Temperature affects contractile rate properties in muscle, which may affect locomotor performance. Endotherms are known to maintain high core body temperatures, but temperatures in the periphery of the body can fluctuate. Such a phenomenon occurs in bats, whose wing musculature is relatively poorly insulated, resulting in substantially depressed temperatures in the distal wing. We examined a wing muscle in the small-bodied tropical bat and a hindlimb muscle in the laboratory mouse at 5°C intervals from 22 to 42°C to determine the thermal dependence of the contractile properties of both muscles. We found that the bat extensor carpi radialis longus had low thermal dependence from near body temperature to 10°C lower, with values of less than 1.5 for relaxation from contraction and shortening velocities in that interval, and with no significant difference in some rate properties in the interval between 32 and 37°C. In contrast, for all temperature intervals below 37°C, values for the mouse extensor digitorum longus were 1.5 or higher, and rate properties differed significantly across successive temperature intervals from 37 to 22°C. An ANCOVA analysis found that the thermal dependencies of all measured isometric and isotonic rate processes were significantly different between the bat and mouse muscles. The relatively low thermal dependence of the bat muscle likely represents a downward shift of its optimal temperature and may be functionally significant in light of the variable operating temperatures of bat wing muscles.
Many endothermic animals experience variable limb temperatures, even as they tightly regulate core temperature. The limbs are often cooler than the core at rest, but because the large locomotor muscles of the limbs produce heat during exercise, they are thought to operate at or above core temperature during activity. Bats, small-bodied flying mammals with greatly elongated forelimbs, possess wings with large surfaces lacking any insulating fur. We hypothesized that during flight the relatively small muscles that move the elbow and wrist operate below core body temperature because of elevated heat loss. We measured muscle temperature continuously in the small fruit bat Carollia perspicillata before and during wind tunnel flights, and discretely in diverse bats at rest in Belize. We found that bats maintained high rectal temperatures, but that there was a steep proximal-to-distal gradient in wing muscle temperature. Forearm muscles were 4–6°C cooler than rectal temperature at rest and approximately 12°C cooler during flights at an air temperature of 22°C. These findings invite further study into how bats and other endotherms maintain locomotor performance in variable environments, when some muscles may be operating at low temperatures that are expected to slow contractile properties.
Flight is a demanding form of locomotion, requiring fast activation and relaxation in wing muscles to produce the necessary wingbeat frequencies. Bats maintain high body temperatures during flight, but their wing muscles cool under typical environmental conditions. Because distal wing muscles are colder during flight than proximal muscles, we hypothesized that they would be less temperature sensitive to compensate for temperature effects, resulting in proximal–distal differences in temperature sensitivity that match differences in muscle operating temperature. We measured contractile rates across temperatures in the proximal pectoralis muscle and an interosseous in the handwing of Carollia perspicillata , a small neotropical fruit bat, and compared their thermal dependence with that of a forearm muscle measured in a previous study. We found that the contractile properties of the pectoralis were significantly more temperature sensitive than those of the distal muscles. This suggests that cooling of the distal wing muscles imposes a selective pressure on muscle contractile function which has led to shifts in temperature sensitivity. This study is the first to demonstrate differences in temperature sensitivity along the length of a single limb in an endotherm and suggests that temperature variation may be underappreciated as a determinant of locomotor performance in endotherms generally.
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