Stereotypic leg searching movements in the stick insect: kinematic analysis, behavioural context and simulation

Abstract

Insects are capable of efficient locomotion in a spatially complex environment, such as walking on a forest floor or climbing in a bush. One behavioural mechanism underlying such adaptability is the searching movement that occurs after loss of ground contact. Here, the kinematic sequence of leg searching movements of the stick insect Carausius morosus is analysed. Searching movements are shown to be stereotypic rhythmic movement sequences consisting of several loops. The typical loop structure allows the mean tarsus trajectory to be calculated using a feature-based averaging procedure. Thus, it is possible to describe the common underlying structure of this movement pattern. Phase relationships between joint angles, analysed for searching front legs, indicate a central role for the thorax-coxa joint in searching movements. Accordingly, the stereotyped loop structure of searching differs between front-, middle- and hindlegs, with leg-specific patterns being caused by differing protraction/retraction movements in the thorax-coxa joint. A simple artificial neural network that had originally been devised to generate simple swing movements allows two essential features of empirical searching trajectories to be simulated: (i) cyclic movements and (ii) the smooth transition into a search trajectory as a non-terminated swing movement. It is possible to generate several loops of a middle-leg search, but the precise size and shape of the loops fall short of a real-life approximation. Incorporation of front-leg retraction or hind-leg protraction during searching will also require an extension to the current model. Finally, front-leg searching occurs simultaneously with antennal movements. Also, because leg searching movements are a local behaviour, the legs remaining on the ground continue their stance phase, causing a forward shift of the body, including the searching leg. As a result of this shift, the centre of the searched space is close to the anterior extreme position of the tarsus during walking, representing the location of most likely ground contact according to past experience. Therefore, the behavioural relevance of searching movements arises from the combined actions of several limbs.