Comparative Biochemistry and Physiology Part A 137(2004) 419–423

1095-6433/04/$ - see front matter� 2003 Elsevier Inc. All rights reserved.doi:10.1016/j.cbpb.2003.11.004

Differential energy costs of winter acclimatized common spiny miceAcomys cahirinus from two adjacent habitats

Michael Scantlebury *, Uri Shanas , Hagai Kupshtein , John R. Speakman , Abraham Haima, a a b,c a

Department of Biology, University of Haifa-Oranim, Tivon 36006, Israela

Aberdeen Centre for Energy Regulation and Obesity (ACERO), School of Biological Sciences, University of Aberdeen,b

Aberdeen AB24 2TZ, Scotland, UKACERO, Rowett Research Institute, Aberdeen, Scotland AB21 9SB, UKc

Received 28 July 2003; received in revised form 10 November 2003; accepted 11 November 2003

Abstract

The common spiny mouseAcomys cahirinus, of Ethiopian origin, has a widespread distribution across arid, semi-aridand Mediterranean parts of the Arabian sub-region. We compared the daily energy expenditure(DEE), water turnover(WTO) and sustained metabolic scope(SusMSsDEEyresting metabolic rate) of two adjacent populations during thewinter. Mice were captured from North- and South- facing slopes(NFS and SFS) of the same valley, comprising mesicand xeric habitats, respectively. Both DEE and SusMS winter values were greater in NFS than SFS mice and weresignificantly greater than values previously measured in the summer for these two populations in the same environments.However, WTO values were consistent with previously established values and were not significantly different fromallometric predictions for desert eutherians. We suggest that physiological plasticity in energy expenditure, which existsboth temporally and spatially, combined with stable WTO, perhaps reflecting a xeric ancestry, has enabledA. cahirinusto invade a wide range of habitats.� 2003 Elsevier Inc. All rights reserved.

Keywords: Acomys; Energy; Doubly labelled water; Resting metabolic rate; Body temperature; Thermoregulation; Water turnover;Desert; Ecophysiology; Evolution

1. Introduction

The link between energy expenditure and phys-iological adjustment to the environment has beenextensively studied and reviewed(McNab andMorrison, 1963; Degen, 1997; Lovegrove, 2000;Speakman, 2000). Small mammals such asrodents, that inhabit arid environments with

*Corresponding author.Present address: Mammal ResearchInstitute, Department of Zoology and Entomology, Universityof Pretoria, 0002 Pretoria, South Africa. Tel.:q27-12-420-2538; fax:q27-12-362-5242.

E-mail address:m.scantlebury@zoology.up.ac.za(M. Scantlebury).

restricted amounts of both water and food, char-acteristically have lower rates of energy expendi-ture and water turnover(WTO) than thoseoccupying more mesic areas(Nagy and Peterson,1988; Nagy et al., 1999). For species living inMediterranean ecosystems, summer may be aphysiologically demanding season when tempera-tures are maximal and the availability of moisturefrom the environment is minimal(Nevo, 1995).By comparison, for non-hibernating small mam-mals inhabiting cooler climates, winter is oftenconsidered the most energetically challenging peri-od because low ambient temperatures require anincreased energy intake(Speakman, 2000). Rodent

420 M. Scantlebury et al. / Comparative Biochemistry and Physiology Part A 137 (2004) 419–423

species inhabiting these cooler mesic areas typi-cally have higher resting metabolic rates(RMR)and daily energy expenditures(DEE) than speciesfrom hot and xeric habitats(Haim and Izhaki,1993).We have previously shown that there are differ-

