The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly,<Emphasis Type="Italic"> Pieris rapae crucivora</Emphasis>

The compound eye of Pieris rapae crucivora contains ventrally three types of histologically distinct ommatidia. An ommatidium contains nine photoreceptors, four of which (R1-4) construct the distal tier of the rhabdom. We determined the sensitivity spectra of the R1-4 distal photoreceptors in each type of ommatidia by intracellular electrophysiology and identified UV, blue, double-peaked blue, green, and a green receptor with depressed sensitivity in the violet. We localized these receptors in each type of ommatidia by injecting dye after the recording. In type I ommatidia the R1 and R2 cells are UV and blue receptors. When R1 is UV sensitive, R2 is always blue sensitive, or vice versa. R3 and R4 in type I are both green receptors. In type II, R1 and R2 are both double-peaked blue receptors and R3 and R4 are both green receptors with depressed sensitivity in the violet. In type III, R1 and R2 are both UV, and R3 and R4 are green receptors. The double-peaked blue, and green receptors with depressed sensitivity in the violet in type II ommatidia have depressed sensitivity at 420 nm, which is probably due to the filtering effect of a fluorescing material present in the type II ommatidia. Spectral heterogeneity of ommatidia seems to be a common design of insect compound eyes.     

Photoreceptor spectral sensitivities of the Small White butterfly <Emphasis Type="Italic">Pieris rapae crucivora</Emphasis> interpreted with optical modeling

The compound eye of the Small White butterfly, Pieris rapae crucivora, has four classes of visual pigments, with peak absorption in the ultraviolet, violet, blue and green, but electrophysiological recordings yielded eight photoreceptors classes: an ultraviolet, violet, blue, double-peaked blue, green, blue-suppressed-green, pale-red and deep-red class. These photoreceptor classes were identified in three types of ommatidia, distinguishable by the different eye shine spectra and fluorescence; the latter only being present in the eyes of males. We present here two slightly different optical models that incorporate the various visual pigments, the light-filtering actions of the fluorescent, pale-red and deep-red screening pigment, located inside or adjacent to the rhabdom, and the reflectance spectrum of the tapetum that abuts the rhabdom proximally. The models serve to explain the photoreceptor spectral sensitivities as well as the eye shine.     

Regional distribution of three ultrastructural retinula types in the retina of Cataglyphis bicolor Fabr. (Formicidae,Hymenoptera)

Summary The retina of Cataglyphis bicolor was investigated by electron microscopy. Three types of structurally distinct retinulae were found and mapped throughout the compound eye: Type I is composed of four unpigmented thin cells, four larger pigmented cells as well as a basal ninth cell. Its rhabdom possesses a round cross section and four microvilli directions. This type occupies most of the dorsal two-thirds of the retina. Type II consists of two thin cells, two intermediate cells and four large cells. A basal ninth cell is also present; the rhabdom is as in type I. Type II retinulae are located in the ventral third of the retina. Type III ommatidia are unique within the Hymenoptera: there are four large pigmented cells, four thinner unpigmented cells and a basal ninth cell. The rhabdom, however, has a dumb-bell shaped cross section; two small cells lie at its opposed extremities and the remaining six cells have mutually perpendicular microvilli orientations. This type of retinula is found at the dorso-medial eye margin. Serial sectioning in this region revealed a conical shaped rhabdom without any torsion along the longitudinal axis. The rhabdomere cross section was calculated from distal and proximal thin sections. Angular statistics were applied to the microvilli directions of all three ommatidial types to determine the degree of order. A possible functional significance of the structural specializations of the different eye regions is discussed.Supported by Swiss National Science Foundation, Grant No. 3.814.72 awarded to Prof. Dr. R. Wehner. This work is part of a Ph. D. thesis. I wish to thank Prof. Dr. R. Wehner for continuous support and my colleagues Dr. P. Duelli and Dr. E. Meyer for a fruitful collaboration     

Blue and double-peaked green receptors depend on ommatidial type in the eye of the Japanese yellow swallowtail Papilio xuthus

The compound eye of the butterfly Papilio xuthus is composed of three spectrally distinct types of ommatidia. We investigated the blue and double-peaked green receptors that are encountered distally in type I and III ommatidia, by means of intracellular recordings, in vivo fluorescence microscopy, and histology. The blue receptors are R1 and/or R2 photoreceptors; they contain the same mRNA encoding the opsin of the blue-absorbing visual pigment. However, here we found that the sensitivity in the UV wavelength region strongly depends on the ommatidial type; the blue receptors in type I ommatidia have a distinctly depressed UV sensitivity, which is attributed to lateral filtering in the fused rhabdom. In the main, fronto-ventral part of the eye, the R3 and R4 photoreceptors of all ommatidia contain the same set of two mRNAs encoding the opsins of green-absorbing visual pigments, PxL1 and PxL2. The spectral sensitivities are double-peaked, but the UV sensitivity of the R3 and R4 photoreceptors in type I ommatidia appears to be reduced, similar to that of the co-localized blue receptors.     

