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.

Behavioral flexibility of a group of bearded capuchin monkeys (Cebus libidinosus) in the National Park of Brasília (Brazil): consequences of cohabitation with visitors / Flexibilidade comportamental de um grupo de macacos-prego (Cebus libidinosus) no Parque Nacional de Brasília (Brasil): conseqüências da convivência com os visitantes

Increasing urbanization and deforestation have enhanced the opportunities of contact between humans and monkeys and the impact of human activities on primate behavior is receiving growing attention. This study explores whether activity budgets and diet of a group of capuchin monkeys (Cebus libidinosus) inhabiting the area of the swimming pools of the National Park of Brasília is affected by the presence of visitors providing food to them. During one year, both in the dry and the wet seasons, we scored capuchins' behavior via scan sampling every ten minutes. Results showed that this group spent less time foraging for wild foods than other comparable groups living in similar habitats. Moreover, capuchins relied more on human food during the dry season, when pulpy fruits were less available, than in the wet season. Our findings confirm other studies on different monkey species that have shown that access to human food decreases the time spent foraging for wild food and the home range size. They also show that capuchins are able to modify their diet, to exploit alternative food sources, and to change their activity budget in response to the availability of new food opportunities and to seasonal food availability.

Recentemente, o impacto de atividades humanas sobre o comportamento de primatas tem recebido maior importância dado o crescente desmatamento e urbanização, que têm favorecido o aumento do contato entre humanos e macacos. O presente estudo descreve os padrões de atividade e a dieta de um grupo de macacos-prego (Cebus libidinosus) que vive no Parque Nacional de Brasília. O Parque é freqüentado diariamente por visitantes, de modo que os animais estão habituados à presença humana, bem como ao consumo de itens de sua dieta. Observações comportamentais do grupo foram realizadas ao longo de um ano, compreendendo a estação seca e a chuvosa, utilizando-se registro de varredura a cada 10 minutos. Resultados obtidos indicaram que o grupo despendeu menos tempo forrageando itens naturais do que outros grupos vivendo em habitats similares. Além disso, durante a estação seca, quando há menor disponibilidade dos frutos de polpa, os macacos-prego alimentaram-se mais de itens da dieta humana como uma fonte alternativa de recurso. Como demonstrado em estudos anteriores realizados com outras espécies de macacos, a alimentação baseada em itens da dieta humana pareceu diminuir a motivação dos animais para forragear no seu habitat natural, assim como promoveu a redução do tempo gasto no forrageamento e a redução de sua área de uso. Nossos resultados indicaram ainda que o consumo de comida humana reflete o caráter adaptável dos animais em explorar fontes alternativas de recurso, bem como a sua habilidade em modificar a sua dieta e padrões de comportamento face às mudanças ambientais.

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.

An experimental analysis of ingestion rates in an omnivorous species.

Food intake is difficult to estimate under natural conditions. We investigated ingestion rates of 14 different food types in 26 captive capuchin monkeys (Cebus apella). The procedure consisted in weighing a piece of food and using a two alternative choice tests to present food to the subject, alone in its cage. We recorded the food chosen and the time it took the subject to consume the food entirely. Consumption time was converted into ingestion rates (g/s) for each food type. Ingestion rates of food types significantly differed, and the difference was significantly higher among foods than among subjects. In particular, ingestion rates of the fruits were higher than those of human-processed food. Interestingly, food preferences were significantly related to energy intake rate, i.e., to the amount of energy ingested per unit of time, but not with ingestion rates or energy content alone. The energy acquired by eating different types of food cannot be calculated on the basis of the time spent eating unless a correction factor for each given food (or similar ones) is applied. Future controlled studies should provide field researchers with such corrections factors, possibly using foods collected in the wild.

Behavioral flexibility of a group of bearded capuchin monkeys (Cebus libidinosus) in the National Park of Brasília (Brazil): consequences of cohabitation with visitors.

Increasing urbanization and deforestation have enhanced the opportunities of contact between humans and monkeys and the impact of human activities on primate behavior is receiving growing attention. This study explores whether activity budgets and diet of a group of capuchin monkeys (Cebus libidinosus) inhabiting the area of the swimming pools of the National Park of Brasília is affected by the presence of visitors providing food to them. During one year, both in the dry and the wet seasons, we scored capuchins' behavior via scan sampling every ten minutes. Results showed that this group spent less time foraging for wild foods than other comparable groups living in similar habitats. Moreover, capuchins relied more on human food during the dry season, when pulpy fruits were less available, than in the wet season. Our findings confirm other studies on different monkey species that have shown that access to human food decreases the time spent foraging for wild food and the home range size. They also show that capuchins are able to modify their diet, to exploit alternative food sources, and to change their activity budget in response to the availability of new food opportunities and to seasonal food availability.

Do capuchin monkeys (Cebus apella) use tokens as symbols?

