Macaques That Lived Through a Deadly Outbreak Avoid Contaminated Food

Macaque monkeys that lived through a deadly disease outbreak became markedly more reluctant to eat food that appeared contaminated, even though the virus that swept through their groups was never spread through food, according to a new study from the University of California San Diego. The research, published in Royal Society Open Science, suggests that pathogen-avoidance behavior can be shaped by direct experience of an epidemic, offering clues about the evolutionary roots of disgust and what scientists call the behavioral immune system.

The behavioral immune system is a collection of behaviors that help animals avoid infection before the body’s biological immune system ever has to respond. In humans, this often takes the form of disgust: we recoil from feces, spoiled food and other potential sources of infection, and our sensitivity to those cues can shift depending on context. Whether non-human primates show a comparable, experience-driven flexibility has been difficult to demonstrate. The new findings indicate that, in macaques at least, exposure to others getting sick and dying changes the likelihood of engaging in behaviors that could lead to sickness, even when the animals have no knowledge of how disease is transmitted.

“We can show now, in non-human primates, that this is the same for them,” said Federico Rossano, an associate professor in the Department of Cognitive Science at UC San Diego’s School of Social Sciences and senior author of the study. “Even with no knowledge of how disease is transmitted, being exposed to others getting sick and dying changes the likelihood of engaging in behaviors that potentially could lead to some form of sickness.”

The research grew out of an unexpected event at a primate sanctuary in southern Texas, where the researchers conduct behavioral studies. The sanctuary is home to several groups of Japanese macaques descended from monkeys originally brought from Japan to Texas in 1972. Because the groups live in separate enclosures, the team had a rare opportunity to compare animals with similar backgrounds that had experienced very different social and disease environments. In 2020, staff confirmed the presence of simian retrovirus Type II, which can cause an AIDS-like immunodeficiency, in some of the sanctuary’s Japanese macaque groups. The virus was primarily transmitted through bites and scratches and caused severe illness and death in some animals. The sanctuary responded by separating groups and implementing strict testing and quarantine measures.

That created an unusual natural experiment. Three groups had experienced the outbreak. One group had not. The researchers then tested 55 macaques to see how they responded to a choice between food placed on a clean wooden surface and food placed on a surface covered with real macaque feces sealed under a layer of clear epoxy. The epoxy preserved the visual cues of contamination while removing the smell and any risk of infection. Within the outbreak-exposed groups, some individuals had been infected while others had lived alongside sick monkeys without becoming infected themselves, allowing the researchers to ask whether experiencing an outbreak, even without becoming sick, could change behavior. In some trials, the clean surface was replaced with a brightly colored kitchen sponge to determine whether the animals were simply avoiding unfamiliar objects.

The results were striking. Macaques from groups that had experienced the outbreak were far less likely to eat food from the contaminated surface. They ate from what appeared to be a contaminated surface in just 47 percent of trials, compared with 79 percent of trials for monkeys from the group that had never experienced the outbreak. Importantly, monkeys from outbreak-exposed groups behaved similarly whether or not they themselves had been infected. That suggests the behavioral change was associated with having lived through the outbreak, rather than actually experiencing illness. “Groups have histories, and those histories show up in behavior,” said Stephan Kaufhold, who led the study as a doctoral researcher in Cognitive Science. “Living through the disease outbreak appears to have made those monkey groups more cautious around food that looks contaminated.”

One of the most intriguing aspects of the finding is that the virus was not spread through contaminated food. Instead, it was transmitted through blood and saliva via bites and scratches. Regardless, the macaques that saw their fellow primates get sick, in some cases, became more reluctant to eat food placed on a surface that visually suggested contamination. The study raises a parallel question for humans: could the experience of living through a disease outbreak affect behavior long after the immediate threat has passed? The researchers say the macaque findings cannot answer that question directly, but they provide evidence that experience-dependent changes in pathogen avoidance are not unique to humans.

The study also found that pathogen avoidance was linked to early-life experience. In an additional experiment reported in the same paper, the researchers tested 54 macaques from seven species with different rearing backgrounds, including sanctuary-born animals, former laboratory research animals, zoo-born animals and former pets. Former pet macaques, who grew up living with humans instead of being under the care of other macaques, were significantly more likely to eat contaminated food than sanctuary-born macaques raised by their mothers. “One possibility is that these monkeys didn’t have the opportunity to learn typical avoidance behaviors from their mothers and other macaques early in life,” Kaufhold said. “Even after living with other monkeys for several years, that early experience may still shape how they respond to potential sources of disease.” For the researchers, the findings underscore the importance of giving young primates opportunities to grow up in species-appropriate social environments.

Earlier research had shown that macaques are not necessarily deterred by contamination when the payoff is tempting. Given a favorite treat like a peanut, wild Japanese macaques would still eat food off a feces-covered surface, while avoiding it for less valued food like wheat grains. The new results add a layer to that picture: the willingness to take such risks is not fixed, but can shift after a group lives through a deadly epidemic. Because primates are capable of social learning, the researchers say it is possible that heightened pathogen avoidance could be learned from other group members and potentially persist over time. Future studies could determine whether newly introduced animals adopt the behavior of a group that has experienced an outbreak.

The findings also shed light on the evolution of disgust, although the researchers did not measure disgust directly. What they showed is that macaques’ avoidance of potential sources of infection can change with experience, similar to what is seen in humans. For now, the research offers a new perspective on an experience many people thought they understood all too well after COVID-19: living through a disease may change how individuals behave even after the peak of that threat has passed, and humans, it turns out, may not be alone in that response.

Subject of Research: Experience-dependent pathogen avoidance behavior in macaques after a deadly disease outbreak

Article Title: Like humans, some primates become cautious of germs in the wake of a viral outbreak

Article References: Like humans, some primates become cautious of germs in the wake of a viral outbreak. Original publication (Bibliographic details unavailable.)

Image Credits: AI Generated

DOI: Not provided

Keywords: macaques, pathogen avoidance, behavioral immune system, disgust, simian retrovirus Type II, outbreak experience, social learning, early-life experience, Japanese macaques, Royal Society Open Science, contaminated food, primates