Look and turn: landmark-based goal navigation in honey bees
1 Institute of Neuroinformatics, ETH/University of Zürich
2 Institute of Zoology, University of Zürich, Winterthurerstrasse 190,
CH-8057 Zürich, Switzerland
* Author for correspondence (e-mail: steven{at}ini.phys.ethz.ch)
Accepted 11 August 2005
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Summary |
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Key words: honey bee, Apis mellifera, behavior, flight, vision, landmark
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Introduction |
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Though image matching is widely accepted to underlie goal-directed piloting
behavior in bees, a direct verification of the predictions made by the model
has been precluded by the technical limitations related to a precise and
detailed measurement of flight paths extending beyond the immediate goal
location. Such analyses have become possible through the use of pan-tilt
cameras and appropriate software, which allows the observation area to be
extended several fold without significant loss of spatial detail
(Fry et al., 2000; reviewed by
Reynolds and Riley, 2002
). We
applied this technique in a conceptual bottom-up approach to explore
navigational mechanisms in highly defined goal-seeking tasks. Bees entered a
large uniform flight, in which one or a pair of landmarks provided prominent
visual cues for locating an inconspicuous target associated with a food
reward. We acquired the flight paths under standard conditions and in
occasional tests with modified landmark positions. In separate experiments, we
varied the position, number and appearance of the landmarks for a systematic
analysis of the resulting flight paths toward the goal. The results of our
experiments show that honey bees combine beacon navigation and an intricate
motor behavior for a robust and flexible navigation strategy. A simple
rule-based model is able to explain the structure of approach flights measured
in various landmark settings, ranging from search-like flight behavior in the
absence of a suitable landmark to highly stereotyped, direct approach flights
in the presence of a landmark close to or behind the goal. Furthermore, our
model is consistent with the gradual effect of operant learning observed
during training.
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Materials and methods |
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Training and testing procedures
Bees were trained using the standard procedures described by von Frisch
(1967). A small group of bees
was recruited from a permanent feeding station installed on the balcony
outside the laboratory and guided into the laboratory-based flight tent by
stepwise displacement of a feeder that contained highly concentrated sucrose
solution. Inside the tent, the artificial landmarks were present in the final
training situation, and the food hole was marked with a conspicuous yellow
paper ring. During this phase of training, the bees took off from the
temporary feeder, where they were observed to perform short learning flights
(`turn-back-and-look': Lehrer,
1991
,
1993
;
Lehrer and Bianco, 2000
), and
were manually released from the tent. Next, the bees were trained to enter the
feeder box through the food hole and to exit it through the Plexiglas tube. In
the course of the subsequent training phase, the bees were marked individually
with pigmented shellac solution, and the marker around the food hole was
reduced in size until it became visible to the bees only in the close vicinity
of the food hole.
We typically began our measurements of flight paths from the third day of training, when the bees showed a consistent flight behavior. In most cases, we filmed the bees' approach flights without altering the experimental conditions. In some tests, we covered the food hole with an inconspicuous disc attached to a thread. After a trained bee had searched for a few seconds, we drew the disc away to give the bee access to the food hole. Covering the food hole had no noticeable effect on the bees' approach flights, indicating that it was not used as a cue until the bees were close to it.
Data acquisition and analysis
In a first series of experiments, we filmed the bees using a standard video
camera (Panasonic F-10; f=10.5 mm, equipped with a 7x
wide-angle converter) and recorded the data on video tape. We used custom
software based on LabView (National Instruments, Austin, TX, USA) in order to
extract the 2-D position of the bee measured at intervals of 1/50 s. We later
performed our measurement using Trackit 2D (BIOBSERVE GmbH, Bonn, Germany)
equipped with a Sony LSX-PT1 pan-tilt camera (Fry et al.,
1998,
2000
). Using this system, we
were able to automatically acquire the position and the orientation of the
bee's body axis at 50 Hz in 2-D coordinates. Parallax errors resulting from
the bees' changes in flight altitude were insignificant due to the elevated
position of the camera.
Analysis of the flight data was performed using custom programs developed in Matlab (R14, The Mathworks, Inc., Natick, MA, USA). During the approach flights, the bees typically flew at a velocity above 0.5 m s1, except for a brief period just after take-off and before landing or searching. At the elevated speeds observed, the bee's body axis was closely aligned with the flight direction, as confirmed by Trackit 2D measurements (Fig. 4). For reasons of consistency and simplicity, we therefore inferred the body axis direction from the measured flight direction. On the basis of these data, and further assuming that the bee's head does not move significantly with respect to the body, the azimuthal retinal landmark positions can be determined. Portions of the flights during which the speed was below 0.5 m s1 were excluded from the analyses, because during these parts the bees' body axis might have deviated from the flight direction. For the largest part of the data, our recording method provides a robust and sufficiently precise way of measuring retinal landmark position within the context of the present experiments.
