Jeffrey M. Knowles

Spatial memory and stereotypy of flight paths by big brown bats in cluttered surroundings

SUMMARY The big brown bat, Eptesicus fuscus, uses echolocation for foraging and orientation. The limited operating range of biosonar implies that bats must rely upon spatial memory in familiar spaces with dimensions larger than a few meters. Prior experiments with bats flying in obstacle arrays have revealed differences in flight and acoustic emission patterns depending on the density and spatial extent of the obstacles. Using the same method, combined with acoustic microphone array tracking, we flew big brown bats in an obstacle array that varied in density and distribution in different locations in the flight room. In the initial experiment, six bats learned individually stereotyped flight patterns as they became familiar with the space. After the first day, the repetition rate of sonar broadcasts dropped to a stable level, consistent with low-density clutter. In a second experiment, after acquiring their stable paths, each bat was released from each of two unfamiliar locations in the room. Each bat still followed the same flight path it learned originally. In a third experiment, performed 1 month after the first two experiments, three of the bats were re-flown in the same configuration of obstacles; these three resumed flying in their accustomed path. The other three bats were flown in a mirror-image reconfiguration of the obstacles; these bats quickly found stable flight paths that differed from their originally learned paths. Overall, the flight patterns indicate that the bats perceive the cluttered space as a single scene through which they develop globally organized flight paths.

Spatial location influences vocal interactions in bullfrog choruses

A multiple sensor array was employed to identify the spatial locations of all vocalizing male bullfrogs (Rana catesbeiana) in five natural choruses. Patterns of vocal activity collected with this array were compared with computer simulations of chorus activity. Bullfrogs were not randomly spaced within choruses, but tended to cluster into closely spaced groups of two to five vocalizing males. There were nonrandom, differing patterns of vocal interactions within clusters of closely spaced males and between different clusters. Bullfrogs located within the same cluster tended to overlap or alternate call notes with two or more other males in that cluster. These near-simultaneous calling bouts produced advertisement calls with more pronounced amplitude modulation than occurred in nonoverlapping notes or calls. Bullfrogs located in different clusters more often alternated entire calls or overlapped only small segments of their calls. They also tended to respond sequentially to calls of their farther neighbors compared to their nearer neighbors. Results of computational analyses showed that the observed patterns of vocal interactions were significantly different than expected based on random activity. The use of a multiple sensor array provides a richer view of the dynamics of choruses than available based on single microphone techniques.

Non‐random patterns of acoustic interactions in chorusing bullfrogs.

Male bullfrogs form choruses to vocally advertise for females and to announce territory occupation to rival males. In dense choruses, calls of individual males may temporally overlap due to the large numbers of vocalizing neighbors. Overlapping calls may be a deliberate communicative strategy, perhaps to form a more salient auditory object in order to effectively guide females to a particular location within the chorus. We used a custom‐written MATLAB program to simulate the proportions of overlapping and nonoverlapping calls in five mock choruses, and then compared model output to empirical data from natural choruses of equal size. The simulation assumed that each bullfrog called independently of his neighbors according to a Poisson process so that overlapping calls occur randomly rather than through cooperation. In four of the five empirical recordings, the number of overlapping calls was significantly smaller than the averages produced by corresponding simulations, indicating that more males vocalized together in bouts than predicted by the random simulation. Empirical and simulated data also differed significantly in the remaining chorus, but in the opposite direction. These data suggest that overlapping calls may confer some communicative advantage. [Work supported by NSF Advance program.]

Implications of the variety of bat echolocation sounds for understanding biosonar processing

The variety of echolocation sounds used by different species of bats have implications for target ranging. Signals recorded at individual sites reveal species stacked in different frequency bands, perhaps to avoid cross-interference. Search-stage signals include short single-harmonic or multi-harmonic tone-bursts, or very shallow FM bursts. These narrowband sounds have abrupt onsets to evoke phasic on-responses that register echo delay, but with limited acuity. Wider FM sweeps used for searching by other bats evoke on-responses at many more frequencies for better delay acuity. These sound types may signify foraging in the open, within broad spaces bounded relatively remotely by trees or the ground. Intervals between broadcasts are consistent with biosonar operating ranges set by the boundaries of the scene in relation to atmospheric attenuation. Most species make transitions to wider signal bandwidth during interception by increasing FM sweep-width or adding harmonics. Additionally, wideband, multi-harmon...

Echolocation behavior of pairs of flying Eptesicus fuscus recorded with a Telemike microphone.

Four big brown bats (Eptesicus fuscus) were flown singly and in pairs in a room containing a sparse array of vertically hanging plastic chains as obstacles. Each bat carried a lightweight radio telemetry microphone (Telemike) that recorded their emitted echolocation sounds without artifacts from Doppler shifts, directional effects, and atmospheric attenuation. The broadcasts of both bats were also recorded with two stationary ultrasonic microphones located at the far end of the flight room. The echolocation broadcasts of bats flying singly were compared to those emitted when the bats were flown together. The principal change was shifting of harmonic frequencies very slightly (<5 kHz) away from each other and from frequencies used when flying alone. In contrast, the duration of emissions was more stable between single and double bat flights. Changes in ending frequency have been associated with a jamming avoidance response in big brown bats and could indicate attempts to avoid interference while flying wit...

