Fine structure of the anteromedial eye of the liphistiid spider Heptathela kimurai.код для вставкиСкачать
THE ANATOMICAL RECORD 240141-147 (1994) Fine Structure of the Anteromedial Eye of the Liphistiid Spider, Heptathela kimurai AKIRA UEHARA, KIYOKO UEHARA, AND KOICHI OGAWA Department of Biology, Faculty of Science, Kyushu University (A.U.), First Department of Oral Anatomy, Fukuoka Dental College (K.U.), and Department of Anatomy, School of Medicine, Fukuoka University (K.O.), Fukuoka, Japan ABSTRACT Background: The presence of efferent fibers in the anteromedial eye of liphistiid spiders kept in natural daily cycles of illuminance has been reported. However, this report is limited to innervation by the efferent fiber and daily rhabdomal changes, and there have been no detailed ultrastructural accounts of the eye. Methods: The fine structure of this eye was examined by electron microsCOPY. Results and conclusions: The eye consists of a cornea, a lens, a vitreous body, and a retina. The retina contains 13or 14 receptor cells and glial cells. The rhabdoms are distal to the nuclei of the receptor cells. In the distal region of the receptive segment, the rhabdomeres lie in the center of the cell. In the middle region, anisomorphic rhabdoms formed by microvilli from adjacent cells are at the cell periphery. In the proximal region, the rhabdomeres are situated in the center of the cell. The ocellar nerve of the eye runs toward the protocerebrum and enters the posterior part of the first optic ganglion of the secondary eyes. Pigmented cells and nonpigmented cells are observed. The pigmented cells are located in the most lateral of the eye and cover the whole eye. The nonpigmented cells are located in the receptor cell bodies and extend to the origin of the ocellar nerve. They wind to form capillaries filled with electron-dense material. These structures are discussed in comparison with those of other spiders and other chelicerates. o 1994 WiIey-Liss, Inc. Key words: Anteromedial eye, Retina, Rhabdom, Nonpigmented cells, Capillary, Liphistiid spider, Heptathelu kimurai (Chelicerata) The eyes of a few arthropods have been reported to be innervated by efferent fibers; the ventral, median, and lateral eyes of the horseshoe crab, Limulus polyphemus (Fahrenbach, 1969, 1973), the median and lateral eye of the scorpion, Androctonus australis (Fleissner and Schliwa, 1977; Schliwa and Fleissner, 1980), and the anteromedial eye of the liphistiid spider, Heptathela k i m u r a i (Uehara et al., 1993). Fine structure and function of the eyes of Limulus (Fahrenbach, 1975; Barlow et al., 1980; Battelle, 1991; Kass and Barlow, 1992) and the scorpion (Fleissner and Fleissner, 1985,1988)have been well examined. Consequently, it has been shown that the efferent fibers contribute to the circadian sensitivity change and control of transductive membrane turnover in these eyes. Furthermore, with regard to the retinal anatomy and function, there are striking similarities between the Limulus median and lateral eyes and the scorpion median eyes (Fleissner and Fleissner, 1985, 1988). However, in the anteromedial eye of the liphistiid spider, the reports in the literature (Uehara et al., 1993) are limited to innervation by the efferent fiber and the daily rhabdomal changes. There have been no 0 1994 WILEY-LISS, INC. detailed ultrastructural accounts of this eye. Additionally, the liphistiid spider has vestigial segments in its abdomen, poorly developed mandibles, two pairs of book lungs and no tracheae, and seven or eight spinnerets. Because this spider belongs to the suborder Archaeothelae, considered to be a primitive type in the order Araneae, their eyes are interesting subjects for study when considered from a phylogenetic or evolutionary viewpoint. In this study, the fine structure of the anteromedial eye of the liphistiid spider was examined by electron microscopy. The structure and possible function of the anteromedial eye are discussed in comparison with the other eyes of Chelicerata. Received October 4,1993;accepted February 24, 1994. Address reprint requests to Dr. Akira Uehara, who is now at the First Department of Physiology, School of Medicine, Fukuoka University, Fukuoka, 814-01Japan. Dr. Kiyoko Uehara is now at the Department of Anatomy, School of Medicine, Fukuoka University, Jonan-ku, Fukuoka, 814-01Japan. 