Adopting the approach taken with New Caledonian crows (Corvus moneduloides), we present evidence of design complexity in one of the termite-fishing tools of chimpanzees (Pan troglodytes) in the Goualougo Triangle, Republic of Congo. Prior to termite fishing, chimpanzees applied a set of deliberate, distinguishable actions to modify herb stems to fashion a brush-tipped probe, which is different from the form of fishing tools used by chimpanzees in East and West Africa. This means that ‘brush-tipped fishing probes’, unlike ‘brush sticks’, are not a by-product of use but a deliberate design feature absent in other chimpanzee populations. The specialized modifications to prepare the tool for termite fishing, measures taken to repair non-functional brushes and appropriate orientation of the modified end suggest that these wild chimpanzees are attentive to tool modifications. We also conducted experimental trials that showed that a brush-tipped probe is more effective in gathering insects than an unmodified fishing probe. Based on these findings, we suggest that chimpanzees in the Congo Basin have developed an improved fishing probe design.
tool use; tool modification; cognitive template
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.
capuchins; social traditions; social conventions; Cebus; social learning
Decades of research have revealed rich cultural repertoires encompassing multiple traditions in wild great apes, a picture crucially complemented by experimental simulations with captive apes. Studies with wild capuchin monkeys, the most encephalized simian species, have indicated a New World convergence on these cultural phenomena, involving multiple traditions and tool use. However, experimental studies to date are in conflict with such findings in concluding that capuchins, like other monkeys, show minimal capacities for social learning.
Here we report a new experimental approach in which the alpha male of each of two groups of capuchins was trained to open an artificial foraging device in a quite different way, using either a slide or lift action, then reunited with his group. In each group a majority of monkeys, 8 of 11 and 13 of 14, subsequently mastered the task. Seventeen of the successful 21 monkeys discovered the alternative action to that seeded in the group, performing it a median of 4 times. Nevertheless, all 21 primarily adopted the technique seeded by their group's alpha male. Median proportions of slide versus lift were 0.96 for the group seeded with slide versus 0. 01 for the group seeded with lift.
These results suggest a striking effect of social conformity in learned behavioral techniques, consistent with field reports of capuchin traditions and convergent on the only other species in which such cultural phenomena have been reported, chimpanzees and humans.
This report addresses phylogenetic variation in a spatial skill that underlies tool use: aligning objects to a feature of a surface. Fragaszy and Cummins-Sebree’s  model of relational spatial reasoning and Skill Development and Perception-Action theories guided the design of the study. We examined how capuchins and chimpanzees place stick objects of varying shapes into matching grooves on a flat surface. Although most individuals aligned the long axis of the object with the matching groove more often than expected by chance, all typically did so with poor precision. Some individuals managed to align a second feature, and only one (a capuchin monkey) achieved above-chance success at aligning three features with matching grooves. Our findings suggest that capuchins and chimpanzees do not reliably align objects along even one axis, and that neither species can reliably or easily master object placement tasks that require managing two or more spatial relations concurrently. Moreover, they did not systematically vary their behavior in a manner that would aid discovery of the affordances of the stick-surface combination beyond sliding the stick along the surface (which may have provided haptic information about the location of the groove). These limitations have profound consequences for the forms of tool use we can expect these individuals to master.
Allocentric; Egocentric; spatial reasoning; object manipulation; alignment; tool use
Capuchin monkeys (Cebus apella) are New World primates with relatively large brains for their body size. The developmental trajectories of several brain regions – including cortical white matter, frontal lobe white matter, and basal ganglia nuclei – are similar to humans. Additionally, capuchins have independently evolved several behavioral and anatomical characteristics in common with humans and chimpanzees – including complex manipulative abilities, use of tools, and the use of precision grips – making them interesting species for studies of comparative brain morphology and organization. Here we report the first investigation into the development of the corpus callosum and its regional subdivisions in capuchins. Corpus callosum development was quantified using high-resolution structural MRI images from 39 socially reared subjects (male n = 22; female n = 18) ranging in age from 4 days (infancy) – 20 years (middle adulthood). The total area of the corpus callosum and the subdivisions of the genu, rostral midbody, medial midbody, caudal midbody, and splenium were traced from the midsagittal section. Total corpus callosum area displayed significant differences across this time span and was best explained by quadratic growth. Sustained linear growth was observed in the subdivisions of the genu, rostral midbody, and splenium; sustained quadratic growth was seen in the subdivision of the medial midbody. Differences in growth were not detected in the subdivision of the caudal midbody. Females had a larger raw area of the total CC and of the medial midbody and caudal midbody throughout the lifespan. Our results indicate that capuchins show continued white matter development beyond adolescence in regions related to cognitive and motor development.
