Planning actions with a magnetic tool: how initial tool orientation and number of functional ends influence motor planning abilities in capuchin monkeys (Sapajus spp.).

The way in which animals grasp objects to perform subsequent action execution allows studying their anticipatory abilities. We examined whether 11 capuchin monkeys (Sapajus spp.) were able to prospectively grasp a magnetic dowel to use it as a tool to retrieve a baited metallic container from a plexiglas box placed in front of them. We investigated whether and how initial dowel orientation (horizontal vs vertical) affected grasping and using the dowel to retrieve the container in two testing conditions: (1) 2-FE condition in which the dowel had two functional magnetic ends; (2) 1-FE condition in which the dowel had only one functional magnetic end. In the 2-FE condition, capuchins had to take into account the initial dowel orientation since both ends were functional, whereas in the 1-FE condition capuchins had also to take into account the initial functional end position when grasping the dowel. Capuchins were trained to grasp the dowel to put one functional end in contact with the metallic container. However, they did not learn to associate the functional end of the 1-FE dowel to successful retrieval. Capuchins showed better anticipatory planning (1) in 2-FE than in 1-FE condition and (2) when the dowel was initially positioned on the horizontal plane than on the vertical one. Moreover, hand preferences affected planning in the 1-FE condition. Results were discussed within the frameworks of primates' abilities to use abstract cues and on their abilities to process functional features and spatial cues and to perform mental rotations.

Anticipating future actions: Motor planning improves with age in wild bearded capuchin monkeys (Sapajus libidinosus).

Self-directed object manipulation tasks illuminate development of motor planning. Grasping strategies that lead to good object control to perform the following action(s) reveal second-order motor planning. Motor planning for efficient grips develops slowly in children. Age-related differences in other primates have been poorly investigated. Here, we investigated anticipatory motor planning of infant, juvenile and adult wild capuchin monkeys grasping a horizontally positioned stick baited to the left or right side (a version of the elevated spoon task). We recorded the grasps capuchins used to bring the baited end of the stick to the mouth. The percentage of efficient radial grips positively correlated with age and adults used efficient grips significantly more frequently than infants. Adult wild capuchins' use of radial grips was higher than that reported for adult captive capuchins in similar tasks, suggesting that experience throughout life may influence motor anticipation. Self-directed object manipulation tasks will be useful to compare this aspect of cognition across primates. A video abstract of this article can be viewed at https://youtu.be/a1Zbr_AQkb8.

Versatile grasping ability in power-grip actions by tufted capuchin monkeys (Sapajus spp.).

OBJECTIVES: Capuchin monkeys are well known to have a high degree of manual dexterity. In this study, we assessed the variability of capuchin grasping actions involving power grips, i.e., manual actions in which the object is grasped between the palm and one or several parts of the fingers and that do not necessarily involve individually controlled finger movements. Planning abilities in executing actions were also evaluated. METHODS: Twenty tufted capuchins (Sapajus spp.) were tested in a task requiring individuals to grasp a dowel inserted into a vertical tube. We examined their grasping techniques, focusing on the following aspects: (i) the different hand postures made during grasping, (ii) the frequency of thumb use in opposition to the other fingers, (iii) the asymmetric use of the hands, and (iv) the configuration of the grasping action for the purpose of comfortably bringing the food to the mouth. RESULTS: Eight power-grip variants were identified, with individual capuchins performing an average of more than five different grips. The use of the thumb in opposition to the other areas of the hand, as reported in studies of precision grips, also appears to be a common feature in power grips. No evidence of group-level manual asymmetries was found. Adult capuchins were better than immature individuals in planning grasping actions in relation to following task demands. DISCUSSION: Overall, these findings clarify the extent to which manual dexterity and cognitive abilities can be expressed in the grasping tasks of highly manually skilled primate species.

Exploration and learning in capuchin monkeys (Sapajus spp.): the role of action-outcome contingencies.

