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Primate life

The matriarchs of the forest

Co-existence with the mother increases the reproductive success of the male muriquis

That hug: Yago, Leo, Evita and Elvis in a moment of relaxation

DANIEL DA SILVA FERRAZThat hug: Yago, Leo, Evita and Elvis in a moment of relaxationDANIEL DA SILVA FERRAZ

The muriquis [woolly spider monkeys], the largest monkeys in the Americas, and candidates for mascot of the Olympic Games to be held in Rio, have a very particular sexual behavior. During the mating season, the majority of males copulate with all the fertile females in the group, except for their own mothers. The North-American anthropologist Karen Strier identified this sexual behavior pattern, which is unusual among the primates, in the 1980s, when she began to study the muriquis from one area of the Atlantic Rainforest in the State of Minas Gerais. And one question has always bothered her: in the midst of so much sexual freedom, who are the fathers of the infant monkeys?

Only now, three decades later, does it appear that Karen and her collaborators have found the answer. In the groups of muriquis there is not one, but various fathers – although each infant obviously has just one father. This information is important because it could help preserve this Brazilian monkey, which is at risk of extinction.

Presented in the November 22 issue of the journal Proceedings of the National Academy of Sciences (PNAS), this result is not as obvious as it may seem, given that, in many animal species, including monkeys, it is common for a single male to be the father of almost all offspring.

It was necessary to wait for advances in genetic testing, which can nowadays analyze minute quantities of DNA extracted from blood or feces, in order to determine that muriquis have a standard of paternity that is very different from that of other monkeys.

In order to carry out the study, Karen selected 22 infant monkeys born between 2005 and 2007 and entrusted the biologist Paulo Bomfim Chaves, who was doing his PhD at New York University, with the task of collecting their genetic material, from their mothers (21 females) and their possible fathers (24 males). After this had been done, with the help of researchers from the Federal University of the State of Espírito Santo (Ufes), they cross-referenced the genetic data with information on the life history and sexual habits of these monkeys, which live on the Feliciano Miguel Abdala reserve, in the municipality of Caratinga, in the eastern part of the State of Minas Gerais.

The analysis showed that 12 out of the 24 males in the group had fathered at least one child. The most successful of the males was the father of just 4 infant monkeys, which translates into 18% of the babies. According to the North American anthropologist, this paternity pattern is a consequence of the social structure of the muriquis, which are well-known for their peaceful nature and for forming societies in which there seems to be an absence of any visible power struggles.

In societies with a rigid hierarchy, such as that of gorillas, the largest male gorilla – the alpha male – usually imposes his will by force and may be the father of as many as 85% of the infant monkeys. Even among the bonobos or pygmy chimpanzees (the chimpanzee’s peaceful cousins), the number of offspring that a male usually fathers is higher. The most prolific of these monkeys, who do not have fixed partners and copulate even when the females are not in heat, is usually the father of 30% of the infant monkeys – almost double the rate seen in the case of the muriquis.

For some time, Karen and her collaborators had suspected that there was no predominance in terms of paternity among the muriquis. But they lacked the data that would enable them to state that the infant monkeys born seven months after mating – each female gives birth to just one baby at a time – did indeed have different fathers. “The genetic data has confirmed what behavioral observations had been indicating”, explains the anthropologist, who is a researcher at the University of Wisconsin.

Although open competition was not observed among the muriquis, it was not possible to rule out the hypothesis that the dispute occurred in some other way or even at the cellular level – for instance, the sperm of a specific male might be faster than those of the others. There could also be other forms of social interaction that the researchers had failed to register once the monkeys had gone off into the forest. The article in PNAS does not completely eliminate these possibilities, but it makes them extremely unlikely. This study, conducted jointly with the primatologist Sérgio Mendes and the geneticist Valéria Fagundes, both from Ufes, and the anthropologist Anthony di Fiore, from the University of Texas, produced two other observations that could help with the preservation of the muriquis.

042_Muriquis_190-1The first is that, even though they practice free love, male muriquis do not copulate with their own mothers – at least, they do not produce offspring with them. This is an important observation because mating between blood relatives reduces the genetic diversity of the species and makes it more vulnerable to disease.

“When we reanalyzed the behavioral data, we saw that this result made sense”, states Karen. Years ago she had observed that in general it is the females who seek out a new group when they reach puberty. The males remain in the company of their mothers, in the same group as their father, grandfather and uncles on their father’s side. “We do not know whether the mothers do not allow their sons to copulate with them or whether they simply do not regard them as being attractive”, explains Karen.

The second and most intriguing observation is that, although there is no clear predominance in terms of paternity, certain males are more successful than others from the reproductive point of view. Some have three or four offspring while others have none. When they looked into the reason for this difference, the researchers found that the males that fathered the greatest number of offspring were those that, after becoming adults, spent more time in the company of their mothers when the group was all together. “Closeness to the mother appears to benefit certain males, but we do not yet know how or why”, declared Karen.

