Capuchin monkey (Sapajus spp.) diet: current knowledge, gaps, and future directions.

Knowledge of the feeding habits of primate species is important for an understanding of their natural history and ecological interactions between their groups, and their interactions with their environments. Capuchin monkeys (Sapajus spp.) present significant diet flexibility and are a good model for investigating diet diversity between species. We undertook a systematic literature review of publications on the diet of free-living Sapajus spp. groups by using the Web of Science platform. We performed scientometric analyses of the objectives and hypotheses of the reviewed works, identified knowledge gaps, and evaluated the composition of each group's diet. Our results indicate geographic and taxonomic biases among the 59 published studies that we examined. The studies were focused on Sapajus nigritus, Sapajus libidinosus, and Sapajus apella, and undertaken in long-term study sites. Foraging and behavioral aspects of how food is processed were recurring themes. Capuchin monkeys increase their consumption of anthropogenic food according to its supply. Despite the similar objectives of these studies, standardized data collection protocols were not employed. Although Sapajus spp. are widely distributed and are used for cognitive studies, basic aspects of their natural history, such as their diet, remain unknown. We emphasize the importance of undertaking studies on this genus to fill the identified knowledge gaps, and propose that investigations should be carried out on the effects of dietary changes on individuals and groups. We stress that, as the Neotropical region is one of those most affected by anthropogenic impacts, opportunities to study these primates in their natural environments are diminishing daily.

Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Endogenous cortisol correlates with performance under pressure on a working memory task in capuchin monkeys.

Humans often experience striking performance deficits when their outcomes are determined by their own performance, colloquially referred to as "choking under pressure." Physiological stress responses that have been linked to both choking and thriving are well-conserved in primates, but it is unknown whether other primates experience similar effects of pressure. Understanding whether this occurs and, if so, its physiological correlates, will help clarify the evolution and proximate causes of choking in humans. To address this, we trained capuchin monkeys on a computer game that had clearly denoted high- and low-pressure trials, then tested them on trials with the same signals of high pressure, but no difference in task difficulty. Monkeys significantly varied in whether they performed worse or better on high-pressure testing trials and performance improved as monkeys gained experience with performing under pressure. Baseline levels of cortisol were significantly negatively related to performance on high-pressure trials as compared to low-pressure trials. Taken together, this indicates that less experience with pressure may interact with long-term stress to produce choking behavior in early sessions of a task. Our results suggest that performance deficits (or improvements) under pressure are not solely due to human specific factors but are rooted in evolutionarily conserved biological factors.

The use of individual, social, and animated cue information by capuchin monkeys and children in a touchscreen task.

The distinctiveness of human cumulative culture raises the question of whether humans respond differently to information originating from social sources, compared with information from other sources. Further, does any such differential responding set humans apart from other species? We studied how capuchin monkeys and 2- to 5-year-old children used information originating from their own actions, those of a human demonstrator, or an animated cue. This information, presented via a touchscreen, always revealed in the first trial (T1) the reward value (rewarded or unrewarded) of one stimulus from a 2- or 3-item array, and could be used in a follow-up trial (T2) involving the same stimulus array. Two monkeys achieved a level of proficiency indicating their appreciation of the T1-T2 relationship, i.e., reliably repeating rewarded ("win") selections and actively avoiding repetition of unrewarded ("lose") selections well above chance levels. Neither the two task-proficient monkeys nor the children showed overall performance differences between the three source conditions. Non-task-proficient monkeys, by contrast, did show effects of source, performing best with individually-acquired information. The overall pattern of results hints at an alternative perspective on evidence typically interpreted as showing a human advantage for social information use.

Non-human primates use combined rules when deciding under ambiguity.

