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Cited by 105Primate Behavior and EcologyPhysiological and biochemical adaptationsAnimal Behavior and Reproduction

Metabolic adaptation for low energy throughput in orangutans.

Open access
Pontzer, Herman, Raichlen, David A., Shumaker, Robert W., Ocobock, Cara, Wich, Serge A.·2010·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1001031107PMC PMC2922585
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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.

AI snapshot

Written from the paper’s full text.

TL;DR

Free-living orangutans at the Great Ape Trust showed exceptionally low daily energy expenditure despite activity levels similar to wild orangutans, suggesting orangutans are adapted for low energy throughput rather than altered energy allocation. This low metabolism may explain their slow growth and reproduction and has implications for captive feeding and wild habitat management.

Key findings

  • Adult orangutans had the lowest mass-adjusted daily energy expenditure (DEE) ever measured for a eutherian mammal except sloths, with a mean z-score of –2.81 (range –2.55 to –3.33), placing them in the lowest 1% of mammals.
  • Orangutan DEE was significantly lower than human DEE (P < 0.001), even compared with sedentary industrial and active subsistence/agriculture human populations; the probability of drawing orangutan DEE values from a large low-activity human population was less than 0.0001% (0.002% if the lowest orangutan value was excluded).
  • Adult orangutan resting metabolic rate (RMR) averaged 23% lower than predicted for body mass (range 7–35% lower), and if RMR overestimated true BMR by 20%, BMR was approximately 36% lower than similarly sized mammals.
  • Adult orangutans had moderate physical activity levels (mean PAL 1.7, range 1.6–1.8) and low body fat (adult mean 16.9%, range 13.2–21.8%; juvenile 5.5%), indicating low DEE was not due to inactivity.

Methods

  • DEE was measured over 2-wk periods using doubly labeled water in four orangutans at the Great Ape Trust: one adult male (Azy, 30 y, 116 kg), two adult females (Knobi, 27 y, 56 kg; Katy, 19 y, 53 kg), and one juvenile male (Rocky, 4 y, 25 kg); all were Bornean/Sumatran hybrids.
  • DEE was measured twice in Azy and Knobi (August and October 2008), and the mean was used; urine samples were analyzed by gas-isotope MS, lean body mass was calculated by 2H dilution, and CO2 production was converted to energy using a food quotient of 0.95.
  • RMR was measured by open-flow respirometry while subjects sat quietly and awake; activity data were recorded for a subset of days and compared with published values for humans and other mammals.

Limitations

  • The paper states that RMR was measured with subjects recently fed, alert, and sitting quietly, which likely overestimates true BMR by approximately 20%; it also states that more primate DEE measurements and more research on species-specific energy requirements are needed.
  • Evident from the text: the sample was very small (n = 4, only 3 adults), all subjects were captive hybrids at a single facility, and DEE was measured in only one or two seasons, limiting generalization to wild orangutans and other apes.
  • Evident from the text: the conversion of CO2 production to DEE assumed a food quotient of 0.95, higher than the RQ of 0.85 often used for humans and other mammals, though the paper notes that assuming 0.85 would not change the main comparisons.

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Integrity signals

Registry

Crossref · 10.1073/pnas.1001031107

Cites

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Statistics

Nothing to recompute.

Claims the paper makes

0 of 49 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § Results

    The pattern of orangutans using less energy than humans holds for juveniles.

    “This pattern holds for juveniles, which have greater size-adjusted DEE than adults as a result of the energy cost of growth (19) (Fig. 2B).”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Results

    The difference between human and orangutan DEE is not an artifact of small sample size: the probability of drawing orangutan DEE values from a large, low-activity level human population is less than 0.0001%.

    “The difference between human and orangutan DEE is not an artifact of small sample size: the probability of drawing orangutan DEE values from a large, low–activity level human population is less than 0.0001% (Fig. S1).”
    Quote in the paperSubstantial claim
  • Findingown data
    § Results

    Variation in DEE among orangutans appeared to vary with age and activity level.

    “Variation in DEE among orangutans appeared to vary with age and activity level.”
    Quote in the paperNot a substantial claim
  • Findingown data
    § Results

    For the two adult orangutans in which DEE was measured twice (in August and October), DEE was somewhat higher in the later session (10% and 22% greater for Azy and Knobi, respectively).

