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Unorthodox pattern of microvilli and intercellular junctions in regular retinular cells of the porcellanid crab Petrolisthes

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Summary

  1. 1.

    Retinular fine structure in compound eyes of the porcellanid crab Petrolisthes differs significantly from two paguroid anomurans Clibanarius and Pagurus which basically conform to the usual conservative decapod crustacean retinular pattern.

  2. 2.

    Bidirectional orientation of microvilli has been discovered in rhabdomeres of retinular cells R1–R7 in Petrolisthes. Distally the regular rhabdom has mainly a typical banded microvillus structure (Figs. 7, 8). Proximally rhabdom banding continues but uniquely all seven regular retinular cells contribute sets of alternately orthogonal microvilli to each band (Figs. 5, 6, 12). This unorthodox pattern should reduce polarization sensitivity and enhance sensitivity to unpolarized light.

  3. 3.

    In this special region microvillus layers are strongly elliptical in cross section with the minor axis parallel to the microvilli (Fig. 12). Hence the ends of the major axes protrude considerably from the central area of overlap (Fig. 6).

  4. 4.

    Retinular cell eight has bidirectional microvilli (Figs. 5–7) as usual in brachyuran crabs. Unlike the latter as well as paguroid crabs, Petrolisthes has square facets and a rectangular retinular array (Figs. 1, 3) similar to other galatheids and macruran decapods generally. It also resembles macrurans (shrimps and lobsters) in having perirhabdomal vacuoles absent or much reduced.

  5. 5.

    Tight junctions occur widely between adjacent retinular cells (Figs. 14, 17) especially basally immediately distal to longitudinal zonular adherentes (Figs. 6, 16) typical of compound eyes. Freeze fracture reveals in addition numerous rectangular arrays of particles on the protoplasmic face of retinular cell membrane near, but not part of, the rhabdom (Figs. 19, 20). Other authors have hypothesized polarized transfer functions for similar particle aggregates in certain vertebrate cells.

  6. 6.

    Experiments and further comparative study are needed to test whether the special fine structural features of the eye depend on Petrolisthes' sedentary photophobic habits or on its particular anomuran affiliation.

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References

  • Bennett MVL (1978) Junctional permeability. In: Feldman J, Gilula NB, Pitts JD (eds) Intercellular junctions and synapses: Receptors and recognition, Ser B, Vol 2. Chapman and Hall, London, pp 25–36

    Google Scholar 

  • Bennett MVL, Goodenough DA (1978) Gap junctions, electrotonic coupling, and intercellular communication. Neurosciences Res Prog Bull 16:373–486

    Google Scholar 

  • Bernhard CG (ed) (1966) The functional organization of the compound eye. Pergamon Press, Oxford, 591 pp

    Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function in the nervous system of invertebrates, Vol II. Freeman, San Francisco, London, pp 1068–1076

    Google Scholar 

  • Chi C, Carlson SD (1980a) Membrane specializations in the first optic neuropil of the housefly, Musca domestica L. I. Junctions between neurons. J Neurocytol 9:429–449

    Google Scholar 

  • Chi C, Carlson SD (1980b) Membrane specializations in the first optic neuropil of the housefly, Musca domestica L. II. Junctions between glial cells. J Neurocytol 9:451–469

    Google Scholar 

  • Chi C, Carlson SD (1981a) Lanthanum and freeze fracture studies on the retinular cell junction in the compound eye of the housefly. Cell Tissue Res 214:541–552

    Google Scholar 

  • Chi C, Carlson SD (1981b) The perineurium of the adult housefly: ultrastructure and permeability to lanthanum. Cell Tissue Res 217:373–386

    Google Scholar 

  • Chi C, Carlson SD, St. Marie RL (1979) Membrane specializations in the peripheral retina of the housefly Musca domestica L. Cell Tissue Res 198:501–520

    Google Scholar 

  • Coles JA, Tsacopoulos M (1979) Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol 290:525–549

