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.

Blood python (Python brongersmai) strike kinematics and forces are robust to variations in substrate geometry.

Snake strikes are some of the most rapid accelerations in terrestrial vertebrates. Generating rapid body accelerations requires high ground reaction forces, but on flat surfaces snakes must rely on static friction to prevent slip. We hypothesize that snakes may be able to take advantage of structures in the environment to prevent their body from slipping, potentially allowing them to generate faster and more forceful strikes. To test this hypothesis, we captured high-speed video and forces from defensive strikes of juvenile blood pythons (Python brongersmai) on a platform that was either open on all sides or with two adjacent walls opposite the direction of the strike. Contrary to our predictions, snakes maintained high performance on open platforms by imparting rearward momentum to the posterior body and tail. This compensatory behavior increases robustness to changes in their strike conditions and could allow them to exploit variable environments.

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.

Generation of propulsive force via vertical undulations in snakes.

Lateral undulation is the most widespread mode of terrestrial vertebrate limbless locomotion, in which posteriorly propagating horizontal waves press against environmental asperities (e.g. grass, rocks) and generate propulsive reaction forces. We hypothesized that snakes can generate propulsion using a similar mechanism of posteriorly propagating vertical waves pressing against suitably oriented environmental asperities. Using an array of horizontally oriented cylinders, one of which was equipped with force sensors, and a motion capture system, we found snakes generated substantial propulsive force and propulsive impulse with minimal contribution from lateral undulation. Additional tests showed that snakes could propel themselves via vertical undulations from a single suitable contact point, and this mechanism was replicated in a robotic model. Vertical undulations can provide snakes with a valuable locomotor tool for taking advantage of vertical asperities in a variety of habitats, potentially in combination with lateral undulation, to fully exploit the 3D structure of the habitat.

Experimental modification of morphology reveals the effects of the zygosphene-zygantrum joint on the range of motion of snake vertebrae.

Variation in joint shape and soft tissue can alter range of motion (ROM) and create trade-offs between stability and flexibility. The shape of the distinctive zygosphene-zygantrum joint of snake vertebrae has been hypothesized to prevent axial torsion (twisting), but its function has never been tested experimentally. We used experimental manipulation of morphology to determine the role of the zygosphene-zygantrum articulation by micro-computed tomography (µCT) scanning and 3D printing two mid-body vertebrae with unaltered shape and with the zygosphene digitally removed for four species of phylogenetically diverse snakes. We recorded the angular ROM while manipulating the models in yaw (lateral bending), pitch (dorsoventral bending) and roll (axial torsion). Removing the zygosphene typically increased yaw and dorsal pitch ROM. In the normal vertebrae, roll was <2.5 deg for all combinations of pitch and yaw. Roll increased in altered vertebrae but only for combinations of high yaw and ventral pitch that were near or beyond the limits of normal vertebra ROM. In the prairie rattlesnake and brown tree snake, roll in the altered vertebrae was always limited by bony processes other than the zygosphene, whereas in the altered vertebrae of the corn snake and boa constrictor, roll ROM was unconstrained when the pre- and post-zygapophyses no longer overlapped. The zygosphene acts as a bony limit for yaw and dorsal pitch, indirectly preventing roll by precluding most pitch and yaw combinations where roll could occur and potentially allowing greater forces to be applied across the vertebral column than would be possible with only soft-tissue constraints.