Primates in a Brazilian national park spend 41% of their time on the ground. Territoriality influences stone tool use, the behavior of females while on heat, and care of disabled individuals (photo: Tiago Falótico)

Published on 08/14/2023

By Karina Ninni  |  Agência FAPESP – In an article published in the American Journal of Biological Anthropology, primatologist Tiago Falótico and ethologist Eduardo Ottoni correlate diversity of tool use with terrestriality in a group of monkeys living in Serra da Capivara National Park in Piauí state, Northeast Brazil. According to Falótico, these monkeys differ significantly from any others observed previously in the ways they use tools. 

“We found that this group of Bearded capuchin monkeys [Sapajus libidinosus] in Serra da Capivara spend 41% of their time on the ground. That’s an unusually high proportion. Neotropical monkeys are almost all arboreal, so there are few studies on this topic. According to the literature, Neotropical primates normally spend less than 1% of their time on the ground. Now we’ve determined that these monkeys are mostly terrestrial in the Cerrado [savanna-like biome in Central Brazil] and Caatinga [semi-arid biome in Northeast Brazil] and have hardly been studied at all,” Falótico said. He is a researcher at the University of São Paulo’s School of Arts, Sciences and Humanities (EACH-USP) in São Paulo state, Brazil.

These monkeys differ markedly from others in terms of the context for their tool use, he said, comparing them with a group that inhabit Fazenda Boa Vista, also in Piauí. “In that area, they use tools only to crack open seed pods and palm nuts. They spend 27% of their time on the ground, already a lot for these primates. In Serra da Capivara, they not only crack open nuts and seeds with stones but also use stone tools to dig for spiders, roots and other food. In addition, they bang stones together to communicate aggression and threatening behavior,” he said.

In another article, published in 2013, the two scientists showed that females in this specific group inhabiting Serra da Capivara even used small stones for sexual display. “They throw pebbles at males to draw attention. When female capuchin monkeys are in heat, they vocalize and use facial expressions to attract males, but this group innovated by casting stones,” he recalled.

The correlation between terrestriality and tool use was a hypothesis. “Some populations of capuchin monkeys use tools because they need to. They have to dig to find food, which is scarce. We and other groups had previously advanced an ‘opportunity’ hypothesis, according to which they use tools when pebbles and food are available. In this study, I set out to investigate whether this population, which had more diverse tools, was also more terrestrial, and compared them with the group inhabiting Fazenda Boa Vista, which is in the same region. Both groups use tools, but the Serra da Capivara group uses a much greater diversity,” he said.

Time and resources

The longer the monkeys stay on the ground, the more opportunities they have to make use of the available resources, and to innovate, as in the case of the stone-throwing females, he explained. “They have to be on the ground a lot to have time to innovate like the Serra da Capivara group, which even uses tools to dig,” he said.

Terrestriality is not the only factor that influences tool diversity. “Resource availability is another. Fazenda Boa Vista has fewer stones, and this could also influence tool use. On the other hand, we know stone size limits tool use. Fazenda Boa Vista has large stones and the monkeys that live there crack open large palm nuts. If large stones are available, so are small ones, but they don’t use them to dig, unlike the monkeys in Serra da Capivara,” he said.

In the study, the researchers measured ground use by means of scan sampling – watching the animals and writing down what they were doing at certain intervals. “We followed the group for two years and observed them practically every day. There were 30 to 40 individuals, half adults and half immature. Every 20 minutes we took notes on the activities of all of them. This is a basic methodology for studying the behavior of social animals,” he said. “In addition to tool use, I was interested in what they ate, when and how they groomed each other [cleaning, stroking and massaging], and when and where they moved about, especially on the ground. In this case, I made note of the substrate. All these results were grouped by season – rainy and dry – and by individual – adult, juvenile, male, female.”

Among the hypotheses raised in the scientific literature is the possibility that females are risk-averse and spend less time on the ground, but Falótico and Ottoni could not prove this theory. “We found no difference between the sexes in time spent on the ground. There was only a small difference in time spent on the ground by the group as a whole, which was 41%, and time spent on the ground by adults only, which was 43%,” Falótico said.

The study was supported by FAPESP via a doctoral scholarship in Brazil, a Regular Research Grant and a Young Investigator Grant.

Falótico plans to investigate whether the correlation between terrestriality and tool use diversity also applies to a third group of capuchin monkeys. “It’s a population we’re studying in Ubajara National Park, in Ceará state. Again, we’re interested in the influence of terrestriality and perception of ground risk on tool use. We want to try to observe how they respond to perceived risk and whether they’re more attentive to possible threats while they’re on the ground,” he said.

Adapted care

An article on the Ubajara National Park study has also been published recently in the journal Primates. Falótico’s co-author in this case is Tatiane Valença, a PhD candidate in experimental psychology at EACH-USP. The article provides a detailed account of the interactions of a mother and other group members with her infant before and after its death. The baby had a disabled leg and lived only two months. According to the authors, terrestriality may also influence the behavior of these monkeys toward disabled, injured or sick members of the group.

“Our main contribution in this case was observing how the female dealt with this individual who behaved differently. There was nothing in the literature about care of disabled or defective offspring before death. Ours was the first such account for capuchin monkeys. This care differed little from the known repertoire but with some adjustments. The baby was unstable on its mother’s back and couldn’t hold on like the others, so the mother had to adjust its position more frequently. Adjusting the position of an infant is normal behavior, but in this case she did so far more frequently than usual. An adult male who also carried the disabled infant occasionally increased the frequency of adjustment, too,” Valença said.

The novelty is the hypothesis that terrestriality may have influenced the evolution of behavior toward defective individuals. “The hypothesis that arboreality makes carrying dead individuals more difficult had been raised in the literature, but we’re now proposing the hypothesis, based on our observations, that this could affect care of the disabled or sick,” she said.

Carrying a dead infant is common. “The mother’s bond with her offspring, which includes carrying and grooming, normally persists even after the death of an infant, but its duration varies. This female carried the body for hours and didn’t forage during all that time, apart from eating flies removed from the corpse. She didn’t pick fruit or look for invertebrates. She didn’t feed at all.  She carried a corpse with 14% of her own weight for over 1 km,” Valença recalled.

This kind of behavior has been observed in terrestrial monkeys such as chimpanzees and Long-tailed macaques (Macaca fascicularis). “Some females leave the corpse of a dead infant behind after a few hours. Others carry it for days. There have been extreme cases of chimpanzees doing so for months,” she said.

Another type of care observed in the case of the female capuchin was use of her tail to hold the infant while she was cracking open husks and hulls. “These animals typically keep balance while foraging by placing their tail on the ground or using it to hold on to the tree they’re in. Cracking open a nut or seed with a stone requires fine manipulation and strength. This female sometimes lifted her tail, and we assumed she was doing so to hold on to the infant, which was particularly unstable while she was cracking open nuts and seeds. She couldn’t balance so well without using her tail,” Valença said.

“This third population in Ubajara National Park has access to many pebbles and stones on the ground. It will be very interesting to compare it with the group in Serra da Capivara, because we’ll be able to control for the variable ‘lithic resource availability’,” Falótico said.

The article “Greater tool use diversity is associated with increased terrestriality in wild capuchin monkeys” is at: onlinelibrary.wiley.com/doi/10.1002/ajpa.24740. 

The article “Life and death of a disabled wild capuchin monkey infant” is at: link.springer.com/article/10.1007/s10329-023-01052-1. 

 

Source: https://agencia.fapesp.br/42137