Charlotte M. Stinson

Bio: Charlotte M. Stinson is an academic researcher from University of South Florida. The author has contributed to research in topics: Salamandridae & Salamandra. The author has an hindex of 3, co-authored 3 publications receiving 32 citations. Previous affiliations of Charlotte M. Stinson include California State University, Bakersfield.

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.

Functional morphology of terrestrial prey capture in salamandrid salamanders.

Abstract: Salamanders use the hyobranchial apparatus and its associated musculature for tongue projection on land and for suction feeding in water. Hyobranchial apparatus composition and morphology vary across species, and different morphologies are better suited for feeding in aquatic versus terrestrial environments. We hypothesize that differences in hyobranchial morphology result in functional trade-offs in feeding performance. We predict that semi-aquatic and aquatic salamandrids with hyobranchial morphology suited for aquatic feeding will have lower performance, in terms of tongue-projection distance, velocity, acceleration and power, compared with terrestrial salamandrids when feeding in a terrestrial environment. We found that semi-aquatic and aquatic newts had lower velocity, acceleration and muscle-mass-specific power of tongue projection when compared with the terrestrial salamanders Chioglossa lusitanica and Salamandra salamandra . The fully aquatic newt, Paramesotriton labiatus , has a robust, heavily mineralized hyobranchial apparatus and was unable to project its tongue during terrestrial feeding, and instead exhibited suction-feeding movements better suited for aquatic feeding. Conversely, terrestrial species have slender, cartilaginous hyobranchial apparatus and enlarged tongue pads that coincided with greater tongue-projection distance, velocity, acceleration and power. Chioglossa lusitanica exhibited extreme tongue-projection performance, similar to that seen in elastically projecting plethodontid salamanders; muscle-mass-specific power of tongue projection exceeded 2200 W kg −1 , more than 350 times that of the next highest performer, S . salamandra , which reached 6.3 W kg −1 . These findings reveal that two fully terrestrial salamandrids have morphological specializations that yield greater tongue-projection performance compared with species that naturally feed in both aquatic and terrestrial environments.

Snap-jaw morphology is specialized for high-speed power amplification in the Dracula ant, Mystrium camillae

Abstract: What is the limit of animal speed and what mechanisms produce the fastest movements? More than natural history trivia, the answer provides key insight into the form-function relationship of musculoskeletal movement and can determine the outcome of predator-prey interactions. The fastest known animal movements belong to arthropods, including trap-jaw ants, mantis shrimp and froghoppers, that have incorporated latches and springs into their appendage systems to overcome the limits of muscle power. In contrast to these examples of power amplification, where separate structures act as latch and spring to accelerate an appendage, some animals use a 'snap-jaw' mechanism that incorporates the latch and spring on the accelerating appendage itself. We examined the kinematics and functional morphology of the Dracula ant, Mystrium camillae, who use a snap-jaw mechanism to quickly slide their mandibles across each other similar to a finger snap. Kinematic analysis of high-speed video revealed that snap-jaw ant mandibles complete their strike in as little as 23 µsec and reach peak velocities of 90 m s-1, making them the fastest known animal appendage. Finite-element analysis demonstrated that snap-jaw mandibles were less stiff than biting non-power-amplified mandibles, consistent with their use as a flexible spring. These results extend our understanding of animal speed and demonstrate how small changes in morphology can result in dramatic differences in performance.

Aquatic–terrestrial transitions of feeding systems in vertebrates: a mechanical perspective

Abstract: Transitions to terrestrial environments confront ancestrally aquatic animals with several mechanical and physiological problems owing to the different physical properties of water and air. As aquatic feeders generally make use of flows of water relative to the head to capture, transport and swallow food, it follows that morphological and behavioral changes were inevitably needed for the aquatic animals to successfully perform these functions on land. Here, we summarize the mechanical requirements of successful aquatic-to-terrestrial transitions in food capture, transport and swallowing by vertebrates and review how different taxa managed to fulfill these requirements. Amphibious ray-finned fishes show a variety of strategies to stably lift the anterior trunk, as well as to grab ground-based food with their jaws. However, they still need to return to the water for the intra-oral transport and swallowing process. Using the same mechanical perspective, the potential capabilities of some of the earliest tetrapods to perform terrestrial feeding are evaluated. Within tetrapods, the appearance of a mobile neck and a muscular and movable tongue can safely be regarded as key factors in the colonization of land away from amphibious habitats. Comparative studies on taxa including salamanders, which change from aquatic feeders as larvae to terrestrial feeders as adults, illustrate remodeling patterns in the hyobranchial system that can be linked to its drastic change in function during feeding. Yet, the precise evolutionary history in form and function of the hyolingual system leading to the origin(s) of a muscular and adhesive tongue remains unknown.

Conserved spatio-temporal patterns of suction-feeding flows across aquatic vertebrates: a comparative flow visualization study.

Abstract: Suction feeding is a widespread prey capture strategy among aquatic vertebrates. It is almost omnipresent across fishes, and has repeatedly evolved in other aquatic vertebrates. By rapidly expanding the mouth cavity, suction feeders generate a fluid flow outside of their mouth, drawing prey inside. Fish and other suction-feeding organisms display remarkable trophic diversity, echoed in the diversity of their skull and mouth morphologies. Yet, it is unclear how variable suction flows are across species, and whether variation in suction flows supports trophic diversity. Using a high-speed flow visualization technique, we characterized the spatio-temporal patterns in the flow fields produced during feeding in 14 species of aquatic suction feeders. We found that suction-feeding hydrodynamics are highly conserved across species. Suction flows affected only a limited volume of ∼1 gape diameter away from the mouth, and peaked around the timing of maximal mouth opening. The magnitude of flow speed increased with increasing mouth diameter and, to a lesser extent, with decreasing time to peak gape opening. Other morphological, kinematic and behavioral variables played a minor role in shaping suction-feeding dynamics. We conclude that the trophic diversity within fishes, and likely other aquatic vertebrates, is not supported by a diversity of mechanisms that modify the characteristics of suction flow. Rather, we suggest that suction feeding supports such trophic diversity owing to the general lack of strong trade-offs with other mechanisms that contribute to prey capture.

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

Abstract: 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.

Food Capture in Vertebrates: A Complex Integrative Performance of the Cranial and Postcranial Systems

Abstract: Prey-capture behavior is unique because in many vertebrates, it requires the coordination between cranial and postcranial functional systems, which are traditionally defined by their separate contributions to feeding and locomotor performance, respectively. Such coordination is referred to as functional integration. First, this chapter reviews the current state of knowledge regarding cranial–postcranial integration during prey-capture behavior in aquatic and terrestrial environments, including quantitative data demonstrating cranial–postcranial coordination unequivocally, and promising qualitative observations and reports that remain to be tested explicitly. The evidence for cranial–postcranial coordination during prey capture in vertebrates are presented to show that (1) integration is an important biological phenomenon occurring across environments and (2) differences in integration can be hypothesized across and within clades. Second, the perspectives for investigating cranial–postcranial integration and its variability within and across vertebrate clades are discussed to assess the role of cranial–postcranial integration in the evolution of feeding. In particular, future research on food capture is suggested to focus on the flexibility of coordination patterns in response to food properties, as well as the sensorimotor control of cranial–postcranial coordination. The goal of this chapter is to inspire and promote future research on integration in order to extend the concept of food capture, and feeding behavior in general, beyond the cranial system in a more holistic approach to function.