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Reflections on colourful ommatidia of butterfly eyes

Doekele G. Stavenga

Department of Neurobiophysics, University of Groningen, NL-9747 AG Groningen, the Netherlands

View larger version (15K): [in a new window]   Fig. 1. The optical apparatus used to photograph the eye shine of butterfly eyes. The objective lens L1 has a large aperture. A light source is focused by lens L2 in its back focal plane, where the field diaphragm D1 is positioned. D1 is in the focal plane of lens L3, which is confocal with L1 because of a half-mirror placed at 45° with respect to the optical axes of L1 and L3. A more-or-less parallel beam, depending on the size of D1, enters L1 and is focused on the deep pseudopupil (DPP) in the centre of the butterfly's eye. The telescope lens pair L1 and L4 images the DPP in the back focal plane of L4, where diaphragm D2 is positioned. The image of the corneal eye shine, projected by lens L5, confocal with L4, is photographed by a photomicroscope. The dotted lines are the back-focal planes of L1 and L5. Inset: incident light entering a butterfly ommatidium is focused by the facet lens and crystalline cone (fc) into the rhabdom (rh) and then propagates to the tapetal reflector (tr), where it is mirrored back into the rhabdom and out of the eye again, unless it is absorbed by visual pigments in the rhabdom or by screening pigments in the medium surrounding the rhabdom. The rhabdom organization of a pierid butterfly is indicated schematically: the distal part of the rhabdom consists of the rhabdomeres of photoreceptors R1-R4, the proximal part consists of the rhabdomeres of photoreceptors R5-R8 and the most basal part consists only of rhabdomere R9, which is indicated by an asterisk (see Qiu et al., 2002). The rhabdom is surrounded by photoreceptor screening pigment that absorbs light from the propagating light wave.

View larger version (86K): [in a new window]   Fig. 2. The eye shine patterns in the eyes of the satyrine Bicyclus anynana (A), the heliconian Heliconius melpomene (B) and the small white Pieris rapae (B) observed with the large-aperture optical apparatus depicted in Fig. 1. The ommatidia in the three species reflect either predominantly yellow or predominantly red light. The red reflection is absent from a large dorsal area of the eye of Bicyclus anynana and from a small dorsal area of the eye of Pieris rapae; in Heliconius melpomene, both reflection types co-exist throughout the eye. The central `hot spot' is due to reflection on the lens surfaces of the microscope objective. The dark areas in A and B are caused by specks of dust; the dark facets in C have a strong deep-red reflection. The scale bars, 300 µm in A-C, refer to the central part of the figures only because the optical apparatus suffers from slight barrel-type distortion.

View larger version (69K): [in a new window]   Fig. 3. The eye of the small copper Lycaena phlaeas photographed from four dorsal to ventral directions, differing by 30° from each other, with broad-band, white light (halogen lamp) and monochromatic red (670nm) and green (550nm) light. The effective aperture of the objective is approximately 60°. The frontal and ventral parts of the eye contain a mixture of red- and yellow-green-reflecting ommatidia, but dorsally the reflection colours are a mixture of blue and green; red reflection is absent from the dorsal region. The central `hot spot' is due to reflection on the lens surfaces of the microscope objective. 0° is approximately horizontal.

View larger version (19K): [in a new window]   Fig. 4. Reflectance spectra measured from single-facet lenses in the eye of the satyrine Bicyclus anynana. The spectra fall into two classes, yellow and red. The reflectance spectrum of the yellow class is broad, extends into the ultraviolet, is very minor above 600nm and peaks at around 580nm; the reflectance spectrum of the red class is a restricted band around 650nm and is negligible below 560nm. The spectra are normalized to the peak value of the yellow class.

View larger version (34K): [in a new window]   Fig. 5. Modelling of the shift in spectral sensitivity induced by photoreceptor screening pigment when accumulated near the rhabdom on the basal photoreceptor R9. (A) The screening pigment, with a transmittance spectrum given by the dashed curve (compare the red reflectance spectrum in Fig. 4 and see text), acts on four different visual pigments, peaking at 530, 550, 570 and 590 nm (continuous curves). The absorption by the visual pigments (dotted curves) is obtained by multiplying the absorption spectrum of rhodopsin by the filter transmittance spectrum. (B) Normalizing the resulting spectra yields the sensitivity spectra. (C) Four different red filters (dashed curves) act on a visual pigment peaking at 570 nm (continuous curve), giving rise to absorption spectra of lower magnitude (dotted curves). (D) Normalization yields the sensitivity spectra.

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