Basking and Torpor in a Rock-Dwelling Desert Marsupial: Survival Strategies in a Resource-Poor Environment

J Comp Physiol B DOI 10.1007/s00360-007-0186-z

ORIGINAL PAPER

Basking and torpor in a rock-dwelling desert marsupial: survival strategies in a resource-poor environment

Fritz Geiser · Chris R. Pavey

Received: 30 April 2007 / Revised: 24 June 2007 / Accepted: 27 June 2007 © Springer-Verlag 2007

Abstract Australian deserts are characterized by unpre- Our study suggests that by frequently employing daily tor- dictability, low primary productivity, and high temperature por and basking and by appropriately coordinating their Xuctuations. Despite these adverse conditions the diversity thermal biology with that of speciWc locations in their envi- of small insectivorous marsupials of the family Dasyuridae ronment, Pseudantechinus can reduce daily energy expen- is surprisingly high. We quantiWed the thermal biology of diture and thus can live and reproduce in a challenging the dasyurid Pseudantechinus madonnellensis (body mass environment. It is likely that the success of other small das- »30 g) in the wild to gain some understanding of whether yurids and perhaps many other small mammals living in the success of dasyurids in the arid zone may be related to deserts is linked to employment of torpor and basking for some extent to their use of energy conservation strategies. energy conservation. In winter, most free-ranging Pseudantechinus frequently (58.3% of 131 animal days) entered daily torpor after mid- Keywords Activity patterns · Basking · Desert mammals · night (mean 0157 hours) in rock crevices when outside Daily torpor · Energy conservation · Pseudantechinus ambient temperatures (Ta) were low. Most animals macdonnellensis · Thermal environment remained torpid until the next morning when they moved while still torpid from rock crevices to sun-exposed basking Abbreviations sites. We visually observed basking during rewarming from MR Metabolic rate torpor (mean commencement at 0943 hours) at body tem- Ta Air temperature peratures (Tb) as low as 19.3°C when radiant heat was high Ta bask Basking temperature and Ta was rising. Basking continued for the rest of the day. Ta cave Cave temperature Torpor use was not strongly correlated with Ta, but the tem- Tb Body temperature poral organization of daily torpor and activity were apparently linked to the thermal characteristics of basking sites. Introduction

Arid regions represent extreme environments for the persis- Communicated by I.D. Hume. tence of animal and plant life particularly as a result of low primary productivity, limited supply of food and water, and F. Geiser (&) X pronounced daily and seasonal uctuations of Ta. Australia Centre for Behavioural and Physiological Ecology, is a dry continent with almost half its land area experienc- Zoology, University of New England, Armidale, NSW 2351, Australia ing mean annual rainfall of less than 250 mm (Trewin e-mail: [email protected] 2006) and with infertile soils (StaVord Smith and Morton 1990), but despite these adverse conditions the diversity of C. R. Pavey small mammals in the Australian arid zone is high (Dick- Biodiversity Conservation, Department of Natural Resources, Environment and of the Arts, P.O. Box 1120, Alice Springs, man 2003). The most successful group of mammals are NT 0871, Australia small insectivorous/carnivorous marsupials of the family 123 J Comp Physiol B

