The key to winter survival: daily torpor in a small arid-zone marsupial

Mammalian hibernation, which lasts on average for about 6 months, can reduce energy expenditure by >90% in comparison to active individuals. In contrast, the widely held view is that daily torpor reduces energy expenditure usually by about 30%, is employed for a few hours every few days, and often occurs only under acute energetic stress. This interpretation is largely based on laboratory studies, whereas knowledge on daily torpor in the field is scant. We used temperature telemetry to quantify thermal biology and activity patterns of a small arid-zone marsupial, the stripe-faced dunnart Sminthopsis macroura (16.9 g), in the wild and to test the hypothesis that daily torpor is a crucial survival strategy of this species in winter. All individuals entered torpor daily with the exception of a single male that remained normothermic for a single day (torpor on 212 of 213 observation days, 99.5%). Torpor was employed at air temperatures (T _a) ranging from approximately −1°C to 36°C. Dunnarts usually entered torpor during the night and aroused at midday with the daily increase of T _a. Torpor was on average about twice as long (mean 11.0 ± 4.7 h, n = 8) than in captivity. Animals employed sun basking during rewarming, reduced foraging time significantly, and occasionally omitted activity for several days in sequence. Consequently, we estimate that daily torpor in this species can reduce daily energy expenditure by up to 90%. Our study shows that for wild stripe-faced dunnarts daily torpor is an essential mechanism for overcoming energetic challenges during winter and that torpor data obtained in the laboratory can substantially underestimate the ecological significance of daily torpor in the wild.     

Was basking important in the evolution of mammalian endothermy?

The first mammals were small, nocturnal, and presumably had low metabolic rates and were therefore probably unable to maintain a constant high body temperature throughout cool nights. How these animals, without sufficient heat production for endogenous rewarming, were able to become warm and active again before the next activity period remains unresolved. However, we discovered that, similar to reptiles, the carnivorous marsupial mammal Pseudantechinus macdonnellensis (body mass 30.8LJ.0 g) uses the morning sun to rewarm from low (26.3dž.5°C) body temperatures during torpor. Our findings provide the first evidence of basking during rewarming from torpor in mammals and may provide an alternative explanation as to how ancestral mammals could have become nocturnal to avoid diurnal predators despite their small size and a low endogenous heat production.     

Roost type influences torpor use by Australian owlet-nightjars

Australian owlet-nightjars (Aegotheles cristatus; ～50?g) are one of only a few avian species that roost in cavities year-round and regularly enter torpor. Cavity roosts act as thermal buffers, and roost type likely affects energy expenditure of small birds. We used radiotelemetry to locate diurnal winter roost sites of owlet-nightjars in central Australia and to measure body (T (b)) and skin (T (skin)) temperature. We also recorded ambient temperature inside (T (IN)) and outside roosts. Individual owlet-nightjars used one to seven different roosts (tracking time 3-10?weeks), selecting either rock crevices (four birds) or tree hollows (four birds), or switching between the two roost types (seven birds). Rock crevices (T (IN) +9°C to +33°C) were warmer and thermally more stable than tree hollows (T (IN) -4.0°C to +37°C). Torpor, often expressed by a reduction of T (skin)/T (b) by >10°C for 3-4?h at dawn, was influenced by roost selection; torpor use in tree hollows was almost twice that in rock crevices. Despite the potential energy savings accrued from roosting in well-insulated cavities, owlet-nightjars roosted in tree hollows more often (65% bird days, n?=?398) than in rock crevices (35% bird days, n?=?211). Lower costs of arousal from torpor via passive rewarming and basking and decreased risk of predation are two possible explanations for the preference to roost in tree hollows. We provide the first evidence for the influence of cavity roost selection on torpor use in a free-ranging bird and show that roost selection and thermal biology are strongly interrelated in determining energy expenditure.     

