Fast-moving bat ears create informative Doppler shifts

Xiaoyan Yin; Rolf Müller

doi:10.1073/pnas.1901120116

Edited by James A. Simmons, Brown University, Providence, RI, and accepted by Editorial Board Member Thomas D. Albright April 30, 2019 (received for review January 26, 2019)

Significance

Many animal species are known for unparalleled abilities to encode sensory information that supports fast, reliable action in complex environments, but the mechanisms remain often unclear. Here, we present a nonlinear principle for sensory information encoding in bats. Through fast ear motions, bats can encode information on target direction into time-frequency Doppler signatures. These species were thought to be evolutionarily tuned to Doppler shifts generated by a prey’s wing beat. Self-generated Doppler shifts from the bat’s own flight motion were, for the most part, considered a nuisance that the bats compensate for. Our findings indicate that these Doppler-based biosonar systems may be more complicated than previously thought because the animals can actively inject Doppler shifts into their input signals.

Abstract

Many animals have evolved adept sensory systems that enable dexterous mobility in complex environments. Echolocating bats hunting in dense vegetation represent an extreme case of this, where all necessary information about the environment must pass through a parsimonious channel of pulsed, 1D echo signals. We have investigated whether certain bats (rhinolophids and hipposiderids) actively create Doppler shifts with their pinnae to encode additional sensory information. Our results show that the bats’ active pinna motions are a source of Doppler shifts that have all attributes required for a functional relevance: (i) the Doppler shifts produced were several times larger than the reported perception threshold; (ii) the motions of the fastest moving pinna portions were oriented to maximize the Doppler shifts for echoes returning from the emission direction, indicating a possible evolutionary optimization; (iii) pinna motions coincided with echo reception; (iv) Doppler-shifted signals from the fast-moving pinna portion entered the ear canal of a biomimetic pinna model; and (v) the time-frequency Doppler shift signatures were found to encode target direction in an orderly fashion. These results indicate that instead of avoiding or suppressing all self-produced Doppler shifts, rhinolophid and hipposiderid bats actively create Doppler shifts with their own pinnae. These bats could hence make use of a previously unknown nonlinear mechanism for the encoding of sensory information, based on Doppler signatures. Such a mechanism could be a source for the discovery of sensing principles not only in sensory physiology but also in the engineering of sensory systems.

Conspicuous pinna motions (1 ⇓⇓⇓–5) are an integral part of biosonar behaviors in horseshoe bats and Old World leaf-nosed bats [families Rhinolophidae and Hipposideridae (6, 7)]. These motions have been demonstrated to enhance sensing and navigation performance (8 ⇓–10), but the functional role of these dynamic features and the underlying mechanisms have yet to be fully understood (7). In the acoustic domain, source or receiver motions can result in Doppler shifts, i.e., nonlinear scaling of signals in time and frequency. The possibility of pinna-induced Doppler shifts had been mentioned as an aside in early work by Pye and coworkers (2, 3, 11) but has not been considered further—let alone investigated in any depth—in the literature since. This complete neglect is regrettable, because ear-generated Doppler shifts could constitute a previously unknown, nonlinear mechanism for the active encoding of sensory information. To test this hypothesis, we have carried out a quantitative experimental investigation of the hypothesis that pinna motions cause functionally relevant Doppler shifts in bats. For pinna-generated Doppler shifts to have a functional role, five necessary conditions must be met: (i) pinna surface speeds must be high enough to produce Doppler shifts that exceed the animal’s perception threshold [here, we use the ∼50-Hz SD of Doppler-shift compensation (12 ⇓⇓–15)], (ii) the directions of pinna surface velocity and echo propagation must be aligned well enough to translate the surface speeds into sufficiently large Doppler shifts, (iii) fast pinna motions must occur during echo reception, (iv) Doppler-shifted waves from the fast moving portions of the pinna surface must enter the ear canal, and (v) the Doppler signatures must convey useful sensory information.

Results

Using reconstructed 3D trajectories of landmark points placed on the pinna tips of individuals from three species with fast pinna motions (greater horseshoe bat, Rhinolophus ferrumequinum; and two hipposiderid species, Hipposideros armiger and Hipposideros pratti; Fig. 1 and Movie S1), motion speeds up to ∼2.2 m/s were found (Fig. 1A). While the ranges of the speed values overlapped among all species, there were statistically significant differences between them (Tukey’s range test, P < 0.0001 for all differences). Since all three species share a constant-frequency–frequency-modulated (cf-fm) biosonar system (16, 17), we have used the cf-component of the strongest (second) harmonic of the animals’ biosonar pulses (18, 19) for estimating the Doppler shifts corresponding to the tip speeds. Maximum Doppler shifts were calculated under the assumption that the direction of the maximum pinna surface velocity is aligned with the radiation direction of the echoes. The highest Doppler shift determined in this way was 383 Hz (for H. pratti; Fig. 1B). For the Doppler shifts, the difference between the two hipposiderid species was no longer significant (P = 0.47), but the difference between the hipposiderids and the horseshoe bats remained significant (with P < 0.0001). The greater similarity in the Doppler shifts among the hipposiderids was due to the higher speeds occurring in the species with the lower cf-frequency (H. pratti, cf at ∼60 kHz vs. ∼70 kHz in H. armiger). Hence, it could be hypothesized that the pinna motion speeds in these hipposiderid species are adapted to produce similar Doppler shifts regardless of carrier frequency.

