Encoding spatial information in the waggle dance
Freie Universität Berlin, Fachbereich Biologie/Chemie/Pharmazie, Institut für Biologie Neurobiologie, Königin-Luise-Strasse 28-30, 14195 Berlin, Germany
* Author for correspondence (e-mail: rjdm02{at}yahoo.com.ar)
Accepted 11 August 2005
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Summary |
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Key words: Apis mellifera, waggle dance, spatial information, visual landmark, path integration
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Introduction |
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Honeybees are remarkable navigators that display circuitous flight paths on
the way to their goals as well as conspicuous shortcuts on the way back to
their colonies (von Frisch,
1965; Wehner and Menzel,
1990
; Dyer, 1998
;
Collett and Collett, 2002
;
Wehner and Srinivasan, 2003
;
Menzel et al., 2005
). Like
other central-place foragers (Müller
and Wehner, 1988
), they navigate by means of a celestial compass
and landmark-based information (von
Frisch, 1965
; Dyer,
1998
; Collett and Collett,
2002
; Wehner and Srinivasan,
2003
; Menzel et al.,
1998
,
2000
,
2005
). Certainly, bees
recruited through the waggle dance fly the distance and direction encoded in
the dance (Riley et al.,
2005
), and it is often concluded that a dancing bee communicates a
flight vector pointing towards the indicated location. Nevertheless, little is
known about how the compass (direction) and the odometric (distance)
information acquired during the foraging flight are finally combined in the
waggle dance.
First, an accurate indication of distance in the waggle dance presupposes
that the dancer has correctly measured the flight length. We know that the
retinal image flow that honeybees experience while flying provides them with
some means of monitoring the distance travelled (Esch and Burns,
1995,
1996
; Srinivasan et al.,
1996
,
1997
,
1998
,
2000
;
Esch et al., 2001
;
Tautz et al., 2004
). However,
although the flown distance seems to be primarily gauged on the way to a food
source (Heran and Wanke, 1952
;
Heran, 1956
;
Otto, 1959
;
von Frisch, 1965
; Srinivasan
et al., 1997
,
1998
), honeybees also monitor
distance information on the way back to their colonies
(Otto, 1959
;
von Frisch, 1965
; Srinivasan
et al., 1997
,
1998
). Hence, evaluating the
encoding of the visually measured distance in the waggle dance first requires
analysing how the distance information available both on the way to the goal
and on the way back to the colony is finally represented in the length of the
waggle-run. Such analysis does not yet exist.
Furthermore, von Frisch
(1965) designed some
remarkable `detour' experiments to analyse how the waggle dance encodes both
compass and odometric information. In one of his experiments (reviewed in
von Frisch, 1965
), for
instance, a group of foragers was guided around a jutting mounting ridge
separating the food source from the colony. In their dances, the foragers
indicated the straight line towards the goal (even when they followed the
detour on the way back to the colony). Similar results were reported for bees
flying indirect paths around a large building or a forest edge to finally
reach an artificial source of food, i.e. they computed the direct line of the
flight from the two legs of the detour, and this computed `global vector'
corresponded to the direction indicated in the waggle dance
(von Frisch, 1965
). Moreover,
under these circumstances, the bees indicated the actual flown distances in
their dances and not the distance of the shortcut towards the goal (i.e. a
straight segment connecting the food source and the nest's entrance;
von Frisch, 1965
). Hence,
dancing bees flying detour paths communicate the direction of a
non-experienced shortcut together with the actual flown distance, thus
reporting a subjective performance-dependent, but not a real, location. Since
the bee's perception of the distance flown is scene dependent
(Esch et al., 2001
;
Tautz et al., 2004
), this
subjective location can only be found if the recruited bees were to follow
more or less the same flight path as the dancer. The simplest explanation
about how a forager may indicate a non-experienced shortcut in its waggle
dance relies on path integration, i.e. an internal process by which an animal
continuously measures the distances and directions from a particular point and
computes its current position in the environment
(Mittelstaedt and Mittelstaedt,
1982
; Wehner,
1992
; Collett and Collett,
2002
; Wehner and Srinivasan,
2003
). Using path integration, for instance, Cataglyphis
ants are able to establish global vectors at the end of their outbound
(nest-to-food) paths, which allow them to follow straight trajectories of the
appropriate distance and direction during their inbound (food-to-nest) paths
(Wehner and Srinivasan, 1981
;
Müller and Wehner, 1988
).
Indeed, desert ants also use global vectors to follow straight trajectories
from the nest back to a previously visited food site
(Schmid-Hempel, 1984
;
Collett et al., 1999
;
Wolf and Wehner, 2000
). In von
Frisch's detour experiments described above, the direction of the global
vector computed by path integration of either the outbound or the inbound
flight always corresponded to the `subjective' direction connecting the food
site and the hive (von Frisch,
1965
). Hence, experiments must still be performed to test the
integration of the compass and the odometric information available throughout
the different flight segments of the foraging bout (e.g. the outbound and the
inbound flight) on the encoding of spatial information in the waggle
dance.
