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First published online August 17, 2007
Journal of Experimental Biology 210, 3075-3081 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002725
Absence of eye shine and tapetum in the heterogeneous eye of Anthocharis butterflies (Pieridae)
1 Graduate School of Integrated Science, Yokohama City University, 22-2
Seto, Kanazawa-ku, Yokohama 236-0027, Japan
2 Department of Neurobiophysics, University of Groningen, Nijenborgh 4,
NL-9747 AG Groningen, The Netherlands
3 Laboratory of Neuroethology, The Graduate University for Advanced Studies
(Sokendai), Shonan Village, Hayama, 240-0193, Japan
Author for correspondence (e-mail:
arikawa{at}soken.ac.jp)
Accepted 28 June 2007
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Key words: rhabdom shape, ommatidial heterogeneity, yellow tip, orange tip, screening pigment
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). It contains the day-flying true butterflies
(Papilionoidea), the skippers (Hesperioidea), and a newly identified group of
the nocturnal Hedyloidea (Scoble,
1986). The eyes of true butterflies are of the apposition type
(Nilsson et al., 1988),
whereas those of skippers and Hedyloidea are of the superposition type
(Yack et al., 2007), which is
typical in moths (Nilsson,
1989). The eyes of moths have two characteristic optical
structures that probably function to increase the light sensitivity: the
tapetal mirror and the corneal nipple array
(Miller, 1979). The tapetum is
composed of tracheoles at the proximal portion of the rhabdom and reflects
unabsorbed light back into the rhabdom, thus providing a second chance for
light to be absorbed. The corneal nipple array, known as the `moth-eye'
structure, is a set of protuberances of height about 200 nm, acting as a
thin-film antireflection coating. These structures are basically retained in
the apposition eyes of true butterflies, but all species in the family
Papilionidae lack both (Bernhard et al.,
1970; Stavenga et al.,
2006).
Recent studies on the cellular organization of butterfly eyes have
demonstrated that the ommatidia are spectrally heterogeneous and typically
form three classes containing different sets of spectral photoreceptors
(Qiu et al., 2002;
Arikawa, 2003;
Briscoe et al., 2003;
Sauman et al., 2005). The
three types of ommatidia are randomly distributed in the regularly arranged
hexagonal lattice of the compound eye. The ommatidial heterogeneity and random
distribution of the different ommatidial types are shared by other insects
(Ribi, 1978;
White et al., 2003;
Spaethe and Briscoe, 2005;
Wakakuwa et al., 2005) and are
probably related to color vision (Frisch,
1914; Kelber and Henique,
1999; Kelber and Pfaff,
1999; Kinoshita et al.,
1999; Kelber et al.,
2002; Zaccardi et al.,
2006).
The ommatidial heterogeneity of butterfly eyes can be attractively observed
by epi-illumination microscopy, because diurnal butterflies exhibit a colorful
eye shine due to the tapetum (Miller and
Bernard, 1968; Stavenga et
al., 2001). The color of the eye shine is determined by three main
components: (i) the spectral reflectance of the tapetum, (ii) the absorption
spectra of the visual pigments that are concentrated in the rhabdom, and (iii)
photostable screening pigments that often exist as clusters of granules in the
photoreceptor cell bodies near the rhabdom
(Arikawa and Stavenga, 1997;
Arikawa, 1999;
Qiu et al., 2002;
Briscoe and Bernard, 2005;
Zaccardi et al., 2006). The
colors of the eye shine pattern appeared to be species-dependent
(Bernard and Miller, 1970), so
we performed a survey of a number of butterfly species to investigate whether
there exists a general rule underlying the eye structure and eye shine colors
(Stavenga et al., 2001).
In the course of the survey, we recently discovered that the yellow tip
Anthocharis scolymus (Pieridae, Lepidoptera) does not exhibit eye
shine. This is quite exceptional, because the eye shine has been observed in
all inspected species from all butterfly families except the Papilionidae
(Miller and Bernard, 1968;
Miller, 1979). We therefore
investigated the ommatidial anatomy of the yellow tip, and we found that the
species does not have a structure resembling the tapetum. The anatomical
investigations also revealed that the yellow tip retina is heterogeneous,
containing at least two distinct types of ommatidia. The eye of the yellow tip
appears to be rather simple compared to other insects.