142 A. UEHARA ET AL. MATERIALS AND METHODS For Scanning Electron Microscopy receptive segment, the receptor cells project rhabdomeral microvilli intracellularly and a rhabdom is Adult female of liphistiid spiders, Heptathela kimu- formed in the center of the cell (Fig. 4a). In the middle rai, were collected in the field in Southern Kyushu, region, the receptor cells extrude microvilli extracelluJapan. The spiders were kept in glass tubes stuffed larly in all directions. The microvilli from adjacent receptor cells form anisomorphic rhabdoms at the cell with moist soil and fed small insects. To observe the gross anatomy of the eyes, the ceph- periphery, and they abut on each other in the rhabdom alothrace of the liphistiid spider was cut away and in various positions. Furthermore, the rhabdomeral fixed for 2 h in 2% glutaraldehyde in 0.1 M cacodylate microvilli are directed variously and do not have a buffer. The specimens were dehydrated in a graded se- fixed orientation. No projections of glial cells are present in this region (Fig. 4b). In the proximal region, ries of acetone rinses and air dried. To examine how the ocellar nerve enters the proto- the rhabdom is situated again in the center of the recerebrum, the ocular tubercle a t the frontal region of ceptor cell. The intermediate segment between recepthe cephalothrace, with the protocerebrum still at- tive segment and receptor cell body is almost absent, tached to the ocellar nerves of four pairs of eyes from and so the upper part of the nucleus can be seen tothe ocular tubercle, was cut away by a sharp blade and gether with the basal part of the receptive segment a pair of microscissors. After removal of the connective (Fig. 412). The receptor cells contain abundant cell organelles. tissue surrounding the samples in the normal physiological saline (217 mM NaC1,5 mM KCl, 4 mM CaCl,, Especially, rough endoplasmic reticulum is well devel1.1 mM MgCl,, 3 mM NaHCO,) (Rathmayer, 1965), oped in the vicinity and inferior portion of the nucleus, they were fixed for 2 h in 2% glutaraldehyde in 0.1 M and it is frequently filled with electron-dense material. cacodylate buffer and postfixed for 2 h in 2%osmium At this level, they are interrupted by glial cells (Fig. 5). tetroxide in the same buffer. After dehydration in a The receptor cell protrudes the axon from its proximal graded series of ethanol rinses, they were immersed in end, and the 13 or 14 axons are assembled in the posisoamyl acetate, and then critical-point dried by using terior of the eye to form the ocellar nerve. The ocellar nerve runs toward the protocerebrum away from the liquid carbon dioxide. These specimens were coated with platinum, and ex- other ocellar nerves of the anterolateral, posteromedial, and posterolateral eyes and enters the posterior amined with a JSM 50-A electron microscope. part of the first optic ganglion of these secondary eyes (Figs. 6a, 6b). For Transmission Electron Microscopy The frontal parts of the cephalothraces of the liphistiid spider were cut out with a sharp blade, fixed for 2 h in 2% glutaraldehyde in 0.1 M cacodylate buffer a t pH 7.3, and postfixed for 2 h in 2%osmium tetroxide in the same buffer. After dehydration through ethanol rinses, specimens were embedded in Epon. Ultrathin sections were stained with uranyl acetate and lead tartrate and examined with a Hitachi H-500 electron microscope. Glial Cells There are two kinds of glial cells in the anteromedial eye: pigmented cells and nonpigmented cells. There are hemocylic spaces among these glial cells. (Fig. 4c; see also Fig. 8b). The pigmented cells are situated in the most lateral part of the eye and envelop the cone cells, the receptor cells, and the nonpigmented cells from the apex of the vitrous body to the initial region of the ocellar nerve. RESULTS However, they do not shield the whole eye. A part of The anteromedial eyes are located in the top of an the receptor cell is not covered by them. Their processes ocular tubercle at the frontal region of the cephalo- project into the receptor cells and the nonpigmented thrace, together with the anterolateral, posteromedial, cells (Fig. 7). and posterolateral eyes. The anteromedial eyes are the The nonpigmented cells are situated under the resmallest of the four pairs of eyes (Fig. 1, arrow). On ceptor cell bodies and extend to the axon hillock of the gross inspection, the live ones appear dark, whereas optic nerve, and their nuclei lie near the