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.     

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.     

A multi-task assessment of hand lateralization in capuchin monkeys (Cebus apella)

Eight tasks were presented to ten tufted capuchin monkeys and hand preferences were recorded for each subject on each task. The strength of hand preferences varied accross tasks. Although no significant population-level left- or right-hand bias emerged for any of the tasks, there was a tendency toward greater left-hand use in a task requiring the use of probing tools. The data also confirm that simple reaching is of limited value as a measure of hand preference. Hand preferences in capuchin monkeys appear to be determined by a number of individual, species, and environmental factors.     

Mirror inspection varies with age and tool-using ability in tufted capuchin monkeys (Cebus apella)

We examined mirror inspection in tufted capuchin monkeys (Cebus apella). Capuchins were presented with a non-reflective surface for 30 minutes and then a mirror for 3 hours. Inspection of the non-reflective surface did not vary significantly as a function of tool-using ability, age, or sex. Mirror inspection was lowest in older animals, and was greater in animals that used tools than in animals that did not use tools. Mirror-aided self-inspection was not observed. These results indicate that mirror inspection varies with age and tool-using ability in tufted capuchin monkeys. We hypothesize that psychological capacities associated with mirror inspection correspond with those related to the use of tools, and that these capacities facilitate the emergence of self-recognition in some primate species.     

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.     

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.     

Multi-generational persistence of traditions in neighbouring meerkat groups

Reports of socially transmitted traditions based on behavioural differences between geographically separated groups of conspecifics are contentious because they cannot exclude genetic or environmental causes. Here, we report persistent differences between neighbouring groups of meerkats (Suricata suricatta) where extensive gene flow precludes genetic differentiation. Over 11 years, some groups consistently emerged later from their sleeping burrows in the morning than others, despite complete turnovers in group membership and the influx of immigrants. Group territories overlapped and, in many cases, the same sleeping burrows were used by different groups. Differences persisted even after accounting for effects of group size, weather and burrow characteristics, and were unrelated to food availability within territories. These results provide compelling evidence that the emergence times of meerkat groups represent conservative traditions.     

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.     

Resource patch size and flexible foraging in white-faced capuchins (Cebus capucinus)

White-faced capuchins (Cebus capucinus)on Barro Colorado Island, Panama, have a flexible foraging strategy. Typically, foraging party size is small and individuals feed dispersed from one another. When seasonal fruiting of large volume trees occurs, the majority of the group forages simultaneously. As C. capucinusdo not display a rigorous dominance structure and there are few indications that individuals or coalitions monopolize food patches,individuals are expected to display scramble strategies instead of high frequencies of contest competition. I recorded foraging party size (simultaneous foragers), the total number of animals to feed successively, and the diameter at breast height (DBH) of fruit trees used in two habituated troops. Individuals in each group spent a substantial amount of time — 65 and 48% of foraging time for each group — foraging in party sizes of one. Monkeys predominantly foraged alone in small trees (0- to 20- cm DBH), successively in medium trees (21- to 60- cm DBH), and simultaneously in large trees (>61- cm DBH). They used small trees more frequently than all other tree classes. In medium-sized trees, although fruit was plentiful, space was limited. In these trees Cebusforaged successively. In large-volume trees, space and fruit were abundant and several individuals fed together. As the DBH of fruiting trees increased, the average foraging party size increased exponentially. Cebus capucinusat Barro Colorado Island modify their foraging party size to adapt to the seasonal patterns of fruit production.     

Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus

This study tested the "challenge hypothesis" and rank-based predictions for temporal steroid production in male tufted capuchin monkeys, Cebus apella. Fecal samples (n = 209) collected from six wild males were analyzed for testosterone and cortisol concentration by enzyme immunoassay. The temporal pattern in male steroid production was compared to female sexual activity and rates of male aggression. The top-ranking adult male did not differ from other adult males in testosterone or cortisol concentration. Mean adult testosterone was significantly higher than mean subadult testosterone throughout the year. There was a clear elevation of testosterone and cortisol in both adult and subadult males during the peak of adult female sexual activity after the birth season. In fact, the magnitude of increase in testosterone was higher than predicted for a species with low male-male aggression. However, there was no difference between nonbreeding baseline testosterone levels during the birth season, and the "breeding" baseline of testosterone in males found during asynchronous female sexual activity. Of all behavioral indices examined, the distribution of female-maintained consortships was the best predictor of mean adult male testosterone concentrations. Although in many species, elevated testosterone coincides with increased male-male aggression, in the present study, the sustained high-magnitude increase in steroids during the peak of adult female sexual activity was associated with a relatively low rate of male-male intragroup aggression.     

