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First published online February 12, 2007
Journal of Experimental Biology 210, 845-853 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002089
Honeybee navigation: distance estimation in the third dimension
Centre for Excellence in Vision Science, Research School of Biological Sciences, Australian National University, PO Box 475, Canberra, ACT 2601, Australia
* Author for correspondence (e-mail: marie.dacke{at}anu.edu.au)
Accepted 4 January 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: odometer, distance estimation, honeybee, Apis mellifera, optic flow
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), which
consists of a series of alternating left-hand and right-hand loops,
interspersed by a segment in which the bee waggles her abdomen from side to
side. The length of this waggle run increases with the distance flown to reach
the food source, and the orientation of the waggle axis relative to gravity
specifies the azimuthal direction of the food source, relative to the
direction of the sun. The waggle dance also allows analysis of the bee's
internal representation of space, revealing that she is able to estimate how
far she has flown in her search for food.
A bee trained to fly around a building or a mountain ridge to reach a food
reward signals a direction pointing directly to the food source upon her
return, a direction that she has never actually flown
(von Frisch, 1967). The
direction of this novel shortcut is in part based on her experience of the
terrain (De Marco and Menzel,
2005), but the direction and distance to the food can also be
calculated using path integration, an internal process by which an animal
continuously integrates courses steered and distances travelled along the
route into a global vector (Collett, M. and
Collett, 2000; Collett, T. S.
and Collett, 2000; Wehner and
Srinivasan, 2003; Wehner et
al., 2002). Interestingly, bees flying a circuitous route around
an obstacle do not signal the distance of the shortcut, but rather the total
distance of the detour (von Frisch,
1967; De Marco and Menzel,
2005).
A relevant measurement of distance is important not only for returning to a
previously discovered food site but also for communicating the location of the
food source to other colony members. Bees gauge distance flown in terms of the
extent to which the image of the environment moves in the eye
(Esch and Burns, 1995;
Esch and Burns, 1996;
Si et al., 2003;
Srinivasan et al., 1996;
Srinivasan et al., 1997;
Srinivasan et al., 2000;
Esch et al., 2001). In other
words, the optic flow experienced by the eye (that is, the speed of motion of
the image of the environment) is integrated over time to obtain a distance
measurement. The nature of this visual odometer was unravelled by training
bees to fly to a feeder placed inside a short, narrow tunnel
(Srinivasan et al., 2000).
When bees returned to the hive from the tunnel, they indicated a highly
exaggerated distance to the feeder (
200 m), despite the fact that they
had only flown 6 m. This is because the total amount of image motion depends
upon the distances to the various objects that are passed; the closer the
objects, the larger the image motion perceived by the eye. The narrow tunnels
also permit close control of the flight path of the bee. So far, all
tunnel-based studies of the odometer have only investigated flight in the
horizontal plane (DeMarco and Menzel,
2005; Si et al.,
2003; Srinivasan et al.,
1996, Srinivasan et al.,
1997; Srinivasan et al.,
2000). In free-flight experiments, such as the detour experiments
described above, it is of course impossible to control the bees'
three-dimensional flight paths.
While honeybees indicate the distance and azimuthal direction in which to
fly to reach the food source, they do not appear to have a means of signalling
the height or elevational angle in their dances, at least as far as current
knowledge suggests (von Frisch,
1967). To our knowledge, very little is known about how honeybees
estimate distance travelled when they fly three-dimensional trajectories.
Earlier studies of bees feeding from elevated food sources suggest that bees
use the extent of image motion produced by the ground to estimate the distance
flown (Esch and Burns, 1995;
Esch and Burns, 1996). However,
in these studies, the image would have moved in the same direction in the eye
as during level flight (front to back in the ventral field). Thus, we have yet
to explore how the estimate of distance travelled is affected when the
direction of image motion changes within a given eye region. In the lateral
eye regions, for example, the image of the environment would move in the
front-to-back direction during horizontal flight and in the downward direction
during vertically upward flight.
