Prolonged Torpor Research Articles

ADAPTIVE MODIFICATION<i> </i>OF AMINO ACID POOLS IN THE MYOCARDIUM OF THE LONG-TAILED GROUND SQUIRREL <i>UROCITELLUS UNDULATUS</i> AT DIFFERENT STAGES OF HIBERNATION

The state of hibernation is characterized by increased resistance to the effects of prolonged deep hypothermia, hypoxia, lack of food and water. At the same time, the restructuring of the adaptive mechanisms of animals at low temperatures, even for a short time, causes significant changes in metabolism, reflected in the pattern of amino acids. The change in the metabolism of free myocardial amino acids during hibernation has not yet been studied by anyone, but the idea of it is necessary to understand the mechanisms of the hibernation state, which is relevant for clinical medicine. In this regard, the task of this work was to study the changes in the composition of free amino acids of the myocardium of the ground squirrel U. undulatus at different stages of hibernation. A negative interdependence of glutamic acid and alanine pools at different stages of torpor was revealed. The decrease in the level of glutamic acid compared to the summer control (5.08 ± 0.44 μmolе/g wet weight) began in the first, December bout, continued with prolonged torpor (up to 1.57 ± 0.14 μmolе/g) and was accompanied by a corresponding increase in the alanine pool. During the winter awakening, the glutamic acid pool rose above the summer level; The pool of alanine fell below the summer level, but their total level did not change. The pools of aspartic acid and glycine decreased in parallel with the decrease in pools of glutamate and aspartate, but during the winter awakening, glycine was not even detected. Taking into account the participation of glutamic acid and aspartate in the anaplerotic reactions of the Krebs cycle and the reciprocal relationship of glutamic acid and alanine, it is concluded that the change in the content of these metabolites at different stages of bouts is associated with a gradual transition of aerobic glycolysis (Krebs cycle and oxidative phosphorylation) to anaerobic, and during euthermia, on the contrary, with a return to aerobic.

Heat shock factor 1 induces a short burst of transcription of the clock gene Per2 during interbout arousal in mammalian hibernation

During winter hibernation, a diverse range of small mammals can enter prolonged torpor. They spend the nonhibernation season as a homeotherm but the hibernation season as a heterotherm. In the hibernation season, chipmunks (Tamias asiaticus) cycle regularly between 5 and 6days-long deep torpor with a body temperature (Tb) of 5 to 7 °C and interbout arousal of ∼20h, during which, their Tb returns to the normothermic level. Here, we investigated Per2 expression in the liver to elucidate the regulation of the peripheral circadian clock in a mammalian hibernator. In the nonhibernation season, as in mice, heat shock factor 1, activated by elevated Tb during the wake period, activated Per2 transcription in the liver, which contributed to synchronizing the peripheral circadian clock to the Tb rhythm. In the hibernation season, we determined that the Per2 mRNA was at low levels during deep torpor, but Per2 transcription was transiently activated by heat shock factor 1, which was activated by elevated Tb during interbout arousal. Nevertheless, we found that the mRNA from the core clock gene Bmal1 exhibited arrhythmic expression during interbout arousal. Since circadian rhythmicity is dependent on negative feedback loops involving the clock genes, these results suggest that the peripheral circadian clock in the liver is nonfunctional in the hibernation season.

Evidence for a Growth Zone for Deep-Subsurface Microbial Clades in Near-Surface Anoxic Sediments.

