Lee A. Miller

The echolocation and hunting behavior of the bat,Pipistrellus kuhli

SummaryThe echolocation and hunting behavior ofPipistrellus kuhli was studied in the field using multi-exposure photography synchronized with high-speed tape recordings. During the search phase, the bats used 8–12 ms signals with sweeps (sweep width 3–6 kHz) and pulse intervals near 100 ms or less often near 200 ms (Figs. 1 and 2). The bats seemed to have individual terminal frequencies that could lie between 35 and 40 kHz. The duty cycle of searching signals was about 8%. The flight speed of hunting bats was between 4.0 and 4.5 m/s. The bats reacted to insect prey at distances of about 70 to 120 cm. Given the flight speed, the detection distance was estimated to about 110 to 160 cm. Following detection the bat went into the approach phase where the FM sweep steepened (to about 60 kHz bandwidth) and the repetition rate increased (to about 30 Hz). The terminal phase or ‘buzz’, which indicates prey capture (or attempted capture), was composed of two sections. The first section contained signals similar to those in the approach phase except that the pulse duration decreased and the repetition rate increased. The second section was characterized by a sharp drop in the terminal frequency (to about 20 kHz) and by very short pulses (0.3 ms) at rates of up to 200 Hz (Figs. 1 and 3). Near the beginning of the buzz the bat prepared for capturing the prey by extending the wings and forming a tail pouch (Fig. 4). A pause of about 100 ms in sound emission after the buzz indicated a successful capture (Fig. 4). Pulse duration is discussed in relation to glint detection and detection distance. It is argued that the minimum detection distance can be estimated from the pulse duration as the distance where pulse-echo overlap is avoided.

Echolocation in two very small bats from Thailand Craseonycteris thonglongyai and Myotis siligorensis

SummaryThe echolocation and hunting behavior of two very small bats, Craseonycteris thonglongyai (Hill) and Myotis siligorensis (Horsfield), from Thailand, were investigated using multiflash photographs, video, and high-speed tape recordings with a microphone array that allowed determination of distance and direction to the bats. C. thonglongyai is the worlds smallest mammal and M. siligorensis is only slightly larger. Both bats hunted insects in open areas. The search signals of C. thonglongyai were 3.5 ms long multiharmonic constant frequency (CF) signals with a prominent second harmonic at 73 kHz repeated at around 22 Hz. The band width (BW) of the short terminal frequency modulated (FM) sweep increased during the very short approach phase. In the final buzz the CF component disappeared, the duration decreased to 0.2 ms, and the repetition rate increased to 215 Hz (Figs. 2, 3, 4). There was no drop in frequency in the buzz. The video recordings of C. thonglongyai indicated that it seizes insects directly with the mouth (Fig. 1). M. siligorensis produced 5.4 ms long CF search signals at 66 kHz. The repetition rate was around 13 Hz. In the approach phase an initial broad band FM sweep was added. The buzz consisted of two phases, buzz I and buzz II. Buzz 11 was characterized by short cry durations (around 0.3 ms), a constant high repetition rate (185 Hz), a distinct drop in frequency, and a prominent second harmonic (Figs. 5, 6, 7). The drop in frequency, apparently typical of vespertilionid bats, has been explained by physiological limitations in sound production. However, C. thonglongyai produced very short signals at very high repetition rates without any frequency drop. The drop may be of adaptive value since it enables M. siligorensis to produce very short signals with high sweep rates. The drop moves the pronounced second harmonic into the frequency range of most interest to the bat (Fig. 7D). The sweep rate in this frequency range may now increase to twice the maximum rate that the vocal cords can produce directly. C. thonglongyai and M. siligorensis belong to different superfamilies, Emballonuroidea and Vespertilionoidea, respectively. In spite of their phylogenetic distance they produce strikingly similar search signals of narrow BW around 70 kHz with high source levels (100–115 dB peSPL peak equivalent sound pressure level). We argue that the signal resemblance is due to the similarity in size and hunting behavior of the two bats both hunting insects in open areas. High frequencies are heavily attenuated in air, but because of their small size the bats are restricted to hunting small insects which only reflect echoes at high frequencies. Thus, the emitted frequency is probably the lowest possible given the prey size. Hence, the two bats can only maximize the range of their sonar by decreasing the BW and emitting high intensities.

