Factors reducing the expected deflection in initial orientation in clock-shifted homing pigeons
Dipartimento di Etologia, Ecologia ed Evoluzione, Via Volta 6, I-56126 Pisa, Italy
* Author for correspondence (e-mail: annag{at}discau.unipi.it)
Accepted 11 November 2004
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Summary |
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Key words: homing pigeon, sun compass, anosmia, visual landmark, orientation
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Introduction |
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Several experiments in which the sun compass and the topographical
information were put into conflict, by releasing pigeons from familiar sites
after the manipulation of their internal clock, yielded variable results in
terms of the extent of the deviation in their initial orientation
(Bingman and Ioalè,
1989; Bonadonna et al.,
2000
; Füller et al.,
1983
; Gagliardo et al.,
1999
,
2001a
;
Holland et al., 2000
;
Luschi and Dall'Antonia,
1993
). These inconsistencies might be explained by two different
hypotheses. (1) The first hypothesis takes into account two distinct
strategies that may be used by the birds for orienting at familiar locations.
During previous homing flights from a certain location, a bird might memorise
different information relative to both the site and the homing route. For
example, the pigeons can learn the general feature of a location and its
compass bearing with respect to home, but can also learn several landmarks and
their geometrical relationship, so as to build a topographical representation
of the familiar site (and/or familiar area); or they can learn both. These
concepts have been discussed in detail by several authors and different
terminology is sometimes used (Chappell,
1997
; Holland,
2003
; Wallraff,
1991
; Wallraff et al.,
1999
). In the first strategy, the landmarks have to be used in
association with a compass bearing; this mechanism was named `mosaic map' by
Wallraff (1974
) and also more
recently by Holland (2003
),
and `point map' by Wallraff
(1991
). In the second
strategy, the landmarks are independent from the `map and compass' system and
are used for piloting (Holland,
2003
). Wallraff
(1991
) referred to the latter
mechanism as a `pattern map'. Recent experiments on hippocampal ablated
pigeons released at familiar sites support the existence of both strategies,
as the hippocampal lesions disrupt the ability to refer to a topographical
map, but leave intact the compass orientation (Gagliardo et al.,
1999
,
2002
). Other studies, in which
the homing routes of clock-shifted intact pigeons were tracked from familiar
sites, suggest that the release site might also determine which strategy is
used (Bonadonna et al., 2000
).
(2) The second hypothesis attributes the variable reduction of the deflection
due to the clock-shift treatment to the conflicting information given by the
sun and the magnetic compass (Chappell,
1997
; Wiltschko and Wiltschko,
2001
; Wiltschko et al.,
1994
).
In some of the papers cited above the orientation of clock-shifted anosmic
pigeons has been reported, and a tendency of the anosmic birds to deviate less
than the clock-shifted smelling controls can be observed. This suggests that
the use of the olfactory navigational map might bias the choice of the pigeons
towards the use of the `mosaic map and compass' strategy. As a possible
contribution in clarifying the role of the landscape and the sun compass for
orientation over familiar areas, we trained a large number of pigeons from
three familiar release sites located in different directions with respect to
home. We compared the initial orientation of a group of anosmic birds and a
group of intact (smelling) pigeons either in natural dark-light cycle or after
a fast clock-shift manipulation. Moreover, we also recorded the orientation of
the birds in the arena (Gagliardo et al.,
2001b; Mazzotto et al.,
1999
) with the aim of assessing whether, even before take-off,
they use the visual cues for piloting or within a `map and compass strategy',
as Holland (2003
) also
recently suggested.
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Materials and methods |
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During the training releases seven pigeons got lost. The remaining 103
birds were divided into two groups. 3 days before the first test they were
subjected to the following treatments: (Group 1) FA-pigeons (N=52),
birds familiar with the release sites, were made anosmic by washing their
olfactory mucosa with a 4% ZnSO4.7H2O solution,
according to the procedure described in Guilford et al.
(1998). (Group 2) FC-pigeons
(N=51), control birds, familiar with the release sites, whose
olfactory mucosa was washed with Ringer solution.
