Reflections on colourful ommatidia of butterfly eyes
Department of Neurobiophysics, University of Groningen, NL-9747 AG Groningen, the Netherlands
e-mail: stavenga{at}phys.rug.nl
Accepted 30 January 2002
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Summary |
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Key words: butterfly, eye shine, colour, vision, photoreceptor, red sensitivity, regionalization, heterogeneity, tapetum, screening pigment
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Introduction |
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The organization of the spectral types of photoreceptor appears to be much
more complex for butterflies. At least six rhodopsins are present in
papilionids (Briscoe, 1998),
five of which have been shown to be expressed in the retina (Kitamoto et al.,
1998
,
2000
). Parts of the
sensitivity spectra of the (at least) five photoreceptor types of Papilio
xuthus, with peak sensitivities in the ultraviolet, violet, blue, green
and red (Arikawa et al., 1987
),
deviate strongly from known rhodopsin absorption spectra. Some of the
deviations are due to filtering by red and yellow screening pigments, present
in two distinct groups of ommatidia
(Arikawa and Stavenga, 1997
).
The pigments are concentrated in four clusters, more-or-less symmetrically
grouped around the rhabdom, i.e. the cylindrical structure that contains the
visual pigments and acts as an optical waveguide. The screening pigments
selectively absorb short-wavelength light and, thus, fine-tune the sensitivity
spectrum of long-wavelength receptors
(Arikawa et al., 1999b
).
Moreover, a proportion of the ommatidia that contain red screening pigment
also harbour an ultraviolet-absorbing pigment, which sharpens a photoreceptor
class with an ultraviolet rhodopsin into a narrow-band violet receptor
(Arikawa et al., 1999a
). The
five rhodopsins and three photostable pigments are expressed in the retina in
unique combinations, determining three classes of ommatidia
(Kitamoto et al., 2000
). The
three classes are randomly distributed.
Ommatidial heterogeneity appears to be a widespread characteristic of
compound eyes, as follows from anatomical and spectrophotometrical evidence;
e.g. flies (Franceschini et al.,
1981; Hardie,
1986
; Salcedo et al.,
1999
), sphecid wasps (Ribi,
1978a
), moths (Meinecke and
Langer, 1984
), backswimmers
(Schwind et al., 1984
) and
butterflies (Arikawa and Stavenga,
1997
; Stavenga et al.,
2001
). The heterogeneity in the eyes of butterflies can be most
exquisitely observed by epi-illumination microscopy
(Bernard and Miller, 1970
).
Diurnal butterflies, but not Papilionidae
(Miller, 1979
), exhibit a
colourful eye shine due to a reflecting tapetum, present in each ommatidium
proximal to the rhabdom (Miller and
Bernard, 1968
). The tapetum is formed by a tracheole folded into a
stack of layers, alternately consisting of air and cytoplasm, thus creating an
interference reflection filter. Incident light that has travelled through the
rhabdom without being absorbed is mirrored by the tapetum. The eye shine is
the fraction of light also escaping absorption on its way back.
In an early study, Ribi
(1979a) compared the colour of
the tapetal reflection as seen in eye slices, from which the photoreceptor
layer had been removed, with the colour of the eye shine, i.e. with the
tapetum in the intact eye. He found that tapetal reflection and eye shine
colours were virtually identical in Nymphalidae, Satyridae and Lycaenidae, but
not in Pieridae. In pierids, a major part of the eye exhibited a prominent red
eye shine, whereas the colour of the tapetum with the retina removed was
green-yellow. The anatomy of the eye of the small white Pieris rapae
showed that the red eye shine is the result of the presence of a red screening
pigment, which exists in four clusters near the rhabdom, where it selectively
absorbs short-wavelength light propagating along the rhabdom
(Ribi, 1979b
). Evidently, the
function of the pigment clusters in Pieris rapae is identical to that
of the corresponding pigment clusters in Papilio xuthus, namely to
suppress short-wavelength light, thereby shifting the sensitivity spectrum of
the long-wavelength receptors into the red to produce a spectrum corresponding
to sensitivity spectra measured electrophysiologically
(Shimohigashi and Tominaga,
1991
).
