Does swarming cause honey bees to update their solar ephemerides?
Department of Biology, Kutztown University of Pennsylvania, Kutztown, PA 19530, USA
* Author for correspondence (e-mail: towne{at}kutztown.edu)
Accepted 1 September 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: bee, sun compass, landmark, learning, orientation, swarming, cognition
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Here we focus on one of these systems, namely the mechanisms by which honey
bees update, or fail to update, their solar ephemeris functions, that is,
their memories of the sun's daily pattern of movement in relation to the
landscape. Both bees (Dyer,
1987) and ants (Wehner and
Lanfranconi, 1981
) do indeed acquire reasonably accurate solar
ephemeris functions for use in their celestial compass orientation. In both
cases, the insects begin with an innate expectation that the sun's azimuth in
the morning is about 180° from its azimuth in the afternoon
(Wehner and Müller, 1993
;
Dyer and Dickinson, 1994
) and
fill in the details of the local ephemeris function with experience
(Lindauer, 1959
; reviewed by
Dyer, 1996
).
Although it has often been assumed that bees keep their solar ephemerides
fully up to date (Gould, 1980,
1984
;
Dyer, 1987
), Lindauer
(1971
) had suggested, based on
a long-distance latitudinal displacement experiment
(Lindauer, 1957
), that bees
might imprint on the solar ephemeris functions at their natal sites. More
recently, Towne and Kirchner
(1998
) have shown that bees
can indeed fail strikingly to update their solar ephemerides. Their technique
was a minor modification of Dyer's treeline-to-treeline transplantation
technique (Dyer and Gould,
1981
; Dyer, 1987
),
in which Dyer transplanted a hive from one treeline (the bees' natal site) to
a visually similar but differently oriented treeline (the recipient site).
After transplantation, some of Dyer's bees found a feeder at the recipient
site placed in its accustomed location relative to the treeline. On sunny
days, these bees oriented their communicative waggle dances according to their
usual convention: a dance oriented upwards on the vertical comb corresponded
to a food source in the direction of the sun in the field. When Dyer
transplanted bees on overcast days, however, bees that found the feeder at the
new site usually oriented their dances as if they were still at their natal
treeline, relying on a memory of the relationship between the solar ephemeris
function and the natal landscape. This is how Dyer and Gould
(1981
) first showed that bees
learn this relationship.
Towne and Kirchner (1998)
basically repeated Dyer's procedure, but allowed the transplanted bees to
forage under sunny skies at the recipient site for one to several days before
observing the same bees' dances under overcast skies. Most of these long-term
transplantees danced under overcast skies as if they were still at their natal
site; they had not realigned their solar ephemerides to the new treeline,
despite ample opportunity to do so. Thus the sun-learning mechanism seems to
be surprisingly resistant to revision after the initial acquisition.
Here we extend these observations in two ways. First, we simultaneously compare the orientation of long-term treeline-to-treeline transplantees with the orientation of newly transplanted bees and also with that of un-transplanted bees native to the recipient treeline. The results clarify the effect of experience at the new site.
Second, we ask whether it is important that the bees in Towne and
Kirchner's experiments (Towne and
Kirchner, 1998) were transplanted passively, that is, carried to
the recipient site by the experimenters. Assuming that the bees' learning
mechanisms are designed to work under natural conditions, we might expect bees
to be able to realign their solar ephemerides only when transplanted under
circumstances that mimic natural events. One process by which bees normally
transplant themselves is swarming, wherein roughly half of the workers in a
colony leave their natal nest and, after a period of living outdoors in a
cluster, move to a new nest site some distance away. Thus we hypothesized that
bees put through a swarming process as they are transplanted from one treeline
to another would, unlike passively transplanted bees, realign their solar
ephemerides with respect to the recipient treeline.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In all cases, bees were trained to visit pneumatic feeders offering lightly
scented sucrose solutions and were individually marked with numbered,
color-coded tags after having been recruited to the feeders at their natal
sites (techniques reviewed in Seeley,
1995). The feeders' locations at both sites were marked with
conspicuous colored or patterned signs 61 cm square mounted 1 m off the ground
on posts. These signs were intended to help the newly transplanted bees find
the feeders at the recipient sites, and they were identical at both sites for
any given experiment.
Honey bees rarely survive beyond 3 weeks as field bees
(Visscher and Dukas, 1997),
and in all experiments reported here, the transplanted bees lived at their
`natal' sites for at least four weeks, ensuring that they had their first
flight experience there. In all experiments, feeders were generally set up for
two feeding periods every day, typically 7:00 h-9:00 h and 13:00 h-15:00 h
local solar time (LST), although the exact time and duration of the feeding
periods varied. Hereafter, all times are given in LST.
Field sites (2000, 2001 and 2002)
We used two panoramically similar but oppositely oriented field sites 2.2
km apart. Both sites had conspicuous treelines from which agricultural fields
sloped away to valleys about 30 m of elevation below
(Fig. 1). In each case, the
bottom of the valley was approximately 400 m from the treeline, and the next
ridge, beyond the valley (not shown in Fig.
1), was about 400 m farther. The hives and feeders were placed 200
m apart at corresponding locations at the two sites (see H and F in
Fig. 1). Hereafter, we refer to
these sites as the `north-facing treeline'
(Fig. 1A) and the `south-facing
treeline' (Fig. 1B), even
though the correspondences between the two landscapes include not just the
treelines but also several broader features of the landscapes and the visually
conspicuous hives and signs.
|
Since the recipient site was only 2.2 km from the donor site, within the
foraging range of naturally sized colonies
(Visscher and Seeley, 1982),
some of our transplanted bees were familiar with the area around the recipient
site, and typically about 20% returned to the donor site after
transplantation. Although the two experimental sites ideally would have been
farther apart to ensure that transplanted bees were initially unfamiliar with
the recipient site, we were constrained by the available topography and the
need to travel frequently between the two sites. Two types of evidence suggest
strongly, however, that the transplanted bees we later observed under cloudy
skies were indeed initially unfamiliar with the recipient site: (1) these bees
had failed to return to their natal site after transplantation, as if they did
not recognize the recipient site as part of their former colony's foraging
range, and (2) most of these bees later mistook the recipient site for their
natal site and oriented their dances accordingly on subsequent cloudy days, as
if they had no information about the sun's location relative to the landscape
at the recipient site.
Creation, transplantation and re-hiving of swarms (2000)
We transplanted three different colonies by putting them through artificial
swarming processes as they were transplanted. In all cases, the swarms' natal
site was the south-facing treeline (Fig.
