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A histochemical and ultrastructural study of oogenesis in Aristaeomorpha foliacea (Risso, 1827)

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Abstract

Ovaries from mature giant red shrimp Aristaeomorpha foliacea were investigated histochemically and ultrastructurally. Four growing stages of the oocytes were distinguished: premeiosis stage, previtellogenetic stage, early vitellogenic stage and late vitellogenic stage. In addition, occasional resorptive oocytes were found. Oogonia and premeiotic oocytes were found in germinative zones. Previtellogenic and vitellogenic oocytes were localized in maturative zones. As vitellogenesis proceeded, oocytes showed a progressive development in the number of lipid droplets as well as in the extension of RER, constituted of dilated cisternae, uniformely scattered throughout the cytoplasm. The RER produced yolk granules and a lampbrush-like substance. The latter was released under the oolemma and constituted a characteristic cortical zone. The oolemma did not develop microvilli or micropinocytotic vesicles to incorporate yolk precursors. Thus, the protein yolk appeared to be of endogenous origin. Few somatic cells were found around the oocytes, but they never gave place to a continuous epithelial layer around oocytes, thus it is not possible to speak of ovarian follicle. The cytoplasm of these mesodermal-oocyte associated cells (MOAC) was characterized by a typical steroidogenic apparatus. Few resorptive immature oocytes were found inside late vitellogenic oocytes. Since the ovaries were packed with late vitellogenic oocytes and the few immature oocytes were hardly detectable, oocyte maturation occurred in a synchronous way.

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References

  • Adiyodi, R. G., 1969. Protein metabolism in relation to production and moulting in the crab, Paratelphusa hydrodromous. Part III. RNA activity and protein yolk biosynthesis during normal vitellogenesis and under conditions of acute inanition. Indian J. exp. Biol. 7: 13–16.

    Google Scholar 

  • Adiyodi, R. G. & T. Subramonian, 1983. Arthropoda – Crustacea. In Adyiodi, R. G. & K. G. Adyiodi (eds), Reproductive Biology of Invertebrates, I. Oogenesis, Ovoposition and Oosorption. J. Wiley & Sons, Chichester: 443–495.

    Google Scholar 

  • Arcier, J. M. & M. Brehelin, 1982. Étude histologique et ultrastructurale du tissu folliculaire au cours des cycles de développement ovarien chez Palaemon adspersus (Rathke, 1837). Arch. Biol. 93: 79–97.

    Google Scholar 

  • Beams, H.W. & R. G. Kessel, 1963. Electron microscope studies on developing crayfish oocytes with special reference to the origin of yolk. J. Cell Biol. 18: 621–649.

    Google Scholar 

  • Beams, H. W. & R. G. Kessel, 1980. Ultrastructure and vitellogenesis in the oocyte of the crustacean, Oniscus asellus. J. Submicrosc. Cytol. 12: 17–27.

    Google Scholar 

  • Brian, A., 1931. La biologia del fondo a 'scampi' nel Mar ligure. 5-Aristaeomorpha, Aristeus, ed altri macruri natanti. Boll. Mus. Zool. Anat. Comp. R. Univ. Genova 11: 1–6.

    Google Scholar 

  • Carayon, J., 1941. Morphologie et structure de l'appareil génital femelle chez quelques Pagures. Bull. Soc. Zool. Fr. 66: 95–122.

    Google Scholar 

  • Cau, A., A. M. Deiana & M. Mura, 1982. Nuovi dati sull'accrescimento e sulla maturità sessuale di Aristaeomorpha foliacea (Risso, 1827) (Decapoda, Penaeidae). Naturalista Siciliano, 6 (Suppl.): 429–434.

    Google Scholar 

  • Cau, A., A. M. Deiana & M. Mura, 1987. Ecological observations on Aristaeomorpha foliacea (Risso, 1827) (Decapoda, Penaeidae) in the mid-Western Mediterranean Sea. Inv. Pesq., Barcelona 51: 456.

    Google Scholar 

  • Charniaux-Cotton, H., 1975. L'ovogenèse et sa régulation chez les Crustacés supérieurs. Ann. Biol. Anim. Biochem. Biophys. 15: 715–724.

    Google Scholar 

  • Charniaux-Cotton, H., 1980. Experimental studies of reproduction in Malacostraca crustaceans. Description of vitellogenesis and its endocrine control. In Clark, N. H. Jr. & T. S. Adams (eds), Advances in Invertebrate Reproduction. Elsevier North Holland, Inc.: 177–186.

