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First published online November 14, 2008
Journal of Experimental Biology 211, 3737-3743 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.003640
Honeybees can learn the relationship between the solar ephemeris and a newly-experienced landscape
Department of Biology, Kutztown University of Pennsylvania, Kutztown, PA 19530, USA
e-mail: towne{at}kutztown.edu
Accepted 6 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: honeybee, sun compass, landscape, learning, orientation
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) as a
compass, animals must know the time course of the sun's daily pattern of
azimuthal movement (the solar ephemeris function). While some animals, for
example sandhoppers, know the solar ephemeris function innately (reviewed by
Scapini, 2006), most animals
must learn it, as the sun's movements are different at different geographical
locations and times of year. The process of learning the sun's course is best
understood in desert ants (Cataglyphis), honeybees, and homing
pigeons. In the latter, the fixed reference against which the sun's movements
are learned appears to be earth's magnetic field
(Wiltschko et al., 1983)
(reviewed by Wiltschko and Wiltschko,
2003). In ants and bees, the fixed reference seems likely to be
the landscape or skyline panorama around the nest
(Dyer and Gould, 1981;
Wehner and Lanfranconi, 1981;
Dyer, 1987;
Wehner, 1996;
Towne and Moscrip, 2008),
although other possible references have not been entirely ruled out (see
Towne and Moscrip, 2008). All
three animals can approximate parts of the sun's course that they have never
seen [pigeons (Budzynski et al.,
2000); ants (Wehner and
Müller, 1993); honeybees
(Dyer and Dickinson, 1994;
Dyer and Dickinson, 1996)],
indicating that the ephemeris is learned with much innate guidance. Thus, the
learning mechanisms appear to be adaptively specialized and problem-specific
(Gallistel, 2000;
Gallistel, 2003).
Adaptively specialized, purpose-built learning mechanisms often entail
sensitive periods – developmental windows of time during which the
learning occurs best. Furthermore, the resultant memories are sometimes highly
resistant to revision with further experience; in such cases, the sensitive
periods are called critical periods (reviewed by
Knudsen, 2004). Pigeons seem
to have a sensitive period for sun-compass learning: the relationship between
the solar ephemeris function and geographic direction is learned best at a
certain developmental age but the resultant memory can be revised with
experience (Wiltschko et al.,
1976; Wiltschko et al.,
1984) (reviewed by Wiltschko
and Wiltschko, 1998), although perhaps with a time lag
(Schmidt-Koenig et al., 1991)
(reviewed by Dyer, 1998). The
possibility of a sensitive period in the sun-compass learning of ants and bees
has not been studied in detail but in bees, at least, the solar ephemeris
function seems to be acquired within several days of beginning flight
(Lindauer, 1959) (reviewed on
pp. 121–126 in Lindauer,
1971) and the ephemeris, once learned, appears to resist change.
Lindauer (Lindauer, 1957), for
example, transplanted bees from a tropical latitude where the sun, at the
time, traveled counter-clockwise to a northern latitude where the sun travels
clockwise, and his bees seemed unable to use the sun compass properly until
weeks later, probably after the transplanted foragers had been replaced by
younger bees. Based on these observations, Lindauer speculated that bees might
`become imprinted...with the direction of movement of the sun and its angular
velocity across the sky' (p. 116 in
Lindauer, 1971).
Lindauer's experiment suggests that bees may never update their memories of
the shape of the solar ephemeris function. Other experiments show that bees
sometimes also fail to update their memories of the relationship between the
solar ephemeris function and the landscape: when bees are transplanted from
their natal landscape to a panoramically similar one, the bees do not learn
the new relationship between the sun and landscape – they retain only
their memory from their natal site (Towne
and Kirchner, 1998; Towne et
al., 2005). Dyer and Gould first showed that bees learn the
relationship between the solar ephemeris and the landscape by transplanting
bees from their natal site alongside a conspicuous treeline to a differently
oriented treeline (Dyer and Gould,
1981; Dyer, 1987).
