ELECTROCARDIOGRAPHIC PARAMETERS OF CAPTIVE TUFTED CAPUCHINS (CEBUS APELLA) UNDER CHEMICAL IMMOBILIZATION

This study presents the electrocardiogram findings from 97 captive tufted capuchin monkeys (Cebus apella) at the Sao Paulo Zoo (Sao Paulo, Brazil) while under ketamine anesthesia. The results did not differ greatly from data of domestic carnivores or other studied primate species. The most common rhythm recorded was normal sinus rhythm, followed by normal sinus rhythm with wandering pacemaker. Electrical axis varied from 0 degrees to -150 degrees but was most commonly between +60 degrees and +90 degrees. QRS complexes were predominantly positive in leads DI, DII, DIII, and AVF. These findings allow for the recognition of abnormal rhythms in these primate species and can contribute to future investigations into the cardiovascular diseases routinely diagnosed in primates and humans.

Investigation of Rudimentary Meta-Cognition in Lion-Tailed Macaques and Tufted Capuchins

Meta-cognition, or "thinking about thinking," has been studied extensively in humans, but very little is known about the process in animals. Although great apes and rhesus macaques (Macaca mulatta) have demonstrated multiple apparently meta-cognitive abilities, other species have either been largely ignored or failed to convincingly display meta-cognitive traits. Recent work by Marsh, however, raised the possibility that some species may possess rudimentary or partial forms of meta-cognition. This thesis sought to further investigate this possibility by running multiple comparative experiments. The goal of the first study was to examine whether lion-tailed macaques, a species that may have a rudimentary form of meta-cognition, are able to use an uncertainty response adaptively, and if so, whether they could use the response flexibly when the stimuli for which the subjects should be uncertain changed. The macaques' acquisition of the initial discrimination task is ongoing, and as such there were not yet data to support a conclusion either way. In the second study, tufted capuchins were required to locate a food reward hidden beneath inverted cups that sat on a Plexiglas tray. In some conditions the capuchins were shown where the food was hidden, in others they could infer its location, and in yet others they were not given information about the location of the food. On all trials, however, capuchins could optionally seek additional information by looking up through the Plexiglas into the cups. In general, capuchins did this less often when they were shown the food reward, but not when they could infer the reward's location. These data suggest capuchins only meta-cognitively control their information seeking in some conditions, and thus, add support to the potential for a rudimentary form of meta-cognition. In convergence with other studies, these results may represent early models for rudimentary meta-cognition, although viable alternative explanations still remain.

Goniometric evaluation of both forelimbs and hind limbs in two species of Neotropical monkeys

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus). Frequency, efficiency and tool selectivity

Chimpanzees have been the traditional referential models for investigating human evolution and stone tool use by hominins. We enlarge this comparative scenario by describing normative use of hammer stones and anvils in two wild groups of bearded capuchin monkeys (Cebus libidinosus) over one year. We found that most of the individuals habitually use stones and anvils to crack nuts and other encased food items. Further, we found that in adults (1) males use stone tools more frequently than females, (2) males crack high resistance nuts more frequently than females, (3) efficiency at opening a food by percussive tool use varies according to the resistance of the encased food, (4) heavier individuals are more efficient at cracking high resistant nuts than smaller individuals, and (5) to crack open encased foods, both sexes select hammer stones on the basis of material and weight. These findings confirm and extend previous experimental evidence concerning tool selectivity in wild capuchin monkeys (Visalberghi et al., 2009b; Fragaszy et al., 2010b). Male capuchins use tools more frequently than females and body mass is the best predictor of efficiency, but the sexes do not differ in terms of efficiency. We argue that the contrasting pattern of sex differences in capuchins compared with chimpanzees, in which females use tools more frequently and more skillfully than males, may have arisen from the degree of sexual dimorphism in body size of the two species, which is larger in capuchins than in chimpanzees. Our findings show the importance of taking sex and body mass into account as separate variables to assess their role in tool use. (C) 2011 Elsevier Ltd. All rights reserved.

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

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli. Am. J. Primatol. 74:299314, 2012. (c) 2011 Wiley Periodicals, Inc.

The interface between morphology and action planning: a comparison of two species of New World monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities.

