Adaptive behavior for texture discrimination by the free-flying big brown bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

This study examined behavioral strategies for texture discrimination by echolocation in free-flying bats. Big brown bats, Eptesicus fuscus, were trained to discriminate a smooth 16 mm diameter object (S+) from a size-matched textured object (S−), both of which were tethered in random locations in a flight room. The bat’s three-dimensional flight path was reconstructed using stereo images from high-speed video recordings, and the bat’s sonar vocalizations were recorded for each trial and analyzed off-line. A microphone array permitted reconstruction of the sonar beam pattern, allowing us to study the bat’s directional gaze and inspection of the objects. Bats learned the discrimination, but performance varied with S−. In acoustic studies of the objects, the S+ and S− stimuli were ensonified with frequency-modulated sonar pulses. Mean intensity differences between S+ and S− were within 4 dB. Performance data, combined with analyses of echo recordings, suggest that the big brown bat listens to changes in sound spectra from echo to echo to discriminate between objects. Bats adapted their sonar calls as they inspected the stimuli, and their sonar behavior resembled that of animals foraging for insects. Analysis of sonar beam-directing behavior in certain trials clearly showed that the bat sequentially inspected S+ and S−.     

The role of prey-generated sounds,vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae)

Summary Cardioderma cor responded with head movements and flight toward speakers broadcasting calls of frogs and crickets which contained only sonic frequencies. Unlike the frog-eating bat,Trachops cirrhosus, they did not make contact with the speakers. Prey movements that generated sonic and ultrasonic sounds were both sufficient and necessary for the bats to localize and capture prey. Prey dragged across a glass sheet with a thin layer of water did not generate sounds and bats did not attempt to capture these prey, even with the availability of visual and echolocation cues. There was no evidence for the use of visual cues while hunting; bats did not localize prey more readily in light than darkness. Prey were presented such that their movements initially generated sounds, but then the prey moved onto the water layer of the glass sheet and sounds were eliminated. The bats emitted echolocation signals while hunting in this situation; however, the information from these signals was not utilized. The bats landed at the site that prey last made sound. These results demonstrate the importance of passive hearing for prey localization in this bat, and further suggest that when preygenerated sounds and echolocation signals offer conflicting information the bat's behavior is guided by the former.     

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°–100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat’s pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.     

Different Auditory Feedback Control for Echolocation and Communication in Horseshoe Bats

Auditory feedback from the animal''s own voice is essential during bat echolocation: to optimize signal detection, bats continuously adjust various call parameters in response to changing echo signals. Auditory feedback seems also necessary for controlling many bat communication calls, although it remains unclear how auditory feedback control differs in echolocation and communication. We tackled this question by analyzing echolocation and communication in greater horseshoe bats, whose echolocation pulses are dominated by a constant frequency component that matches the frequency range they hear best. To maintain echoes within this “auditory fovea”, horseshoe bats constantly adjust their echolocation call frequency depending on the frequency of the returning echo signal. This Doppler-shift compensation (DSC) behavior represents one of the most precise forms of sensory-motor feedback known. We examined the variability of echolocation pulses emitted at rest (resting frequencies, RFs) and one type of communication signal which resembles an echolocation pulse but is much shorter (short constant frequency communication calls, SCFs) and produced only during social interactions. We found that while RFs varied from day to day, corroborating earlier studies in other constant frequency bats, SCF-frequencies remained unchanged. In addition, RFs overlapped for some bats whereas SCF-frequencies were always distinctly different. This indicates that auditory feedback during echolocation changed with varying RFs but remained constant or may have been absent during emission of SCF calls for communication. This fundamentally different feedback mechanism for echolocation and communication may have enabled these bats to use SCF calls for individual recognition whereas they adjusted RF calls to accommodate the daily shifts of their auditory fovea.     

