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Bats
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Bats Maja Zagmajster University of Ljubljana, Ljubljana, Slovenia
Introduction Bats (order Chiroptera) are the second most speciose order of mammals, with currently more than 1400 known species, and new ones described every year. Traditionally, they were divided into Microchiroptera and Megachiroptera, but now a different separation based on molecular findings is accepted, termed Pteropodiformes (or Yinpterochiroptera) and Vespertilioniformes (or Yangochiroptera). In Pteropodiformes, the only family of “megabats”, Pteropodidae, is grouped together with five of “microbat” families. Bats are the only mammals able to actively and continuously fly, opposed to gliding which is present in flying squirrels. Elongated bones of bats’ forelimbs are transformed into wings, with thin but elastic membrane extended among the limbs, body, and tail. Due to special system of ligaments in toes and at the start of claws, the body weight pulls the ligaments downward and forces the extension of claws, that attach to the surface. As no extra energy is needed for this upside down hanging, it is not unusual to find even dead individuals in such position. Bats are nocturnal and able to fly in complete darkness even in dense vegetation. This is possible due to a very sophisticated orientation system, echolocation, in which bats generate sound, and then listen to the echoes reflected from the surroundings. All but one bat family create sound in larynx, while in Pteropodidae only a few species use sound for orientation. Species of the genus Rousettus produce sound with tongue clicks, while some other species of this family are apparently able to produce sound with wing clapping (Furey and Racey, 2016). All bats have functional eyes, which are largest in Pteropodidae due to their dependency on night vision. But only echolocation allows the bats to enter the zones of absolute darkness, such as deep parts of caves and other subterranean sites. Bats are found in almost all parts of the world, with exception of polar and cold high-altitude regions. They occupy a variety of ecological niches, which is reflected also in the large span of body sizes: the smallest Kitti’s hog nosed bat (Craseonycteris thonglongyai) weighs only about 2 g, while the great Indian flying fox (Pteropus giganteus) can reach even up to 1600 g (Dietz and Kiefer, 2014). Bats exhibit different dietary habits, including insectivory, frugivory, nectarivory, piscivory, predation on other small vertebrates, and even hemophagy (feeding on blood). Bat diversity is highest near the tropics, and decreases with increasing latitude; this pattern is especially pronounced in the New World continents (Dietz and Kiefer, 2014). Living in groups brings fitness benefits for individuals from interacting with other group members, as opposed to living separately. Bats form the largest aggregations among all vertebrates, and such groups are found almost exclusively in caves. Massive cave colonies are known especially in the family of free-tailed bats (Molossidae), spread all over the world. Wrinkle-lipped freetailed bats (Chaerephon plicata) are widely distributed in Southern Asia, with millions of individuals in caves; when such colonies leave the caves, they form dense clouds kilometers long (Fig. 1). Similarly, the Brazilian free-tailed bats (Tadarida brasiliensis) form colonies of tens of millions of individuals in caves in Southwestern United States (Furey and Racey, 2016). Such large gatherings in caves are known also in some Old World fruit bats, for example, over 850.000 individuals of the Geoffroy’s Rousette fruit bat (Rousettus amplexicaudatus) roost in Monfort cave in the Philippines (Carpenter et al., 2014). Caves present one of the most important natural roosts, but bats can use also other subterranean structures (artificial tunnels, mines, cellars) with similar climatic conditions. In China, nearly 80% of known bat species roost in caves and other subterranean sites, and this proportion is similarly high in other regions around the world (Furey and Racey, 2016). Bats are among the most endangered mammals on the globe, almost a quarter of species are globally threatened according to IUCN criteria (Mickleburgh 94
Encyclopedia of Caves. https://doi.org/10.1016/B978-0-12-814124-3.00013-3 Copyright © 2019 Elsevier Inc. All rights reserved.
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FIG. 1 When emerging from a cave in Vietnam, millions of wrinkle-lipped free-tailed bats (Chaerephon plicata) form dense cloud, extending kilometers in length. (Photo by C. Dietz. Used with permission.)
et al., 2002). Protection of caves and other subterranean sites is therefore a very important factor in bat conservation, though not the only one.
Caves as roosts Bats spend at least half of their life in roosts. They look for safe places, out of reach of potential predators, with microclimatic conditions that suit bats’ seasonal needs. Typically they use existing structures in the environment, either natural (trees, caves, rock crevices, abandoned bird nests) or manmade (buildings, bridges, mines). There are only a few species that form own roosts by folding the foliage into tent-like shelters, or by making holes in termite nests. Caves and similar subterranean sites are available in almost all parts of the world, but whether they will be used by bats depends on various factors. First, even though these are stable environments compared to surface, their characteristics differ among geographical regions, as well as according to their altitudinal position, length, depth, and morphological complexity. Second, bat species differ in roosting requirements, and can use subterranean sites permanently or seasonally. Differences can also be intraspecific, related to sex or geographic position of different populations. Bats may retreat to caves also temporarily during the night, in between feeding bouts. In such roosts they rest, or eat the food. Remains of insects can be found among bat droppings, witnessing hanging places where bats were removing the hard and less nutritious parts of insects (like elytrae or wings). Seeds, that even sprout inside caves, are remains of fruits that have been brought in by frugivorous bats. While eating, bats are less attentive, and caves present safe retreats to finish the meal undisturbed.
Nursery roosts Bats have different life histories than other mammals of comparative size. This is most obvious in reproductive strategies; bats have long periods of pregnancy and lactation; they give birth only once a year, having one, exceptionally two, juveniles. Bat mothers invest a lot of their resources in raising the young until they become independent. In most insectivore bats, juveniles suckle until they are 90% of adult size (Crichton and Krutzsch, 2000). Longevity of bats is exceptional in mammal world— in many species, life spans of over 30 years have been recorded. In summers, bats exhibit strong sexual segregation. Males either live solitarily or in small groups, while females gather separately in assemblages that can be very large. In such nursery (or maternity) colonies, they give birth and raise the young. Juvenile bats have poor thermoregulatory abilities, and benefit from being in the group—this enables increase in areal temperature, and heating benefits from direct body contacts (Fig. 2). Usually the availability of microclimatically suitable sites is limited, so group living enables more bats to use the sites with optimal conditions. Many different species share similar roosting demands, and interspecific grouping of two or more species is common in bats. Despite many benefits that come from living in such large groups, this also generates certain costs. The potential for transmission of diseases and parasites is greater. Large numbers of bats sharing the same roost need to search for feeding grounds in a wider distance than solitary living bats. The latter is less pronounced in groups of different species that have different foraging habitat preferences and consequently lower competition for food resources. One of the species that uses caves throughout the year, and forms very large colonies, is Brazilian free-tailed bat (Tadarida brasiliensis). This species, distributed in Southern Nearctic, Central and Southern America, commonly uses caves as shelters.