1B). In the few days before the swarms were made, large numbers of
bees were individually marked at the feeder at the natal site. As soon as the
colonies were transplanted, feeders identical to those at the natal site were
set out at the usual location relative to the treeline at the recipient site,
and many of the marked, transplanted foragers visited them regularly.
Each of the three swarms was created using all of the roughly 4000 bees
from a two-frame observation colony. These swarms were small but within the
wide range of sizes that occur naturally (reviewed by
Seeley, 1977;
Winston, 1987
). To make each
swarm, the colony's queen was placed in a small wire cage with several
attendant workers, and the cage was attached to the center of a wooden cross
(45 cm high and 50 cm wide, crosspiece attached 33 cm from the bottom of the
vertical member). The cross was mounted on an octagonal plywood platform 50 cm
across, held about 1 m off the ground on a metal post. A second octagonal
piece of plywood attached on top of the cross provided a bit of shelter for
the swarm. After the cage bearing the queen was attached to the cross, the
bees from the observation colony were shaken onto the lower platform, and the
bees quickly streamed up the vertical member of the cross, many fanning their
Nasanov glands, to form a cluster around the queen. Artificial swarms created
in this and similar ways begin to seek nest sites and otherwise seem to behave
like natural swarms (Lindauer,
1955
; Seeley,
1977
; Robinson and Dyer,
1993
). As soon as each swarm was clustered, the (now empty) hive
was moved away, and the swarm was placed where the hive had been.
After they were created, the three swarms were subjected to somewhat
different treatments. Swarm 1 was created at noon on 30 June 2000 and was
re-hived 7 h later after flight activity for the day had ended. This amount of
time in the swarm cluster is short but within the range of that seen in
natural swarms. Swarms occasionally find new nest sites quickly, apparently
because their scouts sometimes begin searching for nest sites up to 3 days
before they depart the parent colony (reviewed by
Winston, 1987). While Swarm 1
was clustered, the two frames of comb from the observation hive were replaced
with new frames containing only wax comb foundation. To re-hive the swarm, the
queen cage was removed from the swarm cluster and placed inside the
observation hive atop the upper frame. The glass window of the hive was then
folded out to a horizontal position, and the swarm was shaken from the swarm
apparatus onto the glass. The bees streamed from the glass into the new hive,
many fanning their Nasanov glands. When all of the bees were inside, the hive
was closed and transported to the recipient site, and the queen was released.
The bees' first flights from the new hive occurred the next morning at the
recipient site, and the learning flights of the marked bees were recorded at
this time (see below).
Swarm 2 was created similarly at 14:15 h on 28 July 2000, except that the
bees on the original frames were liberally smoked with a bee smoker to cause
the bees to engorge on honey before they were shaken onto the swarm apparatus
(after Robinson and Dyer,
1993). This was intended to mimic the engorgement that occurs in
preparation for natural swarming (Combs,
1972
). This swarm was carried the same evening, as a swarm, to the
recipient site (replacing the Swarm 1 colony) and was allowed to hunt for a
new nest site there. We placed an empty nest box with a pheromone lure on a
tall post near the swarm in hopes of luring the bees to occupy it, so that the
swarming process could run to its natural completion. Unfortunately, the bees
selected instead a natural nest cavity in the wooded area to the northeast of
the hive (Fig. 1A) and departed
for that cavity at about 14:00 h on 30 July, after 2 days in the cluster (1.5
days at the recipient site). Because the queen was still caged, however, the
swarm aborted its relocation effort and straggled back over the next 30 min.
While the bees were away, we removed the swarm apparatus, replaced it with a
new hive, and transferred the queen cage into it. The new hive had two new
frames bearing only comb foundation and had one of its glass sides removed,
allowing the bees to enter. After all of the bees had crawled into the new
hive, we replaced the glass side and released the queen. The learning flights
of these bees upon their first departure were not recorded, as there was too
much flight activity around the hive in the middle of the afternoon.
Upon being hived, Swarm 2 abandoned its search for new nest sites, but the swarm did not settle into its new nest as quickly as did Swarms 1 and 3, which were hived at dusk. The bees of Swarm 2 did not immediately spread across the combs but continued to cluster around the queen inside the hive for more than a day after being hived. Also, although the bees of Swarm 2 started to build new comb during their first day in the new hive, they did not build as much during the first few days as did the other swarmed colonies.
Swarm 3 was created at 14:00 h on 8 August 2000 using the same smoking process that was used for Swarm 2. This swarm was left at its natal site and took to the air twice on its second day, 9 August, once at 13:05 h and again at 14:55 h, each time returning to the (still caged) queen after a short period. The swarm remained at its natal site until the end of flight activity that evening, at which time it was re-hived using the same process that was used for Swarm 1 and transplanted to the recipient site. As for Swarm 1, the learning flights of the marked foragers from this colony were recorded at the recipient site the next morning.
In addition to the three swarmed colonies, a control colony that was not put through a swarming process was transplanted intact on 29 June 2000, one day before Swarm 1 was transplanted. The bees from this control colony visited a feeder of their own, and the bees from the two colonies (swarmed and control) were kept separate at the feeders with the help of powder boxes on the entrances of the hives, which dusted the bees lightly with non-toxic paint powder as they passed through, different colors being used for different colonies. In addition, the two feeders were marked with differently colored signs and offered differently scented sugar water.
The control colony was successfully used to measure the learning flights of non-swarmed bees (see below), but the marked bees originally transplanted with this colony turned out not to be useful as controls for the sun-learning aspect of the experiment, as almost all of the bees were lost (presumably dead) by the time the first solidly overcast day occurred at the recipient site 10 days later (the swarmed bees had a much higher survival rate; see below). Subsequently, we used the caging technique to supply the recipient site with groups of non-swarmed control bees as needed.
Recording and analysis of learning flights (2000 and 2001)
Bees and wasps perform learning flights on their first departures from a
nest or feeder or when they encounter novel circumstances there, and the
flights help the insects to learn the visual features of the targets (Zeil,
1993a,b
;
Lehrer, 1993
;
Wei et al., 2002
; reviewed by
Wehner, 1981
;
Zeil et al., 1996
; Collett and
Zeil, 1997
,
1998
). In the first, hovering
phase of learning flights at the hive entrance, bees leap into the air,
immediately reverse direction to face the hive entrance, and hover in front of
the entrance for several seconds, swinging back and forth through tight arcs
within 1-2 m of the entrance. In the second, circling phase, the bees turn
from the hive entrance and undertake circling or figure-eight flights of
increasing height and diameter within about 5-10 m of the entrance, after
which the bees usually leave the hive's immediate vicinity.
