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.     

Evaluating social influences on food-processing behavior in white-faced capuchins (Cebus capucinus)

Interpopulation variability in patterns of food processing, similar to what is described as "traditional" or "cultural" variation in chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus), was identified in white-faced capuchins (Cebus capucinus). However, recent comparisons of food processing in capuchins were conducted only at the population level, with relatively little attention given to variability among groups, age/sex classes, or individuals. This paper examines variability in the processing of specific food types within the context of various social networks (i.e., patterns of association, rank, and kinship) among free-ranging Cebus capucinus at Santa Rosa National Park in Costa Rica. We collected data on two groups of white-faced capuchins in 2001, identifying rates of "food interest" for each individual, as well as forms of processing for specific food types. Juveniles exhibited the most interest in the food-processing behavior of other group members, and food interest was directed most frequently toward adult females. We identified distinctive processing techniques for several food items (Luehea candida pods, Sloanea terniflora fruits, and caterpillars) that facilitated comparisons among individuals within groups. Food-processing techniques for Sloanea fruit and caterpillars appeared to vary independently of the social networks examined in this study. However, we found evidence that variation in Luehea candida processing is to some degree linked to both patterns of association and social rank. The potential influence of these variables on observed food processing patterns warrants further scrutiny.     

Reconciliation in wild white-faced capuchins (Cebus capucinus)

The likelihood of reconciliation (defined as preferential peaceful contact among former opponents following conflicts) has been predicted to vary positively with relationship value and compatibility, and negatively with relationship security. Long-term data on wild white-faced capuchins (Cebus capucinus) indicate that dyads consisting of an adult female and an alpha male have high value and compatibility, but low security. Two studies of C. capucinus postconflict (PC) behavior were carried out at Lomas Barbudal Biological Reserve, Costa Rica. One study consisted of 30-min PC and matched control (MC) follows. The second study extracted PC and MC periods from long follows, yielding PC/MC periods averaging 105 min. In study 2, but not study 1, significantly more PC/MC pairs were attracted (former opponents affiliated with each other sooner in the PC period than in the MC period) than were dispersed (former opponents affiliated with each other sooner in the MC period than in the PC period). Reconciliation in study 2 could not be explained as a by-product of former opponents' tendency to seek affiliative contact with conspecifics generally, or of the spatial proximity of opponents following conflicts. Attempted reconciliation was less likely to be followed by renewed aggression when reconciliation attempts were delayed following conflicts. The data were insufficient for a formal test of differences in conciliatory tendency (the difference between the number of attracted and dispersed PC/MC pairs, divided by the total number of pairs) among dyad types to be conducted.     

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.     

Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus)

I examined sex differences in diet and foraging behavior in two groups of white-faced capuchin monkeys (Cebus capucinus)in a tropical dry forest at Santa Rosa National Park, Costa Rica. I tested three hypotheses: sex differences in diet and foraging behavior are best explained by (1) sexual dimorphism, (2) the energy demands of pregnancy and lactation for females;and (3) avoidance of competition between the sexes. Sexual dimorphism offered the best explanation of sex differences in the diet and foraging behavior of C. capucinus,accurately predicting that males do more strenuous foraging activity, make less use of small foraging supports, and spend more time on or near the ground. Females spent more time foraging than males did but probably obtained a lower protein yield per unit foraging time. Females exploited more small and embedded invertebrates, while males ate more large invertebrates and vertebrate prey. Pregnant and lactating females spent more time resting and less time foraging than other females did, increasing their foraging return by focusing on foods requiring little handling. There was little evidence of competition avoidance between the sexes.     

Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

Carrying and hand-use patterns in Panamanian white-faced capuchins (Cebus capucinus)

The aim of this project was to examine the potential influence of postural regulation on capuchin hand-use patterns by focusing on tasks that involved the carrying of objects. Two months were spent on Barro Colorado Island, Panama, collecting data on ten white-faced capuchins (Cebus capucicus) (four adult males/six adult females). Over 215 contact hours were spent with the monkeys, and a total of 213 carries were recorded. No hand preference bias at the population level was found for the carry task; and no detectable hand-use patterns for carry were correlated with the weight of the object carried (except a right-hand bias for carrying medium-sized objects), the plane of the monkey's movement, its locomotor pattern, or its height above the ground. Therefore, the results of this study do not support the hypothesis that the need for postural regulation while carrying an object influences hand-use patterns in free-ranging capuchins. Our results are especially important because they are contrary to the results of the only other free-ranging capuchin laterality study conducted to date (Panger, 1998).     

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.     

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.     

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.     

Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus)

In many primate species, conspicuous behavioral and/or morphological changes are indicators of the fertile phase of the female cycle. However, several primate species, such as the white-faced capuchin, lack these cues. This is referred to as "concealed ovulation," and is argued to be a reproductive strategy that confuses paternity and lowers the risk of infanticide. We studied 10 adult female white-faced capuchins in Santa Rosa National Park, Costa Rica, from January to June 2002. We determined their ovarian cycling patterns by analyzing fecal ovarian hormones, and compared simultaneously collected behavioral data to determine which, if any, cues females use to signal their fertile phases. We found that four females cycled during the study period but ceased to cycle without becoming pregnant. We considered several explanations for the lack of conception during our study, including reproductive seasonality. We found that female C. capucinus showed only small increases in rates of affiliative/proceptive behaviors directed toward adult males during their periovulatory phases. The best indicator of cycle phase was a significant increase in male affiliative behaviors (e.g., following and grooming bouts) and sexual behaviors (e.g., copulations and courtship displays) directed toward females during the periovulatory phase compared to the nonovulatory phase. Our finding that females exhibit little proceptive behavior, but that copulations and male courtship are nonetheless concentrated in periovulatory phases suggests that even though females do not provide behavioral and morphological cues to ovulation, males are still able to detect it. Infanticide occurs with some frequency in these monkeys, and there is evidence for postconceptive mating as a female strategy to lower risk of infanticide via paternity confusion. However, despite this occurrence of nonconceptive mating and the absence of female cues to ovulation, truly concealed ovulation does not appear to be characteristic of this study population of white-faced capuchins.     

Resource patch size and flexible foraging in white-faced capuchins (Cebus capucinus)

White-faced capuchins (Cebus capucinus)on Barro Colorado Island, Panama, have a flexible foraging strategy. Typically, foraging party size is small and individuals feed dispersed from one another. When seasonal fruiting of large volume trees occurs, the majority of the group forages simultaneously. As C. capucinusdo not display a rigorous dominance structure and there are few indications that individuals or coalitions monopolize food patches,individuals are expected to display scramble strategies instead of high frequencies of contest competition. I recorded foraging party size (simultaneous foragers), the total number of animals to feed successively, and the diameter at breast height (DBH) of fruit trees used in two habituated troops. Individuals in each group spent a substantial amount of time — 65 and 48% of foraging time for each group — foraging in party sizes of one. Monkeys predominantly foraged alone in small trees (0- to 20- cm DBH), successively in medium trees (21- to 60- cm DBH), and simultaneously in large trees (>61- cm DBH). They used small trees more frequently than all other tree classes. In medium-sized trees, although fruit was plentiful, space was limited. In these trees Cebusforaged successively. In large-volume trees, space and fruit were abundant and several individuals fed together. As the DBH of fruiting trees increased, the average foraging party size increased exponentially. Cebus capucinusat Barro Colorado Island modify their foraging party size to adapt to the seasonal patterns of fruit production.     

Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus)

I aim to explicate the pattern of differences and relations between the sexes in two groups ofC. capucinus, in terms of phylogenetic, social and ecological predictors. I use three lines of evidence to develop predictions as to how male and femaleC. capucinus interact and how the sexes differ in behavior: (1) phylogenetic similarities to other species ofCebus; (2) a general model of sex differences in female-bonded social systems; and (3) ecological analogy of Old World monkeys. First, I conclude that phylogenetic affinity is a good predictor in thatC. capucinus are similar to other species ofCebus in many patterns of sex-differentiated behavior. An exception is that, unlikeC. apella andC. olivaceus, in which a single breeding male is reported to be highly conspicuous in each group,C. capucinus live in a decidedly multimale system. Secondly, the general model of sex differences in female philopatric, male-dispersal societies, which was originally developed for Old World species, also accurately predicts several aspects of social behavior inC. capucinus. Thirdly, a proposed ecological analogy betweenCercopithecus ascanius andspecies of Cebus is not substantiated in this study of C. capucinus, though the analogy is apparently well suited to the social dynamics of other species in the genusCebus.     

Social factors influencing natal dispersal in male white-faced capuchins (Cebus capucinus)

White-faced capuchin males disperse from their natal group at around 4.5 years of age, but there is much variation in dispersal timing: our youngest confirmed disperser was 19 months and the oldest 11 years old. In this study, we investigate possible factors influencing dispersal decisions in this species. Between 1983 and 2010, 64 males were born into three study groups in Santa Rosa National Park, Area de Conservación Guanacaste, and Costa Rica. As of August 2010, 21 died or were presumed dead (<14 months), 13 remained natal residents, and 30 were presumed dispersers. We used backward logistic regression to identify proximate factors that predict the occurrence of male natal dispersal. The occurrence of a takeover (significant positive association) and group size (nonsignificant negative association) were included in the model. Male age, number of maternal brothers, and number of adult males were not significant predictors of natal dispersal. The resultant model correctly classified 97% of dispersed and 89% of resident natal males, for an overall success rate of 95%. The occurrence of a group takeover was the strongest predictor of male dispersal, with natal males being 18.7 times more likely to disperse in the context of a group takeover than during peaceful times. A linear regression model showed that the tenure length of a male's probable father influences the age of natal dispersal, explaining 15% of the observed variation in age. However, when our oldest disperser was removed (an outlier) this effect disappeared. Collectively, these results indicate that group instability, as evidenced by the occurrence of a takeover, shorter tenure length of a natal male's father, and smaller group size, triggers natal dispersal in this species while the converse leads to a delay. These data add to our growing evidence of the enormous impact that takeovers have on the behavioral ecology of this species.     

