Echolocating bats can use acoustic landmarks for spatial orientation
1 Department of Psychology, University of Maryland, College Park, Maryland,
USA
2 Institute of Biology, University of Southern Denmark, DK-5230 Odense,
Denmark
* Author for correspondence at present address: Tønder Gymnasium and HF, DK-6270 Tønder, Denmark (e-mail: mj{at}toender-gym.dk)
Accepted 27 September 2005
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Summary |
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Key words: bat, Eptesicus fuscus, echolocation, acoustic landmark, orientation
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Introduction |
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Surprisingly, the exclusive use of acoustic landmarks has never before been
reported for any species. Even in rats, animals that have well developed
hearing, there are only negative findings for the use of acoustic landmarks
alone for spatial orienting. For example, Rossier et al.
(2000) demonstrated that the
addition of acoustic cues improved the performance of a rat using a visual
landmark in a water maze, but a sound stimulus alone was not sufficient for
the rat to orient properly. Indeed, there is no evidence for exclusive use of
acoustic landmarks for spatial orientation, even among auditory specialists
like echolocating bats. This raises the question of whether distal sensing of
sound can serve as a reliable reference for spatial orientation.
Microchiropteran bats use echolocation for spatial orientation, along with
the detection and tracking of prey
(Griffin, 1958). These animals
probe the surroundings with high frequency sound pulses and listen for
information about objects carried by their reflected echoes. They can detect
echoes from small objects at a distance up to 5 m
(Kick, 1982
). For object
localization, bats compute the direction using interaural differences in the
returning echoes and the distance from the time delay between sound emission
and returning echo. The spatial resolution of the bat's directional hearing is
comparable to many mammals, approximately 1° in the horizontal plane
(Masters et al., 1995
;
Simmons et al., 1983
) and
3° in the vertical plane (Lawrence and
Simmons, 1982
). By contrast, the bat's range resolution is highly
specialized (reviewed in Moss and
Schnitzler, 1995
). The bat processes information about the
environment from the direction and distance information extracted from sonar
echoes, computing a three-dimensional (3-D) acoustic representation which, in
turn, can be used to establish acoustic spatial landmarks for orientation.
Although bats have a high resolution echolocation system that allows them
to operate in complete darkness, their vision is adequate to provide spatial
information about landmarks in the environment
(Suthers, 1970;
Neuweiler, 1999
). The bat
retina responds best at low light levels and saturates at medium light levels
(Hope and Bhatnagar, 1979
).
Visual acuity of bats is poor compared with diurnal mammals, but is comparable
with many other nocturnal mammals
(Pettigrew et al., 1988
).
Visual acuity of the big brown bat is about 1°
(Bell and Fenton, 1986
),
similar to that of rodents.
Almost 30 years ago, Williams et al.
(1966) reported that
phyllostomid bats can indeed use vision to reference landmarks as they
navigate in familiar territory over several kilometers. This was demonstrated
in homing experiments, in which bats were wearing either opaque masks that
eliminated spatial vision or identical transparent masks, and were able to
home only with the transparent masks that permitted the use of vision.
Field observations also suggest that bats may use spatial memory in favor
of echolocation. For example, bats living in large numbers in caves appear to
rely on spatial memory when exiting at dusk. Under these conditions, bats
produce echolocation pulses, but if a barricade is placed at the opening of a
cave they crash into it (Griffin,
1958), which indicates that they may rely on spatial memory, not
echoes to orient in familiar environments.
