Infectious Diseases in Free-Ranging Blonde Capuchins, <Emphasis Type="Italic">Sapajus flavius,</Emphasis> in Brazil

The main threats to primates worldwide are the degradation, fragmentation, and loss of their habitats; hunting (especially for bushmeat); and illegal trade. For many species, the most important threat is forest fragmentation, resulting in small populations that are restricted to isolated forest patches. In this situation, primates are particularly vulnerable to disease. The Endangered blonde capuchin (Sapajus flavius) is now restricted to a few forest patches in Northeast Brazil. We investigated the occurrence of parasites and bacterial diseases in one of three free-ranging groups of S. flavius in a small forest patch in Paraíba state, Northeast Brazil. We tested for antibodies against Leishmania spp., Trypanosoma cruzi, Toxoplasma gondii, Leptospira spp. (24 strains), and Brucella spp.. We used molecular analysis to detect Plasmodium spp., and evaluated blood smears for the presence of hemoparasites. All individuals tested negative for Leptospira spp. and B. abortus, but 8 of 48 (16%) presented antibodies for both Leishmania spp. and T. cruzi. We identified antibodies to T. gondii in 12% of the individuals tested. Plasmodium brasilianum infection was present in 4% of the individuals tested, and blood smears showed microfilariae parasites in 46% of the individuals tested. The occurrence of these infectious diseases in S. flavius may pose a significant threat in terms of reduced recruitment and poor survival rates, and an understanding of the influence of pathogens is crucial for the management of small populations of primates.     

Stone Anvil Damage by Wild Bearded Capuchins (Sapajus libidinosus) during Pounding Tool Use: A Field Experiment

We recorded the damage that wild bearded capuchin monkeys (Sapajus libidinosus) caused to a sandstone anvil during pounding stone tool use, in an experimental setting. The anvil was undamaged when set up at the Fazenda Boa Vista (FBV) field laboratory in Piauí, Brazil, and subsequently the monkeys indirectly created a series of pits and destroyed the anvil surface by cracking palm nuts on it. We measured the size and rate of pit formation, and recorded when adult and immature monkeys removed loose material from the anvil surface. We found that new pits were formed with approximately every 10 nuts cracked, (corresponding to an average of 38 strikes with a stone tool), and that adult males were the primary initiators of new pit positions on the anvil. Whole nuts were preferentially placed within pits for cracking, and partially-broken nuts outside the established pits. Visible anvil damage was rapid, occurring within a day of the anvil''s introduction to the field laboratory. Destruction of the anvil through use has continued for three years since the experiment, resulting in both a pitted surface and a surrounding archaeological debris field that replicate features seen at natural FBV anvils.     

Modification of Clay Forms by Tufted Capuchins (Cebus apella)

We examined modification of clay forms by tufted capuchins (Cebus apella) by presenting groups of subjects with clay, paint, stones, leaves, and sticks. In Experiment 1, 7 of 10 subjects reshaped portable forms with their hands and with stones, and decorated them with leaves and paint. In Experiment 2, 9 subjects marked clay slabs manually and with stick and stone tools. The manipulative propensities of Cebus can help us to understand psychological processes that underlie artistic expression in Homo and Pan.     

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.     

Ant-Gathering with Tools by Captive Tufted Capuchins (Cebus apella)

We examined ant-gathering with tools by captive tufted capuchins (Cebus apella) via two experiments. In Experiment 1, we provided groups of subjects with sticks and small branches and an apparatus that accommodated the use of tools to gather ants. In Experiment 2, we sealed the apparatus with acetate and provided the same subjects with sticks and stones. Seven of 14 subjects used sticks and leaves as probes to extract ants from the apparatus. Six of them modified probes by detaching sticks from larger branches, breaking sticks into two or more pieces, and subtracting leaves and bark. Three subjects later used a stone and stick tool-set to penetrate acetate barriers and to extract ants. These results demonstrate the use of tools by Cebus to capture moving prey and are consistent with the idea that sensorimotor skills associated with the production and use of tools in primates evolved convergently in capuchins and great apes.     

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.     

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 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.     

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.     