Decision outcomes in unpredictable environments may not have exact known probabilities. Yet the predictability level of outcomes matters in decisions, and animals, including humans, generally avoid ambiguous options. Managing ambiguity may be more challenging and requires stronger cognitive skills than decision-making under risk, where decisions involve known probabilities. Here we compare decision-making in capuchins, macaques, orangutans, gorillas, chimpanzees and bonobos in risky and ambiguous contexts. Subjects were shown lotteries (a tray of potential rewards, some large, some small) and could gamble a medium-sized food item to obtain one of the displayed rewards. The odds of winning and losing varied and were accessible in the risky context (all rewards were visible) or partially available in the ambiguous context (some rewards were covered). In the latter case, the level of information varied from fully ambiguous (individuals could not guess what was under the covers) to predictable (individuals could guess). None of the species avoided gambling in ambiguous lotteries and gambling rates were high if at least two large rewards were visible. Capuchins and bonobos ignored the covered items and gorillas and macaques took the presence of potential rewards into account, but only chimpanzees and orangutans could consistently build correct expectations about the size of the covered rewards. Chimpanzees and orangutans combined decision rules according to the number of large visible rewards and the level of predictability, a process resembling conditional probabilities assessment in humans. Despite a low sample size, this is the first evidence in non-human primates that a combination of several rules can underlie choices made in an unpredictable environment. Our finding that non-human primates can deal with the uncertainty of an outcome when exchanging one food item for another is a key element to the understanding of the evolutionary origins of economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Capuchin and rhesus monkeys show sunk cost effects in a psychomotor task.

Human decision-making is often swayed by irrecoverable investments even though it should only be based on future-and not past-costs and benefits. Although this sunk cost effect is widely documented and can lead to devastating losses, the underlying psychological mechanisms are unclear. To tease apart possible explanations through a comparative approach, we assessed capuchin and rhesus monkeys' susceptibility to sunk costs in a psychomotor task. Monkeys needed to track a moving target with a joystick-controlled cursor for variable durations. They could stop at any time, ending the trial without reward. To minimize the work required for a reward, monkeys should have always persisted for at least 1 s, but should have abandoned the trial if that did not yield a reward. Capuchin monkeys and especially rhesus macaques persisted to trial completion even when it was suboptimal, and were more likely to complete the trial the longer they had already tracked the target. These effects were less pronounced, although still present, when the change in expected tracking duration was signalled visually. These results show that sunk cost effects can arise in the absence of human-unique factors and may emerge, in part, because persisting can resolve uncertainty.

Cooperative rescue of a juvenile capuchin (Cebus imitator) from a Boa constrictor.

The threat of predation by snakes is considered to have played a significant role in the evolution of primate sensory systems and behavior. However, we know relatively little about individual and group responses given the rarity of observed predation events. Here we report an observed (filmed) predation attempt by an adult Boa constrictor (~ 2 m) on a juvenile white-faced capuchin (Cebus imitator) in the Sector Santa Rosa of the Área de Conservación Guanacaste, Costa Rica. The snake caught the juvenile monkey on the ground during a terrestrial play session. When the victim screamed, the alpha male, alpha female, and another adult female ran to the scene, physically attacked the snake (with bites and hits), and pulled the victim to safety. Most group members participated in the vocal mobbing of the snake both during and after the attack. Based on the outcomes of this predation attempt and published reports of other B. constrictor attacks on primates, the coordinated efforts of ≥ 2 group members is needed for a successful rescue. This observation adds to our growing knowledge of cooperative group behavior and its importance in predator defense.

Capuchin monkey rituals: an interdisciplinary study of form and function.

Many white-faced capuchin monkey dyads in Lomas Barbudal, Costa Rica, practise idiosyncratic interaction sequences that are not part of the species-typical behavioural repertoire. These interactions often include uncomfortable or risky elements. These interactions exhibit the following characteristics commonly featured in definitions of rituals in humans: (i) they involve an unusual intensity of focus on the partner, (ii) the behaviours have no immediate utilitarian purpose, (iii) they sometimes involve 'sacred objects', (iv) the distribution of these behaviours suggests that they are invented and spread via social learning, and (v) many behaviours in these rituals are repurposed from other behavioural domains (e.g. extractive foraging). However, in contrast with some definitions of ritual, capuchin rituals are not overly rigid in their form, nor do the sequences have specific opening and closing actions. In our 9260 h of observation, ritual performance rate was uncorrelated with amount of time dyads spent in proximity but (modestly) associated with higher relationship quality and rate of coalition formation across dyads. Our results suggest that capuchin rituals serve a bond-testing rather than a bond-strengthening function. Ritual interactions are exclusively dyadic, and between-dyad consistency in form is low, casting doubt on the alternative hypothesis that they enhance group-wide solidarity. This article is part of the theme issue 'Ritual renaissance: new insights into the most human of behaviours'.

