PHOTORECEPTOR STRUCTURES : III. DROSOPHILA MELANOGASTER

The eyes of three eye mutants of Drosophila melanogaster were fixed and thin sections studied for its structural detail in the electron microscope. Each ommatidium was found to have seven retinula cells with an equal number of rhabdomeres (visual units). The rhabdomeres average 1.2 µ in diameter and 60 µ in length. Each rhabdomere consists of osmium-fixed dense bands averaging 120 A in thickness, and with less dense interspaces 200 to 400 A. There is an average of 23 dense bands or 46 interfaces per micron within the rhabdomere. The rhabdomere as we have presented it is a single structure of packed rods or tubes. The "fine structure" within the rhabdomere is similar to that observed by electron microscopy for the retinula of the house fly, and to the retinal rods of the vertebrate eye, and to the chloroplasts of plant cells in a variety of animal and plant photoreceptor structures. In addition, the radial arrangements within the ommatidium of radially unsymmetrical units, the rhabdomeres, is probably related to the analysis of polarized light in the insect eye.     

The compound eye of Parnara guttata (Insecta,Lepidoptera, Hesperiidae): Fine structure of the ommatidium

Summary The fine structure of an ommatidium of a skipper butterfly, Parnara guttata, has been studied using the electron microscope. Each ommatidium has nine retinula cells, which were classified into three groups: two distal, six medial and one basal retinula cells. The rhabdomeres of the distal retinula cells are localized in the distal part of the rhabdom, while those of the six medial retinula cells appear throughout most of the rhabdom. The rhabdomere of the basal retinula cell occupies only the basal part of the rhabdom. The rhabdomeres of four medial cells are constructed of parallel microvilli, while fan-like microvilli form the rhabdomeres of other two medial retinula cells. The distal and basal retinula cells have rhabdomeres consisting of both parallel and fan-like microvilli. This is the first time the construction of the rhabdomeres of the distal and basal retinula cells has been described in such fine detail for a skipper butterfly. Nine retinula cell axons of each ommatidium extend to the first neuropile of the optic lobe, the lamina ganglionaris. No difference was found in the number of retinula cells of an ommatidium or the shape of the rhabdom between the dorsal and ventral regions of the compound eye.     

The eye of Dytiscus (Coleoptera)

The eye of Dytiscus (Coleoptera) has rhabdomeres at three different levels. The crystalline threads stretch from the ends of the crystalline cones only as far as the distal layer of rhabdomeres. There is one distal rhabdo-mere per ommatidium, and in this system the ommatidia are anatomically separate. Between the distal rhabdomere and the rhabdomeres of the next six retinula cells is a wide clear zone in which light entering by one facet could possibly reach deep rhabdomeres of a different ommatidium. Of the six proximal rhabdomeres, four have rhabdomere tubules which lie horizontal with reference to the normal posture, the other two having vertically oriented tubules. The eighth cell, with nucleus near the basement membrane, has a small rhabdomere. All eight retinula cells have axons and there is no other class of axons in the eye.     

The ultrastructural organization of the visual system of the wax moth,Galleria mellonella: The retina

Summary The ultrastructural organization of ommatidial components of the retina of the moth, Galleria mellonella are described from electron microscopic observations. Each ommatidium is composed of 12 common retinula cells and one basal eccentric cell. The retinula cells are connected together by a desmosomal strip along their length. The rhabdom occupies the basal thirty percent of the ommatidium and can be divided into nine segments of parallel microvilli. Several cells may contribute to an individual rhabdomere. The rhabdomeres are arranged in a cross with single cell rhabdomeres lying between the arms of the cross. Thin sections of ommatidium absorb polarized light differentially. The total amount of plane polarized light absorbed varies with angle of rotation for an entire ommatidium but there are also differences between the amount of absorption of adjacent rhabdomeric segments. Galleria appears to be the only lepidopteran in which the possibility of the polarized light reception has been reported.     

Fine structure of the ommatidia and the occurrence of rhabdomeric twist in the dorsal eye of male Bibio marci (Diptera,Nematocera, Bibionidae)

