When and where to practice: social influences on the development of nut-cracking in bearded capuchins (Sapajus libidinosus).

The habitual use of tools by wild capuchin monkeys presents a unique opportunity to study the maintenance and transmission of traditions. Young capuchins spend several years interacting with nuts before cracking them efficiently with stone tools. Using a two-observer method, we quantified the magnitude of the social influences that sustain this long period of practice. During five collection periods (over 26 months), one observer recorded the behavior of 16 immature monkeys, and another observer concurrently recorded behavior of group members in the focal monkey's vicinity. The two-observer method provides a means to quantify distinct social influences. Data show that immatures match the behavior of the adults in time and especially in space. The rate of manipulation of nuts by the immatures quadrupled when others in the group cracked and ate nuts, and immatures were ten times more likely to handle nuts and 40 times more likely to strike a nut with a stone when they themselves were near the anvils. Moreover, immature monkeys were three times more likely to be near an anvil when others were cracking. We suggest a model for social influence on nut-cracking development, based on two related processes: (1) social facilitation from observing group members engaged in nut-cracking, and (2) opportunity for practice provided by the anvils, hammer stones and nut shells available on and around the anvils. Nut-cracking activities by others support learning by drawing immatures to the anvils, where extended practice can take place, and by providing materials for practice at these places.

The fourth dimension of tool use: temporally enduring artefacts aid primates learning to use tools.

All investigated cases of habitual tool use in wild chimpanzees and capuchin monkeys include youngsters encountering durable artefacts, most often in a supportive social context. We propose that enduring artefacts associated with tool use, such as previously used tools, partly processed food items and residual material from previous activity, aid non-human primates to learn to use tools, and to develop expertise in their use, thus contributing to traditional technologies in non-humans. Therefore, social contributions to tool use can be considered as situated in the three dimensions of Euclidean space, and in the fourth dimension of time. This notion expands the contribution of social context to learning a skill beyond the immediate presence of a model nearby. We provide examples supporting this hypothesis from wild bearded capuchin monkeys and chimpanzees, and suggest avenues for future research.

Kinematics and energetics of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piauí, Brazil.

Wild bearded capuchins (Cebus libidinosus, quadrupedal, medium-sized monkeys) crack nuts using large stones. We examined the kinematics and energetics of the nut-cracking action of two adult males and two adult females. From a bipedal stance, the monkeys raised a heavy hammer stone (1.46 and 1.32 kg, from 33 to 77% of their body weight) to an average height of 0.33 m, 60% of body length. Then, they rapidly lowered the stone by flexing the lower extremities and the trunk until the stone contacted the nut. A hit consisting of an upward phase and a downward phase averaged 0.74 s in duration. The upward phase lasted 69% of hit duration. All subjects added discernable energy to the stone in the downward phase. The monkeys exhibited individualized kinematic strategies, similar to those of human weight lifters. Capuchins illustrate that human-like bipedal stance and large body size are unnecessary to break tough objects from a bipedal position. The phenomenon of bipedal nut-cracking by capuchins provides a new comparative reference point for discussions of percussive tool use and bipedality in primates.

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus).

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.

Characteristics of hammer stones and anvils used by wild bearded capuchin monkeys (Cebus libidinosus) to crack open palm nuts.

Capuchins living in Boa Vista (Piauì, Brazil) crack open hard palm nuts on hard, level surfaces (anvils) using stones (hammers) as percussive tools. This activity leaves diagnostic physical remains: distinctive shallow depressions (pits) on the surface of the anvil, cracked shells, and stone hammers on the anvil. To initiate comparison of percussive stone tool use and interpretation of the artifacts it produces across capuchins, chimpanzees, and hominins, we describe a sample of the anvils and hammer stones used by capuchin monkeys at our site. Anvils (boulders and logs) were located predominantly in the transition zone between the flat open woodland and ridges, in locations that offered some overhead coverage, and with a tree nearby, but not necessarily near palm trees. Anvils contained shallow, hemispherical pits with smooth interiors. Hammers represent a diverse assemblage of ancient rocks that are much harder than the prevailing sedimentary rock out of which they eroded. Hard stones large enough to serve as hammers were more abundant on the anvils than in the surrounding area, indicating that capuchins transport them to the anvils. Capuchins use hammers weighing on average more than 1 kg, a weight that is equivalent to 25-40% of the average body weight for adult males and females. Our findings indicate that capuchins select stones to use as hammers and transport stones and nuts to anvil sites. Wild capuchins provide a new reference point for interpreting early percussive stone tool use in hominins, and a point of comparison with chimpanzees cracking nuts.

