Insects Use Two Distinct Classes of Steps during Unrestrained Locomotion

Background: Adaptive, context-dependent control of locomotion requires modulation of centrally generated rhythmic motor patterns through peripheral control loops and postural reflexes. Thus assuming that the modulation of rhythmic motor patterns accounts for much of the behavioural variability observed in legged locomotion, investigating behavioural variability is a key to the understanding of context-dependent control mechanisms in locomotion. To date, the variability of unrestrained locomotion is poorly understood, and virtually nothing is known about the features that characterise the natural statistics of legged locomotion. In this study, we quantify the natural variability of hexapedal walking and climbing in insects, drawing from a database of several thousand steps recorded over two hours of walking time. Results: We show that the range of step length used by unrestrained climbing stick insects is large, showing that step length can be changed substantially for adaptive locomotion. Step length distributions were always bimodal, irrespective of leg type and walking condition, suggesting the presence of two distinct classes of steps: short and long steps. Probability density of step length was well-described by a gamma distribution for short steps, and a logistic distribution for long steps. Major coefficients of these distributions remained largely unaffected by walking conditions. Short and long steps differed concerning their spatial occurrence on the walking substrate, their timing within the step sequence, and their prevalent swing direction. Finally, ablation of structures that serve to improve foothold increased the ratio of short to long steps, indicating a corrective function of short steps. Conclusions: Statistical and functional differences suggest that short and long steps are physiologically distinct classes of leg movements that likely reflect distinct control mechanisms at work.