White-faced Monkeys Research Articles

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.
 
 

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.

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.

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.

The nutritional importance of invertebrates to female Cebus capucinus imitator in a highly seasonal tropical dry forest

Invertebrates are important foods for many primates and provide valuable nutrients often unavailable from plant sources. We examine the diet of white-faced capuchins (Cebus capucinus imitator) to determine: (a) timing and types of invertebrate food consumption; (b) whether invertebrate consumption varies with availability of plant foods; and (c) how invertebrates contribute to energy and protein intake of females during different reproductive states. We analyze 2 years of behavioral data from 25 adult female capuchins to determine which invertebrates are eaten. We describe annual and monthly invertebrate consumption patterns, and, employing circular statistics, analyze seasonal consumption of the four most important invertebrate groups eaten. We apply logistic regression analyses to tree density and fruit energy data to determine whether capuchin invertebrate foraging is related to fruit energy availability of their most commonly consumed fruits. We evaluate the nutritional contribution of invertebrates to energetic and protein requirements of females over time and across reproductive stages. Capuchins consumed invertebrates from 21 identifiable groups, but their diet was dominated by four orders: Lepidoptera, Orthoptera, Hemiptera, and Hymenoptera. All four orders were consumed in a significantly seasonal pattern, and reduced fruit energy availability was a significant predictor of increased invertebrate foraging. Capuchin females often required invertebrate energy intake to meet their overall monthly energetic needs, particularly while they were lactating, even though they appear to exceed their protein requirements every month. These results indicate that invertebrate consumption is critical for capuchin energetic needs, particularly during periods of reduced fruit availability and lactation.

Hematology and Serum Biochemistry Values of Healthy Free-Ranging Panamanian White-Faced Capuchins (Cebus imitator) in Costa Rica

We describe the hematology and serum biochemistry values for 26 free-ranging Panamanian white-faced capuchins (Cebus imitator) in Costa Rica. Howell-Jolly bodies and microfilariae were observed in some animals. This baseline information is a tool for health assessment and species conservation.

Detection of antibodies against flavivirus over time in wild non-human primates from the lowlands of Costa Rica.

Two-hundred-nine free ranging non-human primates from 31 locations throughout Costa Rica were captured and released between 1993 and 2012, and blood samples, sera or plasma were collected, to detect antigens and antibodies, and so assess the distribution of active and passive flavivirus infections over time. A competitive enzyme-linked immunoassay for the detection of antibodies was used to determine the distribution of past flavivirus infections over time, while Reverse Transcriptase Polymerase Chain Reaction (RT-PCR) was used to detect active West Nile Virus (WNV) and Dengue virus (DENV) infections. The first serological evidence of flavivirus in these animals was determined in 1993, at the same time when DENV re-emerged in humans from Costa Rica. An increase in the number of seropositive wild monkeys to flavivirus was determined over time in the country (11.3% seropositivity in 1993–1996, 20.7% in 2001–2008, and finally 52.9% in 2010–2012). Furthermore, the presence of DENV2 was detected in samples from four howler monkeys collected in 2001–2002, whereas DENV2, DENV3, and DENV4 were found in samples from four white-faced monkeys, and WNV in three howler monkeys living in the Pacific coast of Costa Rica during 2010–2012. The habitat where the positive PCR individuals lived were characterized as fragmented forests, having temperatures ranging from 26°C to 28°C, altitudes below 250 meters above sea level, high precipitation during 7 to 9 months (1500–4000 mm), and a marked dry season of 3 to 5 months. All these animals were living near mangroves; however, they did not show clinical signs of illness at the time of sampling. Results obtained show that the number of seropositive wild non-human primates to flavivirus were increasing during time in the country, longitudinal studies are needed to investigate their role as sentinels of these viruses and to determine if flavivirus infections can affect these species.

El mono Cebus imitator (Primates: Cebidae) se alimenta del fruto de Hedyosmum mexicanum (‎Chloranthaceae) en las alturas de Costa Rica

En los bosques neotropicales se conoce con amplitud los hábitos alimenticios del mono carablanca. Sin embargo, en los ecosistemas tropicales de altas elevaciones, se dispone de poca información respecto a su dieta y comportamiento. Motivo, por el cual, presento con evidencias (fotografías) el primer reporte del consumo del fruto Hedyosmum mexicanum por parte de una tropa de Cebus imitator, en las faldas del Volcán Barva, Costa Rica, 2 625m sobre el nivel del mar.

