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1.
PLoS Pathog ; 20(8): e1012342, 2024 Aug.
Article in English | MEDLINE | ID: mdl-39207947

ABSTRACT

The emergence of white-nose syndrome (WNS) in North America has resulted in mass mortalities of hibernating bats and total extirpation of local populations. The need to mitigate this disease has stirred a significant body of research to understand its pathogenesis. Pseudogymnoascus destructans, the causative agent of WNS, is a psychrophilic (cold-loving) fungus that resides within the class Leotiomycetes, which contains mainly plant pathogens and is unrelated to other consequential pathogens of animals. In this review, we revisit the unique biology of hibernating bats and P. destructans and provide an updated analysis of the stages and mechanisms of WNS progression. The extreme life history of hibernating bats, the psychrophilic nature of P. destructans, and its evolutionary distance from other well-characterized animal-infecting fungi translate into unique host-pathogen interactions, many of them yet to be discovered.


Subject(s)
Ascomycota , Chiroptera , Hibernation , Chiroptera/microbiology , Animals , Ascomycota/pathogenicity , Hibernation/physiology , Host-Pathogen Interactions , Mycoses/veterinary , Mycoses/microbiology , Dermatomycoses/veterinary , Dermatomycoses/microbiology , Dermatomycoses/pathology , Skin/microbiology , Skin/pathology , White
2.
PLoS One ; 19(8): e0307551, 2024.
Article in English | MEDLINE | ID: mdl-39197002

ABSTRACT

The effect of hibernation on cognitive capacities of individuals is not fully understood, as studies provide conflicting results. Most studies focus on behavioural observations without taking the physiological state of individuals to account. To mechanistically understand the effect of hibernation on the brain, physiological parameters need to be included. The implantation of bio-loggers can provide insights on i.e. body temperature without further manipulation of the animals. Surgeries and anaesthesia, however, can harm animals' health and cause cognitive dysfunction, potentially biasing data collected through bio-loggers. We investigated the effects of bio-logger implantation surgery on cognitive performance and learning, controlling for animal and study design characteristics. First, juvenile dormice successfully learned to solve a spatial cognition task using a vertical maze. Distance, transitions, velocity, and duration were measured as indicators for performance. After training, bio-loggers were implanted intra-abdominally under general anaesthesia. Animals were re-tested in the maze two weeks after. We found no effect of bio-logger implantation and surgery on performance. This study is the first to show spatial cognition learning in edible dormice and provides a full description of the peri-anaesthetic management and a protocol for bio-logger implantation surgery in dormice. Importantly, measures were taken to mitigate common anaesthetic complications that could lead to post-operative cognitive dysfunction and influence animal behaviour. By pairing physiological measurements through bio-logger implantation with behaviour and cognition measurements, future research will significantly advance the understanding on mechanisms of learning and behaviour.


Subject(s)
Anesthesia, General , Cognition , Hibernation , Animals , Cognition/physiology , Hibernation/physiology , Maze Learning , Spatial Learning , Male
3.
Sci Total Environ ; 948: 174852, 2024 Oct 20.
Article in English | MEDLINE | ID: mdl-39029756

ABSTRACT

Bumblebees and other key pollinators are experiencing global declines, a phenomenon driven by multiple environmental stressors, including pesticide exposure. While bumblebee queens spend most of their life hibernating underground, no study to date has examined how exposure to pesticide-contaminated soils might affect bumblebee queens during this solitary phase of their lifecycle. We exposed Bombus impatiens queens (n = 303) to soil treated with field-realistic concentrations of two diamide insecticides (chlorantraniliprole and cyantraniliprole) and two fungicides (boscalid and difenoconazole), alone or combined, during a 30-week hibernation period. We found that exposure to boscalid residues in soil doubled the likelihood of queens surviving through the colony initiation period (after successful hibernation) and laying eggs. Our data also revealed complex interactions between pesticide exposure and queen body mass on aspects of colony founding. Among others, exposure to cyantraniliprole led to lethal and sublethal post-hibernation effects that were dependent on queen size, with larger queens showing higher mortality rates, delayed emergence of their first brood, and producing smaller workers. Our results show that effects of pesticide exposure depend on intrinsic traits of bumblebee queen physiology and challenge our understanding of how bees respond to pesticides under environmentally realistic exposure scenarios.


