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A backpropagation network model of the monaural localization information available in the bat echolocation system.

The information echolocating bats receive is a combination of the properties of the sound they emit and the sound they receive at the eardrum. Convolving the emission and the external ear transfer functions produces the full spectral information contained in the echolocation combination. Spatially dependent changes in the magnitude spectra of the emission, external ear transfer functions, and the echolocation combination of Eptesicus fuscus could provide localization information to the bat. Principal component analysis was used to reduce the dimensionality of these complex spectral data sets. The first eight principal component weights were normalized, rotated, and used as the input to a backpropagation network model which examined the relative directionality of the emission, ear, and the echolocation combination. The model was able to localize more accurately when provided with the directional information of the echolocation combination compared to either the emission or ear information alone.

Animals↗

Detection of ultrasonic tones and simulated dolphin echolocation clicks by a teleost fish, the American shad (Alosa sapidissima).

The authors previously reported that American shad (Alosa sapidissima) can detect sounds from 100 Hz to 180 kHz, with two regions of best sensitivity, one from 200 to 800 Hz and the other from 25 to 150 kHz [Mann et al., Nature 389, 341 (1997)]. These results demonstrated ultrasonic hearing by shad, but thresholds at lower frequencies were potentially masked by background noise in the experimental room. In this study, the thresholds of the American shad in a quieter and smaller tank, as well as thresholds for detecting stimulated echolocation sounds of bottlenosed dolphins was determined. Shad had lower thresholds for detection (from 0.2 to 0.8 kHz) in the quieter and smaller tank compared with the previous experiment, with low-frequency background noise but similar thresholds at ultrasonic frequencies. Shad were also able to detect echolocation clicks with a threshold of 171 dB re: 1 microPa peak to peak. If spherical spreading and an absorption coefficient of 0.02 dB/m of dolphin echolocation clicks are assumed, shad should be able to detect echolocating Tursiops truncatus at ranges up to 187 m. The authors propose that ultrasonic hearing evolved in shad in response to selection pressures from echolocating odontocete cetaceans.

Animals↗

The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach.

We studied the efficiency and effects of the multiple sensory cues of tiger moths on echolocating bats. We used the northern long-eared bat, Myotis septentrionalis, a purported moth specialist that takes surface-bound prey (gleaning) and airborne prey (aerial hawking), and the dogbane tiger moth, Cycnia tenera, an eared species unpalatable to bats that possesses conspicuous colouration and sound-producing organs (tymbals). This is the first study to investigate the interaction of tiger moths and wild-caught bats under conditions mimicking those found in nature and to demand the use of both aerial hawking and gleaning strategies by bats. Further, it is the first to report spectrograms of the sounds produced by tiger moths while under aerial attack by echolocating bats. During both aerial hawking and gleaning trials, all muted C. tenera and perched intact C. tenera were attacked by M. septentrionalis, indicating that M. septentrionalis did not discriminate C. tenera from palatable moths based on potential echoic and/or non-auditory cues. Intact C. tenera were attacked significantly less often than muted C. tenera during aerial hawking attacks: tymbal clicks were therefore an effective deterrent in an aerial hawking context. During gleaning attacks, intact and muted C. tenera were always attacked and suffered similar mortality rates, suggesting that while handling prey this bat uses primarily chemical signals. Our results also show that C. tenera temporally matches the onset of click production to the ;approach phase' echolocation calls produced by aerial hawking attacking bats and that clicks themselves influence the echolocation behaviour of attacking bats. In the context of past research, these findings support the hypotheses that the clicks of arctiid moths are both an active defence (through echolocation disruption) and a reliable indicator of chemical defence against aerial-hawking bats. We suggest these signals are specialized for an aerial context.

Adaptation, Physiological↗

Interaction of vestibular, echolocation, and visual modalities guiding flight by the big brown bat, Eptesicus fuscus.

