Conservation Strategies for Bats Flying at High Altitudes

Conservation Strategies for Bats Flying at High Altitudes Abstract Numerous bats use the troposphere for hunting, commuting, or migrating. High-altitude flying bats face various direct and indirect threats, including collision with tall anthropogenic structures and aerial vehicles, aerial fragmentation, reduced insect biomass, and the altered ambient conditions associated with climate change. Furthermore, dust and chemical pollutants in the troposphere might impair the health and survival of bats. Such indirect threats are diffuse regarding their origin and effect on bats, whereas direct threats are site and context specific. Overall, troposphere habitat conservation is hampered by the “Tragedy of the Commons” because its stewardship is in the hands of many. We conclude that high-altitude flying bats are likely to become more threatened in the near future because of the increased use of the troposphere by humans. Therefore, we should target the protection of the troposphere for organisms, such as high-altitude flying bats, that strongly depend on intact skies. Despite ever-growing knowledge about flying megabiota and drifting microbiota in the troposphere, researchers and managers have only recently recognized two important aspects associated with the lifestyle of airborne organisms. First, the lower boundaries of the troposphere represent valuable habitat for a variety of organisms (Diehl 2013). Second, the troposphere should be included in global conservation strategies (Lambertucci et al. 2015, Davy et al. 2017). Indeed, airborne species represent a substantial portion of global biodiversity (Kunz et al. 2008, Diehl 2013, Davy et al. 2017). Nonetheless, conservation needs related to the use of the aerosphere have been largely neglected. For example, the International Union for Conservation of Nature (IUCN) scheme recognizes only terrestrial and aquatic habitats but ignores aerial habitats (Davy et al. 2017). The reason for this negligence might lie in the fact that specific stewardship of the three-dimensional aerosphere is difficult to define. Because most areas of the troposphere are in public hands, mitigation of any human-induced perturbations in the aerosphere may be prone to the “Tragedy of the Commons,” similar to the diluted responsibilities documented for marine habitats in the fight against the overexploitation of fish populations. Moreover, conservation efforts are constrained by human perception bias and limited to our immediate geographical surroundings. Consequently, current policy and research programs ignore the major conservation gap for aerial species and their habitats (Davy et al. 2017). Conservation strategies that do exist for the troposphere have mainly targeted birds, but recent studies have highlighted the lower troposphere as important habitat for bats as well (Kunz et al. 2008, Frick et al. 2013, Davy et al. 2017), although the cryptic nature of bats and the limited accessibility of the troposphere for recording and documenting bat activities have severely hampered initial efforts. Bats have been active in the so-called open-space for millions of years, and many of the 1300 extant bat species ascend into the skies nightly to hunt prey. Morphology and echolocation frequency separate bat species that preferentially forage in cluttered habitats (i.e., forests) from those that exploit the open space (Schnitzler and Kalko 2001). For example, some families of Chiroptera, such as the Molossidae and Rhinopomatidae, are particularly well adapted to hunt in open space because they have long, slender wings and a high aspect ratio (Voigt and Holderied 2012). Open-space foraging bats play an important regulatory role as predators in natural ecosystems and anthropogenic habitats such as farmland and managed forests. The estimated value of the ecosystem services provided by bats is worth billions of dollars (box 1; McCracken et al. 2008, Boyles et al. 2011). Box 1. Ecosystem services provided by bats during high-altitude flights. View largeDownload slide View largeDownload slide High-altitude flying bats offer ecosystem services for agriculture and silviculture (Boyles et al. 2011,). For example, open-space bats are considered to play a key role in the regulation of pest insects, such as corn earworms in Northern America and planthoppers in Southeast Asia. Millions of these bats roost in single caves and therefore have to spread over vast areas during their foraging flights (Williams et al. 1973, Bat Conservation International 2013,). Several studies confirmed the foraging activity of bats via acoustic recording at high altitudes (Fenton and Griffin 1997,, McCracken et al. 2007). Recent advancements in GPS technology also allow fine-scale observations of flight behavior at high altitudes, showing rapidly undulating changes in the flight altitude of high-flying insect-feeding bats that may be used to scan the aerosphere in search of high-flying prey insects (Cvikel et al. 2015, Roeleke et al. 2017 ). In this article, we briefly summarize how bats use the troposphere and the threats they might face in this space, expanding significantly on what has already been established (Kunz et al. 2008). We outline some problems and possible solutions for the protection of bats in the lower boundaries of the troposphere. In the remainder of the text, we consider the troposphere as outlined by Davy and colleagues (2017): the basoaerial zone includes the air column between ground level to 1 kilometer above sea level (ASL), and the ­mesoaerial zone includes the adjunct air column between 1 and 8 kilometers ASL. The boundaries of these layers are dynamic and vary across landscapes, and bats may travel between both layers. For simplicity, we refer to these two layers as the aerosphere. We use the term high altitude to describe bat flight behavior that goes well beyond the landscape topography, including vegetation structure (forest canopy). How do bats exploit the aerosphere, and at what altitude? Bats are the only mammals capable of active flight and have specialized organs for efficient oxygen uptake and transport, allowing them to fly in different environments all over the world (Canals et al. 2011). High altitudes pose a number of constraints on aerodynamics: at high altitude (more than 5000 m ASL), oxygen partial pressure falls to less than 50% of that at sea level, and air density is lower. However, some open-space foragers fly at relatively high altitudes on a daily basis (Williams et al. 1973, Fenton and Griffin 1997, McCracken et al. 2008, Roeleke et al. 2017). Fast-flying molossid bats such as Tadarida brasiliensis or Tadarida aegyptiaca have some of the highest reported hematocrits and a slightly lower oxygen affinity than other species, potentially a specialization for flight at high altitude (Black and Wiederhielm 1976). Bats may occur in large numbers in the aerosphere; for example, T. brasiliensis emerge from Bracken Cave in Texas in the millions each night to hunt at high altitudes (Williams et al. 1973, Chilson et al. 2012). Radar scans from weather stations indicate that these bats can cover vast areas during their nightly search for insects (Chilson et al. 2012, Mirkovic et al. 2016). It is important to acknowledge that such mass phenomena may be widespread around the tropical belt. In the Old World, open-space foraging bats have been recorded at altitudes ranging from ground level to more than 800 m (figure 1; Cvikel et al. 2015). Migratory bats, such as the North American Lasiurus cinereus, have been documented at up to 3000 m (Peurach 2003). Studies propose that such high-altitude migration may be associated with insect migration (Chapman et al. 2015). Figure 1. View largeDownload slide The flight altitudes of bats inhabiting the aerosphere. (a) The altitudinal records of seven selected species: Tb, Tadarida brasiliensis (Williams et al. 1973); Lc, Lasiurus cinereus (Peurach 2003); Nn, Nyctalus noctula (Ahlén et al. 2007); Rm, Rhinopoma microphyllum (Cvikel et al. 2015); Tb, Taphozous theobaldi (Roeleke et al. 2017); Pp, Pteropus poliocephalus (Parsons et al. 2008). The silhouettes in the bars depict examples of the tallest buildings in the species distribution ranges (One World Trade Center, United States; CN Tower, Canada; Berlin TV Tower, Germany; Milad Tower, Iran; MahaNakhon, Thailand; and Eureka Tower, Australia). The basoaerial and mesoaerial zones are indicated with atmospheric pressure values (Davy et al. 2017). (b) An excerpt from a GPS track of T. theobaldi. Flight altitudes reach more than 800 m above ground. Density plots of flight altitude of three species can be found in the supplemental materials. Photograph credits: Tb, Lc, and Pp copyright by MerlinTuttle.org; Rm copyright by Christian Dietz. Figure 1. View largeDownload slide The flight altitudes of bats inhabiting the aerosphere. (a) The altitudinal records of seven selected species: Tb, Tadarida brasiliensis (Williams et al. 1973); Lc, Lasiurus cinereus (Peurach 2003); Nn, Nyctalus noctula (Ahlén et al. 2007); Rm, Rhinopoma microphyllum (Cvikel et al. 2015); Tb, Taphozous theobaldi (Roeleke et al. 2017); Pp, Pteropus poliocephalus (Parsons et al. 2008). The silhouettes in the bars depict examples of the tallest buildings in the species distribution ranges (One World Trade Center, United States; CN Tower, Canada; Berlin TV Tower, Germany; Milad Tower, Iran; MahaNakhon, Thailand; and Eureka Tower, Australia). The basoaerial and mesoaerial zones are indicated with atmospheric pressure values (Davy et al. 2017). (b) An excerpt from a GPS track of T. theobaldi. Flight altitudes reach more than 800 m above ground. Density plots of flight altitude of three species can be found in the supplemental materials. Photograph credits: Tb, Lc, and Pp copyright by MerlinTuttle.org; Rm copyright by Christian Dietz. Pteropodid bats, which depend on ground-based food resources (i.e., fruits or nectar), can also be found flying at high altitudes when commuting between feeding and roosting sites (Tsoar et al. 2011). For instance, some pteropodid individuals have been found at altitudes of more than 1500 m (Parsons et al. 2008). It is likely that many more species exploit the aerosphere, but our current knowledge is impeded by the technical constraints associated with the relatively small size of bats and the high costs of miniaturized global positioning system (GPS) or data loggers. Bats use high altitudes for a range of purposes, such as orientation, foraging, and migration, among others. For example, bats have been observed flying to high altitudes from a release site presumably for orientation before commuting to their colony (Tsoar et al. 2011). Observations of high-altitude flights include straight flights at high speed and complex aerial maneuvers likely associated with hunting and catching prey (Cvikel et al. 2015, Roeleke et al. 2016). Nevertheless, the primary goal of most high-altitude bats is to forage for insects (Fenton and Griffin 1997, Boyles et al. 2011). Acoustic recorders attached to helium-filled kite balloons provided the first evidence of hunting events at high altitudes (Griffin and Thompson 1982, Fenton and Griffin 1997). This observation was later confirmed by bats carrying GPS loggers with onboard ultrasonic microphones (Cvikel et al. 2015). Some species, such as Rhinopoma microphyllum and Taphozous theobaldi, seem to scan the three-dimensional airspace with undulating altitudinal flights ranging from a few meters’ to several hundred meters in altitude (Cvikel et al. 2014, Roeleke et al. 2017). During the ascent, these bats may benefit energetically by taking advantage of updrafts (i.e., soaring; Siefer and Kriner 1991, Thomson et al. 2002), and they may probe high-altitude winds to catch mass movements of insects (Siefer and Kriner 1991, Chapman et al. 2010). Typology of threats for open-space foraging bats in the aerosphere Bats face severe threats when flying