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Materials and methods |
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Eye shine and fluorescence
A butterfly was immobilized with beeswax, with the head gently glued to the
thorax, and put on the stage of a fluorescence microscope (BX-60, Olympus,
Tokyo, Japan) equipped with an epi-illumination attachment. The possible
existence of eye shine was investigated by focusing the microscope at the
level of the cornea or the center of the eye. Using white light, in the main,
fronto-ventral part of the eyes of pierid butterflies a clear red eye shine is
then normally observed (Ribi,
1979; Stavenga et al.,
2001; Qiu et al.,
2002; Stavenga,
2002a; Stavenga,
2002b). The possible existence of ommatidial fluorescence was also
checked under ultraviolet and blue-violet excitation light.
Retinal anatomy
For electron microscopy, compound eyes isolated from the heads were
prefixed in 2% paraformaldehyde and 2% glutaraldehyde in 0.1 mol
l–1 sodium cacodylate buffer (CB, pH 7.3) for 30 min at
20–25°C. After a brief wash with 0.1 mol l–1 CB,
the eyes were postfixed in 2% osmium tetroxide in 0.1 mol l–1
CB for 2 h at 20–25°C. Embedding in Epon followed dehydration with a
graded series of acetone and infiltration with propylene oxide. The tissues
were cut into 60–70 nm ultrathin sections, either longitudinally or
transversely to the ommatidial long axes. The sections were observed using
transmission electron microscopes (JEM 1200EX, JEOL Tokyo; H7650, Hitachi
Tokyo). For light microscopy, the prefixed eyes were dehydrated and embedded
in Epon without being postfixed with osmium tetroxide. The tissues were cut
into 5 µm sections and observed using a microscope (BX60, Olympus).
To correlate the ommatidial fluorescence and pigmentation, the fluorescence
under 420 nm excitation was first recorded from a large number of ommatidia
using a modified epi-illumination optical set-up
(Stavenga, 2002b) equipped
with an objective lens of large numerical aperture (NA) and long working
distance (WD) (Olympus MPLFLN20X, NA=0.45, WD=6.6 mm). The eyes were then
processed for light microscopy as described above. When cutting sections, the
eyes were carefully aligned so that the ommatidia in the region from which the
fluorescence was recorded were cut perpendicular to the ommatidial axes.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The
eyes of both male and female yellow tip Anthocharis scolymus,
however, failed to display anything like an eye shine. The absence of the eye shine in papilionid butterflies can be immediately understood from the absence of tapeta proximally of the rhabdoms. We thus hypothesized that the lack of eye shine of the yellow tip is also due to a non-functional or absent tapetum. To test this hypothesis we investigated the anatomy of the yellow tip retina.
Transmission electron microscopy: absence of a tapetal structure
Transverse sections in the proximal and basal part of an ommatidium are
shown in Fig. 1A,B. There are
nine photoreceptor cells, R1–R9, of which the rhabdomeres of the
R5–R8 form the proximal part of the rhabdom
(Fig. 1A) and the R9 cell body
occupies the basal part of the ommatidium immediately distal to the basement
membrane (Fig. 1B).
Fig. 1C shows a longitudinal
section of an ommatidium, in the proximal region of the retina, where normally
the tracheoles are folded into a multilayer stack. Such a structure appears to
be non-existent in the eye of the yellow tip. A small tracheal cell is
nevertheless clearly present, and its cell body exists near the end of the
rhabdom. The cell body of the tracheal cell lies around the ommatidium
(Fig. 1A), and it seems almost
to have crawled under the rhabdom at the base of the ommatidium
(Fig. 1B). Each tracheal cell
sends four extensions into the retina, very similar to other butterfly eyes
(Ribi, 1979;
Qiu et al., 2002).