A first set of three releases, one for each site, was performed (No-Shift
condition). In each test the pigeons' orientation while exiting from the arena
and at vanishing were recorded. After homing, the same birds were subjected to
a fast clock-shift treatment, keeping them in a light-tight room with the
light:dark cycle 6 h fast with respect to the natural one for a period ranging
from August 15th to September 5th, except for a few hours in which the birds
took part in the release tests. The phase-shifted pigeons were then tested in
a second series of releases from the same sites (Clock-Shift condition). Thus
we adopted an experimental protocol allowing intra-individual comparisons.
Although we could not record the initial orientation of the unshifted and
shifted birds in the same day by this method, we consider this protocol valid
due to the extreme stability of the initial orientation of both anosmic and
intact unshifted pigeons familiar with Calambrone, La Costanza and Arnaccio
(see the data reported in Diekamp et al.,
2002; Gagliardo et al.,
2001b
). In this case each release took 3 days to be performed (see
Table 1 for details) since the
clock-shifted pigeons had to be released before the beginning of their
subjective night. Once homed from each release site, the birds were
immediately caught and placed again in the light-tight room until the next
test release. Due to their familiarity with the release sites, all the birds
homed within the same day of the release and most of them homed before the end
of their subjective day. Therefore they were unlikely to re-adjust their
internal clock to the natural light:dark cycle.
All the experimental releases took place in sunny conditions, with no or light wind.
The circular arena used to record the orientation before take-off is
described in Gagliardo et al.
(2001b) and Mazzotto et al.
(1999
). In brief, the arena
(1.8 m in diameter) was made of non-magnetic material and placed on a 1.2 m
high pedestal. The ceiling consisted of a net which allowed both a full view
of the sky and free circulation of the air. The birds were able to escape by
pushing through aluminium bars hanging down around the edge of the arena. The
bars are familiar to the pigeons since they are the same as those used at the
entrance to their loft. At the centre of the arena there is a remotely
operated release box made of a net, where the pigeons were kept for 2 min
before the beginning of the test.
Each bird was placed in the release box, which was opened by the experimenter pulling a rope while sitting under the arena out of the view of the bird. The escape bearing was recorded using a compass referring to the mid-point between the bars lifted by the pigeon. For each bird, the time spent in the arena before taking off was also recorded. If a bird spent more than 20 min before exiting from the arena, we tried to catch it in order to release it later. If the bird escaped as the experimenter approached, the exit direction was not recorded.
After take-off the pigeon's flight was observed using 10 x40 binoculars and the azimuth of the vanishing bearing was recorded. The vanishing time was also recorded.
For each release, two bearing distributions were obtained: one referring to
the pigeons' directional choices while exiting from the arena and the second
referring to the birds' vanishing directions. For each distribution a mean
vector and homeward component were calculated, the latter ranging from
1.0 to +1.0. The 95% and 99% confidence limits of the mean vectors were
also calculated. The circular distributions were tested for randomness by
means of both the Rayleigh and V-test, the latter taking into account
an expected direction (Batschelet,
1981). For the non-shifted group distributions the expected
direction was the home direction, while for the clock-shifted distributions
the V-test was also performed considering the shifted home direction
(see below). Comparisons between two circular distributions were achieved by
the Watson U2 test.
Second order mean vectors were calculated for each pigeon, for both the orientation in the arena and at vanishing. The vectors were obtained by pooling the orientation data obtained from each single pigeon in the three tests and setting the home direction to 360°. For most of the birds each vector was calculated from three bearings, but the individual mean vectors of a few pigeons were calculated from the data of two sites. If only one bearing was recorded the datum was excluded from the second order statistics.
The one-sample Hotelling test
(Batschelet, 1981) was applied
to test for randomness the individual mean vector distributions relative to
the orientation in cage and at vanishing. The two-sample Hotelling test
(Batschelet, 1981
) was applied
to compare the mean vector distributions of C-pigeons and A-pigeons. The
Hotelling test for paired samples of angles
(Zar, 1984
) was used in order
to compare, for each experimental group of birds, the orientation in the arena
in the no-shift and clock-shift conditions.
