Variability in food-processing behavior among white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica

Observed patterns of variability in the food-processing behavior of white-faced capuchins (Cebus capucinus) across populations may reflect foraging traditions. However, there has been relatively little attention given to intrapopulation variability in food processing among groups and age/sex classes, making recent cross-population comparisons difficult to interpret. In this paper, we provide data on patterns of object use in foraging that we observed at Santa Rosa National Park, Costa Rica, for comparison with published data from a neighboring research site, Palo Verde National Park. We also describe the techniques used to process two food items consumed by Cebus capucinus at Santa Rosa, and discuss the factors that may underlie observed variability. We conducted a 6-month study on two groups of capuchins in 2001, and collected data on general activity and feeding patterns, rates and forms of object use, and distinctive processing techniques employed for two specific foods (Sloanea terniflora and Luehea candida). Rates of object-use behavior at Santa Rosa were considerably higher than those reported for Palo Verde and showed significant variation between groups and age/sex classes, as did patterns of Sloanea and Luehea processing. Observed differences in feeding rates between groups may reflect food availability or relative profitability, whereas variation between age/sex classes seems to reflect differences in the physical capabilities, foraging strategies, and the relative experience of mature and immature animals. Further research is needed to identify how a social context may influence the acquisition of food-processing techniques in juveniles and the development of foraging traditions in social groups.     

Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus)

Researchers have identified a variety of cross-site differences in the foraging behavior of free-ranging great apes, most notably among chimpanzees (Pan troglodytes) and more recently orangutans (Pongo pygmaeus), that are not due to obvious genetic or ecological differences. These differences are often referred to as "traditions." What is not known is whether this high level of interpopulation variation in behavior is limited to hominoids. In this study, we use long-term data from three Costa Rican field sites that are geographically close and similar ecologically to identify potential foraging traditions in white-faced capuchins (Cebus capucinus). Foraging traditions are predicted in Cebus because of many behavioral and morphological convergences between this genus and the great apes. The processing techniques used for the same food species were compared across sites, and all differences found were classified as present, habitual, or customary. Proximity data were also analyzed to determine if social learning mechanisms could explain variation in foraging behavior. Of the 61 foods compared, we found that 20 of them are processed differently by capuchins across sites. The differences involve pound, rub, tap, "fulcrum," "leaf-wrap," and "army ant following." For most of the differences with enough data to analyze, the average proximity score of the "matched" dyads (two individuals within a group who shared a "different" processing technique) was statistically higher than the average proximity score of the remaining "unmatched" dyads.     

Social traditions and social learning in capuchin monkeys (Cebus)

Capuchin monkeys (genus Cebus) have evolutionarily converged with humans and chimpanzees in a number of ways, including large brain size, omnivory and extractive foraging, extensive cooperation and coalitionary behaviour and a reliance on social learning. Recent research has documented a richer repertoire of group-specific social conventions in the coalition-prone Cebus capucinus than in any other non-human primate species; these social rituals appear designed to test the strength of social bonds. Such diverse social conventions have not yet been noted in Cebus apella, despite extensive observation at multiple sites. The more robust and widely distributed C. apella is notable for the diversity of its tool-use repertoire, particularly in marginal habitats. Although C. capucinus does not often use tools, white-faced capuchins do specialize in foods requiring multi-step processing, and there are often multiple techniques used by different individuals within the same social group. Immatures preferentially observe foragers who are eating rare foods and hard-to-process foods. Young foragers, especially females, tend to adopt the same foraging techniques as their close associates.     

Vertebrate predation in Cebus capucinus: meat eating in a neotropical monkey

A long-term study of two groups of white-faced capuchins (Cebus capucinus) in Santa Rosa National Park in Costa Rica provides evidence of unusually high levels of vertebrate predation compared to those reported in other field studies of Cebus. The hunting techniques for different prey types are described, and several questions concerning vertebrate predation in primates are addressed. Why is there variation between individuals and between groups in the rate of predation? Why do males hunt more than females? Previous hypotheses to explain hunting in Old World primates are applied to this Neotropical example. Finally, I argue that successful vertebrate predation can readily arise in species like Cebus, which are characterized by opportunistic foraging patterns, manipulative and cognitive skills and well-developed techniques for locating and subduing invertebrate prey.     

Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica

We examined thermoregulatory behaviors in a wild population of white-faced capuchins (Cebus capucinus) inhabiting a highly seasonal dry forest in Santa Rosa National Park (SRNP), Costa Rica. The dry season in SRNP lasts approximately 5 months and is characterized by high ambient temperatures regularly exceeding 37 degrees C, low relative humidity, and the near absence of precipitation. This study demonstrates that capuchins rest more and travel shorter distances during the hottest and driest hours of the day, and suggests that they extend their tongues to lower body temperature via evaporative cooling. Seasonal weather patterns and group movement data reported here are based on 940 h of observations on three social groups of capuchins (wet season: 370 h, dry season: 570 h). In the dry season, the proportion of time spent resting increased at higher temperatures whereas the proportion of time spent traveling decreased. Distance traveled between location points taken at half-hour intervals decreased significantly as temperature increased, although the correlation was not strong. Capuchins exposed their tongues during hot, dry, windy conditions, and this behavior was much more frequent in the dry season. Temperature was significantly higher and humidity significantly lower for "tongue-out" events than expected for a random event in the dry season. Finally, as surface water became scarce, home-range areas of heavy use became increasingly centered on the remaining permanent water sources. These results suggest that heat stress and water scarcity are significant influences on the behavior of capuchins in hot, dry conditions.     

Urine Washing and Sniffing in Wild White-faced Capuchins (<Emphasis Type="Italic">Cebus capucinus</Emphasis>): Testing Functional Hypotheses

Urine washing (UW) is taxonomically widespread among strepsirhines and platyrrhines, yet its functional significance is still unclear. We used 2274 h of focal follows of 35 adult and subadult wild white-faced capuchins (Cebus capucinus) to test 1) the intergroup signaling, intragroup social signaling, and thermoregulatory hypotheses for UW and 2) the hypothesis that individuals sniff each other's urine and other traces to gather socially significant information. Males engaged in significantly more UW than females. All 5 α-males engaged in more UW than subordinate males did, including 4 α-males that increased their UW rate above that of their male groupmates after their rise to α rank. Males engaged in significantly less UW while in view of other males than at other times. Male-male sniffing rates do not correlate with either aggression rate or dominance rank distance. Urine washing rates did not increase while subjects were in parts of their home range where more intergroup encounters occurred. Urine washing rates were highest early in the morning and late in the afternoon, presumably when temperatures were coolest. The data do not support either the thermoregulatory or social signaling hypothesis. We suggest that experiments with captive capuchins are necessary to resolve the issue of the function of urine washing in the taxon.     

Variation in substrate use by white-faced capuchins

We examined substrate use by a group of white-faced capuchins (Cebus capucinus) during the dry season in the seasonally dry forest at Palo Verde National Park, Costa Rica. The group's most common terrestrial activities were foraging and traveling. Subjuveniles were most terrestrial, traveling terrestrially 55% of the time and foraging terrestrially 42% of the time. Juveniles were least terrestrial (36% travel, 24% forage). Rest and social activity were highly arboreal for all age classes. Terrestrial foraging was most common in the middle of the day. Terrestrial traveling became increasingly common over the course of the day.     

Wild capuchins (Cebus capucinus) fail to use tools in an experimental field study

From September through November 2000 we conducted an experimental field study of tool use in a group of 15 wild white-faced capuchins (Cebus capucinus) in Costa Rica. The problem presented to the capuchins involved the use of wooden dowels as probes to obtain a food reward (two bananas) located inside a clear Plexiglas box. Specifically, the task required the capuchins to manually insert a dowel into any of six holes drilled into the box in order to push the bananas off a shelf. The banana could then be retrieved through a large opening at the bottom of the box. The capuchins visited the tool-use platform 702 times over the course of 55 consecutive days and under several experimental conditions. During the first 21 days of the study, they explored the box but made no attempt to touch or pick up the dowels. Even after we placed the dowels in the holes, the capuchins only occasionally manipulated them. Overall, the results indicate that the capuchins did not use a tool to solve this novel foraging problem.     

