
==== Front
Sci Rep
Sci Rep
Scientific Reports
2045-2322
Nature Publishing Group UK London

39289438
72189
10.1038/s41598-024-72189-2
Article
Thermal and morphometric correlates of the extremely low rate of energy use in a wild frugivorous primate, the Mayotte lemur
Simmen B. bruno.simmen@mnhn.fr

1
Quintard B. 2
Lefaux B. 2
Tarnaud L. 1
Correa-Pimpao G. 1
Ibanez R. 1
Blanc S. 3
Zahariev A. 3
1 grid.508487.6 0000 0004 7885 7602 UMR 7206, Eco-Anthropologie, Centre National de la Recherche Scientifique, Muséum National d’Histoire Naturelle, Université de Paris, Brunoy, France
2 Parc Zoologique et Botanique de Mulhouse, 68100 Mulhouse, France
3 grid.11843.3f 0000 0001 2157 9291 UMR 7178, Institut Pluridisciplinaire Hubert Curien, Centre National de la Recherche Scientifique, Université Louis Pasteur, Strasbourg, France
17 9 2024
17 9 2024
2024
14 2170011 4 2024
4 9 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Primates spend on average half as much energy as other placental mammals while expressing a wide range of lifestyles. However, little is known about how primates adapt their rate of energy use in the context of natural environmental variations. Using doubly labelled water, behavioral and accelerometric methods, we measured the total energy expenditure (TEE) and body composition of a population of Eulemur fulvus (N = 12) living in an agroforest in Mayotte. We show that the TEE of this medium-sized cathemeral primate is one of the lowest recorded to date in eutherians. Regression models show that individual variation in the rate of energy use is predicted by fat-free mass, body size, thigh thickness and maximum temperature. TEE is positively correlated with increasing temperature, suggesting that thermoregulation is an important component of the energy budget of this frugivorous species. Mass-specific TEE is only 10% lower than that of a closely related species previously studied in a gallery forest, consistent with the assertion that TEE varies within narrow physiological limits. As lemur communities include many species with unique thermoregulatory adaptations, circadian and/or seasonal temperature variations may have constituted a major selective pressure on the evolution of lemur metabolic strategies.

Keywords

Doubly labeled water
Field metabolic rate
Fattening
Seasonality
Heat stress
Body composition
Subject terms

Ecology
Physiology
Fondation François Sommer, CNRS, FRBissue-copyright-statement© Springer Nature Limited 2024
==== Body
pmcIntroduction

Animal survival and reproductive success are linked to how individuals manage their energy balance. Because environments provide limited food supply and can be climatically constraining, the allocation of internal resources to major biological functions while maintaining stable energy balance requires energy trade-offs1–4. Energy allocation can result in sub-optimal fitness outcomes in dynamic environments, whether natural or anthropogenic, when food resources are unusually limited or climate varies unpredictably, which is characteristic of today’s rapidly changing world5,6. This problem is particularly acute in frugivorous species, which are exposed to energy stress in the face of marked spatial and temporal variations in fruit resources7–9. Attempts at estimating the total energetic costs of physiological and behavioral activity in wild mammals have been mostly restricted to small-sized taxa, including rodents, using the doubly-labelled water (DLW) method10,11. In larger-sized taxa (i.e., above 2 kg), the costs are generally indirectly estimated, relying on demographic (e.g., mortality rate, litter size), behavioral (e.g., activity budget, parental care) and physiological (resting metabolic rate or RMR) proxies1,12–16. However, even the use of RMR can be misleading as the ratio of total energy expenditure (TEE) to RMR varies considerably depending on the body mass of the species and how much energy is invested in adjustments to the ecological and social environment17. Among the few large mammals studied, ungulates and carnivores including seals have been the taxa of choice for TEE measurements. More recently, primates have been the focus of attention in this field. They expend much less energy than other placental mammals, which has led to the development of new metabolic evolutionary scenarios for humans10,11,18. However, in order to trace the metabolic evolution of primates, we need to better understand the relationship between energy budget, lifestyle and environmental constraints. Studies in human and non-human primates show that TEE is primarily determined by body mass (or fat-free mass), with body mass variation accounting for 97% of the variation in TEE in interspecies comparison, controlling for phylogeny11,18. Comparisons of mammalian TEE between seasons, between captivity and the wild, and according to activity levels, have led some authors to conclude that energy expenditure varies only within a narrow physiological range (reviewed in10,19,20). This ‘constrained total energy expenditure’ model, highlighted by11,21, is exemplified in ring-tailed lemurs in captivity whose energy expenditure for their mass is 20% higher than that of their wild counterparts19. Similarly, it has been estimated that the cost of walking and climbing in active chimpanzees and orangutans would represent only 10 to 20% of their total energy expenditure22,23, a result that is somewhat counter-intuitive to the common notion of high locomotion costs associated with foraging over large home ranges. Even human hunter-gatherers do not expend more energy than sedentary Western human populations, once the effects of body mass, age and sex are taken into account19. It is argued that the existence of physiological limits to TEE is genetically determined and has been shaped by selective pressures19. The major effect of body mass on a species’ TEE does not rule out the existence of variation, as comparative measurements of TEE among primates show that species deviate positively or negatively from the allometric regression line linking TEE with body mass18. For instance, orang-utans expend very little energy compared to other hominoids and, although the measurements were taken in captivity, the interpretation is that their low metabolic rate enables them to cope with the unpredictable and long-lasting food shortage in the tropical forests of South-East Asia22. Unfortunately, to date, the relationship between TEE and environmental constraints has not been formally examined in any non-human primate species (with one exception in a species expressing torpor24,25).

Lemurs are an ideal model for investigating this functional relationship because they cope with a hypervariable environment26,27. The selective pressures that have influenced the evolution of lemur socio-ecological traits and metabolism are thought to be unpredictable climates (rainfall variability, cyclones) and habitats with highly variable food resources over time26. Contemporary lemur communities include species with unique thermoregulatory characteristics among primates, including heterothermic species (Microcebus and Cheirogaleus spp., Hapalemur griseus28–30) and homeothermic species that deviate from the standard metabolic model (Eulemur fulvus, E. rufus). Several of them (Eulemur rufifrons x collaris, Lemur catta) subsist on a limited energy budget, according to measurements with doubly labelled water and, when this is not the case, they are capable of consuming less easily digestible resources (the folivorous Propithecus and Lepilemur18). Moreover, mouse lemurs (Microcebus murinus) and other solitary cheirogaleids (Cheirogaleus spp.) undergo a fattening period prior to the austral winter29,30. There is suspicion from field measurements that a few gregarious lemurs (Lemur catta, Propithecus verreauxi) also store fat. However, in the latter cases, variations in body fat are deduced from isotopic methods performed on only two individuals (L. catta20), and from measurements of skinfold thickness (P. verreauxi31) which would need to be validated for the species32.

