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.

     

The Repertoire and Social Function of Facial Displays in Cebus capucinus

Systematic studies on facial displays in capuchins are limited and based mainly on studies of tufted capuchins (Cebus apella). Despite the great social-morphological variability within Cebus suggesting possible morphological and functional variations in the facial displays of different species, no study has considered thoroughly visual communication in the genus. Our aim was to describe the facial displays of white-faced capuchins and to assess their distribution and communicative function. We observed 15 captive white-faced capuchins in the Primate Centre of the Louis Pasteur University of Strasbourg, for a total of 198 h. We described the following facial displays: relaxed open-mouth, lip-smacking, open-mouth threat-face, silent bared-teeth, open-mouth silent bared-teeth, protruded-lip face, and tongue-out. We never observed the scalp-lifting display, one of the most common displays characterizing tufted capuchins. White-faced capuchins use the majority of facial displays in an affiliative or playful context; only the open-mouth threat-face display is associated with aggressive behaviors. White-faced capuchins lack ritualized signals of submission. The fact that in white-faced capuchins the silent bared-teeth display conveys only a positive message, while in tufted capuchins it signals submission as well as affiliation, supports the covariation hypothesis (Thierry 2004 Social epigenesis. In B. Thierry, M. Singh, & W. Kaummans (Eds.), Macaque societies: A Model for the study of social organization, pp. 267–294. Oxford University Press).     

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.     

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.     

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.     

Vertebrate Predation and Food-Sharing in Cebus and Pan

Capuchins and chimpanzees are the only nonhuman primates apart from baboons known to prey systematically upon relatively large vertebrates. Vertebrate predation is common and well documented in Pan troglodytes, rare in Pan paniscus, and commonly reported but infrequently studied in Cebus. Food-sharing is common in both Pan species but rarely reported for wild capuchins. I present data on vertebrate predation and food-sharing by white-faced capuchins (Cebus capucinus) from ongoing field studies at Santa Rosa National Park, Costa Rica. We have observed 106 successful predation events resulting in the capture of 156 prey items during 2929 observation hr (5.35 prey per 100 hr). Squirrels and nestling coatis comprised half of the prey taken; the remainder were mainly nestling birds and eggs. Adult males took 52% of all prey and 67% of squirrels. Squirrels are actively hunted and about 65% of them are adults. I estimated that the average capuchin group kills 43–50 squirrels annually, mostly during the dry season. Capuchins hunt squirrels in groups 81% of the time, and 17% of hunts are successful. There is no evidence for cooperative hunting, but occasional collaboration is suggested. Rates of food-sharing were low (1.7 per 100 hr), and meat was the only food shared between adults. I compare predation and food-sharing in C. capucinus with published data for Pan troglodytes, primarily in Gombe and Taï National Parks. I discuss sex differences, hunting strategies, the relationship between hunting and food-sharing, and various ecological and social factors that may promote vertebrate predation in Pan and Cebus.     

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).     

Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus)

Primate vocalizations that appear to occur independently of specific contexts typically are considered to be contact calls. However, results from several recent studies indicate that these calls function to facilitate social interactions. White-faced capuchin monkeys (Cebus capucinus) emit a high-frequency vocalization, termed a "trill," in social interactions and during travel. In this study, immatures emitted most trills, but adult females also trilled; by contrast, adult males rarely trilled. Infants emitted the majority of trills, and they trilled at significantly higher rates than adult females. Infants trilled most when approaching other individuals. Furthermore, infants emitted proportionately more trills than other age classes when approaching other individuals. I therefore focused on the detailed context and immediate behavioral correlates of trilling by infants. Infants that trilled when approaching others tended to interact affiliatively with them subsequently (i.e., climbing on, touching, receiving grooming, and performing food inspection) more than infants that did not trill when approaching. Therefore, infant trilling may have had an immediate effect on the recipient's behavior.     

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.     

