Metabolism Hits a Ceiling in Athletic Endurance Feats – The Scientist

We all have limits, and a new study suggests those limits are pretty similar among individual humans—at least at the metabolic level. Researchers tracked runners’ energy expenditure before and after they completed the equivalent of a marathon six days a week for nearly five months straight, then compared their results with studies of other high-intensity activities, and found that the longer the event, the lower the metabolic rate participants were able to sustain. 

The maximum metabolic rate for longer-term activities, they report today (June 5) in Science Advances, is about two and a half times an individual’s resting energy use—likely a reflection of a limit on the number of calories the human digestive system is able to absorb.

“Conceptually, people had been looking for one number—they were looking for some level of energy expenditure that is sustainable indefinitely. . . . They looked to really extreme events like the Tour de France to give them a sense of what that number was,” says Herman Pontzer, an evolutionary anthropologist at Duke University. The new paper, he says, is the first to look for a limit in the context of how long the energy output is maintained.

Pontzer saw his chance to get at the limits of human energy expenditure in a new way in 2014, when he talked with Bryce Carlson, then an anthropologist at Purdue University in Indiana, at a meeting. Carlson was the research director for an upcoming event called the Race Across the USA (RAUSA) in which he and other participants would run from Huntington Beach, California, to Washington, DC, over several months, covering an average of 42 kilometers per day. He asked Pontzer, who was then at Hunter College in New York City, if he’d like to join the team conducting research on the runners.

We don’t think it’s a limit on how much food’s available, or how fast you can stuff it in your face, we think it’s a limit on what your digestive tract is able to actually absorb.

—Herman Pontzer, Hunter College

Pontzer readily accepted and found a graduate student, Caitlin Thurber, who now teaches at Nassau Community College on Long Island, to help with the study. “The opportunity to do this project seemed too good to pass up,” Thurber says. The researchers recruited six of the 12 RAUSA runners who planned to complete the entire race to participate in their study, and a week before the event began in January 2015, Thurber dosed them with “doubly labelled water”—fluid with isotopes of hydrogen and oxygen. The participants then turned in samples of their urine in the days leading up to and just after the start of the race. By analyzing the relative proportions of the isotopes present, Thurber and Pontzer could calculate the runners’ energy expenditure rates. She repeated the labelled-water dosing and sample collection at the end of the race.

The runners’ energy expenditure rose sharply by the fifth day of the race relative to their baseline pre-running values. But by the end of the race, their metabolisms had slowed a bit compared to their rates on day five. “That’s an example of constrained energy expenditure, which has been well-documented,” Thurber says. That is, total energy expenditure plateaus as people reach higher activity levels, perhaps because the body compensates for the calories used in movement by dialing back the energy used for other physiological processes. (She wrote up her results as a master’s thesis the following year; in her acknowledgements, she thanks her mother for storing urine samples in the freezer.)

The research team then compared the RAUSA data with those from metabolic rates in published studies on demanding physical challenges, such as the Tour de France, 100-mile ultramarathons, and even pregnancy. Plotting those data, they found a steep drop-off in participants’ metabolic rates with increasing duration of the event; the trend line for that curve flattened at about two and a half times participants’ basal metabolic rates. “We tried hard to find any case of people who break those limits, who’ve broken through that metabolic ceiling—we can’t find it,” Pontzer says.

Where did that limit come from? Study coauthor John Speakman, a biologist at the University of Aberdeen and the Chinese Academy of Sciences, had previously found that the ability to dissipate excess heat appears to limit the performance of small rodents. Heat didn’t seem to be the limiting factor for long-term human activity, though, given that energy expenditure in arctic trekking fell along the same curve as competitions in warmer climes. 

So the research team turned to published studies that overfed people and observed the effect on their physiology. However much those subjects took in, the calories they actually absorbed maxed out at around the amount required to fuel their metabolisms at two and a half times their resting rate, the researchers found. 

Race Across the USA participant Patrick Sweeney finishes a segment near Joshua Tree, California, as race assistant Samantha Upton marks his time.

CAITLIN THURBER

“We don’t think it’s a limit on how much food’s available, or how fast you can stuff it in your face, we think it’s a limit on what your digestive tract is able to actually absorb,” says Pontzer.

The idea that the limits of the human digestive system constrain performance is a “sound hypothesis” says Audrey Bergouignan, an integrative physiologist at the University of Colorado and CNRS in Strasbourg, France, who was not involved in the study. But she’s not yet convinced. Many assumptions went into the building of the model, she notes—for example, some of the included studies didn’t measure participants’ resting metabolic rates, so Pontzer and his colleagues estimated them. Prospective studies of very long races under hot and cold conditions would be needed to test the hypothesis, Bergouignan says.

Brent Ruby, who studies work physiology and exercise metabolism at the University of Montana and was not involved in the study, says he thinks the new model is “compelling,” in part because he compared it with some of his own data that weren’t included in the Science Advances paper and found them consistent. 

In Ruby’s studies, he used labelled water to examine the energy expenditure of 32 wildland firefighters as they worked to combat blazes. “When individuals are right around two-and-a-half times basal metabolic rate, they seem to do an adequate job of maintaining body mass over an assignment, which might be five to seven days or so,” he says. “We’ve only had five of them that have been above three times basal metabolic rate, and four of the five started to lose weight. That does speak to the concept of sustainability.” But Ruby notes that this ceiling probably doesn’t reflect what our ancient hominin ancestors were capable of, because they wouldn’t have had access to the constant “provision of nutrients and fluids” available to modern humans performing feats of endurance.

For Pontzer, the apparent alignment of the metabolic ceiling in endurance events with that in pregnancy is one of the most interesting aspects of the model. “Humans are the ultimate endurance primates,” he tells The Scientist, with long-distance running capabilities that far outstrip those of other apes. If the same machinery limits both pregnancy and vigorous physical activity, it raises the question of whether evolution selected for endurance running, giving humans the ability to “have bigger babies [and] have them more often” as a side effect—or the other way around. “There’s kind of a fun evolutionary connection between these two very different tasks that we didn’t know was possible before.”

C. Thurber et al., “Extreme events reveal an alimentary limit on sustained maximal human energy expenditure,” Sci Adv, 5:eaaw0341, 2019.

Correction (June 5): The original version of this article erroneously stated that Herman Pontzer is at Hunter College. Pontzer was a faculty member at Hunter College when the study was conducted, but is now at Duke University. The Scientist regrets the error.
Correction (June 6): This article originally stated that Bryce Carlson organized the Race Across the USA; in fact, he was its research director. The Scientist regrets the error.