Bats integrate multiple echolocation and flight tactics to track prey.

The ability of "target tracking," such as keeping a target object in sight, is crucial for various activities. However, most sensing systems experience a certain degree of delay due to information processing, which challenges accurate target tracking. The long history of studies on animal behavior has revealed several tactics for it, although a systematic understanding of how individual tactics are combined into a strategy has not been reached. This study demonstrates a multifaceted tracking strategy in animals, which mitigates the adverse delay effects with small implementation costs. Using an active-sensing bat to measure their sensing state while chasing natural prey, we found that bats use a tracking strategy by combining multiple echolocation and flight tactics. The three echolocation tactics, namely the predictive control of sensing direction accompanied by adjusting the sensing rate and angular range, produce a direct compensation effect. Simultaneously, the flight tactic, the counter maneuver, assists echolocation by stabilizing the target direction. Our simulation results demonstrate that these combined tactics improve tracking accuracy over a wide range of delay constraints. In addition, a concise rule based on the angular velocity between bats and targets explains how bats control these tactics, suggesting that bats successfully reduce the burden of multitasking management. Our findings reveal the sophisticated strategy in animals' tracking systems and provide insights into understanding and developing efficiently integrated strategies in target tracking across various disciplines.

A glimpse into the foraging and movement behaviour of Nyctalus aviator; a complementary study by acoustic recording and GPS tracking.

Species of open-space bats that are relatively large, such as bats from the genus Nyctalus, are considered as high-risk species for collisions with wind turbines (WTs). However, important information on their behaviour and movement ecology, such as the locations and altitudes at which they forage, is still fragmentary, while crucial for their conservation in light of the increasing threat posed by progressing WT construction. We adopted two different methods of microphone array recordings and GPS-tracking capturing data from different spatio-temporal scales in order to gain a complementary understanding of the echolocation and movement ecology of Nyctalus aviator, the largest open-space bat in Japan. Based on microphone array recordings, we found that echolocation calls during natural foraging are adapted for fast flight in open-space optimal for aerial-hawking. In addition, we attached a GPS tag that can simultaneously monitor feeding buzz occurrence, and confirmed that foraging occurred at 300 m altitude and that the flight altitude in mountainous areas is consistent with the turbine conflict zone, suggesting that the birdlike noctule is a high-risk species in Japan. Further investigations on this species could provide valuable insights into their foraging and movement ecology, facilitating the development of a risk assessment regarding WTs.

Discriminating predation attempt outcomes during natural foraging using the post-buzz pause in the Japanese large-footed bat, Myotis macrodactylus.

Bats emit a series of echolocation calls with an increasing repetition rate (the terminal buzz) when attempting to capture prey. This is often used as an acoustic indicator of prey-capture attempts. However, because it is directly linked to foraging efficiency, predation success is a more useful measure than predation attempts in ecological research. The characteristics of echolocation calls that consistently signify predation success across different situations have not been identified. Owing to additional influencing factors, identification of these characteristics is particularly challenging for wild bats foraging in their natural environment compared with those in flight chambers. This study documented the natural foraging behavior of wild Japanese large-footed bats (Myotis macrodactylus) using synchronized acoustic and video recordings. From the video recordings, we could assign 137 attacks to three outcome categories: prey captured (51.8%), prey dropped (29.2%) and failed attempt (19%). Based on previous indications from laboratory studies that the length of the silent interval following the terminal buzz (post-buzz pause) might reflect the prey-capture outcome, we compared post-buzz pause durations among categories of attack outcomes. The post-buzz pause was longest in the case of successful capture, suggesting that the length of the post-buzz pause is a useful acoustic indicator of predation success during natural foraging in M. macrodactylus. Our finding will advance the study of bat foraging behavior using acoustic data, including estimations of foraging efficiency and analyses of feeding habitat quality.

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.

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.

Echolocating bats use future-target information for optimal foraging.

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.

Rapid shifts of sonar attention by Pipistrellus abramus during natural hunting for multiple prey.

Flight paths of echolocating Japanese house bats, Pipistrellus abramus, were tracked during insect hunting in a natural setting using a 32-microphone array. The array surrounded the foraging area, locating each bat, and determined the directional aim of the sonar beam. Successive interceptions, indicated by feeding "buzzes" and post-buzz pauses, occurred singly at intervals from over 20 s down to multiple interceptions at 2-3 s intervals. Bats flew on looping, curved paths. Turning radius tightened as rate of interceptions increased, keeping the bat in a smaller area of higher capture density. Broadcast beams shifted direction during search, often alternating between the direction of flight and another direction where, moments later, the next interception would occur. Broadcasts also shifted direction between the current target and the next target. Bats time-share biosonar attention between objects by alternating acoustic gaze. During search, most interpulse intervals (IPIs) were 70-120 ms, but bats interspersed long IPIs up to 200 ms when the rate of interception was low and flight paths followed broad curves. Mathematical modeling of search paths demonstrated that circular flight-paths with occasional long IPIs would be more effective for target search than either random, correlated random, or linear flights.

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 [Formula: see text] 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 [Formula: see text] 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 [Formula: see text] angles. Finally, the mathematical model was extended to include a bat and [Formula: see text] prey. Parameter estimation of the extended model based on laboratory experiments revealed the existence of bat's dynamical attention towards [Formula: see text] prey, that is, simultaneous pursuit of [Formula: see text] 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.

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

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.

Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey.

Echolocation sounds of Rhinolophus ferrumequinum nippon as they approached a fluttering moth (Goniocraspidum pryeri) were investigated using an on-board telemetry microphone (Telemike). In 40% of the successful moth-capture flights, the moth exhibited distinctive evasive flight behavior, but the bat pursued the moth by following its flight path. When the distance to the moth was approximately 3-4 m, the bats increased the duration of the pulses to 65-95 ms, which is 2-3 times longer than those during landing flight (30-40 ms). The mean of 5.8 long pulses were emitted before the final buzz phase of moth capture, without strengthening the sound pressure level. The mean duration of long pulses (79.9 ± 7.9 ms) corresponded to three times the fluttering period of G. pryeri (26.5 × 3 = 79.5 ms). These findings indicate that the bats adjust the pulse duration to increase the number of temporal repetitions of fluttering information rather than to produce more intense sonar sounds to receive fine insect echoes. The bats exhibited Doppler-shift compensation for echoes returning from large static objects ahead, but not for echoes from target moths, even though the bats were focused on capturing the moths. Furthermore, the echoes of the Telemike recordings from target moths showed spectral glints of approximately 1-1.5 kHz caused by the fluttering of the moths but not amplitude glints because of the highly acoustical attenuation of ultrasound in the air, suggesting that spectral information may be more robust than amplitude information in echoes during moth capturing flight.

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.

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.