Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

Hand Preference in Free-Ranging White-Throated Capuchins (Cebus capucinus) in Costa Rica

I studied the hand preference patterns of individuals in three troops of white-throated capuchins (C. capucinus) in Palo Verde, Costa Rica, during 11 months from February 1995 to January 1996. I used focal and ad libitum sampling techniques and tested several frameworks that seek to explain and to predict primate hand use patterns via a variety of spontaneous tasks that differ in manipulative difficulty and required postural regulation: reach, tap, grab, carry, and object-use. The monkeys showed symmetrical hand use patterns for the easy tasks, reach and tap; strongly asymmetrical patterns for the highly manipulative task, object-use, at the individual level; and weak population-level biases for tasks requiring a degree of postural regulation, carry. The results for data on grab are inconclusive. These results do not support the available primate hand use frameworks and differ from most of the captive literature on hand preference in Cebus. The findings indicate that postural regulation may influence hand use patterns in nonhuman primates at the population level.     

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).     

Violent coalitionary attacks and intraspecific killing in wild white-faced capuchin monkeys (<Emphasis Type="Italic">Cebus capucinus</Emphasis>)

During 12 years of observation, we have observed three confirmed and two inferred lethal coalitionary attacks on adult male white-faced capuchins (Cebus capucinus) by members of two habituated social groups at Lomas Barbudal Biological Reserve, Costa Rica. In one case, an alpha male was badly wounded and evicted from his group, and when later found by his former groupmates he was attacked by several of them and died less than 24 h later. In two other cases, lone extra-group males were mobbed by adult and immature males of a bisexual group. One victim's abdomen was torn open and he died less than 24 h later. A second victim was quite badly bitten but may have escaped. The fourth and fifth cases resulted from intergroup encounters. One victim lost the use of both arms but may have survived, whereas the other died of unknown causes within an hour of the attack. The observed death rate from coalitionary aggression at our site is approximately the same as that reported for eastern chimpanzees. Because at least three of the five observed incidents involved large coalitions attacking lone victims, they support the general hypothesis that imbalances of power contribute to intraspecific killing in primates. However, the occurrence of lethal coalitional attacks in a species lacking fission–fusion social organization poses a challenge to the more specific version of the imbalance-of-power hypothesis proposed by Manson and Wrangham in 1991 to explain chimpanzee and human intergroup aggression.     

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.     

Effect of Male Emigration on the Vigilance Behavior of Coresident Males in White-Faced Capuchins (Cebus capucinus)

I examined the vigilance behavior of male Cebus capucinus residing in four groups in Santa Rosa Park, Costa Rica. One male emigrated from each of three study groups, providing ideal experimental conditions for examining the effect of coresident males on male vigilance behavior (social and non-social). Following the predator and conspecific defense theories for the adaptive value of male vigilance behavior and the occurrence of multimale groups, I predicted that male nonsocial vigilance would increase after the emigration of a coresident male. My prediction was supported in only one of the three study groups. Males in two groups decreased their nonsocial vigilance after the emigration of a coresident male, which was probably influenced by seasonal changes and the peripherality of one group's coresident male before his emigration. The social vigilance hypothesis proposes that for species with rigid dominance hierarchies, social vigilance should increase with an increase in same sex competitors. Therefore, I predicted that male social vigilance would decrease after the emigration of a coresident male. The hypothesis is generally supported in my findings, as two of the three groups displayed a decrease in social vigilance after the emigration of a coresident male. Increased social vigilance in the third group is best explained by the change in the alpha male's social behavior after the emigration of his only coresident male.     

Manipulative Tendencies of Captive Cebus albifrons

We conducted two experiments to examine the manipulative tendencies of captive Cebus albifrons. In Experiment 1 we examined hand preference for reaching by providing subjects with food either on the cage floor (to facilitate quadrupedal reaching) or at the height of an upright subject's shoulder (to facilitate bipedal reaching). In Experiment 2 we examined combinatorial manipulation by providing subjects with nesting containers and other portable manipulanda. Results indicate that C. albifrons exhibits greater use of the right hand for bipedal versus quadrupedal reaching (exhibiting a group-level lack of bias for bipedal reaching and a left-hand bias for quadrupedal reaching), combines objects using a simple pairing strategy, and uses and produces simple tools. Aspects of these findings parallel those for Cebus apella.     