brain development; Cebus; corpus callosum
Researchers of “culture” have long been interested in the role of social learning in establishing patterns of behavioral variation in wild animals, but very few studies examine this issue using a developmental approach. This 7-year study examines the acquisition of techniques used to process Luehea candida fruits in a wild population of white-faced capuchin monkeys, Cebus capucinus, residing in and near Lomas Barbudal Biological Reserve, Costa Rica. The two techniques for extracting seeds (pounding or scrubbing) were approximately equal in efficiency, and subjects experimented with both techniques before settling on one technique—typically the one they most frequently observed. In a sample of 106 subjects that had already settled on a preferred technique, the females adopted the maternal technique significantly more often than expected by chance, but the males did not. Using a longitudinal approach, I examined the acquisition of Luehea processing techniques during the first 5 years of life. Regression analysis revealed that the technique most frequently observed (measured as proportion of Luehea processing bouts observed that used pounding as opposed to scrubbing) significantly predicted the technique adopted by female observers, particularly in the second year of life; the amount of impact of the observed technique on the practiced technique was somewhat less significant for male observers. These results held true for (a) observations of maternal technique only, (b) observations of technique used by all individuals other than the mother, and (c) observations of maternal and non-maternal techniques combined.
Electronic supplementary material
The online version of this article (doi:10.1007/s10071-009-0230-3) contains supplementary material, which is available to authorized users.
Social influence; Cebus capucinus; Food processing; Capuchins; Development
Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (ΦST = 0.49, ΦCT = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes.
The use of ‘tactical deception’ is argued to have been important in the cognitive evolution of the order Primates, but systematic studies of active deception in wild non-human primates are scant. This study tests whether wild tufted capuchin monkeys (Cebus apella nigritus) use alarm calls in a functionally deceptive manner to usurp food resources. If capuchins use alarm calls ‘deceptively’, it was predicted that false alarms should be: (i) given by subordinates more than by dominants, (ii) more frequent when food is most contestable, (iii) more frequent when less food is available, and (iv) given when the caller is in a spatial position in which it could increase its feeding success if conspecifics react to the call. These predictions were tested by observing subjects in experimental contexts, in which the amount and distribution of a high-value resource (banana pieces) were manipulated using wooden platforms suspended from tree branches. While false alarms were non-significantly more common when more food was available, the three remaining predictions were supported. These results generally support the hypothesis that alarm calls are used by capuchins to reduce the effects of feeding competition. Whether this is intentional on the part of the caller requires further investigation.
alarm calls; feeding competition; deception; communication; primates; Cebus apella nigritus
It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among ‘generations’ of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.
social learning; tradition; culture; primates; diffusion chains; Cebus apella
Earthworms, termites, and ants are common macroinvertebrates in terrestrial environments, although for most ecosystems data on their abundance and biomass is sparse. Quantifying their areal abundance is a critical first step in understanding their functional importance. We intensively sampled dead wood, litter, and soil in eastern US temperate hardwood forests at four sites, which span much of the latitudinal range of this ecosystem, to estimate the abundance and biomass m−2 of individuals in macroinvertebrate communities. Macroinvertebrates, other than ants and termites, differed only slightly among sites in total abundance and biomass and they were similar in ordinal composition. Termites and ants were the most abundant macroinvertebrates in dead wood, and ants were the most abundant in litter and soil. Ant abundance and biomass m−2 in the southernmost site (Florida) were among the highest values recorded for ants in any ecosystem. Ant and termite biomass and abundance varied greatly across the range, from <1% of the total macroinvertebrate abundance (in the northern sites) to >95% in the southern sites. Our data reveal a pronounced shift to eusocial insect dominance with decreasing latitude in a temperate ecosystem. The extraordinarily high social insect relative abundance outside of the tropics lends support to existing data suggesting that ants, along with termites, are globally the most abundant soil macroinvertebrates, and surpass the majority of other terrestrial animal (vertebrate and invertebrate) groups in biomass m−2. Our results provide a foundation for improving our understanding of the functional role of social insects in regulating ecosystem processes in temperate forest.
A comparative study of chimpanzee (Pan troglodytes) and capuchin monkey (Cebus apella) cerebellar asymmetry and its relationship to handedness was conducted. Magnetic resonance images of the brain and behavioral data on a coordinated bimanual task were obtained from 16 chimpanzees and 11 capuchins. Chimpanzees displayed a greater rightward bias of the posterior cerebellum and capuchins displayed a greater leftward bias of the anterior cerebellum. Cerebellar asymmetries were significantly associated with handedness in capuchins but not chimpanzees, and this effect was most pronounced in right-handed capuchins.