    Google Scholar 

  • Cummins D, Goldsmith TH (1981) Cellular identification of the violet receptor in the crayfish eye. J Comp Physiol 142:199–202

    Google Scholar 

  • Deurs B van, Luft JH (1979) Effects of glutaraldehyde fixation on the structure of tight junctions. J Ultrastruct Res 68:160–172

    Google Scholar 

  • Eguchi E (1978) Comparative fine structure of lepidopteran compound eyes, especially skippers (Hesperioidea). Zool Mag 87:32–43

    Google Scholar 

  • Eguchi E (1982) Retinular fine structure in compound eyes of diurnal and nocturnal sphingid moths. Cell Tissue Res: in press

  • Eguchi E, Waterman TH (1966) Fine structure patterns in crustacean rhabdoms. In: Bernhard CG (ed) The functional organization of the compound eye. Pergamon Press, Oxford, pp 105–124

    Google Scholar 

  • Eguchi E, Waterman TH (1967) Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Z Zellforsch 79:209–229

    Google Scholar 

  • Eguchi E, Waterman TH (1968) Cellular basis for polarized light perception in the spider crab, Libinia. Z Zellforsch 84:87–101

    Google Scholar 

  • Eguchi E, Waterman TH (1973) Orthogonal microvillus pattern in the eighth rhabdomere of the rock crab Grapsus. Z Zellforsch 137:145–157

    Google Scholar 

  • Eguchi E, Waterman TH (1976) Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes. Cell Tissue Res 169:419–434

    Google Scholar 

  • Eley S, Shelton PMJ (1976) Cell junctions in the developing compound eye of the desert locust Schistocerca gregaria. J Embryol Exp Morphol 36:409–423

    Google Scholar 

  • Ellisman MH, Brooke MH, Kaiser KK, Rash JE (1978) Appearance in slow muscle sarcolemma of specializations characteristic of fast muscle after reinnervation by a fast muscle nerve. Exp Neurol 58:59–67

    Google Scholar 

  • Farges G (1975) Anatomie comparée du système neurosécréteur protocérébral chez cinq anomoures. Bull Soc Zool France 100:477–487

    Google Scholar 

  • Fernández HR, Nickel EE (1976) Ultrastructrual and molecular characterisitics of crayfish photoreceptor membranes. J Cell Biol 69:721–732

    Google Scholar 

  • Fincham AA (1980) Eyes and classification of malacostracan crustaceans. Nature 287:729–731

    Google Scholar 

  • Goldsmith TH, Bernard GD (1974) The visual system of insects. In: Rockstein M (ed) The physiology of the insecta, 2nd Ed. Academic, New York San Francisco London, pp 165–262

    Google Scholar 

  • Goodenough DA, Gilula NG (1979) Functional membrane differentiation at sites of cell-cell interaction. In: Nicholls JG (ed) The role of intercellular signals: Navigation, encounter, outcome. Dahlem Konferenzen, Berlin 1979, pp 135–154

    Google Scholar 

  • Graf F (1978) Diversité structurale des jonctions intercellulaires communicantes (gap junctions) de l'épithélium des caecums postérieurs du Crustacé Orchestia. CR Acad Sc Paris 287:41–44

    Google Scholar 

  • Gribakin FC (1979) Cellular mechanisms of insect photoreception. Int Rev Cytol 57:127–184

    Google Scholar 

  • Hanström B (1948) The brain, the sense organs, and the incretory organs of the head in the Crustacea Malacostraca. Bull Biol France et Belgique, Suppl XXXIII, pp 98–126

  • Hatton JD, Ellisman MH (1981) The distribution of orthogonal arrays and their relationship to intercellular junctions in neuroglia of the freeze-fractured hypothalamo-neurohypophysial system. Cell Tissue Res 215:309–323

    Google Scholar 

  • Horridge GA (ed) (1975) The compound eye and vision of insects. Clarendon Press, Oxford, 595 pp