In the present study, we provide quantitative results on the energetics and body composition of a frugivorous/folivorous lemur (Eulemur fulvus) subjected to climatic variability but relative resource stability in an anthropogenic habitat in Mayotte. A previous study in a closely related species (Eulemur rufifrons × collaris) living in a gallery forest in Madagascar suggested the possibility of fattening and reported a thrifty energy budget using isotopic methods20. However, as with all TEE measurements carried out in homeothermic primates, the TEE data from the latter population was not analyzed in relation to environmental factors and did not assess the possibility of seasonal variation.

Here, we applied statistical models to identify morphometric, climatic and astronomic drivers of TEE measured during part of the rainy and dry seasons in Mayotte. The TEE measurements, which explicitly included a seasonal factor for the first time, were supplemented by information on group activity and diet, collected using behavioral methods and accelerometry techniques. Furthermore, to test the existence of metabolic flexibility in taxa known for their ecological adaptability, we relied on the contrast in habitat structure and food supply between our site (an agroforestry system) and the gallery forest of the population of E. × rufifrons × collaris previously studied20. The comparison seems all the more relevant in that individuals of both species, which reproduce seasonally, were tested at the same time in their reproductive cycle, just before the mating period in the wet season (supplemented by the dry season for the Mayotte lemur).

Materials and methods

Ethics

All procedures were carried out in accordance to the ARRIVE guidelines and the guidelines for animal experiments of the European Communities Council Directive of 2010 (2010/63/EU). Captures and DLW experiments were approved by the prefecture of Mayotte (#2020/DEAL/SEPR/274), the Cuvier ethical committee of the MNHN and French Ministry of research (MESRI, APAFIS#27331-20200921173365). Agreements were conditional on a limited number of captures.

Lemur population description and study area

Brown lemurs are primarily arboreal and (sometimes) terrestrial primates that live in small groups and have a highly seasonal breeding season (birth occurs mainly in September/October in Mayotte). The Mayotte lemur has been introduced on the island during the ninth century from Eulemur fulvus populations in northwestern Madagascar. The Malagasy and Mayotte groups form a single clade33, so the Mayotte lemur does not merit a sub-level taxonomic distinction. Lemurs are well adapted to the island environmental characteristics, with an estimated population of seven tens of thousands of individuals over 376 km234. The lemur groups extend well beyond natural forests to occupy all types of forest, agroforests and agricultural areas with some tree cover. Being part of an on-going program on human-primate relationships in Mayotte, the study took place from March to July 2022 in an agroforestry plot of several hectares dedicated to fruit tree cultivation (Tsararano; 12°49′53′′ S, 45°10′22.8′′ E) where 56 individuals were counted. The wooded area is essentially a system of polycultures, mainly orchards, associated with a fairly present tree cover. It is made up of plots of cultivated (e.g., mango tree, guava, Cythera prune, star fruit, avocado trees, edible Annonaceae, Albizia, etc.), and native trees and vines (Saba comorensis), small banana plantations, spaced by more open areas dedicated to the cultivation of passion fruit, pineapple, papaya, and other edible plants intended for cash crops. From four contiguous groups (out of 5 including 11 to 16 individuals per group) strictly foraging within the agroforest area, we captured a total of 17 adults/subadults during two sessions (March and June, corresponding to the end of the wet season with warm months and the early dry season with cool months, respectively). In Mayotte, sub-adults cannot be distinguished by size from adults (i.e., over 3 years old; N = 72; unpublished data, Laurent Tarnaud) but they tend to play more with infants.

Climate

The climate is characterized by a wet season lasting from October to April, followed by a 5-month dry season. Average annual rainfall is 1637 mm, with an average minimum temperature of 20.1 °C and an average maximum temperature of 30.6 °C (15-year data since 2011, Coconi/Météo France weather station, 4 km from our study site). We extracted from this database the mean rainfall, minimum T°, maximum T° and mean T° data corresponding to each individual experimental session (see below). The daily climate data (rainfall and temperatures) obtained for the study year (2022) did not show any significant deviation from an average year.

Since Eulemur fulvus is active both day and night, depending on nocturnal illumination35, astronomical data (sunrise, sunset, moon phases, moonrise and moonset) were gathered from the U.S. Navy website (https://aa.usno.navy.mil/data/). We calculated a nocturnal luminosity index based on the phases of the moon and the duration of the moon's illumination during the night36.

Morphometrics

Animals were anesthetized by qualified veterinarians (BQ and BL) with a CO2 injection rifle using medetomidine (0.1 mg/kg) /ketamine (6 mg/kg; Axience). After darting, the animals were taken to an experimental field station located less than 15 min' walk from the capture site (Fig. SI1). Their immobilization was prolonged for handling purposes, under gas anesthesia (2.5% isoflurane) to facilitate rapid recovery. They were weighted and skinfold thickness was measured twice to the nearest 0.1 mm using a sliding caliper (Holtain Tanner/Whitehouse) on 4 body areas known to accumulate fat in lemurs37: abdomen, arm, hip and back sites. Summing the means of these measures yielded a composite fat score38. Additionally, we measured thigh thickness, which is devoid of adipose tissue and potentially reflect muscle activity37. We measured body size as crown-rump length (CRL) with an anthropometer, and calculated the Quetelet index (body mass/crown-rump length239). The tail of anaesthetized animals was shaved in different patterns to facilitate individual recognition. The animals were released on the same day and at the same place where they were captured (between 2:45 and 5:00 h after their capture), as soon as they were deemed sufficiently alert after recovery from anesthesia. Monitoring of the released animals (by behavioral observation and telemetry; see below) showed that they were generally able to return to their group quickly, without any apparent social disruption.

