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Energetic aspects of osmoregulation in fish Morgan, John David

Abstract

The energetic aspects of osmoregulation in several species of fish were examined, using an experimental approach on both a whole-animal and tissue level. The first series of experiments examined the metabolic response of temperate and tropical fish species to acute and gradual salinity change, using whole-animal oxygen consumption rates and gill Na⁺,K⁺-ATPase activity as indicators of osmoregulatory energetics. Juvenile dolphin fish (Coryphaena hippurus) were exposed for 24 h to a reduced water salinity (34 to 20 ppt). They responded by decreasing oxygen consumption and gill Na⁺,K⁺-ATPase activity, suggesting a decrease in osmoregulatory costs. Mozambique tilapia (Oreochromis mossambicus) transferred from fresh water (FW) to seawater (SW), showed an elevation in plasma growth hormone levels, gill Na⁺,K⁺-ATPase activity, and a 20% increase in oxygen uptake after 4 d. No increases in these variables were seen in tilapia transferred from FW to isosmotic salinity (ISO). These results indicated that the physiological changes associated with SW entry represent a significant short-term cost, whereas ISO did not impose (or reduce) an energy demand in tilapia during the acclimation process. In a long-term study (6 wk), coho salmon (Oncorhynchus kisutch) smolts did not show any differences in metabolic rate between FW, ISO and SW, whereas gill Na⁺,K⁺-ATPase activity was lowest in ISO, higher in FW and highest in SW. In this case, there was no correlation between whole-animal oxygen consumption rates and the relative activity of ion transport enzymes in the gills. An acute (24 h) transfer of cutthroat trout (O. clarki clarki) from FW to SW resulted in a significant elevation of both oxygen uptake and plasma Cortisol levels. To further examine the influence of Cortisol on oxygen consumption and osmoregulatory variables, cutthroat trout parr were given Cortisol implants that elevated plasma Cortisol titres to a level similar to that found in fish following SW exposure. Cortisol significantly increased oxygen consumption rates and plasma glucose levels of trout in FW, consistent with its glucocorticoid role. This study suggests that some of the increases in oxygen consumption that occurred during the intitial stages of SW exposure may have been related to the metabolic effects of Cortisol, rather than the direct costs usually associated with osmoregulation. To separate the energy costs of NaCl transport from other whole-animal metabolic responses to salinity change, experiments were conducted using isolated preparations of osmoregulatory tissues. Oxygen consumption and Na⁺,K⁺-ATPase activity were measured in excised rectal gland and gill tissue of the spiny dogfish (Squalus acanthias), using ouabain to estimate the portion of tissue respiration required by the Na⁺/K⁺-pump. Ouabain-sensitive oxygen consumption of the rectal gland accounted for 55% of tissue respiration, compared to 22% for the gill. On a wholemass basis, the cost of NaCl secretion in the rectal gland was estimated to be 0.5% of whole animal oxygen uptake. A similar approach was used on excised gill tissue from FW-adapted cutthroat trout, to assess the oxygen cost of NaCl uptake in the FW trout gill. In that study, bafilomycin was also used to inhibit H⁺-pump activity in the gill tissue. A similar portion of gill tissue respiration was required by the Na⁺/K⁺-pump (18%) and H⁺-pump (19%), and the cost of NaCl uptake in the FW trout gill was estimated at 1.8% of resting metabolic rate. Finally, an isolated, perfused gill arch preparation was used to compare gill energetics in FW- and SWadapted cutthroat trout. The total gill oxygen consumption of FW gills was significantly (33%) higher than SW gills, and accounted for 3.9% and 2.4% of resting metabolic rate, respectively. The results of those experiments indicate that the energy demands of ion transport in osmoregulatory organs, such as the rectal gland and gill, represent a relatively small portion of the total energy budget in fish.

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