Why don’tSaimiri oerstedii andCebus capucinus form mixed-species groups?

The instances of association with Cebus capucinustroops were monitored for 11 months as part of a field study of Saimiri oerstediiin a tropical wet forest in Costa Rica, Parque Nacional Corcovado. Contrary to the usual situation in South America, where S. sciureusforms persistent mixed-species groups with Cebus apella,in Corcovado S. oerstediirarely associated with Cebus capucinus;the frequencies were consistent with those expected from random association. Depending on the season, the S. oerstediitroop spent between 2.3 and 11.8% of its time in the vicinity of a Cebus capucinustroop. Most associations appeared to be chance meetings of short duration. When the two species did associate for an extended period, it was Cebus capucinus,and not S. oerstedii,that appeared to maintain the association, possibly in order to benefit from the antipredator behavior of S. oerstedii.There was no evidence that either species benefited from enhanced foraging efficiency when in association.     

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.     

Canine Dimorphism and Interspecific Canine Form in Cebus

I investigated canine dimorphism and interspecific canine form in adult specimens from 4 capuchin species (Cebus albifrons, C. apella, C. capucinus, and C. olivaceus). I used various univariate and multivariate statistics, which are based on 6 variables, to test several hypotheses that are based upon the finding that canine dimorphism is strongly associated with intermale competition in platyrrhines (Kay et al., 1988), Greenfield (1992a), Plavcan and van Schaik (1992, 1994). Results from the indices of canine dimorphism and the unpaired t-tests corroborate the prediction that males of each species possess significantly larger canines than those of females. Large male canines are especially prominent in 2 variables, maxillary and mandibular canine height. Greene's t-test (1989) does not support the prediction that Cebus apella and C. olivaceus possess a larger degree of canine dimorphism relative to C. albifrons and C. capucinus. No interspecific differences in degree of canine dimorphism are indicated by this test. Results of the discriminant function analyses (DFA) do not find that Cebus apella and C. olivaceus possess different canine form relative to C. albifrons and C. capucinus as predicted. However, Cebus apella is differentiated from the untufted capuchins (C. albifrons, C. capucinus, and C. olivaceus) by the DFA. I suggest that intermale competition is the primary selective force underlying the observed morphological patterns; however, it does not explain all the variation associated with canine dimorphism in Cebus.     

Traditions in spider monkeys are biased towards the social domain

Cross-site comparison studies of behavioral variation can provide evidence for traditions in wild species once ecological and genetic factors are excluded as causes for cross-site differences. These studies ensure behavior variants are considered within the context of a species' ecology and evolutionary adaptations. We examined wide-scale geographic variation in the behavior of spider monkeys (Ateles geoffroyi) across five long-term field sites in Central America using a well established ethnographic cross-site survey method. Spider monkeys possess a relatively rare social system with a high degree of fission-fusion dynamics, also typical of chimpanzees (Pan troglodytes) and humans (Homo sapiens). From the initial 62 behaviors surveyed 65% failed to meet the necessary criteria for traditions. The remaining 22 behaviors showed cross-site variation in occurrence ranging from absent through to customary, representing to our knowledge, the first documented cases of traditions in this taxon and only the second case of multiple traditions in a New World monkey species. Of the 22 behavioral variants recorded across all sites, on average 57% occurred in the social domain, 19% in food-related domains and 24% in other domains. This social bias contrasts with the food-related bias reported in great ape cross-site comparison studies and has implications for the evolution of human culture. No pattern of geographical radiation was found in relation to distance across sites. Our findings promote A. geoffroyi as a model species to investigate traditions with field and captive based experiments and emphasize the importance of the social domain for the study of animal traditions.     

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.     

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.     

Activity Patterns,Home Range Size,and Intergroup Encounters in <Emphasis Type="Italic">Cebus albifrons</Emphasis> Support Existing Models of Capuchin Socioecology

Variation in ranging behavior, social organization, and feeding ecology among capuchins (Cebus spp.) is a classic example of how closely related species may be differentially adapted to their local environments. Marked differences in all 3 areas occur among Cebus spp. between the untufted capuchins (Cebus capucinus, C. olivaceous, and C. albifrons) and the tufted capuchins (C. apella, C. xanthosternos, C. nigritus, and C. libidinosus). The key socioecological distinction between the 2 groups has traditionally been that, compared with the tufted group, untufted capuchins eat more ripe foods, as befits their more gracile masticatory system; range more broadly in search of high-quality foods; and live in larger groups with more males and more agonistic interactions between groups. Here I assess how well the basic socioecological characteristics —activity budget, ranging— of previously unstudied Ecuadorian Cebus albifrons fit within this model. Few researchers have conducted studies on Cebus albifrons, despite its prominent role in the initial development of the model for socioecology of Cebus. The results of my 1-yr study of a single social group support the model’s general characterization of untufted capuchins in ranging and feeding behaviors, but also suggest that direct ecological and demographic effects, in addition to adaptation to local conditions, may explain additional variation in group size across species of Cebus.     