Socially biased learning in monkeys.

We review socially biased learning about food and problem solving in monkeys, relying especially on studies with tufted capuchin monkeys (Cebus apella) and callitrichid monkeys. Capuchin monkeys most effectively learn to solve a new problem when they can act jointly with an experienced partner in a socially tolerant setting and when the problem can be solved by direct action on an object or substrate, but they do not learn by imitation. Capuchin monkeys are motivated to eat foods, whether familiar or novel, when they are with others that are eating, regardless of what the others are eating. Thus, social bias in learning about foods is indirect and mediated by facilitation of feeding. In most respects, social biases in learning are similar in capuchins and callitrichids, except that callitrichids provide more specific behavioral cues to others about the availability and palatability of foods. Callitrichids generally are more tolerant toward group members and coordinate their activity in space and time more closely than capuchins do. These characteristics support stronger social biases in learning in callitrichids than in capuchins in some situations. On the other hand, callitrichids' more limited range of manipulative behaviors, greater neophobia, and greater sensitivity to the risk of predation restricts what these monkeys learn in comparison with capuchins. We suggest that socially biased learning is always the collective outcome of interacting physical, social, and individual factors, and that differences across populations and species in social bias in learning reflect variations in all these dimensions. Progress in understanding socially biased learning in nonhuman species will be aided by the development of appropriately detailed models of the richly interconnected processes affecting learning.

Strategic navigation of two-dimensional alley mazes: comparing capuchin monkeys and chimpanzees.

Planning is an important component of cognition that contributes, for example, to efficient movement through space. In the current study we presented novel two-dimensional alley mazes to four chimpanzees and three capuchin monkeys to identify the nature and efficiency of planning in relation to varying task parameters. All the subjects solved more mazes without error than expected by chance, providing compelling evidence that both species planned their choices in some manner. The probability of making a correct choice on mazes designed to be more demanding and presented later in the testing series was higher than on earlier, simpler mazes (chimpanzees), or unchanged (capuchin monkeys), suggesting microdevelopment of strategic choice. Structural properties of the mazes affected both species' choices. Capuchin monkeys were less likely than chimpanzees to take a correct path that initially led away from the goal but that eventually led to the goal. Chimpanzees were more likely to make an error by passing a correct path than by turning onto a wrong path. Chimpanzees and one capuchin made more errors on choices farther in sequence from the goal. Each species corrected errors before running into the end of an alley in approximately 40% of cases. Together, these findings suggest nascent planning abilities in each species, and the prospect for significant development of strategic planning capabilities on tasks presenting multiple simultaneous or sequential spatial relations. The computerized maze paradigm appears well suited to investigate movement planning and spatial perception in human and nonhuman primates alike.

Do apes and monkeys rely upon conceptual reversibility? : A review of studies using seriated nesting cups in children and nonhuman primates.