Dasyuridae with about half of the 53 Australian species liv- dasyurid living in arid regions of Australia with a strong- ing entirely or partially in the arid zone (Menkhorst and hold in the MacDonnell Ranges where they typically Knight 2001; Dickman 2003). inhabit rocky areas, use multiple rock crevices as shelters Small endothermic mammals living in deserts face sev- and, for desert dasyurids (Dickman et al. 2001), show a W W eral challenges because of extreme Ta and frequent lack of strong site- delity (Gil llan 2001; Menkhorst and Knight food and water (Schmidt-Nielsen 1979; Bradshaw 2003). 2001; Dickman 2003; Pavey et al. 2003). We were espe- The large relative surface area of small endotherms requires cially interested in understanding how in the wild these high metabolic rates (MR) and results in high water loss mammals employ torpor and other energy saving mecha- when their Tb is regulated at homeothermic levels particu- nisms such as basking (Geiser et al. 2002) and appropriate larly when they are exposed to extreme environmental con- timing of daily activity and rest phases to permit life in an ditions. Especially in insectivorous endotherms food environment with limited food supply. Use of basking in availability declines with Ta while energy requirements torpid mammals has been discovered only recently as a increase (Speakman and Thomas 2003), and food, but also strategy for energy conservation (Geiser et al. 2002, 2004; water requirements, may exceed available resources. These Mzilikazi et al. 2002; Warnecke et al. 2007) and laboratory limitations appear to be the primary reason why not all data on a small dasyurid marsupial suggest that it can sub- endotherms are permanently homeothermic. Many small stantially reduce the energy cost associated with arousal species are heterothermic and are capable of entering a state from torpor (Geiser and Drury 2003). of torpor, characterised by substantial reductions of Tb, MR, water loss and other physiological processes that reduce water and food requirements (MacMillen and Hinds Methods 1983; Wang 1989; Withers 1992; Frank 1994; Geiser 2004; Gutman et al. 2006). The study was conducted in winter (June/July 2001) at Arid zone dasyurid marsupials employ daily torpor Ormiston Gorge (23°37ЈS, 132°45ЈE, altitude »600 m), in under laboratory conditions, some even when food is freely the West MacDonnell National Park, Northern Territory, in available. Others use torpor during the reproductive season, central Australia. The study site was located largely on when most mammals maintain strict homeothermy, sug- north-facing steep slopes covered in sandstone rocks and gesting that torpor is a crucial adaptation that allows these spinifex (Triodia brizoides) that contained high vertical small mammals to live and reproduce in Australian deserts sandstone cliVs and some caves. We caught seven adult fat- W (Geiser 2003). Dasyurids reduce Tb from »35°C during tailed antechinus (two females, ve males) using Elliott box V normothermia (high MR and high regulated Tb) to »15°C traps along sandstone cli s. Capture body mass of males during torpor. The MR during daily torpor is on average and females was indistinguishable (t test, t =0.7, df =5, reduced to »30% of the basal MR (Geiser 2003), and water P > 0.5) and the overall mean body mass was 30.8 § 5.0 g loss during torpor is reduced to one third of that in normo- (n=7). Animals were transferred to a Weld laboratory and thermic individuals (Cooper et al. 2005). While torpor in temperature-sensitive transmitters were implanted intraper- arid zone dasyurids has been studied in several species, itoneally (using a small, <1 cm, ventral incision) into six almost all of this knowledge is based on laboratory mea- individuals under Oxygen/IsoXurane anaesthesia. The inci- surements quantiWed under constant thermal conditions. sion was sutured with a self-absorbing sterile chromic gut However, recent evidence shows that laboratory data on suture. Animals recovered quickly from surgery, which torpor can diVer substantially from those obtained in the typically lasted »20 min. Incisions were clean and partially Weld and often torpor is less frequent, shallower, and of healed when animals were released. Prior to surgery, trans- shorter duration in captivity than in the Weld (Geiser et al. mitters (Sirtrack, New Zealand, FM single stage, mass 2 g) 2000). Thus, laboratory data may underestimate the ecolog- were coated in ParaYn/Elvax (Minimitter, USA) and cali- ical and functional signiWcance of torpor for survival in a brated against a precision thermometer to the nearest 0.1°C challenging desert environment. in a water bath from 10 to 40°C to derive an equation of The purpose of our study was to investigate the ecology pulse rate as a function of temperature (r2 > 0.99), which and thermal biology of a free-ranging arid zone dasyurid, was used to calculate Tb of free-ranging individuals. Ani- the fat-tailed antechinus (Pseudantechinus macdonnellen- mals were released at their site of capture after recovery for sis) in relation to its diverse and changing thermal environ- one night in captivity. The seventh individual (male) was ment. In particular we sought to determine how natural equipped with an external transmitter glued to the dorsal daily variation in thermal conditions inXuenced thermal skin, however, because this transmitter was dislodged biology, daily activity patterns and space use of these rock- within one day, data from this individual, with the excep- dwelling marsupials. P. macdonnellensis is a rare, small tion of body mass, are not included in analyses. After (»30 g), largely insectivorous, and supposedly nocturnal release animals were tracked/located at least once daily 123 J Comp Physiol B with manual receivers (Telonics TR4, with a Sirtrack fold- because such clumps were occasionally used as shelter ing Yagi antenna) to identify their exact location. Radio- sites, and at known basking sites (Ta bask) used in the morn- tracking commenced soon after sunrise (»0720 hours) and ing (AM, facing NE, n=3) and afternoon (PM, facing NW, well before (»3 h) basking commenced. We used transmit- n=3). Three Pseudantechinus (#1$, #1#, #2#) were ter signals to determine the approximate location of the ani- observed using these basking sites. Animals usually basked mals and then scanned the likely areas with binoculars to on rock surfaces and thus we placed iButtons at sites where determine when and where animals emerged from torpor basking was observed. Basking sites usually consisted of a sites to bask and at what Tb basking commenced. Pseu- narrow rock crevice or overhang that was exposed to the dantechinus entered torpor in rock crevices and caves and sun, but with close access to an underground crevice. Ta moved while still torpid from the sites they entered torpor was also measured in a shallow rock crevice (Ta crevice, 1 m to basking sites. Transmitter pulse rate was recorded manu- deep) and in rock crevices at the end of caves (Ta cave, 3 m ally and animals were observed with binoculars usually deep and 6 m deep) near the area where animals rested or several times/day; however, most continuous thermal data entered torpor as determined by radio-tracking (Table 1). were recorded at 10-min intervals with receiver/loggers Animals entered torpor in rock crevices that were <6 m (Körtner and Geiser 2000) for periods of 18–27 days (mean from basking sites, but transmitter signals indicated that 23 § 4 days, representing a total of 137 animal days). To torpor sites were often within »1 m of basking sites; we do maximise recording of continuous data from the small not know whether animals used nests. All iButtons were implanted transmitters, which had a short transmission wrapped in a sheet of white paper to minimise uptake of range, we employed more than one receiver/logger (usually radiant heat and to measure predominantly convective Ta. 2 near likely torpor sites) for each individual and frequently Obviously, Tas measured by black body devices, especially relocated the receiver/loggers especially in the early morn- at basking sites would have resulted in a further increase in ing when animals often had moved to a new resting/torpor Ta maxima than measured here, but these were not used site. because Pseudantechinus fur is light sandy brown. Data

