Daily torpor in elephant shrews (Macroscelidea: Elephantulus spp.) in response to food deprivation

Patterns of daily torpor were measured in response to photoperiod and food restriction at a constant temperature (18 °C) in two species of elephant shrew (Macroscelidea), Elephantulus rozeti (from Morocco) and Elephantulus myurus (from southern Africa). Body temperature was monitored continuously for ca. 3 months using temperature-sensitive telemeters. Under short photoperiods (8:16 L:D), both species entered spontaneous torpor on an ad libitum diet, but showed a higher frequency of induced torpor when food was restricted. Under long photoperiods (16:8 L:D), E. myurus could be induced to enter daily `summer' torpor. A total of 378 torpor bouts were measured, none of which were longer in duration than 18 h. Under short photoperiods, arousal from torpor was associated with the onset of the photoperiod, whereas the time of entry was variable throughout the scotophase. However, E. myurus tended to phase shift torpor from the photophase to the scotophase under long photoperiods, despite displaying weak circadian amplitudes of body temperature indicative of a photophase rest phase. Both species lacked well-defined circadian amplitudes of body temperature, a pattern thought to be associated with polyphasic activity cycles characteristic of several Elephantulus species. It was concluded that these and other patterns of torpor shown by Elephantulus show similarities with other small Afrotropical insectivores inhabiting semi-arid habitats or unpredictable environments. Accepted: 26 July 2000     

Effect of low-quality diet on torpor frequency and depth in the pichi Zaedyus pichiy (Xenarthra,Dasypodidae), a South American armadillo

Daily torpor is a physiological adaptation that allows mammals to cope with energetic challenges associated with unpredictable periods of food shortage. We experimentally tested whether food quality influences torpor frequency and depth in the pichi (Zaedyus pichiy), a small, opportunistically omnivorous armadillo endemic to arid and semi-arid habitats of southern South America. We recorded body temperature (T_sc) changes in 10 semi-captive, adult female pichis using dataloggers implanted subcutaneously during periods of 21 days. All individuals entered spontaneous daily torpor, but those receiving a low-quality diet had significantly lower daily mean and minimum T_sc, spent more time at T_sc below their individual lower limit of normothermia, and had a higher Heterothermy Index than controls. Five individuals entered prolonged torpor bouts lasting more than 24 h, two of them repeatedly. Nine out of ten prolonged torpor bouts occurred in individuals feeding on a low-quality diet, suggesting that pichis are able to enter prolonged periods of torpor during severe environmental stress. In combination with their ability to hibernate and to respond to a reduced insect abundance by ingesting other food items, this physiological adaptation allows pichis to better cope with food shortages and a more extreme climate than other armadillos. It may explain why Z. pichiy naturally occurs farther south than any other armadillo species.     

Daily torpor and hibernation in birds and mammals

Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (～35°) than daily heterotherms (～25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ～13°C, and the mean minimum torpor metabolic rate was ～35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.     

Adjusting energy expenditures to energy supply: food availability regulates torpor use and organ size in the Chilean mouse-opossum <Emphasis Type="Italic">Thylamys elegans</Emphasis>

We studied how food abundance and consumption regulates torpor use and internal organ size in the Chilean mouse-opossum Thylamys elegans (Dielphidae), a small nocturnal marsupial, endemic in southern South America. We predicted that exposure to food rations at or above the minimum energy levels necessary for maintenance would not lead to any signs of torpor, while reducing food supply to energy levels below maintenance would lead to marked increases in frequency, duration and depth of torpor bouts. We also analyzed the relationship between food availability and internal organ mass. We predicted a positive relationship between food availability and internal organ size once the effect of body size is removed. Animals were randomly assigned to one of two groups and fed either 70, 100 or 130% of their daily energy requirement (DER). We found a positive and significant correlation between %DER and body temperature, and also between %DER and minimum body temperature. In contrast, for torpor frequency, duration and depth, we found a significant negative correlation with %DER. Finally, we found a significant positive correlation between the %DER and small intestine and ceacum dry mass. We demonstrate that when food availability is limited, T. elegans has the capacity to reduce their maintenance cost by two different mechanisms, that is, increasing the use of torpor and reducing organ mass.     