The big brown bat (Eptesicus fuscus) is an aerial-feeding insectivorous species that relies on echolocation to avoid obstacles and to detect flying insects. Spatial perception in the dark using echolocation challenges the vestibular system to function without substantial visual input for orientation. IR thermal video recordings show the complexity of bat flights in the field and suggest a highly dynamic role for the vestibular system in orientation and flight control. To examine this role, we carried out laboratory studies of flight behavior under illuminated and dark conditions in both static and rotating obstacle tests while administering heavy water (D2O) to impair vestibular inputs. Eptesicus carried out complex maneuvers through both fixed arrays of wires and a rotating obstacle array using both vision and echolocation, or when guided by echolocation alone. When treated with D2O in combination with lack of visual cues, bats showed considerable decrements in performance. These data indicate that big brown bats use both vision and echolocation to provide spatial registration for head position information generated by the vestibular system.

Animals↗

[Participation of the auditory centers of Rhinolophus ferrum-equinum in echolocational tracking of a moving target].

Behavioral and bioacoustic techniques were used to investigate the role of the auditory cortex and inferior colliculi in echolocative detection and tracking of moving targets by the greater horseshoe bat as well as their role in the regulation of vocal apparatus. It is demonstrated that complete bilateral auditory cortex destruction leads to considerable and irreversible changes in the process of tracking of moving targets but produce no detectable effect on the functioning of the vocal apparatus. Complete bilateral destruction of the inferior colliculi causes a loss of responses to moving targets (an artificial target or an insect). Animals with bilaterally destructed inferior colliculi show drastic changes in spectra of their echolocation calls manifested as occurence of multiple high- and low-frequency spectral components. The data suggest that the inferior colliculi of the midbrain are directly involved in echolocative tracking of moving targets and in matching of reception-emitting system of the bat. Participation of the auditory cortex in the process of echolocative detection of moving targets involves optimization of the echolocation system performance.

Animals↗

Ontogenesis of the echolocation system in the rufous horseshoe bat, Rhinolophus rouxi (audition and vocalization in early postnatal development).

1. The development of vocalization and hearing was studied in Sri Lankan horseshoe bats (Rhinolophus rouxi) during the first postnatal month. The young bats were caught in a nursing colony of rhinolophids in which birth took place within a two week period. 2. The new-born bats emitted isolation calls through the mouth. At the beginning these calls consisted of pure tones with frequencies below 10 kHz (Fig. 1). During the first postnatal week the call frequency increased to about 15 kHz, and the fundamental was augmented by two to four harmonics. No evoked potentials to pure tone stimuli could be elicited in the inferior colliculus of this age group, i.e., auditory processing at the midbrain level was not demonstrable. 3. Evoked potentials were first recorded in the second week, broadly tuned to 15-45 kHz, with a maximum sensitivity between 15-25 kHz. In the course of the second week, however, higher frequencies up to 60 kHz became progressively incorporated into the audiogram (Fig. 3). The fundamental frequency of the multiharmonic isolation calls, emitted strictly through the mouth, increased to about 20 kHz. 4. In the bats' third postnatal week an increased hearing sensitivity (auditory filter) emerged, sharply tuned at frequencies between 57 and 60 kHz (Fig. 4e). The same individuals were also the first to emit long constant frequency echolocation calls through the nostrils (Fig. 4c). The energy of the calls was arranged in harmonic frequency bands with the second harmonic exactly tuned to the auditory filter. These young bats continued to emit isolation calls through the mouth, which were, however, not harmonically related to the echolocation calls (Fig. 4b, d). 5. During the fourth week, both the auditory filter and the matched echolocation pulses (the second harmonic) shifted towards higher frequencies (Fig. 5). During the fifth week the fundamental frequency of the calls was progressively attenuated, and both the second harmonic of the pulses and the auditory filter reached the frequency range typical for adult bats of 73-78 kHz (Fig. 6). 6. The development of audition and vocalization is discussed with regard to possible interactions of both subsystems, and their incorporation into the active orientation system of echolocation.

Aging↗

Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat, Rhinolophus rouxi. I. Single unit recordings in the ventral motor nucleus of the laryngeal nerves in spontaneously vocalizing bats.