The learning flights of individually marked bees were observed as the bees
exited the hive for the first time on the morning after they were
transplanted. An observer sat beside the hive and watched the bees through the
glass as they approached the hive entrance and then departed. The durations of
the flights were timed with a stopwatch capable of recording two time
intervals after a single starting point, which allowed both phases of each
flight to be recorded. The hovering phase started when an individually marked
bee left the hive and ended when the bee turned more than 90° from the
hive entrance, or when the bee started its circling flight. The circling phase
started immediately after the hovering phase and continued until the bee broke
the circling/figure-eight pattern and flew away. Some bees were lost to the
observer during either the hovering or circling phase of the flight, and only
flights for which the entire phase was observed were included in the analysis.
Statistical comparisons between the flight durations of the three different
types of transplantees were made using the (non-parametric) median test, which
is relatively insensitive but entails minimal assumptions about the shapes of
the distributions (Conover,
1999; Siegel and Castellan,
1988
).
For both phases of the learning flights, the results from Swarms 1 and 3 are not significantly different (Fig. 5Aiii,Biii, black vs shaded; P>0.6 for the hovering flights, and P>0.4 for the circling flights; t-tests), so for statistical comparisons with the results from the non-swarmed bees, the results from the two swarms are pooled.
|
|
|
|
|
|
Dance directions were analyzed for clustering around predicted directions
using the V-test (Batschelet,
1981). All statistical analyses of dance directions from overcast
days exclude dances that occurred after the sun or blue sky first appeared to
us and also bimodal dances (see Results), as the latter could not be assigned
a single direction.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
On several days in July 2002, we transplanted groups of about 20 marked bees native to the north-facing treeline (Fig. 1A) into a hive at the south-facing treeline (Fig. 1B). Meanwhile, a group of marked foragers native to the south-facing (recipient) treeline was trained to visit the feeder there. The transplanted bees adopted into the recipient hive foraged at the feeder alongside the natives under sunny or partly sunny skies for 1-15 days. Then on the day before a predicted overcast, a new cage full of bees was transplanted from the feeder at the north-facing treeline into the recipient hive; these bees would be new to the recipient site when they were released the next morning. If the next morning was indeed overcast, we recorded the dances of all three groups of bees as they visited the feeder at the recipient site.
The results of one such experiment, on 28 July 2002, are shown in
Fig. 2. Throughout the
recording period, all bees native to the recipient site
(Fig. 2A) indicated the correct
direction to the feeder (Ø=68.6°; N=32 dances by 7 bees;
r=0.91; P<0.001, V-test, predicted direction 87.5°;
all analyses here and below exclude dances occurring after the sun or blue sky
first appeared). The newly transplanted bees
(Fig. 2B), by contrast,
initially danced according to their memories of the solar ephemeris function
relative to their natal treeline (Ø=267.2°; N=14 dances by
4 bees; r=0.53; P<0.005, V-test, predicted direction
253.5°). This is what Dyer observed on several occasions
(Dyer and Gould, 1981;
Dyer 1987
), and it indicates
that these bees were not able to locate the sun using celestial cues. As the
sun began to make brief appearances at 8:22, these newly transplanted bees
began to switch their dances to the correct direction for the current site.
Several did bimodal dances for a while (broken vertical lines in
Fig. 2B), indicating both
directions on alternate wagging runs. Dyer
(1987
) sometimes observed such
dances under similar conditions.
The results mentioned so far indicate that there were no celestial cues available to the bees before the sun first appeared to us. During this time, the long-term transplantees (Fig. 2C) danced mainly in a direction corresponding roughly to the `natal site' prediction (Ø=332.9°; N=49 dances by 15 bees; r=0.66; P<0.001, V-test, predicted direction 253.5°). In the preceding days, these bees had all foraged under sunny or partly sunny skies at the recipient site, and 7 of them had more than a week of experience there. Nonetheless their dances mainly resembled those of the freshly transplanted bees and were appropriate for their natal treeline, not for the current site. Most of these bees had clearly not realigned their solar ephemerides to the new treeline.
Several dances of long-term transplantees (Fig. 2C) corresponded roughly to the `current site' prediction before the sun first appeared (11 dances altogether by three different bees). It is possible that these bees had realigned their solar ephemerides to the new treeline. But it is also possible that these bees were able to extract celestial cues that we and the other bees failed to detect. We cannot separate these possibilities based on these data.
Why were almost all of the bimodal dances performed by recent transplantees
(Fig. 2B, broken vertical
lines) rather than long-term transplantees
(Fig. 2C)? This difference is
probably attributable to the celestial cues available as these bees first flew
out to the feeder. The first dances of the long-term transplantees that
oriented by memory of their natal site were performed sooner and indicated
directions more northward (average time of first dance 7:26; average direction
290°, N=12) than the first dances of the newly transplanted bees
that later danced bimodally (average time of first dance 8:15; average
direction 196°; N=3). Thus these two groups of bees probably
first flew out under slightly different sky conditions. The memory of bees
using fresh celestial cues evidently operates with a time lag
(Lindauer, 1963;
Gould, 1984
), and bees in
transplantation experiments sometimes persevere for a while in dancing in an
accustomed direction even after sky conditions change
(Dyer, 1987
). This is
interesting in itself, but for the present purpose it probably means that the
differences between the dances of the newly transplanted bees and those of the
long-term transplantees reflect differences in their recent flight experience,
not long-term differences in their solar ephemeris functions.
A second result similar to that of Fig. 2 is shown in Fig. 3, taken 1 day before the observations shown in Fig. 2 and involving many of the same bees. In this case, the newly transplanted bees had been transplanted the day before and had one afternoon's experience at the recipient site under mostly cloudy skies, and the long-term transplantees had been transplanted 4-14 days earlier. The bees native to the current site danced correctly (Fig. 2A; Ø=77.9°; N=18 dances by 8 bees; r=0.95; P<0.001, V-test, predicted direction 87.5°), and both groups of transplantees danced mainly as if they were at their natal treeline (Fig. 2B,C; new transplantees: Ø=281.1°, N=40 dances by 13 bees, r=0.78, P<0.001; long-term transplantees: Ø=316.3°, N=42 dances by 11 bees, r=0.48, P<0.05; both V-tests with a predicted direction of 253.5°). Again, the long-term transplantees do not appear to have updated their solar ephemerides at the recipient site.
