Seasonality of Torpor and Thermoregulation in Three Dasyurid Marsupials

Home , Kowari, Torpor

Journal of J Comp Physiol B (1987) 157:335-344 Comparative System~,Bi~ and Environ- Physiology B Physiologymental Springer-Verlag 1987

Seasonality of torpor and thermoregulation in three dasyurid marsupials

Fritz Geiser* and R.V. Baudinette School of Biological Sciences, Flinders University, Bedford Park 5042, South Australia

Accepted March 21, 1987

Summary. Seasonal variation in the pattern of tor- gy conserving state of lethargy allows these "heter- por and temperature regulation was investigated othermic endotherms" to survive periodic short- in the closely related arid zone dasyurid marsupials ages of energy and water. Because relative heat Sminthopsis crassicaudata (17 g), S. macroura loss is inversely related to body mass in endo- (24 g), and Dasyuroides byrnei (120 g). The ten- therms (Brody 1945), torpor occurs mainly in small dency to enter torpor was greater, torpor com- species, which may not be able to accumulate menced earlier, torpor duration was longer, and enough energy stores to maintain a constant high body temperatures (Tb) were lower in Sminthopsis Tb during cold exposure. spp. than in D. byrnei. The minimum mass-specific Considering that both cold exposure and food rate of oxygen consumption (lk'o2) of torpid ani- shortage occur predominantly during winter it is mals was similar among the three species despite not surprising that the pattern of thermoregulation the differences in minimum Tb. The mass-specific in many heterothermic mammals shows a seasonal oxygen consumption of normothermic animals was change. Such thermoregulatory changes are most reduced during winter when compared with the pronounced in seasonal hibernators that show summer values in all species, but there was no sea- strong annual rhythms of activity (homeothermy) sonal variation in normothermic Tb in any species. and hibernation (heterothermy) (Pengelley 1967). The tendency to enter torpor was increased during In species that enter daily, rather than prolonged, winter. Torpid Sminthops& spp. had lower values torpor the occurrence of dormancy is more oppor- of Tb and lZo2 during winter than during summer; tunistic; however, even in these species the fre- D. byrnei did not show seasonal changes in these quency of torpor is reduced during summer (Lynch variables. These results suggest that seasonal chan- etal. 1978; Heldmaier and Steinlechner 1981a). ges in the pattern of thermoregulation and torpor The lower proclivity to entering torpor in summer in small dasyurids may be more distinct than in is accompanied by higher Tb's during torpor than larger species. in winter (Gaertner et al. 1973; Lynch et al. 1978; Tannenbaum 1985) suggesting that the "set point" at which Tb is regulated during torpor may vary seasonally. Because our knowledge about seasonal changes Introduction of the physiology of daily torpor is very restricted Torpor in warm-blooded animals is expressed by we investigated how variables of torpor in dasyurid a lowering of body temperature (Tb) and metabo- marsupials may be modified by season. The species lism both of which can be actively raised to the we studied were Sminthopsis crassicaudata (body initial high values after a torpor episode. This crier- mass 14-22 g), S. macroura (body mass 19-30 g), and Dasyuroides byrnei (body mass 96-140 g), Abbreviations: RMR resting metabolic rate; BMR basal meta- three closely related marsupials which have over- bolic rate lapping distribution ranges and similar life histo- * Present address : Department of Zoology, University of Ade- ries (Lee etal. 1982; Aslin 1983; Morton et al. laide, Adelaide 5001, South Australia 1983). 336 F. Geiser and R.V. Baudinette: Seasonal torpor in dasyurids

