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Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans
Physiology & Behavior 138 (2015) 193–199
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Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans Bruno Simmen a,⁎, Pierre Darlu b, Claude Marcel Hladik a, Patrick Pasquet b a b
Centre National de la Recherche Scientifique/Muséum National d'Histoire Naturelle, UMR 7206-Eco-anthropologie et Ethnobiologie, 1 Avenue du Petit Château, 91800 Brunoy, France Centre National de la Recherche Scientifique/Muséum National d'Histoire Naturelle, UMR 7206-Eco-anthropologie et Ethnologie, 43 rue Buffon, 75005 Paris, France
H I G H L I G H T S • Primates have lower field metabolic rate than other similar-sized eutherian mammals. • Hominins and other primates may share a thrifty energy strategy. • Norms for obesity reduction should take into account low primate energy throughput.
a r t i c l e
i n f o
Article history: Received 7 March 2014 Received in revised form 2 October 2014 Accepted 22 October 2014 Available online 30 October 2014 Keywords: Energy balance Metabolic allometry Field metabolic rate Physical activity Doubly labeled water Eutherian mammals Obesity
a b s t r a c t Studies of how a mammal's daily energy expenditure scales with its body mass suggest that humans, whether Westerners, agro-pastoralists, or hunter–gatherers, all have much lower energy expenditures for their body mass than other mammals. However, non-human primates also differ from other mammals in several life history traits suggestive of low energy use. Judging by field metabolic rates of free-ranging strepsirhine and haplorhine primates with different lifestyle and body mass, estimated using doubly labeled water, primates have lower energy expenditure than other similar-sized eutherian mammals. Daily energy expenditure in humans fell along the regression line of non-human primates. The results suggest that thrifty energy use could be an ancient strategy of primates. Although physical activity is a major component of energy balance, our results suggest a need to revise the basis for establishing norms of energy expenditure in modern humans. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Growing prevalence of obesity in both industrialized and developing countries poses challenges for both health and the economy. Overweight is commonly attributed to excessive energy input, low physical activity and low energy expenditure [1,2] yet the relative influence of these factors, and genetic proneness to fat accumulation, are vigorously debated [3,4]. Marked changes in the energy expenditure of human populations have recently occurred in industrialized societies where office work and other sedentary activities comprise a large part of many people's time budget. To improve our understanding of present-day disorders in human energy balance, one empirical approach has been to compare human energy use with that of our closest living relatives, non-human primates. Meeting energy needs is indeed crucial to most
⁎ Corresponding author at: CNRS/MNHN, 1 Avenue du Petit Château, 91800 Brunoy, France. Tel.: +33 1 60 47 92 33. E-mail address: [email protected] (B. Simmen).
http://dx.doi.org/10.1016/j.physbeh.2014.10.018 0031-9384/© 2014 Elsevier Inc. All rights reserved.
aspects of survival and reproduction among primates and other animals. Although species evolved different behavioral and physiological strategies to meet their basal energy requirements, total energy expenditure in mammals varies with species body mass. Accordingly, using comparative models of bioenergetics should highlight relationships between species' energy metabolism and body mass, offering an evolutionary framework to assess the ‘natural’ level of physical activity characteristic of humans [5–8]. In several recent studies, the mismatch of energy expenditure and energy input and its effect on obesity in actual human populations have been assessed by contrasting human energetics with the scaling of energy use with body mass among other mammals. This approach suggested that modern humans have remarkably low daily energy expenditure for their body mass (e.g. [5,9]), a pattern reported for various types of societies and productive systems. In fact, this conclusion is premature because in different mammal clades energy use may scale differently with body mass [8,10]. For instance, primates differ from other mammals by distinct trade-offs between reproductive and maintenance costs, lower resting metabolic
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rate in strepsirhines, and several other life history traits consistent with low energy use [11–14]. In addition, the only study using doubly labeled water to assess the rate of energy use in a society of hunter–gatherers (presumed representative of ancestral lifestyles of Pleistocene human groups), showed that, surprisingly, total energy expenditure was not markedly different from that of Westerners or farmers once the differences of body mass associated with sex and ethnicity were taken into account [9]. Finally, recent analyses using doubly labeled water (the ‘gold standard’ for studies of daily energy expenditure in free-living vertebrates) suggested that primates as a group, including humans, spend less energy than other mammals with similar body mass [15,16]. Unfortunately, these comparative studies have major flaws, in some cases because the primate sample used for comparison mainly included captive animals. These studies also included a limited array of energy expenditure data from Westerners and subsistence groups in humans, or did not use all data available from eutherian mammals. Moreover, closely related species are more likely to have similar biological traits, which leads to non-independent data points, invalidating the use of ordinary least-squares regression of energy expenditure on body mass [17, 18]. Because these studies compared allometric exponents for different taxa using such regression analyses, they failed to formally control for phylogeny. Hence, the conclusion of unusual, low physical activity of humans derived from comparative studies currently suffers from the lack of an appropriate consideration of the role of phylogeny and adaptation on the evolution of primate metabolic strategies. In this paper we analyze the scaling of energy expenditure in freeranging primates, including humans, using doubly labeled water (DLW) data from ourselves and other primatologists and anthropologists. Specifically, we examine whether human daily energy expenditure falls within the variation derived from the scaling of energy expenditure with body mass in non-human primates. We also assess whether the relationship between field metabolic rate and body mass in primates differs from that found in other eutherian mammals, using phylogenetic least squares (PGLS) regressions to control for phylogeny [18].
