Social facilitation of exploratory foraging behavior in capuchin monkeys (Cebus apella)

Much of the research on animal social learning focuses on complex cognitive functions such as imitation and emulation. When compelling evidence for such processes is not forthcoming, simpler processes are often assumed but rarely directly tested for. In this study we address the phenomenon of social facilitation, whereby the presence of a feeding conspecific is hypothesized to affect the motivation and behavior of the subject, elevating the likelihood of exploration and discovery in relation to the task at hand. Using a novel foraging task, sufficiently challenging that only just over half the subjects successfully gained food from it, we compared the performance of capuchin monkeys working either alone, or in a “social” condition where an actively feeding conspecific was in an adjacent chamber. Although similar numbers of subjects in these conditions were eventually successful during the 20 trials presented, the latency to successful solution of the task was over three times faster for monkeys in the social condition. The minority of monkeys that failed to learn (9/23) were then exposed to a proficient model. Only those older than 5 years provided evidence of learning from this. Accordingly, we obtained evidence for the social facilitation the study was designed to test for, and limited supplementary evidence for social learning in the older individuals who had not learned individually. These results are discussed in relation to other recent evidence for social learning in monkeys. Am. J. Primatol. 71:419–426, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

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.     

Substrate optimization in nut cracking by capuchin monkeys (Cebus apella)

We conducted an experiment to examine the effect of substrate on the nut-cracking behavior of a group of semicaptive capuchin monkeys. We wanted to determine whether tufted capuchin monkeys were selective in choosing the substrate on which they pound nuts, and whether the choice of substrate affected the outcome. Eight adult females and eight juveniles were provided with nuts in the outdoor facility. We found that 1) all adult females and three young capuchins succeeded in cracking nuts; 2) they preferred the hardest substrates (concrete and stone); 3) there is a link between the substrate and the amount of time needed to crack a nut; 4) most young capuchins used various substrates, some of which were inadequate, in a haphazard manner; and 5) there are different forms of nut cracking. We conclude that adult capuchins choose the hardest substrates, and that these substrates support efficient cracking.     

Prey capture efficiency in brown capuchin monkeys (Cebus apella) is influenced by sex and corpus callosum morphology

The diet of capuchin monkeys consists largely of fruits, but these monkeys commonly prey upon insects and other invertebrates as well as vertebrates such as lizards, birds, and fish. Capturing small fast‐moving prey requires the ability to process complex visuospatial information such as motion detection, shape, and pursuit. Here we report the results of an experimental investigation into whether capuchins display sex differences in prey capture efficiency, and whether these differences are associated with the morphology of regions of the corpus callosum (CC) involved in visuospatial ability. We examined the prey capture behavior of seven capuchin subjects (four female, three male) in the laboratory by providing subjects opportunities to fish. Additionally, we obtained structural magnetic resonance images from these subjects to determine if spatial‐ability was related to CC anatomy. Over 30 fishing trials, we recorded the number of prey capture attempts, success rate in capturing fish, and hand techniques used in these attempts. Males were significantly faster and more successful than females at capturing prey. In addition, males had smaller total CC:brain ratios than females. Males displayed a left hand bias, as well as significant unimanual usage, whereas females displayed no significant preference for hand usage. Individual capture times were correlated with total CC:brain ratio. Taken together, our results suggest a relationship between prey capture efficiency, sex, and the degree of brain lateralization. Am. J. Primatol. 72:502–508, 2010. © 2010 Wiley‐Liss, Inc.     

Summation and quantity judgments of sequentially presented sets by capuchin monkeys (Cebus apella)

Capuchin monkeys (Cebus apella) were presented with two sets of food items, identical in food type but differing in number. Animals selected one set and were permitted to consume their choice. Set sizes ranged from 1 to 6 items. In experiment 1, each set was uncovered and recovered before a response was made, and the monkeys selected the larger set at high levels. Experiment 2 presented sets that had both visible and nonvisible food items in them at the time of the response, thus requiring the monkeys to sum the total amount of food that was available. The monkeys again selected the larger set with no decrement in performance. Overall, the data indicate that capuchins, like other more extensively studied primate species in this area of research, are responsive to quantitative differences between sets. Capuchins succeed in making these quantity judgments when sets are nonvisible at choice time and when summation of items must be performed, thus demonstrating coordination of quantification skills and memory. Capuchins also inhibit responses to visible food items when those items are only part of an overall smaller quantity of food compared with a completely nonvisible set.     

Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks

In Experiment 1, three capuchin monkeys (Cebus apella) were exposed to a mirror in their home cage for 3 days and then given food treats for touching orange marks located on the surface of an experimental chamber. Following training, a mirror was added to the chamber to see if the monkeys would use it to guide non-reinforced contacts with an orange mark on their foreheads that was only visible as a mirror reflection (mark test). Two monkeys touched the head-mark more often with the mirror present than absent, but no mark touches were emitted while looking at the mirror. In Experiment 2, the monkeys were rewarded for touching orange marks on their bodies that were directly visible, followed by another head-mark test. Again, two monkeys touched the mark more often with the mirror present than absent, but these contacts were not emitted while looking at the mirror. Since facing the mirror while mark touching was not required for reinforcement during training, Experiment 3 further tested the possibility that increased mark touching in the presence of the mirror during Experiments 1 and 2 was the result of a memorial process. For this, a final, novel mark test was conducted using an orange mark on the neck that was only visible as a reflection (Experiment 3). No monkeys passed this test. These are the first mark tests given to capuchin monkeys. The results are consistent with the finding that no monkey species is capable of spontaneous mirror self-recognition. The implications of sequential training and mark testing for comparative evaluations of mirror self-recognition capacity are discussed.     

Intraspecific chromosome variation in Cebus apella (cebidae,platyrrhini): The chromosomes of the yellow breasted capuchin Cebus apella xanthosternos wied, 1820

Chromosome studies in six wild-caught specimens of Cebus apella xanthosternos showed a distinctive chromosome pair number 11 that made it possible to distinguish this subspecies from other Cebus apella. The characteristic chromosome pair had intercalar heterochromatin unlike the “standard” chromosome type of Cebus apella and other species of the same genus, in which this chromosome pair shows a large, terminal, heterochromatic block. A comparison at the chromosomal level between different Cebus apella populations suggests that chromosome 11 in Cebus apella xanthosternos is a derived chromosome that has probably become fixed in this subspecies, either by selection or by drift in a small isolated population.     

Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus)

Tufted capuchin monkeys (Cebus apella) provide an extreme example of active female sexual solicitation of males. In spite of being targeted by females for sex, males may delay copulation for hours or days. Data were collected on the sexual interactions in one wild capuchin group at the Estação Biológica de Caratinga in Brazil from September 1996 to August 1997. All successful conceptions during this year occurred in the dry season, yet sexual behavior was observed during 9 months of the year. This study tested whether male sexual response to female proceptivity was seasonally‐mediated. Male consortship participation, solicitation of females, latency to copulation, and copulation frequency were compared between fertile and nonconceptive females. Seasonal patterns in copulation interference, mating style, and alternative mating strategies were also examined. Thirty‐two copulations were observed. The alpha male was solicited for significantly more consortship days per female, but his mating success, in terms of copulation frequency, did not differ from that of two other adult males in the group. In the dry season, when the females were fertile, the males showed increased contest competition for mates, a higher frequency of alternative mating strategies against copulation interference, and increased monitoring of the females' condition. However, contrary to expectations, the alpha male's latency to copulation was significantly longer in the fertile season than in the nonconceptive months, and no males were observed to mate more than one time per day, even at the conceptive peak. Male mating strategies were affected by both season and rank, and there was evidence for reproductive constraints on males throughout the year. Limited male ejaculatory capacity and male choice in the timing of copulations within female proceptive phases may both be important factors in driving the sexual dynamics of this species. Am. J. Primatol. 67:313–328, 2005. © 2005 Wiley‐Liss, Inc.     

Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella)

Numerous studies investigating behavioral lateralization in capuchins have been published. Although some research groups have reported a population-level hand preference, other researchers have argued that capuchins do not show hand preference at the population level. As task complexity influences the expression of handedness in other primate species, the purpose of this study was to collect hand preference data across a variety of high- and low-level tasks to evaluate how task complexity influences the expression of hand preference in capuchins. We tested eleven captive brown capuchin monkeys (Cebus apella) to determine if they show consistent hand preferences across multiple high- and low-level tasks. Capuchins were expected to display high intertask consistency across the high-level tasks but not the low-level tasks. Although most individuals showed significant hand preferences for each task, only two of the high-level tasks that involved similar hand motions were significantly positively correlated, indicating consistency of hand preference across these tasks only. None of the tasks elicited a group-level hand preference. High-level tasks elicited a greater strength of hand preference than did low-level tasks. No sex differences were found for the direction or strength of hand preference for any task. These results contribute to the growing database of primate laterality and provide additional evidence that capuchins do not display group-level hand preferences.     

Hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella)

The purpose of this study was to examine the hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella). Two experiments were conducted. In Experiment 1 capuchins were presented with an apparatus designed to accommodate the use of probing tools. In Experiment 2 the same capuchins were presented with sets of nesting containers. Five of the ten subjects used probing tools and seven subjects placed objects in the containers. The capuchins' behavior reflected three hierarchically organized combinatorial patterns displayed by chimpanzees and human infants. Although the capuchins sometimes displayed the two more complex patterns (“pot” and “subassembly”), their combinatorial behavior was dominated by the simplest pattern (“pairing”). In this regard capuchins may not attain the same grammar of manipulative action that has been reported for chimpanzees and young human children. © 1994 Wiley-Liss, Inc.     

Social context and consumption of unfamiliar foods by capuchin monkeys (Cebus apella) over repeated encounters

Visalberghi and Fragaszy [Animal Behaviour 49:1089–1095, 1995] have shown that social influences affect acceptance of novel foods. However, little is known about the temporal course on which such influences act (e.g., for how long they persist and for how many encounters they are effective). To explore this issue, 11 adult tufted capuchins were observed during ten successive encounters with eight unfamiliar foods (phase 1, in which subjects were tested in social or individual condition) and ten more encounters 6 months later (phase 2, in which all subjects were tested in social condition). A total of 680 observational sessions were carried out. Results show that during the first five encounters in phase 1, capuchins ate more when they encountered these foods in the presence of their groupmates than if they encountered them alone. Thereafter, during the second five encounters of phase 1, foods were consumed equivalently whether presented to monkeys socially or individually. In phase 2, the foods were consumed equivalently regardless of the previous circumstance of their presentation (social or alone). In phase 2, consumption was similar to that scored in a previous study for familiar foods [Visalberghi & Fragaszy, Animal Behaviour 49:1089–1095, 1995]. We conclude that 1) foods remain unfamiliar to capuchins only for the first few encounters, 2) social facilitation of consumption of unfamiliar foods is of limited duration, and 3) individuals consumed equivalent amounts of an unfamiliar food when they repeatedly encountered it alone or in the presence of groupmates. These results caution those who interpret similar feeding habits in primate groups as evidence of social influences. Am. J. Primatol. 45:367–380, 1998. © 1998 Wiley-Liss, Inc.     

The relationship between locomotor behavior and limb morphology in brown (Cebus apella) and weeper (Cebus olivaceus) capuchins

This study is a comparison of locomotor behavior and postcranial form in two species of capuchin monkey, the brown capuchin (Cebus apella), and the weeper capuchin (Cebus olivaceus). Behavioral data from groups of wild C. apella and C. olivaceus in Guyana were collected during the period of December 1999 through November 2000. Postcranial variables including 40 measurements and three indices were taken from 43 adult and subadult specimens of C. apella and 14 adult and subadult specimens of C. olivaceus housed in American museums, as well as two wild-caught adult specimens of C. olivaceus from the Georgetown Zoo in Guyana. The results of this study indicate that these two capuchins exhibit similar patterns of locomotor behavior, but that there are important differences in how they move through their homerange, particularly with respect to quadrupedalism. These differences in behavior are reflected in their postcranial morphology and can be related to differences in foraging strategies. This study provides an example of the importance of using more exclusive categories of quadrupedal behaviors when comparing closely related arboreal quadrupeds, as well as an alternative explanation for some of the postcranial features of C. apella that may relate to foraging postures and foraging strategy rather than traditionally categorized patterns of locomotor behavior.     

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.     

