Bumblebee search time without ultraviolet light
1 Zoologie II, Biozentrum, Universität Würzburg, Am Hubland, 97074
Würzburg, Germany
2 School of Biological Sciences, Queen Mary, University of London, Mile End
Road, London E1 4NS, UK
3 School of Orthoptics, Faculty of Health Sciences, La Trobe University,
Bundoora Victoria 3086, Australia
* Author for correspondence (e-mail: a.dyer{at}latrobe.edu.au)
Accepted 16 February 2004
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Summary |
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Key words: ultraviolet, vision, foraging efficiency, greenhouse, bumblebee, Bombus terrestris
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Introduction |
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One important example of a greenhouse crop is the tomato Lycopersicon
esculentum Mill. (Morandin et al.,
2001a,
b
,
c
). The pollination of tomato
plant flowers requires the agitation of flower anther cones to release pollen
(Buchman, 1983) and efficient pollination is achieved either by the use of
electronic vibrating systems (Picken,
1984
), or more recently by the use of bumblebees
(Banda and Paxton 1991
;
Kevan et al., 1991
;
van Ravestijn and van der Sande,
1991
).
There is evidence that bees perceive changes in the ultraviolet content of
illumination. For example, Morandin et al.
(2001b) found that in
commercial greenhouses fitted with ultraviolet-transmitting plastic the mean
activity of individual bumblebees Bombus impatiens was
4.82±0.37 trips per day, whilst in commercial greenhouses that excluded
ultraviolet radiation the activity averaged 2.37±0.37 trips per day.
Increased activity in greenhouse environments that transmit more ultraviolet
radiation has also been reported for several other species of insects
(Antignus et al., 1996
;
Costa and Robb, 1999
;
Costa et al., 2002
). However,
in a study using miniature greenhouses in a tightly controlled environment
Morandin et al. (2002
) did not
find that bumblebees were more active under high UV-transmitting
coverings.
To estimate the number of bumblebees required to pollinate greenhouse crops
efficiently it is important to understand the ability of individual bees to
operate visually under conditions where ultraviolet radiation is excluded from
the foraging environment. Spaethe et al.
(2001) showed that search time
is an important parameter for the efficiency with which the bees are able to
make visits to flowers. For large flowers, search time correlated well with
colour contrast, whilst for small flowers search time was more likely to be
explained by green receptor contrast
(Spaethe et al., 2001
). The
spectral signal reflected by a flower to a bee's eye is the product of the
spectral properties of the flower's pigments and the spectral quality of the
radiation source illuminating the flower
(Kevan and Backhaus, 1998
). It
is thus important that bees are able to discount efficiently any effects of
changes in illumination colour, otherwise the value of having colour vision
could be compromised (Dyer,
1998
). It has been demonstrated that bees have the ability to make
a correction for changes in illumination colour
(Neumeyer, 1981
;
Werner et al., 1988
), a
phenomena termed colour constancy. However, it is likely that the mechanism(s)
of colour constancy is imperfect in bees (Dyer,
1998
,
1999
;
Dyer and Chittka, 2004
), and
it is important to understand how the bee's visual system might deal with the
exclusion of ultraviolet radiation from an illumination source.
This study evaluates bumblebee efficiency at finding model tomato flowers
in ultraviolet-rich (UV+) and ultraviolet-poor (UV) illumination
conditions, and the results are interpreted in relation to a colorimetric
analysis of the experimental variables. Most commercial crops are planted with
a single species in a greenhouse (e.g.
Morandin et al., 2001a) and
this study considers search efficiency for a single type of flower rather than
the ability to choose between flowers of different coloration.
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Materials and methods |
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Illumination was provided by six Duro-test 40 W True-Lite tubes and one Osram 36 W Blacklight tube mounted 115 cm above the arena floor (tube frequency converted to 1200 Hz). Illumination was diffused by a Rosco 216 white diffusion (ultraviolet transmitting) screen (Rosco, Germany). For an UV+ environment the illumination was not filtered, and for an UVenvironment an Arri 226 (Munich, Germany) ultraviolet-blocking filter covered the illumination. Spectral irradiance of these the sources was measured with an Ocean Optics (Dunedin, FL S2000, Dunedin, FL, USA) spectrometer relative to a calibrated deuterium/halogen radiation source (DH-2000-CAL) (Fig. 1A).
|
Flower colour for bumblebee vision
Spectral reflectance of a freshly opened tomato flower was measured using
the Ocean Optics spectrometer (Fig.
