Cell junctions and other membrane specializations in the ocellus of the wasp, Paravespula Germanica L. (Hymenoptera : Vespidae)

Int. J. lnsectMorphok &Embryol., Vol. 15, No. 5/6, pp. 331 to 342, 1986. Printed in Great Bri aim

CELL JUNCTIONS

0020 7322/86$3.00; .(30 PergamonJournalsLtd.

AND OTHER MEMBRANE

IN T H E O C E L L U S O F T H E W A S P , P A R A L. ( H Y M E N O P T E R A

SPECIALIZATIONS

VESPULA

GERMANICA

• VESPIDAE).

M. A. PABST and K. KRAL Institute of Histology and Embryology, and Institute of Zoology, University of Graz, Graz, Austria (Accepted 9 Januao' 1986)

Abstract--Five types of cell contacts and other membrane specializations were found in the ocellus of the adult wasp, Paravespula germanica L. (Hymenoptera : Vespidae), based on free;,e-fracture replicas and thin sections. Septate junctions alongside small gap junctions are present between iris cells and between correagenous cells. Gap junctions are sometimes observed between glial cell processes. Photoreceptor cells and glial cells are frequently connected by scalariform junctions. Tight junction-like structures are found on receptor-cell membranes near rhabdomeric microvilli. Desmosomes are widespread in the ocellus, connecting iris cells, corneagenous cells, receptor cells, and glial cell processes. Desmosomes are found next to septate junctions. Glial membranes connected to receptor cells have a non*junctional type of membrane specializations, consisting of intramembraneous particles arranged in a rhombic pattern. Interestingly, both particle arrays and scalariform junctions are often adjacent to each other. Furthermore, a conspicuous modification of the cell surface in freeze cleaved cells is seen between adjacent glial cells intermediating two receptor cells. Index descriptors (in addition to those in title): Wasp ocellus, junctions, membrane specializations, freeze-fracture.

INTRODUCTION

the eyes of Crfistacea, Insecta and Cephalopoda by freeze-fracture (-etch) techniques and/or ultrathin-sectioning, reveal that different kinds of intercellular junctions occur in the retina (e.g. crabs: Eguchi et al., 1982; insects: Eley and Shelton, 1976; Chier al., 1979; Chi and Carlson, :!981; Carlson et al., 1983; cuttlefish: Yamamoto, 1984; Yamamoto and Takasu, 1984). These junctions have functions in membrane biology in sensory reception, and neural signal processing. Knowledge of the spatial distribution of these junctions in the eye enables understanding of the vital chemical and electrical processes involved in vision. For example, the finding that photoreceptor cells are linked by gap junctions (effecting electrical synapses) makes it possible to interpret physiological data arising from lateral interactions of photoreceptors (Lasansky, 1967; Laughlin, 1981; Horridge et al., 1983). In another case, tight-junctional complexes could be the structural basis for the blood-nerve barrier (Lane et al., 1977), while septate junctions could be involved in the turnover of photoreceptor membranes in compound eyes (Waterman, 1982). Studies are still lacking on junctional specializations in insect ocelli, although such structures recently have aroused interest, because their anatomical and physiological STUDIES O[

