Capuchin monkeys (genus Cebus) have evolutionarily converged with humans and chimpanzees in a number of ways, including large brain size, omnivory and extractive foraging, extensive cooperation and ...coalitionary behaviour and a reliance on social learning. Recent research has documented a richer repertoire of group-specific social conventions in the coalition-prone Cebus capucinus than in any other non-human primate species; these social rituals appear designed to test the strength of social bonds. Such diverse social conventions have not yet been noted in Cebus apella, despite extensive observation at multiple sites. The more robust and widely distributed C. apella is notable for the diversity of its tool-use repertoire, particularly in marginal habitats. Although C. capucinus does not often use tools, white-faced capuchins do specialize in foods requiring multi-step processing, and there are often multiple techniques used by different individuals within the same social group. Immatures preferentially observe foragers who are eating rare foods and hard-to-process foods. Young foragers, especially females, tend to adopt the same foraging techniques as their close associates.
In humans, being more socially integrated is associated with better physical and mental health and/or with lower mortality. This link between sociality and health may have ancient roots: sociality ...also predicts survival or reproduction in other mammals, such as rats, dolphins, and non-human primates. A key question, therefore, is which factors influence the degree of sociality over the life course. Longitudinal data can provide valuable insight into how environmental variability drives individual differences in sociality and associated outcomes. The first year of life-when long-lived mammals are the most reliant on others for nourishment and protection-is likely to play an important role in how individuals learn to integrate into groups. Using behavioral, demographic, and pedigree information on 376 wild capuchin monkeys (Cebus imitator) across 20 years, we address how changes in group composition influence spatial association. We further try to determine the extent to which early maternal social environments have downstream effects on sociality across the juvenile and (sub)adult stages. We find a positive effect of early maternal spatial association, where female infants whose mothers spent more time around others also later spent more time around others as juveniles and subadults. Our results also highlight the importance of kin availability and other aspects of group composition (e.g., group size) in dynamically influencing spatial association across developmental stages. We bring attention to the importance of-and difficulty in-determining the social versus genetic influences that parents have on offspring phenotypes. RESEARCH HIGHLIGHTS: Having more maternal kin (mother and siblings) is associated with spending more time near others across developmental stages in both male and female capuchins. Having more offspring as a subadult or adult female is additionally associated with spending more time near others. A mother's average sociality (time near others) is predictive of how social her daughters (but not sons) become as juveniles and subadults (a between-mother effect). Additional variation within sibling sets in this same maternal phenotype is not predictive of how social they become later relative to each other (no within-mother effect).
The type and variety of learning strategies used by individuals to acquire behaviours in the wild are poorly understood, despite the presence of behavioural traditions in diverse taxa. Social ...learning strategies such as conformity can be broadly adaptive, but may also retard the spread of adaptive innovations. Strategies like pay-off-biased learning, by contrast, are effective at diffusing new behaviour but may perform poorly when adaptive behaviour is common. We present a field experiment in a wild primate, Cebus capucinus, that introduced a novel food item and documented the innovation and diffusion of successful extraction techniques. We develop a multilevel, Bayesian statistical analysis that allows us to quantify individual-level evidence for different social and individual learning strategies. We find that pay-off-biased and age-biased social learning are primarily responsible for the diffusion of new techniques. We find no evidence of conformity; instead rare techniques receive slightly increased attention. We also find substantial and important variation in individual learning strategies that is patterned by age, with younger individuals being more influenced by both social information and their own individual experience. The aggregate cultural dynamics in turn depend upon the variation in learning strategies and the age structure of the wild population.
Various aspects of sociality in mammals (e.g., dyadic connectedness) are linked with measures of biological fitness (e.g., longevity). How within- and between-individual variation in relevant social ...traits arises in uncontrolled wild populations is challenging to determine but is crucial for understanding constraints on the evolution of sociality. We use an advanced statistical method, known as the 'animal model', which incorporates pedigree information, to look at social, genetic, and environmental influences on sociality in a long-lived wild primate. We leverage a longitudinal database spanning 20 years of observation on individually recognized white-faced capuchin monkeys (Cebus capucinus imitator), with a multi-generational pedigree. We analyze two measures of spatial association, using repeat sampling of 376 individuals (mean: 53.5 months per subject, range: 6-185 months per subject). Conditioned on the effects of age, sex, group size, seasonality, and El Niño-Southern Oscillation phases, we show low to moderate long-term repeatability (across years) of the proportion of time spent social (posterior mode 95% Highest Posterior Density interval: 0.207 0.169, 0.265) and of average number of partners (0.144 0.113, 0.181) (latent scale). Most of this long-term repeatability could be explained by modest heritability (h
: 0.152 0.094, 0.207; h
: 0.113 0.076, 0.149) with small long-term maternal effects (m
: 0.000 0.000, 0.045; m
: 0.000 0.000, 0.041). Our models capture the majority of variance in our behavioral traits, with much of the variance explained by temporally changing factors, such as group of residence, highlighting potential limits to the evolvability of our trait due to social and environmental constraints.
