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Seasonality of Torpor and Thermoregulation in Three Dasyurid Marsupials

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Seasonality of Torpor and Thermoregulation in Three Dasyurid Marsupials 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 experi- ments 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.
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