The results of a third similar experiment, from 14 July 2002, are shown in Fig. 4. New transplantees were released earlier the same day, and the long-term transplantees were transplanted 1-5 days earlier. As in the other trials, the native bees danced correctly from the outset (Fig. 4A; Ø=84.9°; N=67 dances by 7 bees; r=0.95; P<0.001, V-test with a predicted direction of 87.5°). Both groups of transplanted bees, taken separately or together, were not significantly oriented toward either predicted direction (Fig. 4B,C; for the combined sample: Ø=13.9°; N=123 dances by 14 bees; r=0.16; P>0.1 for both predicted directions, V-tests) until after the sun appeared toward the end of the observations. Moreover, throughout this period we observed a total of 19 dances by transplanted bees (new and long-term), for which we were unable to discern any orientation at all; we scored them as round dances (7 dances), disoriented waggle dances (9), or something in between (3), depending on whether the dances had wagging segments.
The transplanted bees in Fig.
4 were probably so poorly oriented because they were working with
two types of conflicting information, weak polarization or spectral cues
(Wehner and Rossel, 1985;
Wehner, 1994
;
Labhart, 1999
) penetrating the
cloud cover and their long-term memories of the sun's pattern of movement in
relation to their natal treeline. Such compromise orientation has been
observed before (Dyer, 1987
;
Towne and Kirchner, 1998
)
under conditions like this. Indeed, one can see this phenomenon in
Fig. 4 toward the end of the
observations: many of the dances of the transplanted bees indicated roughly
northward (0°) at 10:15 h and then gradually drifted toward the correct
direction over the next hour as the sun emerged. (We see this drifting again
in Fig. 7B below.) The poor
orientation at the beginning of the observation period also calls to mind the
scattered orientation seen by Rossel and Wehner
(1984
; reviewed in
Wehner and Rossel, 1985
), when
bees were given only small patches of unpolarized ultraviolet light with which
to orient their dances. Bees take such patches of light to be any point in the
anti-solar hemisphere, not necessarily on the anti-solar meridian, and their
dances are correspondingly scattered over about 180°.
A noteworthy feature of these results is that all of the bees native to the
recipient site (Figs 2A,
3A,
4A) are consistently well
oriented throughout, even though the celestial cues were weak or ambiguous.
These bees must have been relying on their memories of the solar ephemeris
function at this (their natal) site. Further, while the orientation of these
bees is very good, it is not as good as the orientation one sees on sunny
days, when bees can orient directly by strong celestial cues: The mean vector
for all dances of the native bees in Figs
2A,
3A, and
4A combined (r=0.936,
N=152) is significantly shorter, indicating greater scatter, than the
mean vector for four periods of recordings made under sunny skies
(r=0.964, N=158; P<0.01, Watson and Williams
F-test; Batschelet,
1981, p. 122).
Another noteworthy feature of these results is that the dances of the
long-term transplantees oriented by memory of their natal site seem to be
consistently skewed by about 45° from the natal site prediction (Figs
2C,
3C, dances at the upper left of
each panel). It could be that these dance directions were affected by weak
celestial cues, although if this were the case the dances of the newly
transplanted bees (Figs 2B,
3B)should have been similarly
affected, and they seem not to have been - at least as far as one can tell,
given the considerable variability in the dance directions of the newly
transplanted bees. Dyer (1987)
observed similar skews in some of his cloudy-day displacement experiments, and
their cause remains unknown.
Learning flights
To assess the extent to which our transplanted bees initially re-oriented
to the recipient site, apart from their solar ephemeris functions, we measured
the learning flights of transplanted bees as they first emerged from their
hives after transplantation. We measured both the hovering and circling phases
of the flights of bees transplanted by the three different transplantation
techniques used in this study, i.e. (1) when small groups of bees were
transplanted in cages, (2) when whole hives were transplanted intact, and 3)
when whole colonies were put through a swarming process as they were
transplanted. The caged bees were transplanted in groups of about 20 bees on
several occasions during August 2001. The two hives that were transplanted
intact were the control colony for the swarm experiments, transplanted on 29
June 2000, and a second colony transplanted on 24 August 2000. The swarmed
colonies were Swarm 1 and Swarm 3 (see below), hived on 30 June and 9 August
2000, respectively. The results of all these measurements are shown in
Fig. 5.
The bees whose hives were transplanted intact, without swarming, performed
fewer hovering flights than each of the other two groups
(Fig. 5A), and the hovering
flights of the bees from intact hives were the shortest (P<0.0001
for the flight durations of intact hives compared to those of each of the
other groups; median tests). Robinson and Dyer
(1993) likewise found that
non-swarmed bees performed fewer and shorter hovering flights than swarmed
bees, although more of their non-swarmed bees performed hovering flights (80%
compared to our 51%), probably because our methods for transplanting the
colonies were different. Importantly for the present context, Robinson and
Dyer also found that the great majority of swarmed bees, but not non-swarmed
bees, reoriented quickly to their new nest location, preferring to return to
the location at which they were hived over their original nest site only a
short distance away. That is, the swarmed bees acted as if they knew that
their nest site had changed.
The hovering flights of the caged bees
(Fig. 5Ai) were only slightly
shorter than those of the swarmed bees
(Fig. 5Aiii); the difference is
marginally significant (P=0.0496, median test). It is not surprising
that the caged bees did substantial hovering flights, since they had spent the
night caged in a foreign hive, and learning flights at hives (reviewed by
Collett and Zeil, 1998) and
feeders (Wei et al., 2002
)
both tend to be modulated upwards when bees have experienced changes
there.
For the circling orientation flights
(Fig. 5B), the three groups are
significantly different from each other in all pairwise comparisons
(P<0.0002 for all comparisons; median tests). The swarmed bees
again performed the longest flights, but in this case their flights were
substantially longer than those of the caged bees. This difference can be
attributed to the swarming process, which signals to the bees that they have
moved to a new nest site (Robinson and
Dyer, 1993).
The effect of swarming on relearning the solar ephemeris function
To determine whether swarming causes bees to realign their solar
ephemerides to a rotated landscape, we put colonies through an artificial
swarming process as they were transplanted from the south-facing treeline
(Fig. 1B) to the north-facing
treeline (Fig. 1A). The first
swarm was created in the early afternoon on 30 June 2000, and it was hived and
transplanted at dusk the same evening. A control, non-swarmed colony was also
transplanted the day before. Many of the marked bees from both colonies
visited feeders 200 m to the WSW at the recipient site
(Fig. 1A) in the bees'
accustomed location relative to the treeline but now in the opposite compass
direction. The feeders offered food in the morning and afternoon for the next
2.5 weeks.
