Emyo Fujioka

Adaptive beam-width control of echolocation sounds by CF–FM bats, Rhinolophus ferrumequinum nippon, during prey-capture flight

SUMMARY The echolocation sounds of Japanese CF–FM bats (Rhinolophus ferrumequinum nippon) were measured while the bats pursued a moth (Goniocraspidum pryeri) in a flight chamber. Using a 31-channel microphone array system, we investigated how CF–FM bats adjust pulse direction and beam width according to prey position. During the search and approach phases, the horizontal and vertical beam widths were ±22±5 and ±13±5 deg, respectively. When bats entered the terminal phase approximately 1 m from a moth, distinctive evasive flight by G. pryeri was sometimes observed. Simultaneously, the bats broadened the beam widths of some emissions in both the horizontal (44% of emitted echolocation pulses) and vertical planes (71%). The expanded beam widths were ±36±7 deg (horizontal) and ±30±9 deg (vertical). When moths began evasive flight, the tracking accuracy decreased compared with that during the approach phase. However, in 97% of emissions during the terminal phase, the beam width was wider than the misalignment (the angular difference between the pulse and target directions). These findings indicate that bats actively adjust their beam width to retain the moving target within a spatial echolocation window during the final capture stages.

Adaptive echolocation sounds of insectivorous bats, Pipistrellus abramus, during foraging flights in the field

Echolocation pulses emitted by wild Pipistrellus abramus were investigated while foraging for insects in the field. Similar to other European pipistrelles, the frequency structure during foraging varied. During the search phase, the bats emitted long shallow frequency-modulated pulses 9-11 ms in duration, whereas the maximum pulse duration of the bats approaching a large target wall in the laboratory was 3 ms. No significant difference was observed between decreases in the interpulse interval during these two approach flights. It is concluded that the bats use a long quasi-constant frequency pulse to find a weak echo from a small prey target.

Echolocating bats use future-target information for optimal foraging

Significance This study shows how an animal dynamically and rationally controls its sensing and navigates to capture multiple prey items. To perform this study, we extracted sonar attention and flight attention of foraging wild bats from both empirical data and mathematical modeling. We show that the bats directed their sonar and flight attention toward not only an immediate prey but also the next prey. In addition, numerical simulation shows a possibility that the bats select suitable flight paths for the consecutive capture. Hence, wild echolocating bats plan their flight paths by distributing their attention among multiple prey items, which means that the bats do not forage in a hit-or-miss fashion but rather spatially anticipate their future targets for optimum routing. When seeing or listening to an object, we aim our attention toward it. While capturing prey, many animal species focus their visual or acoustic attention toward the prey. However, for multiple prey items, the direction and timing of attention for effective foraging remain unknown. In this study, we adopted both experimental and mathematical methodology with microphone-array measurements and mathematical modeling analysis to quantify the attention of echolocating bats that were repeatedly capturing airborne insects in the field. Here we show that bats select rational flight paths to consecutively capture multiple prey items. Microphone-array measurements showed that bats direct their sonar attention not only to the immediate prey but also to the next prey. In addition, we found that a bat’s attention in terms of its flight also aims toward the next prey even when approaching the immediate prey. Numerical simulations revealed a possibility that bats shift their flight attention to control suitable flight paths for consecutive capture. When a bat only aims its flight attention toward its immediate prey, it rarely succeeds in capturing the next prey. These findings indicate that bats gain increased benefit by distributing their attention among multiple targets and planning the future flight path based on additional information of the next prey. These experimental and mathematical studies allowed us to observe the process of decision making by bats during their natural flight dynamics.

Echolocation and flight strategy of Japanese house bats during natural foraging, revealed by a microphone array system.

Using only a microphone array system, echolocation pulses and three-dimensional flight paths in the frequency-modulated bat, Pipistrellus abramus, during natural foraging, were simultaneously examined. During the search phase, the inter-pulse interval, pulse duration, and moving distance of the bat between successive emissions were relatively constant at around 89.5 ± 18.7 ms, 6.90 ± 1.31 ms, and 0.50 ± 0.20 m, respectively. The bats started to decrease these acoustical parameters within 2-3 m of the prey capture point. For every emission along a flight path, the distance between a bat and its prey capture point was calculated as both direct distance to capture (DDC), which corresponded to the target distance, and flight distance to capture (FDC) along the flight path. The DDC matched the FDC after the start of the approach phase, indicating that foraging bats followed a straight-ahead path to the target. In addition, the duration of the quasi-constant frequency component of emitted pulses was slightly extended just before the convergence of the DDC with the FDC. These findings suggest that the bats confirm the presence of target prey by extending the duration of the pulse and then select a straight-ahead approach by forecasting the movement of the prey.

Qualitative and quantitative analyses of the echolocation strategies of bats on the basis of mathematical modelling and laboratory experiments.

Prey pursuit by an echolocating bat was studied theoretically and experimentally. First, a mathematical model was proposed to describe the flight dynamics of a bat and a single prey. In this model, the flight angle of the bat was affected by angles related to the flight path of the single moving prey, that is, the angle from the bat to the prey and the flight angle of the prey. Numerical simulation showed that the success rate of prey capture was high, when the bat mainly used the angle to the prey to minimize the distance to the prey, and also used the flight angle of the prey to minimize the difference in flight directions of itself and the prey. Second, parameters in the model were estimated according to experimental data obtained from video recordings taken while a Japanese horseshoe bat (Rhinolphus derrumequinum nippon) pursued a moving moth (Goniocraspidum pryeri) in a flight chamber. One of the estimated parameter values, which represents the ratio in the use of the angles, was consistent with the optimal value of the numerical simulation. This agreement between the numerical simulation and parameter estimation suggests that a bat chooses an effective flight path for successful prey capture by using the angles. Finally, the mathematical model was extended to include a bat and prey. Parameter estimation of the extended model based on laboratory experiments revealed the existence of bat’s dynamical attention towards prey, that is, simultaneous pursuit of prey and selective pursuit of respective prey. Thus, our mathematical model contributes not only to quantitative analysis of effective foraging, but also to qualitative evaluation of a bat’s dynamical flight strategy during multiple prey pursuit.