receptor cell the anterolateral, posteromedial, and posterolateral bodies. Among the prolongations of the nonpigmented eyes are pale. cells, electron-dense material is observed in some of the capillaries (Fig. 7). In the axon hillock of the optic Dioptric Apparatus nerve, two electron-dense capillaries are observed: one The lens is biconvex, and the posterior surface is is longitudinally sectioned and the other is transmuch more convex than the anterior. It consists of sev- versely sectioned (Fig. 8a, b). Subsequent to the axon eral parallel lamellae of whirled bundles formed by hillock of the optic nerve neither prolongation of the numerous accumulated microfibrils (Fig. 2). Cone cells nonpigmented cell nor capillary can be found (Fig. 5a). that comprise the vitreous body have electron-lucent The nonpigmented cells contain abundant amount of cytoplasm and contain electron-dense material. They filaments, endoplasmic reticulum, mitochondria, and are interdigitated with each other and are attached numerous glycogen granules, but lack pigmented granwith septate junctions. Their intercellular spaces and ules. Their intercellular spaces are often filled with the space between the cornea and cone cells are filled electron-dense material and expanses of the intercelluwith electron-dense material (Fig. 3). lar spaces vary from site to site. Near the receptor cell bodies, the extracellular spaces are narrow and the Receptor Cells plasma membranes are smooth (Fig. 9). Toward the The rhabdoms are distal to the nuclei of the receptor ocellar nerve, projections of the nonpigmented cells cells in the anteromedial eye. In the distal region of the wind to form a capillary. They extrude large numbers ANTEROMEDIAL EYE OF THE LIPHISTIID SPIDER Fig. 1. Scanning electron micrograph of an ocular tubercle (dorsal view). AM, anteromedial eye. x 80. Bar: 0.1 mm. Fig. 2. Transmission electron micrograph of a longitudinal section through the cornea. The lens (L) is made up of concentric lamellae filled with microfibrils. C, cornea; CC, cone cell. x 2,300. Bar: 5 pm. 143 Fig. 3. A longitudinal section of the cornea and cone cells. The cone cells (CC) are interdigitated and attached with septate junctions (SJ). They contain electron-dense granules and their intercellular spaces and the space between the cornea (L) and the granules are filled with electron-dense material. x 15,000. Bar: 1 pm. 1971; Homann, 1971; Uehara et al., 1977; Blest, 1985; Land, 1985; Blest et al., 1990). Although considerable intergeneric diversity is apparent from these studies, much of it can be related phylogenetically and to various modes of life. However, the anteromedial eye of liphistiid spider is so different from these eyes of the DISCUSSION other spiders in structure and the number of receptor The structure of the anteromedial eyes of spiders has cells that it is not comparable with those of the other been well examined for a number of species (Melamed spiders. In the liphistiid spider, the microvilli from adand Trujillo-Cen6z, 1966; Eakin and Brandenburger, jacent receptor cells form an anisomorphic rhabdo- of microvilli into the capillary and they have coated vesicles and microtubules (Fig. 10a). Near the capillary, the projections are attached by adherens junctions, and except for this region, they are attached by a great number of septate junctions (Fig. lob). 144 A. UEHARA ET AL. Figs. 4-6. ANTEROMEDIAL EYE O F THE LIPHISTIID SPIDER meral network in the middle region of the receptive segment, and rhabdomeral microvilli have various orientations that are unlikely to play a role in polarized light detection, and furthermore, the receptive segments are not always shielded by the pigmented glial cells. Especially, this eye is comprised of only 13 or so receptor cells, and this number is extremely small compared with that of the anteromedial eye of the other spiders; e.g., wolf spiders, Lycosa erythrognatha and L. thorelli, have 450 receptor cells (Melamed and Trujillo-Cen6z7 19661, jumping spiders, Phidippud johnsoni and Metaphidippus aenelous, have 800-900 receptor cells (Land, 1969; Eakin and Brandenburger, 19711, and the orb weaver, Argiope amoena, has 400-500 receptor cells (Uehara et al., 1977). From this structural evidence, it might be concluded that this eye does not serve image formation, movement detection, and polarized light detection. However, it is well known that wolf, jumping, and