Abstract
The external morphology of two molecularly identified tadpoles of the genus Staurois, S. parvus and S. tuberilinguis is described. These tadpoles display a typical fossorial morphology characterized by a strongly depressed body, small subcutaneous eyes, a vermiform appearance with a long tail and reduced fins, a nearly pigmentless skin, a KRF of 1:1+1 on the upper labium and numerous keratodont rows on the lower one. The two species can be distinguished by several morphological differences, the most conspicuous are the eye condition (not bulging and covered by skin in S. tuberilinguis) and the presence of numerous white isolated acini on the body and tail in S. parvus. These differences support the specific status of S. parvus relatively to S. tuberilinguis despite low genetic divergence between these two taxa. The morphology of these tadpoles, as well as the buccopharyngeal anatomy of S. parvus, are compared to those of the tadpoles in the family Centrolenidae and the definition of the fossorial ecomorphological guild is updated.
References
Altig, R. & Johnston, G.F. (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetological Monographs, 3, 81–109.
https://doi.org/10.2307/1466987
Altig, R. & McDiarmid, R.W. (1999) Body plan. Development and morphology. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles. The biology of anuran larvae. The University of Chicago Press, Chicago and London, pp. 24–51.
Arifin, U., Iskandar, D.T., Bickford, D.P., Brown, R.M., Meier, R. & Kutty, S.N. (2011) Phylogenetic relationships within the genus Staurois (Anura, Ranidae) based on 16S rRNA sequences. Zootaxa, 2744 (1), 39–52.
https://doi.org/10.11646/zootaxa.2744.1.3
Blackburn, D.C. (2008) A new species of Cardioglossa (Amphibia: Anura: Arthroleptidae) endemic to Mount Manangouba in the Republic of Cameroon, with an analysis of morphological diversity in the genus. Zoological Journal of the Linnean Society, 154, 611–630.
https://doi.org/10.1111/j.1096-3642.2008.00397.x
Bossuyt, F., Brown, R.M., Hillis, D.M., Cannatela, D.C. & Milinkovitch, M.C. (2006) Phylogeny and biogeography of a cosmopolitan frog radiation: late Cretaceous diversification resulted in continental-scale endemism in the family Ranidae. Systematic Biology, 55, 579–594.
https://doi.org/10.1080/10635150600812551
Boulenger, G.A. (1918) Remarks on the batrachian genera Cornufer Tschudi, Platymantis Gthr., Simomantis g. n., and Staurois Cope. Annals and Magazine of Natural History, Series 9, 1, 372–375.
https://doi.org/10.1080/00222931808562330
Dubois A. (1995) Keratodont formulae in anuran tadpoles: proposals for a standardization. Journal of Zoological Systematics and Evolutionary Research, 33, 1–15.
https://doi.org/10.1111/j.1439-0469.1995.tb00207.x
Frost, D.R., Grant, T., Faivovich, J., Bain, R.H., Haas, A., Haddad, C.F.B., De Sá, R.O., Channing, A., Wilkinson, M., Donnellan, S.C., Raxworthy, C.J., Campbell, J.A., Blotto, B.L., Moler, P., Drewes, R.C., Nussbaum, R.A., Lynch, J.D., Green, D.M. & Wheeler, W.C. (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History, 297, 1–370.
https://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.
Goutte, S., Dubois, A., Howard, S.D., Marquez, R., Rowley, J.J.L., Dehling, M., Grandcolas, P., Rongchuan, X. & Legendre, F. (2016) Environmental constraints and call evolution in torrent-dwelling frogs. Evolution, 70, 811–826.
https://doi.org/10.1111/evo.12903
Grosjean, S. (2006 [“2005”]) The choice of external morphological characters and developmental stages for tadpole-based anuran taxonomy: a case study in Rana (Sylvirana) nigrovittata (Blyth, 1855) (Amphibia, Anura, Ranidae). Contributions to Zoology, 74, 61–76.
https://doi.org/10.1163/18759866-0740102005
Haas, A., Hertwig, S. & Das, I. (2006) Extreme tadpoles: The morphology of the fossorial megophryid larva, Leptobrachella mjobergi. Zoology, 109, 26–42.
https://doi.org/10.1016/j.zool.2005.09.008
Heyer, W.R., Rand, A.S., Da Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1990) Frogs of Boracéia. Arquivos de Zoologia, 31, 231–410.
Inger, R.F. (1966) The systematics and zoogeography of the Amphibia of Borneo. Fieldiana: Zoology, 52, 1–402.
https://doi.org/10.5962/bhl.title.3147
Inger, R.F. & Haile, N.S. (1959) Two new frogs from Sarawak. Sarawak Museum Journal, 9, 270–276.
