Eva C. Wikberg

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.

Female dispersal patterns in six groups of ursine colobus (Colobus vellerosus): infanticide avoidance is important

Summary Under the dispersal/foraging efficiency model, colobines are predicted to be ‘indifferent mothers’, neither facilitating philopatry for their daughters nor evicting them from the natal home range because food competition is thought to be slight. We observed six groups of Colobus vellerosus at the Boabeng-Fiema Monkey Sanctuary in Ghana (2000‐2007) and recorded changes in female composition caused by observed (N = 11) and inferred (N = 12) emigrations and immigrations (N = 3). We also observed 14 immigration attempts. Most emigrating females were subadult and nulliparous. Parallel emigration was frequent. Resident females behaved aggressively to immigrating females and immigration attempts were rarely successful. Voluntary female emigration (N = 10) occurred mostly when male group membership was unstable or in association with the immigration of all-male bands. Involuntary emigrations (N = 13) associated with increased female‐female aggression occurred in the two largest groups, where parous females targeted nulliparous maturing females. Larger groups tended to lose females and female immigration was successful only in the study group with the lowest number of females. Females appear to emigrate to reduce infanticide threat although feeding competition is reduced in smaller groups as well. C. vellerosus at BFMS are better described as ‘incomplete suppressors’.

Dispersal in male ursine colobus monkeys (Colobus vellerosus): influence of age, rank and contact with other groups on dispersal decisions

[Dispersal is male-biased in ursine colobus monkeys ( Colobus vellerosus ), although female dispersal also occurs (Teichroeb et al., 2009). Here we describe the process of male dispersal and its connection with between-group encounters (BGEs, N = 444) and male incursions (when males left their group and approached within 50 m of another group; N = 128) at the Boabeng-Fiema Monkey Sanctuary in central Ghana. Through BGEs and incursions, particularly those with non-aggressive interactions between individuals in different groups (BGEs, N = 17; incursions, N = 4), males could probably assess other groups for dispersal opportunities. There was a trend for males to perform incursions more frequently before emigrating voluntarily than involuntarily. Incursions were often performed towards the group that the male eventually transferred to. Incursions by alpha males were temporally shorter and more aggressive than those by non-alpha males. We suggest that non-alpha males used incursions to assess other groups for breeding or dispersal opportunities, whereas alpha males performed incursions mainly to convey information about their quality to neighbouring males and females. Male emigrations/disappearances (natal N = 20, secondary N = 43, unknown N = 9) and immigrations ( N = 62) were recorded for seven groups during ten years (2000– 2010). Alpha males always emigrated involuntarily. Parallel emigration and immigration occurred. Males often immigrated into groups with a more favourable adult male/adult female ratio and improved their rank, both of which likely increased their mating opportunities. The most fitting ultimate explanation for both natal and secondary male dispersal in this population was the intrasexual competition for mates hypothesis, as males of all ages appeared to emigrate to improve their reproductive opportunities., Dispersal is male-biased in ursine colobus monkeys (Colobus vellerosus), although female dispersal also occurs (Teichroeb et al., 2009). Here we describe the process of male dispersal and its connection with between-group encounters (BGEs, N = 444) and male incursions (when males left their group and approached within 50 m of another group; N = 128) at the Boabeng-Fiema Monkey Sanctuary in central Ghana. Through BGEs and incursions, particularly those with non-aggressive interactions between individuals in different groups (BGEs, N = 17; incursions, N = 4), males could probably assess other groups for dispersal opportunities. There was a trend for males to perform incursions more frequently before emigrating voluntarily than involuntarily. Incursions were often performed towards the group that the male eventually transferred to. Incursions by alpha males were temporally shorter and more aggressive than those by non-alpha males. We suggest that non-alpha males used incursions to assess other groups for breeding or dispersal opportunities, whereas alpha males performed incursions mainly to convey information about their quality to neighbouring males and females. Male emigrations/disappearances (natal N = 20, secondary N = 43, unknown N = 9) and immigrations (N = 62) were recorded for seven groups during ten years (2000– 2010). Alpha males always emigrated involuntarily. Parallel emigration and immigration occurred. Males often immigrated into groups with a more favourable adult male/adult female ratio and improved their rank, both of which likely increased their mating opportunities. The most fitting ultimate explanation for both natal and secondary male dispersal in this population was the intrasexual competition for mates hypothesis, as males of all ages appeared to emigrate to improve their reproductive opportunities.]