Materials and methods 2O

Animals. The fat-tailed dunnart, Sminthopsis crassieaudata, oc- , me•. Te curs widely in southern Australia and is mainly found in semi- 30 ,*" I/ / 16 , / arid and arid habitats. It is nocturnal and is found in soil cracks and unter stones (Morton 1978). Its diet consists mainly of 25 \ \ ,:/ 14 C invertebrates, with a large proportion of spiders and insects ~eo ,, l? 12 mo (Morton et al. 1983). Torpor in the wild and in captivity have 2O been described (Godfrey 1968; Morton 1978). The animals ",/ 10 (16 males and 12 females) used in the present study were ob- 15 tained from a laboratory colony at the Genetics Department, Adelaide University, with the exception of two individuals ,o ~.Q__/ . i/! / sunrise which had been wild caught. The stripe-faced dunnart, Sminthopsis maeroura is found in arid and semi-arid parts of central and northern Australia. 'AJS'O'N'D'J'F'M'A'M'JAJ'AtS'O'NID'J'F'M ' 'Month ' The animal's behaviour in the field is largely unknown, but 1983 198/* 1985 in the laboratory, S. maeroura readily enters torpor (Geiser and Fig. 1. Monthly minima and maxima of air temperature (T,), Baudinette 1985). In captivity, the animal is largely nocturnal and the times of sunrise and sunset during the experimental (O'Reilly et al. 1984). Food habits in the wild are similar to period. T, was measured in the animal holding pens with a that of S. crassieaudata, but a larger proportion of termites minimum-maximum thermometer. Sunrise and sunset represent are used as prey items (Morton et al. 1983). Animals used in certified times by the Bureau of Meteorology, Adelaide. the present study (10 males, 14 females) were obtained from The austral seasons are defined as: spring: 1 September- laboratory colonies at the Arthur Rylah Institute, Heidelberg, 30November; summer: I December-28February; autumn: Victoria, and from the Evolutionary Biology Unit, South Aus- 1 Marc~31 May; and winter: 1 June.31 August tralian Museum, Adelaide. The kowari, Dasyuroides byrnei is found in the gibber des- erts of south-western Queensland. It lives in burrows, appears to be nocturnal and solitary, and has a diet consisting of insects be the endpoint of the arousal period). Additional measure- and small vertebrates (Aslin 1983). Torpor has been previously ments of shorter periods were used to determine the Vo2 of described in this species (Geiser et al. 1986a). The animals used postabsorpfive, normothermic, inactive animals at Ta around in the present study (8 males, 7 females) were obtained from and above thermoneutrality during their inactive period (day- a laboratory colony at the Evolutionary Biology Unit, South time). All measurements were conducted in a quiet controlled- Australian Museum. temperature room (T,_+0.5 ~ that was acoustically isolated Experiments were conducted on adults only, between au- from the recording equipment; animals were observed by video tumn 1983 and summer 1985. The austral seasons are defined camera during the experiments. as: spring, 1 September-30 November; summer, 1 December- A Servomex Model OA 184 paramagnetic oxygen analyzer 28 February; autumn, 1 March-31 May; and winter, 1 June- was used for the [/% measurements together with a Rikadenki 31 August. Animals were held outside at the Flinders University potentiometric recorder, l/o~ was determined from the differ- of South Australia (34 ~ 56'S, 138 ~36'E), exposed to natural pho- ence between the oxygen content in two parallel open flow toperiod and temperature fluctuations (Fig. 1). They were circuits (room air reference vs the animal). Flow rates of dried housed individually in cages provided with hardwood shavings air in the open flow system were adjusted and measured with and boxes containing nesting material. Animals were fed ad calibrated rotameters to 0,3-0.41/min (S. crassicaudata), libitum a mixture of dried and canned commercial pet food 0.3-0.5 l/rain (S. macroura), and 0.6-1.2 1/min (D. byrnei). Car- and water. Tenebrio larvae and an egg-gelatine mixture were bon dioxide was not scrubbed from the system because the provided every two weeks. absorbant caused large pressure drops in prolonged experiments and thereby changed the partial pressure recorded in Experimental details. Diurnal fluctuations in oxygen consump- the analyzer cell. All volumes were corrected to dry standard tion (t/o2) were determined over an air temperature (Ta) range temperature and pressure (STPD)and rates of oxygen consump- of about 5-32 ~ In S. crassicaudata, 62 tests of mean duration tion were calculated using equation 3a of Withers (1977). An 21.2• were conducted in summer and 40tests of RQ of 0.85 was assumed which would result in a maximum 20.1 _+2.6 h in winter; for S. macroura, 23 tests of 20.1 _+2.1 h error of 3 % if the RQ value was actually 1 or 0.7. Repirometers in summer and 33 tests of 20.8 +- 1.4 h in winter; and for D. byr- were 3 1 for Sminthopsis app. and 7 1 for D. byrnei. For the nei, 39tests of 21.1+_2.1 h in summer and 36tests of calculation of mass specific Vo2 during prolonged experimental 21.0_+2.3 h in winter. These measurements began in the after- periods, the animals were weighed before and after the experi- noon 2-3 h before the lights switched off. The photoperiod ments and body masses were interpolated assuming a constant in all experiments matched local sunrise and sunset. Food and rate of loss. water were not available during measurements of Vow- Mea- Temperature in the respiratory chamber was measured with surements of i/o= were used to determine the metabolic rate two thermocouples; one connected to an Omega 871 Digital of normothermic, inactive animals measured when a variation Thermometer and used for point readings and the other con- of less than 5% over at least 15 min occurred after an inactive nected to an Omega MCJ-T Thermocouple Connector and the period of at least 30 min (RMR); the minimum metabolic rate Rikadenki recorder. Tb was measured with 0.5 mm diameter of torpid animals was determined at times of constant Vo2 over thermocouples inserted into the rectum (20-25 mm Sminthopsis at least 30 min (the f?o~ of S. crassicaudata during torpor spp.; 3040 mm D. byrnei). All thermocouples were calibrated and normothermia are those reported by Geiser et al. 1986b). against a mercury thermometer traceable to a national stan- Furthermore, the duration of torpor and the time required to dard. arouse from torpor to normothermia were derived from these Means of samples are expressed+the standard deviation measurements (the ]'2o2 peak during arousal was assumed to (SD). N = number of individuals; n = number of determinations. F. Geiser and R.V, Baudinette: Seasonal torpor in dasyurids 337

