Daily torpor in relation to photoperiod in a subtropical blossom-bat, Syconycteris australis (Megachiroptera)

Daily torpor in many temperate-zone mammals is affected by photoperiod. As little is known about the effects of photoperiod on torpor in subtropical species, we investigated whether, and if so how, torpor use, duration, and depth are affected by acclimation to three photoperiods (short, intermediate, long) in the blossom-bat Syconycteris australis. In contrast to many other studies, torpor occurrence, duration, and depth did not significantly respond to photoperiod acclimation in S. australis. Interestingly, the trend of a decline in torpor use under long photoperiod was the opposite of that observed previously in S. australis, which had been captured from the wild in summer and winter. Our study suggests that some species living in low latitude areas with unpredictable weather like S. australis may not use photoperiod for seasonal adjustments in physiology because it is not a reliable cue for food availability.     

Seasonal changes in energetics and torpor patterns in the subtropical blossom-bat Syconycteris australis (Megachiroptera)

Little is known about how animals from tropical and subtropical climates adjust their energy expenditure to cope with seasonal changes of climate and food availability. To provide such information, we studied the thermal physiology, torpor patterns and energetics of the nocturnal blossom-bat (Syconycteris australis 18 g) from a subtropical habitat in both summer and winter. In both seasons, S. australis frequently entered daily torpor at ambient temperatures between 12 and 25°C when food and water were withheld. Unlike patterns observed in temperate animals, mean minimum metabolic rates during torpor were lower in summer (0.47 ± 0.07 ml O₂ g⁻¹ h⁻¹) than in winter (0.75 ± 0.11 ml O₂ g⁻¹ h⁻¹). Body temperatures during torpor were regulated at 19.3 ± 1.0°C in summer and at 23.4 ± 2.0°C in winter. Torpor bout duration was significantly longer in summer (7.3 ± 0.6 h) than in winter (5.5 ± 0.3 h), but in both seasons, bout duration was not affected by ambient temperature. Consequently, average daily metabolic rates were also significantly lower in summer than in winter. Body temperatures and metabolic rates in normothermic bats did not change with season. Our findings on seasonal changes of torpor in this bat from the subtropics are opposite to those made for many species from cold climates which generally show deeper and longer torpor in winter and are often entirely homeothermic in summer. More pronounced torpor in subtropical S. australis in summer may be due to low or unpredictable nectar availability, short nights which limit the time available for foraging, and long days without access to food. Thus, the reversed seasonal response of this subtropical bat in comparison to temperate species may be an appropriate response to ecological constraints. Received: 6 May 1997 / Accepted: 19 October 1997     

Field metabolic rates and water uptake in the blossom-bat Syconycteris australis (Megachiroptera)

Blossom-bats, Syconycteris australis (18 g) are known to be highly active throughout the night. Since this species frequently enters torpor, we postulated that their use of heterothermy may be related to a high energy expenditure in the field. To test this hypothesis we measured field metabolic rates (FMR) of S. australis at a subtropical site using the doubly labelled water (DLW) method. We also measured DLW turnover in captive animals held at constant ambient temperature (T _a) with ad libitum food to estimate whether T _a and food availability affect energy expenditure under natural conditions. The FMR of S. australis was 8.55 ml CO₂ g⁻¹h⁻¹ or 76.87 kJ day⁻¹ which is 7.04 times the basal metabolic rate (BMR) and one of the highest values reported for endotherms to date. Mass-specific energy expenditure by bats in the laboratory was about two-thirds of that of bats in the field, but some of this difference was explained by the greater body mass in captive bats. This suggests that foraging times in the field and laboratory were similar, and daily energy expenditure was not strongly affected by T _a or ad libitum food. Water uptake in the field was significantly higher than in the laboratory, most likely because nectar contained more water than the laboratory diet. Our study shows that S. australis has a FMR that is about double that predicted for its size although its BMR is lower than predicted. This supports the view that caution must be used in making assumptions from measurements of BMR in the laboratory about energy and other biological requirements in free-ranging animals. Accepted: 4 January 1999     

Daily torpor in the Djungarian hamster (Phodopus sungorus): photoperiodic regulation,characteristics and circadian organization

1. The daily torpor was measured by oxygen uptake in Djungarian hamsters during adaptation to a short photoperiod (SP: 10L, 14D) at 20 degrees C. In these constant conditions the torpor presented metabolic characteristics and a daily time course independent of the duration of adaptations to SP. 2. The frequency of torpor bouts increased during SP exposure and its maximum was reached after about 130 days. The frequency of torpor was greater in males than in females. 3. The incidence of torpor was increased by constant dark exposure and this is discussed as a protective mechanism for the individual animal's ability to survive. 4. The temporal organization of daily torpor was demonstrated to be directly synchronized by the day-night cycle and to be controlled by an endogenous circadian function.     

