Hibernation and Daily Torpor in Two Pygmy Possums (Cercartetus Spp., Marsupialia)
Author(s): Fritz Geiser
Reviewed work(s):
Source: Physiological Zoology, Vol. 60, No. 1 (Jan. - Feb., 1987), pp. 93-102
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/30158631 .
Accessed: 16/04/2012 20:11
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact [email protected].
The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to
Physiological Zoology.
http://www.jstor.org
HIBERNATION AND DAILY TORPOR IN TWO PYGMY POSSUMS
(CERCARTETUS SPP., MARSUPIALIA)'
FRITZ GEISER2
Schoolof BiologicalSciences,FlindersUniversity,Adelaide,SouthAustralia5042, Australia
(Accepted6/24/86)
The physiologyof torporwas investigatedin the pygmypossumsCercartetusconcinnus(18 g) and C. lepidus(12 g). Bodytemperatures(Tb)duringtorporremained
within 1 C of air temperature(Ta)and showeda minimum of about 5 C in both
species.Oxygenconsumption(Vo2)duringtorporwas reducedto about 0.05 liters
02/kg h, whichamountsto only 1%of the rateof normothermicanimals.Below Ta
of 5 C, the metabolismduringtorporincreasedwith a furtherdecreasein Ta,while
Tbwas regulatedat about 5 C. Ratesof arousalwere fasterthan predictedfor endothermicvertebratesof comparablesize. Durationof torporbouts rangedfrom less
thana dayto a week,withthe longestboutsoccurringat Ta< 10 C. The physiological
characteristics
of torporin these two marsupialspeciesare qualitativelyand quantitativelysimilarto those of placentalhibernators.
INTRODUCTION
nounced reduction of body temperature
and mass-specific oxygen consumption
during torpor (Bartholomew and Hudson
1962), a shorter duration of torpor (Hickman and Hickman 1960; Strahan 1983),
and a slower rewarming from torpor (Bartholomew and Hudson 1962; Fleming
1985a, 1985b) than in placental mammals.
Furthermore, there are no experimental
data on the thermoregulatory ability of
pygmy possums during torpor and thus no
Pygmy possums, small (<50-g) marsupials of the family Burramyidae, are found
in Australiaand New Guinea. Seven species
are recognized, with Distoechuruspennatus
occurring only in New Guinea. The taxonomic membership of the two feathertail
possums (Acrobates pygmaeus and Distoechurus pennatus) to burramyids is currently under review (Archer 1984), and the
remaining species belong to the genera
Cercartetusand Burramys.
Torpor has been observed in all Australian burramyids and is qualitatively similar
to hibernation in placental mammals (Bartholomew and Hudson 1962). It has been
suggested, however, that quantitative differences do exist between the two groups.
Such differences appear to be a less pro-
indicationthatthe reductionin Tbis a con-
'I wishto thankMeredith
Smithforherloanof
severalpygmypossumsandJohnCoventryforallowing
meto usehispitfalltrapsin the BigDesertandpartake
of hisdinkumbushchooks.BronwynMcAllanhelped
me to set up and checktraplines. RussellBaudinette
providedmany helpfulsuggestionsduringthe experimentalperiod,and SaraHiebert,Jim Kenagy,and
two anonymousrefereesconstructivelycriticizedthe
manuscript.The study was supportedby a Flinders
UniversityResearchScholarshipand the paperwas
compiledwhile the author held an Alexandervon
Humboldt-LynenResearchFellowshipat the Universityof Washington.
2 Present address: Department of Zoology, University of Washington, Seattle, Washington 98195.
trolled process. Some of these quantitative
differencesled to the conclusion that torpor
in burramyid marsupials may be less "refined" than in the "perfect" model of hibernating rodents (Lyman 1982).
Physiological data are available for three
of the six Australian burramyids (Bartholomew and Hudson 1962; Fleming 1985a,
1985b). Because large interspecific differences in the pattern of thermoregulation
have been observed in rodent families that
may contain "deep" hibernators and species that enter shallow, daily torpor (Lyman
1982), it was of interest to investigate
whether such specific differencesin the
thermalphysiologyalso occur in the burramyids.I also examinedin greaterdetail
the suggesteddifferencesin the physiology
between placental hibernators and the
marsupialfamilyBurramyidaeby studying
temporaland thermalaspectsof torporin
Cercartetus concinnus, the western pygmy
possum, and C. lepidus (syn. Eudromicia
lepida), the little pygmy possum.
Physiol. Zool. 60(1):93-102. 1987.