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). The
pigment clusters are arranged in a square pattern
(Fig. 2A). In proximal sections
the complementary subset had clusters of pale-red pigment
(Fig. 2C). In the transitional
layer (Fig. 2B) both types of
ommatidia feature peri-rhabdomal pigmentation. Here the pale-red pigment
clusters are trapezoidally arranged (Fig.
2B, broken circle). Note also that the ommatidial type with the
pale-red pigment clusters has additional pigmentation in the cell body of
R5–R8 in the area remote from the rhabdom (white arrowheads in
Fig. 2).
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).
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The shape of the rhabdom appeared to differ between the two ommatidial
types. To clarify this further, we cut transverse, ultrathin sections at 10
µm intervals through the entire thickness of the retina in the ventral
region of the fronto-lateral eye region. The length of the ommatidia, i.e. the
distance between the surface of the cornea and the basement membrane, is about
420 µm. The images in Fig.
4, taken at a depth of 140 µm (A,F), 210 µm (B,G), 260 µm
(C,H), 300 µm (D,I) and 340 µm (E,J) from the corneal surface, obviously
show ommatidial heterogeneity. Whereas similar anatomical work on the small
white Pieris rapae crucivora (Qiu
et al., 2002), demonstrated the existence of three types of
ommatidia, no more than two types of ommatidia can be distinguished in the
yellow tip Anthocharis scolymus.
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In the first, round-type ommatidium, the rhabdomeres of the R1–R4
photoreceptors, which form the rhabdom in the distal half of the retina, have
curved microvilli (Fig. 4A,B).
The cell bodies of R1 and R2 are arranged along the dorso-ventral axis, and
those of R3 and R4 are oriented along the fronto-lateral axis
(Fig. 4K). The R5–R8
photoreceptors contribute microvilli to the rhabdom in the remaining proximal
half of the retina, with the cell bodies arranged diagonally
(Fig. 4C–E,
Fig. 4I,J; see also
Fig. 4K). The R9 is well
recognizable at the basal level, immediately distal to the basement membrane
(Fig. 1B,C), but it appears
that R9 contributes only a minor basal part of the rhabdom, similar to
Pieris. As for Pieris, we define the R1–R4 of
Anthocharis as the distal photoreceptors, the R5–R8 as the
proximal photoreceptors, and the R9 as the basal photoreceptor
(Qiu et al., 2002).
The second, trapezoidal-type ommatidium has basically the same arrangement of photoreceptors, but there are striking differences in the structural organization. The rhabdomeres of R1–R4 contribute to the rhabdom over a distinctly longer distance, about the distal two-thirds of the retina, and the rhabdomeres of R5–R8 together form the rhabdom in the proximal one-third (Fig. 4K). The rhabdomere of the R2 (or the R1) photoreceptor in the trapezoidal-type ommatidia has a wider face than that of the R1 (or the R2), and this fatter receptor cell has straight microvilli, at least over a distance of about 100 µm in the middle part of the retina.
The R5–R8 photoreceptors in all ommatidia bear screening pigment granules, accumulated in clusters near the rhabdom boundary, but the distribution of the granules clearly differs between the two types of ommatidia. The pigment granules in the round-type ommatidia occur in the distal half of the ommatidia (Fig. 4A–C), whereas those in the trapezoidal-type are localized in the proximal one-third (Fig. 4I,J).
Among the 194 ommatidia we counted, there were 90 (46.4%) round- and 104 (53.6%) trapezoidal-type ommatidia. This ratio is consistent with the ratio counted among the non-fluorescing (47.3%) and the fluorescing type ommatidia (52.7%).
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The eye heterogeneity of Anthocharis scolymus with two ommatidial
types seems rather simple, for other insect species so far studied have three
or more types of ommatidia. In another pierid butterfly, Pieris rapae
crucivora, three types of ommatidia are evident, even by light
microscopy, from three distinct patterns of pigment clusters: trapezoidal,
square and rectangular (Qiu et al.,
2002). In a papilionid butterfly, Papilio xuthus,
histology revealed two ommatidial types, with either red or yellow
pigmentation around the rhabdom. The red-pigmented ommatidia in fact form two
separate types of ommatidia, as part of the red-pigmented ommatidia fluoresces
under ultraviolet epi-illumination (Arikawa
and Stavenga, 1997). We have scrutinized the eye of
Anthocharis scolymus to determine whether it was possible to
distinguish three types of ommatidia, but could identify only two types in the
present anatomical study.
