Thermal sensitivity of motor control of muscle-powered versus elastically powered tongue projection in salamanders

Abstract

Elastic-recoil mechanisms can improve organismal performance and circumvent the thermal limitations of muscle contraction, yet they require the appropriate motor control to operate. We compare muscle activity during tongue projection in salamanders with elastically powered, ballistic projection with activity of those with muscle-powered, non-ballistic projection across a range of temperatures to understand how motor control is integrated with elastically powered movements, and how this integration contributes to reduced thermal sensitivity. Species with ballistic tongue projection activated and deactivated their projector muscles significantly earlier than non-ballistic species, in a pattern consistent with a mechanism in which the muscle strains elastic tissue that subsequently recoils to power projection. Tongue projection was more thermally robust in ballistic species, but in both ballistic and non-ballistic species the projector muscles were activated earlier and for longer as temperature decreased. The retractor muscles showed a pattern similar to that of the projector muscles, but declined in a similar manner in the two groups. Muscle activity intensity also decreased at low temperatures in both groups, revealing that compensatory muscle activation does not account for the improved thermal robustness in ballistic species. Thus, relatively minor shifts in motor patterns accompanying morphological changes such as increased elastic tissue are sufficient to improve performance and decrease its thermal sensitivity without specialization of muscle contractile physiology.