In the absence of language, the comprehension of symbols is difficult to demonstrate. Tokens can be considered symbols since they arbitrarily stand for something else without having any iconic relation to their referent. We assessed whether capuchin monkeys (Cebus apella) can use tokens as symbols to represent and combine quantities. Our paradigm involved choices between various combinations of tokens A and B, worth one and three rewards, respectively. Pay-off maximization required the assessment of the value of each offer by (i) estimating token numerousness, (ii) representing what each token stands for and (iii) making simple computations. When one token B was presented against one to five tokens A (experiment 1), four out of ten capuchins relied on a flexible strategy that allowed to maximize their pay-off, i.e. they preferred one token B against one and two tokens A, and they preferred four or five tokens A against one token B. Moreover, when two tokens B were presented against three to six tokens A (experiment 2), two out of six capuchins performed summation over representation of quantities. These findings suggest that capuchins can use tokens as symbols to flexibly combine quantities.

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.

The observation and hearing of eating actions activates motor programs related to eating in macaque monkeys.

The observation of actions can lead, in some cases, to the repetition of those same actions. In other words, motor programs similar to those observed can be recruited. Since this phenomenon is expressed when in the presence of another individual, it has been named social facilitation. In the present study we investigated whether the observation and/or hearing of eating actions facilitate eating behaviors in observing/listening pig-tailed macaques. In experiment 1, the observation of an eating room mate significantly enhanced eating behavior in the observer. Similar results were obtained (experiment 2) in response to the sound of eating actions but not to control sounds (experiment 3). We propose that eating facilitation triggered by observation or listening of eating actions can rely on the mirror neuron system of ventral premotor cortex that provides a matching between the observed/listened action and the executed action. This matching system can subsequently trigger the motor programs necessary for repeating the observed/heard actions.

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.

Social facilitation of eating novel food in tufted capuchin monkeys (Cebus apella): input provided by group members and responses affected in the observer.

Learning about food palatability from watching what conspecifics eat might be one of the advantages of group living. A previous study investigated whether group members' presence or eating activity account for social facilitation of eating of foods never previously tasted. Capuchins encountered novel colored foods when (1) alone (Alone condition) or (2) with group members visible in the nearby cage (Group-present condition) or (3) with group members present and eating a familiar food that had not been colored (Group+food condition). Social facilitation of eating occurred when group members were eating, despite the difference in color between the familiar food eaten by them and the novel food presented to the experimental subject. To clarify what subjects learnt from group members when social facilitation occurred, we further analyze here the data from the previous study. The number of visual exposures to the colored novel food (as a group member) correlated with increased consumption of that novel food when encountered later (as experimental subject). In contrast, the number of times that an individual fed on the familiar food (as a group member) did not decrease its consumption of novel food (as experimental subject). Therefore, capuchins (1) habituated to the colors of the novel foods, and (2) did not take into account that seeing group members eating a food does not provide information about the palatability of a differently colored food. Since social facilitation of eating occurs when foods do not match in color, at least in capuchins, social facilitation of eating should not be considered as a way of learning about a safe diet, but rather as a way of overcoming neophobia.

Learning to cope with two different food distributions: the performance of house mice (Mus musculus domesticus).

Search abilities of mice (Mus musculus domesticus) were evaluated using an arena closed by a ceiling in which 9 food sources (which mice could reach standing on their hind legs) could be arranged according to 2 configurations: a 3 x 3 square matrix and 3 clusters each containing 3 food sources. Testing conditions prevented olfactory and visual cues from being left after visits to food sources, and mice were able to choose alternative routes between food sources. Results showed that mice were more efficient with the matrix than with the cluster configuration. Sex differences were observed: Females improved their performance with both configurations, whereas males improved only with the matrix one. Mice did not develop evident search strategies that would minimize task complexity. Comparison with data published on capuchin monkeys revealed differences, with monkeys performing better with the cluster configuration than with the matrix and applying searching strategies.

Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys.

In primates, social context is one of the factors that increases the acceptance of novel foods. Previous experiments showed that tufted capuchins, Cebus apella, eat significantly more of novel foods when in the presence of group members eating the same novel foods. Several processes may have led to these results. The mere presence of group members may reduce the individual's stress of being alone, or its neophobic response and, consequently, may increase its food consumption. The individual may be influenced by what group members do, and local/stimulus enhancement and/or social facilitation may occur. To investigate the above processes, we assessed whether an individual capuchin monkey's consumption of novel foods is lower when (1) the individual is alone with nobody in the nearby cage than when (2) group members are present in the nearby cage with no food or when (3) they are present and eating a familiar food. We tested 15 subjects with three novel foods, each presented in one condition. In both social conditions, the more group members there were by the food box the more the experimental subject ate. In addition, when group members were present and eating food, there was a significant increase in the acceptance of the three foods, regardless of what group members were eating. We argue that social facilitation of eating is a quicker way to overcome neophobia and only social facilitation of eating what the others are eating can be considered a safe way to learn about a safe diet. Copyright 2000 The Association for the Study of Animal Behaviour.

Response to changes in food palatability in tufted capuchin monkeys, Cebus apella.