Environmental conditions, rather than season, determine torpor use and temperature selection in large mouse-eared bats (Myotis myotis)

We tested whether food availability, thermal environment and time of year affect torpor use and temperature selection in the large mouse-eared bat (Myotis myotis) in summer and winter. Food-deprived bats were torpid longer than bats offered food ad libitum. Bats placed in a gradient of low (0 degrees C-25 degrees C) ambient temperatures (T(a)) spent more time in torpor than bats in a gradient of high (7 degrees C-43 degrees C) T(a)'s. However, we did not observe seasonal variations in the use of torpor. Moreover, even when food deprived in winter, bats never entered prolonged torpor at T(a)'s characteristic of their natural hibernation. Instead, bats preferred shallow torpor at relatively high T(a), but they always maintained a difference between body and ambient temperatures of less than 2 degrees C. Calculations based on respirometric measurements of metabolic rate showed that food deprived bats spent less energy per unit of time in torpor than fed individuals, even when they entered torpor at higher T(a)'s. We conclude that T(a) likely serves as a signal of food availability and daily torpor is apparently an adaptation to unpredictable changes in food availability, such as its decrease in summer or its increase in winter. Thus, we interpret hibernation to be a second step in the evolution of heterothermy in bats, which allows survival in seasonal environments.     

Normothermy,torpor, and arousal in hedgehogs (Erinaceus europaeus) from Dunedin

Abstract

We measured oxygen consumption of hedgehogs from Dunedin during normothermy, torpor, and arousal from torpor during the winter. Basal oxygen consumption and minimum thermal conductance were not significantly different from expected values for an average mammal of the same body mass. Torpid oxygen consumption at 5°C was only 0.5% of resting normothermic oxygen consumption at the same temperature. Oxygen consumption during arousal was not significantly different to that predicted theoretically or to that recorded during resting normothermy over the same time period. Using previous measures of pre‐hibernal body fat content, we build a simple model showing the relative energetic implications for a hedgehog of entering or not entering hibernation, and suggest that, at low temperatures, body fat stores would be depleted in <1 day and >100 days in non‐hibernating and hibernating hedgehogs, respectively.     

Reproduction of the long-tongued nectar bat Macroglossus minimus (Pteropodidae) in Brunei, Borneo

The long‐tongued nectar bat Macroglossus minimus lagochilus (Megachiroptera, Pteropodidae) is a small fruit bat inhabiting South‐east Asia. Its reproduction was studied in Brunei, Borneo, where individuals were usually captured in rainforest (Ulu Temburong). Adult females (n = 23) had body masses of 13.0–19.0 g, with forelimbs 3.83–4.33 cm in length. All adult females were pregnant, with pregnancies observed during every month except May, September and November when no adult females were captured. Female M. minimus in Brunei have a reproductive cycle that is consistent with a pattern of seasonal bimodal polyoestry. Most births appear to occur from November to May, during which time females experience two births: the first centred around November and December, and the second centred around April and May. These two birth seasons appear correlated to the two seasons of greater rainfall in Brunei: October to December, and April to July. Oestrous and mating apparently occur soon after each birth; however, there appears to be a 2‐ to 3‐month period of delayed embryonic development following the births centred around April and May. The data are consistent with embryonic development commencing around July and August (after a delay) for the births centred around November and December, and around December and January for the births centred around April and May. The data suggest that all adult females participate in each breeding season. Adult males (n = 20) had body masses of 12.5–18.0 g, with forelimbs 3.91–4.26 cm in length.     

Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor

We aimed to investigate the pattern of utilisation of torpor and its impact on energy budgets in free-living grey mouse lemurs (Microcebus murinus), a small nocturnal primate endemic to Madagascar. We measured daily energy expenditure (DEE) and water turnover using doubly labelled water, and we used temperature-sensitive radio collars to measure skin temperature (T _sk) and home range. Our results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a) during the dry season, but not during the rainy season. Mouse lemurs remained torpid between 1.7–8.9 h with a daily mean of 3.4 h, and their T _sk s fell to a minimum of 18.8 °C. Mean home ranges of mouse lemurs which remained normothermic were similar in the rainy and dry season. During the dry season, the mean home range of mouse lemurs showing daily torpor was significantly smaller than that of animals remaining normothermic. The DEE of M. murinus remaining normothermic in the rainy season (122 ± 65.4 kJ day⁻¹) was about the same of that of normothermic mouse lemurs in the dry season (115.5 ± 27.3 kJ day⁻¹). During the dry season, the mean DEE of M. murinus that utilised daily torpor was 103.4 ± 32.7 kJ day⁻¹ which is not significantly different from the mean DEE of animals remaining normothermic. We found that the DEE of mouse lemurs using daily torpor was significantly correlated with the mean temperature difference between T _sk and T _a (r ²=0.37) and with torpor bout length (r ² =0.46), while none of these factors explained significant amounts of variation in the DEE of the mouse lemurs remaining normothermic. The mean water flux rate of mouse lemurs using daily torpor (13.0 ± 4.1 ml day⁻¹) was significantly lower than that of mouse lemurs remaining normothermic (19.4 ± 3.8 ml day⁻¹), suggesting the lemurs conserve water by entering torpor. Thus, this first study on the energy budget of free-ranging M. murinus demonstrates that torpor may not only reflect its impact on the daily energy demands, but involve wider adaptive implications such as water requirements. Accepted: 29 August 2000     

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     

The effect of unsaturated and saturated dietary lipids on the pattern of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse Peromyscus maniculatus

Summary Dieary lipids strongly influence the pattern of torpor and the body lipid composition of mammalian hibernators. The object of the present study was to investigate whether these diet-induced physiological and biochemical changes also occur in species that show shallow, daily torpor. Deer mice, Peromyscus maniculatus, were fed with rodent chow (control diet) or rodent chow with either 10% sunflower seed oil (unsaturated diet) or 10% sheep fat (saturated diet). Animals on the unsaturated diet showed a greater occurrence of torpor (80–100% vs 26–43%), longer torpor bouts (4.5 vs 2.25 h), a lower metabolic rate during torpor (0.96 vs 2.25 ml O₂·g^-1·h^-1), and a smaller loss of body mass during withdrawal of food (2.35 vs 3.90 g) than animals on the saturated diet; controls were intermediate. These diet-induced physiological changes were associated with significant alterations in the fatty acid composition of depot fat, leg muscle and brain total lipids, and heart mitochondrial phospholipids. Significant differences in the total unsaturated fatty acid (UFA) content between animals on saturated and unsaturated diet were observed in depot fat (55.7% vs 81.1%) and leg muscle (56.4% vs 72.1%). Major compositional differences between diet groups also occurred in the concentration of n6 and/or n3 fatty acids of brain and heart mitochondria. The study suggests that dietary lipids may play an important role in the seasonal adjustment of physiology in heterothermic mammals.Abbreviations EDTA ethylenediaminetetra-acetic acid - HEPES N-2 hydroxyethylpiperazine-N¹-2-ethanesulphonic acid - MUFA monounsaturated fatty acids - PUFA polyunsaturated fatty acids - RMR Testing metabolic rate - SD standard deviation - SFA saturated fatty acids - SNK Student-Newman-Keuls test - T₁ air temperature - T_b body temperature - UFA unsaturated fatty acids - rate of oxygen consumption Dedicated to the late John K. Raison     

Correlation between torpor frequency and capacity for non-shivering thermogenesis in the Siberian hamster (Phodopus sungorus)

We investigated the correlation between torpor frequency and capacity for non-shivering thermogenesis (NST) in Siberian hamsters (Phodopus sungorus) during 25 weeks of acclimation to cold and short days. We hypothesized that torpor use is conditioned on the development of brown adipose tissue (BAT) capacity for NST. We found that (1) the degree of noradrenaline (NA)-induced hyperthermia was positively correlated with torpor frequency and its length and depth, and (2) the maximum response to NA occurred at the time of day when hamsters naturally arouse from torpor. The present study quantifies the correlation between torpor frequency and NST capacity and we suggest that a well-developed NST capacity is a prerequisite for the occurrence of torpor.     

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.     