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FIG. 2 Two different nursery groups of vespertilionid bats in caves of Southern Europe. Top: Female greater mouse-eared bats (Myotis myotis) and their young during the day; if they change the position, they can take the juveniles with them. Below: Long-fingered bats (Myotis capaccinii) with few mouse-eared bats (Myotis myotis/Myotis oxgnathus), as seen during the night. This cluster consists mainly of juveniles, tightly holding to one another, when females are away. (Photos by P. Presetnik (top) and C. Dietz (down). Used with permission.)
Brazilian free-tailed bats form some of the largest colonies in the world, and as much as 1800 individuals can gather together in 1 m2. The number of individuals per square meter was estimated to be even 5000 for groups of juveniles that are left in the roost while mothers leave for night foraging (McCracken, 1986). Despite such large numbers, mothers are able to find their own young among millions of other juveniles every night. They first use a very good spatial memory to find the right sector of the cave, and then locate their pup by characteristic vocalizations (isolation calls) and scent cues. In Europe, there are a number of species that breed in caves, but there is a latitudinal limit up to which the caves and other subterranean sites have suitable microclimatic conditions for such use. For some species, like long-fingered bats (Myotis capaccinii), this restricts the range to Southern Europe. But others, like greater mouse-eared bats (Myotis myotis) or lesser horseshoe bats (Rhinolophus hipposideros), successfully exploit alternative roosts—buildings, at the north parts of species distribution range. Warm attics of churches and castles present top priority sites in the conservation of such species in Central Europe (Dietz et al., 2009).
Hibernation roosts Bats are homeothermic animals, but they are able to change the metabolic rate and body temperature. They can lower their body metabolism to decrease the use of energy to basic metabolic functions on a daily basis, which is called torpor. They can spend even days in constant torpor to survive periods of bad weather when food availability is low. During winter, temperate bat species are able to survive even months of low or no food availability, living solely on stored energy. This is hibernation, when bats sustain extremely low metabolism and conserve basic life functions to survive. For example, in greater mouse-eared bats (Myotis myotis), the number of heart beats reaches 880 bpm in flight, while it is only 18–80 bpm during hibernation (Dietz et al., 2009). Due to constant low temperatures and high humidity, caves and other subterranean sites are suitable hibernation sites for many bat species, even the ones that roost elsewhere in summer. During hibernation, bats live only on fat reserves gathered in autumn. Decrease in body temperature of around 10°C can save up to 50%–70% energy per time unit (Dietz et al., 2009). Bat’s body temperature is set according to ambient temperature, and when the latter are too low or too high, bats wake up to change the position. Bat species have different preferences on suitable conditions for hibernation, and can be found in very different parts of the same cave (Fig. 3).
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FIG. 3 Simplified presentation of the cave in Central Europe, showing the diversity of compartments that bats can select during hibernation. Different species have different climatic preferences, which differ with distance from the cave entrance. Abbreviations refer to: Bbar, Barbastella barbastellus; Enil, Eptesicus nilssoni; Eser, Eptesicus serotinus; Mbec, Myotis bechsteinii; Mbra, Myotis brandtii; Mdau, Myotis daubentonii; Mema, Myotis emarginatus; Mnat, Myotis nattereri; Mmyo, Myotis myotis; Mmys, Myotis mystacinus; Plsp, Plecotus species; Rsp, Rhinolophus species. (Figure is supplemented and modified after Dietz and Kiefer, 2014, pp. 62.)
Search for suitable hibernation roosts is a strong driver of long distance bat migrations recorded in Europe and North America. For example, Nathusius’ bats (Pipistrellus nathusii) and noctules (Nyctalus noctula) can travel over 1000 km in autumn to find suitable wintering sites in Southern Europe (Dietz et al., 2009). Long distance migrations between summer and winter roosts are also known in Schreiber’s bent-winged bats (Miniopterus schreibersii), where individuals from different summer colonies gather in the same winter roosts, forming tight clusters of thousands of individuals. In some bat species many individuals can gather at the same cave, but hang separately (Fig. 4) or in groups of only few animals. The hibernation period is usually related to a moderate or cold climate, and long winter periods with low food availability. But, a case of hibernation in warm caves was described for two species of mouse-tailed bat (Rhinopoma) species in semiarid and warm areas of Asia and Africa (Levin et al., 2015). They hibernate for 5 months, in caves as warm as 20 °C, even though they do have cold caves available close by. These bats seem to select such warm caves, often heated by geothermal temperature. They are generally subtropical bats, and the ability to go into hibernation is present only at the northern border of their distribution. This is an exceptional case, and the ability to hibernate seems to be a strong limiting factor for many tropical and subtropical species for not extending their range to northern latitudes (Dietz and Kiefer, 2014).
FIG. 4 Some bats hang individually on cave walls during hibernation. Lesser horseshoe bats (Rhinolophus hipposideros) wrap themselves completely in flight membrane (left), and hang separately even when large aggregations of individuals are found in European caves. Vespertilionid bats, like tricolored bat (Perimyotis subflavius) from a cave in Eastern United States, never wrap themselves in wing membrane. Small water drops are seen on bats’ fur. (Photo by M. Zagmajster.)
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Mating sites In temperate zones, bat activity in caves and other underground sites increases substantially at the end of summer and in autumn, for the behavior called swarming. Bats are active and circle in and around the cave entrance throughout the night, while during the day they may roost elsewhere. Bechstein’s bats (Myotis bechsteinii) in Europe, typical forest dwelling species that roosts in tree cavities during summer, come to caves for mating as well as hibernation. In this species, females exhibit very high fidelity to birth sites and, nursery colonies typically present groups of closely related bats. Autumn swarming sites present crucial way to maintain the gene flow among such separated populations, which is facilitated by migrating males (Kerth et al., 2003). This behavior and its function was observed in numerous temperate bat species of Old as well as New World. Swarming sites are not random, and individual bats tend to frequent a few sites more often. Even though swarming behavior is a type of promiscuous behavior, some bats exhibit polygynous mating. Males may establish territories and attract females through self-advertisement. They can defend small territories on cave walls, where they attract females with the scent or special vocalization. Males of greater mouse-eared bats (Myotis myotis) mark small patches on the cave wall with gland excretions and urine to attract females. Once the female comes, the male holds her and defends her against other males. Many bat species can establish true harems, which in tropical species present more or less stable groups throughout the year. For example, in Jamaican fruit bats (Artibeus jamaicensis), one male can guard a group of up to 15 females (McCracken and Wilkinson, 2000). In least long-fingered bat (Miniopterus minor) in East Africa, groups of males were observed in a hole of cave ceiling, having higher mass than males of outside groups. It was assumed that the females come to such group, and mate with the best male, which indicates lek behavior (McCracken and Wilkinson, 2000). Monogamy is rare among bats. Two examples are the African false vampire bat (Cardioderma cor) and the Spectral bat (Vampyrum spectrum). As both species are carnivorous predators, male provides females and young. This care system probably even led to evolution of monogamy (McCracken and Wilkinson, 2000). There are cases when bats can avoid courtship and copulate with females when already in hibernation. This mating is indiscriminant, as in little brown bat (Myotis lucifugus), where males frequently copulate with hibernating females throughout the winter (McCracken and Wilkinson, 2000). Greater horseshoe bats (Rhinolophus ferrumequinum) come to caves in autumn, and exhibit territorial behavior (Furey and Racey, 2016). Males maintain large testes throughout the winter and mating can occur during hibernation period. Besides mating, swarming may play a role also in search for potential hibernation roosts – species compositions in autumn and winter at some sites are indeed very similar. Some observations of mothers being followed by their young also imply, that this is the behavior by which the offspring gets introduced to potential wintering sites.