Physiology and behavior

Total energy expenditure per 24 h was measured using doubly labelled water (DLW), as described in20. Detailed methods can be found in the Supplementary Methods, but in brief, the animals were captured/recaptured between 1 and 11 March during the rainy season, and between 26 June and 4 July during the dry season. No attempt was made to measure TEE of females in June, during the gestation period. Individual TEE was determined over a 3 to 5-day period depending on opportunities to recapture individuals. A short time interval between capture and recapture posed no apparent problems as the lemurs were rapidly alert after anesthesia. The isotopic equilibration time after injection of the isotopic water was determined at 2-h post-dose. Blood samples were taken from the inguinal vein and analyses were performed using isotope ratio mass spectrometry on distilled blood samples. The 2-point method was used for calculation40 and the food quotient was set according to the diet, one for the dry season and the other for the wet season (Supplementary Methods). CO2 production was calculated using Speakman's41 most widely used Eq. (7.17), valid for small mammals weighing around 2 kg (for other equations, see42). Total body water, fat-free mass and fat mass were determined from the 18-oxygen dilution space. Lemurs forage as cohesive groups but in order to recapture them in time, six individuals were fitted with a radio-collar (ATS Europe, Oviedo, Spain; model M2940, 58 g), and one individual from each of the 4 focal groups was fitted with a triaxial accelerometer coupled to a GPS (e-obs GmbH, Grünwald, Germany 2020; collar 1AA, 59 g). One additional accelerometer was used alternately on 5 other lemurs in the focal groups, following successive captures and releases. However, due to the restrictive timetable for injections and blood sampling inherent in the isotopic method and the extreme caution required when shooting, it was not possible to recapture all individuals on time. From the 17 individuals captured, 12 were tested for TEE and body composition (6 males and 3 females in March, and 3 males in June).

Activity

To determine the time budget, we used 5-min instantaneous and scan sampling43 on the focal groups, each followed continuously from dawn to dusk (> 150 h of monitoring by observer 1). We began recording group activity shortly after the end of the two capture/recapture sessions. Although the timing of the observations and TEE measurements did not strictly overlap, the behavioral recordings remain broadly indicative of the lemur's general activity budget. Behavioral items were categorized as moving, foraging, feeding, resting, social and miscellaneous. The diet was determined by a second observer following simultaneously the same group as observer 1, by recording the feeding duration (minutes) a given individual devoted to each food item during a 30-min period (focal animal sampling, alternating observations between group members). A total of 234 30-min periods distributed among the focal groups were recorded (wet season: N = 144, dry season: N = 88). Dietary diversity in this study population as in many other Eulemur44–46 is low, so we considered that increasing the monitoring effort would have provided little information on the main foods in this study. In order to assess cathemerality (day and night activity, as is the case in other Eulemur populations), we recorded 24-h activity data from each of the accelerometer-fitted individuals (N = 4, one in each of the focal groups) for the duration of the study.

Statistical analyses

Energy and body composition data were analyzed cross-sectionally due to the limited number of lemurs captured/recaptured at the two study periods. We first performed a PCA on all 12 morphometric and abiotic variables measured, namely body mass, fat-free mass, fat mass, CRL, Quetelet index, skinfold thickness, thigh thickness, mean rainfall, minimum T°, maximum T°, mean T° and the nocturnal luminosity index. The variables retained for subsequent multiple regression analyses and mixed-effects models contributed substantially to three principal components that explained 87% of the variance in the data. The reduction in the number of correlated morphometric variables was carried out using an informed approach, based on the main recognized factors of individual TEE variation (e.g., fat-free mass11). Multiple regression models were then constructed from these selected variables, controlling for non-collinearity (variance inflation factor < 547). Multiple regression analysis was combined with linear mixed-effects modelling to highlight potential differences between groups. As fixed effects, we entered the morphometric and abiotic variables selected above. As random effects, we entered group identity into the mixed-effects model. We checked the normality of the residuals, the homoscedasticity, and the homogeneity of variance. Behavioral data were pooled to determine an activity budget and diet for the population. The sample size did not allow the data to be split by group, but the groups behaved in much the same way (repeated measures ANOVA with permutation48). Members of the same group generally synchronize their movements. We used the R and RStudio softwares (versions 4.2.2 and 2023.09.149,50), packages FactoMineR51 and Rcmdr2.9-252,53 for the descriptive multivariate analyses, car54, effects54,55, lme456 and lmerTest57 for the multiple regression models and mixed models, and permuco58 for the analyses of variance.

Results

Activity budget, cathemeral activity and diet

Accelerometry data shows that lemurs are mainly diurnal and are active to a lesser extent at night (Fig. 1). During the daytime period the time allocated to rest is very important (wet month: 44%, dry month: 62%, with no significant difference between groups and seasons, p = 0.19 and p = 0.29). The lemurs mainly selected plants grown for their sugar- or fat-rich fruit (88% and 60% of total time spent feeding during the wet and dry seasons, respectively), supplemented by significant leaf matter during dry months (26%). Locomotion for foraging and other purposes accounted for less than 30% of the time budget each season. This, combined with home ranges limited to a few hectares per group (Fig. SI1), indicates a strategy of high energy intake and low foraging costs.Fig. 1 An example of circadian activity rhythm (left) and daily activity profile averaged per month (right) recorded by the accelerometry method. The x-axis of the circadian activity rhythm represents the time of day on two consecutive days. Night and day periods are represented by horizontal black and white bars.

Morphometrics

No significant sex differences in body mass (t = 1.657, p = 0.13, df = 11) or body size (t = 0.718, p = 0.49, df = 10) were found during the wet months, the only season in which both sexes were captured (Table SI1). In males, body weight decreased by an average of 13% (290 g) between the wet and dry months while body size did not differ (unpaired t-test; body mass: t = 2.301, p < 0.05, df = 15; CRL: t = 0.185, p = 0.86, df = 14). Measurements of skinfold thickness and fat mass proportion (Table SI1 and SI2) indicate that the large seasonal difference in body weight corresponded to a loss of fat mass rather than muscle mass (unpaired t-test, skinfold thickness index: t = 6.157, p < 0.001, df = 15; percent fat: t = 2.415, p < 0.05, df = 10). These data strongly suggest that brown lemurs undergo a fattening period before the dry season. Thigh thickness was positively correlated with fat mass and total body mass, but not with fat-free mass (Spearman's rank correlation; p < 0.01, p < 0.01, p = 0.22, respectively).

Energy expenditure

Detailed physiological and climatic characteristics recorded for each individual during the experimental phase of the study are presented in Table SI2, SI3 and SI4. Mean individual TEE was 546 kJ day−1 (sd: ± 137 kJ day−1; N = 12; Table SI3). The TEE of males and females did not differ significantly during the rainy months (t = 1.497, p = 0.19) but the small sample size may be a limitation to this result. A regression model (model 1) including only the morphometric predictor variables fat-free mass and body size (crown-rump length) explained 56% of the variation in TEE (Table 1). Adding two other morphometric and abiotic factors, thigh thickness and mean maximal temperature (Table SI1 and SI4), increased the fit of the model up to 85% (model 2; Table 1). Fat-free mass was the strongest predictor, with a positive effect, while body size had a negative effect on TEE. The effect of temperature was significant, with each change of one degree Celsius having a fifteen percent impact on total energy expenditure over the range of maximum temperatures recorded during the experiments (27 to 31.5 °C; Fig. 2). Rainfall accounted for a further 3% of the overall fit, but the term was not significant (model 3, Table 1). The addition of the nocturnal luminosity index did not improve the fit of model 3 (adj r2 = 0.88). In the latter case, however, the individual measurements were obtained during sessions where low-light lunar phases, essentially the new moon and the first crescent (Table SI4), are less favorable to the nocturnal activity of these cathemeral lemurs. Linear mixed-effect models including group identity as a random factor yielded non-significant differences with model 2 incorporating only fixed effects (p = 0.57; Table SI5). Table 1 Multiple regression models predicting total energy expenditure.

