The start of phonotactic walking in the fly Ormia ochracea: a kinematic study
1 Integrative Behaviour and Neuroscience Group, Department of Life Sciences,
University of Toronto at Scarborough, 1265 Military Trail, Scarborough,
Ontario, Canada M1C 1A4
2 Neurobiology and Behavior, Cornell University, Ithaca, NY 14853,
USA
* Author for correspondence (e-mail: amason{at}utsc.utoronto.ca)
Accepted 12 October 2005
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Summary |
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Key words: Ormia, phonotaxis, kinematics, sound localisation
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Introduction |
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Ormia ochracea (Diptera: Tachinidae) are acoustic parasitoid
flies. Adults are free-living, but their larvae develop as internal parasites
of crickets. Female Ormia locate their cricket hosts by phonotaxis to
the male calling song using an auditory system that functions solely in this
context. Females first fly towards cricket song, then land and walk in
preparation for larviposition as they near the source of the stimulus
(Cade, 1975; Walker, 1983).
Unlike intraspecific acoustic communication systems, in which the sensory
system and the signals co-evolve to optimize the transfer of information
(Bradbury and Vehrencamp,
1998
), acoustic parasites must adapt to the characteristics of
pre-existing host signals. Remarkably, the flies can localize the 5 kHz tone
pulses (wavelength=6.9 cm) produced by crickets, using a pair of ears
separated by less than 500 µm (Edgecomb
et al., 1995
). Flies reliably orient towards sound sources
broadcasting the calls of host species despite the fact that their small size
severely constrains the physical cues available to them for determining the
direction of sound propagation (Robert and
Hoy, 1998
).
This auditory directional sensitivity is derived from mechanical coupling
of the two tympani, which provides sensitivity to tiny interaural
time-differences arising from the minute separation of the two ears (Robert et
al., 1996,
1998
;
Miles et al., 1995
). Previous
work has shown that this tympanal mechanism is combined with specializations
of auditory receptors to provide exquisite sensitivity to sound direction
(Mason et al., 2001
; Oshinsky
and Hoy, 2002). These adaptations allow female Ormia to localize an
appropriate sound source to within 2° of azimuth
(Mason et al., 2001
).
A thorough analysis of behavioural responses to directional acoustic cues
is required in order to determine the relationship between physical acoustic
cues, mechanical cues (at the tympanal level), and neural coding of sound
direction. Previous behavioural analyses have focused on both flying
(Mueller and Robert, 2001) and
walking (Mason et al., 2001
)
acoustic responses. However, the kinematics of walking phonotaxis in Ormia
ochracea has not been described in detail. Here we compare the initial
stages of phonotactic responses in flies tethered on a spherical treadmill
with those of freely walking flies. We analyse the responses of flies to a
single stimulus presentation, during which they reorient to the direction of
the sound source. We describe the dynamic features of these responses with a
view to identifying how the flies modify their walking patterns to achieve
appropriately oriented responses.
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Materials and methods |
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Acoustic stimuli
Acoustic stimuli were synthesized using Tucker-Davis Technologies (TDT,
Gainesville, FL, USA) hardware and custom software. Stimuli for behavioural
experiments consisted of a train of 5 kHz, 10 ms tone pulses with 1 ms
rise/fall times, delivered at a rate of 50 pulses s1 with 10
pulses/train for a total stimulus duration of 200 ms. Stimuli were amplified
(Harman Kardon PM655; Château du Loir, France, or NAD S300; London, UK),
passed through a computer-controlled attenuator (TDT PA4; Tokyo, Japan or PA5)
and broadcast from a speaker (Sony MDR-ED228LP or Radio Shack piezo horn
tweeter; Fort Worth, TX, USA). Stimulus timing and amplitude were controlled
by computer. Stimulus levels were calibrated with a probe microphone (B&K
Type 4182; Naerum, Denmark).
Behavioural recordings
We measured phonotactic walking responses with both freely walking (closed
loop) and tethered flies (open loop). Responses of freely walking flies were
recorded in two ways, using standard and high-speed video (see below).