- 1987 by The University of Chicago. All
rightsreserved.0031-935X/87/6001-8636$02.00
93
94
F. GEISER
MATERIALAND METHODS
THE ANIMALS
Cercartetusconcinnusis foundin South
AustraliaandWesternAustraliaandoccurs
in mallee heath and dry sclerophyll forest.
It is nocturnal, uses tree hollows as daytime
shelters,eats insects, pollen, and nectar, and
storesfatin its prehensiletail(Smith1983).
Three males and two females were live
trapped at various locations on the southeastern coast of South Australia and the
Eyre Peninsula and kept in the laboratory
at Ta 22 C under natural photoperiod. In
autumn (March) they were transferredto a
constant Ta of 19 C with a photoperiod of
12L:12D, a condition similar to the natural
photoperiod at that time of the year, and
held for 3 wk before the experiments commenced. All experiments were performed
in autumn between March and May 1984
and 1985. The mean body mass during the
experimental period was 18.6 - 1.8 g (SD)
(range 16-22 g).
Cercartetus lepidus occurs in Tasmania
and two areas of southeastern Australia. It
is the smallestof all possums.It is mainly
nocturnal and has been found sheltering in
hollow logs and birds' nests (Green 1983).
It appearsto feed primarilyon invertebrates
and stores fat in its tail. One male and one
female were live trapped in the Big Desert,
Victoria, in September and transferred to
the laboratory, where they were kept at Ta
19 C and a photoperiod of 12L:12D (similar
to natural photoperiod at the time of capture) for 5 wk before measurements commenced. Experiments with these two individuals were conducted in spring and
early summer (October to beginning of December) 1984. Another male was caught at
Messent Conservation Park, South Australia, and was L.eptin the laboratory at Ta
22 C and natural photoperiod. In autumn
(March) it was transferredto Ta 19 C and
a photoperiod of 12L:12D and was kept
under these conditions for 3 wk before the
experiments began. The mean body mass
was 12.6 - 1.9 g (range 10-15 g).
The animals were fed with Heinz canned
baby food (fruits), a mixture of Heinz highprotein cereal and honey, and apples. Because pygmy possums held in captivity
become extremely fat, their weight was
controlled by feeding them only apples on
certain nights. Food was exchanged daily
in the afternoon.
EXPERIMENTALDETAILS
Diurnal fluctuations in oxygen consumption (V02) were determined at Ta 631 C for 30 periods of 21.1 - 2.1 h (range
15.5-29.25 h, C. concinnus) and for 20 periods of 22.0 - 2.3 h (range 17.25-25.75 h,
C. lepidus).These experiments began in the
late afternoon. Food and water were not
available during measurements of Vo2. To
determine whether burramyids regulate
their Tbduringperiods of torpor at a specific
"set point," torpid animals were cooled
(<0.05 C/min), and the Vo2 was continuously monitored. Additional measurements
during shorter periods were used to deter-
mine the V02 Of postabsorptive,normothermic, inactive animals at T, around and
above thermoneutrality. The Vo2 of one C.
lepidus was measured during prolonged
torpor over a 7-day period. Flow rates of
air in the open flow system were between
0.15 and 0.30 liters/min and were adjusted
and measured with calibrated rotameters.
Measurements of V02 were used to determine the metabolic rate of normothermic,
inactive animals measuredwhen a variation
of less than 5%over at least 15 min occurred
within an inactivity period of at least 30
min; the metabolic rate of torpid animals
was determined at times of constant Vo2
over at least 30 min. Furthermore, the duration of torpor and the time that was required to arouse from torpor to normothermia were determined from these measurements(the Vo2 peak during arousalwas
assumed to be the end point of the arousal
period). In some instances the displacement
of sawdust from the animal's back was used
to determine the duration of torpor. All
measurements were conducted in a quiet
controlled-temperature room (Ta + 0.5 C)
that was acoustically insulated from the recording equipment. A video camera was
used to observe the animals during the experiments.
A Servomex Model OA 184 paramagnetic oxygen analyzer was used for the Vo2
measurements together with a Rikadenki
potentiometric recorder. The Vo2 was determined from the difference between the
oxygen content in two parallel open-flow
circuits, one being a room air reference and
95
TORPORIN PYGMY POSSUMS
the other containingthe animal. All gas
volumes were correctedto dry standard
temperature and pressure (STPD).The Ta
was measuredcontinuouslyin the respiratorychamber(volume 3 liters)with calibratedthermocouples.The Tbwas measured with calibrated 0.5-mm diameter
thermocouplesinserted 20 mm into the
rectum. Esophagealtemperatureduring
torpor was also determinedoccasionally.