In the present study, we took advantage of the bees' visually driven
odometer (Srinivasan et al.,
2000; Esch et al.,
2001
; Tautz et al.,
2004
) to manipulate the navigational information provided to a
dancing bee. We then addressed two important questions: namely, (1) how the
waggle dance encodes the subjective distance experienced during either the
outbound or the inbound flight and (2) whether the encoding of directional
information in the waggle dance is based on path integration of the outbound
flight, i.e. what direction do the bees indicate in their dances if they
experience a mismatch between the subjective food location, computed by path
integration, and the actual location of the food site? Furthermore, since (1)
honeybees navigate according to a map-like spatial memory
(Menzel et al., 2005
) and use
both path integration and visual landmarks to solve complex navigational tasks
(Dyer, 1998
; Menzel et al.,
1998
,
2000
,
2005
;
Wehner and Srinivasan, 2003
)
and (2) the simultaneous processing of path integration and visual landmarks
may lead to changes in path integration coordinates depending on the animal's
experience of the terrain (Etienne et al.,
2004
; Collett and Graham,
2004
), we also analysed whether the bees' experience of the
foraging area modifies the encoding of spatial information in the waggle
dance.
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Materials and methods |
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In each experiment, 610 bees were allowed to forage on a feeder
placed 2° NE and 125 m from the hive's entrance (close to the
foraging area). The feeder offered unscented 1.8 mol l1
solution for
30 min. Next, 1520 newly recruited bees were marked
with numbered tags so that they could be individually identified (unmarked
bees, as well as those marked bees whose behaviours had been previously
recorded, were caged and released at the end of the experiment). Thus, in all
the series described below (unless specified otherwise), animals were marked
and recorded on the same day and lacked experience of flying inside the
tunnel. The tunnel was absent in all series before the beginning of the single
experimental sessions. In each of these sessions, it was set up (with its
floor positioned 50 cm above the ground) only after a group of newly recruited
bees was established. A second feeder (similar to the training feeder) was
then placed inside the tunnel, 30 cm away from its entrance. Whenever the
feeder was established at the near end of the tunnel (see below), it was
stepped regularly from its initial position (at the near entrance) to its
final position (at the very end of the tunnel). Recordings started
approximately 90 min after the bees were presented with the tunnel.
Experiments were conducted with an open view of the sky (i.e. no experiments
were conducted when the sky was cloudy). Each recording session lasted
approximately 3 h, and single marked bees performed a maximum of 30 foraging
trips to the feeder per session.
Calibration of the odometer
Since the bee's perception of the flown distance is scene dependent
(Esch et al., 2001;
Tautz et al., 2004
), we first
recorded the waggle dances of returning bees foraging on outdoor feeders
(offering unscented 1.8 mol l1 sucrose solution) located
135, 248 and 360 m from the hive. We measured the durations of the waggle
phases of the dances for each of these feeder distances. The results of these
experiments provided us with information about the subjective distances
experienced by the trained bees in our particular outdoor landscape.
The encoding of odometric information provided by either the outbound or the inbound flight
Two different situations were established in this series. In both
situations, measurements were made with the tunnel oriented at 0°, with
respect to the direct line connecting the near end of the tunnel and the
hive's entrance. In the first situation, bees were trained to enter the tunnel
at its near end and to leave it only via a small Plexiglas sliding
door located at the top of the far end of the tunnel. Hence, they followed
different flight paths during the outbound and the inbound component of the
foraging bout, i.e. they flew inside the tunnel during their outbound flights
but not during their inbound flights. By contrast, in the second situation,
the bees were trained to enter the tunnel at its far end (where the feeder was
located) and to leave it via its near end. Hence, they also followed
different flight paths during the outbound and the inbound flight. However, in
this case, the bees flew inside the tunnel only during their inbound flights.
Comparisons between the duration of the waggle phase of the dances recorded
for each of these two different situations were made on the basis of the
subjective distances experienced in our particular landscape.
The encoding of compass information when a mismatch occurs between the subjective and the actual direction towards the goal
In this series, the tunnel was rotated 90°, either to the left or to
the right, with respect to the direct line connecting the near end of the
tunnel and the hive's entrance (Fig.
2). The feeder was then presented at the far end of the tunnel and
the marked bees were trained to enter the tunnel at its near end. Two
different experimental situations were then assayed for each orientation
(90° to the left and 90° to the right). First, bees were allowed to
leave the tunnel via the sliding door located at the top of its very
end (see above), thus following different flight paths during their outbound
and inbound flights. A mismatch was then established between the subjective
location of the feeder, computed by path integration of the outbound flight,
and its actual location. The angles of the waggle axes (relative to vertical)
were measured in parallel to the waggle-phase durations. Second, attempts were
made (see Results) to train the bees to leave the tunnel via its near
end, thus following similar flight paths during their outbound and inbound
flights.