Assessing the personality structure of wild capuchin monkeys (Sapajus xanthosternos) using trait rating and behavioral coding.

The study of personality in nonhuman primates has increased substantially, but most studies so far have been conducted with captive animals. In addition, few studies investigated the personality of Neotropical (Platyrrhini) monkeys. If we aim at investigating the ecological and social significance of personality in nonhuman primates, conducting studies of wild populations and covering a wide range of taxa is essential. In this study, we analyzed the personality structure of a wild group of Neotropical monkeys, the yellow-breasted capuchin (Sapajus xanthosternos). We adopted two widespread methods: trait rating, using the Hominoid Personality Questionnaire, and behavioral coding, analyzing 13 behaviors and 3 derived variables. We described 3 traits with trait rating, labeled Openness-Neuroticism, Assertiveness, and Attentiveness-Sociability. We also described 3 traits with behavioral coding, labeled Prosociality, Aggressiveness, and Reactivity to Humans. Comparing both methods we found not only broad convergences between the structures obtained (e.g., both showed prosocial and aggressive traits) but also some differences (e.g., Openness-Neuroticism was not clearly defined with behavioral coding), concluding that combining both methods provided complementary findings. Some socioecological variables seem to influence the expression of personality in captive versus wild living monkeys. For example, in our study, assertive individuals were more vigilant, whereas in the studies in captivity, neurotic individuals were more vigilant. These questions highlight the need for more research in wild conditions and enlarging the number of species and populations studied. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Use of social network models to understand play partner choice strategies in three primate species.

Although play is seen in many species, its evolutionary function is still largely unknown. Several relevant, proposed hypotheses (such as the training for the unexpected, self-assessment, social skills, and dominance hierarchy hypotheses) make predictions about how animals should optimally choose their play partners based on their familiarity or other demographic variables. We used a social network approach to analyze focal sample data on brown capuchins (Cebus apella), hamadryas baboons (Papio hamadryas), and diademed sifaka (Propithecus diadema) to understand how these species choose their play partners with respect to demographic variables. Using exponential random graph models (ERGMs), we found that sifaka and capuchins generally tended to play with animals who were similar to them. The baboons were only sensitive to age differences in the formation of strong play relationships. Our data most strongly support the training for the unexpected hypothesis, as according to predictions all species preferred to play with animals who were their close social partners, decreasing the possibility of cheating during play. Through the first application (to our knowledge) of ERGMs to primate behavior, we were able to compare the effects of many demographic variables on the complex, interdependent social structure of primates. Applying this tool to additional groups and species will provide further insight into evolutionary mechanisms of play behavior across taxa.

Body inversion effect in monkeys.

Humans visually process human body images depending on the configuration of the parts. However, little is known about whether this function is evolutionarily shared with nonhuman animals. In this study, we examined the body posture discrimination performance of capuchin monkeys, a highly social platyrrhine primate, in comparison to humans. We demonstrate that, like humans, monkeys exhibit a body inversion effect: body posture discrimination is impaired by inversion, which disrupts the configural relationships of body parts. The inversion effect in monkeys was observed when human body images were used, but not when the body parts were replaced with cubic and cylindrical figures, the positions of the parts were scrambled, or only part of a body was presented. Results in human participants showed similar patterns, though they also showed the inversion effect when the cubic/cylindrical body images were used. These results provide the first evidence for configural processing of body forms in monkeys and suggest that the visual attunement to social signals mediated by body postures is conserved through the evolution of primate vision.

(Ir)rational choices of humans, rhesus macaques, and capuchin monkeys in dynamic stochastic environments.

Human and animal decision-making is known to violate rational expectations in a variety of contexts. Previous models suggest that statistical structures of real-world environments can favor such seemingly irrational behavior, but this has not been tested empirically. We tested 16 capuchin monkeys, seven rhesus monkeys, and 30 humans in a computerized experiment that implemented such stochastic environments. Subjects chose from among up to three options of different value that disappeared and became available again with different probabilities. All species overwhelmingly chose transitively (A > B > C) in the control condition, where doing so maximized overall gain. Most subjects also adhered to transitivity in the test condition, where it was suboptimal, but ultimately led to negligible losses compared to the optimal, non-transitive strategy. We used a modelling approach to show that differences in temporal discounting may account for this pattern of choices on a proximate level. Specifically, when short- and long-term goals are valued similarly, near-optimal decision rules can map onto rational choice principles. Such cognitive shortcuts have been argued to have evolved to preserve mental resources without sacrificing good decision-making, and here we provide evidence that these heuristics can provide almost identical outcomes even in situations in which they lead to suboptimal choices.