Importance of bats in caves Vectors of nutrients Bats are among the most important carriers of organic matter in caves, which are typically resource-poor environments. This is especially pronounced in dry caves, where nutrients cannot enter the system via rivers or percolating water. Bats also die in caves, or bring in the remains of their food; this is then used by many different animal species and microorganisms. Especially in the tropics, bats form large groups that inhabit caves throughout the year, and their droppings present constant source of nutrients. Diverse invertebrate communities can feed directly on bat guano, or on the microorganisms that grow on guano deposits. Some invertebrates specialized on certain type of bat guano, like in the case of collembolan species Acherontides eleonorae. These collembolans prefer to live in guano piles of blood feeding bats, like common vampire bat (Desmodus rotundus) (Fig. 5), and possess special morphological adaptations that allow them to walk on such moist surface. Species specialized to living exclusively in guano piles are termed guanobionts, and their species richness as well as abundances can be substantial. Bat guano presents important resource also to aquatic animals. Bat droppings have been identified as the main food source for the adult Mexican cave fish (Astyanax mexicanus), while larval stages of the fish feed mainly on small invertebrates (Espinasa et al., 2017).
Ecosystem services and economic impacts Bats feed in various surface habitats, where they have important ecological roles. From human perspective, they provide various ecosystem services, that is, their activities have benefits to humans (Kunz et al., 2011). Bats feeding on fruits and nectar help in dispersing seeds and in pollinating flowers. Insectivore bats present natural way of regulating the numbers of insects in nature, among which many are considered pests. In Thailand, the wrinkle-lipped free-tailed bat (Chaerephon plicatus) consumes considerable amounts of white-backed planthoppers (Sogatella furcifera), which are a major pest in rice crops (Furey and Racey, 2016).
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FIG. 5 Female common vampire bats (Desmodus rotundus) with juvenile (left) from a cave in Brazil. This species forms large groups in caves, and produce typical dark shiny guano piles (right). (Photo by M. Zagmajster.)
In the United States, the importance of bats in insect pest control was calculated, and it was estimated that loss of bats in Northern America could lead to agricultural losses estimated at more than 3.7 billion US dollars per year (Boyles et al., 2011). In some parts of the world, especially in Asia, the exploitation of bat guano in caves is an important economic activity of local communities (Kunz et al., 2011). Such guano is rich in nitrates and phosphates, and is considered and sold as a valuable fertilizer. Bats can attract tourists. For example, observations of large evening emergences of Brazilian free-tailed bats (Tadarida brasiliensis) are offered as additional tourist attraction in Carlsbad Caverns in New Mexico (Furey and Racey, 2016). It has been established, that bats are carriers of different viral diseases, and able to cope with infections, like Ebola. Knowing these mechanisms may offer important medicinal insights for curing the disease. Common vampire bats (Desmodus rotundus) are carriers of rabies, which in some regions present a threat to humans, but they may in fact hide important medical applications, coming from the chemicals present in their saliva (Kunz et al., 2011).
Conservation of bats in caves Threats Bats are subjected to numerous threats, which affect them at their roosts as well as foraging habitats. They can be very diverse and abundant in caves, and threats to such sites can have immense negative effects on regional populations, which can even result in local extinctions. The importance to protect the caves is especially evident in cases, where bat species are dependent on roosting only in such habitats and exhibit low population sizes. Such is the example of the Kitti’s hog-nosed bat (Craseonycteris thonglongyai), which is known only from caves in Myanmar and Thailand. The population in Thailand is estimated to be 5,100 and has decreased substantially, with more than 10% decrease every decade since 1983 (Bates et al., 2008). Humans visit caves for various reasons, mostly for tourism, as sanctuaries, or for guano mining (Kunz et al., 2011). Disturbance of nursery colonies may cause female bats to drop their nonvolant juveniles, and eventually leave the roost. During hibernation, any extra arousals result in extra use of fat reserves and lower chances of surviving the winter. Introduction of infrastructure to caves (like installation of lights), closing the entrances, as well as visits of large groups of people can alter the microclimatic conditions, introduce noise or prevent access to caves, which can result in bats abandoning the roost. In some parts of Asia, bats are regularly used as food, and hunted also in caves (Kunz et al., 2011). Controlling this is especially challenging, as bat meat is used for local consumption as well as in trading, and it is served to tourists as local specialty (Mickleburgh et al., 2009). Quarrying and destruction of caves is considered as probably the greatest threat to bats in Southeast Asia. This is the region with the highest annual quarrying rates and still growing, which may bring some species close to extinction (Furey and Racey, 2016). Some bat species are considered pests, but the methods to control their numbers can be used too extensively or unselectively. The Egyptian fruit bat (Rousettus aegyptiacus; Fig. 6) is thought to cause economical damage to commercial fruit industry in many Mediterranean countries. Common vampire bats (Desmodus rotundus) in Central and South America are carriers of rabies and regularly killed. When methods like fumigation and closing of the caves are used, they unselectively affect also all other cave bat species (Furey and Racey, 2016).
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FIG. 6 The group of Egyptian fruit bat (Rousettus aegyptiacus) from a cave in Turkey. (Photo by C. Dietz. Used with permission.)
