Horseshoe and Old World leaf-nosed bats have two discrete types of pinna motions Xiaoyan YinPeiwen QiuLili YangRolf Müller

Citation: The Journal of the Acoustical Society of America 141, 3011 (2017); doi: 10.1121/1.4982042 View online: http://dx.doi.org/10.1121/1.4982042 View Table of Contents: http://asa.scitation.org/toc/jas/141/5 Published by the Acoustical Society of America

Articles you may be interested in Measurement of low-frequency tissue response of the seagrass Posidonia oceanica The Journal of the Acoustical Society of America 141, (2017); 10.1121/1.4981925

Three-dimensional sonar beam-width expansion by Japanese house bats (Pipistrellus abramus) during natural foraging The Journal of the Acoustical Society of America 141, (2017); 10.1121/1.4981934 Horseshoe bats and Old World leaf-nosed bats have two discrete types of pinna motions

Xiaoyan Yin Shandong University–Virginia Tech International Laboratory, 27 Shanda South Road, Jinan, Shandong 250100, People’s Republic of Peiwen Qiu Department of Mechanical Engineering, 1075 Life Science Circle, Virginia Tech, Blacksburg, Virginia 24061, USA Lili Yang Shandong University–Virginia Tech International Laboratory, 27 Shanda South Road, Jinan, Shandong 250100, People’s Republic of China Rolf Muller€ a) Department of Mechanical Engineering, 1075 Life Science Circle, Virginia Tech, Blacksburg, Virginia 24061, USA (Received 5 December 2016; revised 3 March 2017; accepted 10 April 2017; published online 2 May 2017) Horseshoe bats (Rhinolophidae) and the related Old World leaf-nosed bats () both show conspicuous pinna motions as part of their biosonar behaviors. In the current work, the kine- matics of these motions in one species from each family (Rhinolophus ferrumequinum and armiger) has been analyzed quantitatively using three-dimensional tracking of land- marks placed on the pinna. The pinna motions that were observed in both species fell into two cate- gories: In “rigid rotations” motions the geometry of the pinna was preserved and only its orientation in space was altered. In “open–close motions” the geometry of the pinna was changed which was evident in a change of the distances between the landmark points. A linear discriminant analysis showed that motions from both categories could be separated without any overlap in the analyzed data set. Hence, bats from both species have two separate types of pinna motions with apparently no transitions between them. The deformations associated with open–close pinna motions in Hipposideros armiger were found to be substantially larger compared to the wavelength associated with the largest pulse energy than in Rhinolophus ferrumequinum (137% vs 99%). The role of the two different motions in the biosonar behaviors of the remains to be determined. VC 2017 Acoustical Society of America.[http://dx.doi.org/10.1121/1.4982042] [AMS] Pages: 3011–3017

I. INTRODUCTION in the biosonar systems of rhinolophid and hipposiderid bats goes beyond this well-known control mechanism and Horseshoe bats (rhinolophids, Rhinolophidae) and Old extends to the interfaces of ultrasound emission and recep- World leaf-nosed bats (hipposiderids, Hipposideridae) are tion. Species in both families emit their biosonar pulses two closely related bat families1 noted for their highly capa- nasally. It has been shown that the noseleaves, baffle shapes ble biosonar systems that allow these animals to navigate that surround the nostrils in species of both groups, can and hunt in acoustically difficult, cluttered environments change their geometry while diffracting the outgoing such as dense vegetation.2,3 One aspect that makes the bioso- pulses.8,9 Changes similar to what has been observed in the nar systems of rhinolophids and hipposiderids unique is a bats have been predicted to have an impact on the ultrasonic pervasive dynamics.4 For example, bats of both families emission characteristics by numerical simulations9,10 as well have been shown to dynamically control the carrier fre- as through experiments with biomimetic prototypes.11 quency of their sonar pulses to compensate for Doppler Furthermore, horseshoe bats have been shown to change the shifts due to their own flight motion.2,5,6 This dynamic con- widths of their biosonar beams,12 but the underlying mecha- trol enables the detection of Doppler shifts induced by the nism remains to be determined. wing motion of an insect prey and hence allows the bats to Similarly, it has been known for more than 50 years that distinguish the insect targets from vegetation clutter as well rhinolophids as well as hipposiderids have highly differenti- as classifying different insect prey.7 However, the dynamics ated ear muscles13,14 and can carry out ear motions during biosonar behaviors.15–17 First attempts at understanding the potential function of the pinna motions in rhinolophids and a)Also at: Shandong University–Virginia Tech International Laboratory, 27 Shanda South Road, Jinan, Shandong 250100, People’s Republic of China. hipposiderids have focused on representing the motion as Electronic mail: [email protected] rigid rotations that change the orientation of a time-invariant