Social modulation of risky decision-making in rats (Rattus norvegicus) and tufted capuchin monkeys (Sapajus spp.).

Both human and non-human animals frequently deal with risky decisions in a social environment. Nevertheless, the influence of the social context on decision-making has been scarcely investigated. Here, we evaluated for the first time whether the presence of a conspecific influences risk preferences in rats and in tufted capuchin monkeys. Subjects received a series of choices between a constant, safe option and a variable, risky option, both alone (Alone condition) and when paired with a conspecific (Paired condition). The average payoff of the risky option was always lower than that of the safe option. Overall, the two species differed in their attitude towards risk: whereas rats were indifferent between options, capuchins exhibited a preference for the safe option. In both species, risk preferences changed in the Paired condition compared to the Alone condition, although in an opposite way. Whereas rats increased their risk preferences over time when paired with a conspecific, capuchins chose the risky option less in the Paired condition than in the Alone condition. Moreover, whereas anxiety-like behaviours decreased across sessions in rats, these behaviours where more represented in the Paired condition than in the Alone condition in capuchins. Thus, our findings extends to two distantly-related non-human species the evidence, so far available for human beings, that a decrease in anxiety corresponds to an increase in risk preferences, and vice versa. This suggests that the modulation of risk preferences by social influences observed in rats and capuchin monkeys may rely on a common, evolutionarily ancient, mechanism.

Social inhibition and behavioural flexibility when the context changes: a comparison across six primate species.

The ability to inhibit previously employed strategies and flexibly adjust behavioural responses to external conditions may be critical for individual survival. However, it is unclear which factors predict their distribution across species. Here, we investigated social inhibition and behavioural flexibility in six primate species (chimpanzees, bonobos, orangutans, gorillas, capuchin monkeys and spider monkeys) differing in terms of phylogenetic relatedness, foraging ecology and social organization. Depending on the social context, individuals could maximize their food intake by inhibiting the selection of a larger food reward in one condition (i.e. inhibition), but not in others, which required them to flexibly switching strategies across conditions (i.e. behavioural flexibility). Overall, our study revealed inter-specific differences in social inhibition and behavioural flexibility, which partially reflected differences in fission-fusion dynamics. In particular, orangutans and chimpanzees showed the highest level of inhibitory skills, while gorillas and capuchin monkeys showed the lowest one. In terms of behavioural flexibility, orangutans and spider monkeys were the best performers, while bonobos and capuchin monkeys were the worst ones. These results contribute to our understanding that inhibition and behavioural flexibility may be linked in more complex ways than usually thought, although both abilities play a crucial role in efficient problem solving.

Irrational choice behavior in human and nonhuman primates.

Choice behavior in humans has motivated a large body of research with a focus on whether decisions can be considered to be rational. In general, humans prefer having choice, as do a number of other species that have been tested, even though having increased choice does not necessarily yield a positive outcome. Humans have been found to choose an option more often only because the opportunity to select it was diminishing, an example of a deviation from economic rationality. Here we extend this paradigm to nonhuman primates in an effort to understand the mechanisms underlying this finding. In this study, we presented two groups of laboratory monkeys, capuchins (Cebus apella) and rhesus macaques (Macaca mulatta), as well as human subjects, with a computerized task in which subjects were presented with two differently colored icons. When the subject selected an icon, differing numbers of food pellets were dispensed (or points were assigned), making each icon correspond to a certain level of risk (one icon yielded 1 or 4 pellets/points and the other yielded 2 or 3). Initially, both options remained constantly available and we established choice preference scores for each subject. Then, we assessed preference patterns once the options were not continuously available. Specifically, choosing one icon would cause the other to shrink in size on the screen and eventually disappear if never selected. Selecting it would restore it to its full size. As predicted, humans shifted their risk preferences in the diminishing options phase, choosing to click on both icons more equally in order to keep both options available. At the group level, capuchin monkeys showed this pattern as well, but there was a great deal of individual variability in both capuchins and macaques. The present work suggests that there is some degree of continuity between human and nonhuman primates in the desire to have choice simply for the sake of having choice.