Fig. 1.

Pinna-tip speeds and maximum Doppler shifts for all three bat species studied. (A) Pinna-tip speeds calculated from reconstructed 3D trajectories of landmarks placed on the pinna tip. (B) Maximum Doppler shifts calculated under the assumption that the pinna moves in the direction of sound propagation (center line: median; box edges: 25th and 75th percentiles; whiskers: minimum and maximum values). Maximum Doppler shifts were calculated under the assumption that the direction of the maximum pinna-surface velocity is aligned with the radiation direction of the echoes.

Doppler shifts do not only depend on the speeds involved but also on how the velocity vectors of these motions are oriented with respect to propagation vectors of the incoming echoes. The maximum Doppler shifts for a given speed are only realized if the velocity vectors are parallel to the direction of sound propagation. We have used dense sampling of the pinna surface with landmark points to reconstruct the distribution of speeds and velocity vectors across most of the inner pinna surface. Based on ultrasonic array recordings done in the same experiments as the pinna surface velocity measurement, we have determined the direction in which most pulse energy was emitted as an estimate for where the bats were directing their biosonar beams and presumably were expecting the echoes to return from. We found that the highest speeds occurred in a region along the outer pinna rim that was a good match for where the orientations of the velocity vectors at maximum speed were close to parallel to the direction of sound radiation (Fig. 2). This spatial coincidence between high surface speeds and small angles between motion and sound radiation vectors could be hypothesized to be an adaptation that maximizes the Doppler shifts resulting from the pinna motions.

Fig. 2.

Distribution of speed, directional cosine between surface velocity and radiation direction, and Doppler shift on the inner surface of the pinna. (A) Maximum surface speed during a pinna motion. (B) Directional cosine between surface velocity and the direction of sound propagation associated with the maximum speed. (C) Doppler-shift estimates based on A and B. Directional cosines were calculated under the assumption that the propagation direction of the echo corresponds to the direction associated with the maximum amplitude of the pulse.

For any potential impact on echo perception, the fast pinna motions must occur during echo reception. To assess whether this is the case, we have analyzed pinna motion speeds during echo returns with synchronized arrays of high-speed cameras and ultrasonic microphones. These data contained only pulse-echo sequences that were accompanied by fast pinna motions. We found that all echoes in these sequences coincided with Doppler shifts that exceeded the 50-Hz accuracy reported for Doppler-shift compensation (12). Depending on species, between 33 and 82% of the echoes coincided with pinna motions fast enough to produce Doppler shifts that exceeded this threshold three times (Fig. 3). Hence, these data suggest that all echoes in echolocation sequences accompanied by pinna motions contain Doppler-shift signatures that should be perceivable by the bats.

Fig. 3.

Fast pinna motions and large Doppler shifts occur during echoes. (A) Pinna-surface speed calculated from the landmark on the tip of the pinna superimposed on the spectrogram of biosonar pulse from greater horseshoe bat (Rhinolophus ferrumequinum) and its echoes. In the shown example recording, the pulses coincided with a forward motion of the pinna (positive speeds). (B) Portion of pulses with maximum Doppler shift exceeding a certain threshold. Number of motion sequences/echoes analyzed: H. armiger, 39; H. pratti, 57; R. ferrumequinum, 36.

Since only certain regions of the pinna surface (near the outer rim) move at speeds that are sufficiently large for the creation of perceivable Doppler shifts, we have investigated whether signal components diffracted by these regions enter the ear canal and could hence be perceived by the animals and supply useful sensory information. These experiments were based on a biomimetic pinna with a static geometry and deformation patterns that were qualitatively similar to the bats’ pinna. We found that the biomimetic pinna motions produced strong Doppler signatures in the ultrasonic signals received inside the ear canal (Fig. 4A). As could be expected from the continuous distributions of speed over the pinna surface, the acoustic effects of the pinna motions took the form of spectral broadenings. We found the pinna-tip velocity to be a useful predictor of the maximum Doppler shift (Fig. 4A). The sign of the observed Doppler shifts depended on the direction of the pinna motions. Since the bat species studied here exhibit alternating ear motions with one ear moving forward while the other moves backward (2), the spectral spread of a combined binaural input could be about twice that produced by a single ear at any given time.

Fig. 4.