Researchers of “culture” have long been interested in the role of social learning in establishing patterns of behavioral variation in wild animals, but very few studies examine this issue using a ...developmental approach. This 7-year study examines the acquisition of techniques used to process Luehea candida fruits in a wild population of white-faced capuchin monkeys, Cebus capucinus, residing in and near Lomas Barbudal Biological Reserve, Costa Rica. The two techniques for extracting seeds (pounding or scrubbing) were approximately equal in efficiency, and subjects experimented with both techniques before settling on one technique--typically the one they most frequently observed. In a sample of 106 subjects that had already settled on a preferred technique, the females adopted the maternal technique significantly more often than expected by chance, but the males did not. Using a longitudinal approach, I examined the acquisition of Luehea processing techniques during the first 5 years of life. Regression analysis revealed that the technique most frequently observed (measured as proportion of Luehea processing bouts observed that used pounding as opposed to scrubbing) significantly predicted the technique adopted by female observers, particularly in the second year of life; the amount of impact of the observed technique on the practiced technique was somewhat less significant for male observers. These results held true for (a) observations of maternal technique only, (b) observations of technique used by all individuals other than the mother, and (c) observations of maternal and non-maternal techniques combined.
An important extension to our understanding of evolutionary processes has been the discovery of the roles that individual and social learning play in creating recurring phenotypes on which selection ...can act. Cultural change occurs chiefly through invention of new behavioral variants combined with social transmission of the novel behaviors to new practitioners. Therefore, understanding what makes some individuals more likely to innovate and/or transmit new behaviors is critical for creating realistic models of culture change. The difficulty in identifying what behaviors qualify as new in wild animal populations has inhibited researchers from understanding the characteristics of behavioral innovations and innovators. Here, we present the findings of a long-term, systematic study of innovation (10 y, 10 groups, and 234 individuals) in wild capuchin monkeys (Cebus capucinus) in Lomas Barbudal, Costa Rica. Our methodology explicitly seeks novel behaviors, requiring their absence during the first 5 y of the study to qualify as novel in the second 5 y of the study. Only about 20% of 187 innovations identified were retained in innovators’ individual behavioral repertoires, and 22% were subsequently seen in other group members. Older, more social monkeys were more likely to invent new forms of social interaction, whereas younger monkeys were more likely to innovate in other behavioral domains (foraging, investigative, and self-directed behaviors). Sex and rank had little effect on innovative tendencies. Relative to apes, capuchins devote more of their innovations repertoire to investigative behaviors and social bonding behaviors and less to foraging and comfort behaviors.
Many mammalian species display sex differences in the frequency of play behavior, yet the animal literature includes few longitudinal studies of play, which are important for understanding the ...developmental timing of sex differences and the evolutionary functions of play. We analyzed social play, solitary play, and grooming using an 18‐year data set on 38 wild white‐faced capuchin monkeys (Cebus capucinus) followed since infancy. Rates of each behavior were measured as the proportion of point samples taken during focal follows in which the individual engaged in each behavior. To determine sex differences in these rates, we ran a series of generalized linear mixed models, considering both linear and quadratic effects of age, and chose the optimal model for each of the three behavioral outcomes based on information criteria. Rates of both social play and solitary play decreased with age, with the exception of social play in males, which increased in the early juvenile period before decreasing. Male and female capuchins had different developmental patterns of social play, with males playing more than females during most of the juvenile period, but they did not display meaningful sex differences in solitary play rates. Additionally, males and females had different patterns of grooming over the lifespan: males participated in grooming at low rates throughout their lives, while adult females participated in grooming at much higher rates, peaking around age 11 years before declining. We suggest that male and female white‐faced capuchins may adopt alternative social bonding strategies, including different developmental timing and different behaviors (social play for males vs. grooming for females). Our results were consistent with two functional hypotheses of play, the practice and bonding hypotheses. This study demonstrates that play behavior may be critical for the development of sex‐specific social strategies and emphasizes the importance of developmental perspectives on social behaviors.