This is a very different form of influence from that observed, for instance, among the bonobos or pygmy chimpanzees. These monkeys form societies ruled by females in which the mothers choose the mates for their sons and help them stand up against the other males in the group. If this is proven, the maternal influence might indicate that the female muriquis are discrete matriarchs and that their sons learn to deal with the other females by watching their mothers. Or even that the more prolific male muriquis take advantage of the network of their mothers’ contacts in order to mate with more females. “We are beginning to look at the interactions between mothers and their adult male offspring”, Karen confirms.

Almost everything that is known about the behavior of the muriquis is recent knowledge, built up over the last 30 years, to a large extent triggered by the work of Karen, who arrived in Caratinga in 1982 at the suggestion of her PhD supervisor at Harvard University, the primatologist Irven DeVore. A baboon specialist, he found out at that time that a group of monkeys that was almost extinct had been discovered in Caratinga. With help from the primatologists Célio Vale, who at the time was a professor at the Federal University of the State of Minas Gerais, and Russell Mittermeier, of Conservation International, Karen began the longest monitoring study of the muriquis carried out to date.

Since the very first time that she entered the 957 hectares of forest of the Montes Claros Farm in Caratinga, Karen has been helping to construct the biography of the muriquis and to redirect actions aimed at the preservation of this primate. “Before these studies, almost nothing was known about the muriquis”, says Mendes.

After implementing a long term study of the northern muriquis (Brachyteles hypoxanthus), which have a grayish yellow coat and pink spots on their faces, by the end of the 1980s she was already at the Carlos Botelho State Park, which covers an unbroken area of Atlantic Rainforest 40 times larger than that found in Caratinga, and which is located in the State of São Paulo. There she got to know the southern muriquis (Brachytheles arachnoides), which have yellowish brown fur and completely black faces.

Karen then decided to undertake a study in the São Paulo State park similar to the one that she was carrying out in Minas Gerais. The aim was to compare the way of life of the animals in a small area, such as Caratinga, with that of those that lived in a larger, better preserved forest area. “She was a pioneer in the sense that she was the first person to undertake long-term monitoring studies of the muriquis”, comments Mauricio Talebi, a bioanthropologist from the Federal University of São Paulo (Unifesp) in the town of Diadema.

Talebi worked with Karen in the early 1990s and since 1993 has been coordinating the studies at Carlos Botelho State Park, in the municipality of São Miguel Arcanjo, 180 kilometers away from the São Paulo state capital. Since he arrived there, he has been investigating not just what the muriquis eat, but more importantly, why they eat what they eat and what strategy they use to select foods.

Female breastfeeding an infant

FERNANDA P. TABACOWFemale breastfeeding an infantFERNANDA P. TABACOW

During the 20 years that he has been following these animals, Talebi has identified distinct habits between the Minas Gerais based muriquis and the São Paulo based ones which cannot be explained simply by the fact that they belong to different species. One of the differences is that the monkeys in the Carlos Botelho State Park eat a lot more fruit and flowers than the monkeys on the Caratinga reserve, which feed almost exclusively on leaves.

While he was doing his PhD at Cambridge University in England, Talebi came to the conclusion that the most important factor in the diet of the muriquis is the availability of food. In Caratinga, the animals live in a small fragment of Atlantic Rainforest, where the trees shed their leaves in the dry season and where there is less fruit available. Carlos Botelho State Park, which contains the largest unbroken expanse of Atlantic Rainforest in Brazil, is located in the Paranapiacaba Range, which has a high level of humidity throughout the year and where the trees are always green.

It was also recently confirmed by Talebi, in partnership with Phyllis Lee, from Stirling University in Scotland, that the muriquis’ diet also varies according to gender. Even in Carlos Botelho State Park, the males eat more leaves than the females, who prefer fruits and flowers. Talebi attributes this difference to nutritional requirements. The females, he explains, need a lot of energy and nutrients in order to give birth to infant monkeys and to produce milk. From the flowers they get phosphorus, potassium and magnesium and from the fruits, they get high sugar content. “The leaves contain a great deal of protein, but on the whole they are harder to digest”, states Talebi.

He and Rebecca Coles both suspected that the environment also influences the way in which the muriquis look for food and the time that they spend on different activities. Environmental conditions may also have favored the appearance of a genetic characteristic that Talebi, Peter Lucas and Nathaniel Dominy discovered only exists among a few females, namely, the ability to detect colors – male muriquis and the majority of females only see shades of grey. “The ability to see colors may help these females to find better foods and to produce more offspring”, explains Talebi.

“This work is crucial for the conservation of the muriquis”, states Leandro Jerusalinsky, head of the National Center for Research and Conservation of Brazilian Primates. “The simple presence of researchers in the areas where the monkeys live, per se, inhibits degradation of the forests and hunting, which is a common cultural habit in many parts of Brazil”, he says.

Despite the significance of the work that Karen began, she was not the first person to study the muriquis. That honor went to the agricultural engineer from the State of Espirito Santo, Alvaro Aguirre, a specialist in handling wildlife who worked for the Ministry of Agriculture, and who in the 1960s was responsible for bringing the muriquis back on to the map of the 116 species of primates that can be found in Brazil. In his travels across the country, Aguirre came across 32 populations, consisting of an estimated total of between 2,100 and 2,200 muriquis, spread across seven Brazilian states, stretching from the north of Paraná to the south of Bahia.

