White-faced Capuchins Research Articles

Farmers’ Perceptions of White-Faced Capuchins (Cebus imitator) and Human–Primate Coexistence in Rural Communities of Renacimiento District, Chiriquí Province, Panama

Farmers’ Perceptions of White-Faced Capuchins (Cebus imitator) and Human–Primate Coexistence in Rural Communities of Renacimiento District, Chiriquí Province, Panama

Female-committed infanticide followed by juvenile-enacted cannibalism in wild white-faced capuchins

On 5 February 2021, we observed the first instance of female-committed infanticide followed by cannibalism in a long-studied (> 35 years) population of wild white-faced capuchins (Cebus imitator) in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. The events leading up to and including the infanticide and cannibalism were observed and documented ad libitum, with segments digitally recorded, and a post-mortem necropsy performed. Here we detail our observations and evaluate the events within the framework of leading adaptive explanations. The infanticide may have been proximately motivated by resource competition or group instability. The circumstances of the observed infanticide provided support for the resource competition, adoption avoidance, and social status hypotheses of infanticide, but not for the exploitation hypothesis, as neither the perpetrator nor her kin consumed the deceased infant. The subsequent cannibalism was performed by juveniles who observed the infanticide and may have been stimulated by social facilitation and their prior experience of meat consumption as omnivores. To our knowledge, cannibalism has been documented only once before in C. imitator, in an adjacent study group, with the two cases sharing key similarities in the context of occurrence and manner of consumption. These observations add to our growing knowledge of the evolutionary significance of infanticide and its importance as a reproductive strategy in nonhuman primates.

Sharing spaces: niche differentiation in diet and substrate use among wild capuchin monkeys

Understanding variation in social grouping patterns among animal taxa is an enduring goal of ethologists, who seek to evaluate the selective pressures shaping the evolution of sociality. Cohesive association with conspecifics increases intragroup feeding competition and may impose constraints on group size. Furthermore, in sexually dimorphic species, males and females may have different nutritional requirements, which can lead to suboptimal foraging in mixed-sex groups. How do animals living in permanent social groups mitigate these foraging costs? Niche differentiation is often hypothesized as a mechanism, but rigorous and detailed tests of the extent and context of differences in diet and habitat use, key tenets of this hypothesis, are rare. We investigated the potential for niche differentiation in foraging activity budget and environment use in a population of wild white-faced capuchin monkeys, Cebus imitator , in northwestern Costa Rica. Using a robust data set of 15 879 foraging scan samples collected from four groups over 13 months, we found that smaller individuals – e.g. juveniles and females – forage more often on smaller branches. We additionally found clear evidence of predator-sensitive foraging wherein the smallest individuals spent less time on the ground during invertebrate foraging. Importantly, niche differentiation was far more evident overall during invertebrate foraging, likely due to spatial constraints and environmental homogeneity imposed by fruit patches. In summary, we found considerable variation in habitat use across age and sex classes, likely attributable to differences in size and relative predation risk. These variables likely reduce intraspecific feeding competition by promoting differential diet and habitat use. Our results also provide insight into the limits of niche differentiation as a strategy for competition reduction and may shed light on the evolution of fission–fusion dynamics in highly frugivorous species. • Niche differentiation was apparent during invertebrate, but not fruit, foraging. • Use of the forest strata was consistent with predator-sensitive foraging. • Foraging time on difficult-to-access foods did not differ for juveniles and adults. • Smaller individuals – juveniles and females – used smaller substrates more often. • Support substrates affected microhabitat differentiation but are often overlooked.

Costs of male infanticide for female capuchins: When does an adaptive male reproductive strategy become costly for females and detrimental to population viability?