orb web spiders have ultraviolet and green receptors in their anteromedial eyes (DeVoe, 1972, 1975; Yamashita and Tateda, 1978; Blest et al., 1981). Additionally, Limulus has an ultraviolet receptor in the median eye (Wald and Krainin, 1963), which is suggested to be the phylogenetical origin of the anteromedial eye of most spiders (Paulus, 1979). Furthermore, other chelicerates, such as scorpions (Machan, 1968), oplionids (Carricaburu and Munoz-Cuevas, 19851,spider mites (McEnroe and Dronka, 1966), and ticks (Carroll and Pickens, 19871, also have the same receptors. Neocarus texanus, a mite, bears the anterior and posterior ocelli consisting of 20 and 14 receptor cells, respectively, considered to have rather low resolution from structural evidence (Kaiser and Alberti, 1991). Since this number is very similar to that of the anteromedial eye of the liphistiid spider, it is conceivable that the anteromedial eye of the liphistiid spider exhibits a spectral sensitivity to ultraviolet and green light and plays a role in detecting their prey like the ticks (Carroll and Pickens, 1987). Because nonpigmented cells and some capillaries formed by them have rarely been reported in eyes of other spiders and other chelicerates, they are a conspicuous feature in the anteromedial eye of the liphistiid spider. The nonpigmented cells are filamentous and the number of spiral turns they make varies. Therefore, they seem to have features of glia. The capillaries among the nonpigmented cells are filled with electron- - 145 dense material and microvilli protrude into the capillaries; coated vesicles and microtubules are observed in the cytoplasm near them. Therefore, it may be that the capillaries are a storage site of the electron-dense material that are absorbed by the nonpigmented cells. Furthermore, they are considered to be quite different from eccentric and arhabdomeric cells of the eyes of Limulus (Fahrenbach, 19751, scorpions (Schliwa and Fleissner, 19801, harvestman (Schliwa, 19791, Acari (Kaiser and Alberti, 19911, and whip scorpions (MeyerRochow, 1978)because the eccentric and arhabdomeric cells bear distal dendrites that contact retinula cells and, therefore, they are considered to play a role as secondary neurons in the processing of visual information. The nonpigmented cells contain endoplasmic reticulum, mitochondria, abundant free ribosomes, and a small number of coated vesicles, so that it seems likely that the nonpigmented cells produce and excrete secretion. However, the receptor cells overlying the nonpigmented cell contain Golgi apparatus, well-developed endoplasmic reticulum, and expanded endoplasmic reticulum filled with electron-dense material similar to the material in the intercellular spaces of the nonpigmented cells near them. Therefore, the receptor cells seem to be a prominent candidate as the source of the electron-dense material. Since the receptor cells are innervated by efferent fibers (Uehara et al., 19931, it is interesting to speculate that they play a role in the regulation of neural secretion. The apposed plasma membranes of the nonpigmented cells in the vicinity of the capillaries are attached with adherens junction and are considered to play a role in cell attachment. The adherens junctions might contribute to the formation of capillaries. Furthermore, a great number of septate desmosomes are observed between nonpigmented cells and between nonpigmented and pigment cells. Since the septa are linear in tangential sections, this septate desmosome is considered to be of Hydra type that is believed to be a site of firm but flexible intercellular adhesion and have been implicated as permeability barriers (Staehelin, 1974). The septate desmosomes in the liphistiid spider might play a role in protecting the electron-dense material from diffusion into the hemocylic spaces and the intercellular spaces even though the nonpigmented cells undergo drastic changes in shape. ~ Fig. 4. Cross sections of the receptive segment of the receptor cell. (a) Distal region. Rhabdom is located in the center of the cell. x 11,000, Bar: 1 pm. (b) Middle region. Anisomorphic rhabdoms are formed by microvilli from adjacent cells a t the cell periphery. x 12,000. Bar: 1 pm. ( c ) Proximal region. Rhabdom is situated in the center of the cell. The nucleus can be seen together with the rhabdom. The receptor cells are surrounded by pigmented and nonpigmented