Temperate regions of the world undergo a marked range of seasonal variation, most becoming extremely cold during the winter. Bats are the only group of vertebrates that have successfully exploited caves as permanent shelter. Although bats may use caves throughout all year, their most important role in ecology of temperate bats is as hibernacula. Here, we summarize various aspects of bat hibernation ecology, including variation in flight activity at the cave entrance; patterns of bat hibernation behaviour; site selection in hibernacula, including the importance of temperature during hibernation; and level of bat movement activity inside the cave. In addition, we review present knowledge on white‐nose syndrome, one of the most important threats to cave‐dwelling bats.
- flight activity
- seasonal use
- white‐nose syndrome
When one thinks about caves, the first image that comes to mind is that of a dark place full of stalactites and stalagmites, with lots of bats hanging on the walls. Bats are mysterious and scary creatures for most people but extremely interesting and enigmatic animals for zoologists. Not only their night activity, longevity, underground roosting, and active flight make them a fascinating species to study but the actual methods used to study them are also of interest . Up to the 1990s, almost all bat research was closely associated with their roosts ; animals being captured at the roost entrances, measured, and marked. As bats have high roost fidelity, they can be here caught and recorded repeatedly . Recent developments in ultrasound detectors and miniaturized telemetry, however, have significantly expanded the range of possible bat research topics to include subjects as time of foraging activity .
While microchiropteran bats are able to use a wide range of natural and mad‐made structures as roosts, roost availability and presence of an abundant food supply are often the main limiting factors for bats, particularly in temperate zone. Roost availability can influence species distribution, foraging behaviour, social and mating behaviours, population size, diversity, and even bat morphology or physiology . While providing many benefits (e.g. protection against bad weather and predators, effective thermoregulation, higher probability of mating and rearing young, lower foraging costs or information transfer), roosts also represent a major evolutionary pressure regarding the survival and reproductive success of each individual bats.
Bats spend a significant proportion of their life hidden in roosts, though their requirements may differ through the year or even at different times of the day. As such, the diversity of bat roosts is very high, ranging from short‐term ephemeral to long‐term permanent sites. Almost half of the approximately 1200 species of living bats, including all European bats, use permanent roost sites such as buildings, caves, mines, tunnels, tree hollows, or rock crevices . Caves and similar underground spaces offer temperate bats long‐term roost sites with specific microclimatic conditions that fulfil two crucial factors: a relatively stable above‐freezing temperature (close to the mean annual surface temperature for the area) and high humidity .
In this review, we focus on the ecology of temperate zone bats roosting in caves of the Moravian Karst, Czech Republic (Figure 1), habitats that supply many of the bats’ needs and that can be used year‐round. In doing so we summarize the results of our research on various aspects of bat ecology over winter, including variation in flight activity at the cave entrance, factors affecting site selection within hibernacula, and level of bat movement activity inside the cave. In addition, we summarize present knowledge on white‐nose syndrome (WNS). The study of these factors, along with a general understanding of bat hibernation, are essential prerequisites to understanding the impact of disturbance on hibernating bat populations and for providing focus to future conservation efforts .
2. Variability in cave use by bats (flight activity at the cave entrance)
The ecology and behaviour of temperate zone bats are fundamentally affected by seasonal changes in day length and other associated climatic variables , the effect of which become more pronounced at increasing latitudes. In order to remain nocturnal, therefore, bats must display behavioural flexibility in circadian and circannual activity patterns. We have been investigating nightly and seasonal changes in bat flight activity at the entrance of a natural karstic cave (Kateřinská cave, Czech Republic), an important hibernaculum monitored for hibernating bats since 1970 [9, 10]. Activity was recorded using a double infrared‐light (IR) automatic logging system that allows discrimination between bats leaving the cave and those entering. Recently, automatic loggers capable of collecting large quantities of data over long periods are increasingly being used to monitor activity at European hibernacula, e.g. in the Netherlands, Denmark and Germany (e.g. [11–13]). The use of such IR automatic loggers has been shown to provide a reliable index of activity levels [14, 15] and, unlike netting, they have the advantage of not disturbing or interfering with the bats’ normal activity. Their main drawback, however, is that they are unable to distinguish between individual bats or bat species [16, 14]. If the study is focused on the activity of the bat assemblage as whole, however, this is a minor problem. Connection of an IR logging system to a camera can help in later species identification, though the use of flashlight will affect natural bat behaviour. Note, however, that some authors (e.g. ) state that species identification using this method can be unreliable. Ultrasound bat detectors can also be connected to IR logging systems and these have been used to monitor activity of a single species (e.g. the lesser horseshoe bat
The level of bat activity (at the cave entrance) varies seasonally and five periods have been defined (Figure 2), all showing a non‐random temporal distribution with flight activity concentrated around a specific time . In each case, activity level is influenced by a range of climatic factors, the effect and contribution of which change nightly and over the year .