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features are b e c o m i n g better defined (reviewed by G o o d m a n , 1981). Such data are scant in ocellar systems, e.g. in the cabbage looper moth ocellus (Dow a n d E a t o n , 1976; E a t o n a n d P a p p a s , 1977) a n d in wasp ocellar tract (Kral, 1983) where gap j u n c t i o n - l i k e structures were f o u n d in thin sections. The aim of the present work was to investigate the type, occurrence, a n d d i s t r i b u t i o n of intercellular j u n c t i o n s in the ocellus of the G e r m a n wasp by freeze-fracture technique a n d thin sections. MATERIALS AND METHODS Ocelli of adult wasps, Paravespula germanica were prepared and then fixed in a mixture of 2.5% glutaraldebyde and 2% paraformaldehyde in sodium cacodylate buffer (pH 7.4; 0.05M) with 0.12M saccbarose at.4°C for 1- 2 hr. Tissue was then transferred to a solution of 30% glycerol and mounted on goldcup specimen holders. Ocelli were frozen in liquid propane and fractured in a Balzers BAF 400D freeze-etching apparatus under a vacuum of 10 6 10 7 torr. Fracturing was performed at 100°C.Coating with platinum/carbon films was controlled with a quartz crystal thin-film monitor. Replicas were floated off on distilled water, cleaned in chromic acid, rinsed in distilled water, bathed in sodium bypochlorite and rinsed in multiple change,, of distilled water. Cleaned replicas were mounted on uncoated grids and examined in a Siemens EM 102 transmission electron microscope. For thin sectioning, tissues were fixed for 2 hr in the same fixative as above (pH 7.4; 4°C), postfixed in 1% OsO4 (pH 7.4; 4°C) and embedded in Epon 812. Ultrathin sections were stained with uranyl acetate and lead citrate. RESULTS Three ocelli are located on the vertex of the head in adult wasps. Each ocellus is c o m p o s e d o f a biconvex corneal lens, partially s u r r o u n d e d by a n iris layer ( p i g m e n t a r y cells), c o r n e a g e n o u s cells, and a retina. The retina c o n t a i n s a b o u t 600 p h o t o r e c e p t o r cells of the r h a b d o m e r i c type a n d glial cells. The proximal processes of the receptor cells a n d the secondary n e u r o n e s make up the subretinal neuropile, which is k n o w n to have complex synaptic contacts (Kral, 1979). Intercellular j u n c t i o n s a n d / o r m e m b r a n e specializations in the iris, c o r n e a g e n o u s layer a n d retina were investigated.

Septate junctions Septate j u n c t i o n s are f o u n d between c o r n e a g e n o u s cells (Figs. 1; 2) a n d between iris p i g m e n t cells (Figs. 3; 4). In both cell types, they are usually associated with d e s m o s o m e s or with small gap j u n c t i o n s (Figs. 1 - 3). The septate j u n c t i o n s show ridges on the P-face a n d c o r r e s p o n d i n g grooves on the E-face in freeze-fracture replicas. These ridges extend either loosely a n d u n d u l a t i n g l y , or are closely set and parallel. The i n t r a m e m b r a n o u s particles (4 = 1 0 - 12 nm) m a k i n g up these ridges lie loosely against one a n o t h e r . The frequency a n d extent of the j u n c t i o n a l strands varies c o n s i d e r a b l y from one m e m b r a n e region to the other. In thin sections, the intercellular cleft between 2 c o r n e a g e n o u s ceils (Fig. 2) a n d that between 2 iris cells (Fig. 4) measures 13 - 17 nm. In these clefts, septa with an interspace of 7 - 1 2 n m are observed. Beside bicellular j u n c t i o n s , putative tricellular j u n c t i o n s also exist (Fig. 2).

Gap junctions G a p j u n c t i o n s are f o u n d between iris cells a n d between c o r n e a g e n o u s ceils, where they are frequently f o u n d side by side with septate j u n c t i o n s (Figs. 1 - 3). Sometimes gap j u n c t i o n s are also observed between glial processes. G a p j u n c t i o n s are recognized by an electron-dense intercellular cleft that measures 2 - 4 n m (Fig. 2), a n d in freeze-fracture replicas small circular plaques appear, consisting of u n i f o r m l y sized i n t r a m e m b r a n e o u s particles, which are usually f o u n d on the E-face with c o r r e s p o n d i n g P-face pits. Such particles have a diameter of 11 - 15 nm.

