Carrying, Sharing, and Hand Preference in Tufted Capuchins (Cebus apella)

We examined the relationship among carrying, food-sharing, and hand preference in tufted capuchins (Cebus apella). The rationale was to evaluate further the use of Cebus as an alternative primate model to Pan for behavior relevant to early hominid evolution. We first examined bipedalism and food-sharing within an established social group, and then examined the direction and strength of hand preference for food carrying in an expanded sample. Several aspects of capuchin behavior warrant discussion. First, bipedal carrying and food-sharing occurred more frequently when we provided bulky foods than when we provided smaller foods. Second, food-sharing was characterized by passive tolerance, rather than active giving, between subjects. Third, subjects shared food primarily with immatures and followed a pattern of reciprocal exchange. Finally, we found no evidence for population-level hand preference for carrying. We posit that an array of behavioral similarities among Cebus, Pan, and Homo evolved through convergent processes, and in this regard capuchins can be seen as an alternative primate model to chimpanzees for the evolution of early hominid behavior.     

Location-specific Responsiveness to Environmental Perturbations in Wedge-capped Capuchins (Cebus olivaceus)

We recorded the responses of the members of a captive group of wedge-capped capuchins to novel and familiar objects placed in different parts of their cage in a study of the spatial dependency of activity with objects. We focused on behavioral pattern variability across subjects and across object location. Results show that, according to the location of the object, a great deal of within-subject response variability exists. The dominant male was slow to interact physically with objects and presented social-like behaviors—essentially grooming—towards objects in only one site. Implicit to the ethological approach is the assumption that consistent spatial location is irrelevant or, at best, of little importance to the definition of stimuli. Nevertheless, stimuli would be best considered as perturbations insofar as the significance of an object or event depends on where and when it is encountered. In order to evaluate how monkey cognition operates, it seems essential to investigate the role of the primate's own spatial structure. As a working hypothesis, we introduce the processes of spatial facilitation and inhibition and suggest that they affect how an individual interacts with objects and events.     

Predictors of Parasitism in Wild White-Faced Capuchins (Cebus capucinus)

Parasite infections in wildlife are influenced by many factors including host demography, behavior and physiology, climate, habitat characteristics, and parasite biology and ecology. White-faced capuchins (Cebus capucinus) host a suite of gastrointestinal and pulmonary parasites, yet the mechanisms affecting host susceptibility and parasite transmissibility have not been examined in this host species. We used the information-theoretic approach (Akaike’s information criterion) and traditional null-hypothesis testing to determine which host characteristics, behaviors, or environmental factors affected the presence of two prevalent capuchin parasites (Filariopsis barretoi and Strongyloides sp.) as well as parasite species richness in four groups of wild capuchins from September 2007 to January 2008 and January to August 2009. Older capuchins were more likely to be infected with Filariopsis barretoi and had higher parasite species richness. Age-biased nematode infections may stem from age differences in capuchin behavior and physiology while high species richness likely results from long- term exposure to numerous parasite species. Infections with Strongyloides sp. were more likely to occur in the dry season when capuchins often descend to the forest floor to drink from terrestrial water sources, potentially increasing their risk of infection from soil-borne larvae. Capuchin behaviors were poor predictors of parasitism, as were female rank, host sex, home range size, and habitat quality. Many of our results were atypical for primate parasitology, suggesting that host–parasite interactions, and subsequently infection risk, may differ in highly seasonal habitats such as tropical dry forests where these monkeys occur.     

Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools

We conducted an exploratory investigation in an area where nut-cracking by wild capuchin monkeys is common knowledge among local residents. In addition to observing male and female capuchin monkeys using stones to pound open nuts on stone "anvils," we surveyed the surrounding area and found physical evidence that monkeys cracked nuts on rock outcrops, boulders, and logs (collectively termed anvils). Anvils, which were identified by numerous shallow depressions on the upper surface, the presence of palm shells and debris, and the presence of loose stones of an appropriate size to pound nuts, were present even on the tops of mesas. The stones used to crack nuts can weigh >1 kg, and are remarkably heavy for monkeys that weigh <4 kg. The abundance of shell remains and depressions in the anvil surface at numerous anvil sites indicate that nut-cracking activity is common and long-enduring. Many of the stones found on anvils (presumably used to pound nuts) are river pebbles that are not present in the local area we surveyed (except on or near the anvils); therefore, we surmise that they were transported to the anvil sites. Ecologically and behaviorally, nut-cracking by capuchins appears to have strong parallels to nut-cracking by wild chimpanzees. The presence of abundant anvil sites, limited alternative food resources, abundance of palms, and the habit of the palms in this region to produce fruit at ground level all likely contribute to the monkeys' routine exploitation of palm nuts via cracking them with stones. This discovery provides a new reference point for discussions regarding the evolution of tool use and material culture in primates. Routine tool use to exploit keystone food resources is not restricted to living great apes and ancestral hominids.     

