The distribution of the Greater horse-shoe bat, Rhinolophus ferrum-equinum, during hibernation, in relation to environmental factors

Hibernation is a vital factor in the ability of bats to survive in temperate countries where insect availability is drastically reduced in winter. The value of hibernation in survival lies in the reduction of the bat's metabolic rate to very low levels, thus reducing their food requirements.
The selection of a site which fulfils the physiological requirements of hibernation must be important in the survival of the Greater horse-shoe bat. The present study shows that temperature is particularly important in the selection of a precise position for hibernation. The temperature required, however, varies throughout the winter.
In England this bat finds suitable conditions in caves, mines, tunnels, cellars, and house attics. All are dark where the bats are found and offer protection from predators. These considerations are not sufficient to explain the distribution of this bat in hibernation.
The present study shows that a large proportion of the population feeds outside the hibernaculum at times during the hibernation period. The evidence suggests that starvation is a cause of death. Hence it is not only the conditions inside the hibernacula which are important in the winter survival of a bat population. The environmental conditions outside may be just as vital.
The Greater horse-shoe bat is vulnerable since the bulk of its population depends upon relatively few sites. Its reproductive rate is very low and active conservation is needed in England, since populations are small. If conservation is to be successful however, both the physical conditions within hibernacula, and the environmental conditions outside will have to be satisfactory.     

Environmental conditions, rather than season, determine torpor use and temperature selection in large mouse-eared bats (Myotis myotis)

We tested whether food availability, thermal environment and time of year affect torpor use and temperature selection in the large mouse-eared bat (Myotis myotis) in summer and winter. Food-deprived bats were torpid longer than bats offered food ad libitum. Bats placed in a gradient of low (0 degrees C-25 degrees C) ambient temperatures (T(a)) spent more time in torpor than bats in a gradient of high (7 degrees C-43 degrees C) T(a)'s. However, we did not observe seasonal variations in the use of torpor. Moreover, even when food deprived in winter, bats never entered prolonged torpor at T(a)'s characteristic of their natural hibernation. Instead, bats preferred shallow torpor at relatively high T(a), but they always maintained a difference between body and ambient temperatures of less than 2 degrees C. Calculations based on respirometric measurements of metabolic rate showed that food deprived bats spent less energy per unit of time in torpor than fed individuals, even when they entered torpor at higher T(a)'s. We conclude that T(a) likely serves as a signal of food availability and daily torpor is apparently an adaptation to unpredictable changes in food availability, such as its decrease in summer or its increase in winter. Thus, we interpret hibernation to be a second step in the evolution of heterothermy in bats, which allows survival in seasonal environments.     

Changes in progesterone concentrations in the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus

In the Japanese long-fingered bat, when compared with the baseline values during non-pregnancy in the autumn, plasma progesterone concentrations were not significantly elevated during the delayed implantation stage that begins before the bats enter hibernation. However, progesterone concentrations were significantly lower during the delayed development stage that occurs during hibernation and rose significantly during the rapid embryogenesis that occurs after arousal from hibernation in the spring. Changes in the corpus luteum volume corresponded closely with those of plasma progesterone values. Maintenance of gravid females at 25 degrees C for 2 weeks in winter resulted in significant increases in the plasma progesterone concentration and the corpus luteum volume.     

Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, <Emphasis Type="Italic">Hipposideros terasensis</Emphasis>, in subtropical Taiwan

The subtropical Formosan leaf-nosed bats, Hipposideros terasensis (Hipposideridae), show little activity during winter. It has never been determined whether in winter they exhibit hibernation and multi-day periods of low body temperature. The objectives of this study were to understand the winter activity pattern of H. terasensis and to examine whether it enters hibernation during winter. We monitored the skin temperature (T _sk) of nine free-ranging H. terasensis by attaching temperature-sensitive transmitters during the winters of 2007–2008 and 2008–2009. The results showed that H. terasensis entered hibernation from late December to early March. H. terasensis, however, differs from temperate hibernating bats in several ways: (1) it is capable of hibernation at roost temperature (T _r) and T _sk > 20°C; (2) hibernation at high T _r and T _sk does not lead to a relatively high arousal frequency; and (3) adults do not increase body mass in autumn prior to hibernation. To test the hypothesis that H. terasensis feeds frequently during the hibernation period to compensate for the high energetic demands of hibernating in warm hibernacula, we recorded the number and timing of bats that emerged from and entered into a hibernaculum, which contained more than 1,000 bats. From 30 December 2007 to 29 February 2008, an average of only 8.4 bats (<1%) per night (29 nights) emerged from the hibernaculum. Adult bats lost an average of 13–14% of body mass during an approximately 70-day hibernation period. We suggest that H. terasensis might have remarkably low torpid metabolic rates during hibernation.     