Direction-dependent Doppler-shift signatures received at the ear canal of a deforming biomimetic pinna. (A) Spectrogam of an example Doppler signature (azimuth, 60○; elevation, 0○) with a superposed prediction of the maximum Doppler shift based on pinna-surface velocity estimates (magenta line). The arrow indicates the start of the pinna motion. (B) Maximum number of direction that could be distinguished based on Doppler signatures as a function of the signal-to-noise ratio. (C) Clustering result showing an orderly breakup of the direction space based on the Doppler signatures. The different gray scale values and numbers denote the clusters that Doppler signatures for the respective direction were assigned to.

Finally, we found that the time-frequency Doppler signatures were direction-dependent (Fig. 4) and could hence be used to obtain information on the direction of a biosonar target. To quantify the available information, we have used an information-theoretic paradigm (20) that puts an upper bound on the number of directions that could be resolved as a function of the available signal-to-noise ratio (Fig. 4B). The results indicate that the Doppler signatures would be suitable to distinguish a large number of different target directions—even at fairly low signal-to-noise ratios, e.g., at a signal-to-noise ratio of 12 decibels (dB), up to about 1 million different directions could be theoretically distinguished. Furthermore, the Doppler signatures varied with direction in a systematic fashion. This was evident from the results of clustering the Doppler signatures based on their spectrogram representation yielded contiguous partitions of the direction space (Fig. 4C). This should help exploiting the direction dependence of the Doppler signatures (SI Appendix, Fig. S5) since small errors in estimating the Doppler shifts should result likewise in small errors in the direction estimates.

Discussion

All Doppler shifts that occur in bat biosonar can be classified as either prey-generated or self-generated. At present, prey-generated Doppler shifts are the only well-established solution to the problem of identifying prey in clutter with active biosonar (21). The importance of prey-generated Doppler shifts is evident from numerous, far-reaching adaptations in bats that range from pulse design to behavior and from the inner ear (22) to the auditory cortex (23, 24). As of now, only the bats’ own flight motions have been considered as sources of self-generated Doppler shifts. The resulting Doppler shifts have been regarded mostly as undesirable side effects of the animals’ mobility that need to be compensated for (25). The possibility of flight-induced Doppler shift conveying information to support navigation has only been investigated using computational methods so far (26), and there is no published experimental evidence that bats make use of flight-induced Doppler shifts. Fast pinna motions constitute a previously unknown second source of self-generated Doppler shifts. In general, horseshoe bat pinna motions are unlikely byproducts since the animals seem to go such a great length to actively produce them, e.g., through an elaborate pinna musculature (1). Furthermore, it has been reported that surgical disruptions of the pinna mobility have led to performance deficits in horseshoe bats (1, 8). Similarly, the match between the regions of highest pinna surface speeds and the best alignment of the motion and sound propagation directions found here could be seen to argue in favor of functional significance of the Doppler shift to which the system has been evolutionarily adapted. However, much more data covering a larger number of species would be needed to test this hypothesis thoroughly.

Taking into account our current results, pinna motions in horseshoe and hipposiderid bats could serve the animals’ sensing in three different, but nonexclusive, ways, i.e., through (i) a rigid component that reorients the beampattern (27); (ii) a nonrigid, linear component that changes the pinna’s beampattern by virtue of the pinna geometry; and (iii) a nonlinear, Doppler-based component. The rigid component is shared by many animals (e.g., head motions in humans) as well as technical sonar and radar systems. It can be readily understood as a scanning operation where the most sensitive region of the beampattern is moved into different directions. The nonrigid, linear motion components have recently been demonstrated to enhance the encoding of sensory information related to direction-finding (9). Changing the pinna geometry to produce a different beam-pattern shape can be seen as an alternative to change the frequency for a fixed pinna geometry (28). The nonlinear transformations due to the pinna-generated Doppler shifts described here add an additional quality to the pinna motions in bats. It remains to be determined if the Doppler transformations of the echoes serve a functional purpose in the animals. If they are an integral part of the peripheral dynamics of the bats’ biosonar system, as the evidence presented here suggests, this would mean that the bats are able to harness nonlinear effects that could lead to new functional principles for enhance sensing of natural environments and enable engineered sensory systems with the same capabilities.

Materials and Methods

Overall Experimental Setup.

During the experiments, each bat was placed on a platform consisting of a piece of planar wire-mesh grid that was rotated 45○ relative to the horizontal, so that the bat’s head was lower than its feet when positioned on the platform. On this platform, the bat was positioned in the center of the setup (SI Appendix, Fig. S1B) and at a distance of 50 cm from the microphones in the array that was used to record the ultrasound and 55 cm from the high-speed video cameras that were used to record the pinna motions. All potential sound-reflecting surfaces in the setup where clad in sound-absorbing foam during the experiment.

Three-Dimensional Reconstruction of Pinna Motions.

