Echolocation signals and pinnae movement in the fruitbat Rousettus aegyptiacus
Abstract
The fruit bat Rousettus aegyptiacus has highly mobile pinnae. Little is known about the role that such movements play in sound localisation however and whether they interact with the process of echolocation in this species. Here we report the correspondence of echolocation signals in free flight with the downward wingbeat and forward movement of the pinnae, and demonstrate that the ears have a greater sensitivity to click stimuli in front of the animal when directed forwards than when back and to the side. The potential significance of the production of echolocation signals whilst the ears are moving from their least sensitive to their most sensitive position is discussed.
1 Figures
INTRODUCTION
Rousettus aegyptiacus is a member of
the only genus within the Megachiroptera to
echolocate. Brief click-like signals are
produced by the tongue (Möhres and
Kulzer, 1956; von Herbert, 1985; Holland
et al., 2004). The signals are low in ener-
gy compared to Microchiropteran echoloca-
tion calls (Holland et al., 2004) and it has
often been assumed that this form of
echolocation is rudimentary compared to
that of Microchiropterans (Griffin et al.,
1958). Nevertheless, it has been demon-
strated that R. aegyptiacus performs compa-
rably with Microchiropteran bats in wire
obstacle avoidance tasks (Waters and Voll-
rath, 2003). Other than this, nothing is
known about the echolocation system of
R. aegyptiacus.
We noted that R. aegyptiacus has highly
mobile pinnae. Several mammalian species
possess highly mobile pinna that can move
independently of head direction. Despite
this common adaptation, very little attention
has been given to the function of pinnae
movements. When not mobile, the pinnae
serve to provide unique spectral cues, the
head related transfer function (HRTF) that
can be used to give information about the
direction of a sound source (Middlebrooks,
1992). Mobile pinnae may aid location of
a sound source by allowing the animal to
obtain multiple samples of an acoustic ob-
ject (Thurlow and Runge, 1967) and to sep-
arate the spectrum of a sound source from
the HRTF (Young et al., 1996). The func-
tional role of pinna movement has received
only limited experimental attention how-
ever (Populin and Yin, 1998). The only
Acta Chiropterologica, 7(1): 83–90, 2005
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS
Echolocation signals and pinnae movement in the fruitbat
Rousettus aegyptiacus
RICHARD A. HOLLAND and DEAN A. WATERS
School of Biology, University of Leeds, Leeds, LS2 9JT, United Kingdom
E-mail: bgyraho@leeds.ac.uk
The fruit bat Rousettus aegyptiacus has highly mobile pinnae. Little is known about the role that such
movements play in sound localisation however and whether they interact with the process of echolocation in
this species. Here we report the correspondence of echolocation signals in free flight with the downward
wingbeat and forward movement of the pinnae, and demonstrate that the ears have a greater sensitivity to click
stimuli in front of the animal when directed forwards than when back and to the side. The potential significance
of the production of echolocation signals whilst the ears are moving from their least sensitive to their most
sensitive position is discussed.
Key words: fruit bat, Rousettus aegyptiacus, echolocation, pinnae movement
demonstration of a sound localisation func-
tion comes from work on the Microchiro-
pteran Rhinolophid bat Rhinolophus fer-
rumequinum. Several authors described the
correspondence of echolocation pulse and
rapid ear movement in these bats (Griffin et
al., 1962; Pye et al., 1962; Pye and Roberts,
1970). Rhinolophus ferrumequinum moves
its ears in a cycle in which one ear moves
forwards as the other moves backwards and
to the side. The bat emits one echolocation
call per half cycle of pinna movement.
Mogdans et al. (1988) demonstrated that
bats with surgically immobilised pinnae
were unable to locate targets in a vertical
plane, suggesting that pinna scanning
movements in this animal were for determi-
nation of target elevation. An investigation
using a robotic model of a bat suggests that
pinna mobility functions to provide dynam-
ic temporal cues that are not possible with
immobile pinna (Walker et al., 1998).
A previous study has demonstrated that
the pinnae of R. aegyptiacus show direc-
tionality in sound localisation (Obrist et al.,
1993), but unlike other bats in which pinna
design matches specialisations in call de-
sign the ears of R. aegyptiacus are not spe-
cialised, conforming to the general pattern
of other mammals such as cats (Obrist et al.,
1993). However, it was not known whether
the ear movements of this species corre-
sponded in any way with echolocation sig-
nal emission, or function to improve the de-
tectability of the signal. It is the aim of this
study to observe and record the pinnae
movements of R. aegyptiacus to discover
what relation they have to echolocation sig-
nal production and to investigate what ef-
fect pinna position has on the reception of
sounds received.
