Daily Torpor and Energy Expenditure in Sminthopsis macroura: Interactions between Food
and Water Availability and Temperature
Author(s): Xiaowei Song and Fritz Geiser
Reviewed work(s):
Source: Physiological Zoology, Vol. 70, No. 3 (May - Jun., 1997), pp. 331-337
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/30164320 .
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331
in Sminthopsismacroura:
DailyTorporand EnergyExpenditure
InteractionsbetweenFoodand WaterAvailabilityand Temperature
Xiaowei Song
Fritz Geiser
Department of Zoology, University of New England,
Armidale, New South Wales 2351, Australia
Acceptedby G.K.S.10/25/96
ABSTRACT
Endothermyallowsmaintenanceof a constantinternalthermal
milieu for optimalphysiologicalfunctionsbut resultsin high
energyexpenditureand water loss. Since torpor can reduce
both expenditureof energyand loss of waterand thus reduces
food and water requirements,we determinedhow different
food and waterregimesaffecttorporoccurrenceand patterns
in the dasyuridmarsupialSminthopsismacrouraat ambient
of 180C(wellbelowthe thermoneutralzone) and
temperatures
280C(close to the thermoneutralzone). At 180C,torporwas
morefrequentandmorepronouncedthanat 280C.Withdrawal
of food reducedthe averagedailymetabolicrateby 20%;withdrawalof wateralonehad little effect.The averagedailymetabolic rateof individualsdisplayingtorporwas 20%lowerthan
thatof individualsremainingnormothermic.At 280C,the averagedailymetabolicrateunderfood restrictionwas 85%of that
with food availablead lib. However,this reductionof average
dailymetabolicrateat 280Cseemsdue not to the use of torpor
but mainlyto a reductionof the restingmetabolicrate. The
resultssuggestthat at low temperature,torporis usedto adjust
energy expenditureto availabilityof food, whereasat high
temperature,reductionsof restingmetabolicrateareemployed.
with higherbody temperatures(Tb'S)lose more waterto the
environmentowing to higherwatervapour pressure(Fisher
and Manery1967).Sinceduringtorpor Tband metabolicrate
are lowered, both pulmonaryand vapour pressure-related
evaporatorywaterloss, in additionto energyexpenditure,are
substantiallyreduced (Fisher and Manery 1967). Therefore,
torporcan be regardedas an avenuefor an animalto extend
its survivaltime on its availableenergy and water reserves
(Thomasand Cloutier1992).Althoughit has been well documentedthat many small mammalsexhibittorporwhen their
food supplyis restricted,there is little informationon torpor
in responseto waterdeprivation(MacMillen1972;Buffenstein
1985). Moreover,little is known about how Taand food and
water availabilityinteract in influencingtorpor and energy
conservationin smallmammals.Thisinformationis important
for understandingthe energeticstrategiesof small mammals
underharshenvironmentalconditions.
The stripe-faceddunnart,Sminthopsismacroura(Dasyuridae), is a mouse-sizednocturnalinsectivorousmarsupial.It
is widespreadin arid and semiaridareasin centralAustralia
characterizedby pronounceddaily and seasonaltemperature
fluctuationsandhighlyvariablerainfall.Consequently,the animal is frequentlyfacedwith periodsof food andwatershortage
(Morton1982).Littleis knownaboutthe biologyof the species
in the field,but in the laboratorydailytorporhasbeen reported
over a rangeof Ta's(Geiserand Baudinette1985).
In this study,we investigatedthe effectsof food and/orwater
withdrawalon torpor frequency,torpor pattern,and energy
expenditureof S. macrouraat a low Tawell below the thermoneutralzone and a high Tacloseto the thermoneutralzone.
We also determinedhow torporinfluencesaveragedailymetabolic rate and the changeof body mass of the animalsunder
differentfood and waterregimes.