Table 1. Frequency of induced torpor (food and water not pro- Table 2. The time of onset of torpor and torpor duration in vided) and spontaneous torpor (food and water ad libitum) Sminthopsis crassicaudata, S. macroura, and Dasyuroides byrnei in Sminthopsis crassicaudata, S. macroura, and Dasyuroides byrnei Species Season Relative time Torpor (h) duration (h) Species Season N n Torpid Normo- % thermic torpid S. crassicaudata summer -1.2_+3.0 (14) 5.4_+2.5 (12) winter -3.0_+3.0 (17) 5.9_+3.0 (8) Induced torpor: S. macroura summer -2.4+2.7 (8) 5.5_+3.4 (8) S. crassicaudata summer 15 59 45 14 76 winter -3.1+2.6 (11) 6.0_+2.8 (11) winter 17 24 23 1 96 D. byrnei summer +1.1-t-1.7 (8) 2.7+_1.9 (8) S. macroura summer 9 16 13 3 81 winter -0.9_+1.3 (9) 2.7+_1.9 (12) winter 9 24 24 0 100 D. byrnei summer 8 25 20 5 80 The time of torpor onset was defined as the time at which winter 11 35 29 6 83 a decrease in Vo2 that resulted in a torpor bout was observed. Relative time represents the time in relation to 'lights on'; Spontaneous torpor: -indicates that torpor occurred before the lights switched on; + indicates torpor entry after the lights switched on. The onset S. crassicaudata spring 6 65 8 57 12 of torpor relative to the onset of light occurred significantly summer 14 77 10 67 13 earlier in winter than in summer in S. crassicaudata and D. byr- winter 9 103 14 89 14 nei (t-test; P<0.05) and torpor onset in D. byrnei occurred S. macroura spring 9 18 3 15 17 later than in the Sminthopsis species (P < 0.01; Kruskal-Wallis summer 15 49 6 43 12 one-way nonparametric ANOVA and Mann-Whitney U-test). autumn 15 45 13 32 29 Mean torpor duration did not show significant seasonal chan- winter 15 97 29 68 30 ges in any species (t-test). Torpor duration in the Sminthopsis species was significantly longer than in D. byrnei (P<0.05; D. byrnei spring 13 90 4 86 4 Kruskal-Wallis one-way nonparametric ANOVA and Mann- summer 12 71 1 70 1 Whitney U-test). Numbers of individuals are shown in paren- winter 13 165 16 149 10 theses

