Individual flexibility in energy saving: body size and condition constrain torpor use

Individual flexibility in energy saving: body sizeand condition constrain torpor usePauline Vuarin*,1, Melanie Dammhahn2 and Pierre-Yves Henry1

1UMR 7179 CNRS-MNHN, 1 avenue du Petit Chateau, 91800 Brunoy, France; and 2Behavioral Ecology &Sociobiology Unit, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 G€ottingen,Germany

Summary

1. Phenotypic flexibility is a major mechanism in compensating climate-driven changes in

resource availability. Heterotherms can use daily torpor to overcome resource shortages and

adverse environmental conditions. The expression of this adaptive energy-saving strategy varies

among individuals, but the factors constraining individual flexibility remain largely unknown.

2. As energy availability depends on individual stores and/or on the ability to acquire food,

the propensity and flexibility in torpor use are expected to be constrained by body condition

and/or size, respectively. The aim of this study was to test whether the dependency of torpor

depth on air temperature was constrained by body condition and/or body size in a small het-

erothermic primate, the grey mouse lemur (Microcebus murinus). During the onset of the dry

season, we monitored air temperature as well as skin temperatures of 14 free-ranging individu-

als (12 females, two males) of known body mass and size.

3. Unexpectedly, torpor depth depended as much on air temperature as on body condition

and size. Fatter, or larger, mouse lemurs underwent deeper torpor than smaller, or leaner,

ones. Individual reaction norms of torpor depth to air temperature also revealed that the pro-

pensity to undergo deep torpor and the flexibility in torpor depth were enhanced by large body

size and high body condition, whereas small, lean individuals remained normothermic.

4. Our study illustrates that alternative physiological strategies to overcome temperature con-

straints co-occur in a population, with body size and condition being key determinants of the

energy conservation strategy that an individual can launch.

Key-words: air temperature, body constitution, energy availability, heterothermy, individual

reaction norm, Microcebus murinus, phenotypic flexibility

Introduction

Energy-saving strategies are adaptive responses to recur-

rent energetic challenges. Daily torpor and hibernation

(heterothermy) enable endothermic species to reduce their

energy expenditure during episodes of energetic constraint

(Heldmaier, Ortmann & Elvert 2004; McKechnie & Mzi-

likazi 2011). These mechanisms rely on a controlled reduc-

tion in body temperature and metabolic rate during

periods of rest (Geiser 2004; Heldmaier, Ortmann & Elvert

2004). Their use improves the chances of survival during

prolonged periods of resource shortage or of harsh cli-

matic conditions (Turbill, Bieber & Ruf 2011). Although

prevalent in temperate regions to overcome winter (Ort-

mann & Heldmaier 2000; McKechnie & Mzilikazi 2011),

heterothermy is also frequent in the tropics where it

enables small endotherms to cope with the dry season

(Dausmann et al. 2004; McKechnie & Mzilikazi 2011;

Canale, Levesque & Lovegrove 2012).

Individuals with high levels of flexibility in physiological

and behavioural traits are more likely to successfully over-

come environmental constraints, like climate change, by

fine-tuning their energy expenditure, and its timing,

according to fluctuations in energy availability (Nussey

et al. 2005; Charmantier et al. 2008; Canale & Henry

2010). Facultative, daily torpor is actually highly flexible,

and this flexibility markedly differs between individuals

(Schmid & Kappeler 1998; Canale & Henry 2011; Canale

et al. 2011; Kobbe, Ganzhorn & Dausmann 2011). How-

ever, the factors constraining individual flexibility in the

use of this energy-saving mechanism remain unknown.

