Bulbus arteriosus of the antarctic teleosts. I. The white-blooded Chionodraco hamatus.

The bulbus arteriosus of teleost fish is a thick-walled chamber that extends between the single ventricle and the ventral aorta. The functional importance of the bulbus resides in the fact that it maintains a steady blood flow into the gill system through heart contraction. Despite of this, a thorough study of the structure of the bulbus in teleost fish is still lacking. We have undertaken a morphologic study of the bulbus arteriosus in the stenothermal teleosts of the Antarctic sea. The structural organization of the bulbus arteriosus of the icefish Chionodraco hamatus has been studied here by conventional light, scanning, and transmission electron microscopy. The inner surface of the bulbus shows a festooned appearance due to the presence of longitudinal, unbranched ridges that extend between the ventricle and the arterial trunk. The wall of the bulbus is divided into endocardial, subendocardial, middle, and external layers. Endocardial cells show a large number of moderately-dense bodies. The endocardium invaginates into the subendocardium forming solid epithelial cords that contain numerous secretory vacuoles. Cells in the subendocardium group into small domains, have some of the morphological characteristics of smooth muscle cells, and appear enmeshed in a three-dimensional network of matrix filaments. Cells in the middle layer are typical smooth muscle cells. They appear arranged into layers and are surrounded by a filamentous meshwork that excludes collagen fibers. Orientation of this meshwork occurs in the vicinity of the smooth muscle cells. Elastin fibers are never observed. The external layer is formed by wavy collagen bundles and fibroblast-like cells. This layer lacks blood vessels and nerve fibers. The endocardium and the endocardium-derived cords are secretory epithelia that may be involved in the formation ofmucins or glycosaminoglycans. These mucins may have a protecting effect on the endocardium. The subendocardium and the middle layer appear to be formed by the same cell type, smooth muscle, with a gradient of differentiation from the secretory (subendocardium) to the contractile (middle layer) phenotype. Despite the absence of elastin fibers, the filamentous matrix could maintain the elastic properties of the bulbus wall. Smooth muscle cells appear to be actively involved in bulbus wall dynamics. The restriction of collagen to the external layer suggests that it may control wall dilatation and bulbus compliance. When comparison was possible, structural differences between C. hamatus and temperate teleosts seemed to be not species-related, but of phenotypic adaptative significance. This is remarkable since Antarctic fishes have lived isolated in freezing waters for the last two million years.