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Issue: Vol. 4247 No. 4: 29 Mar. 2017
Type: Article
Published: 2017-03-28
DOI: 10.11646/zootaxa.4247.4.4
Page range: 413–428
Abstract views: 170
PDF downloaded: 1

The phytotelm tadpoles of Microhyla arboricola (Anura: Microhylidae) from Vietnam, with comments on reproductive biology and development

Department of Vertebrate Zoology, Biological Faculty, Lomonosov Moscow State University, Leninskie Gory, GSP–1, Moscow 119991, Russia A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, 33, Leninsky prospect, Moscow 117071, Russia Joint Russian-Vietnamese Tropical Research and Technological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam
A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, 33, Leninsky prospect, Moscow 117071, Russia Joint Russian-Vietnamese Tropical Research and Technological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam
Department of Vertebrate Zoology, Biological Faculty, Lomonosov Moscow State University, Leninskie Gory, GSP–1, Moscow 119991, Russia Joint Russian-Vietnamese Tropical Research and Technological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam
Joint Russian-Vietnamese Tropical Research and Technological Centre, Nguyen Van Huyen, Nghia Do, Cau Giay, Hanoi, Vietnam Zoological Museum of Moscow University, Bolshaya Nikitskaya st. 2, Moscow 125009, Russia
Amphibia embryonization oophagy phytotelmata Southeast Asia tadpole

Abstract

The reproductive biology of Microhyla arboricola (Microhylidae) was studied in two regions of the southern Annamite Mountains in Vietnam. M. arboricola is an obligate phytotelm-breeder that reproduces in water-filled tree hollows in montane evergreen forests. Clutches are attached above the water level in the hollows and contain 5–37 pigmented, relatively large eggs. Larvae hatch at markedly advanced stages and develop in water until metamorphosis is completed. The developing tadpoles are obligately oophagous and feed on conspecific eggs and embryos. M. arboricola tadpoles differ from tadpoles of pond-dwelling Microhyla species in their external morphology (extremely long tails, dorsolateral position of the eyes, dark pigmentation), digestive tract morphology (large, extensible larval stomach and short intestine), and oral morphology. The larval chondrocranium and hyobranchiumof M. arboricola is described. M. arboricola shares its habitat with other hollow-breeding species of anurans. To date, M. arboricola is the only known arboreal species of the genus Microhyla that has a unique reproductive mode. The ecological niche of this species differs greatly from those occupied by other microhylids of Indochinese Peninsula.

 

References

  1. Abreliano, F.N., Zaracho, V.H. & Sandoval, M.T. (2015) External ontogenetic changes of larval structures in Elachistocleis bicolor (Anura: Microhylidae: Gastrophryninae). Biologia, 70, 958–967.
    https://doi.org/10.1515/biolog-2015-0101

    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.
    https://doi.org/10.2307/1466987

    Altig, R. & Kelly, J.P. (1974) Indices of feeding in anuran tadpoles as indicated by gut characteristics. Herpetologica, 30, 200–203.

    AmphibiaWeb (2016) AmphibiaWeb: Information on amphibian biology and conservation. [web application], AmphibiaWeb, Berkeley, California. Available from: http://amphibiaweb.org/ (accessed 14 December 2016)

    Anstis, M., Parker, F., Hawkes, T., Morris, I. & Richards, S.J. (2011) Direct development in some Australopapuan microhylid frogs of the genera Austrochaperina, Cophixalus and Oreophryne (Anura: Microhylidae) from northern Australia and Papua New Guinea. Zootaxa, 3052, 1–50.

    Blommers-Schlösser, R.M.A. (1975) Observations on the larval development of some Malagasy frogs, with notes on their ecology and biology (Anura: Dyscophinae, Scaphiophryninae and Cophylinae). Beaufortia, 24, 7–26.

    Chou, W.-H. & Lin, J.-Y. (1997) Tadpoles of Taiwan. Special Publication National Museum of Natural Science, 7, 1–98.

    Das, I. & Haas, A. (2010) New species of Microhyla from Sarawak: Old World's smallest frogs crawl out of miniature pitcher plants on Borneo (Amphibia: Anura: Microhylidae). Zootaxa, 2571, 37–52.

    Donnelly, M. A., de Sá, R.O. & Guyer, C. (1990) Description of the tadpoles of Gastrophryne pictiventris and Nelsonophryne aterrima (Anura: Microhylidae), with a review of morphological variation in free-swimming microhylid larvae. Novitates, 2976, 1–19.

    Duellman, W. & Trueb, L. (1994) Biology of Amphibians. Johns Hopkins University Press, Baltimore, MD, 670 pp.