For the three releases after the Clock-Shift treatment, individual expected
directions in arena and at vanishing were also calculated as follows. On the
basis of the sun azimuth at the time of release of each single bird, we
calculated the expected deviation after clock-shift. The latter was added to
the home direction to calculate the individual, and then the mean, shifted
home direction (used in the V-test and in the shifted homeward
component for the clock-shifted birds). The expected deviation was also added
to the mean direction of both C and A groups in the No-Shift condition to
calculate the individual expected directions. We used the mean direction of
the groups released in the No-Shift condition, to keep possible release site
bias out of the analysis. The individual expected directions were pooled,
setting the home direction to 360°, in order to obtain the expected
individual mean vectors, which were used to calculate the second order
expected mean vectors and their confidence ellipses
(Batschelet, 1981).
The times spent in the arena and the vanishing times of FC- and FA-pigeons
were compared using the MannWhitney U test
(Siegel, 1956).
Series II
A second series of test releases was carried out in order to observe the
initial orientation of pigeons unfamiliar with the three release sites used
for Series I and therefore to get a baseline for the pigeon orientation
without any influence of the landscape. An optimal experimental plan would
have provided the simultaneous release of the birds familiar and unfamiliar
with the release sites. Unfortunately this was not possible due to the large
number of pigeons needed and because the releases would have taken too long.
The circular arena was not used and only vanishing bearings were recorded.
Ninety-seven adult pigeons unfamiliar with the release sites were used. They were randomly assigned to two experimental groups: UUC, unshifted unfamiliar controls, and SUC, clock-shifted unfamiliar controls, subjected to a 6 h fast shift of their internal clock. Each bird took part in only one experimental release. Each release took place in the same month of the following year as the clock-shift test of Series I (see Table 4 for details). For other details of the methods, see Series I.
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Results |
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For releases performed in the No-Shift condition (see Fig. 1), at La Costanza and Arnaccio, both control and anosmic birds displayed directional choice distributions in the arena significantly different from random, according to both the Rayleigh and the V-test (see Table 1 for significance levels). The homeward component of the distributions' mean vectors for both C- and A-pigeons was positive at both sites and the mean vector directions were close to the home direction. At Calambrone, the unshifted anosmic birds were significantly oriented while exiting the arena, according to both the Rayleigh and the V-test, while the control (intact) pigeons' distribution turned out to be not significantly different from uniform according to the Rayleigh test. However, the C-birds' mean vector direction was oriented close to the home direction (see also the positive results of the V-test and other details in Table 1). On the whole, in the No-Shift condition, both control and anosmic birds were homeward oriented even before take-off.
In the Clock-Shift condition (Fig. 2), neither C- nor A-pigeons displayed distributions significantly different from random, except for the control birds at Calambrone, which were significantly oriented (Rayleigh test, P<0.01) in a direction different from the home direction (see also the negative homeward component in Table 1).
Within each single release test, in both the No-Shift and the Clock-Shift conditions, the Watson U2 test never revealed a significant difference between the distributions in the arena of C- and A-pigeons.
The median time spent in the arena by the C- and A-pigeons before take-off, which is reported in Table 1, was not significantly different in the three releases (MannWhitney U test, P>0.05).
The second order statistics results are reported in Table 2 and Fig. 3, which show the individual mean vectors distributions. In the No-Shift condition, the second order distributions in the arena were significantly different from random for both anosmic and control (intact) pigeons (one-sample Hotelling test, P<0.001 for both A- and C-birds) and the second order mean vector directions were close to the home direction. By contrast, in the Clock-Shift condition, both second order distributions were not significantly different from random (one-sample Hotelling test, P>0.05 for both A- and C-birds). The comparison between the A and the C vector distributions did not reveal any statistical difference in either No-Shift or Clock-Shift conditions (two-sample Hotelling test on vectors, P>0.05 in both cases).