Summary The ommatidia in the dorsal eye of male Bibio marci (March flies) are comprised of eight retinula cells (R1–8). In the distal region, the open rhabdomeres of retinula cells 1–6 are arranged in a symmetrically circular pattern with their microvilli directed radially. Immediately beneath the crystalline cone, cell 7 forms a rhabdomere that is about 1 m long and lies in the center of the circle formed by the rhabdomeres of cells 1–6. For the remaining length of an ommatidium it is replaced by the rhabdomere of retinula cell 8. The cell body of this retinula cell almost encloses its own rhabdomere by forming a deep invagination. Consequently, no ommatidial cavity is present. In the left eye rhabdomeres R 3, 5 and 6 first twist clockwise along their longitudinal axes, while rhabdomeres R1, 2, 4 and 8 twist counterclockwise. Opposite twisting is observed in the right eye. The twist rate varies along the length of the rhabdomeres. In a middle region of 60 m, within which the direction of twist does not change, the maximal twist rates are approximately 2°–5°/m in R1–6 and even higher in R 8. In a proximal region, the direction of twist is reversed, but the initial orientation of the microvilli not reestablished. Both the cross-sectional shape of the rhabdomeres and their geometric arrangement in the retinula change along with the twisting. It is substantiated that the rhabdomeric twist is not due to artifactual deformation.Supported by the Deutsche Forschungsgemeinschaft (SFB 4: E 2)The authors thank Dr. I. de la Motte for providing the material used in this study, Prof. H. Altner for critical discussion and Dr. M. Burrows for his attentive linguistic corrections     

The fine structure of the retina of the honey bee drone

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

Fine-structure of the compound eye of the buprestid beetle Curis caloptera (Coleoptera, Buprestidae)

Curis caloptera is a buprestid beetle, which is active in bright sunlight. Its eye, like that of many other diurnal arthropods, is of the apposition type, in which dioptric apparatus and receptor layer are not separated by a region devoid of pigment. Perhaps to prevent damage by U. V.-radiation, the cornea is relatively thick (approximately 90 micron) and crystalline cones are of the "eucone-type". In each ommatidium the cone cell extensions occupy regular positions between the 8 retinula cells and reach down to the basement membrane where they end in bulbous swellings and contain grains of screening pigment. Pigment grains, slightly smaller than those present in the primary pigment cells, are also found within the retinula cells. Although the rhabdom possesses a uniform diameter of approximately 2 micron over its entire length of almost 300 micron, the number of rhabdomeres contributing to the rhabdom varies and depends on the level at which the rhabdom is sectioned. At the distal end, only one retinula cell possesses a rhabdomere; the same holds true for the proximal end, where a different rhabdomere (with microvilli at right angles to those of the distal cell) dominates. One retinula cell, of darker appearance in electron micrographs, occupies a distal position in each ommatidium and remains preferentially oriented within a sector of 60 degrees irrespective of the ommatidial axis. The ommatidial axis itself was found to vary 235 degrees. We provide circumstantial evidence for the view that the cell in question could be a U. V.-receptor with a role to play in an unambiguous determination of the E-vector. Separate bundles, each containing 8 axons, pass through the basement membrane together with 1 or 2 tracheoles. A traceheal tapetum is not developed.     

THE MICROSTRUCTURE OF THE COMPOUND EYES OF INSECTS

The apposition eyes of two diurnal insects, Sarcophaga bullata (Diptera) and Anax junius (Odonata), have been examined with the electron microscope. In the latter case only the rhabdom is described. The rhabdom of the fly consists of a central matrix and seven rhabdomeres, one for each retinula cell. The rhabdomeres show an ordered internal structure built up of transverse tubes, hexagonal in cross-section. These slender compartments running the width of the rhabdomere are 370 A in diameter. After fixation with osmium tetroxide the walls of the compartments are more electron dense than the interiors. The retinula cells contain mitochondria, and pigment granules smaller than those found in the pigment cells. These granules tend to cluster close behind the membranes which separate the retinula cells from their rhabdomeres. The rhabdom of the dragonfly is a single structure which appears to be composed of three fused "rhabdomeres," each similar to a rhabdomere of Sarcophaga. Reasons are given for believing that the rhabdom may be the site of photoreception, as well as the organ for analyzing plane-polarized light, as suggested by other workers.     

The effect of short wavelength light on retinula cell structure in white-eye Drosophila.

Recent electron microscopic examination of the retinula cells of white-eyed fruitflies has shown gross disruption of the ordered membrane system of the rhabdomeres, and extensive vesiculation of retinula cells 1 to 6 within each ommatidium following blue irradiation. Central retinula cells 7 and 8 are unaffected. The selective disruption is not observed in white-eyed fruitflies similarly irradiated with equal-energy yellow light.     

