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

Abstract

SUMMARYHabituation 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 dummiesʼ 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.

Socially learned habituation to human observers in wild chimpanzees

“…In invertebrates, the neurophysiological processes that underlie habituation have also been described (Burrell and Sahley 2001 ). Nonetheless, few studies have focused on habituation conducted in the animal's natural environment, despite the evolutionary relevance of the process (Raderschall et al 2011 ). For wild animals, the tacit assumption has always been that habituation to human observers is, at least partly, caused by the same non-associative learning mechanism as described for laboratory animals.…”

“…For wild animals, the tacit assumption has always been that habituation to human observers is, at least partly, caused by the same non-associative learning mechanism as described for laboratory animals. However, the social environment of wild animals is very different from the conditions under which habituation is typically studied in psychological laboratories (Raderschall et al 2011 ). Importantly, wild animals have active control over their environments and can flexibly influence their exposure to external events, such as the presence of humans.…”

Flicker is part of a multi-cue response criterion in fiddler crab predator avoidance

“…Models were selected by sequentially fitting parameters and including those parameters that reached significance at a 5% level when added to the final model. Because burrow distance (the distance between a crab and its burrow at the time of response) and track distance (the distance between a crab and the closest point of the dummy track) are known to be important predictors of response distance (Hemmi, 2005a;Hemmi, 2005b;Hemmi and Merkle, 2009;Hemmi and Pfeil, 2010;Raderschall et al, 2011), they were included in all models even if they did not reach significance. This was the case in two instances (see Table1), but it did not change the significance of other main effects and never changed the estimate of effect sizes by more than 7%.…”

“…It allows for selective habituation of individual cues while still remaining responsive (Hemmi and Merkle, 2009;Hemmi and Zeil, 2005;Raderschall et al, 2011). If, for instance, the crabs experience strong constant flicker due to jittering leaves of a nearby mangrove tree, they can safely choose to ignore flicker in this part of the visual field and identify predators by their strong motion signature.…”

Differences in the escape response of a grapsid crab in the field and in the laboratory

“…For both species, field research has underscored the critical role of the burrow in predator avoidance (Fathala et al, 2010a,b;Hemmi, 2005a;Hemmi and Zeil, 2003a) and has shown that the escape response habituates (Hemmi and Merkle, 2009;Raderschall et al, 2011;Tomsic et al, 1993Tomsic et al, , 1998. There are, however, differences between the observed behaviours that are significant.…”