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The individual mean orientation in the arena in the two phase conditions (No-Shift versus Clock-Shift) was compared by means of the Hotelling test on paired vectors. According to this test, the mean orientation in the arena of both control and anosmic pigeons was significantly different in the No-Shift versus the Clock-Shift condition (C-pigeons: F(2,42)=9.804, P<0.001; A-pigeons: F(2,43)=17.37, P<0.001). Therefore, before the manipulation of their internal clock the birds belonging to both experimental groups (A and C) were already homeward oriented before take-off, while the clock-shift treatment caused a general scattering of both groups in the arena.
Orientation at vanishing
The orientation at vanishing of the C- and A-pigeons in the single releases
is reported in Table 3 and Figs
1 and
2 (outer diagrams).
In the No-Shift condition, the two experimental groups (C and A) were significantly oriented both according to the Rayleigh and V-test at the three release sites (see Table 3 for significance levels). In all releases, the homeward component relative to C- and A-pigeons' distributions was positive and the mean vector direction was close to the home direction. As expected, the vanishing distributions of both groups were on the whole gathered around the home direction.
In the Clock-Shift condition (Fig. 2, outer diagrams), the vanishing distributions of both C- and A-pigeons were significantly different from random according to the Rayleigh test in all releases, and according to the V-test (performed by considering the home direction as expected direction) at La Costanza and Calambrone (see details in Table 3). In fact, only at Arnaccio did both experimental groups display a negative homeward component as a consequence of the clock-shift treatment (see also in Table 3, columns h'c, the statistically significant results given by the V-test performed by considering the shifted home direction as expected direction). Therefore, the clock-shift manipulation did not, at least at La Costanza and Calambrone, produce the expected deviation for C- and A-pigeons (see also Fig. 2, in which the expected mean direction for each release is reported). The Friedmann-repeated-measures ANOVA on ranks applied to the deviations from the mean direction recorded in the No-shift release revealed a significant effect of the release site on the extent of the deviation for both groups of pigeons (C-pigeons, N=38, P<0.0001; A-pigeons, N=36, P<0.0001; post hoc analysis: StudentNewmanKeuls method, P<0.05 in all comparisons for both C- and A-pigeons).
Within each single release, in the No-Shift condition, the Watson U2 test never revealed a significant difference between the vanishing distributions of C- and A-pigeons, while in the Clock-Shift condition C- and A-birds turned out to have different vanishing orientations at Calambrone (see Table 3 for significance levels).
The median vanishing times are reported in Table 3. The MannWhitney U test revealed a statistical difference between A- and C-pigeons in the time taken to vanish from the observer's view in only one release test (Clock-Shift condition, La Costanza P<0.01).
The results of the second order statistics are reported in Table 2 and Fig. 4. The second order vanishing distributions were significantly different from random for the anosmic and control (intact) pigeons in both the No-Shift and Clock-Shift condition (one-sample Hotelling test, P<0.001 in all cases). In the No-Shift condition the second order mean vector direction was close to the home direction for both C- and A-pigeons and the two vector distributions were not statistically different (two-sample Hotelling test, P>0.05). In the Clock-Shift condition the mean vector direction relative to both pigeon groups deviated counterclockwise from the home direction. Although both A- and C-pigeons displayed a deviation smaller than expected (see expected mean direction in Fig. 4) theanosmic birds deviated significantly less than the controls (two-sample Hotelling test, P<0.01).
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According to the Hotelling test for paired data applied to the individual mean vector distributions, the orientation of both control and anosmic pigeons was significantly different in the No-Shift versus the Clock-Shift condition (P<0.001 for both groups).
Series II
Orientation at vanishing
The initial orientation of the unshifted (UUC) and clock-shifted (SUC)
pigeons unfamiliar with the release sites is reported in
Table 4 and
Fig. 5.
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At the three release sites the UUC-pigeons were significantly oriented at vanishing, according to both the Rayleigh and V-test (see Table 4 for significance levels). In all releases, the homeward component of the mean vector was positive and its direction was close to the home direction.
The SUC-pigeons displayed significantly oriented vanishing distributions at the three release sites, according to the Rayleigh test. As a consequence of the clock-shift treatment, the V-test, when performed taking into account the home direction, never turned out to be significant, and in two releases the homeward component of the mean vector was negative. By contrast, when the V-test was performed taking into account the shifted home direction, it gave statistically significant results (see Table 4 for details).
