Vitamin D status and bone and connective tissue turnover in brown bears (Ursus arctos) during hibernation and the active state

Background

Extended physical inactivity causes disuse osteoporosis in humans. In contrast, brown bears (Ursus arctos) are highly immobilised for half of the year during hibernation without signs of bone loss and therefore may serve as a model for prevention of osteoporosis.

Aim

To study 25-hydroxy-vitamin D (25OHD) levels and bone turnover markers in brown bears during the hibernating state in winter and during the active state in summer. We measured vitamin D subtypes (D₂ and D₃), calcitropic hormones (parathyroid hormone [PTH], 1,25-dihydroxy-vitamin D [1,25(OH)₂D]) and bone turnover parameters (osteocalcin, ICTP, CTX-I), PTH, serum calcium and PIIINP.

Material and Methods

We drew blood from seven immobilised wild brown bears during hibernation in February and in the same bears while active in June.

Results

Serum 25-hydroxy-cholecalciferol (25OHD₃) was significantly higher in the summer than in the winter (22.8±4.6 vs. 8.8±2.1 nmol/l, two tailed p - 2p = 0.02), whereas 25-hydroxy-ergocalciferol (25OHD₂) was higher in winter (54.2±8.3 vs. 18.7±1.7 nmol/l, 2p<0.01). Total serum calcium and PTH levels did not differ between winter and summer. Activated 1,25(OH)₂D demonstrated a statistically insignificant trend towards higher summer levels. Osteocalcin levels were higher in summer than winter, whereas other markers of bone turnover (ICTP and CTX-I) were unchanged. Serum PIIINP, which is a marker of connective tissue and to some degree muscle turnover, was significantly higher during summer than during winter.

Conclusions

Dramatic changes were documented in the vitamin D₃/D₂ ratio and in markers of bone and connective tissue turnover in brown bears between hibernation and the active state. Because hibernating brown bears do not develop disuse osteoporosis, despite extensive physical inactivity we suggest that they may serve as a model for the prevention of this disease.     

Liver and kidney structure and iron content in romanian brown bears (Ursus arctos) before and after hibernation

The annual cycle of the brown bear (Ursus arctos) in the Carpathian Mountains (Romania) consists of an active period from April to November, and an inactive period (hibernation) of approximately 4-5 months between November and March. During hibernation, the brown bears sleep continually and do not feed or drink water. Analyses of liver and kidney of male brown bears showed that liver iron content was 3 times higher in bears at the end of hibernation than at the end of the active period. A possible trend towards a decrease in iron content was noted for the kidney. The presence of iron in the liver was confirmed by the presence of the Perls-positive granules in the cytoplasm of Kupffer cells, in other non-parenchymal cells and also in some hepatocytes. The hepatic veins of the bear liver samples obtained in early spring showed narrower lumens with pleated walls, compared to the normal outline of the hepatic veins in the liver from the bears sampled during autumn. Also in the early spring bears, the renal glomeruli were partially fibrosed. Renal glomerular fibrosis was sometimes observed in samples from the prehibernation period. The tissue iron values from the livers and kidneys of brown bears in early spring or autumn might provide useful data on iron metabolism under conditions of hibernation and accompanying starvation.     

Elevated plasma concentrations of haptoglobin in European brown bears during hibernation

Haptoglobin (Hp), a hemoglobin-binding protein, is known as an acute phase protein and increases during the acute phase of inflammation in most mammals. We reported previously in brown bears that the mean Hp concentrations were higher in blood samples obtained in winter than those in spring. To examine a possible relation of the seasonal variations of Hp to hibernation, in the present study, we measured the plasma concentrations of Hp as well as some other acute phase proteins (alpha(2)-macroglobulin, alpha(1)-antitrypsin, C-reactive protein) in 6 European brown bears (Ursus arctos), from which blood samples were obtained at 5-6 different months of year including February, the time of hibernation. The Hp concentrations showed clear seasonal variations, being highest in February. The alpha(2)-macroglobulin concentrations also showed a similar but much smaller rise in February, but those of alpha(1)-antitrypsin and C-reactive protein did not show any seasonal variations. Our results suggest that the seasonal variation of plasma Hp concentration in brown bears is associated with a hibernation-specific mechanism more than that of acute phase response.     

