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First published online September 5, 2008
Journal of Experimental Biology 211, 2976-2988 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.020057
In-flight corrections in free-flying barn owls (Tyto alba) during sound localization tasks
Institute of Biology II, RWTH Aachen, Kopernikusstraße 16, 52074 Aachen, Germany
* Author for correspondence (e-mail: laura{at}bio2.rwth-aachen.de)
Accepted 17 July 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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800 ms. The
landing precision of the owls, defined as their distance to the in-flight
speaker, did not decrease with increasing stimulus delay, but decreased if the
owl failed to perform a correction turn towards that speaker. Landing
precision was higher for a short (50 cm) than for a large (100 cm) distance
between the initial and the new target. Thus, the ability of barn owls to
adapt their flight path to a new sound target depends on the in-flight
stimulus delay, as well as on the distance between initial and novel
targets.
Key words: barn owl, auditory, hearing, sound localization, flight, three-dimensional, target approaching, behavior
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Wagner, 2002) that enhance
spatial localization and a facial ruff that is extremely directionally
sensitive (Brainard et al.,
1992; Campenhausen and Wagner,
2006; Coles and Guppy,
1988; Haresign and Moiseff,
1988; Keller et al.,
1998). These features help the owl to catch prey in complete
darkness (Konishi, 1973a;
Konishi, 1973b;
Payne, 1962). In a natural
environment, prey animals do not necessarily emit ongoing noises. Hence,
striking barn owls must be able to localize short, interrupted stimuli. Even
though owls favor swooping on stationary prey, or at least have higher success
rates on stationary prey (Ilany and Eilam,
2008), they need to adapt their trajectories during flight with
respect to the target if the prey is moving. Thus, it is interesting to
investigate whether barn owls are able to strike at a sound target in
darkness, if the stimulus stops with the owl's take-off and reappears after a
varying time delay (in-flight stimulus delay) at a horizontally displaced
spatial position (Konishi,
1973a; Konishi,
1973b). Such a task requires fast processing of auditory stimuli,
as well as behavioral adaptation to changing target positions.
The ability to hit a target is crucially influenced by the ability to
localize the target. Auditory targets appearing close to the midline are being
localized by barn owls with an accuracy of at least 3 deg., if the bandwidth
of the signal is wide enough and covers the behaviorally relevant range of
about 5.5 to 9.5 kHz (Bala et al.,
2003; Bala et al.,
2007). With increasing eccentricity of the sound source, the
accuracy decreases, especially for the elevational component of the target
(Knudsen et al., 1979). In
free-flight experiments, where the owl had to strike a distant target,
striking accuracy in the horizontal plane was 5 deg., whereas it was 7 deg. in
the vertical plane (Konishi,
1973b).
As the eyes and ears of the owl are virtually immobile, barn owls perform a
saccadic head movement in the direction of broadband stimuli
(Knudsen et al., 1979) to
bring the target into sensory focus. This natural saccadic response was
exploited as a means for localization precision mainly in experiments in which
owls remained sitting on a perch and did not fly (`stationary setups')
(Bala and Takahashi, 2000;
Bala et al., 2003;
Knudsen et al., 1979;
Poganiatz and Wagner, 2001;
Poganiatz et al., 2001;
Saberi et al., 1999). In these
experiments, no impairment in sound localization was observed when the
stimulus was as short as 75 ms (Knudsen
and Konishi, 1979), supporting the notion that barn owls may use
an open-loop strategy for sound localization. Open loop refers to experimental
conditions in which the reaction time (here the latency until the head turn
starts) exceeds the stimulus duration, which prevents ongoing feedback; under
closed-loop conditions, the stimulus duration exceeds the reaction time (see
Knudsen et al., 1979). We
created an open-loop scenario by stopping the stimulus at take-off and let it
reappear after a variable in-flight delay.
Experimental setups using head turns are appropriate to investigate the
basic principles and relevant parameters for sound localization, but do not
take into account the total behavioral sequence of target striking. Recently,
Shifferman and Eilam, Edut and Eilam, and Ilany and Eilam studied how owls
strike at moving prey (Shifferman and
Eilam, 2004; Edut and Eilam,
2004; Ilany and Eilam,
2008). Approaching a distant target requires a higher effort than
does performing a ballistic head saccade in the direction of a sound source.
Free-flight tasks therefore provide more natural conditions for the
investigation of localization performance. Payne and Konishi were the first to
conduct such studies (Payne,
1962; Konishi,
1973a; Konishi,
1973b). These authors exposed barn owls to tonal or noise stimuli
and determined the influence of parameters such as the bandwidth and the
duration of the stimulus on striking precision. Konishi found that three noise
bursts, each of 50 ms duration with a silent interval of 300 ms, enabled
target striking equally as well as with ongoing stimulation
(Konishi, 1973b). These
findings led to the hypothesis that barn owls are able to adapt their flight
path to a new target location as a reaction to short stimuli provided during
flight, even if the stimulation is interrupted.
Although Konishi (Konishi,
1973b) gives insights into the barn owl's general ability to
strike a distant target, it is not clear whether target striking resembles an
all-or-none law or gradually decreases depending on the stimulus parameters.