Here we examine how bees measure distance travelled when they fly in three dimensions, by recording their dances after they are trained to fly along short, narrow tunnels arranged in various three-dimensional configurations. These experiments are supplemented by tests in which we examine the searching behaviour of bees that have been trained to find a reward at a specific position in a tunnel that is oriented vertically or horizontally. We also investigate the extent to which the orientation of the body of the flying bee is influenced by the inclination of the flight path, in order to gain a better knowledge of how the image of the environment moves past the eyes when a bee flies uphill or downhill or ascends a cliff.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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For each experiment, up to 30 individually marked bees were trained to fly to a feeder containing sugar solution placed 4 m or 6 m into the tunnel. The end of the tunnel was closed, so that bees could only enter or leave the tunnel through the near end. Dances performed by marked bees returning from the tunnel were filmed using a digital video camera and later analysed. In some experiments, the bees were also filmed while flying through the tunnel, by positioning a video camera to view them side-on through a 4.5 cm-diameter aperture in one of the side walls. These video images were then analysed to estimate the body orientation during various flight conditions.
Tunnel configurations
In the first series of experiments, the bees flew in a 6 m straight tunnel
that was oriented either (a) horizontally, (b) on a 48° slope or (c)
vertically. In (b) and (c), the bees entered from the top of the tunnel and
flew downward. In a second series of experiments, the first 2 m of the tunnel
was oriented vertically, and the subsequent 4 m horizontally, with the
entrance at the top of the vertical section. In one experiment, the
checkerboard pattern in the vertical section of the tunnel was replaced by an
axial stripe pattern. This was used to create a condition in which the optic
flow experienced by the bees in the first 2 m of the tunnel was very weak.
Data analysis
The walls of the observation hive were transparent, thus enabling the
viewing and filming of bee dances. A dance performed by a bee returning from
the tunnel typically consisted of a number of loops. Most of these loops
displayed a waggle component, whereas a few did not. The duration of the
waggle component and the percentage of waggle loops were measured for 50
dances under each experimental condition. The Student's t-test and
single-factor ANOVA were used to test for statistically significant
differences between the mean waggle durations under different flight
conditions.
The body orientations of bees in flight were calculated from the orientation of the long axis measured through a frame-by frame analysis of the side views from the video data. One frame per flight was analysed from 30 bees trained under each experimental condition. The Student's t-test was used to test for the statistical significance of any differences between the body orientations measured for flights in the horizontal, oblique and vertical tunnels.
Analysis of food searching behaviour
20 honeybees were trained to fly in a 3 m tunnel, with the same cross
section and visual texture as described above, to find a reward of sugar
solution placed 2 m into the tunnel. In the first experiment, a horizontal
tunnel was placed 3 m above the ground on a roof. The hive entrance was 1.25 m
above the ground. The horizontal distance from the hive to the entrance of the
tunnel was 4 m. In a second experiment, the tunnel entrance was kept in the
same position relative to the hive, but the tunnel was now oriented vertically
with the bees entering from the top and flying down. The feeder was suspended
2 m down the tunnel by means of a string. During training, the position of the
tunnel was frequently changed to prevent the bees from using external
landmarks to gauge their position in the tunnel. (This procedure was not
necessary in the first experiment, where bees viewed only the sky and no
external landmarks whilst flying in the tunnel.) After training, the bees were
tested one by one in an identical, fresh tunnel that carried no reward.
Data analysis
For the purpose of analysis, the test tunnel was subdivided into 30 units,
each 10 cm long. In their search for food, the bees typically flew back and
forth along the test tunnel, making a number of U-turns as they searched for
the missing reward. This searching behaviour was quantified by recording
visually the positions in the tunnel at which the bee made the first four
U-turns. By measuring the number of times the bee entered each unit during
these four turns, we could estimate the spatial distribution of its search
(for details, see Srinivasan et al.,
1997). For each test, the mean and standard deviation (s.d.) of
the search position were calculated from the mean of the positions of the four
U-turns measured for each bee. Student's t-tests were used to test
for the statistical significance of any differences between the search
positions in the two experiments, as well as the difference between the
expected and the experimentally measured search positions.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Esch et al., 2001;
Si et al., 2003). In these
earlier studies, the bees flew exclusively in horizontal tunnels.