Infanticide in white-faced capuchins (Cebus capucinus imitator) typically occurs in association with alpha male replacements (AMRs). Although infanticide is likely adaptive for males, it imposes costs on females that are difficult to quantify without long-term demographic data. Here we investigate effects of AMRs and infanticide on female reproductive success and how these costs affect capuchin groups. We investigate (1) effects of AMR frequency on the production of surviving infants; (2) energetic and (3) temporal "opportunity costs" of infant loss; and (4) how AMR frequency impacts capuchin group sizes. We censused six groups (7-33 years/group, 74 adult females). We modeled surviving infant production in relation to AMR. We estimated a female's energy requirements for lost infants and the temporal cost relative to the median reproductive window. We simulated how varying AMR rates would affect future capuchin group sizes. Females exposed to more frequent AMR tended to produce fewer surviving offspring. We estimate the average lost infant requires approximately 33% additional energy intake for its mother and represents 10% of the average reproductive opportunity window available to females. Simulated populations remain viable at the observed rate of AMR occurrence but decrease in size at even slightly higher rates. While infanticide is adaptive for males, for females it affects lifetime reproductive success and imposes energetic and opportunity costs. Although capuchin populations have evolved with AMRs and infanticide, small increases in AMR frequency may lead to population decline/extinction. Infanticide likely plays a large role in population maintenance for capuchins.

Interactions Between Humans and Panamanian White-Faced Capuchin Monkeys (Cebus imitator)

Anthropogenic influence is expanding, threatening primate taxa worldwide. With wildlife tourism a burgeoning industry, understanding human–primate interactions is key in avoiding primate defaunation. We observed interactions between humans and a group of wild Panamanian white-faced capuchin monkeys (Cebus imitator) at Curu Wildlife Refuge, Costa Rica, in June and July, 2019, and compared our findings with findings for the same group in May–October of 2006 and 2007, when the group received more provisioning. We recorded all occurrences of human–primate interactions in 323 15-min samples over 42 consecutive days. We found that capuchins initiated approximately twice as many interactions as humans did (a significant difference). We also found a strong positive correlation between engaging behaviors exhibited by humans and capuchin agonistic behaviors. Capuchins spent significantly more time engaging in moderate behaviors (snatch food, snatch item, vigilance, vocalization) and less time not interacting with humans, in the presence of tourists and staff, than in the presence of staff only. Time spent in moderate and intense behaviors (approach, beg, chase, offer, take food, threat) was lower in 2019 than in 2006 and 2007. These findings suggest that reducing engaging behaviors by humans may reduce primate agonistic behaviors, and that human group composition affects human–primate interactions. The reduction in moderate and intense behaviors between studies also suggests that reducing direct provisioning could reduce the frequency and intensity of human–primate interactions in tourist sites.

Studying animal innovation at the individual level: A ratings-based assessment in capuchin monkeys (Sapajus [Cebus] sp.).

Large-scale studies of individual differences in innovative behavior among nonhuman animals are rare because of logistical difficulties associated with obtaining observational data on a large number of innovative individuals across multiple locations. Here, we take a different approach, using observer ratings to study individual differences in innovative behavior in 127 brown capuchin monkeys (Sapajus [Cebus] sp.) from 15 social groups and 7 facilities. Capuchins were reliably rated by 1 to 7 raters (mean 3.2 ± 1.6 raters/monkey) on a 7-point Likert scale for levels of innovative behavior, task motivation, sociality, and dominance. In a subsample, we demonstrate these ratings are valid: Rated innovation predicted performance on a learning task, rated motivation predicted participation in the task, rated dominance predicted social rank based on win/loss aggressive outcomes, and rated sociality predicted the time that monkeys spent in proximity to others. Across all 127 capuchins, individuals that were rated as being more innovative were significantly younger, more social, and more motivated to engage in tasks. Age, sociality, and task motivation all had independent effects on innovativeness, whereas sex, dominance, and group size were nonsignificant. Our findings are consistent with long-term behavioral observations of innovation in wild white-faced capuchins. Observer ratings may, therefore, be a valid tool for studies of animal innovation. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS

Ecological flexibility, extended lifespans, and large brains have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Cebus imitator Through high-depth sequencing of DNA derived from blood, various tissues, and feces via fluorescence-activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity.