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing,Troides aeacus formosanus

The compound eye of the Golden Birdwing, Troides aeacus formosanus (Papilionidae, Lepidoptera), is furnished with three types of ommatidia, which are clearly different in pigmentation around the rhabdom. Each ommatidium contains nine photoreceptors, whose spectral sensitivities were analyzed electrophysiologically. We identified nine spectral types of photoreceptor with sensitivities peaking at 360 nm (UV), 390 nm (V), 440 nm (B), 510 nm (BG), 540 nm (sG), 550 nm (dG), 580 nm (O), 610 nm (R), and 630 nm (dR) respectively. The spectral sensitivities of the V, O, R and dR receptors did not match the predicted spectra of any visual pigments, but with the filtering effects of the pigments around the rhabdom, they can be reasonably explained. In some of the receptors, negative-going responses were observed when they were stimulated at certain wavelengths, indicating antagonistic interactions between photoreceptors.     

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.     

Visual pigment spectra of the comma butterfly,<Emphasis Type="Italic"> Polygonia c-album</Emphasis>, derived from in vivo epi-illumination microspectrophotometry

The visual pigments in the compound eye of the comma butterfly, Polygonia c-album, were investigated in a specially designed epi-illumination microspectrophotometer. Absorption changes due to photochemical conversions of the visual pigments, or due to light-independent visual pigment decay and regeneration, were studied by measuring the eye shine, i.e., the light reflected from the tapetum located in each ommatidium proximal to the visual pigment-bearing rhabdom. The obtained absorbance difference spectra demonstrated the dominant presence of a green visual pigment. The rhodopsin and its metarhodopsin have absorption peak wavelengths at 532 nm and 492 nm, respectively. The metarhodopsin is removed from the rhabdom with a time constant of 15 min and the rhodopsin is regenerated with a time constant of 59 min (room temperature). A UV rhodopsin with metarhodopsin absorbing maximally at 467 nm was revealed, and evidence for a blue rhodopsin was obtained indirectly.     

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.     

Organisation of the compound eye of a tipulid fly during the day and night

Summary The ultrastructure of the compound eye of the Australian tipulid fly,Ptilogyna spectabilis, is described. The ommatidia are of the acone type. The rhabdom corresponds to the basic dipteran pattern with six outer rhabdomeres from retinular cells 1–6 (R1-6) that surround two tiered central rhabdomeres from R7 and 8. Distally, for about 8 m, the rhabdom is closed. For the remainder, where the rhabdomere of R8 replaces that of R7, the rhabdom is open, and the rhabdomeres lie in a large central ommatidial extracellular space. In the proximal two thirds of the rhabdom, the central space is partitioned by processes from the retinular cells so that the individual rhabdomeres are contained in pockets.At night the rhabdom abuts the cone cells, but during the day it migrates some 20 m proximally and is connected to a narrow (1–2 m) cone cell tract. This tract is surrounded by two primary pigment cells, which occupy a more lateral position at night and thus act like an iris. Pigment in secondary pigment cells also migrates so as to screen orthodromic light above the rhabdom during the day. Between midday and midnight, the rhabdom changes in length and cross-sectional area as a result of asynchrony of the shedding and synthetic phases of photoreceptor membrane turnover. The effects of these daily adaptive changes on photon capture ability are discussed with regard to the sensitivity of the eye.     

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.     

Internal extraocular photoreceptors in a dipteran insect

Within the head capsule of the moth-fly Psychoda cinerea, underlying each of the two compound eyes, are two internal ocelli of different sizes. There are seven photoreceptor cells in Ocellus I and two in Ocellus II. The internal Ocellus I appears clearly different from the retina of the compound eye, by different rhabdom structure, different size of pigment granules and different stability of these pigments to solvents. Ocellus II does not contain any pigment granules. The physiological activity of these photoreceptors is indicated by their well-developed axons, the rhabdom structure, organelles produced by membrane reorganization, and Actaptation phenomena. The internal ocelli are former larval stemmata that have been displaced inward during metamorphosis. Presumably they have a stimulatory action on the CNS, in analogy with the dorsal ocelli, which are lacking in Psychoda. It is plausible to credit the internal ocelli with a photosensitive role in the functional complex of pacemakers and circadian rhythm.     

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.     

The ultrastructure of the uterine epithelium of the pig during the estrous cycle and early pregnancy

Summary In the compound eye of the moth Antheraea polyphemus, three types of visual pigments were found in extracts from the retina and by microspectrophotometry in situ. The absorption maxima of the receptor pigment P and the metarhodopsin M are at (1) P 520–530 nm, M 480–490 nm; (2) P 460–480 nm, M 530–540 nm; (3) P 330–340 nm, M 460–470 nm. Their localization was investigated by electron microscopy on eyes illuminated with different monochromatic lights. Within the tiered rhabdom, constituted of the rhabdomeres of nine visual cells, the basal cell contains a blue-and the six medial cells have a greenabsorbing pigment. The two distal cells of most ommatidia also have the blue pigment; only in the dorsal region of the eye, these cells contain a UV-absorbing pigment, which constitutes a portion of only 5% of the visual pigment content within the entire retina. The functional significance of this distribution is discussed.     

