Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

Transfer index and mediational learning in tufted capuchins (Cebus apella)

The transfer index (TI) is a discrimination reversal paradigm that requires the achievement of a given prereversal criterion of accuracy. The mediational learning (ML) paradigm is a modification of the TI procedure that features the presentation of three different reversal conditions designed to assess whether prereversal learning is based on purely associative processes or mediated by the use of a strategy (win-stay/lose-shift). These two paradigms have been used with apes and several Old World monkey species, proving to be effective tools for the comparison of species on the basis of their transfer abilities and the nature of their learning processes. However, among New World monkeys, only the squirrel monkey has been tested. Capuchin (Cebusspp.) adaptability and their mastery in using tools have led to controversial interpretations of their cognitive and learning skills. We evaluated their mode of learning and the transfer of learning using the TI and the ML paradigms. We tested four tufted capuchins (Cebus apella)in a WGTA using a variety of stimulus object pairs. The results show that they possess rather good transfer abilities and one subject showed an associative learning mode. None of the subjects showed evidence of learning mediated by a win-stay/lose-shift strategy.     

Development of activity patterns,social interactions,and exploratory behavior in infant tufted capuchins (Cebus apella)

Early organization of activity states was studied in 17 tufted capuchin (Cebus apella) infants from birth to 11 weeks of age. Development of exploration and interactions with mothers and other group members were studied in 14 of these infants up to the age of 1 year. Activity profiles changed from 3 to 8 weeks as infants began to move off mothers and explore their environments. From 2 to 6 months time with mothers decreased; time alone increased correspondingly. Time spent with other group members did not vary significantly over the first year. By 7–9 months capuchin infants spent more time alone or with other group members than with mothers, although weaning was still not completed by the end of the first year. Simple environmental exploration began in the 2nd month and reached stable levels by 4 months. Complex manipulation of food and objects first began at 3–4 months and increased to stable levels in the second half of the first year. Some preliminary differences were evident between infants living in indoor cages and those living in indoor/ outdoor runs. Infants in cages spent less time in dorsal contact with mothers, and less time in social play and proximity to other animals than those in runs. Instead, infants in cages spent more time alone and engaged in more manipulation of food. Some measures of social and exploratory behavior showed a high degree of variability which may be useful in exploring individual differences in infant temperament or reactivity. © 1995 Wiley-Liss, Inc.     

Male reunion displays in tufted capuchin monkeys (Cebus apella)

When males in captive tufted capuchin monkey (Cebus apella) groups separate and come together within their group, they have been observed to embrace and vocalize upon reunion. This display has not been observed in any other age/sex class. To investigate this, we deliberately separated six animals, including the only two adult males, from each of two social groups. We hypothesized that only the adult males would embrace upon reintroduction. When two males were consecutively reintroduced to their group, they typically ran to each other and came together in a frontal embrace, emitting stereotyped vocalizations. No other combination of animals showed this “reunion display.” Though dramatic, this behavior was in no way associated with incidents of aggression. We argue affiliative bonds may exist in these tufted capuchin male dyads. © 1996 Wiley-Liss, Inc.     

The stone tools of capuchins (Cebus apella)

We examined the production of stone took by capuchins (Cebus apella). Eleven subjects used five reduction techniques to produce 346 stone tools (48 cores and 298 flakes). They produced a sharp edge on 83% of the cores and largest flakes. Three monkeys later used a sample of these objects as cutting tools. These results demonstrate that monkeys produce lithic tools analogous to those produced by Oldowan hominids.     