	Model 1	Model 2	Model 3	
Predictive factor	β	Std. error	t value	P	β	Std. error	t value	P	β	Std. error	t value	P	
(Intercept)	2048.1	724.8	2.826	*	944.3	533.2	1.774	ns	1750.9	666.8	2.626	*	
Fat-free mass (kg)	568.2	220.3	2.579	*	713.5	158.8	4.494	**	617.8	151.3	4.083	**	
Crown-rump length (cm)	−68.7	19.4	−3.548	**	−104.5	14.6	−7.176	***	−108.9	13.2	−8.281	***	
Thigh thickness (cm)					−139.0	38.3	−3.629	**	−137.1	33.9	−4.036	**	
Temperature maxi (°C)					85.0	20.35	4.179	**	66.9	20.9	3.201	*	
Cumulative rainfall (mm)									2.3	1.4	1.710	ns	
	Adj. r2 = 0.56, df = 9, p < 0.01	Adj. r2 = 0.85, df = 7, p < 0.01	Adj. r2 = 0.88, df = 6, p < 0.01	

Fig. 2 Predictor effect plots of energy expenditure (model 2). Lines and shading in each panel indicate the fitted model and 95% confidence interval, respectively. Dots represent partial model residuals. TEE total energy expenditure, CRL crown-rump length, T° ambient temperature.

Comparison of energy expenditure with other primates and non-primate mammals

The lemurs spent on average 69 ± 17% of the energy expenditure predicted by the TEE:mass regression of primates, controlling for phylogeny (log10 TEE (kJ day−1) = 0.714 + 0.665 × log10 mass (grams)18; Fig. 3). In comparison, the field metabolic rate of adult/subadult brown lemurs (Eulemur rufifrons × collaris) living in a gallery forest in southern Madagascar (Berenty reserve; calculation from Tables 1 and 2 in20) is 79 ± 10% of the energy expected for their body mass. The difference between the two lemur populations (based solely on data collected during the same pre-reproductive period, i.e. just before the mating season during the rainy season) is not significant (Student t-test on the deviation from the TEE:mass regression, t = 1.504, p = 0.15, df = 18). If we consider not only the wet-season TEE measurements but also the dry-season data for Mayotte lemurs, the difference between species is almost significant (t = 2.052, p = 0.052, df = 22) but remains low, at 12%.Fig. 3 Bi-logarithmic plot of total energy expenditure as a function of body mass in primates, highlighting the low field metabolic rate of the Mayotte brown lemur (blue dot). Each dot represents a species. Orange dots: Strepsirrhines (excepted for the Mayotte brown lemur). Black dots: Haplorrhines. The phylogenetic least square regression line is taken from18.

Compared with other non-primate placental mammals, the Mayotte lemur and the Berenty lemur are among the eutherians with the lowest rate of energy use, expending only 43% and 50% respectively of the energy expended by a species of similar size (allometric regression, controlling for phylogeny: log10 TEE (kJ day−1) = 0.684 + 0.736 × log10 mass (grams)59).

Discussion

Populations of brown lemurs in Mayotte (Tsararano, Eulemur fulvus) and Madagascar (Berenty, Eulemur rufifrons × collaris) exhibit the lowest TEE recorded for their body mass compared to a set of 18 primate species tested so far with DLW (Fig. 3). It is tempting to conclude that the low field metabolic rate of the brown lemurs studied here is a direct consequence of their lifestyle in a favorable anthropogenic habitat. In fact, their foraging and locomotor activity characteristics do not differ considerably from those of several other Eulemur populations. The activity budget and the general typology of the diet are similar between the lemurs of Mayotte and those of Berenty, with a large part of the day spent resting, low dietary diversity and a mainly frugivorous diet supplemented by leaves during the dry season44,45,60,61. The brown lemurs of Berenty have larger home ranges62, but in southwestern continuous canopy forests in Madagascar, home ranges as low as 1.0 ha have been found, in association with extremely high population densities (Eulemur rufus63). The broad socio-ecological traits of our lemur population are also similar to those reported in a dry deciduous forest in the south of Mayotte (Saziley): group size and adult sex ratio are comparable to those in the agroforestry plot, and the animals show regular signs of cathemeral activity, with increased nocturnal locomotion during the dry season. In this southern population, the home ranges are also small (< 2 ha), and the poorly diversified diet remains predominantly frugivorous throughout the year (46,64; see also65 for more humid habitats). Strikingly, the only other population of Eulemur equipped with accelerometers (Eulemur rufifrons, Kirindy dry forest, Madagascar) shows a cathemeral activity profile very similar to that found in our study, with predominant daytime activity combined with periods of nocturnal activity circumscribed around the full moon35. Finally, variation in climate, mean annual temperature and annual rainfall all fall within the range reported for several Eulemur habitats in Madagascar. Accordingly, the fact that the energy budget of Mayotte lemurs differs little from that of the Berenty population despite variations in habitat structure and composition would confirm the notion of narrow physiological limits for variation in TEE of a species (or of closely related species in the present case). Recent measurements carried out on captive ring-tailed lemurs (Lemur catta66) show that their TEE differs little from that of their wild counterparts (% deviation from the TEE:mass regression of primates in the ‘Results’ section: 74–81% depending on season versus 71% in Madagascar; calculation from Supplementary data in20,66). Brown lemurs in Mayotte and Madagascar are also among the eutherians with the lowest energy budgets. To date, the few other non-torpid large placental mammals with a very low metabolic rate belong to the folivore guild, such as three-toed sloths or giant pandas (e.g., 28% in wild pandas using the equation for non-primate mammals in the ‘Results’ section;67,68), and by comparison, other mammals such as koalas expend 51% of the energy expected for their mass (versus 43% and 50% in Eulemur; this study). Some believe that cellular metabolic adaptations rather than behavioral adjustments could explain the comparatively low metabolic rates observed in primates19. Once phylogenetic group variation is taken into account, fat-free mass is considered one of the main determinants of energy expenditure11. In our lemur population, fat-free mass had a strong positive effect on TEE while body size and thigh thickness appeared to be negative predictors of TEE variation. The ‘ideal’ somatic conditions for low energy expenditure therefore seem to be met by animals with low fat-free mass and muscular hind limbs. The fact that thigh thickness had a negative impact on TEE (Table 1) and correlates with fat mass and total body mass (but not with fat-free mass) suggests that adipose individuals need more muscular limbs to support their extra weight, but they could save energy by reducing costly activities such as locomotion.