Consequently, they experienced image motion that was oriented primarily in the
horizontal direction. The above experiments with the horizontal tunnel provide
a baseline against which to compare data obtained from flights in tunnels of
other orientations, described below.
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Abrupt changes in the direction of optic flow
In the experimental conditions given above, the bees experienced a more or
less constant direction of image motion throughout the length of their flight
tunnel. Will the direction of image motion influence the distance estimate if
it is drastically changed en route?
To test this, we used an L-shaped tunnel consisting of a 2 m vertical section followed by a 4 m horizontal section. The bees were trained to forage at a feeder placed initially 4 m and then 6 m into the tunnel. To reach the feeder at 6 m, the bees thus had to fly 2 m down the vertical section, change flight direction abruptly at the corner and then fly 4 m along the horizontal section. If the odometer treated image motion in the vertical and horizontal directions equally, we would expect the mean waggle duration with the feeder at 6 m to be similar to that for a 6 m flight in any of the other tunnel configurations described above. This is precisely what was observed. The mean waggle duration of 223 ms (644 loops) was not significantly different from those for flights to rewards 6 m into the horizontal, oblique or vertical tunnels (P>0.80). A 4 m flight into the L-shaped tunnel elicited dances with a mean waggle duration of 126 ms (591 loops), which was again not significantly different from that obtained after a 4 m flight into any of the other tunnels (P>0.11) (Fig. 1).
Is optic flow the primary cue for the visual odometer?
Is the amount of image motion experienced by the eye the primary cue to
gauge the distance flown to the reward? This was tested by replacing the
checkerboard pattern lining the vertical section of the L-shaped tunnel with
axial stripes. A bee flying through this tunnel would now experience very
little image motion in the first 2 m, since it flies in a direction parallel
to the stripes. Based on optic flow cues, a 6 m flight in this tunnel would
now effectively resemble a 4 m flight in a horizontal tunnel. This is also
what is observed. The mean waggle duration of 174 ms (577 loops) is
significantly different from that measured after a 6 m flight in the
horizontal tunnel (P<0.01, N=12, 16) but corresponds well
to the waggle duration after a 4 m flight in the same tunnel
(P>0.13) (Fig.
1).
The percentage of waggle loops in the dance
In an earlier study, Si et al. documented that dances observed after a
flight in a narrow tunnel are often somewhat different from those elicited
after free flights in open, natural terrain
(Si et al., 2003). In contrast
to dances following long flights outdoors, where almost every loop contains a
waggle, the bees returning from tunnels exhibit dances in which some loops do
not contain a waggle phase. The percentage of waggle-bearing loops after a
flight in an experimental tunnel was found to increase systematically with the
length of the tunnel (Si et al.,
2003). It was suggested by Si et al. that this difference in dance
behaviour reflects a conflict between the odometric signal derived from optic
flow in the tunnel and the `true' distance based on the bee's knowledge of the
environment external to the tunnel.
In line with earlier studies, the percentage of waggle loops in the bees'
dances increased when the feeder was moved from 4 m to 6 m for each of the
three differently oriented tunnels (horizontal, 22
82%; oblique,
3260%; vertical, 4573%) (Fig.
2), but none of the tunnel configurations systematically elicited
the largest or smallest fraction of waggle loops. From this we can conclude
that the percentage of waggle loops increases with increasing flight distance
in the tunnels but that the different orientations of the tunnels, and
consequently the different directions of optic flow, do not influence the
internal conflict between the odometric signal and the `true' distance in any
predictable way.
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; Nieh at el.,
2003).
