Side-impact collision: mechanics of obstacle negotiation in sidewinding snakes.

Snakes excel at moving through cluttered environments, and heterogeneities can be used as propulsive contacts for snakes performing lateral undulation. However, sidewinding, which is often associated with sandy deserts, cuts a broad path through its environment that may increase its vulnerability to obstacles. Our prior work demonstrated that sidewinding can be represented as a pair of orthogonal body waves (vertical and horizontal) that can be independently modulated to achieve high maneuverability and incline ascent, suggesting that sidewinders may also use template modulations to negotiate obstacles. To test this hypothesis, we recorded overhead video of four sidewinder rattlesnakes (Crotalus cerastes) crossing a line of vertical pegs placed in the substrate. Snakes used three methods to traverse the obstacles: a Propagate Through behavior in which the lifted moving portion of the snake was deformed around the peg and dragged through as the snake continued sidewinding (115/160 runs), Reversal turns that reorient the snake entirely (35/160), or switching to Concertina locomotion (10/160). The Propagate Through response was only used if the anterior-most region of static contact would propagate along a path anterior to the peg, or if a new region of static contact could be formed near the head to satisfy this condition; otherwise, snakes could only use Reversal turns or switch to Concertina locomotion. Reversal turns allowed the snake to re-orient and either escape without further peg contact or re-orient into a posture amenable to using the Propagate Through response. We developed an algorithm to reproduce the Propagate Through behavior in a robophysical model using a modulation of the two-wave template. This range of behavioral strategies provides sidewinders with a versatile range of options for effectively negotiating obstacles in their natural habitat, as well as provide insights into the design and control of robotic systems dealing with heterogeneous habitats.

[1]  B. Jayne,et al.  Muscular mechanisms of snake locomotion: an electromyographic study of the sidewinding and concertina modes of Crotalus cerastes, Nerodia fasciata and Elaphe obsoleta. , 1988, The Journal of experimental biology.

[2]  B. Jayne Kinematics of terrestrial snake locomotion , 1986 .

[3]  D. Goldman,et al.  Sidewinding with minimal slip: Snake and robot ascent of sandy slopes , 2014, Science.

[4]  D. Goldman,et al.  Modulation of orthogonal body waves enables high maneuverability in sidewinding locomotion , 2015, Proceedings of the National Academy of Sciences.

[5]  Daniel I Goldman,et al.  Flipper-driven terrestrial locomotion of a sea turtle-inspired robot , 2013, Bioinspiration & biomimetics.

[6]  Jennifer M. Rieser,et al.  Tail use improves performance on soft substrates in models of early vertebrate land locomotors , 2016, Science.

[7]  Carl Gans,et al.  How Snakes Move , 1970 .

[8]  Carl Gans,et al.  Tetrapod Limblessness: Evolution and Functional Corollaries , 1975 .

[9]  A. Biewener,et al.  Negotiating obstacles: running kinematics of the lizard Sceloporus malachiticus , 2006 .

[10]  Howie Choset,et al.  Design and architecture of the unified modular snake robot , 2012, 2012 IEEE International Conference on Robotics and Automation.

[11]  B. Jayne Comparative morphology of the semispinalis‐spinalis muscle of snakes and correlations with locomotion and constriction , 1982, Journal of morphology.

[12]  B. Brattstrom Body Temperatures of Reptiles , 1965 .

[13]  Stephen M. Secor,et al.  Ecological Significance of Movements and Activity Range for the Sidewinder, Crotalus cerastes , 1994 .

[14]  R J Full,et al.  Templates and anchors: neuromechanical hypotheses of legged locomotion on land. , 1999, The Journal of experimental biology.

[15]  Henry C. Astley Traversing Tight Tunnels—Implementing an Adaptive Concertina Gait in a Biomimetic Snake Robot , 2018 .

[16]  M. Hildebrand Chapter 3. Walking and Running , 1985 .

[17]  Henry C Astley,et al.  Effects of perch diameter and incline on the kinematics, performance and modes of arboreal locomotion of corn snakes (Elaphe guttata) , 2007, Journal of Experimental Biology.

