Active and passive mechanics for rugose terrain traversal in centipedes

Abstract

Centipedes coordinate body and limb flexion to generate propulsion. On flat solid surfaces, the limb-stepping patterns can be characterized according to the direction in which limb-aggregates propagate, opposite to (retrograde) or with the direction of motion (direct). It is unknown how limb and body dynamics are modified in terrain with terradynamic complexity more representative of these animal's natural heterogeneous environments. Here, we investigated how centipedes that use retrograde and direct limb-stepping patterns, S. polymorpha and S. sexspinosus, respectively, coordinate their body and limbs to navigate laboratory environments which present footstep challenges and terrain rugosity. We recorded the kinematics and measured the locomotive performance of these animals traversing two rugose terrains with randomly distributed step heights and compared the kinematics to those on a flat frictional surface. S. polymorpha exhibited similar body and limb dynamics across all terrains and a decrease in speed with increased terrain rugosity. Unexpectedly, when placed in a rugose terrain, S. sexspinosus changed the direction of the limb-stepping pattern from direct to retrograde. Further, for both species, traversal of these rugose terrains was facilitated by hypothesized passive mechanics: upon horizontal collision of a limb with a block, the limb bent and later continued the stepping pattern. While centipedes have many degrees of freedom, our results suggest these animals negotiate limb-substrate interactions and navigate complex terrains by offloading complex control and leveraging the innate flexibility of their limbs.

Dynamics of centipede locomotion revealed by large-scale traction force microscopy

“…Hence, the gel selects a particular gait, which is a current limitation of the method. Understanding the walking mechanisms of myriapods will not only aid in unravelling their locomotor abilities but also provide insights for designing multi-legged robots with superior locomotor performance in challenging environments such as disaster areas [5,7]. For instance, on smooth surfaces, it was shown that leg slipping might be important for efficient steering of multi-legged robots [45].…”

“…Centipedes of the orders Scolopendromorpha (i.e. the one used in this study), Geophilomorpha and Craterostigmorpha use retrograde waves, while centipedes of the orders Scutigeromorpha and Lithobiomorpha use direct waves [5]. Each leg movement cycle consists of a retraction phase (active stroke) and a protraction phase (recovery stroke).…”

“…This cyclic behaviour is facilitated by the rotation of the entire leg [6] and by their body segment joint flexibility [7]. Centipedes that use retrograde wave patterns exhibit body undulation [5]. Centipedes also exhibit stopping, raising of the anterior part and turning movements, with typical accelerations ranging from 0 to 0.2 m s −1 in less than 0.25 s, resulting in inertial forces close to 10 mN for a total animal mass of 3 g.…”

Multilegged matter transport: A framework for locomotion on noisy landscapes

“…In addition to the importance of locomotion in artificial locomotors, we posit that our matter-transport framework can give insights into aspects of neuromechanical and morphological evolution ( 39 ) from a physics of living systems perspective. That is, animals ranging from those which generate propulsion through a single bac-pair (i.e., bipeds) ( 40 , 41 ), to those which use many bacs (i.e., myriapods) ( 42 ), are capable of traversing complex natural terrains. The importance of environmental awareness and whole-body coordination is hypothesized to diminish as the number of bacs (redundancy) increases ( 42 – 44 ).…”

“…That is, animals ranging from those which generate propulsion through a single bac-pair (i.e., bipeds) ( 40 , 41 ), to those which use many bacs (i.e., myriapods) ( 42 ), are capable of traversing complex natural terrains. The importance of environmental awareness and whole-body coordination is hypothesized to diminish as the number of bacs (redundancy) increases ( 42 – 44 ). Thus, in biological terrestrial locomotors, there appears to be a shift toward either advanced neuromechanical control with reduced body appendages, or redundant body appendages with simplified neuromechanical control.…”