Onset Of Hibernation Research Articles

The hibernation temperature niche of the steppe marmot Marmota bobak Müller 1776

Before hibernation, steppe marmots (Marmota bobak Müller 1776) close their burrows to prevent convection transfer of heat to the inside of the burrow. As a result, the temperature inside the burrow differs only slightly from that of the surrounding soil. Using data on soil temperature, I described the temperature regime of steppe marmot burrows (depth from 140 to 450 cm) during hibernation (from August to April), within the species and subspecies ranges. Taking into account the total soil depth of the hibernation chamber and the dates for the beginning and end of hibernation, the steppe marmot enters hibernation at a temperature of 8-16 °C, and ends hibernation at a temperature of 2-4 °C. The hibernation temperature regime differs significantly between the subspecies. M. b. bobak winters at a temperature of 3-4 °C higher than M. b. schaganensis. In the range of M. b. schaganensis marmots start hibernation 1 to 2 months earlier than in the range of M. b. bobak. The cause of subspecies differences in dates of onset of hibernation appear to lie in the zonal properties of seasonal changes in air temperature. In the course of hibernation, the soil temperature declines gradually at a rate approaching 1 °C per month.

A role for nuclear receptors in mammalian hibernation

Hibernation is one of the most dramatic examples of phenotypic plasticity in mammals. During periods of food shortage and/or reduced ambient temperatures hibernating mammals become heterothermic, allowing their body temperature to decrease while entering an energy-conserving torpid state. In order to survive the multi-month hibernation season many species engage in hyperphagy, dramatically increasing adipose stores prior to the onset of hibernation. Nuclear receptors are a superfamily of transcription factors many of which bind lipophilic molecules as ligands. They regulate a variety of processes including energy homeostasis, carbohydrate and lipid metabolism, inflammation and circadian rhythm. Given that lipids are integral in the hibernation phenotype they may play important regulatory roles through their interactions with nuclear receptors. Here we review current knowledge and suggest possible roles in mammalian hibernation for peroxisome proliferator-activated receptors (PPARs), farnesoid X receptors (FXRs), liver X receptors (LXRs), retinoid-related orphan receptors (RORs) and Rev-ERBs.

Seasonal changes in cortisol and progesterone secretion in Common hamsters

In this study, we investigated endocrine factors and behaviour in free-living Common hamsters ( Cricetus cricetus) during reproductive and non-reproductive periods of the annual cycle. We applied a non-invasive method to gain information on seasonal changes in adrenocortical activity in male and female hamsters by analysing faecal glucocorticoid metabolite concentrations (FCM). In addition, plasma progesterone concentrations were monitored in females throughout the non-hibernation season. The animals were live-trapped from spring emergence until the onset of hibernation in autumn. Reproductive status was determined at capture and blood and faecal samples were collected. During behavioural observations, agonistic and sexual interactions were recorded. FCM concentrations were significantly higher in males than in females during the reproductive period. In males, a pronounced increase in FCM during the reproductive period coincided with high frequencies of intrasexual aggression. In females, FCM levels remained relatively constant. Aggressive behaviour in females increased during the reproductive period, but was much less frequent than in males. Females, which successfully raised a second litter after a postpartum oestrus and concurrent lactation and gestation had lower FCM levels than individuals, which lost their second litter after parturition. As expected, plasma progesterone concentrations were low before and after the reproductive period. During gestation, levels peaked and remained elevated during lactation. The results of this field study provide insight in critical periods associated with reproduction in male and female Common hamsters.

