Colloquium: Biophysical principles of undulatory self-propulsion in granular media

Biological locomotion, movement within environments through self-deformation, encompasses a range of time and length scales in an organism. These include the electrophysiology of the nervous system, the dynamics of muscle activation, the mechanics of the skeletal system, and the interaction mechanics of such structures within natural environments like water, air, sand, and mud. Unlike the many studies of cellular and molecular scale biophysical processes, movement of entire organisms (like flies, lizards, and snakes) is less explored. Further, while movement in fluids like air and water is also well studied, little is known in detail of the mechanics that organisms use to move on and within flowable terrestrial materials such as granular media, ensembles of small particles that collectively display solid, fluid, and gaslike behaviors. This Colloquium reviews recent progress to understand principles of biomechanics and granular physics responsible for locomotion of the sandfish, a small desert-dwelling lizard that "swims" within sand using undulation of its body. Kinematic and muscle activity measurements of sand swimming using high speed x-ray imaging and electromyography are discussed. This locomotion problem poses an interesting challenge: namely, that equations that govern the interaction of the lizard with its environment do not yet exist. Therefore, complementary modeling approaches are also described: resistive force theory for granular media, multiparticle simulation modeling, and robotic physical modeling. The models reproduce biomechanical and neuromechanical aspects of sand swimming and give insight into how effective locomotion arises from the coupling of the body movement and flow of the granular medium. The argument is given that biophysical study of movement provides exciting opportunities to investigate emergent aspects of living systems that might not depend sensitively on biological details.