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Etiology

With sticks and stones

Capuchin monkey uses tools to break open fruit or hunt ants

BRISEIDA RESENDESome motor skills of the capuchin monkeys resemble those of the chimpanzeesBRISEIDA RESENDE

The excitable capuchin monkeys have activated a scientific debate that seeks to analyze the necessary conditions that constitute intelligence and cultural traditions in the evolutionary process of primates. Native to South America, the small (60 centimeters tall and weighing a little over 3 kilos) monkeys are known for the thick, dark fur on top of their heads, which resembles a hood. Until the last decade, the capuchin monkeys (Cebus apella) were relegated to the sidelines of research into the behavior of primates, even though it had been widely known, as a result of observations of these monkeys in captivity, when they are able to learn how to use tools to, for example open up dry fruit. Very few researchers, however, were enthusiastic about this kind of performance. “This skill could have been stimulated by specific captivity conditions or by contact with human beings, which would disqualify this activity as a spontaneously developed cultural tradition transmitted from one generation to the next”, says Eduardo Ottoni, a researcher at the Psychology Institute of the University of São Paulo, who has studied the behavior of capuchin monkeys for over ten years.

In the last three years, studies conducted by researchers from Brazil, Italy and the United States found that in specific places and under specific circumstances, capuchin monkeys use tools when they are in the wilds and transmit this skill to the next generations in rituals that have special characteristics. “The use of tools can no longer be viewed as an exclusive skill of hominoids, as it is also found among neo-tropical primates”, argues Italy’s Elisabetta Visalberghi, from Rome’s Institute of Science and Cognition Technology, in an article published in the American Journal of Physical Anthropology in January. The article describes this kind of skill among capuchin monkeys that live in an area of Boa Vista, State of Piauí and was written in collaboration with researchers Eduardo Ottoni and Patrícia Izar, from the University of São Paulo (USP), and Dorothy Fragaszy, from the University of Georgia, United States.

For reasons that the researchers are still trying to define precisely, not all populations of this species, which is found from Argentina to Venezuela, use tools. In Brazil, the capuchin monkeys live in such diverse environments as the Amazon Region, the Cerrado region (cattle-grazing land), the Caatinga (a region of stunted vegetation in the drought area of northeastern Brazil) and the Mata Atlântica rain forest. But the images of the simians in activity in Piauí mirror what is seen when the monkeys are in captivity – and this time it cannot be argued that they learned the skills from us or that their behavior is induced by researchers in search of similarities with the human race. The animals carry stones that weigh approximately 1 kilo for various meters – they use these stones as hammers – until they reach a site where they break something open. They use flat rocks or tree trunks as support – this support is referred to as an “anvil”, a reference to the kind of support that is used to strike metal.

The stereotyped use of tools has already been observed in countless species, ranging from spiders that arrange pebbles around their webs, to vultures that use stones to perforate ostrich eggs. This cannot compare to the dexterity of human ancestors when they gained bigger brains, or, since the 1970’s, when it was evidenced that chimpanzees (Pan troglodytes) transmit certain learning skills, such as the use of sticks to get honey or capture ants, from one generation to the next, as an authentic tradition transmitted culturally. In the 1990’s, it was verified that orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in captivity were also able to use sticks and stones as tools – to break open coconuts and chestnuts. The skepticism regarding the capuchin monkeys has an additional explanation. “Chimpanzees and gorillas are close to human beings in the evolution chain, while capuchin monkeys belong to a branch that branched out at least 40 million years ago,” says researcher Patrícia Izar.

The evidence that such a distant relative of man was able to develop the use of tools undermines the idea that our species is the only one to develop this skill, as proposed by Kenneth Oakley in 1949 in his book Man, the toolmaker. Instead, the suggestion is that this kind of behavior can be triggered by more generic conditions than previously imagined. If this theory is confirmed, the capuchin monkey might become the prime model to understand how the human species evolved, about 2.5 million years ago, to the point of being able to use axes, hammers, harpoons and other tools. In the seventies, Jane Goodall, a renowned expert on simians, had already classified chimpanzees in the category of species able to use tools – even though researchers are cautious about comparing these skills to our ancestors’ cognitive leap. “If culture can be defined as an innovation followed by social transmission, then we are finding patterns that suggest that we are indeed contemplating cultures,” proposed Holland’s Carel van Schaik, director of the Anthropological Institute and the Museum of the University of Zurich, in Switzerland, at a conference held in San Francisco in 2003. Van Schaik is an expert on the behavior of orangutans.