Microsatellite Markers for Bearded Capuchins (Sapajus libidinosus): Transferability and Characterization.

Natural Sapajus libidinosus populations are in continuous decline due to fragmentation, habitat loss, and the illegal pet trade. They live in Caatinga scrub forests, which already lost over 50% of their original cover. The lack of studies on S. libidinosus population genetics means that we do not know how they are being affected by this striking habitat loss and other anthropogenic disturbances. Polymorphic markers are not available for the study of S. libidinosus diversity and population genetics. Thus, here we aimed to test the transferability of 14 microsatellite markers to S. libidinosus. These microsatellites were previously isolated from Cebus capucinus (white-faced capuchin), species belonging to the same subfamily (Cebinae) as the study species. We found that six of the tested microsatellite markers (tetra-nucleotide) were cross-amplified in our target species. All loci were polymorphic. The number of alleles varied from 4 to 7, and the expected heterozygosity ranged from 0.588 to 0.869. The microsatellite markers transferred to S. libidinosus and characterised in our study will be valuable tools to evaluate the genetic variability of both wild and captive populations. They will considerably reduce the costs of microsatellite isolations, helping to prioritise currently limited research and conservation budgets in Brazil.

Someday a Big Plague Will Come: Laurie Garrett’sThe Coming Plague: Newly Emerging Diseases in a World out of Balance

Someday a Big Plague Will Come: Laurie Garrett’sThe Coming Plague: Newly Emerging Diseases in a World out of Balance

Infant cannibalism in wild white-faced capuchin monkeys.

Cannibalism has been observed in a variety of animal taxa; however, it is relatively uncommon in primates. Thus, we rely heavily on case reports of this behavior to advance our understanding of the contexts under which it occurs. Here, we report the first observation of cannibalism in a group of wild white‐faced capuchin monkeys (Cebus imitator). The subject was a dead infant, estimated to be 10 days old, and the probable victim of infanticide. Consumption of the corpse was initiated by a 2‐year‐old male (second cousin of the infant), though it was eventually taken over and monopolized by the group's alpha female (grandaunt of the infant). Although most group members expressed interest in the corpse (sniffing, touching, and threatening it), no others made an attempt to consume it. Given that this is the only observation of cannibalism recorded in over 37 years of study on this population, we consider it to be a rare behavior in this species. This detailed record contributes new data, which, when combined with other reports within and across species and contexts, enables the evaluation of adaptive explanations of cannibalism.

Cooperative rescue of a juvenile capuchin (Cebus imitator) from a Boa constrictor

The threat of predation by snakes is considered to have played a significant role in the evolution of primate sensory systems and behavior. However, we know relatively little about individual and group responses given the rarity of observed predation events. Here we report an observed (filmed) predation attempt by an adult Boa constrictor (~ 2 m) on a juvenile white-faced capuchin (Cebus imitator) in the Sector Santa Rosa of the Área de Conservación Guanacaste, Costa Rica. The snake caught the juvenile monkey on the ground during a terrestrial play session. When the victim screamed, the alpha male, alpha female, and another adult female ran to the scene, physically attacked the snake (with bites and hits), and pulled the victim to safety. Most group members participated in the vocal mobbing of the snake both during and after the attack. Based on the outcomes of this predation attempt and published reports of other B. constrictor attacks on primates, the coordinated efforts of ≥ 2 group members is needed for a successful rescue. This observation adds to our growing knowledge of cooperative group behavior and its importance in predator defense.