Recent anatomical work has revealed that the red pigment of Pieris
rapae eyes consists of two types of photoreceptor screening pigment,
coloured red and deep-red; i.e. the four proximal photoreceptors of an
ommatidium are either red- or deep-red-pigmented. The two different types of
ommatidium are arranged in a random, heterogeneous pattern in the retina,
which can be observed in vivo via the eye shine
(Qiu et al., 2002).
In an extensive comparative study of butterfly eye shine, we found that the
colour of the light reflected from individual, neighbouring ommatidia often
varies substantially in many species, testifying to the strong heterogeneity
of butterfly eyes (Stavenga et al.,
2001). Moreover, a substantial proportion of the ommatidia
appeared to reflect in the red. As in the established case for the pierids,
this red reflection is presumably the result of red pigment filtering the
light flux in the rhabdoms, suggesting that the red-reflecting ommatidia
contain photoreceptors with peak sensitivity in the red.
Inspection of the eye shine is a very attractive method of rapidly
surveying the distribution of red-reflecting ommatidia within the
heterogeneous ommatidial lattice. However, classical epi-illumination
microscopy has serious shortcomings because only low-power objectives with
small apertures can be successfully applied. This paper demonstrates that
these limitations can be largely overcome with a special apparatus that
exploits the optical properties of the butterfly compound eye. The apparatus
allows a large-aperture objective to be used so that the tapetal reflections
of numerous ommatidia can be observed simultaneously. This approach will
facilitate the charting of butterfly eyes and thus stimulate further
understanding of eye regionalization and heterogeneity
(Stavenga, 1992;
Stavenga et al., 2001
). In
addition to presenting a few exemplary cases of butterfly eye shine, it is
argued that the physiological functions of the tapetal mirrors and the
screening pigments can be inferred from reflectance spectra measured from
individual ommatidia.
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Materials and methods |
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Apparatus
The optical apparatus (Fig.
1) is, in principle, a modified epi-illumination microscope. The
rationale of the instrument is that incident light applied to a butterfly eye
is channelled by the facet lens and crystalline cone into the light-guiding
rhabdom. Light reaching the ommatidial tapetum is reflected and guided back
through the rhabdom (see Fig. 1
inset); when not absorbed there, it leaves the eye again and is then
observable as the eye shine. Because butterfly eyes, like those of most
insects, are locally more-or-less spherical, the visual axes of the ommatidia
intersect at the eye's centre of curvature. Hence, the optimal way to fill
ommatidia with light is to position the eye's centre at the focal point of an
objective lens (L1 in Fig. 1)
so that a point source at infinity is focused on the eye's centre.
The point source, which is in reality a slightly extended light source, is created by a white light source focused by lens L2 onto diaphragm D1, which is placed in the focal plane of lens L3. The parallel beam leaving L3 is mirrored by a semi-reflecting mirror, angled at 45° with respect to the optical axes of L1 and L3. L1 and L3 form a telescopic lens pair because they are confocal.
The reflected light beams leaving the individual ommatidia diverge
slightly, depending on the extent of the visual fields of the ommatidia. The
beams intersect each other in the eye's centre; the image created there is
called the deep pseudopupil (DPP)
(Franceschini and Kirschfeld,
1971). In the case of the butterfly, it is also called the
luminous DPP (Stavenga, 1979
).
When the DPP is adjusted to the focal point of L1 and this point coincides
with the centre of the goniometer, the eye shine in various areas of the eye
can be rapidly scanned.
