Capuchin monkey (Cebus apella) grips for the use of stone tools

This research examined capuchin monkey (Cebus apella) grips for the use of throwing, nut-cracking, and cutting tools. We provided subjects with stones and apparatus that accommodated the use of stones as tools. Our subjects exhibited five grips, two of which the animals used when force was the primary consideration (power grips) and three of which the animals use when accuracy of sensory judgment and instrumentation was required (precision grips). We believe that the range of contexts in which capuchins use stone tools, combined with the ability of capuchins to employ both power and precision grips as part of their tool repertoire, indicate that Cebus apella can be used to identify grips that facilitated hominid lithic technology. Am J Phys Anthropol 103:131–135, 1997. © 1997 Wiley-Liss, Inc.     

In-Group Conformity Sustains Different Foraging Traditions in Capuchin Monkeys (Cebus apella)

Background

Decades of research have revealed rich cultural repertoires encompassing multiple traditions in wild great apes, a picture crucially complemented by experimental simulations with captive apes. Studies with wild capuchin monkeys, the most encephalized simian species, have indicated a New World convergence on these cultural phenomena, involving multiple traditions and tool use. However, experimental studies to date are in conflict with such findings in concluding that capuchins, like other monkeys, show minimal capacities for social learning.

Methodology/Principal Findings

Here we report a new experimental approach in which the alpha male of each of two groups of capuchins was trained to open an artificial foraging device in a quite different way, using either a slide or lift action, then reunited with his group. In each group a majority of monkeys, 8 of 11 and 13 of 14, subsequently mastered the task. Seventeen of the successful 21 monkeys discovered the alternative action to that seeded in the group, performing it a median of 4 times. Nevertheless, all 21 primarily adopted the technique seeded by their group''s alpha male. Median proportions of slide versus lift were 0.96 for the group seeded with slide versus 0. 01 for the group seeded with lift.

Conclusions/Significance

These results suggest a striking effect of social conformity in learned behavioral techniques, consistent with field reports of capuchin traditions and convergent on the only other species in which such cultural phenomena have been reported, chimpanzees and humans.     

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.     

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.     

Capuchin (Cebus apella) Tool Use in a Captive Naturalistic Environment

Captive tufted capuchins are proficient at both tool use and manufacture. However, their capacity to comprehend cause-effect relationships as they relate to tool use is a subject of debate. An ability to conceptualize task requirements in assessing the appropriateness of potential tools would be essential to efficient tool use in the wild. Observations of tool use among free-ranging populations of Cebus are extremely limited, and the importance of this behavior to capuchin feeding ecology is unclear. I tested tufted capuchins' ability to conceive solutions to a probing task in a naturalistic captive setting. Three out of 5 participants demonstrated an ability to consistently make and use tools selected from a wide variety of natural materials within a forest exhibit. Over 98% (N = 140) of the tools that they modified enabled them to successfully acquire food rewards. It is likely that wild Cebus apella shares this ability, and that tool use occurs under a highly specific set of natural conditions.     

Substrate optimization in nut cracking by capuchin monkeys (Cebus apella)

We conducted an experiment to examine the effect of substrate on the nut-cracking behavior of a group of semicaptive capuchin monkeys. We wanted to determine whether tufted capuchin monkeys were selective in choosing the substrate on which they pound nuts, and whether the choice of substrate affected the outcome. Eight adult females and eight juveniles were provided with nuts in the outdoor facility. We found that 1) all adult females and three young capuchins succeeded in cracking nuts; 2) they preferred the hardest substrates (concrete and stone); 3) there is a link between the substrate and the amount of time needed to crack a nut; 4) most young capuchins used various substrates, some of which were inadequate, in a haphazard manner; and 5) there are different forms of nut cracking. We conclude that adult capuchins choose the hardest substrates, and that these substrates support efficient cracking.     

Determining the Value of Social Companionship to Captive Tufted Capuchin Monkeys (Cebus apella)

In general, guidelines on housing and care of animals in the laboratory state that rats and mice should not be housed in the same room. Mice may perceive rats as predators. Although one theory says this can cause stress, there is little scientific evidence to support this theory. In the wild, rats and mice usually do not share the same microhabitat, but this appears to be true for most small rodent species. Furthermore, reports of predatory behavior of rats toward mice mainly originate from experimental settings using rats with high inbred levels of aggression. This experiment measured heart rate (HR), body temperature (BT), activity (AC), and urinary corticosterone in female C57BL/6 mice before, during, and after introducing Wistar rats into their room. The study found no chronic effects of rat introduction on any parameters. The study concluded that housing rats and mice in the same room is at least less disturbing than cage cleaning, which caused a temporary increase of HR, BT, and AC. Current results do not support legislation based on compromised welfare.     

