Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

Carrying and hand-use patterns in Panamanian white-faced capuchins (Cebus capucinus)

The aim of this project was to examine the potential influence of postural regulation on capuchin hand-use patterns by focusing on tasks that involved the carrying of objects. Two months were spent on Barro Colorado Island, Panama, collecting data on ten white-faced capuchins (Cebus capucicus) (four adult males/six adult females). Over 215 contact hours were spent with the monkeys, and a total of 213 carries were recorded. No hand preference bias at the population level was found for the carry task; and no detectable hand-use patterns for carry were correlated with the weight of the object carried (except a right-hand bias for carrying medium-sized objects), the plane of the monkey's movement, its locomotor pattern, or its height above the ground. Therefore, the results of this study do not support the hypothesis that the need for postural regulation while carrying an object influences hand-use patterns in free-ranging capuchins. Our results are especially important because they are contrary to the results of the only other free-ranging capuchin laterality study conducted to date (Panger, 1998).     

Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus)

I aim to explicate the pattern of differences and relations between the sexes in two groups ofC. capucinus, in terms of phylogenetic, social and ecological predictors. I use three lines of evidence to develop predictions as to how male and femaleC. capucinus interact and how the sexes differ in behavior: (1) phylogenetic similarities to other species ofCebus; (2) a general model of sex differences in female-bonded social systems; and (3) ecological analogy of Old World monkeys. First, I conclude that phylogenetic affinity is a good predictor in thatC. capucinus are similar to other species ofCebus in many patterns of sex-differentiated behavior. An exception is that, unlikeC. apella andC. olivaceus, in which a single breeding male is reported to be highly conspicuous in each group,C. capucinus live in a decidedly multimale system. Secondly, the general model of sex differences in female philopatric, male-dispersal societies, which was originally developed for Old World species, also accurately predicts several aspects of social behavior inC. capucinus. Thirdly, a proposed ecological analogy betweenCercopithecus ascanius andspecies of Cebus is not substantiated in this study of C. capucinus, though the analogy is apparently well suited to the social dynamics of other species in the genusCebus.     

Explaining variation in affiliative relationships among male white-faced capuchins (Cebus capucinus)

Relationships among coresident male white-faced capuchins are highly variable, ranging from affiliative to aggressive. In this paper I examine the affiliative relationships of all adult and subadult males residing in four social groups in Santa Rosa National Park, Costa Rica. Relationships among males in two study groups were neutral and tolerant, while in the remaining two groups males were highly affiliative. Male-male dyadic affiliative interactions were examined to determine which variables (group size, sex ratio, age relationship, relationship duration, and rank distance) influence the quality of male relationships within the study groups. Group size explained much of the variation, with males in small groups being more affiliative. However, the duration and history of the relationship among coresident males appears to be the most important variable in understanding male-male relationships within social groups.     

Social factors influencing natal dispersal in male white-faced capuchins (Cebus capucinus)

White-faced capuchin males disperse from their natal group at around 4.5 years of age, but there is much variation in dispersal timing: our youngest confirmed disperser was 19 months and the oldest 11 years old. In this study, we investigate possible factors influencing dispersal decisions in this species. Between 1983 and 2010, 64 males were born into three study groups in Santa Rosa National Park, Area de Conservación Guanacaste, and Costa Rica. As of August 2010, 21 died or were presumed dead (<14 months), 13 remained natal residents, and 30 were presumed dispersers. We used backward logistic regression to identify proximate factors that predict the occurrence of male natal dispersal. The occurrence of a takeover (significant positive association) and group size (nonsignificant negative association) were included in the model. Male age, number of maternal brothers, and number of adult males were not significant predictors of natal dispersal. The resultant model correctly classified 97% of dispersed and 89% of resident natal males, for an overall success rate of 95%. The occurrence of a group takeover was the strongest predictor of male dispersal, with natal males being 18.7 times more likely to disperse in the context of a group takeover than during peaceful times. A linear regression model showed that the tenure length of a male's probable father influences the age of natal dispersal, explaining 15% of the observed variation in age. However, when our oldest disperser was removed (an outlier) this effect disappeared. Collectively, these results indicate that group instability, as evidenced by the occurrence of a takeover, shorter tenure length of a natal male's father, and smaller group size, triggers natal dispersal in this species while the converse leads to a delay. These data add to our growing evidence of the enormous impact that takeovers have on the behavioral ecology of this species.     