Lens L4 is placed confocal with L1 and, hence, the telescopic lens pair L1 and L4 images the DPP in the back focal plane of L4, where diaphragm D2 is positioned. The eye shine at the level of the corneal facet lenses is finally imaged by lens L5, placed confocal with L4. The projected image is then photographed with a photomicroscope. To obtain an optimal picture, the areas of diaphragms D1 and D2 must be adjusted so that they are slightly wider than the image of the DPP. The number of ommatidia contributing to the eye shine depends directly on the aperture of objective L1. A large number can be captured with a Leitz LM32 0.60 objective, which combines a high numerical aperture with a long working distance. L2-L5 are 80, 100, 80 and 15 mm Spindler and Hoyer (Goettingen, Germany) lenses, respectively. The photomicroscope, with a Zeiss 3.2 0.07 objective, is equipped with a Kodak DC120 digital camera.
The actual experimental apparatus used in the present study has two epi-illumination beams supplied by a 50 W halogen lamp and a 100 W mercury lamp. The halogen lamp provided the white light source in Figs 2 and 3, and the mercury lamp was used in Fig. 3 for applying monochromatic light at 670 or 550 nm (via Schott DAL interference filters, half-width approximately 15 nm). Although stray light and unwanted reflections are largely eliminated, some reflection on the lens surfaces of the microscope objective remains, and this is visible as a central `hot spot'. Its prominence can be diminished by reducing the bandwidth of the illumination beam, as was done in Fig. 2B. A long-pass filter, >550 nm, was used in that case since the eye shine had no components in the shorter wavelength range.
The eye shine photographs were made from dark-adapted eyes. Exposures were
shorter than 1 s so that contamination by the pupil mechanism
(Stavenga et al., 1977) was
circumvented. The exposures lasted a few seconds with the 670 nm illumination
(Fig. 3), but this
long-wavelength light did not activate the pupil.
The apparatus resembles the ophthalmoscopes developed for the analysis of
the visual fields of fly eyes by Franceschini
(1975) and van Hateren
(1984
); the main difference is
the added epi-illumination arm. Land and Osorio
(1990
) used an ophthalmoscope
with a slightly different design to investigate the spatial properties of
butterfly eyes (Land,
1984
).
Reflectance spectra
Reflectance spectra (see Fig.
4) were measured with a conventional epi-illumination microscope
(Leitz Ortholux) equipped with a Leitz NPL10, 0.22 objective. The goniometer
with butterfly was positioned on the stage of the microscope. The eye shine
due to illumination with a broadband, white (150 W Xe) light source was
measured from a single facet by adjusting a diaphragm in front of an Oriel
diode array spectrophotometer attached to the microscope.
|
The measured reflectance spectra can be formally interpreted by realizing
that light emerging from an ommatidium has travelled twice through the length
of the rhabdom while having been reflected at the tapetum. Or, the reflectance
spectrum, Rr(), is given by:
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Results |
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Another example of a butterfly with a distinct dorsal area is the small copper Lycaena phlaeas (Fig. 3). This eye was photographed from four directions, differing by 30° from each other, in a vertical plane. In the main fronto-ventral area, two classes of ommatidium can be distinguished, reflecting predominantly in the green or red. The two classes can be easily discriminated by using suitable monochromatic light, i.e. with wavelengths of 670 or 550 nm. In the dorsal area, a mixed population of bluish-green-reflecting ommatidia exists, but red-reflecting ommatidia are completely absent dorsally.
Reflectance spectra
The different reflection colours in Figs
2 and
3 indicate that the ommatidia
of butterfly eyes can be divided into distinct classes. This is confirmed by
measurements of the reflectance spectra of individual ommatidia.
Fig. 4 presents the spectra of
two members of the two classes, yellow and red, distinguishable in the eye of
Bicyclus anynana (see Fig.
2A). The reflectance spectra of the ommatidia within the same
class appear to scatter slightly, but by no more than 5-10 nm. The reflectance
spectra peak at around 580 and 650 nm and differ distinctly in shape. The
reflectance of the yellow class covers a broad wavelength range, with a
cut-off wavelength at approximately 600 nm, whereas that of the red class is
negligible at wavelengths below 560 nm and its cut-off is at approximately 700
nm.