Accuracy of food search in the vertical and the horizontal directions
The precision of the odometer can be estimated by measuring the accuracy
with which a bee is able to pinpoint the location of a food reward to which it
has been previously trained in the tunnel. Bees were trained to fly to a food
reward placed 2 m into a 3 m-long tunnel, lined with a checkerboard pattern,
and then tested by recording their searching behaviour in a fresh tunnel that
carried no reward, as described in Materials and methods. Two experiments were
performed. In one, bees were trained and subsequently tested in a horizontal
tunnel; in the other, bees were trained and tested in a vertical tunnel.
The results are shown in Fig. 3. The mean search position in the horizontal tunnel (at 18.3±3.8 units) was not significantly different from that in the vertical tunnel (at 18.3±4.3 units) (P>0.81), and neither of these two search positions was significantly different from the position of the reward (at 19.5 units) during training (horizontal, P>0.76; vertical, P>0.71). Furthermore, both searching distributions exhibit a similar width: the widths at half height are 7 units and 10 units for the horizontal and vertical tunnels, respectively. This finding lends further support to our conclusion that the ability to gauge the distance to the food is independent of the orientation of the tunnel. The slightly broader peak of the search distribution in the vertical tunnel may arise from the fact that vertically downward flight is less common than horizontal flight and from the possible reluctance of bees to enter and fly down the vertical tunnel.
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10° from the body orientation of
19.5±8.4° measured in horizontal flight. Interestingly, whilst
flying down the 48° slope in the oblique tunnel, the body was inclined at
an angle of 3.3±9.3° below the horizontal
(Fig. 4). Although the mean
body orientations of bees flying in the differently oriented tunnels differ
significantly from each other (P<0.001, N=26, 19, 23),
these differences are not large: they never exceed a maximum of 23°. Our
video films do not permit measurement of the orientation of the bee's head
relative to the long axis of the body. Nevertheless, it would be safe to
conclude that the bee is physically unable to tilt its head as much as would
be required to experience a consistent direction of optic flow over the eye
under the different experimental conditions.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Esch and Burns, 1996;
Esch et al., 1994;
Esch et al., 2001;
Si et al., 2003;
Srinivasan et al., 1996;
Srinivasan et al., 1997;
Srinivasan et al., 2000). When
the checkerboard pattern lining the 2 m vertical section of a 6 m-long
L-shaped tunnel is replaced by axial stripes, the distance estimate changes
from 6 m to 4 m (Fig. 1). This
is consistent with what one would expect on the basis of optic flow cues.
Given the weak image motion cues in the 2 m vertical section, the visual
odometer does not start to run until the bee enters the 4 m section lined with
checkerboard pattern. The slightly longer distance estimate in the L-shaped
tunnel, compared to the 4 m horizontal, vertical and oblique tunnels, is to be
expected, as the weak motion cues in the axial striped section are probably
sufficient to provide some drive to the sensitive odometer
(Si et al., 2003). Optic flow
cues could have been picked up from small imperfections in the axial pattern,
from stray shadows or from the insect mesh.
Tunnel flights versus outdoor flights
The narrow tunnels used in the present study are known to magnify the
perception of distance flown by a factor of 31 compared to flights in natural
terrain (Srinivasan et al.,
2000). A 6 m flight in the horizontal tunnel is thus equivalent to
a 186 m flight outdoors. The flight in the vertical tunnel corresponds to a
flight of 174 m down into the earth. This effectively means that the two
tunnels simulated flights to food sources that were more than 200 m apart, but
the bees conveyed roughly similar distance estimates upon their return to the
hive. The 4 m horizontal projection of the 6 m oblique tunnel would translate
to a horizontal flight of 124 m in natural terrain, but the bee indicated 194
m to the food source, a distance comparable to those obtained from the 6 m
horizontal and vertical tunnels. It is fair to ask how these odometer readings
can be biologically relevant, either to the experienced bee or to the
recruit.
Odometry is scene dependent
The honeybee odometer does not run at a constant rate: rather, the rate
depends upon the properties of the terrain
(Barron et al., 2005;
Esch et al., 2001;
Tautz et al., 2004). The
odometer runs faster in an environment that presents a high contrast and rich
texture and runs slower in terrain with low contrast and poor texture.