The ability to seriate nesting cups as a sensorimotor task has posed interesting questions for cognitive scientists. Greenfield et al. [(1972) Cognit Psychol 3:291-310] found parallels between children's combinatorial activity with nesting cups and patterns of phonological and grammatical constructions. The parallels suggested the possibility of a neurally based developmental homology between language and instrumental action [Greenfield (1991) Behav Brain Sci 14:531-595]. Children who predominantly used subassembly, a hierarchical method of combining cups, succeeded at seriating nesting cups more often than those who did not. Greenfield and others [e.g., Piaget and Inhelder (1969) The psychology of the child. Basic Books, New York; DeLoache et al. (1985) Child Dev 56:928-939] argued that success in seriation reflects the child's growing recognition of a reversible relationship: a particular element in a series is conceived of as being smaller than the previous element and larger than the subsequent element. But is a concept of reversibility or a hierarchical form of object manipulation necessary to seriate cups? In this article, we review studies with very young children and nonhuman primates to determine how individuals that do not evidence conceptual reversibility manage the seriation task. We argue that the development of skill in seriation is experientially, rather than conceptually, driven and that it may be unnecessary to link seriation with cognitive conceptions of reversibility or linguistic capacities. Rather, in ordering a set of objects by size, perceptual-motor learning may enable contemplative refinement.

Prehension in infant capuchins (Cebus apella) from six weeks to twenty-four weeks: video analysis of form and symmetry.

We analyzed the spontaneous prehensile activity of two infants living with their mothers in social groups, using videotapes taken once weekly from weeks 5 to 24. Prehensile activities were laterally symmetric. Unimanual activity predominated, although bimanual activity appeared at the same ages as unimanual activity. In most bimanual activity the two hands performed the same action, but complementary actions occurred from the onset of bimanual activity. Extrusion of the tongue towards objects out of reach was observed occasionally, as was precision grasping. Early prehension in capuchins is organized, as in human infants, in a matrix of exploratory activity integrated with vision and oral exploration. Capuchins present a useful model system for the study of manipulative development.

Strategies used to combine seriated cups by chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and capuchins (Cebus apella).

The authors investigated strategies used to combine seriated cups by apes (Pan troglodytes and P. paniscus) and monkeys (Cebus apella) using a protocol reported in P. M. Greenfield, K. Nelson, and E. Saltzman's (1972) study with children. It was hypothesized that apes would exhibit more hierarchical combinations of cups than monkeys, given apes' language capacity, and that apes would seriate the cups more efficiently than monkeys. As predicted, apes made many structures with the cups using a variety of strategies, and monkeys rarely combined the cups. After a training phase to orient monkeys to the task, the 2 genera did not differ in the strategies used to combine the cups or in efficiency in seriating the cups. Success in this task suggests that sensorimotor versions of hierarchically organized combinatorial activity are well within apes' and monkeys' abilities.

Left hand preferences in capuchins (Cebus apella): role of spatial demands in manual activity.

Sixteen capuchins (Cebus apella) participated in four tasks that differed in their exploration demands and availability of visual cues. The two explorative tasks required the monkeys to discover sunflower seeds hidden in crevices in objects of various shapes, with vision (Haptic-Visual task) or without vision (Haptic task). Two other tasks required the capuchins to grasp sunflower seeds directly on a flat support, with vision (Visual reaching) or without vision (Tactual reaching). The presence or absence of exploration demands had a significant effect on the direction of hand preferences. The group displayed greater left hand preferences for the Haptic and Haptic-Visual tasks than for the two reaching tasks. The strength of manual preferences did not differ significantly among the four tasks. These findings suggest that the manipulo-spatial demands of a task are of particular importance for the expression of left hand bias in a population of capuchins. It is argued that left hand preferences for the haptic tasks may reflect a right hemisphere specialisation to integrate the spatial and motor components of action.

Social context and consumption of unfamiliar foods by capuchin monkeys (Cebus apella) over repeated encounters.