The present study is the first to measure in-flight correction in a
free-flying owl. We investigated whether the time delay of an in-flight
stimulus is a crucial parameter for accurate target localization when
in-flight corrections are required. In addition, we wanted to learn at which
threshold delay the owl is no longer able to adapt its flight path to a new
target sound during flight.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Apparatus and stimuli
All free-flight experiments were carried out in a sound-proof room of 4.2
mx3.2 mx3.2 m (lengthxwidthxheight,
Fig. 1). Sound attenuation was
achieved by covering the walls, ceiling and floor with planar and pyramidal
foam. Two devices, each containing two shielded loudspeakers, could be placed
at variable horizontal distances (2.35 m, 2.85 m and 3.35 m) to a wooden perch
(1.75 m above the floor; Fig.
1). The speakers formed a row approximately perpendicular to the
owl's flight direction and were numbered from LS1 to LS4, with LS1 being the
outermost left speaker and LS4 the outermost right speaker, seen from the
owl's perspective. The solid angles from the perch to the speakers varied
inherently with the resulting distance that the owl had to fly from the perch
to the speaker (Table 1).
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The signals consisted of 1–10 kHz broadband noise bursts with 10 ms
rise/fall time, either as a pulsed stimulus of 500 ms length and 500 ms silent
interval (initial stimulus), or as a single stimulus of 200 ms length
(in-flight stimulus). These auditory targets simulated prey location
(Konishi, 1973a;
Konishi, 1973b) and were
presented via loudspeakers (Visaton F8 SC, 80–15,000 Hz) with a flat
frequency spectrum (±5 dB) in the relevant range from 80 Hz to 15 kHz.
An array of five background speakers (Visaton F8 SC, Haan, Germany) in the
rear (`target') half of the free-flight room provided an equally distributed
noise (1–12 kHz) at 33 dB sound pressure level (SPL) as measured from
the position of the owl's perch. The target stimulus was attenuated to 10 dB
above the background masker amplitude for any of the 12 possible speaker
positions. Sound level was calibrated prior to experimentation for all speaker
positions using a sound level meter (Brüel and Kjaer, model 2236,
Brüel and Kjaer, Naerum, Denmark) with an accuracy of ±0.5 dB at
the position of the owl's head on the perch in the free-flight room.
A red laser beam (model OLSH 705P, 650 nm wavelength) was mounted above the
perch. When the owl was sitting on the perch, the laser beam was directed to
the back of its head and was thus prevented from hitting a receiver box below
the perch. As soon as the owl left the perch, the laser beam hit the receiver
box and triggered a latency counter (the time difference between stimulus
onset and the owl's take-off for target striking). Latency was used as an
indicator for motivation during experiments, as latency is correlated with an
animal's arousal level and motivation
(Damos, 1991).
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Training
The owls learned the paradigms within 15–20 days by operant
conditioning. In the early training phase, a piece of meat was placed in the
illuminated room on top of one of the target loudspeakers during isochronous
emission of ongoing broadband noise from the target speaker. Once the owls
associated the auditory stimulus with the food reward, the illumination was
reduced until the owl struck the target speaker in complete darkness (no light
detectable with a luminescence meter). The owls remained on the floor after
landing. Turning on a pale white light diode (LED) mounted above the perch
triggered the return flight. In the following trials, food was provided only
after the owl flew back to the perch. During later experiments, the owl
received a small piece of chicken meat as reward for successful task
accomplishment (i.e. the owl flew in the direction of the target speaker,
waited for the LED to turn on, then returned to the perch) before the next
trial was initiated.
Procedure
The task required that the owl should localize the initial stimulus emitted
from one of four target speakers at variable distances to the perch. The
distance from the speaker devices to the perch was varied only between daily
experimental sessions, and not within a session. The average flight duration
for the most distant speaker device position (3.35 m) was determined in
preliminary experiments and confirmed in the actual experiments to be about
1300 ms. After the owl left the perch to strike the target, the in-flight
stimulus was introduced with a variable delay of 300, 500, 700, 900, 1000,
1100 or 1200 ms. Stimulus delays were randomized within a daily experimental
session.
Either LS 2 or LS 3 emitted the initial stimulus (Fig. 1, Fig. 2J). The active speakers were chosen in random order. The in-flight stimulus appeared from any of the four loudspeakers, also chosen on a random basis. This resulted in eight different stimulus sequences, which ensured that the owl could not predict whether the in-flight stimulus would arise left or right from the direction of the initial stimulus. In the following, the stimulus regime (speaker sequence) is noted by separating the location of the initial stimulus from the location of the in-flight stimulus by a hyphen (e.g. LS 2-3).
Although three different loudspeaker device positions were used during experiments to prevent the owls from memorizing speaker positions, it is mainly the flights to the position with maximum distance (3.35 m) from the perch that are taken into account in the present study. This particular distance was chosen because it provided a longer flight time and thus a maximum of testable delays. Each speaker sequence was tested in at least 10 trials per delay. At 1100 and 1200 ms delays the owls did not perform any correction turn in initial trials. These delays were not tested further in the course of the experimental series.
Data analysis
The timing device measuring the in-flight stimulus delay started with the
activation of the laser trigger caused by the owl's take-off. Head turn
latency after the onset of the in-flight stimulus was defined as the period
between the onset of the in-flight stimulus (the first video frame in which
the laser beam was no longer visible on the back of the owl's head) and the
first video frame in which the owl had started to turn its head in the
direction of the in-flight target speaker. For the analysis of head turn
latencies, the flight time between take-off and completion of the head turn
was determined with 40 ms accuracy, owing to the frame rate of the cameras
being 25 Hz. The in-flight stimulus delay, however, was provided with an
accuracy of about 1 ms. The delay was subtracted from the flight time
calculated from the video recordings. Hence, if the flight time was, for
example, 800 ms, and the in-flight stimulus was provided with 700 ms delay,
the head turn latency was determined to be 100 ms. Therefore, the head turn
latency could be determined with higher accuracy (±20 ms) from the
video recordings.