[18]  Henry C Astley,et al.  Arboreal habitat structure affects the performance and modes of locomotion of corn snakes (Elaphe guttata). , 2009, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[19]  S. J. Arnold,et al.  The effects of substrate and vertebral number on locomotion in the garter snake Thamnophis elegans , 1997 .

[20]  W. Mosauer Adaptive Convergence in the Sand Reptiles of the Sahara and of California: A Study in Structure and Behavior , 1932 .

[21]  N. Gravish,et al.  Uneven substrates constrain walking speed in ants through modulation of stride frequency more than stride length , 2020, Royal Society Open Science.

[22]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[23]  R. B. Cowles,et al.  Sidewinding Locomotion in Snakes , 1956 .

[24]  Ian E. Brown,et al.  A Reductionist Approach to Creating and Using Neuromusculoskeletal Models , 2000 .

[25]  W Mosauer,et al.  ON THE LOCOMOTION OF SNAKES. , 1932, Science.

[26]  Christian M. Hubicki,et al.  Mitigating memory effects during undulatory locomotion on hysteretic materials , 2020, eLife.

[27]  S. Secor,et al.  Bioenergetic correlates of foraging mode for the snakes Crotalus cerastes and Masticophis flagellum , 1994 .

[28]  A. F. Bennett,et al.  LOCOMOTOR PERFORMANCE AND ENERGETIC COST OF SIDEWINDING BY THE SNAKE CROTALUS CERASTES , 1992 .

[29]  A. Biewener,et al.  Running over rough terrain: guinea fowl maintain dynamic stability despite a large unexpected change in substrate height , 2006, Journal of Experimental Biology.

[30]  Carl Gans,et al.  KINEMATIC DESCRIPTION OF THE SIDEWINDING LOCOMOTION OF FOUR VIPERS , 2013 .

[31]  R. D'ambrosia,et al.  Muscular coactivation , 1988, The American journal of sports medicine.

[32]  B. Jayne,et al.  Arboreal habitat structure affects locomotor speed and perch choice of white-footed mice (Peromyscus leucopus). , 2012, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[33]  J. Tingle Facultatively sidewinding snakes and the origins of locomotor specialization. , 2020, Integrative and comparative biology.

[34]  Peter Greenaway,et al.  The effect of emersion on haemolymph acid-base balance and oxygen levels in Scylla serrata Forskal (Brachyura:Portunidae) , 1992 .

[35]  Jennifer M. Rieser,et al.  Mechanical diffraction reveals the role of passive dynamics in a slithering snake , 2019, Proceedings of the National Academy of Sciences.

[36]  R. A. Anderson,et al.  Rock-dwelling lizards exhibit less sensitivity of sprint speed to increases in substrate rugosity. , 2013, Zoology.

[37]  G. E. Goslow,et al.  Electrical activity and relative length changes of dog limb muscles as a function of speed and gait. , 1981, The Journal of experimental biology.

[38]  W. Mosauer,et al.  The Reptiles of a Sand Dune Area and Its Surroundings in the Colorado Desert, California: A Study in Habitat Preference , 1935 .

[39]  W. Mosauer A Note on the Sidewinding Locomotion of Snakes , 1930, The American Naturalist.

[40]  R. Hutton,et al.  Was Sherrington right about co-contractions? , 1986, Brain Research.

[41]  Howie Choset,et al.  Surprising simplicities and syntheses in limbless self-propulsion in sand , 2020, Journal of Experimental Biology.

[42]  R J Full,et al.  Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain , 2008, Journal of Experimental Biology.

[43]  Howie Choset,et al.  A review on locomotion robophysics: the study of movement at the intersection of robotics, soft matter and dynamical systems , 2016, Reports on progress in physics. Physical Society.

[44]  Lance D McBrayer,et al.  The effects of multiple obstacles on the locomotor behavior and performance of a terrestrial lizard , 2016, Journal of Experimental Biology.