Discrimination of fluttering targets by the FM-batPipistrellus stenopterus?

Summary Five bats of the speciesPipistrellus stenopterus were trained in a two-alternative forced-choice procedure to discriminate between two fluttering targets. The positive target simulated an insect with a 50 Hz wingbeat rate. The negative target was varied between 0 and 48 Hz.The bats were able to discriminate a target with 41 Hz from a target with 50 Hz with 75% correct choices. In the discrimination task, they typically emitted echolocation calls of 2–4 ms duration sweeping from 60 kHz to 30 kHz. The duty cycle (i.e. fraction of time filled with echolocation sounds) increased when the targets fluttered, but was always lower than 3%.The performance ofP. stenopterus in discriminating fluttering targets is comparable to that of bats emitting longer sounds with constant-frequency (CF) components and a higher duty cycle. The FM-sounds ofP. stenopterus are short compared with the period of the fluttering targets, and therefore make it difficult for the animal to measure the time interval between two acoustic glints. Other cues may be prominent, such as the frequency modulation by Doppler shifts from the moving blades.     

Classification of insects by echolocating greater horseshoe bats

Summary Echolocating greater horseshoe bats (Rhinolophus ferrumequinum) detect insects by concentrating on the characteristic amplitude- and frequency modulation pattern fluttering insects impose on the returning echoes. This study shows that horseshoe bats can also further analyse insect echoes and thus recognize and categorize the kind of insect they are echolocating.Four greater horseshoe bats were trained in a twoalternative forced-choice procedure to choose the echo of one particular insect species turning its side towards the bat (Fig. 1). The bats were able to discriminate with over 90% correct choices between the reward-positive echo and the echoes of other insect species all fluttering with exactly the same wingbeat rate (Fig. 4).When the angular orientation of the reward-positive insect was changed (Fig. 2), the bats still preferred these unknown echoes over echoes from other insect species (Fig. 5) without any further training. Because the untrained bats did not show any prey preference, this indicates that the bats were able to perform an aspect-anglein-dependent classification of insects.Finally we tested what parameters in the echo were responsible for species recognition. It turned out that the bats especially used the small echo-modulations in between glints as a source of information (Fig. 7). Neither the amplitudenor the frequencymodulation of the echoes alone was sufficient for recognition of the insect species (Fig. 8). Bats performed a pattern recognition task based on complex computations of several acoustic parameters, an ability which might be termed cognitive.Abbreviations AM amplitude modulation - CF constant frequency - FM frequency modulation - S+ positive stimulus - S- negative stimulus     

FIELD RECORDINGS OF ECHOLOCATION AND SOCIAL SIGNALS FROM THE GLEANING BAT MYOTIS SEPTENTRIONALIS

ABSTRACT

We recorded echolocation and ultrasonic social signals of the bat Myotis septentrionalis. The bats foraged for insects resting on or fluttering about an outdoor screen to which they were attracted by a ‘backlight’. The bats used nearly linearly modulated echolocation signals of high frequency (117 to 49 kHz, see Tables) with a weak second harmonic. The orientational signals from patrolling bats were about 2.4 ms in duration and occurred at a repetition rate of about 18 Hz (see Figure 3). The signals used by bats as they approached the screen were of shorter duration (0.72 ms) and occurred at higher rates (33.8 Hz) (Table 2 and Figure 4). We registered one feeding ‘buzz’ (Figure 5). We recorded social signals when two bats patrolled the hunting area. The social signals were characterized by their longer durations (6 ms, see Table 1), lower frequencies (70 to 30 kHz), and curvilinear sweeps (Figures 7 and 8). We calculated the source levels of orientational and social signals using the differences in arrival times at three microphones in a linear array (Figures 1 and 2). The source levels were on average 102 dB peSPL at 10 cm (Table 1). We could not calculate source levels of the signals used by bats as they approached the screen at close range, but these signals were much weaker (about 65 dB peSPL at the microphone).     