Flight activity at the night roost entrance is influenced by fluctuation in ambient temperature, rather than any absolute temperature threshold, the higher the difference between maximum and minimum daily temperature, the higher the activity level. This corresponds with a model proposing that activity changes in temperate insectivorous bats reflect changes in insect activity , i.e. if day‐insect abundance is high due to warmer nights, bat foraging activity may continue overnight with no visits registered at the cave entrance (low activity). On the other hand, when nights are cooler and the daily temperatures range is higher, bats will tend to spend more time in the night roost. Foraging activity is highest at dusk and just before dawn, after which the bats return to the day roost . This model is also supported by the influence of rainfall, with flight activity at the cave entrance increasing as rainfall increases whether the nights are warm or cold.
3. Caves as hibernacula
Hibernation, an optimal adaptation to a prolonged fall in temperature and reduction in prey availability, is a characteristic of the annual cycle of insectivorous temperate zone bats . Selection of a suitable hibernation site is crucial for overwinter survival and, in temperate zone, caves and mines tend to be the most common hibernacula. Caves can be divided into three basic types based on microclimate and use by bats: (1) warm caves used during the summer, including maternity colonies, (2) relatively cold hibernacula with a stable microclimate and (3) caves used during the autumn swarming . Of course, both warm caves and hibernacula can also be used during the spring and autumn migrations too. At higher latitudes, cave temperatures are too low and they tend to be used mainly during torpor and hibernation. Note, however, that while thousands of bats can hibernate at such sites, those sites with lower numbers may be very important locally and their overall contribution to bat population great .
More than 1200 caves are located in the Moravian and Javoříčský Karst regions of the Czech Republic, many of which host significant and regularly monitored bat hibernacula (Figure 4). Three of these cave systems (Javoříčské, Sloupsko‐šošůvské and Býčí skála) represent the largest bat hibernacula in the Czech Republic , with 17 bat species registered during hibernation, including rare species such as
Both of these karst systems have a long history of bat research, beginning with speleological research of caves made by Dr. Friedrich Anton Kolenati in the second half of nineteenth century . Modern bat research in the region was initiated by Prof. RNDr. Jiří Gaisler in the 1950s and it continues, including our long‐term research of bat hibernation, to the present day. As a result, some of these hibernacula have been monitored for almost 50 years .
As one of the main requirements of our own research was to avoid any disturbance to hibernating bats, we used visual censuses only (including night censuses using Pathfinder 2000s night‐vision scope) with no handling or marking [10, 29]. Thermal profiles were also undertaken to evaluate physiological condition. Fur surface body temperature, which is correlated with core body temperature, was measured using a Raynger MX2 non‐contact IR thermometer (Raytek Corporation, USA). Two major model species were regularly monitored in the caves, the greater mouse‐eared bat (
3.1. Model of bat hibernation in natural caves
In late summer and early autumn, bats undergo a preparation phase for hibernation during which they rapidly accumulate body fat deposits  needed for surviving the torpor period. The fat is accumulated by energy savings achieved through increasingly longer daily torpor bouts during the diurnal resting period. Hibernation is usually interrupted by periodic arousals [45, 46], usually related to drinking, feeding (in mild periods) or even mating [23, 35]. As part of the fat deposits must be metabolized for torpid individuals to become physiologically active during winter, such arousals are energetically costly [47, 48].
These arousals, and any subsequent activity, will be mirrored in ecological parameters such as community structure, bat population abundance, shelter selection or total movement activity. Monitoring of hibernating bats in the Moravian Karst has confirmed that the ratio of ‘visible’ bats changes through the winter, i.e. bats may move from inaccessible shelters to places where they can be monitored by investigators [9, 49]. The total number of hibernating bats grows continuously from October, with highest abundances occurring in February or March, depending on community structure. Any increase in abundance will be influenced by immigration of newcomers during the pre‐hibernation period only (mid‐November–mid‐December). Switching of hibernation sites during the deep hibernation period (i.e. leaving the hibernaculum) has only been registered exceptionally . In April, there is a gradual but relatively rapid emergence from the hibernation sites (approximately 3 weeks), with bat abundance in cave decreasing to a minimum.