Human-monkey interaction dynamics and their dietary impacts on central american white-faced capuchins (<i>Cebus imitator</i>) at Manuel Antonio National Park, Costa Rica


 
 
 Wild capuchin monkeys are highly adaptable to anthropogenic environments. We assessed how the interaction dynamics between humans and three groups of Panamanian white-faced capuchin monkeys (Cebus imitator) in Manuel Antonio National Park, the most visited national park of Costa Rica, affected the feeding behavior and diet of these animals in 2008-2009. On average, individual monkeys acquired 2.4 human food items per focal hour during peak hours of park visitation by humans. Although human visitors directly and indirectly provisioned monkeys in the park, 71 % of monkeys’ acquisition of human food items were a result of monkey-initiated interactions (MIIs) rather than human-initiated interactions (HIIs), and adult male monkeys were the most frequent initiators (with 157 adult male MIIs in the study period, compared to 33 initiated by adult females and 84 by juveniles). Adult male monkeys were also the most likely to make direct contact with humans to grab food (35 of 50 direct grabs of food from humans were by adult male monkeys). Adult females acquired food from humans through HIIs at about the same rate as adult males in their group. Secondary acquisition of human food from other monkeys accounted for about one-third of all events of monkey acquisition of human food, and juvenile monkeys had higher median hourly rates than adults in their group to acquire human food through secondary acquisition. Humans frequently offered fruit when provisioning (61.4 % of provisioning events), but monkeys actively acquired fruit, meat, candy, condiments, chips, crackers and dairy items, and only 36.5 % of MIIs were to acquire fruit. Our results suggest that in parks where humans have frequent contact with capuchin monkeys, park regulations should not only prohibit direct provisioning, but require visitors not to bring food into parks. Stronger measures such as fines or park expulsion for those interacting with monkeys might be more effective, and environmental education is necessary as a strategy to inform visitors what to expect from the monkeys and how to avoid accidental provisioning.
 
 

Population density estimate for the white-faced capuchin monkey (<i>Cebus imitator</i>) in the Multiple Use Area Montaña la Botija, Choluteca, Honduras, and a range extension for the species


 
 
 Honduras is one of the Neotropical countries with the least amount of information available regarding the conservation status of its wild primate species. Understanding the real conservation status of these species is relevant, since they are of great importance for ecosystem dynamics due to the diverse ecological services they provide. However, there are many threats that endanger the conservation of these species in the country such as deforestation, illegal hunting, and illegal wildlife trafficking. The present research is the first official registration of the Central American white-faced capuchin monkey (Cebus imitator) for the Pacific slope in southern Honduras, increasing the range of its known distribution in the country. A preliminary population density estimate of the capuchin monkey was performed in the Multiple Use Area Montaña La Botija using the line transect method, resulting in a population density of 1.04 groups/km2 and 4.96 ind/km2 in the studied area. These results provide us with a first look at an isolated primate population that has never been described before and demonstrate the need to develop long-term studies to better understand the population dynamics, ecology, and behaviour, for this group in the zone.
 
 

Capuchin monkey rituals: an interdisciplinary study of form and function.

Many white-faced capuchin monkey dyads in Lomas Barbudal, Costa Rica, practise idiosyncratic interaction sequences that are not part of the species-typical behavioural repertoire. These interactions often include uncomfortable or risky elements. These interactions exhibit the following characteristics commonly featured in definitions of rituals in humans: (i) they involve an unusual intensity of focus on the partner, (ii) the behaviours have no immediate utilitarian purpose, (iii) they sometimes involve 'sacred objects', (iv) the distribution of these behaviours suggests that they are invented and spread via social learning, and (v) many behaviours in these rituals are repurposed from other behavioural domains (e.g. extractive foraging). However, in contrast with some definitions of ritual, capuchin rituals are not overly rigid in their form, nor do the sequences have specific opening and closing actions. In our 9260 h of observation, ritual performance rate was uncorrelated with amount of time dyads spent in proximity but (modestly) associated with higher relationship quality and rate of coalition formation across dyads. Our results suggest that capuchin rituals serve a bond-testing rather than a bond-strengthening function. Ritual interactions are exclusively dyadic, and between-dyad consistency in form is low, casting doubt on the alternative hypothesis that they enhance group-wide solidarity. This article is part of the theme issue 'Ritual renaissance: new insights into the most human of behaviours'.