in the aerosphere ­(figure 2). These threats can be separated into direct and indirect effects: causing immediate injuries and deaths (direct) or impaired health and long-term reduction in reproductive fitness (indirect). Figure 2. View largeDownload slide Threats to bats flying at high altitudes. The occurrence of obstacles at specific altitudes is depicted by the orange lines (logarithmic scale). Photographs (a)–(d) highlight selected indirect threats to bat health and navigation capacity. (a) Nightly sky glow and wind turbines in a coastal area of Europe. Photograph: copyright by Jasja Dekker. (b) Night lighting and sky glow in urban areas of Central America. Photograph: copyright by Fernando Tomás. (c) Haze formation after slash-and-burn forest clearing in the tropics seen from space, at a 380-kilometer altitude. Source: ISS029-E-8032 NASA’s Earth Observatory via Wikimedia Commons (public domain). (d) Industrial air pollution at sunset. Source: www.pixabay.com (public domain). Figure 2. View largeDownload slide Threats to bats flying at high altitudes. The occurrence of obstacles at specific altitudes is depicted by the orange lines (logarithmic scale). Photographs (a)–(d) highlight selected indirect threats to bat health and navigation capacity. (a) Nightly sky glow and wind turbines in a coastal area of Europe. Photograph: copyright by Jasja Dekker. (b) Night lighting and sky glow in urban areas of Central America. Photograph: copyright by Fernando Tomás. (c) Haze formation after slash-and-burn forest clearing in the tropics seen from space, at a 380-kilometer altitude. Source: ISS029-E-8032 NASA’s Earth Observatory via Wikimedia Commons (public domain). (d) Industrial air pollution at sunset. Source: www.pixabay.com (public domain). Wind turbines Many countries strive to move from conventional energy production to renewable sources in an effort to fight global climate change. Unfortunately, evidence suggests that there is a large-scale negative impact of wind energy production on many wildlife species, including bats (Voigt et al. 2015, Frick et al. 2017). Bat fatality records at wind turbines show that open-space foragers are the most critically affected bat group worldwide (Arnett et al. 2016). However, the number of bats killed at wind turbines annually is largely unknown because there seems to be variability across regions (Arnett et al. 2016). The cumulative installed capacity of wind turbines worldwide was estimated to be 490,000 megawatts in 2015 (GWEC 2016). For Central Europe, annual estimates of fatality rates suggest that approximately 10 bats die per 1 megawatt of energy produced if no mitigation scheme (e.g., cut-in speeds of wind turbines) is practiced (Brinkmann et al. 2011). With implemented mitigation schemes being the exception rather than the norm, global mass mortalities may number in the millions per year. Many open-space foraging bats are killed during their annual migrations (Lehnert et al. 2014, Voigt et al. 2016) and die either by blunt-force trauma from collisions or from barotrauma caused by contact with turbulent vortices in the tailwind of rotors (Baerwald et al. 2008). Recent modeling of air pressure changes indicates that vortices may drift for several hundred meters from wind turbines or even occur in front of turbines (Rohrig 2017). Therefore, the effective three-dimensional sphere that is dangerous for bats may be larger than the circular area swept by the rotor blades. The overall trend for increasing wind turbine size may intensify the threat for bats flying at the operational altitudes of turbines (between 30 and more than 200 m aboveground; Arnett et al. 2016). Aerial vehicles Currently, we lack quantitative data on how often bats are killed by airborne vehicles such as planes, helicopters, or drones. The US Air Force (USAF) has documented around 800 airstrikes within a 10-year period, most often with T. brasiliensis, costing the USAF upwards of US$825,000 in damage to aircraft (Peurach et al. 2009). In addition, collisions with Tadarida teniotis and R. microphyllum have damaged helicopters during military operations (Washburn et al. 2014). Biondi and colleagues (2013) listed 417 incidents with commercial aircraft in the United States between 1990 and 2010. In Australia, several hundred flying foxes (Pteropodidae) were documented in collisions with aircrafts at airports within a 10-year period (Parsons et al. 2008). In addition, a new threat is emerging in the form of unmanned aerial vehicles, which are an ever-increasing economic market. Wildlife strikes are filed only when an aerial vehicle is damaged, so many incidences may go undocumented, making it difficult to assess the total impact of airstrikes on bat populations overall. Aerial fatalities vary depending on the spatial distribution and abundance of high-altitude flying bats and those of aerial vehicles. In addition to the direct threats of collision, bats are sensitive to noise and artificial light, likely causing bats to abandon areas with heavy traffic by aerial vehicles, such as when planes are queuing for landing in the lower strata of the aerosphere in the vicinity of airports. Military and urban areas with high aerial traffic may thus act as barriers for bats, leading to fragmentation of the aerial habitat. We conclude that the potential conflict between open-space bats and aerial vehicles might therefore become ever stronger (Davy et al. 2017). Fragmentation of the aerial habitat Considering the seemingly endless skies, habitat fragmentation in the aerosphere may seem counterintuitive, but there is growing evidence that resources, such as high-flying insects, are not equally distributed across the sky. Indeed, Diehl (2013) pointed out that similar to terrestrial habitats, the troposphere might be highly fragmented as well. For example, some open-space foraging bats, such as Rhinopoma, hunt ephemeral insects with a patchy distribution (i.e., swarming or hilltopping winged ants; Siefer and Kriner 1991, Gillam 2007, Cvikel et al. 2015). The effort required to locate such patches in a three-dimensional space might explain the strong selection for group hunting in many open-space foraging bats (Dechmann et al. 2009). A reduction in insect biomass at the ground level may aggravate the availability and quality of patches of insects in the aerosphere, leading to higher search efforts and decreasing energy gain per distance traveled. This is particularly true for industrialized countries, where insect biomass is already decreasing and may become critical for open-space foraging bats in the future (e.g., Hallmann et al. 2017). In addition, the expansion of urban centers with tall buildings increases collision risk (Crawford and Baker 1981) and aerial fragmentation when bats are forced to take detours to reach foraging patches, probably resulting in increased energy expenditure. Global climate change Rising global temperatures may alter the transmission of sounds and thus the echolocation call efficiency of bats (Luo et al. 2014). For example, the maximum distance of echo-based detection of insects changes with increasing temperature. Most open-space foraging bats call at low frequencies and will benefit from such changes as prey-detection distances increasing. However, for temperate zone bats calling above 40 kHz, prey-detection distances will decrease with increasing temperature (Luo et al. 2014). Detection distances that have been altered by climate change may exacerbate the aforementioned fragmentation of skies in terms of insect resources. During flight, bats must dissipate high heat loads generated by flight muscles. Increased ambient temperature and decreased humidity at high altitudes may change the rate of heat dissipation and evaporative water loss of high-altitude flying bats. This may force bats to return to the ground to drink more frequently or avoid hot aerial layers when foraging. Temperatures decrease approximately 1 degree Celsius per 100 m of altitude, allowing high-altitude flying bats to balance their heat load; a warming climate may make the aerospace less tolerable for many species. The potential to move higher to combat warming body temperatures may prove difficult because air density decreases with altitude. Changing environmental conditions may affect the activity patterns and energy requirements of many open-space foragers. For example, climate change may alter the emergence patterns of bats (Frick et al. 2012). Furthermore, higher temperatures may lead to decreased torpor use throughout the year, forcing animals to forage more to balance their daily energetic requirements, thereby exposing foraging animals to direct threats. In addition, global climate change may change the phenology, intensity, and directions of large-scale insect migrations (Chapman et al. 2015), with yet-unforeseen consequences for bats as insect consumers. Dust and chemical pollutants Soil-derived particles forming dust are known to be carried at high altitudes over long distances as part of a natural process (Kellogg and Griffin 2006). At present, increasing particle emission rates from anthropogenic sources have added to the natural “fog of dust” in the aerosphere. For example, 2.4 billion humans depend on household fires with biomass fuels worldwide, particularly in developing countries of Africa and Asia (IEA and OECD 2004). Aside from producing massive amounts of greenhouse gases, household fires produce ash and dust particles that are released into the aerosphere, where they passively disperse unfiltered over large areas. Emissions from such household fires are known to be harmful to humans (Rehfuess et al. 2006), but the health consequences for wildlife have not yet been considered. Although global climate change may cause hotter and drier environments worldwide, it is likely that wind erosion and associated dust emissions from drylands may become an increasing problem in the future. In addition, increasing amounts of chemical pollutants in the aerosphere produced by industry and agriculture are therefore exposing open-space foraging bats to higher amounts of these particles—but with unknown health implications. Considering the highly specialized respiratory organs of bats, the high metabolic cost of powered flight in low air density, and the unknown impacts of these increasing pollutants on respiratory function, flight in this space may be severely hampered for many species. Recently, combustion-derived metal particles (magnetite crystals) were found to even migrate deep into the human brain, putatively causing cognitive impairment over time (Maher et al. 2016). Similar particles, although of likely natural origin, were detected in the brains of bats, particularly in high-altitude flying species, in which previous speculation considered these particles to be important for the magnetic sense (Tian et al. 2010). If the cost of flight increases because of the impaired navigation skills of bats, the total amount of time taken to migrate or commute long distances could also increase as the need for rest and replenishing fat reserves would also increase. This could introduce new problems for species that have rigid seasonal movement patterns. If individuals are less capable of reaching their desired location in time, new roost sites may be sought out in less favorable habitats. Sensory pollution Open-space bats heavily rely on visual orientation and navigation, whereas low-flying species’ three-dimensional visual range is restricted by habitat structure and landscape topography (Boonman et al. 2013). High-altitude flying bats gain wide panoramic views on the Earth's surface and firmament. However, with increased flight altitude, bats are exposed to more artificial light sources from more distant places. Consequently, they are more vulnerable to impairment of their vision through light pollution and are affected in their route choice depending on species-specific phototactic orientation (Voigt et al. 2017). Although