Thermal effects on motor control andin vitromuscle dynamics of the ballistic tongue apparatus in chameleons

Abstract

SUMMARYTemperature 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.

Impacts of temperature on performance in two species of South African dwarf chameleons,Bradypodion pumilumandB. occidentale

“…The maximal summer temperature predicted (32.5°C) 3834 speed-related traits are highly temperature dependent whereas forcerelated traits are less dependent on temperature. These different performance trait profiles are consistent with studies on the influence of temperature on muscle function (Bennett, 1980;Bergh and Ekblom, 1979;Binkhorst et al, 1977;Petrofsky et al, 1981;Anderson and Deban, 2012) and whole-organism performance (Herrel et al, 2007;Anderson and Deban, 2010). Furthermore, most of the differences found in the comparison of force-related traits involved temperatures under 25°C, whereas temperature independence of force generation by muscle is known to range from 25 to 40°C (Bergh and Ekblom, 1979;Binkhorst et al, 1977;Petrofsky et al, 1981).…”

Thermal effects on the performance, motor control, and muscle dynamics of ballistic feeding in the salamanderEurycea guttolineata

“…In these salamanders, as well as in E. guttolineata, the tongue is typically projected at performance levels that exceed the greatest maximum instantaneous power output of vertebrate muscle (Deban et al, 2007), implicating power amplification via elastic energy storage. These patterns are similar to tongue projection in chameleons (Wainwright and Bennett, 1992a;de Groot and van Leeuwen, 2004;Anderson and Deban, 2010;Anderson and Deban, 2012) and toads (Nishikawa, 2000;Lappin et al, 2006;Deban and Lappin, 2011), which, despite profound differences in morphology, also project their tongues with extreme performance and with activation of their projector muscles in advance of tongue projection.…”

“…This pattern has been shown to be the result not of any compensatory activation of muscle at low temperature in chameleons and toads (Deban and Lappin, 2011;Anderson and Deban, 2012), nor of any unusually reduced effect of temperature on typical muscle contractile physiology in chameleons (Anderson and Deban, 2012). Instead, the specialized morphology and motor control patterns of these elastic recoil-powered tongue-projection mechanisms capitalize on the weak effect of temperature on muscle contractile force (Bennett, 1984;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013) and the thermal independence of the mechanical properties of elastic tissues (Rigby et al, 1959;Alexander, 1966;Denny and Miller, 2006) to impart thermal robustness to these ballistic movements. Movements such as tongue retraction that are powered directly by muscle contraction, in contrast, suffer typical thermal effects resulting from the strong effect of temperature on muscle contractile dynamics, and thus slow significantly with decreasing temperature (Bennett, 1985;Rome, 1990;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013).…”

“…Ballistic tongue-projection performance in chameleons, salamanders, toads and frogs, for instance, exhibits significantly lower thermal dependence than the performance of tongue retraction (Anderson and Deban, 2010;Deban and Lappin, 2011;Deban and Richardson, 2011;Sandusky and Deban, 2012). This pattern has been shown to be the result not of any compensatory activation of muscle at low temperature in chameleons and toads (Deban and Lappin, 2011;Anderson and Deban, 2012), nor of any unusually reduced effect of temperature on typical muscle contractile physiology in chameleons (Anderson and Deban, 2012). Instead, the specialized morphology and motor control patterns of these elastic recoil-powered tongue-projection mechanisms capitalize on the weak effect of temperature on muscle contractile force (Bennett, 1984;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013) and the thermal independence of the mechanical properties of elastic tissues (Rigby et al, 1959;Alexander, 1966;Denny and Miller, 2006) to impart thermal robustness to these ballistic movements.…”

“…Instead, the specialized morphology and motor control patterns of these elastic recoil-powered tongue-projection mechanisms capitalize on the weak effect of temperature on muscle contractile force (Bennett, 1984;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013) and the thermal independence of the mechanical properties of elastic tissues (Rigby et al, 1959;Alexander, 1966;Denny and Miller, 2006) to impart thermal robustness to these ballistic movements. Movements such as tongue retraction that are powered directly by muscle contraction, in contrast, suffer typical thermal effects resulting from the strong effect of temperature on muscle contractile dynamics, and thus slow significantly with decreasing temperature (Bennett, 1985;Rome, 1990;Herrel et al, 2007;Anderson and Deban, 2012;James, 2013). Thermal robustness of independently evolved ballistic movements powered by elastic recoil is well established; however, our understanding of the extent to which these mechanisms have converged on similar modifications to motor patterns, muscle contractile physiology or morphology to overcome strong thermal effects on muscle-powered movements remains limited.…”