Tool use inCebus apella: A case study

The case of a captive Cebus apella,capable of utilizing detached objects as true hammering tools in cracking nuts open, is investigated. In the experimental task administered, the monkey was offered nuts of two different sizes, hazelnuts and walnuts, and a choice among three “hammers” of different percussional efficacy. Its performance was compared to that of one of its cagemates that did not use tools and to its own performance in the absence of tools. Results show that there was a consistent choice of the most efficient tool, that tool use greatly reduces the amount of time needed to crack a nut open (in comparison with either the action of the teeth or pounding the nut against a hard substrate), and that the efficacy of tool use is not conditioned by the relative hardness or size of the nut. In the light of these results, the role of tool use in the exploitation of food resouces is discussed.     

Food-exchange with humans in brown capuchin monkeys

To assess how brown capuchin monkeys (Cebus apella) delay gratification and maximize payoff, we carried out four experiments in which six subjects could exchange food pieces with a human experimenter. The pieces differed either in quality or quantity. In qualitative exchanges, all subjects gave a piece of food to receive another of higher value. When the difference of value between the rewards to be returned and those expected was higher, subjects performed better. Only two subjects refrained from nibbling the piece of food before returning it. All subjects performed two or three qualitative exchanges in succession to obtain a given reward. In quantitative exchanges, three subjects returned a food item to obtain a bigger one, but two of them nibbled the item before returning it. Individual differences were marked. Subjects had some difficulties when the food to be returned was similar or equal in quality to that expected.     

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.     

Tool use in wild capuchin monkeys (Cebus albifrons trinitatis)

White-fronted capuchins were observed to use leaves as cups to retrieve water from tree cavities. On multiple occasions several individuals performed this behavior. Thus, these capuchins engage in habitual tool use, as defined by McGrew's classificatory scheme of tool using behavior. Am. J. Primatol. 46:259–261, 1998. © 1998 Wiley-Liss, Inc.     

Picture processing in tufted capuchin monkeys (Cebus apella)

Although pictures are frequently used in place of real objects to investigate various aspects of cognition in different non-human species, there is little evidence that animals treat pictorial stimuli as representations of the real objects. In the present study, we carried out four experiments designed to assess picture processing in tufted capuchin monkeys (Cebus apella), using a simultaneous Matching-to-Sample (MTS) task. The results of the first three experiments indicate that capuchins are able to match objects with their colour photographs and vice versa, and that object-picture matching in this New World monkey species is not due to picture-object confusion. The results of the fourth experiment show that capuchins are able to recognize objects in their pictures with a high level of accuracy even when less realistic images, such as black-and-white photographs, silhouettes and line drawings, are employed as bi-dimensional stimuli. Overall, these findings indicate that capuchin monkeys are able to establish a correspondence between the real objects and their pictorial representations.     

Responses of capuchin monkeys (Cebus apella) to different conditions of mirror-image stimulation

Group-living brown capuchins were given mirror-image stimulation as follows: (1) mirror 1 m away; (2) mirror attached to the cage-mesh; (3) angled mirrors creating a deflected image; (4) small mirror in the cage; and (5) small, transportable mirrors. The subjects were initially interested in the mirrors in each condition, but they generally habituated to them over the course of repeated presentations. Control (non-reflective) objects were attended to less than mirrors. Facial expressions occurred mostly in Condition 2, lateral and vertical head movements in Condition 3, reaching behind the mirror in Condition 2, looking obliquely into the mirror in Conditions 4 and 5. Despite these diverse conditions of exposure to mirrors, lasting for a total of over three months, no behaviours suggesting self-recognition were seen in the monkeys.     

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.     