Animals have a strong propensity to explore the environment. Spontaneous exploration has a great biological significance since it allows animals to discover and learn the relation between specific behaviours and their consequences. The role of the contingency between action and outcome for learning has been mainly investigated in instrumental learning settings and much less in free exploration contexts. We tested 16 capuchin monkeys (Sapajus spp.) with a mechatronic platform that allowed complex modules to be manipulated and to produce different outcomes. Experimental subjects could manipulate the modules and discover the contingencies between their own specific actions and the outcomes produced (i.e., the opening and lighting of a box). By contrast, Control subjects could operate on the modules, but the outcomes experienced were those performed by their paired Experimental subjects ("yoked-control" paradigm). In the exploration phase, in which no food reward was present, Experimental subjects spent more time on the board and manipulated the modules more than Yoked subjects. Experimental subjects outperformed Yoked subjects in the following test phase, where success required recalling the effective action so to open the box, now baited with food. These findings demonstrate that the opportunity to experience action-outcome contingencies in the absence of extrinsic rewards promotes capuchins' exploration and facilitates learning processes. Thus, this intrinsically motivated learning represents a powerful mechanism allowing the acquisition of skills and cognitive competence that the individual can later exploit for adaptive purposes.

Understanding the functional properties of tools: chimpanzees (Pan troglodytes) and capuchin monkeys (Cebus apella) attend to tool features differently.

We examined whether eight capuchins and eight chimpanzees were able to retrieve a reward placed inside a tube, of varying length, by selecting the correct stick from different sets of three sticks differing in length (functional feature) and handle (non-functional feature). Moreover, to investigate whether seeing the stick inside the tube (visual feedback) improves performance, half of the subjects were tested with a transparent apparatus and the other half with an opaque apparatus. Phase 1 included (a) Training 1 in which each stick had a different handle and (b) Transfer 1 in which the handles were switched among sticks, so that the functional tool had the same length but a different handle than before. The seven chimpanzees and one capuchin that passed Transfer 1 received Transfer 2. The other subjects received (a) Training 2, which used the same sticks from Phase 1 with handles switched in every trial, and (b) Transfer 2 in which the tube was longer, all sticks had the same new handle, and the formerly longest tool became intermediate in length. Eight chimpanzees and three capuchins passed Transfer 2. Results showed that (1) chimpanzees applied relational structures in tool using tasks more quickly than capuchins and (2) capuchins required more varied experience to attend to the functional feature of the tool. Interestingly, visual feedback did not improve performance in either species.

Food transfers in capuchin monkeys: an experiment on partner choice.

Although most primates live in groups, experiments on reciprocity usually test individuals in dyads. This could hide the processes emerging in richer social settings, reducing the ecological validity of the results. We run an experiment on reciprocal food transfers testing capuchin monkeys (Cebus apella) in triads, so that subjects could choose to allow access to their food to either of their two partners. We tested the hypothesis that partner choice was related to a comparison of long-term social bonds with the two partners, more than to a comparison of recent food transfer events from the two partners. The results confirmed this hypothesis, thus supporting the notion that reciprocal partner preferences are based on long-term accounts of benefits that have been exchanged.

A mechatronic platform for behavioral analysis on nonhuman primates.

In this work we present a new mechatronic platform for measuring behavior of nonhuman primates, allowing high reprogrammability and providing several possibilities of interactions. The platform is the result of a multidisciplinary design process, which has involved bio-engineers, developmental neuroscientists, primatologists, and roboticians to identify its main requirements and specifications. Although such a platform has been designed for the behavioral analysis of capuchin monkeys (Cebus apella), it can be used for behavioral studies on other nonhuman primates and children. First, a state-of-the-art principal approach used in nonhuman primate behavioral studies is reported. Second, the main advantages of the mechatronic approach are presented. In this section, the platform is described in all its parts and the possibility to use it for studies on learning mechanism based on intrinsic motivation discussed. Third, a pilot study on capuchin monkeys is provided and preliminary data are presented and discussed.

Tool choice on the basis of rigidity in capuchin monkeys.

