax dringi and Megophrys dringi are species exclusively known  from highly localised areas in isolated mountain ranges on Borneo. The tadpoles and adults in this study were collected at the shared type locality for the three species in Gunung Mulu National Park, Sarawak, Malaysia (Borneo). The species identities of larvae were determined via comparison to syntopic adults using DNA barcoding techniques based on partial 16S rRNA mitochondrial gene sequences. The genetic data supported the status of the three taxa as valid species. Descriptions of colouration in life and after preservation, external morphological features, morphometric measurements and ecological notes in comparison to congeneric species are supplied. The tadpoles of L. brevicrus and L. dringi show similar adaptations to a fossorial lifestyle. These include an elongated, vermiform body, a relatively long tail and small eyes. Both were found in the gravel beds of a small mountain stream. In contrast, the larvae of M. dringi are adapted to occupying and feeding at the surface of pools within the stream.

 


Keywords


Borneo, Leptobrachella brevicrus, Leptolalax dringi, Megophrys dringi, anuran larvae, external morphology, fossorial tadpole, rheophilic tadpole, phylogenetic relationships, DNA barcoding

Full Text:

PDF/A (3.79 MB)

References


Altig, R. (2007) A primer for the morphology of anuran tadpoles. Herpetological Conservation and Biology, 2, 71–74.

Altig, R. & Johnston, G.F. (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetological Monographs, 3, 81–109.
http://dx.doi.org/10.2307/1466987

Altig, R., Whiles, M. & Taylor, C. (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshwater Biology, 52, 386–395.
http://dx.doi.org/10.1111/j.1365-2427.2006.01694.x

Anstis, M. (2002) The Tadpoles of South–eastern Australia. New Holland Publishers (Australia), Sydney, Auckland, London and Cape Town, 281 pp.

AmphibiaWeb (2011) Information on amphibian biology and conservation. Berkeley, California: AmphibiaWeb. Available from: http://amphibiaweb.org/ (accessed 6 July 2013)

Das, I. & Haas, A. (2005) A new species of Rhacophorus (Anura: Rhacophoridae) from Gunung Gading, Sarawak (western Borneo). The Raffles Bulletin of Zoology, 53, 257–263.

Das, I. & Haas, A. (2011) Scientific results of the Volkswagen Stiftung Bornean amphibian biodiversity project. In: Das, I., Haas, A. & Tuen, A.A. (Eds.), Biology and Conservation of Tropical Asian Amphibians. Proceedings of the Conference “Biology of the Amphibians in the Sunda Region, South–east Asia”. Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, Kota Samarahan, Malaysia, pp. 8–25.

Dehling, J.M. (2008) A new treefrog (Anura: Rhacophoridae: Rhacophorus) from Gunung Mulu, Borneo. Salamandra, 44, 193–205.

Dehling, J.M. (2010) A new bush frog (Anura: Rhacophoridae: Philautus) from Gunung Mulu National Park, East Malaysia (Borneo). Salamandra, 46, 63–72.

Dehling, J.M. (2011) A new karst–dwelling species of Kalophrynus (Anura: Microhylidae) from Gunung Mulu National Park, Borneo, Malaysia. Zootaxa, 2737, 49–60.

Dehling, J.M. & Matsui, M. (2013) A new species of Leptolalax (Anura: Megophryidae) from Gunung Mulu National Park, Sarawak, East Malaysia (Borneo). Zootaxa, 3670 (1), 33–44.
http://dx.doi.org/10.11646/zootaxa.3670.1.2

Dring, J.C.M. (1983a) Frogs of the genus Leptobrachella (Pelobatidae). Amphibia–Reptilia, 4, 89–102.
http://dx.doi.org/10.1163/156853883x00012

Dring, J.C.M. (1983b) Some new frogs from Sarawak. Amphibia–Reptilia, 4, 103–115.
http://dx.doi.org/10.1163/156853883x00021

Dring, J.C.M. (1987) Bornean treefrogs of the genus Philautus (Rhacophoridae). Amphibia–Reptilia, 8, 19–47.
http://dx.doi.org/10.1163/156853887x00036

Drummond, A.J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A. (2009) Geneious v4.7. Available from: http://www.geneious.com (accessed 10 June 2014)

Dubois, A. (1987) Miscellanea taxonomica batrachologica (I). Alytes, 5, 7–95.