Desert Tortoise Hibernation: Temperatures, Timing, and Environment

This research examined the onset, duration, and termination of hibernation in Desert Tortoises (Gopherus agassizii) over several years at multiple sites in the northeastern part of their geographic range, and recorded the temperatures experienced by tortoises during winter hibernation. The timing of hibernation by Desert Tortoises differed among sites and years. Environmental cues acting over the short-term did not appear to influence the timing of the hibernation period. Different individual tortoises entered hibernation over as many as 44 days in the fall and emerged from hibernation over as many as 49 days in the spring. This range of variation in the timing of hibernation indicates a weak influence at best of exogenous cues hypothesized to trigger and terminate hibernation. There do appear to be regional trends in hibernation behavior as hibernation tended to begin earlier and continue longer at sites that were higher in elevation and generally cooler. The emergence date was generally more similar among study sites than the date of onset. While the climate and the subsequent timing of hibernation differed among sites, the average temperatures experienced by tortoises while hibernating differed by only about five degrees from the coldest site to the warmest site.

Circannual Control of Hibernation by HP Complex in the Brain

Seasonal hibernation in mammals is under a unique adaptation system that protects organisms from various harmful events, such as lowering of body temperature (Tb), during hibernation. However, the precise factors controlling hibernation remain unknown. We have previously demonstrated a decrease in hibernation-specific protein (HP) complex in the blood of chipmunks during hibernation. Here, HP is identified as a candidate hormone for hibernation. In chipmunks kept in constant cold and darkness, HP is regulated by an individual free-running circannual rhythm that correlates with hibernation. The level of HP complex in the brain increases coincident with the onset of hibernation. Such HP regulation proceeds independently of Tb changes in constant warmth, and Tb decreases only when brain HP is increased in the cold. Blocking brain HP activity using an antibody decreases the duration of hibernation. We suggest that HP, a target of endogenously generated circannual rhythm, carries hormonal signals essential for hibernation to the brain.

Seasonal fat content fluctuations in a gyrinid beetle: comparison between an arctic and a temperate zone population (Coleoptera: Gyrinidae)

Seasonal fluctuations in fat content (percentage of dry body weight) of adult Gyrinus opacus were compared between a lake population at the northern range limit of the species in Greenland (G) and a rock pool population in south-central Sweden (S) near its southern range limit. From equally low values at emergence in summer, beetles of both populations accumulated substantial fat reserves, especially during their first weeks as adults. Hardened S-beetles were fatter than G-beetles at time of onset of hibernation. For late emerging (soft) G-beetles, however, the situation was severe because of an immediate freeze-up of the lake. There was a similar winter fat decline in both populations. During the first month after hibernation there was a significant decrease in fat content of the S-beetles, because they were still utilizing their fat deposits from the previous autumn. This trend was broken at the first emergence peak of chironomids in spring. Hibernating G-beetles used their lesser fat storage to the same extent, and led to some reproductive females reaching extremely low levels of fat. Still lower fat content and smaller body size of beetles in a closely situated small lake to G in early spring shows a between locality variation related to differences in habitat quality at the northern range limit.

Movement, Home Range, and Activity Patterns of the Horned Lizard, Phrynosoma mcallii

Abstract Sixty-nine telemetered Phrynosoma mcallii from the Colorado Desert in California were relocated for up to nine months to examine activity patterns, home-range sizes and overlap, distance traveled between relocations, and onset and duration of hibernation. Total area used by the lizards ranged from 651–59,237 m2. Males had significantly larger mean summer home ranges and traveled significantly further than females. The duration of winter dormancy for eight telemetered lizards was 85 ± 8 (mean ± SE) days. Nearly all telemetered lizards were underground by mid-November and emerged as early as late December. Telemetered P. mcallii were out in the open or underneath a shrub throughout the day during spring and fall. They retreated into burrows to escape the midday summer heat. When out in the open, males perched on an elevated surface 19.0% of the time, whereas females perched 4.3%. Telemetered lizards exhibited considerable overlap among their home ranges; males shared 11% of their home ranges with f...

Body temperature patterns before, during, and after semi-natural hibernation in the European ground squirrel.

