Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys: implications for osmoregulation in fresh and seawater

Abstract

Lampreys, one of the only two surviving groups of agnathan (jawless) vertebrates, contain several anadromous species that, during their life cycle, thus migrate from fresh to seawater and back to freshwater. Lampreys have independently evolved the same overall osmoregulatory mechanisms as the gnathostomatous (jawed) and distantly related teleost fishes. Lamprey gills thus likewise play a central role in taking up and secreting monovalent ions. However, the ultrastructural characteristics and distribution of their epithelial cell types [ammocoete mitochondria-rich (MR) cell, intercalated MR cell, chloride cell and pavement cell] differ in several respects from those of teleosts. The ultrastructural characteristics of these cells are distinctive and closely resemble those of certain ion-transporting epithelia in other vertebrates, for which the function has been determined. The data on each cell type, together with the stage in the life cycle at which it is found, i.e. whether in fresh or seawater, enable the following proposals to be made regarding the ways in which lampreys use their gill epithelial cells for osmoregulating in hypo- and hypertonic environments. In freshwater, the intercalated MR cell takes up Cl- and secretes H+, thereby facilitating the uptake of Na+ through pavement cells. In seawater, the chloride cell uses a secondarily active transcellular transport of Cl- to provide the driving force for the passive movement of Na+ through leaky paracellular pathways between these cells.