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External ontogenetic changes of larval structures in Elachistocleis bicolor (Anura: Microhylidae: Gastrophryninae)

  • Fernanda N. Abreliano , Víctor H. Zaracho EMAIL logo and María T. Sandoval
Published/Copyright: August 25, 2015
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Biologia
From the journal Biologia Volume 70 Issue 7

Abstract

Although the external larval morphology of many species of Microhylidae has been characterized, ontogenetic studies in the family are scarce and partial. In the present study, we describe the development of the oral funnel, external gills, external nares, operculum, spiracle, and adhesive organs of Elachistocleis bicolor with the aim to contribute to future ontogenetic, evolutionary, and phylogenetic studies. The development of E. bicolor is similar to that of other species with free-swimming tadpoles as Microhyla ornata, Dermatonotus muelleri and Uperodon globulosus. The ontogeny of the oral apparatus shows only the early stages of the pattern most common in anurans. After the invagination of the stomodeum, the anterior and posterior labia are defined, but the keratinized structures are not formed. The conical adhesive glands are similar to those of Physalaemus and Dendropsophus tadpoles, but in E. bicolor, these develop in contact with the posterior labium. The external nares remain closed during most of the larval phase. During ontogeny, the external gills are simultaneously covered by a transverse operculum fold, which later advances towards the posteromedial ventral region, forming the spiracle, while in Type IV larvae the operculum folds close from right to left, covering the right gill first. The distinct larval characters of Microhylidae appear between the last embryonic stages and the first larval stages. Therefore, the consideration of these stages can be of great value in future studies of anuran development in phylogenetic and evolutionary contexts. Ontogenetic studies in microhylid tadpoles are fundamental to identify heterochronic processes, to interpret the variability of larval structures, and to establish or reinforce hypotheses about the origin of larval structures.

Keywords: anurans; development; spiracle; oral funnel; external gills; nares

References

Altig R. 2006. Discussions of the origin and evolution of the oral apparatus of anuran tadpoles. Acta Herpetol. 1 (2): 95-105. DOI: http://dx.doi.org/10.13128/ActaHerpetol-1292Search in Google Scholar

Altig R. & Johnston G.F. 1989. Guilds of anuran larvae: relationships among developmental modes, morphologies and habitats. Herpetol. Monogr. 3: 81-109. DOI: 10.2307/146698710.2307/1466987Search in Google Scholar

Altig R. & McDiarmid R.W. 1999. Body plan. Development and morphology, Chapter 3, pp. 24-51. In: McDiarmid R.W. & Altig R. (eds), Tadpoles, The Biology of Anuran Larvae, University of Chicago Press, Chicago and London, 458 pp. ISBN: 9780226557625Search in Google Scholar

Anstis M. 2008. Direct development in the Australian myobatrachid frog Metacrinia nichollsi from Western Australia. Records of the Western Australian Museum 24 (2007-2008) Part 2: 133-150.10.18195/issn.0312-3162.24(2).2008.133-150Search in Google Scholar

Anstis M., Parker F., Hawkes T., Morris I. & Stephen J.R. 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.Search in Google Scholar

Anstis M., Roberts J.D. & Altig R. 2007. Direct development in two myobatrachid frogs, Arenophryne rotunda Tyler and Myobatrachus gouldii Gray, from Western Australia. Records of the Western Australian Museum 23 (2006-2007) Part 3: 259-271.10.18195/issn.0312-3162.23(3).2007.259-271Search in Google Scholar

Baorong G., Qing W. & Qiujin Z. 1996. Early embryonic development in Microhyla ornata Chin. J. Zool. 31 (5): 17-21.Search in Google Scholar

Bowatte G. & Meegaskumbura M. 2011. Morphology and ecology of tadpoles of Ramanella obscura (Anura: Microhylidae). Ceylon J. Sci. (Biol. Sci.) 40 (2): 109-120. DOI: 10.4038/cjsbs.v40i2.392710.4038/cjsbs.v40i2.3927Search in Google Scholar

