Olfactory discrimination of urine odors from five species by tufted capuchin (Cebus apella)

Urine collected from New World monkeys (tufted capuchin, squirrel monkey, cotton-top tamarin) and Old World monkeys (rhesus macaque, Japanese macaque), was used as the odor stimuli. Two adult tufted capuchins were trained on a successive odor-discrimination task with two odors, 30 trials each, in one session per day. Responses to one of the two odors (S+) were reinforced by sweet water. The monkeys failed to discriminate between the urine from the two species of macaques but could discriminate among the urine from the three species of New World monkeys. Furthermore, similarity of urine odors was analyzed by multi-dimensional scaling (MDS) and a cluster analysis. These analysis suggested that the tufted capuchin can distinguish differences among New World monkeys but not between the macaques. The natural distribution of the tufted capuchin overlaps with that of other New World monkeys, but it does not overlap with those of Old World monkeys. Consequently, it can be concluded that this difference in olfactory recognition in the tufted capuchin reflects their sympatric and allopatric relationships with other species.     

Hand preference in capuchin monkeys varies with age

The purpose of this research was to examine the influence of age on hand preference in capuchin monkeys (Cebus apella). Twenty-two capuchins, aged 6 months to 30 years, were presented with a task that involved reaching for food and a task that involved using sponging tools to absorb juice. Adults exhibited a greater percentage of right-handed actions in each task than did immature subjects. Adults also exhibited a stronger lateral bias than did immature subjects in the sponging task. These results are consistent with hypotheses: a) adult capuchin monkeys are biased toward use of their right hand for reaching; b) adult capuchins exhibit a greater incidence of right-hand preference than do immature capuchins; and c) primates exhibit age-related differences in the strength and direction of hand preference in tasks that involve the use of tools.     

Does Presentation Format Influence Visual Size Discrimination in Tufted Capuchin Monkeys (Sapajus spp.)?

Most experimental paradigms to study visual cognition in humans and non-human species are based on discrimination tasks involving the choice between two or more visual stimuli. To this end, different types of stimuli and procedures for stimuli presentation are used, which highlights the necessity to compare data obtained with different methods. The present study assessed whether, and to what extent, capuchin monkeys’ ability to solve a size discrimination problem is influenced by the type of procedure used to present the problem. Capuchins’ ability to generalise knowledge across different tasks was also evaluated. We trained eight adult tufted capuchin monkeys to select the larger of two stimuli of the same shape and different sizes by using pairs of food items (Experiment 1), computer images (Experiment 1) and objects (Experiment 2). Our results indicated that monkeys achieved the learning criterion faster with food stimuli compared to both images and objects. They also required consistently fewer trials with objects than with images. Moreover, female capuchins had higher levels of acquisition accuracy with food stimuli than with images. Finally, capuchins did not immediately transfer the solution of the problem acquired in one task condition to the other conditions. Overall, these findings suggest that – even in relatively simple visual discrimination problems where a single perceptual dimension (i.e., size) has to be judged – learning speed strongly depends on the mode of presentation.     

Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.     

Look before leaping: foraging selectivity of capuchin monkeys on acacia trees in Costa Rica

Acacia trees in Costa Rica have an obligate mutualism with three species of Pseudomyrmex ants, which vigorously defend their host tree from insect and mammalian herbivores. Depending on the size and species of ant colony, individual acacia trees may be differentially protected. For animals able to discern between weakly and highly aggressive ant colonies, costs of ant stings from less active colonies might be offset by nutritional value acquired from feeding on acacia fruit or ant larvae in swollen thorns. We examined foraging selectivity of capuchin monkeys on acacia trees in Santa Rosa National Park, Costa Rica. We measured four characteristics of the acacia trees from which capuchins fed and of acacias immediately adjacent to those in which the monkeys fed: diameter at breast height (DBH), accessibility, species of closest tree and ant species present. We found that capuchins prefer to forage in acacias that are large and accessible. We also made two measurements of ant colony activity on each tree, one before and one after disturbing the ant colony. We found that the three species of mutualistic ants differ in baseline activity levels and that mutualistic ants are more active than non-mutualistic ant species found in acacia trees. We also found that capuchins foraged more frequently in trees colonized by non-mutualistic ants, but the explanatory value (r ²) of this model was low. Furthermore, monkeys did not discriminate between acacias on the basis of baseline ant activity or the ant colony’s response to disturbance. We conclude that these monkeys select acacia trees in which to forage based on characteristics of the trees rather than the ants. In addition, our study suggests that white-faced capuchins act as predators on the acacia ants but they probably benefit the dispersal and reproductive success of acacia trees. Capuchins may in fact function as an additional mutualistic partner for acacia trees via seed dispersal, but they must overcome the ants’ defense of the trees to do so.     

