Ultrastructural investigations of presumed photoreceptive organs in two Saccocirrus species (polychaeta,saccocirridae)

In addition to the pigmented ocelli, four different types of photoreceptor-like organs without shading pigment have been found in Saccocirrus papillocercus and S. krusadensis. The sensory cells of these presumed ocelli are either ciliary or rhabdomeric with ciliary rudiments. With the exception of the multicellular type-2 ocelli they are bicellular consisting of a sensory cell and a supportive cell. In each ocellus the supportive cell forms a thin cup-shaped envelope around the sensory elements. In the type-2 ocellus, 7 supportive cells form an ovoid cavity leaving openings through which dendritic processes of an equal number of sensory cells enter the cavity. The pigmented ocelli possess an ocellar cavity communicating with the exterior through a pore in the eyecup, ciliary rudiments in both sensory and supportive cell, and additional non-photoreceptive sensory cells in the opening of the eyecup. The sensory organs show characteristic differences between the two species, such as presence or absence of a particular type of ocellus (type 2 is absent in S. krusadensis, type 3 in S. papillocercus), number of cilia in type-4 ocelli, density of microvilli, number of non-photoreceptive sensory cells in the pore of the pigmented ocellus, etc. These differences provide important characters which can be used for discrimination either of species or of subgeneric taxa in Saccocirrus. The phylogenetic significance of the different photoreceptive organs is discussed.     

Ultrastructure of Presumed Ocelli in Parenterodrilus taenioides (Polychaeta,Protodrilidae) and their Phylogenetic Significance

Abstract Three different types of presumed unpigmented ocelli have been found in the anterior end of Parenterodrilus taenioides, a small gutless interstitial polychaete. The type-1 ocelli are located in the palps and four ocelli have been found along the length of each palp. The type-2 and type-3 ocelli lie close together in the head segment and are located in posterior ganglionic expansions of the brain. There is one pair of the minute type-2 ocelli but at least two pairs of the type-3 organs, which are the largest ocelli. In each ocellus the sensory cells are of the ciliary type and possess two cilia whose plasma membranes branch into numerous microvilli. With the exception of the type-1 ocelli they consist of a sensory cell and a supportive cell. In each ocellus the supportive cell forms a thin cup-shaped envelope around the densely packed ciliary branches. The type-1 ocelli consist of a single cell forming an intracellular vacuole (phaosome) which contains less densely packed microvillus-like structures. In particular, the structure of these ocelli is compared with that in other polychaetes, with special emphasis on the remaining genera of the Protodrilida.     

The fine structure of photoreceptors in a marine flatworm

Summary The ocelli or eyes of the marine polyclad turbellarian Notoplana acticola are clustered on the paired dorsal nuchal tentacles and in two longitudinal bands lateral to the cerebral ganglion. The ocelli, studied by electron microscopy, were characterized as rhabdomeric and non-ciliary in origin. There are 60 to 80 ocelli per animal each enclosed in a fibrous capsule to which muscle fibers may attach. An ocellus consists of a pigmented eyecup into which 30 to 50 photoreceptor cells send dendritic processes through interruptions in or among pigment cell projections across the eyecup opening. The dendritic processes terminate in numerous long intertwined microvilli which fill the eyecup. The nucleated cell body of each photoreceptor cell lies outside the eyecup and projects an axonal process to the cerebral mass. Within the dendritic processes are observed mitochondria, ribosomes, neurotubules, multivesicular bodies, vesicles and vacuoles. The cell body contains smaller mitochondria, endoplasmic reticulum, ribosomes, vesicles and prominent Golgi complexes.After dark adaptation, there are some structural alterations in terms of swelling of microvilli, increased numbers of vacuoles associated with the microvilli and dendritic processes, and changes in the pigment cell projections.This work was supported by Grant No. GM 10292 from the U.S. Public Health Service to Professor Richard M. Eakin, Department of Zoology at the University of California, Berkeley, U.S.A., where this investigation was conducted during the author's sabbatical leave of absence from the University of Illinois, and by Grant No. 1 SO 1 FR 5369 from the U.S. Public Health Service to the University of Illinois at the Medical Center.I express appreciation to Professor Eakin for interesting discussions and generous hospitality to me as a guest in his laboratory, and to the John Simon Guggenheim Memorial Foundation for the Fellowship which I held during 1964–65. I thank Dr. John P. Marbarger, Director of the Aeromedical Laboratory for the electron microscope facilities used at the University of Illinois.     

