Disease outbreak experience alters food safety behaviors in macaque monkeys

In the early days of the COVID-19 pandemic, many households wiped down groceries with disinfectant before putting them away. Hand sanitizer was in short supply. With little information on how the virus spread – people became more cautious of germs from other people. A new University of California San Diego study suggests that humans may not be alone in changing behavior after experiencing a disease threat.

Researchers found that macaque monkeys who had lived through a deadly disease outbreak became significantly more cautious about food that appeared contaminated, even though they did not know how the disease had spread. The findings suggest that pathogen-avoidance behavior can be shaped by experience, offering clues about the evolutionary roots of disgust. 

The study, published in Royal Society Open Science, provides new insight into what scientists call the "behavioral immune system" - a collection of behaviors that help animals avoid infection before the body's biological immune system ever has to respond. 

We can show now, in non-human primates, that this is the same for them. 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."

Federico Rossano, associate professor, Department of Cognitive Science, UC San Diego's School of Social Sciences and senior author of the study

A deadly outbreak creates a natural experiment

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 researchers 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, to preserve visual cues 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. This allowed the researchers to ask whether experiencing an outbreak - even without becoming sick - could change the animals' 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. 

Earlier research had shown that macaques aren't 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.

However, the researchers found that macaques from groups that had experienced the outbreak were far less likely to eat the food from the contaminated surface. They ate from what appeared to be a contaminated surface in just 47% of trials, compared with 79% 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."

The monkeys did not have to know what made them sick

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 who 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.

A Japanese macaque from a group that experienced a deadly disease outbreak encounters two pieces of food - one placed on a clean surface and one placed on a surface with a visual cue of contamination. In this trial, the macaque passes on the food from the contaminated surface.

Early life experience can shape how cautious monkeys are when it comes to contamination 

The researchers also found that pathogen avoidance was linked to early-life experience.

In an additional study reported in the same paper, they tested 54 macaques from seven species with different rearing backgrounds, including sanctuary-born animals, former laboratory research animals, zoo-born animals and former pets. The researchers observed that 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. 

What does this tell us about disgust?

The findings shed light about the evolution of disgust. While the researchers did not measure disgust directly, they found that macaques' avoidance of potential sources of infection can change with experience, similar to what is seen in humans. 

Human disgust is often thought to have an important role in protecting us from pathogens. We recoil from feces, spoiled food and other potential sources of infection, and our sensitivity to those cues can change depending on context.

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.

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 that may change how people behave even after the peak of that threat has passed.