Warm bodies, cool wings: regional heterothermy in flying bats

Abstract

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.

Thermal robustness of biomechanical processes

“…For example, circulatory heat exchangers keep blood temperature low in extremities to avoid heat loss to the environment and reduce the metabolic costs of maintaining core body temperature (Midtgard, 1981;Scholander and Schevill, 1955). The extremities of some endotherms match environmental temperature despite a relatively constant core body temperature (Irving and Krog, 1955;Midtgard, 1981;Rummel et al, 2019;Scholander and Krog, 1957;Scholander and Schevill, 1955). Because these extremities are often the structures interacting with the environment to produce motion, thermally robust mechanisms may be ecologically important even in large endotherms.…”

A proximal–distal difference in bat wing muscle thermal sensitivity parallels a difference in operating temperatures along the wing

“…The Q 10 s were generally higher in the pectoralis at every temperature than in either distal muscle, (figures 2 and 3, insets). This difference in muscle temperature sensitivity mirrors the gradient in temperature of these muscles during flight [5]. Although temperatures of the muscles of the handwing have yet to be recorded, they are both smaller and more distal than the ECRL, which suggests that they are likely colder during flight than more proximal muscles.…”

“…We hypothesized that the proximal-distal gradient in operating temperature of the wing muscles [5] would correspond with proximal-distal differences in muscle temperature sensitivity, predicting that the warm pectoralis muscle would be more temperature sensitive than the distal muscles, which cool during flight. We found a clear proximal-distal trend in the temperature dependence of the contractile properties of the wing muscles in C. perspicillata, supporting our hypothesis.…”

“…Their wings exhibit a proximal-to-distal temperature gradient during rest and activity. Continuous measurements of internal muscle temperature during wind tunnel flights indicate that the distal wing muscles of Carollia perspicillata operate at up to 12°C below core body temperature (T b ), while the more proximal pectoralis muscle remains near T b during flight [5]. As nocturnal fliers, bats must maintain a high wingbeat frequency in the face of thermal conditions that likely result in net heat loss from their poorly insulated wings.…”

“…We hypothesized that the proximal-distal gradient in operating temperature of the wing muscles [5] would correspond with proximal-distal differences in muscle temperature sensitivity, predicting that the warm pectoralis muscle would be highly temperature sensitive, and that the cooler distal muscles would be less temperature sensitive. We previously reported that a forearm muscle, the extensor carpi radialis longus (hereafter ECRL), in C. perspicillata, a small neotropical fruit bat, has lower temperature dependence than expected based on values from other mammalian skeletal muscle [6].…”