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1084 D. G. Stavenga 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 Recent anatomical and molecular biological work on the moth Manduca sexta (R. H. White, unpublished results) describes a heterogeneous organization of the spectral receptor types in the ommatidial lattice strikingly similar to that of diurnal butterflies,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(Arikawa and Stavenga, 1997; Kitamoto et al., 2000) and the nymphalid Vanessa cardui (A. D. Briscoe and A. S. Szeto, unpublished results).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. I thank Drs P. Brakefield and M. Joron (University of Leiden) for stimulating discussions and supplying butterflies. H. L. Leertouwer provided invaluable technical support. Drs K. Arikawa, G. D. Bernard, A. D. Briscoe, J. Oberwinkler and R. H. White gave valuable comments on an early version of the manuscript. References Arikawa, K., Inokuma, K. and Eguchi, E. (1987). Pentachromatic visual system in a butterfly. Naturwissenschaften 74, 297–298. Arikawa, K., Mizuno, S., Scholten, D. G. W., Kinoshita, M., Seki, T., Kitamoto, J. and Stavenga, D. G. (1999a). 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. Arikawa, K., Scholten, D. G. W., Kinoshita, M. and Stavenga, D. G. (1999b). Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool. Sci. 16, 17–24. Arikawa, K. and Stavenga, D. G. (1997). Random array of colour filters in the eyes of butterflies. J. Exp. Biol. 200, 2501–2506. Arikawa, K. and Uchiyama, H. (1996). Red receptors dominate the proximal tier of the retina in the butterfly Papilio xuthus. J. Comp. Physiol. A 178, 55–61. Bernard, G. D. (1979). Red-absorbing visual pigment of butterflies. Science 203, 1125–1127. Bernard, G. D. (1983). Dark-processes following photoconversion of butterfly rhodopsins. Biophys. Struct. Mech. 9, 227–286. Bernard, G. D., Douglas, J. and Goldsmith, T. H. (1988). Far-red sensitive visual pigment of a metalmark butterfly. Invest. Ophthalmol. Suppl. 29, 350. Bernard, G. D. and Miller, W. H. (1970). What does antenna engineering have to do with insect eyes? IEEE Student J. 8, 2–8. Bernard, G. D. and Remington, C. L. (1991). Color vision in Lycaena butterflies: Spectral tuning of receptor arrays in relation to behavioral ecology. Proc. Natl. Acad. Sci. USA 88, 2783–2787. Briscoe, A. D. (1998). Molecular diversity of visual pigments in the butterfly Papilio glaucus. Naturwissenschaften 85, 33–35. Chittka, L. (1996). Optimal sets of receptors and color opponent systems for coding of natural objects in insect vision. J. Theor. Biol. 181, 179–196. Douglas, R. H. and Marshall, N. J. (1999). A review of vertebrate and invertebrate ocular filters. In Adaptive Mechanisms in the Ecology of Vision (ed. S. N. Archer, M. B. A. Djamgoz, E. R. Loew and S. Vallerga), pp. 95–162. Dordrecht, Boston, London: Kluwer. Franceschini, N. (1975). Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In Photoreceptor Optics (ed. A. W. Snyder and R. Menzel), pp. 98–125. Berlin, Heidelberg, New York: Springer. Franceschini, N. and Kirschfeld, K. (1971). Les phénomènes de pseudopupille dans l’oeil composé de Drosophila. Kybernetik 9, 159–182. Franceschini, N., Kirschfeld, K. and Minke, B. (1981). Fluorescence of photoreceptor cells observed in vivo. Science 213, 1264–1267. Fukushi, T. (1989). Learning and discrimination of coloured papers in the walking blowfly, Lucilia cuprina. J. Comp. Physiol. A 166, 57–64. Govardovskii, V. I. (1983). On the role of oil drops in colour vision. Vision Res. 23, 1739–1740. Hardie, R. C. (1986). The photoreceptor array of the dipteran retina. Trends Neurosci. 9, 419–423. Kelber, A. (1999). Ovipositing butterflies use a red receptor to see green. J. Exp. Biol. 202, 2619–2630. Kelber, A. and Pfaff, M. (1999). True colour vision in the orchard butterfly, Papilio aegeus. Naturwissenschaften 86, 221–224. Kinoshita, M. and Arikawa, K. (2000). Colour constancy in the swallowtail butterfly Papilio xuthus. J. Exp. Biol. 203, 3521–3530. Kinoshita, M., Sato, M. and Arikawa, K. (1997). Spectral receptors of nymphalid butterflies. Naturwissenschaften 84, 199–201. Kinoshita, M., Shimada, N. and Arikawa, K. (1999). Colour vision of the foraging yellow swallowtail butterfly Papilio xuthus. J. Exp. Biol. 202, 95–102. Kitamoto, J., Ozaki, K. and Arikawa, K. (2000). Ultraviolet receptors and violet receptors express identical mRNA encoding an ultraviolet-absorbing opsin: identification and histological localization of two mRNAs encoding short-wavelength-absorbing opsins in the retina of the butterfly Papilio xuthus. J. Exp. Biol. 203, 2887–2894. Kitamoto, J., Sakamoto, K., Ozaki, K., Mishina, Y. and Arikawa, K. (1998). Identification of visual pigment opsins reveals the spectral receptor array in the retina of the butterfly Papilio xuthus. J. Exp. Biol. 201, 1255–1261. Kolb, G. (1985). Ultrastructure and adaptation in the retina of Aglais urticae (Lepidoptera). Zoomorphology 105, 90–98. Kolb, G. and Scherer, C. (1982). Experiments on wavelength specific behavior of Pieris brassicae L. during drumming and egg-laying. J. Comp. Physiol. A 149, 325–332. Land, M. F. (1984). The resolving power of diurnal superposition eyes measured with an ophthalmoscope. J. Comp. Physiol. A 154, 515–533. Land, M. F. and Osorio, D. C. (1990). Waveguide modes and pupil action in the eyes of butterflies. Proc. R. Soc. Lond. B 241, 93–100. Marshall, N. J., Land, M. F., King, C. A. and Cronin, T. W. (1991). The compound eye of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Phil. Trans. R. Soc. Lond. B 334, 57–84. Meinecke, C. C. and Langer, H. (1984). Localization of visual pigments within the rhabdoms of the compound eye of Spodoptera exempta (Insecta, Noctuidae). Cell Tissue Res. 238, 359–368. Menzel, R. and Backhaus, W. G. K. (1989). Color vision in honey bees: phenomena and physiological mechanisms. In Facets of Vision (ed. D. G.PDF Image | Reflections on colourful ommatidia of butterfly eyes
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