FINE STRUCTURE OF THE RETINULAE IN THE COMPOUND EYE OF THE HONEY-BEE

The retinula of the compound eye of the worker honey-bee has been examined with the electron microscope. The rhabdom lies on the ommatidial axis; it is usually cylindrical in shape, about 3 to 4 µ in diameter, and lacks an axial cavity. Cross-sections show it to be four parted, although it is formed from eight retinular cells (Figs. 2, 3). Each quadrant of the rhabdom consists of a closely packed parallel array of tubules with long axes perpendicular to the axis of the rhabdom. The tubules in adjacent quadrants of the rhabdom are mutually perpendicular. At the distal end of the ommatidium these tubules are seen to be microvilli of the retinular cells. Immediately surrounding the rhabdom, the cytoplasm of the retinular cells contains a membranous endoplasmic reticulum which is oriented approximately radially with respect to the axis of the ommatidium. Farther away from the rhabdom the cytoplasm contains numerous mitochondria.     

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 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.     

棉铃虫蛾复眼的微细结构及其区域性差异

用电子显微镜观察棉铃虫蛾复眼的微细结构及其区域性差异。此复眼具有小网膜细胞柱的透明带。每个小眼包括一个外凸内平的角膜,一个晶锥,四个形成晶锥、晶束的晶锥细胞和两个围绕着晶锥的主虹膜细胞,六至八个小网膜细胞和一个基细胞。晶锥末端有一短小固定的晶束。小网膜细胞柱远侧中央有似微绒毛结构的视杆束。每个小眼被六个附色素细胞围绕。 微细结构的区域性差异:1.背方小眼视杆中段横切面近似矩形,主要由六个微绒毛平行排列的三角形视小杯组成,整个视杆包含两个互相垂直的微绒毛轴;腹方、前方、后方和侧方区域的小眼视杆中段横切面为风扇形,“V”字形视小杆内微绒毛排列不平行;2.前方区域小眼视杆中段的横切面要比后方大;3.前方、腹方区域内,有的相邻小眼的小网膜细胞柱互相连结,背方、后方区域未观察到这一现象。     

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 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.     

The retina of the phalangid,Opilio ravennae,with particular reference to arhabdomeric cells

Summary The retina of the phalangid, Opilio ravennae, consists of retinula cells with distal rhabdomeres, arhabdomeric cells, and sheath cells. The receptive segment of retinula cells shows a clear separation into a Proximal rhabdom, organized into distinct rhabdom units formed by three or four retinula cells, and a Distal rhabdom, consisting of an uniterrupted layer of contiguous rhabdomeres. One of the cells comprising a retinula unit, the so-called distal retinula cell (DRC), has two or three branches that pass laterally alongside the rhabdom, thereby separating the two or three principal retinula cells of a unit. The two morphologically distinct layers of the receptive segment differ with respect to the cellular origin of rhabdomeral microvilli: DRC-branches contribute very few microvilli to the proximal rhabdom and develop extremely large rhabdomeres in the distal rhabdom only, causing the rhabdom units to fuse. Principal retinula cells, on the other hand, comprise the majority of microvilli of the proximal rhabdom, but their rhabdomeres diminish in the distal rhabdom. It is argued that proximal and distal rhabdoms serve different functions in relation to the intensity of incident light.In animals fixed 4 h after sunset, pigment granules retreat from the distal two thirds of the receptive segment. A comparison of retinae of day- and night-adapted animals shows that there is a slight (approximately 15%) increase in the cross-sectional area of rhabdomeral microvilli in dark-adapted animals, which in volume corresponds to the loss of pigment granules from the receptive segment. The length of the receptive segment as well as the pattern and shape of rhabdom units, however, remain unchanged.Each retinula unit is associated with one arhabdomeric cell. Their cell bodies are located close to those of retinula cells, but are much smaller and do not contain pigment granules. The most remarkable feature is a long, slender distal dendrite that extends up to the base of the fused rhabdom where it increases in diameter and develops a number of lateral processes interdigitating with microvilli of the rhabdom. The most distal dendrite portion extends through the center of the fused rhabdom and has again a smooth outline. All dendrites end in the distal third of the proximal rhabdom and are never present in the layer of the contiguous distal rhabdom. Arhabdomeric cells are of essentially the same morphology in day- and night-adapted animals. They are interpreted as photoinsensitive secondary neurons involved in visual information-processing that channel current collected from retinula cells of the proximal rhabdom along the optic nerve. A comparison is made with morphological equivalents of these cells in other chelicerate species.     