MATERIALS AND METHODS
Experimental Subjects
Four adult R. aegyptiacus (3 YY, 1 X), on loan
from Tropical World Zoo, Leeds, UK, were housed in
a 3.6 m × 1.8 m × 1.5 m cage in a room at 25ºC on a
12 h light 12 h dark reversed photoperiod. They were
fed 150 g of fruit each per day and had access to wa-
ter at all times.
Procedure
A Kodak digital High Speed Video (HSV) SR-
500 camera with a 12.5 mm lens was used to record
the bats in free flight. A multi channel data link
(MCDL, Kodak Ekta Pro) was connected to a U-30
Bat detector (Ultrasound Advice) and this was linked
to the HSV. From this every time an echolocation
click was detected by the bat detector the MCDL
could convert it to a digital pulse that was displayed
on the video footage. Two Photon Beard A410 300W
lamps were positioned on the camera tripod to pro-
vide illumination above room light levels. The camera
was set to record at a rate of 500 frames per second
giving a time/frame resolution of 2 ms. The camera
was triggered manually to start recording and the bat
was released towards it from a distance of 5 m. If the
footage was acceptable it was downloaded in slow
motion onto Digital 8 tape using a Sony DCR-
TRV355E Digital Handycam in VCR mode. At least
five flights were recorded for each bat. The record-
ings took place in a 20 m × 2 m × 3 m (l × w × h) cor-
ridor that was next to the bats housing room. The bats
flew directly over the camera and towards a perch 10
m away at the end of the corridor.
Analysis
Video was transferred to a PC using a Sony iLink
cable connected to an IEEE 1394 fireboard adapter
(LaCie Ltd, www.Lacie.com). Video was captured us-
ing Adobe Premiere©6.0 at a pixel aspect ratio of
1.067 (D1/DV PAL) and frame size of 720 × 576 pix-
els. Once captured the movie clip was converted to a
video for windows format so that it could be com-
pressed in order to transfer it to digitising software
and saved as an AVI file. The compressor codec used
was Indeo®video 5.10. To digitise the image Dgeeme
1.0 software (GeeWare.com), available in the public
domain, was used. A digitising model was created in
which six points were digitised: centre of left ear tip,
centre of right ear tip, centre of left eye, centre of right
eye, centre of nose and a fixed point on the screen.
The captured AVI file was imported into the digitising
program and the six points were digitised frame by
frame as X-Y co-ordinates. These coordinates were
then imported into an excel spreadsheet which was
constructed to calculate the distance from each ear
to the nose and eye to eye distance using simple
geometry. The nose to ear distance was scaled by the
84 R. A. Holland and D. A. Waters
eye to eye distance, which provided a constant on the
bats head. This distance was then plotted to indicate
the relative distance between each ear and the nose
over time. An example frame with points recorded is
shown to demonstrate how the distance that the pin-
nae moved relative to the nose was calculated (Fig.
1). Only traces where all the fiducial points were vis-
ible throughout the whole video clip were digitised.
There was some noise inherent in the procedure due
to the fact that the image available and therefore the
movement recorded were relatively small, but may
also have been due to the fact that the image was only
available in two dimensions. We tested this by digi-
tising the same image at three different magnifica-
tions (1×, 2×, and 4×) 10 times and comparing the er-
ror. We discovered that the larger the image the small-
er the error (ANOVA, F2, 3 = 10.67, P< 0.0001;
Tukey’s post hoc test: 1× vs. 2×, P> 0.05, 1× vs. 4×,
P< 0.0001, 2× vs. 4×, P< 0.012). This supports our
hypothesis that the small nature of the image con-
tributed greatly to the error in digitizing. When the
original traces were digitised we found that magnify-
ing images when the bat was relatively far from the
camera gave very poor images due to the relatively
small number of pixels making them. Because of this
we decided to use 1× magnification throughout to be
consistent. The data was thus plotted as means of 10
frames per point to smooth out the error from the
digitising.
Echolocation and pinnae movement 85
As well as digitising, the cycle of any wing beats
and ear movements were recorded by noting the
frames in which directional wing beats and ear move-
ments started. The occurrence of any echolocation
clicks were plotted along with these cycles. Echo-
location clicks were categorised according to which
part of the wing beat cycle and any ear movement cy-
cle they corresponded with. Footage was digitised
from the point when the bat was in level flight after
release until the image became too unfocused to
analyse.
