Proceedings of 2nd International Symposium for Color Science and Art 2020

Butterfly Color Vision - Another View of Our World
Kentaro Arikawa
Laboratory of Neuroethology, SOKENDAI-Graduate University for Advanced Studies, Hayama, 240-0193, Japan
rhabdom along the ommatidial longitudinal axis. The rhabdom is surrounded by red or yellow pigment, which act asspectral filters for the photoreceptors. A subset of red-pigmented ommatidia has UV-absorbing fluorescence pigment at the top of the rhabdom. Distribution of the red, yellow and fluorescing ommatidia appears random: thePapilio eye is a random mesh of 3 types of ommatidia.
Spectral properties of rhodopsin and the filter pigments
determine photoreceptors’ spectral sensitivity, which canbe determined by measuring electrical responses of them.
We thus identified UV, violet (V), B, G, R and broad-band(BB) receptors (Fig. 1B). The receptors are embedded in
3 types of ommatidia in 3 fixed combinations [1]. The spectral heterogeneity of butterfly eyes is a particularly pronounced case among insects [2].

ABSTRACT
Butterflies often feed on nectar of colorful flowers. How
do they find flowers? Do they discriminate flowers bycolor? We found a swallowtail butterfly uses sophisticatedcolor vision when searching for food. Surprisingly, color vision system appears to be very much different among animals, even among butterflies. I will overview the current
understanding of insect color vision from the evolutionary
point of view: each animal has its own visual world. Studyof insect vision should also contribute designing novel “visual” devices and to manage insect pests for the crop without using chemical insecticides.
1. INTRODUCTION
Color vision is the ability of discriminating visual stimuli
based on their spectral (wavelength) contents irrespectiveof the intensity. We have a trichromatic system based on
the blue (B), green (G) and red (R) light sensitive sensors(photoreceptor cells) in the eye (Fig. 1A). Color vision appears to be rather common among animals, some of which
in fact exhibit surprisingly good performance in discriminating colors. For example, a swallowtail butterfly Papilio
xuthus can detect only 1 nm difference in wavelength,
which rivals our performance. But Papilio’s performance iseven better because their visible light expands deeply into
the ultraviolet range that we cannot see. We now know thatPapilio has a tetrachromatic system based on the UV, B,
G and R sensitive photoreceptor cells in the compoundeye. We have also demonstrated that Papilio exhibits color
constancy and simultaneous color as well as brightness
contrast. Here I first summarize our current understanding
about the color vision mechanism of Papilio, and then willcompare color vision among animals.

3. COLOR VISION OF PAPILIO
3.1 Color vision with color constancy
To demonstrate color vision in Papilio, we trained naïvePapilio to take nectar on a colored disk, simulating theirflower-visiting behavior in the field (Fig. 1D). Papilio readily
becomes able to visit the colored disk even if it is presented with disks of other colors. Papilio really used chromatic cue of the disk, not the brightness, because they
could select the colored disk among the disks of different
shades of greys.
Perceived colors of objects basically remain constant irrespective of spectral contents of the illumination. This
property is known as color constancy, which is important
for animals that assess object quality by color. We confirmed that Papilio has color constancy by testing them under differently colored illuminations [3].

2. COMPOUND EYES
2.1 Photoreceptor spectral sensitivities
Compound eyes are composed of multiple units calledommatidia. The ommatidial array is visible from outside as
a number of hexagonally-packed facets. The diameter ofa facet is about 25 µm in most insects, which makes thenumber of ommatidia roughly proportional to the size ofcompound eyes. An ommatidium is a long structure, which
are tightly packed to each other making the compound eye
a dome-shaped structure. A compound eye of Papilio
xuthus is made up with about 12,000 ommatidia.
An ommatidium of Papilio contains nine photoreceptor
cells. Each photoreceptor bears numerous microvilli containing photosensitive protein, rhodopsin, forming a single

Fig. 1: Photoreceptor spectral sensitivities of humans (A), theJapanese yellow swallowtail, Papilio xuthus (B), and honeybee
Apis mellifera (C). D) Color vision test in Papilio xuthus.

