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.

Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus

Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in Sao Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi-arid habitat in Piaui state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low-quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus. Am. J. Primatol. 74:315331, 2012. (c) 2011 Wiley Periodicals, Inc.

Anatomical and radiographic appearance of the capuchin monkey thoracic cavity (Cebus apella)

The capuchin monkey is widespread both north and south of the Legal Amazon and in the Brazilian cerrado. Ten clinically healthy capuchin monkeys were submitted to an anatomical and radiographic study of their thoracic cavities. The radiographic evaluation allowed the description of biometric values associated with the cardiac silhouette and thoracic structures. Application of the VHS (vertebral heart size) method showed positive correlation (P<0.05) with depth of the thoracic cavity, as well as between the body length of vertebrae T 3, T 4, T 5 and T 6 and the cardiac length and width. The lung fields showed a diffuse interstitial pattern, more visible in the caudal lung lobes and a bronchial pattern in the middle and cranial lung lobes. The radiographic examination allowed preliminary inferences to be made concerning the syntopy of the thoracic structures and modifiication of the pulmonary patterns and cardiac anatomy for the capuchin monkey.

Transport of Functionally Appropriate Tools by Capuchin Monkeys (Cebus apella)

Capuchin monkeys are notable among New World monkeys for their widespread use of tools. They use both hammer tools and insertion tools in the wild to acquire food that would be unobtainable otherwise. Evidence indicates that capuchins transport stones to anvil sites and use the most functionally efficient stones to crack nuts. We investigated capuchins’ assessment of functionality by testing their ability to select a tool that was appropriate for two different tool-use tasks: A stone for a hammer task and a stick for an insertion task. To select the appropriate tools, the monkeys investigated a baited tool-use apparatus (insertion or hammer), traveled to a location in their enclosure where they could no longer see the apparatus, made a selection between two tools (stick or stone), and then could transport the tool back to the apparatus to obtain a walnut. Four capuchins were first trained to select and use the appropriate tool for each apparatus. After training, they were then tested by allowing them to view a baited apparatus and then travel to a location 8 m distant where they could select a tool while out of view of the apparatus. All four monkeys chose the correct tool significantly more than expected and transported the tools back to the apparatus. Results confirm capuchins’ propensity for transporting tools, demonstrate their capacity to select the functionally appropriate tool for two different tool-use tasks, and indicate that they can retain the memory of the correct choice during a travel time of several seconds.

Audience Effects in COgnitive Task Performance in Capuchin Monkeys (Cebus apella)

Primates as a taxonomic Order have the largest brains corrected for body size in the animal kingdom. These large brains have allowed primates to evolve the capacity to demonstrate advanced cognitive processes across a wide array of abilities. Nonhuman primates are particularly adept at social learning, defined as the modification of behavior by observing the actions of others. Additionally, primates often exploit resources differently depending on their social context. In this study, capuchin monkeys (Cebus apella) were tested on a cognitive task in three social contexts to determine if social context influenced their performance on the task. The three social contexts included: alone, having a dominant individual in an adjacent compartment, and having a subordinate individual in the adjacent compartment. The benefits to this design were thatthe social context was the only variable influencing performance, whereas in previous studies investigating audience effects other animals could physically and directly influence a subject's performance in an open testing situation. Based on past studies, Ipredicted that the presence of a dominant individual would reduce cognitive task performance compared to the other conditions. The cognitive test used was a match-tosample discrimination task in which animals matched combinations of eight geometric shapes. Animals were trained on this task in an isolated context until they reached a baseline level of proficiency and were then tested in the three social contexts in a random order multiple times. Two subjects (Mt and Dv) have successfully completed trials under all conditions. Results indicated that there were no significant difference in taskperformance across the three conditions (Dv x^2 (1) = 0.42, p=0.58; Mt x^2 (1) = 0.02, p=0.88). In all conditions, subjects performed significantly above chance (i.e., 39/60 trials determined by a binomial distribution). Results are contrary to previous studies thatreport low status monkeys 'play dumb' when testing in a mixed social context, possibly because other studies did not account for aggressive interference by dominants while testing. Results of this study suggest that the mere presence of a dominant individualdoes not necessarily affect performance on a cognitive task, but rather the imminence of physical aggression is the most important factor influencing testing in a social context.