Handedness; asymmetry; cerebellum; chimpanzees; capuchins
Cebus apella is renowned for its 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 the tufted capuchin (C. apella; n = 12 ) and two “untufted” capuchins (C. capuchinus, 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 C. apella exhibits 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, whole 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 C. apella 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 Cebus apella. 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.
Tufted capuchins; Feeding behavior; Masseter; Temporalis; Fiber length; PCSA; Early hominin diet
The basal ganglia are subcortical structures involved in the planning, initiation and regulation of movement as well as a variety of non-motor, cognitive and affective functions. Capuchin monkeys share several important characteristics of development with humans, including a prolonged infancy and juvenile period, a long lifespan, and complex manipulative abilities. This makes capuchins important comparative models for understanding age-related neuroanatomical changes in these structures. Here we report developmental volumetric data on the three subdivisions of the basal ganglia, the caudate, putamen and globus pallidus in brown capuchin monkeys (Cebus apella). Based on a cross-sectional sample, we describe brain development in 28 brown capuchin monkeys (male n = 17, female n = 11; age range = 2 months – 20 years) using high-resolution structural MRI. We found that the raw volumes of the putamen and caudate varied significantly with age, decreasing in volume from birth through early adulthood. Notably, developmental changes did not differ between sexes. Because these observed developmental patterns are similar to humans, our results suggest that capuchin monkeys may be useful animal models for investigating neurodevelopmental disorders of the basal ganglia.
brain development; basal ganglia; Cebus
Chimpanzee tool behaviours vary dramatically in their complexity and extent of geographical distribution. The use of tool sets with specific design features to gather termites extends across a large portion of central Africa. Detailed examination of the composition and uniformity of such complex tool tasks has the potential to advance our understanding of the cognitive capabilities of tool users and processes underlying the maintenance of technological skills. In this study, we examined variation in chimpanzee tool use in termite gathering from video-recorded sequences that were scored to the level of functionally distinct behavioural elements. Overall, we found a high degree of similarity in tool-using techniques exhibited by individuals in this population. The number of elements in each individual's repertoire often exceeded that necessary to accomplish the task, with consistent differences in repertoire sizes between age classes. Adults and subadults had the largest repertoires and more consistently exhibited element strings than younger individuals. Larger repertoires were typically associated with incorporation of rare variants, some of which indicate flexibility and intelligence. These tool using apes aid us in understanding the evolution of technology, including that of our human ancestors, which showed a high degree of uniformity over large spatial scales.
technology; Congo Basin; tool use
The present study describes the flexor and extensor muscles in Cebus libidinosus' forearm and compares them with those from humans, chimpanzees and baboons. The data is presented in quantitative anatomical indices for similarity. The capuchin forearm muscles showed important similarities with chimpanzees and humans, particularly those that act on thumb motion and allow certain degree of independence from other hand structures, even though their configuration does not enable a true opposable thumb. The characteristics of Cebus' forearm muscles corroborate the evolutionary convergence towards an adaptive behavior (tool use) between Cebus genus and apes.
There is continued debate over the factors influencing handedness in captive and wild primates, notably chimpanzees. Previous studies in wild chimpanzees have revealed population-level left handedness for termite fishing. Here we examined hand preferences and performance on a tool use task designed to simulate termite fishing in a sample of 190 captive chimpanzees to evaluate whether patterns of hand use in captive chimpanzees differed from those observed for wild apes. No population-level handedness was found for this task; however, significant sex differences in preference and performance were found, with males showing greater left handedness and poorer performance compared to females. We also found that the hand preferences of offspring were significantly positively correlated with the hand preferences of their mothers. Lastly, older females performed more slowly on the task compared to younger individuals. The overall results neither confirm nor reject previous hypotheses claiming that raising chimpanzees in captivity induces right-handedness, but rather suggest that other factors may account for differences in hand preferences for tool use seen in wild and captive chimpanzees.
