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Energeticsandbehavior:manypathstounderstandingARTICLEinTRENDSINECOLOGY&EVOLUTIONMAY2015ImpactFactor:15.35DOI:10.1016/j.tree.2015.04.007

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VincentCareauDeakinUniversity43PUBLICATIONS818CITATIONS

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TheodoreGarlandUniversityofCalifornia,Riverside11PUBLICATIONS613CITATIONS

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Energetics and behavior: many

Vincent Careau1 and Theodore Garland Jr2

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CorreKeywpersoel. When both DEE and RMR are measured in free-g animals, it is highly informative to look at thetionship between the two per se, without any need toke energy management models. This is what was donehe cited vole [5] and chipmunk [6] studies. We agree

0.37 [9], the value for maintenance metabolism (afterconditioning on body mass) is only slightly higher at0.42 [10]. Even if metabolism were truly more repeatablethan and driving variability in behavior, the questionbecomes what drives individual differences in metabo-lism?, which leaves us no closer to understanding mecha-nism in the strict sense [11]. Because metabolic andpersonality traits are labile, the question becomes whatexplains consistent individual covariance in these complexphenotypes and whether they are part of coadaptations toheterogeneous and variable environmental conditions.

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5 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2015.04.007

sponding author: Careau, V. (vcareau@deakin.edu.au).ords: allocation; basal metabolic rate; energy expenditure; increased intake;nality.

Trends in Ecology & Evolution, July 2015, Vol. 30, No. 7 365tre for Integrative Ecology, Deakin University, Waurn Ponds, Vpartment of Biology, University of California, Riverside, CA 9252

recent Opinion, Mathot and Dingemanse [1] drawntion to a claimed major assumption of studies linkingal personality and energetics: that the selected mea-

of [metabolism] is a valid proxy for energetic con-ints. They argue that unless this assumption is tested,lts from many studies are uninterpretable. We would

to argue that the definition of energetic constraints propose would make it difficult if not impossible to test

assumption.

lems with the redefinition of energetic constraints allocation principle goes back to Fisher [2] and is basedhe idea that energetic (or time or space) constraints canrate trade-offs (i.e., a situation in which one trait ortion cannot increase unless another decreases [3]). Yet,adopted definition of energetic constraints is problem-. Energy requirements in and of themselves are nottraints. Otherwise, if constraints equate to energyirements, and energy requirements are more directlyted to the total energy expenditure, an organismaining high levels of daily energy expenditure (DEE)n it has unlimited access to food would be considerede constrained than an organism with lower DEEng periods of low food abundance. As a sensible wayiew constraints, one might, for example, compare thegy required for a bat to survive winter with the energylable as fat stores [4].

her common nor flawed practiceur reading of the literature, we would dispute that it ismon practice to test for a relationship between restingabolic rate (RMR) and DEE to distinguish betweenrnative models of energy management. The wordc* is mentioned in seven of ten studies in Mathot

Dingemanses Table 2, but in every case allocation discussed in relation to additional components of thegy budget such as workload, activity level, parental, growth, or immune function. Thus, we would argue itot the case that nonsignificant correlations betweenR and DEE are often assumed to support the allocation

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the slope between DEE and RMR should always beided, but it could be misleading to distinguish amonggy management models based on that informatione (Box 1).

versus basal metabolic rate (BMR)hot and Dingemanse [1] state that the trend to mea-

RMR has probably arisen in part because of theculty of obtaining post-absorptive measures...; for ex-le, in small mammals...there is a fine line betweeng post-absorptive and metabolizing energy stores. Westion this statement in terms of both animal energetics

the history of the field. By definition, a post-absorptiveal needs to metabolize energy stores, so there can bene line between the two. RMR was introduced because

or more criteria for measuring BMR are sometimesually exclusive. Some rodents and insectivorans, forple, become hyperactive or enter torpor when de-

ed of food [7]. It is also interesting to measure theR of growing juveniles or lactating females, so ecophy-gists felt the need to free themselves from the overlyrictive criteria for measuring BMR. When intentional-iolating one criterion due to logistic constraints (or forogical reasons), precautions are usually taken to stan-ize measurements across individuals. When animalsot all be fasted, for example, they should be housedvidually and provided with an equal amount of foodre testing.