The vocal motor control of the larynx was studied with single unit recordings from the efferent motor nucleus (nucleus ambiguus) in the CF-FM-bat Rhinolophus rouxi, spontaneously emitting echolocation sounds. The experiments were performed in a stereotaxic apparatus that allowed differentiation of activities in the recorded nucleus depending on the electrode position (Fig. 1). Echolocation calls and respiration activity were monitored simultaneously, thus it was possible to compare the time course of the motor control activity during respiration with and without concurrent vocalization. Unit discharges were classified as laryngeal motoneuron activity according to their correlation with the time course (onset and end) of echolocation calls and their discharge rate as: Pre-off-tonic, pre-off-phasic, off-pauser, off-tonic, on-chopper, on-tonic, prior-tonic and inhibitory (Fig. 4). The on-chopper and on-tonic discharge patterns were assigned to the motor activity of the lateral cricoarytenoid muscle and the off-pauser and off-tonic discharge patterns to the motor activity of the posterior cricoarytenoid muscle controlling the time course of vocal pulses. Motoneuron activities recorded under the condition of systematically shifted frequencies in the emitted echolocation calls were investigated in Doppler-shift compensating bats responding to electronically simulated echoes. Of all neurons classified as motor control, only units of the pre-off-tonic discharge type (cricothyroid muscle) changed their activity with frequency shifts in the vocalized pulses; they showed a positive linear correlation with the emitted sound frequency (Fig. 6). In addition, single unit activities in strict synchronization to vocalization were recorded, that by their low discharge rate were not valid as motor control, and were considered to represent activities of interneurons or internuclear neurons connecting the nucleus ambiguus with other vocalization- and respiration-centers (Fig. 3c). Electric lesions in the brain stem and iontophoretically applied horseradish peroxidase (HRP) served as references for localization and morphological identification of the recording sites in cell stained brain slices.

Animals↗

Functional laminar and columnar organization of the auditory centers in echolocating Japanese greater horseshoe bats.

During echolocation, bats coordinately employ the vocalization system to emit orientation sounds and the auditory system to hear returning echoes. The brain in these animals should be functionally organized to process such biologically significant sounds. Here we utilized the autoradiographic 2-deoxy-[14C]glucose (DG) method to visualize functional organization of the auditory centers of echolocating Japanese greater horseshoe bats, Rhinolophus ferrumequinum nippon. Autoradiographic color images made from the brains of echolocating bats revealed a functional laminar structure in the inferior colliculus. Furthermore, a functional columnar organization appeared in the auditory cortex during echolocation. These laminar and columnar organization were not observed in the brain of resting bats.

Acoustic Stimulation↗

Brain activity patterns in flying, echolocating bats (Pteronotus parnellii): assessment by high resolution autoradiographic imaging with [3H]2-deoxyglucose.

Brain activity patterns during echolocation and flight were assessed in mustached bats (Pteronotus parnellii parnellii). Bats were injected intraperitoneally with [3H]2-deoxyglucose and restrained in a foam holder or allowed to fly for 20 min. Under resting conditions, low levels of [3H]2-deoxyglucose uptake were observed throughout the forebrain but relatively high uptake was found in brainstem auditory and vestibular centers. In flying, echolocating bats, marked increases in regional [3H]2-deoxyglucose uptake were apparent. All structures of the classical ascending auditory pathway were intensely labeled in autoradiograms. Other brain regions that exhibited high [3H]2-deoxyglucose uptake in flying bats included the cingulate cortex, stratum lacunosum-moleculare of the hippocampus, thalamus, caudate-putamen, superior colliculus, pontine reticular formation, nucleus ambiguus, parts of the midbrain central gray, and cerebellum. In the cerebellum, the most prominent increase in [3H]2-deoxyglucose uptake was found in discrete patches of the granule cell layer. The results provide the first overview of brain activity patterns during echolocation and flight in bats. In addition, uptake of [14C]fluorodeoxyglucose was used to compare brain activity patterns in flying bats to bats that were imaging their environment via biosonar while hanging in a wire cage. The echolocating-not-flying bats emitted 6931 +/- 1226 pulses in 20 min compared to 8972 +/- 1273 pulses in 20 min for flying bats. The uptake of the metabolic marker was significantly more in the flying bats compared to the emitting-not-flying bats in the medial geniculate, superior colliculus, auditory cortex, cingulate cortex and thalamus. In the nucleus ambiguus, cochlear nucleus, and inferior colliculus, uptake was similar for the flying and emitting-not-flying bats. These results suggest that the high metabolic activity observed in forebrain auditory regions of flying bats is related in part to neural processes that involve sensory motor integration during flight and not simply the perception of acoustic information.