IMPULSE CONTROL AND COOPERATION IN CAPUCHIN MONKEYS (Cebus apella)

The benefits animals derive from living in social groups have produced the evolution of many forms of cooperative behavior. To cooperate, two or more individuals coordinate their actions to accomplish a common goal. One cognitive process that has the potential to influence cooperation is self control. Individuals delaying their impulsive choice for an immediate reward may potentially receive a larger reward later by cooperating with others. In this study, I measured whether brown capuchin monkeys (Cebus apella) were capable of impulse control and whether impulse control was related to cooperation. Impulse control and cooperation were measured using a lazy susan-like apparatus, on which animals could turn a wheel to receive food rewards. The capuchins went through two training phases that taught them how to turn the wheel efficiently to obtain rewards and how to turn the wheel to obtain the larger of two rewards. After training, I tested impulse control by giving the capuchins a choice between a smaller and a larger reward placed at shorter or more distant locations on the wheel. The capuchins demonstrated impulse control in that they tended to inhibit the impulse to select the smaller reward when it was closer and easier to reach and instead selected the larger reward when it was farther away. Cooperation was tested in all possible dyads of seven individuals, a total of 21 dyads, by allowing each dyad 10 trials to work together with effort on the lazy-susan so that each would obtain a reward. Seventeen out of 21 dyads cooperated by simultaneously moving the wheel in the same direction. The correlation between how often a particular dyad cooperated and their average impulse control score was not statistically significant, r(21) = -.125, p = .591. Capuchins demonstrated impulse control and cooperation using this novel apparatus but the two abilities were not related. Other factors such as the unique social relationship between two individuals may play a more prominent role in the motivation to cooperate rather than the cognitive capacity to inhibit behavior.

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.

The Expression Of Motor Planning In Squirrel Monkeys (Saimiri sciureus) And Brown Capuchins (Cebus apella)

Multiple recent studies provide evidence that both human and nonhuman primates possess motor planning abilities. I tested for the demonstration of motor planning in two previously untested primate species through two experiments. In the first experiment, I compared the extent to which squirrel monkeys (Saimiri sciureus) and brown capuchins (Cebus apella) plan their movements in a grasping task. Individuals were presented with an inverted cup that required being turned and held upright in order to extract a food reward from the inside of the cup. This task was most efficiently solved by using an initially awkward inverted grasp that affords a comfortable hand and arm orientation at the end of the movement (known as end-state comfort). While certain individuals from both species exhibited end-state comfort, many of the capuchins never demonstrated this type of motor planning. Furthermore, the squirrel monkeys used the efficient grasp significantly more than the capuchins. In the second experiment, I presented the capuchins with another grasping task to test if they would express motor planning abilities in a different context. Here, the capuchins were offered a dowel that was baited on either the left or right end. A radial grasp with the thumb pointing towards the baited end was considered to be the most efficient grasp because it afforded a comfortable final position. The capuchins switched hands and used an overhand radial grasp on the dowel significantly more often than not, thus demonstrating motor planning in this task. The grasps typically utilized by these two closely related species differ considerably in that capuchins are capable of exercising precision grips, whereas squirrel monkeys are limited to whole-handed power grips. Moreover, unlike capuchins, squirrel monkeys are not particularly dexterous nor are they capable of precise manipulative actions. It is therefore more beneficial for squirrel monkeys to plan their movements efficiently because they are less capable of compensating for inappropriate initial grasps. Due to the appreciable variability in the expression of motor planning skills across species, I proposed that morphological constraints might explain the observed discrepancies in movement planning among different primate species.