1B). A variety of plastic yellow surfaces were also tested to find
a surface that had similar spectral reflectance properties to the tomato
flower. A plastic yellow flooring tape (Tape Pacific, NSW, Australia) had
similar spectral characteristics to the yellow tomato flower, including
ultraviolet reflectance (Fig.
1B), and was used to make model flowers. This was done by
attaching the tape to a thin plastic surface and using a punch to make 15 mm
diameter model flowers, or hand cutting starshaped model flowers with a
maximum distance of 26 mm between the opposing points.
To represent the colour loci of the tomato and model flower in a colour
space for the two illumination conditions a hexagon colour space was used
(Chittka, 1992).
The relative amount of light absorbed by each photoreceptor class is given
by P:
![]() | (1) |
The variable R is the adaptation coefficient, which assumes
adaptation to the green painted background (IB),
![]() | (2) |
![]() | (3) |
Loci were calculated considering that the bees' visual system was adapted
to the green background such that E equals 0.5 in each photoreceptor
(Equation 3). The excitation of
each photoreceptor can vary between 0 and 1.0, and so the maximum contrast in
the green photoreceptor is 0.5 (Spaethe et
al., 2001). The colour contrast that a flower makes with the
background ranges from 0 at the centre of the hexagon to 1.0 at the corners of
the hexagon (Chittka, 1992
;
Spaethe et al., 2001
).
Search time
To evaluate search time for model flowers we used a similar methodology to
Spaethe et al. (2001), testing
one bee at a time. Three model flowers were presented in the arena arranged in
the corners of an equilateral triangle shape with a side length of 30 cm. In
each foraging bout the triangle position was randomly located on the arena
floor, and between each bout the flowers and floor were washed with 30%
alcohol to eliminate any use of olfactory cues. A 15 µl drop of 2 mol
l1 sucrose solution was placed in the center of each model
flower. A digital timer was used to measure the flight time from when a bee
started foraging until a flower was landed on. Time spent on flowers drinking
the sucrose solution was excluded. After a bee had visited all three flowers
it was then fed using a micropipette at one of the model flowers until
satiated, at which stage it returned to the nest box and the foraging bout
concluded.
Each bee was tested for a total of 20 bouts, ten bouts in one illumination
condition and ten bouts in the alternative illumination condition. The
illumination was changed at the completion of the 10th foraging bout when the
bee had returned to the nest box. In each bout the search time for landing on
the first flower, and then the search time to find subsequent flowers was
measured. To exclude the distance variability introduced by the random
positioning of triangle in the arena, the time it took from leaving the first
flower until landing on the second flower was statistically evaluated
(Spaethe et al., 2001).
Experiment 1: 26 mm star model flowers
Five bees were individually tested to evaluate efficiency at finding 26 mm
star model flowers. Each bee was tested in the UV+ illumination for 10 bouts,
and then in the UVillumination for ten bouts. To measure search
efficiency the flight times between the first and second flower within the
equilateral triangle were compared for the UV+ and UVillumination
conditions. Data for search efficiency was analyzed for the last five bouts of
each illumination condition, so that the bees had an opportunity to
familiarize themselves with the condition.
To measure the bees' perception of illumination change, the search time to the first flower within the triangle was also evaluated. Whilst this introduces a variable of distance, search time for the first flower tests whether or not the bees perceive a change in flower colour when illumination conditions change.
Experiment 2: 15 mm model flowers
In this experiment we used 15 mm model flowers to evaluate the bees' search
efficiency. Ten bees were evaluated and the sequence order of illumination
conditions being tested was reversed for five of the bees. This tested if bees
perceive an illumination change when ultraviolet was either added or removed
from the lighting environment. The bees' perception of a change in
illumination conditions was evaluated with the search time to find the first
flower.
To measure search efficiency the flight times between the first and second flower within the equilateral triangle were compared for the UV+ and UVillumination conditions. Data for search efficiency were analyzed for the last five bouts of each illumination condition, so that the bees had an opportunity to familiarize themselves with the condition.
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Results |
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Experiment 1: 26 mm star model flowers
Five bees were tested for their ability to find flowers in a UV+
environment, and then in an UVenvironment.