Global marine sediments harbor a large and highly diverse microbial biosphere, but the mechanism by which this biosphere is established during sediment burial is largely unknown. During burial in marine sediments, concentrations of easily metabolized organic compounds and total microbial cell abundance decrease. However, it is unknown whether some microbial clades increase with depth. We show total population increases in 38 microbial families over 3 cm of sediment depth in the upper 7.5 cm of White Oak River (WOR) estuary sediments. Clades that increased with depth were more often associated with one or more of the following: anaerobes, uncultured, or common in deep marine sediments relative to those that decreased. Maximum doubling times (in situ steady-state growth rates could be faster to balance cell decay) were estimated as 2 to 25 years by combining sedimentation rate with either quantitative PCR (qPCR) or the product of the fraction read abundance of 16S rRNA genes and total cell counts (FRAxC). Doubling times were within an order of magnitude of each other in two adjacent cores, as well as in two laboratory enrichments of Cape Lookout Bight (CLB), NC, sediments (average difference of 28% ± 19%). qPCR and FRAxC in sediment cores and laboratory enrichments produced similar doubling times for key deep subsurface uncultured clades Bathyarchaeota (8.7 ± 1.9 years) and Thermoprofundales/MBG-D (4.1 ± 0.7 years). We conclude that common deep subsurface microbial clades experience a narrow zone of growth in shallow sediments, offering an opportunity for selection of long-term subsistence traits after resuspension events.IMPORTANCE Many studies show that the uncultured microbes that dominate global marine sediments do not actually increase in population size as they are buried in marine sediments; rather, they exist in a sort of prolonged torpor for thousands of years. This is because, although studies have shown biomass turnover in these clades, no evidence has ever been found that deeper sediments have larger populations for specific clades than shallower layers. We discovered that they actually do increase population sizes during burial, but only in the upper few centimeters. This suggests that marine sediments may be a vast repository of mostly nongrowing microbes with a thin and relatively rapid area of cell abundance increase in the upper 10 cm, offering a chance for subsurface organisms to undergo natural selection.

The heart of a hibernator: EGFR and MAPK signaling in cardiac muscle during the hibernation of thirteen-lined ground squirrels, Ictidomys tridecemlineatus.

BackgroundThirteen-lined ground squirrels (Ictidomys tridecemlineatus) experience dramatic changes in physiological and molecular parameters during winter hibernation. Notably, these animals experience reduced blood circulation during torpor, which can put numerous stresses on their hearts. The present study evaluates the role played by the epidermal growth factor receptor (EGFR) in signal transduction during hibernation at low body temperature to evaluate signaling mechanisms. By investigating the regulation of intracellular mitogen activated protein kinase (MAPK) pathway responses, anti-apoptosis signals, downstream transcription factors, and heat shock proteins in cardiac muscle we aim to determine the correlation between upstream tyrosine phosphorylation events and downstream outcomes.MethodsProtein abundance of phosphorylated EGFR, MAPKs and downstream effector proteins were quantified using immunoblotting and Luminex® multiplex assays.ResultsMonitoring five time points over the torpor/arousal cycle, EGFR phosphorylation on T654, Y1068, Y1086 was found to increase significantly compared with euthermic control values particularly during the arousal process from torpor, whereas phosphorylation at Y1045 was reduced during torpor. Phosphorylation of intracellular MAPK targets (p-ERK 1/2, p-JNK, p-p38) also increased strongly during the early arousal stage with p-p38 levels also rising during prolonged torpor. However, of downstream MAPK effector kinases that were measured, only p-Elk-1 levels changed showing a decrease during interbout arousal (IA). Apoptosis markers revealed a strong reduction of the pro-apoptotic p-BAD protein during entrance into torpor that remained suppressed through torpor and IA. However, active caspase-9 protein rose strongly during IA. Levels of p-AKT were suppressed during the transition phases into and out of torpor. Of four heat shock proteins assessed, only HSP27 protein levels changed significantly (a 40% decrease) during torpor.ConclusionWe show evidence of EGFR phosphorylation correlating to activation of MAPK signaling and downstream p-ELK1 suppression during hibernation. We also demonstrate a reduction in p-BAD mediated pro-apoptotic signaling during hibernation with active caspase-9 protein levels increasing only during IA. I. tridecemlineatus has natural mechanisms of tissue protection during hibernation that is largely due to cellular regulation through phosphorylation-mediated signaling cascade. We identify a possible link between EGFR and MAPK signaling via p-ERK, p-p38, and p-JNK in the cardiac muscle of these hibernating mammals that correlates with an apparent reduction in caspase-9 apoptotic signaling. This reveals a piece of the mechanism behind how these mammals are resilient to cardiac stresses during hibernation that would otherwise be damaging.