Wild capuchin monkeys select stone tools to crack open nuts on the basis of their weight and friability, two non-visual functional properties. Here, we investigated whether they would select new stick-like tools on the basis of their rigidity. In Experiment 1, subjects faced an out-of-reach reward and a choice of three unfamiliar tools differing in color, diameter, material, and rigidity. In order to retrieve the reward, capuchins needed to select the rigid tool exemplar. Capuchins gathered information regarding tools' pliability either by (1) manipulating the tools themselves (manipulation condition), (2) observing a human demonstrator repeatedly bending the tools (observation condition), or (3) seeing the tools placed on a platform without any manipulation taking place (visual static condition). Subjects selected the rigid tool above chance levels in both the manipulation and observation conditions, but not in the visual static condition. In Experiment 2, subjects needed to select and use a flexible tool to access a liquid reward (as opposed to the rigid tool, as in previous experiment). Again, capuchins selected above chance levels the appropriate tool (i.e., flexible), thus demonstrating a good appreciation of the relation between the tool properties and the task requirements.

Great apes (Pan troglodytes, Pan paniscus, Pongo abelii) exploit better the information of failure than capuchin monkeys (Sapajus spp.) when selecting tools to solve the same foraging problem.

In a previous study, chimpanzees, bonobos, orangutans, and capuchin monkeys faced a task that required the use of a rigid stick-like tool to displace an out-of-reach food reward, which was located outside the cage either hanging on a string (e.g., apes) or on a table (e.g., capuchins). Three unfamiliar stick-like tools were placed on a wooden platform for the subjects to choose. Testing consisted of two consecutive trials, each with the same set of tools. Previous to the test subjects learned about the rigidity of the tool either by handling the tools (manipulation), or by observing an experimenter bending and unbending them in sequence (observation); or did not receive any information since the three tools were presented lying on the platform (visual static). In the current study, we investigated whether failing to select the right type of tool in the first trial affected subjects' choices in the second trial. Results showed that when information about the tool rigidity was obtained before selection, great apes and capuchin monkeys changed options in their second choices. However, in the visual static condition, where no information about the rigidity of the tools had been provided before their selection, only great apes discarded wrong tool exemplars in their second trials benefitting from their own mistakes. In contrast, capuchin monkeys did not. We argue that lower attentional focus and lack of stimuli distinctiveness might account for capuchins monkeys' failure to benefit from their own experience. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Inferences about the location of food in capuchin monkeys (Cebus apella) in two sensory modalities.

The authors tested the ability of capuchin monkeys (Cebus apella) to make inferences about hidden food. In Experiment 1, we showed the content of 2 boxes, 1 of which was baited (visual condition, VC) or we shook both boxes producing noise from the baited box (auditory condition, AC). Seven subjects (out of 8) were above chance in the VC, whereas only 1 was above chance in AC. During treatment, by manipulating empty and filled objects subjects experienced the relation between noise and content. When tested again, 7 capuchins were above chance in the VC and 3 in AC. In Experiment 2, we gave visual or auditory information only about the empty box and, consequently, successful choice implied inferential reasoning. All subjects (out of 4) were above chance in the VC, and 2 in the AC. Control tests ruled out the possibility that success resulted from simply avoiding the shaken noiseless box, or from the use of arbitrary auditory information. Similar to apes (Call, 2004), capuchins were capable of inferential reasoning.

Motor planning in different grasping tasks by capuchin monkeys (Sapajus spp.).

Studies on motor planning and action selection in object use reveal that what we choose to do in the present moment depends on our next planned action. In particular, many studies have shown that adult humans initially adopt uncomfortable hand postures to accommodate later task demands (i.e., the end-state comfort effect). Recent studies on action planning in different non-human primates species have provided contrasting results. Here, we tested whether capuchin monkeys (Sapajus spp.), natural tool users, would show planning abilities in two tasks with varying complexity: (i) an object-retrieval task involving self-directed actions (Experiment 1) and (ii) a tool-using task involving actions directed toward an external target (Experiment 2). In Experiment 1, six of 10 monkeys preferentially used a radial grip (i.e., with the thumb-side oriented towards the baited end) to grasp a horizontal dowel with either the left- or right-end baited and bring it to their mouth. In Experiment 2, all six tested capuchins preferentially used a radial grip (i.e., with the thumb-side oriented towards the center of the dowel) to grasp a dowel that was positioned horizontally at different orientations and to dislodge an out-of-reach food reward. Thus, we found that the capuchins showed second-order planning abilities in both tasks, but performance differences emerged in relation to hand preference and learning across sessions. Our findings support the idea that second-order motor planning occurred in an early stage of the primate lineage. Factors affecting the ability of nonhuman primates to estimate motor costs in action selection are discussed.

