Life in the slow lane: Primate metabolisms run at half the pace of other mammals

22 January 2014 by Anne-Marie Hodge, posted in evolution, mammals, physiology, primates, zoology

 

Western society is obsessed with metabolism. Magazines bombard us with splashy headlines offering hyperbolic advice on how to boost, rev, fire up, jump-start, enhance, or otherwise maximize our metabolic rates. You should eat six meals a day, or fast two days a week, or drink green tea before every meal, or sleep 9 hours a night, or hang upside down, or use company X’s proprietary powder/capsule/plant-extract to ensure that your metabolism is purring along like a jet. We are taught that we can amp up our metabolisms to become fat burning machines, and thus put incredible amounts of money, time, sweat, and psychological stress into achieving these results.

Unfortunately, a study recently published in the Proceedings of the National Academy of Sciences indicates that primates may be stuck with strikingly slow metabolisms--no matter how we space our meals or how many high-intensity interval sessions we do at the gym (Pontzer et al. 2014).

Pontzer and colleagues compared metabolic rates between primates and other placental mammals, and found that primates (including humans) use actually use only half as much energy per day as similarly sized, non-primate mammals. No wonder we have an inferiority complex about metabolism in western culture. This trend extends across primate species that have never heard of Hydroxycut or Jillian Michaels, however, so it is interesting to contemplate the evolutionary reasons and implications for the plodding primate metabolism.

Pontzer and colleagues’ approach highlights an often-overlooked flaw in society’s obsession with metabolism: many online "health" calculators, personal trainers, and even doctors base recommended daily energy intake on your basal metabolic rate (BMR), which is an estimate of the number of calories your body spends just to keep itself alive in a given day—it doesn’t include any movement, growing, healing from wounds, or the costs of reproduction for adults.

This focus on BMR may be misguided. Sure, BMR does tell us something about our daily energy requirements: clearly a 220-pound man needs more energy in a day just to keep his body running than does a 110-pound woman. But Pontzer and colleagues point out that total energy expenditure (TEE) is what actually drives our lifestyles, in terms of acquiring energy, how our bodies allocate their energy budgets, and cellular senescence due to the production of free radicals from metabolic activity. Also, the authors point out that BMR accounts for less than half of the TEE for most mammalian species. BMR alone doesn’t give us much information about the daily energy requirements and expenditures of an animal, leaving us unable to predict how much energy remains available for growth and reproduction—keys to success in the evolutionary scheme of things.

So, how does one measure TEE? The best strategy is to use “doubly labeled water.” This tried-and-true method of measuring energy expenditure involves replacing the hydrogen and oxygen in water with “heavy,” non-radioactive isotopes of those elements: deuterium and oxygen-18. The study subjects drink this isotopically “labeled” water, and then researchers collect some body fluid (urine, saliva, or blood) periodically to measure the elimination rate of the labeled water. The animal’s metabolic rate can be calculated fairly precisely from its heavy-isotope elimination rate. (For more nitty-gritty detail on how this works, see here).

Pontzer and colleagues did doubly labeled water analyses on six primate species, and obtained TEE data for 11 additional primates and 67 non-primate species from other studies. They also compared the TEE of captive and wild populations of several primates, and used previously published data that compared the TEE of western humans from “developed” nations with those of traditional Hadza foragers (Pontzer et al. 2012).

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Log ratio of TEE to body mass for primate and non-primate mammal species. (Pontzer et al. 2014)

The results were striking: the mean TEE of primates was 50.4% of that expected for their body mass. Yes, even that ultra-buff infomercial fitness guru selling you his secrets to a jet-speed metabolism is only running at half the speed of a non-primate mammal. In addition, the gap in TEE between primates and other mammals grows wider as body size increases (see figure).

Comparing TEE between captive and wild populations of the same species allowed the researchers to discern whether daily activity level or a deeper metabolic mechanism is behind primates’ low TEE values. The data showed that wild primate populations had TEEs about 20% higher than their captive counterparts. This is not trivial, but still doesn’t account for the much broader difference in TEE between primates and non-primate mammals. Pontzer and colleagues claim that this shows that the low TEE of primates isn’t a result of less physical activity overall, but rather a “systemic reduction in cellular metabolism.” It would be interesting to see how differences in body composition (ie, body fat percentage versus proportion of mass that is lean muscle) could have played into the differences between captive and wild primates, and perhaps future work will delve into that issue.

What about humans specifically? After all, we are the only primates that sometimes build entire lifestyles around manipulating our  metabolisms. And even though all primates have relatively slow metabolisms, it appears, we're the only species with high rates of obesity and related health problems. Hadza foragers with an average body mass of 46.6 kg only expended around 200 calories less per day than westerners with an average mass of 72.2 kg (Pontzer et al. 2012). Not bad . . . for a primate. Hadza nearly match westerners in TEE despite the large difference in body mass, and yet Pontzer and colleagues point out that they would still need to run an extra 45 km (27 miles) per day to match the TEE of a non-primate mammal of the same size.

This leaves us with an overarching question: why so slow, primates? The authors point out that not only do primates’ cellular metabolic processes lumber along relatively slowly, but their (and our) entire lives move at a leisurely pace relative to other mammals: primates grow and mature slowly, reproduce slowly, and acquire life skills and social status slowly. Instead of taking the “live fast and die young” approach of many other mammals, primates’ relatively long lives afford them the luxury of plodding along.

The authors suggest that if calculating BMR in addition to controlling for physical activity (although it seems an entire study focused on that issue might be able to quantify activity relative to TEE more precisely) still doesn’t account for taxonomic differences in TEE, there must be some other facet of energy expenditure that we’ve not yet uncovered. Pontzer and colleagues suggest that circadian (daily) fluctuations in cellular metabolic rates can change TEE for a given BMR. In other words, if you are running at the same maximum speed as another animal, but your cellular processes slow down and go at a more leisurely pace for part of the day (creating significant fluctuations in expenditure), your TEE will of course be less. This may especially apply to mammals that undergo torpor to save energy at night. Only one primate in Pontzer and colleagues’ dataset undergoes torpor, however—the mouse lemur; Microcebus murinus)—and torpor periods were excluded from the TEE analysis.

The take-home message from this study is that primates have remarkably slower metabolic rates than other placental mammals, and that this is likely related to the relatively slow rate at which primate lives unfold. The study also points out how much we can miss when we focus solely on BMR to determine energy requirements, especially for non-human animals. Finally, it suggests that we still have much to learn about all of the complicated factors that interact to determine energy balance. As the most metabolism-obsessed species on the planet, I suspect there will be plenty of human researchers tackling this topic in coming years.

 

Pontzer, H., et al. 2014. Primate energy expenditure and life history. Proceedings of the National Academy of Sciences. 201316940 doi/10.1073/pnas.1316940111

Pontzer, H., et al. 2012. Hunter-gatherer energetics and human obesity. PLoS ONE. 7(7):e40503.

 

Orangutan image source

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