artificial light may not present a physical obstacle, it may nonetheless reduce the connectivity between habitats when bats avoid large areas illuminated by artificial light at night (Rowse et al. 2016). Although the effects of light pollution have been widely studied at ground level, our understanding of the ramifications for high-altitude bats remains scant. However, it is probably safe to assume that direct light emission and sky glow may obscure large parts of the firmament, hampering orientation by celestial cues. Bats also respond in an aversive way to noise (Luo et al. 2014). Noise from anthropogenic sources spilling into the sky may therefore amplify the fragmentation of the aerosphere, such as when jet engines repeatedly create sonic booms in military areas. However, sound pollution most likely affects open-space bats only over short distances because of the strong atmospheric attenuation of sound. Another globally increasing but rarely studied sensory stressor for bats is fireworks, which are known to cause significant short-term disturbances (Shamoun-Baranes et al. 2013) or even injuries in birds. Dust particles and chemical pollutants could cause disorientation because smog and haze obscure vision, forcing bats to fly even higher or avoid affected areas. However, paradoxically, the enriched olfactory landscape of air-polluted areas could increase homing efficiency, an observation recently confirmed for pigeons (Li et al. 2016). Whether open-space bats are susceptible to such a sensory trap, offering facilitated olfactory navigation at the cost of impaired health, remains to be seen. Recent evidence suggests that magnetoreception is an important sensory modality for spatial orientation in many bats (Holland et al. 2006). Radar installations emitting electromagnetic fields (EMF), such as civil and military air traffic control and weather radar, have been shown to have aversive effects on the foraging movements of bats (Nicholls and Racey 2007). This is concerning because EMF are known to disrupt the magnetoreception-based orientation capability of nocturnal migratory birds (Engels et al. 2014) and probably also the orientation capability of migrating bats. It has also been argued that EMF aversion of bats could relate to an increased risk of overheating via thermal induction and/or interference with their auditory system (Nicholls and Racey 2007). Importantly, the sensory impacts on open-space bats are often multimodal because they co-occur in time and space. Conservation strategies for the protection of ­
high-altitude flying bats Since the discovery of the troposphere as a valuable habitat for many organisms, aeroconservation has been named the last frontier of conservation biology (Davy et al. 2017). It is a well-known fact that bats foraging at high altitudes cannot exist without their ground-based roosting structures. The conservation strategies to protect such roosts have already been the focus of much research; therefore, those key findings and management recommendations will not be summarized and discussed here. It is fundamental to all conservation efforts related to open-space foraging bats that daytime and night roosts are protected in order to ensure the survival of this guild in the future. Furthermore, negative anthropogenic effects may only be weakly connected with the place of origin (e.g., when bats affected by aerial dust are far from local areas of dust production by industries, individual household fires, or forest fires). Because anthropogenic effects are diluted in the three-dimensional space, it may be difficult to establish site- or context-specific conservation strategies, turning most efforts related to the protection of open-space foraging bats into rather generic approaches directed to the public. A well-known species conservation concept is to protect the network of habitats an animal population requires for survival and reproduction. For bats, previous conservation efforts focused almost exclusively on ground-based habitats that are relevant for foraging, mating, reproduction, and hibernation and the connection between these. Habitats in the aerosphere have not been widely represented in past conservation strategies unless it was clear that areas such as the space above forest canopies were used by foraging bats. A site-specific conservation approach for the protection of the aerosphere could identify those areas where open-space foraging bats are particularly active. Such areas should be protected against human development, traffic of aerial vehicles, construction of tall anthropogenic structures (including wind turbines), and even the occurrence of occasional fireworks. For example, free-tailed bats emerging from caves may total several million individuals, and the flight paths leading to their high-altitude habitats can be easily identified using radar scans (Chilson et al. 2012). Such emergence areas and flight corridors should be protected against any of the aforementioned anthropogenic impacts in order to conserve these bats. Furthermore, some landscape features cause migratory bats to accumulate at specific locations, such as before crossing large water bodies; when moving along a shoreline or a river valley to their destinations (McGuire et al. 2012); or when aggregating at feeding sites, such as Eidolon helvum in the Kasanka National Park (Richter and Cumming 2006). However, by and large, the available data are deficient regarding the specific landscape features that bats use for migration. For example, mountain ridges or hilltops may be used by open-space foraging bats to launch into the night skies (Roeleke et al. 2017). We therefore call for the identification of landscape features with high activities of open-space foraging bats in order to create protection zones where the aerosphere is protected, but not necessarily the ground—that is, we call for the creation of aeroparks. These aeroparks would likely also benefit a suite of species beyond open-space bats. Frameworks from the implementation of prohibited airspace for aviation could be used as a starting point. Consequently, any anthropogenic stressor potentially emitted in the night sky from within a reasonable buffer zone adjacent to aeroparks would need to be identified. International planning of such aeroparks could allow the creation of a network of such protected spaces, following the network approaches that are already well established for protected areas on the ground level. A conservation physiology approach for high-altitude flying bats could identify anthropogenic pollutants emitted toward potential conservation space and whether these are continuously affecting the sites under consideration. In terms of artificial light pollution, for example, mapping efforts (e.g., www.lightpollutionmap.info) could provide a basis for identifying potential target sites and conflict areas. Dark Sky Reserves are one step in this direction by defining areas with special regulation of artificial light at night in order to reduce light pollution (IDA 2017). Worldwide, around 50 of these reserves have been classified by the IUCN. These areas primarily focus on the protection of dark and therefore starry skies rather than targeting biological conservation. Of course, nocturnal animals, such as bats, automatically benefit from dark-sky reserves; however, this type of conservation area is still not designed for the specific purpose of species conservation. Almost all international conservation initiatives and conventions do not consider high-altitude flying animals. UN Environment Programme conventions such as Ramsar (representing here the conservation of important wetland areas for migratory species) and the Convention on the Conservation of Migratory Species of Wild Animals (CMS) are important conservation tools to protect migratory species and their habitats. However, all of these schemes ignore the aerosphere. This can result in paradoxical situations, such as when European wind energy projects are approved in areas that are protected by the European Habitat Directive (EC 2010). Bearing in mind that energy production from wind represents the main source of renewable energy in Europe (EC 2010) and that 21 of 53 European bat species are known to be active at high altitudes, it is concerning that no concepts for aerial conservation areas have been considered at this stage. In the future, bat-friendly wind energy projects should account for high-altitude fliers and apply mitigation schemes based on conditions in which fatalities typically increase, such as during migration, in relatively mild ambient temperatures, at low wind speed, and in no rainfall (Behr et al. 2016). In summary, there is a clear deficiency in the legislation with respect to the protection of high-altitude flying animals, particularly bats. Conclusions We follow Davy and colleagues (2017) in their suggestion (a) to include aerial habitats for bats in national and international conservation policies. Furthermore, we add recommendations (b) to define the responsibilities for aerial bat habitat conservation and (c) to target bat conservation research to support the urgent need to better understand the three-dimensional habitat requirements of high-altitude foraging bats. Therefore, we strongly suggest the implementation of a three-dimensional perspective in international conventions dealing with bats. In defining habitat classification schemes, as was proposed by Davy and colleagues (2017), a subdivision of the troposphere into several zones may be a first step (figure 1). For bats, we propose zone 1 to reach from ground level to 50 m ASL, which may also include the forest canopy. Second, zone 2 would include the air column between 50 and 1000 m, because this is the activity range of most high-altitude flying bat species, such as Nyctalus and Taphozous species (see figure 1). In zone 3, which ranges from 1000 to 3500 m, very-high-flying bat species are observed. In general, our efforts in defining conservation strategies for high-altitude flying bats is hampered by our lack of detailed knowledge concerning how, when, where, and for what purpose bats use the aerosphere. Therefore, research should target the troposphere to better understand how to protect the organisms living within it, as well as how susceptible or resilient they are to, for example, sensory pollution of the aerial habitat. The recent miniaturization of GPS loggers and further attempts to make radar data publicly accessible are important steps toward accessing information about high-altitude flying bats. Forthcoming insights into the behavior of bats foraging at high altitudes promise to have far-reaching consequences for understanding the connectivity of habitats and the ecological value of our skies. Scaling in landscape planning can help to implement aerial conservation into common regulatory frameworks. On the local scale, it is important to apply conservation measures such as the curtailment algorithms for wind turbines previously discussed. To generalize such mitigation measures, they must be derived from conservation legislation of regional or national or even international scales. Defining guidelines and recognizing the cumulative effects of potential threats at a greater scale is urgently required for bat conservation in times when the sixth mass extinction event reaches into the skies. Acknowledgments CCV and MR were supported by a grant from the Deutsche Forschungsgemeinschaft (GRK-RTG 2118 Biomove). SEC was supported by a stipend from the Alexander von Humboldt Foundation. OL was supported by an Elsa Neumann doctoral stipend. Supplemental material Supplementary data are available at BIOSCI online. Christian C. Voigt, Shannon E. Currie, Marcus Fritze, Manuel Roeleke, and Oliver Lindecke are affiliated with the Department of Evolutionary Ecology at the Leibniz Institute for Zoo and Wildlife Research, in Berlin, Germany. References cited Arnett EB, Baerwald EF, Mathews F, Rodrigues L, Rodríguez-Durán A, Rydell J, Villegas-Patraca R, Voigt CC. 2016. Impacts of wind energy development on bats: A global perspective. 