Success and Understanding in Cognitive Tasks: A Comparison Between Cebus apella and Pan troglodytes

The recent boom in cognitive studies on chimpanzees and capuchins allows an analysis of the cognitive processes and behavioral tendencies underlying their performances when faced with a variety of problems. In the laboratory, but less so in nature, Cebus and Pan show remarkable convergence in their overall success in solving problems involving the use of tools and cooperation. Behavioral ingredients such as explorative tendencies, manipulative skills, social tolerance, and cognitive capacities contribute to their success. However, in experiments in which carefully controlled conditions were implemented, e.g., cooperation and tool-using tasks, differences between the two taxa emerged in the role played by such ingredients in fostering success. Although it is difficult to establish the nature of these differences, a profitable way to look at them is from outside: from the point of view of what children do when tested in similar tasks. If we consider the ways in which children experience or achieve initial success and then become fully proficient in solving similar tasks, we can appreciate the different recipes for success that Pan and Cebus present.     

Canine Dimorphism and Interspecific Canine Form in Cebus

I investigated canine dimorphism and interspecific canine form in adult specimens from 4 capuchin species (Cebus albifrons, C. apella, C. capucinus, and C. olivaceus). I used various univariate and multivariate statistics, which are based on 6 variables, to test several hypotheses that are based upon the finding that canine dimorphism is strongly associated with intermale competition in platyrrhines (Kay et al., 1988), Greenfield (1992a), Plavcan and van Schaik (1992, 1994). Results from the indices of canine dimorphism and the unpaired t-tests corroborate the prediction that males of each species possess significantly larger canines than those of females. Large male canines are especially prominent in 2 variables, maxillary and mandibular canine height. Greene's t-test (1989) does not support the prediction that Cebus apella and C. olivaceus possess a larger degree of canine dimorphism relative to C. albifrons and C. capucinus. No interspecific differences in degree of canine dimorphism are indicated by this test. Results of the discriminant function analyses (DFA) do not find that Cebus apella and C. olivaceus possess different canine form relative to C. albifrons and C. capucinus as predicted. However, Cebus apella is differentiated from the untufted capuchins (C. albifrons, C. capucinus, and C. olivaceus) by the DFA. I suggest that intermale competition is the primary selective force underlying the observed morphological patterns; however, it does not explain all the variation associated with canine dimorphism in Cebus.     

Interspecific Interactions Between Cebus capucinus and Other Species: Data from Three Costa Rican Sites

Capuchins exhibit considerable cross-site variation in domains such as foraging strategy, vocal communication and social interaction. We report interactions between white-faced capuchins (Cebus capucinus) and other species. We present comparative data for 11 groups from 3 sites in Costa Rica that are ecologically similar and geographically close, thus reducing the likelihood that differences are due solely to genetic or ecological differences. Our aim is to document both the range of variation and common elements across sites and situations. We also consider factors that contribute to the variation or consistency or both, including social learning, local ecology, and temperament. We consider 4 categories of allospecifics: (1) vertebrate prey, (2) potential predators, (3) feeding competitors, and (4) neutral species. Although we cannot rule out local differences in ecology, our data suggest that social learning may account for at least some cross-site differences in behavior toward allospecifics. Our strongest finding is that boldness, aggression and pugnacity are displayed consistently across sites, groups and circumstances, even in interactions with neutral species, which reflects a critical aspect of species-specific temperament in Cebus capucinus that has been evolutionarily developed and reinforced through highly opportunistic foraging, strong predator defense, and active hunting. We suggest directions for future research, particularly in regard to primate temperament as an evolved trait with consequences for fitness.     

Urine Washing and Sniffing in Wild White-faced Capuchins (<Emphasis Type="Italic">Cebus capucinus</Emphasis>): Testing Functional Hypotheses

Urine washing (UW) is taxonomically widespread among strepsirhines and platyrrhines, yet its functional significance is still unclear. We used 2274 h of focal follows of 35 adult and subadult wild white-faced capuchins (Cebus capucinus) to test 1) the intergroup signaling, intragroup social signaling, and thermoregulatory hypotheses for UW and 2) the hypothesis that individuals sniff each other's urine and other traces to gather socially significant information. Males engaged in significantly more UW than females. All 5 α-males engaged in more UW than subordinate males did, including 4 α-males that increased their UW rate above that of their male groupmates after their rise to α rank. Males engaged in significantly less UW while in view of other males than at other times. Male-male sniffing rates do not correlate with either aggression rate or dominance rank distance. Urine washing rates did not increase while subjects were in parts of their home range where more intergroup encounters occurred. Urine washing rates were highest early in the morning and late in the afternoon, presumably when temperatures were coolest. The data do not support either the thermoregulatory or social signaling hypothesis. We suggest that experiments with captive capuchins are necessary to resolve the issue of the function of urine washing in the taxon.     

