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.     

Craniodental biomechanics and dietary toughness in the genus Cebus

The tufted capuchin (Cebus apella) has been used in a number of comparative studies to represent a primate with craniofacial morphology indicative of hard-object feeding. Researchers have specifically referred to the tufted capuchin as a seed predator. Craniofacial features exhibited by the tufted capuchin, such as thick cortical bone in the mandibular corpus and symphysis, and a broad face associated with large masticatory muscles, permit the production and dissipation of relatively high masticatory forces. These morphologies, however, cannot distinguish between the tufted capuchin's propensity to exert higher forces when opening food with its anterior dentition or with its cheek teeth. It is also unclear whether these are adaptations for biting or chewing foods. This study uses a constrained lever model to compare the masticatory adaptations of C. apella to other cebids and atelids. Results show that the temporalis and masseter muscles in C. apella and C. olivaceus are more anteriorly positioned relative to nine other platyrrhine taxa. This condition, which appears to be ancestral among the Cebinae, increases force production at the incisors and canines while compromising third molar function. Cebus apella, has exaggerated this pattern. Field data on dietary toughness show that both capuchins typically select foods of low toughness, but on occasion, C. apella ingests food items of exceptional toughness. Thus, C. apella appears to maintain these biomechanical relationships by producing particularly high but relatively infrequent bite forces, particularly at the incisors and canines. However, adaptations for anterior dental use do not tightly constrain the diet of Cebus apella. This approach can be used to clarify the dietary adaptations of fossil taxa.     

Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape

Tufted capuchins (sensu lato) are renowned for their dietary flexibility and capacity to exploit hard and tough objects. Cebus apella differs from other capuchins in displaying a suite of craniodental features that have been functionally and adaptively linked to their feeding behavior, particularly the generation and dissipation of relatively large jaw forces. We compared fiber architecture of the masseter and temporalis muscles between C. apella (n = 12) and two “untufted” capuchins (C. capucinus, n = 3; C. albifrons, n = 5). These three species share broadly similar diets, but tufted capuchins occasionally exploit mechanically challenging tissues. We tested the hypothesis that tufted capuchins exhibit architectural properties of their jaw muscles that facilitate relatively large forces including relatively greater physiologic cross-sectional areas (PCSA), more pinnate fibers, and lower ratios of mass to tetanic tension (Mass/P₀). Results show some evidence supporting these predictions, as C. apella has relatively greater superficial masseter and temporalis PCSAs, significantly so only for the temporalis following Bonferroni adjustment. Capuchins did not differ in pinnation angle or Mass/P₀. As an architectural trade-off between maximizing muscle force and muscle excursion/contraction velocity, we also tested the hypothesis that C. apella exhibits relatively shorter muscle fibers. Contrary to our prediction, there are no significant differences in relative fiber lengths between tufted and untufted capuchins. Therefore, we attribute the relatively greater PCSAs in tufted capuchins primarily to their larger muscle masses. These findings suggest that relatively large jaw-muscle PCSAs can be added to the suite of masticatory features that have been functionally linked to the exploitation of a more resistant diet by C. apella. By enlarging jaw-muscle mass to increase PCSA, rather than reducing fiber lengths and increasing pinnation, tufted capuchins appear to have increased jaw-muscle and bite forces without markedly compromising muscle excursion and contraction velocity. One performance advantage of this morphology is that it promotes relatively large bite forces at wide jaw gapes, which may be useful for processing large food items along the posterior dentition. We further hypothesize that this morphological pattern may have the ecological benefit of facilitating the dietary diversity seen in tufted capuchins. Lastly, the observed feeding on large objects, coupled with a jaw-muscle architecture that facilitates this behavior, raises concerns about utilizing C. apella as an extant behavioral model for hominins that might have specialized on small objects in their diets.     

Analysis of the heterochromatin of <Emphasis Type="Italic">Cebus</Emphasis> (Primates,Platyrrhini) by micro-FISH and banding pattern comparisons

The karyotype of the neotropical primate genus Cebus (Platyrrhini: Cebidae), considered the most ancestral one, shows the greatest amount of heterochromatin described among Platyrrhini genera. Banding techniques and restriction enzyme digestion have previously revealed great variability of quantity and composition of heterochromatin in this genus. In this context, we use fluorescence in situ hybridization (FISH) to analyse this genomic region and discuss its possible role in the diversification of Cebus. We used a heterochromatin probe for chromosome 11 of Cebus libidinosus (11qHe+ CLI probe), obtained by chromosome microdissection. Twenty-six specimens belonging to the families Atelidae, Cebidae, Callitrichidae and Pithecidae (Platyrrhini) were studied. Fourteen out of 26 specimens were Cebus (Cebidae) individuals of C. libidinosus, C. xanthosternos, C. apella, C. nigritus, C. albifrons, C. kaapori and C. olivaceus. In Cebus specimens, we found 6 to 22 positive signals located in interstitial and telomeric positions along the different species. No hybridization signal was observed among the remaining Ceboidea species, thus reinforcing the idea of a Cebus-specific heterochromatin composed of a complex system of repetitive sequences.     