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli.     

Patterns of foraging and range use by three species of neotropical primates

This paper describes the diet and range use patterns of the three species of primates in Santa Rosa National Park, Costa Rica (Ateles geoffroyi, Alouatta palliata, andCebus capucinus) and examines the variation in these variables as they relate to seasonal changes and concomitant changes in food availability. These three primate species were studied over a four-year period for a total of 24 months in the field. Santa Rosa National Park is in an area that experiences a long severe dry season in which little if any rain falls and the majority of the non-riparian trees lose their leaves. However, even though the three species were very flexible in terms of diet and range use, the behavioural variability did not correspond to changes in food availability or season.     

A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity

Most New World monkey species have both dichromatic and trichromatic individuals present in the same population. The selective forces acting to maintain the variation are hotly debated and are relevant to the evolution of the ‘routine’ trichromatic colour vision found in catarrhine primates. While trichromats have a foraging advantage for red food compared with dichromats, visual tasks which dichromats perform better have received less attention. Here we examine the effects of light intensity on foraging success among marmosets. We find that dichromats outperform trichomats when foraging in shade, but not in sun. The simplest explanation is that dichromats pay more attention to achromatic cues than trichromats. However, dichromats did not show a preference for foraging in shade compared with trichromats. Our results reveal several interesting parallels with a recent study in capuchin monkeys (Cebus capucinus), and suggest that dichromat advantage for certain tasks contributes to maintenance of the colour vision polymorphism.     

Locomotor and postural behavior in Alouatta palliata and Cebus capucinus

Positional behavior of two platyrrhine monkeys, Alouatta palliata and Cebus capucinus, was observed at La Pacifica and Santa Rosa National Park, Costa Rica. Frequency data for locomotion, postures, support diameters, orientation of supports, and use of canopy were recorded on focal males and females. Alouatta palliata is a frequent user of arboreal quadrupedalism (47%) and climbing (37%), with bridging (10%) representing the next most frequent type of locomotion. Intraspecific comparisons show the smaller-sized females of Alouatta to prefer very small diameter supports, the lower canopy, and to climb more frequently than the larger males—a pattern opposite to that which has been documented to occur with increasing body size across species. A more limited study on Cebus capucinus shows this species to be highly quadrupedal (54%) with moderately high locomotor frequencies for climbing (26%) and leaping (15%).     

Fig Foraging by Dichromatic and Trichromatic <Emphasis Type="Italic">Cebus capucinus</Emphasis> in a Tropical Dry Forest

Figs are important resources for frugivores, and Ficus is an ideal taxon for evaluating patterns of primate foraging related to food color. Ficus spp. can be classified as conspicuous (color change from greenish to reddish during ripening) or cryptic (green throughout ripening). To investigate the effect on foraging of color vision phenotype variation for these 2 types of figs, we conducted a 20-mo study on 4 groups of white-faced capuchins (Cebus capucinus) in the Santa Rosa Sector of the ACG, Costa Rica between May 2004 and September 2008. We genotyped all individuals and collected behavioral data on feeding rates, acceptance indices, and foraging sequences. We found a significant effect of fig type; feeding rates and acceptance indices were higher for conspicuous figs than for cryptic figs, and subjects sniffed cryptic figs more often than conspicuous figs. We also found that dichromats sniffed more figs and had longer foraging sequences than trichromats, especially for cryptic figs. Among 6 subtypes of dichromats and trichromats, monkeys possessing the trichromat phenotype with the most spectrally separated L-M opsin alleles showed the highest acceptance index for conspicuous figs, though there were no differences in feeding rates among phenotypes. We conclude: 1) conspicuous figs are visually salient not only for trichromats but also for dichromats, 2) olfaction is important for evaluating edibility of cryptic figs, and 3) the reliance on olfaction for selecting fruit is greater in dichromats. These results indicate divergent foraging strategies among color vision phenotypes for assessing food items.     

Interaction Between Capuchins and Coatis: Nonagonistic Behaviors and Lack of Predation

We compare the nature of capuchin-coati interactions by Cebus apella in 2 populations under semifree-ranging and wild conditions. We report a similar pattern of interaction at both sites, in spite of their ecological differences. Most frequent capuchin behaviors toward coatis were agonistic, but we noted no predation. Contrarily, the monkeys also exhibited nonagonistic behaviors, such as play and grooming. As tufted capuchins predate other mammalian species, and as the subjects were aggressive towards competitor species, showing their belligerent temperament, we believe the lack of predation can be attributed to 2 different ecological contigencies – the absence of coati pups in a period of food shortage, and the cost of dealing with a dangerous adult coati where other rich resources were available–and also, perhaps, to different traditions in capuchin behavior towards coatis, established via intraspecific social learning.     