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Results |
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Flight duration continually decreased with increasing experience from about
10 s to a stable plateau at around 2 s from the 50th flight onward (red trace
in Fig. 2B). The flight speeds
of experienced bees reached up to 1.2 m s1.
The large number of repetitions required before an effective approach behavior is learned indicates a possible role of operant conditioning. To be considered biologically relevant, a model for a landmark-based goal navigation should therefore be consistent with the observed gradual increase of performance over time.
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Beacon navigation provides a basis for motor learning
For a detailed analysis of the piloting mechanisms, we trained four bees in
the same task, measured their approach paths to the food hole
(Fig. 5AiDi) and
calculated the retinal coordinates of the landmark as perceived by the bees
during their approaches (Fig.
5AiiDii). The food hole was covered briefly so as to allow
us to measure the location of the bee's search paths (red dot in
Fig. 5AiDi). Each bee
approached the food hole in a typical, highly stereotyped flight pattern. In
one case, a bee approached the landmark with exceedingly straight flight paths
and searched precisely over the location of the covered food hole
(Fig. 5Ai), while it kept the
landmark continually within a narrow range of about ±30° of its
frontal (0°) direction of view (Fig.
5Aii). Two other individuals exhibited flights that were slightly
biased to one side, leading to a skewed distribution of the azimuthal
positions of the landmarks (Fig.
5B,C). Finally, in 30 out of 41 cases (73%), one bee approached
the food hole in a slightly curved path but occasionally performed a small
clockwise loop just after take-off or a much wider anti-clockwise loop at a
slightly later stage of its flight (Fig.
5Di). In the latter case, the bee deviated far to the left and
then approached the landmark from various directions along a straight path.
The lopsided distribution of retinal positions resembles those of the two
previous examples, except for a plateau extending over the entire visual
field, due to the 360° loops (compare
Fig. 5D with
Fig. 5B,C). On the one hand,
the bees showed a common tendency to fixate the landmark with the near-frontal
retina, and hence treated it as a beacon. On the other hand, the stereotyped
approach flights of individual bees indicate a probabilistic learning scheme,
such as operant conditioning of visuo-motor patterns.
Beacon navigation is combined with biased detours
Having established basic principles for the use of a single landmark
located directly behind the goal and thus in front of the approaching bee, we
performed similar analyses with bees trained with a black cylinder (height and
diameter, 25 cm) placed to the side of the food hole. In one experiment, we
trained a bee with the cylinder located at an angular distance of 15° from
the food hole, as seen from the bee's starting position (position 2 in the
inset of Fig. 1;
Fig. 6Ai). The bee did not
approach the food hole directly but instead headed in the direction of the
cylinder. As it did so, it occasionally performed detours toward the side of
the food hole. Near the cylinder, the bee consistently turned left and
searched at the location of the covered food hole
(Fig. 6Ai). The distribution of
the azimuthal retinal positions of the landmark peaks around 0° and is
skewed toward the right visual field. The results are well explained with a
combination of beacon navigation and biased detours in the direction of the
goal, similar to the previous results. Hypothetically, the bee could have
relied on alternative strategies to solve the task. First, the bees could have
fixated the landmark at a retinal position of 49.6° for a curved approach
in the form of a logarithmic spiral. Second, the bees could have approached
the hole more directly by relying on image matching of sequentially recalled
snapshot memories (Judd and Collett,
1998; Collett et al.,
1998
). Neither alternative is supported by our data.
We then trained and tested three more bees with the cylinder positioned 40° to the side of the food hole (position 4 in Fig. 1; Fig. 6BDi). In this situation, beacon navigation should be detrimental for rapid approach flights, and, indeed, the bees' flights were no longer headed toward the cylinder. Furthermore, the flight paths no longer showed the stereotyped structure observed in previous experiments. Nonetheless, the flights share in common that the cylinder's image was consistently placed within the right visual field. A simple visuo-motor strategy could account for this observation. The bees could have kept to the left side of the landmark by responding to right-to-left motion of the landmark with a strong corrective turning maneuver toward the left. They could still have been drawn toward the cylinder by responding to left-to-right motion of the cylinder with (a much weaker) corrective maneuver toward the right. This simple look-and-turn strategy would effectively restrict a bee's flight behavior to leftward turns and anti-clockwise loops, bringing the bee successively closer to its desired goal. This model is described in more detail in the Discussion (also see Fig. 9).