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Discussion |
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Visualizing the eye shine with a large aperture gives an immediate impression of the distribution of the various classes of ommatidium over the eye. The striking feature of most butterfly eyes is the large degree of heterogeneity of the eye shine pattern. A survey of different species from the families Nymphalidae, Lycaenidae and Pieridae indicates that the eye shine emerging from individual facet lenses is characteristic of the species. The typical yellow/red pattern of Heliconinae (Fig. 2B) also exists in certain Nymphalinae (e.g. Euphaedra christyi), Charaxinae (e.g. Charaxes fulvescens) and Lycaenidae (e.g. Polyommatus icarus), but very different patterns also occur.
Eye regionalization is apparent when a specialized dorsal area exists. Its
extent can be large as in Bicyclus anynana
(Fig. 2A), rather minor, as in
Pieris rapae (Fig.
2C), or it can even be absent, as in Heliconius melpomene
(Fig. 2B). In a comparative
study of a number of heliconian species that all lacked a distinct dorsal
area, we found that the ratio of the differently coloured facets can change
markedly across the eye (M. Joron and D. G. Stavenga, unpublished
observations), suggesting that heterogeneity and regionalization exist
universally in butterfly eyes (Stavenga et
al., 2001).
Eye regionalization suggests that different eye areas have special
functions (Bernard and Remington,
1991). A plausible interpretation for the function of a distinct
dorsal eye area is that it is specialized for discriminating objects against
the sky, where short-wavelength light is dominant
(Stavenga, 1992
). This
explanation probably holds for several butterfly species, as is suggested by
the commonly shorter wavelengths of the eye shine dorsally compared with the
eye shine of the ventral areas of the eye
(Stavenga et al., 2001
). The
usual absence of red-reflecting ommatidia from the dorsal eye area (Figs
2A,C,
3) also indicates that red
sensitivity is not at a premium there. However, there is substantial
interspecies diversity. For example, the reflection pattern of Hypolimnas
anthedon (Nymphalinae) does not comply with the general rule of
shorter-wavelength reflections dorsally because the eye shine in a large
dorsal area is homogeneous yellow-orange and that in the ventral area is
either yellow or variable-green. Also, electroretinogram recordings in
Papilio xuthus suggest that short-wavelength sensitivity is prominent
ventrally (Arikawa et al.,
1987
).
Tapetum and photoreceptor screening pigment
The reflectance spectra measured from single facets of the two classes in
B. anynana show distinct differences
(Fig. 4). How can these spectra
be interpreted? In general, three main variables determine the reflectance:
the tapetum, the visual pigments inside the rhabdom and the screening pigments
in the photoreceptor cell, when granules containing the latter pigments occur
in the immediate surroundings of the rhabdom. The influence of visual pigment
absorption on the spectra of Fig.
4 can be neglected because the spectra were measured after
repeated bright illumination so that the green rhodopsin was virtually fully
bleached (Bernard, 1983).
Prolonged dark adaptation, for a few hours, yielded a spectrum with much lower
reflectance for the yellow class and with a slightly different shape
(Stavenga et al., 2000a
).
In the case of the red ommatidia, reflectance is negligible below 560nm.
This is probably due to a strongly short-wavelength-absorbing,
red-transmitting screening pigment sequestered in certain photoreceptor cells
near the rhabdom. In the yellow ommatidia, a similar, strongly
short-wavelength-absorbing pigment is clearly absent because reflection is
considerable at all wavelengths below 600nm. The long-wavelength cut-off
values of the reflectance spectra, which are approximately 600 and 700nm for
the yellow and red class, respectively, must be determined by the tapetal
mirrors. In other words, the yellow-reflecting ommatidia have a tapetum that
reflects up to approximately 600nm and no screening pigment, and the
red-reflecting ommatidia have a tapetum that reflects up to approximately
700nm together with a red photoreceptor screening pigment that absorbs up to
approximately 560nm. Tapetum and screening pigments are expressed together in
unique combinations, thus determining the ommatidial classes. The reflectance
spectra measured from single facets in the eyes of several other butterfly
species (Qiu et al., 2002; K.