Data for induced torpor were taken from the measurements of 17o2 at Ta ~20 ~ (see Fig. 3). Observations of spontaneous was more frequent during winter in D. byrnei and torpor were made in the morning at about 0900 h. Significant S. macroura; spring and autumn values were inter- differences between summer and winter in the frequency of torpor were observed in S. crassicaudata and S. macroura (in- mediate (Table 1). S. crassicaudata did not show duced torpor) and in S. macroura and D. byrnei (spontaneous this seasonal variation in spontaneous torpor. torpor) (P < 0.05 ; equality test of two percentages), N = number Induced torpor in Sminthopsis spp. commenced of individuals; n = number of observations earlier than in D. byrnei and in both summer and winter torpor began before the onset of light (Ta- Results ble 2). In D. byrnei, the onset of torpor occurred before the lights switched on in winter and after Distinct differences in the tendency to enter torpor the lights switched on in summer. Significant sea- were observed in the three species investigated (Ta- sonal differences in the timing of torpor relative ble 1). In all species torpor was more frequent to the time of lights on were observed in S. crassi- when food was withdrawn (induced torpor) than caudata and D. byrnei (P < 0.05 ; Mann-Whitney when food and water were available (spontaneous U-test). The time of torpor onset did not appear torpor). Spontaneous torpor was observed only in to be related to T, in any species. the morning. Both Sminthopsis species showed a Torpor bouts were shorter than 24 h in all three greater tendency to enter torpor than D. byrnei, species. The mean duration of torpor did not show the largest species (Table 1). The frequency of in- seasonal variation in either species and was be- duced torpor by food and water deprivation during tween 5.4 and 6.0 h in Sminthopsis spp. which was the measurements of Vo2 at T~ 4-20 ~ (compare significantly longer than the 2.7 h in D. byrnei (Ta- Fig. 3) in Sminthopsis increased from about 80% ble2; P<0.05; Mann-Whitney U-test). Torpor in summer to 100% in winter. Of the 7 individual duration was not strongly dependent on Ta ; how- S. crassicaudata that were tested under these condi- ever, the longest torpor bouts were observed be- tions in both seasons 3 remained normothermic tween Ta 10 and 20 ~ in all species. throughout the experiment in summer whereas all Normothermic Tb'S in animals resting at Ta but one individual entered torpor in winter. In con- <30 ~ were similar in all three species, about trast, D. byrnei showed no seasonal variation in 34 ~ and no seasonal changes were observed the tendency to enter torpor after food depriva- (Fig. 2, Table 3). In animals that had entered tor- tion. Spontaneous torpor in the outdoor facilities por at the Ta at which Tb was measured, Tb during 40 4C ~0 Sminth0psis crassicaudata Sminfhopsis macr0ura Dasyuroides byrnei OO

o o o O0 % o 0 35 o ~ ~ o~ ~~ o ~ g o ~176176176 35 o o e o o 35 o o ~ oOa~o o o~ o o o o o 0 0 c9 o o o ~ / o ooooo :.. 3C ~~176..: ~176 :/ 30 /

25 25 25 . ;-C. O t-J o o . o. " ~ Tb =T 20 ~-= 20 . "0" f-~ 20

i 15 15 o ~ 12 O 0~ summer

10 summer 10 10

i i i i L i l I I I i i I i I I I I i I i I 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35

40 40 40 o o o o 35 o o o o o~ % 8 --~ -- 35 o @ ~176 o 35 o ~ o o o oo o o o ~176 ~176 o o o o o o o ~ o o o o /~o 30 30 oo goO, o Tb__~Ta C) 25 2~ o -# G .. o 25 o o ~ .~ 'We * & 20 20 ~-= 2o ,,; - .< 15 : 15 15

O winfer winter 10 10 10 0

i i i I i I I i i i O/ , i I I I I L I I I I I I I r~ 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35

Ta (~ Ta 1%) Ta {~ E Fig. 2. Body temperatures (Tb) as a function of air temperature (T,) in normothermic, inactive (o), torpid (*), and hypothermic (<>) dasyurid marsupials in summer (upper) S~ and winter (lower). Animals with a Tb< 31 ~ were considered to be torpid because they showed a conspicuous loss of coordination. Each point represents an individual R measurement of Tb. The constructed solid line represents Tb = T~ F. Geiser and R.V. Baudinette: Seasonal torpor in dasyurids 339

Table 3. Body temperatures (Tb) and rates of oxygen consumption (12o2) during normothermia and torpor in Srninthopsis crassicaudata, S. macroura, and Dasyuroides byrnei

Species Tb rest BMR Tb torpor 12o2min Body mass (Season) (~ (1 O2/kg h) (~ (1 O2/kg h) (g)

