Bat Ears Research Articles

Reconstructing the acoustic scenes encountered by free-flying, foraging bats

Aerial insectivorous bats face the challenge of efficient echo scene analysis for localizing obstacles and capturing prey in flight. Data collected with a telemetry microphone mounted on the foraging bat's head provide a valuable opportunity to reconstruct acoustic scenes comprised of echoes returning to the bat's ears. This study explores the information embedded in echoes from a tethered insect and background clutter recorded by the telemetry microphone in laboratory experiments. Using images from high-speed video cameras and recordings from a far-field microphone array, angular information about different objects in the echoes are restored by assimilating the reconstructed bat's position and echolocation beam aim with respect to the objects along its flight trajectory toward prey capture. This procedure is further augmented by theoretical simulations using acoustic scattering principles to circumvent the limitation imposed by the sensitivity and signal-to-noise ratio of the telemetry microphone. The reconstructed acoustic scenes offer an avenue for detailed analysis of important cues for figure-ground separation in a cluttered environment, and serve as a basis for subsequent neurocomputational modeling of auditory scene analysis performed by the bat's sonar receiver.

English

Auditory neuropathy is a hearing disorder in which sound enters into the inner ear normally but the transmission of signals from the inner ear to auditory cortex is impaired due to the poor brain development. We report a case of 7 year male child presented with hard of hearing, deformed both external ears and inability to speak since birth. On examination bilateral bat ears , accessory auricles, hypertelorism, hyperactive attention deficit and from auditory brainstem response and otoacoustic emission reports it is diagnosed as auditory neuropathy and associated with various forms which is not included in ENT syndromes till date.

Evaluation of Strategies for the Decontamination of Equipment for Geomyces destructans, the Causative Agent of the White-Nose Syndrome (WNS)

White-nose syndrome is an emerging infectious disease that has led to a dramatic decline in cave-hibernating bat species. White-nose syndrome is caused by the newly described fungal pathogen Geomyces destructans, which infects the ear, muzzle, and wing membranes of bats. Although the exact mechanism by which the fungus causes death is not yet understood, G. destructans leads to a high mortality rate in infected animals. While the primary mechanism of infection appears to be bat-to-bat transfer, it is still unclear what role human activity may play in the spread of this pathogen. Here we evaluate the effectiveness of decontamination protocols that can be utilized by speleologists to reduce the likelihood of spreading this dangerous pathogen to naive bats or uninfected hibernacula. Our results show that pre-cleaning to remove muds and/ or sediments followed by the use of commercially available disinfectants can effectively remove G. destructans from caving fabrics. Alternatively, immersion in water above 50 uC for at least 20 minutes effectively destroys the fungal spores. These results have allowed the development of a decontamination protocol (http://www.fws.gov/ WhiteNoseSyndrome/cavers.html) that, when appropriately followed, can greatly reduce the likelihood of the human mediated transfer of G. destructans from an infected to uninfected site.

Characterization of the time-variant behavior of a biomimetic beamforming baffle

Horseshoe bats can actively change the shapes of their noseleaves and outer ears on time scales that are comparable to the duration of the biosonar pulses and echoes. When the shape deformations and the emission or reception of the ultrasonic signals overlap in time, the result is a time-variant diffraction process. Such a dynamic process provides additional flexibility that could potentially be used to enhance the encoding of sensory information. However, such a function remains hypothetical at present. To investigate the time-variant properties of deforming baffles such as the outer ears of horseshoe bats, the acoustic behavior of a biomimetic microphone baffle modeled on these biological structures has been investigated. The methods employed to characterize this device included representations in the time-delay domain as well as in the time-frequency domain. It was found that characterization methods which do not employ Fourier transforms revealed even more substantial time-variant effects than were apparent from time-frequency domain characterizations such as beampatterns obtained for different times in the deformation cycle. Furthermore, conspicuous correlates of asymmetries in the time-variant physical shapes were found in some characterizations that could be used to link dynamic baffle geometry with acoustic behavior.

Range dependent characteristics in the head-related transfer functions of a bat-head cast: part 1. Monaural characteristics

Knowledge of biological sonar systems has revolutionized many aspects of sonar engineering and further advances will benefit from more detailed understanding of their underlying acoustical processes. The anatomically diverse, complex and dynamic heads and ears of bats are known to be important for echolocation although their range-dependent properties are not well understood, particularly across the wide frequency range of some bats' vocalizations. The aim of this and a companion paper Kim et al (2012 Bioinspir. Biomim.) is to investigate bat-head acoustics as a function of bat-target distance, based on measurements up to 100 kHz and more robust examination of hardware characteristics in measurements than previously reported, using a cast of a bat head. In this first paper, we consider the spectral features at either ear (i.e. monaural head-related transfer functions). The results show, for example, that there is both higher magnitude and a stronger effect of distance at close range at relatively low frequencies. This might explain, at least in part, why bats adopt a strategy of changing the frequency range of their vocalizations while approaching a target. There is also potential advantage in the design of bio-inspired receivers of using range-dependent HRTFs and utilizing their distinguished frequency characteristics over the distance.