Standard-speed video recordings were used to capture complete phonotactic
responses to single stimulus presentations from which we extracted trajectory
and velocity information for comparison with open loop recordings (tethered
flies, see below). High-speed recordings were used to obtain a detailed
description of the walking patterns flies displayed during phonotactic
responses.
High-speed recordings
We made high-speed video recordings at 1000 frames s1
(Redlake Motionscope HR2000; San Diego, CA, USA), using a macro lens (Nikon
Micro-Nikkor 55 mm; Tokyo, Japan) at a distance of 1 m. This provided a
viewable area of approximately 5 cm2 with a resolution of
240x210 pixels. The movement of individual limbs was clear and the
animal could walk 34 steps before moving out of the viewable area.
Variation in the sound field within the viewable area of the arena was
±2 dB.
We centred untethered flies on a platform between two speakers separated by 40 cm. A fibre optic ring light (5 cm diameter) placed 6.5 cm above the animal illuminated the immediate area around the fly. With the room lights turned off (trial conditions) the speaker locations were dark. The video camera was mounted above the ring-light. The arena centre and radial angles relative to the speakers were marked on a video monitor on which the flies were displayed during experiments. By placing the flies on a blank sheet of paper in the arena, we could rotate or position them to allow precise placement relative to the fixed speakers. In most cases, gravid females were quiescent in the absence of acoustic stimulation. Under these conditions, we could control the angle of the fly relative to the speakers to within 10°. Occasionally flies took flight immediately upon being placed in the arena. These individuals were not tested further.
In these experiments, we positioned flies with their body axis perpendicular to the direction of the speakers and randomly presented stimuli from either of the two speakers (i.e. right or left side of the arena). The direction in which flies were facing along this perpendicular axis was randomized between trials (i.e. front or back of the arena). We recorded details of limb and body movements during the initiation of phonotactic turns. These measurements were derived from frame-by-frame analysis of high-speed video recordings. We recorded responses to single presentations for speaker positions of 0° (straight ahead), 90° (perpendicular to midline axis) and 180° (directly behind).
Standard video recordings
Phonotactic responses were recorded with a video camera (Panasonic
WV-GP460; Matsushita Electric Industrial Co., Osaka, Japan) mounted above the
arena and VCR (Hitachi DA4; Tokyo, Japan). The analog video data were
digitized at 15 or 30 frames s1 using Adobe Premiere 6.0 and
Cinepak compression codec (Radius). Digitized video clips were imported into
motion analysis software (Midas 2.0, Xcitex; Cambridge, MA, USA) to extract
distance, velocity and direction of movement frame by frame. Setup and
stimulus presentation were similar to high speed recordings, except that flies
were 40 cm from the speakers.
Responses of tethered flies
We measured the responses of tethered flies on a spherical treadmill
(Mason et al., 2001) that
transduced the locomotor responses of flies fixed in position relative to the
sound source. Flies were attached to a wire with low-melting-point wax applied
to the dorsal surface of the thorax. Using a micromanipulator under red light,
we then placed mounted flies in a normal walking position on a spherical
treadmill consisting of an optically actuated computer pointing device
(Logitech Marble Mouse; Fremont, CA, USA) that was modified to hold a
lightweight (2.5 g) hollow plastic sphere floating on an air stream. A random
dot pattern on the sphere activated the optical sensor when the fly's walking
movements rotated the ball. The fly's virtual trajectory was recorded by
computer (40 Hz sampling rate), using custom software. The treadmill was
located at the centre of rotation of a speaker that was attached to a moveable
arm at a distance of 12 cm from the position of the fly. The speaker could be
rotated through 40° azimuth on either side of the midline axis of the fly
and positioned with an accuracy of 0.5°. An additional pair of fixed
speakers was located at ±90°. Stimulus levels were monitored during
experiments with a probe microphone (B&K Type 4182) positioned within 0.5
cm of the fly's tympani. The treadmill was calibrated by rotating the sphere
by a measured distance (1 cm) in the x- and y-axes
(representing lateral and forward/backward movements, respectively). Data were
captured as coordinates representing cumulative displacement in these two axes
relative to the position at stimulus onset. The spatial resolution of the
system was 0.1 mm. From these data we calculated the walking paths of flies in
equivalent real-world distances and directions. References below to locations
and distances during the course of open loop phonotactic responses are derived
from these virtual paths.