The fine structure of the lateral ocellus of the dobsonfly larva

The lateral ocelli of the dobsonfly (Protohermes grandis, Neuroptera) larva have been examined with light and electron microscopy. The larva has six ocelli on both sides of the head, each containing a single corneal lens. A conical crystalline body, of some 10–20 cells is situated immediately posterior to the lens. From 100 to 300 elongated retinular cells are arranged perpendicular to the crystalline body except at the innermost surface of the lens, where they are absent. The distal process of each retinular cell is enclosed by a tube-like rhabdom formed by the close association of microvilli from the same and adjacent distal processes. The distal process contains many mitochondria, multivesicular bodies, microtubles and pigment granules. In the dark-adapted ocellus the pigment granules are concentrated near the nucleus which lies under the rhabdomic layer. The granules diffuse toward the rhabdomic microvilli during light adaptation. Each retinular cell has a single axon, which extends from the ocellus as an ocellar nerve fiber into the optic lobe, where it frequently synapses upon second order neurons. In addition to these afferent synapses, there are two other synaptic combinations: (1) a feedback synapse from a second order neuron to a retinular axon, and (2) a synapse between second order neurons. These results suggest that photic signals reach the more proximal part of the brain via second order neurons after some degree of integration in the optic lobe.     

Remodeling of the Nauplius Eye into the Adult Ocelli during Metamorphosis of the Barnacle, Balanus amphitrite hawaiiensis

The planktonic barnacle larva has a single median ocellus (nauplius eye), while the adult possesses two distinct sets of photoreceptors; a pair of lateral ocelli and a single median ocellus. The nauplius eye of the cypris larva of Balanus amphitrite hawaiiensis is composed of 14 visual cells grouped into three components (a pair of lateral components and a single ventral component) surrounding two centrally located pigment cells; each lateral component consists of 5 visual cells and the ventral component, 4 visual cells. In each component, the rhabdom is made up of apposing microvilli arising directly from the neighboring visual cell bodies.
During metamorphosis into the adult form, the three components of the median ocellus become separated. Each lateral component migrates laterally on the mantle and is remodeled into the adult lateral ocellus, losing two visual cells but gaining new pigment and tapetum cells in the process. The ventral component remains in the mid portion and becomes the adult median ocellus without fundamental modification in composition. The visual cells in both ocelli undergo a marked increase in volume and form many finger-like dendrites. Rhabdomes are made up of interdigitating microvilli arising from the the dendrite tips.     

The micromorphology of the nauplius eye of the estuarine calanoid copepod, Sulcanus conflictus Nicholls (Crustacea)

The nauplius eye consists of one median and two lateral ocelli, each within a pigment cup. The three pigment cups are made up from two multi-nucleate pigment cells: each cell forming one lateral cup and half of the median cup. The three cups are lined on the insides by tapetal cells which contain layers of reflectile crystals. Each of the ocelli contains six sensory cells which protrude from the rims of the pigment cups and the protruding parts are sheathed by the conjunctiva cells. The whole eye is enveloped by a thin membrane which also sheaths the proximal parts of the five nerve bundles that leave the eye. All the sensory cells of the lateral ocelli are similar and have rhabdomeric microvilli on the terminal end, and contain phaosomes and a multitude of other organelles and cytoplasmic inclusions. The complex median ocellus contains a superior group of three retinular cells, linked by interdigitating processes, and an inferior group consisting of a large central cell enclosed in two cup-shaped peripheral retinular cells. A two-tiered rhabdome arrangement exists, with a rather complex inferior rhabdome set made up of a central rhabdomere and two hemi-annulate rhabdomeres. The cytoplasm of the retinular cells of the median ocellus lack phaosomes but instead contain double-walled tubular elements, possibly formed by the inpushings of microvilli into adjacent cells. The possible functional significance of the unique arrangement seen in the median ocellus is discussed. The retinular cells are of the inverse type. There are no efferent nerve fibres from the brain nor any nervous connection between the lateral and the median ocelli.     

