FM Bat Research Articles

Molecular adaptations underlying high-frequency hearing in the brain of CF bats species

BackgroundThe majority of bat species have developed remarkable echolocation ability, especially for the laryngeally echolocating bats along with high-frequency hearing. Adaptive evolution has been widely detected for the cochleae in the laryngeally echolocating bats, however, limited understanding for the brain which is the central to echolocation signal processing in the auditory perception system, the laryngeally echolocating bats brain may also undergo adaptive changes.ResultIn order to uncover the molecular adaptations related with high-frequency hearing in the brain of laryngeally echolocating bats, the genes expressed in the brain of Rhinolophus ferrumequinum (CF bat) and Myotis pilosus (FM bat) were both detected and also compared. A total of 346,891 genes were detected and the signal transduction mechanisms were annotated by the most abundant genes, followed by the transcription. In hence, there were 3,088 DEGs were found between the two bat brains, with 1,426 highly expressed in the brain of R. ferrumequinum, which were significantly enriched in the neuron and neurodevelopmental processes. Moreover, we found a key candidate hearing gene, ADCY1, playing an important role in the R. ferrumequinum brain and undergoing adaptive evolution in CF bats.ConclusionsOur study provides a new insight to the molecular bases of high-frequency hearing in two laryngeally echolocating bats brain and revealed different nervous system activities during auditory perception in the brain of CF bats.

Bats to belugas: Functional anatomy of air versus water biosonar

Acoustic task similarities of odontocetes (toothed whales) and microchiropterans (insectivorous bats) suggest they have common biosonar mechanisms. However, media differences; e.g., sound speeds in air versus water, may have driven variations in auditory system adaptations. We examined the peripheral auditory system of an FM bat (big brown bat Eptesicus fuscus) and two toothed whale species (harbor porpoise Phocoena phocoena; bottlenose dolphin Tursiops truncatu) using ultra high resolution (11 μm) isotropic voxel microCT. Significant differences were found among species for oval window location, cochlear length, basilar membrane gradients, cochlear spiral morphometry, cochlear curvature, and basilar membrane stiffness. High and low frequency hearing range cut-offs correlate with basilar membrane thickness/width ratios and cochlear radii of curvature. These features predict species specific high and low frequency hearing limits. Harbor porpoises, the highest frequency echolocator in the study, have large basal basilar membrane ratios and a “foveal” region with a constant membrane ratio similar to those reported for some bat species, consistent with a “stretched” frequency region. Furthermore, both the bats and harbor porpoises examined displayed unusual stapedial input locations and tightly coiled cochleae, specializations that may enhance ultrasonic frequency signal resolution and diminish low frequency cochlear propagation.

Echolocating Daubenton's bats call louder, but show no spectral jamming avoidance in response to bands of masking noise during a landing task.

Echolocating bats listen for weak echoes to navigate and hunt, which makes them prone to masking from background noise and jamming from other bats and prey. As for electrical fish that display clear spectral jamming avoidance responses (JAR), bats have been reported to mitigate the effects of jamming by shifting the spectral contents of their calls, thereby reducing acoustic interference to improve echo-to-noise ratio (ENR). Here, we tested the hypothesis that frequency-modulating bats (FM bats) employ a spectral JAR in response to six masking noise bands ranging from 15 to 90 kHz, by measuring the -3 dB endpoints and peak frequency of echolocation calls from five male Daubenton's bats (Myotis daubentonii) during a landing task. The bats were trained to land on a noise-generating spherical transducer surrounded by a star-shaped microphone array, allowing for acoustic localization and source parameter quantification of on-axis calls. We show that the bats did not employ spectral JAR as the peak frequency during jamming remained unaltered compared with that of silent controls (all P>0.05, 60.73±0.96 kHz, mean±s.e.m.), and -3 dB endpoints decreased in noise irrespective of treatment type. Instead, Daubenton's bats responded to acoustic jamming by increasing call amplitude via a Lombard response that was bandwidth dependent, ranging from a mean of 0.05dB/dB (95% confidence interval 0.04-0.06dB/dB) noise for the most narrowband noise (15-30 kHz) to 0.17dB/dB (0.16-0.18dB/dB) noise for the most broadband noise (30-90 kHz). We conclude that Daubenton's bats, despite having the vocal flexibility to do so, do not employ a spectral JAR, but defend ENRs via a bandwidth-dependent Lombard response.