Cell Junctions in the Ocellus of Paravespula germanica

FIG. 1. 1-'reeze-fracture replica of corneagenous cells, connected by septate junctions (arrows). coexisting with gap junctions (arrowheads). Septate junctions appear as ridges on P-face and grooves on E-face. Gap junctions are seen here as aggregates of E-face particles. × 40,000. FiG. 2. Thin section showing septate junctions (thick arrow), gap junctions (arrowhead) and desmosomes (thin arrows) between corneagenous cells. Notice also putative tricellular septate junctions (-*). Desmosomes are mostly near nuclear layer. × 54,000.

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FI(;. 3. Freeze-fracture replica of an iris pigment cell, with septate junctions (arrow) and gap junctions (arrowhead). Gap junctions appear as grooves on P-face. PG - pigment granule. × 60,000 FiG. 4. Thin section of same area as in Eig. 3. Septate junctions (arrows) between iris pigment cells. PG pigment granule. × 75,000

Rhombic particle arrays Large areas of intramembraneous (E-face) particle arrays are only seen on glial membranes adjacent to photoreceptor cells (Figs. 5; 6). These arrays are comprised of particles lying at the intersections of 2 sets of parallel rows of particles. These particle rows are usually well aligned, forming a 2-dimensional lattice with repetitive rhombic units. Center-to-center distances between particles of a row are 1 6 - 2 2 nm and 2 2 - 2 6 nm, and the acute angle is 7 1 - 81 °. Average distances between particles and angle are given in Fig. 7. The E-face particles themselves range from 8 to 10 nm in diameter. Irregularities in the arrangement of the particles sometimes occur. Intramembraneous particles are always associated with the E-face and complementary pits on the corresponding P-face of adjacent receptor cells have not been found. Often particle-free zones between the rhombic particle arrays continue in particle-poor zones in the P-face (Figs. 5; 6; 9). On the other hand, particle-rich zones on the P-face may be correlated with the rhombic particle arrays on the E-face (Fig. 6).

Scalariform junctions Specialized intercellular connections covering large areas could be observed in thin sections between receptor cells and neighboring glial cells (Fig. 8). These structures look like scalariform junctions which have been found binding epithelial cells of different insects (Lane and Skaer, 1980). The intercellular cleft in scalariform junctions has a range of 1 0 - 12 nm and contains striations. The distances between such indistinct septa are

Cell Junctions in the Ocellus of

Paravespula germanica

Ft6. 5. Freeze-fracture image of receptor cells (RC) and intermediating glial cells (GC). On E-face of gila[ merr brahe adjacent to receptor cell membrane a large area of rhQmbic arrays of particles appear (arrow). Note that on P-face of receptor celt membrane, zones with densely packed, irregularly arranged particles and zones with few particles are seen, whereby particle-poor zones often correspond to zones on E-face without rhombic arrays (,It). HS = hemolymph space; PG - pigment granule, x 30,000. Fic;. 6. Higher magnification of rhombic particle arrays on E-face of glia[ cell membrane joined closely to receptor-cell membrane. Particle-rich zones on P-face (,It). x 100,000.

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© © © © FIG. 7. Schematic drawing of a rhombic array of E-face particles (circles). Average distances between particles and angle are given. between 8 and 12 nm. The scalariform junctions could not be definitely identified in freeze-fracture replicas. But as described for scalariform junctions in other tissues, large numbers o f i n t r a m e m b r a n e o u s particles on P-face o f receptor-cell m e m b r a n e are also f o u n d here (Fig. 6). These particles measure 6 - 12 nm and exhibit no obvious regular pattern o f arrangement (see Lane and Skaer, 1980).

Tight junction-like structures A p p a r e n t tight junctional appositions are observed on the P-face (Fig. 9) and E-face (Fig. 10) of receptor-cell membranes in the vicinity of rhabdomeric microvilli. On the P-face, these junctions appear as branching and anastomosing P-face particle strands. Correlative grooves on the E-face also contain some particles. These particles are 8 - 10 nm in diameter. We almost never saw fractures crossing the intercellular space to reveal the 2 m e m b r a n e faces in the region o f a ridge/groove. Furthermore, we could not find these junction-like structures in thin sectioned material.