We needed to observe the dances of the swarmed bees on overcast days when
the clouds obscured all celestial cues useful to the bees. We ourselves cannot
detect all of these cues (see Wehner and
Rossel, 1985; Wehner,
1994
), however, so we transplanted non-swarmed bees as controls.
Because non-swarmed bees do not re-learn the solar ephemeris function at the
recipient site (Figs 2,
3,
4 above), they should dance
correctly at the recipient site only when fresh celestial cues are available;
conversely, they should dance by memory of their natal site when such cues are
absent. Unfortunately, there was no period of solid overcast until 16 days
after the control colony was transplanted, and by then only one (2.3%) out of
the 43 marked control bees that had regularly visited the feeder at the
recipient site had survived. This is not surprising, as these bees were not
necessarily young when they were first tagged at the donor site, and field
bees rarely survive as long as 3 weeks
(Visscher and Dukas, 1997
).
Interestingly, however, the swarmed bees showed greater longevity: 23 (32.4%)
of the 71 marked foragers survived for at least 16 days after transplantation.
In any case, because the non-swarmed control bees had largely disappeared, we
resorted to transplanting additional control bees using the caging technique
(beginning on 9 July) for the remainder of the study, and it is the caged
transplantees that served as the control bees for all cloudy-day dance
recordings reported below.
The morning of 15 July was overcast, and the surviving foragers from the Swarm 1 colony and some of the cage-transplanted control bees visited the feeders and danced. The dances were recorded by two observers, one at each colony, and the results are shown in Fig. 6A,B. Before the sun appeared at 8:32 h LST, the dances of the bees from the Swarm 1 colony were oriented mainly according to the `natal site' prediction (Fig. 6B; Ø=63.7°; N=32 dances by 10 bees; r=0.71; P<0.001, V-test with a predicted direction of 87.5°); that is, the bees took the current treeline to be their natal treeline and danced accordingly. The control bees (Fig. 6A), from which we were able to record only a small sample during this time, gave more scattered dances, not significantly clustered around either predicted direction (Ø=168.8°; N=11 dances by 6 bees; r=0.63; P>0.1, V-tests for both predicted directions). After the sun had been out for a while, all of the bees switched over to the dance direction appropriate for the current site, and the Swarm 1 bees performed a few bimodal dances briefly as they made the transition (Fig. 6B, broken vertical lines). The Swarm 1 bees, then, clearly had not realigned their solar ephemerides to the new site, even with over 2 weeks' experience there.
Another overcast period occurred 2 days later. This time we had only one observer to record dances, so we recorded only from the Swarm 1 hive. (Ideally, these experiments would involve three observers, one tending the feeders and one at each hive, but this day we had to proceed, on short notice, with only two.) The results are shown in Fig. 6C. The results mimic those of 15 July (Fig. 6B): the dances of swarmed bees that occurred before we first saw blue sky are significantly clustered around the `natal site' prediction (Ø=89.8°; N=39 dances by 9 bees; r=0.71; P<0.001, V-test with a predicted direction of 87.5°), confirming that the Swarm 1 bees had not realigned their solar ephemerides to the landscape at the recipient treeline.
Bees that experience swarming processes like the one we used for Swarm 1
perform extensive learning flights (Fig.
5) and, importantly, return reliably to their new hive, even when
the old hive is available at its original location nearby
(Robinson and Dyer, 1993). One
might also expect, therefore, that the swarming process would induce bees to
realign their solar ephemerides to the landscape around their new nest. But
our Swarm 1 bees seem to have retained only their memory of the sun's course
relative to their natal landscape.
Then again, there are many stimuli associated with natural swarming that
the Swarm 1 bees did not experience and that could possibly trigger
re-alignment of the solar ephemeris under natural conditions. These stimuli
include, among others, engorgement of the workers with honey before they leave
their natal nest (Combs, 1972);
the shaking or vibration signals that occur throughout the period in the swarm
cluster (Donahoe et al.,
2003
); wings-together worker piping
(Seeley and Tautz, 2001
) and
swarm warming (Seeley et al.,
2003
), both of which build during the last hour before take-off;
and buzz-running, which may be the final signal for departure
(Lindauer, 1955
;
Esch, 1967
). Thus we moved the
Swarm 1 colony away and transplanted two additional swarms using modified
swarming procedures that included more of the stimuli experienced by bees in
natural swarms.
Swarm 2 was created on 28 July 2000 from a colony native to the donor site. This time the bees were liberally smoked with a bee smoker to stimulate engorgement of the workers with honey before they were shaken from the comb. The swarm was then transplanted as a swarm, searched for nest sites, and took to the air 1.5 days later (30 July). Thus the bees experienced all of the stimuli associated with searching for nest sites and lift-off. Because the queen was still caged, however, the swarm aborted its relocation effort and returned. While the swarm was away, we replaced the swarm apparatus with a hive, and the bees moved in. A number of marked bees from this colony then visited a feeder at the recipient site until an overcast period occurred over 2 weeks later on 14 August.
A third swarm was created similarly on 8 August. This swarm was allowed to remain at the donor site until it lifted off for a new nest site the following day. Because the queen was still caged, the swarm returned, and it lifted off and returned again 2 h later. The Swarm 3 colony was finally hived and transplanted to the recipient site at dusk that same evening (9 August), and the bees were allowed to forage at the recipient site for the next 4 days until the first overcast period occurred.
In addition to these two swarmed colonies, 69 control bees were transplanted in cages between 2 and 4 August into the colony of Swarm 2 after it had been hived at the recipient site. Most of these non-swarmed control bees were adopted into the Swarm 2 colony, although 14 (20.3%, a typical fraction) found their way back to their natal site. Some of the control bees that remained at the recipient site foraged from the feeder there until the first overcast period occurred 10 days later.
The morning of 14 August was mostly cloudy, although small patches of blue sky were available from time to time. Nonetheless, we recorded dances for an hour from about 7:30 h-8:30 h LST, and most bees from both colonies (4 out of 5 from the Swarm 2 colony and 7 out of 11 from the Swarm 3 colony) danced toward the current site prediction, as if they knew the sun's location. By the afternoon feeding period the cloud cover had become complete, and we again recorded dances.
