Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella)

The responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella) were investigated. In both species the amount of fear behavior was higher in the presence of the model than during baseline conditions. Unlike the macaques, in the capuchins the frequency of these behaviors decreased across trials. In the two species the amount of explorative and manipulative behaviors and the use of space were also different. Unlike macaques, all capuchins manipulated the objects available in the testing room, and three subjects contacted the apparatus by using objects. Macaques did not show significant preferences for any particular part of the testing room. In both conditions, capuchins used the floor more than macaques did. Further, capuchins increased the use of the floor across experimental trials. Latency to reach the floor was higher in macaques than in capuchins. When on the floor, capuchins spent most of the time close to the snake apparatus. It is proposed that the behavioral differences between capuchins and macaques in the responses to a potential predator indicate that capuchins have a greater propensity to explore and to contact the novel stimulus directly, or by means of objects, than macaques do. These tendencies may lead to the exploitation of novel features in the environment.     

Reunion displays in captive male brown capuchins (Cebus apella)

Separation and subsequent reintroduction of brown capuchins (Cebus apella) can lead to reunion displays during which individuals will embrace and emit high-pitched, loud vocalizations. These displays were investigated in three male capuchins: two adults and one juvenile. These subjects were part of a larger captive social group held at the Capuchin Laboratory, Hiram College, OH, USA. We hypothesized that males would engage in reunion displays following separation regardless of the order of reintroduction, as evidence of an affiliative bond judged by concurrent social behavior. Sixty separations were conducted as part of weekly husbandry over a period of 13 months. Occurrence of reunion displays between the males was recorded with the initiator also noted. Reunion displays among males were found to occur only between the juvenile and alpha male, and all displays were initiated by the juvenile. Displays were highly influenced by the order of reintroduction. We suggest that reunion displays operate to reaffirm social relationships, particularly during situations of social tension.     

Response to novel housing in two groups of captive tufted capuchin monkeys (Cebus apella)

The influence of age, maternal status, and the presence of a group male on use of space was assessed in two groups of captive tufted capuchin monkeys that underwent a move from indoor housing to a larger outdoor facility. Both groups originally contained two adult males, but only one group retained a male after the move. Following the move, mothers spent less time on the ground when carrying their infants than they did when not carrying their infants. In the group with no male (1) individuals decreased time spent on the ground relative to pre-move levels, whereas no such difference was noted in the group with the male; (2) females spent more time carrying their infants than did females in the group with a male. In the group with the adult male, juveniles spent less time on the ground than did non-mother adult females, whereas no difference had existed prior to the move. Grooming rates dropped from pre-move to post-move, but the mean number of partners with which each animal was in contact increased. Measures of social behavior varied across post-move observation periods inversely to time spent on the ground. These results are consistent with the view that an individual's relative vulnerability influences behavioral conservatism in novel environments, and suggests a relatively profound role for males in promoting exploration of new space in this species.     

The stone tools of capuchins (Cebus apella)

We examined the production of stone took by capuchins (Cebus apella). Eleven subjects used five reduction techniques to produce 346 stone tools (48 cores and 298 flakes). They produced a sharp edge on 83% of the cores and largest flakes. Three monkeys later used a sample of these objects as cutting tools. These results demonstrate that monkeys produce lithic tools analogous to those produced by Oldowan hominids.     

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.     

Olfactory discrimination of urine odors from five species by tufted capuchin (Cebus apella)

Urine collected from New World monkeys (tufted capuchin, squirrel monkey, cotton-top tamarin) and Old World monkeys (rhesus macaque, Japanese macaque), was used as the odor stimuli. Two adult tufted capuchins were trained on a successive odor-discrimination task with two odors, 30 trials each, in one session per day. Responses to one of the two odors (S+) were reinforced by sweet water. The monkeys failed to discriminate between the urine from the two species of macaques but could discriminate among the urine from the three species of New World monkeys. Furthermore, similarity of urine odors was analyzed by multi-dimensional scaling (MDS) and a cluster analysis. These analysis suggested that the tufted capuchin can distinguish differences among New World monkeys but not between the macaques. The natural distribution of the tufted capuchin overlaps with that of other New World monkeys, but it does not overlap with those of Old World monkeys. Consequently, it can be concluded that this difference in olfactory recognition in the tufted capuchin reflects their sympatric and allopatric relationships with other species.     