Subject(s)
Hibernation , Pesticide Residues , Soil Pollutants , Animals , Bees/physiology , Bees/drug effects , Pesticide Residues/analysis , Female , Hibernation/physiology , Soil Pollutants/toxicity , Soil Pollutants/analysis , ortho-Aminobenzoates/toxicity , Insecticides/toxicity , Insecticides/analysis , Biphenyl Compounds , Fungicides, Industrial/toxicity , Pyrazoles/toxicity , Triazoles/toxicity , Body Size/drug effects , Dioxolanes , Niacinamide/analogs & derivatives
4.
PLoS One ; 19(7): e0306537, 2024.
Article in English | MEDLINE | ID: mdl-39083476

ABSTRACT

In wild brown bears, likely factors triggering hibernation response to harsh environmental conditions are temperature, photoperiod, and food resources availability. In fact, constantly fed captive brown bears are described as skipping hibernation being active all year-round. Is the hibernation response so flexible and subordinate to contingencies, or else is an adaptation that, if dismissed, may negatively impact on bear well-being? This study investigates the potential hibernation response in captive brown bears under unvaried management conditions using an integrative approach simultaneously analyzing multiple animal-based variables together with environmental covariates. Data from a mid-latitude zoo revealed distinct behavioral, fecal glucocorticoids, and body condition score seasonal fluctuations, resembling natural hibernation cycles, despite constant food access. Environmental variables like photoperiod and visitor numbers significantly influenced activity levels. Bears exhibited behaviors indicative of hyperphagia and fall transition, such as appetitive feeding and denning behaviors. Hormonal analyses revealed high fecal cortisol metabolites levels during hyperphagia, suggesting physiological responses to seasonal changes. Findings underscore the importance of environmental cues and food availability in shaping zoo bear behavior and physiology. Considering that the hibernating vs. non-hibernating description might represent an oversimplification, management strategies should deal with captive bear potential need to freely express their adaptive predispositions by accommodating their natural behaviors, such as providing denning spots and adjusting diet composition as soon as typical hyperphagic and predenning behaviors emerge, ultimately enhancing their well-being.


Subject(s)
Animals, Zoo , Hibernation , Seasons , Ursidae , Animals , Ursidae/physiology , Hibernation/physiology , Animals, Zoo/physiology , Male , Female , Hydrocortisone/metabolism , Hydrocortisone/analysis , Behavior, Animal/physiology , Cues , Animal Welfare , Photoperiod , Feces/chemistry , Environment
5.
J Therm Biol ; 123: 103909, 2024 Jul.
Article in English | MEDLINE | ID: mdl-39084175

ABSTRACT

Fine-scale variation in microclimates between habitats may impact energy consumption for the organisms that inhabit them. This may be particularly important for sedentary species or those unable to change habitats for long periods, such as hibernators. Low ambient temperatures were traditionally thought key to microclimatic selection for hibernation locations, but recent research suggests that other factors may contribute or exceed ambient temperature in importance. We aimed to characterise microclimates at hibernacula of wild hibernating hazel dormice Muscardinus avellanarius, and test how these microclimates differ to those at locations without hibernacula using a microclimatic modelling approach. Dormice hibernated in areas with warmer soil temperatures and lower variability in humidity and relative shortwave radiation. These results add to the growing body of evidence that low ambient temperatures may not be the primary driver of hibernation microclimate selection, although temperature is still likely to play an important role. We also found that ambient temperatures measured at the microclimatic level were substantially buffered compared to point samples taken at the nearest weather station (∼1.6 km away), highlighting the importance of considering microclimates in wildlife conservation in the face of future environmental change.


Subject(s)
Hibernation , Microclimate , Animals , Hibernation/physiology , Seasons , Temperature , Myoxidae/physiology , Nesting Behavior , Ecosystem
6.
Sci Transl Med ; 16(758): eadg3894, 2024 Jul 31.
Article in English | MEDLINE | ID: mdl-39083588

