Fast sensory–motor reactions in echolocating bats to sudden changes during the final buzz and prey intercept

Abstract

Echolocation is an active sense enabling bats and toothed whales to orient in darkness through echo returns from their ultrasonic signals. Immediately before prey capture, both bats and whales emit a buzz with such high emission rates (≥180 Hz) and overall duration so short that its functional significance remains an enigma. To investigate sensory-motor control during the buzz of the insectivorous bat Myotis daubentonii, we removed prey, suspended in air or on water, before expected capture. The bats responded by shortening their echolocation buzz gradually; the earlier prey was removed down to approximately 100 ms (30 cm) before expected capture, after which the full buzz sequence was emitted both in air and over water. Bats trawling over water also performed the full capture behavior, but in-air capture motions were aborted, even at very late prey removals (<20 ms = 6 cm before expected contact). Thus, neither the buzz nor capture movements are stereotypical, but dynamically adapted based on sensory feedback. The results indicate that echolocation is controlled mainly by acoustic feedback, whereas capture movements are adjusted according to both acoustic and somatosensory feedback, suggesting separate (but coordinated) central motor control of the two behaviors based on multimodal input. Bat echolocation, especially the terminal buzz, provides a unique window to extremely fast decision processes in response to sensory feedback and modulation through attention in a naturally behaving animal.ost sensory systems passively sample the environment by relying on extrinsic energy sources like light or sound to stimulate sensory receptors. Truly active senses, e.g., the electric sense of weakly electric fishes (1) and echolocation (2), where the animal itself produces the energy used to probe the surroundings, are rare (3). The advanced echolocation systems of bats and toothed whales involve dynamic adaptation of the outgoing sound and behavior based on perception of the surroundings through information processing of returning echoes.The temporal pattern of echolocation signals during prey pursuit changes through three phases: search, approach, and terminal buzz. The buzz, immediately preceding prey capture, is characterized by a dramatic increase in signal repetition rate and is universally present in both bats and whales capturing moving prey (4-8). Repetition rates up to 640 Hz have been reported for porpoises and, contrary to bats, odontocete buzzes usually continue beyond prey contact (6). The buzz of many vespertilionid and molossid bats has two distinct subphases: buzz I with decreasing call durations and intervals, followed by buzz II, with a constant maximum call repetition rate and a characteristic frequency drop of up to an octave (4,(9)(10)(11)(12)(13)(14).The function of the terminal buzz is still not understood (15). It has been hypothesized that odontocete buzzes not only track prey before capture (7), but may also serve to follow escaping prey (6). Bat buzzes have also been hypothesized to help track ev...

Fishing Technique of Long-Fingered Bats Was Developed from a Primary Reaction to Disappearing Target Stimuli

“…daubentonii , suggesting that our observations in M . capaccinii might extend to other trawling bats too [21]. …”

Ecology and evolutionary biology of fishing bats

“…, Geberl et al. , and six in Hulgard & Ratcliffe ) could provide skewed results. Ideally, laboratory experiments should be complemented by field experiments in which fish densities are manipulated by the researchers if the experimental area is enclosed, or researchers track variation in bat behaviour in response to natural fluctuation in fish density.…”

“…Although bats usually abort their attacks upon flying insects if the intended prey suddenly disappears in the early phase of the capture process (Marimuthu , Geberl et al. ), when a fish disappears under the water, bats continue their attack towards the last tracked location of the item, so they are likely to be performing a blind capture attempt (Aihartza et al. ).…”

Bats pre-adapt sensory acquisition according to target distance prior to takeoff even in the presence of closer background objects

“…refs. 9, 12 and 13) but bats’ flexibility in initiating it has hardly been tested. For a given species and a given task (e.g., landing), the approach behavior has been described as highly stereotypical, beginning at a certain distance and including a reduction of signal duration and signal-intervals from a specific initial value to a specific ending value.…”

“…Several previous studies have examined bats’ flexibility in terminating the approach sequence 9, 12, 13 but their flexibility when initiating it is yet to be studied. The success of the approach depends on emitting signals with appropriate distance dependent parameters.…”