Katharine M. Jack

Male dispersal patterns in white-faced capuchins, Cebus capucinus. Part 1: patterns and causes of natal emigration

Abstract This is the first of two papers examining male dispersal patterns in white-faced capuchins. Our study was based on behavioural and demographic data collected on multiple groups of white-faced capuchins in Santa Rosa National Park, Costa Rica since 1985. Here we examine the patterns and proximate causation of male natal dispersal. Natal dispersal in white-faced capuchins occurred at a median age of 4.5 years, with no males remaining in the natal group past 8 years. Initial departure from the natal group appeared to be in response to an attraction to extragroup males and dispersing groupmates. Rates of parallel dispersal (dispersal with co-resident males and/or into groups containing familiar males) were very high for natal males (71–82%), and this pattern of dispersal may have evolved to increase inclusive fitness benefits in male-dispersed species. Additionally, this pattern of dispersal probably increases survivorship among dispersing males who are not yet physically mature, as is common in white-faced capuchins.

Interspecific interactions between Cebus capucinus and other species: Data from three Costa rican sites

Capuchins exhibit considerable cross-site variation in domains such as foraging strategy, vocal communication and social interaction. We report interactions between white-faced capuchins (Cebus capucinus) and other species. We present comparative data for 11 groups from 3 sites in Costa Rica that are ecologically similar and geographically close, thus reducing the likelihood that differences are due solely to genetic or ecological differences. Our aim is to document both the range of variation and common elements across sites and situations. We also consider factors that contribute to the variation or consistency or both, including social learning, local ecology, and temperament. We consider 4 categories of allospecifics: (1) vertebrate prey, (2) potential predators, (3) feeding competitors, and (4) neutral species. Although we cannot rule out local differences in ecology, our data suggest that social learning may account for at least some cross-site differences in behavior toward allospecifics. Our strongest finding is that boldness, aggression and pugnacity are displayed consistently across sites, groups and circumstances, even in interactions with neutral species, which reflects a critical aspect of species-specific temperament in Cebus capucinus that has been evolutionarily developed and reinforced through highly opportunistic foraging, strong predator defense, and active hunting. We suggest directions for future research, particularly in regard to primate temperament as an evolved trait with consequences for fitness.

Predictors of Reproductive Success in Female White-Faced Capuchins (Cebus capucinus)

Early investigations into variable reproductive success in nonhuman primates tended to focus on the benefits conferred by high dominance rank. However, the effect of high rank on individual reproductive success has been found to vary both intra- and interspecifically, requiring researchers to expand their investigations to include additional factors. Here we examine the age and rank of the mother, sex of the infant, group size, number of close kin, replacement of group males, and resource availability as possible predictors of female reproductive success in white-faced capuchins (Cebus capucinus) in the Santa Rosa sector of the Area de Conservación Guanacaste, Costa Rica. We examine the length of interbirth intervals (IBI) and infant survivorship as measures of individual reproductive success for the 31 adult females that resided in our three study groups between 1986 and 2007. The greatest predictor of IBI length was whether or not the first infant in the interval survived (number of matrilineal kin and resource availability were also significant predictors); while infant survivorship was most significantly predicted by the occurrence of a turnover in group males in the year following the birth of an infant (infant sex was also a significant factor). Based on these findings, we conclude that male and female reproductive strategies are at odds in this species, with male strategies strongly influencing female reproductive success.

Tracking Neotropical Monkeys in Santa Rosa: Lessons from a Regenerating Costa Rican Dry Forest

The Santa Rosa primate project began in 1983 and we have studied the behavioral ecology of the resident primate species (Cebus capucinus, Alouatta palliata and Ateles geoffroyi) continuously since then. Most of our research has concentrated on the behavior, ecology, and life history of multiple groups of capuchins and on documenting the effects of forest protection and regeneration on the howler and capuchin populations. Our examination of capuchin life histories has shown that they lead complex and intriguing lives, many aspects of which are affected by the frequent movement of adult males between social groups throughout the course of their lives. Over the past 28 years, we have documented increases in both the capuchin and howler populations. However, the howler population apparently reached carrying capacity in 1999, whereas the capuchin population continues to grow, probably because of their ability to occupy early-regeneration habitats. Our long-term examination of the population structure and life history of these two species clearly demonstrate that many species-specific aspects of biology and behavioral ecology differentially influence patterns of primate population recovery. It is only after decades of research that we can begin to understand the underlying constraints and variability in the lives of these animals.