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Results |
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The encoding of odometric information provided by either the outbound or the inbound flight
Next, we evaluated the encoding of distance information provided by either
the outbound or the inbound flight. Bees flying through the 0°-oriented
tunnel during their outbound flights showed waggle-phase durations that lasted
significantly longer than those performed by the bees that did not fly through
the tunnel (Fig. 1A, black
circle; P<0.01, Tukey comparisons;
Fig. 2C, striped bar). The 6-m
flight in the tunnel during the outbound flight was thus perceived as
equivalent to an outdoor flight of 141 m
(Fig. 1A, black circle;
Fig. 2C, striped vs
grey bar). This result is in close agreement with published data
(Srinivasan et al., 2000;
Esch et al., 2001
). By
contrast, bees did not overestimate the travelled distance when they flew
through the tunnel during their inbound flights, although a tendency was
observed that indicated a slightly longer flown distance
(Fig. 1A, grey circle;
P=0.68, Tukey comparisons).
The encoding of odometric information in the 90°-oriented tunnel
Next, we evaluated the encoding of distance information when the tunnel was
rotated 90°, either to the left or to the right, with respect to the
direct line connecting the near end of the tunnel and the hive's entrance.
Comparisons were made based on data from bees that entered the tunnel at its
near end and left it via the sliding door located at the top of the
very end of the tunnel, thus following different flight paths during their
outbound and inbound flights. Under these circumstances, we found that the
bees' subjective flight distance travelled inside the tunnel did not change
statistically (Fig. 1C, grey
circles; P=0.36, Tukey comparisons;
Fig. 2F,I, striped bars). Bees
flying through the 90°-oriented tunnel showed waggle-phase durations that
lasted significantly longer than those performed by bees that did not fly
through the tunnel, irrespective of the tunnel orientation (either to the left
or to the right of the reference line; Fig.
1C, grey circles; P<0.01, Tukey comparisons).
Moreover, the subjective flight distances recorded for both orientations of
the tunnel did not differ statistically from those recorded previously for the
0°-oriented tunnel (Fig.
1A,C, black circle vs grey circles; 0° vs
90°-Left, P=0.99; 0° vs 90°-Right,
P=0.52, Tukey comparisons; Fig.
2C,F,I, striped bars). Averaging the results obtained for the two
different orientations showed that the 6-m flight in the tunnel was equivalent
to an outdoor flight of 129 m (Fig.
1C, grey circles).
The directional scatter of the waggle-runs
A feature of the waggle dance is that consecutive waggle-runs are performed
with some directional scatter, i.e. the directions of single waggle-runs
usually diverge from each other, erring alternately to the right and left of
the main vector (von Frisch,
1965). Early works demonstrated that the distance flown to reach
the food source affects these divergences
(von Frisch, 1965
).
Fig. 1B,D (open circles) shows
the effects of the distance travelled in our particular landscape on the
individual directional scatter obtained from the waggle dances for each of the
recorded feeder distances. Data fit an inverse polynomial function
(R=0.66, P<0.001) whose corresponding equation is
Y=Y0+a(x)1, in which Y
corresponds to the individual directional scatter, x corresponds to
the distance travelled, and Y0 (1.1) and a
(3062.4; P<0.001) are constants. Bees flying through the
0°-oriented tunnel during their outbound flights showed a directional
scatter smaller than that corresponding to the same absolute distance
travelled in the absence of the tunnel
(Fig. 1B, black circle;
P<0.002, Tukey comparisons). By contrast, the bees that flew
through the 0°-oriented tunnel during their inbound flights showed a
directional scatter that did not differ statistically from that recorded for
the same absolute distance travelled in the absence of the tunnel
(Fig. 1B, grey circle,
P=0.18, Tukey comparisons). As in the case of the 0°-oriented
tunnel, the bees that flew through the 90°-oriented tunnel (rotated either
to the left or the right) also showed a directional scatter clearly smaller
than that recorded for the same absolute distance travelled outdoor
(Fig. 1D, grey circles, Left,
P=0.01; Right, P<0.05, Tukey comparisons).
The encoding of compass information when a mismatch occurs between the subjective and the actual direction towards the goal
The global vectors (pointing toward subjective locations) computed by path
integration of the outbound flight have different directions at the end of the
different flight paths recorded throughout the experiments, i.e. those assayed
with the tunnel oriented at 0°, 90° to the left and 90° to the
right (see Materials and methods). According to early detour experiments by
von Frisch (1965), these
global vectors might provide the bees with the directional information encoded
in the waggle dance. If that were the case, the expected directions to be
signalled by dancers flying inside the 90°-rotated tunnel can be easily
calculated by considering the actual food location and the subjective flight
distance recorded for the 0°-oriented tunnel. These expected directions
are 48.7°, either to the left or to the right, with respect to the direct
line connecting the near end of the tunnel and the hive's entrance
(Fig. 2E,H,K, open arrowhead).