ences in energy expenditure and WTO betweentwo populations of common spiny miceAcomyscahirinus inhabiting opposing slopes of the lowerNahal Oren(the ‘Evolution Canyon’; Nevo, 1995)during the summer(Scantlebury et al., 2003).Mice inhabiting the cooler, more mesic Northern-facing slope(NFS) had higher DEE but similarWTO compared with those inhabiting the warmermore xeric Southern-facing slope(SFS). Thesedifferences were interpreted as physiologicaladjustments to aridity and heat on the SFS. How-ever, during the winter, minimal ambient temper-atures in this area may fall as low as 88C,approximately 158C lower than during the summer(Shanas et al., 2002). At these temperatures hypo-thermia has been recorded inA. cahirinus (Haimand Rubal, 1994). Hence, the major challengefacing species likeA. cahirinus during winter inthe eastern Mediterranean ecosystem is probablyto cope with low ambient temperatures duringactivity. The extent of this challenge may bedifferent for mice inhabiting the NFS and the SFSas the different amounts of solar radiation receivedon the two slopes result in 3–48C lower minimaltemperatures on the NFS(Pavlıcek, personal com-´munication). Due to this climatic variability, wepredicted that energy expenditure and water turn-over in NFS mice during winter would be higherthan in SFS mice. We expected these differencesto be more pronounced during the winter, than thatpreviously measured during the summer, as theenergy costs of thermoregulation are expected toincrease. Therefore, the aim of the present researchwas to determine the DEE and WTO of NFS andSFS mice from the field during the winter, and tocompare the levels of these traits to those measuredin the same populations during the summer.

2. Materials and methods

Adult males and non-lactating adult femaleswere trapped on the NFS(three males and twofemales) and SFS(four males and four females)of the lower Nahal Oren during mid-winter(endof January). We used the doubly labelled water(DLW) technique(Lifson and McClintock, 1966;

Speakman, 1997) to determine DEE and WTO ofmice in the field. The methodology for applyingthis technique in this species has been describedpreviously(Scantlebury et al., 2003). Briefly, thisinvolves capture of the animal and collection of abackground blood sample, injection of DLW, col-lection of an initial enriched blood sample some60 min after dosing, release of the animal backinto the wild, recapture and a final blood samplebeing taken some 3–4 days post dose. The isotoperatios O: O and H: H from the blood samples18 16 2 1

are then analysed using gas source isotope ratiomass spectrometry(Optima, Micromass IRMS andIsochrom uG, Manchester, UK) prior to calculationof DEE (Speakman and Lemen, 1997). We tookrecaptured animals back to the laboratory wheretheir RMR was measured using the set-up previ-ously reported(Scantlebury et al., 2003). (M.Scantlebury et al., unpublished). Sustained meta-bolic scope(SusMSsDEEyRMR; Peterson et al.,1990), an index of how hard an animal is working,was determined for each population. WTO values(mlyday) were calculated using the measured deu-terium elimination rates(k ) and deuterium dilu-d

tion spaces(N ) (Lifson and McClintock, 1966;d

Nagy and Costa, 1980).We used analysis of covariance(ANCOVA) to

examine differences in body mass(g), DEE (kJygØday), N (ml), WTO (mly100 gØday) andd

SusMS (no units) between mice from all fourgroups(male and female mice from both the NFSand SFS populations). Slope of origin and sexwere included as categorical factors. Body masswas included as an additional covariate whenexamining differences in DEE(kJyday) and WTO(mlyday). We used initial values of body mass, asthere was no significant change in body mass ofmice between capture and recapture for eitherpopulation (initial masss45.40, final masss42.78, ts2.16,Ps0.07 for NFS mice and initialmasss51.11 g, final masss48.67 g, pairedts1.37,Ps0.24 for SFS mice).

3. Results

DEE (kJyday) and mass-specific DEE(kJygØday) were significantly higher in NFS mice thanSFS mice(F s6.78,Ps0.026 andF s6.58,1,10 1,10

Ps0.028 for DEE and mass-specific DEE, respec-tively; Table 1). The absolute difference in DEEbetween the two populations amounted to 20.7 kJyday, which was 27% of the mean expenditure

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Table 1Mean and standard deviations(S.D.) of body mass(g), daily energy expenditure(DEE; kJyday and kJyg day), H dilution space2

(N , ml), water turnover(WTO; mlyday and mly100 g day), and sustained metabolic scope(SusMS) of common spiny miceA.d

cahirinus from the North-facing slope(NFS) and the South-facing slope(SFS) of the Nahal Oren in Israel

NFS SFS

Males Females Mean Males Females Mean

n 3 2 4 4Mass(g) 50.01 39.85 45.4 54.50 47.73 51.11S.D. 7.81 7.71 4.24 1.83 9.24 11.40