This graph shows the model predictions for how rates of social play change with age for males and females. Rates of social play are expressed as a proportion of the total point samples per year. The first year of life is coded as 0. Circles represent the proportion of point samples in which an individual monkey was engaging in social play in a given year, with the size of the circle representing the total number of point samples for the individual in the same year. Lines represent predictions from the best regression model chosen from Akaike information criterion (AIC) and Bayesian Information Criterion (BIC) model comparisons. Shaded areas represent bootstrapped 95% confidence intervals of the predictions.
Research Highlights
Relative to females, immature males had higher rates of social play.
There was little to no sex difference in solitary play rates.
Young male capuchins seem to bond mainly via play; females bond more via grooming.
Documenting inbreeding and its potential costs in wild populations is a complicated matter. Early infant death before genetic samples can be collected limits the ability of researchers to measure ...fitness costs, and pedigree information is necessary to accurately estimate relatedness between breeding individuals. Using data from 25 years of research from the Lomas Barbudal Capuchin Monkey Project, and a sample of 109 females that have given birth, we find that despite frequent co-residency of adult opposite-sexed individuals, capuchins produce offspring with close kin (i.e., related at the halfsibling level or higher) less often than would be expected in the absence of inbreeding avoidance. We do not find support for alternative, non-behavioral explanations for this pattern and thus argue for mate choice. Furthermore, we find evidence for fitness costs among inbred animals in the form of delayed female age at first birth but not significantly higher juvenile mortality. Further research is necessary in order to determine the mechanisms by which individuals develop sexual aversion to close kin. Through a combination of demographic records, maternal pedigrees, and genetically determined paternity, this study provides a detailed study of inbreeding and inbreeding avoidance in a well-studied mammal population. This study provides (1) evidence that capuchin monkeys avoid mating with close kin at both the level of parent-offspring and half sibling and (2) evidence of fitness costs to inbreeding in the form of delayed first age at reproduction.
The ability to recognize kin has important impacts on fitness because it can allow for kin-biased affiliative behaviours and avoidance of mating with close kin. While the presence and effects of kin ...biases have been widely studied, less is known about the process by which animals recognize close kin. Here we investigate potential cues that white-faced capuchin monkeys, Cebus capucinus, may use to detect half siblings and closer kin. We focus on the first year of life in a sample of 130 infant (N=65 infant females) wild capuchins from the Lomas Barbudal population in Costa Rica. We show that (1) infant relatedness to juvenile and adult males at the level of half sibling and higher can be predicted by male alpha status, spatial proximity and age proximity, and that (2) infant relatedness to juvenile and adult females at the level of half sibling or higher can be predicted by spatial proximity (but not age proximity). Furthermore, (1) the identities of infants' fathers can also be predicted by male alpha status and the spatial proximity between infants and adult males, and (2) age proximity (but not spatial proximity) is predictive of paternal sibship. These results suggest that infant capuchins have access to multiple cues to close relatedness and paternal kinship, although whether infants use these cues later in life remains to be explored in future research.
•We examined cues available to infant capuchins for detecting close relatives.•Male alpha status predicted paternity and close relatedness.•Age proximity predicted paternal sibship.•Spatial proximity predicted paternity and close relatedness.
Zahavi's “Bond Testing Hypothesis” states that irritating stimuli are used to elicit honest information from social partners regarding their attitudes towards the relationship. Two elements of the ...Cebus capucinus vocal repertoire, the “gargle” and “twargle,” have been hypothesized to serve such a bond‐testing function. The greatest threat to C. capucinus infant survival, and to adult female reproductive success, is infanticide perpetrated by alpha males. Thus, we predicted that infants (<8 months), pregnant females and females with infants would gargle/twargle at higher rates than the rest of the population, directing these vocalizations primarily to the alpha male. Over 16 years, researchers collected data via focal follows in 11 habituated groups of wild capuchins in Lomas Barbudal, Costa Rica. We found some support for our hypothesis. Infants and females with infants (<8 months) vocalized at higher rates than the rest of the population. Pregnant females did not vocalize at relatively high rates. Infants (age 8–23 months) were the only target group that vocalized more when the alpha male was not their father. Monkeys gargled and twargled most frequently towards the alpha male, who is both the perpetrator of infanticide and the most effective protector against potentially infanticidal males.
The scatterplot displays average gargle (open red circles) and twargle (closed blue circles) rate data by age in months. The subplot displays average gargle and twargle rates for individuals 24 months of age and younger. Individuals gargle and twargle the most during infancy, when risk of infanticide is the highest.
Research highlights
Capuchin “gargle” and “twargle” vocalizations are hypothesized to test important social bonds.
Young infants and mothers “gargle” and “twargle” at the highest rates.
The most common recipients of these vocalizations are alpha males, who are the only known infanticide perpetrators.
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