Design of a dynamic sensor inspired by bat ears

In bats, the outer ear shapes act as beamforming baffles that create a spatial sensitivity pattern for the reception of the biosonar signals. Whereas technical receivers for wave-based signals usually have rigid geometries, the outer ears of some bat species, such as horseshoe bats, can undergo non-rigid deformations as a result of muscular actuation. It is hypothesized that these deformations provide the animals with a mechanism to adapt their spatial hearing sensitivity on short, sub-second time scales. This biological approach could be of interest to engineering as an inspiration for the design of beamforming devices that combine flexibility with parsimonious implementation. To explore this possibility, a biomimetic dynamic baffle was designed based on a simple shape overall geometry based on an average bat ear. This shape was augmented with three different biomimetic local shape features, a ridge on its exposed surface as well as a flap and an incision along its rim. Dynamic non-rigid deformations of the shape were accomplished through a simple actuation mechanism based on linear actuation inserted at a single point. Despite its simplicity, the prototype device was able to reproduce the dynamic functional characteristics that have been predicted for its biological paragon in a qualitative fashion.

Comparing Aerodynamic Efficiency in Birds and Bats Suggests Better Flight Performance in Birds

Flight is one of the energetically most costly activities in the animal kingdom, suggesting that natural selection should work to optimize flight performance. The similar size and flight speed of birds and bats may therefore suggest convergent aerodynamic performance; alternatively, flight performance could be restricted by phylogenetic constraints. We test which of these scenarios fit to two measures of aerodynamic flight efficiency in two passerine bird species and two New World leaf-nosed bat species. Using time-resolved particle image velocimetry measurements of the wake of the animals flying in a wind tunnel, we derived the span efficiency, a metric for the efficiency of generating lift, and the lift-to-drag ratio, a metric for mechanical energetic flight efficiency. We show that the birds significantly outperform the bats in both metrics, which we ascribe to variation in aerodynamic function of body and wing upstroke: Bird bodies generated relatively more lift than bat bodies, resulting in a more uniform spanwise lift distribution and higher span efficiency. A likely explanation would be that the bat ears and nose leaf, associated with echolocation, disturb the flow over the body. During the upstroke, the birds retract their wings to make them aerodynamically inactive, while the membranous bat wings generate thrust and negative lift. Despite the differences in performance, the wake morphology of both birds and bats resemble the optimal wake for their respective lift-to-drag ratio regimes. This suggests that evolution has optimized performance relative to the respective conditions of birds and bats, but that maximum performance is possibly limited by phylogenetic constraints. Although ecological differences between birds and bats are subjected to many conspiring variables, the different aerodynamic flight efficiency for the bird and bat species studied here may help explain why birds typically fly faster, migrate more frequently and migrate longer distances than bats.

Identification of sound-localization cues in the HRTF of the bat-head model

Animals such as bats and dolphins exhibit impressive echolocation abilities in terms of ranging, resolution and imaging and therefore represent a valuable learning model for the study of spatial hearing and sound source localization leading to a better understanding of the hearing mechanism and further improvement of the existing localization strategies. This study aims to examine and understand the directional characteristics of a sonar receiver modeled upon the bat auditory system via measurements of the head-related transfer function (HRTF) in the horizontal plane. Four different models of the bat head were considered here and used to evaluate acoustic spectral characteristics of the sound received by the bat's ears – a sphere model, a sphere model with a pinna attached (two pinnae of different size were used in this study) and a bat-head cast. The performed HRTF measurements of the bat-head models were further analyzed and compared to identify monaural spectral localization cues in the horizontal plane defined by the bat's head and pinna shape and size. Our study suggests that the acoustical characteristics of a bio-inspired sonar head measured and specified in advance can potentially improve the performance of a receiver. Moreover, the generated auditory models may hold clues for the design of receiver characteristics in ultrasound imaging and navigation systems.