That bats establish spatial memory of the environment is also suggested by
the results of laboratory studies. For example, Griffin
(1958) required a bat to
perform an S-shaped flight path between a roost site and a feeding site in a
room. Once the bat had become familiar with the room, one of the obstacles, a
large masonite plate, was moved so that the opening was now at the opposite
site. The bat consistently produced around 20 echolocation pulses per second
when flying and yet, when the plate was moved the bat crashed into it at the
previous position of the opening. In another study, bats of the species
Megaderma lyra were trained to fly through a mesh with 70 squares,
each 14 cmx14 cm, to access a feeding station. Both vision and
echolocation were available to the bat in this experiment, and the results
showed that each bat picked a preferred opening to fly through, and remembered
the position of this opening with an accuracy of 2 cm
(Neuweiler and Möhres,
1967
). Also under conditions of illumination that would permit the
bat's use of vision, studies have also demonstrated egocentric navigation in
Phyllostomus discolor
(Höller, 1995
;
Höller and Schmidt,
1996
), and allocentric navigation in Eptesicus fuscus
(Mueller and Mueller,
1979
).
More recent field experiments
(Helversen and Helversen,
2003), and laboratory experiments in a naturalistic environment
(Winter and Stich, 2005
),
demonstrated that phyllostomid bats have a large capacity for spatial memory.
Also, vespertilionid bats like Eptesicus nilssonii visit the same
feeding patches and return to the same roost, not only after a night's hunt,
but also year after year (Rydell,
1990
). These studies do not exclude the bat's use of vision
either, but they show that bats establish a memory of the area in which they
live and forage, and such spatial representations can persist for a long
time.
Although it has been demonstrated conclusively that echolocating bats can
use hearing to represent space with high resolution
(Moss and Schnitzler, 1995)
and that they can rely on 3-D acoustic information to orient in complex
environments (Moss and Surlykke,
2001
), the bat's exclusive use of echolocation to establish
spatial landmarks has not been previously demonstrated. A more complete study
of the bat's use of sensory information to build representations of space is
important, not only for understanding the orientation behavior of this animal
in particular, but for learning more about spatial memory systems in
general.
To determine whether an animal can use acoustic landmarks for spatial orientation, we conducted a series of experiments with echolocating bats under conditions that precluded their use of vision. We examined details of dynamic changes in sonar signal production and flight behavior when bats used echolocation alone to navigate and seize prey in a complicated environment, where it might improve its success if it made use of acoustic landmarks. Eptesicus fuscus was chosen as the study animal because its adaptive echolocation behavior is well described both in the field and the laboratory. We used the bat's adaptive response in sonar pulse design as an indicator of how it perceives its immediate surroundings, to reveal how it exploits landmarks and/or spatial memory while navigating in a complex, but familiar, environment and, importantly, in the absence of visual cues. Our results show that echolocating bats can make use of acoustic landmarks to guide 3-D flight paths.
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Materials and methods |
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Experimental set-up
During experiments the flight room was illuminated with low level (less
than 0.05 lux) long-wavelength light (>650 nm), precluding the bats from
using vision to perform the task (Hope and
Bhatnagar, 1979). Experiments were conducted in a large flight
room (6.5 mx7 mx3 m) lined with acoustic foam. The room was
divided by a mist net (Avinet, Dryden, NY, USA;
Fig. 1) made of 0.1 mm diameter
threads, and the space between adjacent threads was 25 mm. The knots that tied
the threads together in a diamond pattern were 0.4 mm thick. A hole with a
diameter of 35 cm was cut in the net. The bats were trained to fly through
this hole to gain access to a food reward on the other side
(Fig. 1). The position of the
net opening was adjacent to a landmark in some experiments (see below). For
practical reasons the net opening could only be moved in the horizontal plane,
and no vertical movement was possible. The center of the hole was
approximately 1.5 mabove the floor. The behavior of the bats was recorded on
two gen-locked, high-speed video cameras (Kodak Motion Corder; 240 frames
s1) placed in two corners of the room. Using a calibration
frame and commercial software (Motus 3.2, Centennial, CO, USA) this setup
allowed us to reconstruct the 3-D flight path of the bats. Simultaneous with
the video recordings, echolocation calls were picked up by two ultrasound
microphones (Ultrasound Advice; 3.5 cm in diameter) on the floor one on each
side of the net, as shown in Fig.