295– 323 in Voigt CC, Kingston T, eds. Bats in the Anthropocene: Conservation of Bats in a Changing World . Springer. Google Scholar CrossRef Search ADS   Baerwald EF, D’Amours GH, Klug BJ, Barclay RM. 2008. Barotrauma is a significant cause of bat fatalities at wind turbines. Current Biology  18: R695– R696. Google Scholar CrossRef Search ADS PubMed  Bat Conservation International. 2013. HD skies over Edwards Plateau. YouTube. (22 March 2018; www.youtube.com/watch?v=aET0a9fft84) Behr O, Brinkmann R, Korner-Nievergelt F, Nagy M, Niermann I, Reich M, Simon R. 2016. Reduktion des Kollisionsrisikos von Fledermäusen an Onshore-Windenergieanlagen (RENEBAT II). Umwelt und Raum 7. Institut für Umweltplanung. Biondi KM, Belant JL., DeVault TL, Martin JA, Wang G. 2013. Bat incidents with US civil aircraft. Acta Chiropterologica  15: 185– 192. Google Scholar CrossRef Search ADS   Black LL, Wiederhielm CA. 1976. Plasma oncotic pressures and hematocrit in the intact, unanesthetized bat. Microvascular Research  12: 55– 58. (22 March 2018; https://doi.org/10.1016/0026-2862(76)90006-6) Google Scholar CrossRef Search ADS PubMed  Boonman A, Bar-On Y, Cvikel N, Yovel Y. 2013. It's not black or white: On the range of vision and echolocation in echolocating bats. Frontiers in Physiology  4 (art. 248). Boyles JG, Cryan PM, McCracken GF, Kunz TH. 2011. Economic importance of bats in agriculture. Science  332: 41– 42. Google Scholar CrossRef Search ADS PubMed  Brinkmann R, Behr O, Niermann I, Reich M. 2011. Entwicklung von Methoden zur Untersuchung und Reduktion des Kollisionsrisikos von Fledermäusen an Onshore-Windenergieanlagen. Ergebnisse eines Forschungsvorhabens. Umwelt und Raum  4. Cuvillier. Canals M, Iriarte-Diaz J, Grossi B. 2011. Biomechanical, respiratory and cardiovascular adaptations of bats and the case of the small community of bats in Chile. Chapter 13 in Klika V, ed. Biomechanics in Applications. InTech . doi:10.5772/1424 Google Scholar CrossRef Search ADS   Chapman JW, Reynolds DR, Wilson K. 2015. Long-range seasonal migration in insects: Mechanisms, evolutionary drivers and ecological consequences. Ecology Letters  18: 287– 302. Google Scholar CrossRef Search ADS PubMed  Chilson PB, Frick WF, Kelly JF, Howard KW, Larkin RP, Diehl RH, Westbrook JK, Kelly TA, Kunz TH. 2012. Partly cloudy with a chance of migration: Weather, radars, and aeroecology. Bulletin of the American Meteorological Society  93: 669– 686. Google Scholar CrossRef Search ADS   Crawford RL, Baker WW. 1981. Bats killed at a north Florida television tower: A 25-year record. Journal of Mammalogy  62: 651– 652. Google Scholar CrossRef Search ADS   Cvikel N, Berg KE, Levin E, Hurme E, Borissov I, Boonman A, Amichai E, Yovel Y. 2015. Bats aggregate to improve prey search but might be impaired when their density becomes too high. Current Biology  25: 206– 211. Google Scholar CrossRef Search ADS PubMed  Davy CM, Ford AT, Fraser KC. 2017. Aeroconservation for the fragmented skies. Conservation Letters  10: 773– 780. doi:10.1111/conl.12347 Google Scholar CrossRef Search ADS   Dechmann DK, Heucke SL, Giuggioli L, Safi K, Voigt CC, Wikelski M. 2009. Experimental evidence for group hunting via eavesdropping in echolocating bats. Proceedings of the Royal Society B  276: 2721– 2728. Google Scholar CrossRef Search ADS PubMed  Diehl RH. 2013. The airspace is habitat. Trends in Ecology and Evolution  28: 37– 7379. Google Scholar CrossRef Search ADS   [EC] European Commission. 2010. Wind Energy Developments and Natura 2000 . Publications Office of the European Union. Engels S, Schneider N-L, Lefeldt N, Hein CM, Zapka M, Michalik A, Elbers D, Kittel A, Hore PJ, Mouritsen H. 2014. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature  509: 353– 356. Google Scholar CrossRef Search ADS PubMed  Fenton MB, Griffin DR. 1997. High-altitude pursuit of insects by echolocating bats. Journal of Mammalogy  78: 247– 250. Google Scholar CrossRef Search ADS   Frick WF, Stepanian PM, Kelly JF, Howard KW, Kuster CM, Kunz TH, Chilson PB. 2012. Climate and weather impact timing of emergence of bats. PLOS ONE  7 (art. e42737). Frick WF, Chilson PB, Fuller NW, Bridge ES, Kunz TH. 2013. Aeroecology. 149– 167 in Adams RA, Pedersen SC, eds. Bat Evolution, Ecology, and Conservation . Springer. Google Scholar CrossRef Search ADS   Frick WF et al.   2017. Fatalities at wind turbines may threaten population viability of a migratory bat. Biological Conservation  209: 172– 177. Google Scholar CrossRef Search ADS   Gillam EH. 2007. Eavesdropping by bats on the feeding buzzes of conspecifics. Canadian Journal of Zoology  85: 795– 801. Google Scholar CrossRef Search ADS   [GWEC] Global Wind Energy Council. 2016. Global Wind Report 2016: Annual Market Update . GWEC. Hallmann CA et al.   2017. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLOS ONE  12 (art. e0185809). Holland RA, Thorup K, Vonhof MJ, Cochran WW, Wikelski M. 2006. Navigation: Bat orientation using Earth's magnetic field. Nature  444: 702. Google Scholar CrossRef Search ADS PubMed  [IDA] International Dark Sky Association. 2017. (24 November 2017; www.darksky.org) [IEA] International Energy Agency, [OECD] Organisation for Economic Co-operation and Development. 2004. World Energy Outlook 2004 . IEA, OECD. Kellogg CA, Griffin DW. 2006. Aerobiology and the global transport of desert dust. Trends in Ecology and Evolution  21: 638– 644. Google Scholar CrossRef Search ADS PubMed  Kelly TC, Sleeman DP, Coughlan NE, Dillane E, O’Callaghan MJA. 2017. Bat collisions with civil aircraft in the Republic of Ireland over a decade suggest negligible impact on aviation safety. European Journal of Wildlife Research  63 (art. 23). Kunz TH et al.   2008. Aeroecology: Probing and modeling the aerosphere. Integrative and Comparative Biology  48: 1– 11. Google Scholar CrossRef Search ADS PubMed  Lambertucci SA, Shepard EL, Wilson RP. 2015. Human–wildlife conflicts in a crowded airspace. Science  348: 502– 504. Google Scholar CrossRef Search ADS PubMed  Lehnert LS, Kramer-Schadt S, Schönborn S, Lindecke O, Niermann I, Voigt CC. 2014. Wind farm facilities in Germany kill noctule bats from near and far. PLOS ONE  9 (art. e103106). Li Z, Courchamp F, Blumstein DT. 2016. Pigeons home faster through polluted air. Scientific Reports  6 (art. 18989). Luo J, Koselj K, Zsebők S, Siemers BM, Goerlitz HR. 2014. Global warming alters sound transmission: Differential impact on the prey detection ability of echolocating bats. Journal of the Royal Society Interface  11 (art. 20130961). Maher BA, Ahmed AM, Karloukovski V, MacLaren DA, Foulds PG, Allsop D, Mann DMA, Torres-Jardón R, Calderon-Garciduenas L. 2016. Magnetite pollution nanoparticles in the human brain. Proceedings of the National Academy of Sciences  113: 10797– 10801. Google Scholar CrossRef Search ADS   McCracken GF, Gillam EH, Westbrook JK, Lee YF, Jensen ML, Balsley BB. 2008. Brazilian free-tailed bats (Tadarida brasiliensis: Molossidae, Chiroptera) at high altitude: Links to migratory insect populations. Integrative and Comparative Biology  48: 107– 118. Google Scholar CrossRef Search ADS PubMed  McGuire LP, Guglielmo CG, Mackenzie SA, Taylor PD. 2012. Migratory stopover in the long-distance migrant silver-haired bat, Lasionycteris noctivagans. Journal of Animal Ecology  81: 377– 385. Google Scholar CrossRef Search ADS PubMed  Nicholls B, Racey PA. 2007. Bats avoid radar installations: Could electromagnetic fields deter bats from colliding with wind turbines? PLOS ONE  2 (art. e297). Parsons JG, Blair D, Luly J, Robson SK. 2008. Flying-fox (Megachiroptera: Pteropodidae) flight altitudes determined via an unusual sampling method: Aircraft strikes in Australia. Acta Chiropterologica  10: 377– 379. Google Scholar CrossRef Search ADS   Peurach SC. 2003. High-altitude collision between an airplane and a hoary bat, Lasiurus cinereus. Bat Research News  44: 2– 3. Peurach SC, Dove CJ, Stepko L. 2009. A decade of US Air Force bat strikes. Human–Wildlife Conflicts  3: 199– 207. Rehfuess E, Mehta S, Prüss-Üstün A. 2006. Assessing solid fuel use: Multiple implications for the Millennium Development Goals. Environmental Health Perspectives  114: A178. Google Scholar CrossRef Search ADS PubMed  Richter HV, Cumming GS. 2006. Food availability and annual migration of the straw-colored fruit bat (Eidolon helvum). Journal of Zoology  268: 35– 44. Google Scholar CrossRef Search ADS   Roeleke M, Blohm T, Kramer-Schadt S, Yovel Y, Voigt CC. 2016. Habitat use of bats in relation to wind turbines revealed by GPS tracking. Scientific Reports  6 (art. 28961). Roeleke M, Bumrungsri S, Voigt CC. 2017. Bats probe the aerosphere by landscape-guided altitudinal flights. Mammal Review  48: 7– 11. doi:10.1111/mam.12109 Google Scholar CrossRef Search ADS   Rohrig K. 2017. Windenergie Report 2016. Fraunhofer Institut für Windenergie und Energiesystemtechnik . Rowse EG, Lewanzik D, Stone EL, Harris S, Jones G. 2016. Dark matters: The effects of artificial lighting on bats. 187– 213 in Voigt CC, Kingston T, eds. Bats in the Anthropocene: Conservation of Bats in a Changing World . Springer. Google Scholar CrossRef Search ADS   Schnitzler HU, Kalko EK. 2001. Echolocation by insect-eating bats: We define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. BioScience  51: 557– 569. Google Scholar CrossRef Search ADS   Shamoun-Baranes J, Dokter AM, van Gesteren H, van Loon EE, Leijnse H, Bouten W. 2011. Birds flee en mass from New Year's Eve fireworks. Behavioral Ecology  22: 1173– 1177. Google Scholar CrossRef Search ADS PubMed  Siefer W, Kriner E. 1991. Soaring bats. Naturwissenschaften  78: 185. Google Scholar CrossRef Search ADS PubMed  Thomson SC, Brooke AP, Speakman JR. 2002. Soaring behaviour in the Samoan flying fox (Pteropus samoensis). Journal of Zoology  256: 55– 62. Google Scholar CrossRef Search ADS   Tian L, Lin W, Zhang S, Pan Y. 2010 Bat head contains soft magnetic particles: Evidence from magnetism. Bioelectromagnetics  31: 499– 503. Google Scholar CrossRef Search ADS PubMed  Tsoar A, Nathan R, Bartan Y, Vyssotski A, Dell’Omo G, Ulanovsky N. 2011. Large-scale navigational map in a mammal. Proceedings of the National Academy of Sciences  108: E718– E724. Google Scholar CrossRef Search ADS   Voigt CC, Holderied MW. 2012. High manoeuvring costs force narrow-winged molossid bats to forage in open space. Journal of Comparative Physiology B  182: 415– 424. Google Scholar CrossRef Search ADS   Voigt CC, Lehnert LS, Petersons G, Adorf F, Bach L. 2015. Wildlife and renewable energy: German politics cross migratory bats. European Journal of Wildlife Research  61: 213– 219. Google Scholar CrossRef Search ADS   Voigt CC, Lindecke O, Schönborn S, Kramer-Schadt S, Lehmann D. 2016. Habitat use of migratory bats killed during autumn at wind turbines. Ecological Applications  26: 771– 783. Google Scholar CrossRef Search ADS PubMed  Voigt CC, Roeleke M, Marggraf L, Petersons G, Voigt-Heucke SL. 2017. Migratory bats respond to artificial green light with positive phototaxis. PLOS ONE  12 (art. e0177748). Washburn BE, Cisar PJ, DeVault TL. 2014. Wildlife strikes with US military rotary-wing aircraft deployed in foreign countries. Human–Wildlife Interactions  8: 251– 260. Williams TC, Ireland LC, Williams JM. 1973. High altitude flights of the free-tailed bat, Tadarida brasiliensis, observed with radar. Journal of Mammalogy  54: 807– 821. Google Scholar CrossRef Search ADS   © The Author(s) 2018. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BioScience Oxford University Press

Conservation Strategies for Bats Flying at High Altitudes

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American Institute of Biological Sciences
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© The Author(s) 2018. Published by Oxford University Press on behalf of the American Institute of Biological Sciences.