Milk composition of captive tufted capuchins (Cebus apella)

Little is known about the milk composition of nonhuman primates, and it has never been examined in capuchin monkeys (genus Cebus). This article reports on the macronutrient milk composition (fat, crude protein (CP), lactose, dry matter (DM), and total gross energy (GE)) of captive housed tufted capuchins (Cebus apella) (n=8). C. apella milk averaged 5.22% fat, 2.40% CP, 6.94% lactose, 16.48% DM, and 0.89 kcal/g. Fat was the most variable macronutrient and was significantly higher in samples collected after 2 months of lactation. To explore the adaptive significance of C. apella milk composition, results were compared with data on milk composition from a closely related cebid, Saimiri boliviensis boliviensis, and another large‐brained anthropoid, Homo sapiens. C. apella milk was only significantly different from Saimiri milk in CP and the proportion of energy from CP. Compared with human milk, C. apella milk was lower in lactose but higher in fat, CP, DM, GE, and the proportion of energy from CP. Results from this small dataset suggest that among anthropoid primates, the macronutrient composition of milk is influenced by phylogeny, may vary relative to infant growth rates, but may not be related in any direct way to relative brain size. Am. J. Primatol. 72:81–86, 2010. © 2009 Wiley‐Liss, Inc.     

Competition and Facilitation in the Capuchin–Squirrel Monkey Relationship

In Guyana, the range of the brown capuchin, Cebus apella, meets the range of its congener, the wedge‐capped capuchin, C. olivaceus, with the two species exhibiting a mutually exclusive patchy distribution. Squirrel monkeys, Saimiri sciureus, and C. apella form ubiquitous interspecific associations, but the reason remains debatable. With a large biogeographic field study, we tested the degree to which the distribution and abundance of Cebus and S. sciureus is determined by habitat type, fruit availability, and geography (i.e., determinants of the fundamental niche) relative to interspecific interactions, such as competition and facilitation (i.e., the realized niche). We used the competition between the two capuchin monkeys as a natural experiment that subjected S. sciureus to C. apella and C. olivaceus ‘treatments’. Using spatial regression models and principal components analysis, we found that S. sciureus was associated with seasonally flooded forests, and was correlated with fruit abundance and diversity (fundamental niche), but was also correlated with C. apella density even when accounting for habitat and fruit availability (realized niche). Saimiri sciureus density was unrelated to C. olivaceus density. Cebus apella was associated with a variety of forest types, but particularly included disturbed and edge habitats such as logged forests, seasonally flooded forests, and upland savanna, in addition to mature forest. Cebus apella was also positively correlated with S. sciureus density and negatively correlated with the density of C. olivaceus. In contrast, C. olivaceus avoided riparian areas and was associated with mixed‐height forests on sloped mountainous terrain. In sum, interspecific interactions such as competition between species of Cebus and facilitation between C. apella and S. sciureus were as important as habitat and fruit availability in determining the distribution and abundance of these primates.     

Degrees of sexual dimorphism in Cebus and other new world monkeys

Sexual dimorphism in primate species expresses the effects of phylogeny, life history, behavior, and ontogeny. The causes and implications of sexual dimorphism have been studied in several different primates using a variety of morphological databases such as body weight, canine length, and coat color and ornamentation. In addition to these different patterns of dimorphism, the degree to which a species is dimorphic results from a variety of possible causes. In this study we test the general hypothesis that a species highly dimorphic for one size-based index of dimorphism will be equally dimorphic (relative to other species) for other size-based indices. Specifically, the degree and pattern of sexual dimorphism in Cebus and several other New World monkey species is measured using craniometric data as a substitute for the troublesome range of variation in body weight estimates. In general, the rank ordering of species for dimorphism ratios differs considerably across neural vs. non-neural functional domains of the cranium. The relative degree of sexual dimorphism in different functional regions of the cranium is affected by the independent action of natural selection on those regions. Regions of the cranium upon which natural selection is presumed to have acted within a species show greater degrees of dimorphism than do the same regions in closely related taxa. Within Cebus, C. apella is consistently more dimorphic than other Cebus species for facial measurements, but not for neural or body weight measurements. The pattern in C. apella indicates no single best measurement of the degree of dimorphism in a species; rather, the relative degree of dimorphism applies only to the region being measured and may be enhanced by other selective pressures on morphology. Am J Phys Anthropol 107:243–256, 1998. © 1998 Wiley-Liss, Inc.     