Data analysis
We recorded phonotactic responses from 19 flies on the treadmill. Flies did
not always continue to respond long enough to allow measurements at all
stimulus angles. Sample sizes for different datasets are given in figure
legends. At least 10 responses were recorded for each stimulus condition. Data
from repeated responses for individual flies were averaged and individual
averages pooled across flies. Unless otherwise indicated, data are presented
as means ± S.E.M. For comparisons of
different stimulus conditions, flies' angular headings were calculated in two
ways: (1) the overall response angle and (2) the instantaneous angular heading
(Fig. 1). (1) The overall
response angle was determined by calculating two lines, one determined by the
starting position of the fly and a point defined by the location of the fly at
the midpoint of the response (i.e. the position of the fly when it was half
way between its starting position and its final position at the end of the
response) and the other by a line following the midline axis of the fly before
stimulus presentation. This was taken as the overall orientation for that
response. (2) The instantaneous angular heading of the fly was calculated by
converting the location of the fly, relative to its starting point, to polar
coordinates at each time-step. We also calculated the instantaneous speed and
rotational velocity of flies over the course of phonotactic responses.
Statistical analyses were carried out using Matlab (version 6.5) and R
(version 1.9) software.
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Results |
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Fig. 3 shows a typical turn sequence in response to a 90° sound source. Flies did not show separate orientation and locomotion responses. Rather, turning and forward translation begin simultaneously such that the fly walks in a tight curve until it faces the sound source and then continues to walk in that direction. In this example, the initial movement in response to sound onset was a movement of the contralateral mesothoracic leg that occurred with very short latency (28 ms). The fly had turned through 25° and translated forward a full body length in only 84 ms, and was oriented to within 10° of the sound source within 142 ms.
|
Walking speed and distance
Phonotactic responses to the presentation of single stimuli were analysed
using standard video recordings (Fig.
4). In these recordings the sound source was located either
directly ahead of the fly (0°) or laterally (90° right). We calculated
the path, distance and walking speed of flies over a 500 ms interval from
stimulus onset. This was sufficient duration for the flies to reach their
final heading. Walking paths were very consistently oriented in the direction
of the speaker (Fig. 4A,B).
Flies accelerated over the duration of the stimulus and decelerated (usually
to a complete stop) following stimulus offset
(Fig. 4CF).
|
We also recorded the responses of flies for a range of stimulus levels (4296 dB SPL) and measured the total distance flies walked in response to a single stimulus presentation. Surprisingly, the total distance of phonotaxis did not increase monotonically with stimulus level. At low stimulus levels (<66 dB SPL), the distance of phonotaxis increased with increasing stimulus level. At higher stimulus levels, however, the distance walked by flies in response to a single stimulus chirp tended to decrease, such that flies showed strongest responses (in terms of distance travelled) for intermediate levels (approximately 70 dB SPL, Fig. 5).
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Tethered flies
Walking speed and distance
The treadmill sphere used to record tethered phonotaxis was relatively
massive (2.5 g) compared with the flies themselves (mean mass ±
S.D., 19.74±4.7 mg, N=10). Thus the
force required by flies to rotate the sphere was considerably greater than
that required to translate or rotate themselves and we expected some
differences in the dynamics of tethered phonotaxis relative to freely walking
conditions. Nevertheless, phonotactic responses recorded in tethered flies
were qualitatively similar to freely walking conditions in the following
characteristics. Flies typically responded with a short latency, oriented to
the source location (Fig.
6A,B), accelerated through the duration of the stimulus and then
decelerated following the end of the stimulus
(Fig. 6CF). Behavioural
latencies were 93±3.8 ms for tethered flies vs 49±3.7
ms for freely walking (mean ± S.E.M.).
But it should be noted that these two measures are not strictly comparable.