With decreasing air temperature, heterothermic mam-

mals are able to substantially decrease their body tempera-

ture, hence increasing torpor bout duration and depth (e.g.*Correspondence author. E-mail: [email protected]

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society

Functional Ecology 2013, 27, 793–799 doi: 10.1111/1365-2435.12069

Geiser & Kenagy 1988; Schmid 2000; Aujard & Vasseur

2001; Heldmaier, Ortmann & Elvert 2004). As the energy

benefits associated with torpor expression are positively

related to torpor depth and duration, low air temperature

can enhance energy savings in thermoconforming torpid

animals (Heldmaier, Ortmann & Elvert 2004). Heterother-

my expression is also expected to depend on energy avail-

ability, that is, on stored energy reserves or the capacity to

acquire food. Energy reserves, such as internal lipid stores,

constitute the main fuel to sustain metabolic activity dur-

ing torpor bouts and to offset the thermogenic costs asso-

ciated with the regular returns to normothermia (arousals;

Geiser 2004; Heldmaier, Ortmann & Elvert 2004). Indeed,

hibernating individuals consume a large fraction of their

energy reserves during these brief peaks of thermogenesis

associated with arousals (e.g. 19% in ground squirrels:

Wang 1979; 72% in marmots: Heldmaier, Ortmann &

Elvert 2004). Therefore, animals must have stored energy

(internally or externally) when resources are abundant to

be able to survive by using torpor when resources are

scarce (Schmid & Kappeler 1998; Kobbe, Ganzhorn &

Dausmann 2011). The acquisition of resources likely

depends on body size as a larger size is usually associated

with better access to resources, for instance through social

dominance (Price 1984). Hence, both a good body condi-

tion and a large body size are predicted to increase the

ability to use torpor. Up to date, at the individual level,

only two studies reported a positive correlation between

body mass (BM) and torpor use in chipmunks (Levesque

& Tattersall 2010) and hedgehogs (Hallam & Mzilikazi

2011), and three between body condition and torpor use in

bats (Kelm & Von Helversen 2007; Stawski & Geiser 2010)

and mouse lemurs (Kobbe, Ganzhorn & Dausmann 2011).

However, none of these studies disentangled the respective

roles of body condition and body size on the individual

ability to flexibly adjust torpor use to fluctuations in air

temperatures.

In this study, we investigated the expression of hetero-

thermy by free-ranging grey mouse lemurs (Microcebus

murinus), small (60–120 g) primates inhabiting various for-

est types in western and southern Madagascar. Because

Madagascar is characterized by a high climatic unpredict-

ability (Dewar & Richard 2007), the grey mouse lemur rep-

resents a good model to investigate the flexibility of

energy-saving strategies in response to environmental con-

straints. During the dry season, mouse lemurs experience

shortfalls of food and water (Dammhahn & Kappeler

2008a), and face high circadian air temperature fluctua-

tions (daily amplitudes of up to 28 °C; Schmid 2001). They

complement energy storage with energy conservation and

enter daily torpor when environmental conditions become

unfavourable (Ortmann et al. 1997; Aujard, Perret & Van-

nier 1998; Schmid 2001; G�enin & Perret 2003). In this

study, we aimed to quantify the relative dependence of

skin temperature (Tsk) to air temperature (Ta), body condi-

tion and body size, using an individual reaction norm

approach – a suitable statistical framework to quantify

and compare phenotypic plasticity between individuals

(Nussey, Wilson & Brommer 2007; Martin et al. 2011).

The principle is to obtain biologically meaningful statisti-

cal parameters that describe the range of phenotypes (here,

Tsk) that an individual expresses in response to an environ-

mental gradient (here, Ta).

Materials and methods

STUDY SITE AND AN IMALS

The study was conducted in the dry deciduous forest of Kirindy in

western Madagascar, at the onset of the dry season (April–May

2011). We captured 14 free-ranging adult grey mouse lemurs (12

females and two males; Fig. 1) using baited Sherman live traps

(see Dammhahn & Kappeler 2008b for details). Individuals were

briefly anesthetized (10 ll Ketanest 100), weighed and measured

(body length, head width, head length; Dammhahn & Kappeler

2008b). All individuals were equipped with collar-mounted temper-

ature-sensitive radiotransmitters (PIP3 button celled tag, Biotrack

Ltd., UK, with a mass of c. 3 g), which allows to monitor manu-

ally Tsk, a reliable indicator of core body temperature (Dausmann

2005). Transmitters were previously calibrated in a water bath

ranging from 10 to 40 °C against a reference iButton (DS1921G;

Alpha Mach Inc., Sainte-Julie, Canada). As mouse lemurs gener-

ally rest in tree holes (Schmid 1998; Lutermann, Verburgt & Ren-

digs 2010), we recorded Ta in eight tree holes using iButtons, every

15 min, throughout the study period. iButtons were placed in

small plastic bottles (diameter of 2�5 cm, length of 7 cm) to pre-

vent direct contact between the iButton and the trunk, and bottles

were hollowed at the top and the bottom to allow air flow.

