Structural specializations of the cornea and retina at the dorsal rim of the compound eye in hymenopteran insects

Summary Structurally specialized ommatidia at the dorsal rim of the compound eyes of honey bees have been shown to be indispensable for polarized skylight navigation. In this study numerous other hymenopteran genera belonging to various superfamilies are shown to exhibit similar specializations in this part of the eye: (1) The cornea is penetrated by pore canals, which affect the optics of the ommatidia by scattering the light falling into the eye. In Andrena and Ammophila the cornea contains extensive cavities. (2) Each retinula contains 9 long receptor cells as opposed to 8 long ones in the adjacent dorsal area, and the rhabdom area is increased by a factor of up to 2. In all ant species examined there are no corneal but only retinal specializations at the dorsal rim of the eye. They include a specially shaped rhabdom as in Cataglyphis, in which polarization vision has also been demonstrated.     

Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have non-functional reflecting tapeta

Many insects exploit sky light polarization for navigation or cruising-course control. The detection of polarized sky light is mediated by the ommatidia of a small specialized part of the compound eye: the dorsal rim area (DRA). We describe the morphology and fine structure of the DRA in monarch butterflies (Danaus plexippus). The DRA consists of approximately 100 ommatidia forming a narrow ribbon along the dorsal eye margin. Each ommatidium contains two types of photoreceptor with mutually orthogonal microvilli orientations occurring in a 2:6 ratio. Within each rhabdomere, the microvilli are well aligned. Rhabdom structure and orientation remain constant at all retinal levels, but the rhabdom profiles, as seen in tangential sections through the DRA, change their orientations in a fan-like fashion from the frontal to the caudal end of the DRA. Whereas these properties (two microvillar orientations per rhabdom, microvillar alignment along rhabdomeres, ommatidial fan array) are typical for insect DRAs in general, we also report and discuss here a novel feature. The ommatidia of monarch butterflies are equipped with reflecting tapeta, which are directly connected to the proximal ends of the rhabdoms. Although tapeta are also present in the DRA, they are separated from the rhabdoms by a space of approximately 55 μm effectively inactivating them. This reduces self-screening effects, keeping polarization sensitivity of all photoreceptors of the DRA ommatidia both high and approximately equal.     

Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselfies (Odonata)

We have examined the fine structure of dorsal rim ommatidia in the compound eye of the three odonate species Sympetrum striolatum, Aeshna cyanea and Ischnura elegans. These ommatidia exhibit several specializations: (1) the rhabdoms are very short, (2) there is no rhabdomeric twist, and (3) the rhabdoms contain only two, orthogonally-arranged microvillar orientations. The dorsal rim ommatidia of several other insect species are known to be anatomically specialized in a similar way and to be responsible for polarization vision. We suggest that the dorsal rim area of the odonate compound eye plays a similar role in polarization vision. Since the Odonata are a primitive group of insects, the use of polarized skylight for navigation may have developed early in insect phylogeny.     

The structures of dorsal and ventral regions of a dragonfly retina

Summary The apposition eyes of the corduliid dragonfly Hemicordulia tau are each divided by pigment colour, facet size and facet arrangement into three regions: dorsal, ventral, and a posterior larval strip. Each ommatidium has two primary pigment cells, twenty-five secondary pigment cells, and eight receptor cells, all surrounded by tracheae which probably prevent light passing between ommatidia, and reduce the weight of the eye. Electron microscopy reveals that the receptor cells are of two types: small vestigial cells making virtually no contribution to the rhabdom, and full-size typical cells. The ventral ommatidia have a distal typical cell (oriented either horizontally or vertically), four medial typical cells, two proximal typical cells and one full-length vestigial cell. The dorsal ommatidia have only four full-length typical cells, and one distal and three vestigial full-length cells. The cross-section of dorsal rhabdoms is small and circular distally, but expands to a large three-pointed star medially and proximally. The tiered receptor arrangement in the ventral ommatidia is typical of other Odonata but the dorsal structure has not been fully described in other species. Specialised dorsal eye regions are typical of insects that detect others against the sky.     

