Untethered muscle tracking using magnetomicrometry.

Muscle tissue drives nearly all movement in the animal kingdom, providing power, mobility, and dexterity. Technologies for measuring muscle tissue motion, such as sonomicrometry, fluoromicrometry, and ultrasound, have significantly advanced our understanding of biomechanics. Yet, the field lacks the ability to monitor muscle tissue motion for animal behavior outside the lab. Towards addressing this issue, we previously introduced magnetomicrometry, a method that uses magnetic beads to wirelessly monitor muscle tissue length changes, and we validated magnetomicrometry via tightly-controlled in situ testing. In this study we validate the accuracy of magnetomicrometry against fluoromicrometry during untethered running in an in vivo turkey model. We demonstrate real-time muscle tissue length tracking of the freely-moving turkeys executing various motor activities, including ramp ascent and descent, vertical ascent and descent, and free roaming movement. Given the demonstrated capacity of magnetomicrometry to track muscle movement in untethered animals, we feel that this technique will enable new scientific explorations and an improved understanding of muscle function.

Clinging ability is related to particular aspects of foot morphology in salamanders.

The interaction between morphology, performance, and ecology has long been studied in order to explain variation in the natural world. Within arboreal salamanders, diversification in foot morphology and microhabitat use are thought to be linked by the impact of foot size and shape on clinging and climbing performance, resulting in an ability to access new habitats. We examine whether various foot shape metrics correlate with stationary cling performance and microhabitat to explicitly quantify this performance gradient across 14 species of salamander, including both arboreal and nonarboreal species. Clinging performance did not correlate with foot shape, as quantified by landmark-based geometric morphometrics, nor with microhabitat use. Mass-corrected foot centroid size and foot contact area, on the other hand, correlated positively with clinging performance on a smooth substrate. Interestingly, these foot variables correlated negatively with clinging performance on rough substrates, suggesting the use of multiple clinging mechanisms dependent upon the texture of the surface. These findings demonstrate that centroid size and foot contact area are more functionally relevant for clinging in salamanders than foot shape, suggesting that foot shape need not converge in order to achieve convergent performance. More broadly, our results provide an example of how the quantification of the performance gradient can provide the appropriate lens through which to understand the macroevolution of morphology and ecology.

The Effects of Roughness and Wetness on Salamander Cling Performance.

Animals clinging to natural surfaces have to generate attachment across a range of surface roughnesses in both dry and wet conditions. Plethodontid salamanders can be aquatic, semi-aquatic, terrestrial, arboreal, troglodytic, saxicolous, and fossorial and therefore may need to climb on and over rocks, tree trunks, plant leaves, and stems, as well as move through soil and water. Sixteen species of salamanders were tested to determine the effects of substrate roughness and wetness on maximum cling angle. Substrate roughness had a significant effect on maximum cling angle, an effect that varied among species. Substrates of intermediate roughness (asperity size 100-350 µm) resulted in the poorest attachment performance for all species. Small species performed best on smooth substrates, while large species showed significant improvement on the roughest substrates (asperity size 1000-4000 µm), possibly switching from mucus adhesion on a smooth substrate to an interlocking attachment on rough substrates. Water, in the form of a misted substrate coating and a flowing stream, decreased cling performance in salamanders on smooth substrates. However, small salamanders significantly increased maximum cling angle on wetted substrates of intermediate roughness, compared with the dry condition. Study of cling performance and its relationship to surface properties may cast light onto how this group of salamanders has radiated into the most speciose family of salamanders that occupies diverse habitats across an enormous geographical range.

Cling performance and surface area of attachment in plethodontid salamanders.

