Visual ecology of insect superposition eyes

University dissertation from Swedish Natural Science Research Council, P.O. Box 71 42, SE-103 87 Stockholm, Sweden or: Dan-Eric Nilsson, Department of Zoology, Helgonavägen 3, 223 62 Lund, Sweden

Abstract: In the superposition compound eye each rhabdom (light sensitive unit) receives light through many ommatidial facets, while in the apposition compound eye every rhabdom receives light from a single facet. The superposition design increases photon capture, which is an advantage in dark environments. Despite their advantage in dim light, superposition eyes can sometimes be found in insects that live in brighter habitats. The aim of this thesis is to study visual adaptations in insects with superposition eyes. Animals with different lifestyles and activity patterns have been selected for this study. A more general theoretical analysis of the design of superposition eyes is also included in this thesis. The dorsal eyes of male mayflies (family Baetidae) are used only to detect females flying against the sky. Male mayflies that swarm in open habitats where a large portion of the sky is visible, have eyes with large fields of view but with a poor resolution. Other species swarm in forests, and have highly resolved tubular eyes with narrow fields of view that match the visible patches of sky. The elephant hawkmoth (Deilephila elpenor) has superposition eyes adapted for hovering in front of flowers while collecting nectar at night. The eye possesses smooth regional differences. The largest apertures, highest sensitivities and the largest binocular overlap are found in the anterio-ventral region of the eye with which they fixate flowers while feeding. They also have the poorest anatomical resolution in this region. The tiger beetle Cicindela hybrida has an eye that is optimised for visual hunting in a flat environment. It has an apposition eye during the day with a pronounced visual streak (horizontal acute zone) that forms a binocular acute zone at the front of the eye. The eye design matches their hunting behaviour and includes tilting of the head to fixate prey. The tropical tiger beetle Odontocheila chrysis, a close relative of Cicindela hybrida, lives in dark forest habitats and has superposition eyes both during the day and at night and no pronounced regional differences. The bright habitat of Cicindela has resulted in the evolution of apposition eyes, which permit pronounced regional differences, while in Odontocheila superposition eyes provide optimal vision in a dark environment but with limited possibilities for regional differences. Data from real eyes were compared to computer models to asses the basic principles and constraints in superposition eye design. We found several basic assumptions about superposition eye design to be incorrect: (1) the incident and exit angles in each optical unit are not equal for all angles, (2) the focal plane is not always located at half the radius of the whole eye, and (3) spherical aberration is not a major limitation to resolution in superposition eyes. The main conclusion of this analysis is that selection for design tolerance is an overlooked evolutionary force.

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