Quantitative characterizations of the pinna motion kinematics were obtained based on 3D reconstructions of the time trajectories (SI Appendix, Fig. S1C) belonging to discrete landmark points that were placed on the pinna (SI Appendix, Fig. S1A). The landmark points were placed on the bats using a nontoxic dye before the experiments and removed (washed off) immediately after the end of each experiment. For each experiment, approximately 60 different landmark points were distributed over the pinna surface with an emphasis on coverage of the pinna rim. Five to seven additional landmark points each were placed on the top of the head and the noseleaf of the animal to provide an anatomical frame of reference for the pinna motions.

Video image sequences with views of the bats’ heads, their pinnae, and the associated landmarks were captured using an array of four high-speed video cameras (GigaView; Southern Vision Systems) with 50-mm lenses (Rodagon; Rodenstock). All cameras were operated with a frame rate of 400 Hz and a digital image resolution of 1,280 × 1,024 pixels. The high-speed cameras were calibrated to obtain estimates of their internal and external parameters based on calibration images taken of a checkerboard pattern from different viewing directions (29). The image coordinates of each landmark point were obtained using video frames from at least two different high-speed video cameras that had imaged the landmark of interest at the respective time. The image locations of the landmark were picked manually in the rectified video frames. The high-speed video cameras to be included in the stereo reconstruction were selected manually based on how well their images had captured the landmark points during a given motion. Finally, the image coordinates were used to reconstruct the 3D location of the landmark points using stereo triangulation (29).

Ultrasound Recording.

A capacitive measurement microphone (1/8-inch pressure-field microphone, type 40 DP, with type AL0003 preamplifier; G.R.A.S. Sound & Vibration) was used to record the echo returns at the position of the bats. The microphone was placed approximately 1 cm above the bat’s head. The microphone was calibrated with a sound level calibrator (type 4231; Brüel & Kjær) at 114 dB sound pressure level and a frequency of 1 kHz. The output signals of the microphone were digitized with a sampling rate of 512 kHz and 16-bit resolution (common-mode rejection ratio, 75 dB; PXIe-6358 data acquisition board; National Instruments). Additional microphones (measurement microphones, type 40 DP [G.R.A.S. Sound & Vibration]; and capacitive micro-electromechanical systems [MEMS] microphones [Momimic; Dodotronic]) were placed in a vertical and a horizontal line array to record the emissions of the bats in the setup. The microphones and the high-speed video cameras were triggered simultaneously using a custom LabVIEW control software. The control system produced a constant time offset of 16 ms between video and audio recordings that was compensated for during data analysis.

Biomimetic Pinna Experiments.

A biomimetic pinna shape was designed based on the micro-computed tomography scan of an adult horseshoe bat pinna specimen. The shape was simplified by eliminating small geometric detail in the digital domain [Autodesk Maya (30)], while keeping the overall shape of the original. The simplified design was used to create a rigid physical model of the pinna shape with additive manufacturing. This rigid physical model was used to create a mold and then cast a flexible biomimetic pinna in silicone (Ecoflex; Smooth-On, Inc.). The biomimetic pinna designed and fabricated in this way had a height of 5.8 cm, i.e., about twice the size of the pinna in greater horseshoe bats. An electrostatic loudspeaker (Series 600 open-face ultrasonic transducer; SensComp) was used to emit ultrasonic pulses with a constant carrier frequency of 90 kHz [resting cf-frequencies in greater horseshoe bats have been reported to fall slightly above 80 kHz (12) but can exceed 100 kHz in other species of the genus (31)] and a duration of 150 ms [in greater horseshoe bats, pulse durations up to 60 ms have been reported (32)]. The parameters of the biomimetic pinna experiments were chosen for greater ease of experimentation without creating any differences that could affect the applicability of the results to the question whether pinna motions in the bats could create Doppler-shifted signal components that enter the ear canal. The signal length was chosen so that the Doppler shift signature of a full forward and backward pinna motion cycle could be recorded.

The signals mimicking the “echoes” impinging on the biomimetic pinna were emitted by a loudspeaker that was positioned at a distance of 50 cm in front of the biomimetic pinna. A capacitive MEMS microphone (Momimic; Dodotronic) was coupled to the pinna via an artificial ear canal (length, 9 mm; diameter, 4 mm) to record the received ultrasonic signals. The output of the microphone was digitized with a sampling frequency of 500 kHz and a resolution of 16 bits (PXIe-6356 data acquisition board; National Instruments). The 3D trajectory of the tip point of the bat’s moving ear was reconstructed based on the video frames recorded with two synchronized GoPro HERO3+ cameras (Dual HERO System; GoPro) at a frame rate of 120 Hz.