Bidirectional Echolocation in the Bat Barbastella barbastellus: Different Signals of Low Source Level Are Emitted Upward through the Nose and Downward through the Mouth

The Barbastelle bat (Barbastella barbastellus) preys almost exclusively on tympanate moths. While foraging, this species alternates between two different signal types. We investigated whether these signals differ in emission direction or source level (SL) as assumed from earlier single microphone recordings. We used two different settings of a 16-microphone array to determine SL and sonar beam direction at various locations in the field. Both types of search signals had low SLs (81 and 82 dB SPL rms re 1 m) as compared to other aerial-hawking bats. These two signal types were emitted in different directions; type 1 signals were directed downward and type 2 signals upward. The angle between beam directions was approximately 70°. Barbastelle bats are able to emit signals through both the mouth and the nostrils. As mouth and nostrils are roughly perpendicular to each other, we conclude that type 1 signals are emitted through the mouth while type 2 signals and approach signals are emitted through the nose. We hypothesize that the “stealth” echolocation system of B. barbastellus is bifunctional. The more upward directed nose signals may be mainly used for search and localization of prey. Their low SL prevents an early detection by eared moths but comes at the expense of a strongly reduced detection range for the environment below the bat. The more downward directed mouth signals may have evolved to compensate for this disadvantage and may be mainly used for spatial orientation. We suggest that the possibly bifunctional echolocation system of B. barbastellus has been adapted to the selective foraging of eared moths and is an excellent example of a sophisticated sensory arms race between predator and prey.     

Click-based echolocation in bats: not so primitive after all

Echolocating bats of the genus Rousettus produce click sonar signals, using their tongue (lingual echolocation). These signals are often considered rudimentary and are believed to enable only crude performance. However, the main argument supporting this belief, namely the click’s reported long duration, was recently shown to be an artifact. In fact, the sonar clicks of Rousettus bats are extremely short, ~50–100 μs, similar to dolphin vocalizations. Here, we present a comparison between the sonar systems of the ‘model species’ of laryngeal echolocation, the big brown bat (Eptesicus fuscus), and that of lingual echolocation, the Egyptian fruit bat (Rousettus aegyptiacus). We show experimentally that in tasks, such as accurate landing or detection of medium-sized objects, click-based echolocation enables performance similar to laryngeal echolocators. Further, we describe a sophisticated behavioral strategy for biosonar beam steering in clicking bats. Finally, theoretical analyses of the signal design—focusing on their autocorrelations and wideband ambiguity functions—predict that in some aspects, such as target ranging and Doppler-tolerance, click-based echolocation might outperform laryngeal echolocation. Therefore, we suggest that click-based echolocation in bats should be regarded as a viable echolocation strategy, which is in fact similar to the biosonar used by most echolocating animals, including whales and dolphins.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

‘No cost of echolocation for flying bats’ revisited

Echolocation is energetically costly for resting bats, but previous experiments suggested echolocation to come at no costs for flying bats. Yet, previous studies did not investigate the relationship between echolocation, flight speed, aerial manoeuvres and metabolism. We re-evaluated the 'no-cost' hypothesis, by quantifying the echolocation pulse rate, the number of aerial manoeuvres (landings and U-turns), and the costs of transport in the 5-g insectivorous bat Rhogeessa io (Vespertilionidae). On average, bats (n = 15) travelled at 1.76 ± 0.36 m s?1 and performed 11.2 ± 6.1 U-turns and 2.8 ± 2.9 ground landings when flying in an octagonal flight cage. Bats made more U-turns with decreasing wing loading (body weight divided by wing area). At flight, bats emitted 19.7 ± 2.7 echolocation pulses s?1 (range 15.3-25.8 pulses s?1), and metabolic rate averaged 2.84 ± 0.95 ml CO? min?1, which was more than 16 times higher than at rest. Bats did not echolocate while not engaged in flight. Costs of transport were not related to the rate of echolocation pulse emission or the number of U-turns, but increased with increasing number of landings; probably as a consequence of slower travel speed when staying briefly on ground. Metabolic power of flight was lower than predicted for R. io under the assumption that energetic costs of echolocation call production is additive to the aerodynamic costs of flight. Results of our experiment are consistent with the notion that echolocation does not add large energetic costs to the aerodynamic power requirements of flight in bats.     