The results from the afternoon period are shown in Fig. 7. Several bees from each colony danced before the sun appeared at 14:53 h LST. The results from the control bees (Fig. 7A) are not very useful, as we observed only 9 dances, and these are not significantly clustered, although they are closer overall to the `natal site' prediction (Ø=59.2°; N=9 dances by 5 bees; r=0.36; P>0.05, V-test for either predicted direction). The dances of the Swarm 2 bees (Fig. 7B), on the other hand, were consistent with the `natal site' prediction (Ø=92.6°; N=21 dances by 5 bees; r=0.76; P<0.001, V-test with a predicted direction of 87.5°). The Swarm 2 bees, then, had not realigned their solar ephemerides in the 2 weeks they had spent at the recipient treeline.
The dances of two Swarm 2 bees that danced throughout much of observation
period on 14 August are connected with thin black lines in
Fig. 7B to illustrate some
typical observations of individual bees not shown in the other figures. The
results from these bees show (1) that a given bee tends to dance in a
more-or-less consistent direction in sequential bouts of dancing, (2) that
different bees sometimes dance in somewhat different directions, and (3) that
bees using a memory of the sun's course relative to their natal treeline
sometimes shift their dance directions gradually as weak celestial cues become
available. Dyer (1987) has
noted and discussed each of these in the context of his short-term
displacement experiments. The differences between bees could be the result of
different recent experience or the result of different thresholds among bees
for responding to weak celestial cues. We cannot currently separate these
possibilities. And the gradual reorientation evidently represents a compromise
between two different memories, one old and one fresh. There seems to be much
more to learn about how individual bees integrate memories to select dance
directions.
While the Swarm 2 bees clearly failed to realign their solar ephemerides to the recipient site, the Swarm 3 bees observed on the same day gave mixed results (Fig. 7C): The dances of the Swarm 3 bees were clustered around the `current site' prediction overall (Ø=267.6°; N=19 dances by 10 bees; r=0.48; P<0.005, V-test with a predicted direction of 257.5°), although 4 out of the 10 bees indicated only the `natal site' prediction (these dances are labeled with each bee's individual tag number in Fig. 7C). Thus there seems to be a difference between the Swarm 2 and Swarm 3 bees, for which there are a few possible explanations. First, it may be that some of the Swarm 3 bees had realigned their solar ephemerides in the 4 days they had spent at the recipient site, although some (4 out of 10) had not. While the swarming processes used for Swarms 2 and 3 differed somewhat, both swarms selected and departed for new nest sites, and both aborted their departures because the queen was still caged. The two swarms differed mainly in the way they were hived: Swarm 2 was hived in the afternoon as it returned from an aborted departure, and the bees seemed to take a couple of days to fully settle into the new hive, while Swarm 3 was hived in the evening after an aborted departure. It seems possible, but unlikely, that these differences would affect the bees' solar ephemeris learning.
A second possible explanation for the different orientation we observed in Swarms 2 and 3 is that the bees in the two colonies may have had different experience with celestial cues in the hours immediately preceding the afternoon dance recordings. There were certainly celestial cues available earlier in the day, because a large patch of blue sky had become visible by the time we stopped recording dances at 8:40 h LST in the morning. Also, 4 of the bees that danced by memory of their natal site in the afternoon, indicating that they had not re-learned the solar ephemeris function, had nonetheless danced correctly (3 bees) or bimodally (1 bee) in the morning. We do not have detailed records of the sky conditions throughout the period between the two recording sessions, but it seems likely that some of the bees that danced during the afternoon session had flown to the (empty) feeder under an incomplete cloud cover between the sessions. If the Swarm 3 bees, transplanted more recently, flew out more often than the Swarm 2 bees during this time, then this might account for the fact that some of the Swarm 3 bees knew the sun's actual location during the afternoon session.
A third difference between the Swarm 2 and Swarm 3 colonies is that the colonies spent different amounts of time at the recipient site before the first cloudy day occurred: Swarm 2 had been there for 15 days, while Swarm 3 had been there for only 4 days. As unlikely as it may seem, our results overall are consistent with the idea that bees that have been at a recipient site for short periods may be more likely to act on weak celestial cues penetrating the clouds than are bees that have spent many days at the recipient site (see all of the transplantees in Fig. 4 and the control bees in Fig. 6, for example). It is not clear why bees would do this, but it is suggested by our observations. Again, there is much to learn about how bees integrate old and new memories in selecting dance directions.
Overall, it is clear that the bees in Swarms 1 and 2 and about half of the bees in Swarm 3 failed to update their solar ephemerides at the recipient site. We cannot rule out the possibility that some of the Swarm 3 bees re-learned, although it seems unlikely given the results from the other swarmed bees and the other possible explanations for the orientation of the Swarm 3 bees.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The failure of our bees to update their solar ephemerides when transplanted
passively is less surprising when we consider that bees are not carried to new
landscapes under natural conditions, let alone to landscapes that closely
resemble their natal ones. Bees normally do displace themselves in swarming,
however, so we initially expected bees put through a swarming process as they
were transplanted to quickly realign their ephemerides to the new site. Even
our simplest swarming process, in which the bees were re-hived 7 h after the
swarm was created (Swarm 1, Fig.
6B,C), would seem likely to cause realignment of the solar
ephemeris to the new landscape if such realignment normally occurs: bees put
through a swarming process like the one we used quickly start searching for
new nest sites, and our bees did extensive reorientation flights as they
departed their new hive for the first time
(Fig. 5). Such bees readily
adopt their new nest site, choosing the new site over their natal nest a short
distance away (Robinson and Dyer,
1993). Nonetheless, most of our swarmed bees failed to realign
their ephemerides to the recipient site. It remains possible that our swarming
processes simply omitted essential stimuli needed to trigger re-learning in
natural swarms, especially cues that may occur inside the nest starting days
or even weeks before a swarm departs
(Winston, 1987
, pp. 181-186)
or as a swarm moves into its new nest, although this seems unlikely given that
such cues are not needed to trigger reorientation to the nest itself.
The cost of the bees' failure to update their ephemerides after swarming
might be minimized by the rapid turnover of workers that normally occurs in
colonies. Visscher and Dukas
(1997), for example, found
that the mean lifespan of field bees under natural conditions was just 7.7
days. Our own (very limited) observations on this issue suggest, however, that
this rapid turnover of workers may not occur in colonies newly founded by
swarms: the foragers in our Swarm 1 colony showed greater longevity than the
bees in the non-swarmed control colony transplanted at about the same time.
Such increased longevity in swarmed bees, whatever its mechanism, is probably
necessary because newly-founded colonies need at least 3 weeks to produce a
new generation of workers. It would certainly seem advantageous for the colony
founders to update their solar ephemerides in such circumstances. This may be
why younger bees tend to depart with swarms
(Winston 1987
, p. 186);
perhaps many of the bees in natural swarms learn the solar ephemeris for the
first time at their new nest site.
