Structure and function in the excretory system of archaeogastropods and their significance in the evolution of gastropods

Abstract

Three species of archaeogastropod mollusc, Monodonta lineata (da Costa), Emarginula reticulata Sowerby and Patella vulgata L. were selected as representative members of the Trochacea, Fissurellacea and Patellacea, respectively, for a comparative anatomical and ultrastructural study of the excretory system. Primary urine formation takes place by filtration of blood through the walls of the paired auricles in Monodonta and Emarginula and of the single auricle and ventricle in Patella . Urine then passes to right and left kidneys along the renopericardial canals. Contrary to earlier reports the two kidneys are different in structure and function in all three species, the larger right kidney retaining the primitive function of nitrogenous excretion, the left having a predominantly resorptive role and with a capacity to abstract from the blood solutes of larger molecular mass. The difference in the size of the two kidneys is exaggerated in Patella and Emarginula as a consequence of partial restoration of bilateral symmetry in these limpets. It has been possible to demonstrate at the ultrastructural level that the minute left kidney of Emarginula is functional. The vacuolated epithelial cells of the right kidney contain layered excretory spherules composed of purines, melanin and ferric iron in different proportions in the three genera. There is close similarity in the ultrastructural organization of these cells in Monodonta and Emarginula , but those of Patella show marked differences and their excretory spherules contain a higher proportion of melanin. The position of the left kidney in the mantle skirt, as exemplified by Monodonta , is believed to have arisen in the earliest gastropods correlated with the development of helical coiling. This was accompanied by a change in its blood vessels. It has lost its afferent renal vein, which primitively would have carried deoxygenated blood from the viscera, an arrangement which persists in the right kidney. The left efferent renal vein is reduced in Monodonta and lost in Patella and Emarginula . A new vessel has arisen linking left auricle and left kidney and there is evidence to suggest that it carries post-branchial oxygenated blood. It is believed to serve as both an afferent and major efferent route. The physiological implications of this change in the blood supply are discussed and held to be responsible for the functional differences between the two kidneys, creating conditions in the left which favour resorption of organic solutes and ions, and leaving the right kidney with the primary role of nitrogenous excretion. The evolution of the nephridial gland is examined in this context and is also believed to be correlated with the change in the blood supply to the left kidney. Ultrastructural evidence is given in support of its suggested resorptive function. The significance of the differences between right and left kidneys of archaeogastropods is discussed in relation to the evolution of the monotocardian excretory system, and the possible phylogenetic relationships of the groups of archaeogastropods are considered.