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.     

Sex differences in play behavior in juvenile tufted capuchin monkeys (Cebus apella)

According to the motor training hypothesis, play behavior in juvenile primates improves motor skills that are required in later adult life. Sex differences in juvenile play behavior can therefore be expected when adult animals assume distinct sexually dimorphic roles. Tufted capuchin monkeys show sexually dimorphic levels of physical antagonism in both inter- and intra-group encounters. Accordingly, it can be predicted that juvenile capuchins also show sex differences in social play behavior. To test this hypothesis, the play behavior of nine juvenile and two infant capuchins was examined. As predicted, juvenile males showed significantly higher levels of social play (wrestle, chase) than juvenile females, but no differences were found in nonsocial play (arboreal, object). Levels of infant play behavior were comparable to that of juveniles. These results lend support to the motor training hypothesis and highlight the need for more detailed investigations of individual differences in play behavior. An erratum to this article can be found at     

Coping with Acute Crowding by Cebus apella

Traditionally, scientists believed that crowded housing conditions increased aggression in animals. Recent research on captive primates fails to support a linear relationship between population density and aggressive behavior. Our study is the first to investigate the effects of acute crowding on a New World primate. We observed brown capuchins (Cebus apella) under 2 different spatial conditions: a control that offered the full indoor space in the enclosure and a short-term experimental condition that restricted the capuchins to approximately half the amount of space of the control condition. We compared rates of self-grooming, aggression, contact sitting, social grooming, and play between both conditions. We conducted a mixed factorial ANOVA at the individual level while taking subject sex and age class into account. Intense aggression, play, and social grooming decreased significantly in crowded conditions, suggesting that capuchins avoid social encounters if spatially confined. Their strategy for coping with acute crowding via a decrease in all forms of social behavior is intermediate between chimpanzee and macaque strategies in similar experiments. The only behavior to increase under crowding was a nonsocial, self-directed behavior with the potential of reducing arousal: self-grooming.     

The use of probing tools by tufted capuchins (cebus apella): evidence for increased right-hand preference with age

We examined hand preference in the use of tools by tufted capuchins (Cebus apella). We presented a colony of monkeys with an enclosed container designed to accommodate the use of probing tools. Over an 8-month period, 13 monkeys used probes to extract sweet syrup from the narrow opening of the apparatus. Five monkeys exhibited bias toward use of their right hand and eight monkeys exhibited bias toward use of their left hand. Adult monkeys exhibited a greater percentage of right-hand preferent probing sequences than did juveniles. These results are consistent with hypotheses that in tasks that involve the use of tools, nonhuman primates exhibit strong lateral asymmetries at the individual level, a moderate left-hand bias at the population level, and increased bias with age toward use of the right hand.     

Hand Preferences in Different Tasks by Tufted Capuchins (Cebus apella)

We examined hand preferences in 25 tufted capuchins (Cebus apella) in three tasks. The hole task involved a single action of reaching for food in a hole. The horizontal panel and the vertical panel tasks required the alignment of two apertures, by moving or lifting a panel, to reach for food in a hole. We found a significant group-level right-hand preference for reaching actions in the hole and in the horizontal panel tasks, but not in the vertical panel task, in which the food retrieval implied the complementary use of both hands. No significant hand bias emerged for moving or lifting actions with high visuospatial components. There is a stronger hand preference in more complex manual activity—coordinated bimanual hand use for food retrieval—than in other unimanual measures. We discuss the results in the context of previous reports on primate laterality.     

Use of a tool-set by capuchin monkeys (Cebus apella)

The purpose of this study was to examine the use of a tool-set by capuchin monkeys (Cebus apella). Capuchins were presented with an apparatus designed to accommodate the use of pounding tools to crack walnuts and the use of probing tools to loosen and extract the inner meat. Three capuchins used stones and sticks sequentially for these purposes. The capuchins' behavior was similar in form and function to behavior that has been reported for chimpanzees in analogous situations. These results provide further evidence of the extensive tool-using capabilities of capuchin monkeys and are consistent with a hypothesis of cross-species continuity in the skillful use of tools by primates.     