When the muriquis were first described, almost 150 years earlier, French and German naturalists included them in the Ateles genus, which is the same as the spider-monkey. Étienne Geoffroy Saint-Hilaire called the monkeys that he described in 1806, which had light colored coats, black faces and hands in the shape of a hook, Ateles arachnoides. Fourteen years later the German naturalist Heinrich Kuhl classified the animals as distinct from the former group because of their pink faces and genital organs, in addition to a micro thumb, which was absent from the first group, as being another species, which he named Ateles hypoxanthus. In 1823 another German, Johann Baptiste von Spix, proposed that they both belonged to a new genus, Brachyteles, which has since been accepted.

042_Muriquis_190-2In spite of everything that has been learnt since the 1980s about the way of life of the muriquis, the situation of the two species has not improved much over the last 50 years. Fabiano Rodrigues de Melo, an environmentalist from the Federal University of Goiás, who heads up one of the groups that are working to produce a census of the muriquis in the States of Minas Gerais and Bahia, estimates that there are at most 2,400 muriquis in the wild, not much more than Aguirre had estimated. “The total number of animals has remained virtually constant”, says Melo. “What is worrying is that the number of populations is decreasing”.

In the forests in the States of Minas Gerais and Bahia, Melo even managed to find two populations that had not been described by Aguirre. However, he was unable to find any muriquis where they were previously known to exist, such as in the Ilhéus region in Bahia. There are currently just 12 populations of northern muriquis, which it is calculated in total add up to less than a thousand individuals. Talebi, who is carrying out the survey of the southern muriquis, estimates that there are 15 populations of this species, with a total of 1,500 monkeys. Although he suspects that there may well be additional populations, one of the problems, according to Melo, is that a number of these are very small, consisting of less than half a dozen animals, which may make it impossible for them to carry on for much longer without conservation actions.

In 2010, the protection of the muriquis was given backing by federal legislation. A directive from the Chico Mendes Institute for the Conservation of Biodiversity approved the National Plan for the Conservation of the Muriquis (PAN Muriquis). This plan, the first of its kind at a national level for the protection of a primate, establishes 10 targets for the protection of the two species of these monkeys. The aim is to reduce, by 2020, the extinction risk level of the northern muriquis from critically endangered to endangered, and of the southern muriquis from endangered to vulnerable. “The preservation of the muriquis is no longer just a researcher’s dream but is now a state policy”, says Talebi, one of the persons responsible for the creation of the PAN-Muriquis.

To ensure that the plan does not merely remain on the drawing board, says Jerusalinsky, one of the co-authors of the conservation project and coordinator of the PAN Muriquis, it will be necessary that the actions succeed in involving not just researchers and environmentalists, but also landowners and residents of the regions in which the muriquis live. “Many populations of these species are located in conservation areas and, theoretically, are more protected”, he says. “But various others are live on private properties, which may register decreases in their native vegetation area if some of the alterations to the forestry code that have been proposed are approved”.

One strategy that looks interesting and that might complement the demarcation of preservation areas is to transfer females that are about to reach reproductive age to other groups. In 2005, Sérgio Mendes’ team captured Renata, a female who was living in a small stretch of forest in Santa Maria de Jeribá, in the State of Espírito Santo and was at the beginning of puberty, and about to leave her own group. The researchers took her to another forest, where there was another group of muriquis . After three years, Renata had her first baby, a female named Rubi, and in 2010 her second baby, Régia. “The birth of these infant monkeys proves that the strategy works”, says Mendes. “If we had tried this 30 years ago it probably would not have worked, because the trend at that time would have been to transfer a young male, which in the case of other primates, is the one that usually migrates”, he explains.

Fabiano Melo repeated the test in Minas Gerais in 2006 with the female Eduarda, who has also had two babies. On November 30, Melo left with a team for the municipality of Simonésia, which lies close to the border between the States of Minas Gerais and of Rio de Janeiro, where it is their intention to capture a female muriqui who is isolated in a very small area of forest. The idea is to take her to the Belo Horizonte zoo, where she will provide company for Zidane, a male who, like the famous forward of the French soccer team, has given the researchers a lot of trouble. If all goes well, this will be the first northern muriqui colony in captivity, which is essential to ensure that at some unspecified date in the future it will be used to supply new specimens for the wild.

Scientific articles
STRIER, K. et al. Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. PNAS. v. 108, p. 18. 915-19. 22 Nov. 2011.
COLE, R.C. et al. Fission- Fusion Dynamics in Southern Muriquis (Brachyteles arachnoides) in Continuous Brazilian Atlantic Forest. International Journal of Primatology. Forthcoming.
TALEBI, M.G.; LEE, P.C. Activity Patterns of Southern Muriquis (Brachyteles arachnoides) in the last continuous remnant of Brazilian Atlantic Forest. International Journal of Primatology. v. 31, p. 571-83. 2010.

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