Avi Amir

Subterranean locomotion challenges animals to maintain orientation and efficiently navigate confined spaces where vision is limited and local geometry is uncertain. Mole crickets (Gryllotalpidae), which regularly travel through self-excavated tunnels, provide a useful model for studying mechanosensory control of locomotion under these conditions. We hypothesized that backward walking, a prominent component of the mole cricket’s behavioral repertoire, is supported by complementary tactile input from the antennae and cerci. Adult Gryllotalpa tali were filmed while walking forward and backward in a narrow, straight tunnel arena under red light using high-speed video. Markerless pose tracking was used to quantify antennal and cercal tip movements, orientations, and wall-contact events in body and arena coordinates. Backward walking produced clear changes in tactile sampling behavior: antennae were reoriented and extended more posteriorly, while lateral cercal movements increased sensory coverage and posterior tactile input. Wall-contact monitoring suggested more frequent touching during backward locomotion by the antennae. These findings indicate that mole crickets adaptively reorganize active and passive mechanosensory sampling when moving backward, potentially improving boundary detection, stabilizing body posture, negotiating tunnel constraints, and supporting locomotion-related decision making during locomotion in tunnels.

Locomotor behaviour is a hallmark of animal biology and ecology. Mole crickets constitute a unique group of subterranean insects that present extreme morphological and behavioural adaptations. They therefore present a valuable model for locomotion-related research. Despite their remarkable leg-morphology adaptations, mole crickets mostly demonstrate the common insect double-tripod gait for locomotion. Here we report, however, that in response to an aversive stimulus from the front, the mole cricket will consistently adopt a unique backwards gait that we have termed ‘backward-bound’. Our temporal and spatial analysis shows that this previously unreported six-legged gait comprises a cyclic alternation between the middle and hind-leg pairs with rarely observed (in insects) left–right in-phase synchronization, while the front legs display noisy and less-consistent phase dynamics. This exceptional gait is transient and is replaced by regular backwards walking after several cycles. It is employed to distance the animal quickly from danger. A gait that can be characterized as ‘forward-bound’ is also displayed by the mole cricket, albeit for a much shorter duration (up to two cycles).