Brown Capuchins (Cebus apella) Exhibit Self-Control on a Delay of Gratification Food Exchange Task When Food Options Differ Qualitatively

Self-control allows an individual to obtain a more preferred outcome by forgoing an immediate interest. Self-control is an advanced cognitive process because it involves the ability to weigh the costs and benefits of impulsive versus restrained behavior, determine the consequences of such behavior, and make decisions based on the most advantageous course of action. Self-control has been thoroughly explored in Old World primates, but less so in New World monkeys. There are many ways to test self-control abilities in non-human primates, including exchange tasks in which an animal must forgo an immediate, less preferred reward to receive a delayed, more preferred reward. I examined the self-control abilities of six capuchin monkeys using a task in which a monkey was given a less preferred food and was required to wait a delay interval to trade the fully intact less preferred food for a qualitatively higher, more preferred food. Partially eaten pieces of the less preferred food were not rewarded, and delay intervals increased on an individual basis based on performance. All six monkeys were successful in inhibiting impulsivity and trading a less preferred food for a more preferred food at the end of a delay interval. The maximum duration each subject postponed gratification instead of responding impulsively was considered their delay tolerance. This study was the first to show that monkeys could inhibit impulsivity in a delay of gratification food exchange task in which the immediate and delayed food options differed qualitatively and a partially eaten less preferred food was not rewarded with the more preferred food at the end of a delay interval. These results show that New World monkeys possess advanced cognitive abilities similar to those of Old World primates.

Capuchin Monkeys (Cebus apella) Fail to Be Equitable in an Ultimatum Game

The ultimatum game is a commonly used economics game testing humans' sense of fairness. In the game, a "proposer" is given a sum of money and is told they can split it however they want with another human partner. The partner can then either accept the division and both proposer and responder receive the proposed amounts, or the responder can reject the offer and neither player will get anything. Human subjects from most western cultures typically share almost half of an allotted amount, but it remains unknown whether our close primate relatives share this generosity. Recent attempts to present chimpanzees with the ultimatum game have provided inconclusive results, with some studies finding the animals share humans' disposition to behave 'fairly' and others concluding that chimpanzees act selfishly to maximize their own rewards. Capuchin monkeys are known to share many human and chimpanzee social and cooperative behaviors, and this study was the first to present capuchin monkeys with a version of the ultimatum game. Subjects were presented with two differently colored tokens representing different qualitative reward contingencies, one equitable and the other inequitable in favor of the subject proposer. Subjects could select and place one of the tokens in a transfer container. The capuchins were first tested with a "dictator game" where, after the subject monkey selected a token, the rewards (equitable or inequitable) were distributed to the subject and a nearby partner monkey that was not an active participant. The capuchins were then tested on an ultimatum game in which after the subject selected and placed a token in the container, the container was moved to the partner. The partner needed to remove the token and transfer it back to the experimenter for the rewards to be distributed. As such, the partner could reject the subject's offer by refusing to participate and neither would receive a reward. The experiment was conducted to determine if the subject monkey would select the equitable reward option rather than the selfish option in order to maintain the partner's cooperation in the task. Capuchin subjects behaved selfishly and selected the inequitable token significantly more often than the equitable token in both the dictator and ultimatum game with no significant difference in preference between the two games. Interestingly, despite the occasional occurrence of rejection by the partner monkeys (resulting in no reward for the subject), subjects never altered their strategy, continuing to prefer the selfish token. The study may indicate that capuchin monkeys have an inability to judge the effect of their behavior on a conspecific's reward outcome, or an indifference to the outcome if there is an individual cost associated with behaving prosocially.

Capuchin monkey tool use: Overview and implications

Nutcracking capuchins are mentioned in reports dating as far back as the sixteenth century,(1,2) as well as in Brazilian folklore.(3) However, it was barely a decade ago that primatologists ""discovered"" the spontaneous use of stones to crack nuts in a semi-free ranging group of tufted capuchin monkeys. Since then, we have found several more capuchin populations in savanna-like environments which(5-7) employ this form of tool use. The evidence so far only weakly supports geneti cally based behavioral differences between populations and does not suggest that dietary pressures in poor environments are proximate determinants of the likelihood of tool use. Instead, tool use within these capuchin populations seems to be a behavioral tradition that is socially learned and is primarily associated with more terrestrial habits. However, differences in the diversity of ""tool kits"" between populations remain to be understood.

