Capuchins, space, time and memory: an experimental test of what-where-when memory in wild monkeys.

There is considerable controversy about the existence, extent and adaptive value of integrated multimodal memory in non-human animals. Building on prior results showing that wild capuchin monkeys in Argentina appear to recall both the location and amount of food at patches they had previously visited, I tested whether they also track and use elapsed time as a basis for decisions about which feeding patches to visit. I presented them with an experimental array of eight feeding sites, at each of which food rewards increased with increasing elapsed time since the previous visit, similar to the pattern of ripe fruit accumulation in natural feeding trees. Over the course of 68 days, comprising two distinct renewal rate treatments, one group repeatedly visited sites in the feeding array, generating 212 valid choices between sites. Comparison of observations against simulated movements and multinomial statistical models shows that the monkeys' choices were most consistent with dynamic memory for elapsed time specific to each of the eight sites. Thus, it appears that capuchin monkeys possess and use integrated memories of prior food patch use, including where the patch is relative to their current location, how productive the patch is and how long it has been since they last visited the patch. Natural selection to use such integrated memories in foraging tasks may provide an ecologically relevant basis for the evolution of complex intelligence in primates.