Fruit scent and observer colour vision shape food-selection strategies in wild capuchin monkeys

The senses play critical roles in helping animals evaluate foods, including fruits that can change both in colour and scent during ripening to attract frugivores. Although numerous studies have assessed the impact of colour on fruit selection, comparatively little is known about fruit scent and how olfactory and visual data are integrated during foraging. We combine 25 months of behavioural data on 75 wild, white-faced capuchins (Cebus imitator) with measurements of fruit colours and scents from 18 dietary plant species. We show that frequency of fruit-directed olfactory behaviour is positively correlated with increases in the volume of fruit odours produced during ripening. Monkeys with red–green colour blindness sniffed fruits more often, indicating that increased reliance on olfaction is a behavioural strategy that mitigates decreased capacity to detect red–green colour contrast. These results demonstrate a complex interaction among fruit traits, sensory capacities and foraging strategies, which help explain variation in primate behaviour.

Small to modest impact of social group on the gut microbiome of wild Costa Rican capuchins in a seasonal forest.

The horizontal transmission of pathogenic and beneficial microbes has implications for health and development of socially living animals. Social group is repeatedly implicated as an important predictor of gut microbiome structure among primates, with individuals in neighboring social groups exhibiting distinct microbiomes. Here we examine whether group membership is a predictor of gut microbiome structure and diversity across three groups of white-faced capuchins (Cebus capucinus imitator) inhabiting a seasonal Costa Rican forest. We collected 62 fecal samples from 18 adult females during four sampling bouts. Sampling bouts spanned the dry-to-wet-to-dry seasonal transitions. To investigate gut microbial composition, we sequenced the V4 region of the 16S rRNA gene. We used the DADA2 pipeline to assign amplicon sequence variants and the RDP database to classify taxa. Our findings are: 1) gut microbiomes of capuchins clustered by social group in the late dry season, but this pattern was less evident in other sampling bouts; 2) social group was a significant variable in a PERMANOVA test of beta diversity, but it accounted for less variation than season; 3) social group was not an important predictor of abundance for the ten most abundant microbial taxa in capuchins; 4) when examining log2-fold abundances of microbes between social groups, there were significant differences in some pairwise comparisons. While this is suggestive of group-wide differences, individual variation may have a strong impact and should be assessed in future studies. Overall, we found a minor impact of social group membership on the gut microbiota of wild white-faced capuchins. Future research including home range overlap and resource use, as well as fine-scale investigation of individual variation, will further elucidate patterns of socially structured microbes.

Amplification Dynamics of Platy-1 Retrotransposons in the Cebidae Platyrrhine Lineage.

Platy-1 elements are Platyrrhine-specific, short interspersed elements originally discovered in the Callithrix jacchus (common marmoset) genome. To date, only the marmoset genome has been analyzed for Platy-1 repeat content. Here, we report full-length Platy-1 insertions in other New World monkey (NWM) genomes (Saimiri boliviensis, squirrel monkey; Cebus imitator, capuchin monkey; and Aotus nancymaae, owl monkey) and analyze the amplification dynamics of lineage-specific Platy-1 insertions. A relatively small number of full-length and lineage-specific Platy-1 elements were found in the squirrel, capuchin, and owl monkey genomes compared with the marmoset genome. In addition, only a few older Platy-1 subfamilies were recovered in this study, with no Platy-1 subfamilies younger than Platy-1-6. By contrast, 62 Platy-1 subfamilies were discovered in the marmoset genome. All of the lineage-specific insertions found in the squirrel and capuchin monkeys were fixed present. However, ∼15% of the lineage-specific Platy-1 loci in Aotus were polymorphic for insertion presence/absence. In addition, two new Platy-1 subfamilies were identified in the owl monkey genome with low nucleotide divergences compared with their respective consensus sequences, suggesting minimal ongoing retrotransposition in the Aotus genus and no current activity in the Saimiri, Cebus, and Sapajus genera. These comparative analyses highlight the finding that the high number of Platy-1 elements discovered in the marmoset genome is an exception among NWM analyzed thus far, rather than the rule. Future studies are needed to expand upon our knowledge of Platy-1 amplification in other NWM genomes.

Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest

Research on the gut microbiota of free-ranging mammals is offering new insights into dietary ecology. However, for free-ranging primates, little information is available for how microbiomes are influenced by ecological variation through time. Primates inhabiting seasonal tropical dry forests undergo seasonally specific decreases in food abundance and water availability, which have been linked to adverse health effects. Throughout the course of a seasonal transition in 2014, we collected fecal samples from three social groups of free-ranging white-faced capuchin monkeys (Cebus capucinus imitator) in Sector Santa Rosa, Área de Conservación Guanacaste, Costa Rica. 16S rRNA sequencing data reveal that unlike other primates, the white-faced capuchin monkey gut is dominated by Bifidobacterium and Streptococcus. Linear mixed effects models indicate that abundances of these genera are associated with fluctuating availability and consumption of fruit and arthropods, whereas beta diversity clusters by rainfall season. Whole shotgun metagenomics revealed that the capuchin gut is dominated by carbohydrate-binding modules associated with digestion of plant polysaccharides and chitin, matching seasonal dietary patterns. We conclude that rainfall and diet are associated with the diversity, composition, and function of the capuchin gut microbiome. Additionally, microbial fluctuations are likely contributing to nutrient uptake and thehealth of wild primate populations.

Habitual stone-tool-aided extractive foraging in white-faced capuchins, Cebus capucinus.

Habitual reliance on tool use is a marked behavioural difference between wild robust (genus Sapajus) and gracile (genus Cebus) capuchin monkeys. Despite being well studied and having a rich repertoire of social and extractive foraging traditions, Cebus sp. rarely use tools and have never been observed using stone tools. By contrast, habitual tool use by Sapajus is widespread. We review theory and discuss factors which might explain these differences in patterns of tool use between Cebus and Sapajus. We then report the first case of habitual stone tool use in a gracile capuchin: a population of white-faced capuchins (Cebus capucinus imitator) in Coiba National Park, Panama who habitually rely on hammerstone and anvil tool use to access structurally protected food items in coastal areas including Terminalia catappa seeds, hermit crabs, marine snails, terrestrial crabs and other items. This behaviour has persisted on one island in Coiba National Park since at least 2004. From 1 year of camera trapping, we found that stone tool use is strongly male-biased. Of the 205 camera trap days where tool use was recorded, adult females were never observed to use stone tools, although they were frequently recorded at the sites and engaged in scrounging behaviour. Stone tool use occurs year-round in this population; over half of all identifiable individuals were observed participating. At the most active tool use site, 83.2% of days where capuchins were sighted corresponded with tool use. Capuchins inhabiting the Coiba archipelago are highly terrestrial, under decreased predation pressure and potentially experience resource limitation compared to mainland populations—three conditions considered important for the evolution of stone tool use. White-faced capuchin tool use in Coiba National Park thus offers unique opportunities to explore the ecological drivers and evolutionary underpinnings of stone tool use in a comparative within- and between-species context.

Trichromatic perception of flower colour improves resource detection among New World monkeys

Many plants use colour to attract pollinators, which often possess colour vision systems well-suited for detecting flowers. Yet, to isolate the role of colour is difficult, as flowers also produce other cues. The study of florivory by Neotropical primates possessing polymorphic colour vision provides an opportunity to investigate the importance of colour directly. Here we determine whether differences in colour vision within a mixed population of wild dichromatic and trichromatic white-faced capuchins (Cebus capucinus imitator) affect flower foraging behaviours. We collected reflectance data for flower foods and modelled their chromatic properties to capuchin colour vision phenotypes. We collected behavioural data over 22 months spanning four years, determined the colour vision phenotype of each monkey based on amino acid variation of the L/M opsin gene from fecal DNA, and compared foraging behaviours of dichromats and trichromats. Most flowers were more conspicuous to trichromats, and trichromats foraged in small flower patches significantly more often. These data demonstrate a difference in wild primate foraging patterns based on colour vision differences, supporting the hypothesis that trichromacy enhances detection of small, ephemeral resources. This advantage, which may also extend to other foods, likely contributes to the maintenance of colour vision polymorphism in Neotropical monkeys.

Infant mortality in white-faced capuchins: The impact of alpha male replacements.

