Na +-K +-adenosine triphosphatase activities in gills of marine teleost fishes: changes with depth, size and locomotory activity level

Activities of the primary enzyme responsible for monovalent ion regulation, Na÷-K+-adenosine triphosphatase (Na+-K+-ATPase), were measured in gills of marine teleost fishes with different depths of occurrence (0 to 4 800 m), body weights (a range of five orders of magnitude), and locomotory capacities. Specimens were collected off the coasts of California and Oregon in 1983-1989, and at the Galfipagos Spreading Center and 13 °N East Pacific Rise hydrothermal vent sites in 1987 and 1988, respectively. Except for two hydrothermal vent fishes, deep-sea species had much lower Na ÷K ÷-ATPase activities g 1 gill filament than shallow-living species, indicating that osmoregulatory costs, like total metabolic rate, are greatly reduced in most deep-living fishes. Within a species, the total branchial Na ÷-K ÷-ATPase activity per individual was dependent on size; the average allometric scaling exponent was 0.83. Using published values for oxygen consumption rates, and the total branchial Na÷-K+-ATPase activities as an index of osmoregulatory costs, we estimated the maximal cost (as percent of ATP turnover) for osmoregulation in ten teleosts. Osmoregulatory costs averaged about 10% of total ATP turnover among these species, and maximal costs were no greater than about 20%. The percent costs of osmoregulation did not differ between shallowand deep-living fishes. The reduced total ATP expenditure for osmoregulation in deep-living fishes is proposed to result from the sluggish locomotory habits of these fishes, not from selection for reduced osmotic coastper se. Thus, the reduced swimming abilities of these fishes lead to lower rates of water flow over the gills and less blood flow through the gills due to reduced demands for oxygen. Consequently, passive flux of water and ions through the gills is much lower than in more active fishes, and osmotic costs are thereby minimized. The relatively high activities of Na +-K ÷-ATPase in gills of the two hydrothermal vent fishes suggest that these fishes may be more active and have higher metabolic rates than other deep-sea fishes. * Present address: Department of Zoology, Storer Hall, University of California at Davis, California 95616, USA Introduction Total numbers, biomass, caloric contents, enzymatic activities, and metabolic rates of fishes decrease rapidly with depth in the marine water column (reviewed in Siebenaller and Somero 1989). Metabolic rates of deepsea fishes may be over an order of magnitude lower than those of similar-sized shallow-living, cold-adapted fishes (Smith and Hessler 1974, Smith 1978, Torres et al. 1979, Torres and Somero 1988a, b). These depth-related decreases in metabolic rate are not due solely to decreases in temperature with depth, because similar depth-related decreases in metabolic rates have been found in isothermal (Antarctic) and thermally-stratified (Southern California) water columns (Torres and Somero 1988 a). Instead, these decreases are thought to result largely from significant reductions in locomotory energy expenditure in deep-living fishes, which typically have very low capacities for high-speed swimming, relative to shallow-living fishes (Childress and Somero 1979, Sullivan and Somero 1980, Siebenaller et al. 1982, Torres and Somero 1988 a). Although locomotory activity may account for the largest single share of ATP turnover in fishes, osmoregulation also represents a significant fraction of total metabolism. Rao (1968) and Febry and Lutz (1987) estimated that as much as one-fourth of metabolism may be expended in osmoregulation. Thus, the 10to 100-fold reduction in metabolic rate in deep-sea fishes implies that the amount of energy devoted to osmoregulation in these species must be greatly reduced. Deep-sea fishes maintain intracellular and plasma ionic compositions similar to those of shallow-living fishes (Blaxter et al. 1971, Shelton et al. 1985), suggesting that reduction in osmoregulatory energy costs via reduction of osmotic gradients has not occurred in deep-sea fishes. One might predict that osmoregulatory costs would be correlated with the locomotory habits of a fish. Reduced locomotory activities of sluggish fishes like most deep-sea species lead to reduced water flow over the gills and reduced perfusion of the gill tamellae, due to reduced demands for oxygen. Thus, in sluggish species, passive