Functional Analyses of Peripheral Auditory System Adaptations for Echolocation in Air vs. Water

The similarity of acoustic tasks performed by odontocete (toothed whale) and microchiropteran (insectivorous bat) biosonar suggests they may have common ultrasonic signal reception and processing mechanisms. However, there are also significant media and prey dependent differences, notably speed of sound and wavelengths in air vs. water, that may be reflected in adaptations in their auditory systems and peak spectra of out-going signals for similarly sized prey. We examined the anatomy of the peripheral auditory system of two species of FM bat (big brown bat Eptesicus fuscus; Japanese house bat Pipistrellus abramus) and two toothed whales (harbor porpoise Phocoena phocoena; bottlenose dolphin Tursiops truncatus) using ultra high resolution (11–100 micron) isotropic voxel computed tomography (helical and microCT). Significant differences were found for oval and round window location, cochlear length, basilar membrane gradients, neural distributions, cochlear spiral morphometry and curvature, and basilar membrane suspension distributions. Length correlates with body mass, not hearing ranges. High and low frequency hearing range cut-offs correlate with basilar membrane thickness/width ratios and the cochlear radius of curvature. These features are predictive of high and low frequency hearing limits in all ears examined. The ears of the harbor porpoise, the highest frequency echolocator in the study, had significantly greater stiffness, higher basal basilar membrane ratios, and bilateral bony support for 60% of the basilar membrane length. The porpoise’s basilar membrane includes a “foveal” region with “stretched” frequency representation and relatively constant membrane thickness/width ratio values similar to those reported for some bat species. Both species of bats and the harbor porpoise displayed unusual stapedial input locations and low ratios of cochlear radii, specializations that may enhance higher ultrasonic frequency signal resolution and deter low frequency cochlear propagation.

Flutter sensitivity in FM bats. Part II: amplitude modulation

Bats use echolocation to detect targets such as insect prey. The echolocation call of frequency-modulating bats (FM bats) typically sweeps through a broad range of frequencies within a few milliseconds. The large bandwidth grants the bat high spatial acuity in depicting the target. However, the extremely short call duration and the overall low duty cycle of call emission impair the bat’s capability to detect e.g. target movement. Nonetheless, FM bats constitute more than 80% of all echolocating species and are able to navigate and forage in an environment full of moving targets. We used an auditory virtual reality approach to generate changes in echo amplitude reflective of fluttering insect wings independently from other confounding parameters. We show that the FM bat Phyllostomus discolor successfully detected these modulations in echo amplitude and that their performance increased with the rate of the modulation, mimicking faster insect wing-beats. The ability of FM bats to detect amplitude modulations of echoes suggests a release from the trade-off between spatial and temporal acuity and highlights the diversity of selective pressures working on the echolocation system of bats.

Acoustic identification of five insectivorous bats by their echolocation calls in the Sahelian zone of Far North Cameroon