For recording direction-dependent Doppler signatures, the biomimetic pinna assembly (SI Appendix, Fig. S2) was mounted on a pan-tilt unit (model PTU-46-17.5; FLIR Systems, Inc.). The pinna was rotated over a range of 180° in azimuth and 60° in elevation centered on the front-facing direction of the pinna aperture in steps of 3°. Hence, there were 61 different azimuth and 21 different elevation values, resulting in a total of 1,281 different directions that were surveyed in these experiments. For each of these directions, narrow-band ultrasonic pulses were emitted at the biomimetic pinna as described above. During each of the 150-ms recordings, the biomimetic pinna was held static for 20 ms and was in motion for the remaining 130 ms. For each of the motions, an estimate of the maximum Doppler shift was obtained from speed estimates for a landmark point that was placed on the pinna tip.

Acknowledgments

This research has been supported by National Science Foundation Award 1362886; Naval Engineering Education Center Contract N00174-16-C-0026; National Natural Science Foundation of China Grants 11374192, 11074149, and 11574183; Fundamental Research Fund of Shandong University Grant 2014QY008; and the China Scholarship Council. All data are available in the main text or Supporting Information. Phat Ngyuen and Thomas Tucker provided visualization of parameters on bat pinna. Peiwen Qiu helped with conducting the animal experiments.

Footnotes

↵¹X.Y. and R.M. contributed equally to this work.
↵²To whom correspondence may be addressed. Email: rolf.mueller{at}vt.edu.

Author contributions: X.Y. and R.M. designed research; X.Y. performed research; X.Y. and R.M. analyzed data; and X.Y. and R.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. J.A.S. is a Guest Editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1901120116/-/DCSupplemental.

Published under the PNAS license.

