The role of UV in crab spider signals: effects on perception by prey and predators
1 Department of Biological Sciences, Macquarie University, North Ryde, 2109
NSW Australia
2 Centre for the Integrative Study of Animal Behaviour, Macquarie
University, North Ryde, 2109 NSW Australia
3 School of Biological Sciences, Queen Mary College, University of London,
Mile End Road, London E1 4NS, UK
* Author for correspondence (e-mail: astrid.heiling{at}univie.ac.at)
Accepted 25 August 2005
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Summary |
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Key words: Thomisus spectabilis, Apis mellifera, communication, vision, colour signal, ultraviolet
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Introduction |
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Photospectrometry allows us to measure the reflectance of objects, and
advances in neuroethology allow us to calculate the effects of the reflectance
on the perceptual system of some receivers
(Peitsch et al., 1992;
Chittka, 1996
;
Hart et al., 2000
).
The UV component in visual signals has increasingly attracted the attention
of scientists (e.g. Hunt et al.,
2001; Shi and Yokoyama,
2003
; Kellie et al.,
2004
). UV light, however, typically affects more than one receptor
type, and thus can have multiple effects on the visual systems of receivers.
This arises because the sensitivity spectra of different visual receptors
often overlap, and specifically because the sensitivity of long-wavelength
receptors extends into the UV (Stavenga et
al., 1993
). Spectral sensitivity curves need to overlap in order
to convey colour information optimally
(Chittka, 1996
). It is
therefore important to analyse the effects of physical changes in the
electromagnetic reflectance of signals on every visual receptor of
receivers.
Furthermore, visual signals can only be perceived if they are
distinguishable from background noise
(Chittka et al., 1994;
Endler, 1999
), and their
visibility depends on the ambient light conditions and their contrast against
the background colour (Endler,
1991
,
1993
,
1999
;
Vorobyev and Osorio, 1998
;
Fleishman and Persons, 2001
;
Spaethe et al., 2001
;
Heindl and Winkler, 2003
).
Insects, for example, respond to visual signals based on the contrast between
an object and the environment, involving all types of photoreceptors (e.g.
Briscoe and Chittka, 2001
).
A thorough study of visual signals must therefore trace the effects of
light reflectance on photoreceptor excitations and calculate the contrast of
colour stimuli against background colour. Several authors have taken this
approach, using known values for receptor sensitivity to calculate the
relative excitations of different photoreceptors by a colour stimulus and,
based on these, the colour contrast between a stimulus and the background
(Chittka, 1996,
2001
;
Endler and Théry, 1996
;
Andersson et al., 1998
;
Osorio et al., 1999
;
Spaethe et al., 2001
;
Théry and Casas, 2002
;
Théry et al., 2005
). We
followed this approach by studying the signalling communication between
Australian crab spiders Thomisus spectabilis and two types of prey,
European honeybees Apis mellifera
(Heiling et al., 2003
) and
Australian native bees Australoplebia australis
(Heiling and Herberstein,
2004
). The spiders ambush pollinating insects on flowers, and are
visually perceived by bees (Heiling et
al., 2003
; Heiling and
Herberstein, 2004
). Honeybees prefer to land on flowers with crab
spiders sitting on them rather than unoccupied flowers
(Heiling et al., 2003
).
Australian native bees are also attracted to spider-occupied flowers, but
unlike the introduced European bees, do not land on them
(Heiling and Herberstein,
2004
). We found that, in contrast to European crab spiders
(Chittka, 2001
;
Théry and Casas, 2002
;
Théry et al., 2005
),
T. spectabilis reflects more light in the UV than the flowers do
(Heiling et al., 2003
).
UV-reflecting white flowers are rare in nature
(Chittka et al., 1994
) and
therefore white, UV reflecting spiders will appear conspicuous on most
flowers. They attract honeybees to flowers by creating a pronounced UV
contrast and consequently a pronounced overall colour contrast
(Heiling et al., 2003
). The
latter result suggests that the spiders' UV reflection is largely responsible
for the bees' attraction to spider-occupied flowers. Here, we test this
assumption by removing UV reflection from T. spectabilis with an
UV-absorbent substance and observing the response of honeybees. We predict
that the manipulation will make spider-occupied flowers less attractive to
honeybees. Furthermore, we demonstrate how such a manipulation is perceived by
the visual system of honeybees and also a potential predator, a passerine
insectivorous bird.
