_ Evolution Ancestral branches

The divergence among capuchin monkeys, as old as that between humans and chimpanzees, is reflected in their ecology and behavior

Maria Guimarães published in july 2012

32  especial issue october 2012 apuchin monkeys inhabit Central monkeys at a conference held in Japan in 2010. America, the entire Amazon Region, The meeting and the contributions of the gath- the cerrado savannas, the caatinga ered researchers resulted in a special issue of the scrublands and the Atlantic rainforest, American Journal of Primatology, published in extending all the way to Argentina. April of this year. CWithin this territorial range, the monkeys vary While studying the behavior of these mon- greatly in their shape, color, size, food prefer- keys in Caratinga in Minas Gerais state, Jessica ences and behavior. Capuchins are outstanding noticed differences compared to these species in exhibiting complex social systems and other locations, but no evolutionary context was a rare skill – the ability to use tools. Despite the available in which to assess the origin of these large variation between species, until recent- dissimilarities. “We didn’t know how long the ly, experts classified the gracile capuchins, also groups had been separated or anything about known as caiararas, and the capuchin monkeys the relationship between them,” she says. Today, as belonging to the same genus, Cebus. Most of the she studied are classified as Sapajus these monkeys were scientifically registered as nigritus, which is different from their prior des- Cebus apella. In the past 10 years, however, the ignation in terms of both the genus and species classification of these primates has undergone names. In 2001, the initial push for change came a revolution based on the findings of Brazilian from a suggestion made by José de Sousa e Silva and foreign researchers. Prior to this revision, Junior in his doctoral dissertation at the Federal “Their taxonomy was still based on the work of University of Rio de Janeiro. He advocated two naturalists” according to the Brazilian primatol- subgenera: Cebus for the more delicate capuchins ogist Jean-Philippe Boubli, but “the molecular ranging northwards from the Amazon region, and technology era is allowing a full reorganization.” Sapajus for the robust capuchin monkeys, often Boubli, a researcher at the Wildlife Conserva- characterized by a tuft on the head, distributed tion Society, and his American colleague Jessica southwards from the Amazon. “It was courageous Lynch Alfaro from the University of California, of him to propose a division,” says Boubli, “but Los Angeles organized a symposium on these now we can go beyond this.” duardo cesar E photos

Having remained unseen for centuries, the blond capuchin monkeys were rediscovered a few years ago

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1. Sapajus Jessica is convinced that her conclusions are libidinosus correct. Using genetic sequencing and techniques climbs a wall in the Capivara that make it possible to estimate the ramifications mountain range of genealogy trees for these primates as well as 1 accounting for the primates’ current distribu- 2. The tion, her group put forth a proposal regarding white-headed It is only now, a decade later, that the sub-divi- the evolutionary trajectories of these animals. capuchins, inhabitants of sion has been expanded further through the work This hypothesis indicates that the formation of Central America of Jessica, Boubli and their colleagues, published the Amazon River was responsible for creating a in February in the Journal of Biogeography. Cebus north-south divide and isolating the primates liv- and Sapajus have been proven to be sufficiently ing along its waters, thus creating a genealogical different to be considered distinct genera through branch that gave rise to Cebus extensive genetic analyses carried out primarily and Sapajus. It is unclear what in Jessica’s laboratory as well as Izeni Farias’ subsequently took place during facilities at the Federal University of Amazonas the following 4 million years. It (Ufam). The distinction was confirmed, despite was only approximately 2 mil- Genetic data show a similarity in size: the two types of monkeys lion years ago that the group both weigh just over 2 kilograms. More specifi- that gave rise to the more ro- that the robust cally, their study showed that the two lineages bust monkeys spread through- capuchin monkeys separated more than 6 million years ago. This out the Atlantic rainforest, is the same amount of time that was required without leaving descendants and caiarara for chimpanzees and humans to develop from in the Amazon. Their distribu- a common ancestor. This change in the classi- tion along the entire coast of monkeys are fication of these monkeys has been accepted by was rapid and coincid- most primatologists and was published in April ed with species diversification. sufficiently different in the Lista anotada dos mamíferos do Brasil by Approximately 700 thousand to be considered Conservation International; however, opinions years ago, the expansion in the on this topic are not unanimous, as is customary south reached Argentina, near distinct species in scientific circles. In his recently published Iguassu Falls, and turned north, comment on the American Journal of Primatol- where the cerrado savannas in ogy website, Alfred Rosenberger from Brooklyn central Brazil are found. Sub- College in New York claimed that acceptance of sequently, approximately 400 the division within capuchin monkeys was hasty thousand years ago, the robust capuchins re- and somewhat unnecessary. Although he does not turned to the Amazon, where they met their more michael alfaro / ucla / alfaro michael