What traits promote male parallel dispersal in primates

Summary Parallel dispersal occurs when individuals emigrate together with peers or close kin, or immigrate into groups containing familiar or closely related individuals. To understand the evolution of parallel dispersal in male primates, we explore if parallel dispersal co-occurs with male coalitions, or with other traits that may facilitate coalition formation. We conducted a meta-analysis using phylogenetic comparative methods to test for an association between male parallel dispersal and male coalition formation, multi-male social groups, male-biased dispersal, high paternity concentration, and breeding seasonality. These traits were predicted to be correlated with parallel dispersal because they increase the availability of potential dispersal partners, increase individual competitive ability, or provide inclusive fitness benefits for cooperating relatives. Pairwise comparisons revealed that coalitions in general were significantly associated with male parallel dispersal. However, neither intergroup nor intragroup coalitions were associated with parallel dispersal when examined separately, though there was a trend towards significance for intergroup coalitions. Male-biased dispersal was equivocally associated with parallel dispersal, while multi-male social groups, paternity concentration, and breeding seasonality were not. These results suggest that the evolution of male parallel dispersal may be linked with the propensity of males to form coalitions and the need to retain coalition partners.

The effects of observer presence on the behavior of Cebus capucinus in Costa Rica

We report on the responses of Cebus capucinus in the Santa Rosa Sector of the Area de Conservación Guanacaste, Costa Rica, to the presence of observers over a 4‐week period. Study groups were habituated to different degrees: (1) Cerco de Piedra (CP): continuous observations began in 1984; (2) Exclosure (EX): focus of an 18‐month study on males from 1998 to 1999; and (3) NBH: never studied/followed but the group frequently encounters researchers. We collected three types of data: group scans (group state was coded as calm or agitated at observer presence), focal animal data (observer‐directed behaviors were recorded), and fecal cortisol levels. The two less‐habituated groups (NBH and EX) differed significantly from the habituated group (CP) in their behavioral and cortisol responses, and they showed an increase in habituation over the study period (agitation and cortisol levels both dropped). Individuals in NBH also decreased their responses to observers during focal follows; however, at the end of the study the responses of the two less‐habituated groups (NBH and EX) remained elevated in comparison to the habituated group (CP), suggesting the need for further habituation. Unlike capuchin groups that rarely encounter humans, NBH and EX never fled from observers and they rarely emitted observer‐directed alarm calls. We suggest that the permanence of habituation and the ability to habituate animals passively through a neutral human presence are both important considerations for researchers conducting studies in areas where animal safety from poachers, etc. cannot be guaranteed. Am. J. Primatol. 70:490–494, 2008.

Female dispersal in a female-philopatric species, Cebus capucinus

[White-faced capuchins ( Cebus capucinus ) reside in multimale–multifemale groups characterized by female philopatry and frequent male dispersal. However, over the years we have observed five females immigrate into our study groups and 23 disappear/emigrate. We examined long-term demographic and behavioural data on three groups of C. capucinus residing in Santa Rosa, Costa Rica, between 1986 and 2007. During this time, 56 females resided in our study groups and as of June 2007, 23 were still present, ten were confirmed/presumed dead and 23 were missing. Here we review the circumstances surrounding the five immigrations and 23 missing females and evaluate three main hypotheses to explain female dispersal in a female philopatric species: inbreeding avoidance, reduction of intragroup feeding competition and infanticide avoidance. The two main predictions of the inbreeding avoidance hypothesis were not supported by our study; male tenure did not exceed female age at first birth and the majority of dispersers were parous females. The reduction in intragroup feeding competition hypothesis received moderate support; dispersing/disappearing females tend to leave during the dry season and they have fewer matrilineal kin than females remaining in their natal group. Our data were most consistent with the infanticide avoidance hypothesis in that females are more likely to disperse/disappear during years with male replacements, a time when infant deaths are also more common. These data provide further evidence of the large impact that the movement and actions of adult male white-faced capuchins have on the lives of females in this species., White-faced capuchins ( Cebus capucinus ) reside in multimale–multifemale groups characterized by female philopatry and frequent male dispersal. However, over the years we have observed five females immigrate into our study groups and 23 disappear/emigrate. We examined long-term demographic and behavioural data on three groups of C. capucinus residing in Santa Rosa, Costa Rica, between 1986 and 2007. During this time, 56 females resided in our study groups and as of June 2007, 23 were still present, ten were confirmed/presumed dead and 23 were missing. Here we review the circumstances surrounding the five immigrations and 23 missing females and evaluate three main hypotheses to explain female dispersal in a female philopatric species: inbreeding avoidance, reduction of intragroup feeding competition and infanticide avoidance. The two main predictions of the inbreeding avoidance hypothesis were not supported by our study; male tenure did not exceed female age at first birth and the majority of dispersers were parous females. The reduction in intragroup feeding competition hypothesis received moderate support; dispersing/disappearing females tend to leave during the dry season and they have fewer matrilineal kin than females remaining in their natal group. Our data were most consistent with the infanticide avoidance hypothesis in that females are more likely to disperse/disappear during years with male replacements, a time when infant deaths are also more common. These data provide further evidence of the large impact that the movement and actions of adult male white-faced capuchins have on the lives of females in this species.]