Social behavior of the wild black-capped Capuchin (Cebus apella)

The author undertook a field survey of the capuchin (Cebus apella) lasting 60 days from December 1976 to January 1977, and determined the basic daily activity of its groups and spacing of group members in the day time. Furthermore, based on studies of various types of interactions between individuals of the groups, he was able to show that (1) decisive rank orders exist both among adults and among sub-adults of both sexes; (2) grooming at the resting time is peculiar to adult males; (3) with quite mild agonistic interactions being maintained, a high tolerance exists between the group members; (4) alpha males represent individuals which can be called leaders of groups; and (5) a strong psychological or spiritual bond exists among the adult males, which can be termed a “male-bond.” Furthermore, according to comparative studies on some adjoining groups, it was found that the group structure is strongly influenced by the individuality or character of the adult males of each group. The present findings are generally in agreement with those forC. apella studied by the author and other researchers in other localities. It can be safely said therefore that these findings are probably common to this species of monkey. Based on a comparison with findings for three other species ofCebus, the author attempts to clarify the points of difference betweenC. apella and these three other species ofCebus from the viewpoint of behavioral science and sociology.     

A comparative study of the recombination pattern in three species of Platyrrhini monkeys (primates)

Homologous chromosomes exchange genetic information through recombination during meiotic synapsis, a process that increases genetic diversity and is fundamental to sexual reproduction. Meiotic studies in mammalian species are scarce and mainly focused on human and mouse. Here, the meiotic recombination events were determined in three species of Platyrrhini monkeys (Cebus libidinosus, Cebus nigritus and Alouatta caraya) by analysing the distribution of MLH1 foci at the stage of pachytene. Moreover, the combination of immunofluorescence and fluorescent in situ hybridisation has enabled us to construct recombination maps of primate chromosomes that are homologous to human chromosomes 13 and 21. Our results show that (a) the overall number of MLH1 foci varies among all three species, (b) the presence of heterochromatin blocks does not have a major influence on the distribution of MLH1 foci and (c) the distribution of crossovers in the homologous chromosomes to human chromosomes 13 and 21 are conserved between species of the same genus (C. libidinosus and C. nigritus) but are significantly different between Cebus and Alouatta. This heterogeneity in recombination behaviour among Ceboidea species may reflect differences in genetic diversity and genome composition.     

Response Toward Novel Foods and Novel Objects in Wild Cebus apella

Animals respond to novel stimuli via explorative or neophobic behavior or both. The coexistence of these responses toward novel foods may be a successful adaptive strategy for a generalist species such as Cebus apella, because it allows the gradual introduction of new foods into the diet and reduces the risk of poisoning by ingestion of large amounts of toxic compounds (Glander, 1982; Milton, 1993; Visalberghi, 1994). Neophobia has been studied mostly in captivity. We investigated responsiveness to novelty in a group of 25–30 wild tufted capuchins (Cebus apella) in Iguazü National Park (Argentina). They had been habituated to visiting sites where bananas were provided on three elevated platforms. We presented novel stimuli on an adjacent platform. There were 4 experimental conditions with 10 sessions each: the Novel Food condition, the Novel Object condition, the Control condition, in which the platform was empty, and the Banana condition. In the Novel Food and Novel Object conditions, a new stimulus—food or object—was on the platform during each session. The Banana condition provided information on capuchin response to a familiar preferred food. Overall, capuchins were less responsive toward novel objects than toward novel foods; however, although cautious, they ate small amounts of the novel foods. Age affected individual responsiveness toward novel foods, whereas sex affected responsiveness toward novel objects. Capuchins ignored the empty platform. Our findings are in agreement with the idea that tufted capuchins can adapt to new habitats by gradually exploiting new food sources.     

Intra and Interspecific Variation in Cranial Morphology on the Southernmost Distributed Cebus (Platyrrhini,Primates) Species

Capuchin monkeys (Cebus) are one of the genera with the widest distribution among Neotropical primates (New World Monkeys, Platyrrhini), accompanied by an elevated genetic, phenotypic, behavioral, morphological, and ecological diversity, both at the interspecific and population levels. Despite being one of the most studied primate genera, this high diversity has led to a particularly complex and controversial taxonomy. In this contribution, we explored the patterns of skull size and shape variation among the southernmost distributed populations of Cebus using three-dimensional geometric morphometric techniques. Results showed a marked morphological differentiation (in size and shape) between previously recognized species (C. nigritus and southern C. libidinosus), and also among C. libidinosus populations, which were quantitatively related with the geographic distance between them. This pattern supports a differentiation between the northwestern Argentina and southern Bolivia and Paraguay forms. Other taxonomic implications are also discussed.     

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).     

