Dynamics of the echolocation beam during prey pursuit in aerial hawking bats

In the evolutionary arms race between prey and predator, measures and countermeasures continuously evolve to increase survival on both sides. Bats and moths are prime examples. When exposed to intense ultrasound, eared moths perform dramatic escape behaviors. Vespertilionid and rhinolophid bats broaden their echolocation beam in the final stage of pursuit, presumably as a countermeasure to keep evading moths within their “acoustic field of view.” In this study, we investigated if dynamic beam broadening is a general property of echolocation when catching moving prey. We recorded three species of emballonurid bats, Saccopteryx bilineata, Saccopteryx leptura, and Rhynchonycteris naso, catching airborne insects in the field. The study shows that S. bilineata and S. leptura maintain a constant beam shape during the entire prey pursuit, whereas R. naso broadens the beam by lowering the peak call frequency from 100 kHz during search and approach to 67 kHz in the buzz. Surprisingly, both Saccopteryx bats emit calls with very high energy throughout the pursuit, up to 60 times more than R. naso and Myotis daubentonii (a similar sized vespertilionid), providing them with as much, or more, peripheral “vision” than the vespertilionids, but ensonifying objects far ahead suggesting more clutter. Thus, beam broadening is not a fundamental property of the echolocation system. However, based on the results, we hypothesize that increased peripheral detection is crucial to all aerial hawking bats in the final stages of prey pursuit and speculate that beam broadening is a feature characterizing more advanced echolocation.The evolutionary arms race between echolocating bats and their insect prey provides a textbook example of continuous evolution of measures and countermeasures to either acquire prey or escape capture (1). Bats can navigate and forage in complete darkness using echolocation, emitting short ultrasonic sound pulses and locating objects and prey in their surroundings from the returning echoes (2). In response, moths and other nocturnal insects have evolved ultrasound-sensitive ears that enable them to avoid foraging echolocating bats (negative phonotaxis) and to initiate dramatic escape responses when in close proximity to them (3). As a possible countermeasure, some species of bats have evolved echolocation calls with low intensities [Barbastellus barbastella (4)] and/or frequencies [Euderma maculatum (5)] outside the moths’ hearing range, enabling them to sneak up undetected, or at least without eliciting escape maneuvers from the prey.Another potential countermeasure is the sudden broadening of the beam observed in the very last phases of prey pursuit in aerial hawking vespertilionid bats (6) and rhinolophid bats (7). When searching for, and approaching, prey, both vespertilionids and rhinolophids emit a fairly directional sound beam with higher sound pressure in the acoustic axis right in front of the bat and decreasing steeply as the off-axis angle increases (8, 9). Although the directional emissions provide the bats with a number of advantages over an omnidirectional emission (6), the downside is a decreased acoustic “field of view” that would enable prey to escape the bat’s sonar space, especially at close range. Presumably to counteract this effect, vespertilionids and rhinolophids broaden their echolocation beam when closing in on prey (6, 7). Vespertilionids do so by lowering the frequency of their calls by almost an octave. The width of a sound beam depends on the wavelength emitted relative to the size of the emitter. Hence, increasing the wavelength by lowering the frequency by an octave will substantially increase the width of the beam for a constant mouth opening (6). The mechanism is still unknown for rhinolophids, but manipulating the fine structure of their nose-leaf could account for the change in beam directionality (10). By broadening the beam during the final stage of prey pursuit (the buzz), the bats counteract the prey’s evasive maneuvers, keeping larger off-axis angles within their acoustic field of view compared with the approach phase. The ubiquitous nature of this aspect of predator–prey interaction in echolocators is emphasized by recent findings showing that harbor porpoises (Phocena phocena) also broaden their beam during the buzz phase when catching fish (11).Whereas the Vespertilionidae and Rhinolophidae are considered advanced echolocators, the Emballonuridae are thought to emit calls closely resembling those calls emitted by the first echolocating bats (12, 13). Like most vespertilionids, emballonurids hunt airborne insects. They emit sounds through their mouth. Their calls are short, multiharmonic, and of an almost constant frequency, with a suppressed first harmonic and most energy in the second harmonic (14) (Fig. 1). They go through the three standard hunting phases, search, approach, and buzz, when catching airborne prey (Fig. 1), but they do not change the call frequency during the buzz phase. Thus, emballonurids can only broaden their echolocation beam during the buzz by reducing their effective emitter size (e.g., by reducing their gape size). Investigating whether emballonurids broaden their beam during prey pursuit will throw light on whether the beam broadening is a fundamental property of the echolocation system in all aerial hawking bats, or possibly a more advanced trait that has only evolved in some families/species. Hence, the main purpose of this study is to investigate if emballonurids are broadening their beam during the terminal buzz. The only known exception to the general observation of constant frequency throughout the whole pursuit sequence is Rhynchonycteris naso, which is considered an outlier within the emballonurid family. It uses very high frequencies, around 100 kHz, and lowers the frequency to ca. 67 kHz in the terminal phase (15). Thus, a second purpose of our study is to investigate how the frequency shift affects the beam shape of this exception within the emballonurid family.Open in a separate windowFig. 1.Recorded call sequences. Exemplary call sequences for each recorded species and from M. daubentonii for comparison. (Top) Oscillograms of the hunting sequences for each species; the arrow indicates the beginning of the buzz. (Middle) Spectrograms of the hunting sequence showing the frequency drop in the buzz for R. naso and M. daubentonii and the lack of frequency change in S. bilineata and S. leptura. Frequency spectra (Bottom) corresponding to calls marked with colored asterisks (Top) comparing search/approach calls and buzz calls; two search/approach calls are shown for the two Saccopteryx bats as they alternate call frequency.