Fine structure of eyespots in tornarian larvae (Phylum: Hemichordata)

Summary The eyespots of tornariae of enteropneusts (Ptychodera flava from Hawaiian waters and an unknown species from southern California) were studied by electron microscopy. An ocellus is composed of two types of cells: sensory and supportive. The former is characterized by a bulbous cilium (with 9+2 axoneme) at its distal end, one or sometimes two arrays of microvilli from its sides below the cilium, and a basal axon. The latter features large, clear vesicles which presumably contained the reddish-orange pigment seen in the ocellus of a living larva. Five-day old tornariae of P. flava are positively phototactic. Both cilium and microvilli may function as photoreceptors. The tornarian ocellus studied is compared with eyespots of other invertebrates, and the evolutionary significance of its putative photoreceptors is discussed.We acknowledge the kind assistance of Drs. Michael G. Hadfield, University of Hawaii, and Russel L. Zimmer, Santa Catalina Marine Biological Laboratory, and the support of grant 10292 from the USPHS.     

Cytochemical localization of acid phosphatase in light- and dark-adapted eyes of a polychaete worm,Nereis limnicola

Summary The amount and distribution of the lysosomal enzyme acid phosphatase in light- and dark-adapted eyes of the brackish-water annelid Nereis limnicola were studied by standard cytochemical techniques. Precipitate from the acid phosphatase reaction was observed in Golgi-endoplasmic reticulum-lysosomal complexes, primary lysosomes, and secondary lysosomes, formed by fusion of primary lysosomes with phagocytic and pinocytic vesicles containing products of presumed rhabdomeric degradation. The acid phosphatase reaction occurred in these organelles in both sensory and supportive cells of both light- and darkadapted ocelli. Secondary lysosomes were more abundant in sensory cells of illuminated ocelli than in those maintained in the dark. Sparse reaction product was found in Golgi cisternae, none in rough endoplasmic reticulum. We suggest that the increase of lysosomal activity in light-adapted eyes is correlated with the breakdown of photosensory microvilli upon exposure to light. A diagram of our interpretation of recycling of photoreceptoral membrane in N. limnicola is presented.     

CELLULAR MOVEMENT IN THE CENTRIC DIATOM ODONTELLA SINENIS1

Cultured, actively growing cells of Odentella sinensis secrete mucilage, forming gelatinous masses; the mucilage can be visualised with Alcian Blue. When examined live with the light microscope, many cells exhibited continuous small shuffing and rocking movements that could last for long periods (30-40 min); the cells, however, were not translocated and remained relatively fixed in position with respect to their neighbours. Ultrastructural examination of these cells showed prominent aggregations of mucilage vesicles, derived from the Golgi bodies, at the base of the labiate processes, each of which is close to an elevation bearing an ocellus. In Ditylum brightwellii, similar aggreations of these vesides were also located at teh labiate processes; this diatom, too, secretes mucilage but does not have ocelli. We conclude that the movements observed in O. sinenisis are an indirect result of active muilage secretion through the labiate process. It has been suggested that the raphe may have evolved from the labiate process; our conclusion, therefore, has phylogenetic implications, suggesting a functional as well as a morphological relationship between the two valve structures.     

