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First published online April 17, 2009
Journal of Experimental Biology 212, 1365-1370 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.027482
Floral colour signal increases short-range detectability of a sexually deceptive orchid to its bee pollinator
University of Vienna, Department of Evolutionary Biology, Althanstraße 14, 1090 Vienna, Austria
* Author for correspondence (e-mail: johannes.spaethe{at}univie.ac.at)
Accepted 15 February 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: colour vision, pollination, sexual deception, orchids, signal evolution, Ophrys heldreichii, Tetralonia berlandi
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) but it is most
pronounced in the Orchidaceae family. The proportion of deceptive species in
this worldwide family is about 30% whereas in the Western Palearctic it makes
up probably more than half of all species
(Dafni, 1984;
Paulus, 2005;
Paulus, 2006). To attract
potential pollinators, deceptive orchids imitate their models by exploiting
key signals used in plant–pollinator relationships or sexual
communication (Jersáková et
al., 2006). Two major strategies are found in orchids, food
deception and sexual deception, which differ in the quality of involved
signals in respect to their species-specific perceptibility and targeted
audience. Food deceptive species imitate the colour and shape of rewarding
models and thus allow the orchids to achieve visits by pollinators foraging on
the model plants (Vogel, 1972;
Dafni, 1987;
Gumbert and Kunze, 2001;
Galizia et al., 2005). The
involved sensory channel, namely vision, is `non-private' and the signals can
be perceived by both the targeted pollinators and a broad range of unspecific
flower visitors (Kevan and Baker,
1983; Rosenthal and Ryan,
2000; Schaefer et al.,
2004). Sexually deceptive orchids, however, exploit `private'
communication channels to lure pollinators. They produce the behaviourally
active components of the sex pheromone of receptive females of the imitated
insect species to attract males and elicit mating behaviour. During the
subsequent copulation attempt, the so-called pseudocopulation, the pollinaria
become attached to the male's body and pollen is transferred upon visitation
of subsequent flowers (Kullenberg,
1961; Ayasse et al.,
2003; Schiestl et al.,
2004; Schiestl,
2005). Pollinator attraction in these orchids is very specific as
only males of the target species are attracted while other flower visitors do
not respond to the odour bouquet. Due to the highly specific attraction
mechanism, the flowers of sexually deceptive orchids usually do not possess
conspicuous colour signals to avoid accidental attraction of unspecific
pollinators (Alcock, 2005;
Delforge, 2006).
Nearly all species of the Mediterranean orchid genus Ophrys are
sexually deceptive (Kullenberg,
1961; Paulus and Gack,
1990; Paulus,
2005; Paulus,
2006). They mimic the sex pheromone of insect females, usually
solitary bees and wasps, to attract males that seek to copulate
(Kullenberg, 1961;
Paulus and Gack, 1990). The
labellum of an Ophrys flower resembles, in part, features of the body
of the female bee or wasp for males of the respective species and serves as
the substrate on which the attracted males perform pseudocopulations
(Paulus and Gack, 1990;
Paulus, 1997). The three
sepals (herein referred to as perianth for simplification) are usually
inconspicuously greenish and foliage-like. To insects they thus appear
achromatic (Delforge, 2006).
It is noteworthy that of the more than 200 described Ophrys species,
ca. 30% possess a visually conspicuous perianth, which is pink or
white and at least partially matches the spectral reflectance patterns of
other co-flowering plants (Delforge,
2006; Spaethe et al.,
2007). However, the functional significance of this colour signal
with respect to pollinator attraction is unknown. Recently we showed that the
pollinator of the Heldreich's bee orchid Ophrys heldreichii, which
are the males of the long-horned bee Tetralonia berlandi, prefer
flowers with a pink perianth over flowers with removed perianth in a dual
choice test (Spaethe et al.,
2007). Whether this choice behaviour is determined by constraints
imposed by the sensory capacities of the pollinator has yet to be tested.
Also, the relative importance of such colour signals compared with odour
signals for male attraction and guidance towards the flower is unknown.
In the present study, we address the question whether the coloured perianth functions as a close range signal in pollinator attraction and how it interacts with the odour signal (the mimetic sex pheromone). We used artificial perianths of various colours attached to real Ophrys heldreichii flowers to test the effect of visual parameters (chromatic and receptor specific contrast and size) on the pollinator's detection capability.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Ophrys heldreichii shows a conspicuous pink perianth and is the only
representative of the Ophrys oestrifera group found on Crete
(Delforge, 2006;
Kretzschmar et al., 2002). For
the experiments, intact flowers were collected from various sites within an
area of about 20 km around the experimental site. The orchid does not occur at
the experimental site and thus all tested males were naïve to O.
heldreichii flowers.
