Thermal robustness of biomechanical processes

Abstract

Temperature influences many physiological processes that govern life as a result of the thermal sensitivity of chemical reactions. The repeated evolution of endothermy and widespread behavioral thermoregulation in animals highlight the importance of elevating tissue temperature to increase the rate of chemical processes. Yet, movement performance that is robust to changes in body temperature has been observed in numerous species. This thermally robust performance appears exceptional in light of the well-documented effects of temperature on muscle contractile properties, including shortening velocity, force, power and work. Here, we propose that the thermal robustness of movements in which mechanical processes replace or augment chemical processes is a general feature of any organismal system, spanning kingdoms. The use of recoiling elastic structures to power movement in place of direct muscle shortening is one of the most thoroughly studied mechanical processes; using these studies as a basis, we outline an analytical framework for detecting thermal robustness, relying on the comparison of temperature coefficients (Q10 values) between chemical and mechanical processes. We then highlight other biomechanical systems in which thermally robust performance that arises from mechanical processes may be identified using this framework. Studying diverse movements in the context of temperature will both reveal mechanisms underlying performance and allow the prediction of changes in performance in response to a changing thermal environment, thus deepening our understanding of the thermal ecology of many organisms.

Temperature effects on the jumping performance of house crickets

“…As mentioned above, greater relative load results in higher thermal sensitivity of muscle work, at least as demonstrated in frog limb muscles (Olberding & Deban, 2017). These results also emphasizes that Olberding & Deban, 2021).…”

“…As mentioned above, greater relative load results in higher thermal sensitivity of muscle work, at least as demonstrated in frog limb muscles (Olberding & Deban, 2017). These results also emphasizes that thermal robustness conferred by an elastic (or other physical) mechanism can vary somewhat independently of the performance advantage ( sensu Olberding & Deban, 2021).…”

“…Movements driven by elastic‐recoil mechanisms in other arthropods are expected to display thermal robustness (Olberding & Deban, 2021), a prediction for which there is some evidence. Fleas have been shown to extend the period of loading of elastic structures before jumping when cold, but maintain jumping performance, and their lifestyle as parasites often requires them to jump from a cold environment to a warm host (Bennet‐Clark & Lucey, 1967; Rothschild & Schlein, 1975; Rothschild et al, 1972).…”

“…Movements driven by elastic-recoil mechanisms in other arthropods are expected to display thermal robustness (Olberding & Deban, 2021), a prediction for which there is some evidence.…”

Complexity and diversity of motion amplification and control strategies in motile carnivorous plant traps

“…Storage and release of energy by springs have often been framed as a means to overcome limitations imposed by muscles' ability to produce power [7,[10][11][12]. The new framework acknowledges additional and alternative rationales for using springs, such as energy efficiency, motion control, impedance matching between actuators and load, and thermal robustness [3,4,7,8,[13][14][15][16].…”