criticize its genetic foundations, he argues that gracile relatives who, in turn, spread throughout 2 an exaggerated division can create rare species, the northern region around the Andes, reaching

raising more funds for conservation, even if it is Costa Rica in Central America. ico / ip-usp not justified from a scientific point of view. This This relatively recent reinvasion of the Ama- argument is situated more at the philosophical zon region by capuchin monkeys explains the t faló Tiago level, rooted on the fluidity of the species con- low species diversity in the area as well as the 1

cept, which lacks defined boundaries. competition between the two genera that had photos

34  especial issue october 2012 Evolutionary pathways

Genetic analyses have enabled scientists to retrace the trajectory during Cebus and Sapajus evolution over the course of millions of years (left) and to understand how the diversity that is only now being revealed arose. On the right, the proposed distribution of the genera today, showing some overlap in the Amazon region.

2 The branch that gave rise to Cebus spread throughout 2 Macaco Cebus the Amazon region and 3 around the northern end Macaco Sapajus of the Andes mountain range, extending to Central America 4 1 2 1 4 6.1 Ma 3 1 The that 5 gave rise to the capuchin monkeys 2.1 Ma 6 inhabited the 8 western Amazon 7

adani adani Sapajus region more than 6 million years ago 1.1 Ma 1. Sapajus misha G s A misha

o macrocephalus 2. Sapajus apella 3. Sapajus a ção macac 3 The source of Sapajus libidinosus r

ust was an ancestor that 0.5 Ma 4. Sapajus flavius l i Cebus reached the Atlantic Cebus 5. Sapajus Sapajus Rainforest, where xanthosternos diversification occurred 1. Cebus albifrons 6. Sapajus 2. Cebus capucinus robustus laura daviña before these monkeys o 7. Sapajus nigritus fic re-invaded the 0.1253. Cebus Ma olivaceus g rá 6,1 2,1 1,1 0,5 0,125 4. Cebus kaapori 8. Sapajus cay o Amazon region f n i Millions of years ago

been separated for millions of years. “Sapajus from the two sides of the Negro River, which are able to use a wider range of resources, such have been separated for a million years accord- as breaking tougher fruit,” explains Jessica. This ing to genetic data. “At first glance, they look the 6,2 means that when they coexist with their cousins​​ same. But are they different species?” from the north, which is common in the western million years Amazon region for C. albifrons and S. macroceph- To the naked eye alus, the density of the more delicate monkeys is Given the three-dimensional expanse of the Ama- is how long reduced. Boubli examined the genetic diversity zon region, merely collecting material for genetic Cebus and of the Cebus genus more thoroughly in an article analyses is difficult. Furthermore, ecological and published in a special issue of the American Jour- behavioral studies are much more complicated, Sapajus have nal of Primatology, in which he showed that these which is why we are almost entirely ignorant evolved animals, which have not been thoroughly studied, about the animals that live there. Most obser- harbor an enormous diversity. Izeni Farias, who vational studies take place in easy-access areas, separately was responsible for the genetic analyses, was not where monkeys are already acclimated to the surprised. “The distribution is very broad. One presence of humans. In Brazil, this means that would expect a broad variety”. A geneticist, she there have been many more studies performed is head of a project within the program National on Sapajus than on Cebus. And there is much Biodiversity Research System (Sisbiota), which variation among Sapajus species. aims to sample the genetic diversity of Amazo- In an article published in the American Journal nian vertebrates. of Primatology, a group led by Patricia Izar from Boubli, who is experienced in Amazon jungle the Institute of Psychology at the University of walks, sees this genetic analysis as a starting point São Paulo (IP-USP) showed that this variation that will indicate the need for further studies, partially depends on the environment. The team noting that “The interfluves of rivers such as compared S. nigritus from Carlos Botelho State the Jaú, the Purus and others separate popula- Park in São Paulo with S. libidinosus from the Boa tions that may have been isolated long enough Vista farm in the municipality of Gilbués in Piauí. to become species”. One example he observed The ecological differences that were observed in regarding this phenomenon involved monkeys these species are striking: the species from the