Echolocation signals of the bat Eptesicus serotinus recorded using a vertical microphone array: effect of flight altitude on searching signals

Abstractu2002The acoustic behaviour of Eptesicus serotinus was investigated in the field using a 13.5-m vertical, linear microphone array that allowed for simultaneous recordings at three different heights and for the calculation of flight altitude and distance from the array. Recordings were made at two locations that differed in bat species diversity. E. serotinus hunted on average at an altitude of 10.7 m (±2.7) at one location and 6.8 m (±3.6) at the other location. Search signals were 5–17 ms long depending on flight altitude, and consisted of two to three frequency-modulated harmonics. For bats flying below 8–10 m altitude, signal duration decreased with decreasing flight altitude, whereas signal interval, terminal frequency, peak frequency and frequency range of the first harmonic increased. Above 8–10 m flight altitude, the signal parameters were fairly constant. The –10 dB bandwidth and duty cycle did not change with flight altitude. Source levels were calculated to between 121 and 125 dB peSPL re 20 µPa at 10 cm. For bats flying higher than 9 m, the microphone placed 1.5 m above the ground recorded significantly reduced signal durations and frequency ranges of the first harmonic compared to the same signals recorded with the microphones at heights of 7 or 15 m. We caution the use of ground recordings to fully describe the echolocation signals of high-flying bats. We demonstrate that flight altitude significantly influences the structure of sonar signals from E. serotinus.

Echolocation by two foraging harbour porpoises (Phocoena phocoena)

SUMMARY Synchronized video and high-frequency audio recordings of two trained harbour porpoises searching for and capturing live fish were used to study swimming and echolocation behaviour. One animal repeated the tasks blindfolded. A splash generated by the fish being thrown into the pool or– in controls – by a boat hook indicated prey and stimulated search behaviour. The echolocation sequences were divided into search and approach phases. In the search phase the porpoises displayed a clear range-locking behaviour on landmarks, indicated by a distance-dependent decrease in click interval. Only in trials with fish was the search phase followed by an approach phase. In the initial part of the approach phase the porpoises used a rather constant click interval of around 50 ms. The terminal part started with a sudden drop in click interval at distances around 2–4 m. Close to the prey the terminal part ended with a buzz, characterized by constant click intervals around 1.5 ms. The lag time in the search and the initial part of the approach phase seems to be long enough for the porpoise to process echo information before emitting the next click (pulse mode). However, we assume that during the buzz lag times are too short for pulse mode processing and that distance information is perceived as a `pitch with a `frequency corresponding to the inverse of the two-way transit time (pitch mode). The swimming speed of the animal was halved when it was blindfolded, while the click intervals hardly changed, resulting in more clicks emitted per metre swum.

The influence of arctiid moth clicks on bat echolocation; jamming or warning?