Consequently, equally long flights in forests and over open water will
generate different distance estimates. Our findings suggest that every detour
over or around objects in a terrain rich in visual texture will contribute to
a longer distance estimate.
The successful use of a scene-dependent odometer relies on the fact that a
honeybee follows a fixed route each time it flies to its destination
(Collett, 1996). A recent study
using harmonic radar (Riley et al.,
2005) confirms that the recruited bees fly in the direction that
the scout bee signals in her dance. Both the experienced bee and the novice
will thus experience the same terrain, and therefore the same optic flow cues,
on their way to the food source. This applies not only to outdoor flights in
natural terrain but also to flights in short, narrow tunnels. Thus, a
`subjective' distance estimate would be just as useful as an absolute one for
indicating how far a bee should fly to find the food.
Odometry and path integration
Our findings reveal that the honeybee's odometer gauges distance flown by
continuously integrating the apparent motion of the visual panorama in the
eye, regardless of the direction in which this motion occurs. Analysis of body
orientation during flight suggests that the direction in which the image moves
across the eye is very different for flights in the horizontal, oblique and
vertical tunnels. Thus, at least as far as the waggle dance is concerned, bees
do not signal the vector distance to the food source: rather, they signal the
total length of the path that they have flown to reach it. How does this
measure of total path length help a bee determine its location relative to the
hive?
True path integration involves the use of a compass (to obtain estimates of
instantaneous heading direction) and an odometer (to measure travel distance)
(Collett, M. and Collett, 2000;
Collett, T. S. and Collett,
2000; Dyer, 1998;
Wehner and Srinvasan, 2003; Wehner et al.,
2002). By keeping a continuous record of heading direction and
distance travelled during its journey, an animal can, at least in principle,
maintain a continuously updated estimate of where it is in relation to its
starting point. In effect, a tortuous route is approximated by a sequence of
short vectors along the path, which are summed vectorially to obtain a goal
vector that indicates the distance and direction of the animal's current
position relative to its starting point. We shall call this process
`vector-based path integration'.
If a bee that flies repeatedly to a food site is able to eventually
navigate a direct, straight route to it, then it indicates in its waggle dance
a direction that corresponds to the direction of the food source and a
distance that is indicative of the optic flow that is experienced along this
direct route. This is as one would expect from vector-based path integration.
On the other hand, when a bee is forced to fly through a detour in the
vertical plane, as in this study, it signals the correct azimuthal direction
to the feeder from the hive but not the vector (shortcut) distance; rather, it
indicates the total length of the path taken to the food. (With a detour in
the vertical plane the azimuthal direction of the flight path remains
unaffected, as one might expect.) A similar disconnection between distance and
direction is observed when bees make detours in the horizontal plane
(von Frisch, 1967). When a bee
is forced to fly around an obstacle (such as a tall hill or building) to reach
a food source (von Frisch,
1967), she indicates the true azimuthal bearing of the destination
and the total length of the detour path rather than the vector (shortcut)
distance. Considered together, these findings suggest that whenever bees are
forced to make a detour (either in the horizontal plane or the vertical
plane), they signal in their dances (a) the azimuthal direction to the food
and (b) the total path length to the food.
The observation that bees traversing a detour in the horizontal plane indicate the correct direction of the food source (the direction `as the crow flies') implies that this direction is estimated through the use of a vector-based path-integration system – the direction of the goal vector cannot be computed correctly otherwise. On the other hand, the finding that these bees do not signal the shortcut distance (the distance as the crow flies), but rather the total path length, implies that this distance is estimated by a scalar-based path-integration system. It would appear, therefore, that, in general, bees possess two different path-integration systems that operate concurrently during the journey: a vector-based path-integration system keeps track of direction, and a scalar-based path-integration system registers the total path length. The reason for this type of representation is unclear at the moment and requires further investigation.