Preliminary data on voluntary food sharing in brown capuchin monkeys

Spontaneous interactions over fruits and vegetables were observed in a captive group of Cebus apella. The group lacked fully grown males; 3 adult females dominated the remaining 11 individuals, most of which were adolescents and late juveniles. Apart from expressions of interest and unsuccessful attempts to claim food, interactions over food included two types of interindividual food transfer: forced claims (i.e., involuntary transfers) and peaceful sharing. These two categories represented 7.2% and 20.3% of 3,389 observed food interactions, respectively. Sharing of food was subdivided into four categories; the most frequent category was the collection of discarded food items from within reach of the possessor, and the least frequent was active giving of food items by the possessor. The voluntary nature of food transfers was further investigated in an experiment in which two monkeys were placed in adjacent cages with a wire-mesh partition between them. One subject received food; the other did not. Although this setup made it easy for possessors to prevent food transfers, sharing occurred in all 18 tests on different combinations of individuals. In 10 of the tests, possessors were observed to actively push food through the mesh partition to their partner. © 1993 Wiley-Liss, Inc.     

Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella)

The aim of this study was to evaluate simple behavioral enrichment procedures for a captive group of tufted capuchin monkeys (Cebus apella). We examined the effects of providing a manipulatable substrate (straw) and a variety of portable objects in the monkeys' home cage. The animals were observed across three conditions in two replications: 1) No portable objects were present; 2) a set of six identical portable objects was present; and 3) a set of six varied portable objects was present. The cage floor was bare in the first replication; straw was uniformly spread on the cage floor in the second replication. An 18-month period of qualitative note taking followed completion of the initial data collection phase. The presence of straw and portable objects affected patterns of affiliation by decreasing quiet contact and close proximity. Providing additional manipulative opportunities affected both the form and frequency of object-directed activities. Object contacts were directed toward a greater variety of targets, and some objects were spontaneously used as tools. Manipulation of provided objects and use of objects as tools have become routine activities in this group of monkeys. We conclude that providing straw and portable objects in an already well equipped cage is an effective means of long-term behavioral enrichment for captive capuchin monkeys. Enabling captive capuchins to express species-typical manipulative tendencies is apparently conducive to the monkeys' optimal physical and psychological well-being as well as interesting to the human observer.     

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.     

Partner effects on food consumption in brown capuchin monkeys

It has been claimed that capuchin monkeys (Cebus apella) show inequity aversion in relation to food rewards for a simple exchange task. However, other factors may affect the willingness of a monkey to consume foods of high or low value in the presence of a conspecific. In this study, pairs of monkeys were presented with unequally valued foods, but without any task-performance: they simply received the food under four experimental conditions. By looking at the rate of collection and consumption of low-valued cucumber slices we expected to see variation dependent on whether the partner either had 1) cucumber (equity), 2) grape (inequity), 3) inaccessible cucumber or 4) inaccessible grape. Testing 12 adult capuchin monkeys, our findings differed from those of other authors in that the monkeys failed to show negative reactions to inequity, but rather responded with scramble competition (i.e., fast food collection) in the presence of a conspecific without access to food. They also showed facilitated consumption in the presence of a conspecific consuming high-valued food. Possibly, (in)equity plays a different role if food serves as a reward for a task rather than if it is simply made available for consumption.     

Sexual dimorphism and interspecific cranial form in two capuchin species: Cebus albifrons and C. apella

Ontogenetic patterns of sexual dimorphism and cranial form in two capuchin monkeys, Cebus albifrons and C. apella, are investigated by means of univariate, bivariate, and multivariate statistics. The analyses are based on 23 linear variables. Univariate analyses indicate that similar ontogenetic patterns of cranial sexual dimorphism are present; however, interspecific differences exist in timing. Ontogenetic scaling is present in both species' crania; however, it is more prevalent in C. albifrons. Several departures are present in cranial regions associated with orbital shape, the dental arcade, and the muscles of mastication. The latter two indicate that sexual differences in diet and/or foraging strategies may exist. Sexual selection is suggested as being the primary selective regime underlying the observed patterns of cranial sexual dimorphism in each species. Interspecific comparisons confirm that C. apella possesses a more dimorphic cranium than C. albifrons and that sexual dimorphism in C. apella begins earlier in development. Although interspecific ontogenetic scaling is present in some cranial variables, C. apella is not just a scaled-up version of C. albifrons. These sympatric congeners seem to be differentiated by variables related to the orbital region and the masticatory apparatus, as indicated by both departures from ontogenetic scaling and results of the discriminant function analysis. Ecological selection, rather than varying degrees of sexual selection, is likely to be responsible for this finding given that C. apella is known to consume hard-object foods. This is consistent with the predicted outcome of the competitive exclusion principle. Am J Phys Anthropol 104:487–511, 1997. © 1997 Wiley-Liss, Inc.