Summary1.Many arctiid and ctenuchid moths produce clicking sounds in response to the ultrasonic cries of bats. Clicks were recorded from the two arctiid moth speciesArctia caja, the garden tiger, andPhragmatobia fuliginosa, the ruby tiger. The threshold for eliciting clicks was around 60 to 75 dB pe SPL in both species.A. caja produced single clicks, andP. fuliginosa bursts of clicks. The maximum intensity of the clicks was 90 to 94 dB pe SPL at 5 cm forA. caja and 85 dB pe SPL at 5 cm forP. fuliginosa. The clicks contain most energy in the frequency range from 40 to 80 kHz (Figs. 2, 3).2.Pipistrelle bats (Pipistrellus pipistrellus) were trained to sit on a platform and discriminate the difference in range,Δd, to two targets. The minimum Δd the bats could discriminate with more than 75% success rate was 1.5 cm.3.The targets had built-in electrostatic loudspeakers through which different sounds could be played back to the bat. Playback of arctiid moth clicks from both targets did not disturb the bats discrimination accuracy. The success rate did not decrease at anyΔd, and the minimumΔ d in the presence of clicks was 1 cm.4.The clicks played from both loudspeakers did not influence the acoustic behavior or discrimination behavior of the bats in any obvious way. In all trials the bats went through a period with long (3 ms) slowly repeated (12–15 pulses/s) cries, a period with shorter cries and increased PRR (20 pulses/s) in which the decision seemed to be made, and finally a period with very short cries (0.5 ms) repeated at rates of up to 150 pulses/s (Figs. 4 and 5). The cries were FM sweeps from 120 kHz to 55 kHz with a second harmonic, which was strongest in the short cries.5.The bats response to the playback of different sounds, such as noise and recorded bat cries, from either the left or right loudspeaker, suggested that the bats reacted to clicks as if they were noise. The playback of sounds from only one speaker at a time decreased the bats success rate, since the bats were attracted to the sounds (Figs. 6 and 7).6.A secretion from the cervical glands ofA. caja, which contains choline ester, was given to a bat if it crawled towards a clicking target. Both bats tested in this way learned to associate the clicks with a noxious reward and avoided the clicks after just one or two trials (Fig. 8).7.These results suggest that the function of the garden tiger and ruby tiger clicks in nature is to warn the bat of the moths distastefulness, and not to ‘jam’ the bats sonar system.

High Intensity Narwhal Clicks

The hypothesis that some odontocetes use their sonar not only to find prey, but also to debilitate it (Norris and Mohl, 1983) requires that odontocetes produce sound pressures in excess of 230 dB re. 1 μPa (Zaegaesky, 1987; Hubbs and Rechnitzer, 1972). While maximum source levels1 (SL) of clicks recorded from trained Tursiops (Au et al., 1974) and Delphinapterus (Au et al., 1987) are only a few dB short of this value, there is a gap of 50 to 120 dB between the debilitation threshold and the SL’s reported for odontocete clicks in nature (Levenson, 1974; Watkins and Schevill, 1974; Watkins, 1980a, b).

Auditory input to motor neurons of the dorsal longitudinal flight muscles in a noctuid moth (Barathra brassicae L.)

SummaryMotor neurons innervating the dorsal longitudinal muscles of a noctuid moth receive synaptic input activated by auditory stimuli. Each ear of a noctuid moth contains two auditory neurons that are sensitive to ultrasound (Fig. 1). The ears function as bat detectors. Five pairs of large motor neurons and three pairs of small motor neurons found in the pterothoracic ganglia innervate the dorsal longitudinal (depressor) muscles of the mesothorax (Figs. 2 to 5). In non-flying preparations the motor neurons receive no oscillatory synaptic input. Synaptic input to a cell resulting from ultrasonic stimulation is consistent and can be either depolarizing or hyperpolarizing (Figs. 6 to 9). Quiescent neurons only rarely fire a spike in response to auditory inputs. Motor neurons in flying preparations receive oscillatory synaptic drive from the flight pattern generator and usually fire a spike for each wingbeat cycle (Figs. 10 to 12). Ultrasonic stimulation can provide augmented synaptic drive causing a neuron to fire two spikes per wingbeat cycle thus increasing flight vigor (Fig. 11). The same stimulus presented on another occasion can also inhibit spiking in the same motor neuron, but the rhythmic drive remains (Fig. 12). Thus, when the flight oscillator is running auditory stimuli can modulate neuronal responses in different ways depending on some unknown state of the nervous system. Sound intensity is the only stimulus parameter essential for activating the auditory pathway to these motor neurons. The intensity must be sufficient to excite two or three auditory neurons. The significance of these responses in relation to avoidance behavior to bats is discussed.