2. Material and methods 2.1. Databases on daily energy expenditure in humans, non-human primates, and other mammals The database on daily energy expenditure (DEE) and body mass in free-ranging mammals, published by [8] and updated in [10] and the present study, was used in the analysis. Data on human adults tested with the doubly labeled water (DLW) method are taken from Dugas et al. [19] who list results obtained for various human samples from different populations and countries. We extracted data on 86 eutherian mammals (Table S1; Supplementary material) from the larger set of mammals, including 8 free-ranging, non-human primate species and humans from 100 populations or cohorts (Table 1). Primate data recorded in the natural environment were obtained for Lepilemur, for Eulemur and Lemur, for Alouatta, and for Propithecus. Data on lesser mouse lemurs (Microcebus) derive from two studies carried out in both dry and rain forest in Madagascar. We used data collected by Altmann and coworkers for wild baboons (Papio). Orangutan (Pongo) data are documented for semi-free ranging animals. Although Pongo study conditions might have biased the results toward low energy usage, the authors carefully contrasted the activity budget (including the distance walked and climbed daily) between their study animals and wild individuals. In agreement with the authors [25], we consider their results as sufficiently reliable estimates of energy expenditure in wild orangutans. Other data on laboratory primates have recently been published [15] but these data cannot be considered to be representative of energy expenditure in the wild. The non-human primate sample is small (99 individuals from 8 species) due to constraints on capture/recapture schedules of animals, many of which are large arboreal and endangered species. In their meta-analysis of energy expenditure from DLW of human groups, Dugas et al. [19] distinguished populations with low or middle income from populations with high human development index (HDI), as defined by the United Nations Development Program. Populations selected in this review excluded pathological conditions, intervention studies, and subjects above 65 years of age. They consisted of 13 cohorts
Table 1 Body mass, daily energy expenditure (DEE) and lifestyle in non-human primates and human populations studied with doubly labeled water. Species
Sex
Alouatta palliata
M F M F M F M F
Eulemur sp. Lemur catta Lepilemur ruficaudatus Microcebus murinus Dry forest, dry season idem Dry forest, rainy season idem Evergreen, dry season idem Papio cynocephalus Pongo spp. Propithecus diadema Human populations: Low or middle HDI high HDI
Body mass (g) 8415 ± 1435 6025 ± 318 1875 ± 223 1798 ± 223 2319 ± 295 2188 ± 59 746 ± 14 711 ± 181
M F M F M F F M F M, F
57 ± 9 74 ± 17 60 ± 5 67 59 ± 7 54 ± 10 12,000 ± 1400 116,600 54,100 ± 1273 4900
Men Women Men Women
66,100 59,300 81,300 76,600
± ± ± ±
2900 6900 11,100 12,800
DEE (kJ d−1)
N
Diet
Circadian activity
Ref.
L, F, Fl
Diurnal
[20]
F, L, Fl
Cathemeral
[21]
L, F, Fl
Diurnal
[21]
L, Fl
Nocturnal
[22]
11 12 5 1 10 10 6 1 2 6
I, F, Fl
Nocturnal
[23]
144 339 1135 2462
2910 ± 496 2083 ± 110 597 ± 63 624 ± 122 590 ± 132 709 ± 137 385 ± 100 460 ± 217
2 2 6 5 7 3 3 7
113 ± 32 106 ± 29 142 ± 61 111 67 ± 19 68 ± 14 3400 ± 600 8577 6684 ± 171 1446
12,300 ± 1818 9300 ± 1317 13,500 ± 1900 10,300 ± 1500
[23] [24] I, F, T F, L, Fl
Diurnal Diurnal
[5]a [25]
L, F, Fl
Diurnal
[15]
SL, AF
–
[19]
HC
–
[19]
Humans are subdivided into populations living in low or medium versus high income countries (i.e. with different human development index, HDI), following the meta-analysis of [13]. These include populations living at subsistence level (SL), societies depending on agro-pastoral or agro-farming activities (AF) and Western, industrialized economies relying on manufactured high-calorie (HC) diets. Values are mean ± sd for males (M) and females (F). L: leaf, F: fruit, seed, Fl: flower, I: invertebrate, T: tuber. a As reported by J. Altmann and S. Altmann.
B. Simmen et al. / Physiology & Behavior 138 (2015) 193–199
or populations with low or middle HDI (communities of farmers and fishermen, agro-pastoral communities from various continents with an average body mass index for men and women of circa 23 kg/m2) and up to 87 populations with high HDI (mainly Europeans and Americans from the USA, including normal weight and overweight subjects, with an average BMI at circa 26 kg/m2). Additionally, results obtained recently in the Hadza of Tanzania [9] were used in our study to illustrate differences in the physical activity level between a community of hunter–gatherers among low income populations, and other human populations. 2.2. Total energy expenditure and experimental procedure In the databases used above, total daily energy expenditure and fat mass are determined with DLW. Typically, in DLW studies, stable isotopes (2H and 18O) are used for indirectly measuring carbon dioxide production, which is a measure of energy used. The differential depletion of hydrogen and oxygen as carbon dioxide and water according to behavioral and metabolic activities performed per unit time reveals the rate of carbon dioxide production [26,27]. Doubly labeled water is the gold standard for studies of DEE in wild vertebrates but measurements commonly span a brief segment of an animal's life cycle. However, Nagy et al. [8] analyzed DLW studies of at least 19 mammal species over an annual cycle, some of which cope with drastic seasonal changes in climate. They concluded that DEE varied seasonally, but that such variation was associated with a change of body mass that was predictable from the positive association of DEE and body mass at species level. For the purpose of regression analyses, the DEE data in our study were pooled when seasonal records were available. 2.3. Primate basal metabolic rate and physical activity level Basal rate of oxygen consumption was used to calculate species' physical activity level, i.e. the ratio of DEE to basal metabolic rate (BMR). Basal metabolic rate (BMR) is determined by indirect calorimetry and is available for primate species tested for DEE (Table S2; Supplementary material). For 4 species, experimental records comply with the definition of BMR provided by McNab [28] as the minimum rate of oxygen consumption recorded in fasting, resting adults during their inactive period, within the thermoneutral zone. Results meeting these criteria closely reflect the basal rate of oxygen consumption and are analogous to the BMR measured in humans, for which measures are commonly made early in the morning [29]. For the 3 other primate species in our sample, resting metabolic rate (RMR) is available, generally corresponding to records made on resting individuals during their active phase. The metabolic data used for the nocturnal lesser mouse lemur (Microcebus murinus; [30,31]) have to be presented according to the physiological peculiarities of this species. The notion of basal metabolic rate is elusive in the mouse lemur because it exhibits photoperioddependent physiology, facultative heterothermia and torpor episodes lasting from a few hours to several days. Using the strict criteria described above for determining BMR, a minimal and constant consumption of O2 has been measured within the thermoneutral zone defined between 25–30 °C [32,33]. The measurements avoided recording a torpid metabolic rate by controlling for circadian changes in body temperature. Owing to extreme individual variation in body mass due to seasonal fat accumulation in Microcebus, the rate of oxygen consumption was corrected for fat mass to avoid underestimating BMR. In the closely related strepsirhines Eulemur fulvus and Lemur catta, the minimal rates of metabolism reported [21,34] apparently corresponded to depressed rates of oxygen consumption. Values were 34% and 37% of McNab's [28] prediction of basal metabolic rate from body mass (BMR = 3.53 M0.724, with M in g) and even lower when compared to Kleiber's [35] prediction. The extremely low rate in E. fulvus occurred for very high ambient temperatures. Daniels [34] suggests a more consistent basal metabolic rate at 746 ml O2 h−1