J. A. Vanhoutte and D. G. Stavenga, unpublished observations) suggest that
this conclusion holds quite generally.
Spectral shifts induced by red photoreceptor pigment
The sensitivity spectrum of a photoreceptor cell that receives light
filtered by a red screening pigment depends on the absorption spectrum of the
visual pigment and that of the screening pigment and its effective density. A
distinct red sensitivity, with spectra peaking even above 600nm, has been
noted in several butterfly species
(Swihart and Gordon, 1971;
Bernard, 1979
;
Steiner et al., 1987
;
Scherer and Kolb, 1987a
). In
principle, this sensitivity could be based exclusively on red-absorbing
rhodopsins (Bernard, 1979
).
However, the longest peak wavelength of an insect rhodopsin determined so far
is 600nm (Bernard, 1979
;
Bernard et al., 1988
), and the
often aberrant spectral shape of the sensitivity spectra indicates that red
pigment filters play a central role in butterfly red sensitivity. A red filter
can shift the sensitivity spectrum of a photoreceptor, which in the unfiltered
situation peaks in the green or orange, towards longer wavelengths, i.e. into
the red (Arikawa et al.,
1999b
).
The spectral shift will be especially prominent in the basal photoreceptor,
R9. This photoreceptor fills a short, basal part of the rhabdom, as has been
demonstrated in Nymphalinae (Kolb,
1985), Papilionidae (Arikawa
and Uchiyama, 1996
) and Pieridae
(Qiu et al., 2002
). To
investigate the effect of red screening pigments on the sensitivity spectrum
of R9, I have made a simple computational model
(Fig. 5).
Fig. 5A treats the case of the
red-reflecting ommatidia of Bicyclus anynana, where a red pigment
filter is inferred. The transmittance spectrum of the red filter can be
derived from the measured reflectance spectrum by assuming that the absorption
of the visual pigment can be neglected and that the reflectance spectrum of
the tapetum is flat in the wavelength range 550-650 nm. The normalized
reflectance in that range then approximates a modified hyperbolic curve:
R(
)=1/[1+(
h/
)n];
where
is the wavelength of the light. The wavelength of
half-reflectance,
h, and the exponent, n, are
obtained by fitting the experimental data, yielding values of 590 nm and 60,
respectively. The normalized transmittance is then calculated by taking the
square root of R(
). The visual pigment in R9 is unknown, so
four different rhodopsins are considered, peaking at 530, 550, 570 and 590 nm.
Because the rhabdom length of R9 is short, the sensitivity spectrum in the
unfiltered situation is virtually identical to the (normalized) absorption
spectrum of the rhodopsin, whose shape can be assumed
(Stavenga et al., 2000b
).
Multiplying the filter transmittance spectrum by the rhodopsin absorption
spectrum and subsequent normalization yields the sensitivity spectrum of R9
(Fig. 5B). The induced spectral
shift depends on the rhodopsin spectrum. The sensitivity peak wavelengths are
bathochromic-shifted relative to the rhodopsin peak wavelengths by 44, 37, 27
and 16 nm, respectively. Fig.
5A shows that the resulting sensitivity depends strongly on the
overlap between the rhodopsin and filter spectra. Of course, the absolute
sensitivity is enhanced by the reflecting tapetum, but this will never amount
to more than a factor 2. Fig.
5C depicts a photoreceptor with a rhodopsin peaking at 570 nm and
the spectral shifts induced by four red filters with
h
values of 590, 610, 630 and 650 nm (n=60). The induced spectral
shifts are 27, 38, 46 and 51 nm, respectively. It is again clear that
rhodopsin and filter spectra should have at least some overlap, as both the
increment in spectral shift and the absolute sensitivity progressively drop
when the overlap severely declines.
