Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys

Abstract

SUMMARY 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.

Exposure of the gill epithelial cells of larval lampreys to an ion-deficient environment: a stereological study

“…Our results are consistent with the view that the IMRCs play a central role in the uptake of ions from the hypotonic riverine environment in which larval lampreys live [11]. This conclusion is also consistent with the recent demonstration that Vtype H + -ATPase and carbonic anhydrase are present in IMRCs [7].…”

“…A rectangular test field frame (23.15 × 15.25 cm), which defined the area to be analysed, was placed on the screen. The cells at the surface of the gill filaments and lamellae were identified as either an AMRC, IMRC or pavement cell using cytological criteria [11]. The number of each cell type within or cut by the upper or left side of the frame was recorded and expressed as a percentage of the total number of cells counted.…”

“…As in teleost fishes, the gills of lampreys are the main extrarenal organs of ionic regulation and osmoregulation [10,11]. The surfaces of the gill filaments and lamellae of ammocoetes comprise three types of epithelial cells, namely the pavement cells and two types of mitochondria-rich (MR) cells [12] (see Figs.…”

“…One of the MR cell types resembles, both ultrastructurally and through its possession of carbonic anhydrase and vacuolar (V)-type H + ATPase, the intercalated MR cell (IMRC) that is found in other ion-transporting epithelia, such as the toad and turtle urinary bladders, renal collecting duct and amphibian epidermis. In those ion-transporting epithelia, the IMRC actively secretes protons and plays a role in acidbase regulation and/or ion uptake [7,[11][12][13]. The other type of MR cell in the ammocoete gill, the mitochondria of which are characterized by a distinct electron-dense matrix, has no morphological counterpart in the ion-transporting epithelia of other vertebrates.…”

“…Such migrating lampreys possess only the IMRCs and pavement cells in their gill epithelium and yet osmoregulate effectively in fresh water [11,12]. It has thus been argued that, in upstream-migrating lampreys, the IMRC and/or pavement cell must be responsible for ion uptake and that, in larval lampreys, the AMRC may not be involved in taking up Na + and Cl − from the environment [11,12].…”