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First published online July 20, 2006
Journal of Experimental Biology 209, 2873-2879 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02311
Color discrimination at the spatial resolution limit in a swallowtail butterfly, Papilio xuthus
School of Advanced Sciences, The Graduate University for Advanced Studies, Hayama 240-0193, Japan
Author for correspondence (e-mail:
kinoshita_michiyo{at}soken.ac.jp)
Accepted 4 May 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: color vision, detection, rhabdom, compound eye, Papilio xuthus
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) at a more
central level. Therefore if the visual target is as small as the limit of our
spatial resolution, we cannot detect the color of the target
(Wandell, 1995).
The compound eyes of insects consist of a number of functional units called
ommatidia. In many diurnal insects, such as bees and butterflies, each
ommatidium contains several photoreceptor cells that construct together a
single photoreceptive organelle, the fused rhabdom. The fused rhabdom acts as
a single optical waveguide, which receives light via its dioptric
apparatus, a facet lens and crystalline cone, from a limited spatial area. The
visual angle covered by an ommatidium, 1-3° in most cases, corresponds to
a single pixel of the visual field of insects: a rhabdom is therefore
equivalent to a cone outer segment of vertebrate retina
(Land and Nilsson, 2002).
However, rhabdoms strikingly differ from cone outer segments because a rhabdom
is usually made up of the photosensitive organelles of two or more different
spectral photoreceptors. Colocalization of multiple spectral photoreceptors in
a single rhabdom suggests that it is basically possible to analyze wavelength
information within a single pixel. The rhabdom therefore is polychromatic
(Gribakin, 1975;
Menzel, 1979).
How small can a visual target be to still allow insects to detect its
color? This question has been previously addressed in honeybees and in
bumblebees. Honeybees were found to detect objects if their visual angle is
larger than 5° (Giurfa et al.,
1997; Giurfa et al.,
1996), whereas the minimal angle for visual detection was found to
be 3° in bumblebees (Spaethe and
Chittka, 2003; Spaethe et al.,
2001). Color discrimination was lost at larger visual angles,
around 15°, thus showing that target detection at smaller angles was
achromatic. Here we determined the minimal visual angle at which color
detection is possible for the Japanese yellow swallowtail butterfly,
Papilio xuthus. This butterfly has ultraviolet (UV), violet (V), blue
(B), green (G), red (R) and broad-band (BB) receptors in the retina. These
spectral photoreceptors are embedded in fixed combinations in three types of
ommatidia. Types I, II and III ommatidia contain four (UV, B, G, R), three (V,
G, BB) and two (B, G) classes of spectral photoreceptors, respectively
(Arikawa et al., 2003).
Papilio butterflies use these receptors to see colors while foraging:
they can be trained to approach a paper patch of a certain color by feeding
them while they observe the colored stimuli
(Kinoshita et al., 1999). The
trained butterflies distinguish the training color from a range of different
colors as well as from a series of grays. By training butterflies to a colored
target, we were able to measure the minimum angular size that a visual target
should subtend for the butterflies to detect its color in a Y-maze
apparatus.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Kinoshita et al., 1999). The
temperature was set at approx. 30°C.
Stimuli
We used as stimuli disks of chromatic (colored) and achromatic (grey) paper
presented on black background paper. The papers used in this study were all
printed by an inkjet printer (Seiko Epson PM800C, Tokyo, Japan) on super fine
paper (Seiko Epson MJA4SP1), except for the black paper for the background.
Reflectance spectra of the paper were measured with a spectrometer (S2000,
Ocean Optics, Inc., Dunedin, FL, USA) that was calibrated against a MgO-coated
surface as the reference (Fig.
2). Papers of human blue, green and red were used as training
colors.
|
 | (1) |
where I(
) is the illumination spectrum,
S() is the spectral sensitivity determined by mass recording
of photoreceptor potentials by electroretinographic (ERG) recording
(Arikawa et al., 1987), and
Ri() is the reflectance spectrum of paper
i (Fig. 2). The
wavelength range was set from 400 nm to 700 nm, for the halogen lamps used in
the present study emitted virtually no light with wavelengths shorter than 400
nm. The wavelength interval for the calculation (d) was 0.25 nm.