Movement activity of bats inside the hibernaculum, expressed as the percentage of new findings during a visit, is registered throughout the winter, with levels fluctuating in our species‐specific models. Hibernation activity of
Our two model species accounted for more than 80% of all bat observations in the caves. Bat netting at the cave entrances during spring and autumn migrations, however, confirmed a much higher diversity than during hibernation, with other bat species showing a higher dominance. Small species of genus
3.2. Shelter selection during hibernation
As roost site characteristics can play an important role in bat thermoregulation, choice of site will undoubtedly influence bat fitness and survival. Ransome  classified caves used as hibernation sites into three basic types depending on temperature fluctuation: (1) caves displaying a constant temperature regime, (2) caves with dynamic temperatures and (3) caves with fluctuating low temperatures. Note, however, that numerous factors affect the climate of individual caves; and that each cave will be unique in its geomorphologic and microclimatic parameters . Caves with more or less constant temperatures over the year (averaging between 6 and 10°C) usually have just one entrance and temperature fluctuation tends to occur in the outer entrance parts only due to high air flow. Thermally dynamic caves are characterized by large passages with different temperatures. Such caves tend to have two or more entrances, their mutual positions influencing internal temperature conditions. As any two caves will differ significantly, therefore, it will be difficult to specify an average annual temperature. In general, average annual temperature will be in the range of 3–14°C. Hibernating bat communities sheltering in such caves tend to show the most stable abundances. The third cave type always tends to display fluctuating temperatures, despite usually having just one entrance. During winter, air temperature will decrease significantly due to cold air flowing in from the cave entrance [53, 54].
Survival of hibernating bats will be influenced not only by the selection of a suitable hibernaculum but also by the specific microhabitat conditions within. The correct choice will be crucial for the efficient use of stored energy and for the appropriate timing of flight activity. Indeed, studies have shown that bats are able to regulate length and depth of torpor by selecting favourable sites . During our own monitoring of hibernating bats, we monitored a range of parameters including site type (exposed, semi‐exposed and hidden), relative height above the floor and position in the cave . During hibernation,
It is apparent that neither all individuals nor all populations have the same model of hibernation . Our studies suggest that
3.3. Cave temperature and bat hibernation
The length of time that temperate bats can survive without feeding will be dictated by the temperature, at which they hibernate. In general, by hibernating in caves where temperatures are low but above freezing (i.e. between 2 and 5°C), the bat’s metabolism rate is maintained at an efficient level. While the actual temperatures at which different bats hibernate is species specific [61, 62], the interspecific differences are very small due to the low metabolism and small body mass of temperate bats. Such species‐specific differences vary seasonally, being somewhat smaller during deep hibernation and greater during the pre‐ and late hibernation periods. Bats also display intraspecific variations in preferred temperature, as individuals will select locations based on their energy reserves .
Bat arousal may occur as a result of temperature changes in hibernacula, following which the bats may move to a more suitable location . In general, bats prefer to start hibernation at sites with higher temperatures as those with low temperatures may reach freezing point over the coldest months. An optimizing strategy of such type has been observed in
During hibernation, bat body temperature falls to within 1–2°C of ambient temperature and metabolic processes slowdown, thereby reducing energy requirements. As a result, hibernation incurs physiological costs, including the build‐up of metabolic wastes, dehydration, reduced motor function, altered immune response, and sleep deprivation . Hibernation may also impose ecological costs such as decreased detection and response to predators  and an increased likelihood of freezing . At the cellular level, cold stress changes cellular membrane lipid composition and suppresses the rate at which protein synthesis and cell proliferation takes place . We examined the ability of primary skin fibroblast cells from the flying membrane of a hibernating
4. White‐nose syndrome: a threat to bat populations hibernating in caves
Bats are threatened by a range of both natural and anthropogenic stressors, including predation, lack of food, pathogenic agents, climate change, habitat loss, ecological disasters, illegal trade, chemical and light pollution, roosts and hibernacula disturbance, and wind turbine construction. Considering their economic importance to agriculture, the general decline in bat populations documented around the world is of some importance . Recently, a novel threat to insectivorous bat species hibernating in caves and mines has been recognized in North America [71, 72]. White‐nose syndrome (WNS), a fungal infection characterized by fungal growth on the bat’s muzzle (Figure 12A), has caused a dramatic decline in American bat populations.