The association of intergroup encounters, dominance status, and fecal androgen and glucocorticoid profiles in wild male white-faced capuchins (Cebus capucinus).

Androgens play a role in male reproductive competition, frequently via aggression, while glucocorticoids are associated with the stress response. However, the relationships of these hormones with different sources of competition (intra‐ vs. intergroup) and dominance status are highly variable. Here, we consider the fecal androgen (fA) and glucocorticoid (fGC) profiles of alpha and subordinate male Cebus capucinus in the context of intergroup competition during a rare period of low intragroup competition (i.e. all females were either pregnant or lactating). Intergroup encounters (IGEs) are a long‐term reproductive strategy in male white‐faced capuchins, enabling them to assess the composition of neighboring groups. IGEs pose a threat to resident males as these can result in injury or death, loss of dominance rank, group eviction, and group takeovers that are frequently associated with infanticide. From February to July 2007, fecal samples were collected from eight males in three groups of white‐faced capuchins in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. IGE rate was positively associated with both fA and fGC levels, indicating that IGEs are perceived as reproductive challenges by resident males, and may be associated with elevated metabolic costs. Alpha males sire the majority of group offspring and, accordingly, the threat of IGEs to both future (via rank loss or eviction) and current (via infanticide) reproductive success is greater than for subordinate males. Consistent with this observation, alpha males had higher fA and fGC levels than subordinate males. Given that all females were either pregnant or lactating and pronounced overt intragroup competition was absent, we interpret the difference in hormone profiles of alpha and subordinate males as being primarily associated with variation in the perceived threats of IGEs according to dominance status. Future studies should focus on the interaction of intra‐ and intergroup competition by examining hormone levels in the presence of periovulatory females. Am. J. Primatol. 75:107‐115, 2013.

Two girls for every boy: The effects of group size and composition on the reproductive success of male and female white‐faced capuchins

Many factors have been hypothesized to affect the size and adult sex ratios of primate groups and these, in turn, have been argued to influence birth rates. Using park-wide census data collected on a population of capuchins over a 25-year period, we examined whether group size and adult sex ratio affect the per capita reproductive success of male and female white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. We found that the reproductive success of females (measured as the observed minus the expected ratio of immatures to adult females in the group) decreased with increasing group size, whereas that of males was independent of group size. The proportion of adult males residing in groups had significant, yet contrasting effects on males and females. Male reproductive success was negatively associated with the proportion of males residing in groups whereas female reproductive success increased with the proportion of males. The latter finding supports the intersexual conflict hypothesis, which suggests that a conflict of interest occurs between males and females over adult sex ratios. The effects of group size and composition on the reproductive success of capuchins, a male-dispersed omnivorous species, are similar to those reported for howlers, a bisexually-dispersed folivorous species. One common factor between these taxa is that groups with low ratios of males to females are at greater risk of takeovers and resultant infanticide. Our results suggest that regardless of dietary preference and dispersal pattern, the threat of infanticide can constrain primate group size and composition.

Explaining Variation in Affiliative Relationships among Male White-Faced Capuchins (Cebus capucinus)

Relationships among coresident male white-faced capuchins are highly variable, ranging from affiliative to aggressive. In this paper I examine the affiliative relationships of all adult and subadult males residing in four social groups in Santa Rosa National Park, Costa Rica. Relationships among males in two study groups were neutral and tolerant, while in the remaining two groups males were highly affiliative. Male-male dyadic affiliative interactions were examined to determine which variables (group size, sex ratio, age relationship, relationship duration, and rank distance) influence the quality of male relationships within the study groups. Group size explained much of the variation, with males in small groups being more affiliative. However, the duration and history of the relationship among coresident males appears to be the most important variable in understanding male-male relationships within social groups.