If butterflies discriminate two stimuli based on the relative responses of
a particular class of spectral photoreceptors, the butterflies should be
unable to discriminate a chromatic stimulus from an achromatic stimulus that
activates the same photoreceptor class at equivalent brightness levels. To
test this possibility, we prepared a set of four grey papers for each training
color (Table 1,
Fig. 2). We calculated the
quantum catch Q of the spectral photoreceptors for each paper based
on the assumption that the butterflies use B (460 nm), G (520 nm) and R (600
nm) receptors under the present illumination conditions
(Kinoshita and Arikawa, 2000;
Kinoshita et al., 1999). The
UV and violet receptors were excluded here because the illumination contained
virtually no UV light. The BB receptors were also excluded based on the
tentative assumption that the receptors are not involved in color vision
because of their extremely broad sensitivity
(Arikawa et al., 2003). The
quantum catch, Q, of each spectral photoreceptor was calculated by:
 | (2) |
 | (3) |
 | (4) |
|
(4) where SB,G,R() is the spectral sensitivity
of B, G or R receptors determined by intracellular recording
(Arikawa et al., 1987). The
numbers indicate the relative sensitivity at 460 nm (B), 540 nm (G) and 600 nm
(R) calculated from the spectral sensitivity function determined by ERG
recording (Arikawa et al.,
1987).
Training
Newly emerged butterflies were individually marked on a wing and each
butterfly was kept in a separate box. On the day of emergence (day 1), no food
was provided. On day 2, we started to train butterflies. We put a blue, green
or red paper disk on the black floor, covered the whole floor with a piece of
anti-reflection glass, and put some drops of 6% sucrose solution on the glass
at the location of the colored disk. We then released one butterfly in the
training area. If the released butterfly had not visited the disk by itself
after a few minutes, we captured it and uncoiled its proboscis using a needle
towards the drop of sucrose solution to let the butterfly take the reward.
After the manual feeding, virtually all of such butterflies became able to
visit the disk by themselves and to take sucrose. While they were taking
sucrose, we chased the butterflies from the feeding site by waving hands or by
blowing wind from outside of the cage. They then had to visit the disk
spontaneously and repeatedly to get the reward: this procedure promoted their
learning. The butterflies stopped feeding spontaneously after taking a certain
amount of sucrose: they had probably become satiated. Each butterfly was
trained to only one color.
We performed this training session once a day and repeated the training for 3 days. From post-emergence day 5, we presented the training colored disk vertically on a black acrylic board placed between the training and decision areas. The board was equipped with a plastic trough immediately below the training disk, such that the butterflies could take the sucrose reward from the trough while exposed to the colored disk in front of them. Here also we chased the butterflies away from the disk for several times until they stopped feeding spontaneously. We performed the training session once a day and repeated it for 4 more days. To avoid a possible association of the disk size with the reward, we changed the size of the disks (30 or 50 mm in diameter) after every second visit throughout the training period.
Pretest
On day 9, we performed pretests. The purpose of the pretests was to select
appropriate individuals for the tests. We presented a disk (diameter 30 or 50
mm) of the training color vertically at the end of one arm and a grey disk of
the same size at the end of the other arm
(Fig. 1); the distance of 50 cm
to the inspection point means that the disks of 30 mm and 50 mm diameter cover
a 3.4° and 5.7° visual angle, respectively. We then released a trained
butterfly into the training area that was separated by the board from the
decision area. We removed the board to let the butterfly fly into the decision
area, and further into one of the arms: the targets were invisible until the
board was removed. When the butterfly first crossed the imaginary line between
the decision area and one of the arms (Fig.
1), we recorded the behavior as a choice made by the butterfly.
