Idiothetic orientation of a wandering spider: Compensation of detours and estimates of goal distance

Abstract

The wandering spider Cupiennius salei Keys uses idiothetic orientation, i.e., memorized information about its own previous movements, to retrieve lost prey. Spiders, having been chased away from a prey fly, return to the capture site (the goal) over a distance of more than 75 cm even though all external orientation cues were precluded. This behavior and its sensory basis were examined by varying the proprioceptive and ‘motor command’ inputs to the memory and by ablating particular lyriform slit sense organs on the legs of the spider. The success rate of returns to the goal after rectilinear chases over 6 discrete distances ranging from 20 cm to>41 cm declines with increasing distances. At distances>41 cm, more than 50% of the performances of intact spiders are nevertheless ‘successful’, in that the animals approach the capture site as close as 5 cm (or less). Animals that have been operated on (lyriform organs on all femora destroyed) are much less successful even at short distances. The mean starting angles of the returns by intact spiders and by those operated on do not differ signficantly. ‘Walking error e n’ for each segment of the entire return path shows that intact animals deviate little from the ideal return route and correctly estimate the distance to the goal. The operated spiders tend to drift off the ideal return route, while their distance estimates remain largely accurate. Returns after curvilinear chases through a semicircular corridor do not retrace the curved path; instead the spiders take a shortcut. Of all performances by intact and by control spiders (with sham operations) 85% are successful. By contrast, most of the 8 groups with sensory ablations have a success rate of less than 50%. Compensation for the semicircular detours is not quite complete: the mean starting directions of returns are biased, pointing to the corridor, and the shape of many return paths reflects the curved corridor shape. Spiders with unilateral ablations of their femoral lyriform organs show low success rates only if the operated legs are on the inner curve perimeter during the chase, while their return parameters resemble those of the intact group in the reverse situation (operated legs on outer perimeter). These side-specific ablation effects, which are correlated with the geometrical situation existing while idiothetic information is gathered and memorized, suggest that the idiothetic memory depends at least partly on input from proprioceptors.