Abstract
This study examined behavioral strategies for texture discrimination by echolocation in free-flying bats. Big brown bats, Eptesicus fuscus, were trained to discriminate a smooth 16 mm diameter object (S+) from a size-matched textured object (S−), both of which were tethered in random locations in a flight room. The bat’s three-dimensional flight path was reconstructed using stereo images from high-speed video recordings, and the bat’s sonar vocalizations were recorded for each trial and analyzed off-line. A microphone array permitted reconstruction of the sonar beam pattern, allowing us to study the bat’s directional gaze and inspection of the objects. Bats learned the discrimination, but performance varied with S−. In acoustic studies of the objects, the S+ and S− stimuli were ensonified with frequency-modulated sonar pulses. Mean intensity differences between S+ and S− were within 4 dB. Performance data, combined with analyses of echo recordings, suggest that the big brown bat listens to changes in sound spectra from echo to echo to discriminate between objects. Bats adapted their sonar calls as they inspected the stimuli, and their sonar behavior resembled that of animals foraging for insects. Analysis of sonar beam-directing behavior in certain trials clearly showed that the bat sequentially inspected S+ and S−.
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References
Bradbury JW (1970) Target discrimination by the echolocating bat Vampyrum spectrum. J Exp Zool 173:23–46. doi:10.1002/jez.1401730103
Busnel RG, Fish JF (eds) (1980) Animal sonar systems. Plenum Publishing Corporation, New York
Firzlaff U, Schuchmann M, Grunwald JE, Schuller G, Wiegrebe L (2007) Object-oriented echo perception and cortical representation in echolocating bats. PLoS Biol 5:e100. doi:10.1371/journal.pbio.0050100
Ghose K, Moss CF (2003) The sonar beam pattern of a flying bat as it tracks tethered insects. J Acoust Soc Am 114:1120–1131. doi:10.1121/1.1589754
Ghose K, Moss CF (2006) Steering by hearing: a bat’s acoustic gaze is linked to its flight motor output by a delayed, adaptive linear law. J Neurosci 26:1704–1710. doi:10.1523/JNEUROSCI.4315-05.2006
Ghose K, Horiuchi TK, Krishnaprasad PS, Moss CF (2006) Echolocating bats use a nearly time-optimal strategy to intercept prey. PLoS Biol 4:e108. doi:10.1371/journal.pbio.0040108
Ghose K, Triblehorn JD, Bohn K, Yager DD, Moss CF (2009) Behavioral responses of big brown bats to dives by praying mantises. J Exp Biol 212:693–703. doi:10.1242/jeb.019380
Griffin DR (1958) Listening in the dark. Yale University Press, New Haven
Griffin DR, Friend JH, Webster FA (1965) Target discrimination by the echolocation of bats. J Exp Zool 158:155–168. doi:10.1002/jez.1401580204
Habersetzer J, Vogler B (1983) Discrimination of surface-structured targets by the echolocating bat Myotis myotis during flight. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 152:275–282. doi:10.1007/BF00611192
Kalko EKV, Schnitzler H-U (1993) Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection. Behav Ecol Sociobiol 33:415–428
Kick SA, Simmons JA (1984) Automatic gain control in the bat's sonar receiver and the neuroethology of echolocation. J Neurosci 4:2725–2737
Mogdans J, Schnitzler HU, Ostwald J (1993) Discrimination of two-wavefront echoes by the big brown bat, Eptesicus fuscus: behavioral experiments and receiver simulations. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 172:309–323. doi:10.1007/BF00216613
Moss CF, Schnitzler HU (1995) Behavioral studies of auditory information processing. In: Hearing by bats. Springer handbook of auditory research. Springer, Berlin, pp 87–145
Moss CF, Bohn K, Gilkenson H, Surlykke A (2006) Active listening for spatial orientation in a complex auditory scene. PLoS Biol 4. doi:10.1371/journal.pbio.0040079
Nachtigall PE, Moore PWB (eds) (1988) Animal sonar: processes and performance. Plenum Publishing Corporation, New York
Schmidt S (1988) Evidence for a spectral basis of texture perception in bat sonar. Nature 331:617–619. doi:10.1038/331617a0
Schmidt S (1992) Perception of structured phantom targets in the echolocating bat, Megaderma lyra. J Acoust Soc Am 91:2203–2223. doi:10.1121/1.403654
Schnitzler H-U (1968) Die Ultraschall-Ortungslaute der Hufeisen-Fledermäuse (Chiroptera-Rhinolophidae) in verschiedenen Orientierungssituationen. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 57:376–408. doi:10.1007/BF00303062
Schnitzler H-U, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394. doi:10.1016/S0169-5347(03)00185-X
Siemers BM, Schnitzler H-U (2000) Natterer’s bat (Myotis nattereri Kuhl, 1818) hawks for prey close to vegetation using echolocation signals of very broad bandwidth. Behav Ecol Sociobiol 47:400–412. doi:10.1007/s002650050683
Siemers BM, Schnitzler H-U (2004) Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429:657–661. doi:10.1038/nature02547
Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 135:61–84. doi:10.1007/BF00660182
Simmons JA, Vernon JA (1971) Echolocation: discrimination of targets by the bat, Eptesicus fuscus. J Exp Zool 176:315–328. doi:10.1002/jez.1401760307