cells. x 4,700. Bar: 1pm. C, cornea; HC, hemocylic space; N, nucleus of the receptor cell; NP, nonpigmented cell; PC, pigmented cell; RH, rhabdom. Fig. 5. A cross section through the lower part of the receptor cell bodies. The receptor cell contains abundant mitochondria and a welldeveloped web of rough endoplasmic reticulum. Some part of the endoplasmic reticulum is filled with electron-dense material. NP, non- pigmented cell; PC, pigmented cell; RC, receptor cell body. x 5,300. Bar: 1 pm. Fig. 6. (a)Transmission electron micrograph of a cross section of the ocellar nerve. Thirteen receptor axons and three efferent fibers (arrow) are enveloped by the thin sheets of Schwann’s cell. Pigmented cells, nonpigmented cells, and the capillary formed by them are almost nonexistent in this region. In the lower side of the photograph, a part of the first optic ganglion of the secondary eyes is seen. x 4,600. Bar: 1 pm. (b)Scanning electron micrograph of the protocerebrum attached to the ocellar nerves. The ocellar nerve (ON) of the anteromedial eye runs away from the other ocellar nerves of the secondary eyes and enters the posterior part (arrow)of their first optic ganglion (OG). x 290. Bar: 50 pm. 146 A. UEHARA ET AL. Figs. 7-1 0. ANTEROMEDIAL EYE OF THE LIPHISTIID SPIDER ACKNOWLEDGMENTS We are grateful to Drs. H. Tateda and Y. Toh for their valuable discussions. LITERATURE CITED Barlow, R.B. Jr., S.C. Chamberlain, and J.Z. Levinson 1980 Limulus brain modulates the structure and function of the lateral eyes. Science, 210:1037-1039. Battelle, B.-A. 1991Regulation of retinal functions by octopaminergic efferent neurons in Limulus. In: Osborne N.N., and G.J. Chader, eds. Progress in Retinal Research, Vol. 10, Pergamon, Oxford, pp. 333-355. Blest, A.D. 1985 The fine structure of spider photoreceptors in relation to function. In: Neurobiology of Arachnids. Friedrich G. Barth, ed. Springer-Verlag, Berlin, pp. 79-102. Blest, A.D., D.C. O'Carrol, and M. Carter 1990 Comparative ultrastructure of layer 1receptor mosaics in principal eyes of jumping spiders: The evolution of regular arrays of light guides. Cell Tissue Res. 262:445-460. Blest, A.D., R.C. Hardie, P. McIntyre, and D.S. Williams 1981 The spectral sensitivities of identified receptors and the function of retinal tiering in the principal eyes of a jumping spider. J. Comp. Physiol., 145:227-239. Carricaburu, P., and A. Munoz-Cuevas 1985 Regression oculaire et electroretinogramme ches les Opilions. C.R. Seances SOC.Biol. Ses. Fil., 175288-294. Carroll, J.F., and L.G. Pickens 1987 Spectral sensitivity to light two species of ticks (Acarina: Ixodidae). Ann. Entromol. SOC.Am., 80:256-262. DeVoe, R.D. 1972 Dual sensitivities of cells in wolf spider eyes at Fig. 7.A montage of transmission electron micrographs of a longitudinal section through the basalmost layer of the receptor cell bodies and the initiation site of the ocellar nerve. Two kinds of glial cells, pigmented (PC) and nonpigmented cell (NP), are observed. The pigmented cells are located in the most lateral part of the eye but do not cover the whole eye. A part of the receptor cell is not covered by the pigmented cell (double arrow). The nonpigmented cell-bodies are located just beneath the receptor cell bodies and their projections extend downwards to the origin of the ocellar nerve. They whirl and form some capillaries filled with electron-dense material (arrow). In the initiation site of the ocellar nerve, two electron-dense capillaries are observed; one is transversely sectioned and the other is longitudinally sectioned. In the lower left of the photograph, pigmented cells and tapetum cells of the posteromedial eye are seen. x 1,900. Bar: 5 pm. Fig. 8. (a)A longitudinal section of a capillary formed by the nonpigmented cells. The nonpigmented cells extrude microvilli into the capillary. Their intercellular space and the capillary are filled with electron-dense material. PC, pigmented cell. x 9,900. Bar: 1pm. (b) Cross section of a capillary formed by infolding of projections of the nonpigmented cells. HC, hemocylic space; ON, ocellar nerve; PC, pigmented cell. x 13,000. Bar: 1 pm. Fig. 9. A longitudinal section of nonpigmented cells beneath the receptor cell bodies. They run anteroposteriorly in parallel, and their parallel thin intercellular spaces are filled with electron-dense material. N, nucleus of nonpigmented cell. x 19,000. Bar: 