Does reflection polarization by plants influence colour perception in insects? Polarimetric measurements applied to a polarization-sensitive model retina of Papilio butterflies
1 Biooptics Laboratory, Department of Biological Physics, Eötvös
University, H-1117 Budapest, Pázmány sétány 1,
Hungary
2 International University Bremen, School of Engineering and Science, P.O.B.
750561, D-28725 Bremen-Grohn, Campus Ring 1, Germany
3 Institut für Zoologie, Universität Zürich, CH-8057
Zürich, Winterthurerstrasse 190, Switzerland
* Author for correspondence (e-mail: gh{at}arago.elte.hu)
Accepted 6 August 2002
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Summary |
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Key words: polarization sensitivity, colour perception, polarizational false colours, reflection polarization, imaging polarimetry, computer modelling, plant-insect interactions
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Introduction |
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Wehner and Bernard (1993)
proposed that the functional significance of the photoreceptor twist is to
avoid the polarization-induced false colours of natural, bee-relevant surfaces
such as leaves and petals of flowers, which reflect partially linearly
polarized light. The degree and angle of polarization of reflected light
depend on how smooth the plant surfaces are and how they are oriented with
respect to the incoming light at the direction of view. For a flower-visitor,
this could cause difficulties, because the absorbing photopigments responsible
for colour vision are contained in receptors with different microvillar
orientations. Thus, each receptor gives a signal that depends not only on
intensity and wavelength but also on the angle and degree of polarization. If
the sensors of a colour vision system are also polarization sensitive, the
system generates `false colours' that may obscure the real colours defined by
the spectral properties of the object.
Recently, Kelber (1999a)
and Kelber et al. (2001
)
suggested that the butterflies Papilio aegeus and Papilio
xuthus do not process polarization and colour separately, and thus they
may perceive polarization-induced false colours owing to their weakly
polarization-sensitive photoreceptors. As Kelber and collaborators worked with
artificial stimuli that had an unnaturally high degree of linear polarization
(100%; i.e. totally polarized light, which is not characteristic of light
reflected from plant surfaces), no published behavioural data so far support
that there is a significant influence of polarization on butterfly colour
vision under natural conditions, when the receptors are stimulated by
partially linearly polarized light with frequently low degrees of
polarization.
As the PS value of photoreceptors in Papilio species,
ranging between 1.3 and 2 (Bandai et al.,
1992; Kelber et al.,
2001
), is very low (note that PS=1 for
polarization-insensitive receptors), the following question arises: can the
often low degree of polarization of light reflected from plant surfaces induce
sufficiently strong polarizational false colours in Papilio
butterflies to influence their colour vision significantly? How do these
polarization-induced false colours depend on the different parameters of the
butterfly retina (microvillar directions, polarization sensitivity or
orientation of the eye), on the characteristics of the optical stimuli (degree
and angle of polarization of reflected light) and on the illumination
conditions (alignment of the plant surface with respect to the direction of
view and to the solar direction; plant surface in direct sunshine and in
shadow).
In the present study, we have quantitatively estimated the influence of
polarization sensitivity on the perception of natural surface colours by
Papilio butterflies. We measured the characteristics of polarized
light reflected from plant surfaces by imaging polarimetry
(Horváth and Varjú,
1997) in the field under natural illumination conditions.
Recently, Shashar et al.
(1998
) demonstrated some
features of polarized light reflected from leaves in a tropical rain forest.
The first aim of our work is to present some typical reflection-polarization
patterns of plants (flowers and leaves). The second aim is to give a
quantitative model to calculate the quantum flux absorbed by
polarization-sensitive photoreceptors of Papilio butterflies from the
measured polarization patterns and to calculate the loci of the perceived
false colours in the colour triangle of their simplified colour vision system.
We investigated the influence of the microvillar direction, polarization
sensitivity, orientation of the eye, degree and angle of polarization of
reflected light, alignment of the plant surface with respect to the direction
of view, and the solar direction on the polarization-induced false colours
perceived by Papilio butterflies. We also studied how the
polarizational false colours differ under direct sunlight and in the shade.
Finally, we discuss the limitations of our polarimetric technique and computer
modelling.