The effects of provisioning and crop-raiding on the diet and foraging activities of human-commensal white-faced capuchins (Cebus capucinus)

Non-human primates are coming into increasingly frequent contact with humans and with human-modified environments. The potential for monkeys to survive in such modified landscapes is questionable, and is likely related to a species' behavioral plasticity, particularly as it relates to diet. In this study, I explore the ways in which white-faced capuchins (Cebus capucinus) adjust their diet and foraging behaviors in response to anthropogenic impact. I compare a troop of human-commensal monkeys and a similar troop of wild-feeding monkeys living within the Curú Wildlife Refuge in western Costa Rica for differences in overall diet composition and activity budgets to evaluate the impact of habitat change in this context. The commensal-living white-faced capuchins rely on raided coconut (Cocos nucifera) and oil palm (Elaeis guineensis) crops and provisioned or stolen human foods for over one-half of their total diet. Regardless of this highly anthropogenic diet, the two study troops do not significantly differ in their activity budgets, and the human-commensal troop maintains wild-foraging activities consistent with those of the wild-feeding troop. These data suggest that the white-faced capuchins at this site are responding to anthropogenic disturbance primarily through the exploitation of human food resources, but they do not yet appear to have lost the foraging skills required to survive in this modified landscape on their own. This study adds to our growing body of knowledge on primate survival in matrix habitats, and will hopefully inform primate management plans throughout the Neotropics.     

Ecological niche differences betweenAlouatta palliata andCebus capucinus comparing feeding modes,branch use,and diet

During the wet season, two sympatric species of primates,Alouatta palliata (mantled howlers) andCebus capucinus (white-faced capuchins), were assayed for feeding niche differences through behavioral and habitat use patterns at Refugio de Fauna Silvestre Curu in Costa Rica. Differences in the use of relative diameter and thickness of branches and five different modes of feeding were compared between the species. White-faced capuchins used more manipulative modes of obtaining food, a wider range of arboreal habitat, and had a more diverse diet than mantled howlers. Mantled howlers may be more restricted than white-faced capuchins in arboreal microhabitat use due to their possible need for large support branches during feeding bouts and resting periods. We report that differences in feeding behaviors, diet, and arboreal habitat use seem to play a large role in separating these species niches.     

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.     

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.     

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.     

The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

Prehensile tails appear to have evolved at least twice in platyrrhine evolution. In the atelines, the tail is relatively long and possesses a bare area on the distal part of its ventral surface that is covered with der-matoglyphs and richly innervated with Meissner's corpuscles. In contrast, the prehensile tail of Cebus is relatively short, fully haired, and lacks specialized tactile receptors. Little is currently known regarding tail function in capuchins, and whether their prehensile tail serves a greater role in feeding or traveling. In this paper we examine patterns of positional behavior, substrate preference, and tail use in wild white-faced capuchins (Cebus capucinus) inhabiting a wet tropical forest in northeastern Costa Rica. Observational data were collected over the course of 3 months on adult capuchins using an instantaneous focal animal time sampling technique. Differences in the frequency and context of tail use, and the estimated amount of weight support provided by the tail relative to other appendages during feeding/foraging and traveling were used as measures of the ecological role of this specialized organ in capuchin positional behavior. During travel, quadrupedal walking, leaping, and climbing dominated the capuchin positional repertoire. The capuchin tail provided support in only 13.3% of travel and was principally employed during below branch locomotor activities. In contrast, tail-assisted postures accounted for 40.6% of all feeding and foraging records and occurred primarily in two contexts. The tail was used to suspend the individual below a branch while feeding, as well as to provide leverage and weight support in above-branch postures associated with the extraction of prey from difficult to search substrates. A comparison of tail use in Cebus, with published data on the atelines indicates that both taxa possess a grasping tail that is capable of supporting the animal's full body weight. In capuchins and howling monkeys, the tail appears to be used more frequently and serves a greater weight-bearing role during feeding than during traveling. In Ateles, and possibly Brachyteles, and Lagothrix, however, the prehensile tail serves a dual role in both feeding and forelimb suspensory locomotion. Additional relationships between white-faced capuchin feeding, positional behavior, extractive foraging techniques, and prehensile tail use are discussed.     