Desm osomes Desmosomes appear between corneagenous cells, usually near the nuclear layer adjoining the distal retina. They are often f o u n d near septate junctions (Fig. 2). Desmosomes are also present between iris pigment cells, and in the retina between glial processes and between receptor cells. In the latter case, desmosomes occur both between the 2 receptor cells of one pair and between receptor cells o f neighbouring pairs.

Glial membrane specialization A conspicuous modification o f the cell surface is often seen between 2 adjacent glial cell membranes intermediating a pair of receptor cells. Figure 1 1 represents such a peculiar g l i a l - g l i a l intimacy. Note the extremely rough glial membrane. We find it unlikely that this m e m b r a n e specialization is a freezing artifact, as the tissue was pre-fixed and pretreated with 30°70 glycogen; in addition, the neighboring membranes show no modulations. Nothing can as yet be said about its function. DISCUSSION

Septate junctions The same septate junctions, as we have seen between iris pigment cells and between corneagenous cells in the wasp ocellus, also occur in the analogous tissues in the

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compound eye of the housefly (Carlson et al., 1983). There, in each ommatidium the 4 Semper ce!ils (which form the pseudocone) are linked to each other and to primary pigment cells by extensive septate junctions. On the other hand, in the compound eyes of the diurnaL sphingid moth, septate junctions appear between adjacent retinular cells (Eguchi, 1982). The presence of numerous mitochondria alongside these junctions suggests local mobilization of metabolic energy. In contrast, no septate junctions have been observed in the ocellar retina, and the septate junctions in the iris and corneagenous layer of the ocellus have hardly any consistent association with mitochondria. The function of the septate junctions in these regions may be involved in cell-turnover mechanisms, which are important in the iris and corneagenous layer or they could simply serve in intercellular adhesion (Staehelin, 1974).

Gap junctions Gap junctions are present in the iris and corneagenous layer and between glial cells of the wasp ocellus. Recently, gap junctions have also been observed between glial cells in the ocellus of the honey bee (Kral et al., 1985), in the compound eye of flies between glial cells and between photoreceptor-cell axons (Ribi, 1978; Carlson and Chi, 1979; Shaw, 1979, 1984), and in the Astacus retina between tapetum and photoreceptor cells (Winterhager and Stieve, 1982). Based on thin sectioned material, putative gap junctions have been found in the moth ocellus between certain neurones (Eaton and Pappas, 1977) and in the ocellar tract of the wasp between large first-order interneurones (Kral, 1983). These findings point to the fact that gap junctions in ocelli and compound eyes connect excitable a n d / o r no~a-excitable cells. Shaw (1979, 1984) proposes that in visual neurones, the gap junctions might be sites of electrotonic synapses effecting lateral current passage. In glial cells, however, gap junctions may be important for metabolite transfer (e.g., Loewenstein, 1976; Lawrence et al., 1978; Caveney, 1978). Also in the iris and corneagenous layer of the ocellus, it is likely that the gap junctions (in contrast to the septate jutLctions) play a role in metabolic exchange. Rhombic particle arrays Regular arrays of orthogonally directed particles have also been observed in different tissues of various other animals. Such particle arrays have been found, for example, in the central nervous system of ticks, lying on the E-face of glial cells and possibly axons (Binnington and Lane, 1980). There, the E-face particles have a diameter of 16 nm and a center-to-center spacing of approximately 25 nm. These dimensions are of the same order of magnitude as we have found in the rhombic particle arrays. The arrays found in the tick CNS differ, however, from those in the wasp ocellus in 2 essential points. First, they apparentl2~ cover a considerably smaller surface and second, they have pits on the P-face. Probably they are sites of glial - axonal or axo - axonal junctions. Shaw and Stowe (1982) and St.-Marie and Carlson (1982) found relatively dense-packed rhombic particle arrays on the P-~ace of photoreceptor axons of the fly compound eye. These are related to chemical synapses. Rhombic particle arrays have been also found in muscle and nerve cells of freshwater planaria (Quick and Johnson, 1977), in crayfish nerves (Peracchia, 1974) and in Aplysia smooth muscles (Prescott and Brightman, 1976). In all 3 cases, the particles are not, however, found on the E-face but on the P-face of the membranes. Only Quick and Johnson (1977) have been able to see particle arrays on the P-face corresponding to pits on the E-face in planaria. The auth~ s therefore speculate that these