Taken together, our observations seem consistent with Lindauer's hypothesis
that bees imprint on the sun's course
(Lindauer, 1971), but the
observations resonate even more with the view that sun learning in bees is
accomplished by a purpose-built, adaptively specialized cognitive `module'
(reviewed by Gallistel, 1990
;
Shettleworth, 2000
). Such
modules often fail to be affected by information manifestly important to the
animals in other contexts, a property called impenetrability or encapsulation
(Fodor, 1983
), which can leave
the animals seeming almost incredibly obtuse, like our long-term transplantees
dancing as if they had never seen the sun at the recipient site.
This constrained, modular view of sun-learning is consistent with our
understanding of how bees and ants learn the solar ephemeris function in the
first place. These insects enter the world with an innate expectation that the
sun's azimuth in the morning is opposite its azimuth in the afternoon, an
expectation that is reasonably accurate, at least in tropical latitudes
(Wehner and Müller, 1993;
Dyer and Dickinson, 1994
). The
insects need only learn the relationship between their innate ephemerides and
the local landscape and then revise the shapes of their ephemerides (more or
less depending on the latitude and season) to match the local one, using the
fixed landscape as a reference (Dyer and
Dickinson, 1994
; Dyer,
1996
,
1998
). Thus bees learn the
solar ephemeris function with much innate guidance and then seem to store the
memory in an encapsulated form resistant to, perhaps even incapable of,
revision.
Then again, a compelling question that remains is whether the bees' failure to re-learn in our experiments is attributable to the similarity of the landscapes we used. Our results suggest that the bees' solar ephemerides may be inextricably linked to the bees' representations of the landscape around the nest - the direction of the sun's movement and the detailed shape of the ephemeris are first learned, after all, using the landscape as a fixed reference - and that the system linking the ephemeris to the landscape, once formed, may represent an impenetrable module. It remains possible, however, that the ephemeris could be re-learned when bees are forced to learn a new landscape. If this were true, then the failure of swarming alone to trigger realignment of the ephemeris may not be a problem under natural conditions, as most swarms will situate themselves in novel terrains.
Bees, then, link the landscape panorama around their nest to their
celestial compass, as do ants
(Åkesson and Wehner,
2002). Bees can also link local landmarks around a feeder to
celestial cues (Dickinson,
1994
) and to other external directional cues
(Collett and Baron, 1994
;
Fry and Wehner, 2002
). But do
bees normally link panoramic landmarks more distant from the nest to their
celestial compass? Our results are consistent with Dyer's conclusion that they
do not (Dyer, 1996
). On cloudy
days, our long-term transplantees took the treeline at the recipient site to
be their natal treeline, and the bees inferred the sun's direction
accordingly. But the recipient site corresponded closely to the natal site for
only several hundred meters from the hive (or less, depending on the
direction), and bees routinely fly much farther than this. Despite ample
experience at the recipient site, our bees continued to mistake the recipient
site for their natal site for the purposes of inferring the sun's location,
suggesting that the solar ephemeris is linked to panoramic landmarks only in
the vicinity of the nest. The question deserves further work, however.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Åkesson, S. and Wehner, R. (2002). Visual navigation in desert ants Cataglyphis fortis: are snapshots coupled to a celestial frame of reference? J. Exp. Biol. 205,1971 -1978.[Medline]
Batschelet, E. (1981). Circular Statistics in Biology. London: Academic Press.
Capaldi, E. A. and Dyer, F. C. (1999). The role of orientation flights on homing performance in honeybees. J. Exp. Biol. 202,1655 -1666.[Abstract]
Capaldi, E. A., Smith, A. D., Osborne, J. L., Fahrbach, S. E., Farris, S. M., Reynolds, D. R., Edwards, A. M., Martin, A., Robinson, G. E., Poppy, G. M. et al. (2000). Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403,537 -540.[CrossRef][Medline]
Collett, T. S. and Baron, J. (1994). Biological compasses and the coordinate frame of landmark memories in honeybees. Nature 368,137 -140.[CrossRef]
Collett, T. S. and Zeil, J. (1997). The selection and use of landmarks by insects. In Orientation and Communication in Arthropods (ed. M. Lehrer), pp.41 -65. Basel, Boston, Berlin: Birkhäuser Verlag.
Collett, T. S. and Zeil, J. (1998). Places and landmarks: an arthropod perspective. In Spatial Representation in Animals (ed. S. Healy), pp. 18-53. Oxford, New York, Tokyo: Oxford University Press.
Combs, G. F. (1972). The engorgement of swarming worker honeybees. J. Apic. Res. 11,121 -128.
Conover, W. J. (1999). Practical Nonparametric Statistics (3rd edn), pp.218 -224, 291-292. New York: John Wiley and Sons.
Dickinson, J. A. (1994). Bees link local landmarks with celestial compass cues. Naturwissenschaften 81,465 -467.
Donahoe, K., Lewis, L. A. and Schneider, S. S. (2003). The role of the vibration signal in the house-hunting process of honey bee (Apis mellifera) swarms. Behav. Ecol. Sociobiol. 54,593 -600.[CrossRef]
Dyer, F. C. (1987). Memory and sun compensation in honey bees. J. Comp. Physiol. A 160,621 -633.[CrossRef]
Dyer, F. C. (1996). Spatial memory and
navigation by honeybees on the scale of the foraging range. J. Exp.
Biol. 199,147
-154.
Dyer, F. C. (1997). Spatial cognition: lessons from central-place foraging insects. In Animal Cognition in Nature (ed. R. P. Balda, I. M. Pepperberg and A. C. Kamil), pp.119 -154. New York: Academic Press.
Dyer, F. C. (1998). Cognitive ecology of navigation. In Cognitive Ecology: The Evolutionary Ecology of Information Processing and Decision Making (ed. R. Dukas), pp.201 -260. Chicago: University of Chicago Press.
Dyer, F. C. and Dickinson, J. A. (1994).
Development of sun compensation by honeybees: how partially experienced bees
estimate the sun's course. Proc. Natl. Acad. Sci. USA
91,4471
-4474.
Dyer, F. C. and Dickinson, J. A. (1996). Sun-compass learning in insects: representation in a simple mind. Curr. Dir. Psychol. Sci. 5, 67-72.[CrossRef]
Dyer, F. C. and Gould, J. L. (1981). Honey bee orientation: a backup system for cloudy days. Science 214,1041 -1042.