Despite intensive research, the origin of the pathogenic agent associated with this disease remains unknown and it is still not known why the disease appeared so suddenly . The disease was first registered as a point‐source epidemic at Howe’s Cave, Albany, New York, in 2006 , since when it has spread westward at approx. 200–900 km annually . Based on the ‘novel pathogen hypothesis’, Europe was initially thought to be the source of the agent which the following findings tending to suggest that WNS did indeed originate in Europe: (1) a single
Diagnosis of WNS is based on identification of the fungal agent growing on bats using cultivation, morphological characteristics (e.g. crescent shaped conidia), and molecular assays [73, 87]. One of the most useful diagnostic methods is wing membrane transillumination with ultraviolet (UV) light, which reveals fluorescent lesions produced by the infection . The method is non‐lethal, can be used under field conditions and, in combination with photography, can be used to estimate infection intensity (Figure 12B) as it is highly sensitive and specific for WNS. Histopathology findings of typical cupping erosions (Figure 13) are the gold standard of WNS diagnosis [89, 90].
Surprisingly, the WNS fungal infection is restricted to the skin only, with no evidence of systemic fungal invasion in infected bats [71, 89]. Hence, bat mortality is thought to follow complex pathophysiological mechanisms, and a multi‐stage WNS model has recently been proposed to explain the disease’s progression . Hibernating bats positive for WNS have been reported as displaying abnormal behaviour, higher arousal frequency from torpor, emaciation and fat depletion, dehydration, acidosis and electrolyte disbalance [82, 92–94]. The extent of wing pathology in infected bats appears to be directly related to mortality . In general, Palearctic bats tend to have a lower disease intensity (measured as the percentage of wing membrane area affected by WNS lesions) than Nearctic bat species , possibly explaining the intercontinental differences in bat mortality.
Riboflavin or vitamin B2 is the main compound responsible for the distinctive orange‐yellow fluorescence observed under UV light (Figure 12B) after invasive
We would like to thank all our colleagues and students from the Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic Brno and Masaryk University in Brno, who participated in both field and laboratory research. We are especially grateful to Miroslav Kovařík for field assistance in the Moravian Karst. We are grateful to Kevin Roche for his correction and improvement of the English text. The authors received support from the Grant Agency of the Czech Republic (Grant no. 502/17‐20286S).
Kunz TH, Parsons S, editors. Ecological and Behavioral Methods for the Study of Bats. Baltimore: The Johns Hopkins University Press; 2009. p. 901
Kunz TH, editor. Ecology of Bats. New York: Plenum Press; 1982. p. 425
Findley JS. Bats: A Community Perspective. Cambridge: Cambridge University Press; 1993. p. 167
Altringham JD. Bats: Biology and Behaviour. Oxford: Oxford University Press; 1996. p. 262
Wilson DE, Reeder DAM, editors. Mammal Species of the World. A Taxonomic and Geographic Reference. Washington: Smithsonian Inst. Press; 1993. p. 1206
Perry RW. A review of factors affecting cave climates for hibernating bats in temperate North America. Environmental Research. 2013; 21:28-39
Mitchell‐Jones A J, Bihari Z, Masing M, Rodrigues L. Protecting and Managing Underground Sites for Bats. Bonn, Germany: EUROBATS Publication Series No. 2. UNEP/EUROBATS Secretariat; 2007. p. 38
Erkert HG. Ecological aspects of bat activity rhythms. In: Kunz TH, editor. Ecology of Bats. New York: Plenum Press; 1982. pp. 201-242
Řehák Z, Zukal J, Kovařík M. Long‐ and short‐term changes in the bat community of the Kateřinská cave (Moravian Karst)—a fundamental assessment. Folia Zoologica. 1994; 43:425-436
Zima J, Kovařík M, Gaisler J, Řehák Z, Zukal J. Dynamics of the number of bats hibernating in the Moravian Karst in 1983 to 1992. Folia Zoologica. 1994; 43:109-119
Degn HJ, Andersen BB, Baagoe H. Automatic registration of bat activity through the year at Monsted Limestone Mine, Denmark. Zeitschrift für Säugetierkunde. 1995; 60:129-135