Under overcast skies, these bees oriented their communicative dances as if
they were still at their natal treeline; the bees were using a memory of the
sun's compass bearing in relation to their natal treeline at that time of day.
Furthermore, this memory appears to encompass the entire landscape panorama,
not only the bees' familiar flight route along the treeline
(Towne and Moscrip, 2008).
Towne and colleagues (Towne and Kirchner,
1998; Towne et al.,
2005) used a minor modification of Dyer's technique by allowing
the transplanted bees to live and fly at the recipient treeline for days or
weeks. Under sunny skies, these long-term transplantees saw the sun and danced
normally, as did Dyer's bees. But under subsequent overcast skies, most of the
transplanted bees oriented their dances as if they were still at their natal
treeline, even after considerable experience at the new site. The bees had
failed to learn the relationship between the solar ephemeris function and the
new treeline. This was true even when the bees were put through a swarming
process as they were transplanted, mimicking a natural process wherein bees
transplant themselves (Towne et al.,
2005).
The failure of transplanted bees to re-learn the relationship between the
solar ephemeris function and the landscape is surprising, as bees initially
learn this relationship quickly and well, and they attend carefully to both
the sun and landscape routinely as they fly. This failure could represent a
form of blocking in which a previously learned association prevents a new
association from forming (Kamin,
1969; Cheng and Spetch,
2001). In the experiments by Towne et al.
(Towne et al., 2005), the
recipient landscape closely resembled the bees' natal landscape, and several
features of the food source at the recipient site – the design of the
feeder, the scent of the food, the landmarks en route to the feeder,
the feeder's distance from the hive, the local landmarks at the feeder and the
times of day at which food was available – were all familiar. Indeed,
the only conspicuous difference between the two sites, at least in the
vicinity of the hives, was the sun's position in relation to the treelines.
Thus, the previously learned relationship between the flight route or food
source and the landscape may have blocked the formation of a new association
between the sun and the landscape. Alternatively, the bees may have failed to
update their memories of the sun–landscape relationship at the new site
because they imprint on the relationship and cannot revise the resultant
memory.
Therefore, in the present study, I ask whether bees can ever update their memories of the relationship between the sun and landscape. Specifically, I transplanted bees from their natal landscape to a panoramically dissimilar site, allowed the bees to forage at an unfamiliar food source at this site and asked whether these bees would learn the relationship between the sun and the novel landscape. The bees' natal hive was at the bottom of a thinly wooded valley, and the hive that received the transplanted bees was located alongside a sloping treeline in an entirely different landscape. After foraging at the treelined site for several days, the bees were moved to a second, mirror-image treeline on overcast mornings. The dances of these twice-transplanted bees were expected to indicate whether the bees had learned the sun's pattern of movement in relation to the treeline to which they were first moved: if the bees had learned the relationship, then their dances in the mirror-image test landscape (under overcast skies) would be based on their memory of the solar ephemeris function in relation to the first treeline. But if the bees had not learned the relationship between the solar ephemeris function and the first treeline, their dances at the test treeline (again under overcast skies) should be disoriented, as the bees would have no information as to the sun's compass bearing.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and Towne
and Moscrip (Towne and Moscrip,
2008). Feeders were generally set up for one feeding period every
day, typically about 08:00–10:00 h local solar time (LST). All
experimental bees were individually marked at the feeders with numbered tags,
and the identities of all marked bees were recorded at the feeders daily.
Hives were put in place at least four weeks before the experiments began in
order to ensure that all forager bees were indeed native to their respective
sites.
The natal site and transplantation to the training treeline
The natal hive of the experimental bees was at the bottom of a thinly
wooded valley (Fig. 1A), and
the bees visited a feeder placed approximately 2 m from the hive entrance.
Meanwhile, bees from a second hive located along a sloping treeline 2.2 km
away from the first hive visited a feeder of their own placed along the
treeline 190 m uphill to the south-southeast
(Fig. 1B) (hereafter the
`training treeline'). The training treeline was panoramically unlike the
valley site, and the feeders at the two sites were different in color, scent
and local landmarks.