Examples of massive deaths of bats due to different diseases have been registered in various parts of the world in the last decades. But one of the biggest threats to cave bats, which has been severely depleting bat populations in North America, is the white-nose syndrome. It was first registered in 2006 in a few caves of Northeastern United States, when no one anticipated such a rapid spread of the disease, which resulted in massive deaths of millions of bats around the continent. The infection causes bats to wake up more frequently from hibernation, and as they are unable to feed during cold winters, they get exhausted and eventually die. Drops in populations were severe, and brought some species, like Indiana bat (Myotis sodalis), close to extinction. The disease is caused by the fungus Pseudogymnoascus destructans, which was also discovered in caves in Europe, where it did not cause massive mortalities (Puechmaille et al., 2011). Understanding evolved resistance of European bats that is lacking in American bat populations, and other ongoing studies into this phenomenon could eventually help in protecting North American bats. Pesticides, for example, DDT, were suspected to greatly influence the declines of large colonies of Brazilian free-tailed bats (Tadarida brasiliensis) in Southern United States. Carlsbad Caverns was reputed to have housed 8.7 million bats in the 1930s, but for the past 15 years its population has been more or less stable at about 500,000 (Furey and Racey, 2016). In Western Europe, severe declines of lesser horseshoe bats (Rhinolophus hipposideros) started in the middle of 20th century, leading to extinctions in Netherlands and Luxembourg. The main cause of declines were excessive applications of toxic pesticides, such as DDT and lindane (Dietz et al., 2009). Cave-dwelling bats are subjected to threats stemming from changes in the natural environments, which include deforestation, intensive agriculture as well as urbanization and light pollution. In the United States, mass mortalities of bats were discovered at wind turbines, and up to 24% of the bat fatalities at some wind energy facilities have been cave-roosting species (Kunz et al., 2007). Also in Europe, several species of cave-roosting bats are being killed by wind turbines (Dietz and Kiefer, 2014).
Conservation measures One of the most widely implemented approaches in the conservation of caves for bats is closing of cave entrances to prevent unauthorized human visits. But, gates should not change the natural air currents in the cave, which could affect cave microclimate, and they should permit the bats to freely exit and enter the site. Various grilling solutions have been developed and built in caves and other subterranean sites, but it has been reported that grills are not acceptable for all bat species (Dietz et al., 2009). This does not depend only on the flight agility of species, but also on numbers of bats and size of the entrance (Tobin and Chambers, 2017). Fast flying species like Brazilian free-tailed bats (Tadarida brasiliensis) in Americas, or Schreiber’s bent-winged bats (Miniopterus schreibersii) in Europe, could not tolerate grills (Dietz et al., 2009; Furey and Racey, 2016). An alternative approach toward preventing the access to caves is to set the fences at some distance around the cave entrance (Furey and Racey, 2016). Disturbances from tourist exploitation, as well as guano mining, should be prevented in bat important subterranean sites. Cave visits could be permitted only in times when they are not occupied by bats. If morphology of the cave permits, only part of the cave is used for tourism, while parts important for bats are being avoided. Such approaches have been successfully used in some caves around Europe. Implementing conservation measures at roosts seems to be fairly straightforward, but conservation should also include noncave roosts, that bats may use in other seasons, and landscape level protection, as bats fly long distances from roosts to different feeding grounds. All activities that sustain a mosaic and diverse landscape, preserve the natural forests, lower the use of pesticides, also benefit conservation of cave bats. New facilities that could harm bats, like wind farms, should not be built close to bat
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roosts, important feeding grounds and migratory routes. In recent years, potential compromise solution for the use of wind farms includes part time cutoffs, which is achieved by predefined time interval constraints. A lot of research is conducted on improving automatic detection of high bat activity and automatic stopping of wind turbines during such periods. Numerous negative prejudices and misbeliefs about bats can hamper conservation actions, so raising public awareness and educating people on importance as well as endangerment of bats is of high priority. This is the goal of numerous organizations around the world working on international levels, here we name only few. Fauna & Flora International works on many aspects for the conservation of bats and their habitats worldwide (https://www.fauna-flora.org/). Bat Conservation International (www. batcon.org) works mainly within United States and Canada, and also globally, while BatLife Europe (https://www.batlifeeurope.info/) joins national nongovernmental organizations, with the aim to work toward promotion and protection of bats in Europe. Nearly 90% of known bat species are included in the IUCN Red List of Threatened Species, and they are part of different legal protection schemes. Bats are able to migrate long distances between different types of roosts and feeding grounds, so protection should be done beyond borders. An international instrument within Europe and some non-European states is the The Agreement on the Conservation of Populations of European Bats (EUROBATS), set up under the Convention on the Conservation of Migratory Species of Wild Animals. Another strong legal mechanism for bat protection within Europe is European Habitats Directive (92/43/EEC), which protects all bat species, and requests designation of network of important sites for conservation (so called Natura 2000 sites) for 14 bat species. In other continents, bats are protected via species protection acts, which can lead to protection of caves due to their importance for bats.
See related articles Guano Communities White Nose Syndrome