J. Acoust. Soc. Am. 141 (5), May 2017 0001-4966/2017/141(5)/3011/7/$30.00 VC 2017 Acoustical Society of America 3011 device characteristic (beampattern).18 By scanning a time- ferrumequinum,23 pinna length 2.2 cm,24 Fig. 1(b) and eight invariant sonar beam across a target, the bat would be able to were great Himalayan leaf-nosed bats [Hipposideros armi- determine the direction of a target. Such a mechanism could ger,25 seven males and one female, pinna length 3.3 cm,24 explain the experimental finding that horseshoe bats that had Fig. 1(a)]. The rhinolophids were obtained from a cave near their pinna motions disabled performed less well when Jinan, Shandong province and the hipposiderids from caves in avoiding obstacles spaced in elevation.19 However, it has two regions in southern China, in the vicinity of Sanming been demonstrated that the pinna motions in horseshoe bats city, Fujian province, and Suiyang city, Guizhou province. can be non-rigid and result in noticeable changes to the The bats were housed in indoor flight rooms (separated by geometry of the pinna.20 The magnitude of the non-rigid genus) that provided a controlled environment with constant shape changes has been shown to be similar to the ultrasonic temperature (23 C) and humidity (60%). The bats were fed a wavelengths.20 Furthermore, experiments with physical real- diet of mealworms and were provided bottled water ad izations of biomimetic deforming microphone baffles have libitum. demonstrated that non-rigid motions of similar magnitude Quantitative characterizations of the pinna motions and geometry can result in time-variant receiver were obtained based on three-dimensional reconstructions of characteristics.21,22 the positions of discrete landmark points (Fig. 1). The land- At the time of writing, the authors are aware of only a mark points were placed on the bats using a green, nontoxic single published data set on the non-rigid pinna motions in dye before the experiments and removed immediately after rhinolophids20 and no published data on the non-rigid pinna the end of each experiment. For each experiment, approxi- motions in hipposiderids appear to be available. It remains mately 60 distinct landmark points were distributed over the unclear whether all rhinolophid/hipposiderid bat pinna pinna surface with an emphasis on coverage of the pinna motions have a substantial non-rigid component or whether rim. Five to seven additional landmark points each were mostly rigid motions are also part of the animals’ repertoire. placed on the top of the head and the noseleaf of each Hence, the goal of the present work has been to investigate to provide an anatomical frame of reference for the pinna quantitatively which part of the range spanned by entirely motions. During the experiments, the bat was placed on a rigid and strongly non-rigid motions is occupied by the pin- platform consisting of a piece of planar wire-mesh grid that nae motions of rhinolophid and hipposiderid bats. If motions was sloping downwards with a 45 angle relative to the hori- from near both ends of this spectrum can be found, are rigid zontal. On this platform, the bat was positioned in the center and non-rigid pinna motion patterns discrete categories or of the setup (Fig. 2) and at a distance of about 50 cm from extremes of a continuum? Finally, do pinna motions in rhi- the high-speed video cameras that were used to record the nolophid and hipposiderid bats follow the same patterns or pinna motions. are there differences between these two families? To answer While the bat was on the platform, it was attempted to these questions, three-dimensional motion trajectories for a attract the animal’s attention with a rotating propeller (diam- dense set of landmarks placed on the pinnae of rhinolophid eter 9 cm, variable rotation speeds between 10 and 80 revo- and hipposiderid bats have been obtained using a high-speed lutions per second) that was designed to mimic the wing stereo vision approach. The resulting landmark data have been analyzed quantitatively yielding a metric that was used to characterize pinna motions as rigid or non-rigid.