Responses of capuchin monkeys (Cebus apella) to different conditions of mirror-image stimulation

Group-living brown capuchins were given mirror-image stimulation as follows: (1) mirror 1 m away; (2) mirror attached to the cage-mesh; (3) angled mirrors creating a deflected image; (4) small mirror in the cage; and (5) small, transportable mirrors. The subjects were initially interested in the mirrors in each condition, but they generally habituated to them over the course of repeated presentations. Control (non-reflective) objects were attended to less than mirrors. Facial expressions occurred mostly in Condition 2, lateral and vertical head movements in Condition 3, reaching behind the mirror in Condition 2, looking obliquely into the mirror in Conditions 4 and 5. Despite these diverse conditions of exposure to mirrors, lasting for a total of over three months, no behaviours suggesting self-recognition were seen in the monkeys.     

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.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

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.     

Male reunion displays in tufted capuchin monkeys (Cebus apella)

When males in captive tufted capuchin monkey (Cebus apella) groups separate and come together within their group, they have been observed to embrace and vocalize upon reunion. This display has not been observed in any other age/sex class. To investigate this, we deliberately separated six animals, including the only two adult males, from each of two social groups. We hypothesized that only the adult males would embrace upon reintroduction. When two males were consecutively reintroduced to their group, they typically ran to each other and came together in a frontal embrace, emitting stereotyped vocalizations. No other combination of animals showed this “reunion display.” Though dramatic, this behavior was in no way associated with incidents of aggression. We argue affiliative bonds may exist in these tufted capuchin male dyads. © 1996 Wiley-Liss, Inc.     

Activity and ranging patterns in relation to fruit utilization by Brown Capuchins (Cebus apella) in French Guiana

I studied brown capuchins (Cebus apella)in primary forest in French Guiana. They displayed different feeding and ranging patterns in response to changes in fruit availability and distribution. When fruit was scarce and patchily distributed, foliage/stem feeding and invertebrate foraging was high, and capuchins limited their daily movement to <2 km, focusing on large fruit patches. When fruit was in average supply and scattered throughout the forest, the proportions of foliage/stems and invertebrates in the diet decreased, and the day range length increased to 2.8 km. When fruit was abundant and widespread, foliage/stems were rarely eaten, while invertebrate foraging increased, and. the daily locomotor distance was reduced to 2 km.     

Response of Cebus apella to Foods Flavored with Familiar or Novel Odor

What cues support social influences on food preference in tufted capuchins? Although vision is important for food discrimination, we hypothesized that olfactory cues might also be involved. In Experiment 1, we assessed whether semolina flavored with a novel odor and eaten by a demonstrator, elicits more interest than semolina flavored with a familiar odor and eaten by a demonstrator, and to what extent the observer's interest towards the demonstrator was elicited by the food itself or by the odor impregnating the demonstrator's oral area. In Experiment 2, we investigated whether having encountered a novel odor in a social context increases the observer's subsequent consumption of semolina carrying this odor versus semolina carrying another novel odor previously encountered in a non-social context. We tested 15 demonstrator-observer pairs. Eight observers were offspring of the demonstrator; 7 observers were not offspring of the demonstrator. Offspring (but not non-offspring) expressed interest towards the demonstrator's food significantly more when the odor was novel than when it was familiar. Offspring (but not non-offspring) were more interested when the demonstrator's food was present than when only its odor was available. Finally, having encountered the novel odor in the social context did not lead to greater consumption. Our findings demonstrate that in closely bonded pairs, foods carrying novel odors elicit interest, though it is prompted mainly by the food itself. In contrast with other macrosmatic mammalian species, capuchin consumption of a food whose odor was previously encountered in a social context was not greater than that of a food whose odor was previously encountered when alone.     

Problem-Solving Strategies and Hand Preferences for a Multicomponent Task by Tufted Capuchins (Cebus apella)

We examined hand preferences in 23 tufted capuchins (Cebus apella) in 2 tasks requiring the lid of a box to be lifted before taking out a peanut. The first task, Box 1, could entail either 2 or 3 problem-solving acts, with the 3-act solution involving bimanual coordination for food retrieval. The second task, Box 2, involved only the 3-act solution. The results indicated that the types of solution employed to perform the task influenced capuchin hand preferences. In the 2-act solution, capuchins exhibited a significant right-hand bias for the final one-handed reaching action, but not for the initial lid lifting action. In contrast, in the 3-act solution, no significant asymmetry emerged for any act. We noted a significant effect of subject's sex on the strength of laterality, with males being more strongly lateralized than females. We discuss results in the light of recent models of primate laterality.