Stabilization of perceived echo amplitudes in echolocating bats. II. The acoustic behavior of the big brown bat, Eptesicus fuscus, when tracking moving prey.

Big brown bats, Eptesicus fuscus, can be trained to use echolocation to track a small microphone with a food reward attached when it is moved rapidly toward them. This situation mimics prey interception in the wild while allowing very precise recording of the sonar pulses emitted during tracking behavior. The results show that E. fuscus intensity compensates, reducing emitted intensity by 6 dB per halving of target range so that the intensity incident upon the target is constant and echo intensity increases by 6 dB per halving of range. This increase in echo intensity is effectively canceled by the reduction in auditory sensitivity due to automatic gain control (AGC) of 6 to 7 dB per halving of range. Intensity compensation behavior and AGC therefore form a dual-component, symmetrical system that stabilizes perceived echo amplitudes during target approach. The same system is present in the fishing bat, Noctilio leporinus, suggesting that it may be widespread in echolocating bats. Correlation analysis shows that, despite large changes in the duration of the pulses emitted by E. fuscus during an approach, the pulse frequency structure is such that the spatial image of the target perceived along the range axis is highly stable. Pulse duration is not reduced in the manner theoretically necessary to eliminate potential echo distortion effects due to AGC, but is reduced in such a way that this distortion is insignificant. During the terminal buzz, a high degree of temporal overlap (relative to pulse duration) occurs between emitted pulse and returning echo.     

Echolocation and flight strategy of Japanese house bats during natural foraging, revealed by a microphone array system

Using only a microphone array system, echolocation pulses and three-dimensional flight paths in the frequency-modulated bat, Pipistrellus abramus, during natural foraging, were simultaneously examined. During the search phase, the inter-pulse interval, pulse duration, and moving distance of the bat between successive emissions were relatively constant at around 89.5 ± 18.7 ms, 6.90 ± 1.31 ms, and 0.50 ± 0.20 m, respectively. The bats started to decrease these acoustical parameters within 2-3 m of the prey capture point. For every emission along a flight path, the distance between a bat and its prey capture point was calculated as both direct distance to capture (DDC), which corresponded to the target distance, and flight distance to capture (FDC) along the flight path. The DDC matched the FDC after the start of the approach phase, indicating that foraging bats followed a straight-ahead path to the target. In addition, the duration of the quasi-constant frequency component of emitted pulses was slightly extended just before the convergence of the DDC with the FDC. These findings suggest that the bats confirm the presence of target prey by extending the duration of the pulse and then select a straight-ahead approach by forecasting the movement of the prey.     

Doppler-shift compensation in the Taiwanese leaf-nosed bat (Hipposideros terasensis) recorded with a telemetry microphone system during flight

Biosonar behavior was examined in Taiwanese leaf-nosed bats (Hipposideros terasensis; CF-FM bats) during flight. Echolocation sounds were recorded using a telemetry microphone mounted on the bat's head. Flight speed and three-dimensional trajectory of the bat were reconstructed from images taken with a dual high-speed video camera system. Bats were observed to change the intensity and emission rate of pulses depending on the distance from the landing site. Frequencies of the dominant second harmonic constant frequency component (CF2) of calls estimated from the bats' flight speed agreed strongly with observed values. Taiwanese leaf-nosed bats changed CF2 frequencies depending on flight speed, which caused the CF2 frequencies of the Doppler-shifted echoes to remain constant. Pulse frequencies were also estimated using echoes returning directly ahead of the bat and from its sides for two different flight conditions: landing and U-turn. Bats in flight may periodically alter their attended angles from the front to the side when emitting echolocation pulses.     

The interaction of outgoing echolocation pulses and echoes in the false killer whale's auditory system: evoked-potential study

Brain auditory evoked potentials (AEP) associated with echolocation were recorded in a false killer whale Pseudorca crassidens trained to accept suction-cup EEG electrodes and to detect targets by echolocation. AEP collection was triggered by echolocation pulses transmitted by the animal. The target was a hollow aluminum cylinder of strength of -22 dB at a distance from 1 to 8 m. Each AEP record was obtained by averaging more than 1000 individual records. All the records contained two AEP sets: the first one of a constant latency and a second one with a delay proportional to the distance. The timing of these two AEP sets was interpreted as responses to the transmitted echolocation pulse and echo, respectively. The echo-related AEP, although slightly smaller, was comparable to the outgoing click-related AEP in amplitude, even though at a target distance as far as 8 m the echo intensity was as low as -64 dB relative to the transmitted pulse in front of the head. The amplitude of the echo-related AEP was almost independent of distance, even though variation of target distance from 1 to 8 m influenced the echo intensity by as much as 36 dB.     

