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\u27 ability to solve a size discrimination problem is influenced by the type of procedure used to present the problem. Capuchins\u27 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

Stratégies de déplacement et mécanismes décisionnels lors du fourragement chez les primates

Chercher sa nourriture s'avère coûteux et potentiellement exigeant cognitivement, notamment pour des animaux comme les primates, vivant dans un environnement difficilement prévisible. Les fruits étant une ressource éphémère, un régime alimentaire frugivore implique des capacités cognitives élevées. Cette étude comparative s'intéresse aux différentes stratégies mises en place lors du fourragement chez trois espèces de primates (Macaca tonkeana=5, M. fascicularis=3 and Sapajus sp.=6) vivant dans des parcs boisés, au Centre de Primatologie de l'Université de Strasbourg. Ces conditions d'hébergement en semi-liberté nous ont permis de manipuler l'environnement afin de simuler la répartition saisonnière spatio-temporelle des fruits en milieu naturel. Nous avons notamment fait varier la disponibilité de différents fruits chaque semaine avec un rythme saisonnier d'un mois, répété pendant quatre mois. Notre protocole expérimental vise à évaluer le poids des variables Où (localisation, tâche « Fourragement Spatial »), Quoi (distribution, tâches « Groupé vs. Dispersé » et qualité, tâche « Groupé vs. Qualité »), et Quand (disponibilité) sur les décisions individuelles lors de la recherche de nourriture. Nous avons utilisé 42 boîtes à ouverture télécommandée, fixées sur des arbres de l'enclos des singes, dans lesquelles nous avons placé des fruits. Ce dispositif a permis de tester les sujets individuellement dans leur groupe social. Pour chaque essai, nous avons enregistré les trajectoires des sujets, l'ordre des boîtes visitées et la présence de congénères. Dans la tâche « Fourragement Spatial », nous avons comparé les trajectoires observées des essais dans lesquels les sujets ont visité toutes les boites (Ntot=77) avec des trajectoires simulées pour trois stratégies : optimale, de proche en proche, ou aléatoire. Aucune espèce n'a suivi une stratégie aléatoire, les capucins suivent fréquemment une trajectoire optimale, les macaques fascicularis suivent davantage une stratégie de proche en proche alors que les Tonkeans suivent les deux stratégies avec des fréquences similaires. Toutes les espèces ont adopté soit une stratégie globale (trajet optimal) soit une stratégie locale (boite la plus proche) afin de fourrager efficacement. Les expériences de la tâche « Groupé vs. Dispersé » proposent aux animaux de choisir parmi des boîtes dont la répartition spatiale forme deux patchs de nourriture de six boites chacun, l'un groupé, l'autre dispersé. Nous avons testé l'effet de cette distribution spatiale en utilisant les mêmes fruits dans les deux patchs (Nobs=2477). Nos résultats indiquent une préférence pour la distribution groupée (vs. dispersée) chez les trois espèces. Nous avons également testé l'effet de la qualité de la nourriture (tâche « Groupé vs. Qualité ») en proposant deux fruits différents disponibles en même temps, le préféré dans la distribution dispersée vs. le moins préféré dans la distribution groupée (Nobs=2546). Les trois espèces ont continué de choisir préférentiellement la distribution groupée, mais les Tonkeans dans une moindre mesure que les capucins, ce qui indique que la qualité influence également leurs choix. Les Tonkeans ont aussi montré des déplacements plus directs. Enfin, pour la composante Quand, les sujets ont bien adapté leur fourragement à la séquence temporelle de la disponibilité alimentaire, répétée quatre fois, mais des hypothèses alternatives peuvent expliquer ces résultats (e.g. capacité à reconnaitre les boîtes disponibles). Cette étude montre que toutes les espèces utilisent des stratégies de fourragement efficaces. Cependant, contrairement aux omnivores, les frugivores ont davantage pris en compte leurs préférences alimentaires et ont montré des déplacements plus directs vers les sites alimentaires. Cette étude souligne que les contraintes écologiques des espèces peuvent affecter l'évolution des capacités cognitives et, plus généralement, des comportements.Foraging can be a challenging activity, especially for animals like primates living in seasonal environments characterised by not fairly predictable food availability. Since fruit is an ephemeral resource, a frugivorous diet is associated to brain size and high cognitive abilities. This comparative study aims to investigate the spatial foraging strategies of three primate species (Macaca tonkeana=5 individuals, M. fascicularis=3 and Sapajus sp.