The outside air Ta was measured at the study site to the were collected at hourly intervals with the exception of the nearest 0.5°C using data loggers (Thermochron, iButton, Ta in a 3-m cave, which was recorded in 2-h intervals over Dallas Semiconductor) placed 1 m above the ground in the the time of study, and at 4-h intervals over an entire year in shade. In addition, iButtons were used to measure Ta in the a 6-m cave (details in Table 1). Throughout the study centre of a 1.3 £ 1.5-m spinifex hummock (Ta Spinifex) period, the weather was sunny with the exception of a

Table 1 The thermal Mean § SD Minimum Maximum Date N environment of Pseudantechinus (°C) (°C) (°C) macdonnellensis

Ta (measured in shade) 12.6 § 5.8 2.0 24.0 14/06/01 to 10/07/01 659

Ta Spinifex 12.1 § 6.1 2.0 26.5 01/07/01 to 09/07/01 194 Morning basking sites

Ta bask #1# 18.8 § 7.1 8.0 34.5 05/07/01 to 09/07/01 92

Ta bask #2# 20.8 § 7.0 12.5 38.5 01/07/01 to 05/07/01 93

Ta bask #1$ 22.3 § 6.4 12.0 33.5 22/06/01 to 26/06/01 95 Afternoon basking sites

Ta bask #1# 18.7 § 6.8 10.0 38.5 05/07/01 to 09/07/01 84 T #2# 18.5 § 7.7 10.0 37.5 01/07/01 to 05/07/01 93 Ta was measured every hour a bask with the exception of Ta cave #2# Ta bask #1$ 17.1 § 10.8 5.0 39.5 26/06/01 to 01/07/01 122 3 m deep (every 2 h), and Ta cave Torpor sites #2$ cave 6 m deep measured § over a year (every 4 h). Distance Ta crevice 1 m deep 17.2 0.5 16.5 18.0 15/06/01 to 01/07/01 361 of temperature logger from cave Ta cave #2# 3 m deep 19.6 § 0.4 19.0 20.0 28/06/01 to 09/07/01 138 entrance is indicated in meters. Ta cave #2$ 6 m deep 19.5 § 0.8 17.5 21.0 01/07/01 to 09/07/01 193 T bask #1# indicates that this a T #2$ 6 m (year) 25.2 § 3.6 16.0 30.5 09/07/01 to 15/06/02 2047 basking site was used predomi- a cave nantly by this male, but occa- Ta cave #2$ 6m (WI) 20.1§ 3.5 16.0 25.5 09/07/01 to 31/08/01 406 sionally the same basking sites 01/06/02 to 15/06/02 V were used by di erent individu- Ta cave #2$ 6 m (SP) 23.7 § 1.9 17.5 27.5 01/09/01 to 30/11/01 545 als on diVerent days Ta cave #2$ 6m (SU) 27.7§ 1.5 24.0 30.5 09/07/01 to 15/06/02 512 WI winter, SP spring, SU sum- T #2$ 6 m (AU) 28.1 § 1.3 22.0 29.5 01/02/02 to 31/05/02 551 mer, AU autumn a cave 123 J Comp Physiol B single day, which was overcast early in the morning and Results then intermittently for much of the day. Numeric values presented are means § 1 standard devia- Torpor variables tion (SD) for the number of individuals ‘n’ investigated. ‘N’ denotes the number of observations. DiVerences Pseudantechinus employed torpor frequently in the Weld between means were determined using a t test; times were (Fig. 1). Torpor was characterised by a rapid fall of Tb from transformed to angular direction before testing (Zar 1984). values at or above »35°C, to Tb ranging from less than W Linear regressions (Ta as independent variable) were tted 20°C to just below 30°C. Typically after several hours at by using the method of least squares. When observed, ani- low Tb, torpid animals rewarmed and Tb rose to active val- mals were well coordinated immediately after release, and ues of at or above 35°C. The average torpor occurrence was movements were like those of non-tagged individuals seen 58.3 § 25.7% of animal days (n=6, N=131 animal days), basking and foraging at the study site, and did not appear to but females (82.5 § 13.4%, n=2) employed torpor almost be aVected by the transmitters. Nevertheless, we excluded twice as frequently as males (46.3 § 21.4%, n=4). Most day 1 after release (i.e. 2 days after surgery) from the data individuals (n=5) did not enter torpor on the Wrst day after analysis to ensure that behaviour was not aVected by sur- release. W gery. Torpor was de ned as a Tb < 30°C (Körtner and The duration of torpor bouts ranged from short bouts Geiser 2000); the duration of torpor bouts was deWned as lasting only for 50 min to a maximum of 855 min (14.25 h). the time with Tb < 30°C. Commencement of arousal was Most arousals occurred in the morning (Fig. 1) and the W de ned as the time when Tb began to increase from low tor- mean torpor bout duration was 350 § 139 min (n=6, por Tb to normothermic values; arousal completion as the N=46). Females (490 § 34 min, n=2, N=20) displayed W time when the normothermic plateau of Tb was rst reached longer torpor bouts (t test, t = 3.4, df =4, P<0.05) than (Fig. 1). More arousals than torpor entries were available males (280 § 111 min, n=4, N=26). for analysis because animals moved over night and loggers The minimum Tb, a measure of torpor depth, averaged were out of transmitter range during some torpor entries. over all torpor bouts was lower in females (Tb =21.0§ 1.5°C, n=2, N=30) than males (Tb = 26.8 § 1.3°C, n=4, N=27; t test, t = 4.7, df =4, P<0.01). The overall mean