For freely walking flies, we measured latency to the initiation of walking
(i.e. first movement of any leg) with a resolution of 1 ms, whereas tethered
latencies are for approximately 0.1 mm displacement of the treadmill sphere
with a resolution of 25 ms. Flies covered a (virtual) distance of
1.39±0.08 cm in response to a single 200 ms chirp at 0° and
1.28±0.16 cm for a source at 90° (t=0.9691, d.f.=8.91,
P=0.358, Fig. 4C,D). There were no significant differences in walking speed among responses to
different angles (Fig. 4E,F;
see below for statistical comparisons). Peak walking speed was slower on the
treadmill, and since the time course of acceleration/deceleration during
stimulus presentation was similar in both conditions, this meant that tethered
flies covered shorter distances than freely walking flies during the duration
of the stimulus. Tethered flies tended to continue walking beyond the duration
of the stimulus-locked response, however, therefore the total distances walked
by tethered flies over the recording interval were similar to freely walking
flies at the same stimulus level (Figs
4B,E,
6B,E). There was a deceleration
after stimulus offset, but this was quite variable even among different
responses of the same fly. Although some individual responses demonstrated
that flies were capable of stopping on the treadmill with timing similar to
freely walking responses, in most cases tethered flies did not come to a stop
by the end of 0.5 s recording interval
(Fig. 6C,F).
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Orientation
The pattern of changes in angular heading as flies oriented to the
direction of the sound source was similar in freely walking and treadmill
responses (Fig. 7A,B). Flies
walked a curved path until oriented towards the speaker, and then continued in
that direction. The initial stages of this orientation were somewhat
compressed in treadmill responses, however, due to the slower walking speeds.
In addition, walking beyond the duration of the stimulus in treadmill
responses was less consistently oriented towards the sound source
(Fig. 7B).
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We calculated instantaneous rotational velocity from the derivative of angular heading (Fig. 7D). Rotational velocity increased rapidly at stimulus onset, but reached a peak and began to decrease before the end of the stimulus, such that flies usually reached their final heading before the end of the stimulus. This is surprising given that, as described above, the perceived directionality of the stimulus remains constant throughout its duration in these open-loop experiments.
We obtained several measures of the speed and orientation of phonotaxis for comparison of responses to different source azimuths. From the records of instantaneous rotational velocity (Fig. 7D) we extracted two measures: peak rotational velocity and average rotational velocity (measured over the stimulus duration) (Fig. 8A). We also measured the angular variance in the overall orientation of responses (Fig. 8B), the peak walking velocity attained during the response (Fig. 8C), and the latencies to both peak walking velocity and peak rotational velocity (Fig. 8D). For statistical tests, we compared responses for three angles (0°, 10° and 20°) spanning a range over which turn angles varied with source azimuth but did not saturate (see below). For these analyses, responses for left- and rightward angles of the same magnitude were pooled.
Rotational velocity (both peak and average) varied systematically and significantly with source azimuth for angles near the midline, but this pattern saturated at larger angles (average rotational velocity: one-way ANOVA, F2,18=17.26, P<0.0001, peak rotational velocity: F2,18=4.94, P<0.02, Fig. 8A). The variability of phonotactic orientation showed a similar dependence on source azimuth (Rao's test for equality of dispersions, SR=14.71, d.f.=6, P=0.022). Angular variance increased with source azimuth for angles near the midline, but declined at larger angles (Fig. 8B). This decline in angular variance reflects a truncation of the distribution of response angles as the flies' turning response saturated at large angles. Walking velocity was highly variable and a comparison of 0°, 10° and 20° showed no significant difference (one-way ANOVA, F2,18=0.49, P=0.62, Fig. 7C). Neither latency to peak walking velocity nor latency to peak rotational velocity varied significantly with source azimuth (latency to peak rotation: one way ANOVA, F2,18=0.52, P=0.60, latency to peak velocity: F2,18=0.13, P=0.88, Fig. 8D).
