- Email: [email protected]
Rapid descent flight by a molossid bat (Chaerephon plicatus) returning to its cave
Mammalian Biology 95 (2019) 15–17
Contents lists available at ScienceDirect
Mammalian Biology journal homepage: www.elsevier.com/locate/mambio
Short communication
Rapid descent flight by a molossid bat (Chaerephon plicatus) returning to its cave Christian C. Voigt a,b,∗ , Sara Bumrungsri c , Manuel Roeleke a,b a b c
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke- Str. 17, 10315, Berlin, Germany Institute for Biology, Freie Universität Berlin, Takustr. 6, 14195, Berlin, Germany Department of Biology, Prince of Songkla University, Hat Yai, Thailand
a r t i c l e
i n f o
Article history: Received 18 November 2018 Accepted 2 January 2019 Available online 3 January 2019 Handled by Danilo Russo Keywords: Aerodynamics Anti-predator strategy Escape behavior Landscape of fear
a b s t r a c t In Southeast Asia, wrinkle-lipped bats (Chaerephon plicatus) roost in colonies that may count several million individuals. Birds of prey frequently hunt these bats when they emerge from or return to their colonies. Here, we report on an extreme anti-predator behavior of this species during return flights at dawn. Based on data logger, we documented that bats may ascend to several hundred meters altitude above the cave shortly before diving at high speed (maximum 20 m/s) towards the entrance. Dive rates were 40 times higher than those reported for other open-space foraging bats performing flapping descending flights. Based on high speed video recordings, we show that C. plicatus brake the rapid descents close to the cave entrance using the tail wing membrane and partly extended wings. Maximum gravitational forces involved 2.4 G, probably when adjusting abruptly the speed close to ground. We argue that these descending maneuvers may constitute an anti-predator strategy of C. plicatus, since such descents may be too fast and complex for birds of prey at the cave entrance, particularly when performed by thousands of individuals at the same time. ¨ Saugetierkunde. ¨ © 2019 Published by Elsevier GmbH on behalf of Deutsche Gesellschaft fur
Bats are the only mammals capable of powered flight and, in comparison to birds, they are considered to be limited in their ability to glide and to reach high speeds (Hedenström et al., 2009; Voigt et al., 2017). Here, we report on rapid descending flights of wrinklelipped free-tailed bats, Chaerephon plicatus (family Molossidae) that challenge our current understanding of flight performance in Chiroptera. Chaerephon plicatus belongs to a guild of aerial insectivores that hunt at night at high altitude and that spend the daytime in large caves counting several million individuals (McCracken et al., 2008; Voigt et al., 2018). Due to the high-altitude flights of members of this guild, we have little information about their foraging or flight behavior. Most open-space foraging bats have long and slender wings (high aspect ratio) which enable them to reach high flight speeds (McCracken et al., 2016). Other open-space foraging bats exhibit stereotypic patterns of ascending and descending flights, possibly to monitor the availability of insects at various air layers (Cvikel et al., 2015; Roeleke et al., 2018a,b).
∗ Corresponding author at: Leibniz Institute for Zoo and Wildlife Research, AlfredKowalke- Str. 17, 10315, Berlin, Germany. E-mail address: [email protected] (C.C. Voigt).