During induced arousal the rate of rewarming was determined by taping the
wire of the rectallyinserted
therrmocouple
thermocoupleprobeto the animal'stail.
A Student'st-testwas used for comparisons of pairedobservations.Straightlines
werefittedbylinearregressionanalysis.Differencesin slope and elevationweredetermined using the derivedt- and F-values.
Means of samples are expressed-SD. N
= number of individuals, n = number of
determinations.
RESULTS
Both Cercartetusconcinnusand C. lepidus showeda high tendencyto entertorpor.In allbutone experiment,C. concinnus
enteredtorporduringmeasurements
of Vo2
whenno food andwaterwereprovidedand
Tawaslessthan20 C. All C. lepidusentered
torporundertheseconditionswhen Tawas
less than 27 C. Apartfrom these induced
torporperiods,the animalsfrequentlyentered torporspontaneouslyin the laboratorywhenfood andwaterwerefreelyavailable(table 1). Spontaneoustorporat Ta19
C was observedin the morning;in the afternoonanimalsusuallywere normothermic. Cercartetuslepidusshoweda greater
tendency to enter torpor spontaneously
than the largerC. concinnus.
Most entriesinto torporin both species
occurredbetween 2400 and 0600 hours,
beforethe onset of light. The time of day
when torporcommencedwas not related
to Ta.The nocturnalpeaksof Vo2 during
activityof C. concinnusoccurredbetween
1845and 0130 hours,with a mean of 21.1
+ 2.1 h, anddid not appearto be dependent
on Ta. In C. lepidus,the nocturnalpeaks
of oxygenconsumptionassociatedwithactivity occurredbetween 1845 and 2200
hours(withtwo exceptions).
At temperatures
above 15C, bothspecies
usuallyenteredtorporon a dailybasisand
aroused spontaneouslyin the afternoon.
The longesttorporbouts of C. concinnus
were4 days at Ta 12 C and 8 days at Ta8
C. In C. lepidus,torporlastedfor a maximum of 2 daysat Ta19C (sawdustmethod)
and about 6 days at Ta 8.7 C (Vo2 measurement;fig. 1).
Periodsof apnealastingfor about5 min
at Ta10 C wereobservedin torpidC. concinnusand longerthan 30 min at Ta8.7 C
in C. lepidus. These periods were punctuatedby markedpolypnea.
Body temperaturesat restwerestableat
Ta 3-32 C with a mean Tb of 34.4 + 0.5 C
(C. concinnus; N = 5, n = 17) and 33.7
+ 0.8 C (C. lepidus; N = 3, n = 14) (fig. 2).
HigherTb'swereobservedat Ta's> 32 C.
Duringtorpor,Tbdecreasedwith decreasing Ta. The lowest AT values (Tb - Ta)Of
0.3-2.5 C occurredbetweenTa5 and 20 C,
and most A T wereless than 1.0 C in both
species.Below Ta4 C (C. concinnus)and
Ta5 C (C. lepidus),an increasein AT was
TABLE1
SPONTANEOUSTORPORIN Cercartetus concinnus AND C. lepidus
Ta
Species
C. concinnus
(N= 5)
...
C. lepidus
(N=3)
...
(-C)
n
Torpid
Normothermic
%Torpid
19
11-13
8
38
60
24
19
42
21
19
18
3
50
70
88
19
72
51
21
71
NOTE.-Food and waterwere availablead lib. Observationswere made between0800 and 1000 hours.
N = numberof individuals;n = numberof observations.
96
F. GEISER
10
Cercartetus Lepidus
9-
8-
Tb
3520C
7
6
r
r
5
o
3
.>
2
/Tb9.20C
Ok
12
21
12
12
21
21
12
21
12
21
12
21
12
12
21.