Determining the Value of Social Companionship to Captive Tufted Capuchin Monkeys (Cebus apella)

This study used a method similar to one introduced by Dawkins in 1990 to assess the magnitude of the psychological need for social companionship in pair-housed tufted capuchin monkeys (Cebus apella). This method permits classification of commodities as necessities or luxuries. The study directly compared the commodity of social companionship to the commodity of food, a known physiological necessity, in a series of preference tests following commodity deprivations. The majority of subjects chose their social companion over food at baseline and persisted in this preference even after several hours of food deprivation. In addition, subjects' preferences shifted from 1 commodity to the other with manipulation of social and food deprivation levels. Capuchin monkeys perceived social companionship as a necessity at a level similar to that of food.     

Social behavior of the wild black-capped Capuchin (Cebus apella)

The author undertook a field survey of the capuchin (Cebus apella) lasting 60 days from December 1976 to January 1977, and determined the basic daily activity of its groups and spacing of group members in the day time. Furthermore, based on studies of various types of interactions between individuals of the groups, he was able to show that (1) decisive rank orders exist both among adults and among sub-adults of both sexes; (2) grooming at the resting time is peculiar to adult males; (3) with quite mild agonistic interactions being maintained, a high tolerance exists between the group members; (4) alpha males represent individuals which can be called leaders of groups; and (5) a strong psychological or spiritual bond exists among the adult males, which can be termed a “male-bond.” Furthermore, according to comparative studies on some adjoining groups, it was found that the group structure is strongly influenced by the individuality or character of the adult males of each group. The present findings are generally in agreement with those forC. apella studied by the author and other researchers in other localities. It can be safely said therefore that these findings are probably common to this species of monkey. Based on a comparison with findings for three other species ofCebus, the author attempts to clarify the points of difference betweenC. apella and these three other species ofCebus from the viewpoint of behavioral science and sociology.     

Social Monitoring Reflects Dominance Relationships in a Small Captive Group of Brown Capuchin Monkeys (Cebus apella)

In several studies of social monitoring in primates, subordinate animals directed more visual attention toward dominant animals than vice versa. This behavior is thought to enable subordinate animals to avoid conflict. We sought to clarify whether visual attention behavior functions in this manner in a small captive group of brown capuchin monkeys, Cebus apella. We tested the hypothesis that social monitoring is related to dominance status. Dominance status was determined based on the directionality of aggressive behavior, and visual attention was quantified by using focal animal sampling. Subordinate animals directed significantly more visual attention toward others than dominant animals. Subordinate animals also looked more frequently at the animals that attacked them and others the most. The results indicate that social monitoring behavior in this captive group was driven by conflict‐avoidance.     

Transfer of tools and food between groups of tufted capuchins (Cebus apella)

This research examined tool and food transfer between two groups of tufted capcuhin monkeys (Cebus apella). Subjects in one group transferred stones to subjects in a second group who in turn used the stones as cutting tools and then transferred food to subjects in the first group. Aspects of the capuchins' behavior are similar to those described for food-sharing in Cebus, cooperative tool use in Papio, and tool and food exchange in Pan. We propose that tool use and food-sharing facilitate tool and food transfer between captive groups of Cebus apella. Am. J. Primatol. 43:33–41, 1997. © 1997 Wiley-Liss, Inc.     

Laterality of Hand Function in Tufted Capuchin Monkeys (Cebus apella): Comparison between Tool Use Actions and Spontaneous Non-tool Actions

This study examined hand preference for tool use and spontaneous non-tool actions in tufted capuchin monkeys (Cebus apella). We noted a lack of lateral bias across measures, and greater strength of hand preference for tool use than for self-directed or feeding activities. Animals that used tools exhibited a population-level right-hand bias for self-touching whereas animals that did not use tools exhibited a lack of lateral bias for this measure. Our findings are consistent with views that hand preference is expressed more strongly for tool use than for non-tool activities, and that lateral bias for self-directed behavior is related to problem-solving skills in primates.     

Give What You Get: Capuchin Monkeys (Cebus apella) and 4-Year-Old Children Pay Forward Positive and Negative Outcomes to Conspecifics

The breadth of human generosity is unparalleled in the natural world, and much research has explored the mechanisms underlying and motivating human prosocial behavior. Recent work has focused on the spread of prosocial behavior within groups through paying-it-forward, a case of human prosociality in which a recipient of generosity pays a good deed forward to a third individual, rather than back to the original source of generosity. While research shows that human adults do indeed pay forward generosity, little is known about the origins of this behavior. Here, we show that both capuchin monkeys (Cebus apella) and 4-year-old children pay forward positive and negative outcomes in an identical testing paradigm. These results suggest that a cognitively simple mechanism present early in phylogeny and ontogeny leads to paying forward positive, as well as negative, outcomes.     

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.     