黑龙江省10年来熊类资源的分布及变动趋势

熊类是大型动物,其毛皮、油脂以及胆、掌、肉等都有很高的利用价值,因此,在黑龙江省林区,熊类历来是重要的狩猎对象。然而,熊是大型猛兽,每被击伤或受惊扰,常凶猛袭人,故猎熊并非易事。历史文献中曾记载:“熊矫捷而罴憨猛,皆兽之绝有力者”,又说,“刺虎者,不过五人一排…刺熊罴,非十人不能胜。盖其力倍于虎也”(《满洲源流考》)。现在,黑龙江省的猎人,通常是在冬季待熊在树洞或地穴中冬眠时进行猎杀,即猎取洞中冬眠的熊,俗称“掏仓子”,或在春季捕捉刚出洞的幼熊,故每年都有一定的猎取量。     

Hydrogen sulfide and nitric oxide metabolites in the blood of free-ranging brown bears and their potential roles in hibernation

During winter hibernation, brown bears (Ursus arctos) lie in dens for half a year without eating while their basal metabolism is largely suppressed. To understand the underlying mechanisms of metabolic depression in hibernation, we measured type and content of blood metabolites of two ubiquitous inhibitors of mitochondrial respiration, hydrogen sulfide (H₂S) and nitric oxide (NO), in winter-hibernating and summer-active free-ranging Scandinavian brown bears. We found that levels of sulfide metabolites were overall similar in summer-active and hibernating bears but their composition in the plasma differed significantly, with a decrease in bound sulfane sulfur in hibernation. High levels of unbound free sulfide correlated with high levels of cysteine (Cys) and with low levels of bound sulfane sulfur, indicating that during hibernation H₂S, in addition to being formed enzymatically from the substrate Cys, may also be regenerated from its oxidation products, including thiosulfate and polysulfides. In the absence of any dietary intake, this shift in the mode of H₂S synthesis would help preserve free Cys for synthesis of glutathione (GSH), a major antioxidant found at high levels in the red blood cells of hibernating bears. In contrast, circulating nitrite and erythrocytic S-nitrosation of glyceraldehyde-3-phosphate dehydrogenase, taken as markers of NO metabolism, did not change appreciably. Our findings reveal that remodeling of H₂S metabolism and enhanced intracellular GSH levels are hallmarks of the aerobic metabolic suppression of hibernating bears.     

Activity patterns of brown bears (Ursus arctos) in Slovenia and Croatia

In most of Europe, true wilderness areas do not exist and brown bears Ursus arctos generally have to cope with human disturbance and infrastructure. The few studies in Europe that have investigated brown bear activity have demonstrated a predominantly nocturnal and 'shy' behaviour in bears. There is still quite a debate on whether the shy, nocturnal bears of Europe are the result of centuries of persecution by men (genetically fixed trait) or whether hunting and the high disturbance potential in the multi-use landscapes are the driving force (individually learnt trait). We analysed the activity pattern of 16 individual bears monitored for 3372 h between May and October 1982–1998 in the Dinaric Mountains of Slovenia and Croatia. The data were collected via time sampling and basically analysed using two approaches: a general linear model with seasonal component to delineate the most important variables influencing the activity pattern and level and cluster analysis to group bears according to their 24-h activity pattern. Time of day and age were the most important variables predicting activity. Although individual variation in the activity pattern was high among individual bears, in general, yearlings were more diurnal and had a less distinct difference between day- and night-time activity levels than adult bears. Subadults were somewhat intermediate to adults and yearlings. We believe that nocturnal behaviour is most likely driven through negative experiences with humans, giving space for much individual variation. More research is needed to prove the causal relationship of nocturnal behaviour and the degree of disturbance that an individual bear is exposed to.     

Capture, anesthesia, and disturbance of free-ranging brown bears (Ursus arctos) during hibernation

