Gut Check: Mandrills Sniff Poop to Avoid Peers With Parasites

Researchers have documented one of the first instances of social avoidance in a non-human animal

You can't sit with us. You smell like poo. (Alice Percher / Science Advances)

For humans, disgust can be a powerful evolutionary force. In many ways, it works to keep us safe: Repulsion can cause us to discard damaged fruit (which might have worms in it), refuse to eat spoiled meat (which could hold tapeworm eggs) or avoid unwashed people (who could potentially carry lice). This reaction is so powerful that it can counteract logical reasoning—according to one study, people rejected fudge molded in the shape of dog poop, despite being completely aware that it was just fudge.

But the tendency to avoid gross and potentially harmful things may not be just limited to humans. At France’s Center for Functional and Evolutionary Ecology, a team of scientists has long been studying the evolution of social behavior in primates in a population of roughly 160 mandrills. This species of monkeys is known for its mutual grooming behavior, in which two monkeys will help clean each other's fur in a way that can reduce stress and help build social bonds.

However, the monkeys tended to avoid grooming certain monkeys at certain times, says Clémence Poirotte, a spatial ecology researcher there. Poirotte and her team suspected that the monkeys could be engaging in some kind of quarantine behavior. But they wanted to know: How did the mandrills know which of their peers were infected with parasites, so they could effectively avoid them?

In 2012, they decided to intensively monitor a group of 25 monkeys for 2.5 years to find out. The researchers documented how often each monkey was groomed by its peers in a month, documenting which ones would get shunned and which ones wouldn't. To see which monkeys were infected, they also collected fecal samples for all of the monkeys, which tend to be the main medium for transferring intestinal parasites like the protozoan Balantidium coli. Then they tracked which—if any—parasite infections appeared to correlate with less grooming time.

It turned out that getting infected with B. coli seemed to drive away other mandrills. "Parasitized individuals are less groomed by others," Poirotte concludes in a new study published in the journal Science Advances. Skin swabs found that the anal area of the infected mandrills was rich with potentially contagious B. coli. Not to get too disgusting, but healthy mandrills spend roughly 9 percent of their grooming time focusing on that specific area, according to the study, so grooming an infected monkey would put a mandrill at risk of getting infected itself.

So how did the monkeys know which individuals to avoid? They had developed a highly effective strategy: Smell their poop. Prior studies have found that mandrills have a powerful and sensitive sense of smell, which they use to detect chemical signals related to mating and social cues. And the new analysis of feces from infected mandrills found significant changes in the chemistry of the feces compared to healthy mandrill feces.

Mandrills didn’t seem to like poop with parasites: When researchers smeared two types of feces on sticks and presented them to the mandrills to inspect, they physically recoiled at infected ones, Poirotte says.

Mandrill Grooming 2
Grooming is an important social behavior for most primates, including mandrills. However, it can potentially spread parasites. (Nory EL Ksabi / Science Advances)

It may not be pretty, but having an olfactory cue to avoid sick individuals is a crucial strategy for avoiding parasites, which comprise up to half of the world's estimated 7.7 million species. These freeloaders use other species for protection, food and transport, generally to the detriment of their hosts. However, parasites can't usually live solely off one host animal—because if that animal dies, they lose their main source of sustenance.

Instead, they try to spread their spawn to other members of their host species, often through mediums like feces and other bodily discharge. Animals that lead social lives, therefore, are most at risk. "Parasite transmission is one of the major costs linked to sociability," says Poirotte says. Parasites would have a much harder time spreading if every one of its hosts kept to themselves, but then those host animals would lose all the benefits of being in a herd or having social relationships.

Parasites have evolved a number of strategies to make this spread successful. Some are fairly straightforward; lice, for example, make their homes in human hair, and usually can only spread by crawling or falling into another person's hair with head-to-head contact. Others techniques are downright demonic: some parasites hijack the brains and nervous systems of animals to make Artemia shrimp get eaten by flamingos, crickets drown themselves, and cockroaches become the enslaved hosts for parasite eggs.

In response to these atrocities, host animals too have gotten creative with their survival strategies. Biologists have documented a long-running "evolutionary arms race" between the two, with hosts constantly developing new defenses against the parasites’ changing survival strategies. Hosts employ strategies from healing saliva (which animals can use to cover wounds and prevent parasites from colonizing) to tail-swatting instincts (which ward away bloodsucking insects) to immune system defenses (which can kill parasites more effectively).

Behaviors like social avoidance represent yet another kind of anti-parasite defense, part of what University of British Columbia psychologist Mark Schaller has dubbed the "behavioral immune system.

What does that entail, exactly? "It's a suite of psychological mechanisms designed to detect the presence of disease-causing parasites in our immediate environment, and to respond to those things in ways that help us to avoid contact with them," Schaller wrote in an article for Scientific American.

While not directly applicable to humans, Poirotte says that this study does throw into relief the great lengths that humans go to in order to stay far away from each other’s bodily waste. Pipes and waste treatment facilities are a kind of avoidance strategy to avoid any contact that could lead to potential sickness, she points out.

The study marks “a significant contribution to the field," says Martin Kavaliers, a behavioral neuroscientist at Canada's Western University. Kavaliers, who wasn’t involved in the study, adds that it’s one of just a few studies that have confirmed social avoidance behavior in animals. Some human studies have also found that the odor of a person injected with a bacteria-produced endotoxin is more repulsive to other people—perhaps representing a similar defense against getting too close to sick people.

Next, Poirotte plans to look more closely at why some of the mandrills appeared more adept at avoiding infected peers than others, and whether this helped them stay healthy. In the future, she also hopes to study gray mouse lemurs, a small primate species in Madagascar that appears to be succumbing to increasing parasitic infections as it loses its habitat to deforestation, to see whether the species is evolving any behaviors to compensate for this.

If you find yourself the unintended host for a parasite in the near future, don’t lose hope. Fortunately, in mandrills as in humans, social avoidance generally doesn’t last forever. In the study, the researchers actually cured 16 monkeys of their parasitic infections with medication and found that they shortly started receiving much greater amounts of grooming again, says Poirotte.


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