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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

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Absence of eye shine and tapetum in the heterogeneous eye of Anthocharis butterflies (Pieridae)

Shin-ya Takemura^1,*, Doekele G. Stavenga² and Kentaro Arikawa^3,

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

View larger version (215K): [in this window] [in a new window]   Fig. 1. Transmission electron microscopy of an ommatidium of the eye of the yellow tip Anthocharis scolymus. (A) Transverse section of the proximal part of the ommatidium, where only the proximal photoreceptors, R5–R8, contribute rhabdomeres to the fused rhabdom (Rh) (and not the distal photoreceptors, R1–R4, and the basal receptor, R9). Tracheoles (T) with their characteristic rippled walls are well recognizable. (B) Transverse section of the basal part of the ommatidium, where the R9 cell body fully occupies the space proximal to the rhabdom. (C) Longitudinal section of an ommatidium near the basal membrane (BM) that limits the retina at the proximal side. The trachea is clearly not elaborated into a tracheolar tapetum apposed to the fused rhabdom, as is the case in other pierid butterflies (cf. Ribi, 1980; Qiu et al., 2002). The levels of the sections of A and B are indicated by the horizontal dotted lines and the arrowheads. Bar, 5 µm.

View larger version (85K): [in this window] [in a new window]   Fig. 2. Light microscopical unstained sections of the same set of ommatidia at three different levels, 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.

View larger version (126K): [in this window] [in a new window]   Fig. 3. Ommatidial fluorescence (A) and unstained section through the transitional zone (B) of the same region of the eye. Clearly, the fluorescing ommatidia correspond to the trapezoidal type ommatidia. The circles in B indicate the fluorescing ommatidia in the white parallelogram in A. Bar, 10 µm.

View larger version (130K): [in this window] [in a new window]   Fig. 4. Transmission electron microscopy of the two ommatidial types, round and trapezoidal, of the yellow tip. (A–E) Transverse sections of an ommatidium with an approximately circular-cylindrical, round rhabdom. (F–J) Transverse sections of an ommatidium having a trapezoidal rhabdom at the middle level of the retina. Bar, 1 µm. (K) Summary diagram of the two ommatidial types. The total length of the ommatidium, including the dioptrical apparatus, is about 420 µm. In the round type, the photoreceptors R1–R4 contribute their rhabdomeres over about the distal half of the ommatidium, and the R5–R8 do the same over most of the proximal half. The R9 photoreceptor adds some microvilli at the base of the rhabdom. Clusters of pigment granules exist in the cell bodies of the photoreceptors R5–R8 in most of the distal half of the round type ommatidium, over a distance of about 100–300 µm from the corneal surface, but no pigment clusters exist in the proximal half of the ommatidium. In the trapezoidal-type, the rhabdomeres of R1–R4 form the distal two thirds of the rhabdom, those of R5–R8 form most of the proximal one-third, and the R9 photoreceptor again adds some microvilli at the base of the rhabdom. Clusters of pigment granules exist in the cell bodies of the photoreceptors R5–R8 in virtually only the proximal one-third of the trapezoidal-type ommatidium. The levels of the transverse sections A–J are indicated by arrowheads at the left side of the diagram. Four tracheal extensions (T) invade the retina. BM, basement membrane; D, dorsal, V, ventral; P, posterior, A, anterior.