Warming up for dinner: torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry

The frequency and function of arousals during hibernation in free-living mammals are little known. We used temperature-sensitive radio transmitters to measure patterns of torpor, arousal and activity in wild Natterer’s bats Myotis nattereri during hibernation. Duration of torpor bouts ranged from 0.06 to 20.4 days with individual means ranging from 0.9 to 8.9 days. Arousals from torpor occurred most commonly coincident with the time (relative to sunset) typical for bats emerging from summer roosts to forage. Bats with lower body condition indices had a shorter average duration of their torpor bouts. We found a non-linear relationship between duration of torpor bout and ambient temperature: the longest average torpor bouts were at temperatures between 2 and 4°C with shorter bouts at lower and higher ambient temperatures. One individual was radio-tracked for ten nights, remained active for an average of 297 min each night and was active for longer on warmer nights. Our results suggest that vespertilionid bats use relatively short torpor bouts during hibernation in a location with a maritime climate. We hypothesise that Natterer’s bats time arousals to maximise opportunities for potential foraging during winter although winter feeding is not the sole determinant of arousal as bats still arouse at times when foraging is unlikely.     

Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels

Golden-mantled ground squirrels (Spermophilus lateralis) undergo seasonal hibernation during which core body temperature (T(b)) values are maintained 1-2 degrees C above ambient temperature. Hibernation is not continuous. Squirrels arouse at approximately 7-day intervals, during which T(b) increases to 37 degrees C for approximately 16 h; thereafter, they return to hibernation and sustain low T(b)s until the next arousal. Over the course of the hibernation season, arousals consume 60-80% of a squirrel's winter energy budget, but their functional significance is unknown and disputed. Host-defense mechanisms appear to be downregulated during the hibernation season and preclude normal immune responses. These experiments assessed immune function during hibernation and subsequent periodic arousals. The acute-phase response to bacterial lipopolysaccharide (LPS) was arrested during hibernation and fully restored on arousal to normothermia. LPS injection (ip) resulted in a 1-1.5 degrees C fever in normothermic animals that was sustained for > 8 h. LPS was without effect in hibernating squirrels, neither inducing fever nor provoking arousal, but a fever did develop several days later, when squirrels next aroused from hibernation; the duration of this arousal was increased sixfold above baseline values. Intracerebroventricular infusions of prostaglandin E(2) provoked arousal from hibernation and induced fever, suggesting that neural signaling pathways that mediate febrile responses are functional during hibernation. Periodic arousals may activate a dormant immune system, which can then combat pathogens that may have been introduced immediately before or during hibernation.     

Influence of photoperiod and temperature on testicular recrudescence and body growth in the lizards, Lacerta sicula and Lacerta muralis

Annual testicular cycles in the lizards Lacerta sicula and L. muralis appear to be regulated by the interaction between seasonal changes in body temperature and an endogenous rhythmicity in thermal responsiveness. Photoperiodism does not appear to be an important factor; i.e. testicular activity does not appear to be regulated by daylength.
Following testicular regression in July, the lizards are refractory to sexual stimulation by high temperatures (i.e. normal preferred levels) for about five months. High temperatures accelerate gonadal regression and prevent recrudescence during late summer. Reduced temperatures stimulate testicular enlargement and spermatid formation during the autumn; this recrudescence can be blocked by treatment with testosterone. Very low temperatures suppress gonadal activity during mid-winter.
Maintenance of lizards at constant high temperatures (33°C) starting in July suppresses testicular recrudescence until December. Also, testicular collapse occurs in lizards transferred to high temperatures after recrudescence has started. The gonads are stimulated by exogenous gonadotropins at 33°C during the fall indicating that high temperatures reduce circulating levels of gonadotropins.
The refractoriness to high temperatures is "spontaneously" terminated during midwinter (December) under a wide range of photo-thermal conditions. Low temperatures may accelerate the termination of refractoriness. Thereafter, high temperatures stimulate, and are required for the final development of the testes and accessory sexual structures. Thus, the increase in body temperature following hibernation times the onset of breeding in the spring.
Temperature also has a marked influence on appetite and growth, independent of photo-period. Weight gains are greater at 33° than at 20°C. At 33° there is a tendency for abdominal fat bodies to enlarge but with little hepatic growth; whereas, the reverse occurs at 20°C.     

Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation

For temperate endotherms (i.e., mammals and birds) energy costs are highest during winter but food availability is lowest and many mammals depend on hibernation as a result. Hibernation is made up of energy-saving torpor bouts [periods of controlled reduction in body temperature (T _b)], which are interrupted by brief periodic arousals to normothermic T _b. What triggers these arousals in free-ranging hibernators is not well understood. Some temperate bats with intermittent access to flying insects during winter synchronize arousals with sunset, which suggests that, in some species, feeding opportunities influence arousal timing. We tested whether hibernating bats from a cold climate without access to food during winter also maintain a circadian rhythm for arousals or whether cues from conspecifics in the same cluster are more important. We used temperature telemetry to monitor skin temperature (T _sk) of free-ranging little brown bats (Myotis lucifugus) hibernating in central Manitoba, Canada, where temperatures from 22 October to 22 March were too cold for flying insects. We found no evidence bats synchronized arousals with photoperiod but they did arouse synchronously with other bats in the same cluster. Thus, in the northern part of their range where flying insects are almost never available during winter, little brown bats exhibit no circadian pattern to arousals. Warming synchronously with others could reduce the energetic costs of arousal for individuals or could reflect disturbance of torpid bats by cluster-mates.     

Control of plasma sex steroid-binding protein (SBP) in the little brown bat: effects of thyroidectomy and treatment with L- and D-thyroxine on the induction of SBP in adult males

The male little brown bat is a seasonally reproductive mammal that exhibits dramatic increases in plasma concentrations of sex steroid-binding protein (SBP) in the spring, following arousal from hibernation. Adult male bats, aroused prematurely from hibernation, were found to exhibit increases in plasma SBP titers that were comparable to those observed during normal spring arousal. To evaluate the role of the thyroid gland in the control of SBP in this species, plasma SBP concentrations were determined at weekly intervals in adult male bats that were either thyroparathyroidectomized (TRX) or sham operated (SHAM) after arousal from hibernation. Plasma SBP titers in SHAM males increased markedly within the first week after arousal and by 3 wk had reached levels 20-fold higher than those measured in hibernating controls. In contrast, plasma SBP values in the TRX animals did not increase significantly following arousal but were maintained at low basal levels throughout the experiment. The postarousal rise in SBP, which was blocked by TRX, was completely restored by implantation of either L- or D-thyroxine pellets. In male bats, TRX also hindered the normal postarousal atrophy of the sex accessory glands and resulted in attenuation of the postarousal increases in plasma testosterone concentrations. These effects of TRX were also prevented by treatment with thyroxine. Thus, the thyroid appears to play a significant role in the control of the postarousal rise of SBP in the little brown bat and may be an important factor in the regulation of reproductive function in this species.     

Do season and distribution affect thermal energetics of a hibernating bat endemic to the tropics and subtropics?