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0006-3568
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1525-3244
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10.1093/biosci/biy040
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Abstract

Abstract Numerous bats use the troposphere for hunting, commuting, or migrating. High-altitude flying bats face various direct and indirect threats, including collision with tall anthropogenic structures and aerial vehicles, aerial fragmentation, reduced insect biomass, and the altered ambient conditions associated with climate change. Furthermore, dust and chemical pollutants in the troposphere might impair the health and survival of bats. Such indirect threats are diffuse regarding their origin and effect on bats, whereas direct threats are site and context specific. Overall, troposphere habitat conservation is hampered by the “Tragedy of the Commons” because its stewardship is in the hands of many. We conclude that high-altitude flying bats are likely to become more threatened in the near future because of the increased use of the troposphere by humans. Therefore, we should target the protection of the troposphere for organisms, such as high-altitude flying bats, that strongly depend on intact skies. Despite ever-growing knowledge about flying megabiota and drifting microbiota in the troposphere, researchers and managers have only recently recognized two important aspects associated with the lifestyle of airborne organisms. First, the lower boundaries of the troposphere represent valuable habitat for a variety of organisms (Diehl 2013). Second, the troposphere should be included in global conservation strategies (Lambertucci et al. 2015, Davy et al. 2017). Indeed, airborne species represent a substantial portion of global biodiversity (Kunz et al. 2008, Diehl 2013, Davy et al. 2017). Nonetheless, conservation needs related to the use of the aerosphere have been largely neglected. For example, the International Union for Conservation of Nature (IUCN) scheme recognizes only terrestrial and aquatic habitats but ignores aerial habitats (Davy et al. 2017). The reason for this negligence might lie in the fact that specific stewardship of the three-dimensional aerosphere is difficult to define. Because most areas of the troposphere are in public hands, mitigation of any human-induced perturbations in the aerosphere may be prone to the “Tragedy of the Commons,” similar to the diluted responsibilities documented for marine habitats in the fight against the overexploitation of fish populations. Moreover, conservation efforts are constrained by human perception bias and limited to our immediate geographical surroundings. Consequently, current policy and research programs ignore the major conservation gap for aerial species and their habitats (Davy et al. 2017). Conservation strategies that do exist for the troposphere have mainly targeted birds, but recent studies have highlighted the lower troposphere as important habitat for bats as well (Kunz et al. 2008, Frick et al. 2013, Davy et al. 2017), although the cryptic nature of bats and the limited accessibility of the troposphere for recording and documenting bat activities have severely hampered initial efforts. Bats have been active in the so-called open-space for millions of years, and many of the 1300 extant bat species ascend into the skies nightly to hunt prey. Morphology and echolocation frequency separate bat species that preferentially forage in cluttered habitats (i.e., forests) from those that exploit the open space (Schnitzler and Kalko 2001). For example, some families of Chiroptera, such as the Molossidae and Rhinopomatidae, are particularly well adapted to hunt in open space because they have long, slender wings and a high aspect ratio (Voigt and Holderied 2012). Open-space foraging bats play an important regulatory role as predators in natural ecosystems and anthropogenic habitats such as farmland and managed forests. The estimated value of the ecosystem services provided by bats is worth billions of dollars (box 1; McCracken et al. 2008, Boyles et al. 2011). Box 1. Ecosystem services provided by bats during high-altitude flights. View largeDownload slide View largeDownload slide High-altitude flying bats offer ecosystem services for agriculture and silviculture (Boyles et al. 2011,). For example, open-space bats are considered to play a key role in the regulation of pest insects, such as corn earworms in Northern America and planthoppers in Southeast Asia. Millions of these bats roost in single caves and therefore have to spread over vast areas during their foraging flights (Williams et al. 1973, Bat Conservation International 2013,). Several studies confirmed the foraging activity of bats via acoustic recording at high altitudes (Fenton and Griffin 1997,, McCracken et al. 2007). Recent advancements in GPS technology also allow fine-scale observations of flight behavior at high altitudes, showing rapidly undulating changes in the flight altitude of high-flying insect-feeding bats that may be used to scan the aerosphere in search of high-flying prey insects (Cvikel et al. 2015, Roeleke et al. 2017 ). In this article, we briefly summarize how bats use the troposphere and the threats they might face in this space, expanding significantly on what has already been established (Kunz et al. 2008). We outline some problems and possible solutions for the protection of bats in the lower boundaries of the troposphere. In the remainder of the text, we consider the troposphere as outlined by Davy and colleagues (2017): the basoaerial zone includes the air column between ground level to 1 kilometer above sea level (ASL), and the ­mesoaerial zone includes the adjunct air column between 1 and 8 kilometers ASL. The boundaries of these layers are dynamic and vary across landscapes, and bats may travel between both layers. For simplicity, we refer to these two layers as the aerosphere. We use the term high altitude to describe bat flight behavior that goes well beyond the landscape topography, including vegetation structure (forest canopy). How do bats exploit the aerosphere, and at what altitude? Bats are the only mammals capable of active flight and have specialized organs for efficient oxygen uptake and transport, allowing them to fly in different environments all over the world (Canals et al. 2011). High altitudes pose a number of constraints on aerodynamics: at high altitude (more than 5000 m ASL), oxygen partial pressure falls to less than 50% of that at sea level, and air density is lower. However, some open-space foragers fly at relatively high altitudes on a daily basis (Williams et al. 1973, Fenton and Griffin 1997, McCracken et al. 2008, Roeleke et al. 2017). Fast-flying molossid bats such as Tadarida brasiliensis or Tadarida aegyptiaca have some of the highest reported hematocrits and a slightly lower oxygen affinity than other species, potentially a specialization for flight at high altitude (Black and Wiederhielm 1976). Bats may occur in large numbers in the aerosphere; for example, T. brasiliensis emerge from Bracken Cave in Texas in the millions each night to hunt at high altitudes (Williams et al. 1973, Chilson et al. 2012). Radar scans from weather stations indicate that these bats can cover vast areas during their nightly search for insects (Chilson et al. 2012, Mirkovic et al. 2016). It is important to acknowledge that such mass phenomena may be widespread around the tropical belt. In the Old World, open-space foraging bats have been recorded at altitudes ranging from ground level to more than 800 m (figure 1; Cvikel et al. 2015). Migratory bats, such as the North American Lasiurus cinereus, have been documented at up to 3000 m (Peurach 2003). Studies propose that such high-altitude migration may be associated with insect migration (Chapman et al. 2015). Figure 1. View largeDownload slide The flight altitudes of bats inhabiting the aerosphere. (a) The altitudinal records of seven selected species: Tb, Tadarida brasiliensis (Williams et al. 1973); Lc, Lasiurus cinereus (Peurach 2003); Nn, Nyctalus noctula (Ahlén et al. 2007); Rm, Rhinopoma microphyllum (Cvikel et al. 2015); Tb, Taphozous theobaldi (Roeleke et al. 2017); Pp, Pteropus poliocephalus (Parsons et al. 2008). The silhouettes in the bars depict examples of the tallest buildings in the species distribution ranges (One World Trade Center, United States; CN Tower, Canada; Berlin TV Tower, Germany; Milad Tower, Iran; MahaNakhon, Thailand; and Eureka Tower, Australia). The basoaerial and mesoaerial zones are indicated with atmospheric pressure values (Davy et al. 2017). (b) An excerpt from a GPS track of T. theobaldi. Flight altitudes reach more than 800 m above ground. Density plots of flight altitude of three species can be found in the supplemental materials. Photograph credits: Tb, Lc, and Pp copyright by MerlinTuttle.org; Rm copyright by Christian Dietz. Figure 1. View largeDownload slide The flight altitudes of bats inhabiting the aerosphere. (a) The altitudinal records of seven selected species: Tb, Tadarida brasiliensis (Williams et al. 1973); Lc, Lasiurus cinereus (Peurach 2003); Nn, Nyctalus noctula (Ahlén et al. 2007); Rm, Rhinopoma microphyllum (Cvikel et al. 2015); Tb, Taphozous theobaldi (Roeleke et al. 2017); Pp, Pteropus poliocephalus (Parsons et al. 2008). The silhouettes in the bars depict examples of the tallest buildings in the species distribution ranges (One World Trade Center, United States; CN Tower, Canada; Berlin TV Tower, Germany; Milad Tower, Iran; MahaNakhon, Thailand; and Eureka Tower, Australia). The basoaerial and mesoaerial zones are indicated with atmospheric pressure values (Davy et al. 2017). (b) An excerpt from a GPS track of T. theobaldi. Flight altitudes reach more than 800 m above ground. Density plots of flight altitude of three species can be found in the supplemental materials. Photograph credits: Tb, Lc, and Pp copyright by MerlinTuttle.org; Rm copyright by Christian Dietz. Pteropodid bats, which depend on ground-based food resources (i.e., fruits or nectar), can also be found flying at high altitudes when commuting between feeding and roosting sites (Tsoar et al. 2011). For instance, some pteropodid individuals have been found at altitudes of more than 1500 m (Parsons et al. 2008). It is likely that many more species exploit the aerosphere, but our current knowledge is impeded by the technical constraints associated with the relatively small size of bats and the high costs of miniaturized global positioning system (GPS) or data loggers. Bats use high altitudes for a range of purposes, such as orientation, foraging, and migration, among others. For example, bats have been observed flying to high altitudes from a release site presumably for orientation before commuting to their colony (Tsoar et al. 2011). Observations of high-altitude flights include straight flights at high speed and complex aerial maneuvers likely associated with hunting and catching prey (Cvikel et al. 2015, Roeleke et al. 2016). Nevertheless, the primary goal of most high-altitude bats is to forage for insects (Fenton and Griffin 1997, Boyles et al. 2011). Acoustic recorders attached to helium-filled kite balloons provided the first evidence of hunting events at high altitudes (Griffin and Thompson 1982, Fenton and Griffin 1997). This observation was later confirmed by bats carrying GPS loggers with onboard ultrasonic microphones (Cvikel et al. 2015). Some species, such as Rhinopoma microphyllum and Taphozous theobaldi, seem to scan the three-dimensional airspace with undulating altitudinal flights ranging from a few meters’ to several hundred meters in altitude (Cvikel et al. 2014, Roeleke et al. 2017). During the ascent, these bats may benefit energetically by taking advantage of updrafts (i.e., soaring; Siefer and Kriner 1991, Thomson et al. 2002), and they may probe high-altitude winds to catch mass movements of