Functional diversity of snake locomotor behaviors: A review of the biological literature for bioinspiration.

Organismal solutions to natural challenges can spark creative engineering applications. However, most engineers are not experts in organismal biology, creating a potential barrier to maximally effective bioinspired design. In this review, we aim to reduce that barrier with respect to a group of organisms that hold particular promise for a variety of applications: snakes. Representing >10% of tetrapod vertebrates, snakes inhabit nearly every imaginable terrestrial environment, moving with ease under many conditions that would thwart other animals. To do so, they employ over a dozen different types of locomotion (perhaps well over). Lacking limbs, they have evolved axial musculoskeletal features that enable their vast functional diversity, which can vary across species. Different species also have various skin features that provide numerous functional benefits, including frictional anisotropy or isotropy (as their locomotor habits demand), waterproofing, dirt shedding, antimicrobial properties, structural colors, and wear resistance. Snakes clearly have much to offer to the fields of robotics and materials science. We aim for this review to increase knowledge of snake functional diversity by facilitating access to the relevant literature.

Locomotor kinematics on sand versus vinyl flooring in the sidewinder rattlesnake Crotalus cerastes.

For terrestrial locomotion of animals and machines, physical characteristics of the substrate can strongly impact kinematics and performance. Snakes are an especially interesting system for studying substrate effects because their gait depends more on the environment than on their speed. We tested sidewinder rattlesnakes (Crotalus cerastes) on two surfaces: sand collected from their natural environment and vinyl tile flooring, an artificial surface often used to elicit sidewinding in laboratory settings. Of ten kinematic variables examined, two differed significantly between the substrates: the body's waveform had an average of ∼17% longer wavelength on vinyl flooring (measured in body lengths), and snakes lifted their bodies an average of ∼40% higher on sand (measured in body lengths). Sidewinding may also differ among substrates in ways we did not measure (e.g. ground reaction forces and energetics), leaving open clear directions for future study.

The relative contributions of multiarticular snake muscles to movement in different planes.

Muscles spanning multiple joints play important functional roles in a wide range of systems across tetrapods; however, their fundamental mechanics are poorly understood, particularly the consequences of anatomical position on mechanical advantage. Snakes provide an excellent study system for advancing this topic. They rely on the axial muscles for many activities, including striking, constriction, defensive displays, and locomotion. Moreover, those muscles span from one or a few vertebrae to over 30, and anatomy varies among muscles and among species. We characterized the anatomy of major epaxial muscles in a size series of corn snakes (Pantherophis guttatus) using diceCT scans, and then took several approaches to calculating contributions of each muscle to force and motion generated during body bending, starting from a highly simplistic model and moving to increasingly complex and realistic models. Only the most realistic model yielded equations that included the consequence of muscle span on torque-displacement trade-offs, as well as resolving ambiguities that arose from simpler models. We also tested whether muscle cross-sectional areas or lever arms (total magnitude or pitch/yaw/roll components) were related to snake mass, longitudinal body region (anterior, middle, posterior), and/or muscle group (semispinalis-spinalis, multifidus, longissimus dorsi, iliocostalis, and levator costae). Muscle cross-sectional areas generally scaled with positive allometry, and most lever arms did not depart significantly from geometric similarity (isometry). The levator costae had lower cross-sectional area than the four epaxial muscles, which did not differ significantly from each other in cross-sectional area. Lever arm total magnitudes and components differed among muscles. We found some evidence for regional variation, indicating that functional regionalization merits further investigation. Our results contribute to knowledge of snake muscles specifically and multiarticular muscle systems generally, providing a foundation for future comparisons across species and bioinspired multiarticular systems.

Corn Snakes Show Consistent Sarcomere Length Ranges Across Muscle Groups and Ontogeny.

The force-generating capacity of muscle depends upon many factors including the actin-myosin filament overlap due to the relative length of the sarcomere. Consequently, the force output of a muscle may vary throughout its range of motion, and the body posture allowing maximum force generation may differ even in otherwise similar species. We hypothesized that corn snakes would show an ontogenetic shift in sarcomere length range from being centered on the plateau of the length-tension curve in small individuals to being on the descending limb in adults. Sarcomere lengths across the plateau would be advantageous for locomotion, while the descending limb would be advantageous for constriction due to the increase in force as the coil tightens around the prey. To test this hypothesis, we collected sarcomere lengths from freshly euthanized corn snakes, preserving segments in straight and maximally curved postures, and quantifying sarcomere length via light microscopy. We dissected 7 muscles (spinalis, semispinalis, multifidus, longissimus dorsi, iliocostalis (dorsal and ventral), and levator costae) in an ontogenetic series of corn snakes (mass = 80-335 g) at multiple regions along the body (anterior, middle, and posterior). Our data shows all of the muscles analyzed are on the descending limb of the length-tension curve at rest across all masses, regions, and muscles analyzed, with muscles shortening onto or past the plateau when flexed. While these results are consistent with being advantageous for constriction at all sizes, there could also be unknown benefits of this sarcomere arrangement for locomotion or striking.