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Materials and methods |
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Computation of the spectral loci of colours perceived by a
polarization- and colour-sensitive retina
The numerical values of our retina model
(Fig. 1A,B) described in this
subsection are characteristic of the butterfly Papilio xuthus L.
(fig. 1B and
table 1 of
Kelber et al., 2001, pp.
2470-2471). Our model retina contains polarization-sensitive photoreceptors of
spectral types red (R), green (G) and blue (B), with the following sensitivity
maxima:
Rr=600 nm,
Gr=520 nm and
Br=460 nm, respectively. The relative absorption
functions of the receptors are shown in
Fig. 1A. In our retina model,
angle ß is the direction of the microvilli measured clockwise from the
dorso-ventral meridian of the compound eye
(Fig. 1C). For the microvilli
of the blue-sensitive photoreceptors, ßB=0°, for the
microvilli of the green-sensitive receptors ßG=0°,
35°, 90° or 145°, and for the microvilli of the red-sensitive
receptors ßR=0°, 35° or 145°
(Fig. 1B). The colour vision
system of Papilio butterflies is pentachromatic
(Arikawa et al., 1987
).
Treating the short-wavelength receptors (UV, violet, blue) as one receptor
type allows us to demonstrate false-colour effects in a plausible way by
indicating the shifts of colour loci in the equilateral colour triangle
(Fig. 1E). No principally
different false-colour effects are expected by including all five receptor
types in our retina model. The soundness of this simplification is thoroughly
discussed later in this article.
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Let the angle of the eye's dorso-ventral meridian be ° clockwise
from the vertical (Fig. 1C). If
receptor r receives partially linearly polarized light with intensity
I(
), degree of linear polarization
(
), angle
of polarization
(
) (clockwise from the vertical), minimum and
maximum e-vectors Emin(
) and
Emax(
), respectively, then qr
can be calculated as follows (Fig.
1C):
![]() | (1) |
![]() | (2) |
![]() | (3) |
![]() | (4) |
![]() | (5) |
The expressions for k, k' and k'' involve different electrodynamic constants. Using them, one could calculate the absolute value of qr. We omit to give the expressions for k, k' and k'' because they are all eliminated in the final expressions describing the spectral loci of colours perceived by a polarization- and colour-sensitive retina.
As we could measure the spatial distribution of intensity I,
degree of polarization and angle of polarization
of light
reflected from plant surfaces only at wavelengths
Bc=450 nm,
Gc=550
nm and
Rc=650 nm, we took the following
approximations in the calculation (Fig.
1D):
![]() | (6) |
![]() | (7) |
In the literature of colour vision, there are two different conventions to
give the relative absorption functions A() of photoreceptors:
they possess either equal amplitude Amax(
)=1 (e.g.
Przyrembel et al., 1995
; fig.
12, p. 584) or equal integrals
(e.g. Lunau and Maier, 1995
;
fig. 1A, p. 3). Kelber et al.
(2001
), for example, used the
first convention; our Fig. 1A gives the A(
) curves with the same amplitudes adapted from
fig. 1B of Kelber et al.
(2001
). This convention is
called `amplitude normalization'. The second convention, called `integral
normalization', corresponds to the assumption that the quantum absorptions of
receptors of different spectral types are the same if the incident light is
unpolarized [
(
)=0] and physically white
[I(
)=constant]. This has the consequence that `physical (or
optical) white' coincides with `physiological (or perceptional) white'; in
other words, the locus of both physical and physiological white is positioned
at the colourless centre of the equilateral colour triangle of a trichromatic
colour vision system (Fig. 1E).
In this case, the receptor absorption curves are normalized by setting their
integral to 1. In other words, the quantum absorption qr
of receptor type r is divided by the quantum absorption of the
receptor for unpolarized (
s=0) and physically white light
(Is=Iwhite = arbitrary constant):
![]() | (8) |
![]() | (9) |
![]() | (10) |
![]() | (11) |
Using Equations 10, 11, we computed the coordinates Mr (r=R,G,B) of the colour locus for every pixel of a given picture of plant surfaces. The calculated spectral coordinates Mr were plotted within the equilateral colour triangle (Fig. 1E). Note that the peak wavelengths of the colour receptors in the human eye differ significantly from those of the Papilio retina. Thus, the false-colour pictures given in Fig. 4 merely serve to visualize the effect of polarization-induced colour changes for the reader. The false colours will look different to a butterfly.