Experimental field study of problem-solving using tools in free-ranging capuchins (Sapajus nigritus, formerly Cebus nigritus)

Some populations of capuchins are reported to use tools to solve foraging problems in the wild. In most cases, this involves the act of pounding and digging. The use of probing tools by wild capuchins is considerably less common. Here we report on the results of an experimental field study conducted in southern Brazil designed to examine the ability of wild black-horned capuchins (Sapajus nigritus) to use a wooden dowel as a lever or a probe to obtain an embedded food reward. A group of eight capuchins was presented with two experimental platforms, each housing a clear Plexiglas box containing two bananas on a shelf and four inserted dowels. Depending on the conditions of the experiment, the capuchins were required either to pull (Condition I) or push (Conditions II and III) the dowels, in order to dislodge the food reward from the shelf so that it could be manually retrieved. In Condition I, four individuals spontaneously solved the foraging problem by pulling the dowels in 25% (72/291) of visits. In Conditions II and III, however, no capuchin successfully pushed the dowels forward to obtain the food reward. During these latter two experimental conditions, the capuchins continued to pull the dowels (41/151 or 27% of visits), even though this behavior did not result in foraging success. The results of these field experiments are consistent with an identical study conducted on wild Cebus capucinus in Costa Rica, and suggest that when using an external object as a probe to solve a foraging problem, individual capuchins were able to rapidly learn an association between the tool and the food reward, but failed to understand exactly how the tool functioned in accomplishing the task. The results also suggest that once a capuchin learned to solve this tool-mediated foraging problem, the individual persisted in using the same solution even in the face of repeated failure (slow rate of learning extinction).     

A Potential Distribution Model and Conservation Plan for the Critically Endangered Ecuadorian Capuchin, Cebus albifrons aequatorialis

Conservation actions that effectively and efficiently target single, highly threatened species require current data on the species’ geographic distribution and environmental associations. The Ecuadorian capuchin (Cebus albifrons aequatorialis) is a critically endangered primate found only in the fragmented forests of western Ecuador and northern Peru, which are among the world’s most severely threatened ecosystems. We use the MAXENT species distribution modeling method to model the potential distribution and environmental associations of Cebus albifrons aequatorialis, using all known presence localities recorded within the last 2 decades as well as 13 climate, topography, vegetation, and land-use data sets covering the entire geographic range of the subspecies. The environmental conditions that our model predicted to be ideal for supporting Cebus albifrons aequatorialis included ≥20% tree cover, mild temperature seasonality, annual precipitation <2000 mm, and low human population density. Our model identified 5028 km² of suitable habitat remaining, although many of these forest fragments are unprotected and are unlikely to support extant populations. Using the median population density across all sites for which data are available, we estimate the total carrying capacity of the remaining habitat to be 12,500 total individuals. The true number of remaining individuals is likely to be considerably lower due to anthropogenic factors. We highlight four critical regions of high predicted suitability in western Ecuador and northern Peru on which immediate conservation actions should focus, and we lay out clear priorities to guide conservation actions for ensuring the long-term survival of this gravely threatened and little known primate.     

Integration of New Males into Four Social Groups of Tufted Capuchins (Cebus apella)

We examined how aggressive, affiliative, and sexual behavior function to integrate male capuchins (Cebus apella) into a new social group. Nine males were exchanged among four social groups. We performed instantaneous scans and all-occurrence sampling during baseline, introduction, and follow-up periods. The study included three different introduction situations: 1) males familiar to one another were introduced to a group with no other adult male, 2) males unfamiliar to one another were introduced to a group with no other adult male, and 3) males familiar to one another were introduced to a group with an existing elderly, resident male. Severe aggression occurred in situations 2 and 3, but the introductions were peaceful in situation 1. In all cases proceptive females were among the first individuals to affiliate with the males, and males did not appear to compete for access to proceptive females. Following their period of proceptivity, the females that had cycled remained preferred social partners for the males. Immature animals also quickly affiliated with the new males, and the males tolerated the attention from immatures. Affiliative relationships between the males and nonproceptive females developed slowly, and while male-female aggression was mild, aggression among adult males (familiar and unfamiliar) had the potential to be severe.     