Bibliography Bates, P., Bumrungsri, S. & Francis, C. 2008. (Craseonycteris thonglongyai. The IUCN Red List of Threatened Species 2008: e.T5481A11205556). Boyles, J.G., Cryan, P.M., McCracken, G.F., Kunz, T.H., 2011. Economic importance of bats in agriculture. Science 332 (6025), 41–42. Carpenter, E.-S., Gomez, R., Walden, D.L., Sherwin, E.R., 2014. Photographic estimation of roosting density of Geoffroy’s rousette fruit bats Rousettus amplexicaudatus (Chriopteta: Pterodpidae) at Monfort bat cave, Philippines. J. Threat. Taxa 6 (6), 5838–5844. Crichton, E.G., Krutzsch, P.H., 2000. Reproductive Biology of Bats. Academic Press, p. 510. Dietz, C., Kiefer, A., 2014. Die Flederm€ause Europas: Kennen, Bestimmen, Sch€utzen. Kosmos Naturf€uhrer, p. 394. Dietz, C., Helversen, O.V., Nill, D., 2009. Bats of Britain, Europe & Northwest Africa. A & C Black, p. 400. Espinasa, L., Bonaroti, N., Wong, J., Pottin, K., Queinnec, E., Retaux, S., 2017. Contrasting feeding habits of post-larval and adult Astyanax cavefish. Subterr. Biol. 21, 1–17. Furey, N.M., Racey, P.A., 2016. Conservation ecology of cave bats. In: Voight, C.C., Kingston, T. (Eds.), Bats in the Anthropocene: Conservaton of Bats in a Changing World. Springer, pp. 463–500. Kerth, G., Kiefer, A., Trappmann, C., Weishaar, M., 2003. High gene diversity at swarming sites suggest hot spots for gene flow in the endangered Bechstein’s bat. Conserv. Genet. 4, 491–499. Kunz, T.H., Arnett, E.B., Erickson, W.P., Johnson, G.D., Larkin, R.P., Strickland, M.D., et al., 2007. Ecological impacts of wind energy development on bats: questions, hypotheses, and research needs. Front. Ecol. Environ. 5, 315–324. Kunz, T.H., Braun de Torrez, E., Bauer, D.M., Lobova, T.A., Fleming, T.H., 2011. Ecosystem services provided by bats. Ann. N. Y. Acad. Sci. 1223, 1–38. Levin, E., Plotnik, B., Amichai, E., Braulke, L.J., Landau, S., Yom-Tov, Y., Kronfeld-Schor, N., 2015. Subtropical mouse-tailes bats use geothermally heated caes for winter hibernation. Proc. R. Soc. B 282, 20142781. McCracken, G.F., 1986. Why are we losing our Mexican free-tailed bats? Bats 3, 1–4. McCracken, G.F., Wilkinson, G.S., 2000. Bats mating systems. In: Crichton, E.G., Kritzsch, P.H. (Eds.), Reproductive Biology of Bats. Academic Press, pp. 321–362. Mickleburgh, S.P., Hutson, A.M., Racey, P.A., 2002. A review of the global conservation status of bats. Oryx 36, 18–34. Mickleburgh, S., Waylen, K.A., Racey, P.A., 2009. Bats as bushmeat: a global review. Oryx 43 (2), 217–234. Puechmaille, S., Wibbelt, G., Korn, V., Fuller, H., Forget, F., M€uhldorfer, K., Kurth, A., Bogdanowicz, W., Borel, C., Bosch, T., Cherezy, T., Drebet, M., G€ orf€ ol, T., Haarsma, A.-J., Herhaus, F., Hallart, G., Hammer, M., Jungmann, C., Le Bris, Y., Lustar, L., Masing, M., MUlkens, B., Passior, K., Starrach, M., Wojtaszewski, A., Z€ophel, U., Reeling, E.C., 2011. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One 6 (4), e19167. Tobin, A., Chambers, C.L., 2017. Mixed effects of gating subterranean habitat of bats—a review. J. Wildl. Manag. 81 (7), 1149–1160. Zubaid, A., McCracken, G.F., Kunz, T.H., 2006. Functionald and Evolutionary Ecology of Bats. Oxford University Press, p. 360.
Bats Maja Zagmajster University of Ljubljana, Ljubljana, Slovenia
Introduction Bats (order Chiroptera) are the second most speciose order of mammals, with currently more than 1400 known species, and new ones described every year. Traditionally, they were divided into Microchiroptera and Megachiroptera, but now a different separation based on molecular findings is accepted, termed Pteropodiformes (or Yinpterochiroptera) and Vespertilioniformes (or Yangochiroptera). In Pteropodiformes, the only family of “megabats”, Pteropodidae, is grouped together with five of “microbat” families. Bats are the only mammals able to actively and continuously fly, opposed to gliding which is present in flying squirrels. Elongated bones of bats’ forelimbs are transformed into wings, with thin but elastic membrane extended among the limbs, body, and tail. Due to special system of ligaments in toes and at the start of claws, the body weight pulls the ligaments downward and forces the extension of claws, that attach to the surface. As no extra energy is needed for this upside down hanging, it is not unusual to find even dead individuals in such position. Bats are nocturnal and able to fly in complete darkness even in dense vegetation. This is possible due to a very sophisticated orientation system, echolocation, in which bats generate sound, and then listen to the echoes reflected from the surroundings. All but one bat family create sound in larynx, while in Pteropodidae only a few species use sound for orientation. Species of the genus Rousettus produce sound with tongue clicks, while some other species of this family are apparently able to produce sound with wing clapping (Furey and Racey, 2016). All bats have functional eyes, which are largest in Pteropodidae due to their dependency on night vision. But only echolocation allows the bats to enter the zones of absolute darkness, such as deep parts of caves and other subterranean sites. Bats are found in almost all parts of the world, with exception of polar and cold high-altitude regions. They occupy a variety of ecological niches, which is reflected also in the large span of body sizes: the smallest Kitti’s hog nosed bat (Craseonycteris thonglongyai) weighs only about 2 g, while the great Indian flying fox (Pteropus giganteus) can reach even up to 1600 g (Dietz and Kiefer, 2014). Bats exhibit different dietary habits, including insectivory, frugivory, nectarivory, piscivory, predation on other small vertebrates, and even hemophagy (feeding on blood). Bat diversity is highest near the tropics, and decreases with increasing latitude; this pattern is especially pronounced in the New World continents (Dietz and Kiefer, 2014). Living in groups brings fitness benefits for individuals from interacting with other group members, as opposed to living separately. Bats form the largest aggregations among all vertebrates, and such groups are found almost exclusively in caves. Massive cave colonies are known especially in the family of free-tailed bats (Molossidae), spread all over the world. Wrinkle-lipped freetailed bats (Chaerephon plicata) are widely distributed in Southern Asia, with millions of individuals in caves; when such colonies leave the caves, they form dense clouds kilometers long (Fig. 1). Similarly, the Brazilian free-tailed bats (Tadarida brasiliensis) form colonies of tens of millions of individuals in caves in Southwestern United States (Furey and Racey, 2016). Such large gatherings in caves are known also in some Old World fruit bats, for example, over 850.000 individuals of the Geoffroy’s Rousette fruit bat (Rousettus amplexicaudatus) roost in Monfort cave in the Philippines (Carpenter et al., 2014). Caves present one of the most important natural roosts, but bats can use also other subterranean structures (artificial tunnels, mines, cellars) with similar climatic conditions. In China, nearly 80% of known bat species roost in caves and other subterranean sites, and this proportion is similarly high in other regions around the world (Furey and Racey, 2016). Bats are among the most endangered mammals on the globe, almost a quarter of species are globally threatened according to IUCN criteria (Mickleburgh 94
Encyclopedia of Caves. https://doi.org/10.1016/B978-0-12-814124-3.00013-3 Copyright © 2019 Elsevier Inc. All rights reserved.
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FIG. 1 When emerging from a cave in Vietnam, millions of wrinkle-lipped free-tailed bats (Chaerephon plicata) form dense cloud, extending kilometers in length. (Photo by C. Dietz. Used with permission.)
et al., 2002). Protection of caves and other subterranean sites is therefore a very important factor in bat conservation, though not the only one.