The KruskallWallis test applied on the deviations displayed by the clock-shifted birds (SUC) from the mean direction of unshifted pigeons (UUC) at the three release sites, did not reveal a significant effect of the release site on the extent of the deviation (SUC-pigeons, N=15, P=0.059).
The Watson U2 test revealed a significant difference between the unshifted and the shifted pigeons' distributions in all releases (see Table 4 for significance levels).
The median vanishing times are reported in Table 4. The MannWhitney U test never revealed a statistical difference between UUC- and SUC-pigeons in the time taken to vanish from the observer's view.
A comparison between the vanishing distributions of the experimental groups of Series I and Series II, for each release site, is reported in Fig. 6. In particular, Fig. 6N-S shows the mean vectors and their 95% confidence limits of unshifted birds (FC, FA, UUC) and Fig. 6C-S refers to the shifted birds (FC, FA, SUC). Consistent with what can be observed in Fig. 6, the WatsonWilliams test applied to compare the three experimental groups revealed a significant difference between the distributions in all cases, except at Arnaccio in the unshifted condition (Unshifted condition: Calambrone and La Costanza, P<0.001; Arnaccio, P>0.05; Clock-shifted condition: Calambrone and La Costanza, P<0.001; Arnaccio, P<0.01). Although these results must be considered with caution because the experiments of the Series I and II were performed in different years, they are indicative of an effect of familiarity with the release site on the initial orientation in both unshifted and shifted conditions. In particular, in the shifted condition the birds unfamiliar with the release site displayed a deflection greater than both familiar groups (see Fig. 6C-S). Moreover, the anosmic birds familiar with the sites (FA) tended to deviate less than the familiar controls (FC).
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Discussion |
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The combined effect of familiarity with the release site and the general
dominance of the sun compass mechanism over the pilotage strategy determines
an orientation towards an intermediate direction between the true and the
erroneous home direction indicated by the topographical map and the sun
compass, respectively. Some authors have reported a certain degree of
reduction in the deviation of clock-shifted pigeons, regardless of the level
of familiarity with the release site
(Wiltschko et al., 1994) and
they have explained this phenomenon with a contemporary use of the sun and
magnetic compass information, the latter not being influenced by the
clock-shift (Wiltschko and Wiltschko,
2001
). However, we can reasonably interpret the reduction of the
deviation observed in our pigeons released at familiar locations, as mainly
due to the use of topographical information. In fact, different from what was
observed for the pigeons familiar with the release sites, the clock-shifted
birds unfamiliar with the release sites showed a deviation consistent with
expectations (see also Fig. 5). If the magnetic compass information were responsible for a correction
mechanism, we would have observed the same extent of reduction in deviation in
pigeons both familiar and unfamiliar with the release sites.
In principle, the observed reduced deflection showed by the birds familiar
with the release site, might also be interpreted as a consequence of a
recalibration of the sun compass due to consecutive releases in the
phase-shifted condition (Wiltschko et al.,
1976,
1984
). However Foà and
Albonetti (1980
) produced
clear evidence against the occurrence of the recalibration of the sun compass
due to flight experience during the clock-shift period. In fact they observed
that releasing the birds several times at the same familiar site reduced the
deflection, while the homing experience during the clock-shift per se
(tested by releasing the birds at unfamiliar locations) did not. Moreover,
according to the recalibration hypothesis, we should expect in our data a
gradual reduction of the deflection from the first to the third release, which
is actually not observed. In fact, although the deviation in the first release
(Arnaccio) was the largest, it was larger in the third release than in the
second. Finally, the evidence that the anosmic clock-shifted pigeons familiar
with the release site deviated significantly less than their intact (smelling)
companions does not support the recalibration hypothesis, which should in
principle occur in both groups to the same degree.
It has been shown that at familiar sites pigeons have access to two maps,
based on olfactory and visual information
(Gagliardo et al., 2001b): the
olfactory map can only be used in association with a compass, while the map
based on visual cues can be used either coupled with a compass or for piloting
within an array of landmarks.