Dubois, A. & Ohler, A. (1998) A new species of Leptobrachium (Vibrissaphora) from northern Vietnam with a review of the taxonomy of the genus Leptobrachium (Pelobatidae: Megophrynae). Dumerilia, 4, 1–32.

Frost, D.R. (2014) Amphibian Species of the World: an Online Reference. Version 5.5. American Museum of Natural History, New York, USA. Available from: http://research.amnh.org/vz/herpetology/amphibia/ (accessed 6 July 2013)

Frost, D.R., Grant, T., Faivovich, J., Bain, R.H., Haas, A., Haddad, C.F.B., de Sa, R.O. , Channing, A., Wilkinson, M., Donnellan, S.C., Raxworthy, C.J., Campbell, J.A., Blotto, B.L., Moler, P.E., Drewes, R.C., Nussbaum, R.A., Lynch, J.D. & Green, D.M. (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History, 297, 1–370.
http://dx.doi.org/10.1206/0003-0090(2006)297[0001:tatol]2.0.co;2

Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae, with notes on identification. Herpetologica, 16, 183–190.

Gosner, K. & Rossman, A. (1960) Eggs and larval development of the treefrogs Hyla crucifer and Hyla ocularis. Herpetologica, 16, 225–232.

Gould, T. (2006) Inkscape: a vector drawing tool. Version: 0.48M. Available from: http://www.inkscape.org (accessed 10 June 2014)

Grosjean, S. (2005) The choice of external morphological characters and developmental stage for tadpole–based anuran taxonomy: a case study in Rana (Sylvirana) nigrovittata (Blyth 1855) (Amphibia, Anura, Ranidae). Contributions to Zoology, 74, 61–76.

Guindon, S. & Gascuel, O.A. (2003) Simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
http://dx.doi.org/10.1080/10635150390235520

Haas, A. & Das, I. (2008) Larval identities of Ansonia hanitschi Inger 1960 (Amphibia: Bufonidae) and Polypedates colletti (Boulenger, 1890) (Amphibia: Rhacophoridae) from East Malaysia (Borneo). Salamandra, 44, 85–100.

Haas, A. & Das, I. (2011) Describing East Malaysian tadpole diversity: status and recommendations for standards and procedures associated with larval amphibian description and documentation. Bonner Zoologische Monographien, 57, 29–46.

Haas, A., Hertwig, S. & Das, I. (2006) Extreme tadpoles: The morphology of the fossorial megophryid larva, Leptobrachella mjobergi. Zoology, 109, 26–42.
http://dx.doi.org/10.1016/j.zool.2005.09.008

Haas, A., Hertwig, S.T., Krings, W., Braskamp, E., Dehling, J.M., Pui Y.M., Jankowski, A., Schweizer, M. & Das, I. (2012) Description of three Rhacophorus tadpoles (Lissamphibia: Anura: Rhacophoridae) from Sarawak, Malaysia (Borneo). Zootaxa, 3328, 1–19.

Haas, A., Wolter, J., Hertwig, S. & Das, I. (2009) Larval morphologies of three species of stream toads, genus Ansonia (Amphibia: Bufonidae) from East Malaysia (Borneo), with a key to known Bornean Ansonia tadpoles. Zootaxa, 2302, 1–18.

Hamidy, A., Matsui, M., Nishikawa, K. & Belabut, D. (2012) Detection of cryptic taxa in Leptobrachium nigrops (Amphibia, Anura, Megophryidae), with description of two new species. Zootaxa, 3398, 22–39.