To shed light on the behavior of high-altitude foraging bats, we studied flight patterns of C. plicatus in Thailand; a bat of about 18–20 g body mass that specializes on plant hoppers (Hemiptera), a pest insect that potentially damages the rice harvests in Asian countries (Leelapaibul et al., 2005). In January 2018, we captured 20 C. plicatus emerging from a colony with about 200,000 individuals. We equipped each of the 20 captured bats with a data logger (GiPsy-5 data logger; TechnoSmartEurope, Rome, Italy) that recorded ambient temperature, barometric pressure, and tri-axial acceleration at 1 Hz by gluing the loggers temporarily to the dorsal fur with skin glue (Sauer Hautkleber, Lobbach, Germany). VHF transmitters (Telemetrie-Dessau, Germany) were added to facilitate the retrieval of loggers that fell off the bats after a few days. Retrieval of tags was mandatory since data stored by the logger had to be downloaded via cable connected to a computer. Tags weighed about 15% of the bats’ body mass. Since we and others did not experience any problems with tags of similar relative mass in other open-space foraging bats (Cvikel et al., 2015; Roeleke et al., 2016, 2018a,b; Egert-Berg et al., 2018), we did not expect that tag mass would interfere with the health or flight ability of C. plicatus. Within one week of tag attachment, we located VHF signals from 11 bats in the cave, yet tags were still attached to the bats and
https://doi.org/10.1016/j.mambio.2019.01.001 ¨ Saugetierkunde. ¨ 1616-5047/© 2019 Published by Elsevier GmbH on behalf of Deutsche Gesellschaft fur
16
C.C. Voigt et al. / Mammalian Biology 95 (2019) 15–17
Fig. 1. Flight altitude (A), horizontal (ventral-dorsal) acceleration relative to horizontal resting position (B), and climb rate (C). The horizontal line in panel (A) depicts the altitude of the resting place within the cave.
roosting sites were beyond reach. We assume that the other nine loggers had fallen off of the bats during foraging flights, or that bats switched to neighboring colonies beyond the detection range of our VHF receiver. After five days, we found a single logger on farmland near the cave; all other tags could not be retrieved. We assume that the temporarily attached tags fell of bats when bats foraged at some distance to the cave. Converting data of barometric pressure and ambient temperature of the focal bat into altitude above sea level (asl; hypsometric formula) indeed confirmed that the carrier of the logger flew at high altitudes. Recorded data of one 24 h period showed that the flight altitude of this bat peaked at 785 m asl when the bat returned to its cave. Considering the topography of the study site, this equates to a flight altitude of about 500–600 m above ground. The focal bat lost its tag shortly after its second emergence from the cave, thus we lack data on a second return flight. The observed flight altitude of C. plicatus is similar to that of a syntopic openspace foraging bat, Taphozous theobaldi, which we tracked in a previous study at the same cave using loggers with geographical position system (Roeleke et al., 2018a). In the following text, we will focus on the return flight of this individual C. plicatus (starting at 0539 h). Towards the end of the night, the focal bat performed flight maneuvers with relatively high acceleration rates (Fig. 1). On the zaxis (ventral-dorsal), this bat experienced a maximal gravitational force of 4.9 G, but usually gravitational forces ranged for the z-axis between −0.8 and 2.4 G (97.5% quantiles for diving and braking, respectively, Fig. 1). We assume that the relatively high G values on the z-axis may have originated from decelerating movements of bats when descending. On the x-axis (head-tail), we recorded a maximum absolute value of 0.6 G (97.5% quantile) and on the y-axis (left-right) up to 0.8 G. Starting at 0625 h, the focal bat performed a last ascent of about 10 min duration to a maximum altitude of 785 m asl before it descended about 500 m to the cave located at 270 m asl which the bat entered at 0639 h. During the descending flight the bat sank at a rate of up to 20 m/s and gravitational forces equaled up to 2.4 G, probably when adjusting the dive speed, particularly when approaching the cave entrance (Fig. 1, video 1 and 2 in ESM). The maximum recorded descending rates were 40 times higher than those reported before for another open-space foraging bat (Roeleke et al., 2018a), yet the values fell into the lower range of those reported for passerine birds of similar size when descending during migration to a stopover site (Hedenström and Liechti, 2001).