Ground squirrels undergo extreme body temperature fluctuations during hibernation. The effect of low body temperatures on the mammalian circadian system is still under debate. Using implanted temperature loggers, we recorded body temperature patterns in European ground squirrels kept in an enclosure under natural conditions. Although hibernation onset was delayed, hibernation end corresponded closely to that measured in a field population. Circadian body temperature fluctuations were not detected during deep torpor, but indications of circadian timing of arousal episodes at higher temperatures were found at the beginning and end of hibernation. One male exhibited synchronised arousals to a relatively constant phase of the day throughout hibernation. All animals first entered torpor in the afternoon. Daily body temperature fluctuations were decreased or distorted during the first days after hibernation. We hypothesise that hibernation may affect the circadian system by either decreasing the expression of the circadian oscillator, or by decreasing the amplitude of the circadian oscillator itself. possibly due to gradual, temperature dependent, internal desynchronisation. The latter mechanism may be beneficial because it might facilitate post-hibernation re-entrainment rates.

The hibernation of protein synthesis

The onset of hibernation in mammals, along with the associated reduction in metabolism, is a complex process. It is perhaps not surprising, therefore, that such a fundamental change in metabolic rate is subject to intricate regulation. There has been a great deal of investigation into the molecular and cellular processes that occur when a mammal switches to, and maintains, a hibernated state. One of the many changes that reflect the overall slow-down of metabolic activity is a reduction in the rate of protein synthesis. This reduction is caused, at least in part, by inhibition of both the initiation and elongation stages of translation. Eukaryotic elongation factor-2 (eEF-2) is a key component in the elongation stage of translation, mediating the translocation step in peptide-chain elongation by promoting transfer of peptidyl-tRNA from the A to the P site, and the movement of mRNA relative to the ribosome by one codon. Although phosphorylation of eEF-2 by eEF-2 kinase is known to inhibit elongation, the precise physiological role of eEF-2 phosphorylation is not yet understood.

Aboveground activity rhythm in Arctic black-capped marmot (Marmota camtschatica bungei Katschenko 1901) under polar day conditions

Daily aboveground activity of wild black-capped marmots of Yakutia (Marmota camtschatica bungei ) was recorded under 'polar day' conditions at 71°57' N and 127°19' E (north of the Polar Circle). From the beginning of May until the end of August, the sun was permanently above or close to the horizon. However under this condition of continuous lighting, the aboveground activity of these arctic hibernating mammals was periodic. Onset and end of activity showed marked changes throughout the seasons. Activity time increased strongly from hibernation emergence until the end of July and then decreased slowly until onset of hibernation. Below daily mean temperatures of 5 °C, activity started when the sun was 35° above the horizon, and ended when it dropped below 28°. When daily mean temperatures were above 5 °C, activity onset was synchronised with a solar altitude around 17-18° and activity ended at 10°. Activity onset was more precise relative to the solar altitude than the end of activity. This may be explained by late feeding bouts, following a midday thermal stress. In absence of rapid natural light-dark (LD) transitions that occur at civil twilight, our results suggest that the activity pattern of black-capped marmots may be synchronised by the light cycle through the solar altitude and ambient temperature. © 2001 Editions scientifiques et medicales Elsevier SAS

Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat?

The fat-tailed dwarf lemur (Cheirogaleus medius; Cheirogaleidae) lives in the tropical forests of Madagascar. It is exceptional among primates, because this small nocturnal lemur hibernates during the dry season from the end of April until October. This field study was carried out to assess seasonal changes in body mass and behavioral traits (locomotor activity, feeding ecology) of C. medius that enable this species to accumulate large quantities of fat within weeks. Feeding observations of 36 radio-collared individuals were combined with a mark-recapture study in western Madagascar during the rainy seasons from 1995 to 1998. Pulp of fruit species not consumed, as well as fruit species eaten by C. medius was analyzed for lipid and sugar contents. Body mass changes of recaptured individuals revealed that C. medius may double its body mass within a few weeks. Most of the increase in body mass took place between March and April after infants had been weaned and directly before the onset of hibernation. Locomotor activity was significantly reduced during the period of body mass gain. During the entire study, fruits, nectar, and flowers of 34 different plant species comprised about 80% of the diet, supplemented by a seasonally varying intake of animal prey. Lipid contents of consumed fruits were comparatively low throughout the study period. No difference in lipid content was detectable between fruit species consumed and not consumed by C. medius. During prehibernation fattening, C. medius consumed mostly fruit species with a high sugar content, significantly higher than that of fruit species that were not consumed. The results suggest that a reduction in locomotor activity as well as a preference for fruit species with a high sugar content enable C. medius to deposit large quantities of fat in a few weeks.