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Discussion |
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There were some differences between freely walking and tethered (treadmill) phonotaxis. Peak walking velocity is lower in tethered phonotaxis, consistent with the excess inertia of the treadmill sphere. Also, tethered flies tended to continue walking beyond stimulus offset (though with a marked deceleration), whereas freely walking flies tended to stop. It is unclear what causes the greater tendency for flies to continue walking on the treadmill. Two differences between freely walking and treadmill responses may account for this. (1) The greater inertia of the treadmill sphere (relative to the mass of the fly) may limit the flies' ability to stop its rotation. This seems unlikely because flies are able to impose rapid accelerations and directional changes on the treadmill sphere, and in some instances did bring it to a rapid stop. (2) The open-loop nature of the stimulus may amplify flies' locomotor responses. Under freely walking (closed loop) conditions, flies receive sensory feedback, signalling their orientation with respect to the stimulus location. On the treadmill, the initial directionality of the stimulus is maintained throughout the response (analogous to a moving target). This could delay or reduce the tendency of flies to decelerate as they approach the target direction.
We measured several dynamic features of phonotactic responses for a range
of sound source azimuths: two latency measures (latency to peak rotational
velocity, latency to peak walking velocity), two measures of rotational
velocity (peak instantaneous rotational velocity, average rotational velocity
from response onset to peak), and peak instantaneous walking velocity. Of
these, only rotational velocity showed systematic variation with sound source
azimuth. Furthermore, the relationship between rotational velocity and source
azimuth (Fig. 8A) closely
matched previous measurements of directionality in O. ochracea
walking phonotaxis both the overall orientation of phonotactic
responses and interaural latency differences (a measure of auditory
directionality) showed a pattern of response magnitude increasing with
stimulus angle but saturating at the largest angles
(Mason et al., 2001).
Previous analyses of phonotaxis in O. ochracea have examined
flying phonotaxis (Mueller and Robert,
2001). This earlier study did not systematically examine the
effects of source azimuth on responses, but used two source locations
approximately 6° on either side of the midline. A further difference is
that Mueller and Robert (2001
)
recorded free-flight responses in which flies were allowed to complete their
approach to the sound source. Our results are derived from tethered (open
loop) responses, or freely walking responses that correspond only to the onset
and initial orientation of the response for a wider range of source azimuths.
Nevertheless, some comparisons are justified.
In flying phonotaxis, three phases of the response were identified:
take-off, cruising and landing (Mueller and
Robert, 2001). Our results are most comparable to the take-off and
cruising phases. During the take-off phase, flies gain altitude and orient
towards the sound source. In the cruising phase, flies travel in the direction
of the source at a more or less constant altitude, and then make a spiral
descent in the landing phase. Similarly, our results for walking phonotaxis
show an initial orientation phase in which accelerating forward translation is
combined with accelerating rotation. This is followed by forward translation
in a consistent direction that is proportional to the location (azimuth) of
the sound source.
Mueller and Robert (2001)
also observed that when the acoustic stimulus is discontinued during a
phonotactic flight, flies are still able to complete their approach to the
sound source. The accuracy of approach to the speaker location under these
conditions decreases with earlier interruption of the stimulus. The authors
conclude that flies obtain, during the early phases of the response, a measure
of direction and distance to the sound source that they retain beyond the
duration of the stimulus. Walking phonotaxis appears to be more strictly gated
by the duration of the stimulus. This may simply result from the fact that a
pause in forward movement during flight would be much more costly than a pause
during walking and flies are therefore more committed to continued locomotion
during flight. Nevertheless, in walking phonotaxis flies do continue for
varying durations beyond the end of a stimulus particularly in
treadmill responses and maintain the directional heading they
establish during the stimulus (see Fig.