Daily torpor and thermoregulation in antechinus (Marsupialia): influence of body mass,season, development,reproduction, and sex

Summary Season and body mass influence torpor in mammals. However, the effects of the two factors are often difficult to distinguish because body mass in many species changes with season. The present study attempted to separate seasonal and body mass related alterations of torpor. Adult female Antechinus stuartii and A. flavipes (Marsupialia), which were about half the size of males of the respective species, showed longer and deeper torpor than males. When the two species were compared, torpor in A. stuartii, the smaller species, was more pronounced than in A. flavipes. Juveniles of both species had lower body temperatures and longer torpor durations than adults. Torpor was most pronounced in juvenile males during summer; in winter, when males had grown to adult size, the use of torpor was reduced. Seasonal changes in torpor of adults were not distinct. These results suggest that the influence of body mass on torpor in these Antechinus species is stronger than that of season.     

Heterothermy in elephant shrews, Elephantulus spp. (Macroscelidea): daily torpor or hibernation?

The physiological parameters of heterothermy (e.g. minimum body temperature and oxygen consumption, percentage metabolic reduction, and bout length) were measured in two species of Elephantulus elephant shrews (Elephantulus myurus and Elephantulus rozeti; Macroscelidea) as a function of ambient temperature. Both species displayed deep torpor whereby the body temperatures of ca. 5 °C and oxygen consumption as low as 2% of basal metabolic rate were attained. Torpor bout length (n=57 bouts) never exceeded 24 h. These data are characteristic of both hibernation (minimum body temperature and metabolism) and daily torpor (bout length), and argue that these two physiological responses may not necessarily have separate evolutionary origins. Accepted: 26 July 2000     

Heterothermy in an Australian passerine, the Dusky Woodswallow (Artamus cyanopterus)

Information regarding passerine heterothermy and torpor is scant, although many species are small and must cope with a fluctuating food supply and presumably would benefit from energy savings afforded by torpor. We studied whether insectivorous Dusky Woodswallows (Artamus cyanopterus; ∼35 g) enter spontaneous torpor (food ad libitum) when held outdoors as a pair in autumn/winter. Woodswallows displayed pronounced and regular daily fluctuations in body temperature (T _b) over the entire study period. The mean T _b ranged from ∼39°C to 40°C (photophase, day time) and ∼33°C to 36°C (scotophase, night time). However, on 88% of bird nights, nocturnal T _b minima fell to < 35°C. The lowest T _b observed in air was 29.2°C. However, when a bird fell into water its T _b dropped further to ∼22°C; this T _b was regulated for several hours and the bird survived. Our observations suggest that heterothermy is a normal part of the daily thermal regime for woodswallows to minimise energy expenditure. Spontaneous nocturnal torpor in captive woodswallows suggests that torpor in the wild may be more pronounced than recorded here because free-living birds are likely challenged by both low food availability and adverse weather.     

Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance

Patterns and energetic consequences of spontaneous daily torpor were measured in the gray mouse lemur (Microcebus murinus) under natural conditions of ambient temperature and photoperiod in a dry deciduous forest in western Madagascar. Over a period of two consecutive dry seasons, oxygen consumption (VO₂) and body temperature (T _b) were measured on ten individuals kept in outdoor enclosures. In all animals, spontaneous daily torpor occurred on a daily basis with torpor bouts lasting from 3.6 to 17.6 h, with a mean torpor bout duration of 9.3 h. On average, body temperatures in torpor were 17.3±4.9°C with a recorded minimum value of 7.8°C. Torpor was not restricted to the mouse lemurs’ diurnal resting phase: entries occurred throughout the night and arousals mainly around midday, coinciding with the daily ambient temperature maximum. Arousal from torpor was a two-phase process with a first passive, exogenous heating where the T _b of animals increased from the torpor T _b minimum to a mean value of 27.1°C before the second, endogenous heat production commenced to further raise T _b to normothermic values. Metabolic rate during torpor (28.6±13.2 ml O₂ h^–1) was significantly reduced by about 76% compared to resting metabolic rate (132.6±50.5 ml O₂ h^–1). On average, for all M. murinus individuals measured, hypometabolism during daily torpor reduced daily energy expenditure by about 38%. In conclusion, all these energy-conserving mechanisms of the nocturnal mouse lemurs, with passive exogenous heating during arousal from torpor, low minimum torpor T _bs, and extended torpor bouts into the activity phase, comprise an important and highly adapted mechanism to minimize energetic costs in response to unfavorable environmental conditions and may play a crucial role for individual fitness. Received: 8 July 1999 / Accepted: 3 December 1999     

Torpor patterns in the pouched mouse (Saccostomus campestris ; Rodentia): a model animal for unpredictable environments

Patterns of spontaneous and induced daily torpor were measured in the Afrotropical pouched mouse (77–115?g), Saccostomus campestris, in response to photoperiod, temperature, and food deprivation, using temperature telemetry. Photoperiod had no influence on the incidence, depth, or duration of daily torpor in either males and females. Although the testis size index decreased in response to food deprivation and photoperiod by a maximum of 24%, full testis regression did not occur. Torpor bout duration was, on average, 5.3?h, independent of photoperiod and ambient temperature. Males did not enter torpor in response to food deprivation but did in response to low ambient temperature, though significantly less frequently than females. At normothermia, the body temperatures (daily minimum, mean, maximum) of males were significantly lower than those of females. Minimum body temperatures of both males and females during torpor did not fall below 20?°C at an ambient temperature of 15?°C. The patterns of torpor measured here differ from those observed in species from strongly seasonal environments. They suggest adaptation to an environment rendered unpredictable by the El Niño Southern Oscillations. As an aseasonal, opportunistic breeder capable of year-round adaptive hypothermia, the pouched mouse represents an excellent model animal for research on physiological and behavioral adaptations to unpredictable environments.     

Summer heterothermy in Rafinesque’s big-eared bats (Corynorhinus rafinesquii) roosting in tree cavities in bottomland hardwood forests

Many small mammals are heterothermic endotherms capable of maintaining an elevated core body temperature or reducing their thermoregulatory set point to enter a state of torpor. Torpor can confer substantial energy savings, but also incurs ecological costs, such as hindering allocation of energy towards reproduction. We placed temperature-sensitive radio transmitters on 44 adult Rafinesque’s big-eared bats (Corynorhinus rafinesquii) and deployed microclimate dataloggers inside 34 day roosts to compare the use of torpor by different sex and reproductive classes of bats during the summer. We collected 324 bat-days of skin-temperature data from 36 females and 4 males. Reproductive females employed fewer torpor bouts per day than non-reproductive females and males (P < 0.0001), and pregnant and lactating females had higher average (P < 0.0001) and minimum (P < 0.0001) skin temperatures than non-reproductive females. Pregnant females spent less time torpid (P < 0.0001) than non-reproductive females, but lactating females used relatively deep, long torpor bouts. Microclimates varied inside tree species with different configurations of entrances to the roost cavity (P < 0.0001). Bats spent more time torpid when roosting in water tupelo (Nyssa aquatica) trees possessing only a basal entrance to the cavity (P = 0.001). Of the tree species used as roosts, water tupelo cavities exhibited the least variable daytime and nighttime temperatures. These data demonstrate that use of summer torpor is not uniform among sex and reproductive classes in Rafinesque’s big-eared bat, and variation in microclimate among tree roosts due to species and structural characteristics facilitates the use of different thermoregulatory strategies in these bats.     