Plethodontid salamanders inhabit terrestrial, scansorial, arboreal and troglodytic habitats in which clinging and climbing allow them to access additional food and shelter as well as escape from unfavorable temperature and moisture conditions and ground-dwelling predators. Although salamanders lack claws and toe pads found in other taxa, they successfully cling to and climb on inclined, vertical and inverted substrates in nature. Maximum cling angle was tested on smooth acrylic, and the relationship between cling angle, body mass and surface area of attachment (contact area) was investigated. This study found that many salamander species can cling fully inverted using only a portion of their ventral surface area to attach. Salamanders fall into three functional groups based on mass and maximum cling angle: (1) high-performing, very small salamanders, (2) moderately high performing small and medium-sized salamanders and (3) low-performing large salamanders. They show significant differences in maximum cling angle, even between species of similar mass. In species of similar mass experiencing significantly different detachment stress (resulting from significantly different contact area), differences in morphology or behavior affect how much body surface is attached to the substrate. High performance in some species, such as Desmognathus quadramaculatus, is attributable to large contact area; low performance in a similarly sized species, Ensatina eschscholtzii, is due to behavior that negatively impacts contact area. There was no clear evidence of scaling of adhesive strength with increasing body size. Salamander maximum cling angle is the result of morphology and behavior impacting the detachment stresses experienced during clinging.

Evolution of a high-performance and functionally robust musculoskeletal system in salamanders.

The evolution of ballistic tongue projection in plethodontid salamanders-a high-performance and thermally robust musculoskeletal system-is ideal for examining how the components required for extreme performance in animal movement are assembled in evolution. Our comparative data on whole-organism performance measured across a range of temperatures and the musculoskeletal morphology of the tongue apparatus were examined in a phylogenetic framework and combined with data on muscle contractile physiology and neural control. Our analysis reveals that relatively minor evolutionary changes in morphology and neural control have transformed a muscle-powered system with modest performance and high thermal sensitivity into a spring-powered system with extreme performance and functional robustness in the face of evolutionarily conserved muscle contractile physiology. Furthermore, these changes have occurred in parallel in both major clades of this largest family of salamanders. We also find that high-performance tongue projection that exceeds available muscle power and thermal robustness of performance coevolve, both being emergent properties of the same elastic-recoil mechanism. Among the taxa examined, we find muscle-powered and fully fledged elastic systems with enormous performance differences, but no intermediate forms, suggesting that incipient elastic mechanisms do not persist in evolutionary time. A growing body of data from other elastic systems suggests that similar coevolution of traits may be found in other ectothermic animals with high performance, particularly those for which thermoregulation is challenging or ecologically costly.

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

Elastic-recoil mechanisms can improve organismal performance and circumvent the thermal limitations of muscle contraction, yet they require the appropriate motor control to operate. We compare muscle activity during tongue projection in salamanders with elastically powered, ballistic projection with activity of those with muscle-powered, non-ballistic projection across a range of temperatures to understand how motor control is integrated with elastically powered movements, and how this integration contributes to reduced thermal sensitivity. Species with ballistic tongue projection activated and deactivated their projector muscles significantly earlier than non-ballistic species, in a pattern consistent with a mechanism in which the muscle strains elastic tissue that subsequently recoils to power projection. Tongue projection was more thermally robust in ballistic species, but in both ballistic and non-ballistic species the projector muscles were activated earlier and for longer as temperature decreased. The retractor muscles showed a pattern similar to that of the projector muscles, but declined in a similar manner in the two groups. Muscle activity intensity also decreased at low temperatures in both groups, revealing that compensatory muscle activation does not account for the improved thermal robustness in ballistic species. Thus, relatively minor shifts in motor patterns accompanying morphological changes such as increased elastic tissue are sufficient to improve performance and decrease its thermal sensitivity without specialization of muscle contractile physiology.

Effects of larval size and hydrodynamics on the growth rates of the black fly Simulium tribulatum.

Black flies are ubiquitous and important members of lotic ecosystems. Size is known to affect many aspects of their life in the aquatic larval stage, including intraspecific competition for feeding sites. As filter feeders, flow affects their ability to feed and reach sufficiently fast flow. This, in turn, can lead to risky fluid-mediated dispersal behavior in search of better conditions. It is surprising, therefore, that little information is available regarding how physiological and environmental factors combine to affect larval growth rates. The present study determines the relative growth rates of small (0.6 mm) and large (approximately 4 mm) larvae in laboratory flumes designed to produce spatially homogeneous and temporally consistent flow regimes at ecologically relevant velocities (44 and 64 cm/s). Our results indicate that size and flow both influence growth rates and that the 2 interact significantly. Young larvae exhibit faster growth rates and a greater positive response to increased flow speed. This result might help explain why smaller larvae have a greater propensity to disperse than larger larvae: the benefit of increased growth rate that they receive from relocating to faster flow might balance the risks inherent in dispersal.