Respiratory, metabolic, and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs

Abstract

Aerobic metabolic rates (M˙o 2) and respiratory quotients (RQ = CO2production/M˙o 2) were measured contemporaneously in hibernating frogs Rana temporaria (L.), submerged for 90 days at 3°C. After 3 mo of submergence in fully aerated water,M˙o 2levels were 61% of those seen at the same temperature before hibernation. Over the first 40 days of hibernation, RQ values (≤0.82) favored a lipid-based metabolism that progressively shifted to an exclusively carbohydrate metabolism (RQ = 1.01) by 90 days of hibernation. Liver glycogen concentrations fell by 68% during the first 8 wk of submergence, thereafter exhibiting a less rapid rate of utilization. Conversely, muscle glycogen concentrations remained stable over the first 2 mo of the experiment before falling by 33% over the course of the remaining 2 mo, indicating that the frog was recruiting muscle glycogen reserves to fuel metabolism. Submerged frogs exhibited an extracellular acidosis during the first week of submergence, but over the course of the next 15 wk “extracellular pH” values were not significantly different from the values obtained from the control air-breathing animals. The initial extracellular acidosis was not mirrored in the intracellular compartment, and the acid-base state was not significantly different from the control values for the first 8 wk. However, over the subsequent 8- to 16-wk period, the acid-base status shifted to a lower intracellular pH-[Formula: see text] concentration set point, indicative of a metabolic acidosis. Even so, there was no indication that the acidosis could be attributed to anaerobic metabolism, as both plasma and muscle lactate levels remained low and stable. Muscle adenylate energy charge and lactate-to-pyruvate and creatine-to-phosphocreatine ratios also remained unchanged throughout hibernation. The capacity for profound metabolic rate suppression together with the ability to match substrate use to shifts in aerobic metabolic demands and the ability to fix new acid-base homeostatic set points are highly adaptive, both in terms of survival and reproductive success, to an animal that is often forced to overwinter under the cover of ice.