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 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.     

Visual behaviour and the structure of dark and light-adapted larval and adult eyes of the New Zealand glowworm Arachnocampa luminosa (Mycetophilidae: Diptera)

Both larval and adult New Zealand cave glowworms exhibit reactions to light; their photoreceptors must, therefore, be regarded as functional. The two principal stemmata of the larva possess large biconvex lenses and voluminous rhabdoms. Approximately 12 retinula cells are present. In light-adapted larvae the diameter of the rhabdom is 8 μm and that of an individual microvillus is 49.5 nm. Dark-adapted eyes have rhabdoms that measure 14 μm in cross section and microvilli with an average diameter of 54 nm. The compound eye of the adult comprises approximately 750 ommatidia, each with a facet diameter of 27–28 μm. A facet is surrounded by 1–6 interommatidial hairs which are up to 30 μm long. The interommatidial angle is 5.5°. Cones, consisting of 4 crystalline cone cells, are of the ‘acone’ type. Pigment granules in the primary pigment cells are twice as large as those of the retinula cells which measure 0.6–0.75 μm in diameter. The rhabdom is basically of the dipteran type, i.e. six open peripheral rhabdomeres surround 2 central rhabdomers arranged in a tandem position. The microvilli of cells 1–6 and cell 8 have diameters ranging from 68 to 73 nm, but those of the distally-located central rhabdomere 7 are 20% larger. This is irrespective of whether the eye is dark or light-adapted. In the latter the cones are long and narrow, the screening pigment granules closely surround the rhabdomeres, and the rhabdom is less voluminous than that of the dark-adapted eye.     

The microtubular system of crayfish retinula cells and its changes in relation to screening-pigment migration

The organization of the microtubular system in crayfish retinula cells and its changes in relation to the light-dependent migrations of the screening pigment were studied by electron microscopy. A massive column of microtubules extends longitudinally throughout each retinula cell and its axon. The column is formed by overlapping fascicles of microtubules that originate from the vicinity of the rhabdomeres at multiple levels along the rhabdom. The pigment granules and other organelles are in general aligned with these fascicles and peripheral to the microtubular column. Close associations between microtubules and pigment granules are frequent. The total number of microtubules decreases nucleofugally from an average of about 500 at the middle of the rhabdom, to 390 at the proximal end of the rhabdom, and 240 in the axon below the basement membrane. The longitudinal distribution of microtubules was found similar for cells with the screening pigment in opposite extreme positions. In cells with the pigment in an intermediate position the number of microtubules was found to be nearly doubled in each of the mentioned levels; however, this change was correlated with a parallel increase in the cross-sectional area of the cells during the intermediate state. Thus, the density of microtubules tends to remain fairly constant throughout the light/dark adaptation cycle. These observations suggest that the microtubular system of the crayfish retinula cells constitutes a relatively stationary framework during screening-pigment movements, and could possibly act as a supportive guiding track for pigment transport.     

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.     

Retina and dioptric apparatus of the dung beetle Euoniticellus africanus

Retinal fine structure and optics of the eye of the dung beetle Euoniticellus africanus have been studied and compared with those of three other scarabaeid beetles: Repsimus manicatus, Anoplognathus pallidicollis and Sericesthis geminata. The eye of Euoniticellus, in common with that of the other three species, possesses a dioptric system in which light first passes through a thick optically homogeneous cornea, and then enters a non-homogeneous crystalline cone. The lens cylinder properties of the latter cause the light rays to become partially focused across the clear-zone upon the rhabdom layer. Rays traced through a large scale drawing of the eye, with refractive indices measured for each component, predict an acceptance angle of approximately 26°. Since no significant aperture changes, lengthening of crystalline thread, cell or pigment migrations appear to be associated with dark/light adaptation, the eye may be assumed to be permanently poorly focused. In optomotor experiments the beetles did not show their characteristic antennal following response to black and white stripes when the latter had repeat periods of <30°. Structurally the eye of Euoniticellus differs markedly from that of other scarabaeids. It is totally divided into dorsal and ventral eye which are of a different size (the dorsal eye is smaller), but whose structural organization is basically the same. Principal pigment cells (they do not fully surround the cone) as well as accessory pigment cells (they accompany the retinula cells in an extraordinarily regular fashion as far as to the basement membrane) exhibit some unusual features. On the proximal side of the clear-zone, at a level where all retinula cell membranes form complex meanders and convolutions, cell 1 is the first to possess a rhabdomere. In it, all microvilli run parallel. This rhabdomere becomes part of the rectangular proximal rhabdom over the upper 20% of its length. Below this level the rhabdom consists of 6 rhabdomeres, but throughout its length microvilli are oriented in 2 orthogonal directions. It is thought that polarization sensitivity in dung beetles generally is related to the rhabdom organization described for Euoniticellus. An eighth (basal) cell is present in each ommatidium, but it lacks a rhabdomere. A tracheal tapetum is not developed. Finally, the point is made not to regard all different eye structures in insects as perfect adaptations to a particular environment or way of living, for specializations of photoreceptors may either follow, parallel or precede any ecological adaptation.     