insects (Siefer and Kriner 1991, Chapman et al. 2010). Typology of threats for open-space foraging bats in the aerosphere Bats face severe threats when flying in the aerosphere ­(figure 2). These threats can be separated into direct and indirect effects: causing immediate injuries and deaths (direct) or impaired health and long-term reduction in reproductive fitness (indirect). Figure 2. View largeDownload slide Threats to bats flying at high altitudes. The occurrence of obstacles at specific altitudes is depicted by the orange lines (logarithmic scale). Photographs (a)–(d) highlight selected indirect threats to bat health and navigation capacity. (a) Nightly sky glow and wind turbines in a coastal area of Europe. Photograph: copyright by Jasja Dekker. (b) Night lighting and sky glow in urban areas of Central America. Photograph: copyright by Fernando Tomás. (c) Haze formation after slash-and-burn forest clearing in the tropics seen from space, at a 380-kilometer altitude. Source: ISS029-E-8032 NASA’s Earth Observatory via Wikimedia Commons (public domain). (d) Industrial air pollution at sunset. Source: www.pixabay.com (public domain). Figure 2. View largeDownload slide Threats to bats flying at high altitudes. The occurrence of obstacles at specific altitudes is depicted by the orange lines (logarithmic scale). Photographs (a)–(d) highlight selected indirect threats to bat health and navigation capacity. (a) Nightly sky glow and wind turbines in a coastal area of Europe. Photograph: copyright by Jasja Dekker. (b) Night lighting and sky glow in urban areas of Central America. Photograph: copyright by Fernando Tomás. (c) Haze formation after slash-and-burn forest clearing in the tropics seen from space, at a 380-kilometer altitude. Source: ISS029-E-8032 NASA’s Earth Observatory via Wikimedia Commons (public domain). (d) Industrial air pollution at sunset. Source: www.pixabay.com (public domain). Wind turbines Many countries strive to move from conventional energy production to renewable sources in an effort to fight global climate change. Unfortunately, evidence suggests that there is a large-scale negative impact of wind energy production on many wildlife species, including bats (Voigt et al. 2015, Frick et al. 2017). Bat fatality records at wind turbines show that open-space foragers are the most critically affected bat group worldwide (Arnett et al. 2016). However, the number of bats killed at wind turbines annually is largely unknown because there seems to be variability across regions (Arnett et al. 2016). The cumulative installed capacity of wind turbines worldwide was estimated to be 490,000 megawatts in 2015 (GWEC 2016). For Central Europe, annual estimates of fatality rates suggest that approximately 10 bats die per 1 megawatt of energy produced if no mitigation scheme (e.g., cut-in speeds of wind turbines) is practiced (Brinkmann et al. 2011). With implemented mitigation schemes being the exception rather than the norm, global mass mortalities may number in the millions per year. Many open-space foraging bats are killed during their annual migrations (Lehnert et al. 2014, Voigt et al. 2016) and die either by blunt-force trauma from collisions or from barotrauma caused by contact with turbulent vortices in the tailwind of rotors (Baerwald et al. 2008). Recent modeling of air pressure changes indicates that vortices may drift for several hundred meters from wind turbines or even occur in front of turbines (Rohrig 2017). Therefore, the effective three-dimensional sphere that is dangerous for bats may be larger than the circular area swept by the rotor blades. The overall trend for increasing wind turbine size may intensify the threat for bats flying at the operational altitudes of turbines (between 30 and more than 200 m aboveground; Arnett et al. 2016). Aerial vehicles Currently, we lack quantitative data on how often bats are killed by airborne vehicles such as planes, helicopters, or drones. The US Air Force (USAF) has documented around 800 airstrikes within a 10-year period, most often with T. brasiliensis, costing the USAF upwards of US$825,000 in damage to aircraft (Peurach et al. 2009). In addition, collisions with Tadarida teniotis and R. microphyllum have damaged helicopters during military operations (Washburn et al. 2014). Biondi and colleagues (2013) listed 417 incidents with commercial aircraft in the United States between 1990 and 2010. In Australia, several hundred flying foxes (Pteropodidae) were documented in collisions with aircrafts at airports within a 10-year period (Parsons et al. 2008). In addition, a new threat is emerging in the form of unmanned aerial vehicles, which are an ever-increasing economic market. Wildlife strikes are filed only when an aerial vehicle is damaged, so many incidences may go undocumented, making it difficult to assess the total impact of airstrikes on bat populations overall. Aerial fatalities vary depending on the spatial distribution and abundance of high-altitude flying bats and those of aerial vehicles. In addition to the direct threats of collision, bats are sensitive to noise and artificial light, likely causing bats to abandon areas with heavy traffic by aerial vehicles, such as when planes are queuing for landing in the lower strata of the aerosphere in the vicinity of airports. Military and urban areas with high aerial traffic may thus act as barriers for bats, leading to fragmentation of the aerial habitat. We conclude that the potential conflict between open-space bats and aerial vehicles might therefore become ever stronger (Davy et al. 2017). Fragmentation of the aerial habitat Considering the seemingly endless skies, habitat fragmentation in the aerosphere may seem counterintuitive, but there is growing evidence that resources, such as high-flying insects, are not equally distributed across the sky. Indeed, Diehl (2013) pointed out that similar to terrestrial habitats, the troposphere might be highly fragmented as well. For example, some open-space foraging bats, such as Rhinopoma, hunt ephemeral insects with a patchy distribution (i.e., swarming or hilltopping winged ants; Siefer and Kriner 1991, Gillam 2007, Cvikel et al. 2015). The effort required to locate such patches in a three-dimensional space might explain the strong selection for group hunting in many open-space foraging bats (Dechmann et al. 2009). A reduction in insect biomass at the ground level may aggravate the availability and quality of patches of insects in the aerosphere, leading to higher search efforts and decreasing energy gain per distance traveled. This is particularly true for industrialized countries, where insect biomass is already decreasing and may become critical for open-space foraging bats in the future (e.g., Hallmann et al. 2017). In addition, the expansion of urban centers with tall buildings increases collision risk (Crawford and Baker 1981) and aerial fragmentation when bats are forced to take detours to reach foraging patches, probably resulting in increased energy expenditure. Global climate change Rising global temperatures may alter the transmission of sounds and thus the echolocation call efficiency of bats (Luo et al. 2014). For example, the maximum distance of echo-based detection of insects changes with increasing temperature. Most open-space foraging bats call at low frequencies and will benefit from such changes as prey-detection distances increasing. However, for temperate zone bats calling above 40 kHz, prey-detection distances will decrease with increasing temperature (Luo et al. 2014). Detection distances that have been altered by climate change may exacerbate the aforementioned fragmentation of skies in terms of insect resources. During flight, bats must dissipate high heat loads generated by flight muscles. Increased ambient temperature and decreased humidity at high altitudes may change the rate of heat dissipation and evaporative water loss of high-altitude flying bats. This may force bats to return to the ground to drink more frequently or avoid hot aerial layers when foraging. Temperatures decrease approximately 1 degree Celsius per 100 m of altitude, allowing high-altitude flying bats to balance their heat load; a warming climate may make the aerospace less tolerable for many species. The potential to move higher to combat warming body temperatures may prove difficult because air density decreases with altitude. Changing environmental conditions may affect the activity patterns and energy requirements of many open-space foragers. For example, climate change may alter the emergence patterns of bats (Frick et al. 2012). Furthermore, higher temperatures may lead to decreased torpor use throughout the year, forcing animals to forage more to balance their daily energetic requirements, thereby exposing foraging animals to direct threats. In addition, global climate change may change the phenology, intensity, and directions of large-scale insect migrations (Chapman et al. 2015), with yet-unforeseen consequences for bats as insect consumers. Dust and chemical pollutants Soil-derived particles forming dust are known to be carried at high altitudes over long distances as part of a natural process (Kellogg and Griffin 2006). At present, increasing particle emission rates from anthropogenic sources have added to the natural “fog of dust” in the aerosphere. For example, 2.4 billion humans depend on household fires with biomass fuels worldwide, particularly in developing countries of Africa and Asia (IEA and OECD 2004). Aside from producing massive amounts of greenhouse gases, household fires produce ash and dust particles that are released into the aerosphere, where they passively disperse unfiltered over large areas. Emissions from such household fires are known to be harmful to humans (Rehfuess et al. 2006), but the health consequences for wildlife have not yet been considered. Although global climate change may cause hotter and drier environments worldwide, it is likely that wind erosion and associated dust emissions from drylands may become an increasing problem in the future. In addition, increasing amounts of chemical pollutants in the aerosphere produced by industry and agriculture are therefore exposing open-space foraging bats to higher amounts of these particles—but with unknown health implications. Considering the highly specialized respiratory organs of bats, the high metabolic cost of powered flight in low air density, and the unknown impacts of these increasing pollutants on respiratory function, flight in this space may be severely hampered for many species. Recently, combustion-derived metal particles (magnetite crystals) were found to even migrate deep into the human brain, putatively causing cognitive impairment over time (Maher et al. 2016). Similar particles, although of likely natural origin, were detected in the brains of bats, particularly in high-altitude flying species, in which previous speculation considered these particles to be important for the magnetic sense (Tian et al. 2010). If the cost of flight increases because of the impaired navigation skills of bats, the total amount of time taken to migrate or commute long distances could also increase as the need for rest and replenishing fat reserves would also increase. This could introduce new problems for species that have rigid seasonal movement patterns. If individuals are less capable of reaching their desired location in time, new roost sites may be sought out in less favorable habitats. Sensory pollution Open-space bats heavily rely on visual orientation and navigation, whereas low-flying species’ three-dimensional visual range is restricted by habitat structure and landscape topography (Boonman et al. 2013). High-altitude flying bats gain wide panoramic views on the Earth's surface and firmament. However, with increased flight altitude, bats are exposed to more artificial light sources from more distant places. Consequently, they are more vulnerable