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FIG. 8. Thin section of 2 receptor-cells (RC) and intermediating glial cell (arrowhead). Arrows point to scalariform junctions. × 120,000. FIo. 9. Freeze-fractured tight junction-like structures (arrow) on P-face of receptor-cell membrane (RC) in vicinity of rhabdomeric microvilli (My). Note that P-face particles can be in irregular rows on ridges. GC - glial cell membrane with rhombic particle arrays, x 45,000. Flo. 10. Freeze-fractured tight junction-like structures (arrow) on E-face of receptor-cell membrane (RC); My - rhabdomeric microvilli. × 45,000.

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arrays may be a special kind of gap junction. In muscle cell membranes of the earthworm, highly ordeced arrays of particles on the P-face have also been demonstrated (Rosenblut, 1978). Here, the diagonally oriented rows of particles have grooves on the E-face. This author interprets these particles as myoneural junctions. These results show that ordered particle arrays can occur either on the P-face or on the E-face of cell membranes and that some of them also have corresponding pits on the other leaflet. It is also seen that ordered particle arrays are widespread among invertebrates, and that they can mainly be observed in excitable cells, including photoreceptor cells of insects. At least in places where they serve as putative junctions, some authors (Quick and Johnson, 1977; Lane and Skaer, 1980) believe that these junctions somehow affect the electrical properties of nerve and muscle membranes. The non-junctional arrays on the other hand may permit ionic or metabolic exchange between cells (for a review see Lane and Skaer, 1980). In view of the frequency and distribution of these particle arrays in the retina of tlae wasp ocellus, we assume that there is a specific ion (Ca 2÷)- molecule exchange between glial cells and adjacent photoreceptor cells, an exhange that is possibly important for the photosensory reaction (see, e.g. Stieve, 1977).

Scalariform junctions Extended junctions with a regularly spaced striated intercellular cleft have been found between receptor cells and adjacent glial cells, based on thin sectioned material. Heretofore, such junctions have been observed in rectum and secretory tissues of different insects (e.~. Gupta and Berridge, 1966; Berridge and Gupta, 1967; Fain-Maurel and Cassier, 1972; Bode, 1977; Lane, 1978; Noirot-Timoth6e et al., 1979; Noirot-Timoth6e and Noirot, 1980). In these tissues, the scalariform junctions are associated with mitochondvia either over the whole length of the junctional zone (Type I) or only over a part of it (Type II). In the wasp ocellus, there is an incomplete association of mitochondria and junction. As such, the mitochondria of Type II are less precisely positioned (according to Lane and Skaer, 1980). However, in earlier freeze-fracture studies, it has been difficult to identify all these structures (Lane, 1978, 1979; NoirotTimoth6e et al., 1979). The non-junctional rhombic arrays of particles, are certainly not correlates of the scalariform junctions. The intramembraneous particles of these rhombic arrays haw.• no complementary pits on the neighbouring membrane, unlike the situation described in planaria (Quick and Johnson, 1977). Furthermore, the distances between the E-face particles of the rhombic arrays are somewhat larger than the distances measured between the intercellular columns of the scalariform junctions. Scalariform junctions as described by other authors (Lane, 1978, 1979; Noirot-Timoth6e et al., 1979), depict large numbers of P-face particles in an irregular pattern or arrangement, and complementary pits on the E-face are less easily seen. This finding agrees with our observations on this junctional area. Lastly, scalariform junctions differ both in their freeze-fracture and thinsectioned appearance from that of the septate junctions. In the latter technique, intercellular striations of the scalariform junctions are less defined and precisely spaced as the septa of the septate junctions. The spatial association of the scalariform junctions with mitochondria suggests that the junctions may be involved in the transport of A T P (Berridge and Gupta, 1968). ATP, however, is necessary for active ion transport across photosensory membranes (see e.g. Stieve, 1977). Tight juncNon-like structures In the wasp ocellus, tight junction-like structures are found on receptor cells near