Callery E.M. & Elinson R.P. 2000. Opercular development and ontogenetic re-organization in a direct-developing frog. Dev. Genes Evol. 210 (7): 377-381. DOI: 10.1007/s00427000007010.1007/s004270000070Search in Google Scholar PubMed

Del Conte E. & Sirlin J.L. 1951. Serie tipo de los primeros estadios embrionarios en Bufo arenarum. Acta Zool. Lilloana 12: 495-499. Search in Google Scholar

de Sa R.O., Streicher J.W., Sekonyela R., Forlani M.C., Loader S.P., Greenbaum E., Richards S. & Haddad C.F. 2012. Molecular phylogeny of microhylid frogs (Anura: Microhylidae) with emphasis on relationships among New World genera. BMC Evol. Biol. 12: 1-21. DOI: 10.1186/1471-2148-12-24110.1186/1471-2148-12-241Search in Google Scholar PubMed PubMed Central

Desnitskiy A.G. 2012. On the diversity of the initial steps of embryonic development in anuran amphibians. Russ. J. Herpetol. 19 (3): 221-231.Search in Google Scholar

Donnelly M.A., de Sa 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. American Museum Novitates 2976: 1-19.Search in Google Scholar

Echeverria D.H. & Lavilla E.O. 2000. Internal oral morphology of tadpoles of Dermatonotus muelleri and Elachistocleis bicolor (Anura: Microhylidae). J. Herpetol. 34 (4): 517-523. DOI: 10.2307/156526510.2307/1565265Search in Google Scholar

Fabrezi M., Quinzio S., Goldberg J. & de Sa R. 2012. The development of Dermatonotus muelleri (Anura: Microhylidae: Gastrophrynae). J. Herpetol. 46: 363-380. DOI: http://dx.doi.org/10.1670/11-19410.1670/11-194Search in Google Scholar

Fiorito de Lopez L.E. & Echeverria D.D. 1989. Microanatomia e histogenesis del aparato bucal en las larvas de Bufo arenarum (Anura, Bufonidae). Cuadernos de Herpetologia 4 (2): 4-10.Search in Google Scholar

Gosner K.L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16 (3): 183-190.Search in Google Scholar

Griffiths I. & De Carvalho A.L. 1965. On the validity of employing larval characters as major phyletic indices in Amphibia, Salientia. Rev. Bras. Biol. 23: 113-21.Search in Google Scholar

Grosjean S., Glos J., Teschke M., Glaw F. & Vences M. 2007. Comparative larval morphology of Madagascan toadlets of the genus Scaphiophryne: phylogenetic and taxonomic inferences. Zool. J. Linn. Soc. Lond. 151 (3): 555-576. DOI: 10.1111/j.1096-3642.2007.00329.x 10.1111/j.1096-3642.2007.00329.xSearch in Google Scholar

Günther R. 2006. Derived reproductive modes in New Guinean anuran amphibians and description of a new species with paternal care in the genus Callulops (Microhylidae). J. Zool. 268 (2): 153-170. DOI: 10.1111/j.1469-7998.2005.00007.x 10.1111/j.1469-7998.2005.00007.xSearch in Google Scholar

Hall J.A., Larsen J.H. & Fitzner R.E. 1997. Postembryonic ontogeny of the spadefoot toad, Scaphiopus intermontanus (Anura: Pelobatidae): External morphology. Herpetol. Monogr. 11 (1997): 124-178. DOI: 10.2307/1467009 10.2307/1467009Search in Google Scholar

Inger R. 1967. The development of a phylogeny of frogs. Evolution 21 (2): 369-384 DOI: 10.2307/240668510.2307/2406685Search in Google Scholar

Johnson G.R. & Richards S.J. 1993. Observations on the breeding biology of a microhylid frog (genus Oreophryne) from New Guinea. Trans. Roy. Soc. South Australia 117 (2): 105-107.Search in Google Scholar