minimum Tb was 24.8 § 3.2°C (n=6, N=57). The mean minimum Tb from the deepest torpor bout of each individual was 16.0 § 0.4°C in females (n=2, N=2) and 24.4 § 3.0°C in males (n=4, N=4) and these means also diVered 40 between sexes (t test, t = 5.5, df =4, P = 0.012). The single Tb lowest individual T was 15.7°C in a female and 20.4°C in a 35 b

) male. C ° (

30 e r u

t Torpor and the thermal environment

a 25 r e p

m 20 The thermal environment of Pseudantechinus was highly e T variable (Figs. 1, 2; Table 1). In Fig. 2, the outside T mea- y 15 a d X o Basking sured in the shade over 4 days in July uctuated from daily

B T bask 10 a minima of 6.3 § 1.8°C to maxima of 22.8 § 0.9°C. The Ta over the same time period of a morning (AM) basking 5 bask 12 24 12 24 12 24 12 24 12 24 site ranged from 14.4 § 1.9°C to 37.4 § 1.7°C, and that of 22 23 24 25 26 an afternoon (PM) basking site from 11.4 § 1.3°C to 35.5 § 1.8°C (Fig. 2). Thus, the T minima at basking Time and Date in June a bask sites were on average 5–8°C above the outside Ta. While Fig. 1 Body temperature (T , triangles) and ambient temperature at a b the maximum Ta bask was indistinguishable between morn- morning basking site (Ta bask, solid line) of an individual female Pseu- ing and afternoon basking sites, the time when the maxima dantechinus macdonnellensis measured over 4.5 days in June. The were reached diVered signiWcantly (t test, t = 8.3, df =5, horizontal broken line at 19.5°C indicates the mean Ta cave near a torpor site, which was higher than the minimum Tb on 3 of 4 days. The hori- P<0.001) for morning (Ta maximum at 1230 hours § zontal black and white bars indicate day and night. The arrow indicates 35 min) and afternoon (Ta maximum at 1545 hours § when the animal was observed basking with a body temperature of 32 min) basking sites (Fig. 2, Table 1). Moreover, the mean 25.3°C. Note the similar pattern of decreasing T after the fall of T b a bask daily amplitude of T (minimum T 13.3 § 1.3°C, at night and that of increasing Tb shortly after the increase in Ta bask in a bask a bask the morning on all days maximum Ta bask 32.9 § 0.5°C, amplitude 19.6°C) measured 123 J Comp Physiol B between 22 and 26 June (Fig. 1) was almost identical to that commenced at 0029 hours § 8 min and in males at 0240 of Tb (minimum Tb 17.2 § 0.9°C, maximum Tb 36.1 § hours § 0246 hours; these means were indistinguishable 0.5°C, amplitude 18.9°C) measured over the same time (t test, t = 1.4, df =4, P >0.2). period. Surprisingly, even the mean Ta bask (22.2 § 6.4°C) Arousal from all torpor bouts commenced at and the mean Tb (25.1 § 7.8°C) from 22 to 26 June were 0741 § 0340 hours (n=6, N=52), on average about similar (Fig. 1). In contrast, the cave Ta (Ta cave #2$ 6m 20 min after sunrise (»0721 hours). On average, males deep) near a resting site when our Weld measurements were began the arousal process earlier (0707 § 0433 hours, conducted was 19.5 § 0.2°C (range 17.5–21.0°C) and thus »15 min before sunrise) than females (0850 § 0116 hours, showed only small daily Xuctuations. The daily Xuctuations »90 min after sunrise), however, the means were statisti- of Ta Spinifex were similar to the outside Ta, but the maximum cally indistinguishable (t test, t = 0.7, df =4, P >0.5). Ta Spinifex was on average 2.5°C higher (Table 1). The longer Most arousals (81% of all arousals observed) com- term means of these and other Tas and the minima and max- menced in the morning after sunrise, with the exception of ima recorded are listed in Table 1. one male that always aroused at night (N=5), and a total of Pseudantechinus often rested and entered torpor in deep Wve arousals (N=5) by three other individuals. Post-sun- rock crevices, such as near the end of a cave (Fig. 2), where rise arousals commenced at 0943 hours § 50 min (n=5, thermal conditions were stable, therefore it is not surpris- N=42). These arousals began signiWcantly later (t test, ing that the daily minimum or maximum outside Ta did t = 4.1, df =6, P<0.01) than the start of the steepest Ta bask not strongly aVect occurrence of torpor. Overall, torpor increase at morning basking sites (0753 hours § 29 min, occurrence (dependent variable) of all individuals showed from Ta bask = 13.6 § 2.8°C, n=3, N=11). However, the a trend towards a correlation with the daily minimum and time of commencement of post-sunrise arousals was similar maximum outside Ta, but both regressions were not sig- (t test, t = 0.8, df =5, P > 0.4) to the time when the Ta bask at niWcant (r2 =0.14, P =0.085 and r2 =0.15, P =0.079, basking sites had reached the mid-point between minimum respectively). Moreover, variables of torpor (i.e. torpor and maximum values (1003 hours § 20 min, Ta bout duration and minimum Tb) were not correlated with bask = 22.3 § 2.5°C, n=4, N=11). The time when post- the daily minimum or maximum outside Ta. However, sunrise arousals commenced was correlated with both the 2 timing of torpor entry and especially that of arousals were time when Ta bask began to increase (r =0.34, P<0.005) 2 related to Ta bask at basking sites (Figs. 1, 2). Torpor usu- and the temperature of Ta bask at that time (r = 0.54, ally commenced around or soon after midnight (Fig. 1) P<0.001). The rewarming process was completed at W with a mean time of 0157 § 0228 hours (n=6, N=47) 1106 hours § 44 min (Tb » 35°C), which was signi cantly when Ta bask had substantially declined by 23.2°C from earlier (t test, t =2.8, df =5, P<0.05) than the time when maximum values to 13.8 § 2.2°C (n=6), which were the Ta bask at morning basking sites had reached the daily only 4.2 § 2.8°C above the nocturnal Ta bask minima of maximum (1213 hours § 27 min, Ta =31.2§ 5.5°C, 9.6 § 2.8°C (n=6) (Table 1). Torpor in the females n=4, N=11). Thus, post-sunrise arousals typically