Sex differences in play behavior in juvenile tufted capuchin monkeys (Cebus apella)

According to the motor training hypothesis, play behavior in juvenile primates improves motor skills that are required in later adult life. Sex differences in juvenile play behavior can therefore be expected when adult animals assume distinct sexually dimorphic roles. Tufted capuchin monkeys show sexually dimorphic levels of physical antagonism in both inter- and intra-group encounters. Accordingly, it can be predicted that juvenile capuchins also show sex differences in social play behavior. To test this hypothesis, the play behavior of nine juvenile and two infant capuchins was examined. As predicted, juvenile males showed significantly higher levels of social play (wrestle, chase) than juvenile females, but no differences were found in nonsocial play (arboreal, object). Levels of infant play behavior were comparable to that of juveniles. These results lend support to the motor training hypothesis and highlight the need for more detailed investigations of individual differences in play behavior. An erratum to this article can be found at     

Response to novel housing in two groups of captive tufted capuchin monkeys (Cebus apella)

The influence of age, maternal status, and the presence of a group male on use of space was assessed in two groups of captive tufted capuchin monkeys that underwent a move from indoor housing to a larger outdoor facility. Both groups originally contained two adult males, but only one group retained a male after the move. Following the move, mothers spent less time on the ground when carrying their infants than they did when not carrying their infants. In the group with no male (1) individuals decreased time spent on the ground relative to pre-move levels, whereas no such difference was noted in the group with the male; (2) females spent more time carrying their infants than did females in the group with a male. In the group with the adult male, juveniles spent less time on the ground than did non-mother adult females, whereas no difference had existed prior to the move. Grooming rates dropped from pre-move to post-move, but the mean number of partners with which each animal was in contact increased. Measures of social behavior varied across post-move observation periods inversely to time spent on the ground. These results are consistent with the view that an individual's relative vulnerability influences behavioral conservatism in novel environments, and suggests a relatively profound role for males in promoting exploration of new space in this species.     

Olfactory discrimination of eight food flavors in the capuchin monkey (Cebus apella): Comparison between fruity and fishy odors

Operant conditioning was used to investigate how primates discriminate between odor qualities. Eight artificial food flavors, selected from either a “Fishy” or “Aroma/Fruity” category, were used. During the presence of one of the two odors S+ or S−, the monkey was reinforced by pushing a response key when S + was presented. The tufted capuchins discriminated most accurately when both odors were Aroma. Discrimination was more accurate when S+ was Fruity odor and S− was Fishy odor. When both odors were Fishy, discrimination could not be acquired in 20 sessions. All of the flavors used, except apple, were novel for the subjects, which suggests that capuchins can innately discriminate among them. The data also suggest that Aroma odors are more salient than Fishy odors. The results also suggested an innate aversion to Fishy odors.     

Social influence in manipulations of a capuchin monkey raised in a human environment: A preliminary case study

This preliminary study reports manipulations in an 8-month infant capuchin monkey,Cebus apella, confronted with a variety of objects, during five 2-hour sessions. This subject is raised in a human environment as it participates to the “Aide Simienne aux Personnes Handicapées (Kerpape)” project. Objects have been chosen in order to expose the capuchin to manipulations it will be asked to perform when placed with a quadriplegic. This paper reports the analysis of five hours of video recording. During two sub-sessions within an experimental session, the “human mother” pointed the objects to the monkey, sequentially, either with a vocal designation or not. The results show that the monkey tends to contact more objects and manipulates them more when they have been previously designated by the “mother.” This suggests a form of social facilitation. There is no evidence for imitation.     

Tool use and predation of oysters (Crassostrea rhizophorae) by the tufted capuchin,Cebus apella appella,in brackish water mangrove swamp

Cebus apella apella is considered to be omnivorous, manipulative and exploiter. A case of oyster predation is reported from an individual of a population inhabiting mangrove swamps in the village of Canelatiua, Maranhão, Brazil. It is suggested that this behavioural adaptability on mangrove resources is a key factor in the success of the species in this ecosystem.     

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.     

Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella)

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.     