However, the directions actually signalled in the dances clearly differed from
those pointing towards the virtual locations after path integration of the
outbound flight (Fig. 2E,H,
black bars vs open arrowheads): dances indicated directions of only
3.9±2.9° (mean ± S.E.M.,
P<0.001, Rayleigh test) to the left (for the tunnel oriented
90° to the left) and only 6.8±4.0° (mean ±
S.E.M., P<0.001, Rayleigh test)
to the right (for the tunnel oriented 90° to the right), regarding the
linear distance connecting the near end of the tunnel and the hive's entrance.
Each of these directions (Fig.
2E,H, black bars) was not significantly different from the
direction (Fig. 2B, black bars;
1.3°±1.5°, mean ±
S.E.M., P<0.001, Rayleigh test)
recorded for the 0°-oriented tunnel
(Fig. 2B,E,H; 90°-Left
vs 0°, F1,29=3.3, P=0.08;
90°-Right vs 0°, F1,30=2.7,
P=0.11, Watson F-test), although they differed from each
other (Fig. 2E,H;
F1,17=5.6, P<0.001, Watson
F-test).
We also compared the mean duration of the foraging cycle, i.e. the time interval between two successive departures from the nest to the feeder, recorded from four different groups of animals: bees that foraged on the outdoor feeder placed 135 away from the hive's entrance (i.e. in the absence of the tunnel), bees that flew through the 0°-oriented tunnel during their outbound flights, and bees flying through the 90°-rotated tunnel, either to the left or to the right, during their outbound flights. No differences in the mean duration of the foraging cycle were found among these groups (mean ± S.E.M.; 135 m, 6.5±0.56 min, N=6; 0°, 7.92±0.96 min, N=13; 90°-Left, 7.91±0.97 min, N=11; 90°-Right, 7.89±0.89 min, N=6; F3,35=0.37, P=0.77, one-way ANOVA).
Next, we asked what directions the bees indicate in their dances if they leave the tunnel using the same route they followed to reach the feeder, i.e. if they fly through the tunnel during both the outbound and the inbound flights. Hence, a second experimental situation was assayed with the tunnel rotated 90°, either to the left or to the right: attempts were made to train the bees to enter and leave the tunnel via its near end. Surprisingly, the marked bees could not be trained to fly back through the tunnel. They usually covered approximately 1.5 m of their inbound flights (performing circuitous flights inside the tunnel) and then returned to the far end of the tunnel, where the feeder was located. These circuitous displacements could be repeated several times before the bees stopped flying and finally stayed on the walls at the far end of the tunnel. Presumably, the information gathered during the outbound flight with respect to distance and direction prevented them from flying back through the tunnel, thus ignoring the shortcut flight computed by path integration. Furthermore, whenever the bees were flying through the 0°-oriented tunnel, they could not be trained to fly through a 90°-oriented tunnel immediately afterwards. Under these circumstances (i.e. immediately after the tunnel was rotated 90°, either to the left or to the right), all the animals that entered the tunnel displayed repetitive short flights in the former direction (0°), within the first 12 m of the tunnel. Somehow, the directional information available inside the tunnel, which suddenly changed by 90° with respect to the direction recently experienced, compelled the bees to fly no more than a short distance inside the re-oriented tunnel. Throughout several trials performed on different days (which involved different groups of animals), only two marked bees (out of 40) finally reached the feeder after several minutes of circuitous flights in which most of the straight components were also displayed in the former direction. Once returned to the hive, these two animals did not dance and stopped foraging.
The bees' experience of the terrain and the encoding of spatial information in the waggle dance
A comparison was made between the directions indicated in the dances of two
different groups of bees flying through the 90°-oriented tunnel: (1) bees
that lacked experience of flying inside the tunnel (henceforth termed
`naïve' bees) and (2) bees that had previously foraged inside the
0°-oriented tunnel, 24 h prior to the beginning of the experiment
(henceforth termed `experienced' bees). We found that the experienced bees
(Fig. 2K) indicated a mean
direction (± S.E.M.) of
26±2.9° (P<0.01, Rayleigh test), which was different
(F1,13=34.9, P<0.001, Watson F-test)
from that indicated by naïve bees
(Fig. 2H, see above). Moreover,
they also indicated a shorter distance in their dances
(Fig. 2L vs
Fig. 2I, striped bars,
t13=2.4, P=0.032).