Anatomical and physiological evidence for polarisation vision in the nocturnal bee <Emphasis Type="Italic">Megalopta genalis</Emphasis>

The presence of a specialised dorsal rim area with an ability to detect the e-vector orientation of polarised light is shown for the first time in a nocturnal hymenopteran. The dorsal rim area of the halictid bee Megalopta genalis features a number of characteristic anatomical specialisations including an increased rhabdom diameter and a lack of primary screening pigments. Optically, these specialisations result in wide spatial receptive fields (Δρ = 14°), a common adaptation found in the dorsal rim areas of insects used to filter out interfering effects (i.e. clouds) from the sky. In this specialised eye region all nine photoreceptors contribute their microvilli to the entire length of the ommatidia. These orthogonally directed microvilli are anatomically arranged in an almost linear, anterior–posterior orientation. Intracellular recordings within the dorsal rim area show very high polarisation sensitivity and a sensitivity peak within the ultraviolet part of the spectrum.     

Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye

In many insect species, a dorsal rim area (DRA) in the compound eye is adapted to analyze the sky polarization pattern for compass orientation. In the desert locust Schistocerca gregaria, these specializations are particularly striking. The DRA of the locust consists of about 400 ommatidia. The facets have an irregular shape, and pore canals are often present in the corneae. Screening pigment is missing in the region of the dioptric apparatus suggesting large receptive fields. The rhabdoms are shorter, but about four times larger in cross-section than the rhabdoms of ordinary ommatida. Eight retinula cells contribute to the rhabdom. The microvilli of retinula cell 7 and of cells 1, 2, 5, 6, 8 are highly aligned throughout the rhabdom and form two blocks of orthogonal orientation. The microvilli in the minute rhabdomeres of retinula cells 3 and 4, in contrast, show no particular alignment. As in other insect species, microvillar orientations are arranged in a fan-like pattern across the DRA. Photoreceptor axons project to distinct areas in the dorsal lamina and medulla. The morphological specializations in the DRA of the locust eye most likely maximize the polarization sensitivity and suggest that the locust uses this eye region for analysis of the sky polarization pattern.     

Structural specialization in the dorsal retina of the bee,Apis mellifera

Electron microscopic investigations on the eye of the worker bee showed that the ommatidia located in the uppermost part of the dorsal half of the eye are characterized by a distinct structural specialization: Nine visual cells contribute microvilli to the rhabdom over its full length. Within these rhabdoms the microvilli are arranged in at least three different directions. This specialization affects an area of at least 60 ommatidia. The most dorsal eye region differs, therefore, structurally from all other regions which have been investigated to date. Because the ommatidia in question are oriented skyward, their peculiar structure is discussed with respect to several concepts of polarized light detection by the bee.     

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。     

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.     

Microvillar orientation in the photoreceptors of the ant Cataglyphis bicolor

Polarization sensitivity in arthropod photoreceptors is crucially dependent on the arrangement of the microvilli within the rhabdom. Here, we present an electron-microscopical study in which the degree of microvillar alignment and changes in the cross-sectional areas of the rhabdoms along their length were studied in the compound eye of the desert ant, Cataglyphis bicolor. Serial cross-sections through the retina were taken and the orientation of the microvilli was determined in the photoreceptors of individually identified ommatidia. The reconstructions of microvillar alignment were made in the three anatomically and functionally distinct regions of the Cataglyphis compound eye: the dorsal rim area (DRA), the dorsal area (DA), and the ventral area (VA). The following morphological findings are consistent with polarization sensitivities measured previously by intracellular recordings. (1) The microvilli of the DRA photoreceptors are aligned in parallel along the entire length of the cell from the distal tip of the rhabdom down to its proximal end, near the basement membrane. The microvilli of the retinular cells R1 and R5 are always parallel to each other and perfectly perpendicular, with only minor deviation, to the microvillar orientation of the remaining receptor cells. (2) In the DA and VA regions of the eye, the microvillar tufts of the small receptors R1, R3, R5, R7, and R9 change their direction repetitively every 1-4 7m for up to 90°. In contrast, the large receptor cells R2, R4, R6, and R8 maintain their microvillar orientation rigidly. (3) In the DRA ommatidia, the cross-sectional areas of the rhabdomeres do not change along the length of the rhabdom, but substantial changes occur in the DA and VA ommatidia.     