We conducted thirteen immobilizations of previously collared hibernating two- to four-year-old brown bears (Ursus arctos) weighing 21-66 kg in central Sweden in winter 2010 and 2011 for comparative physiology research. Here we report, for the first time, an effective protocol for the capture and anesthesia of free-ranging brown bears during hibernation and an assessment of the disturbance the captures caused. Bears were darted in anthill, soil, or uprooted tree dens on eleven occasions, but two bears in rock dens fled and were darted outside the den. We used medetomidine at 0.02-0.06 mg/kg and zolazepam-tiletamine at 0.9-2.8 mg/kg for anesthesia. In addition, ketamine at 1.5 mg/kg was hand-injected intramuscularly in four bears and in six it was included in the dart at 1.1-3.0 mg/kg. Once anesthetized, bears were removed from the dens. In nine bears, arterial blood samples were analyzed immediately with a portable blood gas analyzer. We corrected hypoxemia in seven bears (PaO(2) 57-74 mmHg) with supplemental oxygen. We placed the bears back into the dens and antagonized the effect of medetomidine with atipamezole. Capturing bears in the den significantly increased the risk of den abandonment. One of twelve collared bears that were captured remained at the original den until spring, and eleven, left their dens (mean ± standard deviation) 3.2±3.6 (range 0.5-10.5) days after capture. They used 1.9±0.9 intermediate resting sites, during 6.2±7.8 days before entering a new permanent den. The eleven new permanent dens were located 730±589 m from the original dens. We documented that it was feasible and safe to capture hibernating brown bears, although they behaved differently than black bears. When doing so, researchers should use 25% of the doses used for helicopter darting during the active period and should consider increased energetic costs associated with den abandonment.     

Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears

Ancient DNA studies have revolutionized the study of extinct species and populations, providing insights on phylogeny, phylogeography, admixture and demographic history. However, inferences on behaviour and sociality have been far less frequent. Here, we investigate the complete mitochondrial genomes of extinct Late Pleistocene cave bears and middle Holocene brown bears that each inhabited multiple geographically proximate caves in northern Spain. In cave bears, we find that, although most caves were occupied simultaneously, each cave almost exclusively contains a unique lineage of closely related haplotypes. This remarkable pattern suggests extreme fidelity to their birth site in cave bears, best described as homing behaviour, and that cave bears formed stable maternal social groups at least for hibernation. In contrast, brown bears do not show any strong association of mitochondrial lineage and cave, suggesting that these two closely related species differed in aspects of their behaviour and sociality. This difference is likely to have contributed to cave bear extinction, which occurred at a time in which competition for caves between bears and humans was likely intense and the ability to rapidly colonize new hibernation sites would have been crucial for the survival of a species so dependent on caves for hibernation as cave bears. Our study demonstrates the potential of ancient DNA to uncover patterns of behaviour and sociality in ancient species and populations, even those that went extinct many tens of thousands of years ago.     

Monitoring the wild black bear's reaction to human and environmental stressors

Background

Bears are among the most physiologically remarkable mammals. They spend half their life in an active state and the other half in a state of dormancy without food or water, and without urinating, defecating, or physical activity, yet can rouse and defend themselves when disturbed. Although important data have been obtained in both captive and wild bears, long-term physiological monitoring of bears has not been possible until the recent advancement of implantable devices.

Results

Insertable cardiac monitors that were developed for use in human heart patients (Reveal® XT, Medtronic, Inc) were implanted in 15 hibernating bears. Data were recovered from 8, including 2 that were legally shot by hunters. Devices recorded low heart rates (pauses of over 14 seconds) and low respiration rates (1.5 breaths/min) during hibernation, dramatic respiratory sinus arrhythmias in the fall and winter months, and elevated heart rates in summer (up to 214 beats/min (bpm)) and during interactions with hunters (exceeding 250 bpm). The devices documented the first and last day of denning, a period of quiescence in two parturient females after birthing, and extraordinary variation in the amount of activity/day, ranging from 0 (winter) to 1084 minutes (summer). Data showed a transition toward greater nocturnal activity in the fall, preceding hibernation. The data-loggers also provided evidence of the physiological and behavioral responses of bears to our den visits to retrieve the data.

Conclusions

Annual variations in heart rate and activity have been documented for the first time in wild black bears. This technique has broad applications to wildlife management and physiological research, enabling the impact of environmental stressors from humans, changing seasons, climate change, social interactions and predation to be directly monitored over multiple years.     

Minimal seasonal alterations in the skeletal muscle of captive brown bears

Abstract Previous studies on wild black bears (Ursus americanus) have shown that skeletal muscle morphology, composition, and overall force-generating capacity do not differ drastically between seasons despite prolonged inactivity during hibernation. However, the amount and characteristics of the seasonal variations were not consistent in these studies. The goals of this study were to compare the amount of muscle atrophy in captive brown bears (Ursus arctos) with that observed in wild black bears and measure seasonal differences in twitch characteristics. Samples from the biceps femoris muscle were collected during the summer and winter. Protein concentration, fiber-type composition, and fiber cross-sectional area were measured along with twitch characteristics. The protein concentration of the winter samples was 8.2% lower than that of the summer samples; fiber cross-sectional area and the relative proportion of fast and slow fibers remained unchanged between seasons. Myosin heavy chain isoforms I, IIa, and IIx were identified by immunoblotting and electrophoresis, and the proportions did not change between seasons. The half-rise time in the twitch contractions increased in winter relative to summer samples, which is unexpected under disuse conditions. These results agreed with a study that showed minimal skeletal muscle atrophy between seasons in wild black bears.     