1. The echolocation pulses were amplified (40 dB), band pass
filtered (10100 kHz, ±3 dB, Stanford Research Systems,
Sunnyvale, CA, USA), and recorded onto two channels on a Wavebook (IoTech,
Cleveland, OH, USA) with sampling rate of 250 kHz for each channel. A manual
end-trigger system was connected to both the video and sound recording
systems. Upon triggering, the preceding 8 s from a buffer of the audio and
video recordings were stored. This set-up allowed us to correlate the bat's
acoustic behavior with its flight behavior in each trial.
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Sound analysis
The echolocation sounds were analyzed using a custom MatLab program
(BatGadget, written by Aaron Shurger and modified by Amaya Perez). Sound
parameters analyzed were signal duration, signal interval (measured from start
of one signal to the start of the next), start- and end-frequency of the first
harmonic, and the bandwidth between these two measurements. Time parameters
were measured from the oscillogram, whereas the frequency parameters were
measured from the spectrogram. Spectrograms were made of 256 points Fast
Fourier Transform (FFT), using a Hanning window and 45% overlap between
consecutive FFTs. Bats using frequency modulated (FM) signals reduce signal
duration as they approach an object, thus continually avoiding an overlap
between outgoing cry and returning echo
(Cahlander et al., 1964;
Kalko and Schnitzler, 1989
;
Hartley, 1992
). The time, or
space, in which such an overlap would occur, has been referred to as the
pulseecho overlap zone (Kalko and
Schnitzler, 1993
) or the `inner window'
(Wilson and Moss, 2004
). It is
assumed that this zone or inner window is an indicator of the shortest range
at which a bat is searching for prey. We used the bats' pulse duration to
calculate the size of the inner window as (
) x signal duration
x speed of sound (Kalko and
Schnitzler, 1993
), i.e. the minimum target distance in front of
the bat where there is just no overlap between outgoing pulse and returning
target echo.
Video analysis
For each video frame, the positions of the bat, the landmark, each
microphone, the edge of the net hole (using eight evenly spaced markings) and
the mealworm were digitized. Each object was marked with a different color to
identify it and match up the spatial coordinates of recordings in the two
cameras. The coordinates were then exported to a database and combined with
the sound recordings to generate a 3-D animation of the bat's flight path in
relation to the hole, the landmark and the worm using a MatLab program
(written by Aaron Schurger and modified by Amaya Perez).
Echo measurements
We measured the echoes from the net, the worm and the landmark. Sounds were
generated using a Tucker-Davis-Technologies System 2 (Alachua, FL, USA;
hardware and software), amplified, filtered (Stanford Research Systems) and
broadcast through a speaker [Tweeter LT800; frequency response flat (±3
dB up to 100 kHz)] powered with Krone-Hite DC amplifier. Echoes were picked up
with a GRAS '' microphone (40BF; Holte, Denmark) amplified
40 dB by a Larsen and Davis amplifier/power supply, filtered by a WaveTech
filter (Karachi, Pakistan; band pass filtered 10100 kHz) and digitized
on-line with a Wavebook (Iotech), using a sampling rate of 500 kHz. The
emitted signal was 1 ms in duration and consisted of a downward linear
frequency modulated (FM) sweep, from 90 kHz to 20 kHz, shaped by a Hanning
window function. The source level from the speaker was 77 dB re SPL at 10 cm.
The signal was repeated every 0.05 s. The speaker and the microphone pointed
towards the same position on the target, but the microphone was placed 10 cm
closer to the target than the speaker to maximize the signal-to-noise ratio
(SNR). The speaker was placed 50 cm from the target. With a signal duration of
1 ms there was no overlap between outgoing sound and incoming echo. We
measured the target strength of the net at two angles, 90° and 45°,
respectively, between the net and the sound beam. Target strengths of the
landmark and the mealworm were only measured from one angle. All target
strength calculations are referenced to 10 cm such that the target strength
was measured in dB as the echo level 10 cm from the target relative to the
incoming sound level at the target. The target strength of the net measured at
an angle of 90° was 26 dB, whereas the target strength measured at
an angle of 45° was 22 dB. The target strength of the tethered worm
was 16 dB, and that of the landmark was measured to 1 dB. All
sound levels are given in dB SPL re 0.0002 Pa rms. The microphones were
calibrated using a Sound Level Calibrator (Brüel & Kjær 4231;
Nærum, Denmark).
