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First published online October 7, 2008
Journal of Experimental Biology 211, 3281-3286 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.021022
Two odometers in honeybees?
1 ARC Centre for Excellence in Vision Science, Queensland Brain Institute,
University of Queensland, St Lucia, QLD 4072, Australia
2 Research School of Biological Sciences, Australian National University,
Canberra, ACT 2601, Australia
Author for correspondence (e-mail:
marie.dacke{at}cob.lu.se)
Accepted 28 August 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: odometer, celestial compass, path integration, honeybee, Apis mellifera
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Chittka and Kunze, 1995). After
returning to the hive, these bees communicate to their nest mates the distance
and direction in which to fly to reach this food source. The information is
encoded in the waggle dance (von Frisch,
1967), which consists of a series of alternating clockwise and
anti-clockwise loops, interspersed by a phase in which the bee waggles her
abdomen from side to side. The length of this waggle run signals the distance
flown and the orientation of the waggle axis relative to gravity signals the
azimuthal direction of the food source, relative to the direction of the sun
(von Frisch, 1967). Thus the
waggle dance not only enables the forager to convey important information
about the location of an attractive food site to her nestmates, but also
allows the experimenter to probe the bee's internal representation of
space.
After the waggle dance, the foraging bee will set out again for the very
same food source, only a few minutes later. The ability to navigate back and
forth between the food source and the hive is partly based on the knowledge of
familiar terrain (De Marco and Menzel,
2005), but also partly on a path integrator, which performs an
approximate form of dead reckoning (Collett
and Collett, 2000; Wehner and
Labhart, 2006; Wehner and
Srinivasan, 2003; Wehner and
Wehner, 1990). To perform path integration, an animal would need
two types of information: (1) directional information with reference to an
external compass cue and (2) information about the distance travelled in a
particular direction (Müller and
Wehner, 1988; Wehner,
1994). It is well established that bees estimate the distance
flown by measuring the optic flow perceived during flight
(Dacke and Srinivasan, 2007;
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). The cues
involved for the assessment of travel direction are however less clear, but
celestial cues are likely to play a major role. When given a view of the sky
– or a beam of artificially polarized light – a dancing bee will
momentarily orient its dance to the orientation of this compass cue
(Rossel and Wehner, 1982;
Rossel and Wehner, 1984;
Rossel and Wehner, 1986;
von Frisch, 1949;
von Frisch, 1967;
Wehner and Strasser, 1985).
Morphological and electrophysiological studies of the bee retina further show
that an extensive part of the dorsal eye is structurally and functionally
similar to the dorsal rim area that is known to used for polarized light
navigation in other insects, such as desert ants, crickets and dung beetles
(Dacke et al., 2003;
Labhart, 1980;
Menzel and Snyder, 1974;
Wehner, 1982; Wehner and Labhart,
2006).
In honeybees, very little is known about how the information on the distance and direction of flight is combined to determine where the food source is located in relation to the nest. Here we address the question by asking how information about travel distance is used in the absence of directional (celestial compass) information. Individually marked bees were trained to find a reward of sugar solution that was placed at a fixed distance inside a tunnel. The length of the tunnel that was visible to the sky (or occluded from it) was under experimental control – part of the open top was closed by means of opaque panels. In one set of experiments, we filmed the waggle dances of the trained bees when they returned to the hive. In another series we recorded the behaviour of the trained bees, one by one, when they searched for the food in a fresh, identical tunnel that carried no reward.
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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 forage from a feeder containing sugar solution placed 4 or 6 m into the tunnel. The bees were allowed to fly back and forth between the nest and the feeder for at least 1 day, in order to get accustomed to the tunnel. The far end of the tunnel was closed, and bees could only enter or leave the tunnel through the end nearest to the hive. Dances performed by marked bees returning from the hive were filmed using a digital video camera and later analysed.
