Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella)

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.     

Schistosoma haematobium: experimental infection in capuchin monkey, Cebus apella

South American capuchin monkeys (Cebus apella) have been included in a series of nonhuman primates under evaluation for their potential use as models in a study of the basic biology of Schistosoma haematobium. Emphasis has been given to involvement of the urogenital system, a prominent feature of infection in man. Preliminary observations on Cebus apella with moderate numbers of S. haematobium from Iran showed that there may be serious involvement of the urogenital system with development of pronounced hydronephrosis accompanied by pathobiological alteration of the urinary bladder, ureters, and kidneys. There were heavy deposits of parasite eggs in the major viscera.     

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.     

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     

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 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.     

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 complete mitochondrial genome sequence of the black-capped capuchin (Cebus apella)

The phylogenetic relationships of primates have been extensively investigated, but key issues remain unresolved. Complete mitochondrial genome (mitogenome) data have many advantages in phylogenetic analyses, but such data are available for only 46 primate species. In this work, we determined the complete mitogenome sequence of the black-capped capuchin (Cebus apella). The genome was 16,538 bp in size and consisted of 13 protein-coding genes, 22 tRNAs, two rRNAs and a control region. The genome organization, nucleotide composition and codon usage did not differ significantly from those of other primates. The control region contained several distinct repeat motifs, including a putative termination-associated sequence (TAS) and several conserved sequence blocks (CSB-F, E, D, C, B and 1). Among the protein-coding genes, the COII gene had lower nonsynonymous and synonymous substitutions rates while the ATP8 and ND4 genes had higher rates. A phylogenetic analysis using Maximum likelihood and Bayesian methods and the complete mitogenome data for platyrrhine species confirmed the basal position of the Callicebinae and the sister relationship between Atelinae and Cebidae, as well as the sister relationship between Aotinae (Aotus) and Cebinae (Cebus/Saimiri) in Cebidae. These conclusions agreed with the most recent molecular phylogenetic investigations on primates. This work provides a framework for the use of complete mitogenome information in phylogenetic analyses of the Platyrrhini and primates in general.     

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.     

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.     

Species discrimination and concept formation by rhesus monkeys (Macaca mulatta)

There are 19 species in genusMacaca and some of them are living in sympatry (Fooden, 1980). Although inter-specific hybrids are relatively easy to produce under artificial conditions, hybridization does not occur naturally. What is preventing that among the species of genusMacaca? Three rhesus monkeys acquired a discrimination between pictures with rhesus monkeys and without rhesus monkeys. All subjects showed positive transfer of this discrimination to new pictures with rhesus monkeys and without rhesus monkeys. A further test showed that these monkeys could discriminate between pictures of rhesus monkeys and pictures of Japanese monkeys. The results suggest that rhesus monkeys recognize rhesus monkeys as a class, independent of the actual stimuli such as a picture or an individual monkey. The ability to recognize members of their own species and the opportunities for such learning may be an important factor preventing hybridization among the species of genusMacaca.     

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.     

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.     

4040 SNPs for genomic analysis in the rhesus macaque (Macaca mulatta)

Although the rhesus macaque (Macaca mulatta) is commonly used for biomedical research and becoming a preferred model for translational medicine, quantification of genome-wide variation has been slow to follow the publication of the genome in 2007. Here we report the properties of 4040 single nucleotide polymorphisms discovered and validated in Chinese and Indian rhesus macaques from captive breeding colonies in the United States. Frequency-matched measures of linkage disequilibrium were much greater in the Indian sample. Although the majority of polymorphisms were shared between the two populations, rare alleles were over twice as common in the Chinese sample. Indian rhesus had higher rates of heterozygosity, as well as previously undetected substructure, potentially due to admixture from Burma in wild populations and demographic events post-captivity.     