Behavioral experiments
Since the only source of light came from low level (<0.05 lux), long
wavelength (>650 nm) illumination, the bats could only obtain information
about the room through echolocation (Hope
and Bhatnagar, 1979). The bats were trained to fly through the
hole in a mist net (see details above) and catch a tethered mealworm on the
other side. After the initial training a landmark, a photo tripod, was
introduced and placed 10 cm to the left of the hole, adjacent to it with the
top of the tripod at level with the center of the hole. The bats were released
from the same area (within 1 m3) in all trials. In the first
56 sessions, the setup was moved every fourth trial. The landmark was
always at that same position relative to the hole, whereas the mealworm was
moved to a new position between each trial. We did this to show the bats that
the landmark provided them with reliable information about the hole's
position. We introduced control trials, in which only the landmark was moved
to a new position, whereas the hole remained in the same position. Only one
control trial was run in each session. After 56 sessions with the setup
being moved every fourth trial, we started moving the setup between every
trial. Again one control trial was conducted in each session. At the end of
each trial the bat was caught in a butterfly net and held in that while the
setup was moved and the video and sound recordings were downloaded for
off-line analyses. This break between trials lasted for approximately 5 min.
In control trials when only the landmark was moved, we caught the bat and made
the same sounds as when we moved the net, and the break lasted as long as
between test trials. Bats were tested 56 days a week. Each test day is
referred to as a session, with 511 trials run for each bat in each
session. We defined a trial as the time from the release of the bat until it
flew through the hole or the experimenter aborted the trial. An aborted trial
occurred when the bat stopped attempts to fly through the hole, hung on the
wall producing few or no echolocation pulses, or repeatedly crashed into the
net in the same position. In control trials the experimenter terminated a
trial after the bat had crashed into the net three times. From the time the
bat was released until it passed through the net opening it was free to fly
around on the release side, exploring the net, the landmark and the hole. The
bat's behaviors were noted on data sheets, and the duration of each trial was
determined. We also noted how often and where the bat crashed into the net,
and how often it inspected the net, and the hole. In control trials it was
further noted if the bats inspected the landmark. In test trials it was not
possible to separate inspections of the hole from inspections of the landmark,
since these were too closely spaced. The bat's behavior was classified as an
inspection when it flew up close to the net (or the hole and the landmark) and
then away, or flew close (within 50 cm of the net) and parallel to the net
using an increased repetition rate of echolocation pulses relative to the
repetition rate used before closing in on the net. The start of the inspection
was noted as the point where the bat came within 50 cm of the net.
Finally, we conducted a series of experiments in which the landmark was removed and the bats were required to find the opening in the net using echolocation and/or spatial memory of the setup. The opening in the net was moved to a new position at the start of the no-landmark sessions and remained in that same position throughout the session. In this way we could test if the bats developed a memory of such a setup within a short time of exposure (six trials per session) as some earlier anecdotal reports have suggested. The bats were still caught between trials and remained in the capture net while video and audio data were downloaded.
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Results |
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General behavior
The three bats had individual approaches to solving the task. When the
female F1 was released, she flew directly to the same spot on the wall from
which she produced echolocation pulses of long duration (around 68 ms).
The time she spent on the wall was highly variable, lasting between a few
seconds and several minutes. When taking off, she reduced pulse duration to
ca. 3 ms and either flew one or two rounds before going back to the wall, or
made an attempt to go through the hole. If the attempt resulted in a crash
into the net she returned to the same spot on the wall. The male M1 never
landed on the wall, but flew continually through an entire trial. Upon release
he used echolocation pulses with durations around 3 ms. The signal duration
was reduced as he approached the net. Most often M1 went straight from the
release site to the hole and attempted to go through it. If he crashed into
the net, he flew one or two rounds in the room and then made a new attempt to
go through the hole. The second male M2 also flew throughout an entire trial
and used the same range of pulse durations as M1. However, M2 flew a couple of
rounds after release and inspected the hole and/or landmark more frequently
than the other bats before he attempted to go through the hole. Thus, the
individual behaviors of the three bats were different, but as the results
show, the relative changes in behavior and performance with changes in the
setup were similar for the three animals.
