Do primates flexibly use spatio-temporal cues when foraging?

Foraging in seasonal environments can be cognitively demanding. Comparative studies have associated large brain size with a frugivorous diet. We investigated the ability of three semi-free-ranging primate species with different degrees of frugivory (Ntrials: Macaca tonkeana = 419, Macaca fascicularis = 197, Sapajus apella = 346) in developing a mental representation of the spatio-temporal distribution of food using foraging experiments. Forty-two boxes were fixed on trees, and each week ("season"), some of them were filled with fruits which were either highly preferred, or less preferred. Spatial (geometrical panels) and temporal (peel skin of the available fruit) cues were present at each season to indicate where (food location), what (which food) was available, and when. To test the flexible use of the cues in primate foraging behaviour, we first removed the spatial and temporal cues one at a time, and then, we manipulated the "seasonal" order of the available fruit. We compared the foraging performances in the absence and the presence of the cues and during the usual and unusual seasonal order. The average proportion of baited boxes chosen by the subjects in presence of both cues was high (between 73% and 98%) for all species. The primates seemed to remember the spatio-temporal food availability (or used other cues) because no difference was found between trials with or without our spatial and temporal cues. When the usual seasonal pattern was changed, they flexibly adjusted the feeding choice by using the provided temporal cues. We discuss these results also in view of a possible experimental bias.

Prolonged care and cannibalism of infant corpse by relatives in semi-free-ranging capuchin monkeys.

Cannibalism is a quite common behaviour in animals that can have survival value when food is scarce or in the case of overpopulation. Conversely, cannibalism can also increase pathogen transmission and reduce fitness. In primates, some cases of cannibalism are associated with infanticide or are performed by mothers after their newborn has died (filial cannibalism). We report here the first observation of cannibalism, specifically infant cannibalism, in a semi-free-ranging group of brown capuchin monkeys (Sapajus apella). The baby was likely stillborn, as parts of the cranial bones were missing and no fresh injuries were visible. After half a day of taking care of the dead infant, the mother ate part of the corpse's skin and the highly nutritional viscera, possibly thereby compensating for the physiological costs of pregnancy. After attentively watching his mother's behaviour, the older brother of the dead newborn similarly ate parts of the corpse. Although we cannot rule out idiosyncrasy and vertical social transmission, it is possible that cannibalism is a normal-albeit rare-part of the behavioural repertoire of capuchin monkeys.

Where and what? Frugivory is associated with more efficient foraging in three semi-free ranging primate species.

Foraging in seasonal environments can be cognitively challenging. Comparative studies have associated brain size with a frugivorous diet. We investigated how fruit distribution (where) and preference (what) affect foraging decisions in three semi-free ranging primate species with different degrees of frugivory: Macaca tonkeana (N indiv = 5; N trials = 430), M. fascicularis (N indiv = 3; N trials = 168) and Sapajus apella (N indiv = 6; N trials = 288). We used 36 boxes fixed on trees and filled with highly and less preferred fruits with different (weekly) spatio-temporal distributions. Individuals were tested in two conditions: (1) same fruit provided concurrently in the same quantity but in a scattered and in a clumped distribution, (2) highly preferred fruit was scattered while the less preferred was clumped. Generally, primates preferred feeding first on the boxes of the clumped distribution in both conditions, with the more frugivorous species at a higher degree than the less frugivorous species in condition (1), but not (2). Therefore, what fruit was available changed the foraging decisions of the more frugivorous species who also engaged more in goal-directed travel. When feeding on preferred fruit, primates probably maximized foraging efficiency regardless of their degree of frugivory. Our findings emphasize that the food type and distribution may be a preponderant driver in cognitive evolution.

What, where and when: spatial foraging decisions in primates.

When exploiting the environment, animals have to discriminate, track, and integrate salient spatial cues to navigate and identify goal sites. Actually, they have to know what can be found (e.g. what fruit), where (e.g. on which tree) and when (in what season or moment of the year). This is very relevant for primate species as they often live in seasonal and relatively unpredictable environments such as tropical forests. Here, we review and compare different approaches used to investigate primate spatial foraging strategies: from direct observations of wild primates to predictions from statistical simulations, including experimental approaches on both captive and wild primates, and experiments in captivity using virtual reality technology. Within this framework, most of these studies converge to show that many primate species can (i) remember the location of most of food resources well, and (ii) often seem to have a goal-oriented path towards spatially permanent resources. Overall, primates likely use mental maps to plan different foraging strategies to enhance their fitness. The majority of studies suggest that they may organise spatial information on food resources into topological maps: they use landmarks to navigate and encode local spatial information with regard to direction and distance. Even though these studies were able to show that primates can remember food quality (what) and its location (where), still very little is known on how they incorporate the temporal knowledge of available food (when). Future studies should attempt to increase our understanding of the potential of primates to learn temporal patterns and how both socio-ecological differences among species and their cognitive abilities influence such behavioural strategies.

Reading wild minds: A computational assay of Theory of Mind sophistication across seven primate species.

Theory of Mind (ToM), i.e. the ability to understand others' mental states, endows humans with highly adaptive social skills such as teaching or deceiving. Candidate evolutionary explanations have been proposed for the unique sophistication of human ToM among primates. For example, the Machiavellian intelligence hypothesis states that the increasing complexity of social networks may have induced a demand for sophisticated ToM. This type of scenario ignores neurocognitive constraints that may eventually be crucial limiting factors for ToM evolution. In contradistinction, the cognitive scaffolding hypothesis asserts that a species' opportunity to develop sophisticated ToM is mostly determined by its general cognitive capacity (on which ToM is scaffolded). However, the actual relationships between ToM sophistication and either brain volume (a proxy for general cognitive capacity) or social group size (a proxy for social network complexity) are unclear. Here, we let 39 individuals sampled from seven non-human primate species (lemurs, macaques, mangabeys, orangutans, gorillas and chimpanzees) engage in simple dyadic games against artificial ToM players (via a familiar human caregiver). Using computational analyses of primates' choice sequences, we found that the probability of exhibiting a ToM-compatible learning style is mainly driven by species' brain volume (rather than by social group size). Moreover, primates' social cognitive sophistication culminates in a precursor form of ToM, which still falls short of human fully-developed ToM abilities.

Does presentation format influence visual size discrimination in tufted capuchin monkeys (Sapajus spp.)?

Most experimental paradigms to study visual cognition in humans and non-human species are based on discrimination tasks involving the choice between two or more visual stimuli. To this end, different types of stimuli and procedures for stimuli presentation are used, which highlights the necessity to compare data obtained with different methods. The present study assessed whether, and to what extent, capuchin monkeys' ability to solve a size discrimination problem is influenced by the type of procedure used to present the problem. Capuchins' ability to generalise knowledge across different tasks was also evaluated. We trained eight adult tufted capuchin monkeys to select the larger of two stimuli of the same shape and different sizes by using pairs of food items (Experiment 1), computer images (Experiment 1) and objects (Experiment 2). Our results indicated that monkeys achieved the learning criterion faster with food stimuli compared to both images and objects. They also required consistently fewer trials with objects than with images. Moreover, female capuchins had higher levels of acquisition accuracy with food stimuli than with images. Finally, capuchins did not immediately transfer the solution of the problem acquired in one task condition to the other conditions. Overall, these findings suggest that--even in relatively simple visual discrimination problems where a single perceptual dimension (i.e., size) has to be judged--learning speed strongly depends on the mode of presentation.