Lasse Jakobsen

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.

Echolocating bats emit a highly directional sonar sound beam in the field

Bats use echolocation or biosonar to navigate and find prey at night. They emit short ultrasonic calls and listen for reflected echoes. The beam width of the calls is central to the function of the sonar, but directionality of echolocation calls has never been measured from bats flying in the wild. We used a microphone array to record sounds and determine horizontal directionality for echolocation calls of the trawling Daubentons bat, Myotis daubentonii, flying over a pond in its natural habitat. Myotis daubentonii emitted highly directional calls in the field. Directionality increased with frequency. At 40 kHz half-amplitude angle was 25°, decreasing to 14° at 75 kHz. In the laboratory, M. daubentonii emitted less intense and less directional calls. At 55 kHz half-amplitude angle was 40° in the laboratory versus 20° in the field. The relationship between frequency and directionality can be explained by the simple piston model. The model also suggests that the increase in the emitted intensity in the field is caused by the increased directionality, focusing sound energy in the forward direction. The bat may increase directionality by opening the mouth wider to emit a louder, narrower beam in the wild.

Convergent acoustic field of view in echolocating bats

Most echolocating bats exhibit a strong correlation between body size and the frequency of maximum energy in their echolocation calls (peak frequency), with smaller species using signals of higher frequency than larger ones. Size–signal allometry or acoustic detection constraints imposed on wavelength by preferred prey size have been used to explain this relationship. Here we propose the hypothesis that smaller bats emit higher frequencies to achieve directional sonar beams, and that variable beam width is critical for bats. Shorter wavelengths relative to the size of the emitter translate into more directional sound beams. Therefore, bats that emit their calls through their mouths should show a relationship between mouth size and wavelength, driving smaller bats to signals of higher frequency. We found that in a flight room mimicking a closed habitat, six aerial hawking vespertilionid species (ranging in size from 4 to 21 g, ref. 5) produced sonar beams of extraordinarily similar shape and volume. Each species had a directivity index of 11 ± 1 dB (a half-amplitude angle of approximately 37°) and an on-axis sound level of 108 ± 4 dB sound pressure level referenced to 20 μPa root mean square at 10 cm. Thus all bats adapted their calls to achieve similar acoustic fields of view. We propose that the necessity for high directionality has been a key constraint on the evolution of echolocation, which explains the relationship between bat size and echolocation call frequency. Our results suggest that echolocation is a dynamic system that allows different species, regardless of their body size, to converge on optimal fields of view in response to habitat and task.

Superfast Muscles Set Maximum Call Rate in Echolocating Bats

Superfast muscles control the rate of call output in echolocating bats. As an echolocating bat closes in on a flying insect, it increases call emission to rates beyond 160 calls per second. This high call rate phase, dubbed the terminal buzz, has proven enigmatic because it is unknown how bats are able to produce calls so quickly. We found that previously unknown and highly specialized superfast muscles power rapid call rates in the terminal buzz. Additionally, we show that laryngeal motor performance, not overlap between call production and the arrival of echoes at the bat’s ears, limits maximum call rate. Superfast muscles are rare in vertebrates and always associated with extraordinary motor demands on acoustic communication. We propose that the advantages of rapid auditory updates on prey movement selected for superfast laryngeal muscle in echolocating bats.

How the bat got its buzz

Since the discovery of echolocation in bats, the final phase of an attack on a flying insect, the ‘terminal buzz’, has proved enigmatic. During the buzz, bats increase information update rates by producing vocalizations up to 220 times s−1. The buzzs ubiquity in hawking and trawling bats implies its importance for hunting success. Superfast muscles, previously unknown in mammals, are responsible for the extreme vocalization rate. Some bats produce a second phase—buzz II—defined by a large drop in the fundamental frequency (F0) of their calls. By doing so, bats broaden their acoustic field of view and should thereby reduce the likelihood of insect escape. We make the case that the buzz was a critical adaptation for capturing night-flying insects, and suggest that the drop in F0 during buzz II requires novel, unidentified laryngeal mechanisms in order to counteract increasing muscle tension. Furthermore, we propose that buzz II represents a countermeasure against the evasive flight of eared prey in the evolutionary arms-race that saw the independent evolution of bat-detecting ears in various groups of night-flying insects.

Bats coordinate sonar and flight behavior as they forage in open and cluttered environments

Echolocating bats use active sensing as they emit sounds and listen to the returning echoes to probe their environment for navigation, obstacle avoidance and pursuit of prey. The sensing behavior of bats includes the planning of 3D spatial trajectory paths, which are guided by echo information. In this study, we examined the relationship between active sonar sampling and flight motor output as bats changed environments from open space to an artificial forest in a laboratory flight room. Using high-speed video and audio recordings, we reconstructed and analyzed 3D flight trajectories, sonar beam aim and acoustic sonar emission patterns as the bats captured prey. We found that big brown bats adjusted their sonar call structure, temporal patterning and flight speed in response to environmental change. The sonar beam aim of the bats predicted the flight turn rate in both the open room and the forest. However, the relationship between sonar beam aim and turn rate changed in the forest during the final stage of prey pursuit, during which the bat made shallower turns. We found flight stereotypy developed over multiple days in the forest, but did not find evidence for a reduction in active sonar sampling with experience. The temporal patterning of sonar sound groups was related to path planning around obstacles in the forest. Together, these results contribute to our understanding of how bats coordinate echolocation and flight behavior to represent and navigate their environment.