ABSTRACT

Patients receiving mechanical ventilation in the intensive care unit (ICU) frequently develop contractile weakness of the diaphragm. Consequently, they may experience difficulty weaning from mechanical ventilation, which increases mortality and poses a high economic burden. Because of a lack of knowledge regarding the molecular changes in the diaphragm, no treatment is currently available to improve diaphragm contractility. We compared diaphragm biopsies from ventilated ICU patients (N = 54) to those of non-ICU patients undergoing thoracic surgery (N = 27). By integrating data from myofiber force measurements, x-ray diffraction experiments, and biochemical assays with clinical data, we found that in myofibers isolated from the diaphragm of ventilated ICU patients, myosin is trapped in an energy-sparing, super-relaxed state, which impairs the binding of myosin to actin during diaphragm contraction. Studies on quadriceps biopsies of ICU patients and on the diaphragm of previously healthy mechanically ventilated rats suggested that the super-relaxed myosins are specific to the diaphragm and not a result of critical illness. Exposing slow- and fast-twitch myofibers isolated from the diaphragm biopsies to small-molecule compounds activating troponin restored contractile force in vitro. These findings support the continued development of drugs that target sarcomere proteins to increase the calcium sensitivity of myofibers for the treatment of ICU-acquired diaphragm weakness.


Subject(s)
Diaphragm , Muscle Contraction , Myosins , Respiration, Artificial , Respiratory Muscles , Humans , Animals , Myosins/metabolism , Diaphragm/metabolism , Diaphragm/physiopathology , Respiratory Muscles/metabolism , Rats , Male , Intensive Care Units , Middle Aged , Female , Aged , Hibernation/physiology , Actins/metabolism
7.
Nat Commun ; 15(1): 5803, 2024 Jul 10.
Article in English | MEDLINE | ID: mdl-38987241

ABSTRACT

Mammalian hibernators survive prolonged periods of cold and resource scarcity by temporarily modulating normal physiological functions, but the mechanisms underlying these adaptations are poorly understood. The hibernation cycle of thirteen-lined ground squirrels (Ictidomys tridecemlineatus) lasts for 5-7 months and comprises weeks of hypometabolic, hypothermic torpor interspersed with 24-48-h periods of an active-like interbout arousal (IBA) state. We show that ground squirrels, who endure the entire hibernation season without food, have negligible hunger during IBAs. These squirrels exhibit reversible inhibition of the hypothalamic feeding center, such that hypothalamic arcuate nucleus neurons exhibit reduced sensitivity to the orexigenic and anorexigenic effects of ghrelin and leptin, respectively. However, hypothalamic infusion of thyroid hormone during an IBA is sufficient to rescue hibernation anorexia. Our results reveal that thyroid hormone deficiency underlies hibernation anorexia and demonstrate the functional flexibility of the hypothalamic feeding center.


Subject(s)
Anorexia , Ghrelin , Hibernation , Hypothalamus , Sciuridae , Animals , Hibernation/physiology , Sciuridae/physiology , Anorexia/physiopathology , Anorexia/metabolism , Hypothalamus/metabolism , Ghrelin/metabolism , Ghrelin/deficiency , Leptin/deficiency , Leptin/metabolism , Arcuate Nucleus of Hypothalamus/metabolism , Neurons/metabolism , Neurons/physiology , Male , Thyroid Hormones/metabolism , Arousal/physiology , Female , Seasons , Feeding Behavior/physiology
8.
Ecol Evol Physiol ; 97(3): 180-189, 2024.
Article in English | MEDLINE | ID: mdl-38875137

ABSTRACT

AbstractDuring periods of torpor, hibernators can reduce metabolic rate (MR) and body temperature (Tb) substantially. However, to avoid physiological dysfunction at low temperatures, they defend Tb at a critical minimum, often between ~0°C and 10°C via an increase in MR. Because thermoregulation during torpor requires extra energy, individuals with lower Tb's and thus minimal MR during torpor should be selected in colder climates. Such inter- and intraspecific variations occur in some placental mammals, but for the evolutionary separate marsupials, available information is scarce. Marsupial eastern pygmy possums (Cercartetus nanus; ~22 g body mass), widely distributed along the Australian southeastern coast including subtropical to alpine areas, were used to test the hypothesis that the defended Tb of torpid individuals is related to the climate of their habitat. Possums were captured from five regions, 1,515 km apart, with midwinter (July) minimum environmental temperatures (min Tenv's) ranging from -3.9°C to 6.6°C. Captive possums in deep torpor were slowly cooled with ambient temperature (Ta), while their MR was measured to determine the minimum torpor metabolic rate (TMR), the Ta at which their MR increased for thermoregulation (min Ta), and the corresponding minimum Tb (min Tb). Partial least squares regression analysis revealed that Ta and Tenv were the strongest explanatory variables for the min Tb. The min Tb and Ta were also correlated with latitude but not elevation of the capture sites. However, the best correlations were observed between the min Tenv and the min Tb and Ta for individuals experiencing min Tenv>0°C; these individuals thermoconformed to min Ta's between -0.8°C and 3.7°C, and their min Tb ranged from 0.5°C to 6.0°C and was 0.5°C-2.6°C below the min Tenv at the capture site. In contrast, individuals experiencing a min Tenv of -3.9°C regulated Tb at 0.6°C±0.2°C or 4.5°C above the Tenv. The minimum TMR of all possums did not differ with Ta and thus did not differ among populations and was 2.6% of the basal MR. These data provide new evidence that thermal variables of marsupials are subject to regional intraspecific variation. It suggests that min Tb is a function of the min Tenv but only above 0°C, perhaps because the Tb-Ta differential for torpid possums in the wild, at a min Tenv of -3.9°C, remains small enough to be compensated by a small increase in MR and does not require the physiological capability for a reduction of Tb below 0°C.