Preferences towards novel foods in Cebus apella: the role of nutrients and social influences.

Information on the process of preference acquisition towards novel foods in nonhuman primates is lacking. This study aims to assess (1) whether nutrient and energy contents affect preferences towards novel foods encountered repeatedly by individuals when alone, (2) whether these preferences change after additional encounters with the novel foods, and (3) if the change is sensitive to social influences. We presented seven novel foods to 26 socially housed tufted capuchins. In Phase 1, each subject was presented individually with the 21 possible binary combinations of the seven novel foods. Afterwards, during treatment, 13 subjects received the novel foods ad libitum with their group members (social condition) and 13 subjects received the foods individually (individual condition); subjects assigned to the individual and social conditions had shown similar food preferences in Phase 1. Finally, in Phase 2, each subject was presented again with 21 binary choices between each of the novel foods. In Phases 1 and 2, the number of times each food was chosen differed among foods. In Phase 1, food preference correlated positively with glucose and fructose and negatively with total fiber content. In Phase 2, irrespective of social or individual prior experience in the treatment condition, food preference changed and became correlated with total energy content. Our results broaden the findings already available for familiar foods by demonstrating that individual experience based on the feedback obtained from novel foods guides the establishment of preferences towards them. Moreover, individual experience is sufficient to determine food preferences similar to those individuals may acquire when together with group members eating the same foods.

Abstract knowledge in the broken-string problem: evidence from nonhuman primates and pre-schoolers.

There is still large controversy about whether abstract knowledge of physical problems is uniquely human. We presented 9 capuchin monkeys, 6 bonobos, 6 chimpanzees and 48 children with two versions of a broken-string problem. In the standard condition, participants had to choose between an intact and a broken string as means to a reward. In the critical condition, the functional parts of the strings were covered up and replaced by perceptually similar, but non-functional cues. Apes, monkeys and young children performed significantly better in the standard condition in which the cues played a functional role, indicating knowledge of the functional properties involved. Moreover, a control experiment with chimpanzees and young children ruled out that this difference in performance could be accounted for by differences of perceptual feedback in the two conditions. We suggest that, similar to humans, nonhuman primates partly rely on abstract concepts in physical problem-solving.

Response toward novel stimuli in a group of tufted capuchins (Cebus libidinosus) in Brasília National Park, Brazil.

We investigated responses toward novel foods and novel objects by wild capuchins that routinely exploit visitors' foods in Brasília National Park. Given the capuchins' daily exposure to human foods and objects, we expected them to be more explorative toward novel foods and objects compared to capuchins that are not habituated to visitors. However, since the safety and palatability of potential foods have to be learned, we also expected the capuchins to be cautious about eating novel foods, as has been reported for wild and captive capuchins. Stimuli were presented on a platform in four experimental conditions: familiar food (FF), novel food (NF), familiar food plus novel object (FF+O), and novel food plus novel object (NF+O). Latencies to approach and contact the platform, and to approach and to ingest food did not differ across conditions. Nevertheless, the capuchins were significantly more responsive (measured in terms of interest, manipulation, etc.) toward familiar foods than novel foods, and ate significantly more of the former. In other words, their explorative response toward novel foods led to little consumption. Our results do not support the "readiness to eat" hypothesis, according to which a lower readiness to eat and food neophobia are the consequences of the presence of a distracting novel object. The finding that capuchins explore novel stimuli but remain cautious about eating novel foods supports the view that neophilia and neophobia are motivationally independent responses.