Although many tropical and subtropical areas experience pronounced seasonal changes in weather and food availability, few studies have examined and none have compared the thermal physiology and energetics of a hibernating mammal that is restricted to these regions. We quantified thermal energetics of northern long-eared bats (Nyctophilus bifax; body mass ～10 g) during summer, winter, and spring from a subtropical habitat, and also during winter from a tropical habitat, to determine how N. bifax cope with climate and seasonal changes in weather. We captured bats in the wild and measured metabolic rates via open-flow respirometry. The basal metabolic rate of subtropical bats at an ambient temperature (T(a)) of 32.6 ± 0.7°C was 1.28 ± 0.06 ml O(2)·g(-1)·h(-1) during both summer and winter, similar to other species of Nyctophilus. Resting metabolic rates below the thermoneutral zone increased similarly with decreasing T(a) during all seasons and in both regions. All individuals showed a high proclivity to enter torpor at T(a) values below the thermoneutral zone. Metabolic rates in torpid thermoconforming bats fell with T(a) and body temperature, and mean minimum metabolic rates during torpor were similar during all seasons and in both regions and as predicted from body mass in temperate zone hibernators. At very low T(a), torpid N. bifax thermoregulated, and this threshold T(a) differed significantly between subtropical (T(a) = 3.5 ± 0.3°C) and tropical (T(a) = 6.7 ± 0.7°C) individuals, but not between seasons. Our data show that thermal energetics of N. bifax do not vary seasonally and in many aspects are similar in tropical and subtropical bats; however, torpid individuals from the subtropics allow body temperature to fall to significantly lower values than those from the tropics.     

Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome

White-nose syndrome (WNS) is a new disease of bats that has devastated populations in eastern North America. Infection with the fungus, Geomyces destructans, is thought to increase the time bats spend out of torpor during hibernation, leading to starvation. Little is known about hibernation in healthy, free-ranging bats and more data are needed to help predict consequences of WNS. Trade-offs presumably exist between the energetic benefits and physiological/ecological costs of torpor, leading to the prediction that the relative importance of spring energy reserves should affect an individual''s use of torpor and depletion of energy reserves during winter. Myotis lucifugus mate during fall and winter but females do not become pregnant until after spring emergence. Thus, female reproductive success depends on spring fat reserves while male reproductive success does not. Consequently, females should be “thrifty” in their use of fat compared to males. We measured body condition index (BCI; mass/forearm length) of 432 M. lucifugus in Manitoba, Canada during the winter of 2009/2010. Bats were captured during the fall mating period (n = 200), early hibernation (n = 125), and late hibernation (n = 128). Adult females entered hibernation with greater fat reserves and consumed those reserves more slowly than adult males and young of the year. Consequently, adult females may be more likely than males or young of the year to survive the disruption of energy balance associated with WNS, although surviving females may not have sufficient reserves to support reproduction.     

Seasonal variation in use of winter roosts by five bat species in south-east Finland

We studied seasonal variation in the use of winter roosts by five bat species (Eptesicus nilssonii, Myotis brandtii/mystacinus, Myotis daubentonii and Plecotus auritus) in south-east Finland during the winters of 2003/2004 and 2004/2005. At the beginning of the bat hibernation season all species used higher temperatures and humidity than by the season’s end. Hibernacula were at their coldest in mid-hibernation season and became warmer towards the end of the season. However, no species hibernated in warmer locations at the end of the season than in mid-season. Results suggest that bats tend to use different strategies throughout the hibernation season, minimizing the cost of hibernation early in the season by hibernating in warmer locations and minimizing energy expenditure later in the season by hibernating in colder locations. M. brandtii/mystacinus were found in locations with stable temperature and humidity, moving to increasingly stable conditions (chambers, crevices, clusters, ceiling) towards spring. All other species hibernated in more variable microclimates throughout the hibernation season.     

Variation in routine metabolism of juvenile muskellunge: evidence for seasonal metabolic compensation in fishes

Metabolic rate of age 0 muskellunge Esox masquinongy ranged from 0·10 at 5° C to 0·24 mg O₂ g^-1 h^-1 at 25° C and was significantly higher in spring and autumn than during winter months at comparable water temperatures. Reduced metabolic rate in winter was consistent with the metabolic compensation hypothesis, implying that metabolism of muskellunge varies independently of acclimation temperature and gonadogenesis. Moreover, seasonal variation in metabolic rate has important implications for energy budget studies. Single-season estimates of esocid metabolism may be inadequate to describe annual energy requirements; the magnitude of errors will depend on the time of year metabolic rate was measured. As a result, it is suggested that seasonal variation in metabolic rate be incorporated into energy budget determinations for fishes.     