Failure to induce tumors in the large intestine of Capuchin mokeys (Cebus apella) by using 1,2-dimethylhydrazine

The purpose of this study was to produce tumors in the large intestine of Capuchin Monkeys (Cebus apella) by the administration of the colonotropic carcinogen 1,2-dimethylhydrazine (DMH). The subjects were 12 monkeys, all males, age 30 months, with a mean weight of 2.858 kg. The DMH was administered subcutaneously to six of the monkeys at a dosage of 25 mg/kg of body weight once a week for 16 weeks; control monkeys received an equivalent volume of the stock solution without DMH. Twenty months after administration of the first dose, the animals were sacrificed. None of the monkeys showed intestinal tumors. Samples of the gastrointestinal tract were removed, fixed, and stained according to standard histological techniques. Histological changes were seen in all of the DMH-treated animals; these consisted of glandular hyperplasia and hyperplasia of the epithelium overlying the lymphoid nodules. In addition, foci of dysplasia were found in three of the animals. Our results suggest that the DMH induced pre-neoplastic changes, characterized by hyperplasia and dysplasia, in the mucosa of the large intestine.     

Capuchin monkeys (Sapajus [Cebus] apella) play Nash equilibria in dynamic games,but their decisions are likely not influenced by oxytocin

Comparative approaches to experimental economics have shed light on the evolution of social decision‐making across a range of primate species, including humans. Here we replicate our previous work looking at six pairs of capuchin monkeys' (Sapajus [Cebus] apella) responses to scenarios requiring both coordination (Assurance Game) and anti‐coordination (Hawk‐Dove Game). This then provides a foundation for assessing their responses to two additional games, one with a scenario of beneficial cooperation with a temptation to defect (Prisoner's Dilemma) and one with an environment requiring changing strategies within short temporal proximity (Alternating Economic Game). We additionally explored the effects of exogenous oxytocin on decision‐making. Oxytocin did not affect decisions in any of our games. Results from the first two games largely replicated our previous findings. Responses to the Prisoner's Dilemma were more varied than was seen in previous games, with pairs respectively cooperating, defecting, and failing to establish stable strategies. Such variability indicates that this game may be a good assay for individual differences in social decision‐making. Finally, capuchins were able to flexibly switch between their previously established strategies within each of the different games, even when the games were presented within the same session, requiring strategy adjustments within short temporal proximity. These results build on earlier findings showing that capuchins can alter decision‐making strategies as the context demands, which is likely essential for decision‐making in naturally occurring contexts.     

Acoustic Analysis and Contextual Description of Food-Associated Calls in White-Faced Capuchin Monkeys (Cebus capucinus)

Since early studies of primates that identified vocalizations that attracted others to a food source, the assumed function of food-associated calls has been to inform others of the presence of food. The label food-associated calls and its implied function has led to a focus in research on many species of the costs/benefits for the signaler and recipient of informing others about the presence of food; however, without clearly identifying the calls contextually or acoustically, it is unclear if calls are specific to a feeding context and thus whether calls provide specific information about the presence of food. If calls occur exclusively in the context of feeding, information about individual identity would allow listeners to decide whether or not to approach a calling individual. I conducted acoustic and contextual analyses on food-associated calls in white-faced capuchins. I identified the calls as distinct vocalizations that occur almost exclusively in a feeding context. Discriminant function analyses demonstrate that information about caller sex and identity are encoded in the calls. Therefore, there is the potential for individuals to use acoustic information when responding to food-associated calls; however, playback experiments are necessary to test more explicitly the hypothesis that recipients are able to recognize the calls of specific individuals.     

Effects of upright posture on hand preference for reaching vs. the use of probing tools by tufted capuchins (Cebus apella)

This research examined the effects of task (reaching vs. Tool use) and posture (quadrupedal vs. bipedal) on hand preference in tufted capuchins (Cebus apella). Regarding direction of hand preference, we found a significant main effect of posture, as the bipedal stance elicited greater use of the right hand than did the quadrupedal stance, and a significant posture × task interaction, as bipedal reaching elicited greater use of the right hand than did other postural and task conditions. Further, we found a significant main effect of task on strength of hand preference, as tool use elicited more consistent use of one hand over the other than did reaching. Our findings indicate that bipedal reaching facilitates a mild right-hand bias in intensely manipulative primates. We speculate that this moderate bias may have been pushed in the direction of nearly exclusive right-hand preference in most humans with the development of complex tool use. Am. J. Primatol. 44:147–153, 1998. © 1998 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.     

Female Choice and Mating System of the Brown Capuchin Monkey Cebus apella (Primates: Cebidae)

Antennal drumming, in which Polistes queens rapidly beat the antennae on the rims of nest cells, is described in detail for P. fuscatus and shown to be performed in the context of feeding prey to the larvae. Following the distribution of solid food to the larvae, the queen goes from cell to cell on the nest, drumming her antennae on the cell rims, producing an audible sound. After several min of this, each drum on a cell is followed by contact with a larva, usually the one in the drummed cell, during which the queen regurgitates prey juice to the larva. The average burst of drumming lasts just under one s. The two antennal flagella strike the cell rim together at an average frequency of 29 strokes per s. Similar behavior is documented in 10 other Polistes species. We hypothesize that antennal drumming communicates to the larva that it is about to receive liquid food from the adult and should withhold the release of salivary secretion. This predicts that a larva that has received the drumming signal will exude less secretion than if it has not been recently signaled. An experimental test of this hypothesis yielded the predicted result, and we therefore conclude that our hypothesis is supported.