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Atlantic rainforest spends most of its time in the crowns of the trees, whereas the other species, from the caatinga scrublands, spends more time 2 on the ground amid less dense vegetation. 1. The juveniles Perhaps because of their naturally more open nuts with stones and use the same type of tools learn through close habitat, the northeastern monkeys were less com- to dig in the sandy soil in search of roots and spi- observation fortable with the presence of the researchers and ders that live in underground nests. Furthermore, 2. A male uses a often made warning cries as if faced with preda- they are also skilled in making and using sticks to stick to collect honey from the tree tors. This increased perception of risk in their obtain honey from hives and ferret bumblebees surroundings may be the reason that the social and other insects from hollow tree trunks. Addi- groups found in this region were more cohesive tionally, they employ long poles to drive out liz- than those in the São Paulo forest. The availabil- ards from cracks in reddish stone walls that rise ity of food, which, surprisingly, was lower in the 50 meters above the ground. “The differences in woods, also affects group structure. In Carlos behavior between groups of the same species in Botelho, the monkeys often disperse in search of similar environments indicate that some tradi- a good meal. However, caatinga palm trees pro- tions may be transmitted through social condi- duce an assortment of nutrient-rich coconuts, tioning,” explains Falótico. Another interesting which demand a certain amount of expertise on application of tools can be observed only among the part of those who seek to eat them due to the females in the mountains of Capivara. They throw requirement of tool use. This behavior is com- rocks at males to get their attention during the monly seen among Sapajus but has never been few days during which they are in heat. observed in Cebus. The blond (S. Flavius),​​ which As noted by Tiago Falótico from IP-USP, was studied in Rio Grande do Norte by Renata “There are very few records of tool use among Ferreira and Ricardo Emidio from the Federal tree monkeys”. In his doctoral work, which was University of Rio Grande do Norte, is another completed in 2011 under the guidance of Eduardo apt user of tools. Only a few studies have been Ottoni, Falótico showed that in addition to the performed with this species, as until recently, the ecological aspect, this behavior is also influenced only evidence of it was found in an eighteenth by group culture. “The monkeys in the Serra da century painting which no one knew if it actu- Capivara National Park have much more varied ally represented an existing . tools than those in Gilbués,” he says, referring to the two sites in Piauí. In Gilbués, the piassava and Alternative skills two types of coconuts (catulé and catuli) can be Even though they do not use tools on a daily basis, quite large and difficult to break. However, the the forest capuchin monkeys do exhibit manual bearded capuchin, Sapajus libidinosus, is not dis- skills, which was shown by the team led by pri- couraged from exploiting these food sources, as matologist Júlio César Bicca-Marques from the it employs stones as large as 3 kilograms (nearly Catholic University of Rio Grande do Sul (PU- its own weight), lifting and knocking this tool CRS) through experiments in Sapajus nigritus on a coconut supported on a flat stone. “The fe- in which bananas were placed in acrylic box- males sometimes even have to jump up and use es on a platform on a private property in Porto the additional force from the descent to break Alegre. This experiment, which was devised by the coconuts,” he observes. anthropologist Paul Garber from the Universi- ico / ip-usp But that’s where the creativity ends at Gilbués. ty of Illinois, a co-author of the article, yielded t faló iago Meanwhile, the groups in the Capivara range, similar results to those obtained by the Ameri- t

where coconuts are not available, open cashew can researcher in Cebus capucinus in Costa Ri- photos

