Extreme Performance and Functional Robustness of Movement are Linked to Muscle Architecture: Comparing Elastic and Nonelastic Feeding Movements in Salamanders

Abstract

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.

Effects of temperature and force requirements on muscle work and power output

“…In vivo studies have found that performance of feeding behaviors that utilize elastic-recoil mechanisms is maintained despite changing temperature and the effects on muscle contractile physiology (Anderson and Deban, 2010;Anderson et al, 2014;Deban and Lappin, 2011;Deban and Richardson, 2011;Deban and Scales, 2016;Scales et al, 2016). Because these salamanders, toads and chameleons are maintaining performance at lower temperatures, their muscles must be shortening to do work with relatively low forces, provided that P 0 is affected by temperature as we have shown in the present study.…”

“…Many ectotherms bypass the limitations of muscle contraction and maintain performance at lower temperatures by using elastic-recoil mechanisms in their feeding movements (chameleons: Anderson and Deban, 2010;toads: Deban and Lappin, 2011;salamanders: Anderson et al, 2014;Deban and Richardson, 2011;Deban and Scales, 2016;Scales et al, 2016). These animals are able to use their muscles to stretch elastic connective tissue, storing energy that is later released rapidly when this tissue recoils (de Groot and van Leeuwen, 2004;Deban et al, 2007;Lappin et al, 2006).…”

“…Therefore, the effects of temperature on muscle contraction in elastic-recoil mechanisms are most relevant under prescribed-load conditions, rather than cycles of imposed length changes and fluctuating load. The thermal robustness of performance has been well established in systems in which single muscle contractions are used to move prescribed forces, including the feeding mechanisms of salamanders, chameleons and toads (Anderson and Deban, 2010;Anderson et al, 2014;Deban and Lappin, 2011;Deban and Richardson, 2011;Deban and Scales, 2016;Scales et al, 2016).…”

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

“…Changes in temperature present a significant challenge to organisms, especially ectotherms; low temperature can result in substantial decreases in ecologically relevant performance such as predator escape and feeding (Huey and Bennett, 1987;John-Alder et al, 1989;Lutz and Rome, 1996;Wintzer and Motta, 2004;Devries and Wainwright, 2006;Herrel et al, 2007;Deban and Scales, 2016;Scales et al, 2016). Reductions in performance such as running and swimming velocities and jumping distances primarily result from lower muscle contractile rates that can decline by half over a 10°C drop in temperature (Bennett, 1984(Bennett, , 1985Hirano and Rome, 1984;Bauwens et al, 1995;Lutz and Rome, 1996;Peplowski and Marsh, 1997;Navas et al, 1999;Donley et al, 2007;Herrel et al, 2007;James, 2013).…”

“…Each epibranchial attaches rostrally to paired ceratobranchials, which then connect rostrally to the unpaired basibranchial that sits in the floor of the mouth and supports the tongue pad (Lombard and Wake, 1977;Wake and Deban, 2000;Deban, 2002). In muscle-powered, non-ballistic projection, the SAR is directly attached to the epibranchials, and little collagen is available in the SAR for energy storage (Lombard and Wake, 1977;Deban et al, 2007;Deban and Scales, 2016;Scales et al, 2016). Thus, during tongue projection, activation of the SAR coincides with tongue movement and the epibranchial does not leave the SAR (Deban and Dicke, 1999;Deban and Scales, 2016;Scales et al, 2016).…”