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

Abstract

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.