    “For the two adult orangutans in which DEE was measured twice (in August and October), DEE was somewhat higher in the later session (10% and 22% greater for Azy and Knobi, respectively; Table 1).”
    Quote in the paperNot a substantial claim
  • Findingcitation
    § Results

    DEE for adult orangutans was lower than macaques undergoing calorie restriction (z-score, -2.25).

    “this is lower than macaques undergoing calorie restriction (z-score, –2.25) (16).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [16] Blanc S, et al. Energy expenditure of rhesus monkeys subjected to 11 years of dietary restriction. J Clin Endocrinol Metabol. 2003;88:16–23. doi: 10.1210/jc.2002-020405. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims. 28
  • Classified as probably not a substantial claim. 12

  • May combine two claims.

    Findingown data
    § Results

    RMR among adult orangutans in our sample was an average of 23% lower (range, 7-35% lower) than the basal rate of metabolism predicted for their body mass, and significantly lower than BMR reported for humans and chimpanzees (Student t test, P < 0.05 for both comparisons).

    “RMR among adult orangutans in our sample was an average of 23% lower (range, 7–35% lower) than the basal rate of metabolism predicted for their body mass, and significantly lower than BMR reported for humans (20) and chimpanzees (13) (Student t test, P < 0.05 for both comparisons; Fig. 3).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [20] Henry CJK. Basal metabolic rate studies in humans: Measurement and development of new equations. Public Health Nutr. 2005;8(7A):1133–1152. doi: 10.1079/phn2005801. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [13] Froehle AW, Schoeninger MJ. Intraspecies variation in BMR does not affect estimates of early hominin total daily energy expenditure. Am J Phys Anthropol. 2006;131:552–559. doi: 10.1002/ajpa.20475. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Findingown data
    § Results

    Orangutans used significantly less energy per day than humans (P < 0.001, Student t test), with body size-adjusted DEE below observed values for humans in both sedentary industrial and active subsistence/agriculture populations.

    “Orangutans used significantly less energy per day than humans (P < 0.001, Student t test), with body size–adjusted DEE below observed values for humans in both sedentary industrial and active subsistence/agriculture populations (Fig. 2A).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Orangutans in our sample had lean body mass percentages somewhat higher than the human mean, making the differences in DEE between these species even greater when expressed in terms of lean body mass.

    “Orangutans in our sample had lean body mass percentages somewhat higher than the human mean (Table 1; see below), making the differences in DEE between these species even greater when expressed in terms of lean body mass.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Doubling estimated locomotor costs in Great Ape Trust orangutans, equivalent to reducing locomotor economy by 50%, increases DEE by only 5% to 9% for adults and 13% for the juvenile, still significantly below the DEE of humans (P < 0.01) and lower than nearly all other mammals.

    “Doubling estimated locomotor costs in Great Ape Trust orangutans, equivalent to reducing locomotor economy by 50%, increases DEE by only 5% to 9% for adults and 13% for the juvenile, still significantly below the DEE of humans (P < 0.01) and lower than nearly all other mammals.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Great Ape Trust orangutans were very active, walking and climbing similar distances each day as their wild counterparts while maintaining similar patterns of resting, feeding, and sleeping.

    “Great Ape Trust orangutans were very active, walking and climbing similar distances each day as their wild counterparts while maintaining similar patterns of resting, feeding, and sleeping (Fig. 4).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingcitation
    § Results

    The body fat percentages of Great Ape Trust orangutans compare favorably to mean body fat percentage in active humans engaged in subsistence/agriculture (adults, 19.9%; children, 14.6%) and are considerably lower than that of less active humans (adults, 28.0%; children, 19.4%).

    “This compares favorably to mean body fat percentage in active humans engaged in subsistence/agriculture (26) (adults, 19.9%; children, 14.6%) and is considerably lower than that of less active humans (adults, 28.0%; children, 19.4%; SI Methods).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [26] Kashiwazaki H, Dejima Y, Orias-Rivera J, Coward WA. Energy expenditure determined by the doubly labeled water method in Bolivian Aymara living in a high altitude agropastoral community. Am J Clin Nutr. 1995;62:901–910. doi: 10.1093/ajcn/62.5.901. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Findingown data
    § Results

    Body composition suggests an active lifestyle, with mean body fat percentages in Great Ape Trust orangutans of 16.9% for adults (range, 13.2-21.8%) and 5.5% for the juvenile.