Listening for bats: the hearing range of the bushcricket Phaneroptera falcata for bat echolocation calls measured in the field

The hearing range of the tettigoniid Phaneropterafalcata for the echolocation calls of freely flying mouseeared bats (Myotis myotis) was determined in the field. The hearing of the insect was monitored using hook electrode recordings from an auditory interneuron, which is as sensitive as the hearing organ for frequencies above 16 kHz. The flight path of the bat relative to the insect's position was tracked by recording the echolocation calls with two microphone arrays, and calculating the bat's position from the arrival time differences of the calls at each microphone. The hearing distances ranged from 13 to 30 m. The large variability appeared both between different insects and between different bat approaches to an individual insect. The escape time of the bushcricket, calculated from the detection distance of the insect and the instantaneous flight speed of the bat, ranged from 1.5 to more than 4s. The hearing ranges of bushcrickets suggest that the insect hears the approaching bat long before the bat can detect an echo from the flying insect.     

Can two streams of auditory information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus

A tenet of auditory scene analysis is that we can fully process only one stream of auditory information at a time. We tested this assumption in a gleaning bat, the pallid bat (Antrozous pallidus) because this bat uses echolocation for general orientation, and relies heavily on prey-generated sounds to detect and locate its prey. It may therefore encounter situations in which the echolocation and passive listening streams temporally overlap. Pallid bats were trained to a dual task in which they had to negotiate a wire array, using echolocation, and land on one of 15 speakers emitting a brief noise burst in order to obtain a food reward. They were forced to process both streams within a narrow 300 to 500 ms time window by having the noise burst triggered by the bats initial echolocation pulses as it approached the wire array. Relative to single task controls, echolocation and passive sound localization performance was slightly, but significantly, degraded. The bats also increased echolocation interpulse intervals during the dual task, as though attempting to reduce temporal overlap between the signals. These results suggest that the bats, like humans, have difficulty in processing more than one stream of information at a time.     

Active head rolls enhance sonar-based auditory localization performance

Animals utilize a variety of active sensing mechanisms to perceive the world around them. Echolocating bats are an excellent model for the study of active auditory localization. The big brown bat (Eptesicus fuscus), for instance, employs active head roll movements during sonar prey tracking. The function of head rolls in sound source localization is not well understood. Here, we propose an echolocation model with multi-axis head rotation to investigate the effect of active head roll movements on sound localization performance. The model autonomously learns to align the bat’s head direction towards the target. We show that a model with active head roll movements better localizes targets than a model without head rolls. Furthermore, we demonstrate that active head rolls also reduce the time required for localization in elevation. Finally, our model offers key insights to sound localization cues used by echolocating bats employing active head movements during echolocation.     

Active listening for spatial orientation in a complex auditory scene

To successfully negotiate a complex environment, an animal must control the timing of motor behaviors in coordination with dynamic sensory information. Here, we report on adaptive temporal control of vocal–motor behavior in an echolocating bat, Eptesicus fuscus, as it captured tethered insects close to background vegetation. Recordings of the bat's sonar vocalizations were synchronized with high-speed video images that were used to reconstruct the bat's three-dimensional flight path and the positions of target and vegetation. When the bat encountered the difficult task of taking insects as close as 10–20 cm from the vegetation, its behavior changed significantly from that under open room conditions. Its success rate decreased by about 50%, its time to initiate interception increased by a factor of ten, and its high repetition rate “terminal buzz” decreased in duration by a factor of three. Under all conditions, the bat produced prominent sonar “strobe groups,” clusters of echolocation pulses with stable intervals. In the final stages of insect capture, the bat produced strobe groups at a higher incidence when the insect was positioned near clutter. Strobe groups occurred at all phases of the wingbeat (and inferred respiration) cycle, challenging the hypothesis of strict synchronization between respiration and sound production in echolocating bats. The results of this study provide a clear demonstration of temporal vocal–motor control that directly impacts the signals used for perception.     

Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey

Echolocation sounds of Rhinolophus ferrumequinum nippon as they approached a fluttering moth (Goniocraspidum pryeri) were investigated using an on-board telemetry microphone (Telemike). In 40?% of the successful moth-capture flights, the moth exhibited distinctive evasive flight behavior, but the bat pursued the moth by following its flight path. When the distance to the moth was approximately 3-4?m, the bats increased the duration of the pulses to 65-95?ms, which is 2-3 times longer than those during landing flight (30-40?ms). The mean of 5.8 long pulses were emitted before the final buzz phase of moth capture, without strengthening the sound pressure level. The mean duration of long pulses (79.9?±?7.9?ms) corresponded to three times the fluttering period of G. pryeri (26.5?×?3?=?79.5?ms). These findings indicate that the bats adjust the pulse duration to increase the number of temporal repetitions of fluttering information rather than to produce more intense sonar sounds to receive fine insect echoes. The bats exhibited Doppler-shift compensation for echoes returning from large static objects ahead, but not for echoes from target moths, even though the bats were focused on capturing the moths. Furthermore, the echoes of the Telemike recordings from target moths showed spectral glints of approximately 1-1.5?kHz caused by the fluttering of the moths but not amplitude glints because of the highly acoustical attenuation of ultrasound in the air, suggesting that spectral information may be more robust than amplitude information in echoes during moth capturing flight.     

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.     

The communicative potential of bat echolocation pulses

Ecological constraints often shape the echolocation pulses emitted by bat species. Consequently some (but not all) bats emit species-specific echolocation pulses. Because echolocation pulses are often intense and emitted at high rates, they are potential targets for eavesdropping by other bats. Echolocation pulses can also vary within species according to sex, body size, age, social group and geographic location. Whether these features can be recognised by other bats can only be determined reliably by playback experiments, which have shown that echolocation pulses do provide sufficient information for the identification of sex and individual in one species. Playbacks also show that bats can locate conspecifics and heterospecifics at foraging and roost sites by eavesdropping on echolocation pulses. Guilds of echolocating bat species often partition their use of pulse frequencies. Ecology, allometric scaling and phylogeny play roles here, but are not sufficient to explain this partitioning. Evidence is accumulating to support the hypothesis that frequency partitioning evolved to facilitate intraspecific communication. Acoustic character displacement occurs in at least one instance. Future research can relate genetic population structure to regional variation in echolocation pulse features and elucidate those acoustic features that most contribute to discrimination of individuals.     

Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus

An echolocating bat actively controls the spatial acoustic information that drives its behavior by directing its head and ears and by modulating the spectro-temporal structure of its outgoing sonar emissions. The superior colliculus may function in the coordination of these orienting components of the bat's echolocation system. To test this hypothesis, chemical and electrical microstimulation experiments were carried out in the superior colliculus of the echolocating bat, Eptesicus fuscus, a species that uses frequency modulated sonar signals. Microstimulation elicited pinna and head movements, similar to those reported in other vertebrate species, and the direction of the evoked behaviors corresponded to the site of stimulation, yielding a map of orienting movements in the superior colliculus. Microstimulation of the bat superior colliculus also elicited sonar vocalizations, a motor behavior specific to the bat's acoustic orientation by echolocation. Electrical stimulation of the adjacent periaqueductal gray, shown to be involved in vocal production in other mammalian species, elicited vocal signals resembling acoustic communication calls of E. fuscus. The control of vocal signals in the bat is an integral part of its acoustic orienting system, and our findings suggest that the superior colliculus supports diverse and species-relevant sensorimotor behaviors, including those used for echolocation.     

Bat echolocation calls: adaptation and convergent evolution

Bat echolocation calls provide remarkable examples of 'good design' through evolution by natural selection. Theory developed from acoustics and sonar engineering permits a strong predictive basis for understanding echolocation performance. Call features, such as frequency, bandwidth, duration and pulse interval are all related to ecological niche. Recent technological breakthroughs have aided our understanding of adaptive aspects of call design in free-living bats. Stereo videogrammetry, laser scanning of habitat features and acoustic flight path tracking permit reconstruction of the flight paths of echolocating bats relative to obstacles and prey in nature. These methods show that echolocation calls are among the most intense airborne vocalizations produced by animals. Acoustic tracking has clarified how and why bats vary call structure in relation to flight speed. Bats using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localized accurately. Recent phylogenetic analyses based on gene sequences show that particular types of echolocation signals have evolved independently in several lineages of bats. Call design is often influenced more by perceptual challenges imposed by the environment than by phylogeny, and provides excellent examples of convergent evolution. Now that whole genome sequences of bats are imminent, understanding the functional genomics of echolocation will become a major challenge.     