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With the landmark next to the hole, the bats found the opening in 99100% of all these trials (Fig. 3). Since they could only fly through the hole once per trial, an average score of 1 in Fig. 3 means that the bat eventually found the hole in all trials. Before finding the opening in the net, the bats occasionally flew into parts of the net. Such crashes into the net occurred on average between 0.3 and 0.4 times per trial when the landmark was adjacent to the hole (Fig. 3A). The vast majority of those few crashes into the net happened just around the hole, with the remaining crashes occurring at the position where the hole had been in the previous trial (47%, Table 2).
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In control trials, the landmark was moved to a position away from the hole. In these trials one bat (M1) never found the hole (thus a value of 0 in Fig. 3B), whereas the two other bats (M2 and F1) found it in 20% of the trials (Fig. 3B). All bats crashed repeatedly into the net next to the landmark where the hole normally was found relative to the landmark. The average number of crashes when the landmark was moved away from the hole was between 1.8 and 3 per trial for the three bats (Fig. 3B), which is significantly more crashes than when the landmark was next to the opening (within bats P<0.05, Student's t-test). For example, M1 flew directly into the net next to the landmark where the net hole was previously found relative to the landmark. He crashed in this position without hesitation three times in a row. Also F1 crashed repeatedly next to the landmark in these control trials. However, the other male bat, M2, did not crash as consistently as the two others. This bat sometimes stalled in front of the net and flew away, as if detecting the faint echoes from the net. Yet, this did not prevent M2 from crashing into the net at this position in the next attempt.
In the experiments with no landmark the two bats (M2 and F1) crashed as often as 1.4 and 2.2 times on average per trial, but eventually found their way through the hole in 8285% of the trials (Fig. 3C). The bats did not crash at random into the net. In fact, the majority of crashes were at the position where the opening had been on the previous session, and a considerable number of crashes occurred just around the hole (within 15 cm from the rim; numbers are listed in Table 2). Bat M1 died before it could be tested in the no-landmark setup.
On average the bats took less than 20 s per trial when the landmark was placed adjacent to the hole, whereas they spent on average 40 s or more when the landmark was moved away from the hole or was absent (Fig. 3D). This is consistent with the increased number of inspections and crashes when the landmark was moved or absent (Figs 3 and 4).
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In the no landmark experiments, the hole remained in the same position throughout the session, which made it possible to investigate whether the bats improved their performance over the course of a session. The average performance improved from trial to trial through the sessions and the bats spent less time seeking the net opening in the later trials compared to the first ones across sessions (Fig. 5A,B). This trend is most clear for the bat F1 (Fig. 5B). The total number of crashes and inspections per trial remain relatively unchanged in the course of a session, but after parsing the crashes into `crash into net' and `crash into net near hole', a different pattern appears (Fig. 5C,D). From trial to trial the number of crashes at the previous position of the hole decreased and by trial 5 or 6, both bats rarely crashed into the old hole position. After 56 trials F1 flew through the new hole without much difficulty, whereas M2 also aimed at the new hole, but had some trouble determining the exact position, and hence crashed now and then.
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The acoustic behavior indicates that the bats crashed into the net because they did not detect it. There were no obvious differences between the sonar behavior of a bat that crashed into the net and one that flew successfully through the hole. In fact, it was not possible to infer from its echolocation pattern if the bat had a successful fly-through or crashed into the net.