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FIG. 11. Freeze-fracture replica of 2 adjacent glial cells (GC) between 2 receptor cells (RC). Arrow points to conspicuous modification of glial membrane. This rough membrane structure is only found between 2 glial cells, x 40,000.

rhabdomeric microvilli. The P-face ridges run irregularly and often in loops and circles and it seems that these ridges are, in addition, covered with irregularly arranged particles. Tight junctions have been found in the glial layer of the fly compound eye (Lane, 1981). Actually, tight junctions are also characteristic in many regions of the optic lobe of flies where they lie between neurones, between neurones and glial cells, and between glial cells (Chi and Carlson, 1980a,b; St. Marie and Carlson, 1983). Recently, tight junctions have also been reported to occur between visual cells in the porecellanid crab (Eguchi et al., 1982). One of the important functions of the tight junctions is to form the permeability barrier. We suggest that the tight junction-like structures between photoreceptor cells in the ocellus could be kept completely separated by a flexible and non-collapsible junctional system (see Lane and Skaer, 1980). Desm osomes

Desmosomes between all cell types have been found in thin sections of the wasp ocellus. In contrast, no evidence for their presence has been obtained by us, using the freezefracture technique. Their absence has also been noted in other insect tissues (see Lane and Skaer, 1980). These desmosomes are probably significantly involved in cellular adhesion. In conclusion, the junctional relationships between the 4 classes of cell in wasp ocellus we found, are as follows. Homocellular connections in form of (1) desmosomes between receptor cells, glial cells, corneagenous cells and iris cells; (2) gap junctions between glial cells, corneagenous cells and iris cells; (3) septate junctions between corneagenous cells and between iris cells; (4) tight junctions between receptor cells. Heterocellular connections in the form of (1) desmosomes between corneagenous cells and receptor cells;