Explaining variation in affiliative relationships among male white-faced capuchins (Cebus capucinus)

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

The behavior of white-faced capuchins (Cebus capucinus) at a dry-season waterhole

During a study of white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, northwest Costa Rica, the study troop drank daily from a single terrestrial waterhole for approximately three months during the dry season. The drinking order of troop members at the waterhole was not random: adult males tended to be in the first quartile of the drinking progression, adult females generally occurred with equal frequency throughout the progression, and juveniles drank most commonly in the third quartile. There were also differences in the usual drinking ranks among individuals of the same age-sex class. It is hypothesized that those adult males which are usually first in the progression are increasing their personal fitness by reducing the risk of predation on their offspring and on potential mates. The tendency of adult females to precede juveniles may similarly reflect protection of offspring. The daily visits to the waterhole by the study troop did not appear to greatly restrict the use of their range. It is suggested, however, that the availability of standing sources of water may be an important factor affecting the local distribution and density of capuchins in seasonally and chronically dry areas.     

Color-vision polymorphism in wild capuchins (Cebus capucinus) and spider monkeys (Ateles geoffroyi) in Costa Rica

New World monkeys are unique in exhibiting a color-vision polymorphism due to an allelic variation of the red-green visual pigment gene. This makes these monkeys excellent subjects for studying the adaptive evolution of the visual system from both molecular and ecological viewpoints. However, the allele frequencies of the pigments within a natural population have not been well investigated. As a first step toward understanding the relationship between vision and behavior, we conducted color-vision typing by analyzing fecal DNA from two wild groups of white-faced capuchin monkeys (Cebus capucinus) and one group of black-handed spider monkeys (Ateles geoffroyi) inhabiting Santa Rosa National Park of Costa Rica. All color-typed monkeys were individually identified. In C. capucinus and A. geoffroyi we found three and two pigment types, respectively, and the spectral mechanism that created one of the two Ateles pigments was found to be novel. In one Cebus group and the Ateles group, all alleles were present, whereas in the other Cebus group only two alleles were found, with one allele predominating. This was likely due to the effect of close inbreeding, indicating that wild populations can exhibit a variety of allele compositions. This result also suggests that the color-vision polymorphism can be easily distorted by natural factors, such as inbreeding, skewing the population structure.     

Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus

New World monkeys exhibit a color vision polymorphism. It resultsfrom allelic variation of the single-locus middle-to-long wavelengthopsin gene on the X chromosome. Females that are heterozygousfor the gene possess trichromatic vision. All other individualspossess dichromatic vision. The prevailing hypothesis for themaintenance of the color vision polymorphism is through a consistentfitness advantage to heterozygous trichromatic females. Suchfemales are predicted to be more efficient than dichromats whendetecting and selecting fruit. Recent experiments with captivecallitrichid primates provided support for this hypothesis bydemonstrating that color vision phenotype affects behavioralresponses to contrived food targets. Yet, the assumptions thattrichromatic females acquire more calories from fruit, or thatnumber of offspring is linked to caloric intake, remain untested.Here, we assess if, in the wild, heterozygous trichromatic individualsin a group of white-faced capuchins (Cebus capucinus) enjoyan energetic advantage over dichromats when foraging on fruit.Contrary to the assumptions of previous theoretical and experimentalstudies, our analysis of C. capucinus foraging behavior showsthat trichromats do not differ from dichromats in their fruitor energy acquisition rates. For white-faced capuchins, theadvantage of trichromatic vision may be related to the detectionof predators, animal prey, or fruit under mesopic conditions.This result demonstrates the importance of using a fitness currencythat is relevant to individual animals to test evolutionaryhypotheses.     

Hand preferences on unimanual and bimanual tasks in white-faced capuchins (Cebus capucinus)

This study examined hand preference in white-faced capuchins on a unimanual task and on a coordinated bimanual task. For the unimanual task, handedness was assessed by observing simple reaching for small grains. For the bimanual task, tubes lined with chocolate paste inside were presented to the capuchins. The hand and the finger(s) used to remove chocolate paste were recorded. Seven individuals out of eight in the reaching task and 12 out of 13 in the tube task exhibited a hand preference. Moreover, test-retest correlations showed stability in hand use across time for the coordinated bimanual task. We found no significant differences in strength of hand preference between sexes. Finally, as noted in other primate species, the capuchins were more lateralized in the bimanual task compared to the unimanual task.