Visalberghi and Fragaszy [Animal Behaviour 49:1089-1095, 1995] have shown that social influences affect acceptance of novel foods. However, little is known about the temporal course on which such influences act (e.g., for how long they persist and for how many encounters they are effective). To explore this issue, 11 adult tufted capuchins were observed during ten successive encounters with eight unfamiliar foods (phase 1, in which subjects were tested in social or individual condition) and ten more encounters 6 months later (phase 2, in which all subjects were tested in social condition). A total of 680 observational sessions were carried out. Results show that during the first five encounters in phase 1, capuchins ate more when they encountered these foods in the presence of their groupmates than if they encountered them alone. Thereafter, during the second five encounters of phase 1, foods were consumed equivalently whether presented to monkeys socially or individually. In phase 2, the foods were consumed equivalently regardless of the previous circumstance of their presentation (social or alone). In phase 2, consumption was similar to that scored in a previous study for familiar foods [Visalberghi & Fragaszy, Animal Behaviour 49:1089-1095, 1995]. We conclude that 1) foods remain unfamiliar to capuchins only for the first few encounters, 2) social facilitation of consumption of unfamiliar foods is of limited duration, and 3) individuals consumed equivalent amounts of an unfamiliar food when they repeatedly encountered it alone or in the presence of groupmates. These results caution those who interpret similar feeding habits in primate groups as evidence of social influences.

Growth and reproduction in captive tufted capuchins (Cebus apella).

We present data on weight and reproduction from a colony of tufted capuchins monkeys (Cebus apella) over a 12 year period. The data constitute a normative record for this species. Weight at birth averages 210 g, and infants gain weight rapidly. Females typically first conceived just after their fifth birthday, and males were fertile by 4 years, 5 months. Interbirth intervals average 576 days. Eighty-seven percent of live-born infants survived past 6 months. Three of eight live-born infants that died prior to 6 months succumbed from trauma inflicted by cage mates.

Transfers of food from adults to infants in tufted capuchins (Cebus apella).

This study examined the behavioral mechanisms that support transfer of food from adults to infants in tufted capuchins (Cebus apella). Two captive groups of capuchins were presented with abundant quantities of unshelled pecans or commercial pellets. Five of 11 infant subjects could not open the nuts. A variety of tolerated interactions were initiated by infants toward adults, and food was frequently transferred. All such interactions were more frequent with nuts (a preferred food) than with pellets. Adult capuchins were equally tolerant of infant capuchins that could open nuts and those that could not. Tolerated interactions during feeding could result in acquisition of dietary information by young capuchins or to important, if intermittent, nutritional support.

Developmental changes in manipulation in tufted capuchins (Cebus apella) from birth through 2 years and their relation to foraging and weaning.

This study examined the contributions of physical and sensorimotor development to manipulation in capuchins (Cebus apella) from birth to 2 years. Between months 1-6 and 7-12, manipulation increased significantly in frequency, in the proportion that was vigorous or required fine motor control, and in the proportion directed at portable objects. Fine motor control, moving objects in relation to the body, and stamina are largely in place by 12 months, after which little changed. All elements of the manipulative repertoire have appeared, and vigorous and dexterous activities have peaked before fully independent foraging. Emergence of permanent dentition and achievement of approximately half of adult body size accompany the attainment of fully independent foraging at 15 months. Thereafter, increasing strength and specific knowledge probably contribute more to changing foraging competence in young capuchins than do stamina and sensorimotor development.

Infant tufted capuchin monkeys' behaviour with novel foods: opportunism, not selectivity

To determine whether young capuchin monkeys, Cebus apellaselectively interacted with others concerning novel foods, 11 infants (4.5-12 months) living in two groups were observed following presentation of familiar or novel foods. Foods were presented either to the whole group or to infants in a section of the home cage to which only they had access. Infants showed more frequent interest in others' food and picked up foods more frequently when foods were novel, and they tended to eat novel foods more frequently than familiar foods. The pattern was the same whether the foods were presented to the group or only to infants. Infants expressed interest in others' novel foods equally often before and after sampling these foods themselves. The frequency of interest in others' food correlated positively with age. It is concluded that acceptance of novel foods in these monkeys occurs readily regardless of socially provided information about edibility. Social interactions do not appear to make important contributions to acceptance of novel foods by infant capuchin monkeys.