Cebus cf. apella exhibits rapid acquisition of complex stimulus relations and emergent performance by exclusion

A "second generation" matching-to-sample procedure that minimizes past sources of artifacts involves (1) successive discrimination between sample stimuli, (2) stimulus displays ranging from four to 16 comparisons, (3) variable stimulus locations to avoid unwanted stimulus-location control, and (4) high accuracy levels (e.g., 90% correct on a 16-choice task in which chance accuracy is 6%). Examples of behavioral engineering with experienced capuchin monkeys included four-choice matching problems with video images of monkeys with substantially above-chance matching in a single session and 90% matching within six sessions. Exclusion performance was demonstrated by interspersing non-identical sample-comparison pairs within a baseline of a nine-comparison identity-matching-to-sample procedure with pictures as stimuli. The test for exclusion presented the newly "mapped" stimulus in a situation in which exclusion was not possible. Degradation of matching between physically non-identical forms occurred while baseline identity accuracy was sustained at high levels, thus confirming that Cebus cf. apella is capable of exclusion. Additionally, exclusion performance when baseline matching relations involved non-identical stimuli was shown.

Desenvolvimento do dimorfismo sexual em espécies de macacos-prego, gênero Cebus Erxleben, 1777 (Primates, Cebidae)

Os trabalhos sobre dimorfismo sexual em Cebus disponíveis na literatura apontam Cebus apella como a espécie mais dimórfica do gênero. Contudo, vale ressaltar que diversas espécies de macacos-prego eram consideradas anteriormente subespécies de C. apella, sendo analisadas em conjunto nestes estudos. O arranjo taxonômico que segui neste estudo considera tais táxons como espécies válidas, com considerável grau de diferenciação morfológica. A maior parte destes estudos utilizou somente exemplares adultos, assumindo que os indivíduos cessariam seu crescimento assim que a sua dentição estivesse completa. A falta de estudos sobre idades anteriores à idade adulta pode resultar em um entendimento incompleto sobre a natureza do dimorfismo sexual, pois níveis similares deste dimorfismo podem ser gerados por diferentes processos ontogenéticos, refletindo causas evolutivas distintas. Com base nestas informações, os objetivos do presente estudo foram verificar as diferenças sexuais cranianas e no grau de desenvolvimento dos tufos do capuz da cabeça ao longo da ontogenia de seis espécies de macacos-prego, todas pertencentes ao subgênero Sapajus (Cebus apella, C. macrocephalus, C. libidinosus, C. cay, C. nigritus e C. robustus) e confrontar os resultados obtidos entre as espécies para constatar se existem diferenças interespecíficas. Para tanto, examinei 774 espécimes depositados em coleções científicas brasileiras. Mensurei 20 variáveis craniométricas, examinei 12 caracteres cranianos discretos e estabeleci quatro estados de caráter para o grau de desenvolvimento dos tufos do capuz. Avaliei o dimorfismo sexual através do teste t de Student com ajustamento de Bonferroni e empreguei Análise de Componentes Principais (ACP), seguida de Análise de Função Discriminante (AFD) para testar a significância dos agrupamentos etários (infantes, jovens, subadultos e adultos, sendo este último grupo dividido em AD1 e AD2 para C. apella). Os resultados mostraram que diferenças sexuais cranianas podem ser evidenciadas no subgênero Sapajus somente a partir da idade subadulta (aproximadamente 3,5 anos de idade), sendo o comprimento dos caninos a mais conspícua. Contudo, estas diferenças ainda não são estatisticamente significativas. Somente a partir da idade adulta (cerca de 5 anos de idade) a maior parte das variáveis cranianas passou a apresentar dimorfismo sexual significativo, com as espécies comportando-se de modo distinto em relação ao tipo e número de variáveis dimórficas. As espécies que apresentaram maior número de variáveis significativas foram C. apella e C. robustus (N=15), seguidas de C. nigritus (N=13), C. libidinosus (N=10), C. cay (N=7) e C. macrocephalus (N=3). Estudos anteriores apontam que o dimorfismo sexual craniano em Cebus (Sapajus) surge em indivíduos jovens (cerca de 27 meses de idade). Os resultados obtidos neste estudo não corroboram esta idéia, pois demonstram que o dimorfismo sexual significativo surge apenas em indivíduos adultos. Tais resultados ainda sugerem que o processo heterocrônico da taxa de hipermorfose representa o principal fator para o padrão ontogenético de dimorfismo sexual craniano exibido. A despeito do dimorfismo sexual craniano, as espécies de macacos-prego diferem entre si em relação ao grau de desenvolvimento dos tufos do capuz. Constatei que o desenvolvimento dos tufos do capuz em Cebus (Sapajus) está diretamente relacionado à idade, não existindo dimorfismo sexual quanto ao grau de desenvolvimento desta estrutura em C. cay, C. robustus e C. nigritus. Em contrapartida, parece existir dimorfismo sexual negativo em relação ao desenvolvimento dos tufos em C. libidinosus, fato que carece de maiores investigações. Por fim, os resultados deste estudo sugerem que as espécies de macacos-prego podem ter experimentado diferentes graus e/ou tipos de pressões seletivas quanto ao dimorfismo sexual ao longo de sua história evolutiva.