Introduction
Material and Methods
Endothermicthermoregulationof small mammals requires
high metabolicrates. This is especiallytrue at low ambient
temperatures(Ta's),since high heat productionis needed to
compensatefor a largeamountof heatloss. The increasedheat
productionrequiresan increasedrespiratoryrate,whichresults
in increasedwater loss. In addition, normothermicanimals
PhysiologicalZoology70(3):331-337. 1997. c 1997 by The University of
Chicago. All rights reserved. 0031-935X/97/7003-9620$03.00
TwelveadultmaleSminthopsis
macroura(bodymass22.5 2.4
_
g) were obtainedfrom a breedingcolony at LaTrobeUniversity,Melbourne.Animalsweremaintainedindividuallyin cages
(30 X 22 X 14 cm) containingsawdust,shreddedpaper,and
nest boxesat the Universityof New Englandin Armidale.They
were fed daily with a mixtureof maceratedcat food pellets
and canneddog food and suppliedwith calciumand vitamins.
The watercontentof the food was approximately
68%.Drinking waterwas provided.The photoperiodthroughoutthe experiment was 12L: 12D (lights on 0600-1800). All experi-
332 X. Song and F. Geiser
ments were conductedbetweenMarch 10 and November4,
1993 (i.e., Australianwinterand spring).N indicatesthe number of animalsand n the total numberof measurements.
After acclimationto a Taof 220 + 1lC for 6 wk, animals
wereseparatedinto two groupsof six individualswith matched
body mass. The animalsin the first groupwere exposedto a
sequenceof Ta's,lastingfor about 6 wk each, of 180 1C,
_+
220 1iC, and 280 1iC. To accountfor a possibleseasonal
_
_
the
individuals
in
the
second
were
influence,
group
exposed
for the same period,but the Tasequencewas 280 + l1C, 220
+ l1C, and 180+ l1C.
At both 180and 280C,all animalsfrom both groupswere
twice subjectedto the same seriesof experimentaltreatments
lasting for 24 h each: food and drinkingwater availablead
lib., food availablead lib. and drinkingwaterwithheld,food
withheldand drinkingwateravailablead lib., food and drinking waterwithheld,and dryfood availablead lib. and drinking
waterwithheld(wherethe food had been driedat 500Cfor 24
h). Betweeneverytwo treatments,animalshad accessto food
and drinkingwaterad lib. for 1 or 2 d until more than 95%
of the originalbody weight was reached.Body mass change,
eye surfacetemperature,and/or Tbwere measuredat 0900
hours aftereverytreatment.
Averagedaily metabolicratesin responseto differentfood
and waterregimeswere determinedat Ta'sof 180and 280Cin
three individualsfrom each group (i.e., a total of six animals
at each Ta).Averagedailymetabolicratesweremonitoredcontinuouslyfor 7 d underdifferentfood and waterregimes.New
regimesof food and waterwereintroducedat 1200hourseach
day, and the animalswere weighed.
Eyesurfacetemperaturewas measuredto the nearest1.00C
by placing the sensor of an infrareddigital thermometer
(Omega,OS-600,Stamford)about2 cm abovethe eye. Rectal
measurementsof Tb(Omega,HH-21 thermocouplethermometer,to the nearest0.10C)weretakentogetherwith readingsof
the eye surfacetemperature,on severaloccasions,to determine
whetherthe surfacetemperaturereliablypredictsTb.Eyesurface temperaturewas linearlyrelatedto Tbmeasuredrectally
at Ta'sof 180C(r2 = 0.98, P < 0.001, N = 11, n = 21) and
280C(r2 = 0.95, P < 0.001, N = 11, n = 21; Fig. 1).
For the determinationof averagedailymetabolicrate,animals were placed into 2-L respiratorychambersfitted with a
smallplasticnestbox. The chamberswereplacedin a temperature-controlledcabinet(+ 0.50C).Fourchannels,threeanimal
channelsand one referencechannel,were scannedwith solenoid valves.Eachchannelwas readfor 3 min (i.e., outsideair
and rateof oxygenconsumption[902] of eachindividualwere
measuredevery12 min). The flow rate(about300 mL min-')
of dryairthroughthe respiratorychamberwasmonitoredwith
a mass flowmeter(Omega,FMA-5606).The oxygen content
of air leavingthe respiratorychamberand air in the reference
chamberwas consecutivelymeasuredwith a single-chamber
oxygen analyser (Ametek Applied ElectrochemistryS-3A/1,
40 -
= 0.95)
28'C:Tb= 2.85 + 0.92 Ts (Pr2
A
p
A
S35
30
U1)
a.