Echolocation intensity and directionality of perching and flying fringe-lipped bats, Trachops cirrhosus (Phyllostomidae)

The Neotropical frog-eating bat, Trachops cirrhosus, primarily hunts stationary prey, either by gleaning on the wing, or in a sit-and-wait mode hanging from a perch. It listens passively for prey-generated sounds, but uses echolocation in all stages of the hunt. Like other bats in the family Phyllostomidae, T. cirrhosus has a conspicuous nose leaf, hypothesized to direct and focus echolocation calls emitted from the nostrils. T. cirrhosus is highly flexible in its cognitive abilities and its use of sensory strategies for prey detection. Additionally, T. cirrhosus has been observed to echolocate both with closed and open mouth. We hypothesize that its flexibility extends to echolocation call design. We investigated the effect of hunting mode, perching or flying, as well as the effect of mouth opening, on the acoustic parameters and directionality of the echolocation call. We used a multi-microphone array, a high-speed video camera, and a microphone-diode-video system to directly visualize the echolocation sound beam synchronized with the bats behavior. We found that T. cirrhosus emits a highly directional sound beam with half amplitude angle (HAM) of 12–18° and DI (directionality index) of ~17 dB, among the most directional bat sonar beams measured to date. The directionality was high both when flying and when perching. The emitted intensity was low, around 88 dB SPL at 10 cm from the mouth, when hanging, but higher, around 100 dB SPL at 10 cm, when flying or just before take-off. Our data suggests that the limited search volume of T. cirrhosus sonar beam defined by the high directionality and the rather low intensity of its echolocation calls is adapted to the highly cluttered hunting habitat and to the perch hunting mode.

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

Significance Many insects have evolved ultrasonic ears to detect and evade hunting bats, performing dramatic escape maneuvers in response to intense ultrasound. Presumably as a response, some bats broaden their echolocation beam in close proximity to insects to keep track of them at large off-axis angles. Here, we investigated if beam broadening is a general property of echolocation when hunting moving prey. The results show that emballonurid bats ensonify a wide area during pursuit, not by broadening the beam but by emitting high-intensity calls throughout pursuit. Thus, beam broadening is not a general property of echolocation, but we hypothesize that maintaining a broad acoustic field of view is crucial for all echolocators hunting moving prey. 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.

Ear-body lift and a novel thrust generating mechanism revealed by the complex wake of brown long-eared bats (Plecotus auritus)

Large ears enhance perception of echolocation and prey generated sounds in bats. However, external ears likely impair aerodynamic performance of bats compared to birds. But large ears may generate lift on their own, mitigating the negative effects. We studied flying brown long-eared bats, using high resolution, time resolved particle image velocimetry, to determine the aerodynamics of flying with large ears. We show that the ears and body generate lift at medium to cruising speeds (3–5 m/s), but at the cost of an interaction with the wing root vortices, likely reducing inner wing performance. We also propose that the bats use a novel wing pitch mechanism at the end of the upstroke generating thrust at low speeds, which should provide effective pitch and yaw control. In addition, the wing tip vortices show a distinct spiraling pattern. The tip vortex of the previous wingbeat remains into the next wingbeat and rotates together with a newly formed tip vortex. Several smaller vortices, related to changes in circulation around the wing also spiral the tip vortex. Our results thus show a new level of complexity in bat wakes and suggest large eared bats are less aerodynamically limited than previous wake studies have suggested.

Big brown bats ( Eptesicus fuscus ) emit intense search calls and fly in stereotyped flight paths as they forage in the wild

ABSTRACT The big brown bat, Eptesicus fuscus, uses echolocation for orientation and foraging, and scans its surroundings by aiming its sonar beam at obstacles and prey. All call parameters are highly adaptable and determine the bats acoustic field of view and hence its perception of the echo scene. The intensity (source level) and directionality of the emitted calls directly contribute to the bats acoustic field of view; however, the source level and directionality of the big brown bats sonar signals have not been measured in the field. In addition, for bats, navigation and prey capture require that they process several streams of acoustic information. By using stereotypic flight paths in known areas, bats may be able to reduce the sensory processing load for orientation and therefore allocate echo processing resources to prey. Here we recorded the echolocation calls from foraging E. fuscus in the field with a microphone array and estimated call intensity and directionality, based on reconstructed flight trajectories. The source levels were intense with an average maximum source level of 138 dB (root mean square re. 20 µPa at 0.1 m). Furthermore, measurements taken from a subset of calls indicate that the echolocation signals in the field may be more directional than estimated in the laboratory (half-amplitude angle 30 deg at 35 kHz). We also observed that E. fuscus appear to follow stereotypic flight paths, and propose that this could be a strategy to optimize foraging efficiency by minimizing the sensory processing load. Summary: Field recordings of Eptesicus fuscus reveal highly intense source levels and stereotypic flight behaviour, potentially as a strategy to optimize foraging efficiency by minimizing sensory processing load.