Source level reduction and sonar beam aiming in landing big brown bats (Eptesicus fuscus)

Reduction of echolocation call source levels in bats has previously been studied using set-ups with one microphone. By using a 16 microphone array, sound pressure level (SPL) variations, possibly caused by the scanning movements of the bat, can be excluded and the sonar beam aiming can be studied. During the last two meters of approach flights to a landing platform in a large flight room, five big brown bats aimed sonar beams at the landing site and reduced the source level on average by 7 dB per halving of distance. Considerable variation was found among the five individuals in the amount of source level reduction ranging from 4 to 9 dB per halving of distance. These results are discussed with respect to automatic gain control and intensity compensation and the combination of the two effects. It is argued that the two effects together do not lead to a stable echo level at the cochlea. This excludes a tightly coupled closed loop feed back control system as an explanation for the observed reduction of signal SPL in landing big brown bats.     

Interaction of emitted sonar pulses and simulated echoes in a false killer whale: an evoked-potential study

Auditory evoked potentials (AEP) were recorded during echolocation in a false killer whale Pseudorca crassidens. An electronically synthesized and played-back (simulated) echo was triggered by an emitted biosonar pulse, and its intensity was proportional to that of the emitted click. The delay and transfer factor of the echo relative to the emitted click was controlled by the operator. The echo delay varied from 2 to 16 ms (by two-fold steps), and the transfer factor varied within ranges from -45 to -30 dB at the 2-ms delay to -60 to -45 dB at the 16-ms delay. Echo-related AEPs featured amplitude dependence both on echo delay at a constant transfer factor (the longer the delay, the higher amplitude) and on echo transfer factor at a constant delay (the higher transfer factor, the higher amplitude). Conjunctional variation of the echo transfer factor and delay kept the AEP amplitude constant when the delay to transfer factor trade was from -7.1 to -8.4 dB per delay doubling. The results confirm the hypothesis that partial forward masking of the echoes by the preceding emitted sonar pulses serves as a time-varying automatic gain control in the auditory system of echolocating odontocetes.     

Forward masking as a mechanism of automatic gain control in odontocete biosonar: a psychophysical study

In a false killer whale Pseudorca crassidens, echo perception thresholds were measured using a go/no-go psychophysical paradigm and one-up-one-down staircase procedure. Computer controlled echoes were electronically synthesized pulses that were played back through a transducer and triggered by whale emitted biosonar pulses. The echo amplitudes were proportional to biosonar pulse amplitudes; echo levels were specified in terms of the attenuation of the echo sound pressure level near the animal's head relative to the source level of the biosonar pulses. With increasing echo delay, the thresholds (echo attenuation factor) decreased from -49.3 dB at 2 ms to -79.5 dB at 16 ms, with a regression slope of -9.5 dB per delay doubling (-31.5 dB per delay decade). At the longer delays, the threshold remained nearly constant around -80.4 dB. Levels of emitted pulses slightly increased with delay prolongation (threshold decrease), with a regression slope of 3.2 dB per delay doubling (10.7 dB per delay decade). The echo threshold dependence on delay is interpreted as a release from forward masking by the preceding emitted pulse. This release may compensate for the echo level decrease with distance, thus keeping the echo sensation level for the animal near constant within a certain distance range.     

Invariance of evoked-potential echo-responses to target strength and distance in an echolocating false killer whale

Brain auditory evoked potentials (AEPs) were recorded in a false killer whale Pseudorca crassidens trained to accept suction-cup EEG electrodes and to detect targets by echolocation. AEP collection was triggered by echolocation pulses transmitted by the animal. The target strength varied from -22 to -40 dB; the distance varied from 1.5 to 6 m. All the records contained two AEP sets: the first one of a constant latency (transmission-related AEP) and a second one with a delay proportional to the distance (echo-related AEP). The amplitude of echo-related AEPs was almost independent of both target strength and distance, though combined variation of these two parameters resulted in echo intensity variation within a range of 42 dB. The amplitude of transmission-related AEPs was independent of distance but dependent on target strength: the less the target strength, the higher the amplitude. Recording of transmitted pulses has not shown their intensity dependence on target strength. It is supposed that the constancy of echo-related AEP results from variation of hearing sensitivity depending on the target strength and release of echo-related responses from masking by transmitted pulses depending on the distance.     