Caves as roosts Bats spend at least half of their life in roosts. They look for safe places, out of reach of potential predators, with microclimatic conditions that suit bats’ seasonal needs. Typically they use existing structures in the environment, either natural (trees, caves, rock crevices, abandoned bird nests) or manmade (buildings, bridges, mines). There are only a few species that form own roosts by folding the foliage into tent-like shelters, or by making holes in termite nests. Caves and similar subterranean sites are available in almost all parts of the world, but whether they will be used by bats depends on various factors. First, even though these are stable environments compared to surface, their characteristics differ among geographical regions, as well as according to their altitudinal position, length, depth, and morphological complexity. Second, bat species differ in roosting requirements, and can use subterranean sites permanently or seasonally. Differences can also be intraspecific, related to sex or geographic position of different populations. Bats may retreat to caves also temporarily during the night, in between feeding bouts. In such roosts they rest, or eat the food. Remains of insects can be found among bat droppings, witnessing hanging places where bats were removing the hard and less nutritious parts of insects (like elytrae or wings). Seeds, that even sprout inside caves, are remains of fruits that have been brought in by frugivorous bats. While eating, bats are less attentive, and caves present safe retreats to finish the meal undisturbed.
Nursery roosts Bats have different life histories than other mammals of comparative size. This is most obvious in reproductive strategies; bats have long periods of pregnancy and lactation; they give birth only once a year, having one, exceptionally two, juveniles. Bat mothers invest a lot of their resources in raising the young until they become independent. In most insectivore bats, juveniles suckle until they are 90% of adult size (Crichton and Krutzsch, 2000). Longevity of bats is exceptional in mammal world— in many species, life spans of over 30 years have been recorded. In summers, bats exhibit strong sexual segregation. Males either live solitarily or in small groups, while females gather separately in assemblages that can be very large. In such nursery (or maternity) colonies, they give birth and raise the young. Juvenile bats have poor thermoregulatory abilities, and benefit from being in the group—this enables increase in areal temperature, and heating benefits from direct body contacts (Fig. 2). Usually the availability of microclimatically suitable sites is limited, so group living enables more bats to use the sites with optimal conditions. Many different species share similar roosting demands, and interspecific grouping of two or more species is common in bats. Despite many benefits that come from living in such large groups, this also generates certain costs. The potential for transmission of diseases and parasites is greater. Large numbers of bats sharing the same roost need to search for feeding grounds in a wider distance than solitary living bats. The latter is less pronounced in groups of different species that have different foraging habitat preferences and consequently lower competition for food resources. One of the species that uses caves throughout the year, and forms very large colonies, is Brazilian free-tailed bat (Tadarida brasiliensis). This species, distributed in Southern Nearctic, Central and Southern America, commonly uses caves as shelters.
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FIG. 2 Two different nursery groups of vespertilionid bats in caves of Southern Europe. Top: Female greater mouse-eared bats (Myotis myotis) and their young during the day; if they change the position, they can take the juveniles with them. Below: Long-fingered bats (Myotis capaccinii) with few mouse-eared bats (Myotis myotis/Myotis oxgnathus), as seen during the night. This cluster consists mainly of juveniles, tightly holding to one another, when females are away. (Photos by P. Presetnik (top) and C. Dietz (down). Used with permission.)
Brazilian free-tailed bats form some of the largest colonies in the world, and as much as 1800 individuals can gather together in 1 m2. The number of individuals per square meter was estimated to be even 5000 for groups of juveniles that are left in the roost while mothers leave for night foraging (McCracken, 1986). Despite such large numbers, mothers are able to find their own young among millions of other juveniles every night. They first use a very good spatial memory to find the right sector of the cave, and then locate their pup by characteristic vocalizations (isolation calls) and scent cues. In Europe, there are a number of species that breed in caves, but there is a latitudinal limit up to which the caves and other subterranean sites have suitable microclimatic conditions for such use. For some species, like long-fingered bats (Myotis capaccinii), this restricts the range to Southern Europe. But others, like greater mouse-eared bats (Myotis myotis) or lesser horseshoe bats (Rhinolophus hipposideros), successfully exploit alternative roosts—buildings, at the north parts of species distribution range. Warm attics of churches and castles present top priority sites in the conservation of such species in Central Europe (Dietz et al., 2009).
Hibernation roosts Bats are homeothermic animals, but they are able to change the metabolic rate and body temperature. They can lower their body metabolism to decrease the use of energy to basic metabolic functions on a daily basis, which is called torpor. They can spend even days in constant torpor to survive periods of bad weather when food availability is low. During winter, temperate bat species are able to survive even months of low or no food availability, living solely on stored energy. This is hibernation, when bats sustain extremely low metabolism and conserve basic life functions to survive. For example, in greater mouse-eared bats (Myotis myotis), the number of heart beats reaches 880 bpm in flight, while it is only 18–80 bpm during hibernation (Dietz et al., 2009). Due to constant low temperatures and high humidity, caves and other subterranean sites are suitable hibernation sites for many bat species, even the ones that roost elsewhere in summer. During hibernation, bats live only on fat reserves gathered in autumn. Decrease in body temperature of around 10°C can save up to 50%–70% energy per time unit (Dietz et al., 2009). Bat’s body temperature is set according to ambient temperature, and when the latter are too low or too high, bats wake up to change the position. Bat species have different preferences on suitable conditions for hibernation, and can be found in very different parts of the same cave (Fig. 3).
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FIG. 3 Simplified presentation of the cave in Central Europe, showing the diversity of compartments that bats can select during hibernation. Different species have different climatic preferences, which differ with distance from the cave entrance. Abbreviations refer to: Bbar, Barbastella barbastellus; Enil, Eptesicus nilssoni; Eser, Eptesicus serotinus; Mbec, Myotis bechsteinii; Mbra, Myotis brandtii; Mdau, Myotis daubentonii; Mema, Myotis emarginatus; Mnat, Myotis nattereri; Mmyo, Myotis myotis; Mmys, Myotis mystacinus; Plsp, Plecotus species; Rsp, Rhinolophus species. (Figure is supplemented and modified after Dietz and Kiefer, 2014, pp. 62.)
Search for suitable hibernation roosts is a strong driver of long distance bat migrations recorded in Europe and North America. For example, Nathusius’ bats (Pipistrellus nathusii) and noctules (Nyctalus noctula) can travel over 1000 km in autumn to find suitable wintering sites in Southern Europe (Dietz et al., 2009). Long distance migrations between summer and winter roosts are also known in Schreiber’s bent-winged bats (Miniopterus schreibersii), where individuals from different summer colonies gather in the same winter roosts, forming tight clusters of thousands of individuals. In some bat species many individuals can gather at the same cave, but hang separately (Fig. 4) or in groups of only few animals. The hibernation period is usually related to a moderate or cold climate, and long winter periods with low food availability. But, a case of hibernation in warm caves was described for two species of mouse-tailed bat (Rhinopoma) species in semiarid and warm areas of Asia and Africa (Levin et al., 2015). They hibernate for 5 months, in caves as warm as 20 °C, even though they do have cold caves available close by. These bats seem to select such warm caves, often heated by geothermal temperature. They are generally subtropical bats, and the ability to go into hibernation is present only at the northern border of their distribution. This is an exceptional case, and the ability to hibernate seems to be a strong limiting factor for many tropical and subtropical species for not extending their range to northern latitudes (Dietz and Kiefer, 2014).