    “Body composition also suggests an active lifestyle, with mean body fat percentages in Great Ape Trust orangutans of 16.9% for adults (range, 13.2–21.8%) and 5.5% for the juvenile (Table 1).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data
    § Results

    Walking and climbing accounted for approximately 5% to 9% of DEE in adult orangutans and 13% of DEE in juvenile orangutans.

    “Walking and climbing accounted for approximately 5% to 9% of DEE in adult orangutans and 13% of DEE in juvenile orangutans (SI Methods).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingcitation
    § Results

    The PAL of adult orangutans (mean 1.7) is comparable to observed PAL of humans in physically demanding agricultural lifestyles (mean PAL, 1.9 for males; 1.7 for females) and wild howler monkeys (PAL, 2.0), and well above estimated PAL for wild orangutans (PAL, 1.4).

    “This is comparable to the observed PAL of humans in physically demanding agricultural lifestyles (mean PAL, 1.9 for males; 1.7 for females) (24) and wild howler monkeys (PAL, 2.0) (25), and well above estimated PAL for wild orangutans (PAL, 1.4) (12).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [24] Dufour DL, Piperata BA. Energy expenditure among farmers in developing countries: What do we know? Am J Hum Biol. 2008;20:249–258. doi: 10.1002/ajhb.20764. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [25] Nagy KA, Milton K. Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata) Ecology. 1979;60:475–480. [Google Scholar] source

      Not checked in the free run.

    • cites [12] Leonard WR, Robertson ML. Comparative primate energetics and hominoid evolution. Am J Phys Anthropol. 1997;102:265–281. doi: 10.1002/(SICI)1096-8644(199702)102:2<265::AID-AJPA8>3.0.CO;2-X. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Study design and conductnone given
    § Results

    Orangutan RMR in our sample was measured with subjects recently fed, alert, and sitting quietly.

    “As a matter of necessity, orangutan RMR in our sample was measured with subjects recently fed, alert, and sitting quietly.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Results

    Decreased basal metabolism has previously been reported in other low-DEE species including sloths and aardwolves.

    “Decreased basal metabolism has previously been reported in other low-DEE species including sloths and aardwolves (4, 22, 23).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [4] McNab BK. The influence of food habits on the energetics of eutherian mammals. Ecol Monogr. 1986;56:1–19. [Google Scholar] source

      Not checked in the free run.

    • cites [22] Nagy KA, Montgomery GG. Field metabolic rate, water flux and food consumption in three-toed sloths (Bradypus variegatus) J Mammal. 1980;61:465–472. [Google Scholar] source

      Not checked in the free run.

    • cites [23] Williams JB, Anderson MD, Richardson PRK. Seasonal differences in field metabolism, water requirements, and foraging behavior of free-living aardwolves. Ecology. 1997;78:2588–2602. [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation
    § Results

    Juveniles have greater size-adjusted DEE than adults as a result of the energy cost of growth.

    “This pattern holds for juveniles, which have greater size-adjusted DEE than adults as a result of the energy cost of growth (19) (Fig. 2B).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [19] Butte NF. Fat intake of children in relation to energy requirements. Am J Clin Nutr. 2000;72(5 suppl):1246S–1252S. doi: 10.1093/ajcn/72.5.1246s. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductown data
    § Methods

    All subjects were weight-stable (i.e., <2 kg fluctuation) over the course of the study, and had been weight-stable during the preceding 6 mo.

    “All subjects were weight-stable (i.e., <2 kg fluctuation) over the course of the study, and had been weight-stable during the preceding 6 mo.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data
    § Discussion

    Our results indicate that the slow life history of orangutans results from decreased energy throughput rather than changes in energy allocation.

    “Specifically, our results indicate that the slow life history of orangutans results from decreased energy throughput rather than changes in energy allocation.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Abstract

    Orangutans have lower reproductive rates than all other hominoids and the slowest growth rates of any primate except humans.

    “Orangutans, including species of Pongo on both Borneo and Sumatra, have lower reproductive rates than all other hominoids and the slowest growth rates of any primate except humans (7, 8).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [7] Hawkes K, O'Connell JF, Jones NG, Alvarez H, Charnov EL. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA. 1998;95:1336–1339. doi: 10.1073/pnas.95.3.1336. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [8] Wich SA, et al. Life history of wild Sumatran orangutans (Pongo abelii) J Hum Evol. 2004;47:385–398. doi: 10.1016/j.jhevol.2004.08.006. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § Methods

    Care was taken to avoid contamination of urine samples.