TIMEOFDAY(h)
lepidusmeasured
FIG.1.-The fluctuationin the rateof oxygenconsumption(0o2) of an individualCercartetus
over a 7-dayperiodat T, 8.7 + 0.7 C. The abscissarepresentsthe local time, and the darkbarsindicatethe
(Tb)areindicatedat the end of the measurement.
periodsof darkness.Bodytemperatures
observed.The lowestindividualTb'smeasuredduringtorporwere 4.7 C in C. concinnusand 5.9 C in C. lepidus.Esophageal
temperaturesduringtorporat Ta10C were
indistinguishable from values measured
rectally in C. concinnus. In torpid C. lepidus, the esophageal temperatures were at
most 1.4 C above the rectal temperatures
40
.0
Cercartetus concinnus
8
o
o
0
Cercartetus lepidus
00
0
0
35
o0
-o
0oo
0
0
0
o
o
30
25
a
*
30
20
20
.*0
15
15
*
15
10
0
10
0
5
0
5
10
15
20
Ta (C) )
25
30
35
0
5
10
15
20
25
30
35
Ta (OC)
concinnusand C.
inactive(0), andtorpid(e) Cercartetus
FIG.2.-Body temperatures
(Tb)Ofnormothermic,
(T,). The solidlinesrepresentTb= T,.
lepidusas a functionof airtemperature
TORPOR IN PYGMY POSSUMS
thesevaluesextrapolatedto the abscissaat
35.0 C (C. concinnus)and 36.5 C (C. lepidus). These interceptswere0.6 and 2.8 C,
respectively,above the mean resting Tb.
The lowercriticaltemperatureof the thermoneutralzone was between28 and 30 C
in both species.The mean metabolicrate
at Ta 28.8-31 C was 1.20 - 0.3 liters 02/
below Ta's of 10 C; at Ta 19 C both temperatures were within 0.2 C.
The Tb Of torpid pygmy possums was
regulatedabove a specific minimum. In the
typicalcase, shownin figure3, Tawas decreased from 10.5 C, the temperature at
which the C. concinnus had entered torpor.
As Ta decreased to 4.1 C, Vo2 remained
stable at a level of about 0.06 liters 02/kg
h. At Ta3.6 C, Vo2 increased to a new pla-
kg h (N = 4; C. concinnus) and 1.49 + 0.2
liters 02/kg h (N = 3, n = 8; C. lepidus),
and both values were slightly greater than
the predicted standard metabolic rate for a
marsupial of the respective body mass
(Dawson and Hulbert 1970).
For the daily Vo2 minima (fig. 4), a
steady decreasewith Tawas observed above
Ta5 C. The Vo2 of torpid C. concinnus was
0.046 - 0.02 liters 02/kg h (N = 5, n = 16;
Ta 5-13 C and 0.052 + 0.01 liters 02/kg h
(C. lepidus, N = 3, n = 17; Ta 6-11 C).
Below Ta5 C, a linear increase in Vo2 during torpor occurred in both species. Extrapolation of these lines intersected the
abscissa at 4.9 C (C. concinnus) and 5.6 C
(C. lepidus). The Vo2 during torpor at the
Tabelow which an increase in metabolism
was observed during torpor was 0.7% and
0.8%, respectively, of the values observed
teau of 0.24 liters02/kg h. An increasein
Tato 4.2 C resultedin a decreasein Vo2 to
0.16 liters 02/kg h, and Tbwas 4.7 C. Manipulations during measurement of Tb at
1445 hours induced arousal. The mean Ta
at whichan increasein Vo2 followedcooling was 4.4 - 0.4 C (N = 3) in torpid C.
concinnusand 5.3 + 0.6 C (N = 3, n = 4)
in C. lepidus.In all but one experiment,
wherecoolinginducedarousal,the pygmy
possums remainedtorpid but had an increasedmetabolicrate.
Reductionin Taresultedin a parallelincreasein Vo2 duringrest and torporat Ta
belowthe minimum Tb(fig.4). The Vo2 of
normothermic, inactive animals below
thermoneutralityincreasedlinearlyas Ta
decreasedin both species;the lines relating
0.4
97
Cercartetus concinnus
0.3
i"
N
0.2
0-
11
.1oC
10
9-
I.-.
6
539
10
11
12
13
14
15
TIME OF DAY
FIG.3.-The rate of oxygenconsumption(Vo2)Ofan individualtorpidCercartetusconcinnusexposedto
induced
changingairtemperature
(Ta).Thebodytemperature
(Tb)is indicated;handlingduringthismeasurement
arousal.The abscissarepresentsthe localtime.
98
F. GEISER
S CercartetusLepidus
8 Cercartetusconcinnus
\
7
o
7
o
cu
2
6
o
5
cm
o5
o
N
00
oc
0000
0
o"o
3
00
o-\o
o8
3
2
o
2%
000
.
0
5
10
15
20
25
0
30
35
Ta (-C)
1.