The fact that body size (CRL) had a negative effect on TEE could be understood in relation to the cost of thermoregulation. Considering the significant effect of ambient temperature on the rate of energy use in this lemur, we might assume that a larger skin surface area, which increases with body size, facilitates cooling by evaporation and leads to lower oxygen consumption. In this respect, the maximum ambient temperatures, which varied between 27 and 31.5 °C during the DLW experimental sessions (Table SI4), were above the thermoneutrality zone recorded in Eulemur fulvus (and E. rufus; 19–26 °C69). During the hottest hours of the day, during the rainy season when temperatures exceed 30 °C (which, in 2022, lasted for at least four months), lemurs display thermoregulatory behavior by resting in the shade of trees and increasing their thermal conductance by adopting relaxed reclining postures and resting against large tree branches, similar to the 'tree-hugging' cooling behavior of koalas and sifakas70,71. But as they also need to forage to store fat reserves before the dry season and the mating period (in June), in a way comparable to the bulk feeding observed in another Eulemur44, they remain subject to solar radiation and potential heat stress (61; see68 for a discussion of the neglected risk of hyperthermia). Strikingly, this species deviates from the standard metabolic model in that it shows an extremely depressed metabolic rate (28% of Kleiber) above 30 °C while maintaining its body temperature, and does not increase oxygen consumption when ambient temperatures fall below the thermoneutral zone69. This unusual metabolic response, close to that described in sloths72, suggests that, for a large part of the year, this homeothermic species incurs high thermoregulatory energy costs, mainly when temperatures are warm. The question may arise as to whether the invoked factor of heat stress is not blurred by the confounding effect of seasonality, the covariates of which are rainfall and food supply. This hypothesis is unlikely since only ambient temperature had an impact on energy expenditure, while rainfall played little role and fruit was available throughout the study due to the temporal staggering of fruit crops. Interestingly, the TEE of captive ring-tailed lemurs living in indoor or outdoor enclosures in the northern hemisphere is slightly higher during the warm season compared with the cold season66.

Finally, regarding the link between dietary specialization and metabolism, it should be noted that with the advent of the use of rigorous methods for determining energy expenditure in wild primates, it is now clear that some frugivorous primates (Eulemur spp., Lemur catta: this study,20) rely on energy-saving strategies. This has important implications for scenarios about the evolution of frugivory and primate socioecology, as fruit specialists have long been thought to exhibit high energy input/high energy foraging costs strategies, linked to the search for high quality but spatially and temporally dispersed resources (e.g.,8). In fact, the costs of locomotion in primates are probably much lower than expected22. Energy-saving strategies in some frugivorous primates have probably been selected when there was a major risk of starvation, resulting from a scarcity of fruit resources over long periods or according to an unpredictable phenological pattern (e.g., in orangutans22).

In conclusion, Mayotte lemurs, like Berenty Eulemur, display an overall energy-saving strategy compared with other primates, partly linked to a restful lifestyle but mainly a result of physiological adaptations. Regarding the regulation of thermogenesis, brown lemurs do not seem to be as well equipped to withstand high temperatures as they are to react to cool thermal conditions. Their estimated metabolic scope (TEE/RMR), at 2.4 (using 65% of Kleiber69), could in this regard be partly the result of a significant allocation of energy resources to thermoregulation. The physiological and behavioral peculiarities of lemurs as a taxonomic group, including heterothermy, a thrifty energy budget and the deviation of certain homeothermic species from the standard metabolic model, suggest that the role of abiotic pressures in the metabolic evolution of this group should be better taken into account, in addition to the drastic dietary constraints often put forward. In the near future, rising ambient temperatures73 could exacerbate heat stress. To date, little is known about the thermoregulatory capacities of most of these lemur species, although this knowledge is needed to predict their ability to cope with temperature changes.

Supplementary Information

Supplementary Information.

Supplementary Information

The online version contains supplementary material available at 10.1038/s41598-024-72189-2.

Acknowledgements

We are grateful to Muslim Payet for allowing us to carry out the field study, Bernard Riera and Clara Hozer for their technical support, and Meteo-France for providing climate data. We thank the M2IS (Unistra, Strasbourg, France) core for the analysis of stable isotopes. We are grateful to the 2 anonymous reviewers who helped improve the form and content of the text.

Author contributions

B.S., A.Z., S.B., B.Q., B.L. and L.T. conceived and designed this study; B.S., BQ., B.L., L.T., R.I. and G.C.P. conducted field work; A.Z. carried out laboratory work; B.S., A.Z., B.Q., R.I., G.C.P. and L.T conducted data analysis; B.S. and L.T. wrote the manuscript; B.Q and A.Z. reviewed and improved it.

Funding

This work was supported by the Fondation François Sommer; the CNRS; and the Fondation pour la Recherche sur la Biodiversité (Master fellowship granted to RI).

Data availability

The data that support the findings of this study are included in the paper or in the online version as supplementary information.

Competing interests

The authors declare no competing interests.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
==== Refs
References