The head turn could be observed best on the video recordings from a frontal or sideward perspective (cameras C1 and C2; Fig. 1; Movie 1 in the supplementary material), as a sudden change of the owl's eyes and beak position (Fig. 2D,E), followed by a change of the body position into the direction of the in-flight target (the correction turn). Only the video recordings from C1 and C2 captured the flight from take-off until the last phase of the flight. Some of these video recordings captured the stretching out of the owl's feet immediately before landing. An exemplary flight path from owl W, seen from the frontal camera's (C1) perspective, is shown in Fig. 2A–H (see also Movie 1 in the supplementary material). The image sequence shows the head turn movement during a flight where LS 2 emitted the initial stimulus and the in-flight stimulus came from LS 3 with 700 ms delay.
In contrast to head turn latencies, the angles of the head and body turns
were calculated based on the video recordings that showed the last few hundred
milliseconds of the owl's flight path from above the speaker devices (camera
C3, Fig. 1; see Movie 2 in the
supplementary material). For this purpose, the images of a flight sequence
were overlaid and the position of the head tracker was analyzed, i.e. the
direction of the flight trajectory before and after the owl performed a
correction turn. In the overlaid images recorded from camera C3, the
discontinuity (bending) of the line formed by the head tracker reflections
(light dots, Fig. 2I) reflects
the change of the owl's trajectory. Another example of this bending is given
in Fig. 2J. In this particular
trial, LS 3 emitted the initial stimulus and LS 1 provided the in-flight
stimulus with a delay of 900 ms. After the in-flight stimulus, the owl
performed first a head turn, with a latency of 200 ms, towards the novel
speaker. This head turn was succeeded by a turn of the body resulting in a
curvature of the flight path. The line through the last three reflections of
the head tracker prior to the characteristic bending of the trajectory (cf.
Fig. 2J, white arrow) was
defined as the initial flight direction. The initial flight direction in the
sample flight is indicated by the first three white dots at the top of
Fig. 2J. The altered flight
direction, defined by the line through the first three reflections of the head
tracker after the sharp bending, differed from the original flight direction
by 16 deg. (angle 
, Fig.
2J). Angle , measured between the lines through initial and
altered flight direction, is referred to as the turning angle. Although the
flight path was occasionally curved in the last part of the flight (see
Fig. 2J), we analyzed only the
initial curvature (white arrow) because there was only one prominent head turn
(as in Fig. 2D,E) visible in
the recordings from camera C1. A remaining angle (β) of 15 deg. would
have been necessary in order to hit the center of the target speaker, which
was defined as the error angle (Fig.
2J).
The turn of the head was clearly visible from the frontal camera perspective (cf. Fig. 2D,E) and allowed the determination of head turn latencies. By contrast, the trace of head tracker reflections in the top view results from both the head turn and the following change of trajectory, which incorporates a body turn. Consequently, head and body turns were segregated for the calculation of head turn latencies, but not for the calculation of turning angles. For some target positions, the owl flew out of sight during the actual landing, which did not influence the analysis of the head turning latencies but which did prevent calculation of the total flight time in most trials. It is not likely that further head turns occurred during this very last flight phase, as no further prominent bending of the flight trajectory (as visible in Fig. 2J, white arrow) was observed in the top view (camera C3) of the landing phase.
The percentage of trials in which correction turns occurred, calculated as the proportion of the absolute number of trials with differing initial and in-flight target speaker at the given stimulus delay, were analyzed for significant differences between two in-flight stimulus delays or between two owls at the same stimulus delays using Fisher's Exact Test (two-tailed, 95% confidence interval). Whenever two sample groups, like turning latencies, were equally distributed (as indicated by a Kolmogorov-Smirnov normality test), a two-tailed t-test (95% confidence interval) served to test for significant differences between them. A Mann–Whitney test (two-tailed) was used if the data samples were not evenly distributed, and a one-sample t-test (95% confidence interval) if only one data sample was available in one of the two sample groups.
For analysis of the landing precision, the distance (in cm) from the
landing position to the target loudspeaker was calculated from the x-
and y-coordinates (horizontal and vertical deviation) that the
DynaSight tracking system recorded. The x- and y-coordinates
were transformed into a scalar distance by unit vector conversion:
 | (1) |
To test whether the landing positions were evenly distributed around the center of the target speaker, a modified [by Fasano and Franceschini (Fasano and Franceschini, 1987)] KS2D1S test (Kolmogorov–Smirnov two-dimensional distributions and one sample) was used, and a two-sample KS2D2S test (Kolmogorov–Smirnov, two dimensions, two samples) for comparison of two different samples.
With the help of Kuiper's test, it was possible to calculate whether the angles were equally distributed, and to find out whether significant differences occurred between the angle distributions of two owls at one parameter, or between the data of one owl at two stimulus parameters.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The owls pointed their heads into the direction of the initial stimulus while sitting on the perch. After a mean pre-flight latency, i.e. the time span between stimulus onset and take-off, of 10–17 s, they left the perch to strike the target. If the initial and the in-flight stimuli were not emitted by the same speaker, the owl turned its head and body towards the novel target speaker in a certain percentage of trials depending on the in-flight stimulus delay.
