Echolocating bats use future-target information for optimal foraging

Abstract

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.bat sonar | aerial capture | microphone array | mathematical modeling | flight dynamics S electively focusing attention on a particular target allows us to effectively extract information (1-4). Animals spatially focus their attention toward prey for suitable foraging (5, 6). During prey pursuit, most animals direct their visual attention toward it [e.g., tiger beetle (7), dragonfly (8), and falcon (9)]. Specifically, for example, dragonflies maintain a prey item at a constant retinal position during approaching it so that they steer an interception flight path (interception strategy) (10). However, for multiple prey items, the direction and timing of attention for effective foraging remain unknown.Echolocating bats actively emit sonar signals to obtain surrounding information and adaptively change the characteristics of the emissions depending on the situation (11). Therefore, their attention in terms of the sonar (sonar attention) is characterized as the direction to which bats emit their sonar beams (12-14). When echolocating bats approach an airborne insect, the sonar attention directs toward the prey (12, 13). During natural foraging, the sonar attention of bats alternately shifts from their flying direction to the side (15). Additionally the wild bats are capable of capturing two prey items within the short interval of 1 s (16).We predicted that bats localize multiple prey items by distributing their attention between them and then select an efficient flight path to successively capture the multiple prey. To test this prediction, ...

Cortical neurons of bats respond best to echoes from nearest targets when listening to natural biosonar multi-echo streams

“…During call emission, the animals can variably adjust their sonar beam49 and the echo perception can be influenced through motor behaviors of the head or the pinnae4950. A recent study on insect-eating bats demonstrated that, while hunting, the bats shift their sonar beam and flight path towards the second prey before capturing the immediate prey which increases the capture rate51. In the present study, the effects of attention could not be tested because neuronal recordings were performed in anesthetized bats.…”

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

“…From our observation, we concluded that these prey are roughly ten times slower than P . abramus (which has an average speed of 5 m/s) and therefore assumed that the movement of the prey, at this study site, was negligible during the brief period of approach and capture (< 3 s) in each flight sequence examined in this study [17]. …”

“…We also reported that the bats directed their pulse toward the subsequent target before capturing the immediate one when attacking two successive targets [5]. On the other hand, our recent study adopted a mathematical methodology to estimate parameters representing the flight attention of bats for their measured flight paths during the phase of approaching prey [17]. (Note that the flight attention is derived from a parameter of weighing factors to minimize the angular difference between the bat’s flight direction and the direction to its prey.…”

“…We proposed two hypotheses: 1) bats physically shift their pulse direction between immediate and subsequent targets in somewhat of a time-sharing manner (time-sharing manner hypothesis), or 2) bats aim their beam across a wide area to cover both immediate and subsequent targets simultaneously within their acoustical field of view (acoustical field hypothesis). Based on our previous studies [5,17], we propose an acoustical field hypothesis in which the bats are assumed to aim their pulses in a certain direction. This keeps multiple targets within their acoustical field of view, including the peripheral part.…”

Environmental acoustic cues guide the biosonar attention of a highly specialised echolocator

“…Saccadic eye movements sequentially sample a visual scene in fast temporal succession by steering the gaze to points of interest and can be used to infer the underlying attentional process (Hayhoe and Ballard, 2005;Henderson, 2003;Yarbus, 1967). Correspondingly, we here evaluated the scanning movements of the biosonar beam of horseshoe bats to infer the bats' sonar attention (Fujioka et al, 2016;Ghose and Moss, 2003;Seibert et al, 2013;Surlykke and Moss, 2000) towards passive acoustic environmental cues.…”