Specialized ommatidia for polarization vision in the compound eye of cockchafers,Melolontha melolontha (Coleoptera,Scarabaeidae)

Summary The superposition eye of the cockchafer, Melolontha melolontha, exhibits the typical features of many nocturnal and crepuscular scarabaeid beetles: the dioptric apparatus of each ommatidium consists of a thick corneal lens with a strong inner convexity attached to a crystalline cone, that is surrounded by two primary and 9–11 secondary pigment cells. The clear zone contains the unpigmented extensions of the secondary pigment cells, which surround the cell bodies of seven retinula (receptor) cells per ommatidium and a retinular tract formed by them. The seven-lobed fused rhabdoms are composed by the rhabdomeres of the receptor cells 1–7. The rhabdoms are optically separated from each other by a tracheal sheath around the retinulae. The orientation of the microvilli diverges in a fan-like fashion within each rhabdomere. The proximally situated retinula cell 8 does not form a rhabdomere. This standard form of ommatidium stands in contrast to another type of ommatidium found in the dorsal rim area of the eye. The dorsal rim ommatidia are characterized by the following anatomical specializations: (1) The corneal lenses are not clear but contain light-scattering, bubble-like inclusions. (2) The rhabdom length is increased approximately by a factor of two. (3) The rhabdoms have unlobed shapes. (4) Within each rhabdomere the microvilli are parallel to each other. The microvilli of receptor 1 are oriented 90° to those of receptors 2–7. (5) The tracheal sheaths around the retinulae are missing. These findings indicate that the photoreceptors of the dorsal rim area are strongly polarization sensitive and have large visual fields. In the dorsal rim ommatidia of other insects, functionally similar anatomical specializations have been found. In these species, the dorsal rim area of the eye was demonstrated to be the eye region that is responsible for the detection of polarized light. We suggest that the dorsal rim area of the cockchafer eye subserves the same function and that the beetles use the polarization pattern of the sky for orientation during their migrations.     

栖境不同的两种跳甲复眼结构比较

栖息于荫暗隐蔽处的蛇莓跳甲(Altica fragariae)和向阳开阔地的萎陵跳甲(A.Ampelophaga)的复眼外部形态及小眼微细结构有如下相同特征：两复眼均比较小,呈“八”字型排列在头部近背方的两侧;每个小眼含有一个双凸面的角膜锥体、4个森氏细胞和7个小网膜细胞;2个主色素细胞及11-12个附色素细胞围绕在小眼的外缘;小网膜细胞和色素细胞内均有丰富色素颗粒,当光照强度发生变化时,小网膜细胞内的色素颗粒发生位移;在视杆中段横切面上,视杆由7个微绒毛呈平行排列的矩形视小杆组成,其中的6个视小杆互相连成一个近似六边形的框架,将另一个视小杆围在中央。两种跳甲复眼结构的主要差异有：蛇莓跳甲每个复眼大约仅有150个小眼,而萎陵跳甲约有2印个;复眼曲率半径前者只有后者的一半;视杆中段横切面上,视杆占整个小网膜面积的比率两虫分别为37%和25%,蛇莓跳甲高于萎陵跳甲。对以上形态结构特征可能具有的功能意义进行了初步讨论。     

Ultrastructure of the larval eye of the scorpionfly Panorpa dubia (mecoptera: Panorpidae) with implications for the evolutionary origin of holometabolous larvae

The evolutionary origin of holometabolous larvae is a long‐standing and controversial issue. The Mecoptera are unique in Holometabola for their larvae possessing a pair of compound eyes instead of stemmata. The ultrastructure of the larval eyes of the scorpionfly Panorpa dubia Chou and Wang, 1981 was investigated using transmission electron microscopy. Each ommatidium possesses a cornea, a tetrapartite eucone crystalline cone, eight retinula cells, two primary pigment cells, and an undetermined number of secondary pigment cells. The rhabdomeres of the eight retinula cells form a centrally‐fused, tiered rhabdom of four distal and four proximal retinula cells. The rhabdomeres of the four distal retinula cells extend distally into a funnel shape around the basal surface of the crystalline cone. Based on the similarity of the larval eyes of Panorpidae to the eyes of the hemimetabolous insects and the difference from the stemmata of the holometabolous larvae, the evolutionary origin of the holometabolous larvae is briefly discussed. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

The nucleolar fibrillar centres in various cell types in vivo or in vitro

Summary The compound eye of male (haploid) Xyleborus ferrugineus beetles was examined with scanning and transmission electron microscopy. The eye externally consists of ca. 19 to 33 facets. Each ommatidium is composed of a thickly biconvex lenslet with about 50 electron dense and rare layers, but at the junction area between two lenslets there are only about 35 to 37 layers that can be distinguished. A very short (3.4–4.0 m) acone type crystalline cone is located directly beneath the lenslet. Each ommatidium is surrounded by pigment cells, and pigment granules also appear throughout the cytoplasm of the retinular cells. Some pigment granules are even present below the basement membrane. There are 8 retinular cells. The rhabdomeres of 2 centrally situated photoreceptor cells fuse into a rhabdom which is enveloped by the rhabdomeres of 6 peripheral retinular cells. The rhabdomeres of the 6 peripheral retinular cells join laterally to form a rhabdomeric ring around the central rhabdom. No tracheation was observed among the retinular cells. Virus-like particles are evident near the nucleus in each Semper cell of the crystalline cone.This research was supported by the Director of the Research Division, C.A.L.S., University of Wisconsin, Madison; and in part by research grant No. RR-00779 from the Division of Research Resources, National Institutes of Health and by funds from the Schoenleber Foundation, Milwaukee, WI to D.M.N.     