occurred after basking sites were warmed to Ta > 20°C at »1000 hours (Figs. 1, 2) and were completed during the

40 time the Ta bask increased steeply, suggesting that many or T bask AM a all of these arousals involved basking. W Ta bask PM Direct evidence of basking came from observing ve 30 Pseudantechinus

) individual exposing themselves to the sun C °

( with a Tb < 30°C (e.g. Fig. 1, on 26 June). This was

e r T cave observed for 18% of all torpor bouts. The mean Tb when u a t

a 20 W

r torpid individuals were rst observed basking was e

p 27.5 § 1.6°C (n=5, N=14) at 1039 hours § 50 min, m

e somewhat later than the time arousals commenced. Basking T 10 in torpid individuals commenced earlier (t test, t =4.3,

Ta df =5, P<0.01) on sunny days (0947 hours § 42 min, n=4, N=11) than on the single cloudy day 0 1 2 3 4 5 6 (1136 hours § 12 min, n=3, N=3). The lowest Tb that July was observed in a basking individual was 19.3°C. After normothermic T of »35°C had been reached, Pseudante- Fig. 2 Ambient temperatures (Ta, circles), the cave temperature near b a torpor site (Ta cave, triangles), the ambient temperature at a morning chinus continued to bask for most of the afternoon. They W basking site (Ta bask AM, lled circles) and an afternoon basking site were also seen foraging during the day and continued to T solid line ( a bask PM, ) over 4 days in July forage for the Wrst, warmer (Figs. 1, 2) half of the night. 123 J Comp Physiol B