II. METHODS Pinna motion patterns were observed qualitatively or quantitatively in a study group that comprised a total of 15 individual bats. These animals belonged to two different spe- cies: seven greater horseshoe bats (Rhinolophus

FIG. 2. Experimental setup: The three-dimensional motion trajectories of the landmarks on the pinnae were determined with an array of four high- speed video cameras. The echo returns were registered with a horizontal and a vertical microphone array. All cameras and microphones were triggered FIG. 1. Individuals from the two bat species for which the pinna motions simultaneously. Illumination was provided by six sets of light emitting diode were studied: (a) (Hipposideros armiger), (b) greater (LED) lights. During the experiment, the bats were placed on a platform (Rhinolophus ferrumequinum). Both individuals have land- about 50 cm in front of the high-speed camera (close to the vantage point marks (paint spots) placed on noseleaf, pinnae, and head. from which this photo was taken and not visible in the image).

3012 J. Acoust. Soc. Am. 141 (5), May 2017 Yin et al. flutter of an insect prey. The propeller was held and moved were produced by eight individual bats, four greater horse- around over small distances in the vicinity of the high-speed shoe bats (Rhinolophus ferrumequinum), and four male great video cameras. Himalayan leaf-nosed bats (Hipposideros armiger). An addi- Video image sequences with views of the bats’ heads and tional 10 video recordings (5 s duration each) that contained the pinnae with the landmarks were captured using an array 919 identified pinna motions in total were used to perform a of four high-speed video cameras29 (GigaView; Southern manual qualitative characterization/classification of the Vision Systems Inc., Huntsville, AL) with Rodagon 50 mm motion patterns into rigid vs non-rigid motions to estimate lenses (Rodenstock, Feldkirchen, Germany). All cameras the frequency of occurrence for each pattern type. were operated with a frame rate of 400 Hz and a digital image To characterize the extent to which the different resolution of 1280 1024 pixels. At a typical position of the recorded pinna motions were rigid or non-rigid, a pairwise pinna, one image pixel corresponded to about 40 lm. The maximum-distance matrix between five landmark points captured images were in gray-scale format with 8-bit resolu- placed on the anterior rim and five points placed on the pos- tion per pixel. The high-speed cameras were calibrated to terior rim of the pinna was computed for each motion obtain estimates of their internal and external parameters sequence. For each pair of landmark points, the Euclidean based on calibration images of a checkerboard pattern. distance between the points was computed as a function of Estimation of the camera parameters was done exploiting the time over the entire duration of a pinna motion sequence geometrical relationships between planes, lines, and points (Fig. 3). The difference between the longest and the shortest in space (Camera Calibration Toolbox for Matlab, Mathworks 26 distance between the points in the pair that was observed Natick, MA ). Optical distortion of the video frames was over the duration of the motion sequence was entered into corrected using a radial distortion model and the images the maximum-distance matrix and used to characterize the obtained from cameras to be used for reconstruction of amount of non-rigid motion, i.e., deformation. The name the three-dimensional landmark coordinates were rectified “maximum-distance matrix” was used for this measure to onto a common image plane.26 The image coordinates of each emphasize that each entry in the matrix represents the maxi- landmark point were obtained for video frames from at least mum deformation that was registered for a given pinna two high-speed video cameras by manually picking the land- motion sequence. mark’s image location in the rectified video frames. The high- To answer the question whether the observed motions speed video cameras to be included in the stereo reconstruction fell into different categories and investigate the separation were selected manually based on how well they had captured between these categories, the data from the maximum- the landmark points during a given motion. Finally, the image distance matrices, i.e., the 25-dimensional vectors containing coordinates were used to reconstruct the three-dimensional all pairwise maximum differences, were hand-labeled as location of the landmarks points using stereo triangulation.26 “rigid” and “non-rigid” and then subjected to a linear discrim- A capacitive measurement microphone (1/8 in. pressure- inant analysis27 to test if a low-dimensional space can be field microphone, type 40 DP, with type AL0003 preamplifier, G.R.A.S. Sound & Vibration A/S, Holte, Denmark) was used to found where the two types of motion patterns are separate. record the echo returns at the position of the bats. The micro- phone was placed approximately 1 cm above the bat’s head. The microphone was calibrated with a sound level calibrator (type 4231, Bruel€ & Kjær, Nærum, Denmark) at 114 dB sound pressure level (SPL) and 1 kHz. The output signals of the microphone were digitized with 512 kHz sampling rate, 16 bits resolution, common-mode rejection ratio 75 dB, and total har- monic distortion 80 dB full-scale (PXIe-6358 data acquisition board mounted in a PXIe-1073 chassis, National Instruments, Austin, TX). Additional microphones (type 40 DP, G.R.A.S. Sound & Vibration A/S, Holte, Denmark and Momimic, Dodotronic, Castel Gandolfo, Italy) 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 control software (written in LabVIEW, National Instruments, Austin, TX). The control system produced a constant time offset of 16 ms between video and audio recordings that was compensated for during data analysis. Concurrent acquisition of video and audio data were triggered manually whenever the experimenter observed ear motions occurring in the experimental subject. FIG. 3. Trajectories of two pinna-rim points, one on the anterior rim (point Quantitative, in-depth analysis of the pinna motions was 2) and one on the posterior rim (point 10) over a time window of 32.5 ms based on a total of 10 video recordings (each with a duration (13 video frames). The distances between the points at each time step (video frame) are indicated by a double-headed arrow. For each sequence, the short of 5 s), from which 100 pinna motion sequences were ana- and longest distances between the points were identified and the difference lyzed qualitatively. The analyzed 100 motion sequences was used to quantify the amount of non-rigid motion (shape deformation).