E
U1)
-
0
25
0,
)
0
20
18C:Tb=- 0.35 +1.05Ts (r2= 0.98)
15
SI .
15
.
.
.
1I.
20
.
.
.
r I.
25
.
.
.
I.
30
.
.
.
.
35
~. .
I
I
40
Surface temperature('C)
betweeneye surfacetemperature(Ts)
Figure1. The relationship
and the rectaltemperature
macroura
at Ta's
(Tb)of Sminthopsis
of 180C(circles,N = 11, n = 21) and 280C(triangles,N = 11,
n = 21). Tband T, arelinearlyrelatedat Ta'sof 18i and 280C(P
< 0.01).
Pittsburgh) fitted with a high-resolution output board
(80335SE).Analyseroutputfromthe flowmeterandthe oxygen
analyserwere interfacedto a personalcomputervia a 12-bit
analog/digitalcard.
Animalswere consideredtorpidwhen the eye surfacetemperaturewas less than 300Cat a Taof 180Cand less than 310C
at a Taof 280C,which is equivalentto Tb'SOfless than 310C
(see Fig. 1). When only metabolicrate measurementswere
available,animalswereconsideredtorpidwhentheirmetabolic
ratesfell below 75%of the restingmetabolicrate at the same
Ta.Torporfrequencywas determinedfor eachindividual,and
percentageof torporwas calculatedfromthe individualmean.
Restingmetabolicrate was determinedfrom the mean of
the three lowest consecutiveVo2 values (i.e., over 36 min) of
normothermicindividualsobtained in the afternoonbefore
1700hours.The metabolicrateduringtorporwas determined
from the mean of the three lowest consecutive ro02valuesin
a torporbout. Theaveragedailymetabolicratewasdetermined
as the averageof all mass-specificVo2'stakenat 12-minintervals over 24 h. A linearchangeof body massduring 1-d measurementwas assumedto calculatethe mass-specific902.
Body mass changeovernightwas determinedas the change
in body mass in milligramsper gram of initial mass. Food
intakewas determinedas the dry mass of food consumedin
milligramsper gram of body mass. Resultsare presentedas
mean + 1 standarddeviation.Torporfrequenciesunderdifferent experimentaltreatmentswere examinedby means of chisquare analysis.The impact of the various food and water
Daily Torporand EnergyExpenditure 333
a: Ta= 18'C
7
6
35
T
5
frequencydifferedbetween 180and 280Cunder all food and
water regimes (P < 0.05, X2-test;Fig. 3). Although torpor
frequencyappearedto be somewhatelevatedwhen food was
withheld,it was not significantlyaffectedby the differentfood
and waterregimesat either 180or 280C(P > 0.05, X2-test).
40
-
,-
,
"
30
25
4
20
3
15
10
o
E
Eye SurfaceTemperature
l
1
5
MR
--L0
The eye surfacetemperatureduringtorpor at Taof 180Cwas
influencedby the variousfood and waterregimes(P < 0.001,
o"
B
ANOVA;Fig. 4a). When food and waterwere available,the
average eye surface temperatureduring torpor was 26.70
7 b:Ta= 28C
40
3.10C(N = 9, n = 14). When both food and waterwere
Tb
6
+
....,..
.
350
the eye surface temperaturedecreasedto 22.90
withheld,
.,
30
-.
.
.
3.30C
= 11, n = 18). When only dry food was available
(N
+
25
4
and waterwas withheld,the eye surfacetemperaturewas 24.60
20
3
+ 2.60C(N = 11, n = 18). However,withdrawingdrinking
15
15
waterwhile food was availableresultedin an eye surfacetem10
2
peratureof 28.20 + 0.70C (N = 9, n = 14), which was not
significantlydifferentfrom that with food and wateravailable
o
o -'
ad lib.
16:00 19:00 22:00 01:00 04:00 07:00 10:00 13:00 16:00
At a Taof 280C,the eye surfacetemperatureof individuals
that showedspontaneoustorporwas 30.1i 0.60C(N = 6, n
Timeof day
_and the different
= 8) when food and waterwere available,
of metabolicrate(MR)andbodytempera- food and waterregimesdid not cause a changein eye surface
Figure2. Fluctuations
ture (Tb)Ofa Sminthopsis
macroura
at Ta'sof 180(a) and 280C temperatureduringtorpor (P > 0.05, ANOVA;
Fig. 4b).