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Discussion |
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In the present study, an echolocating bat searched for an opening in a mist net, which allowed it access to a food reward. The bat performed this task under conditions that excluded its use of vision, and therefore only echoes from its sonar vocalizations provided spatial information about the environment. An echo-reflecting landmark provided the bat with a spatial reference to find the opening in the net. After the bat had learned that the landmark provided spatial information about the opening in the mist net, it successfully found its way to the food reward. In experimental trials, the relative position of the landmark and net opening was held constant, though they were both moved inbetween trials. In control trials, the landmark and net opening were moved independently. Although the sonar returns from the mist net can be detected by the echolocating bat, the animals favored use of the landmark over the net echoes to guide orientation behavior. The bat's reliance on the acoustic landmark was indicated by repeated crashes into the net in control trials, in which the spatial cue was invalid.
The bats produced echolocation calls continuously during all trials, but
since the animals crashed into the net adjacent to the landmark in control
trials, they either ignored or failed to perceive the echoes from the net. The
echoes from the landmark were 2125 dB more intense than the net echoes.
Listening for the intense echo from the landmark is undoubtedly an easier task
than searching for opening of the net that produced echoes with a target
strength around 22 dB and 26 dB at 10 cm, which is less than
target strengths measured from some of the smallest moths that bats feed on
(around 17 dB at 10 cm, at 30 kHz;
Surlykke et al., 1999).
When the landmark was removed altogether from the setup, the bats spent more time searching for the hole, and they crashed into the net more frequently than when the landmark was present and positioned adjacent to the net opening. Over the course of a test day when the landmark was absent, the bats spent less time searching for the net opening and found the net opening more consistently. Furthermore, in the first trials of a session the bats crashed most frequently into the net at the position where the hole had been on the previous session, and in the later trials, when bats crashed into the net, they did so in regions adjacent to the opening. We therefore conjecture that the bats had adequate acoustic information to detect the net, but relied more on the strong echoes obtained from the landmark when it was available to reference the position of the net opening.
The bats' crashes around the net opening in the final trials of a session
without the adjacent landmark suggest that they learned the approximate
position of the opening, likely referenced to other fixed objects in the room,
such as the microphones on the floor, but that the resolution of the spatial
reference was too low for complete clearance through the opening in each
attempt. Other studies of spatial memory in different bat species report
higher memory resolution than we found in the present study of E.
fuscus (Höller,
1995; Neuweiler and
Möhres, 1967
). In fact, the bat, M. lyra, remembered
the position of an opening with an accuracy of 2 cm
(Neuweiler and Möhres,
1967
). One might therefore infer that M. lyra shows much
better resolution in spatial memory than the bats in our study. However, in
the study on M. lyra the bats had several days (the exact number of
days is not provided by the authors) to learn the position of a preferred
opening in the grid, whereas the bats in our study only had one session
(consisting of 6 trials) to learn the position of the net opening.
Furthermore, the lights were on during the experiment with M. lyra,
and the authors argue that bats require visual cues to obtain spatial memory
of an area (Neuweiler and Möhres,
1967
). This argument is based on the observation that sighted bats
found their roost with a higher success rate than blinded bats
(Barbour et al., 1966
;
Williams et al., 1966
).
It is indeed noteworthy that all prior studies of spatial memory in bats
have been conducted with illumination permitting the use of vision
(Hahn, 1908;
Neuweiler and Möhres,
1967
; Höller,
1995
). The reduced performance accuracy we find in the present
study, compared to the study on M. lyra, can be explained by a
combination of species differences, lack of visual cues, or the difference in
time allowed for the bats to develop a high resolution spatial representation
of the environment, or perhaps all three possibilities. It is likely that a
combination of visual and auditory cues can improve the bats' performance, as
has been shown for rats (Rossier et al.,
2000
), and this could possibly be true for other animals as well.
Importantly, the data reported here demonstrate that bats can develop spatial
references through the auditory system alone.