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within the assumed thermoneutral zone. This corresponds to 77% of McNab's prediction, a figure that we used to calculate the physical activity level of E. fulvus and L. catta. 2.4. Statistical analyses We used phylogenetic least squares (PGLS) regressions to test the association between two variables taking into account the phylogenetic relationships between species [18]. We first reconstructed a phylogenetic tree (Fig. 1) from the published database of Bininda-Emonds et al. [36, 37] on mammal phylogenetic relationships with branch length specified. Polytomies were accounted by randomly adding lengths of 1% of the total length of the tree. We then plotted log10 DEE according to log10 body mass with various PGLS models and derived a set of allometric exponents and coefficients. We determined the strength of the phylogenetic signal (λ) in the regressions according to the maximum likelihood in BayesTraits (on-line version of July 2013; [38,39]). Alternative models assume either no effect of phylogeny on the variation observed (λ = 0, as in conventional least-square regressions where the shape of the phylogenetic tree looks like a star and traits evolve following independent Brownian motion along the branches of the star-shaped tree) or full effect (λ = 1, where the tree accounts for the phylogenetic relationships between species and traits evolve along the branches of the phylogenetic tree, as in phylogenetic independent contrast analyses). Intermediate λ values indicate that the traits evolved following a pattern less similar than that expected only from species phylogenetic relationships [39]. Best-fit models were assessed from log-likelihood (Lh) scores [40]. Covariance analysis with bilateral Student's t-test was used to detect differences in slopes and intercepts of regression lines between taxonomic groups according to the best PGLS models, to test the interaction effects between log body mass and these groups, and finally to compare their log DEE residuals from a common regression. Differences are considered significant at α b 0.05 (or lower where mentioned). 3. Results Using phylogenetic generalized least squares (PGLS) models, we find that the correlation between DEE and body mass with log10transformed data is influenced by phylogeny (Table 2). The highest log-likelihood score found for the regression of field metabolic rate on body mass in eutherian mammals including primates (N = 86) indicates a best-fit model when λ = 0.446 (with λ differing significantly from 0 or 1). The slope of the regression line, i.e. the allometric exponent, for eutherian mammals is 0.71 ± 0.03. Best-fit regression indicates that daily energy expenditure in nonhuman primates also increases non-isometrically (i.e. with a slope differing from 1 at 0.55 ± 0.04) with species body mass. Including humans in the primate sample yields a best-fit model with the allometric equation: DEE (in kJ d−1) = 9.8 M0.60 (with M in g). It is noticeable that a disproportionate (95%) part of the variation in log10 DEE in this model is explained by variation in species log10 body mass even though primate species included in the analysis differed considerably in feeding niche, ranging behavior, activity budget, degree of terrestriality, circadian rhythm, thermoregulation ability, and for humans, sociocultural traits. The residual log daily energy expenditure calculated for humans does not differ significantly from the mean residual found in primates (two-way t-test, t = 1.76; ns with α = 0.003; df = 7). This is reflected in Fig. 2 in which average DEE for various human populations including agro-pastoralists and Westerners, is predicted by the scaling of energy expenditure among non-human primates (i.e. they range within the 95% confidence interval of the prediction). In other eutherian mammals, best-fit regression lines indicate an allometric exponent at 0.736 (Table 2). Comparing primates and non-primate eutherian mammals (Fig. 3) shows that the slope of regression lines derived from phylogenetic least squares analyses does not differ significantly between the two groups (t = 1.18; ns; df = 82). The y-intercepts also
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Fig. 1. Phylogenetic tree of eutherian mammals used in PGLS analyses.
do not differ (t = 1.66; ns; df = 84). Accordingly, we calculated the residuals from a common regression using all data and the best-fit PGLS model (N = 86; Table 2) to compare the DEE of primates and other eutherian mammals controlling for body mass differences. The difference between the mean residual values of log DEE for the two groups was significant (t = 2.73; P = 0.008) indicating that primates have significantly lower DEE than other eutherian mammals with similar body mass. The results presented here extend previous findings derived from nonphylogenetically controlled analyses: Homo sapiens is not a unique outlier for the non-primate mammal trendline, and primates overall appear to have low energy expenditure among eutherian mammals. Physical activity level (PAL), the ratio of daily energy expenditure (DEE in kJ d−1) to basal metabolic rate (BMR in kJ d− 1), is a widely
used index that allows assessing the amount of energy spent in various behavioral activities (e.g. locomotion, feeding …) above basal requirements. Given the lack of significant difference in the scaling of basal metabolic rate between primates and other eutherian mammals (allometric exponent without or with phylogenetic inference: 0.71–0.75; [10,41–43]) but low relative DEE in primates (this study), we expect comparatively low PAL for primates. In addition, because low PAL is frequently associated with high levels of adiposity in humans, especially among Westerners, one may expect relatively high body fat proportions in non-human primates. The comparison of PAL between taxa is only tentative due to limited data on both DEE and BMR in medium and large sized mammals including primates (review in [10]). However, from the eight primate species tested here (Fig. 4), six have low PAL
B. Simmen et al. / Physiology & Behavior 138 (2015) 193–199
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Table 2 The relationship between daily energy expenditure and body mass (log DEE = α + β logBM, with DEE in kJ d−1 and BM in g) in eutherian mammals.
All species (N = 86)
Non primates (N = 77) Primates (N = 9)
Lh
α
s.e (β)
β
s.e. (β)
r2
λ
−13.627 7.715 13.513 −13.294 9.590 11.056 7.496 7.658 7.987
0.646 0.681 0.709 0.627 0.654 0.684 1.062 0.805 0.992
0.192 0.051 0.088 0.206 0.050 0.085 0.187 0.141 0.165
0.727 0.738 0.711 0.744 0.760 0.736 0.578 0.645 0.596
0.046 0.018 0.026 0.051 0.018 0.027 0.049 0.038 0.044
0.741 0.954 0.896 0.733 0.958 0.904 0.940 0.970 0.954
[1] [0] 0.446 [1] [0] 0.353 [1] [0] 0.659
Note: Results are shown according to phylogenetic generalized least-square models testing the strength of the phylogenetic signal (λ). Best-fit models occur where log-likelihood (Lh) is maximum. The allometric exponent (β) and coefficient (α) and their standard error (s.e.) are reported for various Lh and λ. The proportion of the variance explained is indicated (r2). Figures in brackets indicate forced values with either no ([λ = 0]) or maximum ([λ = 1]) account of the phylogeny for explaining the variation of field metabolic rate.