Thedarkbarindicatesthe
(b).Foodandwaterwerenot available.
The
different
food
and
water
also
did
not signifiregimes
darkphase.
affect
the
surface
of
individuals
cantly
reeye
temperature
maining normothermicat both air temperatures(P > 0.05,
regimeson eyesurfacetemperatureandaveragedailymetabolic
rate were analysedby ANOVA. Pairwisecomparisonswere
10018"C
madewith Tukey'stest. Changeof body masswas analysedby
90
three-wayANOVA,and a posterioricomparisonsof means
80 _i-Q28"C
werecarriedon food andwaterregimes.Foodintakewasexamined by two-wayANOVA.Differencesin averagedaily metaS70
bolicratebetweenanimalsenteringtorporandthoseremaining
60
normothermicwereexaminedwith Student'st-test.Linearreo-50
gressionswere fittedby the least squaresmethod.
40
0 '7-
iD"
"
5
S
iiM
'
R
'
I
"
'
I
'
I
'-"
I
Results
30
20
10
TorporPatternsand Frequency
macrouradisplayedtorporat Ta'sof 180and 280C
Sminthopsis
(Fig. 2). Afterlights-out,animalswere activeand had an elevatedmetabolicrate.Torporbeganduringthe darkphaseand
was characterized
by a substantialdrop in both metabolicrate
and bodytemperature.Torporwasterminatedby spontaneous
arousalusuallybeforemidday(Fig. 2).
Torporfrequencywas affectedby Ta(Fig. 3). When food
and waterwere freelyavailable,the frequencyof spontaneous
torporwas 63.6%+ 14.1%(N = 12, n = 22) at a Taof 180C
and 33.3%+ 13.6%(N = 12, n = 24) at a Taof 280C.Torpor
10
"
+
o
-
+
Foo+
a
o
o
0
.t
0
i
+
Food and water regime
macroura
underdifferFigure3. Torporfrequencyof Sminthopsis
ent food and waterregimesat T,'sof 180Cand 280C.The error
barsrepresentthe standarddeviations.Torporwasmorefrequent
at 180Cthanat 280C(P < 0.05,X2-test).
334 X. Song and F. Geiser
40-
of torpor (P < 0.001, three-wayANOVA).When food and
waterwere available,body mass remainedstableor increased
slightly.While withdrawalof drinkingwater had little effect
on body mass change,the withdrawalof both food and water
and the withdrawalof waterwhen dry food was availableresulted in a substantialbody mass loss. Body mass loss was
intermediatewhen drinkingwaterwas availableand food was
withheld(Table 1).
Food intakewas influencedby both Taand the food and
waterregimes(P < 0.001,two-wayANOVA).Whenboth food
andwaterwerefreelyavailable,animalsconsumed119.2 + 15.0
mg g-' (N = 11, n = 20) at 180Cand 70.0 + 16.1 mg g-' at
280C (N = 11, n = 18). Food intake increased to 200.2 + 18.4
mg g-' at 180Cand 145.4 + 20.6 mg g-' at 280Cwhen water
waswithheld.However,no dryfood wasconsumedwhenwater
was withheld.
a: 18"C
p
35
S30
Eas
-) 25
20
:
0
:
S15
40-
p
a
a-
b:28"C
35
30
Average Daily Metabolic Rate
25
The averagedailymetabolicratewas affectedby differentfood
and waterregimesat both a Taof 180C(P < 0.005, ANOVA;
20
C/
Fig. 5a) and a Ta of 280C (P < 0.01, ANOVA; Fig. 5b). The
15
+
+
08
+
0"
+'
"E
0
'
80
Sa+
Food and water regimes
of Sminthopsis
macroura
under
Figure4. Eyesurfacetemperature
differentfood andwaterregimesat T,'sof 180C(a) and280C(b).
was measuredat 0900 hoursaftereach
Eyesurfacetemperature
24-h treatment.Solid symbolsrepresenttorpidindividualsand
individuals.Significantdifferences
open symbolsnormothermic
aregivenin the text.
averagedailymetabolicratewas significantlylowerwhen both
food andwaterwerewithheldor whenonlywaterwasavailable
than when food was availablewith or withoutdrinkingwater.