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Transplantation to the test treeline
To determine whether or not the transplantees from the valley could learn
the relationship between the sun's course and the training treeline, I allowed
the valley natives to forage under sunny skies at the training treeline for at
least three days. I then transplanted the entire hive to an oppositely
oriented treeline (the `test treeline')
(Fig. 1C) on an overcast
morning. The valley natives (now twice-transplanted) and several control bees
native to the training treeline visited a feeder placed in its usual location
relative to the treeline, although now in the opposite compass direction
(Fig. 1C). The dances of the
transplantees revealed whether or not the bees knew the sun's pattern of
movement in relation to the training treeline (from which they had just been
transplanted).
Recording and analysis of dances
The directions of the bees' dances under overcast skies at the test site
were recorded on a small voice recorder by an observer at the hive, as in
Towne and Moscrip (Towne and Moscrip,
2008). Each measurement was based on the visual average of at
least five wagging runs, and each bee was scored only once for each round trip
to the feeder. Dance directions were analyzed for clustering around predicted
directions using the V-test (Batschelet,
1981). Because repeated dances by a single bee are not independent
of each other, I used the overall mean direction for each bee as a single
observation for the statistical analyses, regardless of how many dances each
bee performed. Furthermore, the statistical analyses included only well
oriented dances that occurred before the sun or blue sky first appeared;
bimodal and disoriented dances (see Results) are reported below but are
excluded from the statistical analyses as these dances gave no single
direction. Finally, sky conditions during recordings were monitored
continuously by an observer at the feeder.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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On the morning of 7 August 2005, the sky was overcast, and the hive from
the training treeline was transplanted as a whole to a second, mirror-image
treeline (the `test treeline'). The feeder was set out in its usual location
relative to the hive and treeline, although now in the opposite compass
direction (Fig. 1C). The bees
began to visit the feeder and dance at 08:00 h (LST) under a light rain, and
the dances of the marked bees were recorded at the hive for the next 1.5 h.
Before the sun first appeared at 08:38 h
(Fig. 2A,B, vertical lines),
two different control bees performed a single dance each and both oriented as
if they were still at the their natal treeline
(Fig. 2A) (`training treeline'
prediction; Ø=151 deg.; N=2 dances by 2 bees; r=0.97;
P<0.03, V-test with a predicted direction of 165 deg.). This was
more-or-less opposite the correct direction for the current site, indicating
that the control bees had mistaken the test treeline for the training treeline
(their natal site) and were dancing according to their memories of the sun's
course in relation to the latter. This is what Dyer observed in his
treeline-to-treeline transplantation experiments
(Dyer, 1987).
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The sun became continuously visible at approximately 08:50 h, and the dances of all bees soon shifted to the correct direction for the test site (Fig. 2A,B, right). The remainder of the day was partly cloudy, and the next day (8 August 2005) promised to be overcast so I left the hive at the test treeline overnight and returned at 06:00 h the next morning to perform another trial of the experiment, or to close the hive and move it back to the training treeline if the clouds failed. At 06:00 h, the sun was visible as a dim disk so I closed the hive and waited to see if the clouds would thicken. Meanwhile, several marked bees had escaped and they were excluded from the experiment. The clouds did indeed thicken such that the sun was no longer visible by 07:00 h, at which time I opened the hive and put out the feeder.
Nine different control bees native to the training treeline danced before the sun again appeared at 08:22 h, and their dances are shown in Fig. 3A. In this figure, the two bees that danced the most are distinguished with open and shaded circles and a third bee that danced toward both predicted directions at different times is shown with black triangles. The remaining six bees are all shown with black circles. Overall the dances are significantly clustered around the `test treeline' prediction (Fig. 3A) (Ø=2 deg.; N=9 bees that had performed 1–8 dances each; r=0.73; P<0.001, V-test with a predicted direction of 353.5 deg.). Seven of these bees (open and black circles) danced only according to the sun's actual location (the `test treeline' prediction), another (shaded circles) danced only according to a memory of the sun's course in relation to the bees' natal site (the `training treeline' prediction), and one other bee (black triangles) danced in both directions at different times.
