ABSTRACT Journal of Experimental Biology has a long history of reporting research discoveries on animal echolocation, the subject of this Centenary Review. Echolocating animals emit intense sound pulses and process echoes to localize objects in dynamic soundscapes. More than 1100 species of bats and 70 species of toothed whales rely on echolocation to operate in aerial and aquatic environments, respectively. The need to mitigate acoustic clutter and ambient noise is common to both aerial and aquatic echolocating animals, resulting in convergence of many echolocation features, such as directional sound emission and hearing, and decreased pulse intervals and sound intensity during target approach. The physics of sound transmission in air and underwater constrains the production, detection and localization of sonar signals, resulting in differences in response times to initiate prey interception by aerial and aquatic echolocating animals. Anti-predator behavioral responses of prey pursued by echolocating animals affect behavioral foraging strategies in air and underwater. For example, many insect prey can detect and react to bat echolocation sounds, whereas most fish and squid are unresponsive to toothed whale signals, but can instead sense water movements generated by an approaching predator. These differences have implications for how bats and toothed whales hunt using echolocation. Here, we consider the behaviors used by echolocating mammals to (1) track and intercept moving prey equipped with predator detectors, (2) interrogate dynamic sonar scenes and (3) exploit visual and passive acoustic stimuli. Similarities and differences in animal sonar behaviors underwater and in air point to open research questions that are ripe for exploration.
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Adaptive Echolocation and Flight Behaviors in Bats Can Inspire Technology Innovations for Sonar Tracking and Interception
Target tracking and interception in a dynamic world proves to be a fundamental challenge faced by both animals and artificial systems. To track moving objects under natural conditions, agents must employ strategies to mitigate interference and conditions of uncertainty. Animal studies of prey tracking and capture reveal biological solutions, which can inspire new technologies, particularly for operations in complex and noisy environments. By reviewing research on target tracking and interception by echolocating bats, we aim to highlight biological solutions that could inform new approaches to artificial sonar tracking and navigation systems. Most bat species use wideband echolocation signals to navigate dense forests and hunt for evasive insects in the dark. Importantly, bats exhibit rapid adaptations in flight trajectory, sonar beam aim, and echolocation signal design, which appear to be key to the success of these animals in a variety of tasks. The rich suite of adaptive behaviors of echolocating bats could be leveraged in new sonar tracking technologies by implementing dynamic sensorimotor feedback control of wideband sonar signal design, head, and ear movements.
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- Award ID(s):
- 1734744
- NSF-PAR ID:
- 10174925
- Date Published:
- Journal Name:
- Sensors
- Volume:
- 20
- Issue:
- 10
- ISSN:
- 1424-8220
- Page Range / eLocation ID:
- 2958
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Unlike other predators that use vision as their primary sensory system, bats compute the three-dimensional (3D) position of flying insects from discrete echo snapshots, which raises questions about the strategies they employ to track and intercept erratically moving prey from interrupted sensory information. Here, we devised an ethologically inspired behavioral paradigm to directly test the hypothesis that echolocating bats build internal prediction models from dynamic acoustic stimuli to anticipate the future location of moving auditory targets. We quantified the direction of the bat’s head/sonar beam aim and echolocation call rate as it tracked a target that moved across its sonar field and applied mathematical models to differentiate between nonpredictive and predictive tracking behaviors. We discovered that big brown bats accumulate information across echo sequences to anticipate an auditory target’s future position. Further, when a moving target is hidden from view by an occluder during a portion of its trajectory, the bat continues to track its position using an internal model of the target’s motion path. Our findings also reveal that the bat increases sonar call rate when its prediction of target trajectory is violated by a sudden change in target velocity. This shows that the bat rapidly adapts its sonar behavior to update internal models of auditory target trajectories, which would enable tracking of evasive prey. Collectively, these results demonstrate that the echolocating big brown bat integrates acoustic snapshots over time to build prediction models of a moving auditory target’s trajectory and enable prey capture under conditions of uncertainty.
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To study sensorimotor behaviour in wild animals, it is necessary to synchronously record the sensory inputs available to the animal, and its movements. To do this, we have developed a biologging device that can record the primary sensory information and the associated movements during foraging and navigating in echolocating bats. This 2.6‐g tag records the sonar calls and echoes from an ultrasonic microphone, while simultaneously sampling fine‐scale movement in three dimensions from wideband accelerometers and magnetometers. In this study, we tested the tag on an European noctula Nyctalus noctula during target approaches and on four big brown bats Eptesicus fuscus during prey interception in a flight room. We show that the tag records both the outgoing calls and echoes returning from objects at biologically relevant distances. Inertial sensor data enables the detection of behavioural events such as flying, turning, and resting. In addition, individual wing‐beats can be tracked and synchronized to the bat's sound emissions to study the coordination of different motor events. By recording the primary acoustic flow of bats concomitant with associated behaviours on a very fine time‐scale, this type of biologging method will foster a deeper understanding of how sensory inputs guide feeding behaviours in the wild.more » « less
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Thaler, Lore (Ed.)Animals utilize a variety of active sensing mechanisms to perceive the world around them. Echolocating bats are an excellent model for the study of active auditory localization. The big brown bat ( Eptesicus fuscus ), for instance, employs active head roll movements during sonar prey tracking. The function of head rolls in sound source localization is not well understood. Here, we propose an echolocation model with multi-axis head rotation to investigate the effect of active head roll movements on sound localization performance. The model autonomously learns to align the bat’s head direction towards the target. We show that a model with active head roll movements better localizes targets than a model without head rolls. Furthermore, we demonstrate that active head rolls also reduce the time required for localization in elevation. Finally, our model offers key insights to sound localization cues used by echolocating bats employing active head movements during echolocation.more » « less
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Echolocating bats must process temporal streams of sonar sounds to represent objects along the range axis. Neuronal echo-delay tuning, the putative mechanism of sonar ranging, has been characterized in the inferior colliculus (IC) of the mustached bat, an insectivorous species that produces echolocation calls consisting of constant frequency and frequency modulated (FM) components, but not in species that use FM signals alone. This raises questions about the mechanisms that give rise to echo-delay tuning in insectivorous bats that use different signal designs. To investigate whether stimulus context may account for species differences in echo-delay selectivity, we characterized single-unit responses in the IC of awake passively listening FM bats, Eptesicus fuscus, to broadcasts of natural sonar call-echo sequences, which contained dynamic changes in signal duration, interval, spectrotemporal structure, and echo-delay. In E. fuscus, neural selectivity to call-echo delay emerges in a population of IC neurons when stimulated with call-echo pairs presented at intervals mimicking those in a natural sonar sequence. To determine whether echo-delay selectivity also depends on the spectrotemporal features of individual sounds within natural sonar sequences, we studied responses to computer-generated echolocation signals that controlled for call interval, duration, bandwidth, sweep rate, and echo-delay. A subpopulation of IC neurons responded selectively to the combination of the spectrotemporal structure of natural call-echo pairs and their temporal patterning within a dynamic sonar sequence. These new findings suggest that the FM bat’s fine control over biosonar signal parameters may modulate IC neuronal selectivity to the dimension of echo-delay.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/s20102958