Pre-flight latencies were assumed to be indicative of the owl's motivation,
which might influence its performance. The distribution of the pre-flight
latencies was, therefore, tested for significant differences between trials
with and without correction turns, or between the three owls. The latencies
were not normally distributed and varied within a daily session; the standard
deviation was in the range of the overall mean latency. Owl H responded
significantly (P
0.009) faster in trials with correction turns
(latency 10.52±7.94 s, mean ± s.d.) than in those without
correction turns (13.08±10.31 s). For owl W (with turns,
17.41±11.79 s; without turns, 16.63±11.92 s) and owl Q (with
turns, 16.69±11.91 s; without turns, 16.83±11.91 s), this was
not the case. In summary, variation within a session with a particular owl was
larger than differences between the owls. This was also the case for most
other parameters studied. Therefore, the data for the three birds were pooled
for most of the following analyses.
We used the turning of the owl's head in the direction of the target speaker as an indicator for a correction turn, as it always preceded a change of the owl's trajectory (see Materials and methods). In order to quantify the adaptive change of the flight path, we analyzed the percentage of trials in which the owl performed a correction turn, as well as the head turn latencies and the angular extent of the change in the trajectory. Trials in which the owls flew out of the camera's sight, left the perch prior to stimulation, or showed signs of irritation due to disturbing noises from outside the experimental chamber were excluded from the analysis. In total, we were able to analyze 1936 valid trials. One trial for owl W (with a correction turn) was captured in the video recordings, but was not tracked by the DynaSight system. This trial was included in the analysis of head turn latencies, but not in the analysis of landing precision.
Correction turns and hit rates
The effect of displaced target locations was compared with the situation in
which the target position remained constant. We used the loudspeaker sequences
LS 2-2 and LS 3-3 as a control for the owl's striking precision for in-flight
stimulation that did not require correction (483 trials). Under these control
conditions none of the owls performed a head turn. Here, the owls landed with
mean distances of 21.29 cm (owl W, 152 trials), 22.19 cm (owl Q, 168 trials)
and 25.20 cm (owl H, 163 trials) to the center of the target speaker. No
significant differences were found for varying stimulus delays. Hence, when no
correction turn was required, the owls achieved a mean landing precision of
around 20 cm, which can be considered as a `baseline' for striking accuracy in
the present paradigm.
In 634 out of 1453 trials (rate of correction turns: 43.63%; owl W, 60.47%;
owl Q, 42.95%; owl H, 28.51%) where the in-flight target speaker differed from
the initial speaker, the owls performed a correction turn. The relationship
between in-flight stimulus delay and the rate of correction turns can be
described by a sigmoid-like curve (Fig.
3A). The shape of the curves did not depend on whether initial and
in-flight target speakers were separated by a distance of 50 cm or 100 cm
(data not shown). The rate of correction turns was about 40–80% for
in-flight delays up to 700 ms, and decreased almost linearly with longer
in-flight stimulus delays down to 0% at an in-flight stimulus delay of
1000–1100 ms. The decrease in percentage became significant (Fisher's
Exact test, P0.05) at an in-flight delay of 800 ms for owl H and
of 900 ms for the other two owls (dotted lines,
Fig. 3A). Owl H performed
significantly (P0.01) fewer correction turns than owl W for any
in-flight stimulus delay below 1100 ms
(Fig. 3A).
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Trials using shorter distances (2.85 m and 2.35 m) between perch and the speaker device (cf. Fig. 1) were introduced in 10–20% of the experimental sessions (Fig. 3C). The percentage of correction turns correlated with the in-flight stimulus delay in a similar way to in trials using the largest perch-to-speakers distance (3.35 m), in that the owls achieved a relatively high percentage at short in-flight delays that dropped down to 0% at longer delays. However, the resulting curves were shifted to the left (compare Fig. 3C with Fig. 3A), indicating that the owls failed to correct their flight path at shorter in-flight stimulus delays. For example, the decrease in the percentage of correction turns started already at 500 ms in owls W and H. The differences between the owls were not significant, but this analysis was based on only a small number of trials (owl W, N=59; owl H, N=76; owl Q, N=80).
Although the three owls differed slightly from one another at some stimulus delays, the general tendency in all owls was a decrease of hit rates for longer in-flight stimulus delays. This emphasizes that the adaptation of flight direction is restricted in the last part of the target approach. The later a change of the target position occurred, the harder it was for the owl to react properly.
Head turn latencies
Head-turn latencies were only determined for those trials that included
correction turns. If the video sequence of a trial included the correction
turn but failed to capture the take-off moment, this trial was excluded from
the analysis of head-turn latencies. Such trials were nevertheless valid for
the analysis of the percentage of correction turns performed, as well as for
the analysis of the landing precision. In total, 249 out of 286 turns were
analyzed to determine the head-turn latencies for owl W, 197 out of 204 turns
for owl Q and 137 out of 144 turns for owl H. The minimum head turn latency
ever observed for all owls was 60 ms; the maximum was 360 ms for owl W, 340 ms
for owl Q and 500 ms for owl H. The median latency was 180 ms averaged over
all turns of each owl (Fig.