References

↵
1. H. Schneider,
2. F. P. Möhres
, Die Ohrbewegungen der Hufeisennasenfledermäuse (Chiroptera, Rhinolophidae) und der Mechanismus des Bildhörens. Z. Vergl. Physiol. 44, 1–40 (1960).
OpenUrl
↵
1. J. D. Pye,
2. M. Flinn,
3. A. Pye
, Correlated orientation sounds and ear movements of horseshoe bats. Nature 196, 1186–1188 (1962).
OpenUrl CrossRef
↵
1. J. D. Pye,
2. L. H. Roberts
, Ear movements in a hipposiderid bat. Nature 225, 285–286 (1970).
OpenUrl CrossRef
↵
1. L. Gao,
2. S. Balakrishnan,
3. W. He,
4. Z. Yan,
5. R. Müller
, Ear deformations give bats a physical mechanism for fast adaptation of ultrasonic beampatterns. Phys. Rev. Lett. 107, 214301 (2011).
OpenUrl CrossRef PubMed
↵
1. X. Yin,
2. P. Qiu,
3. L. Yang,
4. R. Müller
, Horseshoe bats and old world leaf-nosed bats have two discrete types of pinna motions. J. Acoust. Soc. Am. 141, 3011–3017 (2017).
OpenUrl
↵
1. F. P. Möhres
, Über die Ultraschallorientierung der Hufeisennasen (Chiroptera-Rhinolophinae). J. Comp. Physiol. A 34, 547–588 (1953).
OpenUrl
↵
1. R. Müller
, Dynamics of biosonar systems in horseshoe bats. Eur. Phys. J. Spec. Top. 224, 3393–3406 (2015).
OpenUrl
↵
1. J. Mogdans,
2. J. Ostwald,
3. H.-U. Schnitzler
, The role of pinna movement for the localization of vertical and horizontal wire obstacles in the greater horseshoe bat, Rhinolopus ferrumequinum. J. Acoust. Soc. Am. 84, 1676–1679 (1988).
OpenUrl CrossRef
↵
1. R. Müller et al.
, Dynamic substrate for the encoding sensory information in bat biosonar. Phys. Rev. Lett. 118, 158102 (2017).
OpenUrl
↵
1. R. Müller
, Quantitative approaches to sensory information encoding by bat noseleaves and pinnae. Can. J. Zool. 96, 79–86 (2018).
OpenUrl
↵
1. J. D. Pye
, A theory of echolocation by bats. J. Laryngol. Otol. 74, 718–729 (1960).
OpenUrl CrossRef PubMed
↵
1. G. Schuller,
2. K. Beuter,
3. H.-U. Schnitzler
, Response to frequency shifted artificial echoes in the bat Rhinolophus ferrumequinum. J. Comp. Physiol. 89, 275–286 (1974).
OpenUrl
↵
1. J. A. Simmons
, Response of the Doppler echolocation system in the bat, Rhinolophus ferrumequinum. J. Acoust. Soc. Am. 56, 672–682 (1974).
OpenUrl CrossRef PubMed
↵
1. U. Heilmann
, “Das Frequenzunterscheidungsvermögen bei der großen Hufeisennase, Rhinolophus ferrumequinum” PhD thesis, Tübingen University, Tuebingen, Germany (1984).
↵
1. H.-U. Schnitzler
, “The performance of bat sonar systems” in Localization and Orientation in Biology and Engineering (Springer, New York, NY, 1984), pp. 211–224.
↵
1. G. Jones,
2. E. C. Teeling
, The evolution of echolocation in bats. Trends Ecol. Evol. 21, 149–56 (2006).
OpenUrl CrossRef PubMed
↵
1. M. B. Fenton,
2. P. A. Faure,
3. J. M. Ratcliffe
, Evolution of high duty cycle echolocation in bats. J. Exp. Biol. 215, 2935–2944 (2012).
OpenUrl Abstract/FREE Full Text
↵
1. G. Jones,
2. J. M. V. Rayner
, Foraging behavior and echolocation of wild horseshoe bats rhinolophus ferrumequinum and r. hipposideros (chiroptera, rhinolophidae). Behav. Ecol. Sociobiol. 25, 183–191 (1989).
OpenUrl CrossRef
↵
1. S. Hiryu,
2. K. Katsura,
3. L. K. Lin,
4. H. Riquimaroux,
5. Y. Watanabe
, Doppler-shift compensation in the taiwanese leaf-nosed bat (hipposideros terasensis) recorded with a telemetry microphone system during flight. J. Acoust. Soc. Am. 118, 3927–3933 (2005).
OpenUrl CrossRef PubMed
↵
1. J. R. Buck
, “Information theoretic bounds on source localization performance” in Sensor Array and Multichannel Signal Processing Workshop Proceedings, 2002 (IEEE, Piscataway, NJ, 2002), pp. 184–188.
↵
1. A. J. Corcoran,
2. C. F. Moss
, Sensing in a noisy world: Lessons from auditory specialists, echolocating bats. J. Exp. Biol. 220, 4554–4566 (2017).
OpenUrl Abstract/FREE Full Text
↵
1. V. Bruns,
2. E. Schmieszek
, Cochlear innervation in the greater horseshoe bat: Demonstration of an acoustic fovea. Hear. Res. 3, 27–43 (1980).
OpenUrl CrossRef PubMed
↵
1. J.P. Ewert,
2. R.R. Capranica,
3. D.I. Ingle
1. H.-U. Schnitzler,
2. J. Ostwald
, “Adaptations for the detection of fluttering insects by echolocation in horseshoe bats” in Advances in Vertebrate Neuroethology, J.P. Ewert, R.R. Capranica, D.I. Ingle, Eds. (Plenum Press, New York, NY, 1983), pp. 801–827.
↵
1. H.-U. Schnitzler,
2. A. Denzinger
, Auditory fovea and Doppler shift compensation: Adaptations for flutter detection in echolocating bats using cf-fm signals. J. Comp. Physiol. A 197, 541–559 (2011).
OpenUrl CrossRef PubMed
↵
1. H.-U. Schnitzler
, Control of Doppler shift compensation in the greater horseshoe bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 82, 79–92 (1973).
OpenUrl CrossRef
↵
1. R. Müller,
2. H.-U. Schnitzler
, Acoustic flow perception in cf-bats: Properties of the available cues. J. Acoust. Soc. Am. 105, 2958–2966 (1999).
OpenUrl CrossRef PubMed
↵
1. V. A. Walker,
2. H. Peremans,
3. J. C. T. Hallam
, One tone, two ears, three dimensions: A robotic investigation of pinnae movements used by rhinolophid and hipposiderid bats. J. Acoust. Soc. Am. 104, 569–579 (1998).
OpenUrl CrossRef PubMed
↵
1. A. K. Gupta,
2. D. Webster,
3. R. Müller
, Entropy analysis of frequency and shape change in horseshoe bat biosonar. Phys. Rev. E 97, 062402 (2018).
OpenUrl
↵
1. J. Y. Bouguet,
2. P. Perona
, Camera calibration from points and lines in dual-space geometry (1998). https://pdfs.semanticscholar.org/df4e/24c7b651beeb4d8b34e7de302cf4f869ef49.pdf. Accessed 13 May 2019.
↵
1. J. F. Hughes
, Computer Graphics: Principles and Practice (Addison-Wesley, Upper Saddle River, NJ, ed. 3, 2014).
↵
1. K.-G. Heller,
2. O. v. Helversen
, Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80, 178–186 (1989).
OpenUrl CrossRef
↵
1. G. Schuller
, Echo delay and overlap with emitted orientation sounds and Doppler-shift compensation in the bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 114, 103–114 (1977).
OpenUrl CrossRef

Article Alerts

Email Article

Citation Tools

Request Permissions

Article Classifications

Biological Sciences
Applied Biological Sciences

Proceedings of the National Academy of Sciences: 116 (25)

Table of Contents

Submit

[1] ↵
H. Schneider,
F. P. Möhres
, Die Ohrbewegungen der Hufeisennasenfledermäuse (Chiroptera, Rhinolophidae) und der Mechanismus des Bildhörens. Z. Vergl. Physiol. 44, 1–40 (1960).
OpenUrl