Complex behavior forms in the lower monkeys in the process of identification of quantitative signs of visual stimuli

Complex behavior forms and the ability of monkeys to recognize and to compare by identity the two-dimensional images and three-dimensional objects of various colors in the amount from 5 to 9 were studied. The study was carried out on two species of the lower monkeys of different levels of phylogenetic development: on rhesus monkeys (Macaca mulatta) and on brown capuchins (Cebus apella). It has been established that the representatives of the studied monkey species are able to differentiate large counted multitudes of two-dimensional (images of squares) and three-dimensional (objects of round shape) stimuli of red, yellow, and green colors in different quantitative ratios—from 5 to 9 at solving modifications of task of the type “choice by the sample.” In the course of learning, species-related differences of the monkeys’ behavior are revealed. The brown capuchins managed solving all tasks and their combinations better than rhesus monkeys. The obtained data indicate the capability for recognition of counted multitudes (from 5 to 9) regardless of color of the stimuli and the existence of quantitative notions of the idea of “quantity” in the lower monkeys.     

Carrying and hand-use patterns in Panamanian white-faced capuchins (Cebus capucinus)

The aim of this project was to examine the potential influence of postural regulation on capuchin hand-use patterns by focusing on tasks that involved the carrying of objects. Two months were spent on Barro Colorado Island, Panama, collecting data on ten white-faced capuchins (Cebus capucicus) (four adult males/six adult females). Over 215 contact hours were spent with the monkeys, and a total of 213 carries were recorded. No hand preference bias at the population level was found for the carry task; and no detectable hand-use patterns for carry were correlated with the weight of the object carried (except a right-hand bias for carrying medium-sized objects), the plane of the monkey's movement, its locomotor pattern, or its height above the ground. Therefore, the results of this study do not support the hypothesis that the need for postural regulation while carrying an object influences hand-use patterns in free-ranging capuchins. Our results are especially important because they are contrary to the results of the only other free-ranging capuchin laterality study conducted to date (Panger, 1998).     

Hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella)

The purpose of this study was to examine the hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella). Two experiments were conducted. In Experiment 1 capuchins were presented with an apparatus designed to accommodate the use of probing tools. In Experiment 2 the same capuchins were presented with sets of nesting containers. Five of the ten subjects used probing tools and seven subjects placed objects in the containers. The capuchins' behavior reflected three hierarchically organized combinatorial patterns displayed by chimpanzees and human infants. Although the capuchins sometimes displayed the two more complex patterns (“pot” and “subassembly”), their combinatorial behavior was dominated by the simplest pattern (“pairing”). In this regard capuchins may not attain the same grammar of manipulative action that has been reported for chimpanzees and young human children. © 1994 Wiley-Liss, Inc.     

Study of intellectual activity at recognition of numerical multitudes of two-dimensional and three-dimensional stimuli of different color in lower monkeys

The capability of monkeys for recognition and comparison by identity of two-dimensional images and three-dimensional objects of different color and number (from 1 to 5) was studied at solution of tasks of the “selection by sample” type. The study was carried out on two species of the lower monkeys of different levels of phylogenetic development: rhesus macaques (Macaca mulatta) and brown capuchins (Cebus apella). Representatives of the studied monkey species were established to able to differentiate two-dimensional stimuli (images of squares) and three-dimensional stimuli (objects of rounded shape) of red, yellow, and green color in different quantitative ratios (from 1 to 5) by selecting identical signs when solving modifications of the “selection by sample” tasks. The obtained data indicate the presence in primates of numerical notion and their ability to differentiate objects in the number from 1 to 5 regardless of the color of these objects. Speciesspecific differences in monkeys were revealed; rhesus macaques, as compared with capuchins, experienced difficulties at solution of complex combinatory tasks. The obtained experimental results give grounds to believe the presence in the lower monkeys the notion “quantity” as well as of the sufficiently high level of pre-verbal thinking.     

Transport of tools and mental representation: is capuchin monkey tool behaviour a useful model of Plio-Pleistocene hominid technology?

Capuchin monkeys display greatly developed tool-using capacities, performing successfully a variety of tool-tasks. Impressed by their achievements in this respect, some investigators have suggested that capuchin tool-using behaviour could be used as a model of the tool behaviour of the first hominids. The transport of tools, a task requiring complex cognitive capabilities, is an essential ingredient in the technological behaviour of the first hominids. In this way, to qualify as another source for modelling hominid behavioural evolution, capuchins had to exhibit proficiency in the transport of tools. We investigated this problem through experiments designed to elicit the transport of objects. The results showed that the monkeys were able to transport food to be processed with the use of tools, but failed when the tools themselves had to be transported. Our hypothesis is that a limited capacity for abstract representation, together with the lack of a regulatory system ensuring that the food would not be lost and consumed by another individual during the search for and transport of the tools, were responsible for such a failure. We conclude that the tool-using behaviour of capuchins presents no functional analogy with the tool behaviour of the Plio-Pleistocene hominids, and that capuchin monkeys are a very inadequate source for modelling Plio-Pleistocene hominid's technological behaviour.     