Subject(s)
Body Temperature Regulation , Animals , Body Temperature Regulation/physiology , Basal Metabolism/physiology , Hibernation/physiology , Marsupialia/physiology , Australia , Body Temperature/physiology , Temperature , Species Specificity , Female
9.
Article in English | MEDLINE | ID: mdl-38810773

ABSTRACT

Spotted stem borer, Chilo partellus, undergoes larval diapause (hibernation and aestivation), and depends on the food reserve accumulated during feeding stage for its survival. Lipids are the primary source of energy during diapause, and essential for different cellular, biochemical and physiological functions. However, there is no information on lipid and lipophilic compound contents during different stages of hibernation, aestivation and nondiapause in C. partellus. Thus, we compared the concentration and composition of lipids in pre-diapause, diapause and post-diapause stages of hibernation and aestivation with nondiapause stages of C. partellus. The studies revealed significant differences in total lipids and various lipophilic compounds during different stages of diapause as compared to nondiapause C. partellus. The total lipids were significantly lower during diapause stage of aestivation and hibernation as compared to nondiapause larvae. Further, the linoleic acid, Methyl 3-methoxytetradecanoate, and l-(+)-Ascorbic acid 2,6-dihexadecanoate were significantly lower, and oleic and palmitoleic acids greater during pre-diapause and diapause stages of hibernation and aestivation as compared to nondiapause larvae. The cholesterol content was significantly greater during pre-diapause stage of hibernation, and diapause and post-diapause stages of aestivation as compared to nondiapause stages. The unsaturation ratio was significantly higher in the pre-diapause and diapause stages and lower in post-diapause stage of aestivation than the hibernation and nondiapause states. This study provides insights on differential lipid profiles during different phases of diapause, which could be useful for further understanding biochemical and physiological cross-talk, and develop target-specific technologies for the management of C. partellus.


Subject(s)
Diapause, Insect , Larva , Moths , Animals , Diapause, Insect/physiology , Moths/physiology , Moths/growth & development , Larva/physiology , Larva/growth & development , Lipids/chemistry , Hibernation/physiology , Lipid Metabolism/physiology , Linoleic Acid/metabolism , Diapause/physiology
10.
Ecol Evol Physiol ; 97(1): 53-63, 2024.
Article in English | MEDLINE | ID: mdl-38717368

ABSTRACT

AbstractMany animals follow annual cycles wherein physiology and behavior change seasonally. Hibernating mammals undergo one of the most drastic seasonal alterations of physiology and behavior, the timing of which can have significant fitness consequences. The environmental cues regulating these profound phenotypic changes will heavily influence whether hibernators acclimate and ultimately adapt to climate change. Hence, identifying the cues and proximate mechanisms responsible for hibernation termination timing is critical. Northern Idaho ground squirrels (Urocitellus brunneus)-a rare, endemic species threatened with extinction-exhibit substantial variation in hibernation termination phenology, but it is unclear what causes this variation. We attached geolocators to free-ranging squirrels to test the hypothesis that squirrels assess surface conditions in spring before deciding whether to terminate seasonal heterothermy or reenter torpor. Northern Idaho ground squirrels frequently reentered torpor following a brief initial emergence from hibernacula and were more likely to do so earlier in spring or when challenged by residual snowpack. Female squirrels reentered torpor when confronted with relatively shallow snowpack upon emergence, whereas male squirrels reentered torpor in response to deeper spring snowpack. This novel behavior was previously assumed to be physiologically constrained in male ground squirrels by testosterone production required for spermatogenesis and activated by the circannual clock. Assessing surface conditions to decide when to terminate hibernation may help buffer these threatened squirrels against climate change. Documenting the extent to which other hibernators can facultatively alter emergence timing by reentering torpor after emergence will help identify which species are most likely to persist under climate change.