Behavioural experiments
Males of T. berlandi approaching O. heldreichii flowers
were filmed from above with a digital video camera (Sony DCR-SR50, Tokyo,
Japan) at a rate of 25 frames s–1. The camera was mounted at
a height of 180 cm and the viewed area subtended approximately 110x70
cm. To account for perspective distortion we included a 10x10 cm grid
that was used as a reference when calculating the flight path and flight
distance (see below).
A single flower of O. heldreichii was placed in the lower centre of the filmed area. Approaching bees were immediately caught after contact with the flower and individually marked with a colour marker. Only approaches of single males that resulted in contact with or landing on the flower labellum were included in the analysis. All individuals re-visiting the same flowers were excluded.
For each approach we measured wind speed at flower level by means of an
anemometer (Windmaster 2, Kaindl Electronic, Rohrbach, Germany). Males are
attracted from a distance by the odour produced by the flower
(Kullenberg and Bergström,
1976) and thus they usually approach upwind guided by the odour
plume. Therefore, we continuously rotated the entire setup to allow the wind
to come from behind the flower.
In the first experiment, we tested whether the presence or absence of the
coloured perianth has any effect on the flight behaviour of the males. We
first recorded approaches towards an intact flower for 30 min. Then we removed
the perianth and recorded approaches to the same flower for another 30 min.
Using the same flower minimises variance that originates from differences of
odour strength and quality between individual flowers
(Ayasse et al., 2000). To
prevent any bias due to tissue injury, we incised all three sepals of the
intact flowers before its initial use
(Spaethe et al., 2007).
Altogether, 14 individual flowers were tested.
In the second experiment, we tested for those spectral parameters of the perianth that determine flower detection. The original perianth was replaced by an artificial one cut from coloured cardboard, which resembled the original in size and shape. We tested five different colours: pink, green, blue, yellow and an UV-absorbing grey (see below). The perianth was randomly exchanged every 15 min, and flowers were replaced every 2 h.
Video files were transferred to a personal computer and individual approach
flights were analysed frame-by-frame using free software (DGeeMe 1.0 beta
version,
www.geeware.com).
The position of the bee's head and the position of the orchid were marked in
every frame. We used the reference grid to remove perspective distortion by
applying projective transformation (Wolf
and Ghilani, 1997). The final coordinates were used for
calculating the distance between the head of the male and the orchid.
Positional errors that resulted from changes of flight altitude were assumed
to be negligible because bees usually flew at a constant height close above
the ground when approaching a flower (M.S., H.F.P. and J.S., personal
observation).
Bees possess apposition compound eyes, which provide them with a relatively
coarse image of their environment (Land,
1997). For honeybees, the distance threshold for detection of a
single object similar to the size of an Ophrys flower (ca.
2.5 cm in diameter) is about 30 cm, which is the distance at which the object
subtends a visual angle of 5 deg. to the bee's eye
(Giurfa et al., 1996;
Dyer et al., 2008). According
to this known limitation in honeybees, we defined an inner circle (close
range; 30 cm around the flower) within which the males should be able to use
their visual system for detecting the flower and an outer circle (mid range;
between 30 and 60 cm) in which the males should be able to use olfactory but
not visual information for orientation. We calculated the amount of time a
male needed once it entered the outer circle to reach the inner circle (`mid
range search time') and once it entered the inner circle to touch or land on
the flower's labellum (`close range search time').
In the third experiment, we tested whether the size of the perianth
influences the choice behaviour of males by means of a dual choice experiment.
To completely eliminate odour-variance-induced bias, we used both artificial
orchid labellae and artificial perianths. The labellum models were cast in
latex and painted according to the original labellum. Artificial perianths of
three different sizes (normal size and 0.5 and 1.5 times the original size in
respect to area) were cut from pink cardboard (see below). The flower models
were presented in a paired design (small vs normal, normal
vs large size) at a height of 25 cm and at a distance of 10 cm from
each other facing the same direction. As visual properties alone do not
suffice to attract pollinators
(Kullenberg, 1961;
Paulus, 1988;
Spaethe et al., 2007), we
channelled air through an acrylic glass jar, containing about 2–5
inflorescences of O. heldreichii, via a Y-shaped tube equally to both
flower models by means of an air pump (SCHEGO optimal, Offenbach am Main,
Germany) (Spaethe et al.,
2007). Choices of individual male bees were recorded. The bees
were caught and marked after each visit. Bees approaching from the side and
re-visiting bees were not included in the analysis. The position of the
flowers and the perianths were interchanged in a random order to exclude
position biases.