0
5
10
15
20
25
30
35
T, (-C)
FIG.4.-Rates of oxygenconsumption(Vo2)OfCercartetus
concinnusandC. lepidusas a functionof ambient
temperature(T,). The symbolsindicate:normothermicinactive(0), and the Vo2 minimaat constantT0(e) or
after T, had been lowered(U). The equationsfor the lines are:C. concinnus,normothermicinactive:y = 7.5
- 0.21x, r = -.98; in torpor:y = 0.83 - 0.17x, r = -.93. Cercartetus
lepidus,normothermicinactive:y = 7.7
- 0.21x, r = -.97; in torpor:y = 0.98 - 0.17x, r = -.64.
in normothermic,restinganimalsand only
3.8%and 3.5%when comparedwith the
basalmetabolicrates.
The relativeweight loss was 4.6 - 1.5
mg/g h (C. concinnus)and 4.9 + 1.6 mg/g
h (C. lepidus)for animalsthat had entered
torpor.Weightloss (WL, mg/g h) was inverselyrelatedto torporduration(TD, in
hours)in both species(WL= 6.4-0.21 TD,
r = -.60, C. concinnus;WL = 5.6-0.04 TD,
r = -.69, C. lepidus)(datanot shown).
The rateof increasein Tbduringarousal
was directlyrelatedto Tain both species
(table2). The fastestoverallarousalratewas
0.65 C/min in C. concinnus and 0.81
C/minin C. lepidus.The fastestarousalrate
determinedover a period of 10 min was
0.79 and 0.90 C/min, respectively.The
availabilityof food duringthe night precedingarousaldid not influencethe arousal
rates.Initialdifferences(0.2-1.4 C) between
esophagealand rectal temperaturein C.
lepidusobservedat low Tawere gradually
reducedduringarousal.
The time requiredto arousefromtorpor
to normothermiaincreasedexponentially
with decreasingTa(fig. 5). No significant
differencesbetween induced and spontaneous arousalwereobservedin eitherspecies.
DISCUSSION
The presentstudysuggeststhattorporin
marsupialsis underprecisecontrolandthat
their thermoregulationis not inferiorto
theirplacentalcounterparts.Thereappear
to be no generalphysiologicaldifferences
in the characteristicsof torporand hibernation in placentaland marsupialmammals.Bothgroupscontainspeciesthatshow
profoundtorporwhileothersentershallow,
dailytorpor.
Minimum Tb'Saround5 C as in pygmy
possums (table 3) have been reportedin
many placental"deep" hibernators(e.g.,
Strumwasser1960;Pengelley1964;Wang
and Hudson 1971). However, the minimum Tb'sin the burramyidsare much
lowerthanthose observedin marsupialsof
otherfamilies(Morrisonand McNab 1962;
Wallis 1976;Geiser 1985a, 1986).
The metabolicrateof torpidpygmypossums was reducedto less than 1%of the
restingvalues(table 3). Duringactivityof
concinnusand C. lepidusat Ta's
Cercartetus
below 10 C, oxygen consumptionwas increasedabout 200-fold in comparisonto
the torporvalues.The low metabolicrate
of pygmy possums was accompaniedby
A T'sthatwereusuallylessthan 1 C (Fleming 1985a, 1985b;present study). Hiber-
TORPORIN PYGMY POSSUMS
nating placentals show a similar metabolic
rate and AT during torpor (Kayser 1961;
Lyman 1982; French 1985).
Body temperatures during torpor ofburramyids are regulatedto remain at or above
a specific minimum similar to dasyurids
(Geiser et al. 1986). However, the thermoregulatoryincrease in the metabolic rate
occurred at a much lower Tain burramyids
(at Ta = 5 C) than in dasyurids (Ta > 11
C). The regulation of Tb at a specific minimum during torpor and the sensitivity to
changes in Ta of less than 0.5 C show that
torpor in pygmy possums is a controlled
process.
In burramyid marsupials, the longest
torpor bouts last from 2 to 13 days, with
the possible exception of C. caudatus, which
is foundin Queenslandrainforests
andNew
99
Guinea (for review,Geiser 1985b).In hibernatingrodentsrhythmicalarousalalso
occursabouteveryweek or two (Pengelley
andFisher1961;Pohl 1961;Kenagy1981;
French 1982). However, in contrast to
many placentalhibernators,some pygmy
possumsappearto forageand feed during
winter(Coventryand Dixon 1984).A less
distinctseasonalityin the torporpatternof
most pygmy possums is not surprising,
consideringthe relativelymild wintersin
many parts of Australia. However, the
mountainpygmy possum, Burramysparvus, which is exposed to strong seasonal
fluctuations,appearsnot to emergeduring
winter(Mansergh1984);nor do femaleC.
nanusin partsof Victoria(A. K. Lee 1985,
personal communication).