Directional properties of bat ears for target localization

Among several bat acoustic capabilities, it is reported that the error they show in discriminating the direction of a target in the elevation plane is within a few degrees. Many researchers have investigated bat echolocation and attempted to explain which features their accuracy relies on. Some works have pointed out the importance of beam patterns associated to the ears of the bats: indeed, ear shapes are very complex and different across species. This allows bats to significantly discriminate among the directions the echoes of their calls come from. Also, binaural cues for sound localization have been found to be determinant for some bat species. A method to estimate target orientation based on the beam patterns of the receivers and their binaural geometric relationship is developed for a sonar system emulating bats echolocation: a broadband signal is produced in the ultrasonic range and the echoes are collected by two receivers. The location of the target with respect to the bat is given by spherical coordinates including the distance from the bat and the orientation (defined by azimuth and elevation angles). While distance of the target from the sonar system is recovered through the time from the emission to the reception of the signal, the orientation is estimated from knowledge of the beam profiles of the receivers. The ratios between received and original signals’ spectra are calculated for the left and the right receiver across frequencies after compensating for distance effects. Orientations ensuring attenuation values in the beam patterns closest to the ratios are selected. Among these, one orientation for the left receiver and one for the right, fulfilling appropriate mutual geometric relations given by the geometry of the situation, are selected, these two defining the direction of the signal echo. The beam patterns associated to the left and the right ear of the Phyllostomus discolor bat are used within a limited range of orientations. A model of the emission of the signal and its reception is simulated for a set of target orientations spanning the beam pattern domain. Additionally, several noise levels are considered. Estimates of directions of the echoes are performed and the error for each of them with respect to the true orientation is calculated. Most error values are comparable to those reported in the literature and associated to some bat species. The beam patterns have very irregular shapes over the set of orientations that change with the frequency range: indeed, the accuracy of the method in estimating the true orientation depends on the choice of the frequency range and on the area of orientations over which the beam pattern is defined. This approach makes it possible to investigate which acoustic features ensure good orientation estimates in order to explain why bats have such complex beam patterns filtering the echoes. As this method relies only on knowledge of the receivers’ beam patterns and geometric relations based on the binaural configuration, it appears feasible that bats utilise this effect.

Bats’ avoidance of real and virtual objects: Implications for the sonar coding of object size

Fast movement in complex environments requires the controlled evasion of obstacles. Sonar-based obstacle evasion involves analysing the acoustic features of object-echoes (e.g., echo amplitude) that correlate with this object's physical features (e.g., object size). Here, we investigated sonar-based obstacle evasion in bats emerging in groups from their day roost. Using video-recordings, we first show that the bats evaded a small real object (ultrasonic loudspeaker) despite the familiar flight situation. Secondly, we studied the sonar coding of object size by adding a larger virtual object. The virtual object echo was generated by real-time convolution of the bats' calls with the acoustic impulse response of a large spherical disc and played from the loudspeaker. Contrary to the real object, the virtual object did not elicit evasive flight, despite the spectro-temporal similarity of real and virtual object echoes. Yet, their spatial echo features differ: virtual object echoes lack the spread of angles of incidence from which the echoes of large objects arrive at a bat's ears (sonar aperture). We hypothesise that this mismatch of spectro-temporal and spatial echo features caused the lack of virtual object evasion and suggest that the sonar aperture of object echoscapes contributes to the sonar coding of object size.

The Sonar Aperture and Its Neural Representation in Bats

As opposed to visual imaging, biosonar imaging of spatial object properties represents a challenge for the auditory system because its sensory epithelium is not arranged along space axes. For echolocating bats, object width is encoded by the amplitude of its echo (echo intensity) but also by the naturally covarying spread of angles of incidence from which the echoes impinge on the bat's ears (sonar aperture). It is unclear whether bats use the echo intensity and/or the sonar aperture to estimate an object's width. We addressed this question in a combined psychophysical and electrophysiological approach. In three virtual-object playback experiments, bats of the species Phyllostomus discolor had to discriminate simple reflections of their own echolocation calls differing in echo intensity, sonar aperture, or both. Discrimination performance for objects with physically correct covariation of sonar aperture and echo intensity ("object width") did not differ from discrimination performances when only the sonar aperture was varied. Thus, the bats were able to detect changes in object width in the absence of intensity cues. The psychophysical results are reflected in the responses of a population of units in the auditory midbrain and cortex that responded strongest to echoes from objects with a specific sonar aperture, regardless of variations in echo intensity. Neurometric functions obtained from cortical units encoding the sonar aperture are sufficient to explain the behavioral performance of the bats. These current data show that the sonar aperture is a behaviorally relevant and reliably encoded cue for object size in bat sonar.