Resource patch size and flexible foraging in white-faced capuchins (Cebus capucinus)

White-faced capuchins (Cebus capucinus)on Barro Colorado Island, Panama, have a flexible foraging strategy. Typically, foraging party size is small and individuals feed dispersed from one another. When seasonal fruiting of large volume trees occurs, the majority of the group forages simultaneously. As C. capucinusdo not display a rigorous dominance structure and there are few indications that individuals or coalitions monopolize food patches,individuals are expected to display scramble strategies instead of high frequencies of contest competition. I recorded foraging party size (simultaneous foragers), the total number of animals to feed successively, and the diameter at breast height (DBH) of fruit trees used in two habituated troops. Individuals in each group spent a substantial amount of time — 65 and 48% of foraging time for each group — foraging in party sizes of one. Monkeys predominantly foraged alone in small trees (0- to 20- cm DBH), successively in medium trees (21- to 60- cm DBH), and simultaneously in large trees (>61- cm DBH). They used small trees more frequently than all other tree classes. In medium-sized trees, although fruit was plentiful, space was limited. In these trees Cebusforaged successively. In large-volume trees, space and fruit were abundant and several individuals fed together. As the DBH of fruiting trees increased, the average foraging party size increased exponentially. Cebus capucinusat Barro Colorado Island modify their foraging party size to adapt to the seasonal patterns of fruit production.     

The behavior of white-faced capuchins (Cebus capucinus) at a dry-season waterhole

During a study of white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, northwest Costa Rica, the study troop drank daily from a single terrestrial waterhole for approximately three months during the dry season. The drinking order of troop members at the waterhole was not random: adult males tended to be in the first quartile of the drinking progression, adult females generally occurred with equal frequency throughout the progression, and juveniles drank most commonly in the third quartile. There were also differences in the usual drinking ranks among individuals of the same age-sex class. It is hypothesized that those adult males which are usually first in the progression are increasing their personal fitness by reducing the risk of predation on their offspring and on potential mates. The tendency of adult females to precede juveniles may similarly reflect protection of offspring. The daily visits to the waterhole by the study troop did not appear to greatly restrict the use of their range. It is suggested, however, that the availability of standing sources of water may be an important factor affecting the local distribution and density of capuchins in seasonally and chronically dry areas.     

Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus)

I examined sex differences in diet and foraging behavior in two groups of white-faced capuchin monkeys (Cebus capucinus)in a tropical dry forest at Santa Rosa National Park, Costa Rica. I tested three hypotheses: sex differences in diet and foraging behavior are best explained by (1) sexual dimorphism, (2) the energy demands of pregnancy and lactation for females;and (3) avoidance of competition between the sexes. Sexual dimorphism offered the best explanation of sex differences in the diet and foraging behavior of C. capucinus,accurately predicting that males do more strenuous foraging activity, make less use of small foraging supports, and spend more time on or near the ground. Females spent more time foraging than males did but probably obtained a lower protein yield per unit foraging time. Females exploited more small and embedded invertebrates, while males ate more large invertebrates and vertebrate prey. Pregnant and lactating females spent more time resting and less time foraging than other females did, increasing their foraging return by focusing on foods requiring little handling. There was little evidence of competition avoidance between the sexes.     

Hand preferences on unimanual and bimanual tasks in white-faced capuchins (Cebus capucinus)

This study examined hand preference in white-faced capuchins on a unimanual task and on a coordinated bimanual task. For the unimanual task, handedness was assessed by observing simple reaching for small grains. For the bimanual task, tubes lined with chocolate paste inside were presented to the capuchins. The hand and the finger(s) used to remove chocolate paste were recorded. Seven individuals out of eight in the reaching task and 12 out of 13 in the tube task exhibited a hand preference. Moreover, test-retest correlations showed stability in hand use across time for the coordinated bimanual task. We found no significant differences in strength of hand preference between sexes. Finally, as noted in other primate species, the capuchins were more lateralized in the bimanual task compared to the unimanual task.     

A case report of a male rank reversal in a group of wild white-faced capuchins (Cebus capucinus)

During the course of a study of social relationships in wild, white-faced capuchins at Lomas Barbudal, Costa Rice (May 1990–May 1993), the alpha male was deposed by a subordinate male. The rank reversal was preceded by a decline in proximity maintenance by females to the alpha male, and an increase, in the amount of aggression directed toward the alpha male by the beta female and her female coalition partners. At the time of the rank reversal, females switched from giving thegargle vocalization exclusively to the old alpha male to gargling to the new alpha male; however, juveniles were less consistent with regard to which male they gargled to. At the time of the rank reversal, most adult females reduced the time spent in proximity and grooming with the old alpha male, and increased the time spent in proximity and grooming with the new alpha male. In contrast, juveniles' patterns of affiliation with males did not change in a predictable way following the reversal. The social strategies employed by capuchin monkeys during this rank reversal are compared with those of chimpanzees.     

