Abstract
Temperature strongly affects whole-organism performance through its effect on muscle contractile rate properties, but movements powered by elastic recoil are liberated from much of the performance decline experienced by muscle-powered movements at low temperature. We examined the motor control and muscle contractile physiology underlying an elastically powered movement - tongue projection in chameleons - and the associated muscle powered retraction to test the premise that the thermal dependence of muscle contractile dynamics is conserved. We further tested the associated hypothesis that motor control patterns and muscle contractile dynamics must change as body temperature varies, despite the thermal robustness of tongue-projection performance. We found that, over 14-26°C, the latency between the onset of the tongue projector muscle activity and tongue projection was significantly affected by temperature (Q(10) of 2.56), as were dynamic contractile properties of the tongue projector and retractor muscles (Q(10) of 1.48-5.72), supporting our hypothesis that contractile rates slow with decreasing temperature and, as a result, activity durations of the projector muscle increase at low temperatures. Over 24-36°C, thermal effects on motor control and muscle contractile properties declined, indicating that temperature effects are more extreme across lower temperature ranges. Over the entire 14-36°C range, intensity of muscle activity for the tongue muscles was not affected by temperature, indicating that recruitment of motor units in neither muscle increases with decreasing temperature to compensate for declining contractile rates. These results reveal that specializations in morphology and motor control, not muscle contractile physiology, are responsible for the thermal robustness of tongue projection in chameleons.
Highlights
The effect of temperature on diverse physiological and biochemical processes is a significant challenge to organisms living in variable environments
Six feedings at 15±1°C, 10 feedings at 25±1°C, and five feedings at 35±1°C were collected for the m. accelerator linguae
The performance of ballistic tongue projection in C. calyptratus exhibits significantly lower thermal dependence than tongue retraction (Anderson and Deban, 2010). This differential thermal response was proposed to be the result of the difference between the mechanism of tongue projection, which is powered by recoil of preloaded elastic elements, and that of tongue retraction, which is powered by muscle contraction alone (Wainwright and Bennett, 1992a; Herrel et al, 2001b)
Summary
The effect of temperature on diverse physiological and biochemical processes is a significant challenge to organisms living in variable environments. Ectothermic animals are vulnerable because environmental conditions directly affect their body temperature, and physiological rate processes. The decline of these rates, including muscle contractile velocity, with body temperature can affect whole-organism performance and, in the process, limit an organism’s ability to perform critical behaviors, such as predator avoidance and feeding (Huey and Stevenson, 1979; Bennett, 1985; Huey and Bennett, 1987; Rome, 1990; Lutz and Rome, 1996; Herrel et al, 2007). We examine the motor control and muscle contractile physiology underlying an elastically powered movement, tongue projection in chameleons, to better understand the thermal robustness of this integrated system
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