Evolution of color vision in pierid butterflies: blue opsin duplication,ommatidial heterogeneity and eye regionalization in <Emphasis Type="Italic">Colias erate</Emphasis>

This paper documents the molecular organization of the eye of the Eastern Pale Clouded Yellow butterfly, Colias erate (Pieridae). We cloned four cDNAs encoding visual pigment opsins, corresponding to one ultraviolet, two blue and one long wavelength-absorbing visual pigments. Duplication of the blue visual pigment class occurs also in another pierid species, Pieris rapae, suggesting that blue duplication is a general feature in the family Pieridae. We localized the opsin mRNAs in the Colias retina by in situ hybridization. Among the nine photoreceptor cells in an ommatidium, R1-9, we found that R3-8 expressed the long wavelength class mRNA in all ommatidia. R1 and R2 expressed mRNAs of the short wavelength opsins in three fixed combinations, corresponding to three types of ommatidia. While the duplicated blue opsins in Pieris are separately expressed in two subsets of R1-2 photoreceptors, one blue sensitive and another violet sensitive, those of Colias appear to be always coexpressed.     

THE DEVELOPMENT OF PIGMENT GRANULES IN THE EYES OF WILD TYPE AND MUTANT DROSOPHILA MELANOGASTER

The eye pigment system in Drosophila melanogaster has been studied with the electron microscope. Details in the development of pigment granules in wild type flies and in three eye color mutants are described. Four different types of pigment granules have been found. Type I granules, which carry ommochrome pigment and occur in both primary and secondary pigment cells of ommatidia, are believed to develop as vesicular secretions by way of the Golgi apparatus. The formation of Type II granules, which are restricted to the secondary pigment cells and contain drosopterin pigments, involves accumulation of 60- to 80-A fibers producing an elliptical granule. Type III granules appear to be empty vesicles, except for small marginal areas of dense material; they are thought to be abnormal entities containing ommochrome pigment. Type IV granules are characteristic of colorless mutants regardless of genotype, and during the course of development they often contain glycogen, ribosomes, and show acid phosphatase activity; for these reasons and because of their bizarre and variable morphology, they are considered to be autophagic vacuoles. The 300-A particles commonly found in pigment cells are identified as glycogen on the basis of their morphology and their sensitivity to salivary digestion.     

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.     

A crustacean compound eye adapted for low light intensities (Isopoda)

Summary The optical performance of the apposition compound eye of the marine isopodCirolana borealis Lilljeborg (Crustacea) was investigated. The ommatidia comprise large lenses (diam. ca. 150 m), spherical crystalline cones and hypertrophied rhabdoms. The 7 rhabdomeres are fused distally and open proximally. We have designated this rhabdom type as semifused. Distal pigment cells screen neighbouring ommatidia, and a well developed reflecting pigment layer surrounds the rhabdom. The focal length was determined in situ and refractive index measurements, raytracings, and eye mappings were made. The focus was found to lie well below the distal rhabdom tip. A theoretical acceptance function was constructed and a 50% acceptance angle of 45 ° was estimated. The eye parameter (p, according to Snyder 1977) of different ommatidia was between 44 and 14. This together with the anatomy demonstrate an optimation to extremely low light intensities. TheCirolana eye provides an example where acuity is sacrificed for the eye to be able to see at the low light intensities of the inhabitat.The investigation has been supported by a grant from the Swedish Natural Science Research Council (grant no. 2760-103). Our thanks are due to the staff of the marine biological station in Espegrend (Norway). The skilled technical assistance of Miss Inger Norling, Mrs. Rita Wallen, and Miss Maria Walles is gratefully acknowledged. And finally, we would like to express our deep appreciation to Professor Rolf Elofsson for constructive discussions and for his interest and encouragement throughout the investigation.     

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.     

The physical and morphological properties of the pigment screen in the compound eye of a shrimp (Crustacea)

Summary The pigment cells of the compound eye of the shrimps (Crangon crangon andC. allmani) were studied by electron microscopy (SEM and TEM) and microspectrophotometry. The compound eyes of these species contain light-absorbing and -reflecting pigments contained in granules, located in 5 different cells. The light absorbing pigment granules (light screen) are situated in (1) the distal pigment cells, (2) the retinular cells, (3) the basal pigment cells. The reflecting pigment granules are located in (4) the distal, and (5) the proximal reflecting pigment cells. Another innominate cell type investing the ommatidia contains vacuoles without pigment content. The innominate cell type, and the basal absorbing pigment cell (3) listed above, have not earlier been reported for a crustacean species. Measurements of the spectral absorption on sliced and squashed ommatidia show that all components of the light screen have an increased absorption in the wavelength regions 400–450 nm and 530–570 nm, probably due to xanthommatin and ommin. The spectral absorbancy of the reflecting pigment cells were not determined. Similar cells in other species are known to contain pteridines.We thank Prof. Dr. Langer, Bochum, Germany, for his kind help. The work was supported by funds from the Karolinska Institutet to Doc. G. Struwe, and grant NFR No. 2760-007 to Doc. R. Elofsson.     

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.