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The hypoxic metabolic response : how time and PO₂ shape the way fishes combine aerobic, anaerobic and depressed metabolism in hypoxic environments Regan, Matthew D.


Animals rely on O₂ to balance cellular ATP supply and demand. In O₂-limited hypoxic environments, survival depends on the maintenance of this balance and is accomplished through some combination of aerobic metabolism, anaerobic metabolism and metabolic rate depression (MRD). My thesis studied how fishes combine these three metabolic strategies as a total hypoxic metabolic response (HMR) to survive hypoxic environments that vary in O₂ level (PwO₂) and duration. Calorimetry is required to accurately measure the metabolic rates (MR) of hypoxia (or anoxia)-exposed fishes that are partially reliant on anaerobic glycolysis and/or MRD. Thus, I started by building a novel calorespirometer that simultaneously measures indices of aerobic metabolism, anaerobic metabolism and MRD, and used it for the remainder of my thesis projects. Using goldfish, I found that time influences how PwO₂ affects HMR. Under acute and continually decreasing PwO₂ conditions, goldfish maintained routine O₂ uptake rates (ṀO₂) to ~3.0 kPa PwO₂ (i.e., Pcrit), but sustained routine MR to 0.5 kPa by up-regulating anaerobic glycolysis. Under constant hypoxia (1 or 4 h) at a variety of PwO₂s, however, goldfish maintained routine ṀO₂ to ~0.7 kPa and consequently reduced their reliance on anaerobic glycolysis. I confirmed this rapidly enhanced O₂ uptake ability in subsequent experiments by using different rates of hypoxia induction (RHI) to vary the amount of time goldfish spent at hypoxic PwO₂s. Gradual RHIs yielded greater lamellar surface areas, haemoglobin-O₂ binding affinities, and subsequently, lower Pcrits than rapid RHIs. However, goldfish only induced MRD below 0.7 kPa. To test the idea that MRD is reserved for extreme hypoxia, I compared two threespine stickleback populations from two isolated lakes: one that experiences deep, long-term hypoxia due to winterfreeze (Alta Lake), and the other that does not (Trout Lake). The two populations did not differ in Pcrit or capacities for anaerobic metabolism, but Alta Lake sticklebacks, which were 2-fold more hypoxia-tolerant than Trout Lake sticklebacks, employed hypoxia-induced MRD while Trout Lake sticklebacks did not. My results reveal that the HMR varies with an animal’s biology and the abiotic aspects of its natural hypoxic environment in a way that may optimize hypoxic survival.

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