We classified the two types of Anthocharis ommatidia as round and
trapezoidal, according to the cross-sectional profile of the rhabdom. The main
reason for the different shapes of the rhabdom is the enlarged rhabdomere of
either photoreceptor R1 or R2 in the trapezoidal-type
(Fig. 4). The larger rhabdomere
is invariably composed of straight microvilli
(Fig. 4G–I). A similar
situation has been reported for Pieris, where the enlarged rhabdomere
of R1 (or that of R2) also causes a trapezoidal cross-section of the rhabdom
and consists of straight microvilli. The trapezoidal ommatidial type of
Pieris is called type I, and its fatter rhabdomere has been shown to
belong to a blue-sensitive photoreceptor, while the accompanying
photoreceptor, R2 (or R1), is ultraviolet sensitive
(Qiu and Arikawa, 2003).
Presumably, therefore, the fatter R1 (or R2) rhabdomere of the trapezoidal
ommatidial type of Anthocharis also belongs to a blue-sensitive
photoreceptor, while the more slender R2 (or R1) is an ultraviolet sensitive
photoreceptor. The straight microvilli of the enlarged photoreceptor may play
a role in polarization detection (Qiu et
al., 2002).
We found that the trapezoidal type ommatidia emit fluorescence under 420 nm
excitation light. A very similar fluorescence is also observed in the eyes of
male Pieris rapae crucivora. In male Pieris, the fluorescing
pigment is located in type II ommatidia, whose R1 and R2 photoreceptors both
contain a violet-absorbing visual pigment. There the fluorescing pigment acts
as a spectral filter, peaking at 420 nm, with the result that the R1 and R2
are double-peaked blue receptors, specific for males
(Arikawa et al., 2005). The
eyes of Papilio xuthus contain ommatidia that fluoresce
under 360 nm epi-illumination. The fluorescing material, most likely
3-hydroxyretinol, is accumulated in the most distal portion of type II
ommatidia, whose R1 and R2 photoreceptors have the same ultraviolet-absorbing
visual pigment as that of the ultraviolet receptors in type I ommatidia.
Electrophysiological recordings demonstrated that the R1 and R2 of type II
ommatidia are violet receptors with an extraordinary narrow spectral
sensitivity, due to the filtering effect of 3-hydroxyretinol
(Arikawa et al., 1999). We
assume that the fluorescing pigment of Anthocharis also acts as a 420
nm-peaking spectral filter. If R1 and R2 of the trapezoidal type contain a
blue- (e.g. 460 nm) and ultraviolet- (e.g. 360 nm) absorbing visual pigment,
similar to Pieris, the effect of the fluorescing pigment will be that
the sensitivity peaks of R1 and R2 are shifted away from each other, in
opposite spectral directions. Experimental evidence for this conclusion will
require further electrophysiological analysis.
The rhabdom of Anthocharis is tiered, and thus the visual pigments in the distal tier act together as an optical filter in front of the photoreceptors in the proximal tier. For instance, when short-wavelength absorbing visual pigments are concentrated in the distal tier and long-wavelength absorbing visual pigments in the proximal tier, this will result in a reduced absorption and thus a reduced sensitivity of the proximal receptors in the short-wavelength range. In addition to the visual pigments, perirhabdomeral screening pigment clusters affect the light flux in the rhabdom. In the tiered retina of Papilio and Pieris, the proximal photoreceptors, R5–R8 do not bear microvilli in the distal tier. However, the cell bodies of R5–R8 exist throughout the length of the retina, and they contain dense clusters of pigment granules over most of the length of the distal tier. The pigment clusters thus act as an effective light filter for the proximal receptors themselves. The design principle of a pigment filter in the distal extensions of the proximal photoreceptors is also applied in the retina of Anthocharis, although only in the round ommatidial type. In the trapezoidal type the pigment granule clusters are, surprisingly, deposited only in the proximal tier.