S. crassicaudata (s) 34.3-t-1.0 (14) 1.25_+0.20 (6) 20.2+_2.5 (10) 0.40___0.16 (8) 17.7_+ 2.1 (19) (w) 34.1+_0.9 (15) 1.22+0.15 (8) 16.9+-2.4 (12) 0.29+0.10 (12) 17.3+- 2.5 (15) S. maeroura (s) 33.9___1.3(11) 1.07+-0.10 (5) 20.7+_2.3 (11) 0.57__.0.22 (5) 22.0+_ 2.3 (11) (w) 34.0_+0.9 (11) 1.01+_0.26 (6) 18.4_+2.2 (13) 0.33+_0.13 (8) 26.9_+ 3.4 (13) D. byrnei (s) 34.3_1.1 (8) 0.70+_0.11(6) 24.6-+2.2 (9) 0.44_+0.04 (6) 118.2__.14.7 (9) (w) 34.2+_0.9 (9) 0.78+_0.12 (5) 25.4_+1.1 (7) 0.40+_0.03 (5) 115.0+_12.9 (13)

Values represent means +- SD. The body masses (with number of individuals) are the corresponding values for the ~2o2measurements in Fig. 3. Significant seasonal differences were observed in I)o2min and the Tb during torpor in S. crassicaudata and S. macroura (t-test; P<0.05), but not in D. byrnei. The mean Tb during torpor of the three species in both seasons were determined from measurements that had been taken below the T, of the l/o2 intercept in torpor; i.e. the highest T, below which individuals of each species regulated Tb during torpor (see Fig. 3). Numbers of individuals are shown in parentheses. (s) = summer, (w) = winter

torpor decreased with Ta and the difference be- 12o2 during torpor in winter was significantly lower tween these temperatures (A 7) was usually > 1 ~ than in summer (P<0.05; t-test); only a slight re- The lowest Tb'S (13.0 ~ S. crassicaudata; 14.0 ~ duction in the 1?o2 minima during winter was ob- S. macroura) were observed in winter. In summer served in D. byrnei. When the 12o2 minima during the minimum Tb'S were 16.3 and 15.0 ~ respec- torpor of 7 individual S. crassicaudata that had tively. The mean Tb's during torpor in the Smin- been measured in both summer and winter were thopsis species were significantly lower during compared within a Ta range of 3 ~ for each indi- winter than during summer (P<0.05; t-test), but vidual, the summer animals showed a 1.6-fold in- not in D. byrnei (Table 3). The minimum Tb of crease in ~7o2 over the winter animals and the D. byrnei was 20.4 ~ and Tb during torpor was means in summer were significantly greater than greater than in Sminthopsis spp. (P < 0.001; t-test). during winter (P<0.05; t-test). In D. byrnei most At Ta below the seasonal Tb minimum of each individuals were used in summer and winter, but species, an increase in A T during torpor occurred; no significant seasonal differences in 12o~ during the absolute values of Tb's of torpid animals in torpor could be detected. A linear increase in Vo2 this range of T, were also increased. Individuals below a critical Ta was observed in all species that further decreased Tb were unable to arouse (Fig. 3). The lines relating 17o2 of torpid dasyurids at the T, at which they had entered torpor. and Ta (at Ta's below which Vo2 during torpor However, most hypothermic individuals completed increased, in the Sminthopsis species - this temper- arousal after partial rewarming. atures varied seasonally; in D. byrnei the increase Rates of oxygen consumption of normo- of 12o2 occurred below Ta 15 ~ in both seasons) thermic, resting dasyurids (RMR) were strongly were significantly lower in elevation during winter temperature dependent and increased linearly in than in summer (P < 0.01 ; F-test). In the Srninthop- all species in both summer and winter as T, de- sis species this shift was more pronounced than creased below thermoneutrality (Fig. 3). During that observed for the RMR. The intercepts of these summer, the lines relating resting metabolic rate derived lines with the abscissa occurred at a lower (RMR) and Ta were significantly higher in eleva- temperature during winter than in summer in tion than in winter (F-test; P<0.01). The inter- Sminthopsis spp., suggesting a shift in the set point cepts of these lines with the abscissa (T~) were at which Tb is regulated during torpor. This was within 3.2 ~ of the mean Tb determined. No sig- not the case in D. byrnei. The intercepts of these nificant seasonal differences could be detected in lines with the abscissa were within 1.9 ~ of the the basal metabolic rate (BMR) (Table 3). minimum Tb determined for each species and sea- In the range of T~'s below the thermoneutral son. zone and above the T~ at which Tb was regulated, Several individuals at low Ta were unable to torpid animals decreased/2o2 steadily with decreas- maintain a constant "high" Vo2 during torpor and ing Ta (Fig. 3). The mean values of lJ'o2 of the 12o2 steadily declined after an initial constant level three species in torpor ranged from 0.3-0.6 1 02/ of 1-2 h (Fig. 3). These animals were unable to kg h (Table 3). In Sminthopsis spp., the minimum arouse without partial rewarming. Sminfhopsis crassicaudata summer 8 winter