The impact of dietary fats,photoperiod, temperature and season on morphological variables,torpor patterns,and brown adipose tissue fatty acid composition of hamsters,Phodopus sungorus

We investigated how dietary fats and oils of different fatty acid composition influence the seasonal change of body mass, fur colour, testes size and torpor in Djungarian hamsters, Phodopus sungorus, maintained from autumn to winter under different photoperiods and temperature regimes. Dietary fatty acids influenced the occurrence of spontaneous torpor (food and water ad libitum) in P. sungorus maintained at 18°C under natural and artificial short photoperiods. Torpor was most pronounced in individuals on a diet containing 10% safflower oil (rich in polyunsaturated fatty acids), intermediate in individuals on a diet containing 10% olive oil (rich in monounsaturated fatty acids) and least pronounced in individuals on a diet containing 10% coconut fat (rich in saturated fatty acids). Torpor in P. sungorus on chow containing no added fat or oil was intermediate between those on coconut fat and olive oil. Dietary fatty acids had little effect on torpor in animals maintained at 23°C. Body mass, fur colour and testes size were also little affected by dietary fatty acids. The fatty acid composition of brown fat from hamsters maintained at 18°C and under natural photoperiod strongly reflected that of the dietary fatty acids. Our study suggests that the seasonal change of body mass, fur colour and testes size are not significantly affected by dietary fatty acids. However, dietary fats influence the occurrence of torpor in individuals maintained at low temperatures and that have been photoperiodically primed for the display of torpor.Abbreviations BAT brown adipose tissue - bm body mass - FA fatty acid(s) - MR metabolic rate - MUFA monounsaturated fatty acid(s) - PUFA polyunsaturated fatty acid(s) - SFA saturated fatty acid(s) - T _a air temperature - T _b body temperature - T_s body surface temperature(s) - TNZ thermoneutral zone - UFA unsaturated fatty acid(s)     

Interactive effects of temperature and photoperiod on the daily activity and energy metabolism of pouched mice (Saccostomus campestris: Cricetidae) from southern Africa

The daily activity and energy metabolism of pouched mice (Saccostomus campestris) from two localities in southern Africa was examined following warm (25 °C) and cold (10 °C) acclimation under long (LD 14:10) and short (LD 10:14) photoperiol. There was no differential effect of photoperiod on the daily activity or metabolism of pouched mice from the two localities examined, which suggests that reported differences in photoresponsivity between these two populations were not the result of differences in daily organisation. Neverthe-less, there was a significant increase in metabolism at 10 °C, irrespective of photoperiod, even though seven cold-acclimated animals displayed bouts of spontaneous torpor and saved 16.4–36.2% of their daily energy expenditure. All but one of these bouts occurred under short photoperiod, which suggests that short photoperiod facilitated the expression of torpor and influenced the daily energy metabolism of these individuals. As expected for a noctureal species, the amount of time spent active increased following acclimation to short photoperiod at 25 °C. However, there was a reduction in mean activity levels under short photoperiod at 10 °C, possibly because the stimulation of activity by short photoperiod was masked by a reduction in activity during bouts of spontaneous torpor. Cold temperature clearly had an overriding effect on the daily activity and metabolism of this species by necessitating an increase in metabolic heat production and eliciting spontaneous torpor which overrode the effect of short photoperiod on activity at an ambient temperature of 10 °C.Abbreviations 3-ANOVA three-way analysis of variance - %ACT percentage of time spent active - ADMR average daily metabolic rate - M _b body mass - MR metabolic rate - MR_dark metabolic rate recorded during the dark phase - MR_light metabolic rate recorded during the light phase - NST non-shivering thermogenesis - RQ respiratory quotient - STPD standard temperature and pressure, dry - T _a ambient temperature - T _b body temperature - VO₂ oxygen consumption     

Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition?

