Crawling without wiggling: muscular mechanisms and kinematics of rectilinear locomotion in boa constrictors

Abstract

A central issue for understanding locomotion of vertebrates is how muscle activity and movements of their segmented axial structures are coordinated, and snakes have a longitudinal uniformity of body segments and diverse locomotor behaviors that are well suited for studying the neural control of rhythmic axial movements. Unlike all other major modes of snake locomotion, rectilinear locomotion does not involve axial bending, and the mechanisms of propulsion and modulating speed are not well understood. We integrated electromyograms and kinematics of boa constrictors to test Lissmann's decades-old hypotheses of activity of the costocutaneous superior (CCS) and inferior (CCI) muscles and the intrinsic cutaneous interscutalis (IS) muscle during rectilinear locomotion. The CCI was active during static contact with the ground as it shortened and pulled the axial skeleton forward relative to both the ventral skin and the ground during the propulsive phase. The CCS was active during sliding contact with the ground as it shortened and pulled the skin forward relative to both the skeleton and the ground during the recovery phase. The IS shortened the ventral skin, and subsequent isometric activity kept the skin stiff and shortened during most of static contact while overlapping extensively with CCI activity. The concentric activity of the CCI and CCS supported Lissmann's predictions. Contrary to Lissmann, the IS had prolonged isometric activity, and the time when it shortened was not consistent with providing propulsive force. Decoupling propulsion from axial bending in rectilinear locomotion may have facilitated economical locomotion of early snakes in subterranean tunnels.

What Defines Different Modes of Snake Locomotion?

“…Electromyographic experiments ( Newman and Jayne 2018 ) support Lissmann’s hypotheses regarding the antagonistic functions of the CCS and CCI ( Fig. 1B and D ).…”

“…Video images of the right side of the snake (top) and ventral scales (bottom) of the snake for the same data as shown in (B–E) ( F ). Adapted from Newman and Jayne (2018) . See supplementary video at https://www.youtube.com/watch?v=wwHkAMo-Mj0 .…”

“…Since the mid-1980s, electromyography has been used to determine the muscular mechanisms of all four of the previously recognized snake locomotor modes ( Jayne 1988b , 1988c ; Gasc et al. 1989 ; Moon and Gans 1998 ; Newman and Jayne 2018 ). The energetic costs have also been determined for terrestrial lateral undulation, sidewinding, and concertina locomotion ( Walton et al.…”

Dynamics of a Vibration Driven Bristlebot

“…The surface of these organisms have some micro/nano scales oriented at some angle causing mechanical anisotropy. This anisotropy leads to the generation of asymmetric contact forces with the substrate when they periodically shift their centre of mass or change their shape [1,11,15].…”

“…15: θ vs time when the system exhibits slip-stick behaviour with a periodic bristle slip in the positive direction. Forcing parameters are ω = 40π rad/sec and A = 4mm.…”