Nocturnal navigation by whip spiders: antenniform legs mediate near-distance olfactory localization of a shelter

Abstract

Navigation by terrestrial arthropods that wander away from a shelter in search of food or mates in uncluttered environments invariably relies on path integration mechanisms, which provide distance and direction information used to compute a straight-line return trajectory. Navigation in cluttered habitats is more typically visually guided, even in species that are nocturnal. Nocturnal, tropical arachnids in the order Amblypygi, however, depend neither on path integration nor on vision to navigate and are hypothesized to instead rely on highly sensitive olfactory structures. The distal articles of their antenniform legs are covered with receptors that presumably bind the odour stimuli thought to control, at least in part, their impressive ability to relocate a shelter after they wander in a rainforest understory. To test the hypothesis that olfactory inputs from the antenniform legs support their near-distance ability to localize a shelter, we conducted a laboratory experiment with the amblypygid Phrynus marginemaculatus in which an olfactory cue (with contact chemoreception precluded) identified the location of a shelter, the position of which was varied as subjects were trained. Localization of a shelter was readily learned and performance was fully retained over a 2-week period in which subjects were not trained. Localization of the odour-cued shelter declined markedly, however, when the distal articles of the antenniform legs were amputated. Moreover, the residual discrimination ability displayed by subjects when they were subsequently retrained depended on how many olfactory receptors had been removed. The results clearly demonstrate that odour cues can support near-distance goal localization and that receptors on the antenniform legs are the locus of the peripheral neural transduction necessary when odour is used to identify the position of a shelter.