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。     

ELECTRON MICROSCOPIC STUDY OF THE CYTOPATHOLOGY OF ECHO VIRUS INFECTION IN CULTIVATED CELLS

The cultivated monkey kidney cell is subject to changes when infected with ECHO viruses 6, 9, and 19. The electron microscope reveals three stages of infection: (a) initial stage. The nucleus appears granular with chromatin condensation on the nuclear envelope. The cytoplasm contains electron transparent vesicles and vacuoles forming nests. (b) Intermediate stage. The nucleus seems to diminish, appearing more pycnotic and displaced toward the periphery. The cytoplasm is filled with electron transparent vacuoles and vesicles, and dense masses as well as some spiral bodies are seen. The mitochondria retain their shape. Dense particles are seen, which are possibly of viral nature. (c) Final stage. The nucleus is contracted to a narrow strip close to the cellular membrane or is completely destroyed. The cytoplasm shows no apparent changes. Crystals are frequently observed in cells infected with ECHO viruses 6 and 19, consisting of dense particles with an average diameter of 14.4 mµ ranging from approximately 13.2 to 15.6 mµ for ECHO virus 6, and 14.5 mµ ranging from approximately 12.5 to 16.5 mµ for ECHO virus 19. These particles are clustered in hexagonal packages forming angles of 75° and 105°. The particles in most crystals are arranged in rows separated by a constant distance, the latter varying from one crystal to another and being approximately 1.5 and 2.5 times the distance between particles. Other particles were observed which, however, are not considered to be of viral nature.     

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.     

Larval and adult eye of the Western Rock Lobster (Panulirus longipes)

A number of differences exists between the compound eyes of larval and adult rock lobsters, Panulirus longipes. The larval eye more closely resembles the apposition type of compound eye, in which retinula cells and rhabdom lie immediately below the cone cells. The adult eye, on the other hand, is a typical clear-zone photoreceptor in which cones and retinula cell layers are separated by a wide transparent region. The rhabdom of the larval eye, if cut longitudinally, exhibits a "banded" structure over its entire length; in the adult the banded part is confined to the distal end, and the rhabdom is tiered. Both eyes have in common an eighth, distally-located retinula cell, which possesses orthogonally-oriented microvilli, and a peculiar lens-shaped "crystal", which appears to focus light onto the narrow column of the distal rhabdom. Migration of screening pigment on dark-light adaptation is accompanied by changes in sensitivity and resolution of the eye. Retinula cells belonging to one ommatidium do not arrange into one single bundle of axons, but interweave with axons of four neighbouring facets in an extraordinarily regular fashion.     

AN ELECTRON MICROSCOPE STUDY OF THE CYTOLOGY OF THE PROTOZOAN EUPLOTES PATELLA

1. Structurally the "sensory bristles" in Euplotes patella are typical cilia, but no ciliary rootlets connect their bases. 2. The "neuromotor fibrils" are composed of filaments 21 mµ in diameter. At the point of junction of the filaments with the peripheral ciliary fibrils a granular structure 65 to 90 mµ in diameter is seen which has dense central and peripheral zones separated by a less dense layer. Information on the interconnection of organelles is expanded. 3. A system of subpellicular fibrils is described. The external fibrillar system described by others could not be found. 4. The motorium is shown to be a mass of intertwining rootlet filaments. 5. The micronucleus is shown to have a spongy, dense material in a less dense material, all of which is surrounded by a double-layered membrane. 6. The double-layered macronuclear membrane contains annuli whose outside diameter is 70 mµ; the macronuclear bodies are sometimes closely applied to the membrane. In the macronuclear reorganization bands, the solution plane is a fine network, while the reconstruction plane is devoid of structure at the level of resolution observed. 7. The mitochondria are composed of tubules, only occasionally oriented, usually embedded in a surrounding material of lower density. 8. Microbodies whose diameters are 250 to 350 mµ are frequently observed in close association with mitochondrial surfaces. 9. The food vacuoles, contractile vacuoles, and ciliary vacuoles are bounded by single-layered membranes. In the food vacuoles, the bacteria are surrounded by membranes individually or in small groups. 10. Cytoplasmic rods localized in the oral region, and cytoplasmic granules dispersed at random, are described. No typical ergastoplasm, endoplasmic reticulum, or Golgi material was observed.     