Activity patterns of insectivorous bats during a seasonal transition period from hibernation to reproduction

Bat activity is influenced by fluctuating environmental variables. It may also be influenced by energetic pressures related to pregnancy, lactation, and emergence following winter inactivity. We evaluated nightly changes in relative bat activity at Royal National Park in response to Julian date, ambient temperature, precipitation, wind speed and moon phase on a nightly scale for six weeks during spring, as insectivorous bats move out of hibernation or frequent, prolonged torpor, and into the maternal season. Interestingly, later Julian date (reflecting seasonal transition) was the sole variable that best predicted total nightly activity. In addition, we opportunistically assessed bat activity in response to a severe storm, considered a Category 1 cyclone, resulting in 96.4mm of rain in one night and wind speeds up to 94km h–1. Only one species of bat, Chalinolobus gouldii, was active during the storm, with activity restricted to the latter part of the evening when precipitation had reduced, indicating rapid resumption of activity following severe weather. The results of this research can be used as an indicator of emergence from winter inactivity and highlight activity patterns of bat species in relation to environmental variables to inform timing of monitoring programs, bat surveys, and targeted research.

Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats.

Hibernation, the use of prolonged torpor to depress metabolism, is employed by mammals to conserve resources during extended periods of extreme temperatures and/or resource limitation. Mammalian hibernators arouse to euthermy periodically during torpor for reasons that are not well understood, and these arousals may facilitate immune processes. To determine whether arousals enable host responses to pathogens, we used dual RNA-Seq and a paired sampling approach to examine gene expression in a hibernating bat, the little brown myotis (Myotis lucifugus). During torpor, transcript levels differed in only a few genes between uninfected wing tissue and adjacent tissue infected with Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome. Within 70-80min after emergence from torpor, large changes in gene expression were observed due to local infection, particularly in genes involved in pro-inflammatory host responses to fungal pathogens, but also in many genes involved in immune responses and metabolism. These results support the hypothesis that torpor is a period of relative immune dormancy and arousals allow for local immune responses in infected tissues during hibernation. Host-pathogen interactions were also found to regulate gene expression in the pathogen differently depending on the torpor state of the host. Hibernating species must balance the benefits of energy and water conservation achieved during torpor with the costs of decreased immune competence. Interbout arousals allow hibernators to optimize these, and other, trade-offs during prolonged hibernation by enabling host responses to pathogens within brief, periodic episodes of euthermy.

Thrifty Females, Frisky Males: Winter Energetics of Hibernating Bats from a Cold Climate.

Mammalian hibernation consists of energy-saving torpor bouts (periods of controlled reduction in body temperature [Tb]) interspersed with brief arousals to normothermic Tb. Frequency and duration of torpor bouts and arousals can affect winter survival and are thought to be influenced by an optimization balancing the energetic benefits of prolonged torpor against the physiological and ecological costs (e.g., accumulation of metabolic wastes). Female little brown bats (Myotis lucifugus) spend their fat reserves more slowly than males during winter, presumably so they can emerge from hibernation in good condition to initiate pregnancy. We used temperature telemetry over three winters to test a prediction of the optimization hypothesis that female M. lucifugus would use longer torpor bouts and/or shorter arousals than males. Females did conserve energy relative to males by adjusting the magnitude and duration of arousals but not the duration of torpor bouts. Although torpor bout duration did not vary by sex for adults, it did vary by age. Adults initially used longer torpor bouts than young-of-the-year, but this difference declined as cave temperature warmed in spring. Males and females in better condition spent more energy during hibernation, again via increased arousal duration rather than decreased torpor bout duration. Longer arousals by males could increase reproductive fitness if males mate with torpid females throughout winter. Our results highlight demographic differences in winter behavior for small hibernators facing extreme energy limitation in cold climates and illustrate the influence that reproductive costs have on hibernation energetics.