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.     

粘虫蛾复眼背、腹区视杆结构的差异

根据光学和电子显微镜的观察,粘虫蛾复眼背、腹区域的视杆结构具有以下主要差异:1)背方小眼视杆的长度短于腹方小眼视杆的长度。2)在横切面上,背方小眼视杆的中段近似方形。该段间细胞的视小杆为三角形,每个具有平行排列的微绒毛。整个视杆包含两个互相垂直的微绒毛轴。腹方小眼视杆的中段为风扇形。间细胞的视小杆为“V”字形,微绒毛排列不平行。3)背方小眼基细胞的视小杆几乎位于气管反光层远侧,而腹方小眼甚至延伸到气管反光层内。 在背方和腹方小眼视杆的内段,每个间细胞的微绒毛均平行,且排列在基细胞的大形视小杆周围。更深层,在其它细胞的轴突均已相继出现的水平上,基细胞的大形视小杆仍然可见。 最后,对形态上的特点,在功能上可能具有的一些意义也进行了初步讨论。     

Ultrastructure of the single-chamber stemmata of Arge pagana (Panzer, 1798) (Hymenoptera: Argidae)

Stemmata are peculiar visual organs of most larvae in holometabolous insects. In Hymenoptera, Symphyta larvae exclusively possess a pair of stemmata, whose cellular organizations have not been thoroughly elucidated to date. In this paper, the morphology and fine structure of stemmata were investigated in the large rose sawfly Arge pagana (Panzer, 1798) using light and electron microscopy. The larvae possess a pair of stemmata, which belong to the “unicorneal composite eye” or single-chamber stemmata. Each stemma is composed of a biconvex cornea lens, a layer of corneagenous cells, numerous pigment cells, and hundreds of retinula cells. According to the number of retinula cells forming a rhabdom, the stemma can be divided into two regions, the larger Region I and the smaller Region II. The former occupies the largest area of the stemma and contains the majority of rhabdoms, each of which is formed by the rhabdomeres of eight retinula cells. The latter occupies a narrow posterior margin, where each rhabdom consists of nine retinula cells. Based on the different cellular organizations of rhabdoms, the stemma of Argidae is likely developed by the fusion of two types of ommatidial units.     

Orthogonal microvillus pattern in the eighth rhabdomere of the rock crab Grapsus

Summary The eighth retinular cell (R 8) of Grapsus lacks cytoplasmic pigment granules and basically resembles those previously known in the ghost crab Ocypode and the mysid Praunus. Distally located, R 8 comprises four lobes inserted between the outer ends of the seven regular retinular cells (R 1–R 7). A thin cytoplasmic bridge connects these lobes. One lobe adjacent to R 1 contains the nucleus of R 8 and gives rise proximally to the cell's axon. The short distal eighth rhabdomere consists of microvilli (mvl) protruding axially from all four lobes. Similar R 8's were found also in two other crab families and in two other genera of mysids.In Grapsus the eighth rhabdomere is extraordinary in possessing mvl oriented in two orthogonal directions parallel to the mvl of R 1–R 7. The distal 20% of the rhabdom consists of mvl originating exclusively from R 8. These appear in somewhat irregular bands and are alternately oriented parallel to the animal's vertical or horizontal axis. More proximally the retinula contains eleven sectors but the rhabdom still comprises bands of alternating mvl with those from R 8 joined respectively by the rhabdomeres of R 1, 4, and 5 (horizontal) and R 2, 3, 6 and 7 (vertical). The rest of the rhabdom shows typical decapod organization with seven interdigitating rhabdomeres.This research has been aided by grants from the United States Public Health Service (5 RO1 EY 00405) and the National Geographic Society. The authors are grateful to Mabelita Campbell for her helpful assistance.     