Animals↗

Neurobiology of echolocation in bats.

Echolocating bats (sub-order: Microchiroptera) form a highly successful group of animals, comprising approximately 700 species and an estimated 25% of living mammals. Many echolocating bats are nocturnal predators that have evolved a biological sonar system to orient and forage in three-dimensional space. Acoustic signal processing and vocal-motor control are tightly coupled, and successful echolocation depends on the coordination between auditory and motor systems. Indeed, echolocation involves adaptive changes in vocal production patterns, which, in turn, constrain the acoustic information arriving at the bat's ears and the time-scales over which neural computations take place.

Animals↗

Automatic gain control in the echolocation system of dolphins.

In bats and technological sonars, the gain of the receiver is progressively increased with time after the transmission of a signal to compensate for acoustic propagation loss. The current understanding of dolphin echolocation indicates that automatic gain control is not a part of their sonar system. In order to test this understanding, we have performed field measurements of free-ranging echolocating dolphins. Here we show that dolphins do possess an automatic gain control mechanism, but that it is implemented in the transmission phase rather than the receiving phase of a sonar cycle. We find that the amplitude of the dolphins' echolocation signals are highly range dependent; this amplitude increases with increasing target range, R, in a 20 log(R) fashion to compensate for propagation loss. If the echolocation target is a fish school with many sound scatterers, the echoes from the school will remain nearly constant with range as the dolphin closes in on it. This characteristic has the same effect as time-varying gain in bats and technological sonar when considered from a sonar system perspective.

Acoustics↗

Echolocation signals reflect niche differentiation in five sympatric congeneric bat species.

Echolocating bats can be divided into guilds according to their preferred habitat and foraging behaviour, which coincide with distinct adaptations in wing morphology and structure of echolocation signals. Although coarse structuring of niche space between different guilds is generally accepted, it is not clear how niches differ within guilds, or whether there is fine-grained niche differentiation reflected in echolocation signal structure. Using a standardized performance test, here we show clutter-dependent differences in prey-capture success for bats from five species of European Myotis. These species are morphologically similar, sympatric, and all belong to the guild labelled "edge space aerial/trawling foragers". We further demonstrate a strong correlation between the prey-detection ability of the species and the respective search-call bandwidth. Our findings indicate that differences in echolocation signals contribute to within-guild niche differentiation. This is the first study relating sensory abilities of a set of potentially competing animal species to a direct measure of their respective foraging performance, suggesting an important role of sensory ecology in the structuring of animal communities.

Acoustics↗

Bimodal echolocation in pipistrelle bats: are cryptic species present?

The pipistrelle bat Pipistrellus pipistrellus is the most widespread in Europe, and is often the most abundant bat species in northern and central Europe. P. pipistrellus has traditionally been considered as one species throughout Europe. Here we show that: (i) the echolocation calls of pipistrelles fall into two distinct frequency bands in Britain, with frequencies containing most energy averaging 46 kHz and 55 kHz; (ii) roosts consist of bats which use only one form of echolocation; (iii) small but significant differences in average gross morphology exist between the phonic types; and (iv) the two phonic types occur in sympatry over much of Britain. Recordings made from European populations show that bimodal echolocation is also typical of continental pipistrelles, with only one phonic type found in some areas, two types in sympatry in others. The sympatric occurrence of two phonic types, the lack of mixing of types between colonies, and the morphological divergence between phonic types suggests that P. pipistrellus may actually consist of at least two cryptic sibling species. The evolution of bimodal echolocation in bats is discussed, and a model involving disruptive selection is presented to show how sympatric speciation may occur.