Compound grips in tufted capuchin monkeys (Sapajus spp and Sapajus libidinosus)

An experimental study with captive individuals and study of video recordings of wild monkeys explored whether and how tufted capuchin monkeys use onehand to hold one or more objects with multiple grips (compound grips). A task designed to elicit compound grip was presented to five captive tufted capuchin monkeys (Sapajus spp). The monkeys held one to four balls in onehand and dropped the balls individually into a vertical tube. Multiple simple grips and independent digit movements enabled separate control of multiple objects in one hand. Monkeys always supported the wrist on the horizontal edge of the tube before releasing the ball. Increasing the number of balls decreased the likelihood that the monkeys managed the task. Wild bearded capuchins (Sapajus libidinosus) used compound grips spontaneously to store multiple food items. Compound grips have been described in macaques, gorillas, chimpanzees, and humans, and now in a New World primate. We predict that any primate species that exhibits precision grips and independent digit movement can perform compound grips. Our findings suggest many aspects of compound grip that await investigation.     

Tool use in Cebus

This paper summarizes early anecdotal information and systematic studies of tool use in capuchin monkeys (Cebus spp.). Tool use in capuchins is neither context specific nor stereotyped. The success of capuchins in using tools and in exploiting a variety of food resources in the wild derives from several factors: their manipulative abilities, interest in external objects and a tendency to explore the environment. In using tools, capuchins are similar to apes and more proficient than other monkey species. A cognitive approach indicates, however, that (in contrast with chimpanzees) they never develop an understanding of the requirements of the tool tasks presented.     

Peculiarities of recognition and comparison by size of two-dimensional images and three-dimensional objects of different colors in the lower monkeys

The ability of monkeys to recognize and compare two-dimensional images and three-dimensional objects of different colors by size was studied. The study was carried out on two species of monkey of different level of phylogenetic development: rhesus macaques (Macaca mulatta) and brown capuchin (Cebus apella). The monkeys were established to be able to recognize and to compare by size the two-dimensional pictures and three-dimensional objects of red, yellow, and green colors with identification of the relative sign “more.” Solution of visual tasks of the “more-less” type was achieved at any combination of stimuli regardless of color. The age-and specie-related differences were revealed during the course of training. In all monkeys the “transfer of learning” and formation of generalization were traced. This indicates a sufficiently well developed level of elementary thinking in the lower monkeys.     

Study of capability for recognition of complex visual stimuli of different quantities in the lower monkeys

Capability of monkeys for identification of quantitative signs has been studied at recognition and comparison of two-and three-dimensional objects in quantities from 1 to 8. The work was carried out on two species of the lower monkeys: rhesus macaque (Macaca mulatto) and brown capuchins (Cebus apella). The studied representatives of the monkeys have been established to be able to differentiate planar images and casts of cherries in various quantity combinations from 1 to 8 and to identify identical signs of visual stimuli. The obtained data indicate the ability of monkeys to abstract and to form preverbal notions of quantitative signs of objects.     

Use of a tool-set by capuchin monkeys (Cebus apella)

The purpose of this study was to examine the use of a tool-set by capuchin monkeys (Cebus apella). Capuchins were presented with an apparatus designed to accommodate the use of pounding tools to crack walnuts and the use of probing tools to loosen and extract the inner meat. Three capuchins used stones and sticks sequentially for these purposes. The capuchins' behavior was similar in form and function to behavior that has been reported for chimpanzees in analogous situations. These results provide further evidence of the extensive tool-using capabilities of capuchin monkeys and are consistent with a hypothesis of cross-species continuity in the skillful use of tools by primates.     

Aimed throwing of stones by tufted capuchin monkeys (Cebus apella)

The purpose of this research was to examine aimed throwing of stones by tufted capuchin monkeys (Cebus apella). Three capuchins (two adults and one juvenile) threw stones at a stationary target located outside their home cages. The monkeys subsequently discriminated between stationary targets and threw stones at a moving target. Each subject exhibited a distinct manual and postural throwing preference. These results demonstrate that capuchins have throwing capabilities which are thought to have been associated with early hominid evolution.     