4A). Significant differences between owls or stimulus delays were
not detected.
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0.001) smaller in
trials with a shorter distance between the initial and the in-flight target
speaker, i.e. 50 cm vs 100 cm
(Fig. 4B). Likewise, latencies
significantly decreased with increasing stimulus delay for each owl (linear
regression, P0.0307; goodness of fit,
r2=0.7280 to 0.9524), as well as for the pooled owls
(Fig. 4C, P0.0070,
r2=0.8661; slope, –0.14930±0.02935).
Head-turn latencies were significantly correlated with landing precision
(Pearson correlation test, P0.001), measured as deviation in
centimeters from the target loudspeaker, meaning that shorter head-turn
latencies typically caused more precise landings
(Fig. 4D). Head turn latencies
directly relate to the remaining flight time. The shorter the head turn
latency, the more time is left for the owl to perform a correction turn. This
explains the correlation between short latencies and higher landing precision.
In addition to head turn latencies there are further parameters that,
likewise, can influence the owl's landing precision after a correction turn;
for example, the extent of the head turn (the turning angle) and the following
change of trajectory.
Turning angles
If the owl performed a correction turn towards the target speaker in order
to strike it, the angle of the turn should be larger for long in-flight
stimulus delays than for short delays. This situation is demonstrated in
Fig. 5 for a short and a long
in-flight stimulus delay. It was assumed that the time needed to process the
stimulus and the time needed for the generation of the motor reaction (the
head and body turn) remained constant irrespective of the stimulus delay. For
the same reason, with increasing distance between the initial and the
in-flight target, the turning angle was supposed to be larger. This hypothesis
was tested by comparing the turning angle of each owl after different stimulus
delays, as well as following trials with a distance of 50 cm and a distance of
100 cm between the initial and the in-flight target speaker, respectively.
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,
could be determined best using the video recordings of the camera mounted at
the ceiling (C3 in Fig. 1),
which showed the flight trajectory directly from above; however, this camera
covered only the last 500–600 ms of the flight. Therefore, the turning
angle was measured only for stimulus delays between 700 (if the moment of the
head turn was captured in the video recording) and 1000 ms. Some recordings
were excluded from the analysis because the head tracker was not continuously
visible, predominantly because the owl bent its head, so that the reflection
of the tracker disappeared. A total of 90 trials were analyzed for owl W, 45
trials for owl Q and 28 trials for owl H.
The turning angles increased significantly with increasing stimulus delay
(Fig. 6A; Spearman correlation
test, P0.0018). The linear regression (black line,
Fig. 6A) was significantly
non-zero (P0.0001) and had a slope of 0.03691±0.009410
(goodness of fit, r2=0.09250). The turning angles for
speaker sequences with a distance of 100 cm between the initial and the
in-flight target were significantly larger than for sequences with a distance
of 50 cm between speakers (Fig.
6B) in all owls. Hence, the owl adapted the change of its
trajectory to both the stimulus delay and the speaker distance, as would be
expected (cf. Fig. 5). It was
of further interest whether these adaptive changes had an impact on the
accuracy of target strike, i.e. the landing precision.
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0.001), neither in tests of the speaker sequences,
nor for delays or individual owls. The angles (theta, 
) exhibited a
two-peaked distribution for trials without a correction turn, which resulted
from pooling speaker sequences where the in-flight target speaker lay left (LS
2-1, 3-2 and 3-1) or right (LS 2-3, 3-4 and 2-4) of the initially aimed
speaker. One peak lay between 75 and 135 deg. and a second peak of similar
height between 195 and 255 deg. (Fig.
7B). This implies that all three owls landed short of the target
in most of the trials. In trials with a correction turn the angles were widely
spread (Fig. 7C). Within the
no-turn trials, the landing distances (rho, 
) were concentrated between
35 and 115 cm from the target. (Fig.
7D). By contrast, in trials with correction turns, the
distribution of the landing distances was asymmetric, with most lying between
5 and 35 cm off the target (Fig.
7E). The median distance in trials without a correction turn was
61.96 to 62.93 cm for the three owls. In trials with correction turns, the
median distance was 21.52 to 30.03 cm, comparable to the landing precision in
control trials. The distribution of both distance towards the target speaker
(KS2D2S test) and angles (Kuiper's test) of the landing positions differed
between trials with and without a correction turn
(Table 2A), as well as between
the three owls (Table 2B).
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Landing precision was thought to be of great importance, as it influences
the amount of prey the owl can catch in a natural environment. The landing
precision hardly varied as a function of the in-flight stimulus delay, so
these trials were pooled for further analysis for each owl. All three owls
were significantly (P0.001) more precise when they had performed
a correction turn, than in trials without a correction turn
(Fig. 8). The landing precision
of the owls was also dependent on the speaker sequence. In the speaker
sequences LS 2-1, LS 2-3, LS 3-2 and LS 3-4, the distance between initial and
in-flight target speaker was 50 cm, whereas in LS 2-4 and 3-1 both speakers
were separated by 100 cm. Supposedly, the owls might land more precisely if
the speakers were adjacent to each other, compared with double the distance.
The mean precision was higher (P0.001) for speaker sequences with
adjacent speakers than for those with a distance of 100 cm between the
speakers (Fig. 8). It was,
however, not correlated with the turning angle (Pearson correlation test,
two-tailed, 95% confidence interval).