HRTF Measurement
In order to investigate how ear positions effect
the reception of sounds, full head casts from two re-
cently naturally deceased bats were made out of latex.
Casts were made with the ears directed forward and
the ears directed to the side to mimic the positions in
flight. Ears were held in place with pins until the la-
tex set. A hole was cut in the ear canal and the cast
was placed over a Larson Davis 2520 ¼” microphone
with the protective grid on (±4 dB 20 Hz–40 kHz)
that was in a fixed position. The cast was secured to
the microphone with putty. Thus when casts with ear
forward were exchanged for casts with ear back and
to the side the microphone would remain in the same
position, i.e. with the nose pointing directly at the
speaker. When the cast was in position 200 µs square
wave gated sine waves produced by a Grass
Instruments SD5 stimulator were played through
an Ultrasound Advice speaker and these were
captured via the microphone onto a Keithley
Metrabyte DAS 50 data acquisition card at 12 bits at
a rate of 1 MHz. The power spectrum of each of 10
of the captured 200 µs sine waves was calculated
from a 128 point FFT (Hanning window) using
Testpoint©(Capital Equipment). Recordings were
made for the 2 bats with ears forward and ears back-
ward and with no cast and the microphone pointing
directly at the speaker. All recordings were made 1 m
from the speaker. For each ear position the mean of
10 sine waves received from the microphone only
was subtracted from the mean of 10 sine waves re-
ceived by microphone in the cast. This was done at
each frequency point in the 128 point FFT. These
were then plotted to compare the level to which the
ear position enhanced or subtracted from the sound
reception when the ear was forward and the ear was
backward at each frequency. Since the difference be-
tween the microphone with the ear cast in place and
without the ear cast in place was used as a measure-
ment of the gain of the ear, it is independent of the
frequency response of both the speaker and the mi-
crophone.
FIG. 1. Sample frame to demonstrate digitising:
A — right ear-nose distance, B — left ear nose
distance, C–D — eye–eye scaling distance
AB
CD
RESULTS
Pinnae Movements
The pattern of pinnae movement ob-
served was that they made regular forward
and backward sweeping arcs during flight.
This could be observed in the video clips by
the fact that the inside of the pinnae disap-
peared from view as they moved backwards
and reappeared again as they moved for-
wards. Thus when the pinnae were directed
forward this exposed the ear canal to
sounds approaching from in front. When di-
rected to the side this occluded the ear canal
from such sounds. Both pinnae of these bats
moved forward and backwards simultane-
ously. An approximate sinusoidal pattern
can be observed in the digital trace of pinna
movement as the pinnae move closer to the
nose as they are directed forward and then
86 R. A. Holland and D. A. Waters
0
1
2
3
4
5
6
7
0 50 100 150 200 250 300
frame
arbitrary distance
right ear
left ear
FIG. 2. Digitised traces of ear movements in bat 1. The averaged trace is shown superimposed over each ear
further away as they are directed back and
to the side for each of the bats recorded
(Fig. 2). Echolocation clicks were signifi-
cantly more likely to occur on the down-
ward wing beat (down stroke: 117, up-
stroke: 20, χ2= 69.19, d.f. = 1, P< 0.001)
and significantly more likely to occur as the
ears were moving forward (forward: 118,
backward: 18, χ2= 73.53, d.f. = 1, P<
0.001; see Fig. 3).
HRTF Measurement
The ears forward consistently show
higher gain than ears backwards in the fre-
quency range with the exception that cast 1
shows a dip at 35 kHz (Fig. 4).
DISCUSSION
Occurrence of echolocation clicks dur-
ing the downward wing beat phase in
Echolocation and pinnae movement 87
Fig. 3. Wing beat and pinnae movements in relation to echolocation signals in bat 2. Clicks are shown by spikes.
The points at which the pinnae are furthest forward and furthest to the side are plotted by the line with
(peaks represent furthest to the side and troughs represent furthest forward on an arbitrary scale). The wing beat
cycle is represented by the line with (peaks represent the wings at their highest point and troughs represent
the wings at their lowest point on an arbitrary scale)
R. aegyptiacus is in agreement with earlier
work by von Herbert (1985). Here we
demonstrate for the first time that the ear
movements of R. aegyptiacus during flight
consist of a sweep forward and then back
and to the side and that echolocation signals
are significantly more likely to be emitted
during the forward sweep. These ear move-
ments are not similar to those reported to be
displayed by R. ferrumequinum, which
have been shown to aid in vertical target lo-
cation. The HRTF measurements from two
casts of bats heads indicate that there is a
higher gain to a sound directed at the bat
when the ear is forward than when it is back
and to the side. This in itself is not a sur-
prising finding and Obrist et al. (1993) have
also previously demonstrated directionality
in the pinnae of this bat. However the fact
that the bats are emitting their echolocation
signals as the ears are moving from least
sensitive to most sensitive is interesting.