A ten-month study of endogenous testosterone levels and behaviour in outdoor-living female rhesus monkeys (Macaca mulatta)

Endogenous testosterone levels were measured in association with sexual, aggressive, and social/affiliative behaviors in 11 outdoor-housed female rhesus monkeys over a ten-month period. Several behaviors (sex directed toward the male, sex received from the male, aggression directed toward the male, submission directed toward the male, submission directed toward the female, and groom another female) were significantly (p<0.05) positively correlated with testosterone in from one to five females. No trends were strong enough across all females to suggest that any of these correlations have species-wide significance. Factor analysis revealed clearcut clusters of behaviors, but elevations in testosterone were not strongly associated with any of these clusters. It is concluded that endogenous testosterone levels have little measurable effect on overt behavior in female rhesus monkeys.     

Varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta)

The behaviour of members of a group of rhesus monkeys was observed in experimentally created, competitive feeding situations. Socially dominant members of the group tended to start eating before lower-ranking subjects, and generally ate more. Dominants sometimes used aggression to control access to food, but overall, intermediate-ranking monkeys were involved in most agonistic episodes. Non-dominant subjects improved their feeding performance when food was presented in three piles rather than one pile, often by snatching food and consuming it away from the pile. These general patterns were less evident when realistic snake models were placed on some of the food piles. Feeding was disrupted by the presence of snakes, but notably, subordinates risked feeding in these conditions. Piles containing preferred foods and snakes were eaten from, but a low-preference food (carrot) under snakes went untouched by all subjects. The results suggest that group-members evaluate potential risks and benefits of competing for a restricted resource, and that dominance status, while an important factor, is only one element in the equation.     

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.     

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.     

Gestation length in rhesus macaques (Macaca mulatta)

We describe some of the sources of variation in gestation length among rhesus macaques. the data were obtained from the timed-mating breeding program at the California Regional Primate Research Center (CRPRC). Information about approximately 700 pregnancies that resulted in spontaneous vaginal deliveries of liveborn young is presented. The average length of these pregnancies was 166.5 days. In this population, older females with higher parities had significantly longer pregnancies and significantly heavier infants than other females did. Other factors, including infant sex, month of conception, maternal reproductive history, and paternal identity, had no consistent effect upon gestation length.     

Salivary progesterone for the assessment of the ovarian function in the capuchin monkey (Cebus apella)

Salivary and plasma progesterone were measured in normally cycling (n=10) and castrated (n=4) femaleCebus monkeys (Cebus apella). During the follicular phase, progesterone levels in saliva ranged between 0.05 and 1.40 ng/ml and in the luteal phase they increased to between 0.22 and 4.70 ng/ml. These values represented on average 6.5 and 3.2% of those values measured in plasma, for the follicular and luteal phases, respectively. The regression analysis of the steroid concentrations in both fluids showed a highly significant correlation (r=0.8985,n=180,P<0.0001). Ovariectomized monkeys had consistently low salivary (0.37±0.02 ng/ml) and plasma (4.70±0.25 ng/ml) progesterone, showing a low, but significnat, correlation coefficient (r=0.2592,n=58,P=0.047). The ratio of plasma/salivary progesterone was significantly higher in the luteal phase (31.09±1.65) than in the follicular phase (23.06±2.26) and in castrated monkeys (16.00±1.38). The free fraction of progesterone constituted 5.3±0.2% of the total plasma progesterone during the follicular phase and 3.3±0.1% during the luteal phase. Ovariectomized monkeys showed a significantly higher percentage of free progesterone in plasma (7.7±0.1%). In contrast, free progesterone made up 64.4 and 70.9% of the total salivary progesterone for the follicular and luteal phases, respectively. The proportion of free progesterone in castrated animals was within the range observed in cycling animals. We suggest that the levels of progesterone in the saliva of capuchin monkey follow a pattern similar to that for plasma progesterone, reflecting the free steroid fraction. Thus, the measurement of such steroid in saliva may offer a valuable alternative to plasma determinations for the assessment of the ovarian function inCebus and probably other New World monkey species.