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.     

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.     

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.     

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.     

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.     

Systematic variations in microvilli banding patterns along fiddler crab rhabdoms

Polarisation sensitivity is based on the regular alignment of dichroic photopigment molecules within photoreceptor cells. In crustaceans, this is achieved by regularly stacking photopigment-rich microvilli in alternating orthogonal bands within fused rhabdoms. Despite being critical for the efficient detection of polarised light, very little research has focused on the detailed arrangement of these microvilli bands. We report here a number of hitherto undescribed, but functionally relevant changes in the organisation of microvilli banding patterns, both within receptors, and across the compound eye of fiddler crabs. In all ommatidia, microvilli bands increase in length from the distal to the proximal ends of the rhabdom. In equatorial rhabdoms, horizontal bands increase gradually from 3 rows of microvilli distally to 20 rows proximally. In contrast, vertical equatorial microvilli bands contain 15–20 rows of microvilli in the distal 30 µm of the rhabdom, shortening to 10 rows over the next 30 µm and then increase in length to 20 rows in parallel with horizontal bands. In the dorsal eye, horizontal microvilli occupy only half the cross-sectional area as vertical microvilli bands. Modelling absorption along the length of fiddler crab rhabdoms suggests that (1) increasing band length assures that photon absorption probability per band remains constant along the length of photoreceptors, indicating that individual bands may act as units of transduction or adaptation; (2) the different organisation of microvilli bands in equatorial and dorsal rhabdoms tune receptors to the degree and the information content of polarised light in the environment.     

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。     

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。     

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.     

Fine structure of the compound eye of the fungus beetle Neotriplax lewisi (Coleoptera, Cucujiformia, Erotylidae)

Abstract. In many ways, the apposition eye of the erotylid fungus beetle Neotriplax lewisi resembles that of chrysomelids: its 400–500 mostly hexagonal ommatidia are of the acone type and possess "open rhabdoms," a tapetum is not present, and axons penetrate the basement membrane in distinct bundles of eight. The eye also shows some unusual features that, at present, defy clear functional interpretation. Firstly, the cuticle of the interfacetal areas stains differently from that of the corneal lenses and, secondly, the two rhabdom systems in each ommatidium (central and peripheral) both possess microvilli that are oriented in such a way as to permit e-vector discrimination. On the basis of comparisons with other open rhabdom eyes, it is postulated that vision in N. lewisi involves neither high resolving power nor superior absolute sensitivity. However, this beetle can distinguish illuminated from shaded areas, and seems specialized to make use of sky polarization (probably in the UV and green regions of the spectrum) and/or the position of the sun as a course-stabilizing function during flights.     

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.     

Ommatidial structure in relation to turnover of photoreceptor membrane in the locust

Summary In the compound eye of the locust, Locusta, the cross-sectional area of the rhabdoms increases at dusk by 4.7-fold due to the rapid assembly of new microvillar membrane, and decreases at dawn by a corresponding amount as a result of pinocytotic shedding from the microvilli. The rhabdoms at night have more and longer photoreceptor microvilli than rhabdoms during the day. The orientations of the six rhabdomeres that comprise the distal rhabdom also change. The density of intramembrane particles on the P-face of the microvillar membrane, putatively representing mostly rhodopsin molecules, or aggregates thereof, does not change.An alteration in the size of the ommatidial field-stop, produced by the primary pigment cells, is concomitant with the change in rhabdom size. At night the increase in size of the field-stop must widen the angular acceptance of a rhabdom, increasing the capture of photons from an extended field. Conversely, during the day, when photons are more abundant, its decrease must narrow the acceptance angle, increasing angular resolution. Because of the presence of this field-stop, the optics of the ommatidium would not be greatly affected if the rhabdom were to remain always at its night size. It is argued, therefore, that the variable-size rhabdom must have resulted from some demand other than that of light/dark adaptation.Changes in size and organisation of the rhabdoms in response to various light regimes indicate that: (1) Rapid shedding of photoreceptor membrane is induced by the onset of light, but shedding also occurs slowly in darkness during the day. (2) Microvillar assembly is initiated by the onset of darkness, but also occurs at the normal time of dusk without a change in ambient lighting, provided there has been some light during the day. Therefore, both shedding and assembly of microvillar membrane are affected by the state of illumination, but also appear to be under some endogenous control.     

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.     