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The small white Pieris rapae has two types of red-filtering
pigment (Qiu et al., 2002),
with
h values of approximately 610 and 640 nm. The induced
spectral shifts in the red- and deep-red-pigmented ommatidia will be
distinctly different. As indicated by Fig.
5, the shifts will depend strongly on the visual pigments in the
corresponding R9 photoreceptors. We would expect P. rapae to have
rhodopsins peaking near 600 nm because the rhodopsin and filter spectra will
then overlap. Of course, the screening pigments will also induce spectral
shifts in the proximal photoreceptors, R5-R8, but these shifts may be less
pronounced because the pigment is distributed along an extended part of the
rhabdom. As shown for Papilio xuthus, a more detailed analysis of the
spectral effects of the screening pigments will be greatly facilitated when
the sensitivity spectra of the various photoreceptor types are known (Arikawa
et al., 1999a
,
b
); such an analysis will then
also allow the function of the tapetal mirrors to be assessed.
Function of red sensitivity
Shifting the sensitivity spectrum of a photoreceptor with a
short-wavelength-absorbing filter is well known, e.g. the oil droplets in bird
cones (Govardovskii, 1983) and
the carotenoid filters in stomatopod rhabdoms
(Marshall et al., 1991
; for a
review, see Douglas and Marshall,
1999
). Filtering inevitably causes a reduction in absolute
sensitivity, but this cost can be reduced by the tapetal mirror, and it can be
easily worth the benefit of enhanced colour contrast discrimination
(Govardovskii, 1983
). The red
receptors of butterflies may be of special importance during oviposition for
discriminating suitable leaves for the larvae
(Bernard and Remington, 1991
;
Chittka, 1996
;
Kelber, 1999
). The extremely
dense red pigmentation in the Pieridae and the apparently dual system for
enhancing red sensitivity strongly suggest that spectral discrimination in the
red part of the spectrum is especially well-developed in this family
(Kolb and Scherer, 1982
;
Scherer and Kolb, 1987a
).
However, red sensitivity is probably common among butterflies and may serve
several functions, including feeding and mate recognition
(Bernard, 1979
;
Scherer and Kolb, 1987b
;
Kinoshita et al., 1997
).
Creating red receptors via selective red filtering by
photoreceptor screening pigments is not restricted to butterflies; for
example, sphecid wasps apply the same principle
(Ribi, 1978b). It is
intriguing that sphecids, like butterflies, also arrange their red pigments in
four clusters in one class of ommatidium, this class being randomly
distributed within a rather crystalline ordered ommatidial lattice
(Ribi, 1978a
).
Heterogeneity and colour vision
The design concepts underlying the ubiquitous heterogeneity in butterfly
eyes are not understood. The available evidence, coming from different insect
orders, suggests that heterogeneity and colour vision are somehow connected.
For example, the central photoreceptors, R7 and R8, of fly ommatidia exist in
two fixed combinations. The two classes of R7/8 pairs, which are distributed
in a random pattern in the retina of flies
(Franceschini et al., 1981;
Hardie, 1986
;
Salcedo et al., 1999
),
probably together mediate colour vision
(Fukushi, 1989
;
Troje, 1993
).
Recent anatomical and molecular biological work on the moth Manduca
sexta (R. H. White, unpublished results) describes a heterogeneous
organization of the spectral receptor types in the ommatidial lattice
strikingly similar to that of diurnal butterflies, e.g. the papilionid
Papilio xuthus (Arikawa and
Stavenga, 1997; Kitamoto et
al., 2000
) and the nymphalid Vanessa cardui (A. D.
Briscoe and A. S. Szeto, unpublished results). The local heterogeneity of the
spectral photoreceptor types in the eye of Papilio xuthus
(Arikawa and Stavenga, 1997
)
and the possession of colour vision by this butterfly
(Kinoshita et al., 1999
;
Kinoshita and Arikawa, 2000
)
may indeed indicate that heterogeneity and colour vision are intimately
related.
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Acknowledgments |
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