7C). If continued walking on the treadmill is due to inertial
effects, then the sphere would tend to continue rotating in the same direction
and consistent orientation of walking paths beyond the stimulus duration would
be an artefact. However, another feature of walking responses is consistent
with the possibility that flies obtain localisation information to be used
independently of an ongoing stimulus. As discussed above, only rotational
velocity varies systematically with source azimuth, and this parameter
determines the final directional heading. Flies do not, however, simply rotate
throughout the duration of the stimulus. Rather, rotational velocity peaks
midway through and decreases during the latter part of the acoustic stimulus,
so that flies have reached their final heading and stopped rotating at the end
of the stimulus (or shortly thereafter; Figs
7D,
8D). This contrasts with
translational velocity, which tends to accelerate throughout the stimulus and
decelerate following stimulus offset. These details suggest that flies obtain
directional information early in the stimulus. Possibly, walking interferes
with the accuracy of directional hearing and flies must derive most of their
directional information in the interval between detecting the stimulus and
beginning to walk. Furthermore, our results suggest a simple mechanism for
distance estimation by flies. For intermediate to high stimulus levels,
phonotactic walking distance declines with increased stimulus amplitude.
Assuming that crickets tend to call with similar amplitudes, stimulus level
should predict source proximity. Flies may therefore reduce the distance they
cover with each stimulus as they approach the source more closely. The weaker
responses at low stimulus levels may reflect a transition between sources at
greater distances that elicit flying phonotaxis and closer sources that elicit
walking phonotaxis.
Our results allow some inferences about the processing of localisation cues
by the flies' auditory system that can be tested with neurophysiological
measurements. First, flies derive a measure of the directionality (not simply
laterality) of a sound source. This is consistent with previous results
showing that flies discriminate source locations on the same side of the
midline that differ by only a small angle. In other words, the flies obtain a
graded signal of binaural disparity that encodes source azimuth. Second,
directionality of responses is determined by the rotational component of
phonotaxis. Flies don't run faster or longer, or turn longer for larger
angles, they simply turn faster. Therefore the rotational component of
phonotactic responses reflects the underlying binaural disparity cue that
encodes sound direction. The pattern of variation in rotational velocity with
source azimuth is strikingly similar to the pattern of interaural latency
difference in auditory receptors (a putative neural code for auditory
directionality; Mason et al.,
2001). This allows for more precise testing of candidate
directional codes in neural responses. Finally, these results also suggest
possible mechanisms for multiple stimulus characteristics to be encoded in the
sparse responses of auditory receptors
(Mason et al., 2001
; Oshinsky
and Hoy, 2002). Flies are sensitive to differences in stimulus amplitude
(Wagner, 1996
;
Ramsauer and Robert, 2000
).
Source azimuth could thus be encoded as interaural latency differences that
ultimately affect the rotational component of phonotactic responses. Stimulus
amplitude may be independently encoded by variation in response amplitude to
affect speed and/or duration of phonotactic responses.
Such a mechanism would not exclude the possibility of binaural differences
in response amplitude also playing a role in directional coding, as suggested
by Oshinsky and Hoy (2002), but this may be significant only for large angles.
Our analyses demonstrate that, even for the largest stimulus angles, flies
have oriented to the sound source azimuth within 300 ms and then continue to
walk with little meander (see also Mason et
al., 2001). For most of the phonotactic approach, therefore, flies
are maintaining a course with only a small error angle relative to the sound
source. Because of the physiology of Ormia auditory receptors
(phasic, sound-onset responses with intensity-dependent variation in spike
latency, but not in spike rate or number), interaural differences in response
amplitude are based on differential recruitment of receptors in the two ears.
Such direction-dependent differences in receptor recruitment are due to
amplitude differences in tympanal vibration
(Robert et al., 1996
) combined
with threshold variation among receptors (Oshinsky and Hoy, 2002). In other
words, interaural differences in response amplitude are due to differences in
the number of receptors in each ear that are stimulated above threshold, with
each receptor making an all-or-nothing contribution to response amplitude. In
contrast, interaural latency differences are derived from pooling
intensity-dependent variation in spike latencies of individual receptors
potentially a more fine-grained measure of acoustic directional cues.
Measurements of auditory directional responses have not been made for the
smallest angles of sound incidence that Ormia have been shown to
discriminate behaviourally. Physiological measurements of interaural latency
and amplitude differences at small source angles are required to test these
hypotheses.
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Acknowledgments |
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Footnotes |
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