Determinants of reproductive success in female Columbian ground squirrels

Summary We studied the reproductive success of female Columbian ground squirrels (Spermophilus columbianus) in southwestern Alberta for nine years. We defined reproductive success as the number of offspring surviving their first hibernation, classified as yearlings. The number of weaned juveniles explained one third of the variance in number of yearlings at emergence from their first hibernation the following spring, and much of the variance in individual reproductive success originated after weaning. Weight of adult females at emergence from hibernation was correlated with annual reproductive success. The mother's survival beyond weaning and the subsequent winter's snow accumulation had positive effects on annual reproductive success, whereas population density and summer temperature had negative effects. We found no effects on annual reproductive success of date of litter emergence, weight at emergence as a yearling, presence or absence of adult kin, distance from the natal site, location within the study area, winter temperature or summer precipitation. Age of first breeding did not affect lifetime reproductive success, which ranged from 0 to 19 yearlings produced over a lifetime. The greatest source of variation in lifetime reproductive success for females surviving to breeding age was offspring survival, followed by reproductive lifespan.     

Blood chemistry of black bears from Pennsylvania during winter dormancy

Twenty-four serum chemistries were measured in blood samples collected from 20 adult female black bears (Ursus americanus) and their offspring, including 14 yearlings and 37 cubs, in northeastern Pennsylvania during winter 1984. Four other captive adult females were bled before, during, and after they were subjected to unseasonably warm temperatures during February. Levels of serum urea nitrogen (SUN) and creatinine were lower (P less than 0.05), and iron was higher (P less than 0.05) in male cubs compared to female cubs; serum chemistries were similar (P greater than or equal to 0.05) between sexes for yearlings. Total protein, albumin and creatinine levels increased with age of bears, whereas chloride, alkaline phosphatase, potassium, inorganic phosphorus and SUN/creatinine were higher (P less than 0.05) in cubs than in yearlings and adults. The relatively high serum calcium in cubs was probably related to rapid bone development and dietary intake of calcium during winter dormancy in cubs. Low serum calcium in adults was attributed to lactation and a lack of dietary intake. Urea/creatinine ratios averaged 5.5 and 4.6 for yearling females and males, respectively, 6.3 for adult females, and 29.0 and 22.8 for female and male cubs, respectively. Levels of serum chemistries of black bears apparently are relatively stable during winter denning, when bears are without food or water and do not urinate or defecate for several months. This stability indicates that black bears are resistant to the extremes in extrinsic environmental conditions. Abnormal blood chemistry values may indicate metabolic stresses that are not being controlled by bears.(ABSTRACT TRUNCATED AT 250 WORDS)     

Room without a view—Den excavation in relation to body size in brown bears

Hibernation is an adaptive strategy to survive harsh winter conditions and food shortage. The use of well‐insulated winter dens helps animals minimize energy loss during hibernation. Brown bears (Ursus arctos) commonly use excavated dens for hibernation. Physical attributes of excavated dens are expected to impact the bear's heat retention and energy conservation. The objective of this study was to examine the determinants of cavity size of excavated dens and the impact of physical attributes of excavated dens on energy conservation in hibernating bears, hypothesizing that bears excavate dens in a way to minimize heat loss and optimize energy conservation during hibernation. We predicted that den cavity size would be determined by the bear's body size and that older bears would excavate better‐fitting cavities to minimize heat loss, due to their previous experience. We further predicted that physical attributes of excavated dens would affect the bears’ posthibernation body condition. Our results revealed that bears excavated a den cavity in relation to their body size, regardless of sex, and that older bears tended to excavate better‐fitting den cavities compared to young bears, as we expected. Older bears excavated better‐fitting den cavities, suggesting a potentially experience‐based shift with age in den‐excavation behavior and an optimum cavity size relative to a bear's body size. Our key finding is that insulation of excavated dens provided by wall/rood thickness and bedding materials had a significant positive effect on bears’ posthibernation body condition. We believe that our study provides new insight into how not only the quality of denning habitat, but also the quality of dens may affect hibernating animals, by presenting a potential adaptive aspect of den preparation (age effect on efficiency in den excavation) and effect of den attributes on the posthibernation body condition of brown bears.     