Parameters of Mating Effort and Success in Male European Ground Squirrels, Spermophilus citellus

AbstractBehavioural and physiological changes during the reproductive period were documented in male European ground squirrels including: initiated conflict, scent marking, locomotion and range size, as well as testis size, scrotal pigmentation, testosterone levels and changes in body mass. Spring emergence dates in adult males varied but preceded those of females. Gonadal maturation was complete in adult males at emergence. Most yearlings did not mature and emerged with females. After a quiescent premating phase, male range, range overlap, conflict rates and locomotion increased at female emergence. The synchrony of females, their small ranges and short latencies to ovulation produced a highly male‐biased operational sex ratio (OSR) and potential for scramble competition polygyny. In contrast to other ground squirrel species, each female apparently mated with only a single male. Scramble competition did appear to occur, in that males tried to contact as many females as often as possible before copulation. Females placed high temporal prerequisites on males. Costs of scrambling were documented by body mass loss during mating, which covaried with the number of ‘acquired’ females. Testicular regression occurred earlier, and fattening, moult and onset of next hibernation were delayed in successful males. The determinant factor in these costs was found to be mass loss intensity during the main mating period. Surprisingly, this factor was best related to feeding changes and not to locomotion or aggression. Time budget constraints perhaps imposed by the female, with compounding influences of exercise and stress effects of conflict, then negatively affected ensuing seasonal activities. The individual changes may adversely affect individual survivability and/or future reproductive success.

Effects of cold exposure and hibernation on renal Na,K-ATPase of the jerboa Jaculus orientalis.

Changes in activity and abundance of renal Na,K-ATPase were evaluated during cold exposure and hibernation of the jerboa Jaculus orientalis by measuring the hydrolytic activity, the number of units and the transport activity of Na,K-ATPase in isolated nephron segments. As compared to controls, jerboas exposed to cold (6 degrees C) for 4-5 weeks displayed mild diuresis, decreased urinary osmolality and increased kaliuresis. In cold-exposed jerboas, Na,K-ATPase hydrolytic activity was reduced in the medullary thick ascending limb and enhanced in the cortical and outer medullary collecting duct, whereas it was not altered in other nephron segments. The number of Na,K-ATPase units and the activity of Na,K-pump, determined by [3H]-ouabain binding and by ouabain-sensitive rubidium uptake respectively, changed in parallel with the hydrolytic activity in the medullary thick ascending limb and cortical collecting duct. The maximal rate of activity (Vmax) of Na,K-ATPase was not modified further during hibernation. Thus, cold exposure, but not the onset of hibernation, induces segment-specific changes in the abundance and activity of Na,K-ATPase units which are likely to be related to the entry into hibernation, but not to the maintenance of some renal functions during deep hibernation.