This suggests some possible hypotheses for
the function of ear movements during flight
in R. aegyptiacus. First the bat may be di-
recting its ears forward in order to receive
the echoes of its echolocation signals. This
raises the question however of why the bats
move them back. Asecond possibility, if the
ear is less sensitive to echoes returning
from objects in front of the bat when fur-
thest back, is that producing the signal be-
fore the ears are at their furthest forward
(and by implication most sensitive) serves
to prevent forward masking of early return-
ing echoes. Some Microchiropteran bats are
known to increase the sensitivity of their
hearing as a function of time after call by
desensitising the ossicles at the point of
emission and then gradually increasing
0
2
4
6
8
10
12
1 16 31 46 61 76 91 106 121 136 151 166 181 196 211 226 241
frame
arbitrary distance
click
wing beat
ear movements
88 R. A. Holland and D. A. Waters
FIG. 4. (A) and (B). Head related transfer functions (HRTFs) for the two casts recorded with the ear directed
forward and the ear directed to the side
-50
-40
-30
-20
-10
0
10
0 20000 40000 60000 80000 100000 120000
frequency (Hz)
dB (relative scale)
ears forward
ears to side
-40
-35
-30
-25
-20
-15
-10
-5
0
5
10
15
0 20000 40000 60000 80000 100000 120000
frequency (Hz)
dB (relative scale)
ears forward
ears to side
A
B
their sensitivity (Simmons et al., 1992).
This allows the bat to call at maximum in-
tensity without masking early returning ech-
oes as well as achieving gain control. Other
Microchiropterans and dolphins achieve a
similar effect by modulating call amplitude
(Hartley, 1992; Boonman and Jones, 2002;
Au and Benolt-Bird, 2003). Evidence sug-
gests that R. aegyptiacus does not modulate
call amplitude (Holland et al., 2004). If ear
movements in R. aegyptiacus were tightly
linked to echolocation call emission then
these might serve the function of masking/
gain control.
This research demonstrates that the ear
movements of R. aegyptiacus coincide in a
predictable way with the emission of its
echolocation signals. Further research is
necessary to determine what function these
ear movements may provide.
ACKNOWLEDGEMENTS
This research was supported by BBSRC grant
number S15544. We thank CBS technical staff for
animal husbandry and Tropical World Zoo, Leeds
for the loan of the fruit bats. Paolo Viscardi provid-
ed invaluable help with developing the digitising
model.
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Received 17 November 2004, accepted 21 December 2004
- CitationsCitations12
- ReferencesReferences22
- The second noise model (S9Fig. -right) has both a bias in the estimation of θ(t) and additive Gaussian noise that is θ-dependent[20][21][22]: ~ y ¼ asinðybÞ þ 0:4ny þ 0:15n ð23Þ with the parameters a = 2.22 and b = 0.458, and n is the Gaussian noise. In the light conditions, the simulated bat estimated the angle-to-target θ by using both vision and echolocation (the real bats did not completely stop echolocating at this light level).
[Show abstract] [Hide abstract] ABSTRACT: Author Summary Bats are extremely skillful aviators: they are able to capture prey and land on targets under challenging flight conditions, as well as maneuver accurately using either echolocation or vision. It remains a mystery, however, how bats—or other flying animals—rapidly translate the noisy incoming sensory information into correct motor commands in order to converge onto a target. To address this question, we developed a sensorimotor control model that explains animal flight guidance and tested it in bats with experiments conducted under dark and light conditions. The model reproduced the bats’ flight trajectory with very high accuracy, suggesting that bats have to estimate not only the angle to target but also changes in the angle over time (angular velocity). Additionally, we demonstrate that the bat must suppress its sensory noise by integrating sensory information over several sonar pulses in order to successfully guide its flight. Comparisons of flight trajectories in light and dark suggest that the surprisingly curved flights exhibited by bats in the dark are due to sensory noise, not motor limitations. We hypothesize that rapidly moving animals must adaptively change their motor control strategy to optimally match the sensory conditions.- It should be pointed out however, that while these signals were recorded returning to the bat, it does not necessarily hear them all. This is because, unlike the sensor, the bat has pinnae that it is known to actively scan (Holland and Waters, 2005) whilst echolocating. This may provide directional filtering of the returning echoes not available to the sensor microphone.