Hand Preferences in Different Tasks by Tufted Capuchins (Cebus apella)

We examined hand preferences in 25 tufted capuchins (Cebus apella) in three tasks. The hole task involved a single action of reaching for food in a hole. The horizontal panel and the vertical panel tasks required the alignment of two apertures, by moving or lifting a panel, to reach for food in a hole. We found a significant group-level right-hand preference for reaching actions in the hole and in the horizontal panel tasks, but not in the vertical panel task, in which the food retrieval implied the complementary use of both hands. No significant hand bias emerged for moving or lifting actions with high visuospatial components. There is a stronger hand preference in more complex manual activity—coordinated bimanual hand use for food retrieval—than in other unimanual measures. We discuss the results in the context of previous reports on primate laterality.     

Factors Affecting Urine Washing Behavior in Tufted Capuchins (Cebus apella)

Urine washing is a common behavior in strepsirrhine and platyrrhine primates, but its function is still poorly understood. We investigated the factors influencing urine washing behavior in 2 captive groups of tufted capuchins (Cebus apella). Urine washing was affected by group membership (subjects in the 2 groups urine washed at different rates) and was negatively related to age, but was not influenced by sex or dominance rank. Females urine washed less when in estrus, and the presence of an estrous female did not affect male urine washing behavior. We observed independent effects of diurnal and climatic variables on urine washing. Tufted capuchins urine washed more at midday and under conditions of higher temperatures and lower relative humidity. Both of the latter effects were evident only at the lowest temperatures (5?C20°C). Our results indicate that urine washing is sensitive to multiple influences, and that hypothetical communicative or thermoregulatory functions do not fully account for its occurrence.     

Hand Preference in Free-Ranging White-Throated Capuchins (Cebus capucinus) in Costa Rica

I studied the hand preference patterns of individuals in three troops of white-throated capuchins (C. capucinus) in Palo Verde, Costa Rica, during 11 months from February 1995 to January 1996. I used focal and ad libitum sampling techniques and tested several frameworks that seek to explain and to predict primate hand use patterns via a variety of spontaneous tasks that differ in manipulative difficulty and required postural regulation: reach, tap, grab, carry, and object-use. The monkeys showed symmetrical hand use patterns for the easy tasks, reach and tap; strongly asymmetrical patterns for the highly manipulative task, object-use, at the individual level; and weak population-level biases for tasks requiring a degree of postural regulation, carry. The results for data on grab are inconclusive. These results do not support the available primate hand use frameworks and differ from most of the captive literature on hand preference in Cebus. The findings indicate that postural regulation may influence hand use patterns in nonhuman primates at the population level.     

Spontaneous tool use by wild capuchin monkeys (Cebus libidinosus) in the Cerrado

Among primates, only chimpanzees and orang-utans are credited with customary tool use in nature. Among monkeys, capuchins stand out with respect to the number of accounts of tool use. However, the majority of capuchin tool use observations reported in nature is anecdotal or idiosyncratic. In this report, we documented the stone pounding of dry fruits (Hymenea courbaril and Acrocomia aculeata) in two wild free-ranging groups of Cebus libidinosus in the Brasilia National Park, a preserved area representative of the Cerradobiome of Central Brazil. In 2004, we noted 2 episodes at which 4 monkeys used stones to crack open nuts. In 2005, we recorded 5 pounding episodes involving 2 different monkeys. Observations of tool use over the course of 2 consecutive years by some individuals, as well as other indirect evidence, indicate that this behaviour could be habitual in the studied groups. We propose that the probability of the emergence of the use of pounding stones as tools may be dependent on the ecological variables that influence the degree of terrestriality and extractive foraging and the complex interaction of these factors.     

Reproductive Socioecology of Tufted Capuchins (Cebus apella nigritus) in Northeastern Argentina

We describe the reproductive parameters of tufted capuchins (Cebus apella nigritus) in the Iguazú National Park, NE Argentina. We obtained data on six different groups (33 individually recognized adult females) studied for periods of 2–9 years. Estimated birthrate is 0.59 infants per female per year in unprovisioned groups. A group that was provisioned for 6 years during the winter period of low fruit availability (May–August), showed a similar birth rate of 0.61, but a lower infant mortality rate than unprovisioned groups. The birthrate estimated for this population is higher than the one reported for white-faced and wedge-capped capuchins. The mean interbirth interval is 19.35 months, but a female can have infants in successive years, even when her previous infant has survived. The modal age at first delivery is 7 years, which is similar to the one observed in wedge-capped capuchins. When young adult females come into estrous they avoid copulating with the alpha male that sired them, thus providing evidence for a behavioral mechanism of inbreeding avoidance. Births are very seasonal at Iguazú, occurring during the spring and summer months (October–February) when food availability is at its peak. Tufted capuchins at Iguazú are more seasonal breeders than other capuchin populations, probably as a result of their more seasonal environment. The secondary sex ratio does not deviate significantly from 1:1, despite the known ability of capuchins to adjust secondary sex ratio to local conditions.     