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The control bees that oriented correctly
(Fig. 3A) (`test treeline'
prediction) are unlikely to have learned the sun's course in relation to the
test treeline (Towne et al.,
2005), so they were probably detecting the sun's azimuth using
weak skylight polarization or spectral cues
(Wehner and Rossel, 1985;
Wehner, 1994;
Labhart, 1999;
Hegedüs et al., 2007)
that we ourselves could not detect. The dances of the control bees, therefore,
indicate that there were probably weak celestial cues available to some of the
bees on this morning.
Numerous valley natives with experience at the training treeline (mean: 8 days; range: 3–9 days) also danced before the sun first appeared on this day, and their combined dances (Fig. 3B) are not significantly clustered around either predicted direction (Ø=242 deg.; N=28 bees that had performed 1–11 dances each; r=0.04; P>0.4, V-tests for both predicted directions), although the dances clearly cluster around the two predicted directions. Furthermore, each valley native danced consistently toward just one of the two predicted directions; typical are the dances of the two individual valley natives that danced the most this morning (distinguished by open and shaded circles in Fig. 3B). Altogether, 14 different bees danced (only) toward the `test treeline' prediction, and 14 danced (only) toward the `training treeline' prediction (ignoring bimodal and disoriented dances, which are discussed below).
These observations show that at least half of the valley natives had learned the sun's course in relation to the training treeline and that the bees were flying under a sky that allowed some of the bees to determine the sun's actual location at the test site using fresh celestial cues. When the sun eventually emerged, all of the bees shifted their dances toward the `test treeline' prediction (Fig. 3B, far right).
A few of the dances of the valley natives on 8 August 2005 were bimodal,
that is, the bees consistently indicated the two different predicted
directions on alternate wagging runs within a single bout of dancing. Such
dances occur when bees have two conflicting sources of information as to the
sun's position, in this case, a memory of the sun's course in relation to the
training treeline and weak, fresh celestial cues
(Dyer, 1984;
Dyer, 1987;
Towne et al., 2005;
Towne and Moscrip, 2008).
Moreover, these bimodal dances occur especially when bees have been dancing by
memory of their natal site and have detected conflicting celestial cues on the
preceding flight, that is, the bees were simultaneously expressing old and
newly acquired memories – from their natal site and acquired on the
preceding flight – in a single dance. Dyer discusses these dances
further (Dyer, 1984;
Dyer, 1987). A typical pattern
can be seen in Fig. 3B, where
the individual bee whose dances are shown with shaded circles danced first
toward the `training treeline' prediction, then bimodally after a flight under
clearing skies (two shaded circles with dots in the center connected by a
broken vertical line), and finally toward the `test treeline' prediction.
Altogether on this day, six different bees performed a total of nine bimodal
dances (Fig. 3, broken vertical
lines connecting two dance directions), and all but one of these bees had
danced first according to a memory of the sun's course at the training
treeline; the other bee danced bimodally on her first dance. Overall, the
bimodal dances are consistent with the results of the well oriented (unimodal)
dances discussed above: there were weak celestial cues available throughout
the morning but some of the bees nonetheless initially danced according to
their memories of the sun's course in relation to the training treeline,
indicating that they had learned that relationship.
On this same morning, two different bees performed a total of four
disoriented dances, which had distinct but inconsistently oriented wagging
segments (Fig. 3B, shaded
triangles on the bottom axis). All of these dances occurred just before or
after the same bee danced bimodally, suggesting that disoriented dances can
result when bees are forced to orient by conflicting or ambiguous cues. Towne
et al. (Towne et al., 2005)
and Towne and Moscrip (Towne and Moscrip,
2008) have observed disoriented dances under similar
conditions.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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),
although it is possible that the sun's ephemeris is learned first with respect
to another reference and only later connected to the landscape (see
Towne and Moscrip, 2008).
