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The fine structure of the retina of the honey bee drone

An electron microscopical study

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Summary

The eye of the honey bee drone is composed of approximately 8,000 photoreceptive units or ommatidia, each topped by a crystalline cone and a corneal facet. An ommatidium contains 9 visual or retinula cells whose processes or axons pierce a basement membrane and enter the optic lobe underlying the sensory retina. The visual cells of the ommatidium are of unequal size: six are large and three, small. In the center of the ommatidium, the visual cells bear a brush of microvilli called rhabdomere. The rhabdome is a closed-type one and formed mainly by the rhabdomeres of the six large retinula cells. The rhabdomeric microvilli probably contain the photopigment (rhodopsin), whose modification by light lead to the receptor potential in the retinula cells. The cytoplasm of the retinula cells contains various organelles including pigment granules (ommochromes), and peculiar structures called the subrhabdomeric cisternae. The cisternae, probably composed of agranular endoplasmic reticulum undergo swelling during dark adaptation and appear in frequent connection with Golgi cisternae. Three types of pigment cells are associated with each ommatidium. The crystalline cone is entirely surrounded by two corneal pigment cells. The ommatidium, including its dioptric apparatus and corneal pigment cells, is surrounded by a sleeve of about 30 elongated cells called the outer pigment cells. These extend from the base of the corneal facet to the basement membrane. Near the basement membrane the center of the ommatidium is occupied by a basal pigment cell. Open extracellular channels are present between pigment cells as well as between retinula cells. Tight junctions within the ommatidium are restricted to the contact points between the rhabdomeric microvilli. These results are discussed in view of their functional implications in the drone vision, as well as in view of the data of comparative morphology.

Résumé

L'oeil composé du faux-bourdon est formé d'environ 8000 unités photoréceptrices ou ommatidies. Chaque ommatidie, surmontée d'un appareil diotrique constitué d'une lentille cornéenne et d'un cône cristallinien, comporte 9 cellules visuelles dont les parties proximales (axones) pénètrent dans le lobe optique. Le lobe optique est séparé de la rétine sensorielle par une membrane basale. Les cellules visuelles formant l'ommatidie sont de taille inégale: six sont grandes et trois petites. Au centre de l'ommatidie, les grandes cellules visuelles forment de nombreuses microvillosités dont l'ensemble constitue le rhabdome. Celui-ci est du type fermé. La membrane des microvillosités contient probablement le photopigment. Le cytoplasme des cellules visuelles est riche en organites parmi lesquels des vacuoles allongées de réticulum endoplasmique lisse appelées citernes périrhabdominales. Les citernes changent de volume lors de l'adaptation à la lumière et à l'obscurité et apparaissent fréquemment en contact avec des complexes de Golgi ou des profiles de réticulum endoplasmique granulaire.

Trois types de cellules pigmentaires sont associés à l'ommatidie: les cellules pigmentaires du cristallin, les cellules pigmentaires externes, et la cellule pigmentaire basale. Les cellules pigmentaires du cristallin sont au nombre de deux et enveloppent le cône cristallinien. 27 à 30 cellules pigmentaires externes entourent l'ommatidie depuis la base de la cornée jusqu'à la membrane basale. La cellule pigmentaire basale occupe le centre de l'ommatidie lorsque les cellules visuelles se transforment en axones. Les divers types cellulaires de la rétine sont séparés les uns des autres par de minces espaces extracellulaires. Dans l'ommatidie, des jonctions serrées ne sont trouvées qu'entre les microvillosités rhabdomériques. Ces résultats sont discutés du point de vue de leur implication fonctionelle et de leur signification vis-à-vis de la morphologie comparée.

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  1. Institute of Histology, University of Geneva School of Medicine, Geneva, Switzerland

    Alain Perrelet

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I am most indebted to Dr. Fritz Baumann, assistant professor in the Department of Physiology, University of Geneva School of Medicine, who contributed to this work with innumerable suggestions and precious advice. I also wish to thank Professors Ch. Rouiller and J. Posternak for constant support, and Mrs. A. Perrelet-Bridges for the correction of the English manuscript. Fig. 1 was done by R. Mira and the photographical work by Mrs. M. Sidler whose skilful assistance is gratefully acknowledged.

This work was supported by a grant from the “Fonds National Suisse de la Recherche Scientifique”.

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Perrelet, A. The fine structure of the retina of the honey bee drone. Z. Zellforsch. 108, 530–562 (1970). https://doi.org/10.1007/BF00339658

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