The effect of preceding sonar emission on temporal integration in the bat, Megaderma lyra

The present study investigated whether and to which extent temporal integration in bats is influenced by echolocation behavior. One way to quantify temporal integration is to measure the detection threshold for a pair of short tone pips as a function of the temporal separation between the pips. To asses the effect of preceding sonar emission on temporal integration in the bat, Megaderma lyra, the detection thresholds of identical subjects were measured in a passive as well as in an active paradigm. In the passive paradigm, the presentation of the pip pairs was independent of the bats' sonar emissions; in the active paradigm, the presentation was triggered by the bats' sonar emissions. In both cases, the bats showed a very short integration time in the range of 100-200 micros. Moreover, the comparison of the active and passive results within each bat revealed no systematic differences in the two measuring paradigms. These results indicate that temporal integration is not influenced by echolocation. Simulations with a computer model of cochlear filtering based on measurements of M. lyra cochlear tuning suggest that the perceptual temporal integration is dominated by the integration of the cochlear filters.     

‘Compromise’ in Echolocation Calls between Different Colonies of the Intermediate Leaf-Nosed Bat (Hipposideros larvatus)

Each animal population has its own acoustic signature which facilitates identification, communication and reproduction. The sonar signals of bats can convey social information, such as species identity and contextual information. The goal of this study was to determine whether bats adjust their echolocation call structures to mutually recognize and communicate when they encounter the bats from different colonies. We used the intermediate leaf-nosed bats (Hipposideros larvatus) as a case study to investigate the variations of echolocation calls when bats from one colony were introduced singly into the home cage of a new colony or two bats from different colonies were cohabitated together for one month. Our experiments showed that the single bat individual altered its peak frequency of echolocation calls to approach the call of new colony members and two bats from different colonies adjusted their call frequencies toward each other to a similar frequency after being chronically cohabitated. These results indicate that the ‘compromise’ in echolocation calls might be used to ensure effective mutual communication among bats.     

Size Constancy in Bat Biosonar? Perceptual Interaction of Object Aperture and Distance

Perception and encoding of object size is an important feature of sensory systems. In the visual system object size is encoded by the visual angle (visual aperture) on the retina, but the aperture depends on the distance of the object. As object distance is not unambiguously encoded in the visual system, higher computational mechanisms are needed. This phenomenon is termed “size constancy”. It is assumed to reflect an automatic re-scaling of visual aperture with perceived object distance. Recently, it was found that in echolocating bats, the ‘sonar aperture’, i.e., the range of angles from which sound is reflected from an object back to the bat, is unambiguously perceived and neurally encoded. Moreover, it is well known that object distance is accurately perceived and explicitly encoded in bat sonar. Here, we addressed size constancy in bat biosonar, recruiting virtual-object techniques. Bats of the species Phyllostomus discolor learned to discriminate two simple virtual objects that only differed in sonar aperture. Upon successful discrimination, test trials were randomly interspersed using virtual objects that differed in both aperture and distance. It was tested whether the bats spontaneously assigned absolute width information to these objects by combining distance and aperture. The results showed that while the isolated perceptual cues encoding object width, aperture, and distance were all perceptually well resolved by the bats, the animals did not assign absolute width information to the test objects. This lack of sonar size constancy may result from the bats relying on different modalities to extract size information at different distances. Alternatively, it is conceivable that familiarity with a behaviorally relevant, conspicuous object is required for sonar size constancy, as it has been argued for visual size constancy. Based on the current data, it appears that size constancy is not necessarily an essential feature of sonar perception in bats.