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.     

Torpor and basking in a small arid zone marsupial

The high energetic cost associated with endothermic rewarming from torpor is widely seen as a major disadvantage of torpor. We tested the hypothesis that small arid zone marsupials, which have limited access to energy in the form of food but ample access to solar radiation, employ basking to facilitate arousal from torpor and reduce the costs of rewarming. We investigated torpor patterns and basking behaviour in free-ranging fat-tailed dunnarts Sminthopsis crassicaudata (10 g) in autumn and winter using small, internal temperature-sensitive transmitters. Torpid animals emerged from their resting sites in cracking soil at ∼1000 h with body temperatures as low as 14.6°C and positioned themselves in the sun throughout the rewarming process. On average, torpor duration in autumn was shorter, and basking was less pronounced in autumn than in winter. These are the first observations of basking during rewarming in S. crassicaudata and only the second direct evidence of basking in a torpid mammal for the reduction of energetic costs during arousal from torpor and normothermia. Our findings suggest that although overlooked in the past, basking may be widely distributed amongst heterothermic mammals. Therefore, the energetic benefits from torpor use in wild animals may currently be underestimated.     

Hibernation and daily torpor minimize mammalian extinctions

Small mammals appear to be less vulnerable to extinction than large species, but the underlying reasons are poorly understood. Here, we provide evidence that almost all (93.5%) of 61 recently extinct mammal species were homeothermic, maintaining a constant high body temperature and thus energy expenditure, which demands a high intake of food, long foraging times, and thus exposure to predators. In contrast, only 6.5% of extinct mammals were likely heterothermic and employed multi-day torpor (hibernation) or daily torpor, even though torpor is widespread within more than half of all mammalian orders. Torpor is characterized by substantial reductions of body temperature and energy expenditure and enhances survival during adverse conditions by minimizing food and water requirements, and consequently reduces foraging requirements and exposure to predators. Moreover, because life span is generally longer in heterothermic mammals than in related homeotherms, heterotherms can employ a ‘sit-and-wait’ strategy to withstand adverse periods and then repopulate when circumstances improve. Thus, torpor is a crucial but hitherto unappreciated attribute of small mammals for avoiding extinction. Many opportunistic heterothermic species, because of their plastic energetic requirements, may also stand a better chance of future survival than homeothermic species in the face of greater climatic extremes and changes in environmental conditions caused by global warming.     

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.     

Deep, prolonged torpor by pregnant, free-ranging bats

Many mammals save energy during food shortage or harsh weather using controlled reductions in body temperature and metabolism called torpor. However, torpor slows offspring growth, and reproductive individuals are thought to avoid using it because of reduced fitness resulting from delayed offspring development. We tested this hypothesis by investigating torpor during reproduction in hoary bats (Lasiurus cinereus, Vespertilionidae) in southern Canada. We recorded deep, prolonged torpor bouts, which meet the definition for hibernation, by pregnant females. Prolonged torpor occurred during spring storms. When conditions improved females aroused and gave birth within several days. Our observations imply a fitness advantage of torpor in addition to energy conservation because reduced foetal growth rate could delay parturition until conditions are more favourable for lactation and neonatal survival.     

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.     

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.     

Specific dynamic action affects the hydrostatic pressure tolerance of the shallow-water spider crab <Emphasis Type="Italic">Maja brachydactyla</Emphasis>

The bathymetric distribution of marine benthic invertebrates is likely governed by a combination of ecological and physiological factors. The present study investigates oxygen consumption and heartbeat rate in response to attempted feeding at 1, 100 and 150 atm in the shallow-water spider crab, Maja brachydactyla, from temperate European waters. No significant difference was evident between the resting heartbeat rate of specimens at 1 or 100 atm, which were 56 and 65 bpm, respectively (Mann–Whitney, U = 5382.0; n = 95, 98; p = 0.079). However, at 150 atm the resting heartbeat rate was significantly higher than that observed for 100 atm at 108 bpm (Mann–Whitney, U = 149.0; n = 45, 98; p < 0.001). At 150 atm, feeding was never observed and coupled with the elevated resting heartbeat rate; it is suggested by 150 atm continued survival is unfeasible. At 1 and 100 atm, feeding instigated a distinct increase in heartbeat rate, which remained elevated for over 30 h. This increase peaked within 1 h at 1 atm. At 100 atm, this required 4 h and postprandial oxygen consumption was significantly higher than at 1 atm (Kruskal–Wallis, H = 85.036; df = 2; p < 0.001). Elevated hydrostatic pressure is hypothesized to extend the duration and the total metabolic energy devoted to specific dynamic action. The metabolic requirements of feeding under hyperbaric conditions may even reach such a critical demand that feeding is entirely inhibited.     

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.     