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Results |
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Fig. 3 shows that the
reflectance of the red flower petals of C. radicans decreases from
the red spectral range towards shorter wavelengths, while the reflectance of
the leaves is the highest in the blue and green ranges. The degree of
polarization of light reflected from the reddish petals is highest in
the blue and green ranges (
30-40%) and smallest in the red range
(
<10%). Depending on their orientation, leaves reflect partially
polarized light with 10%
80%, and
is the highest in the
blue range. In contrast to other leaves, the bright green leaves in the
immediate vicinity of the flower at the centre of
Fig. 2 (e.g. points 1 and 2)
possess very low
, because the light is not reflected but transmitted
through their blades towards the camera, viewing upward with an elevation of
45°; the degree of polarization of transmitted light is reduced owing to
diffuse scattering in the leaf tissue. Although the average
of light
reflected from the leaves is about 90° - meaning horizontal polarization,
which is the consequence of (i) the illumination (skylight) coming from above
and (ii) the approximately horizontal alignment of the majority of the leaf
blades -
often differs considerably from 90° owing to the random and
oblique orientation of many leaf blades.
In Fig. 4A, the colours of
C. radicans are shown as perceived by a polarization-blind retina.
They are considered as `real' colours and serve as a reference; the shifts of
the polarization-induced false-colour loci in the colour triangle are measured
from the loci of these real colours. Fig.
4B-E shows the false colours of the plant perceived by the weakly
polarization-sensitive retina of P. xuthus as a function of the
alignment of the dorso-ventral symmetry plane of the eye with respect
to the vertical, when a given set of photoreceptors rotates in front of the
plant. By rotating the polarization-sensitive receptor set by 180°, the
perceived false colours shift continuously in the colour triangle, passing
within an approximately elliptical chromatic area; in parts B, C, D and E of
Fig. 4 the false colour of the
leaves, for example, is slightly blue-green, blue, red and green,
respectively. Note that the rectangular images in
Fig. 4 are isoluminant,
containing information on colour alone (expressing the colour coordinates
MR, MG and MB);
they give no information on intensity. These colours are, however, more or
less masked by the whitish reflected light (see
Fig. 2). Similar shifts of the
perceived colour occur if the relative position of the plant surface with
respect to the receptor set (orientation of the dorso-ventral meridian of the
eye) changes because of rotation and/or translation. In the case of P.
xuthus, the chromatic distances of the polarization-induced false colours
from the real colour are small owing to the relatively small polarization
sensitivity value (PS=2) of the retina. These chromatic distances are
even smaller for the matt petals, which possess a lower
, than for the
shiny leaves, which reflect light with a much higher
.
Fig. 4 also demonstrates how
the real and polarization-induced false colours depend on the orientation of
leaf blades. Although the average alignment of leaf blades is approximately
horizontal, there are considerable deviations from this direction (see
Fig. 3F; the e-vector alignment
of specularly reflected light is always perpendicular to the plane of
reflection determined by the incident ray, the reflected ray and the normal
vector of the reflecting surface). The more or less randomly curved leaf
blades are more or less randomly oriented around the horizontal direction,
thus both and
change from site to site. The consequence is that
the almost homogeneous green real colour of the leaves being independent of
and
(see the narrow colour distribution around the most frequent
real green colour of leaves in the right colour triangle of
Fig. 4A) becomes more
heterogeneous for a polarization-sensitive retina, resulting in different
colour hues that range from violet (although partly white-masked) through
blue, green, yellow and orange to red (see the relatively broad false-colour
distribution around the most frequent green false colour of leaves in the
colour triangles of Fig. 4B-E).
This shows one of the consequences of the polarization sensitivity of colour
vision; owing to the high diversity of the degree and angle of polarization of
light reflected from plant surfaces, the perceived polarizational false
colours are more diverse than the real colours, which is also demonstrated by
further examples in Figs
6,7,8,
10. This phenomenon makes it
more difficult to recognize a given real colour and demonstrates a
disadvantage of the perception of polarization-induced false colours.