Harrje C. Etho‐ökologische Untersuchungen an winterschlafenden Wasserfleder‐mäusen ( Myotis daubentoni). Nyctalus (N.F.), Berlin. 1999; 7:78-86
Simon M, Kugelschafter K. Die Ansprüche der Zwergfledermaus ( Pipistrellus pipistrellus) an ihr Winterquartier. – Nyctalus (N.F.), Berlin. 1999; 7:102-111
Parsons KN, Jones G, Greenaway F. Swarming activity of temperate zone microchiropteran bats: Effects of season, time of night and weather conditions. Journal of Zoology, London. 2003; 261:257-264
Rivers NM, Butlin RK, Altringham JD. Autumn swarming behaviour of Natterer’s bats in the UK: Population size, catchment area and dispersal. Biological Conservation. 2006; 27:215-226
Ransome RD. The Natural History of Hibernating Bats. London: Christopher Helm; 1990. p. 256
Baroň I. Seasonal changes in flight activity of lesser horseshoe bat ( Rhinolophus hipposideros) in cave entrance [thesis]. Brno: PřF MU 2000. p. 53
Park JK, Jones G, Ransome RD. Winter activity of a population of greater horseshoe bats ( Rhinolophus ferrumequinum). Journal of Zoology, London. 1999; 248:419-427
Glover AM, Altringham JD. Cave selection and use by swarming bat species. Biological Conservation. 2008; 141:1493-1504
Parsons S, Jones G. Acoustic identification of twelve species of echolocating bat by discriminant function analysis and artificial neural networks. Journal of Experimental Biology. 2000; 203:2641-2656
Berková H, Zukal J. Flight activity of bats at the entrance of a natural cave. Acta Chiropterologica. 2006; 8:187-195
Berková H, Zukal J. Cave visitation by temperate zone bats: Effects of climatic factors. Journal of Zoology, London. 2010; 280:387-395
Speakman JR, Racey PA. Hibernal ecology of the pipistrelle bat: Energy expenditure, water requirements and mass loss, implications for survival and the function of emergence flights. Journal of Animal Ecology. 1989; 58:797-813
Thomas DW. Hibernating bats are sensitive to nontactile human disturbance. Journal of Mammalogy. 1995; 76:940-946
Boyles JG, Dunbar MB, Whitaker Jr. JO. A review of activity following arousal in winter in North American vespertilionid bats. Mammal Review. 2006; 36:267-280
Thomas DW. Lack of evidence for a biological alarm clock in bats ( Myotisspp.) hibernating under natural conditions. Canadian Journal of Zoology. 1993; 71:1-3
Nagel A, Nagel R. Nutzung eines Untertagequartieres durch die Kleine Hufeisennase ( Rhinolophus hipposideros). Tagungsband: ‘‘Zur Situation der Hufeisennasen in Europa“Nebra, den 26. ‐ 28. Mai 1995, Arbeitskreis Fledermäuse Sachsen‐Anhalt e.V. 1997:97-108
Hope PR, Jones G. Warming up for dinner: Torpor and arousal in hibernating Natterer’s bats ( Myotis nattereri) studied by radio telemetry. Journal of Comparative Physiology B. 2012; 182:569-578
Zukal J, Berková H, Madaraszová J. Flying or sleeping: Influence of WNS on flight activity of bats during deep hibernation. Folia Zoologica. 2016; 65:46-51
Zukal J, Berková H, Řehák Z. Activity and shelter selection by Myotis myotisand Rhinolophus hipposideroshibernating in Kateřinská cave (Czech Republic). Mammalian Biology. 2005; 70:271-281
Ciechanowski M, Zajac T, Bilas A, Dunajski R. Spatiotemporal variation in activity of bat species differing in hunting tactics: Effects of weather, moonlight, food abundance, and structural clutter. Canadian Journal of Zoology. 2007; 85:1249-1263
Dunbar MB, Whitaker Jr. JO, Robbins LW. Winter feeding by bats in Missouri. Acta Chiropterologica. 2007; 9:305-310
Skiba R. Bestandsentwicklung und Verhalten von Fledermäusen in einem Stollen des Westharzes. Myotis. 1987; 25:95-103
Bauerová Z, Zima J. Seasonal changes in visits to a cave by bats. Folia Zoologica.1988; 37:97-111
Whitaker Jr. JO, Rissler LJ. Seasonal activity of bats at Copperhead cave. Proceedings of the Indiana Academy of Science. 1992; 101:127-134
Anthony ELP, Stack MH, Kunz TH. Night roosting and the nocturnal time budget of the little brown bat, Myotis lucifugus: Effects of reproductive status, prey density, and environmental conditions. Oecologia. 1981; 51:151-156
Lučan R, Hanák V. Population structure of Daubenton’s bats is responding to microclimate of anthropogenic roosts. Biologia. 2011; 66:690-695
Horáček I, Zima J. Net‐revealed cave visitation and cave‐dwelling on European bats. Folia Zoologica. 1978; 27:135-148
Horáček I, Uhrin M, editors. A tribute to bats. Kostelec nad Černými lesy: Lesnická práce; 2010. p. 314.
