Mackenzie L. Bergstrom

Social networks in primates: smart and tolerant species have more efficient networks

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.

Dominance among female white-faced capuchin monkeys ( Cebus capucinus ): hierarchical linearity, nepotism, strength and stability

Research on Old World primates provided the foundation for understanding competitive strategies resulting from social and ecological pressures. The neotropical primate, Cebus capucinus shares many social patterns with Old World cercopithecines (e.g., female philopatry, male dispersal), which may contribute to similar expression of competitive strategies. To clarify the nature of dominance patterns among female white-faced capuchins we examined hierarchical linearity, rank acquisition, matrilineal rank inheritance, hierarchical strength and stability. We collected focal data on 22 adult females (2008) and long-term dominance data (1986–2008) on 33 adult females in Sector Santa Rosa, Costa Rica. Females displayed linear hierarchies based on the direction of dyadic submission. At sexual maturity females quickly acquired rank positions beneath their mother and older sisters. Hierarchies were considered strong based on high proportions of food-related agonism, short latency to detection of hierarchies (21 h/female) and low directional inconsistency scores (<5%). Hierarchies were considered stable based on lack of tied submissive interactions (indicative of uncontested rank positions), low rates of rank change (0.510 changes/year), and long-term stability in matrilineal rank order. These findings enhance our understanding of capuchin social systems and how the competitive strategies of white-faced capuchins compare to those of Old World primates.

Drivers of home range characteristics across spatiotemporal scales in a Neotropical primate, Cebus capucinus

The factors that drive within-species variation in animal space use remain poorly understood. A growing body of evidence suggests that both home range attributes and biological interpretations of the home range may depend fundamentally on the scale of analysis. We utilize a multiscale mixed effects modelling framework to examine how seasonal fluctuations in climate, food resource abundance and group mass affect variance in home range area and the maturity stage of forest used by a group-living Neotropical primate, the white-faced capuchin, Cebus capucinus. Using an 8-year data set representing over 20 000 contact hours, we estimated home ranges for seven social groups at four nested temporal scales and three nested spatial scales using a movement-based kernel method. Group mass was consistently the most important predictor of home range size in our models, and its effects were relatively insensitive to spatial or temporal scale. Mean daily maximum temperature was an influential factor in shaping monthly range area and composition, with hotter weather favouring smaller home range size and increased use of mature evergreen forest. Greater fruit availability was also associated with smaller monthly range area. The effects of temperature and fruit availability were both scale dependent: the impact of both variables was greatest on the core zone. The different study groups showed marked variation in the habitat composition of their home ranges, but in all groups, higher-use zones consisted of older, more evergreen forest. Our study illustrates the complex ecological processes that affect movement behaviour in a Neotropical primate across a range of spatial and temporal scales, highlighting the importance of group mass, climatic seasonality, landscape heterogeneity and dietary shifts in shaping the home range.

Dominance style of female white-faced capuchins

Dominance style, the level of tolerance displayed by dominant individuals toward subordinate ones, is exhibited along a continuum from despotic to relaxed. It is a useful concept to describe the nature of dominance relationships in macaque species and it bridges among multiple features of dominance hierarchies, aggression, kinship and conflict resolution. Capuchins share many behavioral similarities with Old World monkeys and like macaques, may exhibit a suite of covarying characteristics related to dominance. Here, we provide an assessment of dominance style by examining measures of aggression and kin bias in 22 adult female white-faced capuchin monkeys (Cebus capucinus) in three social groups at Santa Rosa Sector, Costa Rica. We found that bidirectionality of aggression was low (mean = 6.9% ± SE 1.6). However, there were few significant correlations between kin relatedness and social behavior (approaching, grooming, proximity, and co-feeding), even though the intensity of kin bias in grooming was moderate and higher in the larger group. We conclude that patterns of aggression and kin-biased behavior in our study animals are dissimilar to the patterns of covariation observed in macaque species. While unidirectional aggression suggests a despotic dominance style, the moderate expression of kin bias suggests an intermediate to relaxed classification when compared with results from an analysis of 19 macaque species. Additional studies of capuchin species and behaviors associated with dominance style (i.e., conciliatory tendencies) would help to create a comparative framework for the genus Cebus, and allow for more detailed cross-species comparison of dominance relationships across all primates.