Discussion Our study provides further evidence that arousals from torpor in endotherms do not always rely entirely on endo- X Survival in deserts requires frugal use of energy and conse- thermic heat production, but rather use uctuations in Ta quently ectothermic reptiles with their low energy require- (Lovegrove et al. 1999; Chruszcz and Barclay 2002; Brice ments are the most common desert vertebrates (Bradshaw et al. 2002; Turbill et al. 2003; Dausmann et al. 2005; 2003). Our study suggests that by employing torpor and Geiser et al. 2004; Willis et al. 2006) or exposure to radiant basking and by appropriately coordinating its thermal biol- heat (Geiser et al. 2002, 2004; Mzilikazi et al. 2002; Brig- ogy to that of speciWc locations in their environment, the ham et al. 2006) to facilitate passive rewarming. As endo- endothermic arid zone dasyurid marsupial P. macdonnell- thermic rewarming from daily torpor requires a substantial ensis can minimise energy expenditure and thus also can increase in MR, often to about twice that during rest and live in this challenging environment. >10-fold of that during torpor (Geiser and Drury 2003), and Pseudantechinus in winter organise their daily activity, thus compromises energy savings gained from employing rest, and torpor phases and select sites with appropriate torpor, these Wndings are important for estimating energy thermal conditions for various functional states apparently expenditure in the wild. In S. macroura, another small to minimise daily energy expenditure. The occurrence of dasyurid marsupial from arid Australia, passive rewarming daily torpor on 82.5% of animal days we observed in in captivity via radiant heat can reduce energetic costs of females is well above that observed for free-ranging daily rewarming to only 15% of that required during active endo- heterotherms from mesic areas, however, data on the latter thermic rewarming because during much of the rewarming are currently scarce (Geiser et al. 2000; Körtner and Geiser process MR could be maintained below basal values 2000; Christian and Geiser 2007). Laboratory data show (Geiser and Drury 2003). Nevertheless, movement from that spontaneous daily torpor (food ad libitum) occurs pre- torpor sites to basking sites requires coordinated locomo- dominantly in small arid zone dasyurids (Sminthopsis spp., tion. We observed a torpid individual running up a vertical V Antechinomys laniger, Planigale gilesi) suggesting that in cli with a Tb of 19.3°C, which is remarkable for a mam- these species torpor is a strategy that is regularly employed mal, but in comparison to endothermic rewarming, locomo- to reduce daily energy expenditure (Geiser and Baudinette tion is associated with little energetic costs especially if 1987; Geiser 2003). In contrast, mesic dasyurids (Antechi- basking sites are near resting/torpor sites. nus spp.) mainly enter torpor after withdrawal of food Obviously, basking during the normothermic resting (induced torpor) (Geiser 1988, 2003), suggesting that in phase, as we observed in Pseudantechinus, also can con- these species, living in richer, more predictable environ- tribute to minimisation of energy expenditure. Even at low ments, daily torpor is used during acute energetic stress and Ta, radiant heat can maintain MR near basal levels and is predominantly an emergency strategy. reduce energy requirements by »50–80% (Ohmart and Pseudantechinus basked during rewarming from torpor Lasiewski 1971; Geiser and Drury 2003). Overall, it has when solar radiation was high and Ta was rising, continued been estimated that a combination of daily torpor and bask- to bask for much of the day and commenced foraging in ing during rewarming and rest can reduce daily energy the afternoon, which continued during the Wrst half of the expenditure of small mammals with a comparable daily night when Ta was relatively high (Fig. 2) and insects were thermal cycle and similar size as Pseudantechinus by about likely to be active (Speakman and Thomas 2003). Torpor 50% (Geiser et al. 2004), with resulting low food and thus entry commenced soon after midnight in thermally foraging requirements. Whereas this may appear moderate V bu ered rock crevices when outside Ta and Ta bask at bask- in comparison to energy saving made during hibernation, ing sites were low. Torpor usually lasted until the morning which generally reduces energy expenditure by >80% when torpid individuals returned again to basking sites (Wang 1989), species employing daily torpor, unlike most with increasing Ta bask and high radiant heat. Overall, the Tb hibernators who rely on stored fat or food, can forage of Pseudantechinus on days they entered torpor and the between torpor bouts and replenish fuels from external X Ta bask showed similar daily uctuations both in timing and resources (Geiser 2004). amplitude. While solar energy is used by Pseudantechinus during We did not observe basking during all arousals likely arousal from torpor and rest as an alternative source of because animals often basked in sun-exposed crevices energy in an environment with low primary productivity, along high vertical sandstone cliVs and were diYcult to the question remains as to why Pseudantechinus rewarm in approach and see. However, interrelations between Tb and the morning rather than staying torpid at even lower MR for Ta at basking sites and the »110-min delayed commence- longer and rewarm passively in the afternoon shortly before ment of basking during the single cloudy day in comparison their main activity phase. Arousals may occur in the morn- to the sunny days strongly suggest that most, if not all, post- ing for several reasons detailed below. (1) Even in winter, sunrise arousals did indeed involve basking. Pseudantechinus may need to avoid reptile predators such 123 J Comp Physiol B as varanid lizards (unpublished observations), which also Since our study was conducted during the beginning of the rewarm in the morning and forage only after they reach a reproductive season of the species (GilWllan 2001; McAllan high Tb when they could capture Pseudantechinus if these 2003), it is likely that males extended the period of activity were to rewarm in the afternoon and thus would not be fully in search of females or in territorial defence or vigilance coordinated. (2) Our study was conducted near the begin- (Buck and Barnes 1999). Deep and long torpor bouts by ning of the mating season of Pseudantechinus (GilWllan female dasyurids during the mating season and prior to par- 2001; McAllan 2003); rewarming in the morning may have turition and lactation have been interpreted as an energy allowed prolonged interactions with other individuals. (3) conserving strategy to enhance fat storage during mating Normothermic phases may facilitate capture of and diges- and especially pregnancy. During pregnancy female marsu- tion of food captured the previous night. Thus, while pas- pials require only little energy for growth of their small sive rewarming from torpor in the morning may not aVord (<0.5% body mass of mother) altricial young, and appar- all the energy savings of a longer torpor bout, energy ently therefore can aVord to enter torpor and store energy expenditure during basking is still low and allows animals that then can be consumed during the energy-demanding to undertake important daily activities. time of lactation (Geiser and Masters 1994). We observed