Uhrin M, Benda P, Obuch J, Urban P. Changes in abundance of hibernating bats in central Slovakia (1992-2009). Biologia. 2010; 65:349-361
Kolenati FA.Monographie der europäischen Chiropteren. Jarhesh. natw. Sect. k.k. Mähr.‐Schl. Gesellsch. Förd. Brünn: Ackerbaues; 1860. p. 156
Gaisler J, Řehák Z, Zukal J. Bat research in the Moravian Karst: History and present state. Vespertilio. 2006; 9-10:75-85
Zukal J, Kovařík M, Řehák Z, Berková H. Numbers of bats hibernating in two caves in the northern part of Moravian Karst and their long‐term changes. Vespertilio. 2001; 5:321-328
Ewing WG, Studier EH, O’Farrell MJ. Autumn fat deposition and gross body composition in three species of Myotis. Comparative Biochemistry and Physiology. 1970; 36:119-129
Avery MI. Winter activity of pipistrelle bats. Journal of Animal Ecology. 1985; 54:721-738
Brack Jr. V, Twente JW. The duration of the period of hibernation of three species of vespertilionid bats. I. Field studies. Canadian Journal of Zoology. 1985; 63:2952-2954
French AR. Allometries of the durations of torpid and euthermic intervals during mammalian hibernation: A test of the theory of metabolic control of the timing of changes in body temperature. Journal of Comparative Physiology B. 1985; 156:13-19
Geiser F, Ruf T. Hibernation versus daily torpor in mammals and birds: Physiological variables and classification of torpor patterns. Physiological Zoology. 1995; 68:935-966
Zukal J, Řehák Z, Kovařík M. Bats of Sloupsko‐šošůvské cave (Moravian Karst, Central Moravia). Lynx (Praha) n.s. 2003; 34:205-220
Harmata W. Dynamika fenologiczna hibernacji podkowców małych, Rhinolophus hipposideros(Bechst.) (Chiroptera, Rhinolophidae). Studia Chiropterologica. 2000; 1:13-28
Nagel A, Nagel R. Bestandsentwicklung winterschlafender Fledermäuse auf der Schwäbischen Alb bis zum Winter 1987/88 und ihr Schutz. Mitt. Verb. dt. Höhlen‐ und Karstforsch. 1989; 35:17-23
Ransome RD. The distribution of the Greater horse‐shoe bat, Rhinolophus ferrumequinum, during hibernation, in relation to environmental factors. Journal of Zoology, London. 1968; 154:77-112
Nagel A, Nagel R. Remarks of the pattern of optimal ambient temperatures in hibernating bats. Myotis. 1991; 29:109-114
Postawa T. A cave microclimate as modelled by external climatic conditions and its effect on a hibernating bat assemblage: A case of the “Pod Sokolą Górą” cave. Proceedings of the VIIIth EBRS. 2000; 1:199-217
Brosset A, Poillet A. Structure d’une population hibernante de grands rhinolophes Rhinolophus ferrumequinumdans l’est de la France. Mammalia. 1985; 49:221-233
Hanzal V, Průcha M. Annual course of cave visitation by bats (Mammalia: Chiroptera) in the Bohemian karst (Czech Republic). Acta Societatis Zoologicae Bohemoslovacae. 1996; 60:25-30
Fuszara E, Kowalski M, Lesinski G, Cygan JP. Hibernation of bats in underground shelters of central and northeastern Poland. Bonner Zoologische Beiträge. 1996; 46:349-358
Dunbar MB, Brigham RM. Thermoregulatory variation among populations of bats along a latitudinal gradient. Journal of Comparative Physiology. 2010; 180:885-893
Pörter HO, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH. Tradeoffs in thermal adaptation: The need for a molecular to ecological integration. Physiological and Biochemical Zoology. 2006; 79:296-313
Gaisler J, Hanák V, Hanzal V, Jarský V. Results of bat banding in the Czech and Slovak Republics, 1948-2000. Vespertilio. 2003; 7:3-61
Nagel A, Nagel, R. How do bats choose optimal temperatures for hibernation? Comparative Biochemistry and Physiology. 1991; 99A:109-114
Webb PI, Speakman JR, Racey PA. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Canadian Journal of Zoology. 1995; 74:761-765