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.     

MORPHOLOGY OF THE OMMATIDIA OF THE COMPOUND EYE OF LIMULUS

The sensory portion of the ommatidium of the compound eye of Limulus has been studied with the electron microscope. In axial longitudinal section the rhabdom appears to be made up of small polygons, and in transverse section the rhabdom appears as a banded structure of dark lines. Thus in three dimensions the rhabdom resembles a honeycomb composed of tubular units, the long axes of which lie in transverse planes and are oriented perpendicular to the retinula cell's contours. The tubular units, which are about 140 mµ in diameter in Limulus (70 mµ in diameter in the spider and Scutigera), are microvilli of the borders of the retinula cells. The walls of these microvilli are continuous with fine linear structures (membranes) in the cytoplasm of the retinula cells. In transverse sections of the ommatidium oval bodies interpreted as mitochondria are observed in an annular zone at the tips of the rhabdom's rays. These mitochondria, which are 2 to 10 µ in diameter, are crowded with irregular closed outlines about 100 mµ in diameter. Possible functions of components of the ommatidium are discussed.     

Direction ofE for maximum response of a retinula cell

Summary Except for very special fused rhabdoms, e. g. those with orthogonal microvilli like the worker bee, the direction of the electric vector E of linear polarized light necessary for a maximum response from a retinula cell is not parallel (or perpendicular) to the microvilli of the recorded cell. This is because the rhabdomeres of a fused rhabdom are optically coupled, i. e. the properties of each rhabdomere influence the manner in which light is transmitted down the composite rhabdom structure. A rhabdom is analogous to a non-uniform absorbing optical crystal. Such a crystal has two coordinate (optical) axes along which E remains linear polarized as it propagates. Only when the microvilli of the recorded cell are parallel to one of these axes will the direction ofE for maximum retinula cell response be parallel to the microvilli. The locust-type of rhabdom is used as an example.     

The fine structure of some carabid beetle eyes,with particular reference to ciliary structures in the retinula cells

Paired centrioles and associated ciliary root material occur in all eight retinula cells in the nine species investigated. In the diurnal Notiophilus, Elaphrus and Bembidion where the distal rhabdomere of cell 7 is fused with the proximal rhabdom formed by cells 1 to 6, the roots in cells 1 to 6 extend for the entire length of the retinula. In Notiophilus their arrangement around the rhabdom suggests a complementary mechanical relationship between the six large roots and the four Semper cell processes. In five relatively nocturnal species a retinula cell column separates the distal rhabdomere from the proximal rhabdom. In cells 1 to 6 root material is associated with the distally located centrioles as follows. In Leistus roots extend into the proximal rhabdom layer. In Loricera and Agonum roots at the level of the proximal rhabdom are not continuous with the rootlets or short roots associated with the centrioles. In Pseudophonus and Feronia, and in the diurnal Cicindela, short rootlets link the centrioles. Cell movements on dark-adaptation of Notiophilus and Cicindela include shortening of the crystalline tract. In Notiophilus the entire rhabdom is apparently displaced, whereas in Cicindela the narrow distal rhabdomere becomes dissociated from the proximal rhabdom.     

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.     

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。     

飞蝗复眼生理和结构上的节律变化

采用细胞内记录和光镜方法研究了飞蝗(Locusta migratoria)夜间和日间在暗适应和明适应状态下小网膜细胞角敏感度以及晶锥和小网膜细胞之间区域结构上的变化.结果表明小网膜细胞角敏感度的变化不仅仅由于晶锥周围主色素细胞色素颗粒的移动,而且也由于小眼感杆束结构上的节律变化.     

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.     

The ommatidium of the termite mastotermes darwiniensis

An electron microscope study of the compound eye of the termite Mastotermes darwiniensis shows that the ommatidia have both primitive and specialized features. The ommatidia are of the apposition type with eight similar retinular cells, a fused rhabdom, irregularly orientated rhabdomere tubules and no tracheae. The retinula cells contain lipid. The cone cells have unusual processes, which thicken towards the basement membrane and contain rough endoplasmic reticulum, granules and dense bodies. These processes may act as a primitive transport system for nutrients.     

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 micro in diameter and 60 micro 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.