Kenny J.S. 1969. The amphibia of Trinidad. Studies on the Fauna of Cura，cao and other Caribbean Islands, No. 108, 78 pp.Search in Google Scholar

Krügel P. & Richter S. 1995. Syncope antenori-A bromeliad breeding frog with free-swimming, nonfeeding tadpoles (Anura, Microhylidae). Copeia 4: 955-963. DOI: 10.2307/ 144704510.2307/1447045Search in Google Scholar

Kwet A. & Di-Bernardo M. 1998. Elachistocleis erythrogaster, a new microhylid species from Rio Grande do Sul, Brazil. Studies on Neotropical Fauna and Environment 33 (1): 7-18. DOI: 10.1076/snfe.33.1.7.216910.1076/snfe.33.1.7.2169Search in Google Scholar

Langone J.A., Lavilla E.O., Echeverria D.D., Mangione S. & Segalla M.V. 2007. Morfologia externa e interna de la larva de Chiasmocleis leucosticta (Boulenger, 1888) (Amphibia, Anura, Microhylidae). Publicacion Extra, Museo Nacional de Historia Natural y Antropologia (Montevideo) 2: 1-17.Search in Google Scholar

Laufer G., Pereyra L.C., Akmentins M.S. & Borteiro C. 2013. A comment on the oral dermal flaps of Elachistocleis Parker, 1927 (Anura: Microhylidae) larvae. Zootaxa 3710 (5): 498-500. DOI: http://dx.doi.org/10.11646/zootaxa.3710.5.710.11646/zootaxa.3710.5.7Search in Google Scholar PubMed

Lavilla E.O. 1992. The tadpole of Dermatonotus muelleri (Anura: Microhylidae). Bolletino del Museo Regionale di Scienze Naturali di Torino 10: 63-71.Search in Google Scholar

Lavilla E.O. & Langone J.A. 1991. Ontogenetic changes in spiracular and proctodeal tube orientation in Elachistocleis bicolor (Anura: Microhylidae). J. Herpetol. 25 (1): 119-121. DOI: 10.2307/156481110.2307/1564811Search in Google Scholar

Lavilla E.O. & Langone J.A. 1995. Estructura del condrocraneo y esqueleto visceral de larvas de Elachistocleis bicolor (Valenciennes, 1938) (Anura: Microhylidae). Cuadernos de Herpetologia 9 (1): 45-49.Search in Google Scholar

Lavilla E.O. & Rouges M. 1992. Reproduccion y desarrollo de anuros argentinos. Asociacion Herpetologica Argentina Serie Divulgacion Cientifica 5: 1-66.Search in Google Scholar

Lehr E., Trueb L., Venegas P. & Arbelaez E. 2007. Descriptions of the tadpoles of two Neotropical Microhylid frogs, Melanophryne carpish and Nelsonophryne aequatorialis (Anura: Microhylidae). J. Herpetol. 41 (4): 581-589.10.1670/06-252.1Search in Google Scholar

Mac Culloch R.D., Lathrop A., Minter L.R. & Khan S.Z. 2008. Otophryne (Anura: Microhylidae) from the highlands of Guyana: redescriptions, vocalizations, tadpoles and new distributions. Papeis Avulsos de Zoologia (S˘ao Paulo) 48 (22): 247-261.Search in Google Scholar

Magalhäes F.M., Santana D.J., Neto A.M. & Garda A.A. 2012. The tadpole of Elachistocleis cesarii Miranda-Ribeiro, 1920 (Anura, Microhylidae). Zootaxa 3187: 54-56.Search in Google Scholar

Marinelli M.D., Tei M. & Sensi P. 1985. SEM observation on the development and the regression of the oral disc of Bufo vulgaris larvae. Acta Embryol. Morphol. Exp. 6 (1): 31-39.Search in Google Scholar