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Fig. 5 shows the loci of the real colours (beginning of arrows) perceived by a polarization-blind retina and the false colours (arrowheads) perceived by a weakly polarization-sensitive retina for these twelve points within the colour triangle. If the light reflected from or transmitted through a leaf or petal is unpolarized or weakly polarized and has medium or high colour saturation (points 1-4 and 7-10 in Fig. 5), the shift of false colours from the real colours is generally very small. If the light reflected from a leaf or petal is highly polarized and whitish with low colour saturation (points 5, 6, 11 and 12 in Fig. 5), the differences between the polarization-induced false colours and the real colours are larger than in the former case but remain small.
In P. xuthus, the microvilli in the red and green receptors can
have three or four different directions, as given in
Fig. 1B, and at present it is
not known how the receptors contribute to the net neural polarizational
signal. It is only known that in the blue receptors, the microvillar direction
(ßB) is 0°. Apart from the contribution of
ßR=145°, ßG=35° and
ßB=0° (Figs
4,
5), we also used other possible
combinations of ßR and ßG (together with
ßB=0°). Fig.
6D shows how the polarization-induced false colours of an
Epipremnum aureum plant (golden pothos; Aracea) perceived by P.
xuthus depend on ßR and ßG. The
foreground of Fig. 6A shows the
inflorescence of E. aureum, which possesses a large, shiny,
petalimitating red leaf called a `spathe', while the background is composed of
the shiny green leaves of the plant. Fig.
6B,C shows the patterns of and
of the plant measured
at a wavelength of 450nm (blue).
Fig. 6 demonstrates the chromatic diversity of the polarizational false colours versus the microvillar direction. Depending on ßG and ßR, all false colours (bm) perceived by P. xuthus shift slightly towards the red and/or green hues with respect to the real colour a, which possesses the largest blue component, MB. This is because (i) the light reflected from the investigated areas of the plant was approximately horizontally polarized (Fig. 6C) and (ii) the microvillar direction of the blue receptor is dorso-ventrally (vertically) fixed. The false colours are scattered within areas (Fig. 6D), the dimensions of which are similar for both the spathe and the leaf because both are shiny and reflect strongly polarized light (Fig. 6B). By changing ßG from 0° to 145°, the false colours b, c, d and e (ßR=0°), f, g, h and i (ßR=35°) and j, k, l and m (ßR=145°), belonging to given values of ßR, are positioned in the colour triangle approximately along straight and parallel lines. By changing ßR from 0° to 145°, the same is true for the false colours b, f and j (ßG=0°), c, g and k (ßG=35°), d, h and l (ßG=90°) and e, i and m (ßG=145°), belonging to given values of ßG. The angle between these lines is about 120°.
Having based our previous considerations on a low polarization sensitivity
of PS=2, let us now consider visual systems with high PS
values. High PS values have been measured in the specialized dorsal
rim area of the compound eye of several insects: PS10 in
honeybees A. mellifera (Labhart,
1980
) and in crickets G. campestris
(Blum and Labhart, 2000
). Apart
from the dorsal rim area, high PS values (mean PS=7) were
found in the lateral retina of waterstriders (Gerris lacustris;
Bartsch, 1995
).
Fig. 7 shows the dependence of
the polarization-induced false colours on
PB=PG=PR=P
as a function of ßG and ßR. When P
increases from 1 to 20, all false colours shift to some degree from the real
unsaturated, bluish-green colour (locus a) of the leaf towards
relatively saturated red, orange, yellow or green colours. The chromatic
distance of the false colours from the real colour can be considerable if the
polarization sensitivity is strong enough.
The degree of polarization of light reflected from plant surfaces
depends on the angle of incidence, the surface roughness and the wavelength.
At wavelengths where the amount of light coming from the subsurface layers is
negligible in comparison with the amount of light reflected from the surface,
the reflected light can be almost totally polarized if the angle of incidence
is near the Brewster angle (Horváth
and Varjú, 1997
). This is the situation for shiny green
leaves in the blue or red range of the spectrum
(Fig. 3), for instance. The
increasing surface roughness decreases the
. Hence, in natural
conditions, the
of light reflected from plant surfaces can vary
between 0% and almost 100%. Fig.
8 shows the dependence of the polarization-induced false colour on
the
of reflected light as a function of ßG and
ßR.
Comparing Fig. 8 with
Fig. 7, we see that the
dependence of the polarization-induced false colours on the
(Fig. 8) is qualitatively the
same as that on the polarization sensitivity P of the photoreceptors
(Fig. 7). The only essential
quantitative difference between Fig.