0 o 0@~ ~ o ~ ",\o

~ o ~ c~ o oO \\\\ ~176xo~xx @ t~ o oo ""%% o oN~ x o -x \~ o o %\N\%% \ \ N,O\\0 \ o ooo o

%. , 5 10 15 20 25 30 3'5 0 5 10 15 20 25 30 35

Ta (~ Ta (~

Sminthopsis macroura summer 8-\ winter

6 \\\ o \\\

5, o o 0~ o\\\ o \o,,, .> 4, o o \\ o aB \o

o o 3

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j , \ %1"{ j n a "~. \ 5 10 15 20 25 30 35 5 10 15 20 25 30 35 Ta (~ Ta (o[)

Das)ur0ides byrnei summer winter o

--..< o .c: 3 "---1 o o o~o o ~ o 2 ~o ~o--..~ o o C] o o ~ ~ ~o o o 1 ~ o

9 n I I ~L L n 0 0 5 10 15 20 25 30 "-3'5 0 5 10 15 20 25 30 "35 - Ta (~ Ta (~

Fig. 3. Rates of oxygen consumption (12o2) as a function of air temperature (Ta) of the three dasyurids in summer and winter. The symbols indicate: normothermic, inactive (o); J2o2 minima during torpor that were constant over at least 30 rain (o); and animals in hypothermia (o). Lines were fitted by least squares regressions to the 12%'s that were increased due to thermoregulation during both normothemfia and torpor. In the Sminthopsis species this thermoregulatory increase of [202 during torpor showed strong seasonal changes; in D. byrnei it occurred below T~ 15 ~ in both seasons. The equations are: S. crassicaudata, summer: y=7.82-0.23x; r=-0.96 (normothermic, inactive), y=4.28-0.29x; r=-0.92 (in torpor); winter: y=7.69-0.20x; r=-0.96 (normothermic, inactive), y = 3.58- 0.30 x; r = -0.95 (in torpor). S. rnacroura, summer: y = 7.81 -0.21 x; r = -0.97 (normothermic, inactive), y = 4.95 - 0.28 x; r = - 0.87 (in torpor); winter: y = 6.38 - 0.18 x; r = 0.93 (normothermic, inactive), y = 3.84 - 0.30 x; r = - 0.96 (in torpor). D. byrnei, summer: y = 3.53 - 0.10 x; r = -- 0.94 (normothermic, inactive), y = 1.65 - 0.08 x; r = - 0.95 (in torpor); winter: y-2.92--0.08x; r= -0.84 (normothermic, inactive), y= 1.20-0.06x; r= --0.73 (in torpor). The broken lines in the winter graphs represent the summer values F. Geiser and R.V. Baudinette: Seasonal torpor in dasyurids 341

500 Sminfhopsis crassicaudafa

1.5- 2LoC 200

"5 1.0- c t00 2O o z~ o zAz~ o o \ o~ 50 .> .4.- 0.5"

to 20 0 0 & 7//~9 10 1'1 1'2 1'3

TIME OF DAY (h) 10 Fig. 4. The rate of oxygen consumption (/2o= ; solid line) of 5' 10' 15' 2"0 "25 30' an individual torpid S. crassicaudata exposed to a changing 500 air temperature (T~ ; broken line). The T.'s at which an increase Sminfhopsis macroura in Vo~ occurred are indicated. The increase in 12% that occurred after cooling was reversed and the T, was increased suggests that the increase in f)% below T~ = 11 ~ was due to thermore- 200 gulation, not arousal. Arousal was induced when T, reached 24 ~ The abscissa represents the local time, the dark bar indi- lal cates the period of darkness. The I2o~ between 0700 and 0900 h 100 was constant and was omitted 'V=