Disruption of insect photoreceptor membrane by divalent ions: Dissimilar sensitivity of light- and dark-adapted mosquito rhabdomeres

Summary The conditions that lead to the formation of myelin figures in rhabdomere microvilli were studied in the larval ocelli of the mosquito Aedes aegypti. These artifacts can result from the addition of divalent ions, such as Ca²⁺, to primary-aldehyde fixatives, but they form subsequently during postfixation with OsO₄. In light-adapted ocelli, myelin figures are concentrated at the proximal ends of the microvilli along the cytoplasmic margin of the rhabdomere. The severity of the artifact is proportional to the ion concentration: scattered myelin whorls are induced by Ca²⁺ concentrations as low as 5 mM; they become abundant at 15 mM to 25 mM, and displace much of the rhabdomere margin at 50 mM. In contrast, even at high concentrations of Ca²⁺ few membrane whorls form in dark-adapted rhabdomeres, and these are mostly located at the distal ends of the microvilli. The differential response of the rhabdomere microvilli in light and darkness does not result from a direct action of light during fixation; it reflects an underlying difference between light- and dark-adapted photoreceptor membranes. We suggest that this differential sensitivity to divalent ions is associated with the shedding of membranes from the rhabdomere, a process that is enhanced by light and reduced in darkness.This work was supported by a grant (BNS 76-18623) from the National Science Foundation     

Ocellus variation and possible functions in the genus Neobythites (Teleostei: Ophidiidae)

Based on the examination of almost 1200 specimens representing 50 species of the secondary deep-sea fish genus Neobythites (family Ophidiidae), this study provides an overview of body coloration and a detailed comparison among species that have typical ocelli or eyespots consisting of a dark spot surrounded by a contrasting pale ring on their dorsal fins. Special interest concerns the possible functions of ocelli as antipredator and social signaling devices and the hypothesis that species differences in ocellus size and position are more pronounced in areas of overlap. Color patterns were found in 78% and ocelli in 44% of the Neobythites species. The 22 ocellus-bearing species occur at shallower depths than those without. Ocellus number varied between one and four ocelli with single-ocellus-bearing species reaching shallower minimum depths than those with multiples. Variation in both ocellus size and position was found among co-occurring species with a single ocellus. For instance, the Northern Indian Ocean population of N. stefanovi differs in ocellus position from the co-occurring N. steatiticus, while the allopatric Red Sea population of N. stefanovi does not. This evidence of character displacement is also supported by the marked difference in ocellus position and size between two specimens of N. meteori that were collected widely separated from each other and co-occurring with two other single-ocellus-bearing species in the Pacific and Indian Ocean, respectively. Ocelli in Neobythites may therefore serve antipredator as well as social communication functions.     

Fine structure of the cerebral ocelli of a sipunculid,Phascolosoma agassizii

Summary The brain ofPhascolosoma agassizii, a sipunculid worm, contains a pair of ocelli. Each ocellus lies at the inner end of the ocular tube, an invagination that connects the concavity of the ocellus with the anterior surface of the head. The cuticle which covers the epidermis of the worm extends into and lines the ocular tube. The cells of the neck of the tube are columnar and contain longitudinally oriented tonofilaments extending into microvilli that project into the cuticle in the tube. Cilia also project from the apices of these cells. Toward the base of the ocular tube are two kinds of columnar cells: supportive and photoreceptive. The supportive cells contain varying concentrations of melanin-like granules forming the pigmented component of the ocellus. Numerous longitudinally oriented tonofilaments in these cells extend into microvilli projecting into the cuticular layer. The photoreceptor cells, containing many microtubules, lie between the supportive cells and spread out at their tips giving off an irregular array of miorovilli, the presumed photoreceptors, and cilia. These photoreceptors are regarded as belonging to the rhabdomeric type, albeit cilia are present.This investigation was financed by grant number GM 10292 from the National Institute of General Medical Science.     

Fine structure of the dorsal ocellus of the worker honeybee

The three dorsal ocelli of worker honeybees have been studied by light and electron microscopy. Each ocellus has a single flattened spheroidal lens and about 800 elongated retinular cells. Retinular cells are paired and form a two-part plate-like rhabdom between their distal processes. Each rhabdomere comprises parallel microvilli projecting laterally from the apposed retinular cells. Primary receptor cell axons synapse within the ocellus with ocellar nerve fibers of two different calibers. Each ocellus has eight thick fibers ca 10 m?m in diameter and several thinner ones less than 3 m?m in diameter. Fine structural evidence suggests that retinular axons end presynaptically on both types of ocellar nerve fibers. Since all retinular cells apparently synapse repeatedly with the thick fibers this involves a convergence of about 100:1. Thick fibers always terminate postsynaptically within the ocellus while thin fibers terminate presynaptically on other thin fibers, thick fibers or retinular axons. Structural evidence for synaptic polarization indicates that retinular cells and thick fibers are afferent, thin fibers efferent. Thus complex processing of the ocellar visual input can occur before the secondary neurons of the three ocelli converge to form the single short ocellar nerve which runs to the posterior forebrain.     