The averagedaily metabolicrate was also significantlyaffectedby Ta.At a Taof 180Cthe averagedailymetabolicrate
was higherthan that at 280Cfor both individualsdisplaying
torpor and remainingnormothermic(P < 0.01, t-test). At a
Taof 18iC,the averagedailymetabolicrateof individualsthat
entered daily torpor (3.15 + 0.44 mL g-' h-', N = 6, n = 27)
was about 80% of those that remainednormothermic(3.80
+ 0.69 mL g-' h-', N = 6, n = 15; P < 0.01, t-test). In
contrast,at a Ta of 280C, the averagedaily metabolic rate
did not differsignificantlybetweenindividualsdisplayingdaily
torpor (2.26 + 0.59 mL g-' h-', N = 6, n = 23) and those
remainingnormothermic(2.46 + 0.24 mL g-' h-', N = 6, n
= 19;P > 0.05, t-test).
ANOVA;Fig.4a, b). The averageeye surfacetemperaturewas
31.80 + 0.90C (N = 7, n = 26 ) at a Ta of 180C and 34.3i
+ 1.10C (N = 9, n = 58) at a Taof 280C, which reflects rectal
temperaturesof 32.4iC and 34.4iC, respectively(see Fig. 1).
Body Mass and Food Intake
The Ta, use of torpor, and food and water regimesall had
independent,but not interactive,effectson bodymass.Animals
at 180Clost more body mass than at 280C (P < 0.05, threeway ANOVA;Table 1). Bodymass reductionwas significantly
smaller for individualsthat entered torpor than those that
remainednormothermic(P < 0.001,three-wayANOVA;Table
1). Bodymasschangeovernightvariedprofoundlyamongvarious food and waterregimesat both temperatures,irrespective
Discussion
Effect of Environmental Temperature
on Torporand EnergyExpenditure
Our studyshowsthat both energyexpenditureand the use of
torpor in Sminthopsismacrouraare strongly affected by Ta. At
a Taof 180C(wellbelow the thermoneutralzone), the average
dailymetabolicrate of individualsthat remainednormothermic was much (about 55%) higherthan that of the animals
at 280C(closeto the thermoneutralzone) sincea largeramount
of energyis requiredfor thermoregulation.Consequently,at
the low TaS. macrouradisplayed torpor more frequently, espe-
ciallyunderfood restriction,most likelyowingto the depletion
Daily Torporand EnergyExpenditure 335
Table 1: Changesin body mass of Sminthopsismacrouraafter24 h under differentfood and waterregimes
Treatments
AnimalsDisplayingTorpor
AnimalsRemainingNormothermic
180C
180C
Food and wateravailable:
18.6 + 30.1
Changein body mass (mg g-') ...........
2.7
Body mass (g) ....................................... 22.0
Observations
14 +_
..........................................
Food available,waterwithheld:
19.1 + 23.2
Changein body mass (mg g-') ...........
Body mass (g) ....................................... 22.6 + 2.5
Observations
14
..........................................
Food withheld,wateravailable:
Changein body mass (mg g-') ........... -91.9 + 14.4
Body mass (g) ....................................... 23.2 + 3.0
Observations
17
..........................................
Food and waterwithheld:
Changein body mass (mg g-') ........... -117.9 + 35.6
Body mass (g) ....................................... 21.1 + 2.6
Observations
18
..........................................
food
water
withheld:
available,
Dry
Changein body mass (mg g-') ........... -135.0 + 22.9
Body mass (g) ....................................... 21.9 + 3.2
Observations
18
..........................................