(b2.2) compared with other eutherian mammals (mean PAL = 3.4; [44] ). We also observe (Table S3; Supplementary material) that body fat proportion of several primate species overlaps with that reported in human populations. For such comparisons, we used exclusively the few data available for wild animals (most published results on body composition have been obtained from captive animals). Data on fat mass in the lesser mouse lemur, M. murinus, are not available for wild individuals, but it is known that this species undergoes a spectacular seasonal weight increase under natural conditions [45,46]. 4. Discussion Because there is a close connection between body mass, basal energy requirements, energy intake, adiposity and lifestyle among animal species, it is important to determine whether the relationship between energy expenditure and body mass in humans derives from a peculiar regression line distinguishing primates from all other eutherian mammals, or is an unusual deviation from a general mammalian trend that includes non-human primates. Although there are presently few data available on field metabolic rate determined by DLW in wild primates — DLW is hard to use under natural conditions, our results suggest that primate energetics shows a peculiar trendline among mammals, i.e. free-ranging primates, including humans, spend less energy than other eutherian mammals with similar body mass. In the present study, a disproportionate part of the variation in total energy expenditure was explained by variation in species body mass (Table 2) despite other potential sources of variability in our primate sample, such as (i) taxonomic heterogeneity (Malagasy lemurs among strepsirhine versus haplorhine species including howler monkeys, baboons and orangutans), (ii) ecological variability, especially related to distinct dietary adaptations (insectivores, folivores, omnivores), and (iii) differences in the daily activity cycle (nocturnal, cathemeral, diurnal). In addition primate species tested span the full range of body size found in living primates, suggesting that the results may reflect a general pattern of low energy expenditure in primates. The allometric exponent (0.55 ± 0.04) corresponding to the slope for wild primates in the PGLS regression is lower than that (0.69 ± 0.03) reported for a set of captive and wild primates studied with DLW [15] but it is likely that these exponents do not differ statistically — in the same way as the exponents for primates do not differ significantly from those for other mammals (close to 0.75) in both studies. Although lemurs are heavily represented in our sample, the slope difference between the two primate studies is not due to taxonomic bias arising from lemurs having low DEE for their body mass. Lemurs have low body mass compared to the other primates that we sampled. Insofar as they are hypometabolic, one would expect them to steepen the slope found in our study, nonetheless, our slope is
Fig. 2. Plot of daily energy expenditure (DEE) on body mass in primate species. The best-fit regression line (solid line) is drawn for non-human primates using mean species data fitted from PGLS analyses. DEE at species level (determined with the doubly labeled water method) varies as DEE = 14.3 M0.548. Human groups with different human development index (HDI) are shown but are not included in the calculation of the regression. Human data fall within the 95% confidence interval of the prediction for non-human primates (dotted line).
significantly lower than that reported by Pontzer et al. A low DEE is also not consistently predicted from a low BMR in lemurs. The daily energy expenditure in 2 (Microcebus and Lepilemur) out of 4 lemur species tested in our study reaches up to 4 times the BMR (i.e. PAL = 4). Assuming that basal metabolic rate in Propithecus diadema is only 45% of Kleiber's equation (as found in the closely related species Propithecus verreauxi), we calculate a PAL at 1446 kJ d−1/433 kJ d−1 = 3.3 for this lemur species. In contrast, the PAL of 4 anthropoid species tested is ≤2 (Table S3; see also [47]). We note however that the mixed sample of captive and wild primate species [15] includes a larger proportion of terrestrial species in the sample, especially species above 10 kg. Muscle mass proportion varies between 21 and 50% of the total body mass in primates, and terrestrial primates have larger muscle mass proportion than arboreal primates after controlling for body mass differences [48] . Accordingly terrestrial species might spend more energy to sustain this metabolically active tissue and to perform their locomotor activity. Although more data is needed on the field metabolic rate of wild primates showing various lifestyles and taxonomic diversity, both studies of the scaling of energy expenditure concur to show the low energy expenditure of primates relative to other eutherian mammals. The anatomical and functional bases for this metabolic pattern may result from the low proportion of muscular mass relative to total body mass in primates compared with other mammals, as recently shown by
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Fig. 4. Physical activity level (PAL) in free-ranging primate species and humans in various populations. PAL is defined as the ratio of daily energy expenditure to basal rate of energy use. Values are means ± sd (except in Papio where sd is not available). The data for a community of hunter–gatherers (the Hadza) and results averaged for human populations with low to middle human development index (HDI) or high HDI (mainly Westerners) are shown. M: men; F: women. The number of individuals used per species is indicated in Table 1. The average PAL (±sd; hatched area) for eutherian mammals studied with similar methods (n = 45 for species b2 kg; [44]) is shown for comparison.
Fig. 3. Daily energy expenditure in relation to body mass in primates and other eutherian mammals. Energy expenditure is determined using doubly labeled water. Allometric exponents (β) are derived from PGLS models (see Table 2).
Applied to public health policies, the range of physical activity and energy intake that could adequately match variation in human body size and energy requirements should be evaluated taking into account the scaling of primate daily energy expenditure. Although in some human cultures, massive fat accumulation reflects social prestige [29], the increasing prevalence of human obesity is indeed a worldwide concern because of its impact on health. Weight loss in obese or overweight sedentary individuals is often postulated to depend on a combination of appropriate physical activity, feeding behavior and diet quality. As a matter of fact, low energy expenditure in human populations partly reflects the prevalence of thrifty energy strategies among primates. Although physical activity remains a necessary component of everyday life, it seems at least as important to focus on controlling excessive food intake and poor diet, for instance by promoting changes in preferences and attitudes toward foods [51,52]. Acknowledgments
Muchlinski et al. [48]. In parallel, our preliminary analyses of adiposity show that wild primates tested have relatively high body fat proportions, with species peculiarities: for instance, baboons (Papio cynocephalus) have relatively low fat mass, but interestingly, they also are largely terrestrial and show high DEE for their body mass. As hypothesized above, a high degree of terrestriality may involve higher energy costs compared with arboreal species. From an evolutionary perspective, thrifty energy metabolism may have evolved early in primates since both strepsirhines and haplorhines share this trait. Small-bodied strepsirhine species that fall on the eutherian mammal regression line actually correspond to species that rely on facultative heterothermy and a torpid metabolism during extreme decrease of food availability [30,32]. This also suggests that the metabolic peculiarity distinguishing primates from other placental mammals may have been shared by hominins. According to the present database on primates, early hominins, a diverse primate group adapted to various environmental conditions and food sources, could have been thrifty energy-users. Transition from hunter–gatherers to agricultural societies during the Neolithic did not necessarily involve a major change in the energy balance. In contrast, reduced activity and proneness to fattening thanks to an increasing supply of high-calorie foods became maladaptive in modern sedentary societies [49], especially if fructose and other sweeteners perturb the cellular metabolism, as recent qualitative models of metabolic disorders suggest [50].
We are grateful to Egbert G. Leigh Jr. who made valuable comments on this manuscript. We are also indebted to Jonathan C. Wells and two other anonymous reviewers for their constructive remarks. Funding for this study was provided by the CNRS and the National Museum of National History. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.physbeh.2014.10.018. References [1] Tsigos C, et al. Management of obesity in adults: European clinical practice guidelines. Obes Facts 2008;1:106–16. [2] World Health Organization global recommendations on physical activity for health. Geneva: WHO Press; 2010. [3] Barness LA, Opitz JM, Gilbert-Barness E. Obesity: genetic, molecular, and environmental aspects. Am J Med Genet A 2007;143A:3016–34. [4] Tate DF, Jeffery RW, Sherwood NE, Wing RR. Long-term weight losses associated with prescription of higher physical activity goals. Are higher levels of physical activity protective against weight regain? Am J Clin Nutr 2007;85:954–9. [5] Hayes M, et al. Low physical activity levels of modern Homo sapiens among freeranging mammals. Int J Obes 2005;29:151–6. [6] Leonard WR, Ulizaszek SJ. Energetics and evolution: an emerging research domain. Am J Hum Biol 2002;14:547–50.