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Materials and methods |
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Manipulation of spider colour
To investigate whether the UV-reflection of T. spectabilis affects
the response of honeybees, we applied a mixture of two different UV
light-absorbing chromophores on adult female spiders. The chromophores, both
common ingredients in sunscreens, were
2-ethylhexyl-p-methoxycinnamate (Parsol® MCX), an UV-B
light absorber, and 4-tert-butyl-4'-methoxydibenzoylmethane
(Parsol® 1789), an UV-A light absorber. The spiders
(N=28) were briefly brushed with the mixture. By covering the
spiders' body surfaces using Parsol® (DSM, Heerden, The
Netherlands), we were able to cut off any reflectance of light below 395 nm
(Fig. 1).
|
Colour analyses of T. spectabilis and C. frutescens
We measured spider and flower reflectance using a USB 2000 spectrometer
with a PX-2-pulsed xenon light source attached to a PC running OODBase32
software (Ocean Optics Inc., Dunedin, FL, USA). The measurements covered the
range from 300 nm to 700 nm. Each spider and flower was measured six times and
the median value taken for further calculations. We calculated the relative
receptor excitation values (E) for the different types of
photoreceptors of honeybees, which have peak sensitivities in the UV, the blue
and the green (for methods, see Chittka,
1996; Briscoe and Chittka,
2001
). Receptor voltage signals E were also calculated
for passerine insectivorous birds (blue tits), which have tetrachromatic
vision, with their receptor sensitivities peaking in the UV (UVS), blue (SWS),
green (MWS) and red (LWS; Hart,
2001
).
We included blue tits as a model for avian predators, even though this
particular species is not a natural predator of T. spectabilis. The
spiders are often predated upon by other species of passerine songbirds, such
as noisy miners Manorina melanocephala (A. M. Heiling, personal
observation), but the receptor sensitivities of these have not been studied.
All passeriform birds studied so far possess a tetrachromatic set of cones,
with little interspecific variation in the tuning of photopigments
(Bowmaker et al., 1997;
Cuthill et al., 2000
;
Hart, 2001
). Among 12
different passerines studied, for example, the wavelengths of maximum
absorbance ranged from only 355-380 nm for the UV pigment, 440454 nm
for the short-wave pigment, 497504 nm for the medium-wave pigment, and
557567 for the long-wave pigment (summarised in
Hart, 2001
). The blue tit thus
serves as a typical example of a passerine predator of crab spiders.
The calculations of E-values generate the proportion of the
maximum potential excitation in each receptor type. Based on the
E-values, we determined the colour loci in the hexagon colour space
of honeybees (Chittka et al.,
1994) and of blue tits (a tetrahedron;
Goldsmith, 1990
). For honeybee
vision, we illustrated the colour space, which is based on two colour opponent
processes (Backhaus, 1991
) and
shows how the colour of the spiders and flowers is perceived
(Chittka, 1996
). Specifically,
a colour's angular position in the colour hexagon indicates a bee-subjective
hue, while increasing distance from the centre of the hexagon indicates
increasing spectral purity or saturation.
We used the colour coordinates in the colour spaces of honeybees and blue
tits to calculate the Euclidean distances. These calculations were performed
for each spider-flower combination used in the experiments. Euclidean distance
in the colour hexagon is correlated with the colour contrast as perceived by
the bee receiver of visual signals
(Chittka, 1996;
Théry et al., 2005
).
This approach takes into consideration the colour opponent processes that
influence how the brain integrates a colour signal
(Chittka, 1996
).
The identification of UV, blue and green through a bee's eye relies on
different neuronal channels (Giurfa and
Lehrer, 2001). An object seen at an area subtending at least
5° (and no more than 15°) is perceived by the green receptor of bees
(Giurfa and Lehrer, 2001
;
Spaethe et al., 2001
). For a
bee to perceive signals using all three spectral receptor types, the stimulus
must subtend an area of at least 15°, which corresponds to 59 ommatidia of
its compound eye. Hence, compared to green contrast, colour contrast is
perceived from a shorter distance to an object. Moreover, the sensitivity of
bees in the UV is 16 times higher compared to the sensitivity in the blue and
in the green (Helversen, 1972). The sensitivities of photoreceptors are
adjusted to the quantity of light reflected from the predominant background.
Due to the low reflectance of UV from green foliage background
(Chittka et al., 1994
), the UV
receptor is relatively more sensitive. Similarly, the sensitivities of the
four cone types of passerine birds (UVS, SWS, MWS and LWS) peak in different
regions of the light spectrum, with a combination of MWS and LWS receptors
(double cones) used for detecting achromatic contrast between objects and all
four types of cones responsible for the detection of colour contrast (e.g.