At high Ta, both C. concinnus and C.
TABLE2
AROUSAL RATESOF Cercartetusconcinnus AND C. lepidus
Tb
Ta(-C)
Initial
(-C)
Tb
End
(oC)
OverallArousal
(-C/min)
FastestArousal
(-C/min)
Food
C. concinnus (N = 5)
4.1
4.4
6.0
9.0
6.0
4.7
7.2
10.9
32.4
33.9
34.7
36.0
.11
.13
.18
.28
.28
ND
.34
.44
-
9.8
10.0
36.9
.30
10.6
12.0
17.0
19.0
19.0
12.7
13.7
18.1
20.0
21.3
.55
+
35.0
34.8
36.5
33.4
34.5
28.9
.39
.48
.48
.58
.64
+
26.9
.31
.33
.46
.56
.60
34.5
.59
ND
7.0
35.0
.56
35.0
.65
.71
-
-
5 - 23
19 - 22
19.4
.79
+
-
+
+
+
-
+
C.lepidus(N = 3)
6.0
6.9
8.7
35.1
.19
9.2
.47
35.2
.34
.62
18.3
18.5
34.8
18.5
18.9
.71
.77
36.0
.81
.88
+
19.0
24.0
19.5
25.2
3.4 - 20
19-* 23
36.0
35.5
7.7
19.3
.71
.81
.80
.90
35.9
36.0
.67
.73
.83
.80
-
-
+
+
-
+
NOTE.-Thefastestarousalratesweredeterminedovertimeperiodsof at least10min at Tb'saboveT,. Arrows
indicatethattheanimalsweretransferred
fromthe T, theyhadenteredtorporto a differentTaat whichrewarming
wasmeasured.ND: not determined.Foodduringthe nightpriorto the measurementwaseitheravailable(+) or
not available (-).
100
F. GEISER
500
Cercartetus concinnus
Cercartetus lepidus
200
200
100
o
S100
50
.E
E
sos
50
L
C~
'
20
o
20
10
10
5
0
5
10
15
20
25
30
0
10
5
15
20
25
30
Ta (OC)
Ta(oC)
concinnusand C. lepidusas a functionof
FIG.5.-Semilogarithmicplot of the arousaltimes of Cercartetus
airtemperature(T,). The symbolsindicateinduced(0) and spontaneous(0) arousal.No significantdifferences
betweenthe two couldbe detected.The equationsare:C. concinnus,induced:logy = 2.65 - 0.060x, r = -.97,
spontaneous:
logy = 2.64 - 0.053x,r = -.98; C. lepidus,induced:logy = 2.35 - 0.054x,r = -.99, spontaneous:
log y = 2.48 - 0.062x, r = -.998.
lepidusenteredtorporon a dailybasis;and
it appearsthat the torporbouts increased
with decreasingTa, as in groundsquirrels
(French1982).Thissuggeststhatprolonged
torporof pygmypossumsin the wildoccurs
during cold weather.In dasyuridmarsupials, prolongedtorpor has not been observedeven at low Ta(Wallis1976;Geiser
and Baudinette1985).
Arousal in C. concinnus and C. lepidus
was rapid, with the fastest arousal rates
about20%abovethe predictedarousalrates
formammalsandbirds(Heinrichand Bartholomew1971).Thisdoes not supportthe
view that marsupialspossessa lowerthermogeniccapacitythanplacentals(Fleming
1985a).The absenceof a lag of the rectal
behindthatof the anteriorpart
temperature
of the body duringarousalis most likely a
reflectionof the smallbody size of pygmy
possums.
The tendency to enter torpor spontaneously was high in both burramyidsinvestigated.Torporcouldbe inducedin au-
TABLE3
MARSUPIALS
DATA
OFAUSTRALIAN
BURRAMYID
SUMMARY
OFPHYSIOLOGICAL
Vo2 INTORPOR
SPECIES
Cercartetus
nanus
C. concinnus
C. lepidus
C. caudatus..........
Burramysparvus
Acrobatespygmaeus
TORPOR
BMR
BODY TbMIN Min Mean DURATION
TbREST(liter02/
MASS0
(OC)
(days)
kg h) SOURCES
(g) (oC) (liter02/kg h)
24 (35-90)
13 (18.6)
>8 (12.6)
30
42(44.3)
12 (14)
6
4.7
5.9
.05
.023
.032
.19
.046
.052
6
7
.022
.07"
.063
13
11
6
<1
7
2
34.9b
34.4
33.7
.86
1.20
1.49
36.1
34.9
.83
1.08
1, 2
3, *
*
4
5
6
Bartholomewand Hudson 1962;2, Dimpeland Calaby1972;3, Wakefield1970;4, Atherton
SOURCES.-1,
and Haffenden1982;5, Fleming1985b;6, Fleming1985a;*, presentstudy.