FIG. 4 Some bats hang individually on cave walls during hibernation. Lesser horseshoe bats (Rhinolophus hipposideros) wrap themselves completely in flight membrane (left), and hang separately even when large aggregations of individuals are found in European caves. Vespertilionid bats, like tricolored bat (Perimyotis subflavius) from a cave in Eastern United States, never wrap themselves in wing membrane. Small water drops are seen on bats’ fur. (Photo by M. Zagmajster.)
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Mating sites In temperate zones, bat activity in caves and other underground sites increases substantially at the end of summer and in autumn, for the behavior called swarming. Bats are active and circle in and around the cave entrance throughout the night, while during the day they may roost elsewhere. Bechstein’s bats (Myotis bechsteinii) in Europe, typical forest dwelling species that roosts in tree cavities during summer, come to caves for mating as well as hibernation. In this species, females exhibit very high fidelity to birth sites and, nursery colonies typically present groups of closely related bats. Autumn swarming sites present crucial way to maintain the gene flow among such separated populations, which is facilitated by migrating males (Kerth et al., 2003). This behavior and its function was observed in numerous temperate bat species of Old as well as New World. Swarming sites are not random, and individual bats tend to frequent a few sites more often. Even though swarming behavior is a type of promiscuous behavior, some bats exhibit polygynous mating. Males may establish territories and attract females through self-advertisement. They can defend small territories on cave walls, where they attract females with the scent or special vocalization. Males of greater mouse-eared bats (Myotis myotis) mark small patches on the cave wall with gland excretions and urine to attract females. Once the female comes, the male holds her and defends her against other males. Many bat species can establish true harems, which in tropical species present more or less stable groups throughout the year. For example, in Jamaican fruit bats (Artibeus jamaicensis), one male can guard a group of up to 15 females (McCracken and Wilkinson, 2000). In least long-fingered bat (Miniopterus minor) in East Africa, groups of males were observed in a hole of cave ceiling, having higher mass than males of outside groups. It was assumed that the females come to such group, and mate with the best male, which indicates lek behavior (McCracken and Wilkinson, 2000). Monogamy is rare among bats. Two examples are the African false vampire bat (Cardioderma cor) and the Spectral bat (Vampyrum spectrum). As both species are carnivorous predators, male provides females and young. This care system probably even led to evolution of monogamy (McCracken and Wilkinson, 2000). There are cases when bats can avoid courtship and copulate with females when already in hibernation. This mating is indiscriminant, as in little brown bat (Myotis lucifugus), where males frequently copulate with hibernating females throughout the winter (McCracken and Wilkinson, 2000). Greater horseshoe bats (Rhinolophus ferrumequinum) come to caves in autumn, and exhibit territorial behavior (Furey and Racey, 2016). Males maintain large testes throughout the winter and mating can occur during hibernation period. Besides mating, swarming may play a role also in search for potential hibernation roosts – species compositions in autumn and winter at some sites are indeed very similar. Some observations of mothers being followed by their young also imply, that this is the behavior by which the offspring gets introduced to potential wintering sites.
Importance of bats in caves Vectors of nutrients Bats are among the most important carriers of organic matter in caves, which are typically resource-poor environments. This is especially pronounced in dry caves, where nutrients cannot enter the system via rivers or percolating water. Bats also die in caves, or bring in the remains of their food; this is then used by many different animal species and microorganisms. Especially in the tropics, bats form large groups that inhabit caves throughout the year, and their droppings present constant source of nutrients. Diverse invertebrate communities can feed directly on bat guano, or on the microorganisms that grow on guano deposits. Some invertebrates specialized on certain type of bat guano, like in the case of collembolan species Acherontides eleonorae. These collembolans prefer to live in guano piles of blood feeding bats, like common vampire bat (Desmodus rotundus) (Fig. 5), and possess special morphological adaptations that allow them to walk on such moist surface. Species specialized to living exclusively in guano piles are termed guanobionts, and their species richness as well as abundances can be substantial. Bat guano presents important resource also to aquatic animals. Bat droppings have been identified as the main food source for the adult Mexican cave fish (Astyanax mexicanus), while larval stages of the fish feed mainly on small invertebrates (Espinasa et al., 2017).
Ecosystem services and economic impacts Bats feed in various surface habitats, where they have important ecological roles. From human perspective, they provide various ecosystem services, that is, their activities have benefits to humans (Kunz et al., 2011). Bats feeding on fruits and nectar help in dispersing seeds and in pollinating flowers. Insectivore bats present natural way of regulating the numbers of insects in nature, among which many are considered pests. In Thailand, the wrinkle-lipped free-tailed bat (Chaerephon plicatus) consumes considerable amounts of white-backed planthoppers (Sogatella furcifera), which are a major pest in rice crops (Furey and Racey, 2016).
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FIG. 5 Female common vampire bats (Desmodus rotundus) with juvenile (left) from a cave in Brazil. This species forms large groups in caves, and produce typical dark shiny guano piles (right). (Photo by M. Zagmajster.)
In the United States, the importance of bats in insect pest control was calculated, and it was estimated that loss of bats in Northern America could lead to agricultural losses estimated at more than 3.7 billion US dollars per year (Boyles et al., 2011). In some parts of the world, especially in Asia, the exploitation of bat guano in caves is an important economic activity of local communities (Kunz et al., 2011). Such guano is rich in nitrates and phosphates, and is considered and sold as a valuable fertilizer. Bats can attract tourists. For example, observations of large evening emergences of Brazilian free-tailed bats (Tadarida brasiliensis) are offered as additional tourist attraction in Carlsbad Caverns in New Mexico (Furey and Racey, 2016). It has been established, that bats are carriers of different viral diseases, and able to cope with infections, like Ebola. Knowing these mechanisms may offer important medicinal insights for curing the disease. Common vampire bats (Desmodus rotundus) are carriers of rabies, which in some regions present a threat to humans, but they may in fact hide important medical applications, coming from the chemicals present in their saliva (Kunz et al., 2011).