Reproductive parameters of a captive colony of capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) from 1984 to 2006

This paper presents the results of a demographic analysis of 22 years of data recorded on a colony of tufted capuchin monkeys (Cebus apella) in captivity at the CNR Primate Centre (Rome, Italy). Information is provided on reproduction, sex ratio, inter-birth interval (IBI), seasonality, and body weight. From 1984 to 2006, 46 live births were recorded. There were births in almost all months of the year, but a higher frequency was observed during spring and summer (71.1%). The sex ratio was 1:1 M:F for newborns and 1:1.06 M:F for surviving offspring. At birth, infants’ average weight was 238.13 ± 37.51 g, i.e. 250 ± 56.79 g for males and 231 ± 26.08 g for females. Age at first birth for females ranged from 4.9 to 7 years (n = 9), while males achieved first paternity between the ages of 5 and 9.2 years (n = 6). Only one pair of twins was recorded during this period. For females, the mean IBI was 17.88 ± 1.84 months, when they reared infants, and 12.70 ± 1.73 months, when they did not rear offspring. Infant mortality within the first 2 months was 28.3%.     

The use of probing tools by tufted capuchins (cebus apella): evidence for increased right-hand preference with age

We examined hand preference in the use of tools by tufted capuchins (Cebus apella). We presented a colony of monkeys with an enclosed container designed to accommodate the use of probing tools. Over an 8-month period, 13 monkeys used probes to extract sweet syrup from the narrow opening of the apparatus. Five monkeys exhibited bias toward use of their right hand and eight monkeys exhibited bias toward use of their left hand. Adult monkeys exhibited a greater percentage of right-hand preferent probing sequences than did juveniles. These results are consistent with hypotheses that in tasks that involve the use of tools, nonhuman primates exhibit strong lateral asymmetries at the individual level, a moderate left-hand bias at the population level, and increased bias with age toward use of the right hand.     

A multi-task assessment of hand lateralization in capuchin monkeys (Cebus apella)

Eight tasks were presented to ten tufted capuchin monkeys and hand preferences were recorded for each subject on each task. The strength of hand preferences varied accross tasks. Although no significant population-level left- or right-hand bias emerged for any of the tasks, there was a tendency toward greater left-hand use in a task requiring the use of probing tools. The data also confirm that simple reaching is of limited value as a measure of hand preference. Hand preferences in capuchin monkeys appear to be determined by a number of individual, species, and environmental factors.     

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.     

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.     

Salivary progesterone for the assessment of the ovarian function in the capuchin monkey (Cebus apella)

Salivary and plasma progesterone were measured in normally cycling (n=10) and castrated (n=4) femaleCebus monkeys (Cebus apella). During the follicular phase, progesterone levels in saliva ranged between 0.05 and 1.40 ng/ml and in the luteal phase they increased to between 0.22 and 4.70 ng/ml. These values represented on average 6.5 and 3.2% of those values measured in plasma, for the follicular and luteal phases, respectively. The regression analysis of the steroid concentrations in both fluids showed a highly significant correlation (r=0.8985,n=180,P<0.0001). Ovariectomized monkeys had consistently low salivary (0.37±0.02 ng/ml) and plasma (4.70±0.25 ng/ml) progesterone, showing a low, but significnat, correlation coefficient (r=0.2592,n=58,P=0.047). The ratio of plasma/salivary progesterone was significantly higher in the luteal phase (31.09±1.65) than in the follicular phase (23.06±2.26) and in castrated monkeys (16.00±1.38). The free fraction of progesterone constituted 5.3±0.2% of the total plasma progesterone during the follicular phase and 3.3±0.1% during the luteal phase. Ovariectomized monkeys showed a significantly higher percentage of free progesterone in plasma (7.7±0.1%). In contrast, free progesterone made up 64.4 and 70.9% of the total salivary progesterone for the follicular and luteal phases, respectively. The proportion of free progesterone in castrated animals was within the range observed in cycling animals. We suggest that the levels of progesterone in the saliva of capuchin monkey follow a pattern similar to that for plasma progesterone, reflecting the free steroid fraction. Thus, the measurement of such steroid in saliva may offer a valuable alternative to plasma determinations for the assessment of the ovarian function inCebus and probably other New World monkey species.