J. Acoust. Soc. Am. 141 (5), May 2017 Yin et al. 3013 shape conformations. The alignment was carried out using the iterative closest point (ICP) method.28 The rotation angle was used as a measure for the rotation component of the pinna motion. After this rotation alignment, the root-mean-square (rms) distance between the corresponding points was used as a measure for the deformation component of the pinna shape.

III. RESULTS All bats tested in the experiments showed pinna motions. Spot checks conducted against the audio recordings indicated that pinna motions commonly overlap with the emitted pulses and the received echoes in time. Similar pinna motion patterns were found in both bat species (R. ferrumequinum and H. armiger). Upon qualitative inspection, these patterns appeared to fall into two different categories (Fig. 4). Patterns in the first category (“rigid motion”) caused only small changes to the distances between the points on the ante- rior and posterior rim [Figs. 5(a) and 5(b)]. In this category, the maximum changes to distances between these points did often not exceed one millimeter and were hence indistinguish- able from the measurement noise in many cases. FIG. 4. Typical examples of the observed pinna motions patterns in a great Patterns in the second category (“open-and-close roundleaf bat (Hipposideros armiger), the pinna position in three conditions: motion”) did result in noticeable changes to the distances (a) upright position of the pinna, (a) and (b) result of an “open-and-close” motion, (a)–(c) result of a rigid pinna motion. between the landmark points on the anterior and posterior pinna rims [Figs. 5(c) and 5(d)]. For motions in this cate- Finally, the motions were decomposed into their rigid and gory, the changes in distance were larger than one millimeter non-rigid components. This was done by virtue of a rotational and could reach up to one centimeter. These motions hence alignment of the point clouds given by the reconstructed three- led to a substantial changes in the size and geometry of the dimensional positions of the landmarks in different pinna pinna aperture.

FIG. 5. Examples of landmark motion trajectories associated with the two dif- ferent pinna motion types in a great roundleaf bat (Hipposideros armiger): (a) points labels on the pinna rim, the head, and the noseleaf (with numbers) in the first frame of a “rigid motion” video recording, (b) three-dimensional reconstructions of the trajectories of same points with the position of the pinna rim in the first frame shown for reference, the arrow indicates motion direction with time, (c) same as (a) but for the last frame in the recording of an “open-and-close” motion, (d) same as (b) but for the open-and-close motion example shown in (c).

3014 J. Acoust. Soc. Am. 141 (5), May 2017 Yin et al. FIG. 6. Examples of maximum- differences matrices for pinna motions observed in a great roundleaf bat (Hipposideros armiger): (a) and (c) position of the landmark points used (numbered 1 to 10) on the pinna, (b) and (d) corresponding maximum changes in distance for all point pairs (encoded by gray level). (a) and (b) Show an example of a “rigid motion” (c) and (d) and example of an “open- and-close” motion.

