Surface anatomy of branchial food traps of tadpoles: A comparative study

Abstract

Branchial food traps are regions of specialized secretory tissue in the tadpole pharynx, where suspended food particles are trapped in mucus. Light and scanning electron microscopy were used to study branchial food traps from larvae of ten anuran families (36 species). Most anuran larvae from “advanced” (suborder Neobatrachia) families (e.g., Hylidae, Ranidae, Bufonidae) have distinct secretory pits at the posterior margins of the branchial food traps and secretory ridges elsewhere on these surfaces. The apices of columnar PAS-positive, secretory cells are exposed on the floors of the secretory pits or in rows at the tops of the secretory ridges (secretory zone). Tadpoles from most “archaic” (suborder Archaeobatrachia) families (Ascaphidae, Discoglossidae and Pelobatidae) either lack secretory pits, or have them poorly defined. They also lack secretory ridges but have columnar, mucus-secreting cells whose apices are exposed in a seemingly random fashion in the branchial food traps. Rhinophrynus (Archaeobatrachia: Rhinophrynidae) has secretory ridges, but the apices of secretory cells are not arranged in rows at the tops of the ridges; instead they erupt singly or in small clusters on the epithelial surface, in a pattern similar to that in Ascaphus, the discoglossids and the pelobatids. It is proposed that the generalized condition for the branchial food trap mucosa is one where the apices of secretory cells are exposed haphazardly on a flat epithelium and the derived condition is one where the surface is organized into ridges. The morphology of the branchial food traps in Rhinophrynus suggests that, phylogenetically, ridges preceded the coalescing of secretory cell apices into distinct rows. Pipidae and Microhylidae have unique patterns in the gross and microanatomy of their branchial food traps specific to their families. Branchial food trap morphology relates to diets of tadpoles as well as to taxonomy. Obligate macrophagous (e.g., carnivorous) tadpoles, irrespective of family, tend to have reduced branchial food traps, regularly lack secretory ridges and, in extreme cases, lack columnar mucus-secreting cells. Obligate microphagous forms (midwater suspension feeding of Xenopus, microhylids and Agalychnis), have straight parallel secretory ridges with narrow secretory zones and shallow troughs between the ridges. Secretory ridges may help to form mucus strands in which food particles are trapped, but they are not essential for planktonic entrapment. The hydrodynamic implications of the various topographic patterns remain unclear.