280C
280C
28.3 + 43.6
21.1 + 1.6
8
5.9 + 29.0
22.4 + 1.7
8
7.4 + 32.1
20.0 + 1.9
14
16.3 + 30.7
22.5 + 2.5
8
-14.1 + 25.3
24.1
3.6
8 _
2.7 + 23.7
22.4 + 2.7
13
-58.2 + 20.2
23.5 + 2.9
10
-105.3 + 28.1
23.8 + 3.0
4
-78.7 + 23.3
23.6 + 4.9
11
-126.3 + 23.6
22.2 + 1.3
11
-156.7 + 14.1
22.8 + 1.9
3
-143.4 + 27.1
22.9 + 1.4
10
-122.5 + 14.2
22.4 + 2.4
10
-162.7 + 14.5
21.9 + 2.6
3
-143.4 + 33.2
22.1 + 2.8
11
Note. Values are presentedas mean + SD. Negativesigns indicatea decrease.The Ta, use of torpor, and treatmentaffectedthe change in body mass
independently(P < 0.05, three-wayANOVA).
of stored energy reservesbelow a threshold (Dawson 1989;
Hiebert1990).
As in some other small mammals (Hollowayand Geiser
1995),dailytorporat a low reduceddailyenergyexpenditure
Tareducedaveragedailymetabolic
in S. macroura.However,the
rate (decreasedby 20% in animalsat a Taof 180C)was still
significantlyhigherthanthatat 280C,demonstratingthat daily
torpordoes not completelycompensatefor the energeticcosts
of thermoregulation
in the cold.
Although torpor in S. macrouraat the high Ta was less
frequentthan at the low Ta,it did occur even when food and
water were freely available.At the high Ta, torpor did not
significantlyreduce daily energyexpenditure,apparentlybecausethe differencebetweenthe metabolicrateduringtorpor
and the restingmetabolicratewas too smalland torporbouts
were too short to make a significantimpact.However,in its
desertenvironment,even duringsummerwhen daytime Ta's
arehigh,animalsareexposedto low Ta'sat nightand therefore
are able to significantlyreducemetabolicrate duringtorpor.
The use of torpor at relativelyhigh Ta'salso may reflectthe
lackof insectsduringdry,hot summers.This stronglysuggests
that the use of torporin S. macrouraat the high Taformspart
of a daily routine and reflectsa long-termadaptationto its
environment.Some other species also use torpor routinely
withoutthe needfor an energydeficit,whileshort-termstresses
only enhancethe depthor frequencyof torpor(Hudson1973).
Effectof FoodAvailabilityon EnergyExpenditure
Energyconsumption in a daily heterothermis the sum of
metabolicrateduringactivityand rest and, if the animaldisplaystorpor,the total metabolicrateduringa torporcycle.In
S. macroura,
at Ta'sof 180and 280C,the averagedailymetabolic
rate (ADMR)of individualsthat remainednormothermicwas
closely relatedto the resting metabolic rate (RMR;ADMR
= 1.16 + 1.01 RMR,r2 = 0.88, P < 0.01, N = 6, n = 15 at
180C;ADMR = 1.44 + 0.55 RMR, r2 = 0.29, P < 0.05, N
= 6, n = 19 at 280C).In individualsthat displayedtorpor,the
averagedailymetabolicratenot only was relatedto the resting
metabolic rate (ADMR = 2.03 + 0.41 RMR, r2 = 0.17, P
< 0.05, N = 6, n = 27 at 180C;ADMR= 0.55 + 0.85 RMR,
2 = 0.69, P < 0.01, N = 6, n = 23 at 280C)but also was a
function of the metabolicrate during torpor (TMR;ADMR
= 2.70 + 0.34 TMR,r2 = 0.37, P < 0.01, N = 6, n = 27 at
180C;ADMR = 1.42 + 1.06 TMR, r2 = 0.36, P < 0.01, N
= 6, n = 23 at 280C).Moreover,the metabolicrate during
torporand the restingmetabolicratewerepositivelycorrelated
(TMR = -1.13 + 0.87 RMR,r2 = 0.20, P < 0.05, N = 6,
336 X. Song and F. Geiser
U#1
a:18-c
5
I VoO
#66
6
5
-a-
b,4
.
4.
o
cu
R
-.
3-
\
\
S31
2
0
2
<
0
/,
/,"\\
/
F
V#2
065
P
o
10
o
bolic rate (Songet al. 1995),and that in turn prolongstorpor
bouts (Geiseret al. 1990).