Hazebroek, H. & Morshidi, A.b.K. (2000) National Parks of Sarawak. Natural History Publications (Borneo) Sdn Bhd., Kota Kinabalu, xii + 503 pp.

Hertwig, S., de Sá, R.O. & Haas, A. (2004) Phylogenetic signal and the utility of 12S and 16S mtDNA in frog phylogeny. Journal of Zoological Systematics and Evolutionary Research, 42, 2–18.
http://dx.doi.org/10.1111/j.1439-0469.2004.00225.x

Hertwig, S.T., Das, I., Schweizer, M., Brown, R. & Haas, A. (2011) Phylogenetic relationships of the Rhacophorus everetti–group and implications for the evolution of reproductive modes in Philautus (Amphibia: Anura: Rhacophoridae). Zoologica Scripta, 41, 29–46.
http://dx.doi.org/10.1111/j.1463-6409.2011.00499.x

Hertwig, S.T., Lilje, K.E., Das, I. & Haas, A. (2012) Evidence of direct development in the rare bush frog Philautus acutus (Rhacophoridae, Anura) from Borneo. The Raffles Bulletin of Zoology, 60, 559 –568.

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

Inger, R.F. (1983) Larvae of southeast Asian species of Leptobrachium and Leptobrachella (Anura: Pelobatidae). In: Rhodin, A. & Miyata, K. (Eds.), Advances in Herpetology and Evolutionary Biology. Museum of Comparative Zoology, Cambridge, Massachusetts, pp. 13–32.

Inger, R.F. (1985) Tadpoles of the forested regions of Borneo. Fieldiana Zoology, 26, 1–89.

Inger, R.F. (1986) Diets of tadpoles living in a Bornean rain forest. Alytes, 5,153–164.

Inger, R.F. (1999) Distribution of amphibians in southern Asia and adjacent islands. In: Duellman, W.E. (Ed.), Patterns of Distribution of Amphibians: A Global Perspective. The John Hopkins University Press, Baltimore and London, pp. 445–482.

Inger, R.F. & Stuebing, R.B. (1997) A Field Guide to the Frogs of Borneo. First Edition. Natural History Publications (Borneo) Sdn Bhd / Science and Technology Unit, Sabah, Kota Kinabalu, x + 205 pp.

Inger, R.F. & Stuebing, R.B. (2005) A Field Guide to the Frogs of Borneo. 2nd Edition. Natural History Publications (Borneo) Sdn. Bhd. Kota Kinabalu, iv + 201 pp.

Inger, R.F., Stuart, B.L. & Voris, H.K. (2006) High level of cryptic species diversity revealed by sympatric lineages of Southeast Asian forest frogs. Biology Letters, 2, 470–474.
http://dx.doi.org/10.1098/rsbl.2006.0505

Inger, R., Stuebing, R. & Tan, F.L. (1995) New species and new records of anurans from Borneo. The Raffles Bulletin of Zoology, 43,115–131.

Inger, R., Das., I, Stuebing, R., Lakim, M. & Yambun, P.A. (2004a) Leptobrachella brevicrus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Available from: http://www.iucnredlist.org (accessed 10 June 1014)

Inger, R., Das., I, Stuebing, R., Lakim, M. & Yambun, P.B. (2004b) Leptobrachella brevicrus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Available from: http://www.iucnredlist.org (accessed 10 June 1014)

Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.
http://dx.doi.org/10.1093/nar/gkf436

Lathrop, A. (1997) Taxonomic review of the Megophryid frogs (Anura: Pelobatoidea). Asiatic Herpetological Research, 7, 68–79.

Leong, T.M. & Chou, L.M. (1999) Larval Diversity and Development in the Singapore Anura (Amphibia). The Raffles Bulletin of Zoology, 47 (1), 81–137.

Li, C., Guo, M.G. & Wang, Y.Z. (2011) Tadpole types of Chinese megophryd frogs (Anura: Megophrydae) and implications for larval evolution. Current Zoology, 57, 93–100.