[2] H. Schneider,

[3] F. P. Möhres

[4] ↵
J. D. Pye,
M. Flinn,
A. Pye
, Correlated orientation sounds and ear movements of horseshoe bats. Nature 196, 1186–1188 (1962).
OpenUrl CrossRef

[5] J. D. Pye,

[6] M. Flinn,

[7] A. Pye

[8] ↵
J. D. Pye,
L. H. Roberts
, Ear movements in a hipposiderid bat. Nature 225, 285–286 (1970).
OpenUrl CrossRef

[9] J. D. Pye,

[10] L. H. Roberts

[11] ↵
L. Gao,
S. Balakrishnan,
W. He,
Z. Yan,
R. Müller
, Ear deformations give bats a physical mechanism for fast adaptation of ultrasonic beampatterns. Phys. Rev. Lett. 107, 214301 (2011).
OpenUrl CrossRef PubMed

[12] L. Gao,

[13] S. Balakrishnan,

[14] W. He,

[15] Z. Yan,

[16] R. Müller

[17] ↵
X. Yin,
P. Qiu,
L. Yang,
R. Müller
, Horseshoe bats and old world leaf-nosed bats have two discrete types of pinna motions. J. Acoust. Soc. Am. 141, 3011–3017 (2017).
OpenUrl

[18] X. Yin,

[19] P. Qiu,

[20] L. Yang,

[21] R. Müller

[22] ↵
F. P. Möhres
, Über die Ultraschallorientierung der Hufeisennasen (Chiroptera-Rhinolophinae). J. Comp. Physiol. A 34, 547–588 (1953).
OpenUrl

[23] F. P. Möhres

[24] ↵
R. Müller
, Dynamics of biosonar systems in horseshoe bats. Eur. Phys. J. Spec. Top. 224, 3393–3406 (2015).
OpenUrl

[25] R. Müller

[26] ↵
J. Mogdans,
J. Ostwald,
H.-U. Schnitzler
, The role of pinna movement for the localization of vertical and horizontal wire obstacles in the greater horseshoe bat, Rhinolopus ferrumequinum. J. Acoust. Soc. Am. 84, 1676–1679 (1988).
OpenUrl CrossRef

[27] J. Mogdans,

[28] J. Ostwald,

[29] H.-U. Schnitzler

[30] ↵
R. Müller et al.
, Dynamic substrate for the encoding sensory information in bat biosonar. Phys. Rev. Lett. 118, 158102 (2017).
OpenUrl

[31] R. Müller et al.

[32] ↵
R. Müller
, Quantitative approaches to sensory information encoding by bat noseleaves and pinnae. Can. J. Zool. 96, 79–86 (2018).
OpenUrl

[33] R. Müller

[34] ↵
J. D. Pye
, A theory of echolocation by bats. J. Laryngol. Otol. 74, 718–729 (1960).
OpenUrl CrossRef PubMed

[35] J. D. Pye

[36] ↵
G. Schuller,
K. Beuter,
H.-U. Schnitzler
, Response to frequency shifted artificial echoes in the bat Rhinolophus ferrumequinum. J. Comp. Physiol. 89, 275–286 (1974).
OpenUrl

[37] G. Schuller,

[38] K. Beuter,

[39] H.-U. Schnitzler

[40] ↵
J. A. Simmons
, Response of the Doppler echolocation system in the bat, Rhinolophus ferrumequinum. J. Acoust. Soc. Am. 56, 672–682 (1974).
OpenUrl CrossRef PubMed

[41] J. A. Simmons

[42] ↵
U. Heilmann
, “Das Frequenzunterscheidungsvermögen bei der großen Hufeisennase, Rhinolophus ferrumequinum” PhD thesis, Tübingen University, Tuebingen, Germany (1984).

[43] U. Heilmann

[44] ↵
H.-U. Schnitzler
, “The performance of bat sonar systems” in Localization and Orientation in Biology and Engineering (Springer, New York, NY, 1984), pp. 211–224.

[45] H.-U. Schnitzler

[46] ↵
G. Jones,
E. C. Teeling
, The evolution of echolocation in bats. Trends Ecol. Evol. 21, 149–56 (2006).
OpenUrl CrossRef PubMed

[47] G. Jones,

[48] E. C. Teeling

[49] ↵
M. B. Fenton,
P. A. Faure,
J. M. Ratcliffe
, Evolution of high duty cycle echolocation in bats. J. Exp. Biol. 215, 2935–2944 (2012).
OpenUrl Abstract/FREE Full Text

[50] M. B. Fenton,

[51] P. A. Faure,

[52] J. M. Ratcliffe

[53] ↵
G. Jones,
J. M. V. Rayner
, Foraging behavior and echolocation of wild horseshoe bats rhinolophus ferrumequinum and r. hipposideros (chiroptera, rhinolophidae). Behav. Ecol. Sociobiol. 25, 183–191 (1989).
OpenUrl CrossRef