Yearlong hibernation in a marsupial mammal

Many mammals hibernate each year for about 6 months in autumn and winter and reproduce during spring and summer when they are generally not in torpor. I tested the hypothesis that the marsupial pygmy-possum (Cercartetus nanus), an opportunistic nonseasonal hibernator with a capacity for substantial fattening, would continue to hibernate well beyond winter. I also quantified how long they were able to hibernate without access to food before their body fat stores were depleted. Pygmy-possums exhibited a prolonged hibernation season lasting on average for 310 days. The longest hibernation season in one individual lasted for 367 days. For much of this time, despite periodic arousals after torpor bouts of ∼12.5 days, energy expenditure was reduced to only ∼2.5% of that predicted for active individuals. These observations represent the first report on body-fat-fuelled hibernation of up to an entire year and provide new evidence that prolonged hibernation is not restricted to placental mammals living in the cold.     

Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata)

The severity, duration and amplitude of extreme weather events are forecast to intensify with current climate trends, over both long (e.g. seasonal) and short (e.g. daily) time-scales. As such, the predictability of food supplies for many small endotherms is likely to become increasingly important. Numerous small mammals and birds combat food shortages using torpor, a controlled reduction in metabolic rate and body temperature that helps lower their daily energy requirements. As such, torpor often has been cited as a key feature allowing some small endotherms to survive highly unpredictable climates, such as tropics or dry deserts, but mensurative demonstrations of this are lacking. We have shown here that when a small desert marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata), is offered unpredictable levels of daily food, they increase frequency of daily torpor and length of bouts compared with animals offered ad libitum food, but this was not found for animals offered a 70% food-restricted diet. Our data suggest that simple food restriction may not be sufficient for evaluating the efficacy of torpor as a strategy for managing unpredictable climates.     

Vertebrate diet decreases winter torpor use in a desert marsupial

One of the energetic benefits of daily torpor over prolonged hibernation is that it enables animals to regularly forage and, therefore, replenish food reserves between bouts of torpor. However, little is known about the diet of predators undergoing torpor or whether differences in prey composition among individuals influence torpor characteristics. Here, we test the hypothesis that prey composition affects winter torpor use and patterns of a population of carnivorous marsupial, the brush-tailed mulgara (Dasycercus blythi), in the Great Sandy Desert, Australia. Mulgaras in the study population captured a wide range of prey including vertebrates (mammals, reptiles, birds), seven insect orders, spiders and centipedes. The proportion of vertebrates in the diet was negatively correlated with both frequency of torpor use and maximum bout duration. This variation in torpor use with diet can be explained by the higher energetic content of vertebrates as well as their larger size. Even assuming uniform intake of prey biomass among individuals, those that subsisted on an invertebrate-dominated diet during winter apparently suffered energetic shortages as a result of the scarcity of invertebrate taxa with high energy content (such as insect larvae). Our study is the first to demonstrate a link between diet composition and daily torpor use in a free-ranging mammal.     

Torpor in free-ranging antechinus: does it increase fitness?

Antechinus are small, insectivorous, heterothermic marsupial mammals that use torpor from late summer to early winter and reproduce once a year in late winter/early spring. Males die after mating, most females produce only a single litter, but some survive a second winter and produce another litter. As it is not known how these females manage to survive the second winter after the energetically demanding reproductive period and then reproduce a second time, we aimed to provide the first data on thermal biology of free-ranging antechinus by using temperature telemetry. Male Antechinus stuartii and Antechinus flavipes rarely entered torpor in autumn/early winter in the wild, expressing only shallow bouts of <2 h. Female A. stuartii used torpor extensively, employing bouts up to 16.7 h with body temperatures as low as 17.8 °C. Interestingly, although first and second year females used similar torpor patterns, torpor occurrence was almost twofold in second year (93 % of days) than first year females (49 %), and the proportion of the overall monitoring period animals spent torpid was 3.2-fold longer in the former with a corresponding shorter activity period. Our study suggests that intensive use of torpor is crucial for second year females for autumn and winter survival and production of a second litter. We provide the first evidence of an age-related pattern in daily torpor expression in free-ranging mammals and show that torpor use is a complex process that is affected not only by the current energy availability and thermal conditions but also by the reproductive history and age of individuals.     

