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, revealing an elastic mechanism. Plethodon, in contrast, projected its tongue non-ballistically with a mean power of only 18 W kg, 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.

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).…”

“…However, in movements powered by elastic recoil, these temperature effects are largely mitigated by temporally decoupling muscle contraction from the movement itself. For example, ballistic tongue projection in chameleons, toads and salamanders is thermally robust (Q 10 <2) and even temperature independent in some cases (Deban and Richardson, 2011;Deban and Lappin, 2011;Anderson and Deban, 2012;Deban and Scales, 2016). In these systems, the reduced temperature sensitivity does not appear to result from compensatory muscle activity at low temperatures or atypical muscle contractile physiology (Deban and Lappin, 2011;Anderson and Deban, 2012;Anderson et al, 2014).…”