Reversed sex change by widowed males in polygynous and protogynous fishes: female removal experiments in the field

Sex change, either protogyny (female to male) or protandry (male to female), is well known among fishes, but evidence of bidirectional sex change or reversed sex change in natural populations is still very limited. This is the first report on female removal experiments for polygnous and protogynous fish species to induce reversed sex change in the widowed males in the field. We removed all of the females and juveniles from the territories of dominant males in the cleaner wrasse Labroides dimidiatus (Labridae) and the rusty angelfish Centropyge ferrugata (Pomacanthidae) on the coral reefs of Okinawa. In both species, if new females or juveniles did not immigrate into the territories of the widowed males, some of them emigrated to form male–male pairs. When a male–male pair formed, the smaller, subordinate partner began to perform female sexual behaviours (n = 4 in L. dimidiatus; n = 2 in C. ferrugata) and, finally, released eggs (n = 1, respectively). Thus, the reversed sex change occurred in the widowed males according to the change of their social status. These results suggest that such female removal experiments will contribute to the discovery of reversed sex change in the field also in other polygnous and protogynous species.     

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.     

High-field 1H T1 and T2 NMR relaxation time measurements of H2O in homeopathic preparations of quartz, sulfur, and copper sulfate

Quantitative meta-analyses of randomized clinical trials investigating the specific therapeutic efficacy of homeopathic remedies yielded statistically significant differences compared to placebo. Since the remedies used contained mostly only very low concentrations of pharmacologically active compounds, these effects cannot be accounted for within the framework of current pharmacology. Theories to explain clinical effects of homeopathic remedies are partially based upon changes in diluent structure. To investigate the latter, we measured for the first time high-field (600/500 MHz) ¹H T₁ and T₂ nuclear magnetic resonance relaxation times of H₂O in homeopathic preparations with concurrent contamination control by inductively coupled plasma mass spectrometry (ICP-MS). Homeopathic preparations of quartz (10c–30c, n = 21, corresponding to iterative dilutions of 100⁻¹⁰–100⁻³⁰), sulfur (13x–30x, n = 18, 10⁻¹³–10⁻³⁰), and copper sulfate (11c–30c, n = 20, 100⁻¹¹–100⁻³⁰) were compared to n = 10 independent controls each (analogously agitated dilution medium) in randomized and blinded experiments. In none of the samples, the concentration of any element analyzed by ICP-MS exceeded 10 ppb. In the first measurement series (600 MHz), there was a significant increase in T₁ for all samples as a function of time, and there were no significant differences between homeopathic potencies and controls. In the second measurement series (500 MHz) 1 year after preparation, we observed statistically significant increased T₁ relaxation times for homeopathic sulfur preparations compared to controls. Fifteen out of 18 correlations between sample triplicates were higher for controls than for homeopathic preparations. No conclusive explanation for these phenomena can be given at present. Possible hypotheses involve differential leaching from the measurement vessel walls or a change in water molecule dynamics, i.e., in rotational correlation time and/or diffusion. Homeopathic preparations thus may exhibit specific physicochemical properties that need to be determined in detail in future investigations. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

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.     

Cerumen of Australian stingless bees (<Emphasis Type="Italic">Tetragonula carbonaria</Emphasis>): gas chromatography-mass spectrometry fingerprints and potential anti-inflammatory properties

Cerumen, or propolis, is a mixture of plant resins enriched with bee secretions. In Australia, stingless bees are important pollinators that use cerumen for nest construction and possibly for colony’s health. While extensive research attests to the therapeutic properties of honeybee (Apis mellifera) propolis, the biological and medicinal properties of Australian stingless bee cerumen are largely unknown. In this study, the chemical and biological properties of polar extracts of cerumen from Tetragonula carbonaria in South East Queensland, Australia were investigated using gas chromatography-mass spectrometry (GC-MS) analyses and in vitro 5-lipoxygenase (5-LOX) cell-free assays. Extracts were tested against comparative (commercial tincture of A. mellifera propolis) and positive controls (Trolox and gallic acid). Distinct GC-MS fingerprints of a mixed diterpenic profile typical of native bee cerumen were obtained with pimaric acid (6.31 ± 0.97%, w/w), isopimaric acid (12.23 ± 3.03%, w/w), and gallic acid (5.79 ± 0.81%, w/w) tentatively identified as useful chemical markers. Characteristic flavonoids and prenylated phenolics found in honeybee propolis were absent. Cerumen extracts from T. carbonaria inhibited activity of 5-LOX, an enzyme known to catalyse production of proinflammatory mediators (IC₅₀ 19.97 ± 2.67 μg/ml, mean ± SEM, n = 4). Extracts had similar potency to Trolox (IC₅₀ 12.78 ± 1.82 μg/ml), but were less potent than honeybee propolis (IC₅₀ 5.90 ± 0.62 μg/ml) or gallic acid (IC₅₀ 5.62 ± 0.35 μg/ml, P < 0.001). These findings warrant further investigation of the ecological and medicinal properties of this stingless bee cerumen, which may herald a commercial potential for the Australian beekeeping industry.     