Functional morphology of the ommatidia in the compound eye of the moth,Antheraea polyphemus (Insecta,Saturniidae)

Summary The fine structure of the superposition eye of the Saturniid moth Antheraea polyphemus Cramer was investigated by electron microscopy. Each of the approximately 10000 ommatidia consists of the same structural components, but regarding the arrangement of the ommatidia and the rhabdom structure therein, two regions of the eye have to be distinguished. In a small dorsal rim area, the ommatidia are characterized by rectangularly shaped rhabdoms containing parallel microvilli arranged in groups that are oriented perpendicular to each other. In all other ommatidia, the proximal parts of the rhabdoms show radially arranged microvilli, whereas the distal parts may reveal different patterns, frequently with microvilli in two directions or sometimes even in one direction. Moreover, the microvilli of all distal cells are arranged in parallel to meridians of the eyes. By virtue of these structural features the eyes should enable this moth not only discrimination of the plane of polarized light but also skylight-orientation via the polarization pattern, depending on moon position. The receptor cells exhibit only small alterations during daylight within the natural diurnal cycle. However, under illumination with different monochromatic lights of physiological intensity, receptor cells can be unbalanced: Changes in ultrastructure of the rhabdomeres and the cytoplasm of such cells are evident. The effects are different in the daytime and at night. These findings are discussed in relation to the breakdown and regeneration of microvilli and the influence of the diurnal cycle. They are compared with results on photoreceptor membrane turnover in eyes of other arthropod species.     

亲土苔蛾成虫复眼超微结构

【目的】重叠型眼在昆虫复眼演化中起着重要作用。本研究旨在阐明夜出型亲土苔蛾Manulea affineola复眼类型及结构特征,以期填补灯蛾亚科昆虫复眼研究的空白,扩充夜出型昆虫复眼的特征数据,为探讨重叠型眼的变异趋势及复眼演化提供依据。【方法】运用光学和透射电子显微技术观察亲土苔蛾成虫复眼的超微结构。【结果】亲土苔蛾成虫复眼具有一个透明区,由6个次级色素细胞的透明胞质构成。小眼具8个视网膜细胞,其中1个视网膜细胞较短,仅位于小眼基部。在透明区内,7个视网膜细胞聚集成一束,其远端与晶体束末端相接,但并不形成视杆。在透明区下方,这7个视网膜细胞形成一个中心融合的视杆。在复眼背缘区的小眼的视杆具有近似矩形的横截面,而其余小眼的视杆具多分支状截面。【结论】亲土苔蛾成虫复眼属于重叠型眼;复眼背缘区的矩形视杆很可能与昆虫的偏振敏感性有关。     

Patterning the peripheral retina of the fly: decoding a gradient

The peripheral regions of the fly eye show a number of specializations. First, immediately interior to the circumscribing head capsule and completely encircling the rest of the eye lies a thick band of pigment cells (pigment rim; PR). Second, in the dorsal periphery of the eye directly interior to the PR lie the dorsal rim (DR) ommatidia that are specialized polarized light detectors. The equivalent position in the ventral eye is occupied by standard ommatidia. Third, ommatidia characteristically project mechanosensory hairs above their lenses, but in the most peripheral rows (including the DR) the ommatidia are bald. Wingless secreted from the head capsule appears to organize all these peripheral specializations. Higher Wg levels induce PR, intermediate levels induce DR, and lower levels induce baldness. The predisposition of dorsal cells to generate DR ommatidia appears to be endowed by the exclusive dorsal expression of Iroquois genes.     

Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye

We made intracellular recordings from the photoreceptors of the polarisation-sensitive dorsal rim area of the cricket compound eye combined with dye marking. By measuring visual field sizes and optical axes in different parts of the dorsal rim area, we assessed the optical properties of the ommatidia. Due to the large angular sensitivities (median about 20°) and the high sampling frequency (about 1 per degree), the visual fields overlap extensively, such that a given portion of the sky is viewed simultaneously by a large number of ommatidia. By comparing the dye markings in the retina and in the optic lobe, the axon projections of the retinula cells were examined. Receptors R1, R2, R5 and R6 project to the lamina, whereas R7 projects to the medulla. The microvilli orientation of the two projection types differ by 90° indicating the two analyser channels that give antagonistic input to polarisation-sensitive interneurons. Using the retinal marking pattern as an indicator for the quality of the intracellular recordings, the polarisation sensitivity of the photoreceptors was re-examined. The polarisation sensitivity of recordings from dye-coupled cells was much lower (median: 4.5) than that of recordings in which only one cell was marked (median: 9.8), indicating that artefactual electrical coupling between photoreceptors can significantly deteriorate polarisation sensitivity. The physiological value of polarisation sensitivity in the cricket dorsal rim area is thus typically about 10. Accepted: 4 November 1999     

Structure of the dorsal eye region of the moth,Adoxophyes reticulana Hb. (Lepidoptera : Tortricidae)

Ommatidia of the eucon compound eye of Adoxophyes reticulana (Lepidoptera : Tortricidae) were investigated elect ronmicroscopically. The dorsofrontal part and the dorsal rim region were examined in serial sections. Seven radially arranged retinula cells RC₁₋₇ form the rhabdom from distal to proximal region (Fig. 1). The 8th retinula cell RC₈ joins the first 7 at their bases; this cell enlarges proximally (Fig. 1C, D). In the dorsofrontal region, 2 types of rhabdoms are distinguished; Type II (Figs. 1B₂;3b) outnumbers Type I (Figs. 1B₁;3a by a ratio of 4 : l. In the dorsal rim area, the first 2 rows are occupied exclusively by Type 11-rhabdoms; beyond this, the rhabdom of the dorsal rim area is characterized by the fact that its middle and proximal parts are considerably larger in diameter than in the dorsofrontal part; in this region, the microvilli of the horizontally oriented rhabdomeres are also parallel to the ;,-axis of the eye (Figs. 1B₃;3d). Thus, this small eye region meets the structural requirements for the detection of polarized light. The eye is interpreted as an intermediate between apposition and superposition eyes, because the rhabdom begins at the tip of the crystalline tract and the retinula cells are pigmented like those of an apposition eye. On the other hand, the structure of the dioptric apparatus and the tracheal system corresponds to those of superposition eyes. Parallels with the Ephestia eye in basic structural features are discussed in regard to the possible function of this eye and to the systematic position of A. reticulana.     

The Anostracan Rhabdom and the Basement Membrane. An Ultrastructural Study of the Artemia Compound Eye (Crustacea)

Abstract The ommatidia of the compound eyes of Artemia salina L. are normally composed of four crystalline cone cells containing glycogen. The cells are enveloped by two so-called “cellules épidermiques juxta-cristallines”. There are also six pigmented retinula cells, all contributing to the rhabdom. A peculiar feature of the Artemia crystalline cone cells is that their elongated parts, the so-called cone cell roots, widen and flatten proximally, forming interdigitating “endfeet”. The basement membrane thus consists of a cellular portion combined with the basal lamina. The main mass of the rhabdom of the Artemia eye is built up by five retinula cells, two contributing a smaller part. The microvilli are oriented in four directions, two being orthogonal. The sixth cell contributes on two small portions to the rhabdom in the distalmost and a more proximal position. The rest of it runs axon-like outside the omnatidium. Where the sixth cell wedges in, the direction of the microvilli is changed and has no orthogonal pattern. Two rhabdom types of compound eyes are distinguished: the decapod or banded or layered rhabdom: and the anostracan rhabdom with continuous rhabdomeres.     

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.     

