Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at sub-zero temperatures

Abstract

<p>Many hibernating animals thermoregulate during torpor and defend their body temperature (T_b) near 0°C by an increase in metabolic rate. Above a critical temperature (T_crit), animals usually thermoconform. We investigated the physiological responses above and below T_crit for a small tree-dwelling bat (<i>Chalinolobus gouldii</i>, ∼14 g) that is often exposed to sub-zero temperatures during winter. Through simultaneous measurement of heart rate (f_H) and oxygen consumption (V̇_O₂), we show that the relationship between oxygen transport and cardiac function is substantially altered in thermoregulating torpid bats between 1 and -2°C, compared with thermoconforming torpid bats at mild ambient temperatures (T_a 5-20°C). T_crit for this species was at a T_a of 0.7±0.4°C, with a corresponding T_b of 1.8±1.2°C. Below T_crit, animals began to thermoregulate, as indicated by a considerable but disproportionate increase in both fH and V̇_O₂. The maximum increase in f_H was only 4-fold greater than the average thermoconforming minimum, compared with a 46-fold increase in V̇_O₂. The differential response of f_H and V̇_O₂ to low T_a was reflected in a 15-fold increase in oxygen delivery per heart beat (cardiac oxygen pulse). During torpor at low T_a, thermoregulating bats maintained a relatively slow f_H and compensated for increased metabolic demands by significantly increasing stroke volume and tissue oxygen extraction. Our study provides new information on the relationship between metabolism and f_H in an unstudied physiological state that may occur frequently in the wild and can be extremely costly for heterothermic animals.</p>