An association between ear and tail morphologies of bats and their foraging style

Most studies relating bat morphology to flight ecology have concentrated on the wing membrane. Here, canonical variance analysis showed that the ear and tail morphologies of bats also strongly relate to foraging strategy, which in turn is correlated with flight style. Variations in tail membrane morphology are likely to be a trade-off between increases in the mechanical cost of flight and improvements in foraging and flight performance. Flying with large ears is also potentially energetically expensive, particularly at high flight speeds. Large ears, therefore, are only likely to be affordable for slow foraging gleaning bat species. Bats with faster foraging flight styles tend to have smaller ears, possibly to cut the overall drag produced and reduce the power required for flight. Variations in the size of ears and tail membranes appear to be driven primarily by foraging strategy and not by body size, because the scaling relationships found are either weak or not significant. Ear size in bats may be a result of a trade-off between acoustic and aerodynamic performance.

A digital model for the deformation of bat ears.

In bats, the directivity patterns of the biosonar system are shaped by the surface geometry of the pinnae. Since many bat species are capable of large ear deformations, these beampatterns can be time-variant. To investigate this time-variance using numerical methods, a digital model that is capable of representing the pinna geometry during the entire deformation cycle has been developed. Due to large deformations and occlusions, some of the surfaces relevant to sound diffraction may not be visible and hence the geometry of the entire pinna has to be computed from limited data. This has been achieved by combining a complete digital model of the pinna in one position with time-variant sparse sets of three dimensional landmark data. The landmark positions were estimated using stereo vision methods. A finite element model based on elasticity was constructed from CT scans of the pinna post mortem. This elastic model was deformed to provide a good fit to the positions of the landmarks and retain values of smoothness and surface energy comparable to life. This model was able to handle ratios of data to degrees of freedom around 1:5000 and still effect life-like deformations with an acceptable goodness of fit.

A method for analyzing the biodiversity in bat pinnae.

The pinnae of bats show conspicuous interspecific variability in global as well as in local shape features. Evidence from case studies suggests that at least some of these features may serve acoustic functions. Consequently, the variability in pinna shapes may represent evolutionary adaptation patterns to a range of different acoustic sensing tasks. An automated non-parametric method has been developed to extract these patterns from the biodiversity in pinna shapes. It allows the computation of three-dimensional principal components, eigenears, from high-resolution digital representations of the entire pinna surface. To achieve this, the inner and outer pinna surfaces that diffract incoming sound and thereby define the pinna’s acoustic properties have been subjected to a cylindrical transformation. The radius values of discrete points on the pinna’s surfaces have been taken to define members of a continuous valued vector space suitable for a principal component analysis. The results of the analysis show that the biodiversity in pinna shapes can be approximated well by a reduced number of dimensions that could be used to capture design trends. The natural global-to-local ordering of the eigenears can be used as a recipe to describe the sequential “design” of individual bat ears from a basic shape.

Case report of a new pathogenic variant of Aspergillus fumigatus isolated from Hipposideros cervinus (Chiroptera: Hipposideridae) in Sarawak, Malaysia

First record of new Aspergillus fumigatus variant (UNIMAS F009) was reported from the ears of bats at Kubah National Park, Borneo, Malaysia. Morphological characterization of this isolate showed some differences in terms of their growth rate, colony color, size of conidia and pigmentation on different media.

On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude

To understand complex sensory-motor behavior related to object perception by echolocating bats, precise measurements are needed for echoes that bats actually listen to during flight. Recordings of echolocation broadcasts were made from flying bats with a miniature light-weight microphone and radio transmitter (Telemike) set at the position of the bat's ears and carried during flights to a landing point on a wall. Telemike recordings confirm that flying horseshoe bats (Rhinolophus ferrumequinum nippon) adjust the frequency of their sonar broadcasts to compensate for echo Doppler shifts. Returning constant frequency echoes were maintained at the bat's reference frequency +/-83 Hz during flight, indicating that the bats compensated for frequency changes with an accuracy equivalent to that at rest. The flying bats simultaneously compensate for increases in echo amplitude as target range becomes shorter. Flying bats thus receive echoes with both stabilized frequencies and stabilized amplitudes. Although it is widely understood that Doppler-shift frequency compensation facilitates detection of fluttering insects, approaches to a landing do not involve fluttering objects. Combined frequency and amplitude compensation may instead be for optimization of successive frequency modulated echoes for target range estimation to control approach and landing.