Most butterflies that entered into an arm finally reached the disk and
extended the proboscis, indicating that they were actually performing foraging
behavior, although no reward was provided during the pretests. We then chased
the butterfly away from the arm back into the training area, and put the board
back. After a pause of 30 s, we again removed the board and allowed the
butterfly making another choice without reward. After every two visits, we
inserted a board with a disk of the training color and the feeding trough
between the training and decision areas, and fed the butterflies for 3 s: this
was to keep and to check their motivation to feed at the disk of the training
color. We repeated the pretest 6 times for one individual using the same size
of disks. The positions of two disks were changed alternately after every
second choice. We selected butterflies that made at least 5 correct choices in
the pretests.
Test
Tests were started from day 10 post-emergence. We used disks of 6, 10, 15,
30 and 50 mm diameter. We presented a disk of the training color in one arm
and a grey disk in the other arm. The sizes of the two simultaneously
presented disks were always the same. As in the pretests, the butterflies were
not rewarded at the end of the arms, but their motivation was checked and kept
by feeding them for 3 s after every second visit at the board inserted between
the training and decision areas.
We released a butterfly in the training area, and then removed the board separating the training area from the decision area. When a butterfly crossed the imaginary line between the decision area and the arm having the disk with the training color, we recorded the event as a correct choice. When a butterfly crossed the border of the arm presenting the grey disk or did not enter either of both arms after 2 min, we checked whether the individual was motivated for foraging. To this end, we inserted a board between the training and decision areas with a colored and a grey disk attached to it: motivated butterflies immediately visited the colored disk with their proboscises extended. Only when the motivation was confirmed, did we accept the previous negative responses as meaningful negative choices, and continued the tests with the same individual. One session of testing consisted of 6 consecutive choices as in the pretests. The sides of the two disks simultaneously presented were alternated after every second choice. We performed at least five test sessions using each of five sizes of disks for each individual.
Analysis
We scored the choice of the arm with the colored disk as 1, and the choice
of the arm with the grey disk as 0. We omitted the cases in which butterflies
did not enter either of the two arms after 2 min because this behavior does
not fit into the classification `correct' vs `incorrect' choice. We
analyzed the binomial data by using the generalized linear mixed effect model
with restricted maximum likelihood estimation (REML-GLMM) to assess which
parameters in this experiment affected the choice behavior. We treated disk
size, training color, type of grey, combination of color and grey presented
simultaneously as the fixed effects, and individual as the random effect when
the REML-GLMM analysis was performed. To determine the minimum visual angle
that was discriminated for each training color, we fitted curves for each by
using the generalized linear model (GLM). We used the analysis software JMP
version 5.0.1 (SAS Institute Inc. Cary, NC, USA).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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We presented disks of 6, 10, 15, 20, 30 and 50 mm in diameter at the distance of 50 cm in the Y-maze of Fig. 1. The butterflies made decisions not necessarily at the exact border between the decision area and the arm, but somewhere else in the decision chamber or even in the training area while they were flying during the tests. The longest possible distance where the targets are simultaneously visible from the butterflies in the apparatus is 106 cm (see Fig. 1). Actual decisions are therefore made between 50 cm and 106 cm.
When Giurfa et al. measured the minimum detectable visual angle in
honeybees (Giurfa et al.,
1996), they manipulated the distance range more strictly by making
a hole through which the bees entered the decision area, which produced a 10
cm distance range. They tested the bees with three different disk diameters
presented in arms of variable length to confirm that the bees' detection was
independent of either disk diameter or arm length. They eventually analyzed
the results obtained by using the combination of a longer arm and a larger
disk, which makes the effect of the distance range to the visual angle of the
target smaller. Unfortunately such manipulations of distance range are so far
not applicable to Papilio xuthus, because of the difference in
foraging habits of Papilio and honeybees. Papilio requires a
larger area to perform free-flying foraging behavior and in preliminary
experiments never entered a hole made in the separating wall between the
training and decision areas. It was also extremely difficult to let the
butterflies fly into arms longer than 60 cm.
The disks of 6, 10, 15, 20, 30 and 50 mm in diameter when viewed from a 50 cm distance correspond to visual angles of 0.7, 1.1, 1.7, 2.3, 3.4 and 5.7°, respectively. When viewed from a 106 cm distance, the visual angles are 0.3, 0.5, 0.8, 1.1, 1.6 and 2.7°, respectively. The former set of numbers represent the maximum values of visual angles if the disks were discriminated in the present condition. We therefore used these numbers for analyses as the maximum estimated visual angles.
