Active Listening for Spatial Orientation in a Complex Auditory Scene

To successfully negotiate a complex environment, an animal must control the timing of motor behaviors in coordination with dynamic sensory information. Here, we report on adaptive temporal control of vocal–motor behavior in an echolocating bat, Eptesicus fuscus, as it captured tethered insects close to background vegetation. Recordings of the bat's sonar vocalizations were synchronized with high-speed video images that were used to reconstruct the bat's three-dimensional flight path and the positions of target and vegetation. When the bat encountered the difficult task of taking insects as close as 10–20 cm from the vegetation, its behavior changed significantly from that under open room conditions. Its success rate decreased by about 50%, its time to initiate interception increased by a factor of ten, and its high repetition rate “terminal buzz” decreased in duration by a factor of three. Under all conditions, the bat produced prominent sonar “strobe groups,” clusters of echolocation pulses with stable intervals. In the final stages of insect capture, the bat produced strobe groups at a higher incidence when the insect was positioned near clutter. Strobe groups occurred at all phases of the wingbeat (and inferred respiration) cycle, challenging the hypothesis of strict synchronization between respiration and sound production in echolocating bats. The results of this study provide a clear demonstration of temporal vocal–motor control that directly impacts the signals used for perception

Average Turn Rate

<p>Plots mean turning rate of the flying bats in the three clutter conditions (10 cm, <i>n</i> = 7; 20 cm, <i>n</i> = 23; 40 cm, <i>n</i> = 29 trials included in the analysis) and the open room ( <i>n</i> = 10 trials), referenced to target contact time (zero on the abscissa). There was a significant difference in the bat's turning rate between clutter and open room conditions in the final 100 ms before target contact ( <i>F</i> = 4.78, <i>p</i> < 0.05). </p

Bat Performance

<p>Percentage of attempts and successful captures increased as the target–clutter separation increased, whereas the percentage of trials in which animals made no attempt to capture the target decreased. The bats' performance was tested in 51, 63, 70, and 32 trials at clutter distances of 10, 20, and 40 cm and open room, respectively.</p

Sonar Strobing Behavior

<div><p>Summarizes the analysis of sonar strobing behavior (see text for definition) in bats attempting insect capture under different clutter conditions. Included in the analyses summarized in (A), (C), and (E) are data from trials in which the bat hit or captured the insect positioned 20 cm from the clutter (17 trials), 40 cm from the clutter (25 trials), and the open room (11 trials). There were too few successful trials at 10 cm to include in these analyses. Note that the time axes differ across plots in this figure.</p> <p>(A) Shows the mean percentage of time the bats produced sonar strobe groups during the 1,000-ms time period before target contact. Data points plot the mean percentage time strobing at midpoints of 200-ms intervals (e.g., data point at −300 ms shows the mean percentage time strobing between the time interval 200–400 ms before target contact). Note that the highest incidence of strobing at 900 ms or more before contact occurred when the bat encountered the target 20 cm from the clutter.</p> <p>(B) Plots the PIs of successive sounds taken from a single trial, showing changes that occur in the temporal patterning of vocalizations before target contact. The strobe groups are circled in red.</p> <p>(C) Plots the mean PIs of sounds contained within strobe groups under open room and clutter conditions, averaged across 100-ms time intervals during the time period 600–200 ms before target contact. For example, the data point at −350 ms shows the mean strobe PI between −300 and −400 ms.</p> <p>(D) Time waveforms of sonar strobe groups taken from the data shown in (B) are displayed. The strobe groups are circled. Measurement of strobe PI is indicated in one of these strobe groups.</p> <p>(E) Plots the mean duration of sounds contained in strobe groups for the clutter and open room conditions, again referenced to target contact time and averaged over 100-ms time bins.</p> <p>(F) Illustrates the measurement of strobe sound duration for one of the sounds in the strobe groups shown above in (D).</p></div