Narzary J. & Bordoloi S. 2013. Study of normal development and external morphology of tadpoles of Microhyla ornata and Uperodon globulosus of the family Microhylidae (Amphibia: Anura) from North East India. Int. J. Adv. Biol. Res. 3 (1): 61-73.Search in Google Scholar

Nascimento F.A.C. & Shuk G.O. 2006. O girino de Chiasmocleis alagoanus Cruz, Caramaschi & Freire, 1999 (Anura: Microhylidae) [The tadpole of Chiasmocleis alagoanus Cruz, Caramaschi & Freire, 1999 (Anura: Microhylidae)]. Biota Neotrop. 6 (3): 1-5. DOI: 10.1590/S1676-0603200600030002110.1590/S1676-06032006000300021Search in Google Scholar

Nokhbatolfoghahai M. & Downie J.R. 2005a. Embryonic external nares in the microhylid Elachistocleis ovalis, with a review of narial development in microhylid tadpole. Herpetol. J. 15: 191-194.Search in Google Scholar

Nokhbatolfoghahai M. & Downie J.R. 2005b. Larval cement gland of frogs: comparative development and morphology. J. Morphol. 263 (3): 270-283. DOI: 10.1002/jmor.10305 10.1002/jmor.10305Search in Google Scholar PubMed

Nokhbatolfoghahai M. & Downie J.R. 2008. The external gills of anuran amphibians: comparative morphology and ultrastructure. J. Morphol. 269 (10): 1197-1213. DOI: 10.1002/jmor.1065510.1002/jmor.10655Search in Google Scholar PubMed

Orton G. 1953. The systematics of vertebrate larvae. Sys. Zool. 2 (2): 63-75. DOI: 10.2307/241166110.2307/2411661Search in Google Scholar

Padhye A.D. & Ghate H.V. 1989. Preliminary photographic record and description of various developmental stages of the frog Microhyla ornata (Dumeril and Bibron). Herpeton 2: 2-7Search in Google Scholar

Pereyra L.C., Akmentins M.S., Laufer G. & Vaira M. 2013. A new species of Elachistocleis (Anura: Microhylidae) from north-western Argentina. Zootaxa 3694 (6): 525-544. DOI: http://dx.doi.org/10.11646/zootaxa.3694.6.210.11646/zootaxa.3694.6.2Search in Google Scholar PubMed

Rada de Martinez D. 1981. Renacuajos de algunos anfibios de Clarines. (Edo. Anzoategui, Venezuela). Memoria - Sociedad de Ciencias Naturales La Salle 41 (115): 57-75.Search in Google Scholar

Rodrigues D.J., Menin M., Lima A.P. & Mokross K.S. 2008. Tadpole and vocalizations of Chiasmocleis hudsoni (Anura, Microhylidae) in Central Amazonia, Brazil. Zootaxa 1680: 55-58.10.11646/zootaxa.1680.1.3Search in Google Scholar

Rossa-Feres D.C. & Nomura F. 2006. Characterization and taxonomic key for tadpoles (Amphibia: Anura) from the northwestern region of S˘ao Paulo State, Brazil. Biota Neotrop. 6 (1): 1-26. DOI: http://dx.doi.org/10.1590/S1676-0603200 6000100014Search in Google Scholar

Salica M.J., Haad M.B., Vera Candioti F. & Faivovich J. 2011. Early development of two species of Phyllomedusa (Anura: Phyllomedusinae). Salamandra 47 (3): 144-154.Search in Google Scholar

Shaolong L., Zhiming S., Jiazao Z., Mingyou H., Quan Z. & Young L. 1996. Studies on early embryonic development in Microhyla ornata. Journal of Sichuan University (Natural Science Edition) 33 (3): 323-329.Search in Google Scholar

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). Bull. Herpetol. Soc. Japan 22 (2): 73-90. DOI: 10.5358/hsj.22.7310.5358/hsj.22.73Search in Google Scholar