=6) having different degree of frugivory and living in semi-free ranging conditions at the Primate Centre of Strasbourg University. The experimental protocol aims to assess the relative weight of Where (food location, Spatial Foraging Task), Where vs. What (food distribution, Clumped vs. Scattered Tasks and quality, Clumped vs. Quality Task) and When (food temporal availability) variables on the individual foraging decisions. Forty-two boxes were fixed on trees in the outdoor area and were lockable via a remote-control system to individually test subjects in their social group. Each week, a subset of boxes was filled with one/two appealing fruit types; a seasonal pace of one month was repeated for four months to mimic the seasonality of wild fruit. We recorded subjects' trajectories, the order of visited boxes and the presence of other individuals. In the Spatial Foraging Task, considering the trials in which subjects visited all six baited boxes (Tonkeans Ntrials=35, long-tailed macaques Ntrials=31, capuchins Ntrials=11), we compared the observed routes to simulated routes under three strategies: optimal route, nearest neighbour rule, random route. None of the species choose random routes, suggesting that they relied on spatial memory to visit food sites. Capuchins optimized more their travels than long-tailed macaques, which followed mainly a nearest neighbour strategy, while Tonkeans used both strategies at similar frequency. All study species used a global (optimal path) or local strategy (nearest-neighbour rule) to forage efficiently. In the Clumped vs. Scattered Tasks, we tested how the food distribution influences primate spatial foraging. In the Clumped vs. Scattered Task 1, 12 boxes were baited with the same fruit type, six boxes in a circular clumped distribution and other six in a scattered circle. The Task 2 provided a similarly preferred fruit in the same two circular configurations but with opposite reciprocal spatial positions in terms of the side of the outdoor area. All study species (Nvisited boxes=2477) visited at first significantly more the clumped distribution. In the Clumped vs. Quality Task, we assessed the relative impact of food preference versus food distribution: boxes had the similar spatial configuration of the Clumped vs. Scattered Task 1 but the scattered distribution was filled with the most favourite fruit and the clumped one with the least preferred fruit. All species (Nvisited boxes=2546) showed again a preference for visiting first the boxes of the clumped distribution, but the most frugivorous species, Tonkeans, showed a less strong preference compared to the least frugivorous, the capuchins. The higher was the frugivory degree of the species, the higher were the goal-directed travels. Lastly, to investigate if primates developed a temporal knowledge of fruit availability, we investigated if they correctly remembered food spatio-temporal availability: primates visited each month between 79%-98% of baited boxes/tot boxes visited, even if this positive result could be explained by alternative hypothesis (e.g. ability in detecting the available boxes). All primate species maximised foraging efficiency, avoiding random walks. However, frugivorous species took food preference into account in their decisions and showed significantly more goal-directed movement. This study underlines how species feeding ecology may affect the evolution of their abstract mental abilities and more in general, their behaviour

