Experimental evidence for heterospecific alarm signal recognition via associative learning in wild capuchin monkeys

Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator–sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s10071-019-01264-3) contains supplementary material, which is available to authorized users.