In contrast,at a Taof 280C,torpordid not resultin significant energysavings.However,food and waterregimesinfluenced the restingmetabolicrate (P < 0.01, ANOVA)in the
same way as they affectedaveragedaily metabolicrate. This
suggeststhat at high Ta's,energyconservationwas achieved
mainlyby a reductionof restingmetabolicratedue to a lower
Tbduringnormothermiaand perhapsalso due to the lack of
regulatorydiet-inducedthermogenesis.
Effect of Water on Torporand Energy Expenditure
b:28"C
Althoughtorporand energyexpenditurewereaffectedby food
availability,deprivingthe animalsof drinkingwaterhad little
5
effect on the above variablesof S. macrouraat either low or
high Ta's.This suggeststhat freelyavailabledrinkingwater is
S4
less importantthanfood availabilityfor inductionof torporin
O
this species,whichis adaptedto an aridenvironment.However,
when
waterwaswithheld,the animalcompensatedby consum\ I
2 *v-f
r
o
a
ing largeramountof moist food. In the field, S. macrourais
o'
o.
nocturnaland avoidsexposureto high Ta'sand extremedry1
nessandthuswaterloss by hidingunderlogs or rocks(Morton
1
1982). Since desert species including Sminthopsisare known
0
0
0
to have very effectivekidneys (Brookerand Withers 1994),
they have low waterturnoverrates (Kennedyand Macfarlane
+
+
+
1971)andareableto surviveon waterfromfood and metabolic
+
+
+
water (Hudson and Bartholomew1964; MacMillen 1972).
Figure5. Theaveragedailymetabolicrate(ADMR)of Sminthopsis Thus,short-termremovalof drinkingwateris probablynot a
underdifferentfood and waterregimesat Ta'sof 18'C physiologicalstressfor S. macroura.
macroura
(a) and 28'C (b). Theaveragedailymetabolicratewasmeasured This interpretationmay not appearto be supportedby our
continuouslyfor 7 d. Datafromdifferentindividualsareshown observationthat the availabilityof dry food resultedin deeper
by differentsymbols.
and morefrequenttorporwhenwaterwaswithheld.However,
it is likelythat this resultwas not due to lackof waterbut due
n = 27 at 180C; TMR = -0.02 + 0.40 RMR, r2 = 0.47, P to a reductionof food intakebecausethirstyanimalsareknown
< 0.01, N = 6, n = 23 at 280C).This showsthat an individual to dislikedryfood (Hudson1973),and S. macrouraconsumed
that has a low resting metabolic rate also tends to have a none of it. Moreover,it is known that low environmental
low metabolicrateduringtorporand that a low averagedaily humiditycan induce torpidityin small heterothermicendometabolicrate is due to a combined contributionof several therms becauseof a decline of food consumption (Hudson
variables,includinglow metabolicrate during torpor and a and Bartholomew1964).
We concludethatthermoregulation
and energyexpenditure
low restingmetabolicrate.Thesefindingssuggestthat S. macrouracan conserveenergyby decreasingenergeticcosts during of S. macrouraare stronglyaffectedby food availabilitybut
all physiologicalstates, as is known to be the case for other little influencedby restrictionof drinkingwater.Reductionof
species (Ruf and Heldmaier1992;Sheaforand Snyder1996). energyexpendituredue to food shortageat low and high Ta's
While the reduction of averagedaily metabolicrate was is achievedby differentphysiologicalresponses.In the cold,
causedby a reducedenergyexpenditureduringall physiologi- energyconservationis achievedby employingtorpor,whereas
cal states,the relativecontributiondifferedbetweenlow and in a warmenvironmenta reductionof restingmetabolicrate
high Ta's.At the low Tathe resting metabolicrate was not is used to save energy.
affectedby the differentfood and water regimes(P > 0.05,
ANOVA);the energy savings due to food withdrawalwere
Acknowledgments
causedmainlyby enhancedtorpor,as has also been shown for
a hibernatingrodent (Brown and Bartholomew1969). The This workwas supportedby a JohnCrawfordScholarshipand
reducedTb(about40Cin S. macroura)resultsin a lowermeta- a Universityof New Englandpostgraduateresearchgrant to
6
,
o g
Daily Torporand EnergyExpenditure 337
X.S. and a grantfrom the AustralianResearchCouncilto F.G.
torporin the rufoushummingbirdsSelaphorusrufus.Physiol. Zool. 63:1082-1097.
