Capuchins (Sapajus apella) and squirrel monkeys (Saimiri sciureus) fail to attend to the functional spatial relationship between a tool and a reward.

Capuchins (Sapajus apella) and squirrel monkeys (Saimiri sciureus) participated in 3 experiments in which they were presented with 2 objects, one appropriately oriented and the other inappropriately oriented to retrieve a food reward by pulling, replicating prior experiments with nonhuman primates described as evaluating "tool choice." Choice patterns were analyzed to assess whether monkeys learned that tools needed to be oriented with part of the tool on the far side of the reward to pull in the food. Both species learned to choose appropriately oriented tools after a similar number of sessions with a cane-shaped tool in the first task. Both species also transferred to a new tool shape in the second task, but squirrel monkeys' performance on particular trials suggested they did not use the functional relationship between the tool and the food to guide their choices. Tool shapes and configurations in the final task were designed to control for the potential use of extraneous spatial cues. Neither capuchins nor squirrel monkeys chose appropriately oriented tools above chance in control trials. Results suggest both species relied on other spatial cues to perform in previous tasks rather than learning to attend to the functional spatial relationship between a tool and a reward. Species differences emerged in the second task only, as capuchins mastered performance with the new tool shape faster than squirrel monkeys and seemed to use a more complex set of rules to guide their choices. (PsycINFO Database Record (c) 2019 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.

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.

Inference by exclusion in lion-tailed macaques (Macaca silenus), a hamadryas baboon (Papio hamadryas), capuchins (Sapajus apella), and squirrel monkeys (Saimiri sciureus).

Previous research has suggested that several primate species may be capable of reasoning by exclusion based on the finding that they can locate a hidden object when given information about where the object is not. The present research replicated and extended the literature by testing 2 Old World monkey species, lion-tailed macaques (Macaca silenus) and a hamadryas baboon (Papio hamadryas), and 2 New World species, capuchin monkeys (Sapajus apella) and squirrel monkeys (Saimiri sciureus). The New World monkeys were tested on the traditional 2-way object choice task, and all 4 species were also tested on a more complex 3-way object choice task. In addition, the squirrel monkeys were tested on a 2-way object choice task with auditory information. The results showed that, whereas the Old World species were able to infer by exclusion on the 3-object task, some of the capuchin monkeys had difficulty on each of the 2- and 3-cup tasks. All but 1 of the squirrel monkeys failed to infer successfully, and their strategies appeared to differ between the visual and auditory versions of the task. Taken together, this research suggests that the ability to succeed on this inference task may be present throughout Old World monkey species, but is fragile in the New World species tested thus far. (PsycINFO Database Record

Brown capuchin monkeys (Sapajus apella) plan their movements on a grasping task.

Motor planning is a relatively complex cognitive skill in which an actor modifies a behavior to anticipate the future consequences of the action. Studying motor planning in nonhuman primates may provide a better understanding of the roots of human planning abilities. In this study we presented capuchin monkeys (Sapajus apella) with a horizontal dowel baited on either the left or right end. A radial grasp on the dowel with the thumb facing toward the baited end would be the most efficient grip selection when bringing the dowel to one's mouth and indicate motor planning. Ten of the 12 monkeys tested spontaneously used a radial grasp significantly more often than expected by chance. Results demonstrate a more ubiquitous expression of motor planning abilities than previously seen in capuchin monkeys. Adaptation of this method of testing may be useful in evaluating motor planning capacity in other primates.

Crowding increases salivary cortisol but not self-directed behavior in captive baboons.

