High Temperatures Dampen Immune Systems of Wild Capuchins

Tracking climate change impacts on animals

Capuchins de Taboga

Capuchins de Taboga

High temperatures lower the immune performance of wild capuchin monkeys in Costa Rica, especially in young individuals, finds a new study published by Science Advances. The work, led by scientists at Emory University and the University of Michigan, provides some of the first data on the relationship between the immune system and ambient temperature in a wild mammal.

“Capuchin monkeys are super intelligent, highly adaptive primates that do well in diverse ecosystems,” says Marcela Benítez, Emory assistant professor of anthropology and co-senior author of the paper. “The fact that we’re seeing their immune responses affected by high temperatures suggests that many mammalian species that are less adaptive may be experiencing even worse effects as average temperatures warm globally.”

Benítez studies both a captive population of tufted capuchins in a laboratory in Atlanta and wild white-faced capuchins in the Taboga Forest Reserve of northwestern Costa Rica. She is a co-director of Capuchins de Taboga, a research project launched in 2017 in collaboration with the Universidad Nacional Técnica of Costa Rica.

Jordan Lucore, a graduate student at University of Michigan, is first author of the current study, and Andrew Marshall, a professor of anthropology at University of Michigan, is co-senior author.

The international collaboration also included Emory graduate student Sarah Kovalaskas; Lorena Sinclair and Juan Carlos Ordoñez (Capuchins de Taboga); Vasco Alexandre Martins (University of Portsmouth, United Kingdom); Amy White (Durham University, United Kingdom); and Jacinta Beehner and Thore Bergman (University of Michigan).

The researchers gathered urine samples from white-faced capuchin monkeys in the Taboga Forest Reserve. Fifteen days before each urine collection period, they recorded maximum and minimum air temperatures every 15 minutes.

The team collected 670 urine samples from 54 capuchins over a two-year period. 

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An arboreal species, white-faced capuchins spend most of their time in trees.

An arboreal species, white-faced capuchins spend most of their time in trees. (Capuchins de Taboga)

An arboreal species, white-faced capuchins spend most of their time in trees. (Capuchins de Taboga)

C-author Vasco Alexandre Martins extends a urine collection pole beneath a capuchin on a tree limb

C-author Vasco Alexandre Martins extends a urine-collection pole beneath a capuchin on a tree limb. (Capuchins de Taboga)

C-author Vasco Alexandre Martins extends a urine-collection pole beneath a capuchin on a tree limb. (Capuchins de Taboga)

The fieldwork was challenging, says Kovalaskas, shown collecting a urine sample, adding that it is never a dull day in the Taboga Forest Reserve.

The fieldwork was challenging, says Kovalaskas, shown collecting a urine sample, adding that it is never a dull day in the Taboga Forest Reserve. "It's gorgeous and full of all kinds of wildlife. You never know what you're going to see." (Capuchins de Taboga)

The fieldwork was challenging, says Kovalaskas, shown collecting a urine sample, adding that it is never a dull day in the Taboga Forest Reserve. "It's gorgeous and full of all kinds of wildlife. You never know what you're going to see." (Capuchins de Taboga)

The white-faced capuchin population near the research station consists of around 70 individuals living in four different groups.

“We follow them from sunrise to sunset, collecting behavioral data, fecal and urine samples for various studies,” Benítez says.

“It’s quite tricky to collect urine from an arboreal monkey,” says Kovalaskas, who assisted with the fieldwork.

Through observing the capuchins over time in the trees, she explains, you become familiar with the signs that one is about to urinate.

The researchers carry a short bamboo pole split into a Y-shape at one end to hold a cupped bag of plastic. They extend the pole beneath a capuchin as it urinates from a tree-limb perch. They then remove the plastic bag and transfer the liquid to a vial.

Emory graduate student Sarah Sarah Kovalaskas, left, and Jordan Lucore, a graduate student at the University of Michigan, feel triumphant after successfully collecting some urine samples.A capuchin mother carriers a sleeping baby on her back.

Emory graduate student Sarah Kovalaskas, left, and Jordan Lucore (University of Michigan), feel triumphant after successfully collecting some urine samples. "It's difficult to do so it's a real dopamine hit when you get one," Kavalaskas says. (Capuchins de Taboga)

Emory graduate student Sarah Kovalaskas, left, and Jordan Lucore (University of Michigan), feel triumphant after successfully collecting some urine samples. "It's difficult to do so it's a real dopamine hit when you get one," Kavalaskas says. (Capuchins de Taboga)

For the current study, the urine samples were tested to determine their concentration of neopterin — a compound secreted by white blood cells and a biomarker for the performance of the innate immune system.

“The innate immune system is the one that you are born with,” Benítez explains, “while the adaptive immune system is the one that develops as you grow and are exposed to various pathogens.”

Analyses showed a relationship between temperature and neopterin in the wild monkeys that resembled a thermal performance curve. Neopterin increased with temperature until it reached an optimum at 86 degrees Fahrenheit.

In cases where average temperatures climbed above 86 degrees for an extended period of at least 15 days, neopterin rapidly decreased. The drop off was most pronounced in juveniles.

“The impact of high temperatures on young capuchins is particularly alarming,” Benítez says. She points to previous evidence that heat stress early in life leaves mammals more susceptible to infections across their lifespan.

A capuchin mother carriers a sleeping baby on her back.

A capuchin mother carriers a sleeping baby on her back. The study found that the immune systems of juveniles were most impacted by high temperatures. (Capuchins de Taboga)

A capuchin mother carriers a sleeping baby on her back. The study found that the immune systems of juveniles were most impacted by high temperatures. (Capuchins de Taboga)

Climate change is set to exacerbate these heat impacts.

“Over the past decade, Northwestern Costa Rica has experienced an 89% increase in the number of days exceeding 86 degrees Fahrenheit compared to the previous three decades,” Benítez says. “And by 2080 the overall temperature is projected to go up by 4% to 6%. You can imagine the impact that will have on this population of capuchins as well as other animals in this region.”

Previous studies on domesticated cows and chickens have shown a relationship between temperature and immune performance. The consequences of rising temperatures have also been observed in cold-blooded animals that rely more on ambient temperatures for thermoregulation.

Little was known, however, about the effects of heat on the immune systems of wild mammal populations.

“We developed and validated a non-invasive method to measure neopterin levels in wild capuchins, providing critical physiological data on how heat affects the immune systems of wild capuchins.” Benítez says. “This type of data adds to growing understanding of how wild animals are affected by increasing temperatures and is essential for making informed conservation decisions in the face of climate change.”

Story by Carol Clark.

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