Hart et al., 2000
). For these
reasons, we compared not only the overall contrast between spiders and daisies
from the view of honeybees and blue tits, but also the specific contrasts for
the different receptor types.
We used exact binomial P-tests to assess honeybee choice between
flowers occupied by UV spiders or UV+ spiders vs vacant
flowers. Independent t-tests were used to compare spider mass,
E-values and contrasts between UV spiders and UV+ spiders. The
t-tests considered the variances within groups, and in the case of
unequal variances, we used independent t-tests that output fractional
degrees of freedom (for methods, see
Satterthwaite, 1946).
Furthermore, we used MannWhitney U-tests to compare colour
contrasts between spider-flower combinations that were chosen or rejected by
honeybees.
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Results |
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Effect of a spider's presence on the choice of honeybees
The presence of both UV spiders and UV+ spiders clearly affected the
response of European honeybees, but in different ways. While the presence of
UV+ spiders attracted honeybees to flowers
(Heiling et al., 2003;
Fig. 2), UV spiders
deterred them. When given the choice between a daisy occupied by a UV
spider and a vacant daisy, bees clearly preferred the vacant daisy over the
spider occupied one (exact binomial P=0.0257, N=28;
Fig. 2).
|
|
|
The colour of UV+ spiders (described in
Heiling et al., 2003;
N=25) and UV spiders (N=28) generated different
contrasts against the petals of white daisies
(Fig. 4). For honeybees, the
UV spiders against the white petals of daisies created a lower contrast
in the UV (t31.12=9.746, P<0.001). However,
there were no differences in blue contrast and green contrast between UV+
spiders and daisies and UV spiders and daisies
(t51=0.38, P=0.722 and
t51=0.362, P=0.719, respectively;
Fig. 4).
|
Furthermore, in both choice experiments using UV+ spiders and UV spiders, there was no difference in colour contrast between spiderflower combinations that were chosen and those that were rejected by honeybees (Median ± Qi, Qs=0.152±0.126, 0.177, MannWhitney U=54, P=0.849, N=25 and Median ± Qi, Qs=0.0363±0.0197, 0.0472, Mann Whitney U=67, P=0.27, N=28).
From the view of blue tits, UV spiders created a lower contrast in the UV receptor than UV+ spiders (t51=10.701, P<0.001), but a similar contrast in the blue (t48.34=0.178, P=0.86), green (t46.71=0.276, P=0.784), and red receptors (t44.61=0.775, P=0.443; Fig. 4). This combination of spiders and daisies also generated a lower overall colour contrast (t51=12.528, P<0.001; Fig. 4). While the UVS-contrast and the overall colour contrast created by UV spiders on daisies just reached the detection threshold of birds (0.06; Théry and Casas, 2005; Fig. 4), UV+ spiders were well distinguishable from daisy petals by UVS contrast and colour contrast (Fig. 4). The contrasts between both UV+ and UV spiders and daisies in the blue, the green, and the red were far below the detection threshold of birds (Fig. 4).
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Discussion |
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Not surprisingly, our comparison of reflectance data between UV+ spiders and UV spiders revealed different excitation values in the UV for both the honeybee (EUV) and the bird visual system (EUVS), with UV+ spiders inducing a stronger response by the UV-photoreceptors than UV spiders. However, our analyses of the visual appearance of crab spiders revealed that UV+ spiders and UV spiders are not equally perceived beyond the UV spectrum by both honeybees and blue tits. UV+ spiders and UV spiders also differed in the excitations of the green, the blue and, in the case of birds, the red receptors. For both honeybees and birds, UV+ spiders caused significantly lower excitations of these receptor types than UV spiders did. To explain these results we performed additional reflectance measurements on five T. spectabilis, which revealed an average reflectance of 76% above 400nm before and after the treatment with Parsol®. We found that the increased reflectance of UV spiders above 400 nm was not caused by the application of Parsol®. Instead, it might have been caused by the housing conditions of spiders. The spiders were fed a diet of crickets and fruit flies, which may have affected their colouration. Moreover, UV+ spiders were kept in the laboratory for a longer period of time than UV spiders. This means that, at the time of experimentation, UV+ spiders were older than UV spiders, which might have also affected the reflectance properties of spiders. However, the critical values that bees and birds use to distinguish signals are not the receptor excitation values per se, but the colour contrast of the signal against its natural background. Here, our results show no difference between UV+ spiders and UV spiders in contrast other than in the UV. Thus, we are confident that despite natural noise in spider colour, our treatment with Parsol® only manipulated UV-reflection and that honeybees reacted to this manipulation only.