    Google Scholar 

  • Järvilehto M (1979) Receptor potentials in invertebrate visual cells. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6A. Springer, Berlin Heidelberg New York, pp 315–356

    Google Scholar 

  • Krebs W (1972) The fine structure of the retinula of the compound eye of Astacus fluviatilis. Z Zellforsch 133:399–414

    Google Scholar 

  • Kunze P (1979) Apposition and superposition eyes. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6A. Springer, Berlin Heidelberg New York, pp 441–502

    Google Scholar 

  • Kurup NG (1964) The incretory organs of the eyestalk and brain of the porcelain crab, Petrolisthes cinctipes Randall (Reptantia-Anomura). Gen Comp Endocrinol 4:99–112

    Google Scholar 

  • Land MF (1976) Superposition images are formed by reflection in the eyes of some oceanic decapod Crustacea. Nature 263:764–765

    CAS  PubMed  Google Scholar 

  • Land MF (1981) Optics and vision in invertebrates. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6B. Springer, Berlin Heidelberg New York, pp 471–592

    Google Scholar 

  • Landis DMD, Reese TS (1974) Arrays of particles in freeze-fractured astrocytic membranes. J Cell Biol 60:316–320

    Google Scholar 

  • Landis DMD, Reese TS (1981) Astrocyte membrane structure: changes after circulatory arrest. J Cell Biol 88:660–663

    Google Scholar 

  • Lane NJ (1978) Electron microscopy. In: Sturgess JM (ed) State of the art symposia, vol 3. Proc 9th Internatl Congress on Electron Microscopy. The Imperial Press, Ltd, Canada, pp 673–691

    Google Scholar 

  • Lane NJ (1981) Vertebrate-like tight junctions in the insect eye. Exp Cell Res 132:482–488

    Google Scholar 

  • Lane NJ, Chandler HJ (1980) Definitive evidence for the existence of tight junctions in invertebrates. J Cell Biol 86:765–774

    Google Scholar 

  • Lane NJ, Swales LS (1980) Dispersal of junctional particles, not internalization, during the in vivo disappearance of gap junctions. Cell 19:579–586

    Google Scholar 

  • Lane NJ, Treherne JE (1980) Functional organisation of arthropod neuroglia. In: Locke M, Smith DS (eds) Insect biology in the future. Academic, New York, pp 765–795

    Google Scholar 

  • Laughlin SD (1981) Neural principles in the peripheral visual system of invertebrates. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6B. Springer, Berlin Heidelberg New York, pp 133–280

    Google Scholar 

  • Loewenstein WR (1978) Cell-to-cell communication. In: Andreoli TE, Hoffman JF, Fanestil DD (eds) Physiology of membrane disorders. Plenum, New York, pp 335–356

    Google Scholar 

  • Menco BPhM (1980) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory epithelial surfaces of frog, ox, rat, and dog. III. Tight junctions. Cell Tissue Res 211:361–373

    Google Scholar 

  • Meyer-Rochow V (1975) Larval and adult eye of the western rock lobster, Panulirus longipes. Cell Tissue Res 162:439–457

    Google Scholar 

  • Meyer-Rochow V, Walsh S (1979) The eyes of mesopelagic crustaceans: I. Gennadas sp. (Penaeidae). Cell Tissue Res 184:87–101

    Google Scholar 

  • Mote MI (1974) Polarization sensitivity. A phenomenon independent of stimulus intensity or state of adaptation in retinular cells of the crabs Carcinus and Callinectes. J Comp Physiol 90:389–403

    Google Scholar 

  • Nässel DR (1976) The fine structure of photoreceptor terminals in the compound eye of Pandalus (Crustacea). Acta Zool 57:153–160

    Google Scholar 

  • Nässel DR, Waterman TH (1977) Golgi EM evidence for visual information channelling in the crayfish lamina ganglionaris. Brain Res 130:556–563

    Google Scholar 

  • Nässel DR, Waterman TH (1979) Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J Comp Physiol 131:205–216