BackgroundDespite their abundance and ecological importance, bats are under significant threat worldwide. There is little information about their distribution, roosting, and habitat requirement for most species, making assessing which species is threatened or in need of special conservation measures difficult. The knowledge gap may partly be due to limitations of the old methods of studying bats which mainly involved capture/or observational techniques.Material and methodsIn order to evaluate the potential of identifying insectivorous bats by their echolocation calls in the Sahelian zone of northern Cameroon, 65 bats belonging to five species were captured using standard mist netting: Mops condylurus, Chaerephon major, Mops niveiventer, Scotophilus dinganii, and Scotophilus leucogaster. The bats were identified by using morphometric measurements. An Anabat SD1 detector was later used to record echolocation calls of each individual bat in flight after it was hand-released. The sonogram of each individual bat was analyzed using Analook and categorized into two call types (frequency modulation and frequency modulation/quasi constant frequency) in order to develop a library of bat reference calls that could be used for a qualitative acoustic survey and species identification. Discriminant function analysis (DFA) was applied to search phase calls of the 65 individual bats in order to evaluate the potential for classifying calls into five species groups. Seven parameters calculated from each search phase call were used to classify calls.ResultsBats where place into two groups according to the structure of calls: FM bats (Mops condylurus, Chaerephon major, Mops niveiventer) and FM/QCF bats (Scotophilus dinganii and Scotophilus leucogaster). The DFA resulted in a correct overall classification of 69.7%.ConclusionThis preliminary study showed that DFA of call parameters is a feasible method that can be used to identify insectivorous bats in the region by their echolocation calls.

Significance of terminal frequency in FM sweeps for bat echolocation

For echolocation of CF-FM bats, the CF component is expected to detect wing-beat of flying insects. However, it also plays an important role to serve as a stable signal carrier from a distant target. Then, once the carrier frequency is removed, echo signal can be easily detected. For this purpose, Doppler-shift compensation and echo amplitude compensation must be conducted to stabilize the signal carrier. What about the FM bats? FM bats also appear to utilize a relatively long pseudo-CF component to detect wing-beats of flying insects. They might also utilize pseudo-CF component for an echo signal carrier. However, Doppler-shift compensation in FM bats has not been reported. In the inferior colliculus, majority of neurons are tuned to the pseudo-CF frequency, 20 kHz for Eptesicus fuscus while 40 kHz for Pipistrellus abramus, which are corresponding to the terminal frequencies of downward FM sweep. Overrepresentation of a particular frequency may enhance frequency discrimination, detection of insect wing-beat. Therefore, we may expect majority of cochlear nerve fibers are also tuned to the pseudo-CF frequency. However, overrepresentation of hair cells for a particular frequency does not appear to be shown. [Research supported by MEXT, Japan and Shandong University, China.]

Rapid frequency control of sonar sounds by the FM bat, Miniopterus fuliginosus, in response to spectral overlap

In the presence of multiple flying conspecifics, echolocating bats avoid jamming by adjusting the spectral and/or temporal features of their vocalizations. However, little is known about how bats alter their pulse acoustic characteristics to adapt to an acoustically jamming situation during flight. We investigated echolocation behavior in a bat (Miniopterus fuliginosus) during free flight under acoustic jamming conditions created by downward FM jamming sounds mimicking bat echolocation sounds. In an experimental chamber, the flying bat was exposed to FM jamming sounds with different terminal frequencies (TFs) from loudspeakers. Echolocation pulses emitted by the flying bat were recorded using a telemetry microphone (Telemike) mounted on the back of the bat. The bats immediately (within 150ms) shifted the TFs of emitted pulses upward when FM jamming sounds were presented. Moreover, the amount of upward TF shift differed depending on the TF ranges of the jamming sounds presented. When the TF range was lower than or overlapped the bat’s mean TF, the bat TF shifted significantly upward (by 1–2kHz, Student’s t-test, P<0.05), corresponding to 3–5% of the total bandwidth of their emitted pulses. These findings indicate that bats actively avoid overlap of the narrow frequency band around the TF.

Three-dimensional sonar beam control of FM echolocating bats during natural foraging revealed by large scale microphone array system

In this study, 3-D flight paths and directivity pattern of the sounds emitted by Pipistrellus abramus during natural foraging were measured by a large scale microphone array system. The results show that the bats approached prey with covering the direction of them within their sonar beam. The means of horizontal and vertical beam widths were 49 deg and 46 deg, respectively. Just before capturing prey, the bats decreased the terminal frequency (TF) of the pulse. Simultaneously, the beam widths were expanded to 64 deg (horizontal) and 57 deg (vertical). We assumed a circular piston model to estimate how much the beam width was changed by decreasing the frequency of emitted pulse. It was found that the observed expansion of the beam width was smaller than those of theoretical estimations. This suggests that the bats decrease the TF of pulse for compensating their beam width narrowed by taking a large bite for the prey. We also measured echolocation calls and flight behavior of Myotis macrodactylus during natural foraging. M. macrodactylus uses FM echolocation pulse which is similar to P. abramus, but they forage for prey above the water surface. We compare echolocation strategies between two FM bats with different foraging habitat.

