Cold‐blooded snipers: thermal independence of ballistic tongue projection in the salamander <i>Hydromantes platycephalus</i>

Deban, Stephen M.; Richardson, Jason C.

doi:10.1002/jez.708

Cited by 39 publications

(93 citation statements)

References 73 publications

(94 reference statements)

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“…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.…”

Section: Impacts On Elastically and Muscle-powered Movementssupporting

confidence: 57%

“…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).…”

Section: Introductionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

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

Olberding

Deban

2017

Journal of Experimental Biology

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Performance of muscle-powered movements depends on temperature through its effects on muscle contractile properties. In vitro stimulation of Cuban treefrog (Osteopilus septentrionalis) plantaris muscles reveals that interactions between force and temperature affect the mechanical work of muscle. At low temperatures (9-17°C), muscle work depends on temperature when shortening at any force, and temperature effects are greater at higher forces. At warmer temperatures (13-21°C), muscle work depends on temperature when shortening with intermediate and high forces (≥30% peak isometric tetanic force). Shortening velocity is most strongly affected by temperature at low temperatures and high forces. Power is also most strongly affected at low temperature intervals, but this effect is minimized at intermediate forces. Effects of temperature on muscle force explain these interactions; force production decreases at lower temperatures, increasing the challenge of moving a constant force relative to the muscle's capacity. These results suggest that animal performance that requires muscles to do work with low forces relative to a muscle's maximum force production will be robust to temperature changes, and this effect should be true whether muscle acts directly or through elastic-recoil mechanisms and whether force is prescribed (i.e. internal) or variable (i.e. external). Conversely, performance requiring muscles to shorten with relatively large forces is expected to be more sensitive to temperature changes.

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Section: Impacts On Elastically and Muscle-powered Movementssupporting

confidence: 57%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Olberding

Deban

2017

Journal of Experimental Biology

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“…Ballistic tongue-projection performance in chameleons, salamanders, toads and frogs, for instance, exhibits significantly lower thermal dependence than the performance of tongue retraction (Anderson and Deban, 2010;Deban and Lappin, 2011;Deban and Richardson, 2011;Sandusky and Deban, 2012). This pattern has been shown to be the result not of any compensatory activation of muscle at low temperature in chameleons and toads (Deban and Lappin, 2011;Anderson and Deban, 2012), nor of any unusually reduced effect of temperature on typical muscle contractile physiology in chameleons (Anderson and Deban, 2012).…”

Section: Introductionmentioning

confidence: 97%

Thermal effects on the performance, motor control, and muscle dynamics of ballistic feeding in the salamanderEurycea guttolineata

Anderson

Larghi

Deban

2014

Journal of Experimental Biology

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Temperature strongly affects muscle contractile rate properties and thus may influence whole-organism performance. Movements powered by elastic recoil, however, are known to be more thermally robust than muscle-powered movements. We examined the wholeorganism performance, motor control and muscle contractile physiology underlying feeding in the salamander Eurycea guttolineata. We compared elastically powered tongue projection with the associated muscle-powered retraction to determine the thermal robustness of each of these functional levels. We found that tongueprojection distance in E. guttolineata was unaffected by temperature across the entire 4-26°C range, tongue-projection dynamics were significantly affected by temperature across only the 4-11°C interval, and tongue retraction was affected to a higher degree across the entire temperature range. The significant effect of temperature on projection dynamics across the 4-11°C interval corresponds to a significant decline in projector muscle burst intensity and peak contractile force of the projector muscle across the same interval. Across the remaining temperature range, however, projection dynamics were unaffected by temperature, with muscle contractile physiology showing typical thermal effects and motor patterns showing increased activity durations and latencies. These results reveal that elastically powered tongue-projection performance in E. guttolineata is maintained to a higher degree than muscle-powered tongue retraction performance across a wide temperature range. These results further indicate that thermal robustness of the elastically powered movement is dependent on motor control and muscle physiology that results in comparable energy being stored in elastic tissues across a range of temperatures.

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“…Other types of physiological activities also appear to be capped at a similar time scale. For example, salamanders can shoot and fully extend their tongues out in less than 7 ms in order to catch flying prey (4). Throughout these physiological activities it is essential that the extending polypeptide remains elastic.…”

mentioning

confidence: 99%

Rate limit of protein elastic response is tether dependent

Berkovich

Hermans

Popa

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The elastic restoring force of tissues must be able to operate over the very wide range of loading rates experienced by living organisms. It is surprising that even the fastest events involving animal muscle tissues do not surpass a few hundred hertz. We propose that this limit is set in part by the elastic dynamics of tethered proteins extending and relaxing under a changing load. Here we study the elastic dynamics of tethered proteins using a fast force spectrometer with sub-millisecond time resolution, combined with Brownian and Molecular Dynamics simulations. We show that the act of tethering a polypeptide to an object, an inseparable part of protein elasticity in vivo and in experimental setups, greatly reduces the attempt frequency with which the protein samples its free energy. Indeed, our data shows that a tethered polypeptide can traverse its free-energy landscape with a surprisingly low effective diffusion coefficient D eff ∼ 1,200 nm 2 ∕s. By contrast, our Molecular Dynamics simulations show that diffusion of an isolated protein under force occurs at D eff ∼ 10 8 nm 2 ∕s. This discrepancy is attributed to the drag force caused by the tethering object. From the physiological time scales of tissue elasticity, we calculate that tethered elastic proteins equilibrate in vivo with D eff ∼ 10 4 -10 6 nm 2 ∕s which is two to four orders magnitude smaller than the values measured for untethered proteins in bulk.force spectroscopy | protein diffusion | viscoelasticity | single molecule

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Cold‐blooded snipers: thermal independence of ballistic tongue projection in the salamander Hydromantes platycephalus

Cited by 39 publications

References 73 publications

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

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

Thermal effects on the performance, motor control, and muscle dynamics of ballistic feeding in the salamanderEurycea guttolineata

Rate limit of protein elastic response is tether dependent

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