Discrimination of wingbeat motion by bats,correlated with echolocation sound pattern

Summary Bats of the species Rhinolophus rouxi, Hipposideros lankadiva and Eptesicus fuscus were trained to discriminate between two simultaneously presented artificial insect wingbeat targets moving at different wingbeat rates. During the discrimination trials, R. rouxi, H. lankadiva and E. fuscus emitted long-CF/FM, short-CF/FM and FM echolocation sounds respectively. R. rouxi, H. lankadiva and E. fuscus were able to discriminate a difference in wingbeat rate of 2.7 Hz, 9.2 Hz and 15.8 Hz, respectively, between two simultaneously presented targets at an absolute wingbeat rate of 60 Hz, using a criterion of 75% correct responses.The performance of the different bat species is correlated with the echolocation signal design used by each species, particularly with the presence and relative duration of a narrowband component preceding a broadband FM component. These results provide behavioral evidence supporting the hypothesis that bats that use CF/FM echolocation sounds have adaptations for the perception of insect wingbeat motion and that long-CF/FM species are more specialized for this task than short-CF/FM species.Abbreviations CF constant frequency - FM frequency modulation     

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.     

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.     

Neural ensemble coding of target identity in echolocating bats

Most insectivorous bats use echolocation to determine the identity of flying insects. Among the many target features that are so extracted, the insect's wingbeat pattern and frequency appear to serve as useful cues for identification. Biosonar pulses impinging on the fluttering wings of an insect are returned as echoes whose amplitudes vary with time, thus providing a characteristic signature of the insect. It has been shown previously that neurons in the inferior colliculus, a midbrain auditory nucleus, of the little brown bat respond to sound stimuli that mimic echoes from fluttering targets. To examine the manner in which target identity is represented in the inferior colliculus, an ensemble coding analysis using a filter-based approach was undertaken. The analysis indicates that a discrete subset of neurons in the inferior colliculus, the onset units, are strongly tuned to wingbeat frequencies of targets that the bat hunts, and that ensemble response reaches a maximum at a distinct phase of the prey capture maneuver: the late approach stage. On the basis of the analysis it is hypothesized that inferior colliculus neurons may play an important role in target detection-identification processing. Although ensemble coding of temporally sequenced information has not been analyzed in the auditory system so far, this study indicates that this method of coding may provide the information necessary to detect and identify targets during prey capture. Received: 4 December 1995 / Accepted in revised form: 19 April 1996     

Auditory fovea and Doppler shift compensation: adaptations for flutter detection in echolocating bats using CF-FM signals

Rhythmical modulations in insect echoes caused by the moving wings of fluttering insects are behaviourally relevant information for bats emitting CF-FM signals with a high duty cycle. Transmitter and receiver of the echolocation system in flutter detecting foragers are especially adapted for the processing of flutter information. The adaptations of the transmitter are indicated by a flutter induced increase in duty cycle, and by Doppler shift compensation (DSC) that keeps the carrier frequency of the insect echoes near a reference frequency. An adaptation of the receiver is the auditory fovea on the basilar membrane, a highly expanded frequency representation centred to the reference frequency. The afferent projections from the fovea lead to foveal areas with an overrepresentation of sharply tuned neurons with best frequencies near the reference frequency throughout the entire auditory pathway. These foveal neurons are very sensitive to stimuli with natural and simulated flutter information. The frequency range of the foveal areas with their flutter processing neurons overlaps exactly with the frequency range where DS compensating bats most likely receive echoes from fluttering insects. This tight match indicates that auditory fovea and DSC are adaptations for the detection and evaluation of insects flying in clutter.     

Echolocation behavior of rufous horseshoe bats hunting for insects in the flycatcher-style

Summary The echolocation behavior ofRhinolophus rouxi when waiting for insects on a perch and when pursuing them in short hunting flights is described. It reveals that flycatcher-style hunting is one foraging strategy utilized by this species. It also suggests that bats use fluttering target information to classify their prey.     