Subject(s)
Hibernation , Sciuridae , Seasons , Snow , Animals , Sciuridae/physiology , Hibernation/physiology , Female , Male , Torpor/physiology
11.
J Therm Biol ; 121: 103866, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38718621

ABSTRACT

To find out whether a social subterranean rodent-the northern mole vole (Ellobius talpinus)-hibernates in winter, nine individuals from Southern Siberia were captured in late autumn and implanted with loggers [that constantly recorded body temperature (Tb) and locomotor activity] and then released. Eight of them were recaptured the following spring. From October to April, the animals' Tb never dropped below 33 °C, although cosinor analysis revealed a decrease in mesor values and in the amplitude of daily fluctuations of Tb and activity in winter months. Spectral density of circadian rhythms of both indexes also diminished in winter. The magnitude of Tb and fluctuations of activity differed between the two studied familial groups, probably due to their unequal numbers of individuals, which could affect the total heat production. The levels and patterns of temperature and activity fluctuations observed in winter rule out the possibility of hibernation in this species.


Subject(s)
Arvicolinae , Body Temperature , Seasons , Animals , Arvicolinae/physiology , Locomotion , Circadian Rhythm , Male , Hibernation/physiology , Female , Motor Activity
12.
Elife ; 132024 May 16.
Article in English | MEDLINE | ID: mdl-38752835

ABSTRACT

Hibernation is a period of metabolic suppression utilized by many small and large mammal species to survive during winter periods. As the underlying cellular and molecular mechanisms remain incompletely understood, our study aimed to determine whether skeletal muscle myosin and its metabolic efficiency undergo alterations during hibernation to optimize energy utilization. We isolated muscle fibers from small hibernators, Ictidomys tridecemlineatus and Eliomys quercinus and larger hibernators, Ursus arctos and Ursus americanus. We then conducted loaded Mant-ATP chase experiments alongside X-ray diffraction to measure resting myosin dynamics and its ATP demand. In parallel, we performed multiple proteomics analyses. Our results showed a preservation of myosin structure in U. arctos and U. americanus during hibernation, whilst in I. tridecemlineatus and E. quercinus, changes in myosin metabolic states during torpor unexpectedly led to higher levels in energy expenditure of type II, fast-twitch muscle fibers at ambient lab temperatures (20 °C). Upon repeating loaded Mant-ATP chase experiments at 8 °C (near the body temperature of torpid animals), we found that myosin ATP consumption in type II muscle fibers was reduced by 77-107% during torpor compared to active periods. Additionally, we observed Myh2 hyper-phosphorylation during torpor in I. tridecemilineatus, which was predicted to stabilize the myosin molecule. This may act as a potential molecular mechanism mitigating myosin-associated increases in skeletal muscle energy expenditure during periods of torpor in response to cold exposure. Altogether, we demonstrate that resting myosin is altered in hibernating mammals, contributing to significant changes to the ATP consumption of skeletal muscle. Additionally, we observe that it is further altered in response to cold exposure and highlight myosin as a potentially contributor to skeletal muscle non-shivering thermogenesis.


Many animals use hibernation as a tactic to survive harsh winters. During this dormant, inactive state, animals reduce or limit body processes, such as heart rate and body temperature, to minimise their energy use. To conserve energy during hibernation, animals can use different approaches. For example, garden dormice undergo periodic states of extremely low core temperatures (down to 4­8oC); whereas Eurasian brown bears see milder temperature drops (down to 23­25oC). An important organ that changes during hibernation is skeletal muscle. Skeletal muscle typically uses large amounts of energy, making up around 50% of body mass. To survive, hibernating animals must change how their skeletal muscle uses energy. Traditionally, active myosin ­ a protein found in muscles that helps muscles to contract ­ was thought to be responsible for most of the energy use by skeletal muscle. But, more recently, resting myosin has also been found to use energy when muscles are relaxed. Lewis et al. studied myosin and skeletal muscle energy use changes during hibernation and whether they could impact the metabolism of hibernating animals. Lewis et al. assessed myosin changes in muscle samples from squirrels, dormice and bears during hibernation and during activity. Experiments showed changes in resting myosin in squirrels and dormice (whose temperature drops to 4­8oC during hibernation) but not in bears. Further analysis revealed that cooling samples from non-hibernating muscle to 4­8oC increased energy use in resting myosin, thereby generating heat. However, no increase in energy use was found after cooling hibernating muscle samples to 4­8oC. This suggest that resting myosin generates heat at cool temperatures ­ a mechanism that is switched off in hibernating animals to allow them to cool their body temperature. These findings reveal key insights into how animals conserve energy during hibernation. In addition, the results show that myosin regulates energy use in skeletal muscles, which indicates myosin may be a potential drug target in metabolic diseases, such as obesity.