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Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans Bruno Simmen a,⁎, Pierre Darlu b, Claude Marcel Hladik a, Patrick Pasquet b a b
Centre National de la Recherche Scientifique/Muséum National d'Histoire Naturelle, UMR 7206-Eco-anthropologie et Ethnobiologie, 1 Avenue du Petit Château, 91800 Brunoy, France Centre National de la Recherche Scientifique/Muséum National d'Histoire Naturelle, UMR 7206-Eco-anthropologie et Ethnologie, 43 rue Buffon, 75005 Paris, France
H I G H L I G H T S • Primates have lower field metabolic rate than other similar-sized eutherian mammals. • Hominins and other primates may share a thrifty energy strategy. • Norms for obesity reduction should take into account low primate energy throughput.
a r t i c l e
i n f o
Article history: Received 7 March 2014 Received in revised form 2 October 2014 Accepted 22 October 2014 Available online 30 October 2014 Keywords: Energy balance Metabolic allometry Field metabolic rate Physical activity Doubly labeled water Eutherian mammals Obesity
a b s t r a c t Studies of how a mammal's daily energy expenditure scales with its body mass suggest that humans, whether Westerners, agro-pastoralists, or hunter–gatherers, all have much lower energy expenditures for their body mass than other mammals. However, non-human primates also differ from other mammals in several life history traits suggestive of low energy use. Judging by field metabolic rates of free-ranging strepsirhine and haplorhine primates with different lifestyle and body mass, estimated using doubly labeled water, primates have lower energy expenditure than other similar-sized eutherian mammals. Daily energy expenditure in humans fell along the regression line of non-human primates. The results suggest that thrifty energy use could be an ancient strategy of primates. Although physical activity is a major component of energy balance, our results suggest a need to revise the basis for establishing norms of energy expenditure in modern humans. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Growing prevalence of obesity in both industrialized and developing countries poses challenges for both health and the economy. Overweight is commonly attributed to excessive energy input, low physical activity and low energy expenditure [1,2] yet the relative influence of these factors, and genetic proneness to fat accumulation, are vigorously debated [3,4]. Marked changes in the energy expenditure of human populations have recently occurred in industrialized societies where office work and other sedentary activities comprise a large part of many people's time budget. To improve our understanding of present-day disorders in human energy balance, one empirical approach has been to compare human energy use with that of our closest living relatives, non-human primates. Meeting energy needs is indeed crucial to most
⁎ Corresponding author at: CNRS/MNHN, 1 Avenue du Petit Château, 91800 Brunoy, France. Tel.: +33 1 60 47 92 33. E-mail address: [email protected] (B. Simmen).
http://dx.doi.org/10.1016/j.physbeh.2014.10.018 0031-9384/© 2014 Elsevier Inc. All rights reserved.
aspects of survival and reproduction among primates and other animals. Although species evolved different behavioral and physiological strategies to meet their basal energy requirements, total energy expenditure in mammals varies with species body mass. Accordingly, using comparative models of bioenergetics should highlight relationships between species' energy metabolism and body mass, offering an evolutionary framework to assess the ‘natural’ level of physical activity characteristic of humans [5–8]. In several recent studies, the mismatch of energy expenditure and energy input and its effect on obesity in actual human populations have been assessed by contrasting human energetics with the scaling of energy use with body mass among other mammals. This approach suggested that modern humans have remarkably low daily energy expenditure for their body mass (e.g. [5,9]), a pattern reported for various types of societies and productive systems. In fact, this conclusion is premature because in different mammal clades energy use may scale differently with body mass [8,10]. For instance, primates differ from other mammals by distinct trade-offs between reproductive and maintenance costs, lower resting metabolic
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B. Simmen et al. / Physiology & Behavior 138 (2015) 193–199
rate in strepsirhines, and several other life history traits consistent with low energy use [11–14]. In addition, the only study using doubly labeled water to assess the rate of energy use in a society of hunter–gatherers (presumed representative of ancestral lifestyles of Pleistocene human groups), showed that, surprisingly, total energy expenditure was not markedly different from that of Westerners or farmers once the differences of body mass associated with sex and ethnicity were taken into account [9]. Finally, recent analyses using doubly labeled water (the ‘gold standard’ for studies of daily energy expenditure in free-living vertebrates) suggested that primates as a group, including humans, spend less energy than other mammals with similar body mass [15,16]. Unfortunately, these comparative studies have major flaws, in some cases because the primate sample used for comparison mainly included captive animals. These studies also included a limited array of energy expenditure data from Westerners and subsistence groups in humans, or did not use all data available from eutherian mammals. Moreover, closely related species are more likely to have similar biological traits, which leads to non-independent data points, invalidating the use of ordinary least-squares regression of energy expenditure on body mass [17, 18]. Because these studies compared allometric exponents for different taxa using such regression analyses, they failed to formally control for phylogeny. Hence, the conclusion of unusual, low physical activity of humans derived from comparative studies currently suffers from the lack of an appropriate consideration of the role of phylogeny and adaptation on the evolution of primate metabolic strategies. In this paper we analyze the scaling of energy expenditure in freeranging primates, including humans, using doubly labeled water (DLW) data from ourselves and other primatologists and anthropologists. Specifically, we examine whether human daily energy expenditure falls within the variation derived from the scaling of energy expenditure with body mass in non-human primates. We also assess whether the relationship between field metabolic rate and body mass in primates differs from that found in other eutherian mammals, using phylogenetic least squares (PGLS) regressions to control for phylogeny [18].