Fig. 3 demonstrates the results of the tests. Each panel presents the data of individuals trained to blue (Fig. 3A), green (Fig. 3B), or red (Fig. 3C) color. Data were collected from 13 individuals for each color. The four lines in each panel correspond to the choice selection between the colored disk and four different grays (see Fig. 2 and Table 1).
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Parameters that affect the correct choice
Choice behavior may be affected by several independent parameters. We
performed the REML-GLMM analyses by incorporating five parameters, which were
disk size, color, grey intensity, color and grey presented simultaneously and
individually. Table 2 shows the
2 and the probability (P) values for each of these
parameters. Clearly, the correct choice ratio strongly depends on the disk
size (P<0.001) and also on the disk color (P=0.026).
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Minimum disk size for correct choice
Fig. 4 shows the
relationship between angular subtense and correct choices for the three
training colors determined by GLM analysis. The regression curves for blue and
red are rather similar but that for green is different, as expected.
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). Each
regression curve crosses the 60% criterion line at 1.18° for blue,
1.53° for green or 0.96° for red
(Table 3).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Land, 1997;
Land and Nilsson, 2002;
Snyder, 1979;
Snyder and Menzel, 1975). The
best sampling frequency that a compound eye can resolve,
vs, is that for which there is one receptor unit for each
half cycle of the grating. It is given by:
 | (5) |
where 
is the interommatidial angle. The interommatidial angle
in the frontal region of the eye of Papilio xuthus is about 1.0°
(Shibasaki et al., 2006), so
that vs is about 0.5/degree. This indicates that
Papilio can theoretically resolve two 1° dots separated by a
spatial interval of 1°. However, the effective cut-off frequency of the
optics, vopt, is affected by the ommatidial acceptance
angle, 
, which is expressed by:
 | (6) |
where d is the rhabdom diameter, f is the focal length of
the lens, D is the facet diameter and is the wavelength of
light. Assuming that d is 2 µm
(Arikawa et al., 1999),
f is 70 µm (Nilsson et al.,
1988) and D is 25 µm
(Arikawa and Stavenga, 1997)
for Papilio xuthus, should be about 1.95° for 500 nm
light. The value is close enough to the electrophysiologically determined
of a Papilio ommatidium, which is about 1.9°
(Shibasaki et al., 2006) see
also for Papilio aegeus (Horridge
et al., 1983). Note that the is about as twice as
much as the value of (1.0°). This relationship,
=2 , is derived by assuming vs=
vopt (Land,
1997). Therefore we tentatively conclude that the spatial
resolution of Papilio is around 1.0°.
Discrimination and eye structure
In the present work we found that the minimum angular subtense of a colored
target detectable for a foraging Papilio is at 1.18° for blue,
1.53° for green or 0.96° for red, which are angles close to the
spatial resolution predicted from the interommatidial angle, 1.0°. As
described in the Results, the numbers are a maximum estimate: butterflies may
have discriminated the targets from a point further away from the point used
for the calculation above. Assuming that they discriminated the targets at 77
cm, the mid point of 50 and 106 cm, the angles are 0.76° for blue,
1.03° for green or 0.68° for red. Therefore the butterflies appeared
to be able to see the color of targets whose size is close to the spatial
resolution limit, which never happens in humans. This ability may compensate
their poor spatial resolution, which is about 100 times coarser than our own
(Land, 1997).
The ability of discriminating colors of targets of visual angle around 1° should be attributed at least in part to the polychromatic organization of the rhabdom. The eye of Papilio consists of three types of ommatidia, each containing 2-4 classes of spectral photoreceptors contributing to the rhabdom. Multiple spectral detectors with overlapping receptive fields are required for wavelength discrimination in general, and the polychromatic rhabdom of Papilio fulfils the requirement.