Reduced space can lead to crowding in social animals. Crowding increases the risk of agonistic interactions that, in turn, may require additional physiological defensive coping mechanisms affecting health. To determine the stress induced from increased social density in a group of nineteen baboons living in an indoor/outdoor enclosure, saliva cortisol levels and rates of anxiety-related behavior were analyzed across two unique crowding episodes. Initially, mean salivary cortisol levels when animals were restricted to their indoor quarters were compared to those when they also had access to their larger outdoor enclosure. Then, mean cortisol levels were compared before, during, and after two distinct crowding periods of long and short duration. Crowding resulted in significantly elevated cortisol during crowding periods compared to non-crowded periods. Cortisol levels returned to baseline following two crowding episodes contrasting in their length and ambient climate conditions. These cortisol elevations indicate greater metabolic costs of maintaining homeostasis under social stress resulting from reduced space. Self-directed behavior, conversely, was not reliably elevated during crowding. Results suggest that the potential for negative social interactions, and/or the uncertainty associated with social threat can cause physiological stress responses detected by salivary cortisol. Self-directed behavioral measures of stress may constitute inadequate indicators of social stress in colony-housed monkeys or represent subjective emotional arousal unrelated to hypothalamic-pituitary adrenal axis activation.

Picture recognition of food by macaques (Macaca silenus).

Pictorial representations of three-dimensional objects are often used to investigate animal cognitive abilities; however, investigators rarely evaluate whether the animals conceptualize the two-dimensional image as the object it is intended to represent. We tested for picture recognition in lion-tailed macaques by presenting five monkeys with digitized images of familiar foods on a touch screen. Monkeys viewed images of two different foods and learned that they would receive a piece of the one they touched first. After demonstrating that they would reliably select images of their preferred foods on one set of foods, animals were transferred to images of a second set of familiar foods. We assumed that if the monkeys recognized the images, they would spontaneously select images of their preferred foods on the second set of foods. Three monkeys selected images of their preferred foods significantly more often than chance on their first transfer session. In an additional test of the monkeys' picture recognition abilities, animals were presented with pairs of food images containing a medium-preference food paired with either a high-preference food or a low-preference food. The same three monkeys selected the medium-preference foods significantly more often when they were paired with low-preference foods and significantly less often when those same foods were paired with high-preference foods. Our novel design provided convincing evidence that macaques recognized the content of two-dimensional images on a touch screen. Results also suggested that the animals understood the connection between the two-dimensional images and the three-dimensional objects they represented.

Transport of functionally appropriate tools by capuchin monkeys (Cebus apella).

Capuchin monkeys (Cebus sp.) are notable among New World monkeys for their widespread use of tools. Like chimpanzees, they use both hammer tools and insertion tools in the wild to acquire food that would be unobtainable otherwise. Recent evidence indicates that capuchins transport stones to anvil sites and use the most functionally efficient stones to crack nuts. We further investigated capuchins' assessment of functionality by testing their ability to select a tool that was appropriate for two different tool-use tasks: A stone for a hammer task and a stick for an insertion task. To select the appropriate tools, the monkeys investigated a baited tool-use apparatus (insertion or hammer), traveled to a location in their enclosure where they could no longer see the apparatus, made a selection between two tools (stick or stone), and then could transport the tool back to the apparatus to obtain a walnut. We incorporated tool transport and the lack of a visual cue into the design to assess willingness to transport the tools and the monkeys' memory for the proper tool. Six brown capuchins (Cebus apella) were first trained to select and use the appropriate tool for each apparatus. Four animals completed training and were then tested by allowing them to view a baited apparatus and then travel to a location 8 m distant where they could select a tool while out of view of the apparatus. All four monkeys chose the correct tool significantly more than expected and transported the tools back to the apparatus. Results confirm capuchins' propensity for transporting tools, demonstrate their capacity to select the functionally appropriate tool for two different tool-use tasks, and indicate that they can retain the memory of the correct choice during a travel time of several seconds.

Perseveration on a reversal-learning task correlates with rates of self-directed behavior in nonhuman primates.