Thereafter, experienced bees retain the spatial connection between the solar
ephemeris and the landscape and can recall the sun's compass bearing at any
time of day using the landscape alone
(Dyer, 1987). Moreover, the
relevant landscape memory seems to encompass the entire landscape panorama,
not only familiar flight routes (Towne and
Moscrip, 2008). Once acquired, the bees' memory of the spatial
relationship between the solar ephemeris and the landscape sometimes strongly
resists revision: when bees trained to visit a feeder placed alongside a
treeline at their natal site are transplanted to a differently oriented
treeline, most or all of the bees fail to update their memories of the
relationship between the sun's ephemeris and the new treeline, at least when
they forage at a familiar feeder in a (seemingly) familiar location along the
new treeline. This is true even for bees that are put through a swarming
process as they are transplanted and even if the bees have ample experience at
the new site (Towne et al.,
2005). One possible explanation for these observations is that the
learned relationship between the sun and landscape is imprinted and
unchangeable.
I show here, however, that experienced bees can learn the relationship
between the solar ephemeris function and an entirely novel landscape, that is,
a landscape panoramically unlike the bees' natal one. Specifically, bees
transplanted from their natal site at the bottom of a thinly wooded valley to
a second site dominated by a sloping treeline were able to learn the
relationship between the solar ephemeris and the treeline. This result
contrasts starkly with those of previous treeline-to-treeline transplantation
experiments (Towne et al.,
2005). It remains possible that bees imprint on the relationship
between the sun's ephemeris and their natal landscape but can replace the
memory – or add a new one – only when the visual scenery around
the nest must be learned anew. But it is also possible that bees do not
imprint on the sun–landscape relationship and that the similarities of
the flight routes and feeders at the source and recipient sites blocked the
bees' re-learning in previous treeline-to-treeline transplantation
experiments. In this context, it would be useful to know whether bees would
update their memories of the sun–landscape relationship if they were
transplanted between panoramically similar sites and forced to forage at
entirely novel food sources at the recipient site. The latter experiment has
yet to be done.
If the bees' memory of the relationship between the sun's pattern of
movement and the landscape is updated only when the visual scenery around the
nest must be learned anew, would this mean that the stored ephemeris function
is inextricably tied to the landscape in which it was learned? In one sense,
certainly not, as the mature ephemeris function has been shown to function in
any landscape, familiar or not. If, for example, a hive is transplanted into
unfamiliar terrain, the bees can use their skylight compass to find a feeder
in a familiar compass direction (pp. 333–338 in
von Frisch, 1967), (pp.
112–118 in Lindauer,
1971). And bees and ants both routinely use their skylight compass
in path integration, the process by which they integrate the various legs of a
meandering journey to a food source in order to return home (and in bees, in
order to dance), even if the trip takes the insects into unfamiliar territory
[bees (reviewed by Collett and Collett,
2000; Menzel et al.,
2006); ants (Wehner et al.,
1996; Wehner,
2003; Wehner and Srinivasan,
2003)]. Bees also use their sun compass as a directional reference
in learning landmarks at a feeder
(Dickinson, 1994), as do ants
in learning landmarks around their nests
(Åkesson and Wehner,
2002).
Given the usefulness of a portable sun compass, one wonders why bees retain
the relationship between their natal landscape and the sun's ephemeris so
strongly. If bees use the landscape as the fixed reference against which the
solar ephemeris is first learned, which is likely but uncertain
(Towne and Moscrip, 2008),
then bees must learn the spatial relationship between the sun and landscape in
order to learn the shape of ephemeris at all. This would be true, in fact, for
any animal that relies on the landscape as the reference for solar ephemeris
learning (Dyer, 1984;
Dyer, 1987). It would then be a
very small step for the bees to retain this relationship after the learning is
done, which would allow the bees to use the dance communication on overcast
days (Dyer and Gould, 1981;
Towne and Moscrip, 2008). This
is the only obvious benefit of retaining the relationship, but perhaps this is
benefit enough, as the only cost would be the production of navigational
errors when the bees happen to move into a new landscape that resembles their
natal one, and even then only under overcast skies. In this context, it would
be interesting to know whether ants – which have no communication system
that requires all individuals to know the sun's compass bearing around the
nest at all times – permanently retain a strong connection between the
solar ephemeris function and the landscape in which it is learned.
