Stereotyped active sensing in fast-diving echolocating bats

Abstract

Mexican free-tailed bats (Tadarida brasiliensis) often return to their roosts in darkness or low-light conditions from high altitudes (>3 km) during steep, fast dives. We recorded 26 bats as they performed reentry dives to their canyon roost in New Mexico shortly after dawn and analyzed their sensorimotor behaviors. We tracked bats at altitudes up to 25.6 m above the ground; they dove at maximum speeds of 22.1 m/s (82.1 km/h), experienced forces up to 9.2 g, and traversed distances of up to 6 m (∼60 body lengths) between receiving echoes from the ground. Bats adjusted their echolocation in a stereotyped pattern once the ground was within detection range by decreasing signal duration, shortening interpulse intervals, and increasing signal end frequency. Our analyses suggest that bats receive relatively sparse echo information during dives and likely integrate this information with cognitive spatial maps and available visual cues to safely complete their high-speed roost reentry.

Keywords: acoustic signal processing; zoology.

Graphical abstract

Figure 1

Summary of bat flight behavior during reentry (A) Compilation of cropped video frames from camera 4 showing one bat’s flight trajectory. The bat’s position in the first frame is circled in green, and its position in the last frame is circled in orange. Inset: polar histograms of the flight directions in which bats are traveling at the start and end of flight tracking. (B) Reconstructed 3D flight paths of all tracked bats, showing speed (color scale) and positions of echolocation call emissions (gray dots). Triangles indicate video camera positions, and the diamond indicates the position of the ultrasonic microphone. (C) Flight speed was highly correlated with bat height (individual bats represented by different color-shape combinations). (D) Waveform and spectrogram showing an exemplar of a recorded echolocation call. Echolocation calls are frequency-modulated (FM) signals beginning around 41 kHz and sweeping downward to approximately 26 kHz.

Figure 2

Changes in acoustic parameters across height and speed of N = 26 bats Points indicate individual echolocation calls. Solid lines show the linear regression for each panel’s data, with gray shading indicating smoothed 95% confidence intervals. Pearson’s r correlation values and p values are provided on each plot. (A) Call durations decrease as bats approach the cave opening, resulting in durations that remain below the limit of call-echo overlap (black line), defined as the time it would take for the reflected echo to return to the bat and potentially interfere with the emitted signal. Note that the longest call durations we observed would have resulted in call-echo overlap had they been emitted at the lowest heights at which bats were calling. (B) IPI values decrease with decreasing height. (C) Echolocation end frequencies increase as the bats approach the cave opening. (D–F) The same acoustic parameters do not vary as strongly with speed. Note that not all data points are independent, as each bat emitted a consecutive series of calls.

Figure 3

Sensorimotor dynamics across acoustic phases and height (A) Illustration of the acoustic phases, as described in STAR Methods. (B) Composite images of video frames during reentry for one bat, with acoustic periods indicated by color (emitting, yellow; waiting, orange; receiving, pink; responding, purple). (C) Boxplots of speed (m/s, top), pitch angle (degrees, middle), and curvature (bottom) across acoustic phase. Boxplots show medians (center horizontal line), first and third quartiles (upper and lower box limit), and whiskers (vertical lines) representing data within 1.5 times the interquartile range; individual points indicate outlier data. Emit, emitting the call, Wait, waiting for the first echo to return, Rec., receiving the first echo from the ground, Resp., responding to the immediate ground echo and integrating additional echoes before producing the next echolocation call. Curvature and pitch angle did not significantly change across acoustic phases (χ² tests, p > 0.05), whereas speed demonstrated a consistent reduction across acoustic phases (p < 0.01). (D) Calculated distances traveled by bats between pulse emissions in relation to their height (individual bats represented by different color-shape combinations). Bats traveled a maximum of 6.1 m (∼60 body lengths) between pulse emissions, with this distance decreasing as they approached the ground. (E) Estimated time-to-contact (TTC) with the ground based on bats’ heights and speeds. Plotted lines indicate TTC based on average bat speeds and heights (black line); TTC minus the estimated time for a sound to travel to the ground and back (blue line); and TTC minus sound travel time and either 100 ms (pink dashed line) or 300 ms (red dashed line), simulating the time at which a bat would receive an echo when using different IPIs. Green points indicate individual bats’ estimated TTC, accounting for sound travel time and their actual IPI. The shaded area represents the theoretical range at which echoes from the ground are first detectable; see supplemental results.