Environmental temperature impacts the physical activity and ecology of ectothermic animals through its effects on muscle contractile physiology. Sprinting, swimming, and jumping performance of ectotherms decreases by at least 33% over a 10°C drop, accompanied by a similar decline in muscle power. We propose that ballistic movements that are powered by recoil of elastic tissues are less thermally dependent than movements that rely on direct muscular power. We found that an elastically powered movement, ballistic tongue projection in chameleons, maintains high performance over a 20°C range. Peak velocity and power decline by only 10%-19% with a 10°C drop, compared to >42% for nonelastic, muscle-powered tongue retraction. These results indicate that the elastic recoil mechanism circumvents the constraints that low temperature imposes on muscle rate properties and thereby reduces the thermal dependence of tongue projection. We propose that organisms that use elastic recoil mechanisms for ecologically important movements such as feeding and locomotion may benefit from an expanded thermal niche.biomechanics | muscle physiology | elastic storage | thermal ecology | Chamaeleonidae T emperature influences diverse physiological processes, including metabolic rate, muscle dynamics, and nerve conduction velocity, which in turn can affect whole-organism performance. Ectothermic animals are particularly vulnerable to the effects of low ambient temperatures, because their body temperature (T b ) is dictated by environmental conditions. The effect of T b on muscle physiology has a clear impact on an organism's ability to move, escape predators, and engage in foraging behavior (1-6); for example, a 10°C drop in T b reduces sprint speed in lizards, swimming speed in fish, and jumping distance in frogs by at least 33% (2, 5). We find that, unlike these other dynamic movements, ballistic tongue projection in chameleons maintains extremely high performance over a T b range of 20°C.The mechanism of chameleon prey capture is unique among lizards, relying on ballistic projection of the tongue up to twice the length of the body in as little as 0.07 second (7,8). This feeding mechanism is common to all chameleons and gives these slow, cryptic, sit-and-wait predators the element of surprise. Chameleons feed over a wider range of T b than other lizards, using ballistic tongue projection in habitats ranging from deserts, where T b exceeds 39°C (9), to alpine zones above 3,500 m with temperatures below freezing (10). Some chameleon species feed at a T b of 3.5°C (9), exploiting an early morning peak in alpine insect activity (10) before sympatric lizard species become active (11). This ability to feed at low T b has not been explained; we propose that the elastic-recoil mechanism of tongue projection confers this temperature insensitivity.Ballistic tongue projection in chameleons achieves its extreme performance by rapid elastic recoil of collagen tissue within the tongue-tissue that is first stretched by slow contraction of the tongue accel...
Temperature strongly affects muscle contractile rate properties and thus may influence whole-organism performance. Movements powered by elastic recoil, however, are known to be more thermally robust than muscle-powered movements. We examined the wholeorganism performance, motor control and muscle contractile physiology underlying feeding in the salamander Eurycea guttolineata. We compared elastically powered tongue projection with the associated muscle-powered retraction to determine the thermal robustness of each of these functional levels. We found that tongueprojection distance in E. guttolineata was unaffected by temperature across the entire 4-26°C range, tongue-projection dynamics were significantly affected by temperature across only the 4-11°C interval, and tongue retraction was affected to a higher degree across the entire temperature range. The significant effect of temperature on projection dynamics across the 4-11°C interval corresponds to a significant decline in projector muscle burst intensity and peak contractile force of the projector muscle across the same interval. Across the remaining temperature range, however, projection dynamics were unaffected by temperature, with muscle contractile physiology showing typical thermal effects and motor patterns showing increased activity durations and latencies. These results reveal that elastically powered tongue-projection performance in E. guttolineata is maintained to a higher degree than muscle-powered tongue retraction performance across a wide temperature range. These results further indicate that thermal robustness of the elastically powered movement is dependent on motor control and muscle physiology that results in comparable energy being stored in elastic tissues across a range of temperatures.
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.
Vertebrate model organisms have facilitated the discovery and exploration of morphogenetic events and developmental pathways that underpin normal and pathological embryological events. In contrast to amniotes such as Mus musculus (Mammalia) and Gallus gallus (Aves), our understanding of early patterning and developmental events in reptiles (particularly nonavians) remains weak. Squamate reptiles (lizards, snakes, and amphisbaenians) comprise approximately one-third of all living amniotes. But studies of early squamate development have been limited because, in most members of this lineage, embryo development at the time of oviposition is very advanced (limb bud stages and older). In many cases, squamates give birth to fully developed offspring. However, in the veiled chameleon (Chamaeleo calyptratus), embryos have progressed only to a primitive pregastrula stage at the time of oviposition. Furthermore, the body plan of the veiled chameleon is highly specialized for climbing in an arboreal environment. It possesses an entire suite of skeletal and soft anatomical modifications, including cranioskeletal ornamentation, lingual anatomy and biomechanics for projection, autopodial clefting for grasping, adaptations for rapid integumental color changes, a prehensile tail with a lack of caudal autotomy, the loss of the tympanum in the middle ear, and the acquisition of turreted eyes. Thus, C. calyptratus is an important model organism for studying the role of ecological niche specialization, as well as genetic and morphological evolution within an adaptive framework. More importantly, this species is easily bred in captivity, with only a small colony (<10 individuals) needed to obtain hundreds of embryos every year.
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