Hunting bats adjust their echolocation to receive weak prey echoes for clutter reduction

Abstract

How animals extract information from their surroundings to guide motor patterns is central to their survival. Here, we use echo-recording tags to show how wild hunting bats adjust their sensory strategies to their prey and natural environment. When searching, bats maximize the chances of detecting small prey by using large sensory volumes. During prey pursuit, they trade spatial for temporal information by reducing sensory volumes while increasing update rate and redundancy of their sensory scenes. These adjustments lead to very weak prey echoes that bats protect from interference by segregating prey sensory streams from the background using a combination of fast-acting sensory and motor strategies. Counterintuitively, these weak sensory scenes allow bats to be efficient hunters close to background clutter broadening the niches available to hunt for insects.

Fig. 1. Bats adjust their vocalizations to receive unmasked prey echoes from gradually smaller sensory volumes to guide prey capture.

(A) During the chase, the bat reduces the outgoing energy (colored dots) of its calls by ~40 dB and increases call repetition rate. Returning prey echoes (black) are very weak and cover a dynamic range of ~20 dB. Wingbeats (gray line) were derived from oscillations in the body acceleration. (B) The estimated target strength (TS) of the prey insect fluctuates between −30 and −20 dB at 0.1 m. The fast fluctuations in TS and EL at the end of the chase (green dashed box) are probably caused by wingbeats from the prey. (C) The measured range of the bat to the prey is shorter than the estimated maximum range over which the bat can hear the insect (dashed black lines). The sensory volumes of each call decrease during the capture (gray lines). (D) The echogram visualizes the sensory scene during the capture. Here, the prey echo stream consisting of ~35 echoes is clearly visible during the entire last second of the chase. The bat approaches the insect with a constant speed of 1.8 m/s in an open environment, as no clutter echoes are recorded by the tag. The dashed black lines mark the zone between two consecutive calls where the bat listens for returning echoes, i.e., the overlap free zone. (E) The dead-reckoned track (black line) and the calculated sensory volumes [colored shapes marking the three phases from (A): search, approach, and buzz] show how the bat maneuvers and adjusts its sensory volume to capture the insect (movie S2).

Fig. 2. Bats switch from a deliberate to a reactive sensorimotor mode upon prey detection.

(A to E) Bats actively adjust their biosonar parameters to different targets (i.e., prey or large background structures such as a tree) (A and B) to regulate the detection distance (C), sensory volume (D), and spatial redundancy (E) during commuting flight and three stages of aerial capture. (F) The sensory-to-motor range ratio is the relationship between the detection range (C) and reaction range of the bats using a reaction time of 100 ms (solid violins) or 200 ms (black outline violins). All plots depict the k means distribution (shaded area) and means (stars) of the data. n = 10 bats, 121 captures (4 to 15 random prey captures per individual to balance the study because the individual bats attack prey between 4 and 103 times per night), 4562 foraging calls, and 4092 commuting calls.

Fig. 3. Hunting bats actively generate weak prey echoes from a large range of prey items.

(A and B) Estimated TSs of aerial prey vary over a dynamic range of approximately 30 dB. (C and D) Source levels (gray) and prey echo levels (black) change as bats approach their target. (A to C) n = 1387 calls, 204 captures with visible prey echoes. (D) n = 10 bats; 43 recording hours; 1,200,368 calls; 1387 echoes. (E) Distribution of the slope for the distance-dependent change in source level (gray) and received echo level (black). Source levels followed a logarithmic fit to target range with a slope of 29 dB (±11 SD; R² = 0.79); echo levels followed a slope of −10 dB (±10 SD; R² = 0.35). n = 123 captures. This means that call source levels reduce by an average of 8.7 dB [i.e., 29*log₁₀(2)] per halving of distance while echo levels tend to increase by 3 dB over the same distance.

Fig. 4. Bats separate prey and clutter echo streams by acoustic gaze and motor pattern adjustments.

(A) The durations of the current call and the following call determine the inner (gray) and outer (purple) window, which together determine the overlap-free perceptual zone. The echo streams of prey (colored dots) and clutter (colored lines, according to each individually tagged bat; the black line depicts mean clutter distance) are located within the overlap-free zone. Histograms on the right axis show that prey and clutter echoes are spatially separated. (B) Timing of the disappearance of clutter from the auditory scenes (gray) and the maximum change in the flight path (red). The bats approach their prey with flexible nonstereotypic flight patterns, as their maximum change in flight paths span a large time scale (~2 s).