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Discussion |
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The direction of the global vector and the encoding of compass information
Bees benefit from path integration to solve complex navigational tasks
(von Frisch, 1965;
Dyer, 1998
;
Collett and Collett, 2002
;
Wehner and Srinivasan, 2003
;
Menzel et al., 2005
). This
means that they appear to keep continuously updated records of their current
directions and distances from some reference point as they move away from that
place, which allows them to establish global vectors encoding the appropriate
distances and directions of the straight trajectories connecting their current
locations and the reference point
(Mittelstaedt and Mittelstaedt,
1982
). Early detour experiments by von Frisch
(1965
) suggested that the
directions of these global vectors provide the bees with the directional
information encoded in the waggle dance. But does the waggle dance refer only
to the direction of the global vector computed by path integration of the
outbound flight? If that were the case, the directions signalled in some of
our experiments (Fig. 2E,H,K,
black bars) should have matched those of the global vectors computed at the
end of the different outbound flights (Fig.
2E,H,K, open arrowheads). However, when dancers were presented
with conflicting navigational information at the end of their outbound flights
(Fig. 2D,G,J), their waggle
dances did not refer to the directions of the global vectors
(Fig. 2E,H,K, black bars). In
the case of naïve bees (see Materials and methods), the directions
encoded in the dances (Fig.
2E,H, black bars) were close to the direct line connecting the
actual locations of the feeder and the hive's entrance
(Fig. 2E,H, grey arrowheads).
Each of these two directions (recorded when the tunnel was rotated 90°,
either to the left or to the right) was not significantly different from the
mean direction recorded for the 0°-oriented tunnel
(Fig. 2B vs
Fig. 2E,H, black bars; also see
Results). The simplest hypothesis that would presumably explain the signalled
directions is that the dances referred to the entrance of the visually
patterned tunnel, thus ignoring the directional information available inside
the tunnel. However, the signalled directions recorded for both orientations
of the 90°-rotated tunnel, either to the left or to the right of the
direct line connecting the tunnel's entrance and the hive
(Fig. 2E,H), actually differed
from each other (see Results). Moreover, results from experienced bees (see
below) show that directional information is being computed in the
90°-oriented tunnel. This means both that bees
(Fig. 2E,H) did not ignore the
directional information available inside the tunnel and that their waggle
dances did not refer to the tunnel's entrance.
The visually driven odometer is primarily decoupled from the processing of directional information
Thus, we found that the waggle dance does not necessarily refer to the
direction of the global vector computed by path integration of the outbound
flight (Fig. 2E,H). In
addition, dances of naïve bees flying through the 90°-oriented tunnel
signalled similar distances, irrespective of the tunnel's orientation, either
to the left or to the right of the reference line
(Fig. 1C, grey circle;
Fig. 2F,I, striped bars). These
distances, in turn, were longer than those expected according to the length of
the global vectors computed by path integration of the outbound flights
(Fig. 2F,I, striped vs
open bars). Moreover, in these cases, neither the signalled distances nor the
directional scatter of the successive waggle-runs were different from the
corresponding values recorded for the 0°-oriented tunnel
(Fig. 1AD, black and
grey circles; Fig. 2C,F,I,
striped bars; see also Results). Hence, our results also demonstrate that the
bees' visually driven odometer is primarily decoupled from the processing of
directional information, at least in the context of the waggle dance. This
finding is in close agreement with published data
(von Frisch, 1965).
The inbound flight and the encoding of compass information
One might ask whether or not the waggle dance encodes directional
information computed during the inbound flight. Indeed, early detour
experiments addressed the question of whether bees use their inbound vectors
for the purpose of directional indication, for instance, by `neurally'
switching them by 180° (Otto,
1959; Lindauer, 1963; von
Frisch, 1965
). If that were the case, the directions signalled in
our experiments with the 90°-oriented tunnel might have been based on path
integration of the inbound flight. That is, since the bees flew a two-legged
journey to reach the feeder (Fig.
2D,G), travelling relatively equivalent subjective distances
during each of the two flight segments
(Fig. 2F,I; see differences
between grey and striped bars), they might have initially directed their
homing flights in the direction of the global vectors
(Fig. 2E,H, open arrowheads)
and then corrected their subsequent displacements to reach the location of the
hive. The direction computed by path integration of these corrected inbound
flights might have been finally used for the purpose of directional indication
in the waggle dance. In this case, differences must be expected in the mean
duration of the foraging cycle when the results from different experiments are
compared due to the time involved in the erroneous inbound headings and the
subsequent orientation flights. However, we found that bees invested similar
amounts of time in their successive foraging cycles, irrespective of the
tunnel's orientation (see Results). Moreover, the duration of the foraging
cycle recorded for each of the three different orientations of the tunnel
(0°, 90° to the left and 90° to the right) did not statistically
differ from that recorded for the same absolute distance travelled in the
absence of the tunnel (see Results).