Thermal biology,torpor and behaviour in sugar gliders: a laboratory-field comparison

Most studies on animal physiology and behaviour are conducted in captivity without verification that data are representative of free-ranging animals. We provide the first quantitative comparison of daily torpor, thermal biology and activity patterns, conducted on two groups of sugar gliders (Petaurus breviceps, Marsupialia) exposed to similar thermal conditions, one in captivity and the other in the field. Our study shows that activity in captive gliders in an outdoor aviary is restricted to the night and largely unaffected by weather, whereas free-ranging gliders omit foraging on cold/wet nights and may also forage in the afternoon. Torpor occurrence in gliders was significantly lower in captivity (8.4% after food deprivation; 1.1% for all observations) than in the field (25.9%), mean torpor bout duration was shorter in captivity (6.9 h) than in the field (13.1 h), and mean body temperatures during torpor were higher in captivity (25.3°C) than in the field (19.6°C). Moreover, normothermic body temperature as a function of air temperature differed between captive and free-ranging gliders, with a >3°C difference at low air temperatures. Our comparison shows that activity patterns, thermal physiology, use of torpor and patterns of torpor may differ substantially between the laboratory and field, and provides further evidence that functional and behavioural data on captive individuals may not necessarily be representative of those living in the wild.     

Daily torpor in free-ranging common dormice (Muscardinus avellanarius) in Lithuania

Torpid common dormice (Muscardinus avellanarius) were found in nestboxes during all the activity period from early April until late October. Prevalence of torpor among dormice was highest in spring, decreased considerably in summer and increased again in October. The proportion of adult dormice that were torpid was inversely related to mean monthly air temperature, except in September, when dormice prepare for hibernation by accumulating fat reserves. In spring and summer, torpid dormice were found when ambient temperature was up to 14–15 °C and in the arousal phase of torpor – up to 19–20 °C. In autumn, dormice were active at much lower ambient temperatures compared to spring and summer, and only dormice that were fat enough and ready for hibernation were torpid. Torpor bouts usually lasted only until noon, but also in the afternoon during persistently low ambient temperatures in April and October. In April–July, torpor was more frequent among adult males than females (75% vs. 46%), and pregnant females were never found in deep torpor. Prevalence of torpor among young-of-the-year was lower compared to adult dormice at the same time. In October, the average weight of torpid young-of-the-year dormice was significantly higher compared to the weight of active dormice (22.3 vs. 17.5 g).

Zusammenfassung

Tagestorpor bei frei lebenden Haselmäusen (Muscardinus avellanarius) in LitauenHaselmäuse (Muscardinus avellanarius) im Torpor wurden während der gesamten aktiven Saison zwischen zeitigem April und Ende Oktober in Nistkästen gefunden. Im Frühjahr war die Torporfrequenz am höchsten, während des Sommers ging sie beträchtlich zurück, und im Oktober stieg sie wieder deutlich. Der Anteil an Haselmäusen im Torpor war umgekehrt abhängig von der mittleren Monatslufttemperatur, mit Ausnahme des Septembers, wo sich die Haselmäuse Fettreserven in Vorbereitung des Winterschlafes anlegen. Während des Frühlings und des Sommers konnten Haselmäuse im Torpor gefunden werden, wenn die Umgebungstemperatur bis 14–15 °C war, und in der Aufwachphase bei Temperaturen bis 19–20 °C. Im Herbst waren die Haselmäuse bei viel tieferen Temperaturen als im Sommer oder Frühjahr aktiv und nur die Haselmäuse die fett genug waren, um in den Winterschlaf gehen zu können, waren lethargisch. Die Torporphasen dauerten in der Regel nur bis zum Mittag, aber im April und Oktober während lang anhaltenden tiefen Umgebungstemperaturen auch bis in den Nachmittag hinein. Zwischen April und Juli konnten mehr adulte Männchen als Weibchen im Torpor nachgewiesen werden (75% vs 46%). Tragende Weibchen waren niemals im tiefen Torpor zu finden. Die Torporfrequenz war bei Haselmäusen in ihrem ersten Lebensjahr geringer als bei adulten im selben Zeitraum. Im Oktober war bei den lethargischen Jungtieren des Jahres das Durchschnittsgewicht höher als bei den aktiven Haselmäusen (22.3 vs. 17.5 g).     