[Show abstract] [Hide abstract] ABSTRACT: Bats are capable of imaging their surroundings in great detail using echolocation. To apply similar methods to human engineering systems requires the capability to measure and recreate the signals used, and to understand the processing applied to returning echoes. In this work, the emitted and reflected echolocation signals of Rousettus aegyptiacus are recorded while the bat is in flight, using a wireless sensor mounted on the bat. The sensor is designed to replicate the acoustic gain control which bats are known to use, applying a gain to returning echoes that is dependent on the incurred time delay. Employing this technique allows emitted and reflected echolocation calls, which have a wide dynamic range, to be recorded. The recorded echoes demonstrate the complexity of environment reconstruction using echolocation. The sensor is also used to make accurate recordings of the emitted calls, and these calls are recreated in the laboratory using custom-built wideband electrostatic transducers, allied with a spectral equalization technique. This technique is further demonstrated by recreating multi-harmonic bioinspired FM chirps. The ability to record and accurately synthesize echolocation calls enables the exploitation of biological signals in human engineering systems for sonar, materials characterization and imaging.- [Show abstract] [Hide abstract] ABSTRACT: Recent molecular phylogenies have changed our perspective on the evolution of echolocation in bats. These phylogenies suggest that certain bats with sophisticated echolocation (e.g. horseshoe bats) share a common ancestry with non-echolocating bats (e.g. Old World fruit bats). One interpretation of these trees presumes that laryngeal echolocation (calls produced in the larynx) probably evolved in the ancestor of all extant bats. Echolocation might have subsequently been lost in Old World fruit bats, only to evolve secondarily (by tongue clicking) in this family. Remarkable acoustic features such as Doppler shift compensation, whispering echolocation and nasal emission of sound each show multiple convergent origins in bats. The extensive adaptive radiation in echolocation call design is shaped largely by ecology, showing how perceptual challenges imposed by the environment can often override phylogenetic constraints.
- [Show abstract] [Hide abstract] ABSTRACT: For over half a century, the echolocating bat has served as a valuable model in neuroscience to elucidate mechanisms of auditory processing and adaptive behavior in biological sonar. Our article emphasizes the importance of the bat's vocal-motor system to spatial orientation by sonar, and we present this view in the context of three problems that the echolocating bat must solve: (i) auditory scene analysis, (ii) sensorimotor transformations, and (iii) spatial memory and navigation. We summarize our research findings from behavioral studies of echolocating bats engaged in natural tasks and from neurophysiological studies of the bat superior colliculus and hippocampus, brain structures implicated in sensorimotor integration, orientation, and spatial memory. Our perspective is that studies of neural activity in freely vocalizing bats engaged in natural behaviors will prove essential to advancing a deeper understanding of the mechanisms underlying perception and memory in mammals. • active sensing • behavioral neurobiology • echolocation • spatial cognition • navigation
- [Show abstract] [Hide abstract] ABSTRACT: Echolocation is an active form of orientation in which animals emit sounds and then listen to reflected echoes of those sounds to form images of their surroundings in their brains. Although echolocation is usually associated with bats, it is not characteristic of all bats. Most echolocating bats produce signals in the larynx, but within one family of mainly non-echolocating species (Pteropodidae), a few species use echolocation sounds produced by tongue clicks. Here we demonstrate, using data obtained from micro-computed tomography scans of 26 species (n = 35 fluid-preserved bats), that proximal articulation of the stylohyal bone (part of the mammalian hyoid apparatus) with the tympanic bone always distinguishes laryngeally echolocating bats from all other bats (that is, non-echolocating pteropodids and those that echolocate with tongue clicks). In laryngeally echolocating bats, the proximal end of the stylohyal bone directly articulates with the tympanic bone and is often fused with it. Previous research on the morphology of the stylohyal bone in the oldest known fossil bat (Onychonycteris finneyi) suggested that it did not echolocate, but our findings suggest that O. finneyi may have used laryngeal echolocation because its stylohyal bones may have articulated with its tympanic bones. The present findings reopen basic questions about the timing and the origin of flight and echolocation in the early evolution of bats. Our data also provide an independent anatomical character by which to distinguish laryngeally echolocating bats from other bats.
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