Analysis of waggle dance
In the first series of experiments, a group of bees was trained to visit a
feeder placed in an open tunnel. The feeder was placed at a distance of 4 m or
6 m along the tunnel (Fig. 1A).
Dances of bees returning from the tunnel were then recorded for both
distances. A second group of bees was trained to fly 6 m into a straight
tunnel covered with three opaque panels, each 66.6 cm long. The panels were
placed 0.66, 2.0 and 3.33 m down the tunnel
(Fig. 1B). This formed a set-up
in which celestial compass cues for orientation were unavailable in 2 m of the
first 6 m of the tunnel. The dances of bees returning from the partly covered
tunnel were also recorded.
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Analysis of food searching behaviour
As described above, 20 honeybees were trained to fly within a 7 m tunnel
covered with 3 opaque panels, each with a length of 66.6 cm (with a total
length of 2 m), to find a reward of sugar solution placed 6 m into the tunnel
(Fig. 2A). After training, the
bees were individually tested in an 8 m long tunnel that contained no food
reward. Different tunnel lengths for training and testing the bees ensured
that the distance to the end of the tunnel could not be used as an indication
of the position of the reward. Three kinds of tests were performed. In the
first kind of test, the panels used to occlude skylight were identical in
position and size to those used during training
(Fig. 2B). In the second kind
of test, the total occlusion of the tunnel was decreased to 1 m. A panel of
length 66.6 cm was placed 0.66 m from the tunnel entrance, and a second panel
of length 33.3 cm was placed 3.66 m from the entrance.
(Fig. 2C). In the third kind of
test, all panels were removed and the bees flew with a full view of the sky
along the entire length of the tunnel (Fig.
2D).
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For the purpose of analysis the test tunnel was subdivided into 80 sections, 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 position 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 turns, we could estimate the spatial distribution of its search (Fig. 2E). For each test, the mean and standard deviation (s.d.) of the search positions of the four U-turns measured for each bee were calculated. Student's t-tests were used to test for the statistical significance of any difference between the search positions in the three experiments, as well as the difference between the expected and the experimentally measured positions.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), the
duration of these dances increased with distance flown in the tunnel. The mean
waggle duration was 141 ms at a distance of 4 m (N=30, 275 loops) and
260 ms (N=30, 252 loops) at 6 m
(Fig. 3). This is consistent
with earlier conclusions that honeybees gauge the distance flown from the
extent of the image motion that is experienced by the eye en route to the food
source (Dacke and Srinivasan,
2007; 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).
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Distance estimation encoded in the waggle dance after a foraging flight with an interrupted view of the sky
A fresh group of bees was trained to fly to a feeder 6 m into an 8 m long
tunnel fitted with three opaque panels on top, each panel was 66.6 cm long
(Fig. 1C). This set-up
prevented the bees from obtaining any celestial cues for 2 m of the first 6 m
of the tunnel. In other words, the bee had access to celestial compass
information for 4 m of the 6 m long flight to the feeder. If the bees ignore
information on travel distance when there is no concurrent input from the
celestial compass, we would expect the mean waggle duration of the dance
performed after a flight down this partly covered tunnel to be similar to that
obtained after a 4 m flight down a fully open tunnel.
The analysis of the dances of marked bees returning from this partly covered tunnel reveals that this is not the case (Fig. 3). The mean waggle duration of 286 ms (N=30, 335 loops) is significantly different from that measured for a 4 m flight (P<0.001), but is not significantly different from that obtained after a 6 m flight in a fully open tunnel (P=0.27). These results indicate that the waggle dance encodes the total distance flown, irrespective of celestial input.
A dancing bee that shuttles back and forth between the hive and the feeder
in the tunnel is believed to base its navigation between these two sites on
path integration (Collett and Collett,
2000; Wehner and Labhart,
2006; Wehner and Srinivasan,
2003; Wehner and Wehner,
1990). We can estimate the performance of this path integrating
process by examining how precisely a bee is able to pinpoint the location of
the food reward to which is has been trained.
