Graduation Year

2017

Document Type

Dissertation

Degree

Ph.D.

Degree Name

Doctor of Philosophy (Ph.D.)

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Stephen Deban, Ph.D.

Committee Member

Philip Motta, Ph.D.

Committee Member

Jason Rohr, Ph.D.

Committee Member

Bradford Gemmell, Ph.D.

Keywords

elastic recoil, salamander, scaling, allometry, power amplification

Abstract

For many animals, rapid movements place high power demands on underlying muscles. Storage of muscle energy in elastic structures and the subsequent rapid release of that energy can effectively amplify muscle power. Elastic recoil can also confer thermal robustness to performance in behaviors occurring at variable temperatures. Muscle contractile performance tends to decrease at lower temperatures, but elastic recoil is less affected by temperature. Here I examine the impacts of temperature and scale in systems using elastic recoil and I explore possible interactive effects on movement performance.

I explored the role that muscle contractile properties play in the differences in performance and thermal robustness between elastic and non-elastic systems by examining muscles from two species of plethodontid salamanders with elastically powered tongue projection and one with non-elastic tongue projection. These salamanders use tongue projection to capture prey and in species with elastic mechanisms, tongue projection is characterized by higher mechanical power output and thermal robustness compared to tongue projection of closely-related genera with non-elastic mechanisms. In vitro and in situ muscle experiments reveal that species differ in their muscle contractile properties, but these patterns do not predict the performance differences between elastic and non-elastic tongue projection. Overall, salamander tongue muscles are like other vertebrate muscles in contractile performance and thermal sensitivity. I conclude that changes in the tongue-projection mechanism, specifically the elaboration of elastic structures, are responsible for high performance and thermal robustness in species with elastic tongue projection. This suggests that the evolution of high-performance and thermally robust elastic-recoil mechanisms can occur via relatively simple changes to morphology, while muscle contractile properties remain relatively unchanged.

The efficacy of elastic recoil in the face of changing temperature depends on the mechanical work done by muscle contraction being unaffected by temperature. In vitro stimulation of Cuban tree frog (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.

How muscle work and power scale determines, in part, the scaling of movement performance. Muscle-mass-specific work is predicted to remain constant across a range of scales, assuming geometric similarity, while muscle-mass-specific power is expected to decrease with increasing scale. I tested these predictions by examining muscle morphology and contractile properties of plantaris muscles from frogs ranging in mass from 1.28 to 20.60 g. Scaling of muscle work and power was examined using both linear regression on log10-transformed data (LR) and non-linear regressions on untransformed data (NLR). In LR, muscle-mass-specific work decreased with increasing scale, but this is counteracted by a positive allometry of muscle mass to predict constant movement performance at all scales. These relationships were non-significant in NLR, though scaling with geometric similarity also predicts constant jump performance across scales. Both intrinsic shortening velocity and muscle-mass-specific power were positively allometric in both types of analysis. However, these differences between methods are caused not by large changes in scaling slopes, but by changing levels of statistical significance using corrections for multiple tests. The dependence of these conclusions on the method of regression, largely because of the setting and adjusting of an arbitrary alpha, demonstrates the importance of careful consideration of statistical methods when analyzing patterns of scaling. Nonetheless, scale accounts for little variation in contractile properties over the range of scales examined, indicating that other sources of intraspecific variation may be more important in determining muscle performance and its effects on movement.

Elastic recoil used for power amplification is most often found in smaller animals, suggesting that performance in larger animals using less elastic recoil would be affected more by changing temperatures. To examine the interaction between scale and temperature on performance, I recorded jumps from 1-34 g Cuban tree frogs (Osteopilus septentrionalis) at 10, 20, and 30°C and compared jump performance to predictions based on the effects of temperature and scaling on muscle properties. High muscle-mass-specific power requirements from measured jumps indicate that frogs use elastic recoil at all scales to achieve performance that would be impossible using only muscle, and elastic recoil allows small frogs to achieve the same level of performance as large frogs. Performance that is greater at all temperatures than predictions from models using only muscle power could result from some combination of elastic recoil and power directly from muscle. The relative contributions of muscle power and elastic recoil cannot be discerned by examining temperature effects on performance because these effects are predicted to be so similar. Predicted performance from models of elastic recoil is significantly affected by changing temperature at all scales with temperature coefficient (Q10) values similar to predictions for muscle-powered jumping. Measured Q10 values are similar to those from both predictive models and there is no interaction between temperature and scale. Therefore, elastic recoil allows for jump performance that could not be achieved by muscle power alone at all temperatures and scales, but performance predictions from elastic recoil are not more thermally robust than predictions for muscle-powered jumping.

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