The effects of thermally induced gill remodeling on ionocyte distribution and branchial chloride fluxes in goldfish (Carassius auratus)

Abstract

Experiments were performed to evaluate the effects of temperature-induced changes in functional gill lamellar surface area on the distribution of ionocytes and branchial chloride fluxes in goldfish (Carassius auratus). In fish acclimated to warm water (25 degrees C), the ionocytes were scattered along the lamellae and within the interlamellar regions of the filament. In cold water (7 degrees C), the ionocytes were largely absent from the lamellae and filaments but instead were mostly confined to the outer regions of an interlamellar cell mass (ILCM) that formed within the interlamellar channels. Using a ;time-differential double fluorescent staining' technique, it was determined that in fish transferred from 25 degrees to 7 degrees C, the ionocytes on the outer edge of (and within) the ILCM originated predominantly from the migration of pre-existing ionocytes and to a lesser extent from the differentiation of progenitor cells. Despite the greater functional lamellar surface area in the warm-water-acclimated fish, there was no associated statistically significant increase in passive branchial Cl(-) efflux. Because the paracellular efflux of polyethylene glycol was increased 2.5-fold at the warmer temperature, it would suggest that goldfish specifically regulate (minimize) Cl(-) loss that otherwise would accompany the increasing functional lamellar surface area. In contrast to predictions, the numbers and sizes of individual ionocytes was inversely related to functional lamellar surface area resulting in a markedly greater ionocyte surface area in fish acclimated to cold water (5219+/-438 compared with 2103+/-180 microm(2) mm(-1) of filament). Paradoxically, the activity of Na(+)/K(+)-ATPase (as measured at room temperature) also was lower in the cold-water fish (0.43+/-0.06 compared with 1.28+/-0.15 micromol mg(-1) protein h(-1)) despite the greater numbers of ionocytes. There were no statistically significant differences in the rates of Cl(-) uptake in the two groups of fish despite the differences in ionocyte abundance. It is possible that to maintain normal rates of Cl(-) uptake, a greater ionocyte surface area is required in the cold-water fish that possess an ILCM because of the unfavorable positioning of the ionocytes on and within the ILCM, a structure lacking any obvious blood supply.