Between-group variation in female dispersal, kin composition of groups, and proximity patterns in a black-and-white colobus monkey (Colobus vellerosus).

A growing body of evidence shows within-population variation in natal dispersal, but the effects of such variation on social relationships and the kin composition of groups remain poorly understood. We investigate the link between dispersal, the kin composition of groups, and proximity patterns in a population of black-and-white colobus (Colobus vellerosus) that shows variation in female dispersal. From 2006 to 2011, we collected behavioral data, demographic data, and fecal samples of 77 males and 92 females residing in eight groups at Boabeng-Fiema, Ghana. A combination of demographic data and a genetic network analysis showed that although philopatry was female-biased, only about half of the females resided in their natal groups. Only one group contained female-female dyads with higher average relatedness than randomly drawn animals of both sexes from the same group. Despite between-group variation in female dispersal and kin composition, female-female dyads in most of the study groups had higher proximity scores than randomly drawn dyads from the same group. We conclude that groups fall along a continuum from female dispersed, not kin-based, and not bonded to female philopatric, kin-based, and bonded. We found only partial support for the predicted link between dispersal, kin composition, and social relationships. In contrast to most mammals where the kin composition of groups is a good predictor of the quality of female-female relationships, this study provides further support for the notion that kinship is not necessary for the development and maintenance of social bonds in some gregarious species.

Individualistic female dominance hierarchies with varying strength in a highly folivorous population of black-and-white colobus

Females that do not experience strong contest competition for food are presumed to form ‘egalitarian’ relationships (i.e., lacking strong, linear dominance hierarchies). However, recent studies of Gorilla beringei beringei (mountain gorilla) have documented relatively strong, linear female dominance hierarchies despite them having a highly folivorous diet that generates relatively low levels of within-group contest competition (Robbins et al., 2005, 2007). To investigate if this pattern holds true for other highly folivorous species that may experience low levels of contest competition, we examined the linearity and strength of female dominance hierarchies in a population of Colobus vellerosus (ursine colobus or white-thighed colobus) at Boabeng-Fiema, Ghana. From 2004 to 2011, we collected data via ad libitum and focal sampling of 75 adult and subadult females in eight groups. Half of the study groups had few unknown submissive relationships, and females formed individualistic hierarchies with high linearity indices ranging from 0.9 to 1. There was between-group variation in all components of hierarchical strength (i.e., hierarchical expression, consistency, and stability). Groups showed varying rates of submission, and there was a short latency to detect a linear hierarchy in some groups and a long latency in other groups (i.e., varying levels of hierarchical expression). Females in most groups formed unidirectional and stable relationships. Maturing females challenged older females in some groups, and these groups had more non-linear relationships (i.e., dyads with more submissive interactions down rather than up the hierarchy) and higher rates of individual rank change than other groups. Based on low rates of submission, long latencies, and/or some inconsistencies, we conclude that most groups form relatively

Familiarity is more important than phenotypic similarity in shaping social relationships in a facultative female dispersed primate, Colobus vellerosus