The Interface Between Morphology and Action Planning: a Comparison of Two Species of New World Monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities. (C) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys (Cebus apella): a Perception-action perspective

How do capuchin monkeys learn to use stones to crack open nuts? Perception-action theory posits that individuals explore producing varying spatial and force relations among objects and surfaces, thereby learning about affordances of such relations and how to produce them. Such learning supports the discovery of tool use. We present longitudinal developmental data from semifree-ranging tufted capuchin monkeys (Cebus apella) to evaluate predictions arising from Perception-action theory linking manipulative development and the onset of tool-using. Percussive actions bringing an object into contact with a surface appeared within the first year of life. Most infants readily struck nuts and other objects against stones or other surfaces from 6 months of age, but percussive actions alone were not sufficient to produce nut-cracking sequences. Placing the nut on the anvil surface and then releasing it, so that it could be struck with a stone, was the last element necessary for nut-cracking to appear in capuchins. Young chimpanzees may face a different challenge in learning to crack nuts: they readily place objects on surfaces and release them, but rarely vigorously strike objects against surfaces or other objects. Thus the challenges facing the two species in developing the same behavior (nut-cracking using a stone hammer and an anvil) may be quite different. Capuchins must inhibit a strong bias to hold nuts so that they can release them; chimpanzees must generate a percussive action rather than a gentle placing action. Generating the right actions may be as challenging as achieving the right sequence of actions in both species. Our analysis suggests a new direction for studies of social influence on young primates learning sequences of actions involving manipulation of objects in relation to surfaces.

Use Of Conspecific Gestural Cues To Solve An Object-Choice Task In Tufted Capuchin Monkeys (Cebus Apella)

Capuchin monkeys, Cebus sp., utilize a wide array of gestural displays in the wild, including facial displays such as lip-smacking and bare-teeth displays. In captivity, they have been shown to respond to the head orientation of humans, show sensitivity to human attentional states, as well as follow human gazes behind barriers. In this study, I investigated whether tufted capuchin monkeys (Cebus apella) would attend to and utilize the gestural cues of a conspecific to obtain a hidden reward. Two capuchins faced each other in separate compartments of an apparatus with an open field in between. The open field contained two cups with holes on one side such that only one monkey, a so-called cuing monkey, could see the reward inside one of the cups. I then moved the cups toward the other signal-receiving monkey and assessed whether it would utilize untrained cues provided by the cuing monkey to select the cup containing the reward. Two of four female capuchin monkeys learned to select the cup containing the reward significantly more often than chance. Neither of these two monkeys performed over chance spontaneously, however, and the other two monkeys never performed above chance despite many blocks of trials. Successful choices by two monkeys to obtain hidden rewards provided experimental evidence that capuchin monkeys attend to and utilize the gestural cues of conspecifics.

Expression of prox1, lymphatic endothelial nuclear transcription factor, in Kaposiform hemangioendothelioma and tufted angioma.

Kaposiform hemangioendothelioma (KHE) and tufted angioma (TA) are rare tumors mainly occurring in early childhood. Our recent results showed that ectopic overexpression of human Prox1 gene, a lymphatic endothelial nuclear transcription factor, promoted an aggressive behavior in 2 murine models of KHE. This dramatic Prox1-induced phenotype prompted us to investigate immunohistochemical staining pattern of Prox1, podoplanin (D2-40), LYVE-1, and Prox1/CD34 as well as double immunofluorescent staining pattern of LYVE-1/CD31 in KHE and TA, compared with other pediatric vascular tumors. For this purpose, we examined 75 vascular lesions: KHE (n=18), TA (n=13), infantile hemangioma (n=13), pyogenic granuloma (n=18), and granulation tissue (n=13). Overall, KHE and TA shared an identical endothelial immunophenotype: the neoplastic spindle cells were Prox1, podoplanin, LYVE-1, CD31, and CD34, whereas endothelial cells within glomeruloid foci were Prox1, podoplanin, LYVE-1, CD31, and CD34. The lesional cells of all infantile hemangiomas and pyogenic granulomas were negative for Prox1 in the presence of positive internal control. These findings provide immunophenotypic evidence to support a preexisting notion that KHE and TA are closely related, if not identical. Overall, our results show, for the first time, that Prox1 is an immunohistochemical biomarker helpful in confirming the diagnosis of KHE/TA and in distinguishing it from infantile hemangioma and pyogenic granuloma.