Infanticide is common in the context of alpha male replacements (AMR), particularly in groups where alpha males experience high reproductive skew and the infants are unlikely to be related to a new alpha male. We examined the relationship between the rate of infant mortality, infant age, and the occurrence and type of AMR in white-faced capuchin monkeys (Cebus capucinus imitator) of the Santa Rosa population in Sector Santa Rosa, Área de Conservación Guanacaste. Specifically, we investigated how the source of the new alpha male (coresident or extragroup) and relative aggression level during AMRs influenced infant mortality in this species. Between 1986 and 2015, we recorded 221 births in five study groups. Infants present at the time of an AMR, or born within 5.5 months following an AMR (i.e., conceived prior to AMR), experienced significantly higher mortality than those born during periods of group stability. Infant age was a significant predictor of infant survival, with the probability of surviving increasing by 0.4% for each additional day older an infant was at the time of the AMR. Infant mortality rates did not differ between AMRs by coresident males and extragroup males, possibly because the degree of relatedness between infants and new alphas did not significantly differ between coresident and extragroup AMRs. Infant mortality rates did not differ significantly between aggressive AMRs and more peaceful AMRs. Our results are consistent with predictions derived from the sexual selection hypothesis (SSH) of infanticide and suggest that future studies examine the role of testosterone as an underlying proximate mechanism for the aggression leading to this behavior. We argue that the sexual selection and generalized aggression hypotheses (GAH) of infanticide are best considered as different levels of analysis rather than competing hypotheses.

Seasonal importance of flowers to Costa Rican capuchins (Cebus capucinus imitator): Implications for plant and primate.

Our goal is to investigate flower foraging by capuchin monkeys, a behavior rarely studied in wild primates. We ask what drives seasonal variation in florivory rates: flower quality and abundance or fluctuations in fruit and invertebrate abundances. We explore how capuchins affect the reproductive success of flower food species by quantifying the potential pollination rate. We followed capuchin groups from dawn to dusk and recorded all flower foraging bouts. Flower food nutritional composition was compared to fruit and invertebrate foods. We recorded overall flower, fruit, and invertebrate abundances and compared the rate of flower foraging to these. We estimated the likelihood of pollination from the proportion of flower patch visits to each plant species that satisfied minimum behavioral requirements. Flower eating was highly seasonal, and was significantly negatively related to overall fruit and invertebrate abundance but not flower abundance. Although smaller than most fruits, flowers were nutritionally comparable to fruit foods by dry mass and contained higher average concentrations of protein. Capuchins are likely pollinators for Luehea speciosa; most foraging visits to this species occurred in a manner that makes outcrossing or geitonogamous pollination likely. Flowers are an important seasonal resource for capuchins. Flowers likely act as fallback foods during periods of reduced fruit and invertebrate abundance, and may exert evolutionary pressure disproportionate to their consumption. Capuchin florivory likely affects the reproductive success of some plants, potentially shaping forest structure. Our study illustrates the value of assessing the importance of rare foods in the primate diet.

Evidence of albinism in the white-faced monkey <i>Cebus capucinus imitator</i> on Coiba Island, Republic of Panama

No abstract

Ecotourism and primate habituation: Behavioral variation in two groups of white-faced capuchins (Cebus capucinus) from Costa Rica.

The increase of ecotourism operations within Costa Rica during the last 20 yrs has brought more and more humans into close, direct contact with several wildlife species. One of these species is the white-faced capuchin (Cebus capucinos), highly gregarious, and with exposure over time, willing to come into close vicinity of humans and their developments. Such contact has its advantages and disadvantages for the ecotourism industry. We observed white-faced monkeys in order to assess the impact of human presence and development on monkey behavior, with a focus on aggressive, affiliative, and foraging behaviors in Curú Wildlife Refuge (CWR), located in Puntarenas, Costa Rica, and to ascertain the degree of over-habituation of capuchin popula- tions at CWR. Though there exists no discrete behavioral parameters that measure over-habituation, it can be defined as an extreme state of habituation in which non-human primates not only lose fear of humans, but also actively include humans in social interactions or treat them as a food resource. We used instantaneous focal animal and group scan sampling during 8 wks in March and April 2012. Two groups (approximately 20-30 individuals each) of capuchins were observed; the first near the tourist development at the Southwestern area of CWR, representing a habituated population that regularly foraged, rested, and groomed in the presence of humans. The second, was observed in the Northeastern area of CWR, did not visit the center of human activity and exhibited fear of humans. The habituated group exhibited significantly fewer instances of threatened behavior in response to human presence (p < 0.0001) than the non-habituated group, and spent significantly more time eating and foraging (p < 0.0001). While the habituated monkeys at CWR may not be over-habituated, they could become that way as development, especially ecotourism, increases. Over-habituation is a problem that affects capuchins in certain ecotourism sites in Costa Rica. It is critical that the consequences of habituation be studied more carefully, primarily in areas where ecotourism operations draw visitors to wildlife habitats.