Annemarie Surlykke

Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory

Echolocation signals were recorded from big brown bats, Eptesicus fuscus, flying in the field and the laboratory. In open field areas the interpulse intervals (IPI) of search signals were either around 134 ms or twice that value, 270 ms. At long IPIs the signals were of long duration (14 to 18-20 ms), narrow bandwidth, and low frequency, sweeping down to a minimum frequency (Fmin) of 22-25 kHz. At short IPIs the signals were shorter (6-13 ms), of higher frequency, and broader bandwidth. In wooded areas only short (6-11 ms) relatively broadband search signals were emitted at a higher rate (avg. IPI= 122 ms) with higher Fmin (27-30 kHz). In the laboratory the IPI was even shorter (88 ms), the duration was 3-5 ms, and the Fmin 30- 35 kHz, resembling approach phase signals of field recordings. Excluding terminal phase signals, all signals from all areas showed a negative correlation between signal duration and Fmin, i.e., the shorter the signal, the higher was Fmin. This correlation was reversed in the terminal phase of insect capture sequences, where Fmin decreased with decreasing signal duration. Overall, the signals recorded in the field were longer, with longer IPIs and greater variability in bandwidth than signals recorded in the laboratory.

How Some Insects Detect and Avoid Being Eaten by Bats: Tactics and Countertactics of Prey and Predator

S insects have evolved audition and evasive behaviors in response to selective pressure from bats, and other insects were preadapted to detecting ultrasonic signals. Some bats have evolved in turn, improving the range or resolution of sonar signals and serendipitously making them less detectable by insects. In other words, there is a kind of evolutionary escalation going on between bats and insects. Our aim with this review is to present the complex interactions between echolocating bats and insects with bat-detecting ears and show how these interactions may be advantageous for predator or prey. To document our examples, we cite mostly newer studies and reviews in which the reader can find references to original works. Insects occupied all terrestrial habitats at least 300 million years ago, long before bats appeared in the Eocene, about 50 million years ago. Ears have appeared independently 19 times in the class Insecta. In the period before bats, ears and complex acoustical behaviors appeared independently in at least seven orders of insects (Hoy et al. 1989, Robert et al. 1992, Yager 1999). Antibat tactics, which must have appeared in insects since the Eocene, are now known in members of four orders: Lepidoptera (moths and nocturnal butterflies), Orthoptera (crickets), Dictyoptera (praying mantids), and Neuroptera (green lacewings), and possibly also in the Diptera (flies) and Coleoptera (beetles). Insect tympanal organs, or ears, consist basically of an external, thin membrane (the tympanum) and associated internal air sacs, or tracheae. The auditory (sensory) cells attach to the tympanum or to an internal membrane (Yager 1999). Tympanal organs of most modern tympanate insects respond to a wide band of frequencies extending well into the ultrasonic range (above 20 kHz),as was probably true for preEocene tympanate insects as well. Tympanate insects are physically small animals that can produce high-frequency sounds more efficiently; hence, high frequencies are used by many insects for acoustical communication between conspecifics. Consequently, many sonorous insects were preadapted to the evolution of bats (Hoy 1992). According to one possible scenario, a vast larder of nocturnal, flying insects awaited exploitation, and a flying mammal, the microchiropteran bat, was one successful exploiter. Echolocation, or biosonar, was a prerequisite for success in darkness, and even the first nocturnal bats probably used it (see Hoy 1992). Most of the nearly 700 microchiropteran bat species eat insects that they detect using biosonar (Schnitzler and Kalko 2001). However, bat biosonar has two major disadvantages: attenuation and forewarning. The frequencies used by echolocating bats range generally from 20 kHz to 100 kHz, with some outliers using frequen-