Foraging Behavior in Two Species of Ectatomma (Formicidae: Ponerinae): Individual Learning of Orientation and Timing

The foraging behavior of marked individuals of Ectatomma ruidum and E. tuberculatum (Formicidae: Ponerinae) was observed on Barro Colorado Island, Panama, in order to determine whether learning of orientation and timing is involved when foraging on patchy resources on the forest floor. Foraging experiments under seminatural conditions were designed to control for the spatiotemporal distribution of resources at one or two preying sites. Using both single- and multi–event past experience, individual foragers of E. ruidum and (although less significantly) E. tuberculatum made directional and temporal adjustments to their behavior in response to previous differential foraging success. In spite of considerable individual variation in foraging efficiency, it is hypothesized that the observed differences in cognitive abilities can be invoked to explain ecological differences among both species.     

Life history and locomotion in Cebus capucinus and Alouatta palliata

As an individual matures from birth to adulthood, many factors may influence the positional repertoire. The biological and behavioral changes that accompany a growing individual are expected to influence foraging strategy, social status and interaction, diet, predator avoidance strategies, and ultimately positional behavior as a behavioral link between anatomy and the environment. In this work, positional behavior is considered as an important feature of life history in juvenile and adult white‐faced capuchins (Cebus capucinus) and mantled howling monkeys (Alouatta palliata) inhabiting the same tropical forest in Costa Rica. During growth and development ontogenetic changes in body size, limb proportions, and motor skills are likely to influence locomotion and posture through the arboreal canopy. I collected data on positional behavior, activity, branch size, branch angle, and crown location during a 12‐month period at Estación Biológica La Suerte in northeastern Costa Rica. Life history timing and differences in rates of growth did not predictably influence the development of adultlike positional behaviors in Cebus and Alouatta. Young Cebus resembled the adult pattern of positional behavior by 6 months of age while howlers exhibited significant differences in several positional behavior categories through 24 months of age. The positional repertoire of both species revealed similarities in the types of modes used during feed/forage and travel in juveniles and adults. Data presented here suggest that the environment exerts different pressures on growing Cebus and Alouatta that may relate to diet, energy expenditure, foraging skill, and/or social learning. Am J Phys Anthropol, 2009 © 2009 Wiley‐Liss, Inc.     

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.     

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.     

The Behavioral Ecology of Color Vision: Considering Fruit Conspicuity,Detection Distance and Dietary Importance

Primate color vision is well suited for investigating the genetic basis of foraging behavior owing to a clear genotype–phenotype linkage. Finding fruits amid tropical foliage has long been proffered as an adaptive explanation for primate trichromacy, yet there is a dearth of systematic evaluations of frugivory as an ecological selective force. We studied the behavioral ecology of wild capuchins (Cebus capucinus) in northwestern Costa Rica across the annual cycle and modeled the ability of three dichromatic and three trichromatic phenotypes to discriminate fruits from leaves, a task that represents long-distance search for food patches in a tropical forest. Models of the trichromatic phenotypes could correctly discriminate approximately three-quarters of the total capuchin dietary fruits from leaves, including some fruits subjectively classified as having “cryptic” (greenish-brownish) hues. In contrast, models of dichromatic phenotypes could discriminate fewer than one-third of the fruits. This pattern held when we restricted our analysis to only the most heavily consumed diet items, preferred foods, or seasonally critical species. We in addition highlight the potential of fruit species with small patch sizes to confer an advantage to trichromats, as these resources are anticipated to provide a high finder’s reward. Our results are consistent with the hypothesis that long-distance detection of fruit patches exerts a selective pressure on trichromacy in neotropical primates, and suggest that greenish-brownish fruits might have played an underappreciated role in the evolution of primate color vision.     

The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern?

The peak echolocation frequency of insectivorous bats generally declines as body size increases. However, there are notable exceptions to this rule, with some species, such as Rhinolophus clivosus, having a higher than expected peak frequency for their body size. Such deviations from allometry may be associated with partitioning of foraging habitat (the foraging habitat hypothesis) or insect prey (the prey detection hypothesis). Alternatively, the deviations may be associated with the partitioning of sonar frequency bands to allow effective communication in a social context (the acoustic communication hypothesis). We tested the predictions of these hypotheses through comparisons at the family, clade and species level, using species of rhinolophids in general and R. clivosus, a species with a wide distribution, as a specific test case. We compared the wing parameters, echolocation frequency and ecology of R. clivosus to those of the sympatric R. capensis. Rhinolophus clivosus has a much higher echolocation frequency than predicted from its wing loading or body mass. Furthermore, contrary to the predictions of the foraging habitat hypothesis, we found no difference in foraging habitat between R. clivosus and R. capensis. The size range of insect prey taken by the two species also overlapped almost completely, contrary to the prey detection hypothesis. On the other hand, the variation of echolocation frequencies around the allometric relationship for rhinolophids was smaller than that for Myotis spp., supporting the prediction of the acoustic communication hypothesis. We thus propose that the relatively high peak frequency of R. clivosus is the result of partitioning of sonar frequency bands to minimize the ambiguity of echolocation calls during social interactions.