Behavioural variation and learning across the lifespan in wild white-faced capuchin monkeys

Natural selection has evidently mediated many species characteristics relevant to the evolution of learning, including longevity, length of the juvenile period, social organization, timing of cognitive and motor development, and age-related shifts in behavioural propensities such as activity level, flexibility in problem-solving and motivation to seek new information. Longitudinal studies of wild populations can document such changes in behavioural propensities, providing critical information about the contexts in which learning strategies develop, in environments similar to those in which learning strategies evolved. The Lomas Barbudal Monkey Project provides developmental data for the white-faced capuchin, Cebus capucinus, a species that has converged with humans regarding many life-history and behavioural characteristics. In this dataset, focused primarily on learned aspects of foraging behaviour, younger capuchins are more active overall, more curious and opportunistic, and more prone to inventing new investigative and foraging-related behaviours. Younger individuals more often seek social information by watching other foragers (especially older foragers). Younger individuals are more creative, playful and inventive, and less neophobic, exhibiting a wider range of behaviours when engaged in extractive foraging. Whereas adults more often stick with old solutions, younger individuals often incorporate recently acquired experience (both social and asocial) when foraging. This article is part of the theme issue 'Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals'.

Differential impact of severe drought on infant mortality in two sympatric neotropical primates.

Extreme climate events can have important consequences for the dynamics of natural populations, and severe droughts are predicted to become more common and intense due to climate change. We analysed infant mortality in relation to drought in two primate species (white-faced capuchins, Cebus capucinus imitator, and Geoffroy's spider monkeys, Ateles geoffroyi) in a tropical dry forest in northwestern Costa Rica. Our survival analyses combine several rare and valuable long-term datasets, including long-term primate life-history, landscape-scale fruit abundance, food-tree mortality, and climate conditions. Infant capuchins showed a threshold mortality response to drought, with exceptionally high mortality during a period of intense drought, but not during periods of moderate water shortage. By contrast, spider monkey females stopped reproducing during severe drought, and the mortality of infant spider monkeys peaked later during a period of low fruit abundance and high food-tree mortality linked to the drought. These divergent patterns implicate differing physiology, behaviour or associated factors in shaping species-specific drought responses. Our findings link predictions about the Earth's changing climate to environmental influences on primate mortality risk and thereby improve our understanding of how the increasing severity and frequency of droughts will affect the dynamics and conservation of wild primates.

Increased terrestriality in a Neotropical primate living on islands with reduced predation risk

An arboreal lifestyle is thought to be central to primate origins, and most extant primate species still live in the trees. Nonetheless, terrestrial locomotion is a widespread adaptation that has arisen repeatedly within the primate lineage. The absence of terrestriality among the New World monkeys (Platyrrhini) is thus notable and raises questions about the ecological pressures that constrain the expansion of platyrrhines into terrestrial niches. Here, we report the results of a natural experiment, comparing patterns of terrestrial behavior in white-faced capuchin monkeys (Cebus capucinus imitator) living on two islands off the Pacific coast of Panama that lack mammalian predators (island sites) with the behavior of capuchins at three sites in central Panama with more intact predator communities (mainland sites). Surveys with camera traps revealed increased terrestriality in island vs. mainland sites. Capuchin detection rates were higher, the range of party sizes observed was larger, and individuals engaged in a wider range of terrestrial behaviors on the islands lacking mammalian predators. Furthermore, females carrying infants were frequently photographed on the ground at the island sites, but never at the mainland sites. These findings support the long-standing hypothesis that predators constrain the exploitation of terrestrial niches by primates. These results are also consistent with the hypothesis that arboreal locomotion imposes costs that primates will avoid by walking on the ground when predation risk is low.