"Body massesweretakenfromStrahan(1983);C. lepidusfromCoventryand Dixon (1984).Bodymassesin
showthevaluesfortheanimalsusedin the Vo2and Tbmeasurements.
Tbmin andVo2min represent
parentheses
the minimarecordedforeachspecies.The torpordurationis the maximumrecordedforeachspecies.The other
valuesrepresentmeans.
b"Active"animals.
C Calculated
frompercentof Vo2at rest.
TORPORIN PYGMY POSSUMS
tumn, spring,and summerby exposinganimals to low Tain a similarmanneras in
the rodentSicista betulina(Johansenand
Krog 1959).Prolongedand deep torporin
pygmypossumscouldbe inducedwithin 1
day of cold exposurewhen food was withdrawn,andtherewasno evidencethatcold
acclimationwas necessaryfor the process.
However,it is likely that cold acclimatizationwouldlowerthe minimum Tbas in
dasyuridmarsupials(Geiser et al. 1986).
The abilityto entertorporat any time of
the year suggeststhat Cercartetusspp. do
not possessa strongendogenousseasonal
cycleof torporandactivity.Torporin these
marsupialsappearsto be an opportunistic
conditionsrather
responseto unpredictable
101
than to seasonal temperaturestress and
food shortages.
The physiologicalvariablesassociated
with torpor in burramyidsare strikingly
similarbetweenthe variousspecies(table
3). Thisis in contrastto cricetidand sciurid
rodents,which show a largerangeof thermoregulatorymodes and contain species
that are strict homeotherms,species that
entershallow,dailytorpor,and "deep"hibernators(Lyman 1982). Among those
placentalspeciesthat enterprolongedtorpor, therearegreatdifferencesin the minimum Tb,metabolicrate,durationof torpor,andrateofrewarming;andthe pattern
of torporin burramyidmarsupialsis within
this rangeof variations.
LITERATURE
CITED
S1986. Thermoregulation
and torporin the
kultarr,Antechinomys
laniger(Marsupialia:
Dasyeds. Vertebratezoogeographyand evolution in
uridae).J. Comp.Physiol.B156:751-757.
1985.The influAustralasia.
GEISER,
F., and R. V. BAUDINETTE.
HesperianPress,WesternAustralia.
1982. Obserence of temperature
and photophaseon torporin
R., and A. T. HAFFENDEN.
ATHERTON,
vationson thereproduction
andgrowthof thelongSminthopsismacroura(Dasyuridae:
Marsupialia).
tailedpygmypossum,Cercartetus
caudatus(MarJ. Comp.Physiol.B156:129-134.
in captivity.Aust.Mammal.
supilia:Burramyidae),
and E. J. MCMURCHIE.
GEISER,
F., R. V. BAUDINETTE,
5:253-259.
1986.Seasonalchangesin the criticalarousaltemG. A., and J. W. HUDSON.1962. HiBARTHOLOMEW,
peratureof the marsupialSminthopsiscrassicaudata correlatewith the thermaltransitionin mibernation, estivation, temperatureregulation,
tochondrialrespiration.Experientia,
evaporativewaterloss, and heartrate of pigmy
42:543-547.
possumsCercaertusnanus.Physiol.Zool. 35:94R. H. 1983.Littlepygmy-possum,
Cercartetus
GREEN,
107.
lepidus.Pages164-165 in R. STRAHAN,ed. ComA. J.,andJ. M. DIXON.1984.Smallnative
COVENTRY,
pletebookof Australianmammals.Angus& Robmammalsfrom the ChinamanWell area,northertson,Sydney.
westernVictoria.Aust.Mammal.7:111-115.
1971. An
HEINRICH,
B., and G. A. BARTHOLOMEW.
