Dynamics and thermal sensitivity of ballistic and non-ballistic feeding in salamanders

Abstract

Low temperature reduces the performance of muscle-powered movements, but in movements powered by elastic recoil mechanisms, this effect can be mitigated and performance can be increased. To better understand the morphological basis of high performance and thermal robustness of elastically powered movements, we compared feeding dynamics at a range of temperatures (5-25°C) in two species of terrestrial plethodontid salamanders, Plethodon metcalfi and Ensatina eschscholtzii, which differ in tongue muscle architecture and the mechanism of tongue projection. We found that Ensatina is capable of ballistic projection with a mean muscle mass-specific power of 2100 W kg-1, revealing an elastic mechanism. Plethodon, in contrast, projected its tongue non-ballistically with a mean power of only 18 W kg-1, indicating it is muscle powered. Ensatina projected its tongue significantly farther than Plethodon and with dynamics that had significantly lower thermal sensitivity at temperatures below 15°C. These performance differences were correlated with morphological differences, namely elongated collagenous aponeuroses in the projector muscle of Ensatina as compared with Plethodon, which are likely the site of energy storage, and the absence in Ensatina of projector muscle fibers attaching to the tongue skeleton that allows projection to be truly ballistic. These findings demonstrate that, in these otherwise similar species, the presence in one species of elaborated connective tissue in series with myofibers confers not only 10-fold greater absolute performance but also greater thermal robustness of performance. We conclude that changes in muscle and connective tissue architecture are sufficient to alter significantly the mechanics, performance and thermal robustness of musculoskeletal systems.