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.

Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator)

Significance Color vision variation is prevalent among neotropical monkeys. Captive studies indicate that trichromacy should confer a fruit feeding advantage. This hypothesis, however, has yet to be supported by field studies. We collected behavioral and genetic data from 72 capuchins and analyzed ca. 20,000 fruit intake events across 27 plant species. Controlling for plant species and phenological condition, we find that trichromats eat reddish, conspicuous fruits more quickly than do dichromatic (red-green colorblind) groupmates. We demonstrate an advantage of trichromacy for consuming fruit among wild monkeys. Previous research has revealed dichromatic advantage for cryptic tasks; our results suggest fruit foraging plays an important role in the maintenance of primate opsin polymorphism via balancing selection. Intraspecific color vision variation is prevalent among nearly all diurnal monkeys in the neotropics and is seemingly a textbook case of balancing selection acting to maintain genetic polymorphism. Clear foraging advantages to monkeys with trichromatic vision over those with dichromatic “red-green colorblind” vision have been observed in captive studies; however, evidence of trichromatic advantage during close-range foraging has been surprisingly scarce in field studies, perhaps as a result of small sample sizes and strong impacts of environmental or individual variation on foraging performance. To robustly test the effects of color vision type on foraging efficiency in the wild, we conducted an extensive study of dichromatic and trichromatic white-faced capuchin monkeys (Cebus capucinus imitator), controlling for plant-level and monkey-level variables that may affect fruit intake rates. Over the course of 14 months, we collected behavioral data from 72 monkeys in Sector Santa Rosa, Costa Rica. We analyzed 19,043 fruit feeding events within 1,602 foraging bouts across 27 plant species. We find that plant species, color conspicuity category, and monkey age class significantly impact intake rates, while sex does not. When plant species and age are controlled for, we observe that trichromats have higher intake rates than dichromats for plant species with conspicuously colored fruits. This study provides clear evidence of trichromatic advantage in close-range fruit feeding in wild monkeys. Taken together with previous reports of dichromatic advantage for finding cryptic foods, our results illuminate an important aspect of balancing selection maintaining primate opsin polymorphism.

Using urinary parameters to estimate seasonal variation in the physical condition of female white-faced capuchin monkeys (Cebus capucinus imitator)

OBJECTIVES The physical condition of females depends on access to resources, which vary over space and time. Assessing variation in physical condition can help identify factors affecting reproductive success, but noninvasive measurement is difficult in wild animals. Creatinine concentration relative to the specific gravity (i.e., density) of urine has promise for noninvasively quantifying the relative muscle mass (RMM) of wild primates. We verified the relationship between these urinary parameters for wild white-faced capuchin monkeys, and assessed temporal changes in the RMM of females across groups and between periods of high and low resource abundance. MATERIALS AND METHODS We collected urine from 25 adult females in three groups across varying seasons at Sector Santa Rosa, Costa Rica. We measured the specific gravity and creatinine concentration of 692 samples and the effect of specific gravity on creatinine concentration. We used the residuals of this relationship to measure effects of group and season using mixed-effects models. RESULTS Specific gravity significantly predicted creatinine concentration. Season, group membership and the interaction between these variables were significant predictors of residual creatinine variation. Specifically, RMM was higher during months with high fruit energy density, lower in one social group, and less variable among females in the smallest group. DISCUSSION Our findings suggest that specific gravity and creatinine may be used as urinary parameters to make inferences about the RMM of capuchins. Using this technique, we infer that females experienced changes in muscle mass according to variation in resource energy availability and social group variation.