Metabolic adaptation for low energy throughput in orangutans

Abstract

Energy is the fundamental currency of life--needed for growth, repair, and reproduction--but little is known about the metabolic physiology and evolved energy use strategies of the great apes, our closest evolutionary relatives. Here we report daily energy use in free-living orangutans (Pongo spp.) and test whether observed differences in energy expenditure among orangutans, humans, and other mammals reflect known differences in life history. Using the doubly labeled water method, we measured daily energy expenditure (kCal/d) in orangutans living in a large indoor/outdoor habitat at the Great Ape Trust. Despite activity levels similar to orangutans in the wild, Great Ape Trust orangutans used less energy, relative to body mass, than nearly any eutherian mammal ever measured, including sedentary humans. Such an extremely low rate of energy use has not been observed previously in primates, but is consistent with the slow growth and low rate of reproduction in orangutans, and may be an evolutionary response to severe food shortages in their native Southeast Asian rainforests. These results hold important implications for the management of orangutan populations in captivity and in the wild, and underscore the flexibility and interdependence of physiological, behavioral, and life history strategies in the evolution of apes and humans.

Fig. 1.

DEE versus body mass for mammals. (Inset) Full comparative dataset for eutherian mammals (Table S1). Open circles and triangle represent orangutan adults and juvenile; gray circle and triangle represent human adults and juveniles in a subsistence/agricultural economy (25); black circle and triangle represent human adults and juveniles in industrial economies (–38); gray squares represent other eutherian mammals. “S” indicates three-toed sloths (Bradypus variegates); “H” indicates howler monkeys (Alouatta palliata).

Fig. 2.

Standardized residual DEE, calculated from the mammalian trend line. Orangutans (open bars); humans in industrial (Ind) economies (dark gray bars) (–38); and humans in subsistence/agricultural (SA) economies (light gray bars) (26). (A) Adults: dashed line in the orangutan bar indicates the median of the orangutan sample (n = 3). Error bars indicate SD. (B) Juveniles; groups as in A.

Fig. 3.

Basal and resting metabolic rates in hominoids. Mean BMR for adult humans (20) and chimpanzees (13) and RMR for adult orangutans, as a percentage of the expected BMR value for mammals of similar body mass (39). Error bars indicate SD. Estimated BMR, calculated as RMR divided by 1.2 (21), is also shown for orangutans (dashed line in orangutan bar).

Fig. 4.

Activity profiles for orangutans in the wild and at the Great Ape Trust (adults, n = 3; juvenile, n = 1). (A) Feeding and resting. Hashed area indicates time spent feeding. Wild and Great Ape Trust orangutans also sleep approximately 12 h each night. Wild data are from populations in masting forests (i.e., forests that experience periodic crashes in food availability) (40). (B) Walking, which includes the horizontal distance traveled in the canopy and, for Great Ape Trust subjects, the distance traversed along enclosure walls. Wild data are from both Borneo and Sumatra [n = 8 sites; mean, 712 m/d; range, 162–1,077 m/d (41)]. (C) Climbing, which includes all vertical travel (ascent only). Wild data (mean, 88.3 m/d; range, 55.7–121.4 m/d) from full day follows of eight adults (SI Methods). Great Ape Trust data shown in Table S3.