PARAMETERS MEASURED

Parameter measures are presented as means � standard deviation

of the means. Tsk was measured twice per individual and per

morning, once at 6:53 � 18 min and then at 8:08 � 17 min, using

the method described in Schmid & Speakman (2000). Based on

evidences from previous studies (Ortmann et al. 1997; Schmid

2000; Schmid 2001), we chose the 6:00–9:00 a.m. time window so

that minimal Tsk measurements could be assumed to be indicative

of individual, daily maximal torpor depth. As Ta was the lowest

during our time window of measurement (at 6:13 � 2:57 on

Fig. 1. Female grey mouse lemur (Microcebus murinus) in Kirindy

forest, western Madagascar (photograph by Pauline Vuarin).

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 27, 793–799

794 P. Vuarin et al.

average), and as nocturnal heterotherms passively rewarm with

the morning rise in Ta (Schmid 2000; Schmid 2001; Turbill,

K€ortner & Geiser 2008), it is unlikely that torpid individuals

reached a lower Tsk later than this time window. For the analyses

of torpor depth, we used the lowest Tsk measurement per morning

per individual, which occurred at 7:49 � 37. In total, we obtained

17 � 10 Tsk measures per individual. Ta values at the time of Tsk

measurement were averaged across the four spatially closest

iButtons.

Body mass cannot be used as a direct index of interindividual

variation in internal energy stores because it also covaries with

body size. A high BM does not distinguish a small, fat individual

from a large, lean one. Thus, we computed an individual body

condition index (BCI) using the scaled mass index method (Peig &

Green 2009). This index was calculated as the mass of an individ-

ual standardized to the mean body size of all individuals in the

population retaining the population-specific allometric relation-

ship. The population-level statistical relationship between BM and

body size was calibrated on an independent data set, composed of

226 adult individuals (97 females and 120 males) caught during

previous field surveys in the study population (M. Dammhahn,

unpublished data). The morphometric measure taken to account

for body size was head width (HW; �0�1 mm), that is, the dis-

tance between the two bizygomatics, as it was the morphometric

parameter the most tightly correlated with BM (Peig & Green

2009). First, we extracted the slope of the regression of BM to

HW (b):

logðBMiÞ ¼ aþ b� logðHWiÞ þ ei eqn 1

Then, we extracted the Pearson coefficient of correlation of log-

transformed BM and HW (ϕ):

u ¼ corrðlogðBMÞ; logðHWÞÞ eqn 2

Finally, individual BCI values were obtained using the follow-

ing formula:

BCIi ¼ BMi � ðHW=HWiÞbu eqn 3

Body condition index values are independent of HW (Pearson’s

R = �0�10, P = 0�73).

STAT IST ICAL ANALYSES

Because we used temporally repeated measures on the same indi-

viduals, Tsk data were analysed using linear mixed effects models

(built with the ‘nlme’ function), to account for the different

sources of nonindependence among data points. Explanatory vari-

ables were the fixed effects of Ta, HW, BCI and their interactions.

All variables were standardized to achieve comparable ranges of

variation (for a given variable, values were divided by its standard

deviation after subtraction of its mean). Individual identity was

entered as random individual intercept, and a random individual

slope parameter was entered to account for interindividual varia-

tion in Tsk in response to Ta (Schielzeth & Forstmeier 2009). To

account for the remaining nonindependence between data points

(i.e. nonrandom residual error), we also parameterized two struc-

tures for residual variance. An autoregressive structure of order 1

(‘corAR1’ function, parameter q) was included to account for tem-

poral autocorrelation between residuals (Pinheiro & Bates 2000: p.