However, it is important to note that we are unaware of the angle of the flight path in relation to the horizontal, i.e. the actual flight speed of the descending bat could be higher than the assumed vertical descending rate. High speed video recordings at the entrance of a nearby cave confirmed that C. plicatus returns at high speed towards the cave entrance (video 1 and 2 in ESM). Descending flights seem to be regularly interrupted by deceleration maneuvers using the tail wing membrane and the partly extended wings. This could increase profile drag and alter the angle of attack, which might slow down the fall of the bat. Our video observations suggest that C. plicatus mostly glide during the descents without flapping their wings. We speculate that the mechanical stress imposed on the wing membrane and bones may be extreme, considering the small morphological structures, such as the delicate wing bones, involved and the speed at which the bat descended. In consequence, mechanical properties of wings of these open-space foraging bats may not only be adapted towards fast foraging flights, but also to rapid descending flights at the utmost speed possible. We offer two not mutually exclusive explanations for the rapid return flight of the tagged bat to the cave. First, similar to other open-space foraging bats (Cvikel et al., 2015; Roeleke et al., 2018a), C. plicatus is hunting insects at high altitudes and also shortly before returning to their roosts. Yet, considering that the focal bat stayed only for a few minutes at high altitudes, we find it unlikely that the bat hunted insects at around 500 m above ground. Second, individuals from large colonies may be vulnerable to predators, such as hawks and owls (Mikula et al., 2016), and C. plicatus may perform rapid descents as an anti-predatory strategy (see raptor in video 2 of ESM). Predators such as birds of prey may find it difficult to attack bats that descend at these high speeds, particularly when thousands of bats descend almost simultaneously into the cave (video 1 and 2 of ESM). Presumably, C. plicatus may fly to high altitudes to from groups as a defense strategy (Chaverri et al., 2018) and for converting potential energy into kinetic energy in order to reach high descent speeds, beyond its power by flapping flight. We speculate that rapid descending flights may have evolved in bats as an anti-predator strategy when approaching potentially predator rich places like cave entrances. This is the first empirical data on a bat diving at high speed from several hundred meter altitude to its roost, showing that wing morphology and aerodynamics of bats
C.C. Voigt et al. / Mammalian Biology 95 (2019) 15–17
may not only be adapted towards powered flight, but also to rapid gliding descents without large involvement of active wing flapping. Competing interest statement The authors declare no competing interest. Funding sources This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. This work was supported by Deutsche Forschungsgemeinschaft in the framework of the BioMove Training Group (DFG-GRK 2118/1). Acknowledgements We thank that the authorities for granting us permit to conduct the experiment: permit #0002/4508 granted by the National Research Council of Thailand (NRCT) and permit #108/59 granted by the Department of National Park, Wildlife and Plant Conservation (DNP). We thank Nittaya Ruadreo and Supawan Srilopan for help in the field and Shannon Currie for commenting on the manuscript. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.mambio.2019. 01.001.
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References Chaverri, G., Ancillotto, L., Russo, D., 2018. Social communication in bats. Biol. Rev. 93, 1983-1954. Cvikel, N., Berg, K.E., 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. Curr. Biol. 25, 206–211. Egert-Berg, K., Hurme, E.R., Greif, S., Goldstein, A., Harten, L., Herrera, M.L.G., Flores-Martinez, J.J., Vales, A.T., Johnston, D.S., Eitan, O., Borissov, I., Shipley, J.R., Medellin, R.A., Wilkinson, G.S., Goerlitz, H.R., Yovel, Y., 2018. Resource ephemerality drives social foraging in bats. Curr. Biol. 28, 3667–3673. Hedenström, A., Liechti, F., 2001. Field estimates of body drag coefficient on the basis of dives in passerine birds. J. Exp. Biol. 204, 1167–1175. Hedenström, A., Johansson, L.C., Spedding, G.R., 2009. Bird or bat: comparing airframe design and flight performance. Bioinspired Biomim. Nanobiomater. 4, 015001. Leelapaibul, W., Bumrungsri, S., Pattanawiboon, A., 2005. Diet of wrinkle-lipped free-tailed bat (Tadarida plicata Buchannan, 1800) in central Thailand: insectivorous bats potentially act as biological pest control agents. Acta Chiropterol. 