Muscle-powered movements are limited by the contractile properties of muscles and are sensitive to temperature changes. Elastic-recoil mechanisms can both increase performance and mitigate the effects of temperature on performance. Here, we compare feeding movements in two species of plethodontid salamanders, Bolitoglossa franklini and Desmognathus quadramaculatus, across a range of body temperatures (5-25°C) to better understand the mechanism of elastically powered, thermally robust movements. Bolitoglossa exhibited ballistic, elastically powered tongue projection with a maximum muscle mass specific power of 4,642 W kg(-1) while Desmognathus demonstrated nonballistic, muscle-powered tongue projection with a maximum power of 359 W kg(-1) . Tongue-projection performance in Bolitoglossa was more thermally robust than that of Desmognathus, especially below 15°C. The improved performance and thermal robustness of Bolitoglossa was associated with morphological changes in the projector muscle, including elaborated collagen aponeuroses and the absence of myofibers attaching directly to the tongue skeleton. The elongated aponeuroses likely increase the capacity for elastic energy storage, and the lack of myofibers inserting on the tongue skeleton permits ballistic projection. These results suggest that relatively simple changes in myofiber architecture and the amount of connective tissue can improve the performance and functional robustness of movements in the face of environmental challenges such as variable temperature.
Salamanders use the hyobranchial apparatus and its associated musculature for tongue projection on land and for suction feeding in water. Hyobranchial apparatus composition and morphology vary across species, and different morphologies are better suited for feeding in aquatic versus terrestrial environments. We hypothesize that differences in hyobranchial morphology result in functional trade-offs in feeding performance. We predict that semi-aquatic and aquatic salamandrids with hyobranchial morphology suited for aquatic feeding will have lower performance, in terms of tongue-projection distance, velocity, acceleration and power, compared with terrestrial salamandrids when feeding in a terrestrial environment. We found that semi-aquatic and aquatic newts had lower velocity, acceleration and muscle-mass-specific power of tongue projection when compared with the terrestrial salamanders and The fully aquatic newt, , has a robust, heavily mineralized hyobranchial apparatus and was unable to project its tongue during terrestrial feeding, and instead exhibited suction-feeding movements better suited for aquatic feeding. Conversely, terrestrial species have slender, cartilaginous hyobranchial apparatus and enlarged tongue pads that coincided with greater tongue-projection distance, velocity, acceleration and power. exhibited extreme tongue-projection performance, similar to that seen in elastically projecting plethodontid salamanders; muscle-mass-specific power of tongue projection exceeded 2200 W kg, more than 350 times that of the next highest performer, , which reached 6.3 W kg These findings reveal that two fully terrestrial salamandrids have morphological specializations that yield greater tongue-projection performance compared with species that naturally feed in both aquatic and terrestrial environments.
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