T. J., and A. J. HULBERT.
1970.Standard
analysisof pre-flightwarm-upin the sphinxmoth,
DAWSON,
andsurfaceareaof
Manducasexta.J. Exp.Biol. 55:223-239.
metabolism,bodytemperature
Australianmarsupials.Am. J. Physiol.218:1233V. V., and J. L. HICKMAN.1960. Notes on
HICKMAN,
1238.
the habitsof the Tasmaniandormousephalangers
1972.FurtherobserCercaertusnanus (Desmarest)and Eudromicia
DIMPEL,
H., andJ. H. CALABY.
vationson themountainpygmypossum,Burramys
lepida(Thomas).Proc.Zool.Soc. Lond.135:365375.
parvus.VictorianNat. 89:101-106.
M. R. 1985a.Thethermalphysiologyof the
FLEMING,
JOHANSEN,K., and J. KROG. 1959. Diurnal body
feathertail
glider,Acrobates
pygmaeus(Marsupialia:
temperaturevariationsand hibernationin the
Aust.J. Zool. 33:667-681.
Burramyidae).
birchmouse,Sicistabetulina.Am. J. Physiol.196:
1200-1204.
1985b.Thethermalphysiologyof the mountainpygmy-possum
Burramys
parvus(Marsupialia: KAYSER,C. 1961. The physiologyof naturalhiberAust.Mammal.8:79-90.
nation.Pergamon,Oxford.
Burramyidae).
A. R. 1982. Effectsof temperatureon the
FRENCH,
KENAGY,G. J. 1981.Effectsof the day length,temdurationof arousalepisodesduringhibernation.
J.
perature,and endogenous control on annual
Appl.Physiol.52:216-220.
and hibernationin chiprhythmsof reproduction
. 1985. Allometriesof the durationof torpid
munks(Eutamiasspp.).J. Comp.Physiol.A141:
andeuthermicintervalsduringmammalianhiber369-378.
nation:a testof the theoryof metaboliccontrolof
LYMAN,C. P. 1982. Who is who among the hiberthe timing of changesin body temperature.J.
nators. Pages 12-36 in C. P. LYMAN,J. S. WILLIS,
A. MALAN,and L. C. H. WANG.Hibernation and
Comp.Physiol.B156:13-19.
F. 1985a.Physiologicaland biochemicalasGEISER,
torpor in mammals and birds. Academic Press,
New York.
Ph.D.diss.
pectsof torporin Australian
marsupials.
FlindersUniversity,Adelaide.
MANSERGH,
I. M. 1984. Ecological studies and conservation of Burramys parvus. Pages 545-552 in
-. 1985b.Hibernationin pygmypossums(MarA. P. SMITHand I. D. HUME,eds. Possums and
supialia:Burramyidae).
Comp.Biochem.Physiol.
81A:459-463.
gliders. Australian Mammal Society, Sydney.
M. 1984.TheAustralian
radiation.
ARCHER,
marsupial
Pages 633-808 in M. ARCHERand G. CLAYTON,
102
F. GEISER
P. R., andB. K. MCNAB.
1962.DailytorMORRISON,
por in a Brazilianmurineopossum(Marmosa).
Comp.Biochem.Physiol.6:57-68.
E. T. 1964. Responsesof a new hibernator
PENGELLEY,
(Citellusvariegatus)to controlledenvironments.
Nature203:892.
E. T., and K. C. FISHER.1961. RhythPENGELLEY,
STRAHAN,R. 1983. Pygmypossumsand feathertail
ed.Completebook
glider.Page158in R. STRAHAN,
of Australianmammals.Angus& Robertson,Sydney.
F. 1960.Somephysiological
STRUMWASSER,
principles
governinghibernationin Citellusbeecheyi.Bull.
Mus.Comp.Zool. 124:282-318.
mical arousal from hibernationin the goldenWAKEFIELD,N. A. 1970. Notes on Australian pygmy
mantledgroundsquirrelCitelluslateralistescorum.
possums(Cercartetus,
Marsupialia).
Phalangeridae,
Can.J. Zool. 39:105-120.
VictorianNat. 87:11-18.
und Tagespe- WALLIS,R. L. 1976.Torporin thedasyuridmarsupial
POHL,H. 1961. Temperaturregulation
riodik des Stoffwechselsbei Winterschlifern.Z.
Antechinus
stuartii.Comp.Biochem.Physiol.53A:
319-322.
vergleichende
Physiol.45:109-153.
M. J. 1983.Westernpygmy-possum,Cercar- WANG, L. C. H., and J. W. HUDSON.1971. TemperSMITH,
atureregulationin normothermic
andhibernating
tetus concinnus.Pages 162-163 in R. STRAHAN,
ed.Completebookof Australianmammals.Angus
eastern chipmunk, Tamias striatus. Comp.
& Robertson,Sydney.
Biochem.Physiol.38A:59-90.