Whereas the maximum-distance matrices of rigid rhinolophids and the hipposiderids fall into two discrete cat- motions showed uniformly small values [Fig. 6(b)], matrices egories. For both species, a single dimension could be found belonging to open–close motions showed a pattern of large where the maximum-difference data for rigid and open–- values that were found between points positioned opposite close motions were completely separated [Fig. 7(a) and of each other on the anterior and posterior pinna rims with 7(b)]. Even if data from both species was pooled, a pro- points positions near the base and in the middle of the pinna nounced difference between motion patterns labeled as rigid showing larger maximum differences than points near the and open–close remained, albeit with some overlap between apex [Fig. 6(d)]. the two data sets [Fig. 7(c)]. The results of the linear discriminant analysis confirmed When each pinna motion was characterized by a rotation the qualitative observation that pinna motions in both the angle and an rms deformation, pinna motions that had been

FIG. 7. Linear discriminant analysis of the pinna motion patterns: distribution of the analyzed pinna motion samples (N ¼ 100) along the dimension of best separation found by the analysis: white bars: rigid rotation, gray bars: open- and-close motion. (a) Greater horse- shoe bats (Rhinolophus ferrumequi- num, N ¼ 50), (b) great Himalayan leaf-nosed bats (Hipposideros armiger, N ¼ 50), (c) pooled data from both species.

J. Acoust. Soc. Am. 141 (5), May 2017 Yin et al. 3015 IV. DISCUSSION The analysis of the three-dimensional pinna motions undertaken here has demonstrated that the hipposiderid and the rhinolophid species studied have pinna motions that fol- low very similar patterns. Hence, it may be hypothesized that these pinna motion patterns are a common derived fea- ture of both families and could be an integral part of the con- stant frequency–frequency modulated (cf–fm) biosonar system that these species share. With regard to a potential functional, i.e., acoustic sig- nificance, the current results underscore the substantial size of the non-rigid ear motion beyond what has been previously reported. In prior work, pinna deformation up to 15% of the pinna length in R. ferrumequinum had been found.20 For the same species, the data reported here show an average defor- mation amplitude of 25% of the pinna length. For H. armi- FIG. 8. Rotation and deformation components of the pinna motions: ger, the deformation amplitudes were even bigger relative to Maximum rotation angle (abscissa) and maximum rms difference between the landmark points (ordinate) during rigid rotation (open circles, N ¼ 19) the pinna length (30%) and the wavelength of the cf- and open-and-close motions (asterisks, N ¼ 17). All data shown in this graph components of the biosonar pulses (137%). This difference is from H. armiger. could be seen as an indication that non-rigid deformations could play an even greater role in the biosonar system of the manually assigned to the open–close type were again sepa- hipposiderids than is the case for Rhinolophus. rated from the rigid rotations by smaller rms deformations The major new insight from the current work lies in (Fig. 8). In terms of the magnitude of the rotation angles, the finding that open–close and non-rigid motions form pinna motions from both categories showed a large variabil- two separate categories in both of the studied bat families. ity with the rigid rotations in the sample involving larger Hence, the animals seem to switch between two different rotation angles on average. The mean rotation angle was dynamic patterns, one (rigid rotation) that only changes 29.5 (611.4 standard deviation, N ¼ 19) for rigid rotations the orientation of the pinna but not its geometry and vs 22.0 (614.4 standard deviation, N ¼ 17) for open–close another that changes the pinna geometry and—in many motions. cases—its orientation as well. Pinna motions from both Despite the qualitative similarities between in the two categories could provide different views of a biosonar motion patterns across the two species, quantitative differ- scene. For the rigid rotations, these different views are cre- ences between the two analyzed species were found in the ated by changing the orientation of a beampattern that data (Table I). In general, the absolute values deformation remains otherwise constant with respect to the scene. For amplitudes of the open–close pinna motions were larger in the open–close pinna motions, the views are changed due H. armiger than in R. ferrumequinum (t-test, N ¼ 50, to a change in the geometry of the beampattern, i.e., the p ¼ 0.0027, Table I). However, since the pinnae of H. armi- space-frequency weighting imposed by the beampattern on ger are substantially larger than those of R. ferrumequinum a scene. In addition, the open–close motions were found (22.5 mm vs 17.7 mm, N ¼ 50.), the ratio of the deformation to be accompanied by rotations that ranged from very to the overall pinna length differed only slightly between small—and hence probably negligible—to very substantial species (30% in H. armiger vs 25.2% in R. ferrumequinum magnitudes. For the acoustic function of the bats’ sonar (p ¼ 0.183, Table I). When compared to the wavelength of systems, this means that the animals use either pure rigid the constant frequency (cf)-portion of the second harmonic rotations where a space-frequency weighting of constant of the animals biosonar pulses, the pinna deformations in H. shape is swept across the environment or they change the armiger were again found to be substantially larger than shape of their space-frequency filter, either with or without those in R. ferrumequinum (137% vs 99%) although still at a substantial re-orientations of the biosonar beam. lower significance level than for the absolute values Based on the laboratory data available here, it is impos- (p ¼ 0.0156). sible to make a prediction of how common each of the two

TABLE I. Summary statistics for the pinna motion amplitudes by motion type and species (N ¼ 100).