7 and Fig. 8 is
that, in the latter, the chromatic shifts (the lengths of the arrows) are much
smaller than in the former, in spite of the very high
values of 78%,
75% and 99%.
Fig. 9 shows how the
spectral and polarizational characteristics of a sunlit leaf of a Ficus
benjamina tree (weeping fig; Ficacea) depend on the direction of the
sunlight at a given solar elevation and how they change if the leaf is shaded
from direct sunlight. The colours, as well as the and
of light
reflected from the leaf, depend on the orientation of the leaf blade with
respect to the sun. For a given position of the sun, there are chromatic and
polarizational differences between the sunlit and the shaded leaves. The
colour of the sunlit leaf is always greenish
(Fig. 9A,C,E,G) owing to the
diffuse scattering and selective absorption of white sunlight in the green
subcuticular leaf tissue. This greenish hue is, however, more or less masked
by strong specular reflection of white sunlight if the leaf is viewed in the
direction of the sun (Fig. 9G).
The colour of the shaded leaf (Fig.
9B,D,F,H) is always bluish, because it is illuminated by blue
skylight. Owing to the non-planar, curved shape of the leaf blade, the
and
of reflected light changes from point to point. In
Fig. 9, the leaf blade in the
small rectangular left and right window is approximately horizontal and
vertical, respectively. Note that, although in
Fig. 9G the entire leaf is lit
by direct sunlight, both the left and right windows are placed in a local
shaded region because of the curved leaf blade. Thus, both the left and right
windows in Fig. 9G represent a
shaded situation.
In Fig. 10, we can see that, under the clear blue sky, the hues of shaded leaves are always nearer to the blue-green parts of the colour triangle than those of sunlit leaves. In the left window of the leaf in Fig. 9, the false colour shifts (represented by arrows) towards red, orange, yellow or green hues for both shaded and sunlit leaves. In the right window of the leaf in Fig. 9, because the orientation of the leaf blade is different (vertical) from that in the left window (horizontal), the colour shifts in the right window differ from those in the left window. Apart from Fig. 9E in the right window, the false colours shift towards the green hues for both shaded and sunlit leaves. In Fig. 9E, the colour shift is very small.
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Discussion |
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Rough surfaces reflect light diffusely, which reduces polarization. Thus,
the rougher a plant surface (e.g. owing to a waxy layer or other
microstructures), the lower the of reflected light. The e-vector
reflected from a plant surface follows its curvature, because the reflected
light becomes partially linearly polarized perpendicularly to the plane of
reflection for any dielectric (non-metallic) reflector.
The darker a plant surface in a given spectral range, the higher the
of reflected light. The reason for this is as follows. The
of
light reflected by the cuticle or epidermis of plants depends on the incident
angle but is almost independent of the wavelength. The e-vector of reflected
light is parallel to the surface. The colour of plant surfaces arises from the
selective absorption and diffuse scattering of light in the tissue below the
transparent cuticle. The diffuse light emanating from this tissue is
originally unpolarized, but it becomes partially polarized after transmission
and refraction at the epidermis. The e-vector of the tissue-scattered light is
perpendicular to the cuticle because of refraction polarization
(Horváth and Varjú,
1997
). Hence, the net degree and direction of polarization of a
plant surface are determined by the superposition of the epidermis-reflected
and the subcuticle-scattered light. If the former dominates (e.g. in sunlit
shiny leaves observed from the direction of specular reflection), the
direction of polarization is parallel to the cuticle; otherwise, the e-vector
is perpendicular to it (e.g. sunlit leaves observed from behind, when the
leaf-transmitted light is perceived). In those spectral regions where the
subcuticle-scattered light has a considerable contribution to net
polarization, the net
of the returned light is reduced or even
abolished.
These general rules are demonstrated in
Fig. 3. The considerably
reduced amount of subcuticle-scattered light in the blue range causes the red
flowers to be dark and relatively strongly polarized at 450 nm and 550 nm
(Fig. 3E). At 650 nm, the
amount of light emanating from the red tissue below the epidermis of the
flower is greater; thus, the net is reduced. This is the physical
reason for the general rule that, in a given spectral region, the darker
objects polarize light to a higher degree if the illuminating light is
unpolarized and white. Thus, green leaves are less polarized in the green
range than in the blue and the red ranges, as can be well seen in
Fig. 3.