Ant-Gathering with Tools by Captive Tufted Capuchins (Cebus apella)

We examined ant-gathering with tools by captive tufted capuchins (Cebus apella) via two experiments. In Experiment 1, we provided groups of subjects with sticks and small branches and an apparatus that accommodated the use of tools to gather ants. In Experiment 2, we sealed the apparatus with acetate and provided the same subjects with sticks and stones. Seven of 14 subjects used sticks and leaves as probes to extract ants from the apparatus. Six of them modified probes by detaching sticks from larger branches, breaking sticks into two or more pieces, and subtracting leaves and bark. Three subjects later used a stone and stick tool-set to penetrate acetate barriers and to extract ants. These results demonstrate the use of tools by Cebus to capture moving prey and are consistent with the idea that sensorimotor skills associated with the production and use of tools in primates evolved convergently in capuchins and great apes.     

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.     

Transfer of tools and food between groups of tufted capuchins (Cebus apella)

This research examined tool and food transfer between two groups of tufted capcuhin monkeys (Cebus apella). Subjects in one group transferred stones to subjects in a second group who in turn used the stones as cutting tools and then transferred food to subjects in the first group. Aspects of the capuchins' behavior are similar to those described for food-sharing in Cebus, cooperative tool use in Papio, and tool and food exchange in Pan. We propose that tool use and food-sharing facilitate tool and food transfer between captive groups of Cebus apella. Am. J. Primatol. 43:33–41, 1997. © 1997 Wiley-Liss, Inc.     

Tool use in wild capuchin monkeys (Cebus albifrons trinitatis)

White-fronted capuchins were observed to use leaves as cups to retrieve water from tree cavities. On multiple occasions several individuals performed this behavior. Thus, these capuchins engage in habitual tool use, as defined by McGrew's classificatory scheme of tool using behavior. Am. J. Primatol. 46:259–261, 1998. © 1998 Wiley-Liss, Inc.     

Effects of Reproductive Status on Energy Intake,Ingestion Rates,and Dietary Composition of Female <Emphasis Type="BoldItalic">Cebus capucinus</Emphasis> at Santa Rosa,Costa Rica

The limiting factor for fitness in female primates is the acquisition of high-quality food, i.e., food that is high in energy and nutrients, such as protein, fat, and carbohydrates. Reproductive status can influence female feeding patterns, e.g., lactating females in some primate species consume greater quantities of food and specific nutrients than do nonlactating females. We examined the energy intake, ingestion rate, and composition of the diet in female white-faced capuchins in 3 reproductive states: lactating, gestating, and cycling. We observed 12 reproductively active females for 7 mo and compared their energy intake, ingestion rates, and intake rates of nutrients: protein, fat, sugar, and fiber. Lactating females took in significantly more energy per hour while feeding than pregnant and cycling females did. Lactating females also ingested significantly more food items per hour, but they did not spend more time eating than other females did, and they did not differ in the composition of their diet as measured by insect consumption and proportion of protein. Pregnant and cycling females did not differ from each other in any of the measures. We predicted that as the infants aged and began to move independently to forage and play, their mothers’ energy intake rates would decrease in concert with decreased energy demands by the infant. We found a statistically significant relationship between these 2 factors, with infant age explaining 75.4% of variation in mothers’ energy intake, supporting previous studies that found lactation to be the most energetically expensive reproductive state.     

Self-treatment of wounds by a capuchin monkey (Cebus apella)

A captive adult female capuchin monkey spontaneously manufactured and used tools to groom her vaginal area and four of her own wounds over a six-month period. The wounds apparently occurred during fights with other monkeys living in the same social groups. The monkey often groomed her vaginal area and wounds with tools she had coated with a sugar-based syrup. The monkey did not use tools to groom other body areas, nor did she use tools that were coated with substances other than syrup. This monkey’s unusual habit developed in the context of manufacturing and using tools in a feeding task. These observations demonstrate that the serendipitous performance of particular behaviours in appropriate contexts can lead to the discovery and practice of simple treatment of wounds by a monkey. The independent discovery of simple medicinal procedures in human cultures may have occurred in a similar manner. Such discoveries could have predated the development of sophisticated cultures in which medicinal practices were embedded and eventually recorded.     

Intimate social behavior in infant interactions in Cebus apella

The development and individual stability of three intimate social behaviors (Lipsmacking, Carrying Attempts, and Facial Inspection) were examined for 43 group-housed Cebus apella infants from birth to 2 years of age. Occurrence of these behaviors was scored from 10-min videotape samples recorded three times a week over that time. Frequency of Lipsmacking and Carrying Attempts by adult males, adult females, and juveniles were all highest in early months and decreased to low levels by the end of the first year. Facial Inspection of partners by infants, in contrast, first began at 3-4 months and increased over time, at least to adult males and juveniles. Correlational analyses indicated stable individual differences in these interactions with infants and outlined a relationship between these intimate behaviors and more general social patterns reported previously for these animals. Results suggest that adult males may play a special role in affording juveniles opportunities for social learning of foraging and manipulative skills.