2. Material and methods 2.1. Databases on daily energy expenditure in humans, non-human primates, and other mammals The database on daily energy expenditure (DEE) and body mass in free-ranging mammals, published by [8] and updated in [10] and the present study, was used in the analysis. Data on human adults tested with the doubly labeled water (DLW) method are taken from Dugas et al. [19] who list results obtained for various human samples from different populations and countries. We extracted data on 86 eutherian mammals (Table S1; Supplementary material) from the larger set of mammals, including 8 free-ranging, non-human primate species and humans from 100 populations or cohorts (Table 1). Primate data recorded in the natural environment were obtained for Lepilemur, for Eulemur and Lemur, for Alouatta, and for Propithecus. Data on lesser mouse lemurs (Microcebus) derive from two studies carried out in both dry and rain forest in Madagascar. We used data collected by Altmann and coworkers for wild baboons (Papio). Orangutan (Pongo) data are documented for semi-free ranging animals. Although Pongo study conditions might have biased the results toward low energy usage, the authors carefully contrasted the activity budget (including the distance walked and climbed daily) between their study animals and wild individuals. In agreement with the authors [25], we consider their results as sufficiently reliable estimates of energy expenditure in wild orangutans. Other data on laboratory primates have recently been published [15] but these data cannot be considered to be representative of energy expenditure in the wild. The non-human primate sample is small (99 individuals from 8 species) due to constraints on capture/recapture schedules of animals, many of which are large arboreal and endangered species. In their meta-analysis of energy expenditure from DLW of human groups, Dugas et al. [19] distinguished populations with low or middle income from populations with high human development index (HDI), as defined by the United Nations Development Program. Populations selected in this review excluded pathological conditions, intervention studies, and subjects above 65 years of age. They consisted of 13 cohorts
Table 1 Body mass, daily energy expenditure (DEE) and lifestyle in non-human primates and human populations studied with doubly labeled water. Species
Sex
Alouatta palliata
M F M F M F M F
Eulemur sp. Lemur catta Lepilemur ruficaudatus Microcebus murinus Dry forest, dry season idem Dry forest, rainy season idem Evergreen, dry season idem Papio cynocephalus Pongo spp. Propithecus diadema Human populations: Low or middle HDI high HDI
Body mass (g) 8415 ± 1435 6025 ± 318 1875 ± 223 1798 ± 223 2319 ± 295 2188 ± 59 746 ± 14 711 ± 181
M F M F M F F M F M, F
57 ± 9 74 ± 17 60 ± 5 67 59 ± 7 54 ± 10 12,000 ± 1400 116,600 54,100 ± 1273 4900
Men Women Men Women
66,100 59,300 81,300 76,600
± ± ± ±
2900 6900 11,100 12,800
DEE (kJ d−1)
N
Diet
Circadian activity
Ref.
L, F, Fl
Diurnal
[20]
F, L, Fl
Cathemeral
[21]
L, F, Fl
Diurnal
[21]
L, Fl
Nocturnal
[22]
11 12 5 1 10 10 6 1 2 6
I, F, Fl
Nocturnal
[23]
144 339 1135 2462
2910 ± 496 2083 ± 110 597 ± 63 624 ± 122 590 ± 132 709 ± 137 385 ± 100 460 ± 217
2 2 6 5 7 3 3 7
113 ± 32 106 ± 29 142 ± 61 111 67 ± 19 68 ± 14 3400 ± 600 8577 6684 ± 171 1446
12,300 ± 1818 9300 ± 1317 13,500 ± 1900 10,300 ± 1500
[23] [24] I, F, T F, L, Fl
Diurnal Diurnal
[5]a [25]
L, F, Fl
Diurnal
[15]
SL, AF
–
[19]
HC
–
[19]
Humans are subdivided into populations living in low or medium versus high income countries (i.e. with different human development index, HDI), following the meta-analysis of [13]. These include populations living at subsistence level (SL), societies depending on agro-pastoral or agro-farming activities (AF) and Western, industrialized economies relying on manufactured high-calorie (HC) diets. Values are mean ± sd for males (M) and females (F). L: leaf, F: fruit, seed, Fl: flower, I: invertebrate, T: tuber. a As reported by J. Altmann and S. Altmann.
B. Simmen et al. / Physiology & Behavior 138 (2015) 193–199
or populations with low or middle HDI (communities of farmers and fishermen, agro-pastoral communities from various continents with an average body mass index for men and women of circa 23 kg/m2) and up to 87 populations with high HDI (mainly Europeans and Americans from the USA, including normal weight and overweight subjects, with an average BMI at circa 26 kg/m2). Additionally, results obtained recently in the Hadza of Tanzania [9] were used in our study to illustrate differences in the physical activity level between a community of hunter–gatherers among low income populations, and other human populations. 2.2. Total energy expenditure and experimental procedure In the databases used above, total daily energy expenditure and fat mass are determined with DLW. Typically, in DLW studies, stable isotopes (2H and 18O) are used for indirectly measuring carbon dioxide production, which is a measure of energy used. The differential depletion of hydrogen and oxygen as carbon dioxide and water according to behavioral and metabolic activities performed per unit time reveals the rate of carbon dioxide production [26,27]. Doubly labeled water is the gold standard for studies of DEE in wild vertebrates but measurements commonly span a brief segment of an animal's life cycle. However, Nagy et al. [8] analyzed DLW studies of at least 19 mammal species over an annual cycle, some of which cope with drastic seasonal changes in climate. They concluded that DEE varied seasonally, but that such variation was associated with a change of body mass that was predictable from the positive association of DEE and body mass at species level. For the purpose of regression analyses, the DEE data in our study were pooled when seasonal records were available. 2.3. Primate basal metabolic rate and physical activity level Basal rate of oxygen consumption was used to calculate species' physical activity level, i.e. the ratio of DEE to basal metabolic rate (BMR). Basal metabolic rate (BMR) is determined by indirect calorimetry and is available for primate species tested for DEE (Table S2; Supplementary material). For 4 species, experimental records comply with the definition of BMR provided by McNab [28] as the minimum rate of oxygen consumption recorded in fasting, resting adults during their inactive period, within the thermoneutral zone. Results meeting these criteria closely reflect the basal rate of oxygen consumption and are analogous to the BMR measured in humans, for which measures are commonly made early in the morning [29]. For the 3 other primate species in our sample, resting metabolic rate (RMR) is available, generally corresponding to records made on resting individuals during their active phase. The metabolic data used for the nocturnal lesser mouse lemur (Microcebus murinus; [30,31]) have to be presented according to the physiological peculiarities of this species. The notion of basal metabolic rate is elusive in the mouse lemur because it exhibits photoperioddependent physiology, facultative heterothermia and torpor episodes lasting from a few hours to several days. Using the strict criteria described above for determining BMR, a minimal and constant consumption of O2 has been measured within the thermoneutral zone defined between 25–30 °C [32,33]. The measurements avoided recording a torpid metabolic rate by controlling for circadian changes in body temperature. Owing to extreme individual variation in body mass due to seasonal fat accumulation in Microcebus, the rate of oxygen consumption was corrected for fat mass to avoid underestimating BMR. In the closely related strepsirhines Eulemur fulvus and Lemur catta, the minimal rates of metabolism reported [21,34] apparently corresponded to depressed rates of oxygen consumption. Values were 34% and 37% of McNab's [28] prediction of basal metabolic rate from body mass (BMR = 3.53 M0.724, with M in g) and even lower when compared to Kleiber's [35] prediction. The extremely low rate in E. fulvus occurred for very high ambient temperatures. Daniels [34] suggests a more consistent basal metabolic rate at 746 ml O2 h−1