0.5 pm. Fig. 10. (a) Oblique section of a capillary. The projections of the nonpigmented cells extrude microvilli into the capillary. Coated vesicles (arrowhead)and microtubules (double arrows) are observed. The projections near the capillary are attached by adherens junction (arrow) and except in the region of the infolding projections are attached with a great number of septate junctions (53). x 25,000. Bar: 0.5 pm. (b) High magnification of septate junctions. ~41,000.Bar: 0.1 pm. 147 ultraviolet and visible wavelengths of light. J. Gen. Physiol., 59: 247-269. DeVoe, R.D. 1975 Ultraviolet and green receptors in principal eyes of jumping spiders. J. Gen. Physiol., 66:193-207. Eakin, R.W., and J.L. Brandenburger 1971 Fine structure of the eyes of jumping spiders. J. Ultrastruct. Res., 37:618-663. Fahrenbach, W.H. 1969 The morphology of the eyes of Limulus. 11. Ommatidia of the compound eye. Z. Zellforsch., 93~451-483. Fahrenbach, W.H. 1973 The morphology of the Limulus visual system. V. Protocerebral neurosecretion and ocular innervation. Z. Zellforsch., 144: 153-166. Fahrenbach, W.H. 1975 The visual system of the horseshoe crab Limulus polyphemus. Int. Rev. Cytol., 41:285-349. Fleissner, G., and G. Fleissner 1985 Neurobiology of a circadian clock in the visual system of scorpions. In: Neurobiology of Arachnids. Friedrich G. Barth, ed. Springer-Verlag, Berlin, pp. 351-375. Fleissner, G., and G. Fleissner 1988 Efferent control of visual sensitivity in arthropod eyes: With emphasis on circadian rhythms. Gustav Fischer, Stuttgart, pp. 7-67. Fleissner, G., and M. Schliwa 1977 Neurosecretory fibers in the median eyes of the scorpion, Androctonus austraZis L. Cell Tissue Res., 178:189-198. Homann, H. 1971 Die Augen der Araneae. Anatomie, Ontogenie und Bedeutung fur die Systematik (Chelicerata, Arachnida). Z. Morph. Tiere, 69:201-272. Kaiser, T., and G. Alberti 1991 The fine structure of the lateral eyes of Neocarus texunus (Oplioacarida, Acari, Arachnida, Chelicerata). Protoplasma, 163:19-33. Kass, L., and R.B. Jr. Barlow 1992 A circadian clock in the Limulus brain transmits syncronous efferent signals to all eyes. Visual Neurosci., 9:493-504. Land, M.F. 1969 Structure of the principal eyes of jumping spiders (Salticidae: Dendryphantinae) in relation to visual optics. J. Exp. Biol., 51:443-470. Land, M.F. 1985 The morphology and optics of spider eyes. In: Neurobiology of Arachnids. Friedrich G. Barth, ed. Springer-Verlag, Berlin, pp. 53-78. Machan, L. 1968 Spectral sensitivity of the scorpion eyes and the possible role of shielding pigment effect. J . Exp. Biol., 49:95-105. McEnroe, W.D., and K. Dronka 1966 Color vision in the adult female two-spotted spider mite. Science, 154:782-784. Melamed, J., and 0. Trujillo-Cen6z 1966 On the fine structure of the visual system ofLycosu (Araneae, Lycosidae). 1. Retina and optic nerve. Z. Zellforsch. Anat., 74:12-31. Meyer-Rochow, V.B. 1978 Aspect of the functional anatomy of the eyes of the whip-scorpion Thelyphonus caudatus (Chelicerata: Arachnida) and a discussion of their putative performance as photoreceptors. J. R. SOC.New Zealand, 17:325-341. Paulus, H.F. 1979 Eye structure and the monophyly of the arthropoda. In: Arthropod Phylogeny. A.P. Gupta, ed. Van Nostrand Reinhold, New York, pp. 299-383. Rathmayer, W. 1965 Neuromuscular transmission in a spider and the effect of calcium. Comp. Biochem Physiol., 143573487. Schliwa, M. 1979 The retina of the phalangid, Opilio ruuennae, with particular reference to arhabdomeric cells. Cell Tissue Res., 204: 473-495. Schliwa, M., and G. Fleissner 1980 The lateral eyes of the scorpion, Androctonus australis. Cell Tissue Res., 206~95-114. Staehelin, L.A. 1974 Structure and function of intercellular junctions. Int. Rev. Cytol., 39:191-283. Uehara, A,, Y. Toh, and H. Tateda 1977 Fine structure of the eyes of orb-weavers, Argiope umoena L. Koch (Araneae: Argiopidae). 1. The anteromedial eye. Cell Tissue Res., 182:81-91. Uehara, A., K. Uehara, K. Ogawa 1993 Efferent fibers and daily rhabdomal changes in the anteromedial eye of the liphistiid spider, Heptathela kimurui. Cell Tissue Res., 272:517-522. Wald, G., and J.M. Krainin 1963 The median eye of Limulus: An ultraviolet receptor. Proc. N. A., 5O:lOll-1017. Yamashita, S., and H. Tateda 1978 Spectral sensitivities of the anterior median eyes of the orb web spiders Argiope bruennichii and A . amoenu. J. Exp. Biol., 74:47-57.