Coordinated Control of Acoustical Field of View and Flight in Three-Dimensional Space for Consecutive Capture by Echolocating Bats during Natural Foraging

Echolocating bats prey upon small moving insects in the dark using sophisticated sonar techniques. The direction and directivity pattern of the ultrasound broadcast of these bats are important factors that affect their acoustical field of view, allowing us to investigate how the bats control their acoustic attention (pulse direction) for advanced flight maneuvers. The purpose of this study was to understand the behavioral strategies of acoustical sensing of wild Japanese house bats Pipistrellus abramus in three-dimensional (3D) space during consecutive capture flights. The results showed that when the bats successively captured multiple airborne insects in short time intervals (less than 1.5 s), they maintained not only the immediate prey but also the subsequent one simultaneously within the beam widths of the emitted pulses in both horizontal and vertical planes before capturing the immediate one. This suggests that echolocating bats maintain multiple prey within their acoustical field of view by a single sensing using a wide directional beam while approaching the immediate prey, instead of frequently shifting acoustic attention between multiple prey. We also numerically simulated the bats’ flight trajectories when approaching two prey successively to investigate the relationship between the acoustical field of view and the prey direction for effective consecutive captures. This simulation demonstrated that acoustically viewing both the immediate and the subsequent prey simultaneously increases the success rate of capturing both prey, which is considered to be one of the basic axes of efficient route planning for consecutive capture flight. The bat’s wide sonar beam can incidentally cover multiple prey while the bat forages in an area where the prey density is high. Our findings suggest that the bats then keep future targets within their acoustical field of view for effective foraging. In addition, in both the experimental results and the numerical simulations, the acoustic sensing and flights of the bats showed narrower vertical ranges than horizontal ranges. This suggests that the bats control their acoustic sensing according to different schemes in the horizontal and vertical planes according to their surroundings. These findings suggest that echolocating bats coordinate their control of the acoustical field of view and flight for consecutive captures in 3D space during natural foraging.

Three-dimensional sonar beam-width expansion by Japanese house bats (Pipistrellus abramus) during natural foraging

Three-dimensional directivity patterns of sonar sounds emitted by Japanese house bats (Pipistrellus abramus) during natural foraging were measured by a 44-channel microphone array. Just before prey capture, the terminal frequency (TF) of emitted sounds decreased, and the beam width (mean ± standard deviation) expanded from 40 ± 10° to 63 ± 9° (horizontal) and from 32 ± 10° to 52 ± 7° (vertical). P. abramus decrease the TF to simultaneously expand the beam width in both the horizontal and vertical planes, while retaining the target within the three-dimensional acoustic field of view at the final stage of capture.

On-board telemetry of biosonar sounds from free-flying bats

Analysis of the bats reactions to relevant target echoes enables us to directly assess biosonar performance. Here, we recorded the sonar broadcast and its echoes the bat received during flight by using an on-board telemetry microphone (Telemike) mounted on the bats back. Telemike recordings confirmed that flying bats adjust the amplitude and frequency of their sonar broadcasts to compensate for increases in echo amplitude and for Doppler-shifts. For insect capturing, the bat exhibited Doppler-shift compensation for echoes from the static target ahead, but not for echoes from the target moth even though the flying bat attended to the moth for capture. Positive and negative Doppler shifts (acoustic glints) caused by insect fluttering were observed in the constant-frequency component of observed echoes, which synchronized with wingbeat cycle of the moth. Combined frequency and amplitude compensation for the static target may be advantageous for detection of acoustic glints of target prey. We also construct...

Echolocation behavior of pairs of flying Eptesicus fuscus recorded with a Telemike microphone.

Four big brown bats (Eptesicus fuscus) were flown singly and in pairs in a room containing a sparse array of vertically hanging plastic chains as obstacles. Each bat carried a lightweight radio telemetry microphone (Telemike) that recorded their emitted echolocation sounds without artifacts from Doppler shifts, directional effects, and atmospheric attenuation. The broadcasts of both bats were also recorded with two stationary ultrasonic microphones located at the far end of the flight room. The echolocation broadcasts of bats flying singly were compared to those emitted when the bats were flown together. The principal change was shifting of harmonic frequencies very slightly (<5 kHz) away from each other and from frequencies used when flying alone. In contrast, the duration of emissions was more stable between single and double bat flights. Changes in ending frequency have been associated with a jamming avoidance response in big brown bats and could indicate attempts to avoid interference while flying wit...

Echolocation and flight strategies of aerial-feeding bats during natural foraging

Aerial-feeding bats actively emit sonar sounds and capture large amounts of airborne insects a night. Microphone-array system allows us to know not only the positions where the bat emits sonar sounds (i.e., 3-D flight path) but how the bats dynamically control the acoustical field of view during searching and approaching target-prey. Here, we show echolocation strategy of bats during natural foraging revealed by the large-scale microphone-array system which covered the horizontal area of approximately 20 m × 20 m. Pipistrellus abramus was found to expand the width of their sonar beams in both horizontal and vertical planes just before the prey-capture. Since the bats emit echolocation pulses at a high rate (i.e., feeding buzz) just before capturing, the capture positions can additionally be measured. Recently, we have investigated the relationship between flight patterns, capture positions, and foraging efficiency of Myotis macrodactylus during natural foraging above the pond. Further investigation from t...