Integration of distance information when navigating to a food source
Bees were trained to fly to a feeder placed 6 m down a 7 m long tunnel. The
tunnel was covered with three opaque panels, each 66.6 cm long
(Fig. 2A), to prevent the bees
from receiving any skylight input for a total of 2 m of the 6 m they had to
fly to reach the feeder. The bees flew back to the hive along the same tunnel.
After training, bees were subsequently tested by recording their searching
behaviour in a fresh 8 m long tunnel that carried no food reward (see
Materials and Methods). Three types of tests were performed. In the first type
of test, the configurations of the panels on top of the tunnel remained
identical to those used during training
(Fig. 2B). In the second type
of test, half of this covering was removed, and the bees could now receive
directional information from celestial cues for 5 m out of the first 6 m
(Fig. 2C). In the third type of
test, all of the panels were removed and the searching behaviour was recorded
for bees flying with an uninterrupted view of the sky
(Fig. 2D).
The results are shown in Fig. 4. The mean searching position (at 5.9±0.5 m) in the tunnel with panels placed identically to the set-up used during training, is not significantly different from the position of the reward (at 6.0 m) during training (P=0.56; Fig. 4A). When we remove the covering, and provide the bees with celestial compass information over a relatively longer proportion of the tunnel than during training, the position of search can be affected in two possible ways. If the distance to the feeder is again processed independently of the availability of celestial cues, we would expect the bees to continue to search 6 m down the tunnel irrespective of the portion of the tunnel that is covered. If, on the other hand, the bees, do not register distance flown in the absence of skylight input, we would expect them to search progressively closer to the entrance, as more and more of the covering is removed. Finally, when the tunnel is fully open, we would expect them to search for the feeder after they have flown just 4 m into the tunnel.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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There are three plausible explanations for this phenomenon. (1) The panels used to occlude the sky also serve as prominent landmarks, so that the position of the feeder is defined by the spatial distribution of these panels. (2) It is too dark underneath the opaque panels for optic-flow-based odometry to function correctly, so that flight distance is registered only in the open sections of the tunnel. (3) Odometric information is not processed when there is no directional information from the sky.
If the first explanation is correct then the positions of the individual
panels, or the number of panels, served as landmarks to pinpoint the position
of the feeder. Prominent landmarks in similar experimental set-ups are known
to reset the odometer and help to define the distance to the feeder
(Srinivasan et al., 1997), and
the spatial distribution of landmarks can further help to pinpoint the
position of the feeder (Collett and Collett, 2004;
Collett and Zeil, 1996). It is
clear from our test in the open tunnel, where all the panels had been removed,
that the position of the search was not set by the positions of any of the
panels. If the bees were pinpointing the position of the feeder on the basis
of the position of the panels, they would not have commenced their search
until they had encountered at least one of these panels. In the open tunnel
the bees concentrated their search around the middle of the tunnel: a flight
straight down to the end was never observed. By the same line of reasoning, we
can also exclude the possibility that the feeder was pinpointed by counting
the number of panels that preceded it
(Chittka and Geiger, 1995;
Dacke and Srinivasan,
2008).
Even if the prominent panels that covered parts of the tunnel did not serve as the primary cue in pinpointing the feeder, the searching distribution in the open tunnel was slightly wider than that recorded in the tunnel that was identical to the training configuration. This suggests that the spatial distribution of the panels may have played a small, but relatively insignificant role.
The second possible explanation of the change in search positions recorded in the differently covered tunnels, is that the bees could not reliably detect the optic flow cues that were provided by the textured walls and floor underneath the covered sections. This would be the case if the ambient light intensity in these occluded sections was below the critical level for enabling vision in the bee, and in particular, for driving its movement-detecting pathways. The visual odometer would then run only in the open sections of the tunnel where day light levels prevailed. This possibility can be ruled out by the observation that the waggle duration after a 6 m flight into the partly covered tunnel was not significantly different from the waggle duration after a 6 m flight into an open tunnel (Fig. 3).
