Environmental interaction influences muscle activation strategy during sand-swimming in the sandfish lizard Scincus scincus

Abstract

SUMMARYAnimals like the sandfish lizard (Scincus scincus) that live in desert sand locomote on and within a granular medium whose resistance to intrusion is dominated by frictional forces. Recent kinematic studies revealed that the sandfish utilizes a wave of body undulation during swimming. Models predict that a particular combination of wave amplitude and wavelength yields maximum speed for a given frequency, and experiments have suggested that the sandfish targets this kinematic waveform. To investigate the neuromechanical strategy of the sandfish during walking, burial and swimming, here we use high-speed X-ray and visible light imaging with synchronized electromyogram (EMG) recordings of epaxial muscle activity. While moving on the surface, body undulation was not observed and EMG showed no muscle activation. During subsurface sand-swimming, EMG revealed an anterior-to-posterior traveling wave of muscle activation which traveled faster than the kinematic wave. Muscle activation intensity increased as the animal swam deeper into the material but was insensitive to undulation frequency. These findings were in accord with empirical force measurements, which showed that resistance force increased with depth but was independent of speed. The change in EMG intensity with depth indicates that the sandfish targets a kinematic waveform (a template) that models predict maximizes swimming speed and minimizes the mechanical cost of transport as the animal descends into granular media. The differences in the EMG pattern compared with EMG of undulatory swimmers in fluids can be attributed to the friction-dominated intrusion forces of granular media. Supplementary material available online at

Locomotor benefits of being a slender and slick sand-swimmer

“…Data sets were analyzed from previous work (see Sharpe et al, 2013). All experimental procedures were conducted in accordance with the Georgia Institute of Technology IACUC protocol number (A08012) and Radiation Safety protocol (X-272).…”

“…7A) (Gravish et al, 2010;Li et al, 2009;Sharpe et al, 2013). The bed (22.9×40.6 cm 2 ) was filled with glass particles (diameter=0.27±0.04 mm and density=2.5 g cm -3…”

“…1C) have provided insight into the locomotor strategy and performance of this sand swimmer, and have even revealed principles of swimmers in real fluids . X-ray imaging of the sandfish lizard (Maladen et al, 2009;Sharpe et al, 2013) revealed that it swims subsurface using single-period anterior-to-posterior traveling body curvature waves while its limbs remain along its body. A multi-particle discrete element method (DEM) simulation of a granular material (composed of 3 mm diameter particles) coupled to a numerical model of the animal captured swimming kinematics and predicted that sandfish swimming takes place within a self-generated localized 'frictional fluid' (Ding et al, 2012).…”

Modulation of orthogonal body waves enables high maneuverability in sidewinding locomotion

“…Whereas these turns constitute a form of internal perturbation, further testing of this hypothesized template should include how the animal responds to external perturbations (22) (such as obstacles) as well as measurements of the underlying neural controls predicted by template control (e.g., as in sand swimming in ref. 23). Coupling such studies to further investigation of the robot could help explain why the sidewinder rattlesnake moves effectively on granular media, whereas its close relatives do not (9), and establish these organisms as an ideal model system for two-wave template locomotion.…”

Taphonomic patterns of a dinosaur accumulation in a lacustrine delta system in the Jurassic Morrison Formation, San Rafael Swell, Utah, USA

“…Other sand-swimming reptiles, such as the sandfish (Scincus scincus), the Kenyan sand boa (Eryx colubrinus), and the Saharan sand viper (Cerastes cerastes), produce biogenic structures like those of Chalcides ocellatus in similar sediment (Young and Morain, 2003;Hembree and Hasiotis, 2007;Baumgartner et al, 2008). Studies of the mechanics of sand-swimming locomotion have primarily involved the sandfish whose method of sand swimming is nearly identical to that of C. ocellatus (Baumgartner et al, 2008;Maladen et al, 2009;Sharpe et al, 2013). These studies have shown that the burrowing behavior of S. scincus is similar to that of C. ocellatus.…”