Summary The present study addresses the controversy of whether the reduction in energy metabolism during torpor in endotherms is strictly a physical effect of temperature (Q₁₀) or whether it involves an additional metabolic inhibition. Basal metabolic rates (BMR; measured as oxygen consumption, ), metabolic rates during torpor, and the corresponding body temperatures (T _b) in 68 mammalian and avian species were assembled from the literature (n=58) or determined in the present study (n=10). The Q₁₀ for change in between normothermia and torpor decreased from a mean of 4.1 to 2.8 with decreasingT _b from 30 to <10°C in hibernators (species that show prolonged torpor). In daily heterotherms (species that show shallow, daily torpor) the Q₁₀ remained at a constant value of 2.2 asT _b decreased. In hibernators with aT _b<10°C, the Q₁₀ was inversely related to body mass. The increase of mass-specific metabolic rate with decreasing body mass, observed during normothermia (BMR), was not observed during torpor in hibernators and the slope relating metabolic rate and mass was almost zero. In daily heterotherms, which had a smaller Q₁₀ than the hibernators, no inverse relationship between the Q₁₀ and body mass was observed, and consequently the metabolic rate during torpor at the sameT _b was greater than that of hibernators. These findings show that the reduction in metabolism during torpor of daily heterotherms and large hibernators can be explained largely by temperature effects, whereas a metabolic inhibition in addition to temperature effects may be used by small hibernators to reduce energy expenditure during torpor.Abbreviation BMR basal metabolic rate     

Physiological ecology of cheirogaleid primates: variation in hibernation and torpor

Torpor (i.e. the reduction of body temperature and metabolic rate for less than 24 h) and hibernation (i.e. torpor phases longer than 24 h) are among the most extreme adaptations to seasonality in primate habitats. Although widespread among mammals, this form of extreme thermoregulation is rare among primates and is reported only for species of the cheirogaleid family. Understanding their physiological ecology is crucial for many aspects of cheirogaleid socioecology like their social organization and their mating systems. This paper first provides an overview of published information on hibernation and torpor and identifies a patchy distribution for the occurrence of hibernation across genera, species and populations. Based on a review of published studies from the wild and from captivity, we then propose a possible explanation for variation in hibernation behavior among Microcebus species and populations. Accordingly, the amount of energy that can be saved during torpor early in the lean dry season, which is determined by the minimum ambient temperature will be decisive. Only where temperatures are low, early dry season torpor bouts will be long enough to save enough energy to build up fat reserves for longer bouts of hibernation. Finally, we summarize information on the causal factors for the occurrence of hibernation by analyzing sex differences within populations. Further physiological studies on other cheirogaleid species are needed to identify the phylogenetic origin of hibernation in primates.     

Thermal physiology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi

During roosting in summer, reproductive female bats appear to use torpor less frequently and at higher body temperatures (T _b) than male bats, ostensibly to maximise offspring growth. To test whether field observations result from differences in thermal physiology or behavioural thermoregulation during roosting, we measured the thermoregulatory response and energetics of captive pregnant and lactating female and male long-eared bats (Nyctophilus geoffroyi 8.9 g and N. gouldi 11.5 g) during overnight exposure to a constant ambient temperature (T _a) of 15°C. Bats were captured 1–1.5 h after sunset and measurements began at 21:22±0:36 h. All N. geoffroyi entered torpor commencing at 23:47±01:01 h. For N. gouldi, 10/10 males, 9/10 pregnant females and 7/8 lactating females entered torpor commencing at 01:10±01:40 h. The minimum T _b of torpid bats was 15.6±1.1°C and torpid metabolic rate (TMR) was reduced to 0.05±0.02 ml O₂ g⁻¹ h⁻¹. Sex or reproductive condition of either species did not affect the timing of entry into torpor (F=1.5, df=2, 19, P=0.24), minimum TMR (F=0.21, df=4, 40, P=0.93) or minimum T _b (F=0.76, df=5, 41, P=0.58). Moreover, sex or reproductive condition did not affect the allometric relationship between minimum resting metabolic rate and body mass (F=1.1, df=4, 37, P=0.37). Our study shows that under identical thermal conditions, thermal physiology of pregnant and lactating female and male bats are indistinguishable. This suggests that the observed reluctance by reproductive females to enter torpor in the field is predominantly because of ecological rather than physiological differences, which reflect the fact that females roost gregariously whereas male bats typically roost solitarily.     