Vocal control of acoustic information for sonar discriminations by the echolocating bat, Eptesicus fuscus

This study aimed to determine whether bats using frequency modulated (FM) echolocation signals adapt the features of their vocalizations to the perceptual demands of a particular sonar task. Quantitative measures were obtained from the vocal signals produced by echolocating bats (Eptesicus fuscus) that were trained to perform in two distinct perceptual tasks, echo delay and Doppler-shift discriminations. In both perceptual tasks, the bats learned to discriminate electronically manipulated playback signals of their own echolocation sounds, which simulated echoes from sonar targets. Both tasks utilized a single-channel electronic target simulator and tested the bat's in a two-alternative forced choice procedure. The results of this study demonstrate changes in the features of the FM bats' sonar sounds with echolocation task demands, lending support to the notion that this animal actively controls the echo information that guides its behavior.     

Echolocation call intensity and directionality in flying short-tailed fruit bats, Carollia perspicillata (Phyllostomidae)

The directionality of bat echolocation calls defines the width of bats' sonar "view," while call intensity directly influences detection range since adequate sound energy must impinge upon objects to return audible echoes. Both are thus crucial parameters for understanding biosonar signal design. Phyllostomid bats have been classified as low intensity or "whispering bats," but recent data indicate that this designation may be inaccurate. Echolocation beam directionality in phyllostomids has only been measured through electrode brain-stimulation of restrained bats, presumably excluding active beam control via the noseleaf. Here, a 12-microphone array was used to measure echolocation call intensity and beam directionality in the frugivorous phyllostomid, Carollia perspicillata, echolocating in flight. The results showed a considerably narrower beam shape (half-amplitude beam angles of approximately 16° horizontally and 14° vertically) and louder echolocation calls [source levels averaging 99 dB sound pressure level (SPL) root mean square] for C. perspicillata than was found for this species when stationary. This suggests that naturally behaving phyllostomids shape their sound beam to achieve a longer and narrower sonar range than previously thought. C. perspicillata orient and forage in the forest interior and the narrow beam might be adaptive in clutter, by reducing the number and intensity of off-axis echoes.     

Variation in the resting frequency of Rhinolophus pusillus in Mainland China: effect of climate and implications for conservation

This study describes variation patterns in the constant frequency of echolocation calls emitted at rest and when not flying ("resting frequency" RF) of the least horseshoe bat, Rhinolophus pusillus, on a broad geographical scale and in response to local climatic variables. Significant differences in RF were observed among populations throughout the species range in Mainland China, and this variation was positively and significantly related to climate conditions, especially environmental humidity, but the variability was only weakly associated with geographical distance. Sex dimorphism in the RF of R. pusillus may imply that female and male might keep their frequencies within a narrow range for sex recognition. Moreover, bats adjusted resting frequency to humidity, which may imply partitioning diet by prey size or the influence of rainfall noise. The results indicate that bats adjust echolocation call frequency to adapt to environmental conditions. Therefore, environmental selection shape the diversity of echolocation call structure of R. pusillus in geographically separated populations, and conservation efforts should focus on changes in local climate and effects of environmental noise.     

Evoked-potential recovery during double click stimulation in a whale: a possibility of biosonar automatic gain control

False killer whale Pseudorca crassidens auditory brainstem responses (ABR) were recorded using a double-click stimulation paradigm specifically measuring the recovery of the second response (to the test click) as a function of the inter-click interval (ICI) at various levels of the conditioning and test click. At all click intensities, the slopes of recovery functions were almost constant: 0.6-0.8 microV per ICI decade. Therefore, even when the conditioning-to-test-click level ratio was kept constant, the duration of recovery was intensity-dependent: The higher intensity the longer the recovery. The conditioning-to-test-click level ratio strongly influenced the recovery time: The higher the ratio, the longer the recovery. The dependence was almost linear using a logarithmic ICI scale with a rate of 25-30 dB per ICI decade. These data were used for modeling the interaction between the emitted click and the echo during echolocation, assuming that the two clicks simulated the transmitted and echo clicks. This simulation showed that partial masking of the echo by the preceding emitted click may explain the independence of echo-response amplitude of target distance. However, the distance range where this mechanism is effective depends on the emitted click level: The higher the level, the greater the range. @ 2007 Acoustical Society of America.     