chimpanzee; Pan troglodytes; handedness; sex differences; tool use
Termites constitute a considerable fraction of the animal biomass in tropical forest, but little quantitative data are available that indicates their importance in the processes of wood decomposition. This study evaluated the participation of Nasutitermes corniger (Motschulsky) (Isoptera: Termitidae), N. ephratae (Holmgren), and N. macrocephalus (Silvestri) in the consumption of the wood litter in a remnant area of Atlantic Coastal Forest in northeastern Brazil. The populations of this species were quantified in nests and in decomposing tree trunks, while the rate of wood consumption was determined in the laboratory using wood test-blocks of Clitoria fairchildiana Howard (Fabales: Fabaceae), Cecropia sp. (Urticales: Cecropiaceae), and Protium heptaphyllum (Aublet) Marchand (Sapindales: Burseraceae). The abundance of the three species of termites varied from 40.8 to 462.2 individuals/m2. The average dry wood consumption for the three species was 9.4 mg/g of termites (fresh weight)/day, with N. macrocephalus demonstrating the greatest consumption (12.1 mg/g of termite (fresh weight)/day). Wood consumption by the three species of Nasutitermes was estimated to be 66.9 kg of dry wood /ha/year, corresponding to approximately 2.9% of the annual production of wood-litter in the study area. This consumption, together with that of the other 18 exclusively wood-feeders termite species known to occur in the area, indicates the important participation of termites in removing wood-litter within the Atlantic Coastal Forest domain.
abundance; biomass; consumption rates; decomposition; Isoptera; Neotropical region
According to several lines of evidence, the great expansion observed in the primate prefrontal cortex (PfC) was accompanied by the emergence of new cortical areas during phylogenetic development. As a consequence, the structural heterogeneity noted in this region of the primate frontal lobe has been associated with diverse behavioral and cognitive functions described in human and non-human primates. A substantial part of this evidence was obtained using Old World monkeys as experimental model; while the PfC of New World monkeys has been poorly studied.
In this study, the architecture of the PfC in five capuchin monkeys (Cebus apella) was analyzed based on four different architectonic tools, Nissl and myelin staining, histochemistry using the lectin Wisteria floribunda agglutinin and immunohistochemistry using SMI-32 antibody.
Twenty-two architectonic areas in the Cebus PfC were distinguished: areas 8v, 8d, 9d, 12l, 45, 46v, 46d, 46vr and 46dr in the lateral PfC; areas 11l, 11m, 12o, 13l, 13m, 13i, 14r and 14c in the orbitofrontal cortex, with areas 14r and 14c occupying the ventromedial corner; areas 32r, 32c, 25 and 9m in the medial PfC, and area 10 in the frontal pole. This number is significantly higher than the four cytoarchitectonic areas previously recognized in the same species. However, the number and distribution of these areas in Cebus were to a large extent similar to those described in Old World monkeys PfC in more recent studies.
The present parcellation of the Cebus PfC considerably modifies the scheme initially proposed for this species but is in line with previous studies on Old World monkeys. Thus, it was observed that the remarkable anatomical similarity between the brains of genera Macaca and Cebus may extend to architectonic aspects. Since monkeys of both genera evolved independently over a long period of time facing different environmental pressures, the similarities in the architectonic maps of PfC in both genera are issues of interest. However, additional data about the connectivity and function of the Cebus PfC are necessary to evaluate the possibility of potential homologies or parallelisms.
Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.
The evolution of corpus callosum (CC) was integral to the development of higher cognitive processes and hemispheric specialization. An examination of CC morphology and organization across different primate species will further our understanding of the evolution of these specified functions. Using magnetic resonance imaging (MRI) as a non-invasive technique to measure CC size and to approximate the degree of myelination in the corpus callosum, we report differences in CC morphology and organization in capuchin monkeys and chimpanzees, two divergent primate species that have independently evolved several behavioral and anatomical characteristics. Species differences in CC morphology were detected, with chimpanzees having a larger overall CC compared to capuchin monkeys. Additionally, chimpanzees had the genu as the largest subdivision; in capuchin monkeys, the genu and splenium were the largest subdivisions. Sex differences in signal intensity were detected; capuchin monkey males had higher signal intensity values whereas chimpanzee females had higher signal intensity values. Thus, while capuchin monkeys and chimpanzees show some similarity in patterns of CC morphology, these species differ significantly in the regional organization of the CC.
corpus callosum morphology; corpus callosum organization; capuchin monkey; chimpanzee; magnetic resonance imaging; signal intensity
The study of social learning in captivity and behavioral traditions in the wild are two burgeoning areas of research, but few empirical studies have tested how learning mechanisms produce emergent patterns of tradition. Studies have examined how social learning mechanisms that are cognitively complex and possessed by few species, such as imitation, result in traditional patterns, yet traditional patterns are also exhibited by species that may not possess such mechanisms. We propose an explicit model of how stimulus enhancement and reinforcement learning could interact to produce traditions. We tested the model experimentally with tufted capuchin monkeys (Cebus apella), which exhibit traditions in the wild but have rarely demonstrated imitative abilities in captive experiments. Monkeys showed both stimulus enhancement learning and a habitual bias to perform whichever behavior first obtained them a reward. These results support our model that simple social learning mechanisms combined with reinforcement can result in traditional patterns of behavior.
