Skull development during anuran metamorphosis: I. Early development of the first three bones to form--the exoccipital, the parasphenoid, and the frontoparietal.

Abstract

In anuran amphibians, cranial bones typically first form at metamorphosis when they rapidly invest or replace the cartilaginous larval skull. We describe early development of the first three bones to form in the Oriental fire-bellied toad, Bombina orientalis--the parasphenoid, the frontoparietal, and the exoccipital--based on examination of serial sections. Each of these bones is fully differentiated by Gosner stage 31 (hindlimb in paddle stage) during premetamorphosis. This is at least six Gosner developmental stages before they are first visible in whole-mount preparations at the beginning of prometamorphosis. Thus, developmental events that precede and mediate the initial differentiation of these cranial osteogenic sites occur very early in metamorphosis--a period generally considered to lack significant morphological change. Subsequent development of these centers at later stages primarily reflects cell proliferation and calcified matrix deposition, possibly in response to increased circulating levels of thyroid hormone which are characteristic of later metamorphic stages. Interspecific differences in the timing of cranial ossification may reflect one or both of these phases of bone development. These results may qualify the use of whole-mount preparations for inferring the sequence and absolute timing of cranial ossification in amphibians.