The compound eye of<Emphasis Type="Italic"> Scutigera coleoptrata</Emphasis> (Linnaeus, 1758) (Chilopoda: Notostigmophora): an ultrastructural reinvestigation that adds support to the Mandibulata concept

The lateral compound eye of Scutigera coleoptrata was examined by electron microscopy. Each ommatidium consists of a dioptric apparatus, formed by a cornea and a multipartite eucone crystalline cone, a bilayered retinula and a surrounding sheath of primary pigment and interommatidial pigment cells. With reference to the median eye region, each cone is made up of eight cone segments belonging to four cone cells. The nuclei of the cone cells are located proximally outside the cone near the transition area between distal and proximal retinula cells. The connection between nuclear region and cone segment is via a narrow cytoplasmic strand, which splits into two distal cytoplasmic processes. Additionally, from the nuclear region of each cone cell a single cytoplasmic process runs in a proximal direction to the basement membrane. The bilayered rhabdom is usually made up of the rhabdomeres of 9–12 distal retinula cells and four proximal retinula cell. The pigment shield is composed of primary pigment cells (which most likely secrete the corneal lens) and interommatidial pigment cells. The primary pigment cells underlie the cornea and surround, more or less, the upper third of the crystalline cone. By giving rise to the cornea and by functioning as part of the pigment shield these pigment cells serve a double function. Interommatidial pigment cells extend from the cornea to the basement membrane and stabilise the ommatidium. In particular, the presence of cone cells, primary pigment cells as well as interommatidial pigment cells in the compound eye of S. coleoptrata is seen as an important morphological support for the Mandibulata concept. Furthermore, the phylogenetic significance of these cell types is discussed with respect to the Tetraconata.     

Regional differences in a nematoceran retina (Insecta,Diptera)

Summary The compound eye of Psychoda cinerea comprises two types of ommatidia, arranged so as to divide the retina into distinct dorsal and ventral regions. The P-type ommatidium, in the ventral part of the eye, differs fundamentally from the other dipteran ommatidia so far described, and is regarded as a primitive ommatidium. The acone dioptric apparatus is the same in both types, with a spherical lens and four Semper cells, the processes of which expand below the rhabdom to form a ring of pigment sacs. Only the distal region of the rhabdom is surrounded by a continuous ring of screening pigment, formed by 2 primary and 12–16 secondary pigment cells. The highly pigmented retinula cells penetrate the basement membrane proximally at about the level of their nuclei; in this region they are separated from the hemolymph by glial elements. The rhabdomeres R1–6 are fused to form a tube. The two types of ommatidia are defined by the arrangement of the retinula cells R7/8: in the T type the central rhabdomeres are one below the other, in the usual tandem position, whereas in the P type only R8 is central, with R7 in the peripheral ring. In the proximal region of the retina, retinula cells with parallel microvilli in neighboring ommatidia are joined in rows by lateral processes from the R8 cells. All the rhabdomeres are short and not twisted, which suggests that the retinula cells are highly sensitive to direction of polarization. The eye can adapt by a number of retinomotor processes. These findings, together with observations of behavior, imply that the psychodids have well-developed visual abilities.     

Fine structure of light- and dark-adapted eyes of desert ants,Cataglyphis bicolor (Formicidae,Hymenoptera)

Among ants, Cataglyphis bicolor shows the best performance in optical orientation. Its eye is of the apposition type with a fused rhabdom. Morphological studies on the general struture of the eye as well as the effect of light have been carried out with transmission and scanning electron microscopy. An ommatidium is composed of a dioptric apparatus, consisting of a cornea, corneal process and a crystalline cone, the sensory retinula, which is made up of eight retinula cells in the distal half and of an additional ninth one in the proximal half. The ommatidia are separated from each other by two primary pigment cells, which surround the crystalline cone and an average of 12 secondary pigment cells, which reach from cornea to the basement membrane. The eye of Cataglyphis bicolor possesses a light intensity dependent adaptation mechanism, which causes a radial and distal movement of the pigment granules within the retinula cells and a dilatation of cisternae of the ER along the rhabdom. Until now, no overall order in arrangement of retinula cells or direction of microvilli has been found from ommatidium to ommatidium. Such an order, however, must exist, either on the retina or the lamina level, since we have proven the ant's capacity for polarized light analysis.     