Inger, R.F. & Tan, F.L. (1990) Recently discovered and newly assigned frog larvae (Ranidae and Rhacophoridae) from Borneo. Raffles Bulletin of Zoology, 38, 3–9.
Inger, R.F. & Wassersug, R.J. (1990) A centrolenid-like anuran larva from Southeast Asia. Zoological Science, 7, 557–561.
Kurabayashi, A., Yoshikawa, N., Sato, N., Hayashi, Y., Oumi, S., Fujii, T. & Sumida, M. (2010) Complete mitochondrial DNA sequence of the endangered frog Odorrana ishikawae (family Ranidae) and unexpected diversity of mt gene arrangements in ranids. Molecular Phylogenetics and Evolution, 56, 543–553.
https://doi.org/10.1016/j.ympev.2010.01.022
Malkmus, R., Kosuch, J. & Kreutz, J. (1999) Die Larve von Staurois tuberilinguis Boulenger, 1918. Eine neue centrolenidenähnliche Kaulquappe aus Borneo (Anura: Ranidae). Herpetozoa, 12, 17–22.
Matsui M., Shimada, T., Ota, H. & Tanaka-Ueno, T. (2005) Multiple invasions of the Ryukyu Archipelago by Oriental frogs of the subgenus Odorrana with phylogenetic reassessment of the related subgenera of the genus Rana. Molecular Phylogenetics and Evolution, 37, 733–742.
https://doi.org/10.1016/j.ympev.2005.04.030
Matsui M., Mohamed, M., Shimada, T. & Sudin, A. (2007) Resurrection of Staurois parvus from S. tuberilinguis from Borneo (Amphibia, Ranidae). Zoological Science, 24, 101–106.
https://doi.org/10.2108/zsj.24.101
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. Biological Journal of the Linnean Society, 38, 369–388.
https://doi.org/10.1111/j.1095-8312.1989.tb01583.x
Preininger, D., Weissenbacher, A., Wampula, T. & Hödl, W. (2012) The conservation breeding of two foot-flagging frog species from Borneo, Staurois parvus and Staurois guttatus. Amphibian and Reptile Conservation, 5(3) 45–56.
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.
https://doi.org/10.1016/j.ympev.2011.06.012
Rada, M., Dos Santos Dias, P.H., Perez-Gonzalez, J.L., Anganoy-Criollo, M., Rueda-Solano, L.A., Pinto-E, M.A., Quintero, L.M., Vargas-Salinas, F. & Grant, T. (2019) The poverty of adult morphology: Bioacoustics, genetics, and internal tadpole morphology reveal a new species of glassfrog (Anura: Centrolenidae: Ikakogi) from the Sierra Nevada de Santa Marta, Colombia. PLoS ONE, 14 (5), e0215349.
https://doi.org/10.1371/journal.pone.0215349
Roelants, K., Jiang, J. & Bossuyt, F. (2004) Endemic ranid (Amphibia: Anura) genera in southern mountain ranges of the Indian subcontinent represent ancient frog lineages: evidence from molecular data. Molecular Phylogenetics and Evolution, 31, 730–740.
https://doi.org/10.1016/j.ympev.2003.09.011
Senevirathne, G., Garg, S., Kemey, R., Meegaskumbura, M. & Biju, S.D. (2016) Unearthing the fossorial tadpoles of the Indian dancing frog family Micrixalidae. PLoS ONE, 11 (3), e0151781.
https://doi.org/10.1371/journal.pone.0151781
Stuart, B.L. (2008) The phylogenetic problem of Huia (Amphibia: Ranidae). Molecular Phylogenetics and Evolution, 46, 49–60.
https://doi.org/10.1016/j.ympev.2007.09.016
Terán Valdez, A. & Guayasamin, J.M. (2014) The tadpole of the glassfrog Chimerella mariaelenae (Anura: Centrolenidae). CienciAmérica, 3, 6–12.
Wassersug, R.J. (1976) Oral morphology of anuran larvae: terminology and general description. Occasional Papers Museum Natural History University Kansas, 48, 1–23.
Wassersug, R. (1980) Internal oral features of larvae from eight anuran families: Functional, systematic, evolutionary and ecological considerations. University of Kansas Museum of Natural History Miscellaneous Publication, 68, 1–146.
https://doi.org/10.5962/bhl.title.16230
Wiens, J.J., Sukumaran, J., Pyron, R.A. & Brown, R.M. (2009) Evolutionary and biogeographic origins of high tropical diversity in Old World frogs (Ranidae). Evolution, 63, 1217–1231.
https://doi.org/10.1111/j.1558-5646.2009.00610.x