The cochlear size of bats and rodents derived from MRI images and histology.

From the evolutionary perspective, the ear of each animal species is built for effective processing of the biologically relevant signals used for communication and acoustically guided orientation. Because the sound pulses used by echolocating bats for orientation and rodents for communication are quite different, the basic design of the mammalian auditory system commonly shared by echolocating bats must be specialized in some manner to effectively process their species-specific sounds. The present study examines the difference in the cochlea of these animal species using MRI images and histological techniques. We report here that, although all these animal species share a similar cochlear structure, they vary in their cochlear size and turns. Bats using constant frequency-frequency-modulated pulses (CF-FM bats) and frequency-modulated pulses (FM bats) for echolocation have a larger cochlear size and more cochlear turns than rodents (mice and rats). However, CF-FM bats have the largest cochlear size and most cochlear turns. This difference in cochlear size and turns of these animal species is discussed in relation to their biologically relevant sounds and acoustic behavior.

Active enhancement found in responses of the cochlear nerve to detect weak echoes created by the auditory periphery in Japanese house bat, Pipistrelus abramus

Characteristics of frequency tunings related to echolocation were investigated in an FM bat, Japanese house bat (Pipistrellus abramus). A particular attention was paid on their terminal frequency of FM sweep. When search for preys in the field, they stretch duration of echolocation pulses and reduce FM sweeping range, resulting in pseudo constant frequency pulses. Distribution of best frequency in the neurons in the inferior colliculus indicated that about 50% of neurons appeared to be tuned to the pseudo constant frequency, around 40 kHz. The compound action potentials were recorded from medulla oblongata through a metal telectrode. We hypothesized that the bat has a peripheral system to enhance frequency component of 40 kHz to be detected easier than other frequency components. Active enhancement of 40 kHz frequency component by the outer hair cell and overwhelming number of cochlear nerves in charge of 40 kHz would create low threshold and high resolution sensitivity for frequency range around 40 kHz. ...

Segregation of ambiguous pulse-echo streams and suppression of clutter masking in FM bat sonar by anticorrelation signal processing

Big brown bats often fly in conditions where the density and spatial extent of clutter requires a high rate of pulse emissions. Echoes from one broadcast still are arriving when the next broadcast is sent out, creating ambiguity about matching echoes to corresponding broadcasts. Biosonar sounds are widely beamed and impinge on the entire surrounding scene. Numerous clutter echoes typically are received from different directions at similar times. The multitude of overlapping echoes and the occurrence of pulse-to-echo ambiguity compromises the bat’s ability to peer into the upcoming path and determine whether it is free of collision hazards. Bats have to associate echoes with their corresponding broadcasts to prevent ambiguity, and off-side clutter echoes have to be segregated from on-axis echoes that inform the bat about its immediate forward path. In general, auditory streaming to resolve elements of an auditory scene depends on differences in pitch and temporal pattern. Bats use a combination of temporal and spectral pitch to assign echoes to “target” and “clutter” categories within the scene, which prevents clutter masking, and they associate incoming echoes with the corresponding broadcast by treating the mismatch of echoes with the wrong broadcast as a type of clutter. [Supported by ONR.]

