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Visual guided behavior of the swallowtail butterfly, Papilio xuthus


Michiyo Kinoshita(The Graduate University for Advanced Studies)


Flower-Foraging (for the underlined portion, see glossary)

Japanese yellow swallowtail butterfly (Papilio xuthus; hereafter Papilio) is one of a common species visiting flowers between the woods and open fields from spring to autumn in Japan. Papilio are known to be potential pollinators for reddish flowers such as azaleas, lilies, and cluster amaryllis. Pollinators like bees have innate preference in each sensory modality and can associate visual and olfactory information of flowers with nectar of flowers. Among of pollinators, foraging Papilio seems to rely more on vision than olfaction. When a naïve summer form female Paplilio butterflies are released in a small cage where presenting 4 color disks (blue, green, yellow and red), they first landed on either the red or the yellow disk with its extended proboscis, which are innate color preference for Papilio.
Foraging Papilio can discriminate different modalities of light information; wavelength, intensity and polarization. In especially Papilio has sophisticated color vision. After a native Papilio was fed on a yellow-colored disk for a few days, it became discriminate the yellow disk among the 4 colored disks, blue, green, yellow and red (Fig. 1, left). Series of behavioral experiments demonstrated that Papilio has color vision (Fig. 1, right, Kinoshita et al., 1999), brightness vision, and polarization vision. Papilio color vision includes “color constancy” (Fig. 2; Kinoshita, Arikawa, 2000) and “color contrast” (Fig. 3; Kinoshita et al., 2008a), which are important phenomena in human color vision. In addition, Papilio can learn and distinguish monochromatic light at specific wavelength between ultraviolet and red wavelength region. Action spectrum of Papilio foraging behavior shows that light at blue wavelength region appears bright for Papilio (Koshitaka et al., 2004). In experiment of wavelength discrimination ability, Papilio could discriminate only one 1 nm difference at 3 wavelength regions; 430, 480, 560nm (Koshitaka et al., 2008).
Papilio performs very well in color learning and discrimination, while its brightness vision seems to be rather poor. Papilio innately prefers brighter target and can learn and discriminate relative difference of brightness. Learning absolute intensity is difficult (Fig. 4, left, center; Kinoshita et al., 2012). Its brightness vision includes brightness contrast (Fig. 4c; Kinoshita et al., 2012). Papilio innately prefers polarized light, whose e-vector orients perpendicular to the grounds (refer vertical polarization). This is interpreted because vertical polarization appears brighter than horizontal polarization, whose e-vector orients parallel to the ground (Kinoshita et al., 2011). Foraging behavior can be divided into the following 4 steps: searching at a distance, approaching, landing, and getting nectar. Color must be a cue for approaching, while brightness contrast between a target and background is crucial for landing. For landing, contrast between the target and the background itself is important, but its polarity is not essential (Koshitaka et al., 2011).

Glossary

Color vision: The ability is to distinguish an object based on chromatic content of reflected light from the object with regardless of its brightness. To demonstrate color vision in scientific terms, it is essential to show that an animal can learn a colored object and discriminate the object from a gray object with the same brightness as the colored object.

Color constancy: The chromatic contents of reflected light from the object changes depending on the irradiation spectrum of illumination. Even though the spectrum of illumination changes, the color of the object appears approximately same to our eyes, which is so-called color constancy. This phenomenon is important for animals to identify objects depending on their color. Therefore, color constancy is one of the most important phenomena in color vision.

Color contrast (color induction): In human vision, color appearance of an object changes depending on color of background. This is because color of background induces a certain color on the surface of the object. This induced color is so-called complementary color. Blue and yellow and red and green are known in human color vision. A set of complementary color, blue and yellow, has been observed in Papilio color vision.

Brightness contrast: Appearance of the brightness of an object is inverted by the brightness of the background. If the background is dark, the object appears brighter, and if the background is bright, the object appears darker. This phenomenon allows the object to be clearly observed against the background.



Fig. 1: Color vision experiment
. A naïve Papilio fed sugar water on a yellow disk can discriminate yellow disk from other colored disks (left) and also from different shades of gray (right).



Fig. 2: Color constancy experiment . A Papilio trained to visit a yellow disk under white light could discriminate the yellow patch among a mosaic of colored patch “color Mondrian” under the same white light (left). Even though red illumination changes the spectrum of reflected light from the yellow patch, but Papilio still visits the yellow area (right).




Fig. 3: Color contrast (chromatic induction) experiment
. A Papilio trained to a green disk among several similar colors on a black background, visits the correct green one on a gray background (left). When the same colored disks are presented on a yellow background, it selected yellow–green disk (right). This suggests that yellow–green disk appears trained color “green” because of induced color (blue) by yellow background.



Fig. 4: Brightness contrast experiment.
A Papilio is trained to search for nectar on the darker red (left). When two orange disks of different intensities are presented, the darker disk was selected (center). Subsequently, when two orange disk of the same intensity is put on different shades of gray backgrounds, the disk on the light gray background is selected (right). This means that the disk on brighter gray appears darker than the one on the darker background, suggesting brightness contrast is involved in Papilio vision.


References

Kinoshita M, Shimada N, Arikawa K (1999) Color vision of the foraging swallowtail butterfly Papilio xuthus. J Exp Biol 202: 95-102.

Kinoshita M, Arikawa K (2000) Colour constancy in the swallowtail butterfly Papilio xuthus. J Exp Biol 203: 3521-3530.

Koshitaka H, Kinoshita M, Arikawa K (2004) Action spectrum of foraging behavior of the Japanese yellow swallowtail butterfly, Papilio xuthus. Acta Biologica Hungarica 55: 71-79.

Kinoshita M, Takahashi Y, Arikawa K (2008) Simultaneous color contrast in the foraging swallowtail butterfly, Papilio xuthus. J Expl Biol 211: 3504-3511.

Koshitaka H, Kinoshita M, Arikawa K (2008) Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc Biol Sci 275: 947-954.

Kinoshita M, Takahashi Y, Arikawa K (2012) Simultaneous brightness contrast of foraging Papilio butterflies. Proc Biol Sci 279: 1911-1918.

Kinoshita M, Yamazato K, Arikawa K (2011) Polarization-based discrimination in the foraging butterfly, Papilio xuthus. Philos Trans R Soc Lond Biol Sci 366: 688-696.

Koshitaka H, Arikawa K, Kinoshita M (2011) Intensity contrast as a crucial cue for butterfly landing. J Comp Physiol A 197: 1105-1112.

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