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Error angles ranged from 0–39 deg., with a mean of 12.78 deg., for
the 50 cm distance, and from 0–42 deg., with a mean of 20.14 deg., for
the 100 cm distance. They were larger for the 100 cm distance than for the 50
cm distance between the target speakers at any delay
(Fig. 9A), without any
significant difference between the owls. The only exception was owl Q, which
had a significantly (P0.0247) larger error angle at a 700 ms
delay and a 100 cm distance than did the other owls. The difference between
the 50 and 100 cm distance between target speakers was highly significant
(P0.0003) when the angles were pooled over all owls and delays
(Fig. 9B). The error angles of
each owl were analyzed for correlation with the landing precision for the
varying stimulus delays (700–1000 ms), and for the two distances between
the target speakers, respectively. Each of these groups contained between one
and 21 samples. In five cases with a sample number of less than three, no
correlation test could be performed. The landing precision was typically not
correlated with error angles within a stimulus delay and target speaker
distance. By contrast, the correlation was highly significant if the delays
and speaker distances were pooled (Pearson correlation test,
P0.0015), meaning that the landing precision was lower, the
larger the error angle was. The rate of early landing (i.e. the proportion of
trials with undershooting or landing at angles between 90 and 270 deg.,
Fig. 7) in control flights with
identical initial and in-flight targets (72.09%) matched that of early landing
in trials where in-flight correction was required because the initial and the
in-flight target speaker were not identical (75.09%). Conclusively, the owls
exhibited vertical striking errors in control trials, as well as in trials
that required in-flight correction. Both findings support option two (see
above), that the owl's decreased landing precision in in-flight correction
trials was due to additional angular errors (compared with control trials),
whereas distance errors occurred in both control and in-flight correction
trials and caused an undershooting of the target speaker in any case.
|
In conclusion, a correction turn at short head turn latencies – leaving more time for corrective movements – led to higher striking precision. Hence, if the owl performed a correction turn, landing precision was comparable to that in control trials, but the percentage of trials in which the owl performed a corrective turn decreased with increasing stimulus delay. Therefore, the mean striking precision averaged over all trials at a given delay decreased likewise with increasing stimulus delay. The time needed for in-flight corrections limited striking accuracy when the change in target position fell within the range of the final landing phase. The owl achieved high striking accuracy only if the extent of corrective turning angles matched the altered target position. This was the case as the turning angle increased with increasing stimulus delay, as well as with increasing distance between initial and in-flight targets (cf. Fig. 6).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Correction turns
In our experiments, we investigated the flight behavior and landing
precision of barn owls reacting to in-flight broadband sound stimuli at
variable delays. For short in-flight delays the owls adapted their flight path
to the new target in a certain percentage of trials. This adaptation rate was
independent of the in-flight delay and served as a baseline. Above a certain
threshold (defined as the in-flight stimulus delay at which the percentage of
correction turns decreased for the first time significantly compared with the
previous delay, cf. Fig. 3A)
this rate decreased gradually with increasing in-flight stimulus delays. With
an overall flight time of approximately 1300 to 1500 ms, the threshold was 800
ms. The shortest in-flight stimulus delay that elicited no in-flight
corrections by the owls was found to be between 1000 and 1100 ms. Thus, if the
in-flight stimulus appeared before around 50% of the flight time was over (700
ms out of 1300–1500 ms), the number of correction turns was high and was
not influenced by the timing of the in-flight stimulus. By contrast, if the
in-flight stimulus was broadcast after about 80% of the total flight time
(1100 ms out of 1300–1500 ms), a correction turn was not elicited at
all. Our study was similar to a previous study conducted by Konishi
(Konishi, 1973b). The target
stimuli he used disappeared at the owl's take-off and reappeared, after
varying delays, for the remaining flight time at a different location. Under
these conditions, the owl was able to strike the target as precisely as with
ongoing stimulation until the delay exceeded about 80% of the total flight
time.
These observations are comparable to our results. Taking the above
mentioned total flight time into account, the owls essentially needed a
remaining flight time of some 200–500 ms after stimulus onset to make a
correction turn. This measured remaining flight time fits well to the measured
head-turn delays (60–500 ms). As the flight time depends on the flight
distance, a decrease in flight distance was assumed to result in a decrease of
the threshold time necessary for correction turns. Such a dependency was
indeed observed (Fig. 3C). At a
flight velocity of 3.6 to 4.0 m s–1
(Konishi, 1973b), a decrease
in the distance to the target of 1 m should result in a time shift of about
250 ms, which is close to the observed 200 ms. In the present experiments,
flight velocity lay in a comparable range (about 2.6 to 3.0 m
s–1 if the linear distance to the target speaker was divided
by the approximate flight time of the owl). The data suggest that the owl's
attack flight might be divided in two parts, a first part during which the owl
can react to changes in target position, and a second part during which the
owl prepares for target striking and does not react to further changes in
target position. Potentially, there is a phase during late flight prior to
initiation of the landing where the owl reacts faster to displaced stimulus
locations, as suggested by the decreasing head turn latencies during late
flight (Fig. 4C).