Observer choices during experimental foraging tasks in brown capuchin monkeys (Cebus apella)

We investigated whether capuchin monkeys (Cebus apella) would choose to observe a high- or low-status adult female from their group during experimental foraging tests. The subject was located in the center of a test chamber, with a low- and high-ranking demonstrator on either side of two partitions. A peephole allowed the subject to observe the models by looking through either respective partition. Each model was trained on one of the two different methods, lift or pull, for retrieving food from a foraging apparatus. There were 22 subjects and four models. During the 40-trial test sessions, subjects could choose which model they would watch in each trial. It was predicted that subjects would prefer observing the model with whom it was closer in rank, and therefore share greater affiliation with. Results showed that only half the subjects showed a preference and that preference was not linked to status. Relatedness played a larger role in determining if a subject showed a preference for a model, and a correlation was found for relatedness and observer preference. After the observer preference tests, subjects were presented with the foraging apparatus to determine if they displayed a preference for one of the two tasks. The majority of subjects (17/22) showed a preference for the pull method, suggesting that this method may have been more salient to the monkeys in this study.     

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.     

Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

Female-female social relationships in wild white-faced capuchin monkeys,Cebus capucinus

A single social group of wild white-faced capuchin monkeys was studied for a period of 26 months at Lomas Barbudal Biological Reserve, Costa Rica. A total of 604 hr of focal animal data was collected on six adult females in a group of 21 monkeys. Females could be ranked in a stable, linear dominance hierarchy. Adult females spent much more time in proximity to other adult females than to adult males. Females groomed other females twice as often as they groomed males, and about 55 times more often than males groomed males. Females tended to groom up the dominance hierarchy, and dyads with smaller rank distances groomed more often. Higher-ranking females nursed infants other than their own at lower rates than did lower-ranking females; however, females nursed infants of females ranked both above and below them. Although lower-ranking females were more likely than higher-ranking females to be the victims of aggression, higher-ranking females were not necessarily more aggressive than lower-ranking females. In 96% of female-female coalitions vs. a female, the victim was lower-ranking than both coalition partners; in the remaining 4%, the victim was intermediate in rank between the two coalition partners. Higher-ranking female-female dyads formed coalitions more often than did lower-ranking dyads. Those female-female dyads that groomed more frequently also formed coalitions more frequently. The patterning of social interactions indicates that Cebus capucinus at Lomas Barbudal are female bonded. © 1996 Wiley-Liss, Inc.     

Attraction to and learning from social cues in fruitfly larvae

We examined the use of social information in fruitfly larvae, which represent an ideal model system owing to their robust learning abilities, small number of neurons and well-studied neurogenetics. Focal larvae showed attraction to the distinct odour emanating from food occupied by other larvae. In controlled learning experiments, focal larvae preferred novel odours previously paired with food occupied by other larvae over novel odours previously paired with unoccupied food. When we gave groups of larvae a choice between food patches differing in quality, more larvae aggregated on the higher-quality food, suggesting that attraction to and learning about cues associated with other larvae can be beneficial. Furthermore, larvae were more likely to find the best available food patch in trials when that food patch was occupied by other larvae than in trials when that food patch was unoccupied. Our data suggest, however, that the benefits from joining others may be at least partially offset by the fitness costs of increased competition, because larvae reared in isolation did as well as or better than larvae reared in groups on three key fitness parameters: developmental rate, survival rate and adult dry body mass. Our work establishes fruitfly larvae as a highly tractable model species for further research on the mechanisms that modulate behaviour and learning in a social context.