Formation of cartilage in the heart of the Spanish terrapin, Mauremys leprosa (Reptilia, Chelonia).

Abstract

Cartilaginous deposits are regularly present in the heart of several reptilian, avian, and mammalian species. The formation of these extraskeletal cartilages has been studied in birds and mammals, but not in reptiles. The aim here was to elucidate this question in the Spanish terrapin. Hearts from 23 embryos belonging to Yntema (1968) developmental stages 17 to 26 and eight terrapins age 3 months to 10 years were examined using histological, histochemical, and immunohistochemical techniques. In the heart of the Spanish terrapin (Mauremys leprosa), chondrogenesis can start during embryonic life. Cartilaginous tissue develops from a mesenchymal cellular condensation that extends along the aorticopulmonary septum and the incipient pars fibrosa of the ventricular horizontal septum. This cellular condensation, which is smooth muscle alpha-actin (SMalpha-actin)-negative and type II collagen-negative during stages 17 to 22, acts as a prechondrogenic condensation. In stage 23, production of type II collagen begins in the central core of the condensation and gradually spreads toward its periphery. The type II collagen-positive (chondrogenic) cellular condensation remains devoid of perichondrium prior to birth. Thereafter, it converts into hyaline cartilage that extends along the proximal part of the aorticopulmonary septum and the pars fibrosa of the horizontal septum. Our findings are consistent with the assumption that, as in birds and mammals, the precursors of the cardiac chondrocytes in chelonians are neural crest-derived cells of nonmuscular nature. In addition, they point to the possibility that cells from the neural crest populate the embryonic pars fibrosa of the horizontal septum, thereby contributing to its alignment with the aorticopulmonary septum. In the present species, a second cartilaginous deposit of a hyaline nature extends along the sinus wall of the right semilunar valve of the right aorta, penetrating the fibrous cushion that constitutes the proximal support of the corresponding valve leaflet. This cartilage develops after birth, between the third and eighteenth month of life; its morphogenetic origin is unclear. The cartilaginous foci occurring in hearts of Spanish terrapin appear to act as pivots resisting mechanical tensions generated during the cardiac cycle. In the specimens examined there was no sign of replacement of the cardiac cartilages by bone tissue.