    Fabrezi, M., Quinzio, S., Goldberg, J. & de Sá, R.O. (2012) The Development of Dermatonotus muelleri (Anura: Microhylidae: Gastrophryninae). Journal of Herpetology, 46, 363–380.
    https://doi.org/10.1670/11-194

    Frost, D.R. (2016) Amphibian Species of the World: an Online Reference. Version 6.0. Electronic Database. American Museum of Natural History, New York, USA. Available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 14 December 2016)

    Gibson, R.C. & Buley, K.R. (2004) Maternal care and obligatory oophagy in Leptodactylus fallax: A new reproductive mode in frogs. Copeia, 2004, 128–135.
    https://doi.org/10.1643/CE-02-091R2

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

    Haas, A. (2003) Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics, 19, 23–89.
    https://doi.org/10.1016/s0748-3007(03)00006-9

    Haddad, C.F.B., Faivovich, J. & Garcia, P.C.A. (2005) The specialized reproductive mode of the tree frog Aplastodiscus perviridis (Anura: Hylidae). Amphibia-Reptilia, 26, 87–92.
    https://doi.org/10.1163/1568538053693224

    Hendrix, R., Gawor, A., Vences, M. & Ziegler, T. (2008) The tadpole of the narrow-mouthed frog Microhyla fissipes from Vietnam. Zootaxa, 1675, 67–68.

    Heyer, W.R. (1973) Ecological interactions of frog larvae at a seasonal tropical location in Thailand. Journal of Herpetology, 7, 337–361.
    https://doi.org/10.2307/1562868

    Heyer, W.R. (1974) Niche measurements of frog larvae from a seasonal tropical location in Thailand. Ecology, 55, 651–656.
    https://doi.org/10.2307/1935156

    Heying, H. (2004) Reproductive limitation by oviposition site in a treehole breeding madagascan poison frog (Mantella laevigata). In: Lehtinen , R.M. (Ed.), Ecology and Evolution of Phytotelm Breeding Anurans. Miscellaneous Publications, Museum of Zoology, University of Michigan, No. 193. Ann Arbor, Michigan, pp. 23–30.

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

    Inger, R.F. & Colwell, R.K. (1977) Organization of contiguous communities of amphibians and reptiles in Thailand. Ecological Monographs, 47, 229–253.
    https://doi.org/10.2307/1942516

    Jungfer, K.-H. & Weygoldt, P. (1999) Biparental care in the tadpole feeding Amazonian treefrog Osteocephalus oophagus. Amphibia–Reptilia, 20, 235–249.
    https://doi.org/10.1163/156853899X00277

    Kam, Y.-C., Su, Y.-J., Liu, J.-L. & Lin, Y.-S. (2001) Intraspecific interactions among oophagous tadpoles (Chirixalus eiffingeri: Rhacophoridae) living in bamboo stumps in Taiwan. Journal of Zoology, 255, 519–524.
    https://doi.org/10.1017/S0952836901001601

    Krishna, S.N., Krishna, S.B. & Vijayalaxmi, K.K. (2004) Breeding ecology of a rare microhylid, Ramanella montana, in the forests of Western Ghats, India. Current Science, 87, 80–82.

    Krügel, P. & Richter, S. (1995) Syncope antenori: a bromeliad breeding frog with free-swimming, nonfeeding tadpoles (Anura, Microhylidae). Copeia, 1995, 955–963.
    https://doi.org/10.2307/1447045

    Lannoo, M.J., Townsend, D.S. & Wassersug, R.J. (1987) Larval life in the leaves: arboreal tadpole types, with special attention to the morphology, ecology, and behavior of the oophagous Osteopilus brunneus (Hylidae) larvae. Fieldiana Zoology, 38, 1–31.

    Lehtinen, R.M., Lannoo, M.J. & Wassersug, R.J. (2004) Phytotelm-breeding anurans: past, present and future research. In: Lehtinen , R.M. (Ed.), Ecology and Evolution of Phytotelm Breeding Anurans. Miscellaneous Publications, Museum of Zoology, University of Michigan, No. 193. Ann Arbor, Michigan, pp. 1–9.

    Liang, M.-F., Huang, C.-H. & Kam, Y.-C. (2002) Effects of intermittent feeding on the growth of oophagous (Chirixalus eiffingeri) and herbivorous (Chirixalus idiootocus) tadpoles from Taiwan. Journal of Zoology, 256, 207–213.
    https://doi.org/10.1017/S0952836902000249

    Lim, K.K.P. & Ng, P.K.L. (1991) Nepenthiphilous larvae and breeding habits of the sticky frog, Kalophrynus pleurostigma Tschudi (Amphibia: Microhylidae). The Raffles Bulletin of Zoology, 39, 209–214.