1. van Schaik, C. P. & Isler, K. Life-history evolution. In The Evolution of Primate Societies (Mitani, J. et al. eds.). 220–244 (Chicago University Press, 2012).
2. Martin RD MacLarnon AM Gestation period, neonatal size and maternal investment in placental mammals Nature 1985 313 220 223 10.1038/313220a0
Martin, R. D. & MacLarnon, A. M. Gestation period, neonatal size and maternal investment in placental mammals. Nature 313, 220–223 (1985).
3. Read AF Harvey PH Life history differences among the eutherian radiations J. Zool. 1989 219 329 353 10.1111/j.1469-7998.1989.tb02584.x
Read, A. F. & Harvey, P. H. Life history differences among the eutherian radiations. J. Zool. 219, 329–353 (1989).
4. Canale CI Henry P Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability Clim. Res. 2010 43 135 147 10.3354/cr00897
Canale, C. I. & Henry, P. Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim. Res. 43, 135–147 (2010).
5. Visser ME Keeping up with a warming world: Assessing the rate of adaptation to climate change Proc. R. Soc. B. 2008 275 649 659 10.1098/rspb.2007.0997 18211875
Visser, M. E. Keeping up with a warming world: Assessing the rate of adaptation to climate change. Proc. R. Soc. B. 275, 649–659 (2008).18211875
6. Gogarten JF Seasonal mortality patterns in non-human primates: Implications for variation in selection pressures across environments Evolution 2012 66 3252 3266 10.1111/j.1558-5646.2012.01668.x 23025613
Gogarten, J. F. et al. Seasonal mortality patterns in non-human primates: Implications for variation in selection pressures across environments. Evolution 66, 3252–3266 (2012).23025613
7. Janson, C. H. & van Schaik, C. P. Ecological risk aversion in juvenile primates: Slow and steady wins the race. In Juvenile Primates: Life History, Development, and Behavior (Pereira, M. E. & Fairbanks, L. A. eds.). 57–76 (Oxford University Press, 1993).
8. Hladik, C. M. Diet and the evolution of feeding strategies among forest primates. In Omnivorous Primates. Gathering and Hunting in Human Evolution (Harding, R. S. O & Teleki, G. eds.). 215–254 (Columbia University Press, 1981).
9. Oates, J. F. Food distribution and foraging behavior. In Primate Societies (Smuts, B. B., Cheney D. L., Seyfarth, R. M. & Wrangham, R. W. eds.). 197–209 10.7208/9780226220468-019 (University of Chicago Press, 1986).
10. Nagy KA Girard IA Brown TK Energetics of free-ranging mammals, reptiles, and birds Ann. Rev. Nutr. 1999 19 247 277 10.1146/annurev.nutr.19.1.247 10448524
Nagy, K. A., Girard, I. A. & Brown, T. K. Energetics of free-ranging mammals, reptiles, and birds. Ann. Rev. Nutr. 19, 247–277 (1999).10448524
11. Pontzer H Energy expenditure in humans and other primates: A new synthesis Annu. Rev. Anthropol. 2015 44 169 187 10.1146/annurev-anthro-102214-013925
Pontzer, H. Energy expenditure in humans and other primates: A new synthesis. Annu. Rev. Anthropol. 44, 169–187 (2015).
12. 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 10.1002/evan.1360010604
Charnov, E. L. & Berrigan, D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol. Anthropol. 1, 191–194 (1993).
13. Jones JH Primates and the evolution of long, slow life histories Curr. Biol. 2011 21 R708 R717 10.1016/j.cub.2011.08.025 21959161
Jones, J. H. Primates and the evolution of long, slow life histories. Curr. Biol. 21, R708–R717 (2011).21959161
14. Kappeler PM Causes and consequences of life-history variation among strepsirhine primates Am. Nat. 1996 148 868 891 10.1086/285960
Kappeler, P. M. Causes and consequences of life-history variation among strepsirhine primates. Am. Nat. 148, 868–891 (1996).
15. Harvey PH Clutton-Brock TH Primate home-range size and metabolic needs Behav. Ecol. Sociobiol. 1981 8 151 155 10.1007/BF00300828
Harvey, P. H. & Clutton-Brock, T. H. Primate home-range size and metabolic needs. Behav. Ecol. Sociobiol. 8, 151–155 (1981).
16. 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 10.1073/pnas.0707725104 17940028
Sibly, R. M. & Brown, J. H. Effects of body size and lifestyle on evolution of mammal life histories. Proc. Natl. Acad. Sci. USA 104, 17707–17712 (2007).17940028
17. Speakman JR Body size, energy metabolism and lifespan J. Exp. Biol. 2005 208 1717 1730 10.1242/jeb.01556 15855403
Speakman, J. R. Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717–1730 (2005).15855403
18. Simmen B Morino L Blanc S Garcia C The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates Sci. Rep. 2021 11 14196 34244546
Simmen, B., Morino, L., Blanc, S. & Garcia, C. The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates. Sci. Rep. 11, 14196. 10.1038/s41598-021-93764-x (2021).34244546
19. Pontzer H Primate energetics and life history Proc. Natl. Acad. Sci. USA 2014 111 1433 1437 10.1073/pnas.1316940111 24474770
Pontzer, H. et al. Primate energetics and life history. Proc. Natl. Acad. Sci. USA 111, 1433–1437 (2014).24474770
20. Simmen B Total energy expenditure and body composition in two free-living sympatric lemurs PLoS One 2010 5 e9860 20360848
Simmen, B. et al. Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS One 5, e9860. 10.1371/journal.pone.0009860 (2010).20360848
21. Pontzer H Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans Curr. Biol. 2016 26 410 417 10.1016/j.cub.2015.12.046 26832439
Pontzer, H. et al. Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Curr. Biol. 26, 410–417 (2016).26832439
22. Pontzer H Raichlen DA Shumaker RW Ocobock C Wich SA Metabolic adaptation for low energy throughput in orangutans Proc. Natl. Acad. Sci. USA 2010 107 14048 14052 10.1073/pnas.1001031107 20679208
Pontzer, H., Raichlen, D. A., Shumaker, R. W., Ocobock, C. & Wich, S. A. Metabolic adaptation for low energy throughput in orangutans. Proc. Natl. Acad. Sci. USA 107, 14048–14052 (2010).20679208
23. Pontzer, H., Raichlen, D. A. & Sockol, M. D. From treadmill to tropics: Calculating ranging cost in chimpanzees. In Primate Locomotion: Linking Field and Laboratory Research, Developments in Primatology: Progress and Prospects (D’Août, K. & Vereecke, E. E. eds.). 289–309 (Springer, 2011).
24. Schmid J Speakman JR Daily energy expenditure of the grey mouse lemur (Microcebus murinus): A small primate that uses torpor J. Comp. Physiol. B 2000 170 633 641 10.1007/s003600000146 11192269
Schmid, J. & Speakman, J. R. Daily energy expenditure of the grey mouse lemur (Microcebus murinus): A small primate that uses torpor. J. Comp. Physiol. B 170, 633–641 (2000).11192269