In Fig. 2, we selected three
point-pairs of both leaves and petals for calculating polarization-induced
false colours. At point-pairs 5/6 and 11/12
(Table 1), is
relatively high owing to the large amount of skylight reflected from the
cuticle as well as to an alignment of the plant surface resulting in an angle
of view near the Brewster angle. However, the colour saturation is low owing
to the interference with the cuticle-reflected whitish/bluish skylight and the
tissue-backscattered greenish or reddish light. At point pairs 1/2, 3/4, 7/8
and 9/10 in Fig. 2 (Table 1), the situation is
reversed:
(in the dominant wavelength range) is low owing to the small
amount of skylight reflected from the cuticle as well as to an alignment of
the plant surface resulting in an angle of view far from the Brewster angle,
but the colour saturation is higher because the amount of cuticle-reflected
skylight is small.
Surfaces of petals have a matt finish, making them much better diffuse
reflectors than leaves, which have a shiny, smooth cuticle
(Kay et al., 1981;
Wehner and Bernard, 1993
).
Thus, petals usually reflect diffuse and only weakly polarized light, while
leaves reflect more specularly (i.e. the angle of incidence is the same as the
angle of reflection, and the reflected light is in the plane determined by the
incident light and the normal vector of the surface) and the reflected light
is generally highly polarized if the direction of view is near the Brewster
angle.
We propose that the major function of the surface roughness of petals is
not to reduce the of reflected light (and thus to reduce the
polarization-induced false colours) but to reduce the white glare of the
surface, which would overwhelm the petal-tissue-backscattered coloured light
and would make it more difficult to perceive the real, attractive and striking
colour of the petal. An appropriately rough petal surface functions as a
Lambertian reflector, which reflects light uniformly in all directions
independent of the angle of incidence. As a by-product, the light reflected by
a Lambertian surface is unpolarized. The intensity and colour of such a (matt)
Lambertian surface is the same from all directions of view. If the surface of
a petal were smooth, like the red spathe in
Fig. 6A, it would function as a
Fresnel reflector, which reflects light specularly. Then, the intensity and
colour of the petal-tissue-backscattered coloured light would be overwhelmed
by the white glare (i.e. by the specularly reflected white light) from the
smooth cuticle if the direction of view coincides with the angle of
reflection. This problem would not occur for other directions of view. Hence,
the reduction of the
of reflected light seems to be the consequence,
and not the main aim, of the surface roughness of petals. The roughness of
petal surfaces is of great importance for all colour vision systems,
independent of polarization blindness or polarization sensitivity, which must
efficiently detect and distinguish the colours of flowers.
In columns 2 and 3 of Fig.
9, we can see that, at a given illumination direction and in a
given (e.g. blue) part of the spectrum, the gross features of the patterns of
and
of the F. benjamina leaf are similar for both
sunlit and shaded cases, although the colours of the sunlit and shaded leaf
differ considerably. This is because the smooth F. benjamina leaf is
similar to a Fresnel reflector, and the leaf blade is tilted so that sunlight
cannot be reflected specularly from it towards the camera (apart from certain
small curved areas). Thus, the sunlight reflected specularly from the leaf
blade is not visible and does not add to the leaf-tissue-backscattered light.
Large differences between the reflection-polarization characteristics of
sunlit and shaded leaves occur only if the direction of view coincides with or
is near to the direction of specular reflection. This is seen at those regions
of the F. benjamina leaf shown in
Fig. 9G,H, where, owing to the
appropriate local orientation of the curved leaf blade, the sunlight is
specularly reflected. The consequence of this is that, in a considerable
portion of these areas, the leaf blade is overexposed owing to the toobright
reflected sunlight.
All our findings are in accord with the earlier results of Shul'gin and
Moldau (1964), Vanderbilt and
Grant (1985a
,
b
), Vanderbilt et al.
(1985a
,
b
), Grant
(1987
), Grant et al.
(1987a
,
b
,
1993
) and Sarto et al.
