Introduction and integration of strangers into captive groups of tufted capuchins (Cebus apella)

We introduced two to four unfamiliar animals into three established groups (N = 6–9 per group) of tufted capuchins (Cebus apella).We present findings on the behavioral consequences of introductions as a function of age, sex, and residency status and long-term consequences for health and reproduction. No morbidity from aggression occurred at the time of introductions or during several months following, and reproduction was not compromised. Activity budgets and patterns of social spacing and interaction were little changed following the introductions except for increases in vigilance behavior, especially by newly introduced adult females. Adult females exhibited the strongest and longest-lasting response to changes in group composition. The results indicate that in this species (1) introductions of adult females can be carried out with acceptable risk to the newcomers provided that careful monitoring occurs, so that the onset of severe aggression instigated by resident females toward new females can be avoided, (2) juveniles can be introduced with minimal risk, and (3) adult males can be introduced into groups lacking resident adult males with minimal risk. Capuchins differ in important ways from the better-studied Old World monkeys in their response to introductions of strangers. The differences are instructive with regard to processes supporting species-typical social structure, which is less overtly hierarchical in capuchins than in macaques.     

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.     

Milk composition of captive tufted capuchins (Cebus apella)

Little is known about the milk composition of nonhuman primates, and it has never been examined in capuchin monkeys (genus Cebus). This article reports on the macronutrient milk composition (fat, crude protein (CP), lactose, dry matter (DM), and total gross energy (GE)) of captive housed tufted capuchins (Cebus apella) (n=8). C. apella milk averaged 5.22% fat, 2.40% CP, 6.94% lactose, 16.48% DM, and 0.89 kcal/g. Fat was the most variable macronutrient and was significantly higher in samples collected after 2 months of lactation. To explore the adaptive significance of C. apella milk composition, results were compared with data on milk composition from a closely related cebid, Saimiri boliviensis boliviensis, and another large‐brained anthropoid, Homo sapiens. C. apella milk was only significantly different from Saimiri milk in CP and the proportion of energy from CP. Compared with human milk, C. apella milk was lower in lactose but higher in fat, CP, DM, GE, and the proportion of energy from CP. Results from this small dataset suggest that among anthropoid primates, the macronutrient composition of milk is influenced by phylogeny, may vary relative to infant growth rates, but may not be related in any direct way to relative brain size. Am. J. Primatol. 72:81–86, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Object concept and mental representation inCebus apella andMacaca fascicularis

The achievement of Stage 6 object concept as an index of the representational capacity, was studied both in juveniles and adults of two nonhuman primate species,Cebus apella andMacaca fascicularis. The general goal of the present investigation was to evaluate the real nature of the strategy adopted by subjects searching an object in the invisible displacement task. To this purpose, the original Piagetian version of the invisible displacement task was used modifying some parameters and employing additional tasks and analyses in order to differentiate representational solutions from the nonrepresentational ones. With this method it was found that an adult cebus, but not macaques, solved the invisible displacement task with the use of the mental representation.     

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.     

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.     

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     

Perception of stimuli presented as photographic slides in cynomolgus macaques (Macaca fascicularis)

The present study was designed to assess a monkey's perception of specific visual stimuli by measuring both the behavioral responses and duration of attention to the presentation of photographic slides. Five adult male cynomolgus macaques (Macaca fascicularis) were placed individually in an open field apparatus and presented a series of slides consisting of apples, a gorilla mask, a collage of colors, a human being, and a plain field. The slide of the gorilla mask followed by that of the human being received the most attention while the plain field received the least. In addition, the gorilla mask and human being elicited a range of behavioral responses with the higher ranking animals displaying a greater number of aggressive responses and the lower ranking animals displaying a greater number of submissive gestures. Taken together, these data would suggest that the slides of the gorilla mask and the human being were perceived by the monkeys as threatening. These results are consistent with a continuing theme observed among a number of studies of primate social perception — namely, that potentially threatening stimuli are a significant determinant of visual observing.     

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.     

Growth and reproduction in captive tufted capuchins (Cebus apella)

We present data on weight and reproduction from a colony of tufted capuchins monkeys (Cebus apella) over a 12 year period. The data constitute a normative record for this species. Weight at birth averages 210 g, and infants gain weight rapidly. Females typically first conceived just after their fifth birthday, and males were fertile by 4 years, 5 months. Interbirth intervals average 576 days. Eighty-seven percent of live-born infants survived past 6 months. Three of eight live-born infants that died prior to 6 months succumbed from trauma inflicted by cage mates. Am. J. Primatol. 44:197–203, 1998. © 1998 Wiley-Liss, Inc.     

