Briseida Dôgo de Resende

Watching the best nutcrackers: what capuchin monkeys (Cebus apella) know about others’ tool-using skills

The present work is part of a decade-long study on the spontaneous use of stones for cracking hard-shelled nuts by a semi-free-ranging group of brown capuchin monkeys (Cebus apella). Nutcracking events are frequently watched by other individuals - usually younger, less proficient, and that are well tolerated to the point of some scrounging being allowed by the nutcracker. Here we report findings showing that the choice of observational targets is an active, non-random process, and that observers seem to have some understanding of the relative proficiency of their group mates, preferentially watching the more skilled nutcrackers, which enhances not only scrounging payoffs, but also social learning opportunities.

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.

Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys (Cebus apella): a perception-action perspective.

How do capuchin monkeys learn to use stones to crack open nuts? Perception-action theory posits that individuals explore producing varying spatial and force relations among objects and surfaces, thereby learning about affordances of such relations and how to produce them. Such learning supports the discovery of tool use. We present longitudinal developmental data from semifree-ranging tufted capuchin monkeys (Cebus apella) to evaluate predictions arising from Perception-action theory linking manipulative development and the onset of tool-using. Percussive actions bringing an object into contact with a surface appeared within the first year of life. Most infants readily struck nuts and other objects against stones or other surfaces from 6 months of age, but percussive actions alone were not sufficient to produce nut-cracking sequences. Placing the nut on the anvil surface and then releasing it, so that it could be struck with a stone, was the last element necessary for nut-cracking to appear in capuchins. Young chimpanzees may face a different challenge in learning to crack nuts: they readily place objects on surfaces and release them, but rarely vigorously strike objects against surfaces or other objects. Thus the challenges facing the two species in developing the same behavior (nut-cracking using a stone hammer and an anvil) may be quite different. Capuchins must inhibit a strong bias to hold nuts so that they can release them; chimpanzees must generate a percussive action rather than a gentle placing action. Generating the right actions may be as challenging as achieving the right sequence of actions in both species. Our analysis suggests a new direction for studies of social influence on young primates learning sequences of actions involving manipulation of objects in relation to surfaces.

Brincadeira e aprendizagem do uso de ferramentas em macacos-prego (Cebus apella)

Nossa pesquisa tem como objetivo estudar o desenvolvimento dos infantes e juvenis de um grupo de macacos-prego (Cebus apella) em condicao de semiliberdade, com enfase nos comportamentos manipulativos. No presente estudo, relacionamos o aparecimento do uso de instrumentos para quebra de cocos com a brincadeira social e com a brincadeira com objetos. A brincadeira social ocorreu predominantemente em infantes e juvenis. A brincadeira com objetos, muitas vezes indistinguivel das atividades exploratorias, aumentou durante o primeiro ano de vida. A manipulacao exploratoria de pedras constitui uma oportunidade importante para a aprendizagem individual, por tentativa-e-erro, do uso de instrumentos para quebrar cocos, que surge entre o segundo e o terceiro anos de vida. A brincadeira social parece facilitar a tolerância entre os sujeitos, o que favoreceria a aprendizagem por observacao dos episodios de quebra.

Repellent Efficacy of Formic Acid and the Abdominal Secretion of Carpenter Ants (Hymenoptera: Formicidae) Against Amblyomma Ticks (Acari: Ixodidae)

Abstract Formic acid is a substance produced by some ants for defense, trail marking, and recruitment. Some animals are known to rub ants or other arthropods on parts of their plumage or fur to anoint themselves with released substances. A recent study with a semifree-ranging group of capuchin monkeys, Cebus apella L., in the Tietê Ecological Park, Sao Paulo, Brazil, an area of occurrence of the tick species Amblyomma cajennense (F.), revealed that “anting” with carpenter ants, Camponotus rufipes F. (Hymenoptera: Formicidae), occurs frequently, especially during the A. cajennense subadult season. Based on these observations, we tested the repellent effect of the formic acid and the ants themselves against A. cajennense and Amblyomma incisum Neumann nymphs, and Amblyomma parvum Aragão adult ticks in the laboratory. The results revealed a significant repellent effect of formic acid and ant secretion, and a significant duration of the repellent effect. The results suggest that the anting behavior of capuchin monkeys, and other vertebrates, may be related with repellence of ticks and other ectoparasites.

Anting in a Semifree-ranging Group of Cebus apella

Capuchins apply many organic materials, especially leaves, to their skin. Protection against ectoparasites is the most commonly discussed explanation for the behavior. We describe fur rubbing with carpenter ants(Camponotus rufipes) by semifree-ranging tufted capuchins(Cebus apella) in the Tietê Ecological Park, São Paulo, Brazil. Carpenter ants produce and secrete high concentrations of formic acid, which repels tick nymphs. Anting occurred significantly more often during months of seasonal incidence of nymphs of the tick Amblyomma cajennense, and the behavior was not related to ant-eating. We argue that anting behavior in tufted capuchins fits the hypothesis of protection against ectoparasites.