social learning; tradition; reinforcement; object manipulation; Cebus
Cerebral asymmetries are thought to be associated with increased hemispheric specialization of function. We investigated cerebral petalias, the protrusion of one cerebral hemisphere relative to the other, and their relationship to lateralized behavior in capuchin monkeys (Cebus apella). Magnetic resonance images of the brain and behavioral data on a coordinated bimanual task were obtained from 13 capuchins. While a significant population-level left-frontal petalia was found, this was not related to handedness. The role of the morphologically asymmetric frontal cortex in capuchins is unclear, but may reflect developmental gradients or directional selection for various behavioral functions, such as extractive foraging or social group complexity.
Handedness; lateralized behavior; petalias; Cebus
Relative to other primates, Cebus monkeys display unusually fast postnatal brain growth and motor skill development. The neonatal capuchin brain, at approximately 29–34 g, is a smaller proportion of the adult brain weight (c. 50%) than is the brain of other primates except humans and great apes. Here we describe, from a cross-sectional sample, brain development in 29 brown capuchin monkeys (Cebus apella) using high-resolution structural magnetic resonance images, focusing on growth patterns in total brain volume, cortical gray and white matter volume, frontal lobe gray and white matter volume, and corpus callosum area. Non-linear age-related changes in total brain volume, cortical white matter volume and frontal white matter volume were detected from birth – 5 years. Sex differences in corpus callosum:brain ratio were also found, with males having a 10% smaller corpus callosum:brain ratio than females regardless of age. Female corpus callosum:brain ratio showed significant age-related related changes, whereas males did not display any significant changes across age. Sex differences were also found in cortical gray and frontal lobe gray matter volumes, with males having larger volumes than females. These findings support the conclusion that capuchins undergo rapid neurological change during the first few years of life.
Two herpes-like viruses were isolated from capuchin monkey (Cebus apella) brain and (Cebus albifrons) spleen cell cultures, respectively. Both isolates induced similar cytopathic effects consisting of rounded and ballooned cells in the original monkey cell cultures and in a wide range of permissive cell types. Neutralizing antibody to each virus was present in serum from the capuchin monkey from which it was isolated, but the two viruses did not cross-react by neutralization. Fluorescein isothiocyanate conjugates of hyperimmune rabbit serum to one of the isolates showed an antigenic cross relationship between the two isolates. By electron microscopy, herpes-like virus particles were observed in the nucleus and cytoplasm of infected human diploid fibroblast cell cultures. Virus-infected cell cultures stained with acridine orange revealed small deoxyribonucleic acid-containing intranuclear inclusion bodies. Both viruses were inhibited by 5-fluorodeoxyuridine and inactivated by chloroform or exposure to 56 degrees C for 30 min. Antisera prepared against 16 prototype herpesviruses and cytomegaloviruses did not neutralize approximately 100 50% tissue culture infective doses of either capuchin isolate. Neutralizing antibody to the capuchin isolates was detected in sera from 8 of 17 capuchin monkeys but not in sera from 16 humans, 15 chimpanzees, and 10 spider, 6 rhesus, and 5 squirrel monkeys.
The insight that animals' cognitive abilities are linked to their evolutionary history, and hence their ecology, provides the framework for the comparative approach. Despite primates renowned dietary complexity and social cognition, including cooperative abilities, we here demonstrate that cleaner wrasse outperform three primate species, capuchin monkeys, chimpanzees and orang-utans, in a foraging task involving a choice between two actions, both of which yield identical immediate rewards, but only one of which yields an additional delayed reward. The foraging task decisions involve partner choice in cleaners: they must service visiting client reef fish before resident clients to access both; otherwise the former switch to a different cleaner. Wild caught adult, but not juvenile, cleaners learned to solve the task quickly and relearned the task when it was reversed. The majority of primates failed to perform above chance after 100 trials, which is in sharp contrast to previous studies showing that primates easily learn to choose an action that yields immediate double rewards compared to an alternative action. In conclusion, the adult cleaners' ability to choose a superior action with initially neutral consequences is likely due to repeated exposure in nature, which leads to specific learned optimal foraging decision rules.