195
within the assumed thermoneutral zone. This corresponds to 77% of McNab's prediction, a figure that we used to calculate the physical activity level of E. fulvus and L. catta. 2.4. Statistical analyses We used phylogenetic least squares (PGLS) regressions to test the association between two variables taking into account the phylogenetic relationships between species [18]. We first reconstructed a phylogenetic tree (Fig. 1) from the published database of Bininda-Emonds et al. [36, 37] on mammal phylogenetic relationships with branch length specified. Polytomies were accounted by randomly adding lengths of 1% of the total length of the tree. We then plotted log10 DEE according to log10 body mass with various PGLS models and derived a set of allometric exponents and coefficients. We determined the strength of the phylogenetic signal (λ) in the regressions according to the maximum likelihood in BayesTraits (on-line version of July 2013; [38,39]). Alternative models assume either no effect of phylogeny on the variation observed (λ = 0, as in conventional least-square regressions where the shape of the phylogenetic tree looks like a star and traits evolve following independent Brownian motion along the branches of the star-shaped tree) or full effect (λ = 1, where the tree accounts for the phylogenetic relationships between species and traits evolve along the branches of the phylogenetic tree, as in phylogenetic independent contrast analyses). Intermediate λ values indicate that the traits evolved following a pattern less similar than that expected only from species phylogenetic relationships [39]. Best-fit models were assessed from log-likelihood (Lh) scores [40]. Covariance analysis with bilateral Student's t-test was used to detect differences in slopes and intercepts of regression lines between taxonomic groups according to the best PGLS models, to test the interaction effects between log body mass and these groups, and finally to compare their log DEE residuals from a common regression. Differences are considered significant at α b 0.05 (or lower where mentioned). 3. Results Using phylogenetic generalized least squares (PGLS) models, we find that the correlation between DEE and body mass with log10transformed data is influenced by phylogeny (Table 2). The highest log-likelihood score found for the regression of field metabolic rate on body mass in eutherian mammals including primates (N = 86) indicates a best-fit model when λ = 0.446 (with λ differing significantly from 0 or 1). The slope of the regression line, i.e. the allometric exponent, for eutherian mammals is 0.71 ± 0.03. Best-fit regression indicates that daily energy expenditure in nonhuman primates also increases non-isometrically (i.e. with a slope differing from 1 at 0.55 ± 0.04) with species body mass. Including humans in the primate sample yields a best-fit model with the allometric equation: DEE (in kJ d−1) = 9.8 M0.60 (with M in g). It is noticeable that a disproportionate (95%) part of the variation in log10 DEE in this model is explained by variation in species log10 body mass even though primate species included in the analysis differed considerably in feeding niche, ranging behavior, activity budget, degree of terrestriality, circadian rhythm, thermoregulation ability, and for humans, sociocultural traits. The residual log daily energy expenditure calculated for humans does not differ significantly from the mean residual found in primates (two-way t-test, t = 1.76; ns with α = 0.003; df = 7). This is reflected in Fig. 2 in which average DEE for various human populations including agro-pastoralists and Westerners, is predicted by the scaling of energy expenditure among non-human primates (i.e. they range within the 95% confidence interval of the prediction). In other eutherian mammals, best-fit regression lines indicate an allometric exponent at 0.736 (Table 2). Comparing primates and non-primate eutherian mammals (Fig. 3) shows that the slope of regression lines derived from phylogenetic least squares analyses does not differ significantly between the two groups (t = 1.18; ns; df = 82). The y-intercepts also
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B. Simmen et al. / Physiology & Behavior 138 (2015) 193–199
Fig. 1. Phylogenetic tree of eutherian mammals used in PGLS analyses.
do not differ (t = 1.66; ns; df = 84). Accordingly, we calculated the residuals from a common regression using all data and the best-fit PGLS model (N = 86; Table 2) to compare the DEE of primates and other eutherian mammals controlling for body mass differences. The difference between the mean residual values of log DEE for the two groups was significant (t = 2.73; P = 0.008) indicating that primates have significantly lower DEE than other eutherian mammals with similar body mass. The results presented here extend previous findings derived from nonphylogenetically controlled analyses: Homo sapiens is not a unique outlier for the non-primate mammal trendline, and primates overall appear to have low energy expenditure among eutherian mammals. Physical activity level (PAL), the ratio of daily energy expenditure (DEE in kJ d−1) to basal metabolic rate (BMR in kJ d− 1), is a widely
used index that allows assessing the amount of energy spent in various behavioral activities (e.g. locomotion, feeding …) above basal requirements. Given the lack of significant difference in the scaling of basal metabolic rate between primates and other eutherian mammals (allometric exponent without or with phylogenetic inference: 0.71–0.75; [10,41–43]) but low relative DEE in primates (this study), we expect comparatively low PAL for primates. In addition, because low PAL is frequently associated with high levels of adiposity in humans, especially among Westerners, one may expect relatively high body fat proportions in non-human primates. The comparison of PAL between taxa is only tentative due to limited data on both DEE and BMR in medium and large sized mammals including primates (review in [10]). However, from the eight primate species tested here (Fig. 4), six have low PAL
B. Simmen et al. / Physiology & Behavior 138 (2015) 193–199
197
Table 2 The relationship between daily energy expenditure and body mass (log DEE = α + β logBM, with DEE in kJ d−1 and BM in g) in eutherian mammals.
All species (N = 86)
Non primates (N = 77) Primates (N = 9)
Lh
α
s.e (β)
β
s.e. (β)
r2
λ
−13.627 7.715 13.513 −13.294 9.590 11.056 7.496 7.658 7.987
0.646 0.681 0.709 0.627 0.654 0.684 1.062 0.805 0.992
0.192 0.051 0.088 0.206 0.050 0.085 0.187 0.141 0.165
0.727 0.738 0.711 0.744 0.760 0.736 0.578 0.645 0.596
0.046 0.018 0.026 0.051 0.018 0.027 0.049 0.038 0.044
0.741 0.954 0.896 0.733 0.958 0.904 0.940 0.970 0.954
[1] [0] 0.446 [1] [0] 0.353 [1] [0] 0.659
Note: Results are shown according to phylogenetic generalized least-square models testing the strength of the phylogenetic signal (λ). Best-fit models occur where log-likelihood (Lh) is maximum. The allometric exponent (β) and coefficient (α) and their standard error (s.e.) are reported for various Lh and λ. The proportion of the variance explained is indicated (r2). Figures in brackets indicate forced values with either no ([λ = 0]) or maximum ([λ = 1]) account of the phylogeny for explaining the variation of field metabolic rate.