In the present study, the bats produced echolocation sounds throughout a trial and thus had the possibility of using sonar returns to find the opening in the net, rather than using spatial memory. The echo measurements of the net revealed that the sonar returns were weak, but also that their strength depended on the angle of ensonification, such that a bat approaching the net at a perpendicular angle received a weaker echo than a bat approaching it at a smaller angle. During inspections, the bats often flew nearly parallel to the net, thus increasing the net echo strength. This may have helped them to detect the part of the net with the opening, even though the apparent size of the opening is reduced when the angle of approach diminished. Regardless of the angle of approach, the bats had difficulties finding the opening, suggesting that the contrast between the net and the hole was poor, due to the faint echoes from the net. Therefore, the use of spatial landmarks would offer the animal an advantage in finding its way through the net opening.
Acoustic behavior
There were no obvious differences between the patterns of vocal production
from a bat flying successfully through the net opening and those from a bat
flying into the net. In both situations, the bats decreased signal duration
and interval as they approached the net, responding in both cases as if they
were approaching an object. This suggests a dissociation between processing
and responding to echoes that would inform the bats of an imminent crash.
When the bats inspected the net, their acoustic behavior was not entirely
predictable. The signal duration and interval decreased with approach to the
net, but the reduction was not as pronounced as when they flew through the
opening or crashed into the net. All bats occasionally produced high rate
sound groups during an inspection of the net, and this was always accompanied
by sharp turns and/or loops in the flight path. The high rate sound groups
have been described in a number of situations, for example a bat landing at a
roost site or inspecting an object (Faure
and Barclay, 1994). As mentioned above, these high rate sound
groups resemble the feeding buzz, but the pulse duration and pulse interval
never become as short as in a buzz that precedes insect capture. In the
feeding buzz of E. fuscus, pulse duration and interval can become as
short as 0.5 ms and 5.5 ms, respectively. A feeding buzz in E. fuscus
can also be divided into a buzz I and a buzz II phase
(Surlykke and Moss, 2000
;
Griffin et al., 1960
). In the
high rate sound group the pulse duration drops below 1 ms, but the pulse
interval never falls below 10 ms, and this vocal behavior pattern never
develops into the buzz II phase, which is characteristically produced before
feeding. The high rate sound groups provide the bat with a higher rate of
acoustic sampling, and it may be that approach to a roosting perch, or in this
case passage through an obstacle, requires increased accuracy in sonar
localization.
The reduced sonar signal duration and interval is an expected response from
a bat approaching an object. However, at some point before flying through the
hole, or crashing into the net, the bats abruptly increased sonar signal
duration, which resulted in an overlap between the outgoing cry and the net
echo. Since bats that use frequency modulated sonar vocalizations actively
avoid pulseecho overlap under most conditions
(Cahlander et al., 1964;
Kalko and Schnitzler, 1989
;
Hartley, 1992
), the abrupt
increase in cry duration indicates that the bat shifted its acoustic gaze to a
position further away, i.e. to the other side of the net. Exactly, how far out
along the range axis the bat shifted its gaze is not possible to determine
from the signal duration, which only indicates the shortest object range to
which the bat is responding. Indeed, the bat may be attending to echoes from
objects at a distance that extend beyond the inner window constrained by sonar
signal duration. During inspections, the bats adjusted their sonar signal
duration consistently to avoid pulseecho overlap, even in situations
when no high rate sound groups were produced. Therefore, during inspections,
the bats' acoustic gaze was presumably at the net and the landmark, but not
the other side of the net.
In this study, we found that bats can rely on landmarks perceived through auditory cues alone. This, of course, does not rule out the bat's use of visual cues in the development of a spatial representation of the natural environment. Bats often fly out at dusk, and during the commute between the roost and the hunting area, there will often be some level of light available, especially in regions with long dusks and light nights. In some parts of the world, dusk lasts for more than an hour, and it may never get completely dark overnight, leaving the bat with reliable visual cues to orient. In areas where the nights can get very dark, moonlight may provide the bats with sufficient illumination for using vision, along with echolocation to successfully establish and reference spatial landmarks.
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Acknowledgments |
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References |
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