    “Care was taken to avoid contamination.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation
    § Discussion

    An accelerated metabolic rate in the hominin lineage would be consistent with humans' high rate of reproduction and large brains relative to other apes.

    “An accelerated metabolic rate in the hominin lineage would be consistent with humans’ high rate of reproduction (7) and large brains (9, 11) relative to other apes.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [7] Hawkes K, O'Connell JF, Jones NG, Alvarez H, Charnov EL. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA. 1998;95:1336–1339. doi: 10.1073/pnas.95.3.1336. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [9] Charnov EL, Berrigan D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol Anthropol. 1993;1:191–194. [Google Scholar] source

      Not checked in the free run.

    • cites [11] Isler K, van Schaik CP. The Expensive Brain: A framework for explaining evolutionary changes in brain size. J Hum Evol. 2009;57:392–400. doi: 10.1016/j.jhevol.2009.04.009. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given
    § Methods

    Trials were accepted for analysis if the rate of oxygen consumption and CO2 production remained stable for at least 8 min, and a minimum of three trials, collected on separate days, were analyzed for each subject.

    “Trials were accepted for analysis if the rate of oxygen consumption and CO2 production remained stable for at least 8 min. A minimum of three trials, collected on separate days, were analyzed for each subject; results are shown in Table S4.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation
    § Methods

    FQ must equal respiratory quotient (RQ) over long periods (i.e., several days) in weight- and nutrient-stable subjects, and are therefore preferable to RQ measurements from relatively short (approximately 20 min) RMR trials.

    “FQ must equal respiratory quotient (RQ) over long periods (i.e., several days) in weight- and nutrient-stable subjects (31), and are therefore preferable to RQ measurements from relatively short (approximately 20 min) RMR trials.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [31] Westerterp KR. Food quotient, respiratory quotient, and energy balance. Am J Clin Nutr. 1993;57(5 suppl):759S–764S. doi: 10.1093/ajcn/57.5.759S. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data
    § Methods

    The same investigator administered the DLW dose to each animal to ensure all of it was consumed.

    “the same investigator (R.W.S.) administered the dose to each animal to ensure all of it was consumed (Fig. S2A).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data
    § Discussion

    Despite active lifestyles similar to those in the wild, orangutans in our study maintained remarkably low DEE, suggesting a physiological adaptation for minimizing energy throughput previously unknown in apes.

    “Despite active lifestyles similar to those in the wild, orangutans in our study maintained remarkably low DEE, suggesting a physiological adaptation for minimizing energy throughput previously unknown in apes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductnone given
    § Results

    RMR measurements were taken while subjects were seated and awake, and likely overestimate true BMR by approximately 20%.

    “RMR measurements were taken while subjects were seated and awake, and likely overestimate true BMR by approximately 20%.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § Discussion

    Our study suggests that orangutans have adapted by becoming consummate low-energy specialists, decreasing their daily energy needs to avoid starvation in food-poor times.

    “Our study suggests that orangutans have adapted by becoming consummate low-energy specialists, decreasing their daily energy needs to avoid starvation in food-poor times.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation
    § Abstract

    Several comparative studies have suggested a continuum of energy-use strategies among mammals, from high-energy throughput to low, with each species' strategy contingent upon the particular dynamics of food availability and mortality risk it faces.

    “Indeed, several comparative studies have suggested a continuum of energy-use strategies among mammals, from high-energy throughput to low, with each species’ strategy contingent upon the particular dynamics of food availability and mortality risk it faces (1, 4–6).”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [1] Nagy KA, Girard IA, Brown TK. Energetics of free-ranging mammals, reptiles, and birds. Annu Rev Nutr. 1999;19:247–277. doi: 10.1146/annurev.nutr.19.1.247. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [4] McNab BK. The influence of food habits on the energetics of eutherian mammals. Ecol Monogr. 1986;56:1–19. [Google Scholar] source

      Not checked in the free run.

    • cites [5] Sibly RM, Brown JH. Effects of body size and lifestyle on evolution of mammal life histories. Proc Natl Acad Sci USA. 2007;104:17707–17712. doi: 10.1073/pnas.0707725104. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [6] Pontzer H, Kamilar JM. Great ranging associated with greater reproductive investment in mammals. Proc Natl Acad Sci USA. 2009;106:192–196. doi: 10.1073/pnas.0806105106. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation
    § Discussion

    Primates generally have low rates of growth and reproduction relative to other mammals.

