Exceptional features of the embryonic ontogeny of a direct‐developing Robber frog

• Published in: Journal of zoology (1987) Vol. 320; no. 2; pp. 120 - 130
• Main Authors: Salica, M. J., Goldberg, J., Akmentins, M. S., Candioti, F. Vera
• Format: Journal Article
• Language: English
• Published: London Blackwell Publishing Ltd 01-06-2023
• Subjects: Amphibians; Amphibiotic species; Cells; Cytology; embryonic ontogeny; Embryos; enveloping tail; Fins; Frogs; Gas exchange; Gills; Hatching; hatching gland; Juveniles; Larvae; larval operculum; larval stage; Limbs; Morphology; Ontogeny; Operculum; Oreobates berdemenos; Oxygenation; Reduction; Tails; Teeth; Terrarana
• ISSN: 0952-8369; 1469-7998
• DOI: 10.1111/jzo.13060

In frogs, the loss of the free‐living tadpole stage implies deep transformations in morphology and development, and the result is a combination of traits exclusive to direct development with the reduction or absence of typically larval features. Two traits stand out in terraranans, a mostly Neotropical clade with ca. 1200 species known or suspected to have direct development: (1) the development of forelimbs, which unlike in tadpoles and in several unrelated direct‐developing lineages, in this clade is described to occur completely exposed during ontogeny, and (2) the reduction of gills and their physiological replacement by highly vascularized tails for gas exchange. In this contribution, we report unusual aspects of the embryonic ontogeny in the Confused Robber frog Oreobates berdemenos, which complicate the interpretation of morphological diversity in Terrarana and in direct‐developing frogs in general. First, forelimbs develop initially entirely concealed by a larval operculum. Second, tail fins develop dorsal and ventral to the tail muscular core but their arrangement changes to lateral during ontogeny. Third, the expansion of the tail fins appears to be a plastic character whose variation likely responds to individual conditions of humidity and/or oxygenation of each egg within the clutch. Finally, we report cells with the morphology of hatching gland cells in the rostral region of embryos at stages about to hatch. If not vestigial, these cells could assist the egg tooth, which is characteristic of terraranans, with chemical softening of the egg capsules during hatching.
En las ranas, la pérdida del estadio larvas de vida libre implica transformaciones profundas en morfología y desarrollo, y el resultado es una combinación de características exclusivas del desarrollo directo con la reducción o ausencia de características típicamente larvales. Dos rasgos sobresalen en las ranas del clado Terrarana, un grupo mayoritariamente neotropical con ca. 1200 especies en las que se conoce o sospecha desarrollo directo: (1) el desarrollo de los miembros anteriores, que a diferencia de en los renacuajos y otros embriones de desarrollo directo no relacionados, en este grupo ocurre completamente expuesto durante la ontogenia, y (2) la reducción de las branquias y su reemplazo fisiológico por colas muy vascularizadas para el intercambio gaseoso. En esta contribución, reportamos aspectos inusuales en la ontogenia embrionaria de una rana andina con desarrollo directo, Oreobates berdemenos, que complejizan la interpretación de la diversidad morfológica en Terrarana y ranas con desarrollo directo en general. Primero, las patas anteriores se desarrollan durante un tiempo completamente cubiertas por un opérculo larval. Segundo, las aletas caudales se desarrollan dorsoventrales al eje muscular de la cola pero el arreglo cambia a lateral durante la ontogenia. Tercero, la extensión de la cola parece ser un carácter plástico cuya variación posiblemente responda a condiciones individuales de humedad y/u oxigenación de cada huevo en la puesta. Finalmente, reportamos células con morfología de células de glándula de eclosión en la región rostral de embriones próximos a eclosionar; de ser funcionales, estas células podrían asistir al diente del huevo, característico en este clado, con la digestión química de las membranas del huevo durante la eclosión.
We report morphological aspects of the embryonic ontogeny in the Confused Robber frog Oreobates berdemenos, which stand out from what is known in other related direct‐developing frogs. For instance, the tail fins in terraranan embryos are well‐developed and vascularized, and likely compensate the reduction or absence of gills. In O. berdemenos, tail development is also polymorphic, with some tail fins enveloping the embryo completely and some only its posterior half. Our preliminary experiments suggest that fin expansion could respond to individual conditions of humidity and/or oxygenation of eggs within the clutch: a fully enveloping tail would provide a larger and more efficient surface for gas exchange under dry conditions. Further unusual features in this species are a complete operculum concealing part of the forelimb development, and putative hatching gland cells present at hatching. These features, not described to date in terraranan frogs, represent embryonic/larval aspects retained from ancestral biphasic ontogenies.