In humans and several nonhuman animals, repetitive behavior is associated with deficits on executive function tasks involving response inhibition. We tested for this relationship in nonhuman primates by correlating rates of normative behavior to performance on a reversal-learning task in which animals were required to inhibit a previously learned rule. We focused on rates of self-directed behavior (scratch, autogroom, self touch and manipulation) because these responses are known indicators of arousal or anxiety in primates, however, we also examined rates of other categories of behavior (e.g., locomotion). Behavior rates were obtained from 14 animals representing three nonhuman primate species (Macaca silenus, Saimiri sciureus, Cebus apella) living in separate social groups. The same animals were tested on a reversal-learning task in which they were presented with a black and a grey square on a touch screen and were trained to touch the black square. Once animals learned to select the black square, reward contingencies were reversed and animals were rewarded for selecting the grey square. Performance on the reversal-learning task was positively correlated to self-directed behavior in that animals that exhibited higher rates of self-directed behavior required more trials to achieve reversal. Reversal learning was not correlated to rates of any other category of behavior. Results indicate that rates of behavior associated with anxiety and arousal provide an indicator of executive function in nonhuman primates. The relationship suggests continuity between nonhuman primates and humans in the link between executive functioning and repetitive behavior.

Effectiveness of saliva collection and enzyme-immunoassay for the quantification of cortisol in socially housed baboons.

Circulating cortisol levels are often used to assess the biological stress response in captive primates. Some methods commonly used to collect blood samples may alter the stress response. As such, noninvasive means to analyze cortisol levels are increasingly being developed. We adapted an existing collection method to simultaneously obtain saliva from multiple socially living hamadryas baboons (Papio hamadryas hamadryas) and validated an enzyme-immunoassay kit to quantify cortisol within the saliva samples. Over a period of 12 months, saliva samples were regularly collected from approximately half of the 18-member colony, representing younger monkeys who were more willing to participate. The assay met the four criteria typically used to assess the effectiveness of a new analytical technique: parallelism, precision, accuracy, and sensitivity. Cortisol levels were also proportional to those expected given published plasma levels of cortisol in baboons. Further, salivary cortisol levels increased in individuals following significant stress-related events, such as removal from the group, indicating biological validation. The technique provided a reliable and effective means to assess a physiological indicator of stress in a social group without initiating a stress response owing to handling or sedation, and provided a real-time assessment of cortisol levels and reactivity.

Ordinal representation of numeric quantities by brown capuchin monkeys (Cebus apella).

Using techniques established by E. M. Brannon and H. S. Terrace (2000) with rhesus macaques (Macaca mulatta), the authors tested the ability of brown capuchins (Cebus apella) to order arrays of items ranging in quantity from 1 to 9. Three monkeys were trained on a touch screen to select the quantities 1-4 in ascending order. The monkeys exhibited successful transfer of this ability to novel representations of the quantities 1-4 and to pairs of the novel quantities 5-9. Patterns of responding with respect to numeric distance and magnitude were similar to those seen in human subjects, suggesting the use of similar psychological processes. The capuchins demonstrated an ordinal representation of quantity equivalent to that shown in Old World monkeys.

Influence of kinship and spatial density on reconciliation and grooming in rhesus monkeys.

Some cercopithecine primates direct disproportionate amounts of grooming, huddling, and agonistic support toward maternal kin. Disproportionate amounts of aggression are also directed toward maternal kin, however, suggesting that mechanisms that restore relationships damaged by aggression, such as reconciliation, might be biased toward these preferred social partners. Studies investigating kinship effects and reconciliation are inconsistent, however, perhaps because of differences in the environmental conditions under which behavior was observed. In order to test the effects of kinship and spatial density on affiliative and reconciliation behavior, we conducted focal and scan sampling on a group of rhesus monkeys (Macaca mulatta) living in an outdoor corral under low spatial density conditions. We then compared this data to previously published data on a group of the same species living under higher spatial density conditions. Neither overall grooming nor reconciliation were affected by spatial density once correction procedures were applied. Grooming was kin biased at both study sites, whereas reconciliation was kin biased only in the low-density group. Although data failed to support a Coping Model according to which grooming and reconciliation should go up under higher densities, we suggest that coping may be reflected not so much in overall rates of behavior but in strategic partner choices, such as the increased importance monkeys under crowded conditions appear to attach to nonkin partners. © 1996 Wiley-Liss, Inc.

Sex differences in adolescent rhesus monkey (Macaca mulatta) Behavior.