Distribution of potential suitable hammers and transport of hammer tools and nuts by wild capuchin monkeys

Selection and transport of objects to use as tools at a distant site are considered to reflect planning. Ancestral humans transported tools and tool-making materials as well as food items. Wild chimpanzees also transport selected hammer tools and nuts to anvil sites. To date, we had no other examples of selection and transport of stone tools among wild nonhuman primates. Wild bearded capuchins (Cebus libidinosus) in Boa Vista (Piauí, Brazil) routinely crack open palm nuts and other physically well-protected foods on level surfaces (anvils) using stones (hammers) as percussive tools. Here we present indirect evidence, obtained by a transect census, that stones suitable for use as hammers are rare (study 1) and behavioral evidence of hammer transport by twelve capuchins (study 2). To crack palm nuts, adults transported heavier and harder stones than to crack other less resistant food items. These findings show that wild capuchin monkeys selectively transport stones of appropriate size and hardness to use as hammers, thus exhibiting, like chimpanzees and humans, planning in tool-use activities.     

Picture perception in monkeys and pigeons: Transfer of rightside-up versus upside-down discrimination of photographic objects across conceptual categories

Monkeys and pigeons were trained to discriminate between normally oriented full frontal pictures of humans and upside-down reversals of the same pictures as stimuli. Monkeys displayed a high level of transfer to the new pictures of full frontal and rear views of humans and silhouettes, but failed to transfer to the close-up and far human faces. Pigeons showed poorer transfer to the silhouettes and higher transfer to the far human faces than did monkeys. Further transfer tests were performed with non-human pictures, including monkeys, birds, mammals, and man-made objects. Pigeons failed to transfer to the non-human pictures. This indicates that the pigeons had learned to classify the pictures based on some concrete features specific to the humans and that the transfer to the new versions of human pictures could be explained by simple stimulus generalization based on perceptual similarity. Two out of four monkeys did transfer fairly well to the non-human pictures, except for the man-made objects. High levels of transfer to the non-human natural pictures suggested that the monkeys classified the pictures on the basis of the orientation of objects represented by the pictorial displays. A preliminary report was presented by the first author (M. J.) at the 13th Congress of the International Primatological Society, Nagoya, Japan, 1990. The present research was supported in part by a Grant-in-Aid for General Scientific Research, the Ministry of Education, Science, and Culture, No. 02301017 (principal researcher:Tadasu Oyama, Nihon University) to M. J. The monkey experiments were conducted at the Primate Research Institute, Kyoto University, and the pigeon experiments at the Department of Psychology, Chiba University.     

Whole-Body Prepulse Inhibition Protocol to Test Sensorymotor Gating Mechanisms in Monkeys

Prepulse inhibition (PPI) is the decrease of startle reflex amplitude when a slight stimulus is previously generated. This paradigm may provide valuable information about sensorimotor gating functionality. Here we aimed at determining the inhibited and uninhibited startle response of capuchin monkeys (Sapajus spp.), and to evaluate the role of the superior colliculus in PPI. Capuchin monkeys were tested in a whole-body protocol, to determine the best startle amplitude and interstimuli interval. Additionally we tested two subjects with bilateral superior colliculus damage in this protocol. Results show that 115 dB auditory pulse has induced the best startle response. In contrast to reports in other species, no habituation to the auditory stimuli was observed here in capuchins. Also, startle reflex inhibition was optimal after 120 msec interstimuli interval. Finally, there was a downward tendency of percentage inhibition in superior colliculus-lesioned monkeys. Our data provides the possibility of further studies with whole-body protocol in capuchin monkeys and reinforces the importance of the superior colliculus in PPI.     

Response Toward Novel Foods and Novel Objects in Wild Cebus apella

Animals respond to novel stimuli via explorative or neophobic behavior or both. The coexistence of these responses toward novel foods may be a successful adaptive strategy for a generalist species such as Cebus apella, because it allows the gradual introduction of new foods into the diet and reduces the risk of poisoning by ingestion of large amounts of toxic compounds (Glander, 1982; Milton, 1993; Visalberghi, 1994). Neophobia has been studied mostly in captivity. We investigated responsiveness to novelty in a group of 25–30 wild tufted capuchins (Cebus apella) in Iguazü National Park (Argentina). They had been habituated to visiting sites where bananas were provided on three elevated platforms. We presented novel stimuli on an adjacent platform. There were 4 experimental conditions with 10 sessions each: the Novel Food condition, the Novel Object condition, the Control condition, in which the platform was empty, and the Banana condition. In the Novel Food and Novel Object conditions, a new stimulus—food or object—was on the platform during each session. The Banana condition provided information on capuchin response to a familiar preferred food. Overall, capuchins were less responsive toward novel objects than toward novel foods; however, although cautious, they ate small amounts of the novel foods. Age affected individual responsiveness toward novel foods, whereas sex affected responsiveness toward novel objects. Capuchins ignored the empty platform. Our findings are in agreement with the idea that tufted capuchins can adapt to new habitats by gradually exploiting new food sources.