Investigation of acoustic gaze strategy by Pipistrellus abramus and Rhinolophus ferrumequinum Nippon during obstacle avoidance flight

We investigated the acoustic gaze (angle between pulse and flight directions) and the beam width of echolocation pulses emitted by bats during obstacle avoidance flight in a chamber (7×3×2 m). Echolocation pulses were recorded by a telemetry microphone mounted on the bat’s back and a horizontal 20-ch microphone array set up in the chamber. Flight path measurements were conducted using two high-speed video cameras. While the bat showed a circular flight avoiding the surrounding walls, the acoustic gaze showed significant linear correlation to the angular velocity of the flight. This means that the bat adjusted the pulse direction to precede its own flight direction. The correlation coefficient increased with complexity of obstacle conditions. We compared changes in acoustic gaze between FM bats (mean beam width: ±50°) and CF-FM bats (mean beam width: ±22°). We found that FM bats smoothly shifted the acoustic gaze within 10° during the flight whereas the CF-FM bats frequently shifted the acoustic gaze within 25°. These results indicate that the shifting acoustic gaze by CF-FM bats compensates their own narrow beam width. Both bat species may keep approximately ±50° of their echolocation sights in order to sense the space for moving forward safely.

Adaptive beam-width control of echolocation sounds by CF–FM bats,Rhinolophus ferrumequinum nippon, during prey-capture flight

The echolocation sounds of Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) were measured while the bats pursued a moth (Goniocraspidum pryeri) in a flight chamber. Using a 31-channel microphone array system, we investigated how CF-FM bats adjust pulse direction and beam width according to prey position. During the search and approach phases, the horizontal and vertical beam widths were ±22±5 and ±13±5 deg, respectively. When bats entered the terminal phase approximately 1 m from a moth, distinctive evasive flight by G. pryeri was sometimes observed. Simultaneously, the bats broadened the beam widths of some emissions in both the horizontal (44% of emitted echolocation pulses) and vertical planes (71%). The expanded beam widths were ±36±7 deg (horizontal) and ±30±9 deg (vertical). When moths began evasive flight, the tracking accuracy decreased compared with that during the approach phase. However, in 97% of emissions during the terminal phase, the beam width was wider than the misalignment (the angular difference between the pulse and target directions). These findings indicate that bats actively adjust their beam width to retain the moving target within a spatial echolocation window during the final capture stages.

Spatial release from electronic clutter masking in FM bat echolocation

For big brown bats, angular separation of target and clutter echoes causes spatial release from clutter masking. Experiments using echoes that are electronically-generated by loudspeakers show that lowpass-filtering of normally masking echoes also causes clutter masking to disappear. Such lowpass-filtering induces amplitude-latency trading, which retards neural response times from clutter echoes at higher frequencies relative to lower frequencies. Countervailing changes in presentation-times of higher frequencies in electronically-generated clutter echoes restores masking. We present new results showing that moving the clutter-delivering loudspeakers to a different azimuth and elevation causes clutter masking to disappear. But, similar to the earlier experiments, the countervailing changes in presentation of higher frequencies reintroduce masking. In the bat’s inferior colliculus, FM sounds that mimic broadcasts and echoes evoke ~1 spike per sound at each neuron’s best frequency. However, amplitude-tuning is very broad, so bats work in the latency domain instead, to exploit their high acuity for detecting coherence or non-coherence of echo responses. Overall, the results indicate that big brown bats use neuronal response timing for virtually all auditory computations of echo delay, including those involved in clutter rejection derived from echo spectra. [Work supported by ONR and NSF.]

Convergence of reference frequencies by multiple CF–FM bats (Rhinolophus ferrumequinum nippon) during paired flights evaluated with onboard microphones