The effect of brumation on memory retention

Long-term torpor is an adaptive strategy that allows animals to survive harsh winter conditions. However, the impact that prolonged torpor has on cognitive function is poorly understood. Hibernation causes reduced synaptic activity and experiments with mammals reveal that this can have adverse effects on memories formed prior to hibernation. The impact of brumation, the winter dormancy that is observed in ectotherms, on memory remains unknown. The aim of this study was to examine whether an amphibian, the fire salamander (Salamandra salamandra), was able to retain learned spatial information after a period of brumation. Twelve fire salamanders were trained to make a simple spatial discrimination using a T-maze. All subjects learned the initial task. Upon reaching criterion, half of the subjects were placed into brumation for 100 days while the other half served as controls and were maintained under normal conditions. A post-brumation memory retention test revealed that animals from both conditions retained the learned response. Control tests showed that they solved the task using learned information and not olfactory cues. This finding contrasts with much of the mammalian research and suggests that the processes involved in prolonged torpor may have a fundamentally different impact on memory in mammals and amphibians.

Evidence of prolonged torpor in Goodman's mouse lemurs at Ankafobe forest, central Madagascar.

The small-bodied mouse lemurs of Madagascar (Microcebus) are capable of heterothermy (i.e., torpor or hibernation). The expression of these energy-saving strategies has been physiologically demonstrated in three species: M. berthae, the pygmy mouse lemur (daily torpor), M. murinus, the gray mouse lemur (daily torpor and hibernation), and M. griseorufus, the reddish-gray mouse lemur (daily, prolonged torpor and hibernation). Additional evidence, based on radiotracking and seasonal body mass changes, indicated that mouse lemur capabilities for heterothermy extended to M. lehilahytsara, the Goodman's mouse lemur. In this study, we confirm the use of hibernation in Goodman's mouse lemurs at a new location, a high-plateau forest fragment in Ankafobe, central Madagascar. Our evidence is based on sleeping site monitoring of radiocollared individuals and the retrieval of three mouse lemurs from inside a tree hole, all of which displayed a lethargic state. Though our data are preliminary and scant, we show that hibernation occurs in high-plateau mouse lemurs, and suggest that a buffered environment (i.e., tree holes instead of nests) may be crucial to avoiding potentially extreme ambient temperatures.

The effect of body mass and diet composition on torpor patterns in a Malagasy primate (Microcebus murinus).

One of the most obvious physiological changes accompanying seasonal heterothermy in mammals is a fattening stage preceding periods of resource scarcity. This phenomenon reflects the interplay of both diet and physiology. Though the accrual of fat stores is known to be essential for overwintering in some species, the influence of diet on the physiology of torpor is not fully understood. Results from captive studies in heterothermic rodents and marsupials have indicated that when autumn diets are enriched with polyunsaturated fatty acids (PUFAs), animals receiving these diets experience deeper and more frequent torpor bouts than their counterparts receiving a control diet. Our study investigates this potential effect of dietary composition in animals that use daily torpor rather than prolonged torpor (i.e., hibernation). In so doing, we investigate the degree to which dietary effects on torpor are restricted to cold-adapted rodents and marsupials, or are a more general feature of mammalian heterothermy. We examined the effects of a PUFA diet and a control diet on the thermoregulation of one of the few species of primates known to use daily torpor: the grey mouse lemur (Microcebus murinus). Though the results of this study are largely inconclusive regarding the impact of dietary manipulations on torpor frequency and duration, we nonetheless find that the propensity of animals to enter torpor is directly influenced by age and seasonal changes in body mass, and thus reflect important physiological aspects of flexible thermoregulatory responses.

Telomere dynamics in free-living edible dormice (Glis glis): the impact of hibernation and food supply.