Aggression, grooming and group-level cooperation in white-faced capuchins (Cebus capucinus): insights from social networks

The form of animal social systems depends on the nature of agonistic and affiliative interactions. Social network theory provides tools for characterizing social structure that go beyond simple dyadic interactions and consider the group as a whole. We show three groups of capuchin monkeys from Barro Colorado Island, Panama, where there are strong connections between key aspects of aggression, grooming, and proximity networks, and, at least among females, those who incur risk to defend their group have particular "social personalities." Although there is no significant correlation for any of the network measures between giving and receiving aggression, suggesting that dominance relationships do not follow a simple hierarchy, strong correlations emerge for many measures between the aggression and grooming networks. At the local, but not global, scale, receiving aggression and giving grooming are strongly linked in all groups. Proximity shows no correlation with aggression at either the local or the global scale, suggesting that individuals neither seek out nor avoid aggressors. Yet, grooming has a global but not local connection to proximity. Extensive groomers who tend to direct their efforts at other extensive groomers also spend time in close proximity to many other individuals. These results indicate the important role that prosociality plays in shaping female social relationships. We also show that females who receive the least aggression, and thus pay low costs for group living, are most likely to participate in group defense. No consistent "social personality" traits characterize the males who invest in group defense.     

Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus

New World monkeys exhibit a color vision polymorphism. It resultsfrom allelic variation of the single-locus middle-to-long wavelengthopsin gene on the X chromosome. Females that are heterozygousfor the gene possess trichromatic vision. All other individualspossess dichromatic vision. The prevailing hypothesis for themaintenance of the color vision polymorphism is through a consistentfitness advantage to heterozygous trichromatic females. Suchfemales are predicted to be more efficient than dichromats whendetecting and selecting fruit. Recent experiments with captivecallitrichid primates provided support for this hypothesis bydemonstrating that color vision phenotype affects behavioralresponses to contrived food targets. Yet, the assumptions thattrichromatic females acquire more calories from fruit, or thatnumber of offspring is linked to caloric intake, remain untested.Here, we assess if, in the wild, heterozygous trichromatic individualsin a group of white-faced capuchins (Cebus capucinus) enjoyan energetic advantage over dichromats when foraging on fruit.Contrary to the assumptions of previous theoretical and experimentalstudies, our analysis of C. capucinus foraging behavior showsthat trichromats do not differ from dichromats in their fruitor energy acquisition rates. For white-faced capuchins, theadvantage of trichromatic vision may be related to the detectionof predators, animal prey, or fruit under mesopic conditions.This result demonstrates the importance of using a fitness currencythat is relevant to individual animals to test evolutionaryhypotheses.     

Visibility, group size, vigilance, and drinking behavior in coati (Nasua narica) and white-faced capuchins (Cebus capucinus): experimental evidence

I studied the role of visibility on the vigilance behavior of coatis Nasua narica and white-faced capuchins Cebus capucinus in a dry tropical forest in Costa Rica. Vigilance and drinking behavior were observed at a waterhole where the water surface was 2–3 m below ground level for 5 days. Then I provided an artificial water pan of similar size adjacent to the natural waterhole, but level with the ground, and observed the same behaviors. Animals drinking at the natural waterhole had to descend below ground where they could not see above ground, while those drinking from the experimental pan could see approaching predators. Variations in drinking and vigilance behavior were accounted for by site (natural vs. experimental water source) and group size, with site contributing most significantly to variations. Both coatis and capuchins decreased their time to wait at the forest edge before emerging to drink, had more drinking bouts, had longer bout lengths, and decreased their vigilance behavior when they drank at the ground-level waterhole compared to the one below the surface, where their visibility was obscured. For both species, total drinking time increased, and vigilance decreased, with group size. This study demonstrated experimentally that visibility and group size influence drinking and vigilance behaviors. Received: 9 February 2000 / Received in revised form: 3 November 2000 / Accepted: 10 November 2000     

Wild capuchins (Cebus capucinus) fail to use tools in an experimental field study

From September through November 2000 we conducted an experimental field study of tool use in a group of 15 wild white-faced capuchins (Cebus capucinus) in Costa Rica. The problem presented to the capuchins involved the use of wooden dowels as probes to obtain a food reward (two bananas) located inside a clear Plexiglas box. Specifically, the task required the capuchins to manually insert a dowel into any of six holes drilled into the box in order to push the bananas off a shelf. The banana could then be retrieved through a large opening at the bottom of the box. The capuchins visited the tool-use platform 702 times over the course of 55 consecutive days and under several experimental conditions. During the first 21 days of the study, they explored the box but made no attempt to touch or pick up the dowels. Even after we placed the dowels in the holes, the capuchins only occasionally manipulated them. Overall, the results indicate that the capuchins did not use a tool to solve this novel foraging problem.     