Subject(s)
Hibernation , Animals , Hibernation/physiology , Energy Metabolism , Skeletal Muscle Myosins/metabolism , Ursidae/metabolism , Ursidae/physiology , Adenosine Triphosphate/metabolism , Muscle, Skeletal/metabolism , Muscle, Skeletal/physiology , Muscle Fibers, Skeletal/metabolism , Proteomics
13.
BMC Genomics ; 25(1): 454, 2024 May 08.
Article in English | MEDLINE | ID: mdl-38720264

ABSTRACT

BACKGROUND: In response to seasonal cold and food shortage, the Xizang plateau frogs, Nanorana parkeri (Anura: Dicroglossidae), enter a reversible hypometabolic state where heart rate and oxygen consumption in skeletal muscle are strongly suppressed. However, the effect of winter hibernation on gene expression and metabolic profiling in these two tissues remains unknown. In the present study, we conducted transcriptomic and metabolomic analyses of heart and skeletal muscle from summer- and winter-collected N. parkeri to explore mechanisms involved in seasonal hibernation. RESULTS: We identified 2407 differentially expressed genes (DEGs) in heart and 2938 DEGs in skeletal muscle. Enrichment analysis showed that shared DEGs in both tissues were enriched mainly in translation and metabolic processes. Of these, the expression of genes functionally categorized as "response to stress", "defense mechanisms", or "muscle contraction" were particularly associated with hibernation. Metabolomic analysis identified 24 and 22 differentially expressed metabolites (DEMs) in myocardium and skeletal muscle, respectively. In particular, pathway analysis showed that DEMs in myocardium were involved in the pentose phosphate pathway, glycerolipid metabolism, pyruvate metabolism, citrate cycle (TCA cycle), and glycolysis/gluconeogenesis. By contrast, DEMs in skeletal muscle were mainly involved in amino acid metabolism. CONCLUSIONS: In summary, natural adaptations of myocardium and skeletal muscle in hibernating N. parkeri involved transcriptional alterations in translation, stress response, protective mechanisms, and muscle contraction processes as well as metabolic remodeling. This study provides new insights into the transcriptional and metabolic adjustments that aid winter survival of high-altitude frogs N. parkeri.


Subject(s)
Anura , Hibernation , Metabolomics , Muscle, Skeletal , Animals , Hibernation/genetics , Hibernation/physiology , Muscle, Skeletal/metabolism , Anura/genetics , Anura/metabolism , Anura/physiology , Myocardium/metabolism , Transcriptome , Gene Expression Profiling , Seasons , Metabolome , Tibet
14.
PLoS One ; 19(4): e0298515, 2024.
Article in English | MEDLINE | ID: mdl-38669238

ABSTRACT

White-nose syndrome (WNS) is an infectious disease that disrupts hibernation in bats, leading to premature exhaustion of fat stores. Though we know WNS does impact reproduction in hibernating female bats, we are unsure how these impacts are exacerbated by local climate factors. We compiled data from four southeastern U.S. states and used generalized linear mixed effects models to compare effects of WNS, pre-hibernation climate variables, and winter duration on the number of reproductive females in species across the range of WNS susceptibility. We predicted we would see a decline in the number of reproductive females in WNS-susceptible species, with the effect exaggerated by longer winter durations and pre-hibernation climate variables that lead to reductions in foraging. We found that the number of reproductive females in WNS-susceptible species was positively correlated with pre-hibernation local climate conditions conducive to foraging; however, WNS-susceptible species experienced an overall decline with the presence of WNS and as winter duration increased. Our long-term dataset provides evidence that pre-hibernation climate, specifically favorable summer weather conditions for foraging, greatly influences the reproduction, regardless of WNS status.