Of course the present results do not provide any direct evidence that the color discrimination is in fact possible with only a single ommatidium, because we did not precisely stimulate single ommatidia. Rather, the butterflies were flying when making decisions, so the targets must have been stimulating multiple ommatidia successively. The Papilio eye is furnished with six classes of spectral receptors embedded in the ommatidia in three distinct combinations, i.e. type I, UV, blue, green, red; type II, violet, green, broad-band; type III, blue, green. Note that type I is the only type containing the three classes of spectral receptors considered here. This does not necessarily mean that type I ommatidia are exclusively responsible for the task of color discrimination. Spatial and temporal scanning could have important roles, but the underlying mechanisms are fully unknown.
The limit angle of color discrimination is significantly larger for the
green target than for blue and red targets
(Table 3). The reflectance
spectrum of the green paper (Fig.
2B) matches with the main sensitivity band of the green receptors
of Papilio (Arikawa,
2003). It is therefore likely that the green targets have
specifically stimulated the green receptors. In the Papilio compound
eye, all of the six classes of spectral receptors are basically distributed
with some spacing due to the random array of the three types of ommatidia
(Arikawa and Stavenga, 1997).
The array of green receptors is an exception, because the R3 and R4 of all
ommatidia are green receptors. Assuming that the complete hexagonal lattice of
the R3-4 green receptors is part of the color discrimination system, green
colors should be discriminated best. This, however, is not the case and
therefore the R3-4 green receptor system may not be directly involved in color
discrimination. In fact anatomical studies demonstrated that photoreceptors
other than R3 and R4 make elaborate mutual connections in the lamina, which is
presumably crucial for color vision
(Takemura and Arikawa, 2006;
Takemura et al., 2005). The
R3-4 system is probably used for other aspects of vision, such as motion
detection. We have to note that there is another group of green receptors, the
R5-8 of type III ommatidia, that is used for color vision
(Arikawa, 2003;
Takemura and Arikawa, 2006).
However, we have so far no direct behavioral evidence to identify all spectral
receptor classes that are involved in the color vision of
Papilio.
Comparative aspects
Free-flying honeybee foragers are able to detect colored targets with a
visual angle larger than 5°, which corresponded to a visual field covered
by seven ommatidia (Giurfa et al.,
1996). Why is the minimal target size for color detection so large
in honeybees? This cannot be attributed to the structure of the honeybee eye,
because the interommatidial angle is also 
1°
(Land, 1997), and a rhabdom is
also polychromatic with two or three classes of spectral photoreceptors
(Spaethe and Briscoe, 2005;
Velarde et al., 2005;
Wakakuwa et al., 2005). A
possible cause is the difference in the way of flight: honeybee flight is
quite stable, with a small range of zigzag movement. Honeybees sometimes even
hover in front of flowers, while butterflies fly with larger zigzag movements,
which will result in more ommatidia to contribute for target scanning.
In fact, the best performance of target detection of honeybees at 5° is
possible only when the background grey and the target color stimulated the
green receptors differently, i.e. the pair of grey and color created green
contrast. Otherwise the target must be larger than 15° to be
discriminated. A 15° target is extremely large: a 131 mm target viewed
from 50 cm, which corresponds to 55 ommatidia
(Giurfa et al., 1996). Here we
presented the targets on a black background to maximize the image contrast.
The grey disks we used were designed to have the same subjective brightness of
the colored target or to stimulate a specific type of spectral photoreceptor
(blue, green or red receptors) as the colored targets do
(Fig. 2,
Table 1), but owing to the
difference in the way of presentation, we cannot simply compare our results on
Papilio with those of honeybees. Under the present conditions, the
discrimination behavior of butterflies was not affected by the densities of
grey (Table 2), indicating that
the butterflies use multiple classes of spectral photoreceptors to analyze the
chromatic information contained in the targets, rather than depending on
contrast of a specific class of spectral photoreceptors.