Hibernation in the mountain pygmy possum Burramys parvus (Marsupialia)

Mountain pygmy possums Burramys parvus (40 g) disappear from their Mt. Kosciusko boulder fields from May to October/November and it is assumed that they hibernate during this time. However, laboratory studies did not observe the characteristic hibernation pattern of placentals, which, throughout the hibernation season, show long bouts of torpor (several days to weeks) that are interrupted by short (< 1 day) normothermic periods. We investigated the pattern of hibernation in juvenile (N = 8) and adult (N = 8) male and female B. parvus in the laboratory at an air temperature that was similar to that in the field during winter. Adults commenced hibernation earlier and hibernated longer (about seven months) than juveniles (about five months). All adult individuals hibernated whereas only six of the eight juveniles did so. Hibernating animals showed distinct seasonal changes in the duration of torpor bouts. Torpor bouts were short (about five days) at the beginning, long (12–20 days) during the middle, and short again at the end of the hibernation season. Normothermic periods were usually shorter than one day. The pattern of the seasonal change of torpor bout duration differed between juveniles and adults and between sexes. Body temperature during mid-hibernation was regulated at about 2 ° c in females and 3 ° C in males and the metabolic rate was similar to that of hibernating placentals.     

Male Seminole Bat Winter Roost-Site Selection in a Managed Forest

Abstract: Understanding year-round roost-site selection is essential for managing forest bat populations. From January to March, 2004 to 2006, we used radiotelemetry to investigate winter roost-site selection by Seminole bats (Lasiurus seminolus) on an intensively managed landscape with forested corridors in southeastern South Carolina, USA. We modeled roost-site selection with logistic regression and used Akaike's Information Criterion for small samples (AIC_c) and Akaike weights to select models relating roost-site selection to plot- and landscape-level variables. We tracked 20 adult male bats to 71 individual roosts. Bats used a variety of roosting structures, including the canopy of overstory trees, understory vegetation, pine (Pinus spp.) needle clusters, and leaf litter. Roost height, structure type, and habitat type were influenced by changes in minimum nightly temperature. On warmer nights, bats selected taller trees in mature forest stands, but when minimum nightly temperatures were <4° C, bats typically were found roosting on or near the forest floor in mid-rotation stands. We recommend avoiding prescribed burning in mid-rotation stands on days when the previous night's temperature is <4 °C to minimize potential disturbance and direct mortality of bats roosting on or near the forest floor. We encourage forest managers to incorporate seasonal changes in roost-site selection to create year-round management strategies for forest bats in managed landscapes.     

Antioxidant Defenses in the Brains of Bats during Hibernation

Hibernation is a strategy used by some mammals to survive a cold winter. Small hibernating mammals, such as squirrels and hamsters, use species- and tissue-specific antioxidant defenses to cope with oxidative insults during hibernation. Little is known about antioxidant responses and their regulatory mechanisms in hibernating bats. We found that the total level of reactive oxygen species (ROS) and reactive nitrogen species (RNS) in the brain of each of the two distantly related hibernating bats M. ricketti and R. ferrumequinum at arousal was lower than that at torpid or active state. We also found that the levels of malondialdehyde (product of lipid peroxidation) of the two hibernating species of bats were significantly lower than those of non-hibernating bats R. leschenaultia and C. sphinx. This observation suggests that bats maintain a basal level of ROS/RNS that does no harm to the brain during hibernation. Results of Western blotting showed that hibernating bats expressed higher amounts of antioxidant proteins than non-hibernating bats and that M. ricketti bats upregulated the expression of some enzymes to overcome oxidative stresses, such as superoxide dismutase, glutathione reductase, and catalase. In contrast, R. ferrumequinum bats maintained a relatively high level of superoxide dismutase 2, glutathione reductase, and thioredoxin-2 throughout the three different states of hibernation cycles. The levels of glutathione (GSH) were higher in M. ricketti bats than in R. ferrumequinum bats and were significantly elevated in R. ferrumequinum bats after torpor. These data suggest that M. ricketti bats use mainly antioxidant enzymes and R. ferrumequinum bats rely on both enzymes and low molecular weight antioxidants (e.g., glutathione) to avoid oxidative stresses during arousal. Furthermore, Nrf2 and FOXOs play major roles in the regulation of antioxidant defenses in the brains of bats during hibernation. Our study revealed strategies used by bats against oxidative insults during hibernation.     