7, 111–119. McCracken, G.F., Gillam, E.H., Westbrook, J.K., Lee, Y.-F., Jensen, M.L., Balsley, B.B., 2008. Brazilian free-tailed bats (Tadarida brasiliensis: Molossidae, Chiroptera) at high altitude: links to migratory insect populations. Integr. Comp. Biol. 48, 107–118. McCracken, G.F., Safi, K., Kunz, T.H., Dechmann, D.K.N., Swartz, S.M., Wikelski, M., 2016. Airplane tracking documents the fastest flight speeds recorded for bats. R. Soc. Open Sci. 3, 160398. Mikula, P., Morelli, F., Luˇcan, R.K., Jones, D.N., Tryjanowski, P., 2016. Bats as prey of diurnal birds: a global perspective. Mamm. Rev. 46, 160–174. Roeleke, M., Blohm, T., Kramer-Schadt, S., Yovel, Y., Voigt, C.C., 2016. Habitat use of bats in relation to wind turbines revealed by GPS tracking. Sci. Rep. 6, 28961. Roeleke, M., Bumrungsri, S., Voigt, C.C., 2018a. Bats probe the aerosphere during landscape-guided altitudinal flights. Mamm. Rev. 48, 7–11. Roeleke, M., Teige, T., Hoffmeister, U., Klingler, F., Voigt, C.C., 2018b. Aerial-hawking bats adjust their use of space to the lunar cycle. Mov. Ecol., 11. Voigt, C.C., Frick, W.F., Holderied, M.W., Holland, R., Kerth, G., Mello, M.A.R., Plowright, R.K., Swartz, S., Yovel, Y., 2017. Principles and patterns of bat movements: from aerodynamics to ecology. Quart. Rev. Biol. 92, 267–287. Voigt, C.C., Currie, S.E., Fritze, M., Roeleke, M., Lindecke, O., 2018. Conservation strategies for bats flying at high altitudes. BioScience 68, 427–435.
Contents lists available at ScienceDirect
Mammalian Biology journal homepage: www.elsevier.com/locate/mambio
Short communication
Rapid descent flight by a molossid bat (Chaerephon plicatus) returning to its cave Christian C. Voigt a,b,∗ , Sara Bumrungsri c , Manuel Roeleke a,b a b c
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke- Str. 17, 10315, Berlin, Germany Institute for Biology, Freie Universität Berlin, Takustr. 6, 14195, Berlin, Germany Department of Biology, Prince of Songkla University, Hat Yai, Thailand
a r t i c l e
i n f o
Article history: Received 18 November 2018 Accepted 2 January 2019 Available online 3 January 2019 Handled by Danilo Russo Keywords: Aerodynamics Anti-predator strategy Escape behavior Landscape of fear
a b s t r a c t In Southeast Asia, wrinkle-lipped bats (Chaerephon plicatus) roost in colonies that may count several million individuals. Birds of prey frequently hunt these bats when they emerge from or return to their colonies. Here, we report on an extreme anti-predator behavior of this species during return flights at dawn. Based on data logger, we documented that bats may ascend to several hundred meters altitude above the cave shortly before diving at high speed (maximum 20 m/s) towards the entrance. Dive rates were 40 times higher than those reported for other open-space foraging bats performing flapping descending flights. Based on high speed video recordings, we show that C. plicatus brake the rapid descents close to the cave entrance using the tail wing membrane and partly extended wings. Maximum gravitational forces involved 2.4 G, probably when adjusting abruptly the speed close to ground. We argue that these descending maneuvers may constitute an anti-predator strategy of C. plicatus, since such descents may be too fast and complex for birds of prey at the cave entrance, particularly when performed by thousands of individuals at the same time. ¨ Saugetierkunde. ¨ © 2019 Published by Elsevier GmbH on behalf of Deutsche Gesellschaft fur
Bats are the only mammals capable of powered flight and, in comparison to birds, they are considered to be limited in their ability to glide and to reach high speeds (Hedenström et al., 2009; Voigt et al., 2017). Here, we report on rapid descending flights of wrinklelipped free-tailed bats, Chaerephon plicatus (family Molossidae) that challenge our current understanding of flight performance in Chiroptera. Chaerephon plicatus belongs to a guild of aerial insectivores that hunt at night at high altitude and that spend the daytime in large caves counting several million individuals (McCracken et al., 2008; Voigt et al., 2018). Due to the high-altitude flights of members of this guild, we have little information about their foraging or flight behavior. Most open-space foraging bats have long and slender wings (high aspect ratio) which enable them to reach high flight speeds (McCracken et al., 2016). Other open-space foraging bats exhibit stereotypic patterns of ascending and descending flights, possibly to monitor the availability of insects at various air layers (Cvikel et al., 2015; Roeleke et al., 2018a,b).