Acoustics↗

Echolocation range and wingbeat period match in aerial-hawking bats.

Aerial-hawking bats searching the sky for prey face the problem that flight and echolocation exert independent and possibly conflicting influences on call intervals. These bats can only exploit their full echolocation range unambiguously if they emit their next call when all echoes from the preceding call would have arrived. However, not every call interval is equally available. The need to reduce the high energetic costs of echolocation forces aerial-hawking bats to couple call emission to their wingbeat. We compared the wingbeat periods of 11 aerial-hawking bat species with the delays of the last-expected echoes. Acoustic flight-path tracking was employed to measure the source levels (SLs) of echolocation calls in the field. SLs were very high, extending the known range to 133 dB peak equivalent sound pressure level. We calculated the maximum detection distances for insects, larger flying objects and background targets. Wingbeat periods were derived from call intervals. Small and medium-sized bats in fact matched their maximum detection range for insects and larger flying targets to their wingbeat period. The tendency to skip calls correlated with the species' detection range for background targets. We argue that a species' call frequency is at such a pitch that the resulting detection range matches their wingbeat period.

Animals↗

Dynamics of jamming avoidance in echolocating bats.

Animals using active sensing systems such as echolocation or electrolocation may experience interference from the signals of neighbouring conspecifics, which can be offset by a jamming avoidance response (JAR). Here, we report JAR in one echolocating bat (Tadarida teniotis: Molossidae) but not in another (Taphozous perforatus: Emballonuridae) when both flew and foraged with conspecifics. In T. teniotis, JAR consisted of shifts in the dominant frequencies of echolocation calls, enhancing differences among individuals. Larger spectral overlap of signals elicited stronger JAR. Tadarida teniotis showed two types of JAR: (i) for distant conspecifics: a symmetric JAR, with lower- and higher-frequency bats shifting their frequencies downwards and upwards, respectively, on average by the same amount; and (ii) for closer conspecifics: an asymmetric JAR, with only the upper-frequency bat shifting its frequency upwards. In comparison, 'wave-type' weakly electric fishes also shift frequencies of discharges in a JAR, but unlike T. teniotis, the shifts are either symmetric in some species or asymmetric in others. We hypothesize that symmetric JAR in T. teniotis serves to avoid jamming and improve echolocation, whereas asymmetric JAR may aid communication by helping to identify and locate conspecifics, thus minimizing chances of mid-air collisions.

Animals↗

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.

Animals↗

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.

Acoustic Stimulation↗

Target detection, shape discrimination, and signal characteristics of an echolocating false killer whale (Pseudorca crassidens).

This study demonstrated the ability of a false killer whale (Pseudorca crassidens) to discriminate between two targets and investigated the parameters of the whale's emitted signals for changes related to test conditions. Target detection performance comparable to the bottlenose dolphin's (Tursiops truncatus) has previously been reported for echolocating false killer whales. No other echolocation capabilities have been reported. A false killer whale, naive to conditioned echolocation tasks, was initially trained to detect a cylinder in a "go/no-go" procedure over ranges of 3 to 8 m. The transition from a detection task to a discrimination task was readily achieved by introducing a spherical comparison target. Finally, the cylinder was successfully compared to spheres of two different sizes and target strengths. Multivariate analyses were used to evaluate the parameters of emitted signals. Duncan's multiple range tests showed significant decreases (df = 185, p less than 0.05) in both source level and bandwidth in the transition from detection to discrimination. Analysis of variance revealed a significant decrease in the number of clicks over test conditions [F(5.26) = 5.23, p less than 0.0001]. These data suggest that the whale relied on cues relevant to target shape as well as target strength, that changes in source level and bandwidth were task-related, that the decrease in clicks was associated with learning experience, and that Pseudorca's ability to discriminate shapes using echolocation may be comparable to that of Tursiops truncatus.

Animals↗