Acoustic Analysis and Contextual Description of Food-Associated Calls in White-Faced Capuchin Monkeys (Cebus capucinus)

Since early studies of primates that identified vocalizations that attracted others to a food source, the assumed function of food-associated calls has been to inform others of the presence of food. The label food-associated calls and its implied function has led to a focus in research on many species of the costs/benefits for the signaler and recipient of informing others about the presence of food; however, without clearly identifying the calls contextually or acoustically, it is unclear if calls are specific to a feeding context and thus whether calls provide specific information about the presence of food. If calls occur exclusively in the context of feeding, information about individual identity would allow listeners to decide whether or not to approach a calling individual. I conducted acoustic and contextual analyses on food-associated calls in white-faced capuchins. I identified the calls as distinct vocalizations that occur almost exclusively in a feeding context. Discriminant function analyses demonstrate that information about caller sex and identity are encoded in the calls. Therefore, there is the potential for individuals to use acoustic information when responding to food-associated calls; however, playback experiments are necessary to test more explicitly the hypothesis that recipients are able to recognize the calls of specific individuals.     

Ecological niche differences betweenAlouatta palliata andCebus capucinus comparing feeding modes,branch use,and diet

During the wet season, two sympatric species of primates,Alouatta palliata (mantled howlers) andCebus capucinus (white-faced capuchins), were assayed for feeding niche differences through behavioral and habitat use patterns at Refugio de Fauna Silvestre Curu in Costa Rica. Differences in the use of relative diameter and thickness of branches and five different modes of feeding were compared between the species. White-faced capuchins used more manipulative modes of obtaining food, a wider range of arboreal habitat, and had a more diverse diet than mantled howlers. Mantled howlers may be more restricted than white-faced capuchins in arboreal microhabitat use due to their possible need for large support branches during feeding bouts and resting periods. We report that differences in feeding behaviors, diet, and arboreal habitat use seem to play a large role in separating these species niches.     

Development of activity patterns,social interactions,and exploratory behavior in infant tufted capuchins (Cebus apella)

Early organization of activity states was studied in 17 tufted capuchin (Cebus apella) infants from birth to 11 weeks of age. Development of exploration and interactions with mothers and other group members were studied in 14 of these infants up to the age of 1 year. Activity profiles changed from 3 to 8 weeks as infants began to move off mothers and explore their environments. From 2 to 6 months time with mothers decreased; time alone increased correspondingly. Time spent with other group members did not vary significantly over the first year. By 7–9 months capuchin infants spent more time alone or with other group members than with mothers, although weaning was still not completed by the end of the first year. Simple environmental exploration began in the 2nd month and reached stable levels by 4 months. Complex manipulation of food and objects first began at 3–4 months and increased to stable levels in the second half of the first year. Some preliminary differences were evident between infants living in indoor cages and those living in indoor/ outdoor runs. Infants in cages spent less time in dorsal contact with mothers, and less time in social play and proximity to other animals than those in runs. Instead, infants in cages spent more time alone and engaged in more manipulation of food. Some measures of social and exploratory behavior showed a high degree of variability which may be useful in exploring individual differences in infant temperament or reactivity. © 1995 Wiley-Liss, Inc.     

Why don’tSaimiri oerstedii andCebus capucinus form mixed-species groups?

The instances of association with Cebus capucinustroops were monitored for 11 months as part of a field study of Saimiri oerstediiin a tropical wet forest in Costa Rica, Parque Nacional Corcovado. Contrary to the usual situation in South America, where S. sciureusforms persistent mixed-species groups with Cebus apella,in Corcovado S. oerstediirarely associated with Cebus capucinus;the frequencies were consistent with those expected from random association. Depending on the season, the S. oerstediitroop spent between 2.3 and 11.8% of its time in the vicinity of a Cebus capucinustroop. Most associations appeared to be chance meetings of short duration. When the two species did associate for an extended period, it was Cebus capucinus,and not S. oerstedii,that appeared to maintain the association, possibly in order to benefit from the antipredator behavior of S. oerstedii.There was no evidence that either species benefited from enhanced foraging efficiency when in association.     

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.     

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.     

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.     

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.