Directional hearing in the locustSchistocerca gregaria Forskål (Acrididae, Orthophera)

SummaryAt 2 kHz, 3.5 kHz and 5 kHz the locust ear functions as a mixed pressure and pressure-gradient receiver. The ear is inherently directional at these frequencies. The directional characteristics are independent of the amount of body tissue (Figs. 6 and 7). At 15 kHz the locust ear functions mostly as a pressure receiver, and is inherently non-directional (Fig. 6d). Hearing is, however, directional at 15 kHz owing to diffraction caused by the body (Fig. 1). Auditory thresholds are influenced by the amount of body tissue at frequencies from 2 to 15 kHz (Fig. 8). At frequencies less than 6 kHz the sound conducted through the body is attenuated by 1 to 8 dB depending on the amount of body tissue. At frequencies greater than 12 kHz the sound conducted through the body is attenuated by up to 18 dB, and the attenuation is only slightly influenced by body tissue (Fig. 2). The attenuation of sound conducted through the body is independent of the direction of sound, but may be affected by the amount of tissue between the ears (Fig. 4). The tissue in the body appears to act as a ‘resistive’ element, which introduces a phase shift in the sound conducted through the body relative to that striking the front side of the tympanum. Body tissue can set the level of sensitivity, but does not influence the receiver characteristics of the ear.

The behaviour of flying green lacewings, Chrysopa carnea, in the presence of ultrasound

Abstract Green lacewings stop flying in response to ultrasound. The behavioural response begins with folding of the wings, which starts about 40 msec following stimulation. About 66 msec later potentials from the indirect flight muscles cease. Insects resume their stationary flight after a certain period of time, which is dependent on the stimulus duration. Consistent responses occur only during the insects night. Stimuli eliciting the cessation of flight have the following parameters: frequencies of from 15 to 140 kHz, intensities above 55 dB, single pulses of from 1 to 100 msec in duration, and pulse sequences having repetition rates up to 70 or 80 pulses/sec. Pulse sequences from 0·1 to 1 sec produce response durations that last longer than the stimulus, whereas pulse sequences longer than 1 sec, elicit responses that do not last as long as the stimulus. The duration of the response remains nearly constant when single ultrasonic pulses are given. This flight cessation behaviour provides a mechanism whereby green lacewings can avoid predation by bats. Responses seen in green lacewings are compared with similar responses in noctuid moths.

Parallel processing of afferent input by identified interneurones in the auditory pathway of the noctuid moth Noctua pronuba (L.).

Summary1.Interneurones 501 and 504 are identified sound-sensitive interneurones in the pterothoracic ganglion of the noctuid moth Noctua pronuba (Fig. 1). Both neurones receive monosynaptic input from the A1 afferent (Figs. 2, 3) and experiments with current injection suggest that the synapse is chemical (Fig. 4). The EPSPs evoked in either IN 501 or 504 by the A1 afferent do not facilitate (Fig. 5A, B).2.Temporal integration in INs 501 and 504 was compared by presenting the moth with tones at repetition rates found in the search, approach and terminal phases of the echolocating call of a hunting bat (Figs. 6, 7, 8, 9). INs 501 and 504 differ in their capacity to resolve stimulus repetition rates because the mean decay times of their compound EPSPs differ by a factor of three (Fig. 10), although both interneurones receive monosynaptic input from the A1 afferent.3.The features extracted from the authentic, prerecorded, call of an echolocating bat at the level of the pterothoracic ganglion were examined by recording sequentially from a range of interneurones in the same preparation (Fig. 11). The capacity of INs 501 and 504 to encode the various phases of the call was examined in the light of their measured mean decay times and related to the avoidance behaviour of the insect (Figs. 12, 13).