Scaling and relations of morphology with locomotor kinematics in the sidewinder rattlesnake Crotalus cerastes.

The movement of limbless terrestrial animals differs fundamentally from that of limbed animals, yet few scaling studies of their locomotor kinematics and morphology are available. We examined scaling and relations of morphology and locomotion in sidewinder rattlesnakes (Crotalus cerastes). During sidewinding locomotion, a snake lifts sections of its body up and forward while other sections maintain static ground contact. We used high-speed video to quantify whole-animal speed and acceleration; the height to which body sections are lifted; and the frequency, wavelength, amplitude and skew angle (degree of tilting) of the body wave. Kinematic variables were not sexually dimorphic, and most did not deviate from isometry, except wave amplitude. Larger sidewinders were not faster, contrary to many results from limbed terrestrial animals. Free from the need to maintain dynamic similarity (because their locomotion is dominated by friction rather than inertia), limbless species may have greater freedom to modulate speed independently of body size. Path analysis supported: (1) a hypothesized relationship between body width and wavelength, indicating that stouter sidewinders form looser curves; (2) a strong relationship between cycle frequency and whole-animal speed; and (3) weaker effects of wavelength (positive) and amplitude (negative) on speed. We suggest that sidewinding snakes may face a limit on stride length (to which amplitude and wavelength both contribute), beyond which they sacrifice stability. Thus, increasing frequency may be the best way to increase speed. Finally, frequency and skew angle were correlated, a result that deserves future study from the standpoint of both kinematics and physiology.

Functional consequences of convergently evolved microscopic skin features on snake locomotion.

The small structures that decorate biological surfaces can significantly affect behavior, yet the diversity of animal-environment interactions essential for survival makes ascribing functions to structures challenging. Microscopic skin textures may be particularly important for snakes and other limbless locomotors, where substrate interactions are mediated solely through body contact. While previous studies have characterized ventral surface features of some snake species, the functional consequences of these textures are not fully understood. Here, we perform a comparative study, combining atomic force microscopy measurements with mathematical modeling to generate predictions that link microscopic textures to locomotor performance. We discover an evolutionary convergence in the ventral skin structures of a few sidewinding specialist vipers that inhabit sandy deserts-an isotropic texture that is distinct from the head-to-tail-oriented, micrometer-sized spikes observed on a phylogenetically broad sampling of nonsidewinding vipers and other snakes from diverse habitats and wide geographic range. A mathematical model that relates structural directionality to frictional anisotropy reveals that isotropy enhances movement during sidewinding, whereas anisotropy improves movement during slithering via lateral undulation of the body. Our results highlight how an integrated approach can provide quantitative predictions for structure-function relationships and insights into behavioral and evolutionary adaptations in biological systems.

Facultatively Sidewinding Snakes and the Origins of Locomotor Specialization.

Specialist species often possess adaptations that strongly distinguish them from their relatives, obscuring the transitional steps leading to specialization. Sidewinding snakes represent an example of locomotor specialization in an elongate, limbless terrestrial vertebrate. We typically think of sidewinding as a gait that only a handful of very specialized snake species perform, mostly vipers from sandy desert environments. Some of these desert-dwelling vipers are so specialized that they only rarely use more common types of locomotion. However, some non-viper species sidewind facultatively in particular circumstances, and a few may regularly sidewind under natural conditions. Numerous accounts report facultative sidewinding in species that more typically perform other types of locomotion. I have compiled these accounts, uncovering evidence that dozens of species perform sidewinding with varying proficiency under a variety of conditions. These facultative sidewinders can reveal insight into the evolution and biomechanics of sidewinding, and they provide ample opportunities for future study.

Spillover of a biological control agent (Chrysolina quadrigemina) onto native St. Johnswort (Hypericum punctatum).

Biological control agents may have unintended effects on native biota, particularly species that are closely related to the target invader. Here, we explored how Chrysolina quadrigemina, a beetle introduced to control the invasive weed Hypericum perforatum, impacts native H. punctatum in Tompkins County, New York, USA. Using a suite of complementary field surveys and experimental manipulations, we examined beetle preference for native and exotic Hypericum species and whether beetle herbivory influences the spatial distribution of H. punctatum. We found that the introduced beetle readily consumes native H. punctatum in addition to its intended target, and that H. punctatum at our field sites generally occurs along forest edges despite higher performance of experimental plants in more open habitats. However, we found no evidence that the beetle limits H. punctatum to forest edge habitats.