to impairment of their vision through light pollution and are affected in their route choice depending on species-specific phototactic orientation (Voigt et al. 2017). Although artificial light may not present a physical obstacle, it may nonetheless reduce the connectivity between habitats when bats avoid large areas illuminated by artificial light at night (Rowse et al. 2016). Although the effects of light pollution have been widely studied at ground level, our understanding of the ramifications for high-altitude bats remains scant. However, it is probably safe to assume that direct light emission and sky glow may obscure large parts of the firmament, hampering orientation by celestial cues. Bats also respond in an aversive way to noise (Luo et al. 2014). Noise from anthropogenic sources spilling into the sky may therefore amplify the fragmentation of the aerosphere, such as when jet engines repeatedly create sonic booms in military areas. However, sound pollution most likely affects open-space bats only over short distances because of the strong atmospheric attenuation of sound. Another globally increasing but rarely studied sensory stressor for bats is fireworks, which are known to cause significant short-term disturbances (Shamoun-Baranes et al. 2013) or even injuries in birds. Dust particles and chemical pollutants could cause disorientation because smog and haze obscure vision, forcing bats to fly even higher or avoid affected areas. However, paradoxically, the enriched olfactory landscape of air-polluted areas could increase homing efficiency, an observation recently confirmed for pigeons (Li et al. 2016). Whether open-space bats are susceptible to such a sensory trap, offering facilitated olfactory navigation at the cost of impaired health, remains to be seen. Recent evidence suggests that magnetoreception is an important sensory modality for spatial orientation in many bats (Holland et al. 2006). Radar installations emitting electromagnetic fields (EMF), such as civil and military air traffic control and weather radar, have been shown to have aversive effects on the foraging movements of bats (Nicholls and Racey 2007). This is concerning because EMF are known to disrupt the magnetoreception-based orientation capability of nocturnal migratory birds (Engels et al. 2014) and probably also the orientation capability of migrating bats. It has also been argued that EMF aversion of bats could relate to an increased risk of overheating via thermal induction and/or interference with their auditory system (Nicholls and Racey 2007). Importantly, the sensory impacts on open-space bats are often multimodal because they co-occur in time and space. Conservation strategies for the protection of ­
high-altitude flying bats Since the discovery of the troposphere as a valuable habitat for many organisms, aeroconservation has been named the last frontier of conservation biology (Davy et al. 2017). It is a well-known fact that bats foraging at high altitudes cannot exist without their ground-based roosting structures. The conservation strategies to protect such roosts have already been the focus of much research; therefore, those key findings and management recommendations will not be summarized and discussed here. It is fundamental to all conservation efforts related to open-space foraging bats that daytime and night roosts are protected in order to ensure the survival of this guild in the future. Furthermore, negative anthropogenic effects may only be weakly connected with the place of origin (e.g., when bats affected by aerial dust are far from local areas of dust production by industries, individual household fires, or forest fires). Because anthropogenic effects are diluted in the three-dimensional space, it may be difficult to establish site- or context-specific conservation strategies, turning most efforts related to the protection of open-space foraging bats into rather generic approaches directed to the public. A well-known species conservation concept is to protect the network of habitats an animal population requires for survival and reproduction. For bats, previous conservation efforts focused almost exclusively on ground-based habitats that are relevant for foraging, mating, reproduction, and hibernation and the connection between these. Habitats in the aerosphere have not been widely represented in past conservation strategies unless it was clear that areas such as the space above forest canopies were used by foraging bats. A site-specific conservation approach for the protection of the aerosphere could identify those areas where open-space foraging bats are particularly active. Such areas should be protected against human development, traffic of aerial vehicles, construction of tall anthropogenic structures (including wind turbines), and even the occurrence of occasional fireworks. For example, free-tailed bats emerging from caves may total several million individuals, and the flight paths leading to their high-altitude habitats can be easily identified using radar scans (Chilson et al. 2012). Such emergence areas and flight corridors should be protected against any of the aforementioned anthropogenic impacts in order to conserve these bats. Furthermore, some landscape features cause migratory bats to accumulate at specific locations, such as before crossing large water bodies; when moving along a shoreline or a river valley to their destinations (McGuire et al. 2012); or when aggregating at feeding sites, such as Eidolon helvum in the Kasanka National Park (Richter and Cumming 2006). However, by and large, the available data are deficient regarding the specific landscape features that bats use for migration. For example, mountain ridges or hilltops may be used by open-space foraging bats to launch into the night skies (Roeleke et al. 2017). We therefore call for the identification of landscape features with high activities of open-space foraging bats in order to create protection zones where the aerosphere is protected, but not necessarily the ground—that is, we call for the creation of aeroparks. These aeroparks would likely also benefit a suite of species beyond open-space bats. Frameworks from the implementation of prohibited airspace for aviation could be used as a starting point. Consequently, any anthropogenic stressor potentially emitted in the night sky from within a reasonable buffer zone adjacent to aeroparks would need to be identified. International planning of such aeroparks could allow the creation of a network of such protected spaces, following the network approaches that are already well established for protected areas on the ground level. A conservation physiology approach for high-altitude flying bats could identify anthropogenic pollutants emitted toward potential conservation space and whether these are continuously affecting the sites under consideration. In terms of artificial light pollution, for example, mapping efforts (e.g., www.lightpollutionmap.info) could provide a basis for identifying potential target sites and conflict areas. Dark Sky Reserves are one step in this direction by defining areas with special regulation of artificial light at night in order to reduce light pollution (IDA 2017). Worldwide, around 50 of these reserves have been classified by the IUCN. These areas primarily focus on the protection of dark and therefore starry skies rather than targeting biological conservation. Of course, nocturnal animals, such as bats, automatically benefit from dark-sky reserves; however, this type of conservation area is still not designed for the specific purpose of species conservation. Almost all international conservation initiatives and conventions do not consider high-altitude flying animals. UN Environment Programme conventions such as Ramsar (representing here the conservation of important wetland areas for migratory species) and the Convention on the Conservation of Migratory Species of Wild Animals (CMS) are important conservation tools to protect migratory species and their habitats. However, all of these schemes ignore the aerosphere. This can result in paradoxical situations, such as when European wind energy projects are approved in areas that are protected by the European Habitat Directive (EC 2010). Bearing in mind that energy production from wind represents the main source of renewable energy in Europe (EC 2010) and that 21 of 53 European bat species are known to be active at high altitudes, it is concerning that no concepts for aerial conservation areas have been considered at this stage. In the future, bat-friendly wind energy projects should account for high-altitude fliers and apply mitigation schemes based on conditions in which fatalities typically increase, such as during migration, in relatively mild ambient temperatures, at low wind speed, and in no rainfall (Behr et al. 2016). In summary, there is a clear deficiency in the legislation with respect to the protection of high-altitude flying animals, particularly bats. Conclusions We follow Davy and colleagues (2017) in their suggestion (a) to include aerial habitats for bats in national and international conservation policies. Furthermore, we add recommendations (b) to define the responsibilities for aerial bat habitat conservation and (c) to target bat conservation research to support the urgent need to better understand the three-dimensional habitat requirements of high-altitude foraging bats. Therefore, we strongly suggest the implementation of a three-dimensional perspective in international conventions dealing with bats. In defining habitat classification schemes, as was proposed by Davy and colleagues (2017), a subdivision of the troposphere into several zones may be a first step (figure 1). For bats, we propose zone 1 to reach from ground level to 50 m ASL, which may also include the forest canopy. Second, zone 2 would include the air column between 50 and 1000 m, because this is the activity range of most high-altitude flying bat species, such as Nyctalus and Taphozous species (see figure 1). In zone 3, which ranges from 1000 to 3500 m, very-high-flying bat species are observed. In general, our efforts in defining conservation strategies for high-altitude flying bats is hampered by our lack of detailed knowledge concerning how, when, where, and for what purpose bats use the aerosphere. Therefore, research should target the troposphere to better understand how to protect the organisms living within it, as well as how susceptible or resilient they are to, for example, sensory pollution of the aerial habitat. The recent miniaturization of GPS loggers and further attempts to make radar data publicly accessible are important steps toward accessing information about high-altitude flying bats. Forthcoming insights into the behavior of bats foraging at high altitudes promise to have far-reaching consequences for understanding the connectivity of habitats and the ecological value of our skies. Scaling in landscape planning can help to implement aerial conservation into common regulatory frameworks. On the local scale, it is important to apply conservation measures such as the curtailment algorithms for wind turbines previously discussed. To generalize such mitigation measures, they must be derived from conservation legislation of regional or national or even international scales. Defining guidelines and recognizing the cumulative effects of potential threats at a greater scale is urgently required for bat conservation in times when the sixth mass extinction event reaches into the skies. Acknowledgments CCV and MR were supported by a grant from the Deutsche Forschungsgemeinschaft (GRK-RTG 2118 Biomove). SEC was supported by a stipend from the Alexander von Humboldt Foundation. OL was supported by an Elsa Neumann doctoral stipend. Supplemental material Supplementary data are available at BIOSCI online. Christian C. Voigt, Shannon E. Currie, Marcus Fritze, Manuel Roeleke, and Oliver Lindecke are affiliated with the Department of Evolutionary Ecology at the Leibniz Institute for Zoo and Wildlife Research, in Berlin, Germany. References cited Arnett EB, Baerwald EF, Mathews F, Rodrigues L, Rodríguez-Durán A, Rydell J, Villegas-Patraca R, Voigt CC. 2016. Impacts of wind energy development on bats: A global perspective. 