Spatial coordination of foot contacts in unrestrained climbing insects

Animals that live in a spatially complex environment such as the canopy of a tree, constantly need to find reliable foothold in three-dimensional (3D) space. In multi-legged animals, spatial co-ordination among legs is thought to improve efficiency of finding foothold by avoiding searching-movements in trailing legs. In stick insects, a 'targeting mechanism' has been described that guides foot-placement of hind- and middle legs according to the position of their leading ipsilateral leg. So far, this mechanism has been shown for standing and tethered walking animals on horizontal surfaces. Here, we investigate the efficiency of this mechanism in spatial limb co-ordination of unrestrained climbing animals. For this, we recorded whole-body kinematics of freely climbing stick insects and analysed foot placement in 3D space. We found that touch-down positions of adjacent legs were highly correlated in all three spatial dimensions, revealing 3D co-ordinate transfer among legs. Furthermore, targeting precision depended on the position of the leading leg. A second objective was to test the importance of sensory information transfer between legs. For this, we ablated a proprioceptive hair field signaling the levation of the leg. After ablation, the operated leg swung higher and performed unexpected searching movements. Furthermore, targeting of the ipsilateral trailing leg was less precise in anteroposterior and dorsoventral directions. Our results reveal that the targeting mechanism is used by unrestrained climbing stick insects in 3D space and that information from the trochanteral hair field is used in ipsilateral spatial co-ordination among legs.