Singularity
The constitution of human culture involved a set of much more complex elements, such as language and artistic expression. However, research studies, as pointed out by anthropologist Eunice Durhan, from the University of São Paulo, in the article “Do Chimpanzees have culture” Issues for anthropology on a topic to reflect on, – published in 2005 in the Revista de Antropologia journal, do not seek to attribute to simians a special place because of their similarity with human beings. “On the contrary, their intention is to go beyond concepts based on absolute human singularity, bringing it as close as possible to the big apes and other intelligent social animals, starting from in-depth research on their behavior,” wrote Eunice Durhan.

Amazingly enough, the image of capuchin monkeys using tools in the wild was broadcast around the world by chance. In 2004, a British photographer visited an eco-tourism farm in Gilbués, State of Piauí, and became fascinated with what he saw: a capuchin monkey lifted a stone with both hands up to the top of its head and hit the small coconut placed on the ground with precision, just like a hunter who decides to kill a snake in the middle of the jungle. This scene was registered and aired around the world by Britain’s BBC network.. Dorothy Fragaszy saw the photograph of the monkey from Piauí and decided to contact her sources in Brazil. She sent a letter to Eduardo Ottoni and Patrícia Izar, whom she knew had been studying capuchin monkeys for some time. The letter, although it was an incentive for the researchers, also caught them by surprise, because the members of the USP team were in Piauí as well, but in a place far from Boa Vista. The team was working in the rocky and arid Capivara mountain range, also studying the use of tools by wild capuchin monkeys.

The interest of the USP researchers had been aroused ten years before this episode. In 1994, Ottoni was surprised by the report of a first-year science student who had observed the behavior of some 20 capuchin monkeys that live in the Parque Ecológico do Tietê park, in São Paulo City. The student described the same scene: groups of capuchin monkeys would get together to break open the coconuts  on a coconut palm tree. “At that moment, I realized that I was facing a major scientific challenge”, says Ottoni, who is a researcher at the Cognitive Etiology Laboratory of the Experimental Psychology Department of the University of São Paulo’s Psychology Institute.
The problem is that the living conditions of the capuchin monkeys living in the Parque do Tietê park are exceptional. The monkeys were apprehended by environmental authorities from the Ibama (the federal government’s environment protection entity) and placed in the park. They belong to a mixture of sub-species and nobody knows anything about their past. They could very well have learned how to use tools in situations prior to their captivity, as Elisabetta Visalberghi had already observed at zoos in Italy, which would disqualify the hypothesis of cultural tradition. Finally, they do not live in conditions that are comparable to nature. Although they were let loose, they are unable to cross the limits of the park, which is surrounded by the river, and they are also given food.

However, the study of these animals sparked a line of investigation in Brazil. At the beginning of this decade, Holland’s Carel van Schaik, a professor at the Biological Anthropology and Anatomy Department of Duke University in the United States, and an expert on the behavior of orangutans, proposed a theoretical model able to explain the advent of cultures associated with the use of tools. In his opinion, the appearance of such behavior allegedly depended on factors such as genetic predisposition (associated with big brains and manual dexterity), environmental factors (such as the dependence on food to which it is difficult to gain access or such as the sweet mucilage found in the coconuts) and the tolerant behavior of the adults, a condition for younger animals to have a chance to stay close to the older ones and thus learn the technique.

BRISEIDA RESENDEHunger
These hypotheses were tested by USP researchers and took the studies on capuchin monkeys in Brazil up to a new level. The thesis of dependence on food that is difficult to obtain, for example, is difficult to fit into the jigsaw puzzle. The thesis matches the observations at some sites but not at others. In the case of the monkeys in the Parque Ecológico do Tietê park, the ritual of breaking open the coconuts occurs even though the monkeys are fed by the handlers. However, in the Parque Estadual Carlos Botelho state park, located in an area of the Mata Atlântica rain forest in São Miguel Arcanjo, São Paulo State, researcher Patrícia Izar observed the opposite situation. The fact that food is scarce in that region results in the capuchin monkeys’ slower reproduction cycle: the females reproduce every three years, in comparison to an average interval of two years in nature. But no monkeys there seem to have time to break open coconuts. Hunger obliges them to divide themselves into smaller groups to look for protein in the form of insects, after which they re-group – this phenomenon is referred to as fission and merger.

In a study published in Science magazine in 2004, Brazil’s Antonio Christian de Moura, currently at the Federal University of Paraiba (UFPB), and simian specialist Phyllis Lee, from England’s Cambridge University, observed that the capuchin monkeys living in the Serra da Capivara mountain range, in the State of Piauí, use sticks to capture ants and use stones to break open fruit, as a way of ensuring food in the arid region of the Caatinga. In an article published in 2005 in the same Science magazine, Elisabetta Visalberghi, Patrícia Izar, Dorothy Fragaszy and Eduardo Ottoni questioned the hypothesis of the search for food, as some of the monkeys under study had been provided with food. “Comparing the life of the capuchin monkeys living in the Serra da Capivara mountain range and the ones living in the Parque Carlos Botelho state park shows that the Caatinga is not as poor nor the Mata Atlântica rain forest as rich as people suppose”, says Patrícia Izar. The hypothesis explains the occurrence or not of the use of tools by a given population according to the intensity of contact with the ground – in the Caatinga or in the Cerrado, the monkeys spend more time on the ground than those that live in the jungle – and not according to the supply of food in the environment. “This does not mean that the behavior did not evolve because of the huge advantage of being able to access these resources in environments in which there is a scarcity of other sources”, says Eduardo Ottoni.

