Captivity Makes Monkey Microbiomes More Human-Like

Our microbiomes winnowed when we swapped hunting and gathering for cities—and a few months in a zoo will do the same to a monkey.

Monkeys don’t get much more attractive than the red-shanked douc. It looks like it applied a dusting of rouge to its face—a face that is topped by a black cap, flanked by a white beard, and plastered with a permanently innocent expression. From the neck down, it has a black-and-charcoal shirt with a rusty collar, white sleeves, a pair of hipster-red stockings, and a white tail.

Gorgeous. But perhaps slightly less so when you’re running after one, waiting for it to poop.

That’s what Jonathan Clayton from the University of Minnesota did for nine months, in the Vietnamese jungles where the doucs are found. He tracked 66 of them as they scampered through the trees. When they defecated—and for some reason, when one goes, they all go—Clayton and his colleagues ran over to scoop the poop with some pre-labelled  popsicle sticks, one for each individual monkey.

Those sticks captured samples of the doucs’ microbiomes—the thriving communities of bacteria and other microbes that live in their guts. And by comparing these wild communities to those of other doucs living in zoos, he could work out how captivity alters the monkeys’ microbes.

This matters because microbiome changes have been linked to many disorders including diabetes, malnutrition, obesity, inflammatory bowel disease, and more. Doctors are increasingly taking note of these connections, and so are vets and conservationists. “Doucs are highly endangered and don’t survive well in captivity,” says Dan Knights, who led the project. “Jonathan wanted to understand how they might be better cared for.”

To do that, he also collected stools from wild and captive members of another species—the mantled howler, a loud and uniformly black monkey from Central America.

In the wild, both monkeys host different and distinctive communities of gut microbes. But in captivity, these  communities converge, so they become harder to tell apart. Even though doucs and howlers come from different continents and naturally eat different kinds of plants, and even though those specific captive individuals lived in three zoos across three different countries, their gut microbiomes ended up looking very similar. They were closer to each other than to their wild counterparts, and oddly similar to the microbiomes of humans.

Why the changes? Zoo animals often get antibiotics, but Clayton found that even untreated animals had different microbiomes from wild ones. Instead, these changes were most likely due to diet.

In the wild, doucs and howlers eat a wide range of plants that between them contain many complex fibers. No single microbe can digest all of these, and so a plant-rich diet sustains a diverse microbiome; by contrast, low-fibre diets can cause waves of extinction in the gut. This might explain why humans in Western cities have less diverse microbiomes than those in rural or hunter-gatherer societies—we eat fewer plants, and much less fiber. The same goes for zoo-kept monkeys. While Clayton found that wild doucs eat up to 57 different plant species, those in the Vietnamese zoo are fed just 15 species, and those in the American zoo eat just one. The captive individuals are eating the monkey version of a low-fibre Western diet.

To prove his point, Clayton also collected stool from 18 doucs that lived in “semi-captivity” in a Vietnamese sanctuary. “It’s the closest thing that they can get to living in the jungle,” says Knights. “Every day, two guys go on a motorcycle into the jungle and bring plants back to the sanctuary. They’re really doing the best they can to reproduce the wild environment.” Sure enough, their efforts meant that the resident doucs had gut microbiomes that were closer to their wild counterparts than individuals from zoos.

Other scientists have found similar trends. In 2013, Katherine Amato, now at Northwestern University, showed that when black howler monkeys live in forests that are more heavily degraded by human influence, they eat poorer diets and less diverse microbiomes.

So captivity, as Clayton and Knights write, “humanizes” the primate microbiome. That phrase has a double meaning. The first is literal: The zoo-kept animals seem to pick up microbes from human handlers or visitors, including bacteria like Prevotella and Bacteroides that dominate the human gut but. The second meaning is metaphorical. Over human history, our gut microbiomes have become gradually less diverse, so that hunter-gatherers host fewer species than other great apes, and urban city-dwellers host fewer species than hunter-gatherers. That same long-term winnowing plays out in a few years when wild primates enter captivity.

“The gut bacterial communities of modern humans are much less species-rich than were those of our wild-living ancestors, but nobody knows exactly why,” says Andrew Moeller from the University of California, Berkeley. “This study suggests that the transition to fibre-poor diets may have driven the decimation of our gut flora long before the advent of antibiotics. It’s a big step forward in understanding why humans are missing so much of our ancestral microbial diversity.”

The big, lingering question is: Is that a bad thing? Clayton and Knights bill the changes as “disruptions” or “dysbiosis”—the latter refers to microbial communities that have shifted into an imbalanced or harmful state. It’s an evocative term, but it often gets reflexively used to describe any microbiome change, even when it’s not clear if such changes are harmful. Do we know, for example, that a narrower range of microbes (in either humans, howlers, or doucs) is actually harming our health? Could those changes simply reflect the microbiome adapting to a different diet?

“We don’t know that the captive microbiomes or the modern human ones are bad,” Knights admits. Many of the captive animals suffer from gastro-intestinal diseases, and four of the captive doucs actually died from digestive problems during the course of the study. But given the small numbers, the team couldn’t tell if their microbiomes were more severely altered than their neighbors. They also don’t know if doucs naturally die of similar diseases in the wild. “But there’s a common sense aspect to it, thought,” says Knights. “If it’s true that we’ve been living with these microbes for millions of years, then it’s likely a bad thing to lose your native microbes and acquire some other set.”

“Gut microbes are likely to play an important role in determining the health of captive non-human primates,” says Amato. “This paper reinforces the idea that the impact of factors like diet and contact with humans on the gut microbiota must be considered when captive management plans are being evaluated.”

Knights adds, “Solutions might include increase the diversity of plant fibre in their food to mimic wild diets more closely, or even to do fecal transplants from wild animals to captive individuals under some kind of gastrointestinal distress.”