Hence, when the subjective direction towards the goal did not match the actual one, the naïve bees (see Materials and methods) referred in their dances to a direction (Fig. 2E,H, black bars) that was close to both the direction pointing towards the actual location of the feeder (Fig. 2E,H, grey arrowheads) and that of the inbound flight (see above). This means that, at the beginning of the inbound flight, the dancer's nervous system had to correct the directional information provided by the global vector in order to establish the signalled direction, suggesting that the encoding of spatial information in the waggle dance includes a component that detects the deviation between subjective measures of distance and direction and landmark-based information defining the shortcut between the goal and the hive. Our results can only be explained if we assume that landmark-based information is computed during the inbound flight and that it may strongly affect the encoding of directional information in the waggle dance. It would then be interesting to present the dancers with different inbound flights to further evaluate their role in the encoding of spatial information (for instance, by displacing them to unfamiliar environments after the travelled outbound flights in which navigational information is manipulated).
But how do bees establish the direction of the shortcut when they
experience a mismatch between visually defined coordinates and the coordinates
provided by the global vectors? Cataglyphis ants, a walking
central-place foraging insect, also navigate by means of path integration
(Collett and Collett, 2000;
Wehner and Srinivasan, 2003
)
and landmark-based information (Collet et al., 1992;
Wehner et al., 1996
;
Collett and Collett, 2002
).
Their global vectors, unlike their local vectors (nestward-directed vector
memories), seem not to be recalled by familiar landmarks
(Collett et al., 1998
).
However, if the information from path integration is experimentally
eliminated, desert ants associate local vectors with landmarks present during
their inbound paths (Bisch-Knaden and
Wehner, 2003
), indicating that the inbound path constitutes a
temporal stage at which the ants acquire critical navigational information.
Both bees and ants acquire memories of landmarks and of actions associated
with those landmarks to navigate between their nests and a foraging area
(Collett and Collett, 2002
;
Menzel et al., 1998
,
2000
,
2005
). It is often suggested
that, within familiar terrain, the inevitable errors associated with path
integration (Benhamou et al.,
1990
) can be reduced through landmark-based information
(Srinivasan et al., 1997
;
Collett and Graham, 2004
), and
even that path integration controls navigation only as long as the animal
combines it with learned strategies and environmental cues
(Etienne et al., 2004
). In our
experiments, naïve bees might have linked the visual landmarks perceived
at the beginning of their inbound flights with their best estimate of the path
integration coordinates of that place
(Collett and Graham, 2004
).
When provided with conflicting navigational information, namely a strong
mismatch between their current path integration coordinates (computed during
the outbound flight) and a set of different path integration coordinates
previously associated with visual landmarks, they might have used the later
source of navigational information to define the direction of the shortcut.
Either the same coordinates or the compass information acquired during the
inbound flight might be used to indicate direction in the waggle dance.
The bees' experience of the terrain and the encoding of spatial information
The resetting of an integrator using visual landmarks implies that an
animal is able to link the landmarks associated with a particular location
with its best estimate of the path integration coordinates of that location.
For visual resetting to occur, the stored path integration coordinates of a
visually defined location should come from the average path integration
coordinates experienced in that particular location, and thus would change
with the animal's increasing experience of the terrain
(Collett and Graham, 2004).
Intriguingly, we found that the bees' experience of the two-legged journey
changed the encoding of spatial information in the waggle dance, i.e. bees
flying inside the 90°-oriented tunnel modified the encoding of both
direction and distance based on whether (or not) they had foraged inside the
0°-oriented tunnel, approximately 24 hbefore the experiments
(Fig. 2H,I vs
Fig. 2K,L; also see Results).
Most likely, the increasing experience of the visual landmarks present in the
foraging area and of the two different types of landscapes available during
both segments of the two-legged outbound flight (but not of a particular route
defined by subjective measures of both distances and directions) modulated the
encoding of spatial information in the waggle dance. Indeed, the directional
information perceived inside the tunnel was processed differentially in the
context of the waggle dance only after experiencing the prospective path
integration coordinates and visual cues throughout two successive days
(Fig. 2K,L). This means that
the difference observed in the dances of both experienced and naïve bees
might be explained on the basis of the magnitude of the mismatch experienced
at the beginning of the inbound flight between the current and stored path
integration coordinates (see above); particularly since the bees were always
exposed to the same landmark views at the beginning of their inbound flights.
In this context, the higher the number of flights in which the bees are
exposed to the two different types of landscapes available en route
to the goal (i.e. those provided by the successive outdoor- and
tunnel-flights) the lower the magnitude of the experienced mismatch. It is
under these circumstances that the path integration information computed
inside the 90° tunnel becomes more heavily weighted in the context of the
waggle dance; which, in turn, involves a robust interaction between
landmark-based and path integration information. Early experiments by Otto
(1959
) also indicated that the
directional information available during the entire foraging flight may be
combined in the waggle dance only after increasing experience of the terrain.
