Colourful orb-weaving spiders, Nephila pilipes, through a bee's eyes
1 Department of Biology, Tunghai University, Taichung 407, Taiwan
2 Department of Entomology, National Chung Hsing University, Taichung 402,
Taiwan
* Author for correspondence (e-mail: ecyang{at}dragon.nchu.edu.tw)
Accepted 4 May 2004
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Summary |
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Key words: colour contrast, visual signal, Apis mellifera, Nephila pilipes, polymorphism
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Introduction |
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Many researchers attributed the attractiveness of spiders' body colouration
to the UV-reflecting properties. However, insects see by detecting the colour
contrast between the objects they are looking at and the background of that
object using a combination of several receptor signals
(Chittka and Menzel, 1992;
Vorobyev and Brandt, 1997
;
Briscoe and Chittka, 2001
).
Insects do not rely solely on UV signals but instead use light signals
reflected from the objects and backgrounds for visual detection
(Kevan et al., 2001
). In the
honeybee, chromatic vision and achromatic vision are involved in the detection
of colour targets, depending on the subtended visual angle of the target.
While only contrast to the L (long-wavelength)-receptor is used for detecting
targets with subtending small visual angles
(Giurfa and Vorobyev, 1998
),
the chromatic visual system of the honeybee, which receives input from all
three photoreceptor types, is responsible for detecting targets with large
visual angles (Giurfa et al.,
1996
,
1997
;
Niggebrügge and Hempel de Ibarra,
2003
). Recently, the way in which hymenopteran insects perceive
crab spiders (Family: Thomisidae) on flowers was assessed by calculating the
colour contrasts derived from the reflectance spectra of the spiders and the
petals (Chittka, 2001
;
Théry and Casas, 2002
;
Heiling et al., 2003
). So far,
this approach has not been used to assess the visual signals of diurnal
orb-weaving spiders. In the present study, we examined how the colour markings
of spiders were viewed by insects, by measuring their reflectance spectra, and
then calculated the colour contrasts as perceived by hymenopteran insects.
A polymorphic population of the giant wood spider, Nephila pilipes
(formally N. maculata), on Orchid Island, Taiwan had been
demonstrated previously to exhibit colour-associated foraging success
(Tso et al., 2002). Typical
morph female N. pilipes have an olive-green prosoma and a
yellowish-black abdomen decorated with a transverse white band, two
longitudinal yellow bands and numerous yellow spots
(Fig. 1). However, some of the
females are totally dark, and allozyme data has demonstrated that both morphs
are members of an interbreeding population
(Tso et al., 2002
). A previous
study on this population has shown that the typical morphs caught almost twice
as much prey as the melanic morphs (Tso et
al., 2002
). In the present study, we compared the prey
interception rates of two morphs of N. pilipes again to confirm
whether or not a bright colouration will render a higher foraging success.
Moreover, we calculated the colour contrasts of these two morphs in the colour
space of honey bees by measuring spectral reflectance of body surfaces and
background light environment in the study site to assess how these spiders are
perceived by insects.
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Materials and methods |
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![]() | (1) |
Measurements of light environment and spectral properties
Reflectance spectra of the spiders, the background light environment and
the illumination functions of the study sites were used to calculate the
colour contrasts perceived by spiders' prey and predators
(Chittka et al., 1994). We
measured the reflectance spectra of various objects with a spectrometer
(S2000; Ocean Optics, Inc., Dunedin, FL, USA). In the study site, giant wood
spiders usually hang their webs in the forest understorey in front of dense
vegetations. Therefore, the background light environment was estimated by
averaging the reflectance spectra measured from green leaves, fallen leaves
and bark (N=190 in total) collected from the field census site. The
daylight spectrum of the forest understorey illumination was measured at the
study site by placing the end of the probe of the spectrometer 5 mm above
(90°) the standard white. The measurements were taken every day at hourly
intervals from 08.00 h to 18.00 h for three sunny days. The means of these
readings were used in the subsequent calculations of colour contrasts. Eight
typical and six melanic morphs were brought to the laboratory to measure the
reflectance spectra of various areas on their body
(Fig. 1). All the reflectance
spectrum measurements in this study followed the standard procedures described
previously (Tso et al., 2002
).
The spectral reflectance measurements covered the range from 300 nm to 700
nm(increment 0.3 nm). For each wavelength, we measured reflectance 10 times
and we plotted the mean against the wavelength.
Bees were reported to adopt achromatic vision by using the green receptor
signal when searching for objects far ahead and to adopt chromatic vision by
using green, blue and UV receptor signals when approaching objects
(Giurfa et al., 1997;
Spaethe et al., 2001
). Heiling
et al. (2003
) showed that the
visibility of crab spiders on flowers to bees varied when different achromatic
and chromatic neural channels were adopted. Therefore, colour contrasts of
N. pilipes viewed by either achromatic or chromatic vision were
calculated to assess how different morphs were perceived by bees during
different stages of searching.
Calculation of colour contrasts
We calculated the colour contrasts of spiders and decorations by the colour
hexagon model of Chittka
(1992). To determine
photoreceptor excitations for each measured spectra, we used spectral
sensitivity functions of photoreceptors of the honey bee, Apis
mellifera (Briscoe and Chittka,
2001
), to determine the photoreceptor excitations for each
measured spectra. The relative quantum flux absorbed by each type of
photoreceptor, P, can be expressed as:
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![]() | (3) |
![]() | (4) |
The three excitation values in the honey bee's UV, blue and green
photoreceptors can be depicted in a three-dimensional photoreceptor excitation
space or in the colour hexagon (Chittka,
1996). With the three photoreceptor excitation values plotted at
angles of 120°, the x and y coordinates in the colour
plane are given by:
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![]() | (6) |
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Results |
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Reflectance properties and colour contrasts of Nephila pilipes
The daylight illuminating spectrum of the forest understorey in the study
site is shown in Fig. 3A. This
daylight illumination spectral curve was used in all the model calculations.