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Representative examples of approach flights from seven bees are shown in Fig. 7Ai. The bees tended to approach the food hole in a more or less direct path. Only occasionally did they approach one of the cylinders (e.g. the red trace in Fig. 7Ai). Fairly direct approaches toward the goal are documented in Fig. 7Bi (see azimuthal retinal positions of the right and left cylinders in red and black in Fig. 7Bii, respectively). This result would again be consistent with a simple visuo-motor strategy. The bees could have reacted to right-to-left motion of the landmarks with a strong leftward turning response, as in the previous experiment (see above), but with an equally strong rightward turning response to perceived left-to-right motion. As a result, the bees would be `trapped' between the cylinders and would approach the food hole in a more or less direct approach, as was observed. However, the bees' behavior could also be explained by a successive matching-to-memory strategy. Therefore, we conducted additional tests in which one of the two cylinders was removed. According to the above-mentioned visuo-motor strategy, the bees were now expected to approach the remaining cylinder by fixating it with their frontal retina. By contrast, an image-matching strategy would place the cylinder in a lateral retinal position, so that the bees should fly in a wide arc around the remaining cylinder. The bees indeed approached the remaining cylinder (Fig. 7Ci,Di) and hence behaved as predicted from our previous results.
Navigational strategies with two differently colored landmarks
Taking the stance of devil's advocate, the relevance of the previous
results with two identical landmarks might appear questionable, given that
under more natural conditions bees might use additional cues, such as shape,
color or texture, to distinguish between landmarks. We therefore trained bees
under the same conditions as in the previous experiment, except that the right
and left cylinder were wrapped in green and blue paper, respectively
(Fig. 8Ai). Approach flights of
two bees tested in the training configuration revealed that the bees used the
green cylinder as a beacon, apparently ignoring the blue cylinder (red and
black traces in Fig. 8Ai,ii).
The retinal azimuth of the green landmark peaks around 0° and is strongly
skewed toward the right visual field, strikingly similar to the data obtained
from a single, lateral cylinder (compare green distribution in
Fig. 8Aiii with
Fig. 6Aii). This result is
again in conflict with image matching, which predicts a straight approach path
(Möller, 2001),
irrespective of whether or not color information was used. Given the above
evidence, we predicted that if the colored landmarks were exchanged during
tests, the bees should approach the green cylinder in the new position and
hence deviate far away from their habitual flight path, not unlike in earlier
experiments with a displaced single landmark
(Fig. 3). This was indeed the
case. The bees flew left toward the green landmark and even performed their
habitual left turns, after which they turned back and successfully located the
food hole (Fig. 8Bi). The
median approach flights reveal that after heading in the habitual direction
for a short distance (similar to the flights shown in
Fig. 3), the bees steered
toward the green landmark in its new position
(Fig. 8Bii). During the
approach, the green landmark was kept in a near frontal position, whereas the
blue cylinder now appeared far out in the right visual field
(Fig. 8Biii). Interestingly,
the distribution of the green cylinder was skewed toward the right visual
field under standard conditions and toward the left visual field when the
cylinders were interchanged (Fig.
8Biii). Possibly, the blue landmark was not completely ignored,
but the turning responses weighted far lower than in the case of the green
cylinder. How the bees managed to locate the food hole after having been
brought off-course must remain speculative. A possible explanation is
dead-reckoning, assuming that a path integrator was registering the bees'
deviation to a novel location (Chittka et
al., 1995
). Alternatively, the bees could have applied some form
of landmark guidance that did not depend on the landmarks' spectral
properties.
In conclusion, the results obtained with two differently colored landmarks provide further evidence in favor of a simple visuo-motor control loop underlying approach flights toward a goal. The precise visual processing mechanisms underlying the observed behavior remain unknown, but future experiments based on our experiments could further insights into the underlying neural processing mechanisms. For example, a compelling experiment would be to repeat our experiments with landmarks that do not provide luminance contrast to the (color-blind) motion processing pathways to explore their involvement in the given task.
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Discussion |
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Look-and-turn: goal navigation from visuo-motor control loops
Our results are well explained with a simple rule-based model based on
visuo-motor control loops. In the absence of landmarks, the bees performed
unstructured search flights covering a broad area (data not shown). In
presence of a landmark, the bees tended to fixate it with their frontal
retina, and hence treated it as a beacon. Beacon navigation appears to be a
strong, innate disposition of bees, which have been observed to approach novel
landmarks spontaneously (von Frisch,
1967; Frank Bartlett, personal communication). Relying on a beacon
near a food site allows newly recruited bees to approach it with a consistent
flight pattern, which is reinforced during successive foraging trips
(Fig. 2). Even under ideal
conditions, reinforcement learning reaches a stable plateau only after
50
flights. As a result, experienced bees are able to approach the goal fast,
reliably and along consistent routes. This behavior is likely to support
foraging efficiency and to avoid the risk of predation.