Interestingly, our results suggest that the waggle dance may benefit from the
computation of stored path integration coordinates of visually defined
locations. Since honeybees navigate according to a map-like spatial memory
(Menzel et al., 2005
), further
research on dance communication would benefit from the possible interactions
between path integration and landmark-based information, which, in turn, might
allow landmark views to be assigned with metric coordinates.
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Batschelet, E. (1981). Circular statistics in biology. In Mathematics in Biology (ed. R. Sibson and J. E. Cohen), pp. 1-372. London: Academic Press.
Benhamou, S., Sauvé, J.-P. and Bovet, P. (1990). Spatial memory in large scale movements, efficiency and limitation of the egocentric coding process. J. Theor. Biol. 145,1 -12.
Bisch-Knaden, S. and Wehner, R. (2003). Local vectors in desert ants: context-dependent landmark learning during outbound and homebound runs. J. Comp. Physiol. A 189,181 -187.
Bisetzky, A. R. (1957). Die Tänze der Bienen nach einem Fußweg zum Futterplatz. Z. Vergl. Physiol. 40,264 -288.[CrossRef]
Chittka, L. and Tautz, J. (2003). The spectral
input to the honeybee visual odometry. J. Exp. Biol.
206,2393
-2397.
Collett, M. and Collett, T. S. (2000). How do insects use path integration for their navigation? Biol. Cybernet. 83,245 -259.[CrossRef][Medline]
Collett, T. S. and Collett, M. (2002). Memory use in insect visual navigation. Nat. Rev. Neurosci. 3, 542-552.[CrossRef][Medline]
Collett, T. S. and Graham, P. (2004). Animal navigation: path integration, visual landmarks and cognitive maps. Curr. Biol. 14,475 -477.[CrossRef]
Collett, T. S., Dillmann, E., Giger, A. and Wehner, R. (1992). Visual landmarks and route following in desert ants. J. Comp. Physiol. A 170,435 -442.
Collett, M., Collett, T. S., Bisch, S. and Wehner, R. (1998). Local and global vectors in desert ant navigation. Nature 394,269 -272.[CrossRef]
Collett, M., Collett, T. S. and Wehner, R. (1999). Calibration of vector navigation in desert ants. Curr. Biol. 9,1031 -1034.[CrossRef][Medline]
Dyer, F. C. (1998). Spatial Cognition: lessons from central-place foraging insects. In Animal Cognition in Nature (ed. R. Balda, I. Pepperburg and A. Kamil), pp.119 -154. New York: Academic Press.
Dyer, F. C. (2002). The biology of the dance language. Annu. Rev. Entomol. 47,917 -949.[CrossRef][Medline]
Esch, H. E. and Burns, J. E. (1995). Honeybees use optic flow to measure the distance of a food source. Naturwissenschaften 82,38 -40.[CrossRef]
Esch, H. E. and Burns, J. E. (1996). Distance
estimation by foraging honeybees. J. Exp. Biol.
199,155
-162.
Esch, H., Goller, F. and Burns, J. E. (1994). Honeybee waggle dances: the `energy hypothesis' and thermoregulatory behavior of foragers. J. Comp. Physiol. B 163,621 -625.
Esch, H. E., Zhang, S., Srinivasan, M. V. and Tautz, J. (2001). Honeybee dances communicate distances measured by optic flow. Nature 411,581 -583.[CrossRef][Medline]
Etienne, A. S., Maurer, R., Boulens, V., Levy, A. and Rowe,
T. (2004). Resetting the path integrator: a basic condition
for route-based navigation. J. Exp. Biol.
207,1491
-1508.
Gould, J. L. and Gould, C. G. (1988). The Honey Bee. New York: W. H. Freeman.
Heran, H. (1956). Ein Beitrag zur Frage nach der Wahrnehmungsgrundlage der Entfernungsweisung der Bienen. Z. vergl. Physiol. 38,168 -218.[CrossRef]
Heran, H. and Wanke, L. (1952). Beobachtungen über die Entfernungsmeldung der Sammelbienen. Z. vergl. Physiol. 34,383 -393.[CrossRef]
Linaduer, M. (1963). Kompassorientierung. Ergeb. Biol. 26,158 -181.
Menzel, R., Geiger, K., Müller, U., Joerges, J. and Chittka, L. (1998). Bees travel novel homeward routes by integrating separately acquired vector memories. Anim. Behav. 55,139 -152.[CrossRef][Medline]
Menzel, R., Brandt, R., Gumbert, A. and Komischke, B. (2000). Two spatial memories for honeybee navigation. Proc. R. Soc. Lond. B 267,961 -968.[CrossRef][Medline]
Menzel, R., Greggers, U., Smith, A., Berger, S., Brandt, R.,
Brunke, S., Bundrock, G., Hülse, S., Plümpe, T., Schaupp, F.
et al. (2005). Honeybees navigate according to a map-like
spatial memory. Proc. Natl. Acad. Sci. USA
102,3040
-3045.