Adaptive echolocation sounds of insectivorous bats, Pipistrellus abramus, during foraging flights in the field

Echolocation pulses emitted by wild Pipistrellus abramus were investigated while foraging for insects in the field. Similar to other European pipistrelles, the frequency structure during foraging varied. During the search phase, the bats emitted long shallow frequency-modulated pulses 9-11 ms in duration, whereas the maximum pulse duration of the bats approaching a large target wall in the laboratory was 3 ms. No significant difference was observed between decreases in the interpulse interval during these two approach flights. It is concluded that the bats use a long quasi-constant frequency pulse to find a weak echo from a small prey target.     

Range resolution and the possible use of spectral information in the echolocating bat, Eptesicus fuscus

Individuals of the echolocating bat Eptesicus fuscus were trained to discriminate simulated two-wave-front targets with internal time delays of 0 to 100 microns between the wave fronts from a one-wave-front target. The ability of bats to discriminate between such targets can be referred to as range resolution. In Eptesicus fuscus, this ability is limited to distinct internal time delays (12, 32-40, and 52-100 microns) between the two wave fronts of a double-wave-front target. Analysis of the simulated two-wave-front echoes reveals periodic frequency minima in the spectrum. Position and separation of these spectral minima depend on the time delay between the two wave fronts. The occurrence of spectral minima within the frequency range of the first harmonic in the echo of the bats' echolocation call correlates to the bats' ability to discriminate a one-wave-front echo from two-wave-front echoes, suggesting that Eptesicus fuscus uses spectral differences within the first harmonic in echoes for range resolution.     

Discrimination of amplitude-modulated synthetic echo trains by an echolocating bottlenose dolphin

Bottlenose dolphins (Tursiops truncatus) have an acute ability to use target echoes to judge attributes such as size, shape, and material composition. Most target recognition studies have focused on features associated with individual echoes as opposed to information conveyed across echo sequences (feature envelope of the multi-echo train). One feature of aspect-dependent targets is an amplitude modulation (AM) across the return echoes in the echo train created by relative movement of the target and dolphin. The current study examined whether dolphins could discriminate targets with different AM envelopes. "Electronic echoes" triggered by a dolphin's outgoing echolocation clicks were manipulated to create sinusoidal envelopes with varying AM rate and depth. Echo trains were equated for energy, requiring the dolphin to extract and retain information from multiple echoes in order to detect and report the presence of AM. The dolphin discriminated amplitude-modulated echo trains from those that were not modulated. AM depth thresholds were approximately 0.8 dB, similar to other published amplitude limens. Decreasing the rate of modulation from approximately 16 to 2 cycles per second did not affect the dolphin's AM depth sensitivity. The results support multiple-echo processing in bottlenose dolphin echolocation. This capability provides additional theoretical justification for exploring synthetic aperture sonar concepts in models of animal echolocation that potentially support theories postulating formation of images as an ultimate means for target identification.     

The influence of flight speed on the ranging performance of bats using frequency modulated echolocation pulses

Many species of bat use ultrasonic frequency modulated (FM) pulses to measure the distance to objects by timing the emission and reception of each pulse. Echolocation is mainly used in flight. Since the flight speed of bats often exceeds 1% of the speed of sound, Doppler effects will lead to compression of the time between emission and reception as well as an elevation of the echo frequencies, resulting in a distortion of the perceived range. This paper describes the consequences of these Doppler effects on the ranging performance of bats using different pulse designs. The consequences of Doppler effects on ranging performance described in this paper assume bats to have a very accurate ranging resolution, which is feasible with a filterbank receiver. By modeling two receiver types, it was first established that the effects of Doppler compression are virtually independent of the receiver type. Then, used a cross-correlation model was used to investigate the effect of flight speed on Doppler tolerance and range-Doppler coupling separately. This paper further shows how pulse duration, bandwidth, function type, and harmonics influence Doppler tolerance and range-Doppler coupling. The influence of each signal parameter is illustrated using calls of several bat species. It is argued that range-Doppler coupling is a significant source of error in bat echolocation, and various strategies bats could employ to deal with this problem, including the use of range rate information are discussed.     

Range discrimination by big brown bats (Eptesicus fuscus) using altered model echoes: implications for signal processing

The sonar emissions of two big brown bats (Eptesicus fuscus) were modeled to create a "normal" echolocation signal for each bat which was then used as an artificial echo to synthesize a phantom target. The bat's task was to indicate which of two phantom targets (presented singly) was the "near" target and which the "far" target. Threshold range discrimination at a nominal target distance of 80 cm was about 0.6 cm for both bats. The normal signal was then modified to change the relative energy in each harmonic, the signal duration, the curvature of the frequency sweep, the absolute frequency, the phase of the second and third harmonics relative to the first, or the Doppler shift of the signal. To determine which modifications affected ranging performance, the altered models were used in tests of range discrimination that were interleaved on a day-to-day basis with tests using the normal model. Of the 12 modifications tested, only those changing the curvature of the frequency sweep affected performance. This result appears not to be predicted by current models of echo processing in FM bats. Eptesicus may be able to compensate for certain types of distortions of a returning echo, an ability possibly related to Doppler tolerance or to the characteristics of the natural variation in a bat's emissions.     