Optional strategies for reduced metabolism in gray mouse lemurs

Among the order of primates, torpor has been described only for the small Malagasy cheirogaleids Microcebus and Cheirogaleus. The nocturnal, gray mouse lemur, Microcebus murinus (approx. 60 g), is capable of entering into and spontaneously arousing from apparently daily torpor during the dry season in response to reduced temperatures and low food and water sources. Mark–recapture studies indicated that this primate species might also hibernate for several weeks, although physiological evidence is lacking. In the present study, we investigated patterns of body temperature in two free-ranging M. murinus during the austral winter using temperature-sensitive data loggers implanted subdermally. One lemur hibernated and remained inactive for 4 weeks. During this time, body temperature followed the ambient temperature passively with a minimum body temperature of 11.5°C, interrupted by irregular arousals to normothermic levels. Under the same conditions, the second individual displayed only short bouts of torpor in the early morning hours but maintained stable normothermic body temperatures throughout its nocturnal activity. Reduction of body temperature was less pronounced in the mouse lemur that utilized short bouts of torpor with a minimum value of 27°C. Despite the small sample size, our findings provide the first physiological confirmation that free-ranging individuals of M. murinus from the humid evergreen littoral rain forest have the option to utilize short torpor bouts or hibernation under the same conditions as two alternative energy-conserving physiological solutions to environmental constraints.     

Fat and fed: frequent use of summer torpor in a subtropical bat

A widely held view is that torpor is avoided by mammals whenever possible because of potential costs associated with reduced body temperatures and slowed metabolic processes. We examined this hypothesis by quantifying use of torpor in relation to body condition of free-ranging northern long-eared bats (Nyctophilus bifax, approximately 10 g), a species known to hibernate, from a subtropical region during the austral summer when insects were abundant. Temperature-telemetry revealed that bats used torpor on 85% of observation days and on 38% of all nights. Torpor bouts ranged from 0.7 to 21.2 h, but the relationship between duration of torpor bouts and ambient temperature was not significant. However, skin temperature of torpid bats was positively correlated with ambient temperature. Against predictions, individuals with a high body condition index (i.e., good fat/energy reserves) expressed longer and deeper torpor bouts and also employed torpor more often during the activity phase at night than those with low body condition index. We provide the first evidence that use of torpor in a free-ranging subtropical mammal is positively related with high body condition index. This suggests that employment of torpor is maximised and foraging minimised not because of food shortages or low energy stores but likely to avoid predation when bats are not required to feed.     

Torpor use during gestation and lactation in a primate

Torpor is an energy-saving mechanism that allows endotherms to overcome energetic challenges. Torpor should be avoided during reproduction because of potential incompatibility with offspring growth. To test if torpor can be used during gestation and lactation to compensate for food shortage, we exposed reproductive female grey mouse lemurs (Microcebus murinus), a heterothermic primate, to different levels of food availability. Torpor use was characterised by daily skin temperature profiles, and its energetic outcome was assessed from changes in body mass. Food shortage triggered torpor during the end of the gestation period (n = 1), ranging from shallow in response to 40% food restriction to deep daily torpor in response to 80% restriction. During the early period of lactation, females fed ad libitum (n = 2) or exposed to a 40% restriction (n = 4) remained normothermic; but 80% food restricted females (n = 5) gave priority to energy saving, increasing the frequency and depth of torpor bouts. The use of torpor was insufficient to compensate for 80% energetic shortage during lactation resulting in loss of mass from the mother and delayed growth in the pups. This study provides the first evidence that a heterothermic primate can use torpor to compensate for food shortages even during reproduction. This physiological flexibility likely evolved as a response to climate-driven fluctuations in food availability in Madagascar.     

Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests

Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature (T _a). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature (T _sk) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.     