We favour the third explanation, which proposes that the omission of skylight cues does not blind the visual system, but instead suppresses the accumulation of odometric information when a bee navigates back to a previously visited food source. In all of the three tests that recorded searching behaviour, the bees concentrated their search approximately around the point that was reached after a total flight distance of 4 m in the open tunnel. This is the same distance that was left uncovered during training. It is of course possible that the bees could still get a view of the sky for some centimetres while flying in or out from underneath the covered sections of the tunnel. The distance flown with a full view of the sky during training will then effectively be slightly longer than 4 m, which may be one of the reasons for the slight shift of the mean search distribution away from 4 m in Fig. 4C.
It appears that odometric information is either completely omitted, or fed
in with a reduced weight if there is no concurrent input from the celestial
compass. This interpretation is in good agreement with similar studies of the
interplay between these two pieces of information in desert ants
(Sommer and Wehner, 2005;
Ronacher et al., 2006). The
study of the homing paths of these walking insects has led to the same
conclusion, namely, that odometric information is not accumulated when
celestial compass information is absent.
However, the honeybee's estimate of distance flown, as signalled by the duration of the waggle dance that she performs upon her return to the hive, does not seem to depend upon how much of the journey was flown under the open sky. The waggle-dance duration depends only upon the total distance that the bees have flown, regardless of the extent of sky occlusion. In the waggle dance, the bees always indicate the total distance flown to the food source, irrespective of the skylight input. Thus, distance conveyed in the waggle dance after a 6 m flight in a partly covered tunnel is not significantly different from that signalled after a flight of the same length in an open tunnel.
Two odometers in the honeybees?
We propose that the honeybee senses odometric information in two ways,
depending upon the mode, or context in which this information is used. In one
context (reporting distance flown to nestmates through the waggle dance), the
odometer provides a measure of the total distance travelled by
integrating optic flow information along the entire route, regardless of
whether the sky is visible or not. In the other context (navigating back to a
previously visited food source), the distanced estimate is gated by
the presence (or absence) of information from the celestial compass. These two
types of odometric information can serve different functions. The information
that is provided by the waggle dance could serve to inform potential recruits
about the entire flight distance to a food source, irrespective of partial
occlusions by overhead canopies. Together with an appreciation of the quality
of the food source, represented by the duration and liveliness of the dance
(Seeley et al., 1991;
Seeley et al., 2000), the
scouts can – at least in theory – use this information to evaluate
the most energy efficient food source to visit. This assessment would be
difficult to make if the potential recruits were given sky-gated distances,
rather than true distances. From the perspective of what information the
dance-following bees need to find the food source, the total distance flown is
also the most relevant measure. When these bees leave the hive in response to
a dance, and set out to find the advertised food source, all they need to know
is how far they should fly in the indicated direction. Presumably, these
recruits will be performing path integration as they fly out to the food
source, so that they can find their way back home.
However, the sky-gated distance information would be more useful to an
experienced bee that is returning to a well-known food site. It is generally
believed that large scale feeding excursions of honeybees are partly achieved
through the use of a path integrator
(Collett and Collett, 2000;
Wehner and Labhart, 2006;
Wehner and Srinivasan, 2003;
Wehner and Wehner, 1990). For
such a path integrator to work, the animal needs to obtain information about
distance travelled in a particular direction together with
directional information of this leg of the trip
(Müller and Wehner, 1988;
Wehner, 1994). When only one
of these two pieces of information is available, neither distance nor
direction can be processed on its own in a meaningful way in order to produce
a useful home vector. Under such circumstances it would be safest to
temporarily suppress path integration, rather than to continue it by guessing
a distance or direction. If we assume that the trained bees that return to the
tunnel in search of the feeder are using a process of path integration to find
the feeder, then the results are consistent with this interpretation, namely,
that, during path integration, odometric distance is largely ignored if there
is no concurrent input from the celestial compass. Thus, when an experienced
bee flies under a canopy, it would instead have to resort to piloting using
learned local landmarks (De Marco and
Menzel, 2005; Chittka and
Kunze, 1995).