Factors Affecting Date of Implantation,Parturition, and Den Entry Estimated from Activity and Body Temperature in Free-Ranging Brown Bears

Knowledge of factors influencing the timing of reproduction is important for animal conservation and management. Brown bears (Ursus arctos) are able to vary the birth date of their cubs in response to their fat stores, but little information is available about the timing of implantation and parturition in free-ranging brown bears. Body temperature and activity of pregnant brown bears is higher during the gestation period than during the rest of hibernation and drops at parturition. We compared mean daily body temperature and activity levels of pregnant and nonpregnant females during preimplantation, gestation, and lactation. Additionally we tested whether age, litter size, primiparity, environmental conditions, and the start of hibernation influence the timing of parturition. The mean date of implantation was 1 December (SD = 12), the mean date of parturition was 26 January (SD = 12), and the mean duration of the gestation period was 56 days (SD = 2). The body temperature of pregnant females was higher during the gestation and lactation periods than that of nonpregnant bears. The body temperature of pregnant females decreased during the gestation period. Activity recordings were also used to determine the date of parturition. The parturition dates calculated with activity and body temperature data did not differ significantly and were the same in 50% of the females. Older females started hibernation earlier. The start of hibernation was earlier during years with favorable environmental conditions. Dates of parturition were later during years with good environmental conditions which was unexpected. We suggest that free-ranging pregnant brown bears in areas with high levels of human activities at the beginning of the denning period, as in our study area, might prioritize investing energy in early denning than in early parturition during years with favorable environmental conditions, as a strategy to prevent disturbances caused by human.     

Increased oxidative stress and decreased activities of Ca(2+)/Mg(2+)-ATPase and Na(+)/K(+)-ATPase in the red blood cells of the hibernating black bear

During hibernation, animals undergo metabolic changes that result in reduced utilization of glucose and oxygen. Fat is known to be the preferential source of energy for hibernating animals. Malonyldialdehyde (MDA) is an end product of fatty acid oxidation, and is generally used as an index of lipid peroxidation. We report here that peroxidation of lipids is increased in the plasma and in the membranes of red blood cells in black bears during hibernation. The plasma MDA content was about four fold higher during hibernation as compared to that during the active, non-hibernating state (P < 0.0001). Similarly, MDA content of erythrocyte membranes was significantly increased during hibernation (P < 0.025). The activity of Ca(2+)/Mg(2+)-ATPase in the erythrocyte membrane was significantly decreased in the hibernating state as compared to the active state. Na(+)/K(+)-ATPase activity was also decreased, though not significant, during hibernation. These results suggest that during hibernation, the bears are under increased oxidative stress, and have reduced activities of membrane-bound enzymes such as Ca(2+)/Mg(2+)-ATPase and Na(+)/K(+)-ATPase. These changes can be considered part of the adaptive for survival process of metabolic depression.     

青海省人与藏棕熊冲突现状、特点与解决对策

人与野生动物冲突会造成重大经济损失,甚至造成人员伤亡,不利于野生动物的保护。藏棕熊主要分布于我国西部地区,与当地居民的冲突具有与大型食肉动物冲突的典型特点。2012-2015年我们对青海省人与藏棕熊冲突172起案件进行了统计分析,同时采用分层访谈法对86户牧民做了人与藏棕熊冲突调查,以期了解该省人与藏棕熊冲突现状,掌握冲突发生的特点和规律,探讨冲突发生的内在原因。研究结果显示：(1) 全省人与藏棕熊冲突案件集中发生在玉树州和海西州,其中玉树州治多县和曲麻莱县冲突最为严重;(2) 每年6-9月为冲突高发期,藏棕熊冬睡期的2月及11月也有发生;(3) 藏棕熊伤害类型主要表现为损毁房屋构件、取食房屋内储存的粮食以及造成人身伤亡;(4) 大部分受访者认为当地人与藏棕熊冲突事件严重,政府应以货币的形式对野生动物伤害给予适当补偿;(5) 目前牧民普遍采取的防熊措施效果并不理想。我们建议加强牧民游牧期间对房屋巡护、加固工作,建议撤户并村,妥善安置过冬食物与饲料,积极开展野生动物伤害补偿工作;同时建议进一步加强对藏棕熊的科学研究,为缓解人熊冲突现象提供科学理论依据。     