(b2.2) compared with other eutherian mammals (mean PAL = 3.4; [44] ). We also observe (Table S3; Supplementary material) that body fat proportion of several primate species overlaps with that reported in human populations. For such comparisons, we used exclusively the few data available for wild animals (most published results on body composition have been obtained from captive animals). Data on fat mass in the lesser mouse lemur, M. murinus, are not available for wild individuals, but it is known that this species undergoes a spectacular seasonal weight increase under natural conditions [45,46]. 4. Discussion Because there is a close connection between body mass, basal energy requirements, energy intake, adiposity and lifestyle among animal species, it is important to determine whether the relationship between energy expenditure and body mass in humans derives from a peculiar regression line distinguishing primates from all other eutherian mammals, or is an unusual deviation from a general mammalian trend that includes non-human primates. Although there are presently few data available on field metabolic rate determined by DLW in wild primates — DLW is hard to use under natural conditions, our results suggest that primate energetics shows a peculiar trendline among mammals, i.e. free-ranging primates, including humans, spend less energy than other eutherian mammals with similar body mass. In the present study, a disproportionate part of the variation in total energy expenditure was explained by variation in species body mass (Table 2) despite other potential sources of variability in our primate sample, such as (i) taxonomic heterogeneity (Malagasy lemurs among strepsirhine versus haplorhine species including howler monkeys, baboons and orangutans), (ii) ecological variability, especially related to distinct dietary adaptations (insectivores, folivores, omnivores), and (iii) differences in the daily activity cycle (nocturnal, cathemeral, diurnal). In addition primate species tested span the full range of body size found in living primates, suggesting that the results may reflect a general pattern of low energy expenditure in primates. The allometric exponent (0.55 ± 0.04) corresponding to the slope for wild primates in the PGLS regression is lower than that (0.69 ± 0.03) reported for a set of captive and wild primates studied with DLW [15] but it is likely that these exponents do not differ statistically — in the same way as the exponents for primates do not differ significantly from those for other mammals (close to 0.75) in both studies. Although lemurs are heavily represented in our sample, the slope difference between the two primate studies is not due to taxonomic bias arising from lemurs having low DEE for their body mass. Lemurs have low body mass compared to the other primates that we sampled. Insofar as they are hypometabolic, one would expect them to steepen the slope found in our study, nonetheless, our slope is
Fig. 2. Plot of daily energy expenditure (DEE) on body mass in primate species. The best-fit regression line (solid line) is drawn for non-human primates using mean species data fitted from PGLS analyses. DEE at species level (determined with the doubly labeled water method) varies as DEE = 14.3 M0.548. Human groups with different human development index (HDI) are shown but are not included in the calculation of the regression. Human data fall within the 95% confidence interval of the prediction for non-human primates (dotted line).
significantly lower than that reported by Pontzer et al. A low DEE is also not consistently predicted from a low BMR in lemurs. The daily energy expenditure in 2 (Microcebus and Lepilemur) out of 4 lemur species tested in our study reaches up to 4 times the BMR (i.e. PAL = 4). Assuming that basal metabolic rate in Propithecus diadema is only 45% of Kleiber's equation (as found in the closely related species Propithecus verreauxi), we calculate a PAL at 1446 kJ d−1/433 kJ d−1 = 3.3 for this lemur species. In contrast, the PAL of 4 anthropoid species tested is ≤2 (Table S3; see also [47]). We note however that the mixed sample of captive and wild primate species [15] includes a larger proportion of terrestrial species in the sample, especially species above 10 kg. Muscle mass proportion varies between 21 and 50% of the total body mass in primates, and terrestrial primates have larger muscle mass proportion than arboreal primates after controlling for body mass differences [48] . Accordingly terrestrial species might spend more energy to sustain this metabolically active tissue and to perform their locomotor activity. Although more data is needed on the field metabolic rate of wild primates showing various lifestyles and taxonomic diversity, both studies of the scaling of energy expenditure concur to show the low energy expenditure of primates relative to other eutherian mammals. The anatomical and functional bases for this metabolic pattern may result from the low proportion of muscular mass relative to total body mass in primates compared with other mammals, as recently shown by
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Fig. 4. Physical activity level (PAL) in free-ranging primate species and humans in various populations. PAL is defined as the ratio of daily energy expenditure to basal rate of energy use. Values are means ± sd (except in Papio where sd is not available). The data for a community of hunter–gatherers (the Hadza) and results averaged for human populations with low to middle human development index (HDI) or high HDI (mainly Westerners) are shown. M: men; F: women. The number of individuals used per species is indicated in Table 1. The average PAL (±sd; hatched area) for eutherian mammals studied with similar methods (n = 45 for species b2 kg; [44]) is shown for comparison.
Fig. 3. Daily energy expenditure in relation to body mass in primates and other eutherian mammals. Energy expenditure is determined using doubly labeled water. Allometric exponents (β) are derived from PGLS models (see Table 2).
Applied to public health policies, the range of physical activity and energy intake that could adequately match variation in human body size and energy requirements should be evaluated taking into account the scaling of primate daily energy expenditure. Although in some human cultures, massive fat accumulation reflects social prestige [29], the increasing prevalence of human obesity is indeed a worldwide concern because of its impact on health. Weight loss in obese or overweight sedentary individuals is often postulated to depend on a combination of appropriate physical activity, feeding behavior and diet quality. As a matter of fact, low energy expenditure in human populations partly reflects the prevalence of thrifty energy strategies among primates. Although physical activity remains a necessary component of everyday life, it seems at least as important to focus on controlling excessive food intake and poor diet, for instance by promoting changes in preferences and attitudes toward foods [51,52]. Acknowledgments
Muchlinski et al. [48]. In parallel, our preliminary analyses of adiposity show that wild primates tested have relatively high body fat proportions, with species peculiarities: for instance, baboons (Papio cynocephalus) have relatively low fat mass, but interestingly, they also are largely terrestrial and show high DEE for their body mass. As hypothesized above, a high degree of terrestriality may involve higher energy costs compared with arboreal species. From an evolutionary perspective, thrifty energy metabolism may have evolved early in primates since both strepsirhines and haplorhines share this trait. Small-bodied strepsirhine species that fall on the eutherian mammal regression line actually correspond to species that rely on facultative heterothermy and a torpid metabolism during extreme decrease of food availability [30,32]. This also suggests that the metabolic peculiarity distinguishing primates from other placental mammals may have been shared by hominins. According to the present database on primates, early hominins, a diverse primate group adapted to various environmental conditions and food sources, could have been thrifty energy-users. Transition from hunter–gatherers to agricultural societies during the Neolithic did not necessarily involve a major change in the energy balance. In contrast, reduced activity and proneness to fattening thanks to an increasing supply of high-calorie foods became maladaptive in modern sedentary societies [49], especially if fructose and other sweeteners perturb the cellular metabolism, as recent qualitative models of metabolic disorders suggest [50].
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