Vertebrate Predation and Food-Sharing in Cebus and Pan

Capuchins and chimpanzees are the only nonhuman primates apart from baboons known to prey systematically upon relatively large vertebrates. Vertebrate predation is common and well documented in Pan troglodytes, rare in Pan paniscus, and commonly reported but infrequently studied in Cebus. Food-sharing is common in both Pan species but rarely reported for wild capuchins. I present data on vertebrate predation and food-sharing by white-faced capuchins (Cebus capucinus) from ongoing field studies at Santa Rosa National Park, Costa Rica. We have observed 106 successful predation events resulting in the capture of 156 prey items during 2929 observation hr (5.35 prey per 100 hr). Squirrels and nestling coatis comprised half of the prey taken; the remainder were mainly nestling birds and eggs. Adult males took 52% of all prey and 67% of squirrels. Squirrels are actively hunted and about 65% of them are adults. I estimated that the average capuchin group kills 43–50 squirrels annually, mostly during the dry season. Capuchins hunt squirrels in groups 81% of the time, and 17% of hunts are successful. There is no evidence for cooperative hunting, but occasional collaboration is suggested. Rates of food-sharing were low (1.7 per 100 hr), and meat was the only food shared between adults. I compare predation and food-sharing in C. capucinus with published data for Pan troglodytes, primarily in Gombe and Taï National Parks. I discuss sex differences, hunting strategies, the relationship between hunting and food-sharing, and various ecological and social factors that may promote vertebrate predation in Pan and Cebus.     

Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method

Food abundance and distribution have played a central role in the conceptual theory of primate socioecology [Janson, Behaviour 105:53-76, 1988; Isbell, Behavioral Ecology 2:143-155, 1991; Sterck et al., Behavioral Ecology and Sociobiology 41:291-309, 1997; van Schaik, In: Standen V, Foley RA, editors, Comparative Socioecology. Oxford: Blackwell. p 195-218, 1989]. This theory predicts that agonistic ("contest") competition should occur when food is distributed in discrete, defensible patches; in contrast, when food sources are distributed uniformly or randomly, non-agonistic ("scramble") competition is expected. Primatologists usually measure resource density and patchiness from a botanical perspective, ignoring the biology of the animal being studied. Such an approach may be irrelevant in terms of how animals view the dispersion of resources. Using a novel focal-tree method that measures resource availability on a scale that is both spatially and temporally relevant to the animal under investigation, we take a cost-benefit approach to predict the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus) from 11 ecological and social variables. We retained four variables in the regression model: two representing the opportunity for aggression (i.e., feeding bout length and the number of feeding adult females), and two representing opportunity costs (i.e., fruit abundance and the number of potential feeding sites in the focal tree). The results of this study indicate that the amount of food-related aggression in white-faced capuchins can be predicted by variables representing the costs and benefits of contesting a food resource.     