Changes during hibernation in different phospholipid and free and esterified cholesterol serum levels in black bears

During hibernation, fat is known to be the preferred source of energy. A detailed analysis of different phospholipids, as well as free and esterified cholesterol, was conducted to investigate lipid abnormalities during hibernation. The levels of total phospholipids and total cholesterol in the serum of black bears were found to increase significantly in hibernation as compared with the active state. Both free and esterified cholesterol were increased in the hibernating state in comparison with the active state (P < 0.05). The percentage increase during hibernation was more in free cholesterol (57%) than in esterified cholesterol (27%). Analysis of subclasses of serum phospholipids showed that choline containing phospholipids, i.e., sphingomyelin (SPG) (14%) and phosphatidylcholine (PC) (76%), are the major phospholipids in the serum of bear. The minor phospholipids included 8% of phosphatidylserine (PS) + phosphatidylinositol (PI), while phosphatidylethanolamine (PE) was only 2% of the total phospholipids. A comparison of phospholipid subclasses showed that PC, PS + PI and SPG were significantly increased, while PE was significantly decreased (P < 0.05) in the hibernating state as compared with the active state in black bears. These results suggest that the catabolism of phospholipids and cholesterol is decreased during hibernation in black bears, leading to their increased levels in the hibernating state as compared with the active state. In summary, our results indicate that serum cholesterol and phospholipid fractions (except PE) are increased during hibernation in bears. It is proposed that the increase of these lipids may be due to the altered metabolism of lipoproteins that are responsible for the clearance of the lipids.     

Hibernating black bears (Ursus americanus) experience skeletal muscle protein balance during winter anorexia

Black bears spend four to seven months every winter confined to their den and anorexic. Despite potential for skeletal muscle atrophy and protein loss, bears appear to retain muscle integrity throughout winter dormancy. Other authors have suggested that bears are capable of net protein anabolism during this time. The present study was performed to test this hypothesis by directly measuring skeletal muscle protein metabolism during the summer, as well as early and late hibernation periods. Muscle biopsies were taken from the vastus lateralis of six free-ranging bears in the summer, and from six others early in hibernation and again in late winter. Protein synthesis and breakdown were measured on biopsies using (14)C-phenylalanine as a tracer. Muscle protein, nitrogen, and nucleic acid content, as well as nitrogen stable isotope enrichment, were also measured. Protein synthesis was greater than breakdown in summer bears, suggesting that they accumulate muscle protein during periods of seasonal food availability. Protein synthesis and breakdown were both lower in winter compared to summer but were equal during both early and late denning, indicating that bears are in protein balance during hibernation. Protein and nitrogen content, nucleic acid, and stable isotope enrichment measurements of the biopsies support this conclusion.     

The seasonal sensitivity of brown bear denning phenology in response to climatic variability

Background

For brown bears (Ursus arctos), hibernation is a critical part of the annual life cycle because energy savings during hibernation can be crucial for overwintering, and females give birth to cubs at that time. For hibernation to be a useful strategy, timing is critical. However, environmental conditions vary greatly, which might have a negative effect on the functionality of the evolved biological time-keeping. Here, we used a long-term dataset (69 years) on brown bear denning phenology recorded in 12 Russian protected areas and quantified the phenological responses to variation in temperature and snow depth. Previous studies analyzing the relationship between climate and denning behavior did not consider that the brown bear response to variation in climatic factors might vary through a period preceding den entry and exit. We hypothesized that there is a seasonal sensitivity pattern of bear denning phenology in response to variation in climatic conditions, such that the effect of climatic variability will be pronounced only when it occurs close to den exit and entry dates.

Results

We found that brown bears are most sensitive to climatic variations around the observed first den exit and last entry dates, such that an increase/decrease in temperature in the periods closer to the first den exit and last entry dates have a greater influence on the denning dates than in other periods.

Conclusions

Our study shows that climatic factors are modulating brown bear hibernation phenology and provide a further structuring of this modulation. The sensitivity of brown bears to changes in climatic factors during hibernation might affect their ability to cope with global climate change. Therefore, understanding these processes will be essential for informed management of biodiversity in a changing world.