Further evidence for the existence of two odometers comes from observations
that suggest that the distance-measuring capacity of the honeybee appears to
have different characteristics, depending upon how it is measured
experimentally. On the one hand, when this capacity is measured using the
waggle dance, the results indicate that the estimate of distance flown is
rather insensitive to changes in the region or the extent of the visual field
that experiences optic flow. Thus, the bee's estimate of the distance to a
feeder placed inside a tunnel, as indicated by the waggle dance, remains
largely unchanged even when optic flow cues are removed from the walls or the
floor of the tunnel (Si et al.,
2003). This indicates that a forager returning from a food source
is likely to provide a robust indication of the distance that she has flown,
even in conditions where the environment offers relatively sparse visual cues
for the measurement of optic flow. On the other hand, when the honeybee's
capacity to estimate distance flown is measured by using its searching
behaviour (i.e. by training a bee to forage at a feeder and examining its
ability to pinpoint the feeder's location when it is removed), then the bee's
distance estimate depends rather critically on the region of the visual field
that experiences optic flow. In such experiments the estimate of distance
flown (as indicated by the position in the tunnel at which the bee searches
for the missing feeder) is unaffected when optic flow cues are removed from
the floor of the tunnel, but is severely compromised when these cues are
removed from the walls (Srinivasan et al.,
1997). This suggests that an experienced forager returning to find
a previously visited food source relies largely on the optic flow that would
be provided by laterally positioned structures in the environment (such as
trees), and not by the ground beneath the bee. Thus, distance flown, as
estimated by an experienced forager, would be largely independent of the
height at which the bee flies to the food source.
In summary, bees may well possess two different odometers – a `community' odometer that is used by a forager to convey information to its nestmates about the distance to a food source via the dance, and a `personal' odometer that is used by an experienced individual to return to a previously visited food source. In the first case, the odometer provides a measure of the total distance travelled by integrating optic flow information along the entire route, regardless of whether the sky is visible or not. In the other case, the distanced estimate is gated by the presence (or absence) of information from the celestial compass.
In a recent study we have shown that bees flying along three-dimensional
routes that include a vertical component, signal in their dance the
total distance flown irrespective of its three-dimensional
configuration (Dacke and Srinivasan,
2007). The present account which, for the very first time presents
us with the possibility of two odometers in the bee, begs the question of
whether a flying bee can perform path integration in three dimensions to
obtain an accurate `personal' spatial representation of the position of the
food source, for the purpose of re-visiting it.
Celestial input is necessary for directional information
Our result that the foraging bee does not process the distance information
accumulated by the odometer when it is prevented from receiving celestial
input also suggests that neither magnetic nor idiothetic information (which
remained unmanipulated throughout this study) replace the directional
information from the sky. Directional information could possibly be replaced
by interpolating the directions flown before and after the covered sections,
but our results also rule out this option. A number of morphological,
electrophysiological and behavioural studies show that bees posses a dorsal
rim area capable of analyzing the pattern of polarized light in the sky
(Labhart, 1980;
Menzel and Snyder, 1974;
Rossel and Wehner, 1982;
Rossel and Wehner, 1984;
Rossel and Wehner, 1986;
von Frisch, 1949;
von Frisch, 1967;
Wehner and Strasser, 1985;
Wehner, 1992;
Wehner and Labhart, 2006), but
its involvement in the navigation of the bee remains largely unexplored. The
results from this study suggest that celestial cues alone provide sufficient
directional information for the distance estimation of the foraging bee, but
further studies need to be done to determine the relative contributions of the
sun, the polarized light pattern and spectral gradients to the celestial
compass.
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Acknowledgments |
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Footnotes |
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