Boyles JG, Dunbar MB, Storm JS, Brack Jr. V. Energy availability influences microclimate selection of hibernating bats. Journal of Experimental Biology. 2007; 210:4345-4350
Kuipers B, Daan S. Internal migration of hibernating bats: Response to seasonal variation in cave microclimate. Bijdragen tot de Dierkunde, Amsterdam. 1970; 40:51-55
Luis AD, Hudson OJ. Hibernation patterns in mammals: A role for bacterial growth? Functional Ecology. 2006; 20:471-477
Humphries MM, Thomas DW, Kramer D. The role of energy availability in mammalian hibernation: A cost‐benefit approach. Physiological and Biochemical Zoology. 2003; 76:165-179
Clawson RL, Laval RK, Laval ML, Caire W. Clustering behavior of hibernating Myotis sodalisin Missouri. Journal of Mammalogy. 1980; 61:245-253
Fujita J. Cold shock response in mammalian cells. Journal of Molecular Microbiology and Biotechnology. 1999; 1:243-255
Bartonička T, Bandouchova H, Berková H, Blažek J, Lučan R, Horáček I, Martínková N, Pikula J, Řehák Z, Zukal J. Deeply torpid bats can change position without elevation of body temperature. Journal of Thermal Biology. 2017; 63:119-123
Boyles JG, Cryan PM, McCracken GF, Kunz TH. Economic importance of bats in agriculture. Science. 2011; 332:41-42
Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski‐Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. Bat white‐nose syndrome: An emerging fungal pathogen? Science. 2009; 323:227
Lorch JM, Meteyer CU, Behr MJ, Boyles JG, Cryan PM, Hicks AC, Ballmann AE, Coleman JTH, Redell DN, Reeder DM, Blehert DS. Experimental infection of bats with Geomyces destructanscauses white‐nose syndrome. Nature. 2011; 480:376-378
Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS. Geomyces destructanssp. nov. associated with bat white‐nose syndrome. Mycotaxon. 2009; 108:147-154
Verant ML, Boyles JG, Waldrep Jr. W, Wibbelt G, Blehert DS. Temperature‐dependent growth of Geomyces destructans, the fungus that causes bat white‐nose syndrome. PLoS ONE. 2012; 7, e46280
Coleman JTH, Reichard JD. Bat white‐nose syndrome in 2014: A brief assessment seven years after discovery of a virulent fungal pathogen in North America. Outlooks on Pest Management. 2014; 25:374-377
Lorch JM, Palmer JM, Lindner DL, Ballmann AE, George KG, Griffin K, Knowles S, Huckabee JR, Haman KH, Anderson CD, Becker PA, Buchanan JB, Foster JT, Blehert DS. First detection of bat white‐nose syndrome in western North America. mSphere. 2016; 1:00148-16
Sunanda SR, Li X, Rudd RJ, Okoniewski JC, Xu J, Chaturvedi S, Chaturvedi V. Clonal genotype of Geomyces destructansamong bats with white nose syndrome, New York, USA. Emerging Infectious Disease Journal. 2011; 17:1273-1276
Puechmaille SJ, Verdeyroux P, Fuller H, Ar Gouilh M, Bekaert M, Teeling EC. White‐nose syndrome fungus ( Geomyces destructans) in bat, France. Emerging Infectious Diseases. 2010; 16:290-293
Martínková N, Bačkor P, Bartonička T, Blažková P, Červený J, Falteisek L, Gaisler J, Hanzal V, Horáček D, Hubálek Z, Jahelková H, Kolařík M, Korytár L, Kubátová A, Lehotská B, Lehotský R, Lučan R, Májek O, Matějů J, Řehák Z, Šafář J, Tájek P, Tkadlec E, Uhrin M, Wagner J, Weinfurtová D, Zima J, Zukal J, Horáček I. Increasing incidence of Geomyces destructansfungus in bats from the Czech Republic and Slovakia. PLoS ONE. 2010; 5:e13853
Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, Cherezy T, Drebet M, Görföl T, Haarsma AJ, Herhaus F, Hallart G, Hammer M, Jungmann C, Le Bris Y, Lutsar L, Masing M, Mulkens B, Passior K, Starrach M, Wojtaszewski A, Zöphel U, Teeling EC. Pan‐European distribution of white‐nose syndrome fungus ( Geomyces destructans) not associated with mass mortality. PLoS ONE. 2011; 6:e19167
Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, Veith M, Pruger J, Gorfol T, Grosche L, Bontadina F, Zöphel U, Seidl HP, Cryan PM, Blehert DS. White‐nose syndrome fungus ( Geomyces destructans) in bats, Europe. Emerging Infectious Diseases. 2010; 16:1237-1243
Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CKR. Inoculation of bats with European Geomyces destructanssupports the novel pathogen hypothesis for the origin of white‐nose syndrome. Proceedings of the National Academy of Sciences. 2012; 109:6999-7003
Leopardi S, Blake D, Puechmaille SJ. White‐nose syndrome fungus introduced from Europe to North America. Current Biology. 2015; 25:R217–R219
Palmer JM, Kubatova A, Novakova A, Minnis AM, Kolarik M, Lindner DL. Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the fungus causing white‐nose syndrome of bats. G3: Genes|Genomes|Genetics. 2014; 4:1755-1763
Hoyt JR, Sun K, Parise KL, Lu G, Langwig KE, Jiang T, Yang S, Frick WF, Kilpatrick AM, Foster JT, Feng J. Widespread bat white‐nose syndrome fungus, Northeastern China. Emerging Infectious Disease Journal. 2016; 22:140-142
Zukal, J, Banďouchová H, Brichta J, Čmoková A, Jaroň KS, Kolařík M, Kováčová V, Kubátová A, Nováková A, Orlov O, Pikula J, Presetnik P, Šuba J, Zahradníková A, Martínková N. White‐nose syndrome without borders: Pseudogymnoascus destructansinfection tolerated in Europe and Palearctic Asia but not in North America. Scientific Reports. 2016; 6:19829
Shuey MM, Drees KP, Lindner DL, Keim P, Foster JT. Highly sensitive quantitative PCR for the detection and differentiation of Pseudogymnoascus destructansand other Pseudogymnoascusspecies. Applied and Environmental Microbiology. 2014; 80:1726-1731
Turner GG, Meteyer CU, Barton H, Gumbs JF, Reeder DA, Overton B, Bandouchova H, Bartonička T, Martínková N, Pikula J, Zukal J, Blehert DS. Nonlethal screening of bat‐wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white‐nose syndrome. Journal of Wildlife Diseases. 2014; 50:566-573
Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn‐Bochsler V, Thomas NJ, Gargas A, Behr MJ. Histopathologic criteria to confirm white‐nose syndrome in bats. Journal of Veterinary Diagnostic Investigation: Official Publication of the American Association of Veterinary Laboratory Diagnosticians, Inc. 2009; 21:411-414
Pikula J, Banďouchová H, Novotný L, Meteyer CU, Zukal J, Irwin NR, Zima J, Martínková N. Histopathology confirms white‐nose syndrome in bats in Europe. Journal of Wildlife Diseases. 2012; 48:207-211
Verant ML, Meteyer CU, Speakman JR, Cryan PM, Lorch JM, Blehert DS. White‐nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiology. 2014; 14:10
Cryan PM, Meteyer CU, Blehert DS, Lorch JM, Reeder DM, Turner GG, Webb J, Behr M, Verant M, Russell RE, Castle KT. Electrolyte depletion in white‐nose Syndrome Bats. Journal of Wildlife Diseases. 2013; 49:398-402
Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, Vodzak ME, Darling SR, Stihler CW, Hicks AC, Jacob R, Grieneisen LE, Brownlee SA, Muller LK, Blehert DS. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white‐nose syndrome. PLoS ONE. 2012; 7:e38920
Warnecke L, Turner JM, Bollinger TK, Misra V, Cryan PM, Blehert DS, Wibbelt G, Willis CKR. Pathophysiology of white‐nose syndrome in bats: A mechanistic model linking wing damage to mortality. Biology Letters. 2013; 9:20130177
Cryan P, Meteyer C, Boyles J, Blehert D. Wing pathology of white‐nose syndrome in bats suggests life‐threatening disruption of physiology. BMC Biology. 2010; 8:135
Flieger, M. et al. Vitamin B2 as a virulence factor in Pseudogymnoascus destructansskin infection. Scientific Reports. 2016; 6:33200
Zukal J, Banďouchová H, Bartonička T, Berková H, Brack V, Brichta J, Dolinay M, Jaroň KS, Kováčová V, Kovařík M, Martínková N, Ondráček K, Řehák Z, Turner GG, Pikula J. White‐nose syndrome fungus: A generalist pathogen of hibernating bats. PLoS ONE. 2014; 9:e97224