When ants and bees learn the solar ephemeris function for the first time,
they begin with an innate expectation that the sun's azimuth in the morning is
180 deg. from its azimuth in the afternoon [ants
(Wehner and Müller,
1993); bees (Dyer and
Dickinson, 1994)]. The insects then fill in the details of the
local ephemeris function with experience
(Lindauer, 1959) (reviewed by
Dyer, 1996), interpolating
between observed positions of the sun to estimate unobserved positions or
positions that cannot be resolved, as when the sun is near the zenith [bees
(New and New, 1962;
Dyer, 1987); ants
(Wehner and Lanfranconi,
1981)]. It may be that the bees in the current experiments
re-learned the solar ephemeris function in the novel landscape (the training
treeline) as if they were learning it anew, that is, beginning (again) with
their innate 180 deg. step-function ephemeris. A long-distance transplantation
experiment by Lindauer (Lindauer,
1957) suggests, however, that the bees simply brought their mature
ephemerides into the correct relationship with the new landscape: Lindauer
transplanted a colony of bees from a tropical location to a northern one where
the sun and skylight patterns rotated in the opposite direction, and the
displaced bees seemed unable to use, or learn to use, the skylight compass at
the northern site (although Lindauer did not mark individual bees, so one
cannot be certain). If true, this implies that the shape of the solar
ephemeris function – that is, the sun's direction of movement and its
varying speed throughout the day – is learned during a critical period
after which the function is permanently fixed in the bees' memory. This
hypothesis could now be tested using the re-learning reported in the present
study.
Our current working hypotheses regarding how bees learn the solar ephemeris
function can be summarized as follows. First, the shape of the solar ephemeris
function is learned as each bee begins to fly, starting with an innate
expectation that the sun's compass bearing in the morning is opposite to its
bearing in the afternoon (Dyer and
Dickinson, 1994). Second, this learning occurs during a critical
period, in that the shape of the function, once acquired, becomes permanently
fixed in the bees' memory. While this second hypothesis is consistent with the
available evidence, as discussed above, it has yet to be rigorously tested.
Third, the spatial relationship between the ephemeris function and the natal
landscape may also be learned during the same critical period, as the
landscape is probably the frame of reference against which the shape of the
ephemeris is first learned (Dyer,
1987; Towne and Moscrip,
2008), and at some point the ephemeris becomes permanently linked
to the bees' memory of the landscape or skyline panorama around the nest
(Towne et al., 2005;
Towne and Moscrip, 2008).
Finally, however, the stored ephemeris can be used for sun-compass orientation
independently of the landscape, and the relationship between the sun and
landscape can be updated in novel landscapes or, possibly, if bees are forced
to visit novel food sources in familiar landscapes.
Many important details remain unknown but it is clear that the behavioral mechanisms underlying the bees' learning of the solar ephemeris function – and re-learning, to the extent that it happens – are highly specialized. Furthermore, although these mechanisms can yield nonsensical behavior when presented with unnatural situations, as when bees fail to update their memories of the relationship between their solar ephemeris and a new landscape that happens to be a panoramic twin of their natal one, the mechanisms accomplish their task quickly and well under natural conditions.
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Acknowledgments |
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  W. F. Towne and H. Moscrip The connection between landscapes and the solar ephemeris in honeybees J. Exp. Biol., December 1, 2008; 211(23): 3729 - 3736. [Abstract] [Full Text] [PDF]
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