As already mentioned, we observed that, at familiar locations, anosmic pigeons tend to deviate less than intact birds after clock-shifting. Therefore, it seems that the lack of an olfactory navigational map, whose functionality in homing is strictly dependent on a compass mechanism, leads the pigeons to use topographical information more in a pilotage-like strategy rather than in a `map and compass' one.
A study reporting homing routes of clock-shifted pigeons released from two
familiar sites, showed a marked effect of the release site on the homing
strategy (Bonadonna et al.,
2000). In fact, from one site most of the pigeons followed
straight routes towards home, while from the other location most of them made
a long detour, as was expected after the internal clock manipulation.
Therefore, at one site piloting was the preferred strategy while at the other
site the `map and compass strategy' prevailed. Our data are consistent with
the observation that different homing strategies can have different importance
depending on the site. In fact, our clock-shifted pigeons familiar with the
sites tended to orient straight home at Calambrone and to deviate to differing
degrees at the other two locations.
Although it is not clear which local factors generally influence the choice
of the homing strategy after a clock-shift we can speculate that the homeward
orientation observed at Calambrone, for both anosmic and intact birds, might
have been due to their short distance from home. In fact we can hypothesise
that a pilotage strategy is easier to use when fewer landmarks need to be
remembered. Nevertheless, at least for the anosmic birds, a difference in the
extent of deviation can also be observed between La Costanza and Arnaccio,
which are located further from home. It is worth noting that La Costanza is
much closer (about 5 km) to the coast than Arnaccio (about 14 km) and
therefore the sea could represent a useful orienting cue. The latter
explanation has also been suggested by other authors, who observed a similar
reduction of the deflection in initial orientation of clock-shifted birds
released from La Costanza (Bonadonna et
al., 2000). At Arnaccio the anosmic birds, in compromising between
the use of topographical information in a `piloting-like' and in a `map and
compass' strategy, seemed to rely more on the latter.
Since, as already mentioned in the Introduction, different authors have
reported a different degree of deflection in the initial orientation
consequent to the clock-shift at familiar locations, it is worth comparing our
data with those collected by other authors performing similar experiments.
Similar to our observations, Bingman and Ioalè
(1989) and Wallraff et al.
(1994
) also reported a strong
effect of combined familiarity and anosmia in reducing the deviation of
initial orientation after clock-shift. However, different from our
observations in the present work and in Bingman and Ioalè
(1989
), Wallraff et al.
(1994
) and Füller et al.
(1983
) reported an almost full
deflection in the initial orientation of clock-shifted smelling pigeons at
familiar sites. It is worth noting that all these studies are not homogeneous
with respect to the training procedure used for acquisition of familiarity
with the release sites. For example, Wallraff et al.
(1994
), in contrast to all the
other papers on the subject, also trained the birds from several locations
around the experimental release site. Although the aim of the latter training
procedure was to prevent directional bias and, at the same time, induce a
wider topographical map learning, actually it might have made the use of a
pilotage-like strategy more difficult, due to the higher number of landmarks
and their spatial relationship to be remembered. On the other hand, the
extreme directional training (more than 50 times from the same site) as
reported in Füller et al.
(1983
) is likely to have
induced the birds to display a stereotyped directional response that
disregarded the topographical information.
As regards the orientation of our birds while exiting from the circular
arena, our data confirm previous findings that pigeons in the unshifted
condition are already homeward-oriented before take-off
(Chelazzi and Pardi, 1972;
Diekamp et al., 2002
;
Gagliardo et al., 2001b
;
Mazzotto et al., 1999
).
Contrary to our expectation, the clock-shift manipulation increased the
scattering so much that all the distributions of clock-shifted pigeons turned
out to be no different from uniform. Therefore, our data relative to the
orientation in the arena of clock-shifted birds are inconclusive, so that we
could not verify which strategy, piloting or `map and compass', the
clock-shifted pigeons used referring to the visual cues before take-off. It is
difficult to speculate about the causes of the observed scattering as a
consequence of the clock-shift; however, we can suggest that the observed
random distributions might result from the combination of two treatments (test
in the arena and clock-shift), each of which usually produces some
scattering.
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Acknowledgments |
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References |
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