Annual cycles of body weight in the Namie's frosted bat, Vespertilio superans superans

In order to elucidate the circannual cycles of fat deposition and depletion in hibernating bats, annual rhythm of body weight was examined in Vespertilio superans superans under a variety of environmental conditions. Under near natural conditions, adult females put on weight rapidly from October to November. The laboratory born subadult females kept in constant darkness at warm temperature gained weight at the same time as the adults. The length of weight cycle was about 10 months in adult females kept in 14 L : 10 D at about 24°C. These results suggest that cycles of fat deposition and loss are controlled by a modifiable endogenous circannual rhythm. Body weight rhythm persisted normally under warmer environmental conditions preventing the bats from hibernation. It is considered that the circannual cycles of fat gain and loss are relatively stable and not dependent on the hibernation cycle. Prolonged gestation period and delayed beginning of lactation by cold environment in summer did not affect the body weight rhythm. Temperature may be a more important environmental stimulus (or Zeitgeber) for the circannual rhythm than light and its effects may vary with phases.     

Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome

White-nose syndrome (WNS), an emerging infectious disease that has killed over 5.5 million hibernating bats, is named for the causative agent, a white fungus (Geomyces destructans (Gd)) that invades the skin of torpid bats. During hibernation, arousals to warm (euthermic) body temperatures are normal but deplete fat stores. Temperature-sensitive dataloggers were attached to the backs of 504 free-ranging little brown bats (Myotis lucifugus) in hibernacula located throughout the northeastern USA. Dataloggers were retrieved at the end of the hibernation season and complete profiles of skin temperature data were available from 83 bats, which were categorized as: (1) unaffected, (2) WNS-affected but alive at time of datalogger removal, or (3) WNS-affected but found dead at time of datalogger removal. Histological confirmation of WNS severity (as indexed by degree of fungal infection) as well as confirmation of presence/absence of DNA from Gd by PCR was determined for 26 animals. We demonstrated that WNS-affected bats aroused to euthermic body temperatures more frequently than unaffected bats, likely contributing to subsequent mortality. Within the subset of WNS-affected bats that were found dead at the time of datalogger removal, the number of arousal bouts since datalogger attachment significantly predicted date of death. Additionally, the severity of cutaneous Gd infection correlated with the number of arousal episodes from torpor during hibernation. Thus, increased frequency of arousal from torpor likely contributes to WNS-associated mortality, but the question of how Gd infection induces increased arousals remains unanswered.     

Activity following arousal in winter in North American vespertilionid bats

• 1 Many bat species hibernate to conserve energy during winter and like all hibernators they commonly arouse. During these arousals, some bats may undertake activities away from the hibernation site. Systematic ecological studies of the frequency and purpose of winter activity in temperate zone bats of North America are rare and much of the literature involves observations of single individuals or unmarked populations.
• 2 We review the available literature on winter activity among North American vespertilionid bats to highlight the paucity of data on this subject and to stimulate future research. Due to the lack of repeated, systematic studies on most North American species, the conclusions drawn are general or pertain only to parts of the geographical range of any species.
• 3 We suggest that winter activity is ubiquitous among temperate zone bats, but the degree and purpose of activity varies greatly between and within species. In general, cave‐dwelling bats tend to be relatively inactive compared with tree and foliage roosting bats during winter.
• 4 Cave‐dwelling and tree cavity‐dwelling species do not appear to feed, but they do drink and occasionally copulate during the hibernation period. Species that hibernate in foliage or leaf litter are the most active species during winter and may feed and drink throughout winter, although they probably do not copulate because of their solitary nature.
• 5 We encourage researchers to conduct studies on all aspects of winter activity for North American vespertilionids across wide latitudinal and altitudinal gradients. We suggest studies in the near future be focused on estimating the energetic costs and benefits of winter activity through determination of the frequency and intensity of winter feeding activity and more thorough examinations of movements within and among caves. Studies on common, wide‐ranging species have the potential to illuminate large‐scale patterns and differences and should be favoured over studies on rarer species.