Subject(s)
Chiroptera , Climate , Hibernation , Reproduction , Seasons , Animals , Female , Chiroptera/physiology , Hibernation/physiology , Mycoses/veterinary , Mycoses/epidemiology , Reproduction/physiology
15.
J Physiol Sci ; 74(1): 27, 2024 Apr 27.
Article in English | MEDLINE | ID: mdl-38678189

ABSTRACT

Growth and differentiation are reduced or stopped during hibernation, an energy conserving strategy in harsh seasons by lowered metabolism and body temperature. However, few studies evaluated this in a same individual using a non-invasive method. In this study, we applied a non-invasive tracking method of the nail growth throughout the hibernation period in the same hibernating animals, the Syrian hamster (Mesocricetus auratus). We found that nail growth was markedly suppressed during the hibernation period but rapidly recovered by the exit from the hibernation period. Our data suggest that nail growth was arrested during deep torpor, a hypometabolic and hypothermic state, but recovered during periodic arousal, a euthermic phase. Consistent with this, nail stem cells located in the nail matrix did not exit the cell cycle in the deep torpor. Thus, hibernation stops nail growth in a body temperature-dependent manner.


Subject(s)
Hibernation , Animals , Hibernation/physiology , Mesocricetus , Nails/physiology , Body Temperature/physiology , Male , Cricetinae , Torpor/physiology , Cold Temperature
16.
J Comp Physiol B ; 194(2): 203-212, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38587619

ABSTRACT

Winter energy stores are finite and factors influencing patterns of activity are important for overwintering energetics and survival. Hibernation patterns (e.g., torpor bout duration and arousal frequency) often depend on microclimate, with more stable hibernacula associated with greater energy savings than less stable hibernacula. We monitored hibernation patterns of individual big brown bats (Eptesicus fuscus; Palisot de Beauvois, 1796) overwintering in rock-crevices that are smaller, drier, and less thermally stable than most known cave hibernacula. While such conditions would be predicted to increase arousal frequency in many hibernators, we did not find support for this. We found that bats were insensitive to changes in hibernacula microclimate (temperature and humidity) while torpid. We also found that the probability of arousal from torpor remained under circadian influence, likely because throughout the winter during arousals, bats commonly exit their hibernacula. We calculated that individuals spend most of their energy on maintaining a torpid body temperature a few degrees above the range of ambient temperatures during steady-state torpor, rather than during arousals as is typical of other small mammalian hibernators. Flight appears to be an important winter activity that may expedite the benefits of euthermic periods and allow for short, physiologically effective arousals. Overall, we found that big brown bats in rock crevices exhibit different hibernation patterns than conspecifics hibernating in buildings and caves.


Subject(s)
Chiroptera , Hibernation , Animals , Chiroptera/physiology , Hibernation/physiology , Seasons , Behavior, Animal/physiology , Adaptation, Physiological , Circadian Rhythm/physiology , Energy Metabolism , Male , Body Temperature , Female , Temperature , Microclimate , Humidity , Arousal/physiology , Torpor/physiology
17.
Lab Anim (NY) ; 53(5): 117-120, 2024 May.
Article in English | MEDLINE | ID: mdl-38637688

ABSTRACT

Many research groups explore the regulation of hibernation or compare the physiology of heterothermic mammals between the torpid and aroused, euthermic states. Current methods for monitoring torpor (for example, infrared cameras, body temperature or heart-rate telemetry, and motion sensing) are costly, require specialized techniques, and can be invasive. Here we present an alternate method for determining torpor-bout duration that is cost-effective, noninvasive and accurate: paper towel shredding. In the winter, euthermic thirteen-lined ground squirrels will shred paper towels placed in the cage, but torpid animals will not. The presence of a shredded paper towel, indicating an arousal from torpor, is easily evaluated during routine daily monitoring. In 12 animals over 52 days, this simple technique detected 59 arousals with 100% accuracy when compared with the body temperature telemetry of the same animals. Moreover, this novel method avoids some of the drawbacks of other cheap monitoring systems such as the sawdust technique.


Subject(s)
Hibernation , Sciuridae , Animals , Sciuridae/physiology , Hibernation/physiology , Arousal/physiology , Telemetry/methods , Telemetry/veterinary , Body Temperature , Male , Paper , Housing, Animal
18.
Elife ; 122024 Apr 26.
Article in English | MEDLINE | ID: mdl-38669069

ABSTRACT

Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the 'life-history' hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.


