Graduation Year

2013

Document Type

Dissertation

Degree

Ph.D.

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Stephen M. Deban

Keywords

Chamaeleonidae, Contractile Properties, Electromyography, Feeding, Temperature Effects

Abstract

Environmental temperature exhibits profound effects on the activity and ecology of ectotherms through its impact on muscle contractile physiology. While the performance of locomotor behaviors powered by muscle contraction directly decreases by at least 33% over a 10°C drop in body temperature, chameleons are known to feed, presumably with high performance, at body temperatures where sympatric lizard species remain inactive. I propose that ballistic movements that are powered by the recoil of preloaded elastic and collagenous tissues are less thermally dependent than movements that rely on direct muscular power. Despite the reduced thermal sensitivity of the elastic-recoil powered movement, I propose that the muscles associated with preloading these elastic tissues are themselves thermally sensitive and at low temperature, will take longer to load the elastic tissues. Finally, I expect that because of the different effect of temperature on elastic-recoil-powered and muscle-powered movements, performance declines for elastic-recoil-powered tongue projection at low temperature will not vary between species along an environmental temperature gradient (i.e., thermal effects will be the same for all species). Conversely, performance declines for muscle powered tongue retraction at low temperature will be lower in species from colder environments along an environmental temperature gradient. To test these predictions, I used high-speed videography, electromyography and in vitro muscle contractile experiment techniques in conjunction with temperature manipulations to test the mechanistic principles in Chamaeleo calyptratus. I then used high-speed videography at different temperatures in three Bradypodion species from different habitats in South Africa to compare thermal effects on elastic-recoil and muscle-powered movements in different species. I found that the elastic-recoil mechanism of tongue projection in chameleons circumvents the constraints that low temperature imposes on muscle rate properties, thereby reducing the thermal dependence of tongue projection. In all species examined, tongue projection was relatively thermally robust, maintaining a high degree of maximal performance at temperatures as low as 15°C. In contrast, the associated muscle-powered tongue retraction was strongly effected by temperature and experienced substantial performance declines over the same temperature range. While tongue projection performance was itself thermally robust, muscle contractile dynamics of the tongue projector muscle, which preloads the elastic elements responsible for powering projection, was strongly affected by temperature. Similarly, at cooler temperatures the tongue projector muscle became active earlier relative to the onset of tongue projection, due to the reduced rate of tension buildup and the resulting increase in time required to load the elastic elements of the tongue with the required force to subsequently power tongue projection. Further, the effect of temperature on both tongue projection performance and tongue retraction performance was found to vary between species living in different thermal environments. This suggests that despite differences in how temperature affects the performance of these different movement types, both elastic-recoil-powered movements and muscle-powered movements may experience selective pressure to optimize their performance to their environments. Based on these findings, I suggest that the relative thermal independence of tongue projection in chameleons is a more general characteristic of elastic-recoil-powered mechanisms and organisms that use elastic recoil mechanisms for ecologically important movements, such as feeding and locomotion, may benefit from an expanded thermal niche. Further, given the prevalence of elastic power-amplification mechanisms in ectotherms, the benefit of reduced thermal sensitivity may promote the evolution of these mechanisms in other ectothermic animals. Finally, I propose that temperature manipulations may be a useful methodological approach to testing for the presence or prevalence of elastic recoil in powering other biomechanical systems. While these studies examined thermal effects on ballistic tongue projection and tongue retraction in chameleons at difference mechanistic levels and within the framework of how these thermal relationships may be affected by their local environment, many of the results apply more broadly to similar systems in other ectotherms. Comparison of these findings to similar elastically powered systems may help solidify the generality of these findings among other taxa.

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