The detection of phantom targets in noise by serotine bats; negative evidence for the coherent receiver

Summary Using a target simulator three serotine bats,Eptesicus serotinus, were trained to judge whether a phantom target was present or absent. The echolocation sounds emitted by the bats during the detection were intercepted by a microphone, amplified and returned by a loudspeaker as an artificial echo, with a delay of 3.2 ms and a sound level determined by the overall gain and cry amplitude. The cry level of each pulse was measured and the echo level received by the bat was calculated. The target was presented in 50% of the trials and the gain adjusted using conventional up/down procedures. Under these conditions between 40 and 48 dB peSPL were required for 50% detection (Figs. 2, 3).In a subsequent experiment the phantom target was masked with white noise (N_o) with a spectrum level of –113 dB re. 1 Pa·Hz^–1/2. The thresholds were increased by 7–14 dB. Energy density (S) of a single pulse was measured and used to estimate S/N_o, which ranged from 36–49 dB at threshold. Theoretically the coherent receiver model predicts the ratio between hits and false alarms observed for the bats at a S/N_o of ca. 1–2 dB. Since the bats require 40–50 dB higher S/N_o (Fig. 3), this is taken as negative evidence for coherent reception (cross correlation).Furthermore, a strong sensitivity to clutter was found since there seemed to exist a fixed relationship between thresholds and clutter level.Abbreviations C clutter - Nbw noise in a specified bandwidth - No noise in i Hz bandwidth - peSPL peak equivalent sound pressure level - S signal energy - SD standard deviation - Y/N Yes/No psychometry - 2AFC two alternative forced choice psychometry     

Fluttering target detection in Hipposiderid bats

Summary Two species of Hipposiderid bats,Hiposideros speoris andH. lankadiva, which both emit short CF-FM echolocation calls, were trained in a two-alternative forced-choice procedure to discriminate between an oscillating target and a motionless one. Two different targets were used: (1) the membrane of a low-frequency loudspeaker, producing sinusoidal frequency- and amplitude modulations and (2) a small rotating propeller, which produced short acoustical glints. In both casesH. lankadiva learned to discriminate between the oscillating and the motionless target. When the loudspeaker was used, thresholds for minimal modulation depths at different oscillation frequencies were determined. At loudspeaker membrane oscillation frequencies of 10 to 100 Hz the 75% correct thresholds lay between 90 and 300 Hz (Fig. 3).H. speoris could not be trained to react to the moving membrane, even at very high oscillation amplitudes. When the rotating propeller was the positive target, however,H. speoris learned very quickly to discriminate it from a motionless one. By decreasing the rotation speed it was possible to measure the minimal detectable glint-frequency for each bat. It lay at 67, 44, and just under 15 glints/s for the three specimens (Fig. 4). During the discrimination task both bat species increased their duty-cycle just prior to a decision by emitting long sequences of echolocation calls with short inter-pulse intervals. The duration of individual pulses remained relatively constant (Figs. 6 and 7). Possible mechanisms for discrimination of the oscillating targets are discussed and the importance of glints in the echoes for fluttering target detection is emphasized.Abbreviations A₀ amplitude of loudspeaker membrane oscillation - AM amplitude modulation - CF constant frequency - DC duty-cycle - FM frequency modulation - f _max maximal frequency modulation depth in echo - PD pulse duration - PI pulse interval - f _osc oscillation frequency     

Tonotopical organization and pure tone response characteristics of single units in the auditory cortex of the Greater Horseshoe Bat