Classification of broadband echoes from prey of a foraging Blainville's beaked whale

Blainville's beaked whales (Mesoplodon densirostris) use broadband, ultrasonic echolocation signals with a -10 dB bandwidth from 26 to 51 kHz to search for, localize, and approach prey that generally consist of mid-water and deep-water fishes and squid. Although it is well known that the spectral characteristics of broadband echoes from marine organisms vary as a function of size, shape, orientation, and anatomical group, there is little evidence as to whether or not free-ranging toothed whales use spectral cues in discriminating between prey and nonprey. In order to study the prey-classification process, a stereo acoustic tag was deployed on a Blainville's beaked whale so that emitted clicks and the corresponding echoes from targets in the water could be recorded. A comparison of echoes from targets apparently selected by the whale and those from a sample of scatterers that were not selected suggests that spectral features of the echoes, target strengths, or both may have been used by the whale to discriminate between echoes. Specifically, the whale appears to favor targets with one or more nulls in the echo spectra and to seek prey with higher target strengths at deeper depths.     

Auditory scene analysis by echolocation in bats.

Echolocating bats transmit ultrasonic vocalizations and use information contained in the reflected sounds to analyze the auditory scene. Auditory scene analysis, a phenomenon that applies broadly to all hearing vertebrates, involves the grouping and segregation of sounds to perceptually organize information about auditory objects. The perceptual organization of sound is influenced by the spectral and temporal characteristics of acoustic signals. In the case of the echolocating bat, its active control over the timing, duration, intensity, and bandwidth of sonar transmissions directly impacts its perception of the auditory objects that comprise the scene. Here, data are presented from perceptual experiments, laboratory insect capture studies, and field recordings of sonar behavior of different bat species, to illustrate principles of importance to auditory scene analysis by echolocation in bats. In the perceptual experiments, FM bats (Eptesicus fuscus) learned to discriminate between systematic and random delay sequences in echo playback sets. The results of these experiments demonstrate that the FM bat can assemble information about echo delay changes over time, a requirement for the analysis of a dynamic auditory scene. Laboratory insect capture experiments examined the vocal production patterns of flying E. fuscus taking tethered insects in a large room. In each trial, the bats consistently produced echolocation signal groups with a relatively stable repetition rate (within 5%). Similar temporal patterning of sonar vocalizations was also observed in the field recordings from E. fuscus, thus suggesting the importance of temporal control of vocal production for perceptually guided behavior. It is hypothesized that a stable sonar signal production rate facilitates the perceptual organization of echoes arriving from objects at different directions and distances as the bat flies through a dynamic auditory scene. Field recordings of E. fuscus, Noctilio albiventris, N. leporinus, Pippistrellus pippistrellus, and Cormura brevirostris revealed that spectral adjustments in sonar signals may also be important to permit tracking of echoes in a complex auditory scene.     

Wind turbines and bat mortality: Doppler shift profiles and ultrasonic bat-like pulse reflection from moving turbine blades

Bat mortality resulting from actual or near-collision with operational wind turbine rotors is a phenomenon that is widespread but not well understood. Because bats rely on information contained in high-frequency echoes to determine the nature and movement of a target, it is important to consider how ultrasonic pulses similar to those used by bats for echolocation may be interacting with operational turbine rotor blades. By assessing the characteristics of reflected ultrasonic echoes, moving turbine blades operating under low wind speed conditions (<6 m s(-1)) were found to produce distinct Doppler shift profiles at different angles to the rotor. Frequency shifts of up to ±700-800 Hz were produced, which may not be perceptible by some bat species. Monte Carlo simulation of bat-like sampling by echolocation revealed that over 50 rotor echoes could be required by species such as Pipistrellus pipistrellus for accurate interpretation of blade movement, which may not be achieved in the bat's approach time-window. In summary, it was found that echoes returned from moving blades had features which could render them attractive to bats or which might make it difficult for the bat to accurately detect and locate blades in sufficient time to avoid a collision.