Salmonella Yoruba infection in white-tufted-ear marmoset (Callithrix jacchus)

The aim of this study was to describe a fatal salmonellosis case in a non-human female primate (Callithrix jacchus), found in the illegal pet trade in Brazil. The marmoset was sent to the quarantine section of the Guarulhos City Zoo and died in the sequence of an episode of profuse diarrhea. Necropsy findings included mucous enteritis, and liver enlargement and necrosis. Feces and liver fragments were collected for bacteriological tests, which indicated the presence of Salmonella sp.; it was subsequently characterized as pertaining to the Yoruba serotype. The susceptibility profile demonstrated resistance to tetracycline only. The strain was positive for genes that encoded the virulence factors investigated (invA, sefC, pefA and spvC). The results indicated the risk of introduction of Salmonella pathogenic serotypes in primates in captivity.

Comparative anatomical study of the leg's nerves of Cebus (barbed capuchins) with baboons, chimpanzees and modern humans

The anatomical comparative studies among the primates are important for the investigation of ethology, evolution, taxonomy, and comprehension of tools by hominoids. Especially the anatomical knowledge of Cebus contributes to conservation of the species, and to development of surgical procedures and clinical treatments of these animals, as they frequently are victims of automobile accidents. Recent anatomical studies came to a wrong conclusion regarding behavioral traits of Cebus, ascribed to few data available in previous literature. Therefore, to provide anatomical data and to support the other sciences related to anatomy, and to develop surgical and/or clinical procedures, we described the nerves of the legs of Cebus foccusing on their position and trajectory, as wll as innerved muscles, and compared these results with those of humans and other primates. Eight adult capuchin specimens were used for this study. The anatomical comparative study of the leg's nerves of Cebus demonstrated that, in general, structural organization of the nerves is similar among the four primates analyzed here (Cebus, chimpanzees, baboons and humans), which might be attributed to the fact that the all four primates have similar body structures. However, nerve trajectory and muscles innervation in Cebus was more similar to baboons.

Frequency of Toxoplasma gondii antibodies in tufted capuchin monkeys (Cebus apella nigritus) from an ecological station in the State of São Paulo, Brazil

Toxoplasmosis is a worldwide zoonosis caused by Toxoplasma gondii, an obligate intracellular parasite protozoan. A large percentage of animals presents specific antibodies caused by a previous exposition, resulting in a chronic infection. Felides are the definitive hosts and the other warm-blooded animals, including primates, are the intermediate hosts. This study was aimed to determine the prevalence of T. gondii infection in free-living tufted capuchin monkeys (Cebus apella nigritus) from an ecological station located on Mata de Santa Teresa, Ribeirão Preto, SP, Brazil. T. gondii antibodies were analyzed by modified agglutination test (MAT) in serum samples of 36 tufted capuchin monkeys, considering eight as cut-off titer. From the studied animals, 3/36 (8.33%; CI95% 3.0-21.9%) presented T. gondii antibodies, all with titer 32. No significative difference was observed relating to the sex (1/3 male and 2/3 female), and to the age (1/3 young and 2/3 adult) (P>0.05). Thus, these results demonstrate the presence of T. gondii antibodies in primates from São Paulo state.

Cardiothoracic ratio and vertebral heart size (VHS) to standardize the heart size of the tufted capuchin (Cebus apella Linnaeus, 1758) in computerized radiographic images

Abstract: The VHS and CTR were assessed using computerized thoracic radiographs of ten clinically healthy tufted capuchin monkeys (five males and five females) from the Wild Animal Screening Center in São Luís (Centro de Triagem de Animais Silvestres de São Luís-MA-CETAS). Radiographs were taken in laterolateral and dorsoventral projections to calculate the cardiothoracic ratio (VHS) and vertebral heart size (CTR). The VHS showed mean values of 9.34±0.32v (males) and 9.16±0.34v (females) and there was no statistical difference between males and females (p>0.05). The CTR showed mean values of 0.55±0.04 (males) and 0.52±0.03 (females) and there was no statistical difference between the sexes (p>0.05). There was positive correlation between VHS and CTR (r=0.78). The thoracic and heart diameters showed mean values of 5.70±0.48cm and 2.16±0.40cm in the males, respectively. In the females they measured 5.32±0.39cm and 2.94±0.32cm. There was no statistical difference between the sexes. Our results show that the high correlation found between VHS and CTR permitted the verification with similar clinical precision between the two methods to estimate alterations in the heart silhouette by radiographic examination of tufted capuchin, making it an easy technique to apply that can be considered in the investigation of heart problems for this wild species.