Introduction and integration of strangers into captive groups of tufted capuchins (Cebus apella)

We introduced two to four unfamiliar animals into three established groups (N = 6–9 per group) of tufted capuchins (Cebus apella).We present findings on the behavioral consequences of introductions as a function of age, sex, and residency status and long-term consequences for health and reproduction. No morbidity from aggression occurred at the time of introductions or during several months following, and reproduction was not compromised. Activity budgets and patterns of social spacing and interaction were little changed following the introductions except for increases in vigilance behavior, especially by newly introduced adult females. Adult females exhibited the strongest and longest-lasting response to changes in group composition. The results indicate that in this species (1) introductions of adult females can be carried out with acceptable risk to the newcomers provided that careful monitoring occurs, so that the onset of severe aggression instigated by resident females toward new females can be avoided, (2) juveniles can be introduced with minimal risk, and (3) adult males can be introduced into groups lacking resident adult males with minimal risk. Capuchins differ in important ways from the better-studied Old World monkeys in their response to introductions of strangers. The differences are instructive with regard to processes supporting species-typical social structure, which is less overtly hierarchical in capuchins than in macaques.     

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.     

Chromosome studies of Cebus apella: The standard karyotype of Cebus apella paraguayanus,Fischer, 1829

Chromosome studies were performed on 40 specimens identified as Cebus apella paraguayanus, Fischer, 1829, which had been wild-caught in Santa Catalina (Republic of Paraguay). Elongated chromosome spreads obtained from lymphocyte cultures were sequentially stained with different techniques, and a constant pattern of 382 bands was identified in all specimens. A standard karyotype based on the measurements of the total chromosome length and the G-Q banding pattern is proposed.     

Semifree-ranging Tufted Capuchins (Cebus apella) Spontaneously Use Tools to Crack Open Nuts

Naturalistic studies on tool use by nonhuman primates have focused almost exclusively on Old World monkeys or hominoids. We studied the cracking of Syagrus nuts with the aid of stones by a group of semifree-ranging capuchins living in a reforested area (Tietê Ecological Park, São Paulo, Brazil). Our data are from direct observation and from mapping nut-cracking site utilization. All adults, subadults and juveniles (plus one infant) crack nuts, but individual differences in frequency and proficiency are marked. Juveniles do most of the nut-cracking, but adults are, on average, more efficient; the frequency of inept stone manipulation decreases with age. About 10% of the nut-cracking episodes were watched by other individuals—mostly infants and juveniles, suggesting a role for observational learning, even if restricted to stimulus enhancement.     

Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella)

The aim of this study was to evaluate simple behavioral enrichment procedures for a captive group of tufted capuchin monkeys (Cebus apella). We examined the effects of providing a manipulatable substrate (straw) and a variety of portable objects in the monkeys' home cage. The animals were observed across three conditions in two replications: 1) No portable objects were present; 2) a set of six identical portable objects was present; and 3) a set of six varied portable objects was present. The cage floor was bare in the first replication; straw was uniformly spread on the cage floor in the second replication. An 18-month period of qualitative note taking followed completion of the initial data collection phase. The presence of straw and portable objects affected patterns of affiliation by decreasing quiet contact and close proximity. Providing additional manipulative opportunities affected both the form and frequency of object-directed activities. Object contacts were directed toward a greater variety of targets, and some objects were spontaneously used as tools. Manipulation of provided objects and use of objects as tools have become routine activities in this group of monkeys. We conclude that providing straw and portable objects in an already well equipped cage is an effective means of long-term behavioral enrichment for captive capuchin monkeys. Enabling captive capuchins to express species-typical manipulative tendencies is apparently conducive to the monkeys' optimal physical and psychological well-being as well as interesting to the human observer.     

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

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

Pestle use and modification by tufted capuchins (Cebus apella)

We examined the use and modification of pestles by tufted capuchins (Cebus apella). In each of two experiments we presented 18 subjects with an apparatus that held sugarcane along with materials that the animals could use as tools. In Experiment 1 we presented the subjects with sticks, and in Experiment 2 we presented them with sticks, stones, paper towels, and food biscuits. Seven subjects used sticks as pestles to break down fiber to and squeeze sap from sugarcane in Experiment 1. Five of them modified sticks for this purpose. In Experiment 2, 10 animals used pestles and sponges, combined tools, and used pestles to mix together different kinds of food. These results provide further evidence of functional convergence for the use and modification of tools byCebus andPan and are consistent with the view that extractive foraging is associated with the tool-using and toolmaking behavior of primates.     