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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. (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., Inokuma, K. and Eguchi, E. (1987). Pentachromatic visual system in a butterfly. Naturwissenschaften 74,297 -298.[CrossRef]
Arikawa, K., Scholten, D. G. W., Kinoshita, M. and Stavenga, D. G. (1999). Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool. Sci. 16,17 -24.[Medline]
Arikawa, K., Mizuno, S., Kinoshita, M. and Stavenga, D. G.
(2003). Coexpression of two visual pigments in a photoreceptor
causes an abnormally broad spectral sensitivity in the eye of a butterfly,
Papilio xuthus. J. Neurosci.
23,4527
-4532.
Giurfa, M., Vorobyev, M., Kevan, P. and Menzel, R. (1996). Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J. Comp. Physiol. A 178,699 -709.
Giurfa, M., Vorobyev, M., Brandt, R., Posner, B. and Menzel, R. (1997). Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. J. Comp. Physiol. A 180,235 -243.[CrossRef]
Gribakin, F. G. (1975). Functional morphology of the compound eye of the bee. In The Compound Eye and Vision of Insects (ed. G. A. Horridge), pp.154 -176. Oxford: Clarendon Press.
Horridge, G. A., Marcelja, L., Jahnke, R. and Matic, T. (1983). Single electrode studies on the retina of the butterfly Papilio. J. Comp. Physiol. A 150,271 -294.[CrossRef]
Kinoshita, M. and Arikawa, K. (2000). Colour constancy of the swallowtail butterfly, Papilio xuthus. J. Exp. Biol. 203,3521 -3530.[Abstract]
Kinoshita, M., Shimada, N. and Arikawa, K. (1999). Colour vision of the foraging swallowtail butterfly Papilio xuthus. J. Exp. Biol. 202,95 -102.[Abstract]
Land, M. F. (1981). Optics and vision in invertebrates. In Handbook of Sensory Physiology. Vol.VII/6B (ed. H. Autrum), pp.471 -592. Berlin, Heidelberg, New York: Springer-Verlag.
Land, M. F. (1997). The resolution of insect compound eyes. Israel J. Plant Sci. 45, 79-91.
Land, M. F. and Nilsson, D.-E. (2002). Animal Eyes. Oxford: Oxford University Press.
Menzel, R. (1979). Spectral sensitivity and color vision in invertebrates. In Handbook of Sensory Physiology. Vol. VII/6A (ed. H. Autrum), pp. 503-580. Berlin, Heidelberg, New York: 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]
Shibasaki, H., Kinoshita, M. and Arikawa, K. (2006). Interommatidial angle, photoreceptor acceptance angle, and spatial resolution of the compound eye of the butterfly, Papilio xuthus. Zool. Sci., in press.
Snyder, A. W. (1979). Physics of vision in compound eyes. In Handbook of Sensory Physiology. Vol.VII/6A (ed. H. Autrum), pp.225 -313. Berlin, Heidelberg, New York: Springer-Verlag.
Snyder, A. W. and Menzel, R. (1975). Photoreceptor Optics. Berlin, Heidelberg, New York: Springer Verlag.
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.
Spaethe, J. and Chittka, L. (2003).
Interindividual variation of eye optics and single object resolution in
bumblebees. J. Exp. Biol.
206,3447
-3453.
Spaethe, J., Tautz, J. and Chittka, L. (2001).
Visual constraints in foraging bumblebees: flower size and color affect search
time and flight behavior. Proc. Natl. Acad. Sci. USA
98,3898
-3903.
Takemura, S. and Arikawa, K. (2006). Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus. J. Comp. Neurol. 494,663 -672.[CrossRef][Medline]
Takemura, S., Kinoshita, M. and Arikawa, K. (2005). Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus. J. Comp. Neurol. 483,341 -350.[CrossRef][Medline]
Velarde, R. A., Sauer, C. D., Walden, K. K. O., Fahrbach, S. E. and Robertson, H. M. (2005). Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochem. Mol. Biol. 35,1367 -1377.[CrossRef][Medline]
Wakakuwa, M., Kurasawa, M., Giurfa, M. and Arikawa, K. (2005). Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92,464 -467.[CrossRef][Medline]
Wandell, B. A. (1995). Foundations of Vision. Sunderland: Sinauer.
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