229), and we allowed variability in Tsk to exponentially increase

with BCI and HW and decrease with Ta, by adding a variance

function for each covariate (‘varExp’ function, respectively param-

eters d, c and x; Zuur et al. 2009: p. 80; as in Peig & Green 2009).

Hence, the starting model had the following form (notation fol-

lows Zuur et al. 2009), where i is the index for the individual, j is

the index for air temperature (Ta) on day k, and l is the index for

the measure:

Tskijkl ¼ aþ b1 � Taij þ b2 � BCIi þ b3 �HWi þ b4� Taij � BCIi þ b5 � Taij �HWi þ b6 � BCIi

�HWi þ bi1 þ bi2 � Taij þ eijkl

eqn 4

with random intercept bi1 � N(0,d211), random slope bi2� N(0,d222), corr (bi1, bi2) � N(0, d12),

corrðeijk0l; eijklÞ ¼ qjk0�kj if k0 6¼ k;

eijkl �Nð0; r2 � e2d�BCIi � e2c�HWi � e2x�TajÞ:

The final model, containing only significant effects, was

obtained by deletion of the nonsignificant interactions and addi-

tive effects from the fixed part of this starting model. The maxi-

mum likelihood-ratio tests of the significance of effects were

computed with the final model.

Individual linear reaction norms of Tsk to Ta were estimated

using a random slope–random intercept model. For this analysis,

we transformed Ta values so that intercept values of Tsk were esti-

mated for the highest air temperature experienced during the study

period, that is, 24�5 °C. The used transformation for the Ta values

was: T0a = 24�5�Ta. Doing so, individual intercept values can be

interpreted as the individual propensity to use deep torpor at non-

challenging air temperature, 25 °C being the temperature of ther-

moneutrality for the grey mouse lemur (i.e. the temperature at

which the resting metabolic rate is the lowest; Aujard, Perret &

Vannier 1998). Then, the higher the T0a, the stronger is the thermal

constraint (cold). The model had the following form, where i is the

index for the individual and j is the index for air temperature (T0a):

Tskijk ¼ aþ b1 � Ta0ij þ bi1 þ bi2 � Ta0ij þ eijk eqn 5

with random intercept bi1 � N(0,d211), random slope bi2 �N(0,d222), corr (bi1, bi2) � N(0, d12),

eijk �Nð0; r2Þ:

Individual intercept bi1 measures torpor depth at 24�5 °C, andindividual slope bi2 measures the linear response of Tsk to T0

a. d211 is

the between-individual variance of the intercept parameter, d222 is

the between-individual variance of the slope for the effect of T0a, d

212

is the covariance between individual intercepts and slopes, and r² isthe residual variance for the error term. Significant interindividual

variation in the linear response of Tsk to T0a (i.e. H0: d22 = 0) was

tested by a likelihood-ratio test between the restricted maximum

likelihood fit of this model with the fit of the same model but

excluding parameters d22 and d12. Individual intercepts bi1 (also

called elevation; Nussey et al. 2005) and individual slopes bi2 were

estimated with the model (Fig. 3, best linear unbiased predictions

obtained with the ‘ranef’ function). These parameters allowed to

estimate individual propensity to undergo deep torpor and individ-

ual flexibility in torpor depth, respectively. The effects of HW and

BCI on these individual slopes and intercepts were then tested using

linear models, where significances of effects were tested by ANOVAs.

Normality of model’s residuals was checked with normal quan-

tile–quantile plots. The significance level was set to P < 0�05. All

analyses were implemented with R, version 2.13.1 (R Develop-

ment Core Team 2008). Model parameter estimates are presented

as means � standard error of the means.

Results

Throughout the study period, mouse lemurs experienced a

mean Ta of 18�5 � 2�8 °C (averaged across all iButtons


Body constitution constrains heterothermy 795

and all mornings) and exhibited an average Tsk of

28�9 � 6�7 °C, at 7:49 � 37 min. Mean Ta was 12�2 °Cfor the coldest and 24�5 °C for the warmest mornings,

respectively. Mouse lemurs expressed torpor in 45�0% of

the sampled mornings (considering that animals were tor-

pid when Tsk < 30 °C; justified in Schmid 2001). Their

body condition and body size, that is, HW, were

79�6 � 12�2 g and 21�8 � 0�7 mm, respectively, and they

had an initial BM of 79�7 � 19�2 g.

