Warming temperatures impact immune performance of wild monkeys, U-M study shows

Images/videos of capuchin monkeys

ANN ARBOR—The immune performance of wild capuchin monkeys declines when the animals experience higher temperatures, and younger monkeys seem to be particularly vulnerable to heat, according to a University of Michigan study.

U-M anthropology doctoral student Jordan Lucore examined how the immune systems of wild monkeys in Costa Rica were impacted by temperature. Lucore and a team of researchers found that when monkeys experienced about two weeks of warmer temperatures—86 degrees Fahrenheit—their generalized immune system performance declined. This is the part of the immune system that is activated as soon as the body senses a threat. 

Their findings, published in Science Advances, were a surprise, Lucore said. Scientists expect endotherm animals—animals that can regulate their own body temperature, like mammals—to be able to protect themselves against fluctuating temperatures because they can maintain a constant body temperature.

"We think this has implications for understanding the effects of climate change because we're seeing this unlikely relationship between the immune system and temperature in this particular study species, and we're seeing it at much lower temperatures than expected," Lucore said. "Eighty six degrees Fahrenheit is not that hot."

For the study, Lucore examined a population of wild white-faced capuchins in the Taboga forest reserve of Costa Rica. Launched in 2017, the Capuchinos de Taboga Research Project focuses on the cognition, endocrinology and behavior of these primates. The project is co-directed by Jacinta Beehner, U-M professor of anthropology and psychology; Thore Bergman, U-M professor of psychology; and Marcela Benítez, professor of anthropology at Emory University, all of whom are co-authors of the study.

"Capuchins are thought of as generalist species because they live in a lot of different places with different climates and diverse ecologies. They're successful generalists," Lucore said. "That was another concerning thing about the results: I can't believe we're seeing this in capuchins. They are quite resilient."

Studying the immune system can be invasive: Biomarkers are typically found in blood serum, which can only be extracted in invasive ways. But Lucore examined a biomarker called neopterin, which can be measured in urine.

The researchers used a "clean catch" method to collect the urine. Urine that falls on the ground or other leaves often can't be used because it may be contaminated, Lucore said. Taking care to not stress the animals or get too close, the researchers followed the monkeys, which are habituated to human presence, until they urinated. The researchers then caught the urine using a basket wrapped in plastic attached to a stick. Field researchers at the site can individually identify each monkey to keep track of which urine samples belong to particular individuals.  

Lucore measured the amount of neopterin in the urine and modeled the temperature in the days and weeks leading up to the urine collection. The researchers found that immune performance declined when the monkeys experienced two weeks of high temperatures. They also saw that younger monkeys experienced the strongest impact on immune performance. 

"We discovered that young individuals' immune systems may be particularly affected by temperature compared to the rest of the age groups," Lucore said. "This is especially important for potential health and fitness outcomes, because when you're young, you rely on your generalized immune system. Your adaptive immune system has not yet developed."

The adaptive immune system is the component of the immune system that recognizes specific pathogens—something that takes time, up to several years, for young animals to develop.

Lucore said the researchers don't know yet whether this has long-term impacts for health in wild animals. Longer-term studies will need to look at multiple generations to conclude whether the monkeys' decreased immune performance results in poorer health or reproductive outcomes. Lucore also said the results may be difficult to apply to humans, but they can tell us something about how climate change is impacting wild animal populations.

"Climate change is happening. It's going to have effects on anyone living on Earth in ways that you may not expect, and especially on these fundamental systems that we need to survive," Lucore said. "The fact that a graduate student like me can go out there and collect rather short-term data and find strong evidence that temperatures are affecting the physiology of wild animals—I think that's a pretty important thing to keep in mind."

The Capuchinos de Taboga field team, specifically co-authors Amy White, Lorena Sinclair, Vasco Alexandre Martins, Sarah Kovalaskas and Juan Carlos Ordoñez, were instrumental in the study. Co-author Andrew Marshall, U-M professor of anthropology and of ecology and evolutionary biology, provided critical analysis and interpretation of the study.