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Proceedings of 2nd International Symposium for Color Science and Art 2020
3.2 Wavelength discrimination
Dimension of color vision (tri- or tetra-chromacy, etc)
can be studied by measuring wavelength discrimination
ability. We can discriminate about 1 nm difference (≑ 1nm) in two wavelength regions, which are around 500 nm
and 600 nm (see Fig. 2B). These regions respectively correspond to where the sensitivities of B and G receptors,
and G and R receptors overlap. Existence of two highly
sensitive wavelength regions is because the system is trichromatic.
We measured wavelength discrimination in Papilio using its feeding response. We trained butterflies to extend
their coiled mouth towards light of certain wavelength.
When shown the training light with another light of different
wavelength at the same intensity, the butterfly extends its
mouth towards the training light if two lights are discriminable. We thus found that Papilio can detect 1-2 nm difference at around 430, 480 and 560 nm, indicating that theircolor vision system is tetrachromatic. Model calculation
well reproduced the behavioral results when we assumed
the UV, B, G and R receptors contribute the discrimination(Fig. 2A).
Figure 2B shows the wavelength discrimination of someanimals including humans. Honeybees and humans aretrichromatic, while goldfish and Papilio are tetrachromatic.
Papilio’s performance is indeed the best among them [4].

Fig. 2: (A) Wavelength discrimination () function of Papilio.
Troughs (open arrowheads) indicate high-sensitive regions.
Behavioral data (dotted line) are well explained by the model with
inputs from UV, B, G and R receptors (upper), but not by all six
receptors (lower), where significant deviation is observed in the UV
region (red arrowhead). (B) Comparison of wavelength
discrimination of animals.

color vision. If this is also the case of Graphium, other 11
receptors may be useful for detecting specific stimuli, forexample, fast-moving objects against the sky, or particular
light wavelengths reflected from potential mates or enemies.
4.2 Perspectives
We of course cannot see the world as butterflies do, because our eyes and brains are designed differently. It ishowever still exciting to try to understand how the world ofbutterflies looks like by combining evidence from various
kinds of experiments. We are currently studying hard tounderstand how the wavelength information is processedin their tiny brains to produce “colors” as their own experience. We are also interested in how color vision systems
have evolved over time by comparing the eyes and brainsof many different insects.
In this process, we may even discover principles for designing new artificial “visual” systems. It would be fantastic
if we could program drones to use their “eyes” to control
themselves as skillfully as insects do. Another possible application of insect vision research is to control insect pests.
Excess use of chemical insecticides damages environment. Perhaps we can safely keep pest insects away fromcrops by using light instead of chemicals. For this, we firsthave to understand how insect visual systems work.

4. COMPARATIVE ASPECTS
4.1 Photoreceptor diversity
As shown in Figs 1C and 2B, color vision of honeybees
and butterflies are different. Even among butterflies, colorvision properties appear to be different. Because behavioral experiments are not easy to perform, this has notbeen convincingly demonstrated at the behavioral level.
However, we see a clue of the variability at the photoreceptor level.
Some butterflies have only 3 receptor classes (UV, Band G) in their eyes as honeybees do, suggesting their trichromacy. Some have 6 or more. The cabbage white,Pieris rapae, has 6 as in Papilio, but the sensitivity profiles
are different: they are UV, V, B, G, R and dark red. In addition, the V receptors are found only in females. They arereplaced by double-peaked B (dB) receptors in males.
Sexual dimorphism is even more pronounced in the Eastern pale clouded yellow, Colias erate, where males have
one class of R receptors, while females have 3 classes ofthem. Multiple R receptors would make females capableof discriminating subtle differences in greenish, yellowish,
and reddish colors. This is probably beneficial in assessing
quality of leaves on which to lay eggs [5].
In terms of the number of receptor classes in butterflies,
the Common bluebottle, Graphium sarpedon, has the record at this stage, which is 15 [6]. How does Graphium use
these 15 classes of receptors? It seems unlikely that theyare “pentadeca-” chromatic. Papilio uses 4 out of 6 for

5. REFERENCES[1] Arikawa, J Comp Physiol A, 189, 791-800 (2003)[2] Perry, Kinoshita, Saldi, Huo, Arikawa, Desplan, Nature,535, 280–4 (2016)[3] Kinoshita, Arikawa, J Comp Physiol A, 200, 513-26(2014)[4] Koshitaka, Kinoshita, Vorobyev, Arikawa, Proc Biol Sci,275, 947-54 (2008)[5] Marshall, Arikawa, Curr Biol, 24, R1150-4 (2014)[6] Chen, Awata, Matsushita, Yang, Arikawa, Front Ecol
Evol, 4, 1-12 (2016)14