Aimed Throwing as a Means of Food Transfer Between Tufted Capuchins (Cebus apella)

We examined aimed throwing as a means of food transfer in tufted capuchins (Cebus apella). We conducted this research in three phases. In Phase 1 we provided food to monkeys in one of two groups housed 1 m apart. We did not provide food to subjects in the second group. An observer recorded each instance in which a subject in the first group threw food toward one in the second group. In Phase 2 we provided a group of capuchins with food and noted each instance in which a subject threw food toward an empty cage. In Phase 3 we provided food simultaneously to two groups of capuchins and noted each instance of food-throwing between them. In Phase 1 subjects in one group threw food toward subjects in a second group, which, when provided the opportunity, did not throw food toward capuchins in the first group. Thrown food was either caught, retrieved, or lost on the test room floor. The rate of throwing decreased significantly when subjects were presented with an empty cage and when both groups of subjects were given food. We propose that psychological processes which underlie aimed throwing and food sharing came into existence through convergent evolution in large-brained, extractive foraging primates. We further speculate that although a well-developed system of exchange, based on contingent reciprocity, may occur among primates only inHomo,simpler transfer systems involving voluntary unidirectional passing of food from one individual to another appear to be more widespread among primates than previously thought and can be expressed in rather unusual circumstances such as those in this experiment.     

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.     

Using the Hard, Randy, and Rittler Test to Evaluate Color Vision in Capuchins (Cebus libidinosus)

The identification of color vision types in primates is fundamental to understanding the evolution and biological function of color perception. The Hard, Randy, and Rittler (HRR) pseudoisochromatic test categorizes human color vision types successfully. Here we provide an experimental setup to employ HRR in a nonhuman primate, the capuchin (Cebus libidinosus), a platyrrhine with polymorphic color vision. The HRR test consists of plates with a matrix composed of gray circles that vary in size and brightness. Differently colored circles form a geometric shape (X, O, or Δ) that is discriminated visually from the gray background pattern. The ability to identify these shapes determines the type of dyschromatopsy (deficiency in color vision). We tested six capuchins in their own cages under natural sunlight. The subjects chose between two HRR plates in each trial: one with the gray pattern only and the other with a colored shape, presented on the left or right side at random. We presented the test 40 times and calculated the 95?% confidence limits for chance performance based on the binomial test. We also genotyped all subjects for exons 3 and 5 of the X-linked opsin genes. The HRR test diagnosed two subjects as protan dichromats (missing or defective L-cone), three as deutan dichromats (missing or defective M-cone), and one female as trichromat. Genetic analysis supported the behavioral data for all subjects. These findings show that the HRR test can be applied to diagnose color vision in nonhuman primates.     

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.     

Introgression Threatens the Survival of the Critically Endangered Freshwater Crayfish Cherax tenuimanus (Decapoda: Parastacidae) in the Wild

Hybridization and genetic introgression following the introduction of exotic species can pose a significant threat to the survival of geographically restricted species. A remnant population of the critically endangered freshwater crayfish Cherax tenuimanus in the upper reaches of the Margaret River in southwestern Australia is under threat following the introduction and spread of its congener Cherax cainii. Here, we examine the extent of hybridization and introgression between the two species using twelve polymorphic microsatellite loci. Our study reveals there are three times more C. cainii than C. tenuimanus at our study site in the upper reaches of the Margaret River. There is also evidence of hybridization and introgression between C. tenuimanus and C. cainii at this site, with F₁, F₂ and backcrossed individuals identified. While interbreeding was confirmed in this study, our simulations suggest that the levels of introgression are much lower than would be expected under random mating, indicating partial reproductive barriers exist. Nevertheless, it is apparent that hybridization and introgression with C. cainii pose a serious threat to C. tenuimanus and their survival in the wild will require active adaptive management and continued genetic monitoring to evaluate management effectiveness.     

Urine Washing and Sniffing in Wild White-faced Capuchins (<Emphasis Type=Italic>Cebus capucinus</Emphasis>): Testing Functional Hypotheses

Urine washing (UW) is taxonomically widespread among strepsirhines and platyrrhines, yet its functional significance is still unclear. We used 2274 h of focal follows of 35 adult and subadult wild white-faced capuchins (Cebus capucinus) to test 1) the intergroup signaling, intragroup social signaling, and thermoregulatory hypotheses for UW and 2) the hypothesis that individuals sniff each other's urine and other traces to gather socially significant information. Males engaged in significantly more UW than females. All 5 α-males engaged in more UW than subordinate males did, including 4 α-males that increased their UW rate above that of their male groupmates after their rise to α rank. Males engaged in significantly less UW while in view of other males than at other times. Male-male sniffing rates do not correlate with either aggression rate or dominance rank distance. Urine washing rates did not increase while subjects were in parts of their home range where more intergroup encounters occurred. Urine washing rates were highest early in the morning and late in the afternoon, presumably when temperatures were coolest. The data do not support either the thermoregulatory or social signaling hypothesis. We suggest that experiments with captive capuchins are necessary to resolve the issue of the function of urine washing in the taxon.     

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.