DEE (kJyday) 113.00 74.40 97.5 83.70 70.00 76.80S.D. 24.20 17.80 28.6 24.90 18.22 21.50

DEE (kJygØday) 2.34 2.18 2.27 1.82 1.54 1.68S.D. 0.16 0.06 0.22 0.29 0.33 0.46

Nd (ml) 37.61 33.68 36.04 38.42 32.60 35.51S.D. 8.94 13.57 9.52 1.11 6.51 5.33

WTO (mlyday) 6.38 3.31 5.14 6.59 6.15 6.37S.D. 4.65 2.96 3.98 1.32 2.20 1.70WTO (mly100 g day) 9.20 13.34 11.69 12.13 13.62 12.87S.D. 7.02 9.62 8.53 2.55 6.87 4.86

SusMS 4.77 3.14 4.12 2.87 2.40 2.64S.D. 1.02 0.75 1.21 0.86 0.63 0.74

nssample sizes.

Table 2Allometrically predicted values of daily energy expenditure(DEE; kJyday), water turnover(WTO; mlyday) and sustainedmetabolic scope(SusMS; no units) from (1) Speakman(2000)(equation 3 for small mammals), (2) Nagy et al. (1999)(desert rodents), (3) Nagy and Peterson(1988) (desert euth-erians in the field), (4) Nagy and Peterson(1988) (non-deserteutherians in the field), (5) Degen and Kam(1995) (eutheri-ans) for common spiny miceA. cahirinus originating fromNorth-facing slopes(NFS) and South-facing slopes(SFS)

Predicted value Source NFS %D SFS %D

DEE (kJyday) 1 90.47 8 84.05 y9DEE (kJyday) 2 65.75 48* 62.07 24WTO (mlyday) 3 6.19 y17 5.53 15WTO (mlyday) 4 13.93 y63* 12.77 y50**SusMS 5 3.07 34 3.11 y15

* and ** indicate the results oft-tests at significance levelsof P-0.05 andP-0.01, respectively, of the measured valuefrom the predicted value. %D denotes the percent deviation ofthe measured value from the predicted value(a negative valueindicates a lower measured value than the predicted value).

across the two sites. Metabolic intensities(DEEybody mass) were also significantly differentbetween the two sites, with mice from the NFShaving metabolic intensities 40% greater than micefrom SFS. SusMS for the NFS mice at 4.12 wassignificantly greater than for mice on the SFS,which averaged 2.64(F s8.39, Ps0.016).1,10

However, there were no significant differences inbody mass,N , WTO or mass-specific WTOd

between mice from the two slopes. There were nosignificant differences in any of the measuredvariables between male and female mice. Nor werethere any significant interactions between sex andsite of origin for any of the measured variables.

4. Discussion

Previous measurements have shown thatA.cahirinus from both extreme desert regions(Degenet al., 1986; Kronfeld-Schor et al., 2001) andMediterranean areas(Weissenberg and Shkolnik,1994) have both low energy expenditure and lowWTO, which are characteristics of desert-livingfree-ranging eutherians(Degen, 1994). Theseattributes were also evident in mice collected fromboth slopes of the Nahal Oren during the summer(Scantlebury et al., 2003). In the present study,DEE and SusMS of mice were approximately

twice the same values measured during the sum-mer, and were subsequently not significantly dif-ferent from allometric predictions for othermesic-living free-ranging eutherians(Table 2).During winter, NFS mice actually had significantlyhigher DEE values than predicted from allometricequations for desert rodents, whereas SFS mice