ABSTRACTWe studied the impact of hibernation and food supply on relative telomere length (RTL), an indicator for aging and somatic maintenance, in free-living edible dormice. Small hibernators such as dormice have ∼50% higher maximum longevity than non-hibernators. Increased longevity could theoretically be due to prolonged torpor directly slowing cellular damage and RTL shortening. However, although mitosis is arrested in mammals at low body temperatures, recent evidence points to accelerated RTL shortening during periodic re-warming (arousal) from torpor. Therefore, we hypothesized that these arousals during hibernation should have a negative effect on RTL. Here, we show that RTL was shortened in all animals over the course of ∼1 year, during which dormice hibernated for 7.5–11.4 months. The rate of periodic arousals, rather than the time spent euthermic during the hibernation season, was the best predictor of RTL shortening. This finding points to negative effects on RTL of the transition from low torpor to high euthermic body temperature and metabolic rate during arousals, possibly because of increased oxidative stress. The animals were, however, able to elongate their telomeres during the active season, when food availability was increased by supplemental feeding in a year of low natural food abundance. We conclude that in addition to their energetic costs, periodic arousals also lead to accelerated cellular damage in terms of RTL shortening. Although dormice are able to counteract and even over-compensate for the negative effects of hibernation, restoration of RTL appears to be energetically costly.

Unpredictable environments, opportunistic responses: Reproduction and population turnover in two wild mouse lemur species (Microcebus rufus and M. griseorufus) from eastern and western Madagascar.

Small-bodied, nocturnal mouse lemurs (Microcebus) are widespread across diverse forest habitats in Madagascar. They are strict seasonal breeders and can, depending on the habitat and species, undergo daily or prolonged torpor to minimize energy expenditure during periods of food and water scarcity. Duration of reproduction, number of litters per season and timing of births vary across individuals and species. The "polyestry-seasonality" hypothesis proposes that the duration of reproduction and number of litters per year are positively correlated with rainfall but negatively correlated with longevity, whereas the "hypervariability" hypothesis suggests that the duration of reproduction is negatively correlated with the degree of predictability of food resources. We test these hypotheses in two mouse lemur species inhabiting contrasting habitats, the brown mouse lemurs, Microcebus rufus, from Ranomafana (a less seasonal and more climatically predictable habitat) and the gray-brown mouse lemurs, M. griseorufus, from Beza Mahafaly (a more seasonal and less climatically predictable environment). We use capture/mark/recapture techniques and records of female reproductive status. We found evidence of polyestry at both study sites but faster population turnover and longer duration of the reproductive season at Beza Mahafaly. The "polyestry-seasonality" hypothesis is not supported but the "hypervariability" hypothesis could not be rejected. We conclude that reproductive output cannot be tied to climatic factors in a simple manner. Paradoxically, polyestry can be expressed in contrasting habitats: less seasonal forests where females can sustain multiple reproductive events, but also highly seasonal environments where females may not fatten sufficiently to sustain prolonged torpor but instead remain active throughout the year by relying on fallback resources. Am. J. Primatol. 77:936-947, 2015. © 2015 Wiley Periodicals, Inc.

Antioxidant system in Uromastyx philbyi during hibernation and activity periods

AbstractHibernation is an extreme physiological state characterized by profound decreases in oxidative metabolism and body temperature during bouts of prolonged torpor, interrupted by brief periods of arousal with sudden increases in oxidative metabolism, with alterations in antioxidant defenses. We monitored the activities of antioxidant enzymes and oxidative stress during hibernation and activity in Uromastyx philbyi. 20 animals were used, 10 of which were collected in the hibernation season (group I) and the other 10 collected during the active period (group II). Blood, liver, brown adipose tissue (BAT) and brain samples were used to determine free radical and antioxidant levels. The results indicated a significant decrease of free radicals and increase of vitamin C, especially in serum during hibernation. In contrast, during the active period free radicals, enzymatic antioxidants as glutathione peroxidase (GPX), glutathione reductase (GR), superoxide dismutase (SOD) and catalase (CAT) and non-enzymatic antioxidants as reduce glutathione (GSH) and vitamin E increased in all studied tissues. It can be concluded that Uromastyx philbyi has a strong antioxidant defense system that protects it from the injurious effects of free radicals either at the periods of arousal or during activity periods.