Although Tb during rewarming and the Ta bask at basking females and males sharing shelter and basking sites on sev- sites were tightly linked, the Tb minima observed during eral occasions supporting our interpretation that reproduc- V torpor were lower than the Ta cave measured in a cave near a tive behaviour may explain di erences in torpor patterns shelter where animals entered torpor on some days as deter- between the sexes. mined by radio-telemetry (Fig. 1). The Ta cave near the shel- Our study shows that the arid zone Pseudantechinus uses ter remained near 19.5°C throughout the period of torpor and basking during arousal from torpor and the rest measurement whereas the Tb of Pseudantechinus fell to a phase to lower energy expenditure. While this is likely to minimum of 15.7°C, and on 18% of occasions (all in have immediate positive eVects on survival, torpor use also females) the minimum Tb fell below 19.5°C. These low Tb appears to prolong life span (Wilkinson and South 2002), suggests that Pseudantechinus do not always select the which is important in a desert environment where reproduc- warmest available Ta during torpor as is often suggested tion may not be possible every year. Thus, torpor not only from laboratory studies, but rather select resting sites with a may contribute directly to the animal’s short-term survival, lower Ta, which likely are closer to the surface and nearer a but may also facilitate persistence of populations in the basking site, to further reduce Tb and thus minimise energy harsh and unpredictable Australian desert. expenditure during torpor as has been observed in bats and echidnas (Brown and Bernard 1994; Nicol and Andersen Acknowledgments We thank Michael Barritt, Silke Beckedorf, Nic- 2007). A reduction of T by a further 4°C below the avail- ola Goodship, Karen May, and Parks and Wildlife Service of the b Northern Territory staV based at Ormiston for assistance and logistic able shelter Ta cave of 19.5°C should result in a MR reduc- support during the study. Mark Brigham and Bronwyn McAllan pro- tion by »40% assuming a mean Q10 of 2.3 for daily vided constructive comments on the manuscript. The Animal Ethics heterotherms (Geiser 2004). Thus, it appears that even dur- Committee of the University of New England and the Parks and Wild- ing torpor, when MR is already substantially reduced, life Service of the Northern Territory provided permits for the study. The research was supported by grants from the Australian Research Pseudantechinus attempt to further minimise energy expen- Council and The University of New England. diture on some days in winter. On the other hand in the warm season, the Ta cave was near the lower critical Ta of the thermo-neutral zone of Pseudantechinus (lower critical References Ta = 30.1°C, MacMillen and Nelson 1969; mean Ta cave: 27.7°C summer, 28.1°C autumn), suggesting that for much Brice PH, Grigg GC, Beard LA, Donovan JA (2002) Patterns of activ- of the year the species can live without heat stress under ity and inactivity in echidnas (Tachyglossus aculeatus) free-ranging in a hot dry climate: correlates with ambient temperature, time conditions approximating thermo-neutrality and therefore of day and season. Aust J Zool 50:461–475 should require little energy for thermoregulation. It would Brigham RM, Woods CP, Lane JE, Fletcher QE, Geiser F (2006) Eco- be interesting to determine whether even under these appar- logical correlates of torpor use among Wve caprimulgiform birds. ently favourable thermal conditions Pseudantechinus In: Proceedings, 23rd international ornithological congress, Acta Zool Sin 52(Suppl):401–404 employ torpor to further minimise energy expenditure and Buck CL, Barnes BM (1999) Temperatures of hibernacula and changes how the daily activity patterns change in the hot season. in body composition of arctic ground squirrels over winter. J Male and female Pseudantechinus showed similar daily Mammal 80:1264–1276 cycles in T Xuctuations, but some diVerences with regard Bradshaw D (2003) Vertebrate ecophysiology. Cambridge University b Press, UK to timing of torpor and arousal and torpor depth emerged. Brown CR, Bernard RTF (1994) Thermal preference of Schreiber’s On average, males entered torpor about 2 h later than long-Wngered (Miniopterus schreibersii) and Cape horseshoe (Rhi- females and aroused about 15 min earlier than females. nolophus capensis) bats. Comp Biochem Physiol 107A:439–499 123 J Comp Physiol B