Photoperiod affects daily torpor and tissue fatty acid composition in deer mice

Photoperiod and dietary lipids both influence thermal physiology and the pattern of torpor of heterothermic mammals. The aim of the present study was to test the hypothesis that photoperiod-induced physiological changes are linked to differences in tissue fatty acid composition of deer mice, Peromyscus maniculatus (∼18-g body mass). Deer mice were acclimated for >8 weeks to one of three photoperiods (LD, light/dark): LD 8:16 (short photoperiod), LD 12:12 (equinox photoperiod), and LD 16:8 (long photoperiod). Deer mice under short and equinox photoperiods showed a greater occurrence of torpor than those under long photoperiods (71, 70, and 14%, respectively). The duration of torpor bouts was longest in deer mice under short photoperiod (9.3 ± 2.6 h), intermediate under equinox photoperiod (5.1 ± 0.3 h), and shortest under long photoperiod (3.7 ± 0.6 h). Physiological differences in torpor use were associated with significant alterations of fatty acid composition in ∼50% of the major fatty acids from leg muscle total lipids, whereas white adipose tissue fatty acid composition showed fewer changes. Our results provide the first evidence that physiological changes due to photoperiod exposure do result in changes in lipid composition in the muscle tissue of deer mice and suggest that these may play a role in survival of low body temperature and metabolic rate during torpor, thus, enhancing favourable energy balance over the course of the winter.     

To use or not to use torpor? Activity and body temperature as predictors

When food is limited and/or environmental conditions are unfavourable, many mammals reduce activity and use torpor to save energy. Nevertheless, reliable predictors for torpor occurrence, especially in the wild, are currently not available. Interrelations between torpor use and other energy conserving strategies are also poorly understood. We tested the hypothesis that reductions in normothermic body temperature (T _b) and the period of activity before torpor events could be used as predictors for torpor occurrence in sugar gliders, Petaurus breviceps (body mass, ∼125 g), known to display daily torpor in the wild. Occurrence of torpor was preceded by significant (∼10–25%) reductions of the duration of the activity phase. Moreover, the normothermic resting T _b fell by an average of 1.2°C over 3 days before a torpor event, relative to individuals that did not display torpor. Our new findings suggest that before entering torpor, sugar gliders, which appear to use torpor as an emergency measure rather than a routine energy saving strategy, systematically reduce activity times and normothermic resting T _bs to lower energy expenditure and perhaps to avoid employing torpor. Thus, reduced activity and normothermic T _b may provide a predictive tool for the occurrence of daily torpor in the wild.     

Summer dormancy in edible dormice (Glis glis) without energetic constraints

Average longevity in free-living edible dormice (Glis glis) can reach 9 years, which is extremely high for a small rodent. This remarkable life span has been related to a peculiar life history strategy and the rarity of reproductive bouts in these seed eaters. Most females (96%) reproduce only once or twice in their lifetime, predominantly during years of mast seeding of, e.g., beech, but entire populations can skip reproduction in years of low seed availability. Surprisingly, in non-reproductive years, large fractions of populations apparently vanished and were never captured above ground. Therefore, we determined the duration of above-ground activity, and body temperature profiles in a subset of animals, of dormice under semi-natural conditions in outdoor enclosures. We found that non-reproductive dormice returned to dormancy in underground burrows throughout summer after active seasons as short as <2 weeks. Thus, animals spent up to >10 months per year in dormancy. This exceeds dormancy duration of any other mammal under natural conditions. Summer dormancy was not caused by energy constraints, as it occurred in animals in good condition, fed ad libitum and without climatic stress. We suggest that almost year-round torpor has evolved as a strategy to escape birds of prey, the major predators of this arboreal mammal. This unique predator-avoidance strategy clearly helps in explaining the unusually high longevity of dormice.     