The different position of the pigment clusters of the proximal
photoreceptors emphasizes the heterogeneity of the ommatidial lattice
(Fig. 2). Ommatidial
heterogeneity is a widespread characteristic of insect compound eyes. In the
honeybee and bumblebee retina, three randomly distributed ommatidial types
were distinguished on the basis of the ultraviolet- and blue-sensitive distal
photoreceptors (Spaethe and Briscoe,
2005; Wakakuwa et al.,
2005). The retina of some nymphaline butterflies is probably
organized in a very similar way (Briscoe
and Bernard, 2005). Yet, other nymphalids have clearly recruited
red photoreceptor screening pigments that act as red filters
(Stavenga et al., 2001;
Stavenga, 2002a;
Stavenga, 2002b;
Sauman et al., 2005;
Zaccardi et al., 2006), and
the same holds for papilionids (Arikawa and
Stavenga, 1997; Arikawa,
2003) and lycaenids (Arikawa
and Stavenga, 1997; Stavenga,
2002a; Sison-Mangus et al.,
2006). Furthermore, detailed molecular biological analyses
revealed that in the latter case the short-wavelength receptors diversified to
such an extent that no less than six ommatidial types exist
(Sison-Mangus et al.,
2006).
Comparing the retinal organization of the different lepidopteran families
reveals an impressive diversification and specialization. Although some
exceptional cases are known (Yack et al.,
2007), the butterflies are diurnal
(Grimaldi and Engel, 2005).
The ancestral moth eyes are characterized by so-called `moth-eye' corneal
nipple array and tracheolar tapeta, which have been maintained by most
butterfly species. Interestingly, both traits have been lost in the
papilionids (Miller, 1979). In
a relative of the yellow tip, the European orange tip Anthocharis
cardamines, the corneal nipple array is well present
(Stavenga et al., 2006), but
the tapetum has vanished, as concluded from the absence of eye shine (G. D.
Bernard and D.G.S., unpublished observations). The American falcate orange tip
Anthocharis midea also lacks eye shine, and anatomy performed on this
species also demonstrated the absence of a tapetum proximal to the rhabdom (G.
D. Bernard and W. H. Miller, personal communication). It thus appears that the
tapetum is a trait specifically lost by the pierid genus Anthocharis.
Species in other genera of the tribe Anthocharidini basically share the life
style with Anthocharis: adults fly only in early spring. The great
orange tip Hebomoia glaucippe, which belongs to the Colotis
group, is phylogenetically close to the Anthocharidini
(Braby et al., 2006). It has
several generations within a year, however, as is the case for
Pieris, and exhibits bright red eye shine (K.A., unpublished
observation). A more detailed survey of the Pierinae may reveal whether or not
the loss of tapetum is related to the life cycle.
The loss of the tapetum in Anthocharis as well as in Papilionidae
raises the question whether this inflicts a loss in visual functions. Although
the eye shine is a most striking phenomenon, quantitative evaluation of the
tapetal reflections indicates in fact only a small contribution of the tapetum
to the light sensitivity, at least in a diurnal pierid species Pieris
rapae crucivora (Wakakuwa et al.,
2004). The tapetum of the nocturnal moths probably raises the
sensitivity much more substantially. We conclude that the selective pressure
for butterflies to maintain the tapetum is only minor.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Arikawa, K. (1999). Color vision. In Atlas of Sensory Receptors of Arthropods – Dynamic Morphology in Relation to Function (ed. E. Eguchi and Y. Tominaga), pp.23 -32. Tokyo: Springer Verlag.
Arikawa, K. (2003). Spectral organization of the eye of a butterfly Papilio. J. Comp. Physiol. A 189,791 -800.[CrossRef][Medline]
Arikawa, K. and Stavenga, D. G. (1997). Random array of colour filters in the eyes of butterflies. J. Exp. Biol. 200,2501 -2506.[Abstract]
Arikawa, K., Mizuno, S., Scholten, D. G. W., Kinoshita, M., Seki, T., Kitamoto, J. and Stavenga, D. G. (1999). An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio.Vision Res. 39,1 -8.[CrossRef][Medline]
Arikawa, K., Wakakuwa, M., Qiu, X., Kurasawa, M. and Stavenga,
D. G. (2005). Sexual dimorphism of short wavelength
photoreceptors in the small white buterfly, Pieris rapae crucivora.J. Neurosci. 25,5935
-5942.