Conservation of bats in caves Threats Bats are subjected to numerous threats, which affect them at their roosts as well as foraging habitats. They can be very diverse and abundant in caves, and threats to such sites can have immense negative effects on regional populations, which can even result in local extinctions. The importance to protect the caves is especially evident in cases, where bat species are dependent on roosting only in such habitats and exhibit low population sizes. Such is the example of the Kitti’s hog-nosed bat (Craseonycteris thonglongyai), which is known only from caves in Myanmar and Thailand. The population in Thailand is estimated to be 5,100 and has decreased substantially, with more than 10% decrease every decade since 1983 (Bates et al., 2008). Humans visit caves for various reasons, mostly for tourism, as sanctuaries, or for guano mining (Kunz et al., 2011). Disturbance of nursery colonies may cause female bats to drop their nonvolant juveniles, and eventually leave the roost. During hibernation, any extra arousals result in extra use of fat reserves and lower chances of surviving the winter. Introduction of infrastructure to caves (like installation of lights), closing the entrances, as well as visits of large groups of people can alter the microclimatic conditions, introduce noise or prevent access to caves, which can result in bats abandoning the roost. In some parts of Asia, bats are regularly used as food, and hunted also in caves (Kunz et al., 2011). Controlling this is especially challenging, as bat meat is used for local consumption as well as in trading, and it is served to tourists as local specialty (Mickleburgh et al., 2009). Quarrying and destruction of caves is considered as probably the greatest threat to bats in Southeast Asia. This is the region with the highest annual quarrying rates and still growing, which may bring some species close to extinction (Furey and Racey, 2016). Some bat species are considered pests, but the methods to control their numbers can be used too extensively or unselectively. The Egyptian fruit bat (Rousettus aegyptiacus; Fig. 6) is thought to cause economical damage to commercial fruit industry in many Mediterranean countries. Common vampire bats (Desmodus rotundus) in Central and South America are carriers of rabies and regularly killed. When methods like fumigation and closing of the caves are used, they unselectively affect also all other cave bat species (Furey and Racey, 2016).
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FIG. 6 The group of Egyptian fruit bat (Rousettus aegyptiacus) from a cave in Turkey. (Photo by C. Dietz. Used with permission.)
Examples of massive deaths of bats due to different diseases have been registered in various parts of the world in the last decades. But one of the biggest threats to cave bats, which has been severely depleting bat populations in North America, is the white-nose syndrome. It was first registered in 2006 in a few caves of Northeastern United States, when no one anticipated such a rapid spread of the disease, which resulted in massive deaths of millions of bats around the continent. The infection causes bats to wake up more frequently from hibernation, and as they are unable to feed during cold winters, they get exhausted and eventually die. Drops in populations were severe, and brought some species, like Indiana bat (Myotis sodalis), close to extinction. The disease is caused by the fungus Pseudogymnoascus destructans, which was also discovered in caves in Europe, where it did not cause massive mortalities (Puechmaille et al., 2011). Understanding evolved resistance of European bats that is lacking in American bat populations, and other ongoing studies into this phenomenon could eventually help in protecting North American bats. Pesticides, for example, DDT, were suspected to greatly influence the declines of large colonies of Brazilian free-tailed bats (Tadarida brasiliensis) in Southern United States. Carlsbad Caverns was reputed to have housed 8.7 million bats in the 1930s, but for the past 15 years its population has been more or less stable at about 500,000 (Furey and Racey, 2016). In Western Europe, severe declines of lesser horseshoe bats (Rhinolophus hipposideros) started in the middle of 20th century, leading to extinctions in Netherlands and Luxembourg. The main cause of declines were excessive applications of toxic pesticides, such as DDT and lindane (Dietz et al., 2009). Cave-dwelling bats are subjected to threats stemming from changes in the natural environments, which include deforestation, intensive agriculture as well as urbanization and light pollution. In the United States, mass mortalities of bats were discovered at wind turbines, and up to 24% of the bat fatalities at some wind energy facilities have been cave-roosting species (Kunz et al., 2007). Also in Europe, several species of cave-roosting bats are being killed by wind turbines (Dietz and Kiefer, 2014).
Conservation measures One of the most widely implemented approaches in the conservation of caves for bats is closing of cave entrances to prevent unauthorized human visits. But, gates should not change the natural air currents in the cave, which could affect cave microclimate, and they should permit the bats to freely exit and enter the site. Various grilling solutions have been developed and built in caves and other subterranean sites, but it has been reported that grills are not acceptable for all bat species (Dietz et al., 2009). This does not depend only on the flight agility of species, but also on numbers of bats and size of the entrance (Tobin and Chambers, 2017). Fast flying species like Brazilian free-tailed bats (Tadarida brasiliensis) in Americas, or Schreiber’s bent-winged bats (Miniopterus schreibersii) in Europe, could not tolerate grills (Dietz et al., 2009; Furey and Racey, 2016). An alternative approach toward preventing the access to caves is to set the fences at some distance around the cave entrance (Furey and Racey, 2016). Disturbances from tourist exploitation, as well as guano mining, should be prevented in bat important subterranean sites. Cave visits could be permitted only in times when they are not occupied by bats. If morphology of the cave permits, only part of the cave is used for tourism, while parts important for bats are being avoided. Such approaches have been successfully used in some caves around Europe. Implementing conservation measures at roosts seems to be fairly straightforward, but conservation should also include noncave roosts, that bats may use in other seasons, and landscape level protection, as bats fly long distances from roosts to different feeding grounds. All activities that sustain a mosaic and diverse landscape, preserve the natural forests, lower the use of pesticides, also benefit conservation of cave bats. New facilities that could harm bats, like wind farms, should not be built close to bat
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roosts, important feeding grounds and migratory routes. In recent years, potential compromise solution for the use of wind farms includes part time cutoffs, which is achieved by predefined time interval constraints. A lot of research is conducted on improving automatic detection of high bat activity and automatic stopping of wind turbines during such periods. Numerous negative prejudices and misbeliefs about bats can hamper conservation actions, so raising public awareness and educating people on importance as well as endangerment of bats is of high priority. This is the goal of numerous organizations around the world working on international levels, here we name only few. Fauna & Flora International works on many aspects for the conservation of bats and their habitats worldwide (https://www.fauna-flora.org/). Bat Conservation International (www. batcon.org) works mainly within United States and Canada, and also globally, while BatLife Europe (https://www.batlifeeurope.info/) joins national nongovernmental organizations, with the aim to work toward promotion and protection of bats in Europe. Nearly 90% of known bat species are included in the IUCN Red List of Threatened Species, and they are part of different legal protection schemes. Bats are able to migrate long distances between different types of roosts and feeding grounds, so protection should be done beyond borders. An international instrument within Europe and some non-European states is the The Agreement on the Conservation of Populations of European Bats (EUROBATS), set up under the Convention on the Conservation of Migratory Species of Wild Animals. Another strong legal mechanism for bat protection within Europe is European Habitats Directive (92/43/EEC), which protects all bat species, and requests designation of network of important sites for conservation (so called Natura 2000 sites) for 14 bat species. In other continents, bats are protected via species protection acts, which can lead to protection of caves due to their importance for bats.
See related articles Guano Communities White Nose Syndrome
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