Evolutionary and developmental considerations of the diet and gut morphology in ceratophryid tadpoles (Anura)

Abstract

Background: Before metamorphosis, almost all anuran tadpoles are omnivores. Larval carnivory occurs in some species and, it is associated with distinctive morphotypes. Obligatory carnivorous tadpoles exhibit structural changes in the gastrointestinal tract compared to larvae that are predominately omnivores. The most distinctive feature of the anuran family Ceratophyridae (three genera) overall is the enormous gape of adults. This feature increases their ability to capture extremely large and active prey. The larvae of Ceratophyrid genera are remarkably distinct from each other and carnivory has diversified in a manner unseen in other anurans. The larvae of one genus, Lepidobatrachus, has a massive gape like the adult. Herein, we report on larval developmental variation, diet, gross morphology of the gastrointestinal tract, and histology of the cranial segment of the gut before, during and after metamorphosis in larval series for the following ceratophryid species: Chacophrys pierottii, Ceratophrys cranwelli, Lepidobatrachus laevis and Lepidobatrachus llanensis. Results: We described patterns of larval development with variation in growth with consequence to the final size at the end of metamorphosis. These patterns seem to be influenced by food quantity/quality, and most predominant by animal protein. Prey items found in pre and post-metamorphic Lepidobatrachus spp. are similar. Tadpoles of Ceratophrys and Chacophrys (and other anurans) share a short cranial segment of the gut with an internal glandular, mucous secreting epithelium, a double coiled intestine and the sequence of metamorphic changes (tract is empty, the stomach differentiates and the intestine shortens abruptly). In contrast, Lepidobatrachus tadpoles have a true stomach that acquires thickness and increased glandular complexity through development. As larvae they have a short intestine without double coils, and the absence of intestine shortening during metamorphosis. Conclusions: The larval development of the gastrointestinal tract of Lepidobatrachus is unique compared with that of other free-living anuran larvae. An abrupt metamorphic transformation is missing and most of the adult structural features start to differentiate gradually at the beginning of larval stages.

Development of the adult-like larval stomach of Lepidobatrachus laevis

“…The larval stomach of Lepidobatrachus laevis is highly unusual among metamorphosing frogs. The only other tadpole known to have a similar stomach and developmental trajectory belongs to the congeneric species L. llanensis , and to a lesser degree frogs of the genus Ceratophrys (Fabrezi & Cruz, 2020). (Larval stomach morphology of the third species of Lepidobatrachus, L. asper , is not described, but presumably it resembles that of its two congeners.)…”

“…The adult-like morphology of the larval stomach reflects this extreme as well; even relative to carnivorous tadpoles of other species, such as Ceratophrys, the larval stomach of L. laevis is most similar to that of adults (Bloom, 2013;Fabrezi & Cruz, 2020).…”

“…It does, however, bear some resemblance to the larval stomach of other carnivorous tadpoles, such as the closely related Ceratophrys, which independently evolved larval carnivory, although in a less extreme form designated "macrophagous feeding" (Fabrezi et al, 2016;Fabrezi & Cruz, 2020). Ceratophrys also have discrete fundic and pyloric regions of the stomach as tadpoles; however, their stomachs are smaller at the onset of larval feeding and have less-folded epithelia, smaller layers of connective tissue and very little muscle (Bloom et al, 2013;Fabrezi & Cruz, 2020). Despite the adult-like feeding behavior of larval Lepidobatrachus and the adult-like subfunctionalization of its gastric anatomy, its stomach lacks some of the complexity typical of the adult stomach of anurans and other vertebrates (Carroll, et al 1991;Fabrezi & Cruz, 2020).…”

“…Ceratophrys also have discrete fundic and pyloric regions of the stomach as tadpoles; however, their stomachs are smaller at the onset of larval feeding and have less-folded epithelia, smaller layers of connective tissue and very little muscle (Bloom et al, 2013;Fabrezi & Cruz, 2020). Despite the adult-like feeding behavior of larval Lepidobatrachus and the adult-like subfunctionalization of its gastric anatomy, its stomach lacks some of the complexity typical of the adult stomach of anurans and other vertebrates (Carroll, et al 1991;Fabrezi & Cruz, 2020).…”

“…The tadpole is able to capture, ingest and digest live animal prey almost as large as itself (Ruibal & Thomas, 1988; Carroll et al ., 1991; Fabrezi et al ., 2016). They also are able to feed throughout metamorphosis (Ruibal & Thomas, 1988; Fabrezi & Cruz 2020). The ability to consume animal prey continuously from hatching through and beyond metamorphosis, paired with previous studies of larval stomach histology (Ruibal & Thomas, 1988), suggests that L. laevis does not form a typical larval stomach during embryogenesis, but instead forms an adult-like stomach that does not transform significantly during metamorphosis.…”