Flexible patterns in energy savings: heterothermy in primates

AbstractHeterothermy is an energy‐saving strategy usually employed in response to environmental bottlenecks, which is common in almost all mammalian orders. Within the order primates, heterothermy has been physiologically confirmed only in the family Cheirogaleidae (Cheirogaleus, Microcebus, Allocebus, Mirza) of the Malagasy lemurs, and the southern lesser bushbaby (Galago moholi) of the family Galagonidae. These closely related species employ a spectrum of daily torpor, prolonged torpor and obligate hibernation under tropical, but nevertheless seasonal and energetically demanding conditions. There is a remarkable physiological flexibility in regard to their thermoregulatory adaptations not only between species of the same genera within one habitat, but also between populations of the same species, within populations and even within the same individual, permitting immediate responses in seasonal and unpredictable environments, and possibly aiding these species to master challenges of globally changing climatic conditions. Whereas heterothermy is a flexible, but regular seasonal response in the Cheirogaleidae, it is only used as a last emergency strategy in G. moholi. In the other primate species, there is either no or only anecdotal evidence of only minor reductions in metabolic rate, presumably rather reflecting pronounced circadian cycles in body temperature, or local heterothermy. Maybe because of their relatively high degree of sociality and larger body sizes, behavioural and ecological adaptations to seasonality are selected for in other primates.

Body mass dependent use of hibernation: why not prolong the active season, if they can?

Summary Hibernation is the most effective means for energy conservation during winter in mammals. The drawbacks of deep and prolonged torpor include reduced immunocompetence, and consequently, hibernators should be selected to minimize torpor expression when climatic conditions or energy availability (e.g. food or fat stores) permit. Therefore, it seems surprising that some hibernators employ extraordinary long hibernation seasons, lasting well beyond periods with unfavourable conditions. Because of their extended use of torpor, edible dormice (Glis glis) provide an ideal model for scrutinizing interactions between energy reserves (i.e. body fat stores) and thermoregulatory patterns. We used a multimodel inference approach to analyse body temperature data (i.e. use of torpor) from 42 entire hibernation seasons over 4 years in females in relation to body mass. Body mass prior to hibernation did not affect the duration of the hibernation season, but animals hibernated for c. 8 months, that is, 2 months longer than required by environmental conditions. Fatter individuals aroused significantly more often, had a higher mean minimum body temperature during torpor and remained euthermic for longer periods than leaner animals. Surplus energy was therefore not used to shorten the hibernation season, but to rewarm more frequently, and to allow shallower torpor bouts. These adjustments apparently serve to avoid negative effects of torpor and, perhaps equally importantly, to minimize the time active above‐ground. We argue that maintaining a short active season, despite surplus energy reserves, may be explained by known beneficial effects of hibernation on survival rates (via predator avoidance). Our data provide quantitative evidence that hibernation is a flexible tool within life‐history strategies. We conclude that, apart from energetic necessities due to harsh environmental conditions, predator avoidance may be an important factor influencing patterns of hibernation and torpor in mammals. Thus, our study indicates that climatic conditions alone are not a good predictor of hibernation patterns or survival in hibernating species during global climate change.

4. Mammalian hibernation – Clinical implications

Hibernating mammals have amazing capabilities that we, as humans, can only envy. They may spend up to 8 months of the winter in bouts of prolonged torpor with metabolic rates www.carleton.ca/∼kbstorey .