Postnatal growth allometry of the extremities in Cebus albifrons and Cebus apella: A longitudinal and comparative study

Cebus albifrons and Cebus apella, partially sympatric capuchin monkeys from South America, are known to differ substantially in adult body mass and bodily proportions. C. apella possesses a robust, stocky build in contrast to the more gracile, relatively longer limbed body design of C. albifrons. Average birth weights and adult body lengths of these two congeners, however, are remarkably similar and do not serve to distinguish them. This study examines longitudinal growth rates and patterns of ontogenetic scaling in the extremities (humerus, radius, hand, femur, tibia, foot) in order to document the nature and magnitude of skeletal changes associated with increasing age and body mass. Our data indicate that the growth rates of the six skeletal components of the limbs differ only slightly and somewhat inconsistently between the two species. Body mass, however, increases at a consistently faster rate in C. apella. Relative to body mass, therefore, the extremities of C. albifrons scale much faster than those of C. apella. This implies that at any given postnatal body mass, C. albifrons is longer limbed than C. apella. Conversely, C. apella is heavier than C. albifrons at any given limb length or age. We suggest that such differences in body mass distribution are causally related to differences in locomotor behavior and foraging strategies. Specifically, the relatively long-limbed C. albifrons is probably more cursorial and tends to travel longer distances each day than C. apella. C. apella is a much more deliberate quadruped and is also characterized by especially vigorous and powerful foraging and feeding behaviors. We also compare our results to other (mostly cross-sectional) studies of skeletal growth allometry in nonhuman primates.     

Experimental perspective on fallback foods and dietary adaptations in early hominins

The robust jaws and large, thick-enameled molars of the Plio–Pleistocene hominins Australopithecus and Paranthropus have long been interpreted as adaptations for hard-object feeding. Recent studies of dental microwear indicate that only Paranthropus robustus regularly ate hard items, suggesting that the dentognathic anatomy of other australopiths reflects rare, seasonal exploitation of hard fallback foods. Here, we show that hard-object feeding cannot explain the extreme morphology of Paranthropus boisei. Rather, analysis of long-term dietary plasticity in an animal model suggests year-round reliance on tough foods requiring prolonged postcanine processing in P. boisei. Increased consumption of such items may have marked the earlier transition from Ardipithecus to Australopithecus, with routine hard-object feeding in P. robustus representing a novel behaviour.     

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.     

On the occurrence of Cebus flavius (Schreber 1774) in the Caatinga, and the use of semi-arid environments by Cebus species in the Brazilian state of Rio Grande do Norte

Cebus flavius is a recently rediscovered species and a candidate for the 25 most endangered primate species list. It was hypothesized that the distribution of C. flavius was limited to the Atlantic Forest, while the occurrence of C. libidinosus in the Rio Grande do Norte (RN) Caatinga was inferred, given its occurrence in neighboring states. As a result of a survey in ten areas of the RN Caatinga, this paper reports on four Cebus populations, including the first occurrence of C. flavius in the Caatinga, and an expansion of the northwestern limits of distribution for the species. This C. flavius population may be a rare example of a process of geographic distribution retraction, and is probably the most endangered population of this species. New areas of occurrence of C. libidinosus are also described. Tool use sites were observed in association with reports of the presence of both capuchin species.     

Skeletal evidence for precision gripping inCebus apella

We compared the thumb morphology ofCebus apella to that of several other primate species in order to determine whether robust thumbs are associated with tool-use. We found that thumb robusticity was greater forCebus apella than for all other represented nonhuman species exceptGorilla gorilla. Further, thumb robusticity inCebus apella was similar to that ofAustralopithecus afarensis but lesser than that of other represented hominids, including modern humans. We propose that precision gripping similar to that which occurs in tool-using context amongCebus probably occurred among Australopithecines prior to the emergence of sophisticated tool behavior amongHomo andParanthropus.     

Differential habitat use byCebus apella andSaimiri sciureus in central surinam

Cebus apella, the black-capped or tufted capuchin, andSaimiri sciureus, the squirrel monkey, are frequently found in mixed species feeding and foraging groups throughout tropical South America and have been reported previously to show marked differences in techniques of insect foraging. Individuals of these taxa observed in central Surinam show numerous additional species-specific differences in other aspects of habitat utilization including gross dietary preferences, utilization of forest strata, locomotor behavior and arboreal support preferences.Cebus apella is more frugivorous, frequents the middle and lower levels of the main canopy, is predominantly quadrupedal and moves on medium-sized arboreal supports. By contrast, the smallerSaimiri sciureus is more insectivorous, frequents the lower strata of the forest, is more saltatory and moves on the smallest arboreal supports. Many of these differences in habitat use are interrelated and accord with patterns of habitat use seen in other primate taxa. The differences betweenCebus apella andSaimiri sciureus also accord with the types of behavioral differences frequently associated with differences in body size.     

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.