We thank G. Kortnerfor his help with the equipment,B.
Lovegrove,G. Kortner,and T. Ruf for providingsome of the HollowayJ. and F. Geiser.1995. Influenceof torporon daily
computersoftware,S. Cairnsfor his help with statistics,and
energyexpenditureof the dasyuridmarsupialSminthopsis
crassicaudata.
J. Hollowayfor criticalreadingof the manuscript.
Comp. Biochem.Physiol. 112A:59-66.
HudsonJ.W.1973.Torpidityin mammals.Pp. 97-165 in G.C.
Whitow,ed. ComparativePhysiologyof Thermoregulation.
LiteratureCited
AcademicPress,New York.
Hudson
BrookerB. and P.C.Withers.1994.Kidneystructureand renal
J.W.and G.A.Bartholomew.1964.Terrestrialanimals
indicesof dasyuridmarsupials.Aust. J. Zool. 42:163-176.
in dryheat:estivators.Pp. 259-277 in D.B. Dill, ed. AdaptaBrownJ.H.and G.A.Bartholomew.1969.Periodicityandenertion to the Environment.American Physiology Society,
geticsof torporin the kangaroomouse, Microdipodops
palWashingtonD.C.
lidus.Ecology50:705-709.
KennedyP.M.and W.V. Macfarlane.1971.OxygenconsumpBuffensteinR. 1985.The effectof starvation,food restriction,
tion andwaterturnoverof the fat-tailedmarsupialsDasycerand water deprivationon thermoregulationand average
cus cristicaudaand Sminthopsiscrassicaudata.
Comp. Biometabolic
rates
in
Gerbillus
Zool.
chem.
40A:723-732.
daily
pusillus.Physiol.
Physiol.
58:320-328.
MacMillenR.E. 1972.Watereconomyof nocturnaldesertroDawsonT.J.1989.Responsesto cold of monotremesand mardents. Symp.Zool. Soc. Lond. 31:147-174.
supials.Pp. 255-288 in L.C.H.Wang,ed. Advancesin Com- MortonS.R. 1982.Dasyuridmarsupialsof the Australianarid
zone: an ecologicalreview.Pp. 117-130 in M. Archer,ed.
parativeand EnvironmentalPhysiology.Springer,Berlin.
FisherK.C.and J.F.Manery.1967.Waterand electrolytemeCarnivorousMarsupials.R. Zool. Soc. NSW, Sydney.
tabolismin heterotherms.Pp. 235-279 in K.C.Fisher,A.R. Ruf T. and G. Heldmaier.1992.The impactof dailytorporon
Dawe, C.P. Lyman,F. SchOnbaum,and F.E. South, eds.
energyrequirementsin the Djungarianhamster,Phodopus
MammalianHibernationIII. Oliver& Boyd, London.
sungorusPhysiol.Zool. 65:994-1010.
GeiserF. and R.V.Baudinette.1985.The influenceof tempera- SheaforB.A. and G.K. Snyder. 1996. Energypartitioningin
ture and photophaseon daily torpor in Sminthopsismactorpor-sensitiveand torpor-resistantdeer mice (Peromyscus
roura(Dasyuridae:Marsupialia).J. Comp. Physiol. 156B:
maniculatus).Can. J. Zool. 74:1179-1186.
129-134.
Song X., G. K6rtner,and F. Geiser.1995. Reductionof metaGeiser F., S. Hiebert, and G.J. Kenagy. 1990. Torpor bout
bolic rate and thermoregulationduring daily torpor. J.
durationduringthe hibernationseason of two sciuridroComp. Physiol.165B:291-297.
dents: interrelationswith temperatureand metabolism. Thomas D.W. and D. Cloutier.1992. Evaporativewater loss
Physiol.Zool. 63:489-503.
by hibernatinglittle brown bats, Myotislucifugus.Physiol.
Zool. 65:443-456.
HiebertS.M. 1990.Energycosts and temporalorganizationof