Takahama H., Sasaki F., Tachibana T., Iseki H., Horiguchi T., Kinoshita T. & Watanabe K. 1987. Fine structure and degeneration of the horny teeth and the epidermis of the labial ridge of the anuran tadpole. Tsurumi Shigaku 13 (1): 49-63. PMID: 3509793Search in Google Scholar

Thibaudeau G. & Altig R. 1988. Sequence of ontogenetic development and atrophy of the oral apparatus of six anuran tadpoles. J. Morphol. 197 (1): 63-69. DOI: 10.1002/jmor.10519 7010610.1002/jmor.10519Search in Google Scholar PubMed

Towsend D.S. & Stewart M.M. 1985. Direct development in Eleutherodactylus coqui (Anura: Leptodactylidae): a stagning table. Copeia 1985 (2): 423-436. DOI: 10.2307/144485410.2307/1444854Search in Google Scholar

Vera Candioti M.F. 2006. Morfologia larval de Chiasmocleis panamensis, con comentarios sobre la variabilidad morfologica interna en renacuajos de Microhylidae (Anura). Alytes 24 (1): 91-108.Search in Google Scholar

Vera Candioti M.F., Nu˜nez J.J. & Ubeda C. 2011. Development of the nidicolous tadpoles of Eupsophus emiliopugini (Anura: Cycloramphidae) until metamorphosis, with comments on systematic relationships of the species and its endotrophic developmental mode. Acta Zool. (Stockh.) 92: 27-45. DOI: 10.1111/j.1463 6395.2010.00448.x Wassersug R.J. 1980. Internal oral features of larvae from height anuran families: functional, systematic, evolutionary and ecological considerations. Miscellaneous Publication University of Kansas Museum of Natural History 68: 1-146.Search in Google Scholar

Wassersug R.J. 1989. What, if anything is a microhylid (Orton type II) tadpole?, pp. 534-538. In: Splechtna H. (ed.), Trends in Vertebrate Morphology: Proceedings of the 2nd International Symposium on Vertebrate Morphology, Vienna, 1986, G. Fischer, Stuttgart, New York, 647 pp. ISBN: 0895742888 (U.S.) Search in Google Scholar

Wiliams J.D. & Gudynas E. 1987. Descripcion de la larva de Elachistocleis bicolor (Valenciennes, 1838) (Anura: Microhylidae). Amphibia-Reptilia 8 (3): 225-229. DOI: 10.1163/156 853887X00261Search in Google Scholar

Wogel H., Abrunhosa P. & Prado G. 2004. The tadpole of Chiasmocleis carvalhoi and the advertisement calls of three species of Chiasmocleis (Anura, Microhylidae) from the Atlantic rainforest of southeastern Brazil. Phyllomedusa: Journal of Herpetology 3 (2): 133-140. DOI: http://dx.doi.org/10. 11606/issn.2316 9079.v3i2p133-14010.11606/issn.2316-9079.v3i2p133-140Search in Google Scholar

Xu M.Y. & Xu J. 2012. Preliminary observations on postembryonic development of Microhyla ornata in North Guangdong. Sichuan J. Zool. 31 (4): 589-592. DOI: 10.3969/j.issn. 1000-7083.2012.04.015Search in Google Scholar

Zaracho V.H., Cespedez J.A. & Alvarez B.B. 2003. Descripcion de caracteres morfologicos en larvas prometamorficas de Physalaemus biligonigerus (Anura: Leptodactylidae). FACENA 19: 123-134. Search in Google Scholar

Received: 2014-10-9
Accepted: 2015-6-15
Published Online: 2015-8-25
Published in Print: 2015-7-1

© 2015 Institute of Zoology, Slovak Academy of Sciences

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https://doi.org/10.1515/biolog-2015-0101
Keywords for this article
anurans; development; spiracle; oral funnel; external gills; nares

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  5. Reciprocal contamination by invasive plants: analysis of trade exchange between Slovakia and Romania
  6. Agrobacterium-mediated transformation of chitinase gene from the actinorhizal tree Casuarina equisetifolia in Nicotiana tabacum
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