    Google Scholar 

  • Noirot-Timothée C, Noirot C (1980) Septate and scalariform junctions in arthropods. Int Rev Cytol 63:97–140

    Google Scholar 

  • Overton J (1974) Cell junctions and their development. In: Cadenhead DA, Danielli JF, Rosenberg MD (eds) Progress in surface and membrane science, Vol 8. Academic Press, New York, pp 161–208

    Google Scholar 

  • Parker GH (1981) The compound eyes in crustaceans. Bull Mus Comp Zool (Harvard) 21:45–140

    Google Scholar 

  • Peracchia C (1974) Excitable membrane ultrastructure I. Freeze fracture of crayfish axons. J Cell Biol 61:107–122

    Google Scholar 

  • Peracchia C (1980) Structural correlates of gap junction permeation. Int Rev Cytol 66:81–146

    Google Scholar 

  • Ramadan MM (1952) Contribution to our knowledge of the structure of the compound eyes of Decapoda Crustacea. Lunds Univ Arsskrift 48:1–20

    Google Scholar 

  • Revel JP, Karnvsky MJ (1967) Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol 33:C7-C12

    Google Scholar 

  • Ribi WA (1978) Gap juctions coupling photoreceptor axons in the first optic ganglion of the fly. Cell Tissue Res 195:299–308

    Google Scholar 

  • Rodieck RW (1973) The vertebrate retina. Freeman, San Francisco, 1044 pp

    Google Scholar 

  • Rutherford DJ, Horridge GA (1965) The rhabdom of the lobster eye. QJ Microsc Sci 106:119–130

    Google Scholar 

  • Sandri C, Akert K, Bennett MVL (1978) Junctional complexes and variations in gap junctions between spinal cord ependymal cells of a teleost, Sternarchus albifrons (Gymnotoidei). Brain Res 143:27–41

    Google Scholar 

  • Schiller A, Forssmann WG, Taugner R (1980) The tight junctions of renal tubules in the cortex and outer medulla. Cell Tissue Res 212:395–413

    Google Scholar 

  • Shaw SR (1966) Polarized light responses from crab retinula cells. Nature 211:92–93

    Google Scholar 

  • Shaw SR (1978) The extracellular space and blood-eye barrier in an insect retina: an ultrastructural study. Cell Tissue Res 188:35–61

    Google Scholar 

  • Shaw SR (1981) Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially Diptera. In: Roberts A, Bush BMH (eds) Neurones without impulses. Cambridge University Press, Cambridge, pp 61–116

    Google Scholar 

  • Snyder AW (1979) Physics of vision in compound eyes. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6A. Springer, Berlin Heidelberg New York, pp 225–313

    Google Scholar 

  • Staehelin LA (1974) Structure and function of intercellular junctions. Int Rev Cytol 39:191–283

    Google Scholar 

  • Števčić Z (1971) The main features of brachyuran evolution. Syst Zool 20:331–340

    Google Scholar 

  • Stowe S (1980a) Spectral sensitivity and retinal pigment movements in the crab, Leptograpsus variegatus (Fabricius). J Exp Biol 87:73–98

    Google Scholar 

  • Stowe S (1980b) Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell Tissue Res 211:419–440

    Google Scholar 

  • Strausfeld NJ, Nässel DR (1981) Neuroarchitecture serving compound eyes of Crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6B. Springer, Berlin Heidelberg New York, pp 1–132

    Google Scholar 

  • Toh Y, Waterman TH (1982) Diurnal changes in compound eye fine structure in the blue crab Callinectes 1. Differences between noon and midnight retinas on an LD 11∶13 cycle. J Ultrastruct Res, 75: in press

  • Trujillo-Cenóz O (1972) The structural organization of the compound eye in insects. In: Fuortes MGF (ed) Handbook of sensory physiology, Vol VII/2. Springer, Berlin Heidelberg New York, pp 5–62