At the population level, Tsk increased with Ta

(v21 = 12�93, P < 0�001, b = 1�61 � 0�32), but decreased

with BCI (v21 = 6�55, P = 0�01, b = �1�79 � 0�70) and

tended to decrease with HW (v21 = 2�86, P = 0�09,b = �2�50 � 0�89). The slopes indicate that the effects of

HW and BCI were as strong as the effect of Ta. The posi-

tive relationship between Tsk and both HW and BCI indi-

cates that larger mouse lemurs with better body condition

underwent deeper torpor than those with lower body size

and condition, at all Ta (Fig. 2). The responsiveness of Tsk

to Ta was greater in large individuals (Ta 9 HW interac-

tion, v21 = 5�55, P = 0�02, b = 0�68 � 0�33), but did not

depend on BCI (Ta 9 BCI interaction, v21 = 1�40,P = 0�24, b = 0�45 � 0�37). The residual variance of Tsk

increased with increasing BCI (d = 0�06) and HW

(c = 0�08) and decreased with increasing Ta (x = �0�25).The linear reaction norm of Tsk to T0

a significantly var-

ied between individuals (random slope for the linear effect

of T0a, v

22 = 13�66, P = 0�001; Fig. 3, but see also Fig. S1,

Supporting information). The individual propensity to

undergo deep torpor (random individual intercepts) and to

adjust torpor depth to T0a (random individual slopes for

the effect of T0a) was strongly positively correlated (correla-

tion: 0�99), indicating that individuals using deep torpor

were also the most flexible. Both torpor propensity and flexi-

bility increased with HW (b = �2�48 � 0�49, F1,12 = 25�29,P < 0�001, and b = �0�38 � 0�07, F1,12 = 25�32, P < 0�001,respectively) and with BCI (b = �1�86 � 0�49 F1,12 = 14�22,P = 0�003, and b = �0�28 � 0�07, F1,12 = 14�11, P = 0�003,respectively; Fig. 4).

Discussion

We show for the first time that torpor use is largely

determined by two independent dimensions of body consti-

tution, that is, body size and body condition, in a small

free-ranging heterotherm (Fig. 4). As torpid animals actu-

ally have a reduced energy expenditure (Geiser 2004;

Heldmaier, Ortmann & Elvert 2004), it suggests that tor-

por-based energy savings are dependent on individual body

constitution. For a given air temperature, larger individuals

or individuals with a higher body condition underwent dee-

per torpor than smaller ones, or those with lower body con-

dition. Low air temperature is known to increase torpor

expression (e.g. Geiser & Kenagy 1988; Aujard & Vasseur

2001; Heldmaier, Ortmann & Elvert 2004), but body size

and condition proved to be as good predictors of torpor

depth as air temperature. Individual propensity to undergo

(a)

(b)

Fig. 2. Individual daily variations in torpor depth according to (a)

body condition index and (b) body size (indexed on head width)

for 14 free-ranging adult grey mouse lemurs. Box plots show the

median (bold line), the 25% and 75% percentiles (box), and the

non-outlier range (whiskers). Individuals are sorted by body con-

dition or size, respectively.

Fig. 3. Individual linear reaction norms of minimal skin tempera-

ture (i.e. torpor depth) to air temperature estimated for 14 free-

ranging grey mouse lemurs.



deep torpor, and the responsiveness of torpor depth to air

temperature, that is, torpor flexibility, were also strongly

dependent on body size and body condition. Thus, as

expected, these two independent dimensions of body consti-

tution appear to constrain individual flexibility in torpor

use. This result discards the hypothesis which posits that

torpor is used as an emergency response to adverse condi-

tions by individuals with a poor body condition (Christian

& Geiser 2007). Studies on five other heterothermic mam-

mals already suggested that individuals with a high BM or

body condition had a greater use of torpor. Indeed, both

depth and duration of torpor bouts were positively related

to BM or body condition in two bat species (Glossophaga

soricina: Kelm & Von Helversen 2007; Nyctophilus bifax:

Stawski & Geiser 2010) and in the southern African hedge-

hog (Atelerix frontalis: Hallam & Mzilikazi 2011). Fre-

quency of torpor also increased with increasing body

condition in the food-hoarding Eastern chipmunk (Tamias

striatus: Levesque & Tattersall 2010) and in the reddish-

grey mouse lemur (Microcebus griseorufus: Kobbe, Ganz-

horn & Dausmann 2011), for which torpor duration also

increased. However, the conclusions were potentially

confounded by the effect of body size.