Open–close Rigid motion Open–close Rigid motion H. armiger H. armiger R. f R. f N ¼ 34 N ¼ 16 N ¼ 19 N ¼ 31

Maximum difference (mm) 6.8 6 2.40 1.9 6 0.84 4.5 6 2.94 0.9 6 0.26 Maximum difference/ear length (%) 30.3 6 0.11 8.4 6 0.04 25.2 6 0.17 4.9 6 0.01 Maximum difference/k (%) 136.5 6 0.49 38.9 6 0.17 98.7 6 0.60 19.4 6 0.06

3016 J. Acoust. Soc. Am. 141 (5), May 2017 Yin et al. categories would be in nature. In the studied laboratory sit- 12N. Matsuta, S. Hiryu, E. Fujioka, Y. Yamada, H. Riquimaroux, and Y. uations, it was fairly straightforward to elicit pinna motions Watanabe, “Adaptive beam-width control of echolocation sounds by CF–FM bats, Rhinolophus ferrumequinum nippon, during prey-capture from either category, which suggest the hypothesis that both flight,” J. Exp. Biol. 216(7), 1210–1218 (2013). open–close and rigid rotations are part of the natural reper- 13H. Schneider, “Die Ohrmuskulatur von tridens Geoffr. toire of the animals. However, it remains unknown whether (Hipposideridae) und Myotis myotis Borkh. (Vespertilionidae) (Chiroptera)” the two different pinna motion types are used in different [“The ear musculature of Asellia tridens Geoff. (Hipposideridae) and biosonar behaviors and what their functional significance in Myotis myotis Borkh. (Vespertilionidae) (Chiroptera)”], Zool. Jb., Abt. Anat. u. Ontog. 79, 93–122 (1961). these contexts may be. This question should be investigated 14H. Schneider and F. P. Mohres,€ “Die Ohrbewegungen der by observing the pinna motion patterns in bats that are free Hufeisennasenflederm€ause (Chiroptera, Rhinolophidae) und der to engage in natural biosonar behaviors. Mechanismus des Bildhorens”€ (“The ear motions of horseshoe bats (Chiroptera, Rhinolophidae) and the mechanism of image hearing”), Z. Vergl. Physiol. 44(1), 1–40 (1960). ACKNOWLEDGMENTS 15D. R. Griffin, D. C. Dunning, D. A. Cahlander, and F. A. Webster, The authors would like to thank Dr. Cindy Grimm for “Correlated orientation sounds and ear movements of horseshoe bats,” Nature 196, 1185–1188 (1962). help with the computational shape analysis and Mengna 16J. D. Pye, M. Flinn, and A. Pye, “Correlated orientation sounds and ear Zhang for help with the LDA method. This work was movements of horseshoe bats,” Nature 196, 1186–1188 (1962). supported through funding from the National Science 17J. D. Pye and L. H. Roberts, “Ear movements in a hipposiderid bat,” Foundation (NSF Grant No. ID 1362886) and the National Nature 225, 285–286 (1970). 18V. A. Walker, H. Peremans, and J. C. T. Hallam, “One tone, two ears, Natural Science Foundation of China (Grant Nos. 11374192, three dimensions: A robotic investigation of pinnae movements used by 11574183, 31270414-1), the Chinese Ministry of Education rhinolophid and hipposiderid bats,” J. Acoust. Soc. Am. 104(1), 569–579 (Tese Grant), and the Fundamental Research Fund of (1998). 19 Shandong University (No. 2014QY008). J. Mogdans, J. Ostwald, and H.-U. Schnitzler, “The role of pinna move- ment for the localization of vertical and horizontal wire obstacles in the