A hypothesis developed by the USP group for the behavior corroborates another supposition voiced by Carel van Shaik: adults’ tolerance of beginners. In an article published in the journal Animal Cognition in 2005, Ottoni, Patrícia and USP researcher Briseida de Resende noticed a singular correlation in the tool-use ritual: monkeys that break open the coconuts more efficiently tend to attract bigger audiences, comprised of young monkeys. “It is clear that the younger ones are there because they want to eat whatever is left over from the coconuts that were opened,” says Ottoni. They watch the older monkeys, learn the body language and, little by little, start to try until they become efficient adults just like their role models. “The possibility is that the adult males allow the younger ones to watch them and then eat the leftovers as a way of attracting the attention of the females”, says Ottoni. Another hypothesis, raised by Patrícia, is that, instead of satisfying the hunger pangs, teaching how to use the tools is a way of maintaining the group’s social cohesion.

In the past, the general view was that all capuchin monkeys were part of the same species (Cebus apella). However, the nomenclature changed and nowadays, the existence of several species is taken into consideration. A possibility, which the USP researchers do not believe in, is that the distinction in terms of behavior is caused by genetics. Another doubt is related to evidence that, although capuchin monkeys use tools, comparing their skill with the skill of human beings in this respect may be an exaggeration. In 2001, Euphly Jalles-Filho, Rogério Grassetto Teixeira da Cunha and Rodolfo Aureliano Salm, researchers from the Biosciences Institute of the University of São Paulo, published an article in the Journal of Human Evolution, showing that capuchin monkeys are unable to transport tools as they move around their environment, as the Homo Habilis did 2.6 million years ago. The Homo Habilis was the first hominid species to be associated with flint stones used as tools (see Pesquisa FAPESP Nr. 66). “But, when forced to do so, they transport stones and, as for the anvil, transportation is not necessary, because they use rocks, the ground or tree trunks as the base”, answers Eduardo Ottoni.

A web of researchers
The good news is that, in the quest for answers to these questions, the number of researchers that study capuchin monkeys in other parts of Brazil has been growing consistently. In the State of Goiás, Francisco Dyonísio Cardoso Mendes and Rogério Ferreira Marquezan, from the Catholic University of Goiás, joined Eduardo and Patrícia to map the use of tools by one of the capuchin monkey species (Cebus Libininosus) in the state. The yellow-breast capuchin monkey (Cebus xanthosternos), an endangered species, has been the target of studies in the south of the State of Bahia. “The person responsible for this research was one of our trainees, who studied the capuchin monkeys that live in the Parque Ecológico do Tietê park,” says Ottoni. Massimo Mannu, a student in the doctoral program run by Ottoni, observed that the capuchin monkeys living in the Serra da Capivara mountain range in the State of Piauí use several tools at the same time, such as sticks to dig out lizards from their hiding places and stones to gather roots, something which is uncommon even among chimpanzees. “It is essential to expand the scope of the research to be able to state that the use of tools is a cultural tradition,” says Patrícia Izar.

The expansion of those studies has already shown evidence that capuchin monkeys’ development of cultural traditions is not limited to the use of tools. In a study published in February in Swiss journal Folia Primatologica, Brazil’s Antonio Christian de Moura, from the Federal University of Paraíba/ UFPB, discovered what capuchin monkeys living in the Serra da Capivara mountain range do to drive away the threat of predators: they promote a percussion symphony by beating stones on the ground. According to the researcher, this is the only species in which this kind of behavior was observed. “Beating objects on a surface seems to be an innate characteristic which can be shaped into social behaviors for new functions. When the stone is being beaten on the ground, the noise becomes an efficient alarm”, he stated. In the previous observations, this drumming had only been manifested by the monkeys to look for or break open fruit, especially among groups in captivity. “This time, this kind of behavior was witnessed in a wild group. The absence of this action in other populations of the same species, with access to stones, suggests that beating stones could be a social tradition of the population being studied”, he said. Researchers should take this into account.

The Project
The use of tools and the act of  foraging by capuchin monkeys (Cebus apella): sociability, ecology and the social transmission of information
Modality
Regular Line for Research Aid
Coordinator
Eduardo Ottoni – USP
Investment
R$ 212,375.15 (FAPESP)

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