295– 323 in Voigt CC, Kingston T, eds. Bats in the Anthropocene: Conservation of Bats in a Changing World . Springer. Google Scholar CrossRef Search ADS   Baerwald EF, D’Amours GH, Klug BJ, Barclay RM. 2008. Barotrauma is a significant cause of bat fatalities at wind turbines. Current Biology  18: R695– R696. Google Scholar CrossRef Search ADS PubMed  Bat Conservation International. 2013. HD skies over Edwards Plateau. YouTube. (22 March 2018; www.youtube.com/watch?v=aET0a9fft84) Behr O, Brinkmann R, Korner-Nievergelt F, Nagy M, Niermann I, Reich M, Simon R. 2016. Reduktion des Kollisionsrisikos von Fledermäusen an Onshore-Windenergieanlagen (RENEBAT II). Umwelt und Raum 7. Institut für Umweltplanung. Biondi KM, Belant JL., DeVault TL, Martin JA, Wang G. 2013. Bat incidents with US civil aircraft. Acta Chiropterologica  15: 185– 192. Google Scholar CrossRef Search ADS   Black LL, Wiederhielm CA. 1976. Plasma oncotic pressures and hematocrit in the intact, unanesthetized bat. Microvascular Research  12: 55– 58. (22 March 2018; https://doi.org/10.1016/0026-2862(76)90006-6) Google Scholar CrossRef Search ADS PubMed  Boonman A, Bar-On Y, Cvikel N, Yovel Y. 2013. It's not black or white: On the range of vision and echolocation in echolocating bats. Frontiers in Physiology  4 (art. 248). Boyles JG, Cryan PM, McCracken GF, Kunz TH. 2011. Economic importance of bats in agriculture. Science  332: 41– 42. Google Scholar CrossRef Search ADS PubMed  Brinkmann R, Behr O, Niermann I, Reich M. 2011. Entwicklung von Methoden zur Untersuchung und Reduktion des Kollisionsrisikos von Fledermäusen an Onshore-Windenergieanlagen. Ergebnisse eines Forschungsvorhabens. Umwelt und Raum  4. Cuvillier. Canals M, Iriarte-Diaz J, Grossi B. 2011. Biomechanical, respiratory and cardiovascular adaptations of bats and the case of the small community of bats in Chile. Chapter 13 in Klika V, ed. Biomechanics in Applications. InTech . doi:10.5772/1424 Google Scholar CrossRef Search ADS   Chapman JW, Reynolds DR, Wilson K. 2015. Long-range seasonal migration in insects: Mechanisms, evolutionary drivers and ecological consequences. Ecology Letters  18: 287– 302. Google Scholar CrossRef Search ADS PubMed  Chilson PB, Frick WF, Kelly JF, Howard KW, Larkin RP, Diehl RH, Westbrook JK, Kelly TA, Kunz TH. 2012. Partly cloudy with a chance of migration: Weather, radars, and aeroecology. Bulletin of the American Meteorological Society  93: 669– 686. Google Scholar CrossRef Search ADS   Crawford RL, Baker WW. 1981. Bats killed at a north Florida television tower: A 25-year record. Journal of Mammalogy  62: 651– 652. Google Scholar CrossRef Search ADS   Cvikel N, Berg KE, Levin E, Hurme E, Borissov I, Boonman A, Amichai E, Yovel Y. 2015. Bats aggregate to improve prey search but might be impaired when their density becomes too high. Current Biology  25: 206– 211. Google Scholar CrossRef Search ADS PubMed  Davy CM, Ford AT, Fraser KC. 2017. Aeroconservation for the fragmented skies. Conservation Letters  10: 773– 780. doi:10.1111/conl.12347 Google Scholar CrossRef Search ADS   Dechmann DK, Heucke SL, Giuggioli L, Safi K, Voigt CC, Wikelski M. 2009. Experimental evidence for group hunting via eavesdropping in echolocating bats. Proceedings of the Royal Society B  276: 2721– 2728. Google Scholar CrossRef Search ADS PubMed  Diehl RH. 2013. The airspace is habitat. Trends in Ecology and Evolution  28: 37– 7379. Google Scholar CrossRef Search ADS   [EC] European Commission. 2010. Wind Energy Developments and Natura 2000 . Publications Office of the European Union. Engels S, Schneider N-L, Lefeldt N, Hein CM, Zapka M, Michalik A, Elbers D, Kittel A, Hore PJ, Mouritsen H. 2014. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature  509: 353– 356. Google Scholar CrossRef Search ADS PubMed  Fenton MB, Griffin DR. 1997. High-altitude pursuit of insects by echolocating bats. Journal of Mammalogy  78: 247– 250. Google Scholar CrossRef Search ADS   Frick WF, Stepanian PM, Kelly JF, Howard KW, Kuster CM, Kunz TH, Chilson PB. 2012. Climate and weather impact timing of emergence of bats. PLOS ONE  7 (art. e42737). Frick WF, Chilson PB, Fuller NW, Bridge ES, Kunz TH. 2013. Aeroecology. 149– 167 in Adams RA, Pedersen SC, eds. Bat Evolution, Ecology, and Conservation . Springer. Google Scholar CrossRef Search ADS   Frick WF et al.   2017. Fatalities at wind turbines may threaten population viability of a migratory bat. Biological Conservation  209: 172– 177. Google Scholar CrossRef Search ADS   Gillam EH. 2007. Eavesdropping by bats on the feeding buzzes of conspecifics. Canadian Journal of Zoology  85: 795– 801. Google Scholar CrossRef Search ADS   [GWEC] Global Wind Energy Council. 2016. Global Wind Report 2016: Annual Market Update . GWEC. Hallmann CA et al.   2017. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLOS ONE  12 (art. e0185809). Holland RA, Thorup K, Vonhof MJ, Cochran WW, Wikelski M. 2006. Navigation: Bat orientation using Earth's magnetic field. Nature  444: 702. Google Scholar CrossRef Search ADS PubMed  [IDA] International Dark Sky Association. 2017. (24 November 2017; www.darksky.org) [IEA] International Energy Agency, [OECD] Organisation for Economic Co-operation and Development. 2004. World Energy Outlook 2004 . IEA, OECD. Kellogg CA, Griffin DW. 2006. Aerobiology and the global transport of desert dust. Trends in Ecology and Evolution  21: 638– 644. Google Scholar CrossRef Search ADS PubMed  Kelly TC, Sleeman DP, Coughlan NE, Dillane E, O’Callaghan MJA. 2017. Bat collisions with civil aircraft in the Republic of Ireland over a decade suggest negligible impact on aviation safety. European Journal of Wildlife Research  63 (art. 23). Kunz TH et al.   2008. Aeroecology: Probing and modeling the aerosphere. Integrative and Comparative Biology  48: 1– 11. Google Scholar CrossRef Search ADS PubMed  Lambertucci SA, Shepard EL, Wilson RP. 2015. Human–wildlife conflicts in a crowded airspace. Science  348: 502– 504. Google Scholar CrossRef Search ADS PubMed  Lehnert LS, Kramer-Schadt S, Schönborn S, Lindecke O, Niermann I, Voigt CC. 2014. Wind farm facilities in Germany kill noctule bats from near and far. PLOS ONE  9 (art. e103106). Li Z, Courchamp F, Blumstein DT. 2016. Pigeons home faster through polluted air. Scientific Reports  6 (art. 18989). Luo J, Koselj K, Zsebők S, Siemers BM, Goerlitz HR. 2014. Global warming alters sound transmission: Differential impact on the prey detection ability of echolocating bats. Journal of the Royal Society Interface  11 (art. 20130961). Maher BA, Ahmed AM, Karloukovski V, MacLaren DA, Foulds PG, Allsop D, Mann DMA, Torres-Jardón R, Calderon-Garciduenas L. 2016. Magnetite pollution nanoparticles in the human brain. Proceedings of the National Academy of Sciences  113: 10797– 10801. Google Scholar CrossRef Search ADS   McCracken GF, Gillam EH, Westbrook JK, Lee YF, Jensen ML, Balsley BB. 2008. Brazilian free-tailed bats (Tadarida brasiliensis: Molossidae, Chiroptera) at high altitude: Links to migratory insect populations. Integrative and Comparative Biology  48: 107– 118. Google Scholar CrossRef Search ADS PubMed  McGuire LP, Guglielmo CG, Mackenzie SA, Taylor PD. 2012. Migratory stopover in the long-distance migrant silver-haired bat, Lasionycteris noctivagans. Journal of Animal Ecology  81: 377– 385. Google Scholar CrossRef Search ADS PubMed  Nicholls B, Racey PA. 2007. Bats avoid radar installations: Could electromagnetic fields deter bats from colliding with wind turbines? PLOS ONE  2 (art. e297). Parsons JG, Blair D, Luly J, Robson SK. 2008. Flying-fox (Megachiroptera: Pteropodidae) flight altitudes determined via an unusual sampling method: Aircraft strikes in Australia. Acta Chiropterologica  10: 377– 379. Google Scholar CrossRef Search ADS   Peurach SC. 2003. High-altitude collision between an airplane and a hoary bat, Lasiurus cinereus. Bat Research News  44: 2– 3. Peurach SC, Dove CJ, Stepko L. 2009. A decade of US Air Force bat strikes. Human–Wildlife Conflicts  3: 199– 207. Rehfuess E, Mehta S, Prüss-Üstün A. 2006. Assessing solid fuel use: Multiple implications for the Millennium Development Goals. Environmental Health Perspectives  114: A178. Google Scholar CrossRef Search ADS PubMed  Richter HV, Cumming GS. 2006. Food availability and annual migration of the straw-colored fruit bat (Eidolon helvum). Journal of Zoology  268: 35– 44. Google Scholar CrossRef Search ADS   Roeleke M, Blohm T, Kramer-Schadt S, Yovel Y, Voigt CC. 2016. Habitat use of bats in relation to wind turbines revealed by GPS tracking. Scientific Reports  6 (art. 28961). Roeleke M, Bumrungsri S, Voigt CC. 2017. Bats probe the aerosphere by landscape-guided altitudinal flights. Mammal Review  48: 7– 11. doi:10.1111/mam.12109 Google Scholar CrossRef Search ADS   Rohrig K. 2017. Windenergie Report 2016. Fraunhofer Institut für Windenergie und Energiesystemtechnik . Rowse EG, Lewanzik D, Stone EL, Harris S, Jones G. 2016. Dark matters: The effects of artificial lighting on bats. 187– 213 in Voigt CC, Kingston T, eds. Bats in the Anthropocene: Conservation of Bats in a Changing World . Springer. Google Scholar CrossRef Search ADS   Schnitzler HU, Kalko EK. 2001. Echolocation by insect-eating bats: We define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. BioScience  51: 557– 569. Google Scholar CrossRef Search ADS   Shamoun-Baranes J, Dokter AM, van Gesteren H, van Loon EE, Leijnse H, Bouten W. 2011. Birds flee en mass from New Year's Eve fireworks. Behavioral Ecology  22: 1173– 1177. Google Scholar CrossRef Search ADS PubMed  Siefer W, Kriner E. 1991. Soaring bats. Naturwissenschaften  78: 185. Google Scholar CrossRef Search ADS PubMed  Thomson SC, Brooke AP, Speakman JR. 2002. Soaring behaviour in the Samoan flying fox (Pteropus samoensis). Journal of Zoology  256: 55– 62. Google Scholar CrossRef Search ADS   Tian L, Lin W, Zhang S, Pan Y. 2010 Bat head contains soft magnetic particles: Evidence from magnetism. Bioelectromagnetics  31: 499– 503. Google Scholar CrossRef Search ADS PubMed  Tsoar A, Nathan R, Bartan Y, Vyssotski A, Dell’Omo G, Ulanovsky N. 2011. Large-scale navigational map in a mammal. Proceedings of the National Academy of Sciences  108: E718– E724. Google Scholar CrossRef Search ADS   Voigt CC, Holderied MW. 2012. High manoeuvring costs force narrow-winged molossid bats to forage in open space. Journal of Comparative Physiology B  182: 415– 424. Google Scholar CrossRef Search ADS   Voigt CC, Lehnert LS, Petersons G, Adorf F, Bach L. 2015. Wildlife and renewable energy: German politics cross migratory bats. European Journal of Wildlife Research  61: 213– 219. Google Scholar CrossRef Search ADS   Voigt CC, Lindecke O, Schönborn S, Kramer-Schadt S, Lehmann D. 2016. Habitat use of migratory bats killed during autumn at wind turbines. Ecological Applications  26: 771– 783. Google Scholar CrossRef Search ADS PubMed  Voigt CC, Roeleke M, Marggraf L, Petersons G, Voigt-Heucke SL. 2017. Migratory bats respond to artificial green light with positive phototaxis. PLOS ONE  12 (art. e0177748). Washburn BE, Cisar PJ, DeVault TL. 2014. Wildlife strikes with US military rotary-wing aircraft deployed in foreign countries. Human–Wildlife Interactions  8: 251– 260. Williams TC, Ireland LC, Williams JM. 1973. High altitude flights of the free-tailed bat, Tadarida brasiliensis, observed with radar. Journal of Mammalogy  54: 807– 821. Google Scholar CrossRef Search ADS   © The Author(s) 2018. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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BioScienceOxford University Press

Published: May 17, 2018

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