~,~. o 50

When torpid S. crassicaudata were cooled, their

l~o~ showed an increase at a critical T~ (Fig. 4). to "IDAz~~ The mean Ta at which an increase in l?o~ was ob- 20 served during cooling was 15.0+0.9 ~ (N=7) in summer and 11.5+0.8 ~ (N=7) in winter; these 10 t I i i s i means were significantly different (P<0.001; t- 5 10 15 20 25 30 test). For three individuals cooling experiments during torpor were performed in both seasons and 100 Dasyuroides byrnei l?o~ increased at T, 16.0_+0.6 ~ in summer and -'5 T~ 11.9+0.4 ~ in winter. These results further V= 50 o support the view of a seasonal shift in the "set o ~ z~ ~ o point" at which Tb is regulated during torpor (see ,i .4- ~A Fig. 3). Reduction of T~ below these critical tem- z~ ~ ~ o el 20 o peratures resulted in arousal in half the animals, o while the others remained torpid but increased to 10 J 110 ll5 J I 1~o~. 0 5 20 25 30 The time required to arouse from torpor to z a C~ normothermia showed an exponential increase Fig. 5. Semi-logarithmic plots of the arousal times in the three with decreasing T, in most cases (Fig. 5). The dasyurids at a function of air temperature (T,). The symbols slopes relating these variables were a function of indicate: disturbance-induced arousal in summer (o) and winter body mass: values for S. crassicaudata being the (A); and spontaneous arousal in summer (o) and winter (zx). greatest and those for D. byrnei the least. In In S, macroura arousals induced by measurement of Tb in summer at T,'s below 15 ~ were slower than those in winter (bro- S. macroura a paradoxical situation was observed ken line). The solid lines represent fits to all measurements in winter, as arousals induced by measurement of in both seasons in D. byrnei and S. crassicaudata and to all Tb decreased in length at lower T~'s. This suggests measurements in summer in S. macroura. The lines were fitted that at low T~ arousal time during winter is shorter by least squares regressions and the equations are: S. crassicau- than during summer. Maximal arousal rates deter- data, log y=2.41-0.048x; r=-0.86. S. macroura, summer: log y=2.32-0.046x; r=-0.92; winter, induced: log y= mined over a time interval of 10 min were 0.68 ~ 1.40+0.018x ; r=0.46; winter, spontaneous: log y=2.24- rain in S. crassicaudata (Ta 22 ~ 0.70 ~ in 0.035x; r= -0.66. D. byrnei, log y= 1.59-0.011 x; r= -0.36 342 F. Geiser and R.V. Baudinette: Seasonal torpor in dasyurids