[54] G. Jones,

[55] J. M. V. Rayner

[56] ↵
S. Hiryu,
K. Katsura,
L. K. Lin,
H. Riquimaroux,
Y. Watanabe
, Doppler-shift compensation in the taiwanese leaf-nosed bat (hipposideros terasensis) recorded with a telemetry microphone system during flight. J. Acoust. Soc. Am. 118, 3927–3933 (2005).
OpenUrl CrossRef PubMed

[57] S. Hiryu,

[58] K. Katsura,

[59] L. K. Lin,

[60] H. Riquimaroux,

[61] Y. Watanabe

[62] ↵
J. R. Buck
, “Information theoretic bounds on source localization performance” in Sensor Array and Multichannel Signal Processing Workshop Proceedings, 2002 (IEEE, Piscataway, NJ, 2002), pp. 184–188.

[63] J. R. Buck

[64] ↵
A. J. Corcoran,
C. F. Moss
, Sensing in a noisy world: Lessons from auditory specialists, echolocating bats. J. Exp. Biol. 220, 4554–4566 (2017).
OpenUrl Abstract/FREE Full Text

[65] A. J. Corcoran,

[66] C. F. Moss

[67] ↵
V. Bruns,
E. Schmieszek
, Cochlear innervation in the greater horseshoe bat: Demonstration of an acoustic fovea. Hear. Res. 3, 27–43 (1980).
OpenUrl CrossRef PubMed

[68] V. Bruns,

[69] E. Schmieszek

[70] ↵
J.P. Ewert,
R.R. Capranica,
D.I. Ingle
H.-U. Schnitzler,
J. Ostwald
, “Adaptations for the detection of fluttering insects by echolocation in horseshoe bats” in Advances in Vertebrate Neuroethology, J.P. Ewert, R.R. Capranica, D.I. Ingle, Eds. (Plenum Press, New York, NY, 1983), pp. 801–827.

[71] J.P. Ewert,

[72] R.R. Capranica,

[73] D.I. Ingle

[74] H.-U. Schnitzler,

[75] J. Ostwald

[76] ↵
H.-U. Schnitzler,
A. Denzinger
, Auditory fovea and Doppler shift compensation: Adaptations for flutter detection in echolocating bats using cf-fm signals. J. Comp. Physiol. A 197, 541–559 (2011).
OpenUrl CrossRef PubMed

[77] H.-U. Schnitzler,

[78] A. Denzinger

[79] ↵
H.-U. Schnitzler
, Control of Doppler shift compensation in the greater horseshoe bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 82, 79–92 (1973).
OpenUrl CrossRef

[80] H.-U. Schnitzler

[81] ↵
R. Müller,
H.-U. Schnitzler
, Acoustic flow perception in cf-bats: Properties of the available cues. J. Acoust. Soc. Am. 105, 2958–2966 (1999).
OpenUrl CrossRef PubMed

[82] R. Müller,

[83] H.-U. Schnitzler

[84] ↵
V. A. Walker,
H. Peremans,
J. C. T. Hallam
, One tone, two ears, three dimensions: A robotic investigation of pinnae movements used by rhinolophid and hipposiderid bats. J. Acoust. Soc. Am. 104, 569–579 (1998).
OpenUrl CrossRef PubMed

[85] V. A. Walker,

[86] H. Peremans,

[87] J. C. T. Hallam

[88] ↵
A. K. Gupta,
D. Webster,
R. Müller
, Entropy analysis of frequency and shape change in horseshoe bat biosonar. Phys. Rev. E 97, 062402 (2018).
OpenUrl

[89] A. K. Gupta,

[90] D. Webster,

[91] R. Müller

[92] ↵
J. Y. Bouguet,
P. Perona
, Camera calibration from points and lines in dual-space geometry (1998). https://pdfs.semanticscholar.org/df4e/24c7b651beeb4d8b34e7de302cf4f869ef49.pdf. Accessed 13 May 2019.

[93] J. Y. Bouguet,

[94] P. Perona

[95] ↵
J. F. Hughes
, Computer Graphics: Principles and Practice (Addison-Wesley, Upper Saddle River, NJ, ed. 3, 2014).

[96] J. F. Hughes

[97] ↵
K.-G. Heller,
O. v. Helversen
, Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia 80, 178–186 (1989).
OpenUrl CrossRef

[98] K.-G. Heller,

[99] O. v. Helversen

[100] ↵
G. Schuller
, Echo delay and overlap with emitted orientation sounds and Doppler-shift compensation in the bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 114, 103–114 (1977).
OpenUrl CrossRef

[101] G. Schuller

Main menu

User menu

Search

Fast-moving bat ears create informative Doppler shifts

Significance

Abstract

Results

Discussion