    “Primates generally have low rates of growth and reproduction relative to other mammals (9).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [9] Charnov EL, Berrigan D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol Anthropol. 1993;1:191–194. [Google Scholar] source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationown data
    § Discussion

    Whereas orangutans appear to be energy minimizers, the comparatively high DEE of humans may suggest our species is adapted to relatively high energy throughput.

    “For example, whereas orangutans appear to be energy minimizers, the comparatively high DEE of humans may suggest our species is adapted to relatively high energy throughput.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given
    § Methods

    Samples remained frozen until analysis using gas-isotope MS, and an aliquot of the DLW batch used for the doses was used for calibration.

    “Samples remained frozen until analysis using gas-isotope MS (William Wong, Houston, TX). An aliquot of the DLW batch used for the doses was used for calibration.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data
    § Methods

    Even substantial variation in the assumed RQ does not significantly affect comparisons with humans and other mammals: if an RQ of 0.85 is assumed, orangutan DEE in our sample was still significantly lower than that in humans (P < 0.001) and lower than all other eutherian mammals except sloths.

    “We note, however, that even substantial variation in the assumed RQ does not significantly affect comparisons with humans and other mammals: if an RQ of 0.85 is assumed, orangutan DEE in our sample was still significantly lower than that in humans (P < 0.001) and lower than all other eutherian mammals except sloths.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing). May combine two claims.

    Interpretationcitation
    § Discussion

    If increased throughput is linked to decreased variance in food availability as proposed previously, the adoption of provisioning behaviors may ultimately explain why human reproductive rates diverged from those of other hominoids.

    “If increased throughput is linked to decreased variance in food availability as proposed previously (4, 6), the adoption of provisioning behaviors may ultimately explain why human reproductive rates diverged from those of other hominoids.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [4] McNab BK. The influence of food habits on the energetics of eutherian mammals. Ecol Monogr. 1986;56:1–19. [Google Scholar] source

      Not checked in the free run.

    • cites [6] Pontzer H, Kamilar JM. Great ranging associated with greater reproductive investment in mammals. Proc Natl Acad Sci USA. 2009;106:192–196. doi: 10.1073/pnas.0806105106. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data
    § Discussion

    Although the slow primate life history strategy is commonly thought to reflect an energy allocation strategy of increased somatic investment and decreased mortality, our results suggest that low growth and reproduction rates may also stem at least in part from decreased energy throughput.

    “Although this slow primate life history strategy is commonly thought to reflect an energy allocation strategy of increased somatic investment and decreased mortality (9), our results suggest that low growth and reproduction rates may also stem at least in part from decreased energy throughput.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [9] Charnov EL, Berrigan D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol Anthropol. 1993;1:191–194. [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data
    § Results

    Although locomotor economy in the Great Ape Trust habitat is likely greater than in the complex arboreal habitat of wild orangutans, improved locomotor economy cannot account for the exceptionally low DEE seen in Great Ape Trust orangutans.

    “Although locomotor economy (i.e., meters traveled per energy consumed) in the Great Ape Trust habitat is likely greater than in the complex arboreal habitat of wild orangutans, improved locomotor economy cannot account for the exceptionally low DEE seen in Great Ape Trust orangutans.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Locomotor economy in the Great Ape Trust habitat is likely greater than in the complex arboreal habitat of wild orangutans.

  • May combine two claims.

    Premisecitation
    § Discussion

    In addition to their low rates of growth and reproduction, orangutans live solitary lifestyles, avoiding the increased foraging costs incurred in large groups, and use locomotor strategies that minimize the cost of travel through the canopy.

    “In addition to their low rates of growth and reproduction (8), orangutans live solitary lifestyles, avoiding the increased foraging costs incurred in large groups (8, 28), and use locomotor strategies that minimize the cost of travel through the canopy (29).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [8] Wich SA, et al. Life history of wild Sumatran orangutans (Pongo abelii) J Hum Evol. 2004;47:385–398. doi: 10.1016/j.jhevol.2004.08.006. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [28] Sugardjito J, te Boekhorst IJA, van Hooff JARAM. Ecological constraints on the grouping of wild orangutans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia. Int J Primatol. 1987;8:17–41. [Google Scholar] source

      Not checked in the free run.