S. macroura (Ta 23 ~ and 0.55 ~ in D. byr- spp. the slight reduction in Tb during torpor results nei (Ta 9 ~ in I)% values similar to those in Sminthopsis at much lower Tb'S. Relatively high Tb's similar to those in D. byrnei have also been observed in tor- Discussion pid Dasycercus cristicaudata (100 g) and Dasyurus The present study suggests that the pattern of tor- geoffroii (1000 g) (Kennedy and McFarlane 1971; por in the three arid zone dasyurid marsupials in- Arnold 1976), suggesting that larger arid zone da- vestigated is influenced by season and perhaps syurids may not lower Tb below 15-20 ~ unlike body size. While in the two smaller species, Smin- the smaller (<50g) species (Geiser 1985, 1986; topsis crassicaudata and S. macroura, torpor was present study). This observation indicates that the generally more pronounced in winter than in sum- minimum Tb during daily torpor in dasyurids may mer, such distinct seasonal differences were not be influenced by body size with the lower values observed in Dasyuroides byrnei, the largest species. occurring in the smaller species and allowing them The incidence of induced torpor in the dasyur- to maximise energy savings. The increased ten- ids under similar conditions was increased in both dency to entering torpor, longer torpor bouts, and Sminthopsis species in winter suggesting a seasonal lower minimum Tb'S in half grown than in adult change in the proclivity to entering torpor. Similar D. byrnei (Geiser et al. 1986a) supports this view. seasonal changes in the tendency to entering torpor Longer and deeper torpor may contribute to ener- have also been observed in the small (30 g) da- getic balance in the smaller species which lose more syurid Antechinus stuartii (Wallis 1976). Dasyur- heat to the environment than larger species while oides byrnei lacked such seasonal differences, but normothermic. this species showed an increase in spontaneous tor- The Q~0 of oxygen consumption between nor- por in winter, most likely as a response to the mothermia (BMR) and torpor in the Sminthopsis colder temperatures (Fig. 1). A seasonal shift in species was slightly higher in winter. This would the frequency of spontaneous torpor also occurred contribute further to energy conservation. The Qlo in S. macroura in agreement with observations on in both species was, however, between 1.6 and 2.5 heterothermic placentals (Lynch et al. 1978; Held- in both seasons, suggesting that the low metabo- maier and Steinlechner 1981a). The observation lism found during torpor in these dasyurids and of spontaneous torpor in S. crassicaudata during also in hibernating ground squirrels (Snapp and summer contrasts with findings of Morton (1978) Heller 1981) is directly due to a temperature effect who sampled, however, at a time of day when the rather than some suggested physiological inhibi- present study indicates that this species would be tion. normothermic. Spontaneous torpor throughout Although torpor duration was significantly the year in D. byrnei warrants critical re-examina- longer in the Sminthopsis than in D. byrnei, sea- tion of reports on summer homeothermy in smaller sonal differences in the duration of torpor could marsupials. not be observed in any species. This suggests that The Tb'S and l/o2'S of both torpid Sminthopsis the seasonal adjustment of energy balance by he- species were lower in winter than during summer. terothermy in these marsupials is achieved by vary- While lower Tb's in winter have been reported pre- ing the depth rather than the length of torpor. Be- viously in torpid Peromyseus spp. (Gaertner et al. cause species that enter daily torpor forage and 1973; Lynch et al. 1978; Tannenbaum 1985) our feed between their lethargic phases and subse- observation of a seasonal shift in the "set point" quently have to digest the food, an extension of temperature during torpor is the first recorded case torpor duration beyond about 6 h/day may be lim- in the literature. The lower Tb's should allow a ited. greater reduction in metabolic rate during torpor Rewarming from torpor was faster in the Smin- in winter and thus enhance energy conservation. thopsis than in D. byrnei, the largest species, in Dasyuroides byrnei, the larger species, did not show agreement with the prediction that body mass and seasonal shifts in the "set point" temperature. arousal rates from torpor are inversely related However, despite the relatively high Tb of > 20 ~ (Heinrich and Bartholomew 1971). However, in the mass-specific I/o2 of this species was reduced contrast to D. byrnei which showed similar arousal to minima similar to those of Sminthopsis, suggest- times over a wide range of Ta's, these variables ing that a relatively small reduction in Tb is a suffi- varied strongly with Ta in the Sminthopsis. There- cient contribution to energy conservation in fore, at low Ta arousal rates should in fact be faster D. byrnei. Because the BMR of D. byrnei, the larg- in small than in large species and a reversal of est species, is much lower than in the Sminthopsis the inverse relationship between rewarming rate F. Geiser and R.V. Baudinette: Seasonal torpor in dasyurids 343 and body mass can be predicted. Arousal rates in work was supported by a Flinders University Research Scholar- the three dasyurids investigated herein were similar ship to F.G. and by the Australian Research Grant Scheme to or faster (almost twice as fast in D. byrnei) than to R.V.B. The paper was written while F.G. held an Alexander yon Humboldt-Lynen Research Scholarship at the University predicted for birds and mammals (Heinrich and of Washington. Bartholomew 1971). These findings do not support earlier suggestions of a generally slow rewarming from torpor in marsupials. 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J Mammal 54:708 728 Kenagy G J, Vleck D (1982) Daily temporal organization of Acknowledgements. We would like to thank H.J. Aslin, J.H. metabolism in small mammals: adaptation and diversity. Bennett, D.D. Evans, and M.J. Smith for supply of animals, In : Aschoff J, Daan S, Groos G (eds) Vertebrate Circadian M. O'Driscoll for animal maintenance, and D.S. Hinds, G.J. Systems. Springer, Berlin Heidelberg New York, pp 322 Kenagy and M.G. Tannenbaum for advice and criticism. This 338 344 F. Geiser and R.V. Baudinette : Seasonal torpor in dasyurids

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