1 greater horseshoe bat, Rhinolopus ferrumequinum,” J. Acoust. Soc. Am. N. B. Simmons, “Order chiroptera,” in Species of the World: A 84(5), 1676–1679 (1988). Taxonomic and Geographic Reference, 3rd ed. (Johns Hopkins University 20L. Gao, S. Balakrishnan, W. He, Z. Yan, and R. Muller,€ “Ear deformations Press, Baltimore, MD, 2005), Vol. 1, pp. 312–529. 2 give bats a physical mechanism for fast adaptation of ultrasonic J. Habersetzer, G. Schuller, and G. Neuweiler, “Foraging behavior and beampatterns,” Phys. Rev. Lett. 107(21), 214301 (2011). Doppler shift compensation in echolocating hipposiderid bats, 21S. Z. Meymand, M. Pannala, and R. Muller,€ “Characterization of the time- Hipposideros bicolor and Hipposideros speoris,” J. Comp. Physiol. A variant behavior of a biomimetic beamforming baffle,” J. Acoust. Soc. 155(4), 559–567 (1984). Am. 133(2), 1141–1150 (2013). 3G. Neuweiler, W. Metzner, U. Heilmann, R. Rubsamen,€ M. Eckrich, and 22M. Pannala, S. Z. Meymand, and R. Muller,€ “Interplay of static and H. H. Costa, “Foraging behaviour and echolocation in the rufous horse- dynamic features in biomimetic smart ears,” Bioinspiration Biomimetics shoe bat (Rhinolophus rouxi) of Sri Lanka,” Behav. Ecol. Sociobiol. 20, 8(2), 026008 (2013). 53–67 (1987). 23R. Piraccini, The IUCN Red List of Threatened Species (International 4R. Muller,€ “Dynamics of biosonar systems in horseshoe bats,” Eur. Phys. Union for Conservation of Nature and Natural Resources, Cambridge, J.: Spec. Top. 224(17-18), 3393–3406 (2015). 5 UK, 2016), Chap. Rhinolophus ferrumequinum, p. e. T19517A21973253. S. Hiryu, K. Katsura, L. K. Lin, H. Riquimaroux, and Y. Watanabe, 24 “Doppler-shift compensation in the Taiwanese leaf-nosed bat H. Zhao, S. Zhang, M. Zuo, and J. Zhou, “Correlations between call fre- (Hipposideros terasensis) recorded with a telemetry microphone system quency and ear length in bats belonging to the families Rhinolophidae and Hipposideridae,” J. Zool. (London) 259(2), 189–195 (2003). during flight,” J. Acoust. Soc. Am. 118(6), 3927–3933 (2005). 25 6M. Trappe and H.-U. Schnitzler, “Doppler-shift compensation in insect- P. Bates, S. Bumrungsri, C. Francis, and G. Csorba, The IUCN Red List of catching horseshoe bats,” Naturwissenschaften 69(4), 193–194 (1982). Threatened Species (International Union for Conservation of Nature and 7R. Kober and H.-U. Schnitzler, “Information in sonar echoes of fluttering Natural Resources, Cambridge, UK, 2008), chapter Hipposideros armiger, insects available for echolocating bats,” J. Acoust. Soc. Am. 87, 882–896 p. e.T10110A3162617. 26 (1990). J. Y. Bouguet and P. Perona, “Camera calibration from points and lines in 8L. Feng, L. Gao, H. Lu, and R. Muller,€ “Noseleaf dynamics during pulse dual-space geometry,” in 5th European Conference on Computer Vision, emission in horseshoe bats,” PLoS One 7(5), e34685 (2012). Freiburg, Germany, 1998. 27 9W. He, S. Pedersen, A. K. Gupta, J. A. Simmons, and R. Muller,€ “Lancet A. J. Izenman, “Linear discriminant analysis,” in Springer Texts in dynamics in greater horseshoe bats, Rhinolophus ferrumequinum,” PLoS Statistics (Springer ScienceþBusiness Media, New York, 2013), pp. One 10(4), e0121700 (2015). 237–280. 10A. K. Gupta, D. Webster, and R. Muller,€ “Interplay of furrows and shape 28P. J. Besl and N. D. McKay, A Method for Registration of 3-D Shapes dynamics in the lancet of the horseshoe bat noseleaf,” J. Acoust. Soc. Am. (IEEE Computer Society, Washington, DC, 1992), Vol. 14, pp. 138(5), 3188–3194 (2015). 239–256. 11Y. Fu, P. Caspers, and R. Muller,€ “A dynamic ultrasonic emitter inspired 29See supplementary material at http://dx.doi.org/10.1121/1.4982042 for by horseshoe bat noseleaves,” Bioinspiration Biomimetics 11(3), 036007 high-speed video recordings showing examples of rigid rotation and (2016). open–close pinna motions.

J. Acoust. Soc. Am. 141 (5), May 2017 Yin et al. 3017