The extensor and peroneal muscles of the crab-eating monkey (Macaca fascicularis)

On the basis of 60 hindlimbs of 30 crab-eating monkeys (Macaca fascicularis) of each sex, the morphology of the crural extensor and the peroneal group of leg muscles is described and some functional indices are calculated. For the attachments and measurements of the muscles, the results obtained in this study generally agreed with those of otherMacaca species. The crural extensor has minor differences. Some anomalous modes of insertion are observed in the peroneal group. These results indicate the phyletically labile state of the peronei in the crab-eating monkey.     

Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis)

Summary The seeds in fruits consumed by primates may be chewed and digested, swallowed and defecated intact, or separated from the flesh and spat out. We show by a combination of close field observations and experiments with caged animals, that long-tailed macaques (Macaca fascicularis) have a remarkably low threshold of 3–4 mm for swallowing seeds and also that wild macaques rarely break them. The seeds of 69% of the ripe fruit species eaten are spat out intact or cleaned outside the mouth and dropped. Seed-spitting significantly reduces the swallowed food bulk and may lessen the risk of releasing seed toxins during mastication. However, it requires that even small fruits are processed in the mouth one or a few at a time. We suggest that fruit storage in the cheek pouches of cercopithecine monkeys allows them to spit seeds individually without excessively slowing fruit intake while feeding on patchily distributed fruit. In contrast, Apes and New World monkeys apparently swallow and defecate most ripe seeds in their diet and colobine monkeys break and digest them, detoxifying seed defenses by bacterial fermentation.     

Conceptual thresholds for same and different in old-(Macaca mulatta) and new-world (Cebus apella) monkeys

Learning of the relational same/different (S/D) concept has been demonstrated to be largely dependent upon stimulus sets containing more than two items for pigeons and old-world monkeys. Stimulus arrays containing several images for use in same/different discrimination procures (e.g. 16 identical images vs. 16 nonidentical images) have been shown to facilitate and even be necessary for learning of relational concepts ( [Flemming et al., 2007], [Wasserman et al., 2001] and [Young et al., 1997]). In the present study, we investigate the threshold at which a new world primate, the capuchin (Cebus apella) may be able to make such a discrimination. Utilizing a method of increasing entropy, rather than conventional procedures of decreasing entropy, we demonstrate unique evidence that capuchin monkeys are readily capable of making 2-item relational S/D conditional discriminations. In another experiment, we examine the supposed level of difficulty in making S/D discriminations by rhesus monkeys (Macaca mulatta). Whereas pigeons (Columba livia) and baboons (Papio papio) have shown marked difficulty simultaneously discriminating same from different arrays at all when composed of fewer than 8 items each, rhesus monkeys seem to understand that pairs of stimuli connote sameness and difference just the same (Flemming et al., 2007). With sustained accurate performance of 2-item S/D discriminations, both experienced and task-naïve rhesus monkeys appear quite certain in their conceptual knowledge of same and different. We conclude that learning of the same/different relational concept may be less dependent upon high levels of entropy contrast than originally hypothesized for nonhuman primates.     

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.     

Genetic characterization of long-tailed macaques (Macaca fascicularis) on Tabuan Island Indonesia

Protein and mitochondrial DNA variations (D-loop region PCR-RFLP) were analyzed for 7 serum and 40 clot samples collected from long-tailed macaques (Macaca fascicularis) living on Tabuan Island, Indonesia. Protein polymorphisms were examined electrophoretically for 5 and 12 kinds of protein in serum and erythrocytes, respectively. Each of the protein loci tested showed a monomorphic pattern. Polymorphisms were detected in the analysis of the D-loop-containing region of mtDNA (PCR-RFLP) using 32 restriction endonucleases. Two haplotypes, differing 1.03% in sequence divergence were observed, and both were previously undetected in other local populations. Based on genetic features and differences in pelage color as outlined inFooden's (1995) morphological analysis, the present results suggest that long-tailed macaques on Tabuan Island are a unique population. From the genetic analyses performed here, Tabuan monkeys are considered to be the same species group as those populations of Sumatra and Java (Fooden, 1995).     

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.     

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.