Regional,seasonal and interspecific variation in <Superscript>15</Superscript>N and <Superscript>13</Superscript>C in sympatric mouse lemurs

Madagascar provides some of the rare examples where two or more primate species of the same genus and with seemingly identical niche requirements occur in sympatry. If congeneric primate species co-occur in other parts of the world, they differ in size in a way that is consistent with Hutchinson’s rule for coexisting species, or they occupy different ecological niches. In some areas of Madagascar, mouse lemurs do not follow these “rules” and thus seem to violate one of the principles of community ecology. In order to understand the mechanisms that allow coexistence of sympatric congeneric species without obvious niche differentiation, we studied food composition of two identical sized omnivorous mouse lemur species, Microcebus griseorufus and M. murinus with the help of stable isotope analyses (δ ¹⁵N and δ ¹³C). The two species are closely related sister species. During the rich season, when food seems abundant, the two species do not differ in their nitrogen isotope composition, indicating that the two species occupy the same trophic level. But they differ in their δ ¹³C values, indicating that M. griseorufus feeds more on C₄ and CAM (Crassulacean-acid-metabolism) plants than M. murinus. During the lean season, M. murinus has lower δ ¹⁵N values, indicating that the two species feed at different trophic levels during times of food shortage. Hybrids between the two species showed intermediate food composition. The results reflect subtle differences in foraging or metabolic adaptations that are difficult to quantify by traditional observations but that represent possibilities to allow coexistence of species.     

Anatomic and acoustic sexual dimorphism in the sound emission system of Phoenicoprocta capistrata (Lepidoptera: Arctiidae)

Both sexes of Phoenicoprocta capistrata have functional tymbals. The scanning electron microscopy revealed differences in the morphology of these organs in males and females. Male tymbals have a well-developed striated band, constituted by 21 ± 2 regularly arranged striae whereas female tymbals lack a striated band. This type of sexual dimorphism is rare in Arctiidae. The recording of the sound produced by moths held by the wings revealed that while males produced trains of pulses organized in modulation cycles, females produced clicks at low repetition rate following very irregular patterns. Statistically, there are differences between sexes in terms of the duration of pulses, which were 355 ± 24 μs in the case of males and 289 ± 29 μs for females. The spectral characteristics of the pulses also show sexual dimorphism. Male pulses are more tuned (Q ₁₀ = 5.2 ± 0.5) than female pulses (Q ₁₀ = 2.7 ± 0.5) and have a higher best frequency (42 ± 1 kHz vs. 29 ± 2 kHz). To our knowledge, this is the first report on an arctiid moth showing sexual dimorphism in tymbal’s anatomy that leads to a best frequency dimorphism. Males produce sound at mating attempts. The sounds recorded during mating are modulation cycles with the same spectral characteristics as those recorded when males are held by the wings. The morphological and acoustic features of female tymbals could indicate a process of degeneration and adaptation to conditions under which the emission of complex patterns is not necessary. Frank Coro no longer works at Universidad de La Habana.     

Where clocks are redundant: weak circadian mechanisms in reindeer living under polar photic conditions

Biological rhythms are a result of interplay between endogenous clocks and the ambient light–dark (LD) cycle. Biological timing in resident polar organisms presents a conundrum because these experience distinct daily LD cycles for only a few weeks each year. We measured locomotor activity in reindeer, Rangifer tarandus platyrhynchus (SR, n = 5 and 6) and R. tarandus tarandus (NR, n = 6), ranging freely at 78 and 70°N, respectively, continuously throughout 1 year using data loggers. NR, but not SR, are gregarious which enabled us to examine the integrated effects of differences in social organisation and the photic environment at two different latitudes on the organisation of activity. In both sub-species, ultradian bouts of activity and inactivity alternated across the 24-h day throughout the year. This pattern was modified by the LD cycle in NR but barely at all in SR. Periodogram analysis revealed significant ultradian rhythmicity in both sub-species; the frequency of daily cycles of activity increased from three per day in winter to nearly five in summer. We conclude that this increase, and a concomitant increase in the level of daily activity, reflected the seasonal increase in the animals’ appetite and the quality of their forage. Secondly, the combination, most evident in SR, of a weak photic response, weak circadian mechanisms and a weak social synchronization reduces the constraints of biological timing in an environment which is effectively non-rhythmic most of the year and permits expression of the basic ultradian pattern of ruminant activity. Third, the weaker 24-h rhythmicity in SR compared to NR indicates a latitudinal decrease in circadian organization and photic responsiveness in Rangifer.     

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.