Torpor in the Patagonian opossum (Lestodelphys halli): implications for the evolution of daily torpor and hibernation

Hibernation and daily torpor are two distinct forms of torpor, and although they are related, it is not known how and in which sequence they evolved. As the pattern of torpor expressed by the oldest marsupial order the opossums (Didelphimorphia) may provide insights into the evolution of torpor, we aimed to provide the first quantitative data on the thermal biology and torpor expression of the rare Patagonian opossum (Lestodelphys halli). It is the opossum with the southernmost distribution, has a propensity of autumnal fattening, and therefore, is likely to hibernate. We captured two male Lestodelphys, which while in captivity displayed strong daily fluctuations of body temperatures (T_b) measured with implanted miniature data loggers even when they remained normothermic. In autumn and early winter, torpor was expressed occasionally when food was available, but cold exposure and food withdrawal increased torpor use. The mean T_b throughout the study was 32.2?±?1.4 °C, the minimum T_b measured in torpid Lestodelphys was 7.7 °C, average torpor bout duration was 10.3 h, and the maximum torpor bout duration was 42.5 h. Thus, the pattern of torpor expressed by Lestodelphys was intermediate between that of daily heterotherms and hibernators suggesting that it may represent an ancestral opportunistic torpor pattern from which the derived patterns of daily torpor and seasonal hibernation diverged.     

Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure

Small endotherms must change roosting and thermoregulatory behaviour in response to changes in ambient conditions if they are to achieve positive energy balance. In social species, for example many bats, energy expenditure is influenced by environmental conditions, such as ambient temperature, and also by social thermoregulation. Direct measurements of daily fluctuations in metabolic rates in response to ambient and behavioural variables in the field have not been technologically feasible until recently. During different reproductive periods, we investigated the relationships between ambient temperature, group size and energy expenditure in wild maternity colonies of Bechstein’s bats (Myotis bechsteinii). Bats used behavioural and physiological adjustments to regulate energy expenditure. Whether bats maintained normothermia or used torpor, the number of bats in the roosts as well changed with reproductive status and ambient temperature. During pregnancy and lactation, bats remained mostly normothermic and daily group sizes were relatively large, presumably to participate in the energetic benefits of social thermoregulation. In contrast, smaller groups were formed on days when bats used torpor, which occurred mostly during the post-lactation period. Thus, we were able to demonstrate on wild animals under natural conditions the significance of behavioural and physiological flexibility for optimal thermoregulatory behaviour in small endotherms.     

成都市城区大气VOCs季节污染特征及来源解析

为研究成都市城区大气VOCs季节变化特征,本研究在2018年12月至2019年11月对VOCs组分进行监测,并对VOCs的浓度水平、各化学组成、化学反应活性和来源进行分析.结果表明,成都市城区春、夏、秋和冬季VOCs的平均体积分数分别为32.29×10~(-9)、 36.25×10~(-9)、 40.92×10~(-9)和49.48×10~(-9),冬季的浓度明显高于其他季节,春季和夏季的浓度水平相差不大,各季节VOCs的组分浓度水平有所差异,冬季烷烃占总VOCs的比例最大,可能受机动车排放的影响较明显;夏季和秋季含氧(氮)挥发性有机物占比远高于春、冬季,一次源的挥发排放和二次转化的生成贡献较大;成都市城区不同季节大气中VOCs平均浓度排名靠前的关键组分基本无变化,主要是C_2～C_4的烷烃、乙烯、乙炔及二氯甲烷等,可能受机动车尾气、油气挥发、溶剂使用和LPG燃料等影响明显,夏季丙酮以及乙酸乙酯等含氧有机物浓度贡献突出;根据·OH消耗速率和OFP计算可知关键活性物种主要为间/对-二甲苯、乙烯、丙烯、1-己烯、甲苯、异戊烷和正丁烷等,这些物种应该优先减排和控制;四季VOCs源解析结果显示:春、夏季温度较秋、冬季高,光照更强,PMF明显解析出天然源和二次排放贡献,同时,由于夏季温度较高,解析出油气挥发占9%;秋、冬季占比增加的源主要为机动车尾气和燃烧源,燃烧源的排放占比在25%左右,另餐饮源的排放占比在9%左右.     

Body mass dependence of glycogen stores in the anoxia-tolerant crucian carp (<Emphasis Type="Italic">Carassius carassius</Emphasis> L.)