Stimuli spectral properties
Spectral reflection of the O. heldreichii perianth and coloured
cardboards were measured by means of an USB 2000 spectrometer with a
deuterium/halogen light source between 300 and 700 nm
(Fig. 1; Ocean Optics B.V.,
Duiven, The Netherlands). Measurements were conducted on small ca.
0.25 cm2 areas and calibrated with a white standard (Diffuse
Reflectance Standard WS-1, Ocean Optics). To estimate bee specific receptor
contrasts and perceptual colour distances between the perianth and the
background, we applied the bee hexagon model following standard procedures
(Chittka, 1992;
Chittka and Kevan, 2005). Most
hymenopterans are found to have three photoreceptor types with
phylogenetically conserved spectral sensitivities
(Briscoe and Chittka, 2001). It
is thus likely that T. berlandi has receptor sensitivities similar to
other bees. We therefore used spectral receptor curves from the honeybee for
calculations (Peitsch et al.,
1992). In addition to colour information, honeybees and bumblebees
also use an achromatic visual channel for flower detection that relies only on
the green receptor signal as input (Giurfa
et al., 1996; Dyer et al.,
2008). Both channels are deployed depending on the visual angle of
the object. If the subtended visual angle of the object is large (ca.
15 deg.), colour contrast is used; for smaller visual angles, bees deploy the
green contrast alone (Giurfa et al.,
1996; Giurfa and Vorobyev,
1998; Dyer et al.,
2008). Therefore, we quantified colour contrast and green contrast
of the perianths to the background [Table
1; for details of calculation, see Chittka and Kevan and Spaethe
et al. (Chittka and Kevan,
2005; Spaethe et al.,
2006)].
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Statistics
Statistical analyses were performed with SPSS 11.5 (SPSS Inc., Chicago, IL,
USA). All P values above 0.05 were considered as statistically not
significant. Search times did not differ between the years 2007 and 2008 and
were therefore pooled (data not shown). For the first experiment, we applied a
nonparametric Mann–Whitney U-test to compare search times
between flowers with intact and removed perianths.
|
), chromatic
contrast and green-receptor contrast as predictors. For the third experiment,
a two-tailed binomial test (
=0.5) was used to test whether males'
visitation rate differed significantly from random. |
RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Mafra-Neto and Cardé,
1994). When we compared search time of males in the mid range
(30–60 cm distance), we found no differences between approach flights to
intact flowers and to flowers in which the perianth was removed
(Z=–0.65, P>0.05)
(Fig. 3A). By contrast, at
close range (<30 cm) search time was almost three times higher when males
approached flowers with removed perianths compared with intact flowers
(Z=–3.13, P<0.01)
(Fig. 3B), indicating that the
males used visual flower features for detection at short distances.
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When males were allowed to choose between two flowers with identical labellum and odour bouquet but different perianth size, they mostly chose the larger perianth, even when the size was 1.5 times larger than the original one (small vs original size: P<0.001, N=14; original vs large size: P<0.001, N=20; 2-tailed binomial test). Thus males obviously do not prefer a particular perianth size or flower shape but seem to prefer the largest flower.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Dyer et al.,
2008), search time was found to correlate only with wind speed,
indicating that males exclusively depend on olfactory cues. At these
distances, males exhibited the typical zig–zag flight pattern that is
found in insects that orient themselves by means of an odour plume
(Fig. 2)
(Kennedy, 1983). With
increasing wind speed, the odour plume usually narrows and becomes more
directed, allowing the males to orient themselves more precisely
(Fig. 4)
(Brady et al., 1995). However,
when wind speed exceeds a certain level, it might become more difficult for
the approaching males to steer and keep track of the odour plume due to
increased turbulences, which results in an increase in search time
(Fig. 4). As soon as T.
berlandi males come close enough to visually detect a flower, they change
their behaviour. At distances where the flower subtends at least 5 deg. visual
angle, search time was correlated only with the green contrast between the
perianth and the background but not with wind speed
(Table 2). Thus, our field
observations nicely match the behaviour of bumblebees and honeybees tested in
dual choice experiments in the laboratory. Under controlled conditions, bees
trained to detect a rewarding stimulus, e.g. a coloured disc or a real flower
that provides sufficient green contrast, can perceive the stimulus when it
subtends a visual angle between 3 deg. and 5 deg.
