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Calorespirometry reveals that goldfish prioritize aerobic metabolism over metabolic rate depression in all but near-anoxic environments

ABSTRACT Metabolic rate depression (MRD) has long been proposed as the key metabolic strategy of hypoxic survival, but surprisingly, the effects of changes in hypoxic O2 tensions (PwO2) on MRD are largely unexplored. We simultaneously measured the O2 consumption rate (ṀO2) and metabolic heat of goldfish using calorespirometry to test the hypothesis that MRD is employed at hypoxic PwO2 values and initiated just below Pcrit, the PwO2 below which ṀO2 is forced to progressively decline as the fish oxyconforms to decreasing PwO2. Specifically, we used closed-chamber and flow-through calorespirometry together with terminal sampling experiments to examine the effects of PwO2 and time on ṀO2, metabolic heat and anaerobic metabolism (lactate and ethanol production). The closed-chamber and flow-through experiments yielded slightly different results. Under closed-chamber conditions with a continually decreasing PwO2, goldfish showed a Pcrit of 3.0±0.3 kPa and metabolic heat production was only depressed at PwO2 between 0 and 0.67 kPa. Under flow-through conditions with PwO2 held at a variety of oxygen tensions for 1 and 4 h, goldfish also initiated MRD between 0 and 0.67 kPa but maintained ṀO2 to 0.67 kPa, indicating that Pcrit is at or below this PwO2. Anaerobic metabolism was strongly activated at PwO2 ≤1.3 kPa, but only used within the first hour at 1.3 and 0.67 kPa, as anaerobic end-products did not accumulate between 1 and 4 h exposure. Taken together, it appears that goldfish reserve MRD for near-anoxia, supporting routine metabolic rate at sub-Pcrit PwO2 values with the help of anaerobic glycolysis in the closed-chamber experiments, and aerobically after an initial (<1 h) activation of anaerobic metabolism in the flow-through experiments, even at 0.67 kPa PwO2. Summary: Although the goldfish's anoxia tolerance results from conserved energy via metabolic depression, its hypoxia tolerance results from exceptional O2 extraction abilities capable of supporting routine metabolic rate even in severe hypoxia.