Interneurones subserving ocelli in two species of trichopterous insects: morphology and central projections

Summary The central projections of ocellar interneurones in two species of trichopterous insects Agrypnia varia F. and Limnephilus flavicornis F. were analysed by use of cobalt iontophoresis. The interneurones were classified into three groups: large-, medium- and small-caliber neurones based on the diameters of the axons. Seven large-diameter neurones project from each lateral ocellus into the central nervous system. Of these, four neurones terminate in the posterior slope (three ipsilateral and one contralateral). Three neurones possess branches in the contralateral posterior slope and proceed down the cervical connective into the thoracic ganglia. Medium-sized neurones connect the neuropiles of the three ocelli to each other. Small-diameter neurones contact the contralateral lobula and medulla of the optic lobes and connect the three ocellar neuropiles. Large-diameter neurones of the median ocellus were found to terminate bilaterally or ipsilaterally in the posterior slope. In the posterior slope four different subregions can be recognised: (1) the dorso-lateral, (2) the ventro-lateral, (3) the lateral, into which large-diameter interneurones of the lateral ocelli send branches, and (4) the medial, innervated by interneurones of the median ocellus. Interneurones of the median ocellus send branches into the lateral region as well.     

Fine structure of the eyes of Pseudoceros canadensis (Turbellaria,Polycladida)

Summary The cerebral and epidermal ocelli of the Müller's larva and the cerebral and tentacular eyes of the adult turbellarian Pseudoceros canadensis were studied by electron microscopy. The right cerebral ocellus of the larva consists of one cup-shaped pigmented cell and three sensory cells that bear microvilli. The left cerebral eye of the larva has the above named cells plus a sensory cell with many cilia. Evolutionary significance is attributed to the presence of both ciliary and microvillar photoreceptors in an eye of a flatworm. The one epidermal ocellus of the larva is composed of two cells: a cup-shaped pigmented one bearing flattened cilia, the presumed photoreceptors, and a cell above the cup that adds a few nonciliary lamellae to the stack of ciliary ones from the pigmented cell. The adult eyes contain only microvillar receptors; cilia were not observed.     

Fine structure of ocelli in larvae of an archiannelid,Polygordius cf. appendiculatus

Summary The ocelli of trochophore and segmented larvae of the archiannelid Polygordius cf. appendiculatus were studied by electron microscopy. An eye consists of two pigmented supportive cells forming an eyecup that encloses one sensory cell bearing one (trochophore) or two (segmented larva) ranks of microvilli and one adventitious cilium. Remarkably abundant tubules (submicrovillar endoplasmic reticulum) radiate from the perinuclear region of the sensory cell, which lies outside the ocellus, toward its receptoral end. Possible functions of the tubules are proposed: carriers of ions, metabolites and photopigments; pinocytic uptake of products resulting from photoreception; storage of membrane; and light guides. Finally, the eyes of Polygordius larvae are believed to have evolutionary significance and provide further support for Eakin's theory of diphyletic origin of photoreceptors.     