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did not. Throughout the year DEE and SusMSvalues were consistently higher in NFS mice thanSFS mice. Differences between mice from the twoslopes may in part be accounted for by increasedcosts of thermoregulation(Kronfeld et al., 1998),which is required throughout the year on the coolerNFS. Energetic strategies adopted by the miceappear to vary seasonally. During the summer, asimilar behaviour to desert-dwelling rodents isobserved, with low RMR, DEE and SusMS values(Scantlebury et al., 2003). However, during thewinter, DEE and SusMS values increase, signify-ing physiological adjustments to the more mesicconditions. In Israel,A. cahirinus ranges fromextreme desert in the South(-50 mm annualrainfall), up to the Mediterranean live-oak maquisforests in the North(600–700 mm annual rainfall)(Nevo, 1985; Weissenberg and Shkolnik, 1994).This physiological plasticity may enableA. cahir-inus to invade such a wide range of ecosystems(Weissenberg and Shkolnik, 1994).In contrast to the variation in energy expendi-

ture, observed between populations and acrossseasons, WTO values remained low throughoutthe year and were not significantly different fromthe allometric prediction for desert eutherians(Table 2). During the winter, animals increasedtheir DEE, and the ratio of WTO to DEE wasabout half of the values measured in the summerin both populations(Scantlebury et al., 2003).Consequently, as there were no sources of freewater in the study area, this suggests that thewinter diet consisted of less water, relatively, thanthe summer diet and mice increased the energydensity of their food. Degen et al.(1986) com-pared the DEE, WTO and diet of three sympatricdesert-living species,A. cahirinus, golden spinymice (Acomys russatus) and bushy-tailed gerbils(Sekeetamys calurus). The latter two are able tosurvive in extremely arid areas whereA. cahirinusis absent. The results of their study showed thatwhereasA. cahirinus required a high dry matterintake, compared with the other two species, italso required a high water intake. They suggestedthat one reason thatA. cahirinus could be excludedfrom extremely arid areas is if stomach volumewere limiting. This is because they would beforced to obtain more water from energy-poorsources, such as snails(e.g. the land snail,Poma-tias olivieri; Broza and Nevo, 1994) and insects,and consequently they may not be able to consumeenough dry matter to meet energy requirements.

Constraints such as stomach volume might also beimportant in the present study. Given that DEEincreases to almost double the value in winter thanin summer,A. cahirinus may be unable to increasetheir metabolizable energy intake during the winterwithout switching to a more energy-dense diet.Weissenberg and Shkolnik(1994) compared

WTO between two populations ofA. cahirinus,one from Eilat(extreme desert) and one from theGalilee(a mesic Mediterranean area). They foundthat, under controlled laboratory conditions, WTOwas 36% lower in mice from Eilat than those ofthe Galilee. However, when WTO was measuredin free-ranging mice in their natural habitats, WTOrates were similar and close to that measured inGalilee animals in the laboratory. One possibilityis that the Eilat mice select a diet with an increasedwater content(e.g. one which contains many snailsand insects), to enable them to thermoregulate inhot and dry conditions. In both the current studyand that of Weissenberg and Shkolnik(1994), nosignificant differences in WTO were observedbetween free-living populations ofA. cahirinus.Hence, mice seem to be able to manipulate waterintake and water loss to maintain approximatelyconstant WTO under a variety of conditions. It isunclear what mechanisms they may use, but phys-iological means, such as osmoregulation(Shanaset al., 2003) may be important. Alternatively,behavioural mechanisms such as diet selection andactivity patterns(e.g. being active during coolerperiods of the day) may also be used. Furtherwork is needed on this topic.A low water requirement may have been main-

tained in A. cahirinus when it colonised mesicMediterranean habitats because it provided anadvantage in a heterogenic habitat in which thedry season is hot and long(up to 9 months), andin which large areas are sparsely vegetated. Insuch areas,A. cahirinus may have an advantageover common mesic-originating species, such asthe broad-toothed wood mouseApodemus mysta-cinus, which has higher water and energy requi-rements (Haim and Rubal, 1994). TheMediterranean ecosystem on Mount Carmel isvulnerable to fire(Naveh, 1990), which removesthe arboreal cover on both slopes. Following suchevents, the survival ofA. cahirinus could beenhanced, as it will have an advantage re-colonis-ing the recovering ecosystem, when water sourcesare scarce(Haim et al., 1997).

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Acknowledgments

This work was supported in part by grants fromthe Israel Science Foundation, Israel Academy ofScience and Humanities to AH(298y97-2) andfrom the Royal Society(SVyISRyNVB) and Brit-ish Ecological Society(SEPG-1878) to MS. Wewould like to thank the two anonymous refereesfor their helpful and constructive comments withwhich this manuscript was greatly improved.

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