Malkmus, R., Manthey, U., Vogel, G., Hoffmann, P. & Kosuch, J. (2002) Amphibians and Reptiles of Mount Kinabalu (North Borneo). Koeltz Scientific Books, Koenigstein, Germany, 424 pp.

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

Matsui, M. & Dehling, J.M. (2012) Notes on an enigmatic Bornean megophryid, Leptolalax dringi Dubois, 1987 (Amphibia: Anura). Zootaxa, 3317, 49–58.

McDiarmid, R. & Altig, R. (1999) Tadpoles: the Biology of Anuran Larvae. University Chicago Press. Chicago, London, xiv + 444 pp.

Morrison, D.A. (2009) Why would phylogeneticists ignore computerized sequence alignment? Systematic Biology, 58, 150–158.
http://dx.doi.org/10.1093/sysbio/syp009

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

Nicolas, V., Herbreteau, V., Couloux, A., Keovichit, K. & Douangboupha, B. (2012) A remarkable case of micro–endemism in Laonastes aenigmamus (Diatomyidae, Rodentia) revealed by nuclear and mitochondrial DNA sequence data. PLoS ONE, 7.
http://dx.doi.org/10.1371/journal.pone.0048145

Nodzenski, E. & Inger, R. (1990) Uncoupling of related structural changes in metamorphosing torrent–dwelling tadpoles. Copeia, 1990, 1047–1054.
http://dx.doi.org/10.2307/1446488

Nodzenski, E., Wassersug, R.J. & Inger, R.F. (1989) Developmental differences in visceral morphology of megophryine pelobatid tadpoles in relation to their body form and mode of life. The Biological Journal of the Linnean Society, 38, 369–388.
http://dx.doi.org/10.1111/j.1095-8312.1989.tb01583.x

Orton, G.L. (1953) The systematics of vertebrate larvae. Systematic Zoology, 2, 63–75.
http://dx.doi.org/10.2307/2411661

Palumbi, S.R. (1996) The polymerase chain reaction. In: Hillis, D.M., Moritz, C. & Mable, B.K. (Eds.), Molecular Systematics. Sinauer, Sunderland, Massachusetts, pp. 205–247.

Pyron, R.A. & Wiens, J.J. (2011) A large–scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61, 543–583.
http://dx.doi.org/10.1016/j.ympev.2011.06.012

Sabaj Pérez, M.H. (Ed.) (2012) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Version 3.0 (23 February 2012). American Society of Ichthyologists and Herpetologists, Washington, DC. Available from: http://www.asih.org/ (accessed 10 June 2014)

Schmidt, A.A. (1976) Erst–Nachzucht des Zipfelfrosches Megophrys nasuta. Salamandra, 12, 55–88.

Stuart, S., Hoffmann, M., Chanson, J., Cox, N., Berridge, R., Ramani, P. & Young, B. (Eds.) (2008) Threatened Amphibians of the World. Lynx Edicions, IUCN, and Conservation International, Barcelona, Spain; Gland, Switzerland; and Arlington, Virginia, USA, 758 pp.

Vences, M., Thomas, M., Bonnett, R.M. & Vieites, D.R. (2005) Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philosophical Transactions of the Royal Society B, 360, 1859–1868.
http://dx.doi.org/10.1098/rstb.2005.1717

Wildenhues, M., Rauhaus, A., Bach, R., Karbe, D., van der Straeten, K., Hertwig, S.T. & Ziegler, T. (2012) Husbandry, captive breeding, larval development and stages of the Malayan horned frog Megophrys nasuta (Schlegel, 1858) (Amphibia: Anura: Megophryidae). Amphibian and Reptile Conservation, 5, 15–28.


Refbacks

  • There are currently no refbacks.


 
ISSN 1175-5326 (Print Edition) & ISSN 1175-5334 (Online Edition)
Published by Magnolia Press, Auckland, New Zealand
A founding journal of Biotaxa