The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura : benefits of summer ambient temperature cycles

The costs of arousal from induced torpor were measured in the striped-faced dunnart (Sminthopsis macroura; ca. 25 g) under two experimental ambient temperature cycles. The sinusoidal-type temperature cycles were designed to evaluate the effects of passive, ambient temperature heating during arousal from torpor in these insectivorous marsupials. It was hypothesised that diel ambient temperature cycles may offer significant energy savings during arousal in animals that employ daily torpor in summer as a response to unpredictable food availability. The cost of arousal in animals in which passive, exogenous heating occurred was significantly lower than that in animals not exposed to an ambient temperature cycle. The total cost of all three phases of torpor (entry, maintenance and arousal) was almost halved when animals were exposed to an ambient heating cycle from 15 °C to 25 °C over a 24-h period. In all animals, irrespective of the experimental ambient temperature cycle employed, the minimum torpor body temperature was 17–18 °C. The body temperature (T_b) of animals exposed to exogenous heating increased from the torpor T_b minimum to a mean value of 22.59 °C before endogenous heat production commenced. This relatively small increase in T_b of ca. 5 °C through `free' passive heating was sufficient to account for the significant ca. three-fold decrease in the cost of arousal and may represent an important energetic aid to free-ranging animals. Accepted: 4 October 1998     

The effect of temperature on the pattern of torpor in a marsupial hibernator

Physiological variables of torpor are strongly temperature dependent in placental hibernators. This study investigated how changes in air temperature affect the duration of torpor bouts, metabolic rate, body temperature and weight loss of the marsupial hibernator Burramys parvus (50 g) in comparison to a control group held at a constant air temperature of 2°C. The duration of torpor bouts was longest (14.0±1.0 days) and metabolic rate was lowest (0.033±0.001 ml O₂·g^-1·h^-1) at2°C. At higher air temperatures torpor bouts were significantly shorter and the metabolic rate was higher. When air temperature was reduced to 0°C, torpor bouts also shortened to 6.4±2.9 days, metabolic rate increased to about eight-fold the values at 2°C, and body temperature was maintained at the regulated minimum of 2.1±0.2°C. Because air temperature had such a strong effect on hibernation, and in particular energy expenditure, a change in climate would most likely increase winter mortality of this endangered species.Abbreviationst STP standard temperature and pressure - T _a air temperature - T _b body temperature - VO₂ rate of oxygen consumption     

Seasonality of torpor and thermoregulation in three dasyurid marsupials

Summary Seasonal variation in the pattern of torpor and temperature regulation was investigated in the closely related arid zone dasyurid marsupialsSminthopsis crassicaudata (17 g),S. macroura (24 g), andDasyuroides byrnei (120 g). The tendency to enter torpor was greater, torpor commenced earlier, torpor duration was longer, and body temperatures (T _b) were lower inSminthopsis spp. than inD. byrnei. The minimum mass-specific rate of oxygen consumption ( ) of torpid animals was similar among the three species despite the differences in minimumT _b. The mass-specific oxygen consumption of normothermic animals was reduced during winter when compared with the summer values in all species, but there was no seasonal variation in normothermicT _b in any species. The tendency to enter torpor was incrased during winter. TorpidSminthopsis spp. had lower values ofT _b and during winter than during summer;D. byrnei did not show seasonal changes in these variables. These results suggest that seasonal changes in the pattern of thermoregulation and torpor in small dasyurids may be more distinct than in larger species.Abbreviations RMR resting metabolic rate - BMR basal metabolic rate