Summer torpor in African woodland dormiceGraphiurus murinus (Myoxidae: Graphiurinae)

We determined the effect of food availability (presence/absence) and ambient temperature (25/10°C) on daily energy expenditure and the use of activity and torpor in summer-acclimated captiveGraphiurus murinus. Daily energy expenditure declined logarithmically with duration of food deprivation at a mean rate of 11 and 31% per day at 25 and 10°C, respectively. The incidence of torpor in the presence of food at 25°C was low (one in seven individuals) and increased on a single day's exposure to 10°C and with duration of food deprivation. Use of torpor was highest during the day, varied between individuals, and torpor bouts of greater than 24h duration were not noted. With food deprivation, individuals at 25°C initially responded by reducing activity but remained euthermic while the same individuals at 10°C responded by increasing their use of torpor during the light period; this difference in response probably reflects a difference in the relative energetic benefits of torpor at different temperatures.     

Old World phytophagous bats (Megachiroptera) and their food plants: a survey

The Megachiroptera, with a single family, 43 genera and 174 species, are confined to the Old World tropics and subtropics where they are exclusively phytophagous, feeding upon floral resources (largely nectar and pollen but also petals and bracts), fruit, leaves and water. A literature survey revealed information on the food sources for only 21 genera of bats, these feeding upon 75 genera of flowers, 145 genera of fruit and 10 genera of leaves in a total of 34 orders, 66 families and 198 genera. The bats are likely to pollinate flowers of at least 31 genera and presumably may disperse the seeds of the majority of fruits consumed. Despite our ignorance about the relationship between Megachiroptera and plants, it appears that most bats are catholic in their choice of food, and most plants are visited by a diversity of bats.     

How to budget metabolic energy: torpor in a small Neotropical mammal

Neotropical nectar-feeding bats (Glossophaginae) are highly specialized in the exploitation of floral nectar and have one of the highest mass-specific metabolic rates among mammals. Nevertheless, they are distributed throughout the tropics and subtropics over a wide elevational range, and thus encounter many extreme and energetically challenging environmental conditions. Depressing their otherwise high metabolic rate, e.g., in situations of food restriction, might be an important adaptive physiological strategy in these dietary specialists. We investigated the thermoregulatory behavior of captive 10-g nectar feeding bats (Glossophaga soricina; Chiroptera, Phyllostomidae) under variable ambient temperatures (T _a) and feeding regimes and predicted that bats would use torpor as an energy-conserving behavior under energetic constraints. All tested animals entered torpor in response to energetic restrictions and the depth of torpor was dependent on the body condition of the animals and hence on their degree of physiological constraints. Periods of torpor with body temperatures (T _b) below 34°C were precisely adjusted to the photoperiod. The median length of diurnal torpor was 11.43 h. The lowest T _b measured was 21°C at a T _a of 19°C. Estimated energy savings due to torpor were considerable, with reductions in metabolic rate to as low as 5% of the metabolic rate of normothermic bats at the same T _a. However, contrary to temperate zone bats that also employ diurnal torpor, G. soricina regulated their T _b to the highest possible levels given the present energetic supplies. To summarize, G. soricina is a precise thermoregulator, which strategically employs thermoregulatory behavior in order to decrease its energy expenditure when under energetic restrictions. This adaptation may play a crucial role in the distribution and the assembly of communities of nectar-feeding bats and may point to a general capacity for torpor in tropical bats.     

Thermoregulation, energy metabolism, and torpor in blossom-bats, Syconycteris australis (Megachiroptera)

Since little information is available on torpor in bats of the suborder Megachiroptera, we investigated whether the small (18 g) blossom-bat Syconycteris australis displays torpor in the laboratory. Bats entered daily torpor when food and water were withheld for one night and the air temperature (T_a) was below about 26°. Torpor began shortly after lights went on in the morning and lasted for a maximum of 12 hours. During torpor at T_a18°, metabolic rates fell to a minimum of about 15% of that in resting individuals at the same T_a, and to about 40% of the basal metabolic rate. The body temperature (T_b) during torpor was metabolically defended at or above about T_b 18°. Individuals that did not enter torpor in the morning reduced their T_b from about 34.5°, observed in resting individuals that had been fed during the previous night, to values between 30.2 and 32.8°, and the resting metabolic rate fell by about 25%. The ability to undergo short periods of torpor may explain why the distribution range of S. australis extends much further south than that of other small Australian megachiropteran bats.