If the stimulus delay was the only relevant parameter for in-flight correction turns, the baseline of performed correction turns should have been at 100%. However, the overall maximum baseline observed in our study was 80%, which was for owl W; it was even lower for owls Q (60%) and H (40%). We speculate that general arousal or attentiveness, which also seemed to differ between the individual owls, was responsible for this. As shown in Fig. 3, the absolute performance level (percentage of correction turns and hits) of owl W exceeded those of owls Q and H, and owl Q generally outperformed owl H. Besides differences in the absolute performance level, the threshold delay for correction turns lay in a comparable range for all owls (800–900 ms). These results suggest that individual owls are subject to comparable sensory and motor restrictions that limit the maximum stimulus delay for in-flight corrections. However, the percentage of trials during which the owl is attentive enough to react to an in-flight stimulus might, at least partially, be influenced by the owl's individual arousal.
Latencies for head turns
The flight time required to initiate a head turn varied between 60 and 500
ms, with a median latency of 180 ms. These data were in accordance with
previous results from stationary sound-localization experiments
(Knudsen et al., 1979;
Wagner, 1993). Head turn
latencies depended on the in-flight stimulus delay and on the distance between
the speakers. In trials with short stimulus delays, the owl may have turned
the head slowly because the turning angle was smaller
(du Lac and Knudsen, 1990), as
shown in Fig. 6A. This
speculation is consistent with the finding that head turn latencies were
smaller for the 50 cm speaker distance than for the 100 cm distance for all
owls (cf. Fig. 4B), as the
turning angle was smaller for adjacent than for distant target speakers
(Fig. 6B). The latencies are
also indicative of the sensory and motor capacities, which are similarly
restricted in individual owls. They were not expected to decrease with
increasing stimulus delay or decreasing distance between target speakers, but
the owls might react faster to in-flight stimuli in the late flight phase,
prior to initiation of the target strike. The relatively large variability of
head turn latencies suggests that these might be influenced by factors other
than pure reaction time, such as by arousal or attentiveness.
Turning angles and landing precision
Striking a target with equal precision requires a minimum turning angle,
which increases with increasing stimulus delays
(Fig. 5). Our data matched this
explanation, in that striking precision was independent of stimulus delay. A
similar situation is given when the distance between the initial and the
in-flight target increases from 50 to 100 cm. In this case, the turning angles
for the 100 cm distance were larger than those measured for 50 cm distance
(Fig. 6B). The increase in
turning angle, however, was not large enough, therefore the error angle also
increased (Fig. 9B). Hence,
barn owls can react to changing target positions to an extent that is
subjected to larger errors if the target is farther displaced.
Two factors mainly influence the landing precision, namely the turning
angle or the error angle, and the distance that the owl flew in the direction
of the in-flight target before landing. The landing precision was correlated
with the error angle, suggesting that striking precision mainly depends on the
angular error. This is further supported by the observation that the landing
precision in trials with a correction turn lay in a range comparable to that
of control trials (cf. Fig. 7).
Hence, undershooting occurred irrespective of whether the sound source was
stationary or moving. A general undershooting in the localization behavior of
barn owls was also reported in stationary experiments
(Poganiatz et al., 2001).
Stationary or translating human observers who had to approach a stationary
sound source, which emitted a 20 Hz pulse train, overshot near targets (2 m
distance) and undershot distant targets (4 m distance)
(Speigle and Loomis, 1993).
Apparently, misestimating the sound source distance is not limited to barn
owls. For the owl, it might be more beneficial to land short of the target
instead of overshooting it, as this provides the opportunity to swoop again on
the prey with no need for large-amplitude turns.
The switching between loudspeakers in our setup corresponds to sidewise
motion of a target. Shifferman and Eilam reported an inability or at least
severe impairment of tested owls to strike a target as it was moved sideways
(or backwards), compared with a forward or forward/diagonal motion
(Shifferman and Eilam, 2004).
This held true even though the target, a dead mouse or chick, was pulled by a
string and allowed both ongoing visual and auditory feedback. Our data suggest
that this holds true if the sideways motion occurs late during an attack
flight, as short in-flight stimulus delays correspond to a forward/diagonal
rather than a sideways target motion. This is also corroborated by Konishi's
observations (Konishi, 1973b).
He reported that barn owls were able to strike a distant target as precisely
as with ongoing noise stimulation if only three bursts of 50 ms duration each
were presented during a flight time similar to the one used in the present
study (i.e. about 1200–1400 ms). The noise bursts in his experiments
were evenly distributed during the flight time. If, in darkness, the owl did
not receive further feedback during the following 1000 ms of flight time, the
striking precision decreased dramatically
(Konishi, 1973b). We found
this to be consistent with our data, because the precision was clearly reduced
if the owl did not perform a correction turn
(Fig. 7). Interestingly, the
time span of 1000 ms seems to be shorter than the maximum temporal extent of
the spatial working memory (0.1–2 s), as tested by Knudsen and Knudsen
(Knudsen and Knudsen, 1996).
Konishi's as much as our data suggest that the owl requires (intermittent,
albeit possibly short) stimuli throughout most of its attack flight to
precisely hit a target in darkness. Apparently, the owl's striking precision
is influenced by the temporal pattern (inter-stimulus interval) of the
in-flight stimuli, rather than by the absolute stimulus duration.
Comparison with other species
In contrast to barn owls, mammals use interaural time differences (ITD) and
interaural level differences (ILD) for localization in the horizontal plane,
and spectral shapes for localization in the vertical plane
(Tollin and Yin, 2003).