Bat Flight Paths

<p>Shows plots of the bat flight paths and vocal temporal patterns recorded from three selected trials run with target–clutter separations of 10, 20, and 40 cm and open room. The far-left side shows 3-D plots of the bat's flight path with respect to the plant. The direction of the bat's approach is indicated by an arrow. The middle section shows overhead perspectives on the same four trials. Positions of branches are indicated by green asterisks and position of the worm is indicated by blue circles. The segment of the flight path shown in red corresponds to the time period in which the bat produced strobe groups. Again, arrows indicate the direction of the bat's flight path. The far-right side plots PIs of the sonar signals recorded during the approach and terminal phases of insect pursuit in each trial. Note that the example at 10 cm shows no buzz, as this was an aborted trial. In the open room example, the bat produced strobe groups as it first flew close to the target, but not in the final approach and interception of the target. Each of these examples shows a decrease in PI as the bat approaches the target and clear examples of sonar strobe groups. The strobe groups are characterized by stable PIs (up to 5% variation about the mean PI), interrupted by breaks that are at least 1.2 times the mean PI. The strobe groups produced by the bat in each of these examples are circled in the PI plots. In many instances, the production of strobe groups occurs over hundreds of milliseconds.</p

Schematic of Flight Room

<p>Shows setup for video and sound recordings of flight path and acoustic behavior of bats (b) capturing tethered mealworms (w) close to an echo clutter-producing plant (p). Two high-speed video cameras (c1 and c2) were mounted in the room to permit 3-D reconstruction of the bat's flight path in the calibrated space (c.s.). Video recordings were synchronized with audio recordings taken with ultrasonic microphones (m1 and m2) placed on the floor delivering signals to a digital acquisition system (IOtech WaveBook).</p

Behavioral responses of big brown bats to dives by praying mantises

Insectivorous echolocating bats face a formidable array of defenses employed by their airborne prey. One such insect defense is the ultrasound-triggered dive, which is a sudden, rapid drop in altitude, sometimes all the way to the ground. Although many previous studies have investigated the dynamics of such dives and their effect on insect survival rate, there has been little work on how bats may adapt to such an insect defense employed in the middle of pursuit. In this study we investigated how big brown bats (Eptesicus fuscus) adjust their pursuit strategy when flying praying mantises (Parasphendale agrionina) execute evasive, ultrasound-triggered dives. Although the mantis dive occasionally forced the bat to completely abort its chase (25% trials), in a number of cases (75% trials) the bat followed the mantis into the dive. In such cases the bat kept its sonar beam locked onto the target and maneuvered to maintain the same time efficient strategy it adopted during level flight pursuit, though it was ultimately defeated by the dive. This study suggests that although the mantis dive can be effective in evading the bat, it does not always deter the bat from continuing pursuit and, given enough altitude, the bat can potentially capture diving prey using the same flight strategy it employs to intercept prey in level flight

Average Trial Time

<p>The trial duration decreased with increasing target–clutter separation to the shortest duration for open room, measured in 11, 27, 36, and 31 trials at 10-, 20-, and 40-cm clutter distance and open room, respectively.</p

Control over Timing of Pulse Emission

<div><p>(A) shows the timing of sounds from a selected trial and the relation of the sonar strobe groups to the bat's wingbeat cycle, measured from the high-speed video recordings and illustrates that the coupling to wingbeat rate is not strict.</p> <p>(B) plots the distribution of sounds during the upstroke (exhalation; shown in blue) and downstroke (inhalation; shown in red) of the bat's wingbeat for sounds with different PIs, over nine trials. The total number of vocalizations included in the 10-ms PI time bins increases with decreasing PI, because the bat increases the number of vocalizations at shorter intervals as it approaches the target. Note that the distribution of sounds produced during the upstroke and downstroke of the wingbeat cycle becomes more similar for PIs shorter than 50–60 ms (approximately 17–20 sounds/s).</p></div