Glycogen is a vital energy substrate for anaerobic organisms, and the size of glycogen stores can be a limiting factor for anoxia tolerance of animals. To this end, glycogen stores in 12 different tissues of the crucian carp (Carassius carassius L.), an anoxia-tolerant fish species, were examined. Glycogen content of different tissues was 2–10 times higher in winter (0.68–18.20% of tissue wet weight) than in summer (0.12–4.23%). In scale, bone and brain glycogen stores were strongly dependent on body mass (range between 0.6 and 785 g), small fish having significantly more glycogen than large fish (p < 0.05). In fin and skin, size dependence was evident in winter, but not in summer, while in other tissues (ventricle, atrium, intestine, liver, muscle, and spleen), no size dependence was found. The liver was much bigger in small than large fish (p < 0.001), and there was a prominent enlargement of the liver in winter irrespective of fish size. As a consequence, the whole body glycogen reserves, measured as a sum of glycogen from different tissues, varied from 6.1% of the body mass in the 1-g fish to 2.0% in the 800-g fish. Since anaerobic metabolic rate scales down with body size, the whole body glycogen reserves could provide energy for approximately 79 and 88 days of anoxia in small and large fish, respectively. There was, however, a drastic difference in tissue distribution of glycogen between large and small fish: in the small fish, the liver was the major glycogen store (68% of the stores), while in the large fish, the white myotomal muscle was the principal deposit of glycogen (57%). Since muscle glycogen is considered to be unavailable for blood glucose regulation, its usefulness in anoxia tolerance of the large crucian carp might be limited, although not excluded. Therefore, mobilization of muscle glycogen under anoxia needs to be rigorously tested.     

Voluntary exercise at the expense of reproductive success in Djungarian hamsters (Phodopus sungorus)

Energy demands of gestation and lactation represent a severe challenge for small mammals. Therefore, additional energetic burdens may compromise successful breeding. In small rodents, food restriction, cold exposure (also in combination) and wheel running to obtain food have been shown to diminish reproductive outcome. Although exhibited responses such as lower incidence of pregnancy, extended lactation periods and maternal infanticide were species dependent, their common function is to adjust energetic costs to the metabolic state reflecting the trade-off between maternal investment and self-maintenance. In the present study, we sought to examine whether voluntary exercise affects reproduction in Djungarian hamsters (Phodopus sungorus), which are known for their high motivation to run in a wheel. Voluntary exercise resulted in two different effects on reproduction; in addition to increased infanticide and cannibalism, which was evident across all experiments, the results of one experiment provided evidence that free access to a running wheel may prevent successful pregnancy. It seems likely that the impact of voluntary wheel running on reproduction was associated with a reduction of internal energy resources evoked by extensive exercise. Since the hamsters were neither food-restricted nor forced to run in the present study, an energetic deficit as reason for infanticide in exercising dams would emphasise the particularly high motivation to run in a wheel.     

Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field

The radical pair model of magnetoreception predicts that magnetic compass orientation can be disrupted by high frequency magnetic fields in the Megahertz range. European robins, Erithacus rubecula, were tested under monochromatic 565 nm green light in 1.315 MHz fields of 0.48 T during spring and autumn migration, with 1.315 MHz being the frequency that matches the energetic splitting induced by the local geomagnetic field. The birds responses depended on the alignment of the oscillating field with respect to the static geomagnetic field: when the 1.315 MHz field was aligned parallel with the field lines, birds significantly preferred northerly directions in spring and southerly directions in autumn. These preferences reflect normal migratory orientation, with the variance slightly increased compared to control tests in the geomagnetic field alone or to tests in a 7.0 MHz field. However, in the 1.315 MHz field aligned at a 24° angle to the field lines, the birds were disoriented in both seasons, indicating that the high frequency field interfered with magnetoreception. These finding are in agreement with theoretical predictions and support the assumption of a radical-pair mechanism underlying the processes mediating magnetic compass information in birds.