The spectral reflection of the vegetation background averaged from fresh
leaves, fallen leaves and bark is given in
Fig. 3B. The reflectance
spectra of bright and dark body parts of typical Nephila pilipes are
given in Fig. 4. Various bright
body parts of N. pilipes had very similar reflectance properties.
These areas exhibited a strong reflectance between 550 and 700 nm, which
corresponded to the yellow to red region of the visible spectrum. In addition,
bright body parts also had a small reflectance in the UV region of the
spectrum (Fig. 4A). By
contrast, various dark body parts of N. pilipes all had a very low
reflectance across all wavelengths measured
(Fig. 4B). The prosoma, two
yellow bands on the abdomen, and spots on the legs and ventrum of typical
N. pilipes all exhibited colour contrasts significantly higher than
the discrimination threshold for colour contrast detection estimated for honey
bees (Théry and Casas,
2002; Fig. 5A,B),
regardless of whether they were viewed by chromatic or achromatic
(Table 2) vision. The dark
parts of the body (areas 5 and 11) had low colour contrasts that were not
significantly different from the discrimination threshold when viewed by
chromatic vision (Table 2,
areas 5 and 11). However, they had colour contrasts significantly higher than
the threshold when only green receptor signal was used
(Table 2, achromatic vision).
The melanic N. pilipes had weak but visible colour signals when
viewed by chromatic vision (Fig.
6A,B). In most parts of the body, the colour contrasts were
slightly but significantly higher than the discrimination threshold
(Table 3). When viewed by
achromatic vision, the colour contrasts of all body parts of melanics were
even higher (Table 3;
Fig. 6A,B).
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Discussion |
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The insect interception rates of typical yellow morphs and melanic morphs
were significantly different. Compared with typical morphs, melanic N.
pilipes do not have yellow markings but only dark body colour. Colour
signals of the melanics were significantly different from those of dark
markings of the typical morphs. The dark markings of typical morphs looked
yellowish-black but those of melanics were shiny black. Excessive deposition
of dark pigments might have caused such a dramatic change in appearance and
colour signal. While the contrasts and thus the visibility of dark markings of
typical morphs vary when viewed by different chromatic channels, melanics have
high contrasts when viewed by either achromatic or chromatic visions. Although
melanic morphs are visible to insects, the uniformly coloured body renders the
contour of the spiders quite clear (Fig.
6C,D). Nevertheless, melanic morphs lacked colour signals
mimicking those of insects' resources. Therefore, while the visual signals of
the typical N. pilipes could both deceive and attract the insects,
those of melanics exhibit no such properties. This might explain why the
former caught significantly more prey than the latter in this and the previous
study by Tso et al.
(2002).
Results of censuses conducted in 1997, 1999
(Tso et al., 2002) and 2002
(present study) demonstrate that the ratio of melanic to typical N.
pilipes in the study site in Orchid Island was more or less constant
(2030%). Results of this study and that of Tso et al.
(2002
) indicate that melanic
N. pilipes had a significantly low foraging success, which might
result from their altered colour signals. However, given such a disadvantage,
why does the melanic morph persist stably in the population in Orchid Island?
Results of the present study show that colour contrasts of melanic
Nephila were significantly higher than the discrimination threshold.
This result indicates that melanics are actually highly visible to
hymenopteran insects, especially under achromatic vision, when the predators
are searching for prey from a long distance. Although Tso et al.
(2002
) suggested that one
advantage enjoyed by melanics might be a lower mortality resulting from lower
visibility to predators, the colour contrast data indicate that this is not
the case. However, visibility is not the only determinant of predation
pressure. Although melanics were visible to wasps, they did not have the
bright colourations exhibited by the typical morphs. Perhaps hymenopteran
predators use the bright colouration patterns as a cue and form a search image
(Allen, 1988
;
Endler, 1988
) for the more
frequent typical N. pilipes. Melanics might benefit from a lack of
bright colour signal and low frequency in population rather than a lower
visibility generated by reflectance properties. Further field manipulative
studies are needed to evaluate whether melanics have lower mortality and the
underlying mechanisms.
Insects see by detecting contrast between objects and their environments,
and all kinds of colour receptors and colour signals are involved
(Chittka and Menzel, 1992;
Vorobyev and Brandt, 1997
;
Briscoe and Chittka, 2001
).
Many relevant studies have only considered the UV component of the system when
inferring the nature of insectspider visual interactions
(Craig and Bernard, 1990
;
Craig et al., 1994
;
Tso, 1996
;
Blackledge, 1998
;
Watanabe, 1999
;
Blackledge and Wenzel, 2000
;
Tso et al., 2002
;
Zschokke, 2002
). However, all
sorts of colour signals and receptors should be considered when determining
the colour signals of spiders. Compared with the traditional `UV approach'
(measuring the UV reflectance of organisms to infer the nature of visual
interactions), the `colour contrast approach' is more realistic because it
takes into account all colour signals of the objects and the various receptors
of the organisms. We suggest that all types of receptor signals should be
considered when exploring the visual interactions between predators and
prey.
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Acknowledgments |
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