(1989
), who measured the
polarized, non-polarized and specular reflectance of leaves of many different
plant species as functions of the leaf surface features in the visible and
near-infrared parts of the spectrum by point-source polarimetry. They found
that in some viewing directions the surface reflection is so large that leaves
appear white instead of green. In this case, the strong specularly
surface-reflected white light overwhelms the much smaller amount of green
light scattered diffusely by the interior leaf tissue. They showed that the
reflectance of the colourless and transparent leaf epidermis is practically
independent of the wavelength of light, and, in the visible part of the
spectrum, the degree of polarization of light reflected from green leaves is
always the lowest in the green spectral range. They also demonstrated that the
whitish light reflected specularly from leaves is always strongly polarized,
while the green light reflected diffusely and non-specularly is practically
unpolarized.
Do polarization-induced false colours influence the colour vision of
Papilio butterflies under natural conditions?
Figs
4,5,6,7,8,
10 clearly show that, for our
weakly polarization-sensitive model retina, the polarization-induced false
colours of plants fall near the real colours perceived by a polarization-blind
retina, even if they reflect strongly polarized light. Another effect of
specular reflection is that whitish glare strongly masks the colour hue. Is
the colour vision system of Papilio butterflies sensitive enough to
perceive the tiny polarization-induced colour shifts in Figs
4,5,6,7,8,
10 under these circumstances?
Behavioural studies on the discrimination of weakly saturated colours by
insects are scarce. Honeybees seem to be able to discriminate pure white from
white mixed with just a few percent of spectral light
(Daumer, 1963;
Lieke, 1984
). Such stimuli
differ in their locus position to a comparable degree, as the loci of the real
colours differ from some of the polarizational false colours calculated in
this study. However, how well Papilio discriminates unsaturated
colours remains to be demonstrated.
In plant parts with dominating diffuse reflection, the colour saturation is
relatively high but the is low
(Table 1). Although in this
case hue discrimination will be good, the false colour effect is minute (1-4
and 7-10 in Fig. 5). Thus,
under natural conditions, the weak polarization sensitivity of the
photoreceptors might not interfere with the colour vision at all. This may be
the reason why the average PS value of the photoreceptors in proven
colour-sensitive insects is not reduced to 1.0 but is found to be
approximately 2.0-2.5 (Cataglyphis bicolor,
Labhart, 1986
;
Papilio, Kelber et al.,
2001
; Drosophila melanogaster,
Speck and Labhart, 2001
; other
fly species, Hardie, 1985
).
Only in honeybees is the PS value significantly smaller than 2
(Labhart, 1980
). The complete
destruction of the polarization sensitivity in a microvillar photoreceptor is
not a trivial task but calls for a systematic misalignment of the microvilli
along the rhabdom, in which complicated optical effects such as self-screening
and lateral filtering within the rhabdom must be considered. The microvilli
are misaligned by random or continuous direction changes (twisting) along the
rhabdom, but, in most photoreceptors, certain microvillar directions still
dominate (reviewed by Labhart and Meyer,
1999
). In honeybees, the rhabdom twists by about 180°, which
reduces the PS to lower values than in other insects
(Wehner et al., 1975
;
Labhart, 1980
). This might be
taken as an indication that the exquisite colour vision system of honeybees
might be more sensitive to small colour differences than that of other insect
species and, thus, be more compelled to avoid polarizational false
colours.
Recently, Kelber (1999a)
and Kelber et al. (2001
)
showed that the colour choices of butterflies P. aegeus and P.