36  especial issue october 2012 ca. In a first version of the challenge, In a study conducted in Tietê Ecological Park “The behavior the monkeys were required to pull a in São Paulo and published in 2007, Tiago Falóti- stick to knock down a banana to reach- co and his colleague Michele Verderane showed differences ing range. The two males in the group that the Atlantic rainforest capuchin monkeys between the learned the trick easily. However, when show a strong preference for ants. Especially in the experiment was altered and the rod the dry season, when there are more ticks, these groups indicate had to be pushed instead, they were not primates take handfuls of ants and rub their body successful. The researcher from Rio with them thoroughly. “The ants release formic that some of Grande do Sul believes that this failure acid, which acts as a repellent for ticks,” says the was not due to a lack of problem-solv- researcher from USP. He and Michele have dem- their traditions ing abilities. “The association is very onstrated this effect by smearing the substance may be passed easy, but they seem to need more time on a finger, inserting it into a bottle of ticks and to let go of the previous learning,” he counting the amount of time and the distance on through explains. In future studies, this inves- over which the parasites walked on the finger. tigator intends to begin the tests with Falótico observed the same behavior in Piauí, learning,” the second version of the experiment where the monkeys also rub millipedes on them- to prove his hypothesis. selves, which act as a source of benzoquinone according to Another very different type of tool and a mosquito repellent. Falótico use involves the rubbing various prod- Jessica gathered other observations that al- ucts, such as fruit or insects, on its own lowed her to map the rubbing behavior performed fur. Until recently, this practice was by capuchin monkeys, showing that the proce- observed more commonly among Cebus than dure is not limited to a cosmetic preference but Sapajus. “As this behavior is observed only spo- has practical and even medical utility. Some of radically among the Sapajus, almost no one had the Cebus albifrons that live in the middle of a enough data to publish,” says Jessica Lynch Alfa- village in the equatorial Amazon region exhibit ro, who aggregated the information gathered by a curious form of such behaviors, as they often various researchers in a review. steal laundry soap to bathe. Overall, the study showed that Cebus are more There are many new findings in the capuchin likely than their cousins to rub almost anything monkey kingdom, but the experts are far from they find on their fur, though they seem to prefer satisfied. In Jessica’s and Boubli’s eyes, they have plant material, such as citrus fruits and leaves. This merely revealed the tip of the iceberg, which is behavior is not as common among Sapajus, which, an indication of how much remains to be discov- particularly in the Atlantic rainforest, restrict this ered. In the Amazon region, where the behavior activity to insects. The choice of rubbing material and ecology of these monkeys are practically un- In the is influenced by whatever is available in the envi- known, genetic information indicates that there scrublands ronment; however, there is an essential difference may be species that have yet to be described. “I of Piauí, the between the two genera. “In Manu National Park hope that the new populations and species we monkeys use stones as heavy in Peru, the Sapajus don’t smear themselves, but discover help make decisions about conserva- as themselves to the Cebus do,” explains Jessica. tion,” says Jessica. ■ crack nuts

Scientific articles LYNCH ALFARO, J.W. et al. Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys. Journal of Biogeography. v. 39, n. 2, p. 272-88. Feb. 2012. BOUBLI, J.P. et al. Cebus phylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys. American Journal of Primatology. v. 74, n. 4, p. 381-93. Apr. 2012. IZAR, P. et al. Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology. v. 74, n. 4, p. 315-31. Apr. 2012. GARBER, P.A. et al. Experimental field study of problem- solving using tools in free-ranging capuchins (Sapajus nigritus, formerly Cebus nigritus). American Journal of Primatology. v. 74, n. 4, p. 344-58. Apr. 2012. LYNCH ALFARO, J.W. et al. Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus. American Journal of Primatology. v. 74, n. 4, p. 299-314. Apr. 2012.

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