The amount of energy available to an individual would

constrain its ability to make torpor-based energy saving

(Schmid & Kappeler 1998). If an individual does not have

access to a minimal, necessary amount of energy, it should

not use torpor, otherwise incurring the risk of not having

enough energy to return to normothermia at the end of a

profound torpor bout (Terrien et al. 2009). As large body

size is often associated with social dominance, particularly

during contests for food or shelters (e.g. Price 1984), a lar-

ger size would enable an animal to more easily acquire the

energy needed. Hence, to overwinter, large individuals

could rely on both easy access to limited food as well as

high energy savings. Independent of body size, energy

stores release individuals from daily resource acquisition

to cover the residual energetic costs associated with torpor.

Thus, the larger the energy stores, the more an individual

can rely on torpor-based minimization of energy expendi-

ture to make it through the dry season. This explains the

relationship between body condition and torpor use

observed here. Torpor episodes between foraging bouts

could also be used to maximize the amount of energy allo-

cated to fat storage (e.g. Carpenter & Hixon 1988), leading

to a higher body condition the more the animals express

torpor (Schmid 2001). In this alternative scenario, a better

body condition would be the result, and not the facilitator,

of increased torpor use. Although both mechanisms may

operate, in our study, lean individuals, that is, those with

the highest need of fattening, did not use torpor. As these

individuals did not adjust their skin temperature to air

temperature, the good body condition is unlikely to be the

result of torpor-based energy saving. Hence, the opposite

is more likely: torpor-based energy saving may help fat

individuals to maintain a high body condition, whereas

lean individuals would not improve body condition by

using torpor. Thus, our data support the view that suffi-

cient body fattening at the onset of the dry season deter-

mines an individual’s ability to rely on torpor use to

survive the dry season (Schmid & Kappeler 1998; Kobbe,

Ganzhorn & Dausmann 2011).

Individuals that are too small or too lean to use torpor

may not be systematically exposed to higher mortality dur-

ing the dry season, however. Alternative physiological strat-

egies to survive the unfavourable dry season may co-occur

in the same population. Whereas large, fat individuals

would rely on energy conservation and saving, small sized,

lean individuals would remain active, with a reduced torpor

use throughout the dry season, regularly feeding to main-

tain a positive energetic balance. Their strategy would be

based on optimized foraging activity rather than on energy

conservation, as has been hypothesized also for smaller

congeneric mouse lemurs (Microcebus berthae: Dammhahn

& Kappeler 2012). Actually, a large fraction of mouse

lemurs remain active throughout the dry season, mainly

males (Schmid & Kappeler 1998; Dammhahn & Kappeler

2008a,b; Kraus, Eberle & Kappeler 2008). Males fatten less

than females prior to the dry season (Schmid & Kappeler

1998), and 81% of them remain active, whereas most of the

females (73%) are inactive for several weeks or months

(Schmid 1999). However, despite a significant reduced use

of torpor and a higher activity compared with females,

males do not seem to suffer from excess mortality during

the dry season (Kraus, Eberle & Kappeler 2008). Their

access to food may even be relatively high as the densities

(a)

(b)

Fig. 4. Dependence of individual (a) intercept and (b) slope of

reaction norms of skin temperature to air temperature on body

size (black dots) or body condition (open grey dots), for 14 free-

ranging adult grey mouse lemurs.



of active individuals are the lowest during the lean period.

Thus, the difference between sexes in torpor use may be

explained in some part by the differences in body condition,

as our results indicate. This hypothesis is supported by the

fact that female grey mouse lemurs have been shown to be

dominant over males for access to food resources (G�enin

2003), which enables them to achieve higher BM.