Playing hide and seek with primates: A comparative study of Theory of Mind

The ability to anticipate how another individual will behave is a critical skill in the animal kingdom. Humans typically deal with this problem using their Theory of Mind (ToM), i.e. the ability to decipher beliefs and intentions of others. Although non-human primates (apes in particular) exhibit elaborate social behavior, there is no established consensus on whether this mirrors some form of sophisticated ToM. We suggest that ToM sophistication can be operationally defined in terms of the depth of recursive beliefs, as in "I think that you think that I think...". Importantly, mutual social interactions may call for highly recursive beliefs: not only do I think that you think, but I also think that you think that I think... This study aims at comparing how primate species (including humans) differ with respect to this form of ToM sophistication. The main novelty of our experimental approach is to estimate each primate’s ToM sophistication from its performance in repeated interactive games that are calibrated using information theoretic models of (artificial) recursive ToM. We first validated our model in human subjects and then tested 6 species of captive non-human primates (3 species of great apes: orangutans, gorillas, chimpanzees, and 3 species of old-world monkeys: lion-tailed macaques, rhesus macaques and collared mangabeys) in an adaptation of the task used in the human study. Our paradigm consisted in a “hide and seek” game in which individuals played against a human opponent (a familiar zoo keeper). In each trial, the individual had to infer where food had been hidden by the experimenter opponent (either in his right or left hand). In fact, the location of the food was chosen by learning algorithms, some of which endowed with artificial ToM. Critically, we varied the sophistication of these algorithms, yielding three conditions, ranging from a control (a simple random biased sequence) to a mildly sophisticated ToM agent (1-ToM). The profile of primates’ performances against the different algorithms was then used to infer their ToM sophistication. Preliminary results show that the pattern of performance of nonhuman primates differ from those of humans. Although most nonhuman primates tended to win in the control condition, they lost against the 1-ToM agent, in contrast to the human group (that won). Surprisingly, comparing the performances between the non-human primates' species did not reveal any significant inter-species difference. Therefore, great apes did not perform better than monkeys in our task. Interestingly, variability in the performances actually seems more to rely on inter-individual differences rather than on inter-species differences. Moreover, in every species, at least one individual exhibited mild (but statistically significant) ToM sophistication. Taken together, these data indicate that the distribution of ToM sophistication within each of these non-human primate species is quite heterogeneous. Further analyses are in progress to identify predictive factors (e.g. familiarity with humans, age, motivation and frustration during the game) that could explain away inter-individual differences, thus eventually revealing (or not) inter‑species differences [Authors Aurore San‑Galli and Marie Devaine contributed equally to this work]

Experimental apparatuses.

<p>(a) Experimental apparatus used in the <i>Food</i> condition of Experiment 1 and in the <i>Object</i> condition of Experiment 2; (b) Experimental apparatus used in the <i>Image</i> condition of Experiment 1.</p

Data from: 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 (Nindiv=5; Ntrials=430), M. fascicularis (Nindiv=3; Ntrials=168) and Sapajus apella (Nindiv=6; Ntrials=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 likely maximised foraging efficiency regardless of their degree of frugivory. Our findings emphasise that the food type and distribution may be a preponderant driver in cognitive evolution

Stimulus sets.

<p>(a) Stimuli used in the <i>Food</i> condition of Experiment 1 were a pair of salted sticks of different lengths and a pair of wafers of different diameters; (b) Stimuli used in the <i>Image</i> condition of Experiment 1 were a pair of lines of different lengths and a pair of circles of different diameters; (c) Stimuli used in the <i>Object</i> condition of Experiment 2 were a pair of wooden sticks of different lengths and a pair of wooden spheres of different diameters.</p

Monkeys’ performance in Experiment 2.

<p>Monkeys’ performance in the <i>Object</i> condition as a function of stimulus shape (rods and spheres) was reported considering: (a) the number of trials to achieve the learning criterion (mean ± SE); and (b) the mean percentage of correct responses in the last three training sessions (mean ± SE).</p

Data set Trapanese et al_Where and What

This Excel file contains the raw data of each species (Tonkean macaques, long-tailed macaques, capuchin monkeys) for each task/season (CvS1, CvS2, CvQ)

Intel, Guadalajara Design Center

Proyecto de Aplicación Profesional realizado en la empresa Intel en el área de Makers, en la que se trabajó en la coordinación, planeación y difusión de proyectos. Además, se laboró como el encargado del laboratorio de Proof of Concept

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

International audienceTheory 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