Morphology of the compound eye of the giant deep-sea isopod Bathynomus giganteus

The structural organization of the compound eye of the largest known isopod, Bathynomus giganteus, is described from four specimens maintained in the laboratory for as long as two months. Living specimens have not previously been available for study. The two triangular compound eyes measure about 18 mm on the dorsal edge and are separated by an interocular distance of 25 mm. They face forward and slightly downward and may have significant overlap in visual fields. Each eye contains about 3,500 ommatidia in animals of body lengths from 22.5 cm to 37.5 cm. The packing of ommatidia is not uniform across the retina, but is nearly hexagonal in the dorsal central region and nearly square in the ventral and lateral periphery. The dioptric elements in each ommatidium consist of a laminar cornea, which is flat externally and convex internally, and a bipartite crystalline cone. Sometimes seven and sometimes eight retinular cells closely appose the proximal tip of the cone and bear the microvilli of the rhabdom. Proximal to the rhabdom the retinular cells form thin pillars near the periphery of the ommatidium, and the central portion along the optic axis at this level is occupied by interstitial cells that contain massive arrays of clear vesicles thought to serve as reflective elements. The arhabdomeral segments of the retinular cells and the interstitial cells rest on a basement membrane. Within each ommatidium the basement membrane has two extensions with cylindrical cores and thin sheets of dense material and collagen-like filaments. These sheets occupy spaces between adjacent interstitial cells up to the level of the rhabdomeral segments of the retinular cells. Arrays of pigment cells with relatively weak light-screening properties separate adjacent ommatidia. Animals were fixed both in light within a week of being brought from depth into daylight, and after 2 months of maintenance in constant darkness following such daylight exposure. In both cases, microvilli of the rhabdom were severely disrupted and the retinular cytoplasm contained numerous multivesicular bodies. Exposure to natural daylight appears to cause irreversible structural damage to the photoreceptors of these animals.     

Spatial control of photomechanical movements in the lateral eye of the American horseshoe crab, Limulus polyphemus

This study asks whether photomechanical movements in the retinal cells of the lateral eye of the American horseshoe crab, Limulus polyphemus, are controlled locally within each ommatidium, or whether they are a retinal array property involving lateral communication between ommatidia. Three experiments were performed. A small spot, a vertical slit down the center, or the anterior third of an otherwise masked eye was illuminated. The contralateral eye was fully illuminated in each experiment and served as a light-adapted control. Morphometric analyses of aperture length and rhabdom dimensions were made from serial 1-microm plastic sections. The results suggest there is a different spatial threshold for photomechanical movement for aperture lengthening than for rhabdom lengthening. When only a few ommatidia are illuminated, the aperture does not change. When about 10% are illuminated, they lengthen, but the masked ommatidia do not. When about a third are illuminated, all the ommatidia in the eye lengthen together, including the two thirds that were masked. When either only a few ommatidia or about 10% of the ommatidia are illuminated, rhabdom shape is unchanged. When a third of the eye is illuminated, the illuminated rhabdoms lengthen, but the masked rhabdoms do not.     

Fine structural description of the compound eye of the Madagascar 'hissing cockroach'Gromphadorhina portentosa (Dictyoptera: Blaberidae)

The compound eyes of the wingless adults of the Madagascar ‘hissing cockroach’Gromphadorhina portentosa Sachum, 1853 were examined by light and electron microscopy. Each eye contains 2 400‐2 500 mostly hexagonal facets. However, irregularities affecting both shape and size of the ommatidia are relatively common, especially towards the margins of the eye. An individual ommatidium of this eucone type of apposition eye contains eight retinula cells, which give rise to a centrally‐fused, tiered rhabdom. The distal end of the latter is funnel‐shaped and accommodates the proximal end of the cone in its midst. Further below, the rhabdom (then formed by the rhabdomeres of four retinula cells) assumes a squarish profile with microvilli aligned in two directions at right‐angle to each other. Cross sections through the proximal regions of the rhabdom display triangular rhabdom outlines and microvilli (belonging to 3‐4 retinula cells different from those involved in the squarish more distal rhabdom) that run in three directions inclined to one another by 120°. Overall the organization of the eye conforms to the orthopteroid pattern and particularly closely resembles that of the American cockroach Periplaneta americana. However, since G. portentosa possesses fewer ommatidia, this could be a consequence of its inability to fly. On the other hand, the large size of the facets and the voluminous rhabdoms suggest considerable absolute sensitivity and an ability to detect the plane of linearly polarized light. Based on the pattern of microvillus orientations in combination with the crepuscular lifestyle G. portentosa leads and the habitat it occurs in, the prediction is made that this insect uses its green receptors for e‐vector discrimination in the environment of down‐welling light that reaches the forest floor.