Subject(s)
Biological Evolution , Hibernation , Animals , Hibernation/physiology , Male , Female , Seasons , Reproduction/physiology , Phylogeny , Mammals/physiology
19.
J Comp Physiol B ; 194(2): 213-219, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38466418

ABSTRACT

Hibernation is a widespread metabolic strategy among mammals for surviving periods of food scarcity. During hibernation, animals naturally alternate between metabolically depressed torpor bouts and energetically expensive arousals without ill effects. As a result, hibernators are promising models for investigating mechanisms that buffer against cellular stress, including telomere protection and restoration. In non-hibernators, telomeres, the protective structural ends of chromosomes, shorten with age and metabolic stress. In temperate hibernators, however, telomere shortening and elongation can occur in response to changing environmental conditions and associated metabolic state. We investigate telomere dynamics in a tropical hibernating primate, the fat-tailed dwarf lemur (Cheirogaleus medius). In captivity, these lemurs can hibernate when maintained under cold temperatures (11-15 °C) with limited food provisioning. We study telomere dynamics in eight fat-tailed dwarf lemurs at the Duke Lemur Center, USA, from samples collected before, during, and after the hibernation season and assayed via qPCR. Contrary to our predictions, we found that telomeres were maintained or even lengthened during hibernation, but shortened immediately thereafter. During hibernation, telomere lengthening was negatively correlated with time in euthermia. Although preliminary in scope, our findings suggest that there may be a preemptive, compensatory mechanism to maintain telomere integrity in dwarf lemurs during hibernation. Nevertheless, telomere shortening immediately afterward may broadly result in similar outcomes across seasons. Future studies could profitably investigate the mechanisms that offset telomere shortening within and outside of the hibernation season and whether those mechanisms are modulated by energy surplus or crises.


Subject(s)
Cheirogaleidae , Hibernation , Telomere , Animals , Hibernation/physiology , Cheirogaleidae/physiology , Cheirogaleidae/genetics , Male , Female , Telomere Homeostasis/physiology , Telomere Shortening/physiology , Seasons
20.
J Comp Physiol B ; 194(2): 191-202, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38522042

ABSTRACT

Disuse-induced muscular atrophy is frequently accompanied by iron overload. Hibernating animals are a natural animal model for resistance to disuse muscle atrophy. In this paper, we explored changes in skeletal muscle iron content of Daurian ground squirrels (Spermophilus dauricus) during different periods of hibernation as well as the regulatory mechanisms involved. The results revealed that compared with the summer active group (SA), iron content in the soleus muscle (SOL) decreased (- 65%) in the torpor group (TOR), but returned to normal levels in the inter-bout arousal (IBA); splenic iron content increased in the TOR group (vs. SA, + 67%), decreased in the IBA group (vs. TOR, - 37%). Expression of serum hepcidin decreased in the TOR group (vs. SA, - 22%) and returned to normal levels in the IBA groups; serum ferritin increased in the TOR group (vs. SA, + 31%), then recovered in the IBA groups. Soleus muscle transferrin receptor 1 (TfR1) expression increased in the TOR group (vs. SA, + 83%), decreased in the IBA group (vs. TOR, - 30%); ferroportin 1 increased in the IBA group (vs. SA, + 55%); ferritin increased in the IBA group (vs. SA, + 42%). No significant differences in extensor digitorum longus in iron content or iron metabolism-related protein expression were observed among the groups. Significantly, all increased or decreased indicators in this study returned to normal levels after the post-hibernation group, showing remarkable plasticity. In summary, avoiding iron overload may be a potential mechanism for hibernating Daurian ground squirrels to avoid disuse induced muscular atrophy. In addition, the different skeletal muscle types exhibited unique strategies for regulating iron homeostasis.


Subject(s)
Antigens, CD , Ferritins , Hepcidins , Hibernation , Homeostasis , Iron , Muscle, Skeletal , Muscular Atrophy , Receptors, Transferrin , Sciuridae , Animals , Sciuridae/physiology , Hibernation/physiology , Iron/metabolism , Muscle, Skeletal/metabolism , Muscular Atrophy/metabolism , Muscular Atrophy/pathology , Hepcidins/metabolism , Receptors, Transferrin/metabolism , Ferritins/metabolism , Male , Spleen/metabolism , Cation Transport Proteins/metabolism
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