If a landmark is present at or behind the goal, the bee can fixate it with
its frontal retina for a direct approach of the goal. Frontal fixation implies
compensatory turning maneuvers, whenever the landmark moves toward the lateral
visual field (Fig. 9A). Biased
turning could be achieved likewise, but with an asymmetrical weighting of the
compensatory maneuvers. For example, in the experiments with a single cylinder
placed to the right side of the food hole
(Fig. 6), the bees' turning
behavior was strongly biased. Such behavior could be generated from a strong
compensatory reaction to a leftward moving landmark, combined with a much
weaker compensatory reaction to a rightward moving landmark
(Fig. 9B). As a result, the bee
would tend to fixate the landmark frontally but would also make occasional
left turns. The final turning toward the food hole after the bees have arrived
close to the cylinder is likely to be part of a collision avoidance response
to a looming stimulus, similar to the behavior recorded in flies
(Tammero and Dickinson, 2002).
The same scheme holds for the experiments with two black cylinders
(Fig. 7). In the standard
configuration, symmetric compensatory reactions would cause the bees to
approach the food hole directly. When one cylinder was removed experimentally,
the bees fixated the remaining cylinder with their frontal retina
(Fig. 9C). Finally, when
trained with two differently colored cylinders, the bees performed
asymmetrical compensatory maneuvers for one of them (green arrows in
Fig. 9D) and did not react
noticeably to the other cylinder (blue arrows in
Fig. 9D). Consequently, the
bees approached one cylinder directly, irrespective of its relative position
to the other cylinder. Our experiments therefore suggest that the bees form
visuo-motor associations only with respect to one out of several
distinguishable landmarks. It remains to be tested whether our model applies
likewise in a different set of circumstances, such as when there is a richer
or more natural visual surround.
Relevance for natural foraging behavior
For the benefit of experimental control, we performed our experiments under
extremely restrictive sensory conditions. Hence, the question arises as to
whether our results are likely to represent naturally occurring visuo-motor
responses under more complex environmental conditions. Honey bees have indeed
been reported to use prominent single landmarks in the field as beacons
(von Frisch, 1967;
Collett and Baron, 1994
;
Chittka et al., 1995
).
Compelling similarities exist between our data and previous analyses performed
in ants. Wood ants traveling between a learned food site and the nest use
prominent landmarks as beacons for a direct approach
(Nicholson et al., 1999
;
Collett and Collett, 2002
).
Biased detours (Collett et al.,
1992
) and idiosyncratic foraging paths
(Wehner, 2003
;
Kohler and Wehner, 2005
) are
described for desert ants. In summary, the flexible combination of basic
navigational strategies could represent a widespread feature at least in
central place foraging insects.
Putative role of image matching
Goal-approaching honey bees appear not to apply image matching in the form
originally proposed by Cartwright and Collett
(1983). The strongest evidence
against the use of a `snapshot' memory comes from the experiments in which we
trained bees with a pair of black (Fig.
7) or colored (Fig.
8) cylinders and tested them with one cylinder removed. The bees
fixated the remaining landmark with the frontal retina
(Fig. 7C,D) and not at the
positions predicted from a snapshot strategy. Furthermore, an image-matching
strategy would predict a direct goal approach in the case of the symmetric
array of colored cylinders (fig. 3a in
Möller, 2001
), but the
bees instead relied on a single cylinder for an indirect approach of the goal
(Fig. 8D).
It is interesting to ask if the behavior we observed in our experiments is
consistent with recent modeling approaches. Unfortunately, most simulations
were performed with landmark configurations consisting of at least three
landmarks (Franz et al., 1998;
Nicholson et al., 1999
;
Möller, 2000
;
Lambrinos et al., 2000
). One
study did, however, apply a variant form of the `snapshot' model (`partial
image matching model'; fig. 7a in
Möller, 2001
) by using a
symmetrically paired landmark configuration, comparable to the one used in the
present account (Fig. 7). As
this model at any particular time matches a single landmark, the resulting
path toward the goal is curved rather than direct, and hence is reminiscent of
beacon navigation. However, in the presence of two black cylinders, the bees'
approach paths were generally oriented toward the food hole rather than toward
one of the landmarks.
Although snapshot matching can provide a viable navigation strategy, as
demonstrated in numerous numeric (e.g.
Cartwright and Collett, 1983;
Nicholson et al., 1999
;
Möller, 2001
) and robotic
simulations (e.g. Franz et al.,
1998
; Möller,
2000
; Lambrinos et al.,
2000
), its feasibility for free-flight control remains to be
demonstrated. In particular, it is questionable whether an image-matching
mechanism could meet the exceedingly high demands of visuo-motor flight
control in terms of robustness and speed (e.g. 30 ms in mate-chasing
houseflies; Land and Collett,
1974
). Whereas snapshot memories are evidently important in a
large number of visual tasks (reviewed by
Menzel et al., 1996
; Collett
and Collett, 2002
,
2004
;
Wehner, 2003
), the flight
paths of honey bees approaching their goal seem to be based on simple
visuo-motor control strategies that provide flexibility, robustness and
speed.
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Acknowledgments |
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