Esch, H. (1967). The sounds produced by swarming honey bees. Z. Vergl. Physiol. 56,408 -411.[CrossRef]
Fodor, J. A. (1983). The Modularity of Mind. Cambridge, Massachusetts: MIT Press.
Fry, S. N. and Wehner, R. (2002). Honey bees store landmarks in an egocentric frame of reference. J. Comp. Physiol. A 187,1009 -1016.[CrossRef][Medline]
Gallistel, C. R. (1990). The Organization of Learning. Cambridge, Massachusetts: MIT Press.
Gallistel, C. R. (2000). The replacement of general-purpose learning modules with adaptively specialized learning modules. In The New Cognitive Neurosciences, 2nd edn (ed. M. S. Gazzaniga), pp. 1179-1191. Cambridge, MA: MIT Press.
Gould, J. L. (1980). Sun compensation by bees. Science 207,545 -547.
Gould, J. L. (1984). Processing of sun-azimuth information by honey bees. Anim. Behav. 32,149 -152.
Labhart, T. (1999). How polarization-sensitive
interneurones of crickets see the polarization pattern of the sky: a field
study with an opto-electronic model neurone. J. Exp.
Biol. 202,757
-770.
Lehrer, M. (1993). Why do bees turn back and look? J. Comp. Physiol. A 172,549 -563.[CrossRef]
Lindauer, M. (1955). Schwarmbienen auf Wohnungssuche. Z. Vergl. Physiol. 37,263 -324.[CrossRef]
Lindauer, M. (1957). Sonnenorientierung der Bienen unter der Aequatorsonne und zur Nachtzeit. Naturwissenschaften 44,1 -6.[CrossRef]
Lindauer, M. (1959). Angeborene und erlernte Komponenten in der Sonnenorientierung der Bienen. Z. Vergl. Physiol. 42,43 -62.[CrossRef]
Lindauer, M. (1963). Komassorientierung. Ergebn. Biol. 26,158 -181.
Lindauer, M. (1971). Communication Among Social Bees. 2nd edn. Cambridge, MA: Harvard University Press.
Robinson, G. E. and Dyer, F. C. (1993). Plasticity of spatial memory in honey bees: reorientation following colony fission. Anim. Behav. 46,311 -320.[CrossRef]
Rossel, S. and Wehner, R. (1984). How bees (Apis mellifera mellifera) analyze the polarization pattern in the sky: experiments and model. J. Comp. Physiol. A 154,607 -615.
Seeley, T. D. (1977). Measurement of nest cavity volume by the honey bee (Apis mellifera). Behav. Ecol. Sociobiol. 2,201 -227.
Seeley, T. D. (1995). The Wisdom of the Hive. Cambridge, MA: Harvard University Press.
Seeley, T. D. and Tautz, J. (2001). Worker piping in honey bee swarms and its role in preparing for liftoff. J. Comp. Physiol. A 187,667 -676.[CrossRef][Medline]
Seeley, T. D., Kleinhenz, M., Bujok, B. and Tautz, J. (2003). Thorough warm-up before take-off in honey bee swarms. Naturwissenschaften 90,256 -260.[CrossRef][Medline]
Shettleworth, S. J. (1998). Cognition, Evolution, and Behavior. New York: Oxford University Press.
Shettleworth, S. J. (2000). Modularity and the evolution of cognition. In The Evolution of Cognition (ed. C. Heyes and L. Huber), pp. 43-60. Cambridge, Massachusetts: MIT Press.
Siegel, S. and Castellan, N. J., Jr (1988). Nonparametric Statistics for the Behavioural Sciences. New York: McGraw-Hill.
Towne, W. F. and Gould, J. L. (1988). Spatial precision of the honey bees' dance communication. J. Insect. Behav. 1,129 -155.[CrossRef]
Towne, W. F. and Kirchner, W. H. (1998). Honey bees fail to update their solar ephemerides after a displacement. Naturwissenschaften 85,459 -463.[CrossRef]
Visscher, P. K. and Dukas, R. (1997). Survivorship of foraging honey bees. Insectes Soc. 44, 1-5.[CrossRef]
Visscher, P. K. and Seeley, T. D. (1982). Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63,1790 -1801.
von Frisch, K. (1967). The Dance Language and Orientation of Bees. Cambridge, MA: Belknap Press of Harvard University Press.
Wehner, R. (1981). Spatial vision in arthropods. In Handbook of Sensory Physiology, vol.VII/6c (ed. H. Autrum), pp.287 -616. Berlin, Heidelberg, New York: Springer.
Wehner, R. (1994). The polarization-vision project: championing organismic biology. In Neural Basis of Behavioral Adaptation (ed. K. Schildberger and N. Elsner), pp.103 -143. Stuttgart, New York: G. Fischer.
Wehner, R. (2003). Desert ant navigation: how miniature brains solve complex tasks. J. Comp. Physiol. A 189,579 -588.
Wehner, R. and Lanfranconi, B. (1981). What do ants know about the rotation of the sky? Nature 293,731 -733.[CrossRef]
Wehner, R. and Müller, M. (1993). How do ants acquire their celestial ephemeris function? Naturwissenschaften 80,331 -333.[CrossRef]
Wehner, R. and Rossel, S. (1985). The bee's celestial compass - a case study in behavioural neurobiology. Fortschr. Zool. 31,11 -53.
Wehner, R., Michel, B. and Antonsen, P. (1996).
Visual navigation in insects: coupling of egocentric and geocentric
information. J. Exp. Biol.
199,129
-140.
Wei, C. A., Rafalko, S. L. and Dyer, F. C. (2002). Deciding to learn: modulation of learning flights in honeybees, Apis mellifera. J. Comp. Physiol. A 188,725 -737.[CrossRef]
Weidenmüller, A. and Seeley, T. D. (1999). Imprecision in waggle dances of the honeybee (Apis mellifera) for nearby food sources: error or adaptation? Behav. Ecol. Sociobiol. 46,190 -199.[CrossRef]
Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge, Massachusetts: Harvard University Press.
Zeil, J. (1993a). Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera): I. Description of flight. J. Comp. Physiol. A 172,189 -205.
Zeil, J. (1993b). Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera): II. Similarities between orientation and return flights and the use of motion parallax. J. Comp. Physiol. A 172,207 -222.
Zeil, J., Kelber, A. and Voss, R. (1996). The
structure and function of learning flights in bees and wasps. J.
Exp. Biol. 199,245
-252.