Animals often bias affiliative behaviors toward kin, but it is unclear what mechanism most species use to discriminate kin. We investigated if facultative dispersed female primates use phenotype matching and/or familiarity to discriminate female kin. We studied 38 adult female Colobus vellerosus at Boabeng-Fiema, Ghana. We determined dyadic co-residency status and age proximity using long-term demographic data, R-values from 17 short tandem repeat loci, and interaction rates using focal samples collected during one year. Approach rates were not strongly affected by how long females had resided together, which contrasts to the familiarity hypothesis. Females approached and groomed maternal kin more than other females, which supports the mother-mediated familiarity hypothesis. Females did not discriminate paternal half siblings from non-kin, and they did not prefer to interact with females of similar age. Short-term co-resident kin did not bias affiliation toward each other, indicating that female colobus cannot consistently recognize less familiar kin via phenotype matching or that biasing behaviors toward less familiar kin is not beneficial. Despite showing facultative dispersal that may reduce the accuracy of using familiarity as a kin recognition mechanism, female choice of social partners was based on familiarity, which conforms to the pattern observed in many female philopatric primates.

Kinship and similarity in residency status structure female social networks in black-and-white colobus monkeys (colobus vellerosus)

Kinship shapes female social networks in many primate populations in which females remain in their natal group to breed. In contrast, it is unclear to which extent kinship affects the social networks in populations with female dispersal. Female Colobus vellerosus show routine facultative dispersal (i.e., some females remain philopatric and others disperse). This dispersal pattern allowed us to evaluate if facultative dispersed females form social networks shaped by an attraction to kin, to social partners with a high resource holding potential, or to similar social partners in terms of maturational stage, dominance rank, and residency status. During 2008 and 2009, we collected behavioral data via focal and ad libitum sampling of 61 females residing in eight groups at Boabeng-Fiema, Ghana. We determined kinship based on partial pedigrees and genotypes at 17 short tandem repeat loci. Kinship influenced coalition and affiliation networks in three groups consisting of long-term resident females with access to a relatively high number of female kin. In contrast, similar residency status was more important than kinship in structuring the affiliation network in one of two groups that contained recent female immigrants. In populations with female dispersal, the occurrence of kin structured social networks may not only depend on the kin composition of groups but also on how long the female kin have resided together. We found no consistent support for females biasing affiliation toward partners with high resource holding potential, possibly due to low levels of contest competition and small inter-individual differences in resource holding potential.

Factors influencing male affiliation and coalitions in a species with male dispersal and intense male–male competition, Colobus vellerosus

Male Colobus vellerosus compete intensely for access to females, which sometimes leads to mortal wounding. Yet, males often form cooperative relationships to overtake prime-aged males and immigrate into bisexual groups. We investigated the factors that predicted the presence of coalitions and affiliative relationships among males in this species. Interactions among males in 292 dyads from six groups were examined from 2004 to 2010 at Boabeng-Fiema, Ghana. Affiliation rates among males were higher and aggression rates lower when one or both males in the dyad were subadult, compared to adult male dyads. Affiliation rates tended to be higher among males that were kin but no other aspect of male relationships predicted affiliation. Coalitions among males were rarely observed and primarily occurred in the context of joint defense against extra-group males (93.5% of events). Adult males were more likely to provide coalitionary support than subadults and coalitions occurred significantly more often when both males were high ranking, since these males probably benefited most in terms of reproductive success from excluding extra-group males. Rank-changing and leveling coalitions among low-ranking males appear to be quite rare or absent in C. vellerosus. The costs of these types of coalitions may be too high or male group size too small on average for these types of coalitions to have been selected for. The overall low rates of affiliation and coalitions among male C. vellerosus are likely influenced by male-biased dispersal and the high level of male–male competition.

Female sociality and sexual conflict shape offspring survival in a Neotropical primate

Significance In group-living mammals, infants of females with strong social relationships sometimes exhibit higher survivorship than infants of less social females, a finding that holds true in our study population of wild white-faced capuchin monkeys. However, as in many mammals, new alpha male capuchins often kill young infants sired by other males. Our long-term research shows that infants of highly social females are at greater risk of dying or disappearing during periods of alpha male replacements than infants of less social females. These findings indicate that new alpha males are more likely to target the infants of more social, and therefore central, females. Our study provides evidence that female sociality can negatively affect offspring survival by increasing the likelihood of infanticide. Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession models assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha males probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.