Who cares who calls? Selective responses to the lost calls of socially dominant group members in the white‐faced capuchin (Cebus Capucinus)

In many social mammals and birds, soft vocalizations are habitually produced during dispersed moving and foraging, the function being to maintain contact and regulate spacing between group members. In some species, much louder calls are given sporadically by specific individuals when they become separated from the group, or 'lost'. The function of these calls has seldom been specifically tested, particularly among social primates, but is often assumed to involve regaining contact with the group based on a combination of individually distinctive calls and antiphonal responses to them from within the group. To test these assumptions, we conducted research on two groups of white-faced capuchins (Cebus capucinus) in Costa Rica. We analyzed 82 bouts of 'lost' calls given by 13 different adult individuals when separated from the group and the antiphonal responses they elicited. Lost calls were individually distinctive and were answered in 35% of calling episodes. Answers were selective: dominant males and females were answered more than were subordinate callers of either sex. As a result, dominant callers relocated and returned to the group more quickly than did subordinate callers. We discuss the potential proximate motivations for, and ultimate benefits of, such selective answering of dominant group members.     

The Repertoire and Social Function of Facial Displays in Cebus capucinus

Systematic studies on facial displays in capuchins are limited and based mainly on studies of tufted capuchins (Cebus apella). Despite the great social-morphological variability within Cebus suggesting possible morphological and functional variations in the facial displays of different species, no study has considered thoroughly visual communication in the genus. Our aim was to describe the facial displays of white-faced capuchins and to assess their distribution and communicative function. We observed 15 captive white-faced capuchins in the Primate Centre of the Louis Pasteur University of Strasbourg, for a total of 198 h. We described the following facial displays: relaxed open-mouth, lip-smacking, open-mouth threat-face, silent bared-teeth, open-mouth silent bared-teeth, protruded-lip face, and tongue-out. We never observed the scalp-lifting display, one of the most common displays characterizing tufted capuchins. White-faced capuchins use the majority of facial displays in an affiliative or playful context; only the open-mouth threat-face display is associated with aggressive behaviors. White-faced capuchins lack ritualized signals of submission. The fact that in white-faced capuchins the silent bared-teeth display conveys only a positive message, while in tufted capuchins it signals submission as well as affiliation, supports the covariation hypothesis (Thierry 2004 Social epigenesis. In B. Thierry, M. Singh, & W. Kaummans (Eds.), Macaque societies: A Model for the study of social organization, pp. 267–294. Oxford University Press).     

Rescue behavior in white-faced capuchin monkeys during an intergroup attack: support for the infanticide avoidance hypothesis

In this work we report the first published observational evidence of rescue behavior during an intergroup interaction in white-faced capuchin monkeys (Cebus capucinus). The study groups (groups AA and RR) inhabit the forest of Lomas Barbudal Biological Reserve in Guanacaste, Costa Rica, and have been under investigation since 1990 and 1997, respectively. Here we report a single interaction in which a victim mother-infant pair was rescued from potential injury or death by the intervention of an adult male from their social group during an intergroup encounter. We discuss several hypotheses that may be relevant in explaining this unique observation.     

Impact of Male Takeovers on Infant Deaths,Births and Conceptions in Cebus capucinus at Santa Rosa,Costa Rica

Male takeovers are associated with infant wounding and death in 3 of 4 capuchin species. In this paper, I analyze the effects of male takeovers on infant mortality and the subsequent conceptions and interbirth intervals of their mothers over an 18-yr period and test predictions of the sexual selection model of infanticide for white-faced capuchins, (Cebus capucinus). Major findings are that infants are significantly more likely to die in the 3- and 12-mo periods following a takeover than in times of peace and that a female whose infant dies experiences a significantly shorter interbirth interval before her next infant is born than she would have had the former infant survived. In the vast majority of cases, the invading males become resident in the group and are present during the subsequent conceptions of the females in the group. However, overall conception rates do not rise significantly in the year after a takeover, there is no relationship between the age of the infant at death and the length of the mother's subsequent interbirth interval, and it is not yet clear if male infants are preferentially targeted by invading males. Most takeovers occur during the 6-mo dry season and most conceptions occur in the wet season, 3–6 mo later. My findings support the major predictions of the sexual selection model of infanticide in primates and demonstrate that male takeovers of social groups have substantial effects on infant survival and maternal parturition patterns in Cebus capucinus.