Palatability of plant foods may change over time in relation to the concentration of toxic secondary metabolites. We investigated the behavioural response of capuchin monkeys to this type of change and assessed the influence of social conditions. Twenty-seven tufted capuchin monkeys were presented in Social or Individual conditions with a familiar palatable food (phase 1), with the same familiar food to which pepper had been added, making it unpalatable (phase 2), and with the same familiar palatable food of phase 1 (phase 3). Five sessions were carried out in each phase. The capuchins adapted quickly to the change in food palatability by reducing (phase 2) and increasing (phase 3) the amounts of food eaten. The unpalatable food prompted an increase in olfactory exploration and in food processing. The experimental conditions (Social versus Individual) did not influence consumption, or any of the other behaviours. In addition, capuchins were more often near subjects with food in phases 2 and 3 in which palatability changed than in phase 1. These findings show that capuchins readily adjust to changes in flavour and palatability of a familiar food and that sudden unpalatability has no carry-over effects. Therefore, capuchins behave differently towards a familiar food whose palatability has changed than they do towards novel foods. Copyright 2000 The Association for the Study of Animal Behaviour.

Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys.

In many primates species, female sexual attractivity is influenced by behavioral cues as well as by nonbehavioral cues (i.e., visual-morphological or chemical signals). Both kinds of cues are usually related to the ovarian cycle and female hormonal state. Female tufted capuchins (Cebus apella) lack any external morphological change in relation to the ovarian cycle and evidence of scent-marking behavior has never been reported. In addition, tufted capuchin males do not routinely investigate the female's body or urine. Instead, capuchin females are extremely active in sexually soliciting the male(s) and their courtship toward them involves a rich behavioral repertoire. In the present study we defined female tufted capuchin proceptivity and investigated its relationship with female reproductive state. Ovarian hormones were measured in urine and fecal samples from four captive females in order to (a) assess their reliability for monitoring female ovarian function and (b) provide information on the timing of the component cycle phases and in particular the periovulatory phase. Measurements of urinary and fecal progestin metabolites provided the best indicator of ovarian cyclicity and for timing of the periovulatory phase. Through a multivariate analysis of the behavioral data set we distinguished four behaviors (eyebrow raising with vocalization, touching-and-running, nuzzling and head cocking) which showed a marked cyclicity (21.3 days) that matched that of urinary progesterone (21.9 days). Data showed that each period of proceptive behaviors was 2.7 +/- 0.8 days long and the day of a defined luteal phase rise in urinary progesterone levels was markedly shifted toward the end of this period. Furthermore, the ejaculations observed always occurred within proceptive periods. The results clearly indicate that female behavior is a good indicator of the periovulatory phase and can enhance female attractivity.

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.

Primate causal understanding in the physical and psychological domains.

Evidence for primates' understanding of causality is presented and discussed. Understanding causality requires the organism to understand not just that two events are associated with one another in space and time, but also that there is some `mediating force' that binds the two events to one another which may be used to predict or control those events (e.g. a physical force such as gravity or a psychological force such as an intention). In the physical domain, studies of tool use indicate that capuchin monkeys do not have a causal understanding of the functioning of tools in terms of the physical forces involved, but rather they learn to associate aspects of their own behavior with the results it produces. Apes show some possible signs of understanding the causal relations involved in tool use in the sense that they may employ various forms of foresight in approaching novel tasks, perhaps involving an understanding of physical forces-although not to the extent of human children. In the psychological domain, nonhuman primates understand conspecifics as animate beings that generate their own behavior and, thus, they appreciate that to manipulate conspecifics communicative signals, and not physical activities, are required. However, there is very little evidence that nonhuman primates of any species understand others as psychological beings with intentions and other psychological states that mediate their behavioral interactions with the world-as human children begin to do sometime during their second year of life. More research, using a wider range of problem-solving situations, is needed if we are to become more precise in our understanding of how primates understand the causal structure of the world around them.

Capuchin monkeys, Cebus apella fail to understand a cooperative task

We investigated whether capuchin monkeys cooperate to solve a task and to what extent they take into account the behaviour of another individual when cooperating. Two groups of capuchin monkeys (N=5 and 6) were tested in a task whose solution required simultaneous pulling of two handles which were too far from one another to be pulled by one monkey. Before carrying out the cooperation study, individual monkeys were trained to pull one handle (training phase 1) and to pull two handles simultaneously (training phase 2) for a food reward. Nine subjects were successful in training phase 1, and five in training phase 2. In the cooperation study seven subjects were successful, that is, pulled one handle while a companion pulled the other. Further analyses revealed that capuchins did not increase their pulling actions when a partner was close to or at the other handle, that is, when cooperation might occur. These data suggest that capuchin monkeys acted together at the task and got the reward without understanding the role of the partner and without taking its behaviour into consideration. Social tolerance, as well as their tendency to explore and their manual dexterity, were the major factors accounting for the capuchins' success.Copyright 1997 The Association for the Study of Animal Behaviour1997The Association for the Study of Animal Behaviour