    Google Scholar 

  • Vaughn JC, Traeger FJ (1976) Conservation of repeated DNA base sequences in the Crustacea: a molecular approach to decapod phylogeny. J Mol Evol 7:111–131

    Google Scholar 

  • Vogt K (1975) Zur Optik des Flußkrebsauges. Z Naturforsch 30c:691

    Google Scholar 

  • Vogt K (1977) Ray path and reflection mechanisms in crayfish eyes. Z Naturforsch 32c:466–468

    Google Scholar 

  • Vogt K (1980) Die Spiegeloptik des Flußkrebsauges. J Comp Physiol 135:1–9

    Google Scholar 

  • Waterman TH (1961) Light sensitivity and vision. In: Waterman TH (ed) The physiology of Crustacea, Vol II. Academic, New York, pp 1–64

    Google Scholar 

  • Waterman TH (1966) Information channeling in the crustacean retina. In: Nye PW (ed) Proceedings of the symposium on information processing in sight sensory systems, 1965. California Institute of Technology, Pasadena, pp 48–56

    Google Scholar 

  • Waterman TH (1975) The optics of polarization sensitivity. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 339–371

    Google Scholar 

  • Waterman TH (1977) The bridge between visual input and central programming in crustaceans. In: Hoyle G (ed) Identified neurons and behavior of arthropods. Plenum, New York London, pp 371–386

    Google Scholar 

  • Waterman TH (1981) Polarization sensitivity. In: Autrum H (ed) Handbook of sensory physiology, Vol VII/6B. Springer, Berlin Heidelberg New York, pp 281–469

    Google Scholar 

  • Waterman TH (1982) Fine structure and turnover of photoreceptor membranes. In: Westfall JA (ed) Visual cells in evolution. Raven Press, New York, pp 23–42

    Google Scholar 

  • Waterman TH, Fernández HR (1970) E-vector and wavelength discrimination by retinular cells of the crayfish Procambarus. Z Vergl Physiol 68:154–174

    Google Scholar 

  • Waterman TH, Horch KW (1966) Mechanism of polarized light perception. Science 154:467–475

    Google Scholar 

  • Waterman TH, Piekos WB (1981) Light and time correlated migration of invasive hemocytes in the crayfish compound eye. J Exp Zool 217:1–14

    Google Scholar 

  • Waterman TH, Fernandez HR, Goldsmith TH (1969) Dichroism of photosensitive pigment in rhabdoms of the crayfish Orconectes. J Gen Physiol 54:415–432

    Google Scholar 

  • Williams EH, DeHaan RL (1981) Electrical coupling among heart cells in the absence of ultrastructurally defined gap junctions. J Membr Biol 60:237–248

    Google Scholar 

  • Williamson DI (1974) Larval characters and the origin of crabs (Crustacea, Decapoda, Brachyura). Thalassia Jugoslavica 10:401–414

    Google Scholar 

  • Zampighi G, Corless JM, Robertson JD (1980) On gap junction structure. J Cell Biol 86:190–198

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Yokohama City University, Kanazawa-ku, Yokohama, Japan

    Eisuke Eguchi

  2. Department of Physiology, School of Medicine, Gifu University, Tsukasa, Gifu, Japan

    Taichiro Goto

  3. Department of Biology, Yale University, New Haven, Connecticut, USA

    Talbot H. Waterman

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  1. Eisuke Eguchi
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  2. Taichiro Goto
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  3. Talbot H. Waterman
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Supported by grants from the Ministry of Education, Science and Culture of Japan (Special Project Research in Photophysiology, No. 411204, E.E., Principal Investigator) and from the U.S. National Institutes of Health (EY02929, T.H.W., Principal Investigator)

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Eguchi, E., Goto, T. & Waterman, T.H. Unorthodox pattern of microvilli and intercellular junctions in regular retinular cells of the porcellanid crab Petrolisthes . Cell Tissue Res. 222, 493–513 (1982). https://doi.org/10.1007/BF00213850

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