∗ Corresponding author at: Leibniz Institute for Zoo and Wildlife Research, AlfredKowalke- Str. 17, 10315, Berlin, Germany. E-mail address: [email protected] (C.C. Voigt).
To shed light on the behavior of high-altitude foraging bats, we studied flight patterns of C. plicatus in Thailand; a bat of about 18–20 g body mass that specializes on plant hoppers (Hemiptera), a pest insect that potentially damages the rice harvests in Asian countries (Leelapaibul et al., 2005). In January 2018, we captured 20 C. plicatus emerging from a colony with about 200,000 individuals. We equipped each of the 20 captured bats with a data logger (GiPsy-5 data logger; TechnoSmartEurope, Rome, Italy) that recorded ambient temperature, barometric pressure, and tri-axial acceleration at 1 Hz by gluing the loggers temporarily to the dorsal fur with skin glue (Sauer Hautkleber, Lobbach, Germany). VHF transmitters (Telemetrie-Dessau, Germany) were added to facilitate the retrieval of loggers that fell off the bats after a few days. Retrieval of tags was mandatory since data stored by the logger had to be downloaded via cable connected to a computer. Tags weighed about 15% of the bats’ body mass. Since we and others did not experience any problems with tags of similar relative mass in other open-space foraging bats (Cvikel et al., 2015; Roeleke et al., 2016, 2018a,b; Egert-Berg et al., 2018), we did not expect that tag mass would interfere with the health or flight ability of C. plicatus. Within one week of tag attachment, we located VHF signals from 11 bats in the cave, yet tags were still attached to the bats and
https://doi.org/10.1016/j.mambio.2019.01.001 ¨ Saugetierkunde. ¨ 1616-5047/© 2019 Published by Elsevier GmbH on behalf of Deutsche Gesellschaft fur
16
C.C. Voigt et al. / Mammalian Biology 95 (2019) 15–17
Fig. 1. Flight altitude (A), horizontal (ventral-dorsal) acceleration relative to horizontal resting position (B), and climb rate (C). The horizontal line in panel (A) depicts the altitude of the resting place within the cave.