Vocal coordination of troop movement among white-faced capuchin monkeys,Cebus capucinus

Coordinated travel by social groups is well documented, often with evidence that cognitive spatial maps are employed. Yet the mechanisms by which movement decisions are made and implemented within social groups are poorly known. In a field study of white-faced capuchin monkeys in Costa Rica it was demonstrated that a specific call, the “trill,” is used by adults in the initiation and directing of troop movement. The trills of subadults were restricted to vocal exchanges with other subadults. Continuous vocal recordings were collected of the vocalizations of the 14 members of the study troop. A cumulative 33.7 h of continuous samples and 1,892 sonagrams were analyzed. In addition to vocalizations clearly associated with alarm, distress, or agonistic contexts, two distinct call types were identified, trills and huhs. Age-sex classes differed in the rate at which both types of calls were produced in different spatial positions within the troop. Adult females and males produced higher rates of trills when in the leading edge compared to all other spatial positions in a traveling troop. Trills at the edge of a stationary troop represented 36 “successful” and 3 “unsuccessful” start attempts; the troop usually moved in the trajectory predicted by a trilling adult's location on the troop periphery within 10 min of the initiation of trilling. Adults also altered the trajectory of traveling troops by trilling at the side and back of the troop (10 “successful” and 4 “unsuccessful” attempts). Huh vocalizations were most predictably produced when a capuchin is in a dense fruit patch. These results emphasize the role vocalizations serve in the coordination and trajectory of group movement in nonhuman primates, especially those populations that are arboreal or in which visual contact is otherwise impeded. © 1993 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, is in the public domain in the United States of America.

     

Color-vision polymorphism in wild capuchins (Cebus capucinus) and spider monkeys (Ateles geoffroyi) in Costa Rica

New World monkeys are unique in exhibiting a color-vision polymorphism due to an allelic variation of the red-green visual pigment gene. This makes these monkeys excellent subjects for studying the adaptive evolution of the visual system from both molecular and ecological viewpoints. However, the allele frequencies of the pigments within a natural population have not been well investigated. As a first step toward understanding the relationship between vision and behavior, we conducted color-vision typing by analyzing fecal DNA from two wild groups of white-faced capuchin monkeys (Cebus capucinus) and one group of black-handed spider monkeys (Ateles geoffroyi) inhabiting Santa Rosa National Park of Costa Rica. All color-typed monkeys were individually identified. In C. capucinus and A. geoffroyi we found three and two pigment types, respectively, and the spectral mechanism that created one of the two Ateles pigments was found to be novel. In one Cebus group and the Ateles group, all alleles were present, whereas in the other Cebus group only two alleles were found, with one allele predominating. This was likely due to the effect of close inbreeding, indicating that wild populations can exhibit a variety of allele compositions. This result also suggests that the color-vision polymorphism can be easily distorted by natural factors, such as inbreeding, skewing the population structure.     

Begging and transfer of coati meat by white-faced capuchin monkeys,Cebus capucinus

White-faced capuchin monkeys were frequently observed to raid the nests and predate the pups of coatis at two study sites (Santa Rosa National Park and Lomas Barbudal Biological Reserve) in northwestern Costa Rica. Adult monkeys of both sexes were the primary participants in nest-raiding. At Santa Rosa, the original captor of the pup tended to eat the entire carcass, whereas at Lomas Barbudal, the monkeys rapidly became satiated and allowed another monkey to have the carcass. At Lomas Barbudal, there was a tendency for adult females to share preferentially with their own offspring, but only if the offspring were less than 1 year old. Dominance rank of the owner of the carcass relative to the rank of the beggar did not significantly affect the probability of willingly transferring meat to the beggar. In one of two years, carcass theft was more likely to occur when the thief was higher ranking than the carcass owner.     

Early behavioral development in capuchins (Cebus)

Capuchin infants (genus Cebus) are born in a behaviorally more altricial state than is known for infants of other primate taxa except apes. Development in the first 2 months after birth is characterized by the major reorganization of sleeping and waking, assumption of postural control and the appearance of prehension. Capuchins develop postural control, prehension and locomotion later than do squirrel monkeys, baboons or macaques, presenting a pattern of motor development intermediate between these relatively more precocial genera and apes. Capuchins provide a useful model primate system in which to study development and its links with behavioral variability and life history.     

Use of a club by a wild white-faced capuchin (Cebus capucinus) to attack a venomous snake (Bothrops asper)

In Parque Nacional Manuel Antonio, Costa Rica, an adult male Cebus capucinus was observed repeatedly hitting a venomous snake (Bothropsasper) with a branch. Initially a large dead branch overhanging the snake had been broken off in the course of aggressive displays to the snake by the adult and two subadult males. The snake's escape was apparently prevented by the weight of the fallen branch and possibly by the injuries caused by its fall. This is the first direct observation of a capuchin monkey in a natural habitat using a tool.