Position as a cause of deformity in children with cerebral palsy (1976)

Deformities in the child with cerebral palsy have been ascribed to muscle imbalance (Sharrard 1961) and increased tone (Pollock 1959) or to the type of cerebral palsy (Bobath and Bobath 1975). As far as we know, the position in which the child is nursed, especially during the first year of life, has not been considered as a cause of deformity. It is generally agreed that position in the postnatal period can be a cause of deformity in the normal baby. Paine (1961) suggested that plagiocephaly was caused by postnatal head posture, and Hay (1971) found that plagiocephaly was present in 10 percent of normal babies. Scott (1956) reported that infants commonly had lateral curvatures of the spine which could be seen on x-rays but not on clinical examination, all of which had resolved by the age of two years. Other asymmetries associated with plagiocephaly are unilateral fisting, asymmetrical groin creases, apparent shortening of one lower limb and asymmetry of gait (Robson 1968). We accept the asymmetrical deformities of plagiocephaly, unilateral bat ear, facial and thoracic asymmetry, pelvic obliquity and apparent shortening of one leg--some or all of which may be present in normal babies--as forming the 'squint' baby syndrome. Because asymmetrical deformities also occur in children with cerebral palsy, we thought it worthwhile to compare the pattern of deformity in a group of 'quint' but otherwise normal babies with a group of cerebralpalsied children with asymmetrical deformities to see if there is any relationship.

Optimization of the characteristics of receiving echoes by free-flying echolocating bats, revealed by onboard pulse-echo recordings

To understand complex sensory-motor behavior underlying echolocation by bats, we need to precisely measure acoustic characteristics of echoes that the bats actually listen to during flight. However, it has been technically-difficult to develop a small and light enough microphone set at the position of the bat's ear, and information about the echoes is so far virtually lacked. Here, we have successfully monitored these returning echoes by means of an onboard telemetry microphone mounted on the bats, and we confirmed that the free-flying horseshoe bats compensated for Doppler-shifts by adjusting their call frequency, thus maintaining the echo frequency at constant. Furthermore, we found that the bats also adjusted pulse amplitude with the distance to maintain the echo intensity within the narrow range. Receiving echoes with stable amplitude could help the bats to sustain consistent analysis of successive echoes, and combined frequency and amplitude compensation may be for optimization of successive echoes for target range estimation to control approach and landing. [Supported by a grant to RCAST at Doshisha Univ. from MEXT of Japan: Special Research Grants for the Development of Characteristic Education from the Promotion and Mutual Aid Corporation for Private Schools of Japan and the Innovative Cluster Creation Project.]

The simulation of bat-oriented auditory processing using the experimental data of echolocating signals

There are various approaches to understanding the echolocation phenomenon of bats. A part of the echolocating process is assessed here by determining what acoustic signal a bat's ears receive during echolocation. It is simplified in an experimental rig to measure the reflections from objects in different horizontal angles which represents a sound localisation task in bats. It has been assumed in this study that the remarkable echolocating ability of bats, which is not shown in the most other mammalian species, is achieved by their different physical shape of head and ears, and specialised auditory processing of echolocating signals. In human studies in terms of sound localisation, physical characteristics are usually modelled as a head-related transfer function (or HRTF) and gammatone filter banks are widely used to simulate auditory processing in the cochlear. A modified filterbank is used here to represent the auditory processing in bats and combined with the experimental data of object reflections. Bat HRTFs will be used subsequently to determine the acoustic reflections at both ears.

`Binaural echo disparity' as a potential indicator of object orientation and cue for object recognition in echolocating nectar-feeding bats

Echolocating bats emit ultrasonic calls through their mouth or their nostrils and receive echoes from objects with both their ears. Information conveyed in the echoes is the basis for their three-dimensional acoustic perception of the surroundings. The direction of an object is encoded in binaural echo differences, i.e. on the one hand in the different arrival times of its echo at the two ears, and on the other hand in spectral differences through direction-dependent frequency filtering of head and pinnae. Insufficient attention has been paid, however, to the fact that three-dimensional objects produce structured spatial echo fields, and that the position of the ear in this field determines the echo it receives. We were interested to determine whether the two ears, in addition to direction-specific echo differences, receive object-specific echo disparities that might be useful for the bat. Our measurements with an artificial bat head, which consisted of two microphones and a small ultrasound loudspeaker arranged to resemble a bat's ears and mouth, revealed that echoes at the two ears differed largely depending on the shape and orientation of the echo-giving object. Binaural echo disparities of a bat-pollinated flower did indeed carry information about the orientation and, to a lesser extent, the shape of the flower. During flower approach such object-specific binaural echo disparities even exceed the binaural differences encoding direction of echo incidence, because the echo from the flower in front undergoes the same directional filtering by the two symmetrical ears. Nectar-feeding bats could use these object-specific binaural echo disparities not only to determine the object's orientation relative to the approaching bat, facilitating flight planning, but also to improve object recognition through spatial reconstruction of details of the object creating the echo. Our results suggest that the evaluation of binaural echo disparity has a greater importance for these tasks than has previously been assumed.