roosting sites were beyond reach. We assume that the other nine loggers had fallen off of the bats during foraging flights, or that bats switched to neighboring colonies beyond the detection range of our VHF receiver. After five days, we found a single logger on farmland near the cave; all other tags could not be retrieved. We assume that the temporarily attached tags fell of bats when bats foraged at some distance to the cave. Converting data of barometric pressure and ambient temperature of the focal bat into altitude above sea level (asl; hypsometric formula) indeed confirmed that the carrier of the logger flew at high altitudes. Recorded data of one 24 h period showed that the flight altitude of this bat peaked at 785 m asl when the bat returned to its cave. Considering the topography of the study site, this equates to a flight altitude of about 500–600 m above ground. The focal bat lost its tag shortly after its second emergence from the cave, thus we lack data on a second return flight. The observed flight altitude of C. plicatus is similar to that of a syntopic openspace foraging bat, Taphozous theobaldi, which we tracked in a previous study at the same cave using loggers with geographical position system (Roeleke et al., 2018a). In the following text, we will focus on the return flight of this individual C. plicatus (starting at 0539 h). Towards the end of the night, the focal bat performed flight maneuvers with relatively high acceleration rates (Fig. 1). On the zaxis (ventral-dorsal), this bat experienced a maximal gravitational force of 4.9 G, but usually gravitational forces ranged for the z-axis between −0.8 and 2.4 G (97.5% quantiles for diving and braking, respectively, Fig. 1). We assume that the relatively high G values on the z-axis may have originated from decelerating movements of bats when descending. On the x-axis (head-tail), we recorded a maximum absolute value of 0.6 G (97.5% quantile) and on the y-axis (left-right) up to 0.8 G. Starting at 0625 h, the focal bat performed a last ascent of about 10 min duration to a maximum altitude of 785 m asl before it descended about 500 m to the cave located at 270 m asl which the bat entered at 0639 h. During the descending flight the bat sank at a rate of up to 20 m/s and gravitational forces equaled up to 2.4 G, probably when adjusting the dive speed, particularly when approaching the cave entrance (Fig. 1, video 1 and 2 in ESM). The maximum recorded descending rates were 40 times higher than those reported before for another open-space foraging bat (Roeleke et al., 2018a), yet the values fell into the lower range of those reported for passerine birds of similar size when descending during migration to a stopover site (Hedenström and Liechti, 2001).
However, it is important to note that we are unaware of the angle of the flight path in relation to the horizontal, i.e. the actual flight speed of the descending bat could be higher than the assumed vertical descending rate. High speed video recordings at the entrance of a nearby cave confirmed that C. plicatus returns at high speed towards the cave entrance (video 1 and 2 in ESM). Descending flights seem to be regularly interrupted by deceleration maneuvers using the tail wing membrane and the partly extended wings. This could increase profile drag and alter the angle of attack, which might slow down the fall of the bat. Our video observations suggest that C. plicatus mostly glide during the descents without flapping their wings. We speculate that the mechanical stress imposed on the wing membrane and bones may be extreme, considering the small morphological structures, such as the delicate wing bones, involved and the speed at which the bat descended. In consequence, mechanical properties of wings of these open-space foraging bats may not only be adapted towards fast foraging flights, but also to rapid descending flights at the utmost speed possible. We offer two not mutually exclusive explanations for the rapid return flight of the tagged bat to the cave. First, similar to other open-space foraging bats (Cvikel et al., 2015; Roeleke et al., 2018a), C. plicatus is hunting insects at high altitudes and also shortly before returning to their roosts. Yet, considering that the focal bat stayed only for a few minutes at high altitudes, we find it unlikely that the bat hunted insects at around 500 m above ground. Second, individuals from large colonies may be vulnerable to predators, such as hawks and owls (Mikula et al., 2016), and C. plicatus may perform rapid descents as an anti-predatory strategy (see raptor in video 2 of ESM). Predators such as birds of prey may find it difficult to attack bats that descend at these high speeds, particularly when thousands of bats descend almost simultaneously into the cave (video 1 and 2 of ESM). Presumably, C. plicatus may fly to high altitudes to from groups as a defense strategy (Chaverri et al., 2018) and for converting potential energy into kinetic energy in order to reach high descent speeds, beyond its power by flapping flight. We speculate that rapid descending flights may have evolved in bats as an anti-predator strategy when approaching potentially predator rich places like cave entrances. This is the first empirical data on a bat diving at high speed from several hundred meter altitude to its roost, showing that wing morphology and aerodynamics of bats
C.C. Voigt et al. / Mammalian Biology 95 (2019) 15–17
may not only be adapted towards powered flight, but also to rapid gliding descents without large involvement of active wing flapping. Competing interest statement The authors declare no competing interest. Funding sources This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. This work was supported by Deutsche Forschungsgemeinschaft in the framework of the BioMove Training Group (DFG-GRK 2118/1). Acknowledgements We thank that the authorities for granting us permit to conduct the experiment: permit #0002/4508 granted by the National Research Council of Thailand (NRCT) and permit #108/59 granted by the Department of National Park, Wildlife and Plant Conservation (DNP). We thank Nittaya Ruadreo and Supawan Srilopan for help in the field and Shannon Currie for commenting on the manuscript. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.mambio.2019. 01.001.