Christian N, Geiser F (2007) To use or not to use torpor? Activity and Gutman R, Choshniak I, Kronfeld-Schor N (2006) Defending body body temperature as predictors. Naturwissenschaften 94:483–487 mass during food restriction in Acomys russatus: a desert rodent Chruszcz BJ, Barclay RMR (2002) Thermoregulatory ecology of a sol- that does not store food. Am J Physiol 290:R881–R891 itary bat, Myotis evotis, roosting in rock crevices. Funct Ecol Körtner G, Geiser F (2000) Torpor and activity patterns in free-ranging 16:18–26 sugar gliders Petaurus breviceps (Marsupialia). Oecologia Cooper CE, McAllan BM, Geiser F (2005) EVect of torpor on the water 123:350–357 economy of an arid-zone marsupial, the striped-faced dunnart Lovegrove BG, Körtner G, Geiser F (1999) The energetic costs of (Sminthopsis macroura). J Comp Physiol B 175:323–328 arousal from torpor in the marsupial Sminthopsis macroura: ben- Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation eWts of summer ambient temperature cycles. J Comp Physiol B in the tropics: lessons from a primate. J Comp Physiol B 175:147– 169:11–18 155 MacMillen RE, Nelson JE (1969) Bioenergetics and body size in Dickman CR (2003) Distributional ecology of dasyurid marsupials. In: dasyurid marsupials. Am J Physiol 217:1246–1251 Jones M, Dickman C, Archer M (eds) Predators with pouches: the MacMillen RE, Hinds D (1983) Water regulatory eYciency in het- biology of carnivorous marsupials. CSIRO publishers, Mel- eromyid rodents: a model and its application. Ecology 64:152– bourne, pp 318–331 164 Dickman CR, Haythornthwaite AS, McNaught GH, Mahon P, Tamayo McAllan BM (2003) Timing of reproduction in carnivorous marsupi- B, Letnic M (2001) Population dynamics of three species of als. In: Jones M, Dickman C, Archer M (eds) Predators with dasyurid marsupials in arid central Australia: a 10-year study. pouches: the biology of carnivorous marsupials. CSIRO publish- Wildl Res 28:493–506 ers, Melbourne, pp 147–168 Frank CL (1994) Polyunsaturate content and diet selection by ground Menkhorst P, Knight F (2001) A Weld guide to the mammals of Aus- squirrels (Spermophilus lateralis). Ecology 75:458–463 tralia. Oxford University Press, Melbourne Geiser F (1988) Daily torpor and thermoregulation in Antechinus Mzilikazi N, Lovegrove BG, Ribble DO (2002) Exogenous passive (Marsupialia): inXuence of body mass, season, development, heating during torpor arousal in free-ranging elephant shrews, El- reproduction, and sex. Oecologia 77:395–399 ephantulus myurus. Oecologia 133:307–314 Geiser F (2003) Thermal biology and energetics of carnivorous marsu- Nicol SC, Andersen NA (2007) Cooling and body temperature regula- pials. In: Jones M, Dickman C, Archer M (eds) Predators with tion of hibernating echidnas (Tachyglossus aculeatus). J Exp Biol pouches: the biology of carnivorous marsupials. CSIRO publish- 210:586–592 ers, Melbourne, pp 234–249 Ohmart RD, Lasiewski RC (1971) Roadrunners: energy conservation Geiser F (2004) Metabolic rate and body temperature reduction during by hypothermia and absorption of sunlight. Science 172:67–69 hibernation and daily torpor. Annu Rev Physiol 66:239–274 Pavey CR, Goodship N, Geiser F (2003) Home range and spatial orga- Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoreg- nization of the rock-dwelling carnivorous marsupial, Pseudante- ulation in three dasyurid marsupials. J Comp Physiol B 157:335– chinus macdonnellensis. Wildl Res 30:135–142 344 Schmidt-Nielsen K (1979) Desert animals. Dover Publications, New Geiser F, Masters P (1994) Torpor in relation to reproduction in the York Mulgara, Dasycercus cristicauda (Dasyuridae: Marsupialia). J Speakman JR, Thomas DW (2003) Physiological ecology and energet- Therm Biol 19:33–40 ics of bats. In: Kunz TH, Fenton MB (eds) Bat ecology. Univer- Geiser F, Drury RL (2003) Radiant heat aVects thermoregulation and sity of Chicago Press, Chicago, pp 430–490 energy expenditure during rewarming from torpor. J Comp Phys- StaVord Smith DM, Morton SR (1990) A framework for the ecology of iol B 173:55–60 arid Australia. J Arid Environ 18:255–278 Geiser F, Goodship N, Pavey CR (2002) Was basking important in the Trewin B (2006) Australian deserts, climatic aspects of Australia’s evolution of mammalian endothermy? Naturwissenschaften deserts. In: 2006 year book Australia, Australian Bureau of Statis- 89:412–414 tics, Canberra Geiser F, Holloway JC, Körtner G, Maddocks TA, Turbill C, Brigham Turbill C, Law BS, Geiser F (2003) Summer torpor in a free-ranging RM (2000) Do patterns of torpor diVer between free-ranging and bat from subtropical Australia. J Therm Biol 28:223–226 captive mammals and birds? In: Heldmaier G, Klingenspor M Wang LCH (1989) Ecological, physiological, and biochemical aspects (eds) Life in the cold: 11th international hibernation symposium. of torpor in mammals and birds. In: Wang LCH (ed) Animal Springer, Berlin, pp 95–102 adaptation to cold. Springer, Berlin, pp 361–401 Geiser F, Drury RL, Körtner G, Turbill C, Pavey CR, Brigham RM Warnecke L, Turner JM, Geiser F (2007) Torpor and basking in a small (2004) Passive rewarming from torpor in mammals and birds: arid zone marsupial. Naturwissenschaften (in press) energetic, ecological and evolutionary implications. In: Barnes Wilkinson GS, South SM (2002) Life history, ecology and longevity of BM, Carey HV (eds) Life in the cold: evolution, mechanisms, bats. Ageing Cell 1:124–131 adaptation, and application. 12th international hibernation sym- Willis CKR, Brigham RM, Geiser F (2006) Deep, prolonged torpor by posium. Biological Papers of the University of Alaska #27. Insti- pregnant, free-ranging bats. Naturwissenschaften 93:80–83 tute of Arctic Biology, University of Alaska, Fairbanks, pp 51–62 Withers PC (1992) Comparative animal physiology. Saunders, Fort GilWllan SL (2001) An ecological study of a population of Pseudante- Worth chinus macdonnellensis (Marsupialia: Dasyuridae) in central Zar JH (1984) Biostatistical analysis. 2nd edn. Prentice Hall, Engle- Australia. I. Invertebrate food supply, diet and reproductive strat- wood CliVs egy. Wildl Res 28:469–480

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