Summary Tonotopical organization and frequency representation in the auditory cortex of Greater Horseshoe Bats was studied using multi-unit recordings.The auditory responsive cortical area can be divided into a primary and a secondary region on the basis of response characteristics forming a core/belt structure.In the primary area units with best frequencies in the range of echolocation signals are strongly overrepresented (Figs. 6–8). There are two separate large areas concerned with the processing of the two components of the echolocation signals. In one area frequencies between the individual resting frequency and about 2 kHz above are represented, which normally occur in the constant frequency (CF) part of the echoes (CF-area), in a second one best frequencies between resting frequency and about 8 kHz below are found (FM-area).In the CF-area tonotopical organization differs from the usual mammalian scheme of dorso-ventral isofrequency slabs. Here isofrequency contours are arranged in a semicircular pattern.The representation of the cochlear partition (cochleotopic organization) was calculated. In the inferior colliculus and auditory cortex there is a disproportionate representation of the basilar membrane. This finding is in contradiction to the current opinion that frequency representation in the auditory system of Horseshoe Bats is only determined by the mechanical tuning properties of the basilar membrane.Response characteristics for single units were studied using pure tone stimuli. Most units showed transient responses. In 25% of units response characteristics depended on the combination of frequency and sound pressure level used.Frequency selectivity of units with best frequencies in the range of echolocation sounds is very high. Q-10dB values of up to 400 were found in a small frequency band just above resting frequency.Abbreviations BF best frequency - CF constant frequency - FM frequency modulated - MT minimal threshold     

Spectral and temporal gating mechanisms enhance the clutter rejection in the echolocating bat,Rhinolophus rouxi

Summary Doppler shift compensation behaviour in horseshoe bats, Rhinolophus rouxi, was used to test the interference of pure tones and narrow band noise with compensation performance. The distortions in Doppler shift compensation to sinusoidally frequency shifted echoes (modulation frequency: 0.1 Hz, maximum frequency shift: 3 kHz) consisted of a reduced compensation amplitude and/or a shift of the emitted frequency to lower frequencies (Fig. 1).Pure tones at frequencies between 200 and 900 Hz above the bat's resting frequency (RF) disturbed the Doppler shift compensation, with a maximum of intererence between 400 and 550 Hz (Fig. 2). Minimum duration of pure tones for interference was 20 ms and durations above 40 ms were most effective (Fig. 3). Interfering pure tones arriving later than about 10 ms after the onset of the echolocation call showed markedly reduced interference (Fig. 4). Doppler shift compensation was affected by pure tones at the optimum interfering frequency with sound pressure levels down to –48 dB rel the intensity level of the emitted call (Figs. 5, 6).Narrow bandwidth noise (bandwidth from ± 100 Hz to ± 800 Hz) disturbed Doppler shift compensation at carrier frequencies between –250 Hz below and 800 Hz above RF with a maximum of interference between 250 and 500 Hz above resting frequency (Fig. 7). The duration and delay of the noise had similar influences on interference with Doppler shift compensation as did pure tones (Figs. 8, 9). Intensity dependence for noise interference was more variable than for pure tones (-32 dB to -45 dB rel emitted sound pressure level, Fig. 10).The temporal and spectral gating in Doppler shift compensation behaviour is discussed as an effective mechanism for clutter rejection by improving the processing of frequency and amplitude transients in the echoes of horseshoe bats.Abbreviations CF constant frequency - FM frequency modulation - RF resting frequency - SPL sound pressure level     

马铁菊头蝠幼蝠能够辨别种群间回声定位声波差异

蝙蝠的回声定位声波普遍存在地理变化,然而尚不清楚幼蝠在扩散前能否辨别不同种群间的声波差异。本文采用"双选择声学回放实验",研究马铁菊头蝠(Rhinolophus ferrumequinum)幼蝠(1月龄)对回声定位声波地理变化的辨别能力及行为反应。采用4个行为参数衡量幼蝠对本种群(CC)与外种群(JN)回声定位声波的行为反应:每一回放室飞入的次数、飞行时间、停留次数、探测时间。Mann-Whitney U tests表明,马铁菊头蝠1月龄个体对回放声波的行为反应,除每一回放室停留的次数外,其他3个参数均存在显著差异(P0.05),且在本种群声波回放室(CC)的飞行次数和时间以及探测时间均高于外种群声波回放室(JN)。对4个行为参数进行主成分分析,Mann-Whitney U tests表明,回放本种群声波(CC)与外种群声波(JN)之间,第一主成分得分(PC1)存在显著差异(P0.01)。配对T检验表明,幼蝠对本种群声波反应更加强烈(PC1:t10=5.25,P0.001;PC2:t10=2.34,P0.05)。本研究说明马铁菊头蝠幼蝠能够辨别不同种群间回声定位声波的差异。     