Sperm whale clicks: Directionality and source level revisited

In sperm whales (Physeter catodon L. 1758) the nose is vastly hypertrophied, accounting for about one-third of the length or weight of an adult male. Norris and Harvey [in Animal Orientation and Navigation, NASA SP-262 (1972), pp. 397-417] ascribed a sound-generating function to this organ complex. A sound generator weighing upward of 10 tons and with a cross-section of 1 m is expected to generate high-intensity, directional sounds. This prediction from the Norris and Harvey theory is not supported by published data for sperm whale clicks (source levels of 180 dB re 1 microPa and little, if any, directionality). Either the theory is not borne out or the data is not representative for the capabilities of the sound-generating mechanism. To increase the amount of relevant data, a five-hydrophone array, suspended from three platforms separated by 1 km and linked by radio, was deployed at the slope of the continental shelf off Andenes, Norway, in the summers of 1997 and 1998. With this system, source levels up to 223 dB re 1 microPa peRMS were recorded. Also, source level differences of 35 dB for the same click at different directions were seen, which are interpreted as evidence for high directionality. This implicates sonar as a possible function of the clicks. Thus, previously published properties of sperm whale clicks underestimate the capabilities of the sound generator and therefore cannot falsify the Norris and Harvey theory.

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.

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.

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 bats sonar vocalizations were synchronized with high-speed video images that were used to reconstruct the bats 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 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.

Vespertilionid bats control the width of their biosonar sound beam dynamically during prey pursuit

Animals using sound for communication emit directional signals, focusing most acoustic energy in one direction. Echolocating bats are listening for soft echoes from insects. Therefore, a directional biosonar sound beam greatly increases detection probability in the forward direction and decreases off-axis echoes. However, high directionality has context-specific disadvantages: at close range the detection space will be vastly reduced, making a broad beam favorable. Hence, a flexible system would be very advantageous. We investigated whether bats can dynamically change directionality of their biosonar during aerial pursuit of insects. We trained five Myotis daubentonii and one Eptesicus serotinus to capture tethered mealworms and recorded their echolocation signals with a multimicrophone array. The results show that the bats broaden the echolocation beam drastically in the terminal phase of prey pursuit. M. daubentonii increased the half-amplitude angle from approximately 40° to approximately 90° horizontally and from approximately 45° to more than 90° vertically. The increase in beam width is achieved by lowering the frequency by roughly one octave from approximately 55 kHz to approximately 27.5 kHz. The E. serotinus showed beam broadening remarkably similar to that of M. daubentonii. Our results demonstrate dynamic control of beam width in both species. Hence, we propose directionality as an explanation for the frequency decrease observed in the buzz of aerial hawking vespertilionid bats. We predict that future studies will reveal dynamic control of beam width in a broad range of acoustically communicating animals.

Acoustic scanning of natural scenes by echolocation in the big brown bat, Eptesicus fuscus

SUMMARY Echolocation allows bats to orient and localize prey in complete darkness. The sonar beam of the big brown bat, Eptesicus fuscus, is directional but broad enough to provide audible echo information from within a 60–90 deg. cone. This suggests that the big brown bat could interrogate a natural scene without fixating each important object separately. We tested this idea by measuring the directional aim and duration of the bats sonar beam as it performed in a dual task, obstacle avoidance and insect capture. Bats were trained to fly through one of two openings in a fine net to take a tethered insect at variable distances behind the net. The bats sequentially scanned the edges of the net opening and the prey by centering the axis of their sonar beam with an accuracy of ∼5 deg. The bats also shifted the duration of their sonar calls, revealing sequential sampling along the range axis. Changes in duration and directional aim were correlated, showing that the bat first inspected the hole, and then shifted its gaze to the more distant insect, before flying through the net opening. Contrary to expectation based on the sonar beam width, big brown bats encountering a complex environment accurately pointed and shifted their sonar gaze to sequentially inspect closely spaced objects in a manner similar to visual animals using saccades and fixations to scan a scene. The findings presented here from a specialized orientation system, echolocation, offer insights into general principles of active sensing across sensory modalities for the perception of natural scenes.

Probing the Natural Scene by Echolocation in Bats

Bats echolocating in the natural environment face the formidable task of sorting signals from multiple auditory objects, echoes from obstacles, prey, and the calls of conspecifics. Successful orientation in a complex environment depends on auditory information processing, along with adaptive vocal-motor behaviors and flight path control, which draw upon 3-D spatial perception, attention, and memory. This article reviews field and laboratory studies that document adaptive sonar behaviors of echolocating bats, and point to the fundamental signal parameters they use to track and sort auditory objects in a dynamic environment. We suggest that adaptive sonar behavior provides a window to bats’ perception of complex auditory scenes.