Bernard, G. D. and Miller, W. H. (1970). What does antenna engineering have to do with insect eyes? IEEE Student J. 8,2 -8.
Bernhard, C. G., Genme, G. and Saellstroem, J. (1970). Comparative ultrastructure of corneal surface topography in insects with aspects on phylogenesis and function. Z. Vergl. Physiol. 67,1 -25.[CrossRef]
Braby, M. F., Vila, R. and Pierce, N. E. (2006). Molecular phylogenty and systematics of the Pieridae (Lepidoptera: Papilionoidea): higher classification and biogeography. Zool. J. Linn. Soc. 147,239 -275.[CrossRef]
Briscoe, A. D. and Bernard, G. D. (2005).
Eyeshine and spectral tuning of long wavelength-sensitive rhodopsins: no
evidence for red-sensitive photoreceptors among five Nymphalini butterfly
species. J. Exp. Biol.
208,687
-696.
Briscoe, A. D., Bernard, G. D., Szeto, A. S., Nagy, L. M. and White, R. H. (2003). Not all butterfly eyes are created equal: rhodopsin absorption spectra, molecular identification and localization of UV-blue- and green-sensitive rhodopsin encoding mRNA in the retina of Vanessa cardui. J. Comp. Neurol. 458,334 -349.[CrossRef][Medline]
Frisch, K. v. (1914). Der Farbensinn und Formensinn der Biene. Zool. J. Physiol. 37, 1-238.
Grimaldi, D. and Engel, M. S. (2005). Evolution of the Insects. New York: Cambridge University Press.
Kelber, A. and Henique, U. (1999). Trichromatic colour vision in the hummingbird hawkmoth, Macroglossum stellatarum L. J. Comp. Physiol. A 184,535 -541.[CrossRef]
Kelber, A. and Pfaff, M. (1999). True colour vision in the orchard butterfly, Papilio aegeus.Naturwissenschaften 86,221 -224.[CrossRef]
Kelber, A., Balkenius, A. and Warrant, E. J. (2002). Scotopic colour vision in nocturnal hawkmoths. Nature 419,922 -925.[CrossRef][Medline]
Kinoshita, M., Shimada, N. and Arikawa, K. (1999). Colour vision of the foraging swallowtail butterfly Papilio xuthus. J. Exp. Biol. 202,95 -102.[Abstract]
Miller, W. H. (1979). Ocular optical filtering. In Handbook of Sensory Physiology. Vol.VII/6A (ed. H. Autrum), pp.69 -143. Berlin, Heidelberg, New York: Springer-Verlag.
Miller, W. H. and Bernard, G. D. (1968). Butterfly glow. J. Ultrastruct. Res. 24,286 -294.[CrossRef][Medline]
Nilsson, D.-E. (1989). Optics and evolution of the compound eye. In Facets of Vision (ed. D. G. Stavenga and R. C. Hardie), pp. 30-73. Berlin, Heidelberg, New York, London, Paris, Tokyo: Springer-Verlag.
Nilsson, D.-E., Land, M. F. and Howard, J. (1988). Optics of the butterfly eye. J. Comp. Physiol. A 162,341 -366.[CrossRef]
Qiu, X. and Arikawa, K. (2003). The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly, Pieris rapae crucivora. J. Comp. Physiol. A 189,81 -88.[Medline]
Qiu, X., Vanhoutte, K. A. J., Stavenga, D. G. and Arikawa, K. (2002). Ommatidial heterogeneity in the compound eye of the male small white butterfly, Pieris rapae crucivora. Cell Tissue Res. 307,371 -379.[CrossRef][Medline]
Ribi, W. A. (1978). A unique hymenopteran compound eye. The retina fine structure of the digger wasp Sphex cognatus Smith (Hymenoptera, Sphecidae). Zool. Jb. Anat. Bd. 100,299 -342.