The microanatomy of the compound eye of Munida irrasa (Decapoda: Galatheidae)

The compound eye of Munida irrasa differs in several respects from the typical decapod eye. The proximal pigment is found only in retinula cells. The eccentric cell is extremely large and expanded to fill the interstices of the crystalline tract area; thus, a typical "clear-zone" is absent. Six retinula cells course distally to screen two sides of the crystalline cone. There are approximately 12,500 ommatidia in each compound eye. There are several similarities to the typical decapod eye. Each ommatidium is composed of a typical cornea, corneagenous cells, crystalline cone cells, crystalline cone, crystalline cone tract and eight retinula cells. Distal pigment cells are present and surround the crystalline cone. The distal processes of the retinula cells also contain pigment. The retinula cell processes penetrate the basement membrane as fascicles composed of processes from adjacent retinulae.     

Ultrastructure of the compound eye of the diploid female beetle,Xyleborus ferrugineus

Summary The compound eye of female (diploid) Xyleborus ferrugineus beetles was examined with scanning and transmission electron microscopy. The eye is emarginate, and externally consists of roughly 70–100 facets. Each ommatidium is composed of a thickly biconvex lenslet with about 50 electron dense and rare layers. The lens facet overlies a crystalline cone of the acone type which is roughly hourglass-shaped. Pigment cells envelop the entire ommatidium, and pigment granules also are abundant throughout the cytoplasm of the 8 retinular cells. The rhabdomeres of 2 centrally situated photoreceptor cells effectively fuse into a rhabdom that extends from the base of the crystalline cone deeply into the ommatidium. Six distal peripheral retinular cells encircle the 2 central cells, and their rhabdomeres join laterally to form a rhabdomeric ring around the central rhabdom. The rhabdom and rhabdomeric ring are effectively separated by the cytoplasm of the two central retinular cells which contains the usual organelles and an abundance of shielding pigment granules. Eight axons per ommatidium gather in a tracheae-less fascicle before exiting the eye through the fenestrate basement membrane. No tracheation was observed among the retinular cells. Each Semper cell of each observed crystalline cone contained an abundance of virus-like particles near the cell nucleus. The insect is laboratory reared, and the visual system seems very amenable to photoreceptor investigations.This research was supported by the Director of the Research Division, C.A.L.S., University of Wisconsin, Madison; and in part by research grant No. RR-00779 from the Division of Research Resources, National Institutes of Health and by funds from the Schoenleber Foundation, Milwaukee, WI to D.M.N.     

Recording of Retinal Action Potentials from Single Cells in the Insect Compound Eye

Electrical responses were recorded intracellularly from the compound eyes of a fly (Lucilia) and of several dragonflies (Copera, Agriocnemis, and Lestes). An ommatidium of the dragonflies is made up of four retinula cells and a rhabdom composed of three rhabdomeres while the Lucilia has an ommatidium of seven independent retinula cells and rhabdomeres. The intracellular responses presumably recorded from the retinula cell had the same wave form in the two groups of insects: The responses were composed of two components or phases, a transient spike-like potential and a slow one maintained during illumination. The membrane potential, in the range of -25 to -70 mv., was influenced by the level of adaptation, and it was transiently depolarized to zero by high levels of illumination.     

The fine structure of the compound eye of a damsel-fly

Summary The compound eyes of two species of damsel-flies, Ishunura senegalensis and Cersion calamorum, were examined by electron microscopy. Each ommatidium is composed of eight retinula cells which are semistratified in the receptor layer. The retinula cells are divided into four types from the difference of levels in the rhabdom formation; one distal large cell having the rhabdomere only in the distal layer, four middle cells forming the rhabdom in the middle layer, two proximal cells making up the rhabdom in the proximal layer and one distal small cell having no rhabdomere in any layers. In addition, the lamina ganglionaris was partly observed. Some retinula axons terminate at an different level from the other axons. The functional differentiation among these different types of cells is discussed with relation to the analysis of the polarized light and the discrimination of the diffraction images.This work is supported by a grant from the U.S. Army Research and Development Group (Far East), Department of the Army (DA-CRD-AG-S29-544-67-G61).The authors wish to express their gratitude to Drs. H. Morita and H. Tateda for their helpful discussions throughout this study.