25. Schmid J Speakman JR Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): A comparison of dry and wet forests Naturwiss. 2009 96 609 620 10.1007/s00114-009-0515-z 19229507
Schmid, J. & Speakman, J. R. Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): A comparison of dry and wet forests. Naturwiss. 96, 609–620 (2009).19229507
26. Wright PC Lemur traits and Madagascar ecology: Coping with an island environment Yearb. Phys. Anthropol. 1999 42 31 72 10.1002/(SICI)1096-8644(1999)110:29+<31::AID-AJPA3>3.0.CO;2-0
Wright, P. C. Lemur traits and Madagascar ecology: Coping with an island environment. Yearb. Phys. Anthropol. 42, 31–72 (1999).
27. Dewar RE Richard AF Evolution in the hypervariable environment of Madagascar Proc. Natl. Acad. Sci. USA 2007 104 13723 13727 10.1073/pnas.0704346104 17698810
Dewar, R. E. & Richard, A. F. Evolution in the hypervariable environment of Madagascar. Proc. Natl. Acad. Sci. USA 104, 13723–13727 (2007).17698810
28. Bourlière, F., Petter, J. J. & Petter-Rousseaux, A. Variabilité de la température centrale chez les lémuriens. Mém. Inst. Sci. Madagascar Sér. A Tome X, 303–304 (1956).
29. Chevillard, M. C. Capacités Thermorégulatrices d’un Lémurien Malgache, Microcebus murinus (Ph.D. Thesis, University Paris VII, 1976).
30. Blanco MB Dausmann KH Ranaivoarisoa JFV Yoder AD Underground hibernation in a primate Sci. Rep. 2013 3 1768 10.1038/srep01768 23636180
Blanco, M. B., Dausmann, K. H., Ranaivoarisoa, J. F. V. & Yoder, A. D. Underground hibernation in a primate. Sci. Rep. 3, 1768 (2013).23636180
31. Lewis RJ Kappeler PM Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi Am. J. Primatol. 2005 66 1 18 15898070
Lewis, R. J. & Kappeler, P. M. Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi. Am. J. Primatol. 66, 1–18 (2005).15898070
32. Walker ML Schwartz SM Wilson ME Musey PI Estimation of body fat in female rhesus monkeys Am. J. Phys. Anthrop. 1984 63 323 329 10.1002/ajpa.1330630309 6731604
Walker, M. L., Schwartz, S. M., Wilson, M. E. & Musey, P. I. Estimation of body fat in female rhesus monkeys. Am. J. Phys. Anthrop. 63, 323–329 (1984).6731604
33. Pastorini J Forstner MRJ Martin RD Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences Mol. Phylogenet. Evol. 2000 16 418 429 10.1006/mpev.2000.0796 10991794
Pastorini, J., Forstner, M. R. J. & Martin, R. D. Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 16, 418–429 (2000).10991794
34. Tarnaud, L. Eulemur fulvus (Schlegel, 1866), Maki brun. In Atlas des Mammifères Sauvages de France. Vol. 3. Carnivores et Primates (Savouré-Soubelet, A. et al. eds.). 336–341 (Museum National d’Histoire Naturelle, 2024).
35. Kappeler PM Erkert HG On the move around the clock: Correlates and determinants of cathemeral activity in wild redfronted lemurs (Eulemur fulvus rufus) Behav. Ecol. Sociobiol. 2003 54 359 369 10.1007/s00265-003-0652-x
Kappeler, P. M. & Erkert, H. G. On the move around the clock: Correlates and determinants of cathemeral activity in wild redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 54, 359–369 (2003).
36. Curtis D Zaramody A Martin RD Cathemerality in the mongoose lemur, Eulemur mongoz Am. J. Primatol. 1999 47 279 298 10.1002/(SICI)1098-2345(1999)47:4<279::AID-AJP2>3.0.CO;2-U 10206207
Curtis, D., Zaramody, A. & Martin, R. D. Cathemerality in the mongoose lemur, Eulemur mongoz. Am. J. Primatol. 47, 279–298 (1999).10206207
37. Pereira M Pond C Organization of white adipose tissue in lemuridae Am. J. Primatol. 1995 35 1 13 10.1002/ajp.1350350102 31924060
Pereira, M. & Pond, C. Organization of white adipose tissue in lemuridae. Am. J. Primatol. 35, 1–13 (1995).31924060
38. Hamada Y Hayakawa S Suzuki J Watanabe K Ohkura S Seasonal variation in the body fat of Japanese macaques Macaca fuscata Mammal Study 2003 28 79 88 10.3106/mammalstudy.28.79
Hamada, Y., Hayakawa, S., Suzuki, J., Watanabe, K. & Ohkura, S. Seasonal variation in the body fat of Japanese macaques Macaca fuscata. Mammal Study 28, 79–88 (2003).
39. Bowman JE Lee PC Growth and threshold weaning weights among captive rhesus macaques Am. J. Phys. Anthropol. 1995 96 159 175 10.1002/ajpa.1330960205 7755106
Bowman, J. E. & Lee, P. C. Growth and threshold weaning weights among captive rhesus macaques. Am. J. Phys. Anthropol. 96, 159–175 (1995).7755106
40. Schoeller DA Energy expenditure by the doubly labeled water: Validation in humans and proposed calculations Am. J. Physiol. 1986 250 R823 R830 3085521
Schoeller, D. A. et al. Energy expenditure by the doubly labeled water: Validation in humans and proposed calculations. Am. J. Physiol. 250, R823–R830 (1986).3085521
41. Speakman, J. R. Doubly Labelled Water: Theory and Practice (Chapman, Hall, 1997).
42. Speakman JR A standard calculation methodology for human doubly labeled water studies Cell Rep. Med. 2021 16 100203
Speakman, J. R. et al. A standard calculation methodology for human doubly labeled water studies. Cell Rep. Med. 16, 100203. 10.1016/j.xcrm.2021.100203 (2021).
43. Altmann J Observational study of behaviour—Sampling methods Behavior 1974 49 227 267 10.1163/156853974X00534
Altmann, J. Observational study of behaviour—Sampling methods. Behavior 49, 227–267 (1974).
44. Simmen B Hladik A Ramasiarisoa PL Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar Int. J. Primatol. 2003 24 949 968 10.1023/A:1026366309980
Simmen, B., Hladik, A. & Ramasiarisoa, P. L. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar. Int. J. Primatol. 24, 949–968 (2003).
45. Pinkus, S., Smith, J. N. M. & Jolly, A. Feeding competition between introduced Eulemur fulvus and native Lemur catta during the birth season at Berenty reserve, Southern Madagascar. In Ringtailed Lemur Biology: Lemur catta in Madagascar (Jolly, A., Sussman, R. W., Koyama, N. & Rasamimanana, H. eds.). 119–140 (Springer, 2006).
46. Tarnaud L Ontogeny of feeding behavior of Eulemur fulvus in the dry forest of Mayotte Int. J. Primatol. 2004 25 803 823 10.1023/B:IJOP.0000029123.78167.63
Tarnaud, L. Ontogeny of feeding behavior of Eulemur fulvus in the dry forest of Mayotte. Int. J. Primatol. 25, 803–823 (2004).
47. James, G., Witten, D., Hastie, T. & Tibshirani, R. (eds.). An Introduction to Statistical Learning: with Applications in R (Springer, 2013).
48. Kherad-Pajouh S Renaud O A general permutation approach for analyzing repeated measures ANOVA and mixed-model designs Stat. Pap. 2015 56 947 967 10.1007/s00362-014-0617-3