Do Monkeys Avoid Areas of Home Range Overlap Because They Are Dangerous? A Test of the Risk Hypothesis in White-Faced Capuchin Monkeys (Cebus capucinus)

In social animals, areas where the home ranges of neighboring groups overlap are often underused. The Risk Hypothesis posits that the costs of intergroup conflict create a “landscape of fear,” discouraging the use of such shared areas. To test this hypothesis, we observed the behavior of white-faced capuchins (Cebus capucinus) in central vs. peripheral areas of their home ranges. If capuchins perceive areas of home range overlap as “risky,” we predicted they would change activity budgets, vocalization rates, and foraging behavior in these areas. A spatially explicit behavioral comparison based on nearly 100 h of focal follows revealed that capuchins socialize less in the periphery (vs. the center) of their home range. Time spent resting, foraging, and engaging in vigilance, as well as vocalization rates, varied in consistent ways across all four study groups, but these differences did not reach statistical significance. Fruit trees near range borders (vs. the center) contained more ripe fruit, and groups spent more time in these trees, with more individuals entering to feed and consuming more fruits. However, capuchins did not alter their foraging behavior in potentially risky peripheral areas in a manner consistent with predictions of optimal foraging theory: intake rates at patch departure were not significantly lower and groups depleted trees to a greater extent along the periphery vs. in the center of their range. These results suggest that while peripheral areas are perceived as risky and this “landscape of fear” contributes to behavioral changes, they also provide resources whose value may outweigh the cost of intergroup encounters.

High density of white‐faced capuchins (Cebus capucinus) and habitat quality in the Taboga Forest of Costa Rica

Across the globe, primates are threatened by human activities. This is especially true for species found in tropical dry forests, which remain largely unprotected. Our ability to predict primate abundance in the face of human activity depends on different species' sensitivities as well as on the characteristics of the forest itself. We studied plant and primate distribution and abundance in the Taboga Forest, a 516-ha tropical dry forest surrounded by agricultural fields in northwestern Costa Rica. We found that the density of white-faced capuchins (Cebus capucinus) at Taboga is 2-6 times higher than reported for other long-term white-faced capuchin sites. Using plant transects, we also found relatively high species richness, diversity, and equitability compared with other tropical dry forests. Edge transects (i.e., within 100 m from the forest boundary) differed from interior transects in two ways: (a) tree species associated with dry forest succession were well-established in the edge and (b) canopy cover in the edge was maintained year-round, while the interior forest was deciduous. Sighting rates for capuchins were higher near water sources but did not vary between the edge and interior forest. For comparison, we also found the same to be true for the only other primate in the Taboga Forest, mantled howler monkeys (Alouatta palliata). Year-round access to water might explain why some primate species can flourish even alongside anthropogenic disturbance. Forest fragments like Taboga may support high densities of some species because they provide a mosaic of habitats and key resources that buffer adverse ecological conditions.

Non-invasive estimation of the costs of feeding competition in a neotropical primate

A key goal in behavioral ecology is to investigate the factors influencing the access to food resources and energetic condition of females, which are strong predictors of their reproductive success. We aimed to investigate how ecological factors, social factors, and reproductive state are associated with energetic condition in a wild neotropical primate using non-invasive measures. We first assessed and compared urinary C-peptide levels (uCP), the presence of urinary ketones (uKet), and behaviorally assessed energy balance (bEB) in female white-faced capuchin monkeys (Cebus imitator) living in Santa Rosa, Costa Rica. Then, we assessed how these measures were associated with feeding competition, dominance rank, and reproductive state. As predicted, uCP and bEB were positively associated with each other, and bEB was negatively associated with uKet. However, we did not find a relationship between uCP and uKet. Females showed lower uCP and bEB values during periods of intense feeding competition, but this relationship was not dependent on dominance rank. Furthermore, rank was not directly associated with uCP and bEB. Urinary ketones, on the other hand, were only produced in the most adverse conditions: by low-ranking, lactating females during periods of intense feeding competition. Behavioral strategies are assumed to maximize reproductive success and not energetic condition per se, which might explain why rank was not generally associated with energetic condition in our study population. This highlights the importance of considering potential differences between reproductive success and proxies of reproductive success, such as energetic condition or food intake, when investigating predictions of socioecological models.