Sex differences in the behavior of 2.5- to 4.5-year-old rhesus monkeys, living in two social groups approximating natural compositions, were studied over a period of 3 years. Both sexes interacted significantly more often with members of their own sex in agonistic and affiliative interactions even when total rates and durations for male and female subjects did not differ. Strong sexual segregation was also seen in proximity, nonspecific contact, and huddling partners. Males were more involved in play and sex than were females and engaged in these activities primarily with other males. Females did more grooming than males, but groomed both male and female partners. Females also appeared to interact with a wider age range of partners than did males. Although total participation in aggressive interactions did not differ between the two sexes, females used more active forms of agonistic expression than did males. These differences in the behavior of adolescent rhesus are hypothesized to lead to social bonding among adolescent males, while females remain bonded to their matri-lines, including younger males and some fully adult males associated with matrilineal relatives. Adolescent males emigrate from their natal groups but retain sociality and bond to males and females in new groups as they become adult. © 1993 Wiley-Liss, Inc.

Kinship, association, and social relationships in rhesus monkeys (Macaca mulatta).

Data on social interactions with matrilineal kin were collected from two groups of rhesus monkeys for 6 years. All behavioral states, including time within one meter of another, involved kin more often than would be expected by chance. Significant associations were also found between kinship and the frequencies of various forms of agonistic as well as affiliative acts. Frequency of social interaction, however, was not a simple function of time in proximity. Although animals spent more time with kin than nonkin they had more aggressive interactions with kin. Moreover, aggression was biased toward the more serious forms of expression in interactions with kin. Time spent in association was neither predictive of the rate of aggressive interaction nor reduced by high rates of aggressive interaction. Rather than association time influencing rates of interaction, association time may be the consequence of a history of aggressive and affiliative exchanges. Preferential association and high rates of aggressive interaction with kin may be possible due to the existence of compensating social mechanisms nullifying the negative influence of specific aggressive encounters. © 1993 Wiley-Liss, Inc.

Testosterone changes during the period of adolescence in male rhesus monkeys (Macaca mulatta).

Testosterone levels of 59 male rhesus monkeys were monitored over a period of 5 years. Longitudinal comparisons revealed consistent rises in mid-morning levels of circulating hormone in successive years from age 2.5 to 6.5 years of age, whereas cross-sectional comparisons failed to detect significant differences among the older subjects. The first mid-morning hormonal elevation could be detected in some males as young as 2.5 years of age, whereas other males showed no detectable rises until age 5.5 years. Males showing first rises at later ages did not show hormonal levels consistently below age peers who had shown earlier rises. Extreme month-to-month variability and a failure to manifest the seasonal normal curve of fully adult males was characteristic of younger males, but some of these males, nonetheless, proved capable of fertilizing females. Although hormonal and agonistic dominance measures failed to show consistent correlations, the alpha male in an age cohort significantly more often had the highest testosterone levels. These data are used to argue that adolescence is a process that takes place over several years and that classification of adolescent animals as adults, based on a single criterion like fertility, has confounded many prior studies involving cross taxa comparisons as well as developmental variables.

Seasonal weight changes in male rhesus monkeys (Macaca mulatta).

Adult male rhesus monkeys lose weight during the breeding season and regain it during the nonbreeding season. The annual pattern of maximum weight gain just prior to the onset of breeding resembles the seasonal "fattening" seen in squirrel monkeys, but the period of weight gain is less discrete. The magnitude of weight change is less in younger males, in that sexually immature males gain weight in both seasons, but significantly less during the breeding season. Females do not lose weight during the breeding season. Post hoc analyses revealed no significant correlations between male testosterone levels, dominance ranks, weights, or weight changes. The heaviest animals as juveniles were predictably the heaviest as adolescents. The timing of seasonal changes in testosterone did not correlate with the timing of changes in weight; weight losses followed the rise in testosterone, and weight gains continued until early in the breeding season after testosterone levels had already begun to rise. It is suggested that seasonal hormonal changes may influence activities in individuals and that changes in the activities of particular group members may alter the activity patterns of other group members. This alteration of activity patterns due to group influences on individuals as well as individual influences on the group may explain why hormonal regulation of seasonal weight appears to be indirect and why individuals (juveniles) experiencing no seasonal hormonal changes nonetheless show differences in activity patterns and seasonal weight changes.