Kherad-Pajouh, S. & Renaud, O. A general permutation approach for analyzing repeated measures ANOVA and mixed-model designs. Stat. Pap. 56, 947–967 (2015).
49. RStudio Team. RStudio: Integrated Development Environment for R. http://www.rstudio.com/. (RStudio, PBC, 2020).
50. R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (R Foundation for Statistical Computing, 2022).
51. Lê S Josse J Husson F FactoMineR: An R package for multivariate analysis J. Stat. Softw. 2008 25 1 18 10.18637/jss.v025.i01
Lê, S., Josse, J. & Husson, F. FactoMineR: An R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).
52. Fox, J. The R Commander: A basic statistics graphical user interface to R. J. Stat. Softw. 14, 1–42. https://www.jstatsoft.org/article/view/v014i09 (2005)
53. Fox, J., Marquez, M. M. & Bouchet-Valat, M. Rcmdr: R Commander. R package version 2.9-2. https://socialsciences.mcmaster.ca/jfox/Misc/Rcmdr/ (2024).
54. Fox, J. & Weisberg, S. An R Companion to Applied Regression. 3rd Ed. https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (Sage, 2019).
55. Fox J Weisberg S Visualizing fit and lack of fit in complex regression models with predictor effect plots and partial residuals J. Stat. Softw. 2018 87 1 27
Fox, J. & Weisberg, S. Visualizing fit and lack of fit in complex regression models with predictor effect plots and partial residuals. J. Stat. Softw. 87, 1–27. 10.18637/jss.v087.i09 (2018).
56. Bates D Mächler M Bolker B Walker S Fitting linear mixed-effects models using lme4 J. Stat. Softw. 2015 67 1 48
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. 10.18637/jss.v067.i01 (2015).
57. Kuznetsova A Brockhoff PB Christensen RHB lmerTest package: Tests in linear mixed effects models J. Stat. Softw. 2017 82 1 26
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26. 10.18637/jss.v082.i13 (2017).
58. Frossard J Renaud O Permutation tests for regression, ANOVA, and comparison of signals: The permuco package J. Stat. Softw. 2021 99 1 32
Frossard, J. & Renaud, O. Permutation tests for regression, ANOVA, and comparison of signals: The permuco package. J. Stat. Softw. 99, 1–32. 10.18637/jss.v099.i15 (2021).
59. Simmen B Darlu P Hladik CM Pasquet P Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans Physiol. Behav. 2015 138 193 199 10.1016/j.physbeh.2014.10.018 25447337
Simmen, B., Darlu, P., Hladik, C. M. & Pasquet, P. Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans. Physiol. Behav. 138, 193–199 (2015).25447337
60. Tattersall I Patterns of activity in the Mayotte lemur, Lemur fulvus mayottensis J. Mammal. 1979 60 314 323 10.2307/1379802
Tattersall, I. Patterns of activity in the Mayotte lemur, Lemur fulvus mayottensis. J. Mammal. 60, 314–323 (1979).
61. Sato H Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: Implications for seasonal thermoregulation Primates 2012 53 255 263 10.1007/s10329-012-0301-y 22388421
Sato, H. Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: Implications for seasonal thermoregulation. Primates 53, 255–263 (2012).22388421
62. Tanaka M Habitat use and social structure of a brown lemur hybrid population in the Berenty Reserve, Madagascar Am. J. Primatol. 2007 69 1189 1194 10.1002/ajp.20416 17294429
Tanaka, M. Habitat use and social structure of a brown lemur hybrid population in the Berenty Reserve, Madagascar. Am. J. Primatol. 69, 1189–1194 (2007).17294429
63. Sussman, R. W. Ecological distinctions in sympatric species of Lemur. In Prosimian Biology (Martin, R. D., Doyle, G. A. & Walker, A. C. eds.). 75–108 (Duckworth, 1974).
64. Tarnaud L Feeding behavior of lactating brown lemur females (Eulemur fulvus) in Mayotte: Influence of infant age and plant phenology Am. J. Primatol. 2006 68 966 977 10.1002/ajp.20288 16900506
Tarnaud, L. Feeding behavior of lactating brown lemur females (Eulemur fulvus) in Mayotte: Influence of infant age and plant phenology. Am. J. Primatol. 68, 966–977 (2006).16900506
65. Tattersall, I. Ecology and behavior of Lemur fulvus mayottensis, primate lémuriformes. Anthrop. Pap. Am. Mus. Nat. Hist. N. Y. 54, 425–482 (1977).
66. Rimbach R Pontzer H Increased physical activity is not related to markers of cardiometabolic health in two lemur species Am. J. Primatol. 2024 37839049
Rimbach, R. & Pontzer, H. Increased physical activity is not related to markers of cardiometabolic health in two lemur species. Am. J. Primatol.10.1002/ajp.23564 (2024).37839049
67. Nie Y Exceptionally low daily energy expenditure in the bamboo-eating giant panda Science 2015 349 171 174 10.1126/science.aab2413 26160943
Nie, Y. et al. Exceptionally low daily energy expenditure in the bamboo-eating giant panda. Science 349, 171–174 (2015).26160943
68. Speakman JR Król E Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms J. Anim. Ecol. 2010 79 726 746 10.1111/j.1365-2656.2010.01689.x 20443992
Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746 (2010).20443992
69. Daniels HL Oxygen consumption in Lemur fulvus: deviation from the ideal model J. Mammal. 1984 65 584 592 10.2307/1380841
Daniels, H. L. Oxygen consumption in Lemur fulvus: deviation from the ideal model. J. Mammal. 65, 584–592 (1984).
70. Briscoe NJ Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals Biol. Lett. 2014 10 20140235 24899683
Briscoe, N. J. et al. Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals. Biol. Lett. 10, 20140235. 10.1098/rsbl.2014.0235 (2014).24899683
71. Chen-Kraus C Raharinoro NA Lawler RR Richard A Terrestrial tree hugging in a primarily arboreal lemur (Propithecus verreauxi): A cool way to deal with heat? Int. J. Primatol. 2023 44 178 191
Chen-Kraus, C., Raharinoro, N. A., Lawler, R. R. & Richard, A. Terrestrial tree hugging in a primarily arboreal lemur (Propithecus verreauxi): A cool way to deal with heat?. Int. J. Primatol. 44, 178–191. 10.1007/s10764-022-00328-5 (2023).
72. Cliffe RN The metabolic response of the Bradypus sloth to temperature PeerJ 2018 30258712
Cliffe, R. N. et al. The metabolic response of the Bradypus sloth to temperature. PeerJ10.7717/peerj.5600 (2018).30258712
73. Hoegh-Guldberg, O. et al. Impacts of 1.5 ºC global warming on natural and human systems. Global Warming of 1.5 °C. In An IPCC Special Report on the Impacts of Global Warming of 1.5 °C Above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty (Masson-Delmotte, V. et al. eds.). 175–312 10.1017/9781009157940.005 (Cambridge University Press, 2018).