Semifree-ranging Tufted Capuchins (Cebus apella) Spontaneously Use Tools to Crack Open Nuts

Naturalistic studies on tool use by nonhuman primates have focused almost exclusively on Old World monkeys or hominoids. We studied the cracking of Syagrus nuts with the aid of stones by a group of semifree-ranging capuchins living in a reforested area (Tietê Ecological Park, São Paulo, Brazil). Our data are from direct observation and from mapping nut-cracking site utilization. All adults, subadults and juveniles (plus one infant) crack nuts, but individual differences in frequency and proficiency are marked. Juveniles do most of the nut-cracking, but adults are, on average, more efficient; the frequency of inept stone manipulation decreases with age. About 10% of the nut-cracking episodes were watched by other individuals—mostly infants and juveniles, suggesting a role for observational learning, even if restricted to stimulus enhancement.     

Spatial Facilitation in a Probing Task in Wedge-Capped Capuchins (Cebus olivaceus)

Activities ordinarily performed by an animal in a given place may influence the way it behaves towards an object newly found there. We examined the use of probing tools in a group of 4 wedge-capped capuchins (Cebus olivaceus), in the home cage into which we simultaneously introduced two identical apparatuses, one at a site ordinarily used to manipulate objects, and the other at a site mainly used for visual monitoring. We expected that spatial facilitation would occur, i.e., the subjects would be more efficient at the site where manipulative behaviors were more frequently performed. Two monkeys used probing tools to extract syrup from the openings of the apparatuses. Tool use efficiency was higher with the apparatus located at the site where they had performed more manipulative and combinative behaviors. These results are consistent with the hypothesis of spatial facilitation and illustrate the fact that spatial context can be an overwhelming variable that should not be neglected in behavioral research dealing with instrumental tasks.     

Methodological Considerations in the Analysis of Fecal Glucocorticoid Metabolites in Tufted Capuchins (Cebus apella)

Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC metabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing “field extracts” for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest.     

Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone,Dihydrotestosterone, and Glucocorticoids

Reproductive success is linked to dominance in male primates, reflecting the benefits of male competition. However, not all males compete successfully, suggesting that the costs of obtaining and maintaining high dominance status are significant. Here we examine the fecal metabolites of testosterone (fT) and dihydrotestosterone (fDHT) as bioactive androgens reflecting male reproductive effort, as well as fecal glucocorticoid (fGC) excretion as an index of stress in male white-faced capuchins (Cebus capucinus). We investigated the influence of female fertility (periovulatory vs. nonovulatory) on the hormonal responses of alpha and subordinate males. Over a 17-mo field season, we collected and analyzed weekly fecal samples (N = 992) from all 14 adult (> 10 yr) and subadult (≥ 6–10 yr) males residing in three study groups in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. Fecal samples (N > 2250) were also collected from group females (N = 28) to identify the fertile period using progesterone and estradiol assays. Alpha males had significantly higher fT, fDHT, and fGC levels than subordinate males independent of female reproductive state; further, adult subordinates had significantly higher fT, but not fDHT or fGC, than subadult subordinates. Male fT, fDHT, and fGC levels were significantly higher in the presence of fertile females, regardless of male dominance status and age. These findings indicate that the higher reproductive effort of alpha males comes with some costs (increased fGCs), and the presence of periovulatory females is associated with specific endocrine responses reflecting male reproductive effort and stress in white-faced capuchins.     

Activity and ranging patterns in relation to fruit utilization by Brown Capuchins (Cebus apella) in French Guiana

I studied brown capuchins (Cebus apella)in primary forest in French Guiana. They displayed different feeding and ranging patterns in response to changes in fruit availability and distribution. When fruit was scarce and patchily distributed, foliage/stem feeding and invertebrate foraging was high, and capuchins limited their daily movement to <2 km, focusing on large fruit patches. When fruit was in average supply and scattered throughout the forest, the proportions of foliage/stems and invertebrates in the diet decreased, and the day range length increased to 2.8 km. When fruit was abundant and widespread, foliage/stems were rarely eaten, while invertebrate foraging increased, and. the daily locomotor distance was reduced to 2 km.     