Effect of photoperiod and ambient temperature on activity patterns and body weight cycles of mountain pygmy‐possums, Burramys parvus (Marsupialia)

The mountain pygmy‐possum Burramys parvus shows strong seasonal rhythms of reproduction and activity in summer, pre‐hibernation fattening in autumn and hibernation in winter. We investigated whether photoperiod or air temperature (Ta) or interactions of these environmental factors influence activity patterns, fattening and onset of hibernation. In January 1993, 10 Burramys held under long photoperiod were divided into two groups. One group was maintained under the previous long photoperiod (LD 14.5:9.5; n= 5), the other was transferred to short photoperiod (LD 9.5:14.5; n= 5). The Ta was reduced in steps lasting at least one month from 12 to 8 to 4 and to 2°C. All individuals showed pronounced daily activity rhythms and were mainly nocturnal. Individuals under short photoperiod maintained their nocturnal activity pattern irrespective of Ta. In contrast, most individuals under long photoperiod at Ta 4 and 2°C temporarily showed a free‐running activity rhythm and began their activity period during the day. Body weight and total daily activity were negatively correlated. Individuals with low body weight (<50g) generally were more active and showed longer activity periods than heavy animals. Under both photoperiods these lean individuals often extended their activity periods into the light phase. While in the first year after capture all animals showed pre‐hibernation fattening and hibernation, a second body mass cycle was observed in only five individuals and this was independent of Ta and photoperiod. However, total daily activity in these individuals decreased with increasing body weight. Our study shows that photoperiod has little influence on seasonal changes of activity, body weight and hibernation of Burramys. Low Ta has some effect on activity patterns of Burramys held under long photoperiod. Body weight and activity of Burramys were interrelated suggesting that pre‐hibernation fattening occurs during a time of reduced activity and thus low energy expenditure.

Effects of food availability and ambient temperature on hibernation in the Japanese dormouse,Glirulus japonicus

The effects of food availability and ambient temperature (Ta) on hibernation in the Japanese dormouse,Glirulus japonicus, were examined. When the dormice were deprived of food under natural environmental conditions in midwinter, they showed typical hibernation patterns; in contrast, the animals given ad lib food did not show continuous long-term torpor. Furthermore, exposure to constant low temperature did not affect the torpor patterns in the animals receiving adequate food. These results suggest that food availability plays a decisive role in the onset and maintenance of hibernation in this species, and that low Ta does not have a great influence on the torpor patterns in animals with access to food. This differs from the previous study that emphasized the importance of Ta in the occurrence of torpor and discounted the effects of food shortage.

State-dependent variation in the inhibitory effect of [D-Ala 2, D-Leu 5]- enkephalin on hippocampal serotonin release in ground squirrels

Accumulated evidence has suggested that increased endogenous opioid activities may facilitate the onset of hibernation either directly or possibly through modulation of other neurotransmitter systems. The seasonal change of [D-Ala 2, D-Leu 5]-enkephalin (DADLE), a σ receptor agonist, in modulating K + (35 mM)- induced [ 3H]-5-hydroxytryptamine (5-HT) release from the hippocampal and hypothalamic slices of euthermic and hibernating Richardsons' ground squirrels was therefore investigated. DADLE (0.1 – 10 μM) had no effect on 5-HT release in the hypothalamic slices but elicited a dose-related inhibition on [ 3H]-5-HT release from the hippocampal slices of the euthermic ground squirrel. The inhibitory effect of DADLE was completely reversed by naloxone (10 μM), but not by tetrodotoxin (1 μM). In contrast, DADLE failed to alter the K +-induced 5-HT release from the hippocampal slices of the hibernating ground squirrel. This state-dependent reduction in responsiveness to an opioid is consistent with the hypothesis that enhanced endogenous opioid activity in the hibernating phase could lead to down regulation of the opioid receptors and minimize its inhibition on hippocampal serotonergic activity. A high 5-HT activity would inhibit midbrain reticular activating system indirectly through non-serotonergic fibers, which in turn facilitate the onset or maintenance of hibernation.