Nitric oxide synthase-dependent “On/Off” switch and apoptosis in freshwater and aestivating lungfish, Protopterus annectens: Skeletal muscle versus cardiac muscle

African lungfishes (Protopterus spp.) are obligate air breathers which enter in a prolonged torpor (aestivation) in association with metabolic depression, and biochemical and morpho-functional readjustments during the dry season. During aestivation, the lungfish heart continues to pump, while the skeletal muscle stops to function but can immediately contract during arousal. Currently, nothing is known regarding the orchestration of the multilevel rearrangements occurring in myotomal and myocardial muscles during aestivation and arousal. Because of its universal role in cardio-circulatory and muscle homeostasis, nitric oxide (NO) could be involved in coordinating these stress-induced adaptations.Western blotting and immunofluorescence microscopy on cardiac and skeletal muscles of Protopterus annectens (freshwater, 6months of aestivation and 6days after arousal) showed that expression, localization and activity of the endothelial-like nitric oxide synthase (eNOS) isoform and its partners Akt and Hsp-90 are tissue-specifically modulated. During aestivation, phospho-eNOS/eNOS and phospho-Akt/Akt ratios increased in the heart but decreased in the skeletal muscle. By contrast, Hsp-90 increased in both muscle types during aestivation. TUNEL assay revealed that increased apoptosis occurred in the skeletal muscle of aestivating lungfish, but the myocardial apoptotic rate of the aestivating lungfish remained unchanged as compared with the freshwater control. Consistent with the preserved cardiac activity during aestivation, the expression of apoptosis repressor (ARC) also remained unchanged in the heart of aestivating and aroused fish as compared with the freshwater control. Contrarily, ARC expression was strongly reduced in the skeletal muscle of aestivating lungfish.On the whole, our data indicate that changes in the eNOS/NO system and cell turnover are implicated in the morpho-functional readjustments occurring in lungfish cardiac and skeletal muscle during the switch from freshwater to aestivation, and between the maintenance and arousal phases of aestivation.

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 (Tsc) 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 Tsc, spent more time at Tsc below their individual lower limit of normothermia, and had a higher Heterothermy Index than controls. Five individuals entered prolonged torpor bouts lasting more than 24h, 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.

RAISING THE ‘DEAD’ – REPERFUSION FROM TORPOR

> Kelly Drew discusses Paul Chatfield and Charles Lyman's classic paper ‘Circulatory changes during the process of arousal in the hibernating hamster’, published in the American Journal of Physiology in 1950. Over 60 years ago, Paul Chatfield and Charles Lyman described fundamental

Anti-apoptotic signaling as a cytoprotective mechanism in mammalian hibernation

In the context of normal cell turnover, apoptosis is a natural phenomenon involved in making essential life and death decisions. Apoptotic pathways balance signals which promote cell death (pro-apoptotic pathways) or counteract these signals (anti-apoptotic pathways). We proposed that changes in anti-apoptotic proteins would occur during mammalian hibernation to aid cell preservation during prolonged torpor under cellular conditions that are highly injurious to most mammals (e.g. low body temperatures, ischemia). Immunoblotting was used to analyze the expression of proteins associated with pro-survival in six tissues of thirteen-lined ground squirrels, Ictidomys tridecemlineatus. The brain showed a concerted response to torpor with significant increases in the levels of all anti-apoptotic targets analyzed (Bcl-2, Bcl-xL, BI-1, Mcl-1, cIAP1/2, xIAP) as well as enhanced phosphorylation of Bcl-2 at S70 and T56. Heart responded similarly with most anti-apoptotic proteins elevated significantly during torpor except for Bcl-xL and xIAP that decreased and Mcl-1 that was unaltered. In liver, BI-1 increased whereas cIAP1/2 decreased. In kidney, there was an increase in BI-1, cIAP and xIAP but decreases in Bcl-xL and p-Bcl-2(T56) content. In brown adipose tissue, protein levels of BI-1, cIAP1/2, and xIAP decreased significantly during torpor (compared with euthermia) whereas Bcl-2, Bcl-xL, Mcl-1 were unaltered; however, Bcl-2 showed enhanced phosphorylation at Thr56 but not at Ser70. In skeletal muscle, only xIAP levels changed significantly during torpor (an increase). The data show that anti-apoptotic pathways have organ-specific responses in hibernators with a prominent potential role in heart and brain where coordinated enhancement of anti-apoptotic proteins occurred in response to torpor.