Specifying distance in this way may, however, be computationally advantageous in some situations. When the path to a food source is a detour, but is tightly constrained (as when flying around an obstacle in the horizontal plane, or through an L-shaped tunnel in the vertical plane), the direction signal in the dance would specify the true azimuthal direction of the goal, while the distance signal would indicate the total distance that the bee has to fly along this constrained route to reach the goal. A recruit would then simply have to use the directional signal as an indication of the general direction to the food and fly along this constrained route until its odometer has registered the appropriate path length. On the other hand, if the route to the goal is unconstrained, then the path to the food would be a straight line and the dance would correctly signal the odometric distance along this line. Thus, such a scheme would work for constrained as well as unconstrained routes.
Let us now turn specifically to flight paths that include movement in the
vertical plane. If we assume that the dance contains no indication of the
altitude of the food source relative to the hive (as the evidence so far seems
to indicate), then all that is conveyed to the recruit is (a) the azimuthal
direction of the goal (the elevational angle is unspecified) and (b) some
measure of the distance to be flown along this direction, presumably along a
straight line. An outdoor experiment, conducted about 40 years ago
(von Frisch, 1967), suggests
how information of this kind might help recruits locate an elevated food
source.
Von Frisch and his student set up an observation hive on the wall of a cliff and trained the bees to a feeder suspended 53 m directly above the hive. In their dances, the bees indicated a direction directly into the cliff face. Unable to fly in this direction, the recruits flew up the wall instead, presumably facing the wall throughout the flight. The distance estimation given in the dance was unfortunately not measured in these experiments, but in the light of our findings we would expect the bees to have signalled the correct distance to reach the elevated feeder. The fact that the dancing bees were signalling a clear direction indicates that they were performing a waggle dance even when the food source was only 53 m away from the hive, probably because of the strong optic flow cues that would have been generated by flying upwards close to the wall of the cliff. A longer distance estimate, with the same directional component, would presumably have guided the recruits over the cliff to a food source on the plateau.
Esch and Burns (Esch and Burns,
1996) trained one group of bees to forage from a feeder on the
ground, 158 m from the hive. A second group of bees was also trained to a
feeder 158 m from the hive, but now located on top of a 50 m-high building 150
m from the hive. Both groups of bees signalled the same distance upon their
return to the hive. The foragers' route was not observed during this
experiment, but a path to the base of the building and then to the roof (i.e.
along the route they had been trained) was put forward as a possibility to
explain these results. Based on our observations of bees foraging in the
L-shaped tunnel, where the distance estimates in the horizontal and vertical
sections are simply summed, a flight to the base of the building and then up
to the roof would imply a total path length of 200 m, which is considerably
larger than the distance that was actually signalled in the dances. We
therefore suggest that the bees were flying a direct, 158 m route to the
feeder and reporting the optic flow that they had experienced en
route. When flying up and towards the building, the ventral visual field
would have experienced progressively weaker optic flow from the ground as the
bee gained altitude, but this loss would have been compensated to some extent
by the increasing optic flow in the frontal field as the wall was approached,
as well as by optic flow signals that could have been provided by structures
such as trees and buildings in the lateral visual fields. That bees tend to
fly a straight line to elevated food sources, whenever this is possible, is
also suggested by the famous balloon experiment of Esch and Burns
(Esch and Burns, 1996). Their
experienced bees were observed to fly a more-or-less straight path to a feeder
suspended from a helium balloon 90 m above the ground and 70 m from the
hive.
Our experiments reveal that when bees fly routes that involve a horizontal
as well as a vertical component of movement, they do not signal the vector
distance to the food source: rather, they signal the total length of the path
that they have flown to reach it. The situation appears to be somewhat
different, however, from the desert ant Cataglyphis. These ants are
renowned for their ability to perform large-scale foraging excursions in
rather featureless surroundings and to navigate back to their nest by using
path integration (Wehner and Wehner,
1990). Ants trained to move along a series of uphill and downhill
channels, and later tested on flat terrain, indicate homing distances
corresponding to the distance traversed in the horizontal plane rather than
the distance actually travelled along their undulating path
(Wohlgemuth et al., 2001;
Wohlgemuth et al., 2002).