Retinal ultrastructure of the dorsal eye region of Pararge aegeria (Linné) (Lepidoptera: Satyridae)

We examined the fine structure of dorsal rim ommatidia of the compound eye of Pararge aegeria (Lepidoptera: Satyridae) and compared them with ommatidia of the large dorsal region described by Riesenberg (1983 Diploma, University of Munich). 1. The ommatidia of the dorsal rim show morphological specializations known to be typical of the perception of polarized light: (a) the dumb-bell-shaped rhabdoms contain linearly aligned rhabdomeres with only 2 orthogonally arranged microvilli orientations. The rhabdoms are composed of the rhabdomeres of 9 receptor cells, 8 of which are radially arranged. The rhabdomeres of receptor cells VI and V5, as well as D2, D4, D6 and D8 are dorsoventrally aligned, whereas the rhabdomeres of the cells H3 and H7 are perpendicular to them. The rhabdomere of the bilobed 9th retinula cell lies basally and is dorsoventrally aligned, where retinula cell VI and V5 are already axonal. (b) There is no rhabdomeric twist, and (c) the rhabdoms are rather short. 2. However, in the ommatidia of the large dorsal region, only 2 retinula cells (H3 and H7) are suitable for perception of polarized light. 3. Lucifer yellow and horse radish peroxidase were used as tracers to visualize the projections of retinula cell axons of the dorsal rim area and the large dorsal region into the optic neuropils (lamina and medulla). Two receptors (VI and V5) from both the dorsal rim area and the large dorsal region, have long visual fibres projecting into the medulla. The 7 remaining retinula cells of both eye regions, including those that meet the structural requirements for detection of polarized light in the large dorsal region, terminate in the lamina (short visual fibres). These results provide a starting point for further studies to reveal the possible neuronal pathways by which polarized light may be processed.     

Fine structure of the compound eye of Porcellio scaber in light and dark adaption.

The compound eyes of the terrestrial isopod Porcellio scaber comprises about 20 ommatidia. The dioptric apparatus of each ommatidia includes a biconvex corneal lens and a spherical crystalline cone that is secreted by two cone cells. The closed rhabdom is formed by the microvillar extensions of seven pigmented retinula cells and one apical eccentric cell. All retinular axons exit the eye in one bundle. During dark-adaption pigment granules in the retinula cells rapidly withdrew from around the rhabdom and the cell periphery, and migrated basally. Rhabdoms thickened because of movement of the microvilli, and mitochondria moved medially and basally. During light adaption these processes were reversed. Multivesicular bodies became less numerous and rough endoplasmic reticulum and ribosomes proliferated during the initial stages of light adaption.     

Geometrical optics of a galatheid compound eye

The eyes of galatheid squat lobsters (Munida rugosa) are shown to be of the reflecting superposition type. In the dark-adapted state corneal lenses focus light at the level of the rhabdoms and light from more than 1000 facets is redirected to the superposition focus by the reflecting surfaces of the crystalline cones. When the eye is light adapted, apposition optics are used. In this state paraxial light is focused by the corneal lens and the parabolic proximal end of the cone onto the distal end of a rhabdomeric lightguide. The latter transmits light across the clear zone to the rhabdom layer. In the dorsal part of the eye the individual ommatidia become progressively shorter until the cones and rhabdoms are no longer separated by a clear zone. Although formerly considered to be developing ommatidia, they are shown to be retained specifically for scanning the downwelling irradiance.Abbreviations RI refractive index - SEM scanning electron microscope     

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.     

An apposition‐like compound eye with a layered rhabdom in the small diving beetle Agabus japonicus (Coleoptera,Dytiscidae)

The fine structure of the compound eyes of the adult diving beetle Agabus japonicus is described with light, scanning, and transmission electron microscopy. The eye of A. japonicus is mango‐shaped and consists of about 985 ommatidia. Each ommatidium is composed of a corneal facet lens, an eucone type of crystalline cone, a fused layered rhabdom with a basal rhabdomere, seven retinula cells (including six distal cells and one basal cell), two primary pigment cells and an undetermined number of secondary pigment cells that are restricted to the distalmost region of the eye. A clear‐zone, separating dioptric apparatus from photoreceptive structures, is not developed and the eye thus resembles an apposition eye. The cross‐sectional areas of the rhabdoms are relatively large indicative of enhanced light‐sensitivity. The distal and central region of the rhabdom is layered with interdigitating microvilli suggesting polarization sensitivity. According to the features mentioned above, we suggest that 1) the eye, seemingly of the apposition type, occurs in a taxon for which the clear‐zone (superposition) eye is characteristic; 2) the eye possesses adaptations to function in a dim‐light environment; 3) the eye may be sensitive to underwater polarized light or linearly water‐reflected polarized light. J. Morphol. 275:1273–1283, 2014. © 2014 Wiley Periodicals, Inc.     

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.