    • cites [29] Thorpe SK, Crompton RH, Alexander RM. Orangutans use compliant branches to lower the energetic cost of locomotion. Biol Lett. 2007;3:253–256. doi: 10.1098/rsbl.2007.0049. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § Discussion

    Data from the wild support this hypothesis for Bornean orangutans, which appear to withstand selective logging reasonably well, but data on Sumatran orangutans are less clear.

    “Data from the wild support this hypothesis for Bornean orangutans, which appear to withstand selective logging reasonably well, but data on Sumatran orangutans are less clear (30).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [30] Husson SJ, et al. In: Orangutans: Geographic Variation in Behavioral Ecology and Conservation. Wich SA, Atmoko SSU, Setia TM, editors. New York: Oxford Univ Press; 2009. pp. 77–96. [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given
    § Methods

    Institutional Animal Care and Use Committee permission was obtained from the Great Ape Trust and Washington University before conducting the study, and institutional guidelines were followed throughout.

    “Institutional Animal Care and Use Committee permission was obtained from the Great Ape Trust and Washington University before conducting the study, and institutional guidelines were followed throughout.”
    Quote in the paperNot a substantial claim
34 of 34

  • The paper relies on this without support.

    Daily energy expenditure (DEE) has never been measured in nonhuman apes.

    “because DEE has never been measured in nonhuman apes.”

  • The paper relies on this without support.

    Locomotor economy in the Great Ape Trust habitat is likely greater than in the complex arboreal habitat of wild orangutans.

    “Although locomotor economy (i.e., meters traveled per energy consumed) in the Great Ape Trust habitat is likely greater than in the complex arboreal habitat of wild orangutans”
2 of 2

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Humans have greater TEE than orangutans, a closely related ape, but have low TEE compared to other eutherian mammals.

    “Humans are known to have greater TEE than orangutans [50], a closely related ape, but have low TEE compared to other eutherian mammals [50], [51].”

    From Hunter-gatherer energetics and human obesity (2012) · cites this paper as [50]

  • Species' metabolic rates reflect their evolutionary history, as TEE responds over evolutionary time to ecological pressures such as food availability and predation risk.

    “A growing body of work on mammalian metabolism is revealing that species’ metabolic rates reflect their evolutionary history, as TEE responds over evolutionary time to ecological pressures such as food availability and predation risk [49], [50].”

    From Hunter-gatherer energetics and human obesity (2012) · cites this paper as [50]

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. SJ Husson, et al. Orangutans: Geographic Variation in Behavioral Ecology and Conservation, eds SA Wich, SSU Atmoko, TM Setia (Oxford Univ Press, New York), pp. 77–96 (2009).
  2. HC Morrogh-Bernard, et al. Orangutans: Geographic Variation in Behavioral Ecology and Conservation, eds SA Wich, SSU Atmoko, TM Setia (Oxford Univ), pp. 119–133 (2009).
  3. I Singleton, et al. Orangutans: Geographic Variation in Behavioral Ecology and Conservation, eds SA Wich, SSU Atmoko, TM Setia (Oxford Univ Press, New York), pp. 205–213 (2009).

Cited by

Sorted by citations

Related

Authors
Pontzer, H., Raichlen, D. A., Shumaker, R. W., Ocobock, C., & Wich, S. A.
Affiliations
  • Washington University in St. Louis (US)
  • University of Arizona (US)
  • George Mason University (US)
  • University of Zurich (CH)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2010-08-02
Volume
107
Issue
32
Pages
14048-14052
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1001031107
PMC
PMC2922585
OpenAlex
W2060256279
Semantic Scholar
13e1213a78a59f3c01b72ed37c86d2e5c8441edd
Cited by
105
References
40
Citations by year
2026: 6 · 2025: 7 · 2024: 8 · 2023: 3 · 2022: 2 · 2021: 8 · 2020: 3 · 2019: 5 · 2018: 3 · 2017: 6 · 2016: 7 · 2015: 9 · 2014: 7 · 2013: 8 · 2012: 11
FWCI
13.05
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich)
Topics
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
orangutans, daily energy expenditure, metabolic rate, great apes, life history, food shortages, captive primate management, human energy use, primate evolution
MeSH terms
Activities of Daily Living, Animals, Energy Metabolism, Biological Evolution, Humans, Growth and Development, Pongo

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.

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