Ribi, W. A. (1979). Coloured screening pigments cause red eye glow hue in Pierid butterflies. J. Comp. Physiol. A 132,1 -9.[CrossRef]
Sauman, I., Briscoe, A. D., Zhu, H., Shi, D., Froy, O., Stalleicken, J., Yuan, Q., Casselman, A. and Reppert, S. M. (2005). Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46,457 -467.[CrossRef][Medline]
Scoble, M. J. (1986). The structure and affinities of the Hedyloidea: a new concept of the butterflies. Bull. Br. Mus. Nat. Hist. Entomol. 53,251 -286.
Sison-Mangus, M. P., Bernard, G. D., Lampel, J. and Briscoe, A.
D. (2006). Beauty in the eye of the beholder: the two blue
opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually
dimorphic eyes. J. Exp. Biol.
209,3079
-3090.
Spaethe, J. and Briscoe, A. D. (2005).
Molecular chracterization and expression of the UV opsin in bumblebees: three
ommatidial subtypes in the retina and a new photoreceptor organ in the lamina.
J. Exp. Biol. 208,2347
-2361.
Stavenga, D. G. (2002a). Colour in the eyes of insects. J. Comp. Physiol. A 188,337 -348.[CrossRef][Medline]
Stavenga, D. G. (2002b). Reflections on
colourful ommatidia of butterfly eyes. J. Exp. Biol.
205,1077
-1085.
Stavenga, D. G., Kinoshita, M., Yang, E.-C. and Arikawa, K. (2001). Retinal regionalization and heterogeneity of butterfly eyes. Naturwissenschaften 88,477 -481.[CrossRef][Medline]
Stavenga, D. G., Foletti, S., Palasantzas, G. and Arikawa, K. (2006). Light on the moth-eye corneal nipple array of butterflies. Proc. R. Soc. Lond. B Biol. Sci. 273,661 -667.[Medline]
Wakakuwa, M., Stavenga, D. G., Kurasawa, M. and Arikawa, K.
(2004). A unique visual pigment expressed in green, red and
deep-red receptors in the eye of the small white butterfly, Pieris rapae
crucivora. J. Exp. Biol.
207,2803
-2810.
Wakakuwa, M., Kurasawa, M., Giurfa, M. and Arikawa, K. (2005). Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92,464 -467.[CrossRef][Medline]
White, R. H., Xu, H., Munch, T., Bennett, R. R. and Grable, E.
A. (2003). The retina of Manduca sexta:
rhodopsin-expression, the mosaic of green-, blue- and UV-sensitive
photoreceptors and regional specialization. J. Exp.
Biol. 206,3337
-3348.
Yack, J. E., Johnson, S. E., Brown, S. G. and Warrant, E. J. (2007). The eyes of Macrosoma sp. (Lepidoptera: Hedyloidea): A nocturnal butterfly with superposition optics. Arthropod Struct. Dev. 36, 11-22.[CrossRef]
Zaccardi, G., Kelber, A., Sison-Mangus, M. P. and Briscoe, A.
D. (2006). Color discrimination in the red range with only
one long-wavelength sensitive opsin. J. Exp. Biol.
209,1944
-1955.
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  M. P. Sison-Mangus, A. D. Briscoe, G. Zaccardi, H. Knuttel, and A. Kelber The lycaenid butterfly Polyommatus icarus uses a duplicated blue opsin to see green J. Exp. Biol., February 1, 2008; 211(3): 361 - 369. [Abstract] [Full Text] [PDF]
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270 µm (A), 300 µm (B) and 320 µm (C).
The existence of two ommatidial types is clear from the pigmentation. Four
diagonally arranged pigment clusters occur distally in the round type (solid
circles) and proximally in the trapezoidal type ommatidia (broken circles). In
the transitional zone, some pigments exist in both types as in B. Note that
the ommatidia of the trapezoidal type also bear orange pigment in the cell
body (white arrowheads). Bar, 10 µm.