Fine structural organization of the lateral ocelli in two species of Scolopendra (Chilopoda: Pleurostigmophora): an evolutionary evaluation

The lateral ocelli of Scolopendra cingulata and Scolopendra oraniensis were examined by electron microscopy. A pigmented ocellar field with four eyes arranged in a rhomboid configuration is present frontolaterally on both sides of the head. Each lateral ocellus is cup-shaped and consists of a deeply set biconvex corneal lens, which is formed by 230–2,240 cornea-secreting epithelial cells. A crystalline cone is not developed. Two kinds of photoreceptive cells are present in the retinula. 561–1,026 cylindrical retinula cells with circumapically developed microvilli form a large distal rhabdom. Arranged in 13–18 horizontal rings, the distal retinula cells display a multilayered appearance. Each cell layer forms an axial ring of maximally 75 rhabdomeres. In addition, 71–127 club-shaped proximal retinula cells make up uni- or bidirectional rhabdomeres, whose microvilli interdigitate. 150–250 sheath cells are located at the periphery of the eye. Radial sheath cell processes encompass the soma of all retinula cells. Outside the eye cup there are several thin layers of external pigment cells, which not only ensheath the ocelli but also underlie the entire ocellar field, causing its darkly pigmented. The cornea-secreting epithelial cells, sheath cells and external pigment cells form a part of the basal matrix extending around the entire eye cup. Scolopendromorph lateral ocelli differ remarkably with respect to the eyes of other chilopods. The dual type retinula in scolopendromorph eyes supports the hypothesis of its homology with scutigeromorph ommatidia. Other features (e.g. cup-shaped profile of the eye, horizontally multilayered distal retinula cells, interdigitating proximal rhabdomeres, lack of a crystalline cone, presence of external pigment and sheath cells enveloping the entire retinula) do not have any equivalents in scutigeromorph ommatidia and would, therefore, not directly support homology. In fact, most of them (except the external pigment cells) might be interpreted as autapomorphies defining the Pleurostigmophora. Certain structures (e.g. sheath cells, interdigitating proximal rhabdomeres, discontinuous layer of cornea-secreting epithelial cells) are similar to those found in some lithobiid ocelli (e.g. Lithobius). The external pigment cells in Scolopendra species, however, must presently be regarded as an autapomorphy of the Scolopendromorpha.     

The organization of honeybee ocelli: Regional specializations and rhabdom arrangements

We have re-investigated the organization of ocelli in honeybee workers and drones. Ocellar lenses are divided into a dorsal and a ventral part by a cusp-shaped indentation. The retina is also divided, with a ventral retina looking skywards and a dorsal retina looking at the horizon. The focal plane of lenses lies behind the retina in lateral ocelli, but within the dorsal retina in the median ocellus of both workers and drones. Ventral retinula cells are ca. 25 μm long with dense screening pigments. Dorsal retinula cells are ca. 60 μm long with sparse pigmentation mainly restricted to their proximal parts. Pairs of retinula cells form flat, non-twisting rhabdom sheets with elongated, straight, rectangular cross-sections, on average 8.7 μm long and 1 μm wide. Honeybee ocellar rhabdoms have shorter and straighter cross-sections than those recently described in the night-active bee Megalopta genalis. Across the retina, rhabdoms form a fan-shaped pattern of orientations. In each ocellus, ventral and dorsal retinula cell axons project into two separate neuropils, converging on few large neurons in the dorsal, and on many small neurons in the ventral neuropil. The divided nature of the ocelli, together with the particular construction and arrangement of rhabdoms, suggest that ocelli are not only involved in attitude control, but might also provide skylight polarization compass information.     

Intracerebral ocelli in an amphipod: extraretinal photoreceptors of the sandhopper Talitrus saltator (Crustacea, Amphipoda)

Abstract. No morphological clues on the amphipod head indicate the existence of ocelli. However, as in several isopod species studied so far, two rudimentary photoreceptors are integrated into the medio-dorsal part of the brain. This electron microscopical study of the photoreceptors is the first report on the presence of ocelli in amphipods. Each ocellus is made up of 3 receptor cells which contribute to the formation of a photoreceptive surface (the rhabdom) formed by tightly packed microvilli. The rhabdoms are twisted and irregular in outline. Membrane turnover is suggested by the presence of different kinds of lysosomes. Lacking dioptric lenses, these photoreceptors are not likely to be involved in image formation but may function as appraisers of ambient light intensity. Physiological and behavioral studies will, henceforth, have to take into account these unexpected ocelli, which may represent remnants of the naupliar eye.