    Matsuda, R. (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. John Wiley and Sons, New York, 355 pp.

    Matsui, M. (2011) Taxonomic revision of one of the Old World’s smallest frogs, with description of a new Bornean Microhyla (Amphibia, Microhylidae). Zootaxa, 2814, 33–49.
    https://doi.org/10.11646/zootaxa.2814.1.3

    Noble, G.K. (1929) The adaptive modifications of the arboreal tadpoles of Hoplophryne and the torrent tadpoles of Staurois. Bulletin of the American Museum of Natural History, 58, 291–334.

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

    Poyarkov, N.A., Vassilieva, A.B., Orlov, N.L., Galoyan, E.A., Tran, D.T.A., Le, D.T.T., Kretova, V.D. & Geissler, P. (2014) Taxonomy and distribution of narrow-mouth frogs of the genus Microhyla Tschudi, 1838 (Anura: Microhylidae) from Vietnam with descriptions of five new species. Russian Journal of Herpetology, 21, 89–148.

    Ramaswami, L.S. (1940) Some aspects of the chondrocranium of the South Indian frogs. Journal of Mysore University, 1, 15–41.

    Rödel, M.O. (1998) A reproductive mode so far unknown in African ranids: Phrynobatrachus guineensis Guibé and Lamotte, 1961 breeds in tree holes. Herpetozoa, 11, 19–26.

    Rowley, J.J.L., Tran, D.T.A., Le, D.T.T., Hoang, H.D. & Altig, R. (2012) The strangest tadpole: the oophagous, tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam. Journal of Natural History, 46, 2969–2978.
    https://doi.org/10.1080/00222933.2012.732622

    Schiesari, L., Gordo, M. & Hödl, W. (2003) Tree holes as calling, breeding, and developmental sites for the Amazonian canopy frog, Phrynohyas resinifictrix (Hylidae). Copeia, 2003, 263–272.
    https://doi.org/10.1643/0045-8511(2003)003[0263:TACBAD]2.0.CO;2

    Shimizu, S. & Ota, H. (2003) Normal development of Microhyla ornata: The first description of the complete embryonic and larval stages for the microhylid frogs (Amphibia: Anura). Current Herpetology, 22, 73–90.
    https://doi.org/10.5358/hsj.22.73

    Trueb, L., Diaz, R. & Blackburn, D.C. (2011) Osteology and chondrocranial morphology of Gastrophryne carolinensis (Anura: Microhylidae), with a review of the osteological diversity of New World microhylids. Phyllomedusa, 10, 99–135.
    https://doi.org/10.11606/issn.2316-9079.v10i2p99-135

    Vassilieva, A.B., Galoyan, E.A. & Poyarkov, N.A. Jr. (2013) Rhacophorus vampyrus (Anura: Rhacophoridae) reproductive biology: A new type of oophagous tadpole in Asian treefrogs. Journal of Herpetology, 47, 607–614.
    https://doi.org/10.1670/12-180

    Vassilieva, A.B., Galoyan, E.A., Gogoleva, S.S. & Poyarkov, N.A. Jr. (2014) Two new species of Kalophrynus Tschudi, 1838 (Anura: Microhylidae) from the Annamite mountains in southern Vietnam. Zootaxa, 3796 (3), 401–434.
    https://doi.org/10.11646/zootaxa.3796.3.1

    Vera Candioti, M.F. (2007) Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits. Zootaxa, 1600, 1–175.

    Wassersug, R.J. (1980) Internal oral features of larvae from eight Anuran families: functional, systematic, evolutionary, and ecological considerations. Miscellaneous Publications of the Museum of Natural History, University of Kansas, 68, 1–146.
    https://doi.org/10.5962/bhl.title.16230

    Wells, K.D. (2007) The Ecology and Behaviour of Amphibians. Chicago University Press, Chicago, 1148 pp.
    https://doi.org/10.7208/chicago/9780226893334.001.0001

    Yuan, Z.-Y., Suwannapoom, C., Yan, F., Poyarkov, N.A., Nguyen, N.S., Siriwadee, C., Murphy, R., Zhang, Y.-P. & Che, J. (2016) Red River barrier and Pleistocene climatic fluctuations shaped the genetic structure of Microhyla fissipes complex (Anura: Microhylidae) in southern China and Indochina. Current Zoology, 2016, 1–13.
    https://doi.org/10.1093/cz/zow042