Passive acoustic monitoring of bullfrog choruses: Spontaneous and evoked changes in group calling activity

We developed a multiple-microphone array method for recording temporal and spatial interactions of groups of vocalizing male bullfrogs, and for analyzing how this chorusing behavior is perturbed by playbacks of modified frog calls. Chorusing bullfrogs were recorded over 3 nights (90 min sessions) using an array of ten MEMS microphones distributed along a 20-m sector beside a natural pond. Vocal responses were digitized at 50 kHz using Measurement Computing A-to-D boards and customized software on a Lenovo Thinkpad. Individual frogs were located by time-difference-of-arrival measurements at the array. Baseline chorus activity was recorded for 10-20 min before and after playbacks. Playbacks consisted of digitized exemplars of two natural 5-croak advertisement calls, which were manipulated by adding or subtracting spectral components or by introducing masking noise. Baseline chorus activity featured both alternation of calls, mostly between far neighbors, and overlapping of calls, mostly by near neighbors. B...

Computational model of a bioinspired broadband receiver for sonar clutter reduction.

Echolocating bats have the ability to seamlessly navigate through dense foliage and other obstacles at flight velocity using only the information available in acoustic returns. The spatial resolution required to perform this feature cannot be explained by conventional beamforming and pulse design techniques. We describe a biologically inspired broadband sonar receiver that mimics parallel neural processing by echolocating bats to suppress clutter in complex acoustic environments. These results are incorporated into an improved version of the spectrogram correlation and transformation (SCAT) receiver by replacing the original spectrogram transformation block with a process that translates both harmonic coherence and spectral interference patterns into estimates of echo‐delay separations for closely spaced echo highlights. The model treats simple target echoes as highlight reconstructions, and broader lowpass filtered echoes—characteristic of most off‐axis clutter—as numerous overlapping poorly defined shap...

Changes in spectrotemporal features of echolocation signals in multiple bat assemblages.

Echolocating bats face potential acoustical interference when flying and foraging near echolocating conspecifics. Quantifying changes in the signal structure of echolocation emissions between bats flying alone and within a larger group has proven difficult. Here, we use two new methodologies, an onboard radio telemetry microphone and a multiple microphone array to record the sounds of big brown bats (Eptesicus fuscus) flying alone and in small groups both in the laboratory and in the field. In a laboratory flight room, bats changed the ending frequency of their first harmonic when the conspecific with which they were paired emitted calls at a similar frequency. In the field, ending frequency and sweep shape were more variable among groups of bats flying together than among single bats compared to one another. The presence of other nearby bats did not have any effect on the timing of emissions or the interpulse intervals [Work supported by NIH, NSF, ONR, and JSPS.]

Reconstructing echolocation behavior using time difference of arrival localization and a distributed microphone array as a virtual Telemike.

Bats use echolocation to probe their 3‐D environment. New techniques in distributed microphone array processing allow us to record echolocation behavior, reconstruct the flight paths, and generate an acoustic record of individual bats flying the laboratory or the field. Probabilistic methods of time difference of arrival localization allow us to follow bats navigating in flight room mazes, foraging in the wild and using active sonar in the presence of possible jamming from conspecifics. By reversing the localization operation, we back out the changing propagation times of the sounds emitted by bats flying fast in three dimensions. Through beamforming, we then create an amplified acoustic track that follows the reference frame of the bat, amounting to a virtual Telemike based on consensus data from the microphone array. Spatial tracking and virtual on‐board recording allow us to ask new questions about the spectral and temporal strategies employed by echolocating bats and to model the neural and perceptual natures of sonar. [Work supported by ONR and NSF.]

Bioacoustic and behavioral correlates of spatial memory in echolocating bats.

Echolocating bats face a unique orientation problem due to their reliance on echolocation over visual orientation. Each observation (sonar vocalization) only contains information about objects in front of and within at most 5–10 m of the animal. Because their behavior extends over much larger distances, spatial memory might be particularly important during foraging activity and free flight to integrate the shorter views provided by sonar. To investigate memory for object locations, Eptesicus fuscus were allowed to fly freely in an instrumented flight room populated with sparse obstacles (hanging chains). Bat position and vocalization were monitored with a stereo‐registered pair of thermal cameras and an array of ultrasonic microphones synchronized to the video. Data were analyzed for correlates of spatial memory‐flight path dynamics, head aim, and temporal structure of echolocation signals. Data recorded from bats free‐flying in the chain array are consistent with memory of obstacle locations and high‐lev...