Manual exploratory procedures and asymmetries for a haptic search task: a comparison between capuchins (Cebus apella) and humans.

Left-hand preferences in monkeys (capuchins, macaques) for haptic discriminations have been taken to indicate that the right hemisphere is more involved than the left hemisphere in solving these tasks. We confirmed this left-hand bias in a group of 21 capuchins haptically searching for sunflower seeds located in crevices in 12 different objects (Lacreuse & Fragaszy, 1996). In an attempt to specify the relations of the left-hand bias to hand performance and hemispheric lateralisation, we analysed the manual exploratory procedures used by the subjects when exploring the objects, and compared them to those of humans confronted with the same task. All the hand-movement patterns displayed by humans were also observed in capuchins, but humans performed exhaustive explorations, whereas capuchins restricted their haptic investigations to limited portions of the objects. Both species adopted several ''exploratory procedures'' to investigate particular objects. Although capuchins showed a left-hand preference to perform the task, finer analyses of haptic exploratory procedures revealed no difference in the way the left and right hands explored the objects, nor in the efficiency with which each hand solved the task. Nor was any measurable difference in manual exploratory procedure and efficiency found in humans. The discussion emphasises the need to complement measures of manual preference with finer indices of hemispheric lateralisation, for a better understanding of functional asymmetries in primates.

Performance in a tool-using task by common chimpanzees (Pan troglodytes), bonobos (Pan paniscus), an orangutan (Pongo pygmaeus), and capuchin monkeys (Cebus apella).

Performance by individual animals of three species of great apes (Pan troglodytes, Pan paniscus, and Pongo pygmaeus) and capuchin monkeys (Cebus apella) was assessed by presenting a food treat inside a clear tube. The subjects readily used a straight stick to obtain the food. When sticks were bundled together, the apes immediately unwrapped the bundle to obtain an individual stick, whereas capuchins attempted to insert the bundled sticks. When a misshapen stick was provided, apes, but not capuchins, showed an improvement in terms of modifying the misshapen stick before insertion. Our results indicate that all these species can solve these tasks. However, only the performance of apes is consistent with emerging comprehension of the causal relations required for the avoidance of errors in the more complex tasks.

Development of manipulation in capuchin monkeys during the first 6 months.

This study describes the orderly changes in manipulation over the first 6 months in capuchin monkeys (Cebus apella). By 6 months of age, all the basic forms of manipulation seen in adults have appeared. Actions that occur frequently in the first 8 weeks are gentle and involve sustained visual orientation and aimed reaching. Later actions are more vigorous, and involve grasping. Large increases in the rate of activity are evident over the period of development studied. The increase from the first 8 weeks to the second may be due to (a) an increase in the amount of time spent alert and active, (b) a decrease in the amount of time spent in a ventral position, (c) improvements in postural control and stamina and (d) the onset of independent locomotion. Changes in form can be attributed primarily to postural factors and to neuromuscular development (precisely aimed and controlled movements appearing in the 5th and 6th months).

Behavioral sampling in the field: Comparison of individual and group sampling methods.

Sampling decisions affect the efficiency and reliability of data collection, and the appropriateness of the data for analyses of group and individual behavior. We evaluate the correspondence between interval sampling of individual behavior at high temporal density (focal interval sampling) with interval sampling of group behavior at lower density (group scan sampling) in two field studies with neotropical primates, capuchins and squirrel monkeys. The two methods provided consistent estimates of population means and variance for activity profiles, foraging activities, and height above ground. The correspondence between mean values with the two methods was greater when group sampling included individual identities than when a nominal scoring scheme was used. A group scan method (without identification of individuals) can be used alone when information is needed within a brief time, such as initial description of activity budgets of a population. Although individual identities take time to learn, data sets in which the individual is the unit of analysis provide several other kinds of analytical possibilities. We recommend use of a mixed sampling regime containing both of these elements (focal and group sampling) as a good way to minimize the time costs of data collection and as a means to evaluate reliability of data collection by a solo observer.