Dietary composition and echolocation call design of three sympatric insectivorous bat species from China

Studying the diet of echolocating, insectivorous bats can provide important insights into their foraging behaviors and ecological constraints they are facing. By examining an extensive data set covering a period of 2 years, the present study identifies the dietary composition of three sympatric insectivorous bat species in rural areas of Beijing municipality. Each species clearly has different preferences for particular food items. Greater horseshoe bats, Rhinolophus ferrumequinum, preferred to catch nocturnal, actively flying insects, mostly moths (Lepidoptera), and to a lesser percentage flies (Diptera), beetles (Coleoptera), and flying ants and termites (Hymenoptera). Other nocturnal insects which do not exhibit any perceptible wing movements, such as true bugs (Homoptera), or strictly diurnal insects that hardly ever fly in the dark, such as grasshoppers (Orthoptera) and dragon- and damselflies (Odonata), were never found in droppings of horseshoe bats. Large mouse-eared bats, Myotis chinensis, preferentially glean relatively large terrestrial prey of the order Coleoptera (mostly carabid beetles) and Orthoptera, whereas greater tube-nosed bats, Murina leucogaster, consume predominantly smaller, diurnal Coleoptera (mostly soldier beetles, Cantharidae, and ladybugs, Coccinellidae). Our findings also indicate previously not described, significant spectro-temporal differences in the echolocation signals of M. chinensis and M. leucogaster. The results suggest that in our study area the dramatic differences in the dietary composition of these three bat species are mainly based upon differences in their foraging behaviors, including differences in their echolocation signal structure. The dietary data provide important background information for conservational efforts, such as habitat protection.     

Flight performance, echolocation and foraging behaviour in noctule bats Nyctalus noctula

The noctule Nyctulus noctula (Schreber, 1774) is a relatively large (c. 25 g) insectivorous bat which catches insects on the wing (by aerial hawking). Emergence at a maternity roost was earliest relative to sunset when females were lactating, and bats may then have risked predation by flying at higher light levels during a period of high energy demand. Flight performance was quantified by using stereophotogrammetry. At feeding sites bats flew at 6.0 ± 2.1 m/s. This was faster than predicted minimum power speed (V _mp), and either between V _mp and maximum range speed (V _mr), or close to their predicted V _mr, depending on which aerodynamic model of flight power requirements was used. The echolocation behaviour of noctules is flexible. Long duration, low frequency calls (c. 20 kHz) with little frequency modulation were emitted while cruising, but at foraging sites the calls became more frequency-modulated. As the noctule is traditionally thought of as using low frequency echolocation, it was expected to receive weak echoes from small targets and therefore to specialize in eating large insect prey. Although the bats ate mainly beetles, large numbers of small dipterans were also eaten. The noctule is probably able to detect such small items because, when foraging, its calls become broadband and sweep from high frequencies. Higher harmonics are also present, and these may assist in the detection of small prey. In noctules, as in many bats, there appears to be a 1:1 link between wingbeat and call production during the search phase of foraging.     