Desenvolvimento comportamental manipulativo e ocorrência de olhar mútuo entre macacos-prego (Cebus cf. apella) em cativeiro

Os filhotes de Cebus durante os dois primeiros meses de vida, dependem quase que exclusivamente de sua mãe. Só a partir do terceiro mês o filhote passa a se locomover independentemente, e é nesse período que corre uma importante mudança no seu padrão comportamental, pois há um aumento em seu repertório manipulativo. O principal objetivo desse estudo foi acompanhar o desenvolvimento do comportamento manipulativo em três filhotes de Cebus cf. apella e verificar a possível preferência pelo olhar mútuo entre macacos-prego. No Experimento 1, com o método de animal focal foi medida a freqüência de linha de base das categorias comportamentais de três Cebus cf. apella filhotes, e em seguida inseridos quatro tipos de objetos, um a cada semana, para o acesso ao desenvolvimento de comportamentos manipulativos. No Experimento 2, foi realizado teste de discriminação simples, usando como estímulos fotos de macacos-prego com diferentes direções do olhar. No Experimento 3, foi realizado um treino de discriminação simples, com dois pares de estímulos: rosto frontal e olhar direto versus desviado e rosto de frente versus de perfil. Os resultados demonstram que os filhotes de mesma faixa etária despenderam tempo semelhante manipulando objetos. Não foi possível observar um padrão claro quanto a preferência em observar imagens com olhar direto ou desviado (Experimento 2). Os sujeitos foram capazes de discriminar a direção do olhar no Experimento 3.

Efeitos da manipulação do número de escolhas sobre o desempenho em tarefas de discriminação simples em macaco-prego (Cebus cf. apella)

Em um treino discriminativo, há diversas variáveis que podem afetar a precisão da aquisição do repertório. Uma variável pouco analisada é o número de escolhas apresentado nas tentativas discretas de treino, buscando verificar em que situações o controle discriminativo pode ser mais facilmente estabelecido. Este trabalho tem como objetivo geral descrever os efeitos da manipulação do número de escolhas sobre o desempenho em tarefas de discriminação simples em macacos-prego (Cebus cf. apella). No Experimento I, os sujeitos foram submetidos a um treino discriminativo com três tipos diferentes de tentativas (2, 4 e 9 escolhas). Um teste de controle de estímulos avaliou se o repertório aprendido podia ser mantido quando os estímulos utilizados nos três tipos de tentativa eram apresentados na forma de duas escolhas. No Experimento II, buscou-se adicionalmente avaliar se as respostas corretas nos treinos prévios de discriminação ocorriam em função de escolha por seleção do S⁺, por rejeição do S^-, ou por controle misto (seleção e rejeição). Esta avaliação foi realizada através do procedimento de máscara. Os resultados do Experimento I sugerem que a exposição a um número maior de escolhas é uma estratégia eficiente para estabelecer o responder discriminado, pois o desempenho permanece mesmo quando o número de escolhas é posteriormente reduzido para dois. Os resultados obtidos no Experimento II mostram dados diferentes para os dois sujeitos. M30 apresentou controle por rejeição e preferência pela máscara e M31 apresentou controle misto no responder. O presente estudo mostra um caminho para aprofundar a análise do controle de estímulos nos estudos específicos sobre a manipulação do número de escolhas e indica que essa variável pode ser um meio eficaz de reduzir a dificuldade de aquisição de discriminações em contexto aplicado.