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

Abstract

Many hibernating animals thermoregulate during torpor and defend their body temperature (Tb) below 10°C by an increase in metabolic rate. Above a critical temperature (Tcrit) animals usually thermoconform. We investigated the physiological responses above and below Tcrit for a small tree dwelling bat (Chalinolobus gouldii, ∼14 g) that is often exposed to subzero temperatures during winter. Through simultaneous measurement of heart rate (HR) and oxygen consumption (V̇O2) 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 (Ta 5-20°C). Tcrit for this species was Ta 0.7±0.4°C, with a corresponding Tb of 1.8±1.2°C. Below Tcrit animals began to thermoregulate, indicated by a considerable but disproportionate increase in both HR and V̇O2. The maximum increase in HR was only 4-fold greater than the average thermoconforming minimum, compared to a 46-fold increase in V̇O2. The differential response of HR and V̇O2 to low Ta was reflected in a 15-fold increase in oxygen delivery per heart beat (cardiac oxygen pulse). During torpor at low Ta, thermoregulating bats maintained a relatively slow HR 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 HR in an unstudied physiological state that may occur frequently in the wild and can be extremely costly for heterothermic animals.