Simmons JA, Lavender WA, Lavender BA, Doroshow CA, Kiefer SW, Livingston R, Scallet AC, Crowley DE (1974) Target structure and echo spectral discrimination by echolocating bats. Science 186:1130–1132. doi:10.1126/science.186.4169.1130
Simmons JA, Moss CF, Ferragamo M (1990) Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 166:449–470. doi:10.1007/BF00192016
Surlykke A, Kalko EKV (2008) Echolocating bats cry out loud to detect their prey. PLoS One 3:e2036. doi:10.1371/journal.pone.0002036
Surlykke A, Moss CF (2000) Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am 108:2419–2429. doi:10.1121/1.1315295
Surlykke A, Ghose K, Moss CF (2009) Acoustic scanning of natural scenes by echolocation in the big brown bat, Eptesicus fuscus. J Exp Biol 212:1011–1020. doi:10.1242/jeb.024620
Thomas JA, Moss CF, Vater M (eds) (2004) Echolocation in bats and dolphins, 1st edn. University of Chicago Press, Chicago
von der Emde G, Schnitzler H-U (1990) Classification of insects by echolocating greater horseshoe bats. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 167:423–430. doi:10.1007/BF00192577
von Helversen D (2004) Object classification by echolocation in nectar feeding bats: size-independent generalization of shape. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:515–521. doi:10.1007/s00359-004-0492-9
von Helversen D, von Helversen O (2003) Object recognition by echolocation: a nectar-feeding bat exploiting the flowers of a rain forest vine. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:327–336. doi:10.1007/s00359-003-0405-3
Weißenbacher P, Wiegrebe L (2003) Classification of virtual objects in the echolocating bat, Megaderma lyra. Behav Neurosci 117:833–839
Zagaeski M, Moss CF (1994) Target surface texture discrimination by the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 95:2881–2882. doi:10.1121/1.409387
Acknowledgments
This research was supported by the NSF grant, “Active Sensing for Three-Dimensional Auditory Localization” to CFM, an NSF-REU award to BF and an HHMI Undergraduate Research Fellowship and Senior Summer Scholars awards to TW. Data were collected under a research protocol approved by the University of Maryland Institutional Animal Care and Use Committee. We would also like to thank Ray Gracon, Amaya Perez, Wei Xian and Kaushik Ghose for their assistance.
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Supplementary material 1 Video animation of trial presented in Fig. 5a. Video and sound data were slowed down by a factor of 10. The upper-right panel shows the high-speed video recording from each trial. The upper-left panel shows a top-down view of the flight room (note: view rotated in relation to Fig. 5 to match the high-speed video view). The smooth object (S+) is displayed as a white circle, and the textured S- is displayed as a red square. The bat is shown in brown (note: cartoon head aim not corrected for the direction of the sonar beam but instead shows the direction of flight path). The flight path is shown in blue and the vocalization beam directions are indicated by black lines for the first pass and gray lines for the second pass. In this trial, the bat first inspects S- and then immediately goes on to hit S+, as indicated by the beam directions calculated by the 16 microphone array. There is a decrease in the durations of the vocalizations and the pulse interval between vocalizations leading up the inspection of S-. The last vocalization of inspection of S- was highlighted in pink. Before the bat passes S-, the bat makes a vocalization beyond S- (beam directions have been scaled to the minimum overlap zone), indicating a shifting of gaze beyond S- (green). During the final approach and hit of S+, the bat decreases pulse interval and duration of its vocalizations and locks its beam direction to the target (yellow) (AVI 1501 kb)
Supplementary material 2 Video animation of trial presented in Fig. 5b. In this trial, the bat begins with an inspection of S-. The bat makes a loop around the room and ultimately hits S+. The second pass around the targets is indicated in gray. Note the decrease in pulse interval and duration as the bat inspects the targets and also when it hits S+ (AVI 2714 kb)
Supplementary material 3 Video animation of trial presented in Fig. 5c. This trial is similar to SM1 in that the bat first inspects S- and then immediately hits S+. There is a decrease in pulse interval and slight decrease in duration as the bat inspects S- (AVI 1195 kb)
Supplementary material 4 Video animation of trial presented in Fig. 5d. In this trial, the bat makes two passes at the objects. In the first pass, the bat inspects S- and then it flies beneath it. In the second pass, the bat inspects S+ before ultimately hitting S+. Due to the close spacing between S+ and S- in this trial, we were unable to determine if the bat inspected each object sequentially or if it inspected both objects at the same time (AVI 2801 kb)
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Falk, B., Williams, T., Aytekin, M. et al. Adaptive behavior for texture discrimination by the free-flying big brown bat, Eptesicus fuscus . J Comp Physiol A 197, 491–503 (2011). https://doi.org/10.1007/s00359-010-0621-6
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DOI: https://doi.org/10.1007/s00359-010-0621-6