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References Chaverri, G., Ancillotto, L., Russo, D., 2018. Social communication in bats. Biol. Rev. 93, 1983-1954. Cvikel, N., Berg, K.E., 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. Curr. Biol. 25, 206–211. Egert-Berg, K., Hurme, E.R., Greif, S., Goldstein, A., Harten, L., Herrera, M.L.G., Flores-Martinez, J.J., Vales, A.T., Johnston, D.S., Eitan, O., Borissov, I., Shipley, J.R., Medellin, R.A., Wilkinson, G.S., Goerlitz, H.R., Yovel, Y., 2018. Resource ephemerality drives social foraging in bats. Curr. Biol. 28, 3667–3673. Hedenström, A., Liechti, F., 2001. Field estimates of body drag coefficient on the basis of dives in passerine birds. J. Exp. Biol. 204, 1167–1175. Hedenström, A., Johansson, L.C., Spedding, G.R., 2009. Bird or bat: comparing airframe design and flight performance. Bioinspired Biomim. Nanobiomater. 4, 015001. Leelapaibul, W., Bumrungsri, S., Pattanawiboon, A., 2005. Diet of wrinkle-lipped free-tailed bat (Tadarida plicata Buchannan, 1800) in central Thailand: insectivorous bats potentially act as biological pest control agents. Acta Chiropterol. 7, 111–119. McCracken, G.F., Gillam, E.H., Westbrook, J.K., Lee, Y.-F., Jensen, M.L., Balsley, B.B., 2008. Brazilian free-tailed bats (Tadarida brasiliensis: Molossidae, Chiroptera) at high altitude: links to migratory insect populations. Integr. Comp. Biol. 48, 107–118. McCracken, G.F., Safi, K., Kunz, T.H., Dechmann, D.K.N., Swartz, S.M., Wikelski, M., 2016. Airplane tracking documents the fastest flight speeds recorded for bats. R. Soc. Open Sci. 3, 160398. Mikula, P., Morelli, F., Luˇcan, R.K., Jones, D.N., Tryjanowski, P., 2016. Bats as prey of diurnal birds: a global perspective. Mamm. Rev. 46, 160–174. Roeleke, M., Blohm, T., Kramer-Schadt, S., Yovel, Y., Voigt, C.C., 2016. Habitat use of bats in relation to wind turbines revealed by GPS tracking. Sci. Rep. 6, 28961. Roeleke, M., Bumrungsri, S., Voigt, C.C., 2018a. Bats probe the aerosphere during landscape-guided altitudinal flights. Mamm. Rev. 48, 7–11. Roeleke, M., Teige, T., Hoffmeister, U., Klingler, F., Voigt, C.C., 2018b. Aerial-hawking bats adjust their use of space to the lunar cycle. Mov. Ecol., 11. Voigt, C.C., Frick, W.F., Holderied, M.W., Holland, R., Kerth, G., Mello, M.A.R., Plowright, R.K., Swartz, S., Yovel, Y., 2017. Principles and patterns of bat movements: from aerodynamics to ecology. Quart. Rev. Biol. 92, 267–287. Voigt, C.C., Currie, S.E., Fritze, M., Roeleke, M., Lindecke, O., 2018. Conservation strategies for bats flying at high altitudes. BioScience 68, 427–435.