(Giurfa et al., 1996;
Spaethe et al., 2001;
Dyer et al., 2007;
Dyer et al., 2008). However,
when a stimulus provides only chromatic and no green receptor contrast, bee
spatial resolution deteriorates and detection threshold increases to 15 deg.
visual angle (Giurfa et al.,
1996; Dyer et al.,
2008). Tetralonia berlandi males thus initially detect
the flowers by their green-receptor specific contrast. However, they may also
perceive the colour of the perianth when they come closer to the flower but it
is unlikely that the colour affects the final approach and the landing
behaviour. We found that all males which were naïve to O.
heldreichii flowers and which approached close enough to perceive the
flower, also landed on the labellum irrespective of the perianth colour (M.S.,
H.F.P. and J.S., personal observation).
Our results together with recent findings
(Spaethe et al., 2007) provide
strong evidence that the pink perianth in O. heldreichii increases
short-range detection and attractiveness for its pollinator, T.
berlandi males. As visitation rate limits reproductive success, one would
assume a strong selection pressure acting on bee-pollinated Ophrys
flowers to increase attractiveness by means of imitating the sex pheromone of
the pollinator's female and by providing a visual signal for close range
attraction and detection. Surprisingly, the perianth is coloured in only about
30% of all Ophrys flowers. In all other species it is green and thus
provides neither chromatic nor green contrast for bees
(Delforge, 2006). We thus
speculate that the presence of a colour signal is related to the visual system
of the pollinator. Males from the tribes Eucerini and Anthophorini are
frequently the pollinators of Ophrys species
(Kullenberg, 1961;
Kullenberg and Bergström,
1976; Paulus and Gack,
1990). They are fast fliers and exhibit a distinct visual and
olfactory system that is employed to detect receptive females
(Michener, 2000). In a search
of the literature, we discovered that 74% (42 out of 57) of all
Ophrys species, in which the known pollinator has been identified to
be an Eucerini or Anthophorini male, possess a coloured perianth (Deforge,
2006; Paulus and Gack, 1990).
By contrast, only 7% (4 out of 58) of species that are pollinated by males of
the large genus Andrena (Andreninae) show a coloured perianth.
Andrenine bees usually lack a distinct sexual dimorphism of their sensory
system. The presumably small benefit of possessing a coloured perianth for
species pollinated by members of this genus might be outweighed by the
disadvantage of accidentally attracting non-specific flower visitors and thus
increasing the risk of pollen loss. Even though we did not account for
phylogenetic relationships, the data suggest that the occurrence of a coloured
perianth in Ophrys is likely to be correlated with the importance of
the visual system for mate detection in the pollinating males.
The flower colour and shape and the pattern of the labellum in
Ophrys species are often bizarre, and numerous authors have
interpreted the appearance of the flowers as visual mimicry of the body of the
pollinator's female (Detto,
1905; Kullenberg,
1961; Kullenberg and
Bergström, 1976; Paulus
and Gack, 1990). However, we must be cautious when regarding the
visual appearance of flowers to not misinterpret visual similarities or
analogies with the expected female bees. Hymenopteran compound eyes differ
from human eyes in both spatial resolution and spectral sensitivity
(Land, 1997;
Briscoe and Chittka, 2001).
Bees and wasps can perceive ultraviolet light, a part of the light spectrum to
which humans are insensitive, and they use different receptor-specific visual
channels, depending on the angular size of the targeted object. For example,
in this study we showed that close range detection of the Ophrys
flower is improved by the visually conspicuous perianth. However, search time
does not correlate with the colour per se as we perceive it. Rather
search time mainly depends on the green-receptor specific contrast, which is
an important brightness channel for bees but is not perceivable by humans.
Therefore, to arrive at an understanding of the functional significance and
evolution of flower patterns and colourations in sexually deceptive orchids,
we must take into account the specific properties and limitations of the
pollinator's visual system.
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Footnotes |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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