Fig. 2A shows the search time
required to find the first flower in the equilateral triangle over the course
of 20 foraging bouts. The bees also made a number of abortive flights (bees
approached a model flower but did not land on it) immediately following the
illumination change. In the five bouts before the illumination change there
were no abortive flights by the five bees, but in the bout following the
illumination change bees made several abortive flights (mean ±
S.E.M. = 3.6±0.3, N=5). The reaction of the bees
clearly shows that the change in illumination was perceived as there is a
sevenfold increase in mean search time for the 11th foraging bout. This
increase in search time for the 11th bout was likely to be mainly because of
flights where bees approached flowers but did not to land. However, the
increase in search time does not remain high for subsequent foraging bouts
(Fig. 2A) and it appears that
the bees quickly learn to find the model flower in the changed illumination
conditions.
|
To exclude the variability introduced by the random positioning of the
first flower the search times between the 1st and 2nd flowers were evaluated
(Spaethe et al., 2001). The
search time in the UV+ environment (mean ± S.E.M. =
3.3±0.2 s, N=5) was not significantly different from the
search time in the UVenvironment (mean ± S.E.M. =
3.2±0.2 s, N=5) (paired samples t-test N=5,
t=0.910, d.f.=4, P=0.414).
Experiment 2: 15 mm model flowers
Five bees were tested first in a UV+ environment and then a
UVenvironment. Fig. 2B
shows the bees' search time for the first flower in the equilateral triangle
over the course of 20 foraging bouts. There was a 13-fold increase in the mean
search time for the first flower immediately following the switch from the UV+
to UVenvironment. However, the search time in subsequent bouts shows
that the bees quickly learn to operate in an UVenvironment
(Fig. 2B).
A separate group of five bees was tested in the reverse order so that initial testing was in UVillumination, followed by UV+ illumination. Fig. 2C shows that the bees also perceive this change in illumination conditions as the search time showed a sevenfold increase in search time for the UV+ environment. As with the results for experiments described above, the bees quickly learn to operate in the changed illumination conditions (Fig. 2C).
To compare the efficiency for finding the 15 mm flowers the search times in a UV+ environment were grouped (mean ± S.E.M. = 4.3±0.5 s, N=10) and compared to the search times for finding flowers in a UVenvironment (mean ± S.E.M. = 4.6±0.6 s, N=10). These results were not statistically significantly different (paired samples t-test N=10, t=0.487, d.f.=9, P=0.638). This is in agreement with the findings of experiment 1 that bumblebee search efficiency is not affected by the presence of a UV+ or UVillumination environment, at least for the stimuli tested here.
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Discussion |
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The colour hexagon has a built-in assumption of adaptation to the
background stimulus that simulates von Kries colour constancy. However, the
von Kries model of colour constancy does not predict a perfect colour
correction for bee photoreceptors (Dyer,
1999). Indeed the colour hexagon predicts a colour shift of 0.08
units when the illumination changes from UV+ to UV, and this is
qualitatively consistent with the bees' change in behaviour
(Fig. 2). When the ultraviolet
content of the illumination was modified the bees initially made several
abortive flights in which they approached flowers but did not land. This
behaviour continued whilst the bees continued to search the arena, but
eventually the bees did land on the model flowers. This behaviour might be
explained by the bees eventually making a switch flight
(Chittka et al., 1997
) to a
colour that they perceived as being different to the colour they had learnt in
the initial stages of foraging.
Experiments 1 and 2 showed that bumblebee efficiency in finding model
flowers was not influenced by the inclusion or exclusion of ultraviolet
radiation. This result is consistent with the predictions that flower colour
contrast and green contrast are similar in UV+ and UVconditions
(Table 1). A variety of studies
have evaluated the merits of using greenhouse coverings that have the ability
to transmit ultraviolet radiation. For example, Morandin et al.
(2002) found that greenhouses
with UV+ coverings were less likely to suffer from the loss of bumblebees
through vents than greenhouses with UVcoverings. This is probably
because when UVcoverings are used the UV+ vents make a higher colour
contrast and the bees may exhibit positive phototaxic behavior towards the UV+
(Morandin et al., 2002
). There
is some evidence to suggest that in UV+ environments bees are more active
(Costa and Robb, 1999
;
Morandin et al., 2001b
;
Costa et al., 2002
), although
this was not found in the Morandin et al.
(2002
) study. The possibility
that bees might not forage as efficiently in UVenvironments
(Morandin et al., 2001b
) is
likely to be because bees are attracted to any UV+ conditions, so in large
greenhouses with UVcoverings bees seek out any UV+ illumination sources
(such as vents). However, when UV is totally excluded from the foraging
environment the ability of bees to use their visual system to find flowers is
not adversely affected.
Conclusion
The results of the current study show that, whilst bumblebees perceive a
change when ultraviolet radiation is either included or excluded from an
illumination source, the efficiency with which bumblebees use their vision to
find important greenhouse crop flowers is not affected by the type of
greenhouse covering.
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Acknowledgments |
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