Capuchin monkeys' use of human and conspecific cues to solve a hidden object-choice task.

Learning by watching others can provide valuable information with adaptive consequences, such as identifying the presence of a predator or locating a food source. The extent to which nonhuman animals can gain information by reading the cues of others is often tested by evaluating responses to human gestures, such as a point, and less often evaluated by examining responses to conspecific cues. We tested whether ten brown capuchin monkeys (Cebus [Sapajus] apella) were able to use cues from monkeys and a pointing cue from a human to obtain hidden rewards. A monkey could gain access to a reward hidden in one of two locations by reading a cue from a conspecific (e.g., reaching) or a human pointing. We then tested whether they could transfer this skill from monkeys to humans, from humans to monkeys, and from one conspecific to another conspecific. One group of monkeys was trained and tested using a conspecific as the cue-giver and was then tested with a human cue-giver. The second group of monkeys was trained and tested with a human cue-giver and was then tested with a monkey cue-giver. Monkeys that were successful with a conspecific cue-giver were also tested with a novel conspecific cue-giver. Monkeys learned to use a human point and conspecific cues to obtain rewards. Monkeys that had learned to use the cues of a conspecific to obtain rewards performed significantly better than expected by chance when they were transferred to the cues of a novel conspecific. Monkeys that learned to use a human point to obtain rewards performed significantly better than expected by chance when tested while observing conspecific cues. Some evidence suggested that transferring between conspecific cue-givers occurred with more facility than transferring across species. Results may be explained by simple rules of association learning and stimulus generalization; however, spontaneous flexible use of gestures across conspecifics and between different species may indicate capuchins can generalize learned social cues within and partially across species.

Wild capuchin monkeys anticipate the amount of ripe fruit in natural trees.

Tropical forests have a high diversity of tree species which have very low densities and vary across time in their seasons of peak fruiting and maturation rates. As evidence of the ability of primates to track or anticipate changes in fruit production at individual trees, researchers have used the increased speed of primate groups toward more rewarding food patches. We analyzed the speed of approach to natural trees of wild capuchin monkeys under the effect of scramble competition, after excluding any plausible visual, olfactory and auditory cues. We conducted all-day group follows of three habituated capuchin groups at Iguazú National Park, Argentina, collecting data on ranging behavior and patterns of visits to fruit trees in relation with their location and fruit availability. Travel speed varied according to the expected reward at a feeding tree, increasing as rewards increased from low values, but decreasing again at very high values. Also, travel speed varied with time of day, decreasing from the time of first activity as the monkeys became less hungry, and increasing again toward late afternoon. Measures of unripe fruit cover did not explain variation in travel speed at any distance from a focal tree. Our data imply that, after excluding sensory cues, capuchins appear to anticipate time-varying ripe fruit quantity of natural resources, suggesting that they use memory of tree location and anticipation of fruit maturation. We also confirm that speed is a good measure about expectations of resources, as has been shown in previous studies.

Insightful problem solving and emulation in brown capuchin monkeys.

We investigated problem solving abilities of capuchin monkeys via the "floating object problem," a task in which the subject must use creative problem solving to retrieve a favored food item from the bottom of a clear tube. Some great apes have solved this problem by adding water to raise the object to a level at which it can be easily grabbed. We presented seven capuchins with the task over eight trials (four "dry" and four "wet"). None of the subjects solved the task, indicating that no capuchin demonstrated insightful problem solving under these experimental conditions. We then investigated whether capuchins would emulate a solution to the task. Seven subjects observed a human model solve the problem by pouring water from a cup into the tube, which brought the object to the top of the tube, allowing the subject to retrieve it. Subjects were then allowed to interact freely with an unfilled tube containing the object in the presence of water and objects that could be used to solve the task. While most subjects were unable to solve the task after viewing a demonstrator solve it, one subject did so, but in a unique way. Our results are consistent with some previous results in great ape species and indicate that capuchins do not spontaneously solve the floating object problem via insight.

Female sociality and sexual conflict shape offspring survival in a Neotropical primate.

Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.