xuthus is influenced by the e-vector orientation of linearly polarized
light emitted by the colour stimuli to which the butterflies are exposed. They
suggested that the interaction between colour and polarization might help the
butterfly to find the best oviposition sites. Thus, horizontally polarized
green stimuli (mimicking horizontally oriented green leaves) were more
attractive than vertically polarized stimuli of the same colour. At first
glance, the findings of Kelber and collaborators that polarization
influences the colour choices of Papilio butterflies seem to
contradict our conclusion that colour vision is quite insensitive to
reflection polarization. However, in their behavioural tests, the authors used
stimuli that had both a very high degree of polarization (almost 100%) and a
high degree of colour saturation, a situation that does not occur under
natural conditions. Using this hyperstrong polarization/colour saturation
combination, Kelber (1999a
)
and Kelber et al. (2001
)
confirmed behaviourally the polarization sensitivity of the Papilio
photoreceptors that was previously measured electrophysiologically
(Bandai et al., 1992
). We
assume that this receptor property plays only a minor role in real life. To
demonstrate that the polarization sensitivity of the colour vision system can
indeed ease certain vital tasks in the life of a butterfly, further
behavioural experiments with Papilio exposed to stimuli with natural
combinations of degree of polarization and colour saturation are needed. It is
currently unknown how large a false colour shift needs to be in order to be
just detectable and thus useful in a behavioural context. Although we do not
claim that our calculations prove that Papilio is incapable of
detecting false colours under natural conditions, we expect that the
calculated colour shifts in the simulated Papilio retina are not
large enough to be perceived. The question of whether Papilio is
equally sensitive to colours as bees and could perceive spectral shifts
comparable with the polarizational false colour shifts calculated in this work
can be answered only by further studies of the colour sensitivity of
Papilio.
Another finding that seems to contradict our thesis is that, in plants, the
petals are usually less shiny than the leaves
(Kay et al., 1981); i.e.
specular reflection is reduced relative to diffuse reflection and, therefore,
they exhibit less polarization. One might argue that this is to reduce false
colour effects and, thus, to improve flower recognition. However, matter
petals also avoid masking of the hue of a flower by whitish glare. The
avoidance of glare alone may already be reason enough to reduce specular
reflection in petals: the matter the petals, the more constant the appearance
of flower colour when seen from different directions.
Limitations of our polarimetric technique and retina model and their
consequences
Papilionid butterflies have a pentachromatic colour vision system, which
was discovered by Arikawa et al.
(1987). Thus, taking into
account only three of the five known receptor types seems to be an
over-simplification and does not represent the exact (possibly
five-dimensional) colour space of the animal. We admit that our approach has
inherent limitations: our polarimetric technique cannot measure the
reflection-polarization characteristics of plant surfaces in the UV, and our
retina model disregards the violet (V) and UV receptor types. However, these
do not destroy the utility of our approach and, by no means, the validity of
our conclusions owing to the following reasons.
First, the optical phenomenon that low degrees of polarization of light reflected from plant surfaces are always associated with high colour saturations, and strongly polarized reflected light is necessarily associated with low colour saturation is valid for both the UV and visible ranges of the spectrum. Although demonstrated in the visible spectrum only, there is no physical reason why this phenomenon should not occur in the UV. Hence, the wavelength limitations of our instrument do not restrict the mentioned phenomenon to the visible spectrum. Second, the two reasons for the small differences between the real and polarizational false colours of plant surfaces calculated in this work are the above-mentioned optical phenomenon and the weak polarization sensitivity of the Papilio photoreceptors. Involving also the violet and UV receptors in an improved pentachromatic retina model and using additional reflection-polarization data measured by a UV-sensitive polarimeter would not result in larger shifts of polarization-induced false colours with respect to the corresponding real colours. This would only change the position of the colour loci but not the magnitude of chromatic differences. For instance, our retina model could be improved in such a way that the spectral sensitivity function of the `short wavelength macro-receptor' compressing the UV, violet and blue (B) receptors with the same microvilli orientation is chosen to be much broader (e.g. stretching from 300 nm to 550 nm) than that of the blue receptor in Fig. 1A. However, the only effect of the enhanced sensitivity of this macro-receptor on the colour calculations would be a shift of all real and polarizational false colours towards the short-wavelength range of the spectrum, while their chromatic distances would not change significantly and would remain small henceforward. Varying the number of receptor types involved in the model retina and changing their spectral sensitivity functions can drastically alter the loci of the real and polarizational false colours as well as their relative directions within a multi (3, 4 or 5)-dimensional colour space but has only a minor influence on the chromatic distances of the false colours from the corresponding real colours. This was quantitatively shown as follows: all colour calculations for our trichromatic model retina using integral normalization of the red, green and blue sensitivity functions (Fig. 1A) were repeated using amplitude normalization (see Materials and methods). Practically the only effect of this normalization switch was that all colours shifted towards the greenred border of the RGB colour triangle without significant changes of their chromatic distances or relative directions, although the switch did result in significant changes in the relative spectral sensitivity functions.
In our retina model the UV, violet and blue receptors can be treated as one receptor type owing to the following:
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