Studies on sound localization during which animals had to fixate or approach a
sound source to indicate the perceived location have been conducted in several
species [cat (Casseday and Neff,
1973; Casseday and Neff,
1975; Jenkins and Merzenich,
1984; Populin and Yin,
2007); bat (Aytekin et al.,
2004); ferret (Kavanagh and
Kelly, 1987; Kavanagh and
Kelly, 1992; Parsons et al.,
1999); rat (Kavanagh and
Kelly, 1986); mouse (Ehret and
Dreyer, 1984); and seal (Bodson
et al., 2006)], whereas others have used conditioned reflexes
(Ebert et al., 2008). Most of
these species localize sound sources with similar or inferior accuracy when
compared with the barn owl, even though many similarities in localization
behavior can be found. For example, cats, as much as barn owls, orient their
heads towards broadband sound sources in comparable saccadic movements
(Beitel and Kaas, 1993). The
localization acuity in stationary two-choice experiments with cats is with
4–7 deg. somewhat inferior to in barn owls
(Heffner and Heffner, 1988),
although other measurements indicate a better performance, with localization
errors as small as 0.16±0.97 deg. (mean signed error ± s.d.) in
stationary experiments (Tollin et al.,
2005). Casseday and Neff carried out experiments in which the cat
had to approach the loudspeaker that emitted a sound
(Casseday and Neff, 1973). The
minimum detectable angle for pure tone localization was found in the range of
about 5–15 deg. for frequencies below 4 kHz; this strongly increased to
35 deg. at 4 kHz and then decreased again for higher frequencies.
Localization performance varies depending on the species-specific
requirements, but often is subjected to similar physical and physiological
restrictions. Jenkins (Jenkins and
Masterton, 1982; Jenkins and
Merzenich, 1984) demonstrated that midline localization was better
than peripheral localization, which can be explained by the higher spatial
resolution in the frontal field. Albino rats were tested in a similar
localization task, involving sound sources in the peripheral left and right
hemifield (±60 deg. from the midline)
(Kavanagh and Kelly, 1986).
The rats had minimum audible angles of about 12 deg. in the frontal field,
similar to those of the house mice (Ehret
and Dreyer, 1984), but performed poorly when the sound sources
were peripherally displaced.
The localization precision in other species is clearly inferior to what has
been observed in the barn owl, which can aim at a sound source with 2 deg.
accuracy, and detect changes of 3 deg. in its location
(Bala et al., 2003). The
ability of the barn owl to localize auditory targets with a higher accuracy
than most mammalian species is a consequence of the highly directional facial
ruff (Campenhausen and Wagner,
2006; Coles and Guppy,
1988; Knudsen and Konishi,
1979), which allows using interaural time and level differences
(ITD and ILD) for the localization of azimuth and elevation, independently.
Together with the ability to adapt its trajectory to a sound stimulus
appearing during flight, barn owls can strike a distant auditory target with
high accuracy without auditory feedback, even if these targets expose sudden
displacements.
However, natural conditions do not provide auditory feedback only. In fact,
visual feedback improves localization acuity. Populin and Yin demonstrated
that cats performed eye and head saccades to auditory targets with less
accuracy than to visual targets (Populin
and Yin, 2007). The cats in that study were impaired in their
localization accuracy when stimulated with single clicks instead of click
trains. This parallels what Konishi observed in the barn owl with 50 ms bursts
of sound (Konishi, 1973b). A
similar result was found for ferrets approaching a sound source: the ferrets
were significantly better at localizing noise bursts of 500 ms duration than
those of 40 ms duration (Parsons et al.,
1999). Bodson et al. have tested the sound-localization
performance of swimming seals (Bodson et
al., 2006). The animal had to swim towards the sound source and
touch the board of a half circle at the assumed position. The seals were
better at localizing continuous noise than two pulses of noise. Although the
last stimulus paradigm closely resembles our paradigm, to our best knowledge
no one has carried out experiments with freely moving animals in which the
sound source switched between loudspeakers in other animal species.
In nature, adaptive changes of the owl's behavior in response to altered
target positions are required for striking moving prey. In-flight stimuli
improve the barn owl's striking precision as long as they do not appear too
late in the target approaching behavior. We assume that flight maneuvers may
occur during early flight, but not in the final flight phase. In this respect
it is interesting that the prey, through its movements, typically provides
short intermittent auditory information to the predator. One of the avoidance
strategies of the prey is to freeze, i.e. not make any noise, and then jump to
the side and flee shortly before the owl attempts to capture it
(Edut and Eilam, 2004;
Ilany and Eilam, 2008).
Similar observations were made for peregrine falcons
(Howland, 1974). These birds
swoop at prey animals from the air at extremely high velocities. Prey animals
were able to escape with a high probability if they ceased fleeing at a
constant velocity and instead made a turn at an optimal time point, which was
defined by the maneuverability of the falcon. Starting the turn too soon
allowed for correction turns of the falcon, whereas turning too late did not
leave enough time for the prey's turn.
The data presented here show that barn owls succeed in striking
horizontally displaced targets under laboratory conditions by matching the
extent of the corrective movement to the target position. Nevertheless,
striking precision is dependent upon several physiological restrictions, such
as reaction time and localization accuracy. Taken together, barn owls are well
adapted to nocturnal hunting, even though potential prey animals may exploit
the mentioned restrictions in the owl's striking ability in order to escape
(Ilany and Eilam, 2008).
LIST OF ABBREVIATIONS
|
Footnotes |
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|
References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
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