Our study illustrates that alternative phenotypic strate-

gies to overcome challenging environmental conditions

co-occur in a natural population, at the same time of the

year. Which strategy an individual will tend to use is

mainly determined by body size and body condition. There

is probably a physiological continuum, ranging from indi-

viduals that largely rely on torpor-based energy saving to

others that remain normothermic and rely on feeding

opportunities. The study of individual reaction norms of

physiological and behavioural parameters to environmen-

tal constraints is needed to predict to what extent organ-

isms will be able to overcome such constraints, especially

in the context of global changes (P€ortner & Farrell 2008;

Canale & Henry 2010; Chevin, Lande & Mace 2010;

Chown et al. 2010).

Acknowledgements

All handling procedures and experiments were carried out by authorized

experimenters (#A91-616 & #A91-439) and complied with current laws of

Madagascar. This study was partly funded by CNRS, MNHN, the German

Primate Center, and a CNRS-INEE PhD fellowship to P. Vuarin. We

thank P. M. Kappeler, M. Perret, R. Rasoloarison and L. Razafimanantsoa

for their support, the Kirindy team for assistance in the field, and M. Th�ery

and D. Gomez for comments on the manuscript.

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Handling Editor: Theunis Piersma

Supporting Information

Additional Supporting Information may be found in the online

version of this article:

Fig. S1. Individual plots of the relationships between skin temper-

ature and air temperature, and the corresponding individual and

population reaction norms.



Functional Ecology

Individual flexibility in energy saving: body size and condition constrain torpor use

Vuarin, P., Dammhahn, M. & Henry, P.Y.

Figure S1. Individual plots of the relationships between skin temperature and air

temperature, and the corresponding individual and population reaction norms.

Functional Ecology



Functional Ecology



Figure S1. Individual plots of the relationships between skin temperature (Tsk) and air temperature (Ta),

as well as individual (grey line) and population (black dotted line) reaction norms of Tsk to Ta, for 14

free-ranging adult grey mouse lemurs.

Biodiversity is actually threatened by global changes, thus understanding how organisms respond to these changes is of major interest in ecology. In this context, energy saving strategies employed by a variety of organisms are powerful and efficient measures to deal with environmental constraints. However, these strategies remain poorly understood. The grey mouse lemur (Microcebus murinus), a small nocturnal primate inhabiting the dry forests of western Madagascar, represents a good model to study these questions. To face the energetic constraints found in their natural habitat (decrease in food availability and in ambient temperature during the dry season), the grey mouse lemur can enter into torpor, a strategy close to hibernation, which allows a reduction of energy expenditure thanks to a reduction of body temperature, metabolism and activity. Based on a field survey of free ranging grey mouse lemurs, our study aimed to investigate which factors constrain the expression of torpor in this species. At the onset of the dry season, we monitored air temperature as well as skin temperature of 14 free-ranging individuals of known body mass and size. In accordance with previous studies, we found that ambient temperature affects torpor use, torpor depth increasing with decreasing ambient temperature. Nonetheless, behind this already documented effect of ambient temperature, we also demonstrated that both body size and body condition (i.e. an index of energy body reserves) constrain torpor use.

Fatter or larger mouse lemurs expressed deeper torpor than lean or smaller ones. Furthermore, larger and/or fatter mouse lemurs had a greater propensity to express torpor, and a greater flexibility in its expression, meaning that they were able to adjust torpor use to variations in ambient temperature. Hence, our study illustrates that in a single population, different strategies co-occur, with body size and condition being the key determinants of the energy conservation strategy that an individual will adopt. Such studies are needed to predict to what extent organisms will be able to overcome environmental constraints, especially in the context of global changes.

Better keep in shape: importance of being big and fat to use energy saving strategies in mouse lemurs Pauline Vuarin, Melanie Dammhahn and Pierre-Yves Henry

Female grey mouse lemur (Microcebus murinus) in Kirindy forest, western Madagascar (photograph by Pauline Vuarin).

Individual flexibility in energy saving: body size and condition constrain torpor use

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