ELECTRON MICROSCOPY OF GROWING OOCYTES OF RANA PIPIENS

1. In the cytoplasm of oocytes of stage Y₀, prior to the appearance of yolk, one observes a few scattered profiles of endoplasmic reticulum and numerous filamentous mitochondria, usually distributed at random but sometimes clustered. As the nuclear membrane begins to bulge outward, small granules and short rods appear in the perinuclear cytoplasm and endoplasmic reticulum becomes more prominent throughout the cytoplasm. 2. Coincident with the appearance of the first yolk platelets, which are deposited in a narrow peripheral ring within the endoplasm at stage Y₁, protoplasmic processes, the microvilli, push out all over the surface of the oocyte. At the same time follicle cells pull away but remain attached to the oocyte at some points through finger-like processes which interdigitate with neighboring microvilli. It is estimated that the microvilli increase the absorptive area of the surface to about thirty-five times that of a simple sphere. Just beneath the microvillous layer is the basal protoplasm of the cortex, now containing tiny granules probably synthesized from newly absorbed raw materials. Cortical granules appear and become aligned below the basal layer on the external border of the endoplasm. Both the cortical granules and the yolk platelets measure up to 1 µ in diameter at this stage. 3. By stage Y₃ (yolk filling peripheral three-fourths of cytoplasm), the basal layer of the cortex is folded so that it appears in section as alternating ridges and valleys. The microvilli now extend from the summits of the cortical ridges. Small, ring-shaped granules are abundant in the cortex. Cortical granules have increased to 2 µ in diameter. 4. Yolk platelets continue to be synthesized around the cortical granules and in the subjacent endoplasm. The largest platelets measured in the interior cytoplasm at stage Y₄ (cytoplasm filled with yolk) were 3.7 µ wide by 5.8 µ long. Pigment granules increase in size from 0.15 µ in diameter at stage Y₃ to 0.30 µ in diameter at stage Y₄.     

THE FINE STRUCTURE OF Streptomyces coelicolor : II. The Nuclear Material

Colonies and spore suspensions of Streptomyces coelicolor were fixed for electron microscopy by the method of Kellenberger, Ryter, and Séchaud (1958). In thin sections the nuclear regions have a lower average density than the cytoplasm and the outlines of these regions correspond well with the profiles of the chromatinic bodies observed with the light microscope. The nuclear regions contain fibrils, about 5 mµ in diameter. In contrast, after fixation by the method of Palade (1952) the nuclear material is coagulated into irregular dense masses and tubular structures about 20 mµ in diameter, lying in a nuclear "vacuole." The significance of these observations is discussed in relation to the observations of other workers on the fine structure of the nuclear material of other bacteria and the chromosomes of higher cells.     

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.     

A discussion of light scattering in the Squilla rhabdom

The fine structure of the Squilla ommatidium suggests that elastic scattering of light may occur in the rhabdom. A detailed study of this phenomenon allows us to interpret the movement of the pigment granules of the retinula cells and the corresponding change of the rhabdom shape in light — and dark — adaptation.     

Colour receptors in the eye of the digger wasp,Sphex cognatus Smith: Evaluation by selective adaptation

Summary Pigment granule migration in pigment cells and retinula cells of the digger wasp Sphex cognatus Smith was analysed morphologically after light adaptation to natural light, dark adaptation and after four selective chromatic adaptations in the range between 358 nm and 580 nm and used as the index of receptor cell sensitivity. The receptor region of each ommatidium consists of nine retinula cells which form a centrally located rhabdom. Two morphologically and physiologically different visual units can be described, defined by the arrangement of the rhabdomeric microvilli, the topographical relationship of the receptor cells with respect to the eye axes and the unique retinula cell screening pigmentation. These two different sets of ommatidia (type A and B) are randomly distributed in a ratio of 13 throughout the eye (Ribi, 1978b). Chromatic adaptation experiments with wavelengths of 358 nm, 443 nm, 523 nm and 580 nm and subsequent histological examination reveal two UV receptors, two blue receptors and four yellow-green receptors in type A ommatidia and two UV receptors and six green to yellow-green receptors in type B ommatidia. The pigments in cells surrounding each ommatidium (two primary pigment cells, 20 secondary pigment cells and four pigmented cone extensions) were not affected significantly by the adaptation experiments.     

CELL JUNCTIONS IN OMMATIDIA OF LIMULUS

The intercellular relationships in the ommatidia of the lateral eye of Limulus have been investigated. The distal process of the eccentric cell gives origin to microvilli which interdigitate with the microvilli of the retinular cells. Therefore, both types of visual cells contribute to form the rhabdom and may have an analogous photoreceptor function. Quintuple-layered junctions are found within the rhabdom at the lines of demarcation between adjoining microvilli, whether the microvilli originate from a single retinular cell, from two adjacent retinular cells, or from a retinular cell and the eccentric cell. Furthermore, quintuple-layered junctions between the eccentric cell and the tips of the microvilli of the retinular cells occur at the boundary between the distal process and the rhabdom. These findings are interpreted to indicate that the rhabdom provides an extensive electrotonic junction relating retinular cells to one another and to the eccentric cell. Quintuple-layered junctions between glial and visual cells, as well as other structural features of the ommatidial cells, are also described.     

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.     

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.