Habituation under natural conditions: model predators are distinguished by approach direction

Abstract

Habituation is an active process that allows animals to learn to identify repeated, harmless events, and so could help individuals deal with the trade-off between reducing the risk of predation and minimizing escape costs. Safe habituation requires an accurate distinction between dangerous and harmless events, but in natural environments such an assessment is challenging because sensory information is often noisy and limited. What, then, comprises the information animals use to recognize objects that they have previously learned to be harmless? We tested whether the fiddler crab Uca vomeris distinguishes objects purely by their sensory signature or whether identification also involves more complex attributes such as the direction from which an object approaches. We found that crabs habituated their escape responses after repeated presentations of a dummy predator consistently approaching from the same compass direction. Females habituated both movement towards the burrow and descent into the burrow, whereas males only habituated descent into the burrow. The crabs were more likely to respond again when a physically identical dummy approached them from a new compass direction. The crabs distinguished between the two dummies even though both dummies were visible for the entire duration of the experiment and there was no difference in the timing of the dummies' movements. Thus, the position or approach direction of a dummy encodes important information that allows animals to identify an event and habituate to it. These results argue against the traditional notion that habituation is a simple, nonassociative learning process, and instead suggest that habituation is very selective and uses information to distinguish between objects that is not available from the sensory signature of the object itself.