The Effect of Dietary Adaption on Cranial Morphological Integration in Capuchins (Order Primates,Genus Cebus)

A fundamental challenge of morphology is to identify the underlying evolutionary and developmental mechanisms leading to correlated phenotypic characters. Patterns and magnitudes of morphological integration and their association with environmental variables are essential for understanding the evolution of complex phenotypes, yet the nature of the relevant selective pressures remains poorly understood. In this study, the adaptive significance of morphological integration was evaluated through the association between feeding mechanics, ingestive behavior and craniofacial variation. Five capuchin species were examined, Cebus apella sensu stricto, Cebus libidinosus, Cebus nigritus, Cebus olivaceus and Cebus albifrons. Twenty three-dimensional landmarks were chosen to sample facial regions experiencing high strains during feeding, characteristics affecting muscular mechanical advantage and basicranial regions. Integration structure and magnitude between and within the oral and zygomatic subunits, between and within blocks maximizing modularity and within the face, the basicranium and the cranium were examined using partial-least squares, eigenvalue variance, integration indices compared inter-specifically at a common level of sampled population variance and cluster analyses. Results are consistent with previous findings reporting a relative constancy of facial and cranial correlation patterns across mammals, while covariance magnitudes vary. Results further suggest that food material properties structure integration among functionally-linked facial elements and possibly integration between the face and the basicranium. Hard-object-feeding capuchins, especially C.apella s.s., whose faces experience particularly high biomechanical loads are characterized by higher facial and cranial integration especially compared to C.albifrons, likely because morphotypes compromising feeding performance are selected against in species relying on obdurate fallback foods. This is the first study to report a link between food material properties and facial and cranial integration. Furthermore, results do not identify the consistent presence of cranial modules yielding support to suggestions that despite the distinct embryological imprints of its elements the cranium of placental mammals is not characterized by a modular architecture.     

Effect of Male Emigration on the Vigilance Behavior of Coresident Males in White-Faced Capuchins (Cebus capucinus)

I examined the vigilance behavior of male Cebus capucinus residing in four groups in Santa Rosa Park, Costa Rica. One male emigrated from each of three study groups, providing ideal experimental conditions for examining the effect of coresident males on male vigilance behavior (social and non-social). Following the predator and conspecific defense theories for the adaptive value of male vigilance behavior and the occurrence of multimale groups, I predicted that male nonsocial vigilance would increase after the emigration of a coresident male. My prediction was supported in only one of the three study groups. Males in two groups decreased their nonsocial vigilance after the emigration of a coresident male, which was probably influenced by seasonal changes and the peripherality of one group's coresident male before his emigration. The social vigilance hypothesis proposes that for species with rigid dominance hierarchies, social vigilance should increase with an increase in same sex competitors. Therefore, I predicted that male social vigilance would decrease after the emigration of a coresident male. The hypothesis is generally supported in my findings, as two of the three groups displayed a decrease in social vigilance after the emigration of a coresident male. Increased social vigilance in the third group is best explained by the change in the alpha male's social behavior after the emigration of his only coresident male.     

Problem-Solving Strategies and Hand Preferences for a Multicomponent Task by Tufted Capuchins (Cebus apella)

We examined hand preferences in 23 tufted capuchins (Cebus apella) in 2 tasks requiring the lid of a box to be lifted before taking out a peanut. The first task, Box 1, could entail either 2 or 3 problem-solving acts, with the 3-act solution involving bimanual coordination for food retrieval. The second task, Box 2, involved only the 3-act solution. The results indicated that the types of solution employed to perform the task influenced capuchin hand preferences. In the 2-act solution, capuchins exhibited a significant right-hand bias for the final one-handed reaching action, but not for the initial lid lifting action. In contrast, in the 3-act solution, no significant asymmetry emerged for any act. We noted a significant effect of subject's sex on the strength of laterality, with males being more strongly lateralized than females. We discuss results in the light of recent models of primate laterality.     

Biomarkers of genotoxicity and genomic instability in a non-human primate, Cebus libidinosus (Cebidae, Platyrrhini), exposed to nitroimidazole derivatives

The genotoxicity of two nitroimidazole derivatives, ornidazole (ONZ) and metronidazole (MTZ) in the peripheral blood lymphocytes of Cebus libidinosus (CLI) (Primates, Cebidae) was assessed. Endpoints measured included sister chromatid exchange (SCE) frequency, cell proliferation kinetics (CPK), replication index (RI), mitotic index (MI), and damage incidence in or near CLI heterochromatin regions. MI and SCE values following ONZ or MTZ treatments were significantly different (p<0.001) from control. SCE frequency per chromosome was not proportional to chromosome length. The chromosomes most affected for SCE were 1, 2, 4, 6, 11-13, 17, and 18, many of which possess interstitial or terminal heterochromatin. In the CLI genome, chromosomes 11 and 17 showed higher susceptibility to damage RI was the only biomarker that did not show statistically significant differences between control and treated cultures. C. libidinosus bands 11q1.4 and 11q1.5 may be hot-spots in the context of nitroimidazole exposure.