sality or coadaptation?hot and Dingemanse [1] focus on how consistent indi-al differences in metabolism can drive behavior. Thisomewhat understandable, because many models re-ly developed in behavioral ecology attempt to explainexistence of animal personalities by linking behavior

a state variable inherently less flexible than behavior, as body size, condition, life-history stage, or metabo-

[8]. Yet, available data do not support the idea thatabolism is less flexible than behavior. Although theage repeatability of behavior has been estimated as

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Box 1. Assessing the energy management model: more than just DEE and RMR

Mathot and Dingemanse [1] proposed to distinguish among theallocation, independent, and performance models using the slope ofthe regression of DEE on RMR. We agree that a slope of 0 indicatesthat reallocation is occurring within the energy budget, but it does notdemonstrate which components are involved nor whether the trade-off occurs at the among- or within-individual level or both [12].Obviobudgeas an

individuals even if the slope of the relationship between DEE andBMR is >1. In Figure IA, the slope of the least-squares linearregresswould allocatinot, so

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Letters Trends in Ecology & Evolution July 2015, Vol. 30, No. 7

366usly, one needs to quantify more components of the energyt to be able to identify trade-offs, constraints, or even allocation

underlying process. Moreover, allocation can still occur within

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DEE

(W)uding remarkss linking animal personality and energetics havehed in the past 10 years, attesting to the

importance. Although we applaud Mathot andmanses [1] attempt to further elaborate conceptsrgy management, we emphasize that more correla-udies will offer limited insight on how personalityetabolism are coadapted. Instead, we need moremental studies, including both phenotypic manipu-s and selection experiments [11].

nceshot, K.J. and Dingemanse, N.J. (2015) Energetics andvior: unrequited needs and new directions. Trends Ecol. Evol.

199206er, R.A. (1930) The Genetical Theory of Natural Selection, Oxfordversity Pressland, T. (2014) Quick guide: trade-offs. Curr. Biol. 24, R60R61phries, M.M. et al. (2002) Climate-mediated energetic constraintshe distribution of hibernating mammals. Nature 418, 313316

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I. (A) The average daily energy expenditure (DEE) and basal metabolic rate (BMR) in ten

howing the regression lines fitted for the four repeated measures of each individual.ion is significantly >1 (estimate SE = 2.54 0.57), whicheliminate the allocation model. In Figure IB, however,

on is occurring within individuals: as BMR varies, DEE does other components of the budget must be changing in ansatory fashion. However, this allocation is masked inIA by greater variability in DEE and RMR among than withinals [12].

(B)kman, J.R. et al. (2003) Resting and daily energy expenditures of-living field voles are positively correlated but reflect extrinsic rather

intrinsic effects. Proc. Natl. Acad. Sci. U.S.A. 100, 1405714062au, V. et al. (2013) Context-dependent correlation between restingabolic rate and daily energy expenditure in wild chipmunks. J. Exp.. 216, 418426kman, J.R. et al. (1993) Measurement of basal metabolic rates:t lose sight of reality in the quest for comparability. Physiol. Zool.0451049

A. et al. (2015) Animal personality and statebehaviour feedbacks:view and guide for empiricists. Trends Ecol. Evol. 30, 5060, A.M. et al. (2009) The repeatability of behaviour: a meta-analysis.. Behav. 77, 771783

te, C.R. et al. (2013) The repeatability of metabolic rate declines time. J. Exp. Biol. 216, 17631765eau, V. and Garland, T., Jr (2012) Performance, personality, andgetics: correlation, causation, and mechanism. Physiol. Biochem.l. 85, 543571eau, V. et al. (2014) Adding fuel to the fire of life: energy budgetsss levels of variation in ectotherms and endotherms. In Integrativeanismal Biology (Martin, L.B. et al., eds), pp. 219233, Wileyntific

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BMR (W)

TRENDS in Ecology & Evolution

hypothetical individuals. (B) DEE and BMR in the same individuals, this