A circannual cycle in pinealocyte synaptic ribbons in the hibernating and seasonally reproductive 13-lined ground squirrel ( Spermophilus tridecemlineatus)

Pinealocyte synaptic ribbons (SR) in the 13-lined ground squirrel were quantified at monthly intervals over a one-year period spanning the hibernating and reproductive cycles of these animals. SR numbers were high ( 70–90 20,000 μ m 2 ) during periods of activity and reproductive quiescence (May– October). With the onset of hibernation (November–December) there was a rapid 6 to 7-fold reduction in SR frequency. During arousal (January–February) and sexual maturation (March–April) there was a gradual increase in SR frequency. The winter decline in SR frequency is consistent with the decline in pineal melatonin during hibernation and supports the hypothesis that pinealocyte SR play an important role in the neurotransduction of melatonin biosynthesis.

Serial Changes in Metabolic Correlates of Hibernation in Female Black Bears

Captive female black bears were immobilized and sampled at approximately 10-day intervals from September to March during 2 years (six bears/year) in Virginia. Ten of 12 bears hibernated for an average of 92 days. Rectal temperature declined (P < 0.001) during hibernation to as low as 34.6°C. Average loss in mass for hibernators was 260 g/day and represented 23.1% of peak body mass. Urea : creatinine ratios differed (P < 0.01) after hibernation between hibernators and active bears, declining to 7.2 ± 0.3 (X̄ ± SE; 84 samples) during hibernation. Serum concentrations of total protein, urea nitrogen, creatinine, and bilirubin also differed (P < 0.01) between groups after onset of hibernation. Urea : creatinine ratio was a good indicator of the hibernating state, but the sensitivity of serum-urea concentrations to diet suggests careful use of this ratio as a field index of hibernation.

Annual Ovarian Cycle in the Frog, Rana ridibunda, in Northern Greece

The annual ovarian cycle of the frog Rana ridibunda in northern Greece was studied from 1986 to 1988. Young females reached sexual maturity at a mass of 22-25 g and SVL of 62-66 mm. The maximum ovarian mass occurred in March and the minimum in August. Mass changes of the oviducts followed those shown by the ovaries. Three waves of oviposition were observed in a breeding season, and clutch size ranged from 500-7000 ova in the first wave of oviposition. The smallest ovarian follicles were observed in August and the largest in late February to early March. Females oviposit when the mass of their ovaries is at least 5% of the total body mass. Ovarian mass, clutch size, and ovum size were positively correlated with body mass. The masses of the fat body and liver peak in autumn at the onset of hibernation, and were reduced in spring after oviposition. A pause in the reproductive events was observed only in December and January. To estimate the total number of eggs, a por- tion of the ovary was weighed, and the eggs from this portion of the ovary were placed in petri dishes and counted. The total number of eggs from each female was then calculated. Ovum diameter was measured with an ocular micrometer to the nearest 0.001 mm. Clutch size was determined by counting the oviducal eggs from three females using a binocular micro- scope. The minimum ovum diameter observed (1.40 mm) was used as minimum diameter of the ovarian follicles for all the other months. Analysis of covariance (ANCOVA) was con- ducted, considering each variable (body length; masses of body, liver, fat bodies, ovary and ovi- ducts; number of ova; and ovum diameter) sep- arately, with the rest as covariates. The SPSS/ PC (1983) package was used for statistical pro- cedures.

Antioxidant defenses in the ground squirrel Citellus citellus 2. The effect of hibernation

In spring and autumn, the ground squirrel Citellus citellus is awake and active but in winter it usually hibernates. Reawakening from hibernation involves intense metabolic activity in the interscapular brown adipose tissue (IBAT). The IBAT of hibernation animals showed significant increases in the activities of superoxide dismutase (both copper-zinc and manganese-containing enzymes), glutathione peroxidase, and in the amount of ascorbate present. Glutathione peroxidase also increased in the liver, as did ascorbate in the plasma. These changes were not merely a consequence of exposure to low environmental temperatures. It is proposed that antioxidant defenses are increased in the IBAT of ground squirrel at the onset of hibernation in order to protect the tissue from reactive oxygen species generated as a result of the intense metabolic activity sustained by this tissue during reawakening.