Mittelstaedt, H. and Mittelstaedt, M. L. (1982). Homing by path integration. In Avian Navigation (ed. F. Papi and H. G. Wallraff), pp.290 -297. New York: Springer.
Müller, M. and Wehner, R. (1988). Path
integration in desert ants, Cataglyphis fortis. Proc. Natl. Acad.
Sci. USA 85,5287
-5290.
Neese, V. (1988). Die Entfernungsmessung der Sammelbiene: Ein energetisches und zugleich sensorisches Problem. In The Flying Honeybee; Aspects of Energetics, Biona Report 6 (ed. W. Nachtigall), pp. 1-15. New York, Stuttgart: Gustav Fischer.
Otto, F. (1959). Die Bedeutung des Rückfluges für die Richtungs- und Entfernungsangabe der Bienen. Z. vergl. Physiol. 42,303 -333.[CrossRef]
Riley, J. R., Greggers, U., Smith, A. D., Reynolds, D. R. and Menzel, R. (2005). The flight paths of honeybees recruited by the waggle dance. Nature 435,205 -207.[CrossRef][Medline]
Schmid-Hempel, P. (1984). Individually different foraging methods in the desert ant Cataglyphis bicolor (Hymenoptera, Formicidae). Behav. Ecol. Sociobiol. 14,263 -271.[CrossRef]
Scholze, E., Pichler, H. and Heran, H. (1964). Zur Entfernungsschätzung der Bienen nach dem Kraftaufwand. Naturwissenschaften 51,69 -70.[CrossRef]
Seeley, T. D. (1995). The Wisdom of the Hive. The Social Physiology of Honey Bee Colonies. Cambridge, MA: Harvard University Press.
Si, A., Srinivasan, M. A. and Zhang, S. (2003).
Honeybee navigation: properties of the visually driven `odometer'.
J. Exp. Biol. 206,1265
-1273.
Srinivasan, M. V., Zhang, S. W., Lehrer, M. and Collett, T.
S. (1996). Honeybee navigation en route to the goal:
visual flight control and odometry. J. Exp. Biol.
199,237
-244.
Srinivasan, M. V., Zhang, S. W. and Bidwell, N. J.
(1997). Visually mediated odometry in honeybees. J.
Exp. Biol. 200,2513
-2522.
Srinivasan, M. V., Zhang, S. W. and Lehrer, M. (1998). Honeybee navigation: odometry with monocular input. Anim. Behav. 56,1245 -1259.[CrossRef][Medline]
Srinivasan, M. V., Zhang, S., Altwein, M. and Tautz, J.
(2000). Honeybee navigation: nature and calibration of the
`odometer'. Science 287,851
-853.
Tautz, J., Rohrseitz, K. and Sandeman, D. C. (1996). One-strided waggle dance in bees. Nature 382,32 .[Medline]
Tautz, J., Zhang, S., Spaethe, J., Brockmann, A., Aung, S. and Srinivasan, M. V. (2004). Honeybee odometry: performance in varying natural terrain. PloS 2, doi: 10.1371/Journal.pbio.0020211.[CrossRef]
von Frisch, K. (1965). Tanzsprache und Orientierung der Bienen. Berlin, Heidelberg, New York: Springer. [English version: (1967). The Dance Language and Orientation of Bees. Cambridge, MA: The Belknap Press of Harvard University Press.]
von Frisch, K. and Jander, R. (1957). Über den Schwanzeltanz der Bienen. Z. vergl. Physiol. 4, 1-21.
Wehner, R. (1992). Arthropods. In Animal Homing (ed. F. Papi), pp.45 -144. London: Chapman and Hall.
Wehner, R. and Menzel, R. (1990). Do insects have cognitive maps? Annu. Rev. Neurosci. 13,403 -414.
Wehner, R. and Srinivasan, M. V. (1981). Searching behaviour of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J. Comp. Physiol. A 142,315 -338.
Wehner, R. and Srinivasan, M. (2003). Path integration in insects. In The Neurobiology of Spatial Behaviour (ed. K. J. Jeffery), pp. 9-30. Oxford: Oxford University Press.
Wehner, R., Michel, B. and Antosen, P. (1996). Visual navigation in insects: coupling of egocentric and geocentric information. J. Exp. Biol. 199,129 -140.
Wolf, H. and Wehner, R. (2000). Pinpointing food sources: olfactory and anemotactic orientation in desert ants, Cataglyphis fortis. J. Exp. Biol. 203,857 -868.
Zar, J. H. (1984). Biostatistical Analysis. Third edition. New Jersey: Prentice-Hall.
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