The constant frequency component of the second harmonic (CF(2)) of echolocation sounds in Rhinolophus ferrumequinum nippon were measured using onboard telemetry microphones while the bats exhibited Doppler-shift compensation during flights with conspecifics. (1) The CF(2) frequency of pulses emitted by individual bats at rest (F (rest)) showed a long-term gradual decline by 0.22 kHz on average over a period of 3 months. The mean neighboring F (rest) (interindividual differences in F (rest) between neighboring bats when the bats were arranged in ascending order according to F (rest)) ranged from 0.08 to 0.11 kHz among 18 bats in a laboratory colony. (2) The standard deviation of observed echo CF(2) (reference frequency) for bats during paired flights ranged from 50 to 90 Hz, which was not significantly different from that during single flights. This finding suggests that during paired flights, bats exhibit Doppler-shift compensation with the same accuracy as when they fly alone. (3) In 60% (n = 29) of the cases, the difference in the reference frequency between two bats during paired flights significantly decreased compared to when the bats flew alone. However, only 15% of the cases (n = 7) showed a significant increase during paired flights. The difference in frequency between two bats did not increase even when the reference frequencies of the individuals were not statistically different during single flights.

Findings on bat sonar through Telemike system

In order to understand how bats conduct echolocation recording what they listen to is essential. Then, we developed an onboard wireless telemetry microphone system (Telemike) for flying bats in our flight chamber. We also developed a sensitive microphone array system for field recordings and for the flight chamber. Some data through microphone array with Telemike will also be introduced. Both CF-FM (Hipposideros turpis, Hipposideros terasensis and Rhinolophus ferrumequinum nippon) and FM bats (Pipistrellus abramus, Miniopterus fuliginosus, and Eptesicus fuscus) were used in the flight chamber experiments, while only FM bats (Pipistrellus abramus and Eptesicus fuscus) were used for the field experiments. In the flight chamber experiment, through Telemike Doppler-shift compensation was confirmed from flying CF-FM bats. Echo amplitude compensation was found in both FM and CF-FM bats. The bats can fly without any collision against walls or their conspecifics in a narrow space. Telemike has recorded overlapped echoes originated from adjacent bats. How they extract weak echo signals in the situation where own echoes are masked by echoes of other bats may be revealed by Telemike experiments. Further, how bats get information from extremely weak echoes coming from a flying small insect will also be clarified in our experiments with Telemike. [Research supported by ONR grant]

FM bats use transform-based biosonar imaging

Big brown bats (Eptesicus fuscus) perceive target range from echo delay using neuronal-delay lines that extract and display the time that elapses between successive occurrences of individual frequencies in each FM broadcast and its subsequent echoes. The bat's delay accuracy is very sharp for echoes containing all broadcast frequencies. Decreasing the bandwidth of echoes reduces the number of frequencies available for estimating delay, which degrades acuity. However, removal of frequencies triggers the operation of a second, parallel estimation process, loosely related to the cepstrum, whereby delay differences between two or three closely-spaced reflections are estimated from the pattern of modulations (peaks and notches) in the echo spectrum. When a wide span of frequencies is removed, as in lowpass filtering, multiple spectral-modulation solutions coexist, which the bat perceives as many different glints distributed across several hundred microseconds. This defocuses the bat's images for the echoes and renders them not capable of clutter masking. The effect of spectral blurring on delay images is opposite to that expected from time-domain blurring, as demonstrated in 3 different delay-discrimination experiments. [Work supported by ONR and NSF]

Recovery cycles of inferior collicular neurons in the leaf-nosed bat, Hipposideros armiger

When stimulated with biologically relevant constant frequency–frequency modulation (CF–FM) sounds, the inferior collicular neurons of the CF–FM bat, Hipposideros armiger, either only discharged impulses to the onset (76%, single-on neurons) of the CF-FM sounds or to the onset of both CF and FM components of CF–FM sounds (24%, double-on neuron). Some neurons were single-on responders at low sound amplitude but become double-on responders at high sound amplitude. Single-on responders had longer latency and recovery cycle than double-on responders. While most neurons did not respond to the second sound when the paired CF-FM sounds overlapped, 3 single-on and 7 double-on neurons did such that they had “cyclic” recovery cycles with inter-pulse intervals. The different response latency and dynamic variation in the recovery cycle of these two types of neurons suggest they may serve as the neural basis underlying a bat's ability to perform echo ranging throughout different phases of hunting.

New evidence for parallel time-frequency transforms in FM bat biosonar

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