The elimination of UV-reflection from visual signals in other systems such
as in the social interactions in birds affected the behaviour during
femalemale or malemale interactions
(Andersson and Amundsen, 1997;
Sheldon et al., 1999
;
Alonso-Alvarez et al., 2004
).
Like our results, these studies on birds provide strong evidence that the
removal of the UV component from the signal (male plumage) causes the observed
changes in behaviour. Our additional photospectrometric analyses and
calculations of receptor excitations, however, reveal the aspects of the
perceptual changes that may be responsible for these effects.
Different visual systems will not perceive and process the colour of an
object equally, if different types of photoreceptors with different
sensitivities are involved in colour vision (e.g.
Endler, 1990). For example,
flowers that reflect in the UV and in the red range of the electromagnetic
spectrum, will appear ultraviolet to a UV-blue-green-trichromatic bee and red
to our blue-green-red-trichromatic visual system
(Chittka et al., 1994
). In the
visual systems of honeybees and blue tits, the peak spectral absorbance of
their photoreceptors lies in different regions of the spectrum. For example,
honeybees are maximally sensitive to UV at 344 nm
(Menzel and Backhaus, 1991
),
while the UVS cone of blue tits is maximally sensitive at 375 nm
(Hart, 2001
). Similarly, the
sensitivities of the other photoreceptor types of honeybees and blue tits peak
in different regions of the light spectrum
(Menzel and Backhaus, 1991
;
Hart, 2001
). Consequently,
object colours will not equally excite the photoreceptors in different visual
systems.
Receptor excitation values take into account the photoreceptor transduction
process, or how the electromagnetic reflectance of an object translates to
neural firing. Coloured objects such as spiders in our case, however, become
visual signals only in combination with their natural backgrounds, against
which they generate a colour contrast for the perceiver
(Spaethe et al., 2001;
Heindl and Winkler, 2003
). For
both bees and birds, the UV contrast between spiders and daisy petals was
significantly higher in the natural UV+ spiders than in the UV spiders.
Because the contrast between spiders and daisies was similar for all the other
receptors, this translated into a higher colour contrast generated by UV+
spiders on daisy petals. However, the average UV contrast between UV
spiders and daisy petals was also well above the detection threshold of the
honeybee and bird receivers. This detectability is due to two characteristics
of photoreceptors. First, honeybees and most birds are more sensitive in the
ultraviolet than in other spectral ranges (Helversen, 1972;
Maier, 1992
). Second, each
type of photoreceptor is sensitive across a wide range of wavelengths, forming
roughly a Gaussian function (Stavenga et
al., 1993
). To give an example, the sensitivity of the honeybee
UV-receptor reaches its maximum at 344 nm. However, the sensitivity of the
same receptor type, if normalised to a maximum of 1, is still around 0.14 at
405 nm, which falls into the violet range of the light spectrum
(Chittka, 1996
). This explains
why the elimination of a certain range of wavelengths from the colour of an
object affects not only the excitation of one type of photoreceptors involved
in colour vision.
Why did UV spiders repel honeybees, when they still had on average positive UV-contrast with the daisy petals? Fig. 3 shows that the UV excitation of UV spiders is within the natural range found in daisies. In fact, some UV spiders excited UV-receptors less than some daisies. An UV spider on a daisy could alter the radial symmetry of the flower and this chromatic asymmetry may indicate a deteriorating flower to bees, and hence repel them. UV+ spiders, on the other hand, far exceed the daisies in reflecting UV light and exciting the UV receptors (see Fig. 3). This clear signal obviously results in added attraction for the bees. Further research, however, is needed to confirm any interpretation of the differences in the behavioural effects of UV+ and UV spiders.
In sum, our results provide evidence that the reflection of light in the UV range by UV+ T. spectabilis functions to attract honeybees. But it remains uncertain from the spectrometric analysis which components in the perception of the visual signal function to deceive prey. Removing the UV reflectance from spiders translated into a lower UV contrast and a lower overall contrast between spiders and daisies. In conclusion, assigning a change in behaviour to the change in UV-reflection alone may not be straightforward. It is likely that the differences in UV-receptor signals between UV+ and UV spiders generated a behavioural effect, since the effect of the differences in UV-receptor signals on colour contrast is pronounced.
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Acknowledgments |
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