Reproductive Socioecology of Tufted Capuchins (Cebus apella nigritus) in Northeastern Argentina

We describe the reproductive parameters of tufted capuchins (Cebus apella nigritus) in the Iguazú National Park, NE Argentina. We obtained data on six different groups (33 individually recognized adult females) studied for periods of 2–9 years. Estimated birthrate is 0.59 infants per female per year in unprovisioned groups. A group that was provisioned for 6 years during the winter period of low fruit availability (May–August), showed a similar birth rate of 0.61, but a lower infant mortality rate than unprovisioned groups. The birthrate estimated for this population is higher than the one reported for white-faced and wedge-capped capuchins. The mean interbirth interval is 19.35 months, but a female can have infants in successive years, even when her previous infant has survived. The modal age at first delivery is 7 years, which is similar to the one observed in wedge-capped capuchins. When young adult females come into estrous they avoid copulating with the alpha male that sired them, thus providing evidence for a behavioral mechanism of inbreeding avoidance. Births are very seasonal at Iguazú, occurring during the spring and summer months (October–February) when food availability is at its peak. Tufted capuchins at Iguazú are more seasonal breeders than other capuchin populations, probably as a result of their more seasonal environment. The secondary sex ratio does not deviate significantly from 1:1, despite the known ability of capuchins to adjust secondary sex ratio to local conditions.     

Development of maze navigation by tufted capuchins (Cebus apella)

Theories of spatial navigation hypothesize that animals use vector or topological information to choose routes, often including detours, to move objects or themselves to goals. We assessed adult capuchin monkeys’ (Cebus apella) navigation through 192 virtual two-dimensional mazes that incorporated detour problems. Six monkeys initially were significantly less likely to choose the correct paths when detours were required than when not. Three of the six monkeys repeatedly practiced the 192 mazes to asymptotic mastery; the other three did not practice the mazes again. In a subsequent transfer test, each monkey made correct choices equivalently often on familiar and novel mazes, which suggests that they used general planning skills for maze navigation. Of the three monkeys that practiced the 192 maze-set repeatedly, one efficiently detoured and the other two significantly improved detouring compared to their initial performance. Two monkeys, contrary to their performance when completing the 192 maze-set for the first time, made correct choices at the same rate as chimpanzees. Some evidence suggested that two monkeys used topological information, but utilization of vector information was obvious for all monkeys. Our findings suggest that the boundaries of any individual's navigational abilities are not predicted by species, but depend on experience.     

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

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

Behavioral and cortisol responses to repeated capture and venipuncture in Cebus apella

Eight capuchins were trained in a capture and venipuncture procedure. Samples taken immediately following capture indicated that subjects experienced rising cortisol levels over the first 5 weeks of training followed by a return to baseline (equivalent to day 1 levels) in the sixth and seventh weeks. After 7 weeks, samples taken 60 min after initial capture revealed that behaviorally habituated animals exhibited significantly lower cortisol levels in response to venipuncture as opposed to naive and experienced but nonbehaviorally habituated subjects. © 1996 Wiley-Liss, Inc.     

Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella)

The responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella) were investigated. In both species the amount of fear behavior was higher in the presence of the model than during baseline conditions. Unlike the macaques, in the capuchins the frequency of these behaviors decreased across trials. In the two species the amount of explorative and manipulative behaviors and the use of space were also different. Unlike macaques, all capuchins manipulated the objects available in the testing room, and three subjects contacted the apparatus by using objects. Macaques did not show significant preferences for any particular part of the testing room. In both conditions, capuchins used the floor more than macaques did. Further, capuchins increased the use of the floor across experimental trials. Latency to reach the floor was higher in macaques than in capuchins. When on the floor, capuchins spent most of the time close to the snake apparatus. It is proposed that the behavioral differences between capuchins and macaques in the responses to a potential predator indicate that capuchins have a greater propensity to explore and to contact the novel stimulus directly, or by means of objects, than macaques do. These tendencies may lead to the exploitation of novel features in the environment.