Similar results were also obtained in experiments that used more complicated
three-dimensional mazes (Grah at al.,
2005). In order to estimate the horizontal distance that it
traverses, the desert ant must be able to continuously measure the local slope
of the terrain and factor this information into its odometric
computations.
With the desert ant, it would be advantageous to measure distances in the
horizontal plane because this measure preserves the relative positions of
locations irrespective of the undulations of the terrain
(Grah et al., 2005;
Wohlgemuth et al., 2001;
Wohlgemuth et al., 2002). This
scheme works because the ant is earthbound and all locations of interest are
located on the ground, irrespective of local height. This is not the case with
a flying forager, such as the honeybee, which moves in three dimensions and
where food sources can occur at arbitrary heights above the ground. Here, it
would seem advantageous to specify the position of the food source as a vector
in three dimensions. However, at least as far as current knowledge suggests,
honeybees do not appear to have a means of signalling the third dimension
(height or elevational angle) in their dances. Given this, the next best thing
would be to signal some measure of the total length of the path to the food
source. In the case of von Frisch's cliff experiment, described above, the
indication of a definite distance and direction would drive the recruits to
fly up the wall until they have experienced the optic flow that is specified
by the waggle dance. Clearly, a scheme of this sort will not always work
adequately. In the case of an inflorescence on the crown of a tall tree, for
example, such a scheme would work only if bees have some standard `rules' by
which they negotiate environments and obstacles of various kinds. For example,
if foraging for flowers in a forest canopy requires, as a standard procedure,
that bees first fly vertically upwards to a height above the canopy and then
horizontally in the appropriate direction under the open sky, then a dance
that conveys directional information and total optic flow along such a path
would enable the recruit to find the goal.
There is evidence that stingless bees (Meliponae) are able to
communicate the three-dimensional position of a food source to their nestmates
(Nieh and Roubik, 1998;
Nieh et al., 2003). The
mechanisms by which they do this are not yet clear, although it is suspected
that acoustic signals may be involved
(Nieh and Roubik, 1998). While
visual inspection of honeybee dances has yielded no evidence so far of any
signalling of the third dimension, it would be of interest to analyse their
dances acoustically for the possible existence of such information. Pheromone
trails, if present along such routes, could ensure that the same paths are
followed by the scout forager and the recruits, thus making the distance
signals useful. In this context, it would be of interest to investigate where
the recruits from the bees trained in the 6 m vertical tunnel search for the
advertised food source and to examine, in particular, whether they search
outdoors at a horizontal distance of 174 m from the hive or whether they fly
vertically down the tunnel and search at a location 6 m below the tunnel
entrance.
Neural substrates for visual odometry
A major challenge is to uncover the neural basis of the honeybee's visual
odometer. Our finding that the image motion that is experienced by the eye is
incorporated into the odometric calculation irrespective of the direction in
which this motion occurs is reminiscent of the way in which peering locusts
use cues based on non-directional image motion to estimate the distance to a
target onto which they subsequently leap
(Sobel, 1990) or flying
honeybees use such cues to avoid obstacles or negotiate narrow gaps
(Srinivasan et al., 1993;
Srinivasan and Zhang, 1997).
In neural terms, non-directional motion detection could be performed by
appropriately processing the responses of the large-field, directionally
selective motion-detecting neurons in the lobula plate/lobula region of the
insect visual pathway (e.g. Hausen,
1993). Summing the responses of four broadly tuned motion
detectors with leftward, rightward, upward and downward preferred directions
would yield a non-directional, motion-sensitive response. Alternatively, the
summation could be performed at the level of small-field directional motion
detectors, as appears to be the case with the retinotopic, non-directional T4
cells in the lobula plate of the fly
(Douglass and Strausfeld,
1996).
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