Audiovocal interactions during development? Vocalisation in deafened young horseshoe bats vs. audition in vocalisation-impaired bats

Summary Horseshoe bats (Rhinolophus rouxi) were deafened in their 3rd–5th postnatal week. Subsequently their vocalisations were monitored to evaluate the impact of audition on the development of echolocation pulses. Hearing impairment affected the echolocation pulses as follows: the frequency of the constant frequency (CF) component was altered by between + 4 kHz and – 14 kHz, and the dominance of the second harmonic of the pulses was neutralised by a relative increase in intensity of the first and third harmonics.A second experiment focused on possible influences of acoustical self-stimulation with echolocation pulses on the establishment of auditory fovea representation in the inferior colliculus (IC). Frequency control of echolocation pulses was disrupted by larynx denervation. Thereafter, the bats produced multiharmonic echolocation signals (4–11 harmonics) varying in frequency. IC tonotopy, however, as monitored by stereotaxic electrophysiology, showed the same developmental dynamics as seen in control specimens (Fig. 10).Both experiments indicate that throughout postnatal development echolocation pulses are under auditory feedback control, whereas maturation of the auditory fovea and shifts in its frequency tuning represent an innate process. The significance of this postnatal development might be the adjustment of the vocal motor system of each bat to the frequency of its personal auditory fovea.Abbreviations CF constant frequency - CF1, CF2, CF3 harmonics of pure tone components of the echolocation pulses - FM frequency modulation - IC inferior colliculus of the midbrain     

Does body mass restrict call peak frequency in echolocating bats?

1. Echolocation is the ability of some animals to orient themselves through sound emission and interpretation of the echoes. This is bats’ main sense for orientation and recognising biotopes that provide food, water, and roosts. It is widely accepted that echolocation call frequency is related to body mass, and this relationship has been described as the ‘allometric hypothesis’, which proposes a negative correlation between these variables.
2. There is evidence that, in many cases, the allometric hypothesis does not apply. Additionally, studies supporting this hypothesis were done at the family level, resulting in a broad range of correlation values with r ranging from −0.36 to −0.76, and only insectivorous bats were included. Due to the notable exceptions and the lack of a quantitative synthesis of this hypothesis including all echolocating bats, we evaluated the allometric hypothesis of echolocation calls for this group.
3. Using a meta-analysis and phylogenetic generalised least-squares techniques, we evaluated the relationship between echolocation call peak frequency and the body mass of bats.
4. We found a negative relationship between body mass and echolocation call peak frequency for the 85 bat species that were included in our analysis (r = −0.3, p = 0.005). The relationship was consistent when we analysed the data at the insectivorous guild level, and in bats belonging to the families Vespertilionidae, Rhinolophidae, Emballonuridae, and the genus Myotis. However, the wide range of r values suggests that the strength of the relationship between peak frequency and body mass varies within the order Chiroptera.
5. Our results support the allometric hypothesis of sound production in echolocating bats. However, the low coefficient we found suggests that factors other than body mass may influence the peak frequency of echolocation calls produced by bats.

     

Neural coding of echo-envelope disparities in echolocating bats

The effective use of echolocation requires not only measuring the delay between the emitted call and returning echo to estimate the distance of an ensonified object. To locate an object in azimuth and elevation, the bat’s auditory system must analyze the returning echoes in terms of their binaural properties, i.e., the echoes’ interaural intensity and time differences (IIDs and ITDs). The effectiveness of IIDs for echolocation is undisputed, but when bats ensonify complex objects, the temporal structure of echoes may facilitate the analysis of the echo envelope in terms of envelope ITDs. Using extracellular recordings from the auditory midbrain of the bat, Phyllostomus discolor, we found a population of neurons that are sensitive to envelope ITDs of echoes of their sonar calls. Moreover, the envelope-ITD sensitivity improved with increasing temporal fluctuations in the echo envelopes, a sonar parameter related to the spatial statistics of complex natural reflectors like vegetation. The data show that in bats envelope ITDs may be used not only to locate external, prey-generated rustling sounds but also in the context of echolocation. Specifically, the temporal fluctuations in the echo envelope, which are created when the sonar emission is reflected from a complex natural target, support ITD-mediated echolocation.