Interaction between capuchins and coatis: Nonagonistic behaviors and lack of predation

We compare the nature of capuchin-coati interactions by Cebus apella in 2 populations under semifree-ranging and wild conditions. We report a similar pattern of interaction at both sites, in spite of their ecological differences. Most frequent capuchin behaviors toward coatis were agonistic, but we noted no predation. Contrarily, the monkeys also exhibited nonagonistic behaviors, such as play and grooming. As tufted capuchins predate other mammalian species, and as the subjects were aggressive towards competitor species, showing their belligerent temperament, we believe the lack of predation can be attributed to 2 different ecological contigencies – the absence of coati pups in a period of food shortage, and the cost of dealing with a dangerous adult coati where other rich resources were available–and also, perhaps, to different traditions in capuchin behavior towards coatis, established via intraspecific social learning.

Tufted capuchin monkeys (Sapajus sp) learning how to crack nuts: Does variability decline throughout development?

We investigated the process of nut-cracking acquisition in a semi-free population of tufted capuchin monkeys (Sapajus sp) in São Paulo, Brazil. We analyzed the cracking episodes from monkeys of different ages and found that variability of actions related to cracking declined. Inept movements were more frequent in juveniles, which also showed an improvement on efficient striking. The most effective behavioral sequence for cracking was more frequently used by the most experienced monkeys, which also used non-optimal sequences. Variability in behavior sequences and actions may allow adaptive changes to behavior under changing environmental conditions.

Synchronized practice helps bearded capuchin monkeys learn to extend attention while learning a tradition

Culture extends biology in that the setting of development shapes the traditions that individuals learn, and over time, traditions evolve as occasional variations are learned by others. In humans, interactions with others impact the development of cognitive processes, such as sustained attention, that shape how individuals learn as well as what they learn. Thus, learning itself is impacted by culture. Here, we explore how social partners might shape the development of psychological processes impacting learning a tradition. We studied bearded capuchin monkeys learning a traditional tool-using skill, cracking nuts using stone hammers. Young monkeys practice components of cracking nuts with stones for years before achieving proficiency. We examined the time course of young monkeys’ activity with nuts before, during, and following others’ cracking nuts. Results demonstrate that the onset of others’ cracking nuts immediately prompts young monkeys to start handling and percussing nuts, and they continue these activities while others are cracking. When others stop cracking nuts, young monkeys sustain the uncommon actions of percussing and striking nuts for shorter periods than the more common actions of handling nuts. We conclude that nut-cracking by adults can promote the development of sustained attention for the critical but less common actions that young monkeys must practice to learn this traditional skill. This work suggests that in nonhuman species, as in humans, socially specified settings of development impact learning processes as well as learning outcomes. Nonhumans, like humans, may be culturally variable learners.

Capuchin Monkey (Cebus apella) Vocalizations in Response to Loud Explosive Noises

Primates emit different kinds of vocalizations in different contexts (Struhsaker, 1967; Snowdon and Pola, 1978; Seyfarth et al., 1980; Robinson, 1982; Boinski et al., 1999; Oliveira and Ades, 1998; Maccowan et al., 2001; Di Bitetti, 2001, 2003). For example, long calls can serve as localization cues for conspecifics and are often produced in the context of territorial encounters, mate attraction, and isolation/group cohesion (Waser, 1982; Miller and Ghanzanfar, 2002). Vocalizations used in close-range social interactions may be given in many different situations, such as resting, grooming, foraging or playing (Seyfarth, 1988). Some primates have different alarm calls for different predators (Struhsaker, 1967; Fichtel and Hammerschmidt, 2002; Fichtel and Kappeler, 2002). An often-cited example is the alarm repertoire of vervet monkeys. In this system, receivers respond differently to different calls: for example, they look up and move down or into cover just after an eagle alarm call, and they run into the trees just after a leopard call (Struhsaker, 1967; Seyfarth et al., 1980). The appropriate response contingent upon danger increases chances for survival and reproduction, thus, improvement in fitness. Vervet alarm call specificity improves with age: at first, infants do not show much discrimination among predator classes (they may give eagle calls for non-raptors, for example); then, they give alarm calls for raptors that are not their predators; and finally they learn to vocalize only for the correct raptor predator (Seyfarth and Cheney, 1986; Seyfarth, 1988). Nevertheless, it is difficult to separate the role of genetics and environment affecting development (Seyfarth and Cheney, 1986; Seyfarth, 1988).