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A c k n o w l e d g e m e n t s - - W e thank Professor Dr W. Burkl (Department of Histology and Embryology) for his interest and helpful suggestions. The expert technical assistance of Mrs E. Sch6ninkle and Mr R. Schmied is gratefully acknowledged. REFERENCES BERRIDGE, M. J. and B. k. GUPrA. 1967. Fine-structural changes in relation to ion and water transport in the rectal papillae of the blowfly, Calliphora. J. Cell Sci. 2; 89 - 112. BerrlDGE, M. J. and B. k. GUHA, 1968. Fine-structural localization of adenosine triphosphatase in the rectum of Calliphora. J. Cell Sci. 3:17 - 32. BXNNINC;TON, K. C. and N. J. LANE. 1980. Perineurial and glial cells of the tick nervous system: a tracer and freeze-fracture study. J. Neurocytol. 9:343 62. BODE, W. 1977. Die Ultrastruktur der Rektalpapillen von Thrips (Thysanoptera, Terebrantia). Zoomorphology 8 6 : 2.'; 1 70. CARLSON, S. D. and C. CHI. 1979. The functional morphology of the insect photoreceptor. Annu. Rev. Entomol. 24:379 - 416. CARLSON, S. I~., R. L. SI. MARIE and C. CHI. 1983. Interpretation of freeze-fracture replicas of insect nervous tissue, pp. 339 75. In N. J. STRAUSFEID (ed.) Functional Neuroanatomy. Springer, Berlin, Heidelberg, New York. CAVENEY, S. 1978. Intercellular communication in insect development is hormonally controlled. Science ( Wash., D. C.) 199:192 95. CHJ, C. and S. D. CARLSON. 1980a. Membrane specializations in the first optic neuropil of the housefly, Musca domestica L. I. Junctions between neurons. J. Neuroo'tol. 9.: 429 49. CHI, C. and S. D. CARLSON. 1980b. Membrane specializations in the first optic neuropil of the housefly, Musca domestica L. 1I. Junctions between glial cells. J. Neuroo'tol. 9:451 - 6 9 . CHI, C. and S. D. CARLSON. 1981. L a n t h a n u m and freeze fracture studies on the retinular cell junctions in the c o m p o u n d eye of the housefly. Cell Tissue Res. 214:541 52. CHI, C., S. D. CARLSON and R. k. ST MARIE. 1979. Membrane specializations in the peripheral retina of the housefly Musca domestica L. Cell Tissue Res. 198:501 - 20. Dow, M. A. and J. L. EATON. 1976. Fine structure of the ocellus of the cabbage looper moth (Trichoplusia nt). Cell Tissue Res. 171:523 - 33. EATON, J. L. and L. G. PAPPAS. 1977. Synaptic organization of the cabbage looper moth ocellus. Cell Tissue Res. 183:291 - 9 7 . EGUCHI, E. 1982. Retinular fine structure in c o m p o u n d eyes of diurnal and nocturnal sphingid moths. Cell Tissue Res. 223: 2 9 - 42. EGU~"HI, E., T. GOTA and T. H. WATERMAN. 1982. Unorthodox pattern of microvilli and intercellular junctions in regular retinular cells of the porcellanid crab Petrolisthes. Cell Tissue Res. 222:493 - 513. ELEY, S. and P. M. J. SHELTON. 1976. Cell junctions in the developing c o m p o u n d eye of the desert locust Schis~ocerca gregaria. J. Embr)'ol. Exp. Morphol. 36:409 - 23. FAIN-MAUREL, M. A. and P. CASSIER. 1977. Une nouveau type de jonctions: les jonctions scalariformes. Etude ultra~tructurale et cytochimique. J. UItrastruct. Res. 39: 2 2 2 - 38. GOODMAN, L. J. 1981. The organisation and physiology of the insect dorsal ocellar system, pp. 201 - 86. In H. AUTRUM (ed.) Invertebrate Visual Centers and Behavior. Vol. 2. Springer, Berlin, Heidelberg, New York. GUPTA, B. L. and M. J. BERRIDGE. 1966. Fine structural organization of the rectum in the blowfly, Calliphora eryth.,ocephala (Meig.) with special reference to connective tissue, tracheae and neurosecretory innervation in the rectal papillae. J. Morphol. 120:23 - 82. HORRIDGE, G. A., L. MARCELJA, R. JAHNKE and I. MAT~C. 1983. Single electrode studies on the retina of the butterfly Papilio. J. Cornp. Physiol. 150: 2 7 1 - 94. KRAL, K. 1979. Neuronal connections in the ocellus of the wasp (Paravespula vulgaris L.). Cell Tissue Res. 203: 161 - 7 1 . KRAL, K. 1983. Ultrastructural analysis of the ocellar tract of the wasps, Paravespula vulgaris L. and P. germanica L. (Hyrnenoptera : Vespidae). Int. J. Insect Morphol. Embryol. 12:313 20. KRAL, K., H. BRADACS and M. A. PABST. 1985. Freeze-fracture characteristic of the ocellar retina of the honeTbee, Apis mellifica carnica Pollm. (Hymenoptera : Apidae). Int. J. Insect Morphol. Embryol. 1 4 : 6 3 - 73. LANE, N. J. 1978. Intercellular junctions and cell contacts in invertebrates, pp. 673 - 91. In J. M. SrURGESS (ed.) Elect,"on Microscopy, Vol. 3, Proc. 9th Int. Congr. Electron Microsc. State of the Act Imperial Press, Toro:ato, Canada.

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