Abstract
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.
Keywords
- Chiroptera
- hibernation
- flight activity
- seasonal use
- white‐nose syndrome
1. Introduction
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 [1]. Up to the 1990s, almost all bat research was closely associated with their roosts [2]; animals being captured at the roost entrances, measured, and marked. As bats have high roost fidelity, they can be here caught and recorded repeatedly [3]. 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 [1].
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 [4]. 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 [5]. 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 [6].
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 [7].
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 [8], 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. [15]) 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 [21]. 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 [22].
(1)
(2)
(3) S
(4)
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 [8], 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 [36]. 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.
(5)
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 [16]. 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 [6]. 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 [7].
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 [39], 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 [41]. 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 [42].
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 [44] 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 [21]. 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 [52] 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 [6]. 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 [46]. 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 [30]. During hibernation,
Euryvalent
It is apparent that neither all individuals nor all populations have the same model of hibernation [58]. 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 [63].
Bat arousal may occur as a result of temperature changes in hibernacula, following which the bats may move to a more suitable location [64]. 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 [65]. Hibernation may also impose ecological costs such as decreased detection and response to predators [66] and an increased likelihood of freezing [67]. At the cellular level, cold stress changes cellular membrane lipid composition and suppresses the rate at which protein synthesis and cell proliferation takes place [68]. 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 [70]. 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 [75]. The disease was first registered as a point‐source epidemic at Howe’s Cave, Albany, New York, in 2006 [71], since when it has spread westward at approx. 200–900 km annually [76]. 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 [88]. 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 [91]. 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 [95]. 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 [96], 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
As
Acknowledgments
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).
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