  • D'Onghia, G., P. Maiorano, A. Matarrese & A. Tursi, 1998. Distribution, biology and population dynamics of Aristaeomorpha foliacea (Risso, 1827) (Decapoda, Natantia, Aristeidae) in the north-Western Ionian Sea (Mediterranean Sea). Crustaceana 71: 518–544.

    Google Scholar 

  • Demestre, M. & J. M. Fortuño, 1992. Reproduction of the deepwater shrimp Aristeus antennatus (Decapoda: Dendrobranchiata). Mar. Ecol. Progr. Ser. 84: 41–51.

    Google Scholar 

  • Dhainaut, A. & M. De Leersnyder, 1976. Étude cytochimique et ultrastrutturale de l'évolution ovocytaire du crab Eriocheir sinensis. I. Ovogenèse naturelle. Arch. Biol. 87: 261–282.

    Google Scholar 

  • Erribabu, D., K. Shyamasundari & K. Kanumantha Rao, 1978. The structure and cytochemistry of the oocytes in the crab Xantho bidentatus Milne Edwards. Folia Histochem. Cytochem. 16: 57–63+.

    Google Scholar 

  • Eurenius, L., 1973. An electron microscope study on the developing oocytes of the crab Canger pagurus L. with special reference to yolk formation (Crustacea). Z. Morphol. Tiere 75: 243–254.

    Google Scholar 

  • Ganion, L. R. & R. G. Kessel, 1972. Intracellular synthesis, transport and packaging of proteinaceous yolk in oocytes of Orconectes immunis. J. Cell Biol. 52: 420–437.

    Google Scholar 

  • Han, C. H. & H. H. Bae, 1992. Purification of the yolk protein, and identification of the synthetic site of its precursor in Eriocheir japonicus (Decapoda, Brachiura). Bull. Kor. Fish. Soc. 25: 432–442.

    Google Scholar 

  • Hinsch, G. W., 1970. Possible role of intranuclear membranes in nuclear-cytoplasmic exchange in spider crab oocytes. J. Cell Biol. 47: 531–535.

    Google Scholar 

  • Hinsch, G. W. & M. V. Cone, 1969. Ultrastructural observations of vitellogenesis in the spider crab, Libinia emarginata L.. J. Cell Biol. 40: 336–342.

    Google Scholar 

  • Holthuis, L. B., 1980. FAO species catalogue. Shrimps and prawns of the world: an annotated catalogue of species of interest to fisheries. FAO Fish. Synop. 125: 1–261.

    Google Scholar 

  • Hort-Legrand, C., J. Berreur-Bonnenfant & T. Ginsurger-Vogel, 1974. Étude anatomique et histologique comparee de la différenciation des gonades chez les mâles et les femelles chez Orchestia gammarella Pallas (Crustacé Amphipode) pendant le période post-embryonnaire. Bull. Soc. Zool. Fr. 99: 521–524.

    Google Scholar 

  • Kessel, R. G., 1968. Mechanisms of protein yolk synthesis and deposition in crustacean oocytes. Z. Zellforsch. 89: 17–38.

    Google Scholar 

  • Kessel, R. G., & H. W. Beams, 1968. Intranucleolar membranes and nuclear-cytoplasmic exchange in young crayfish oocytes. J. Cell Biol. 39: 735–741.

    Google Scholar 

  • Lachaise, F., M. Goudeau, C. Hetru, C. Kappler & J. A. Hoffman, 1981. Ecdysteroids and ovarian development in the shore crab, Carcinus maenas. hoppe Segler's. Z. Physiol. Chem. ISSN 0018-4888, DEU 382: 521–529.

    Google Scholar 

  • Lachaise, F., & J. A. Hoffmann, 1977. Ecdysone et développement ovarien chez un Décapode, Carcinus maenas. C.R. Acad. Sci., Paris 285: 701–704.

    Google Scholar 

  • Levi, D. & M. Vacchi, 1988. Macroscopic scale for simple and rapid determination of sexual maturity in Aristaeomorpha foliacea (Risso, 1827) (Decapoda, Penaeidae). J. Crust. Biol. 8: 532–538.

    Google Scholar 

  • Matarrese, A., G. D'Onghia, A. Tursi & P. Maiorano, 1997. Vulnerabilità e resilienza di Aristaeomorpha foliacea (Risso, 1827) e Aristeus antennatus (Risso, 1816) (Crostacei, Decapodi) nel mar Ionio. Soc. Ital. Ecol. Atti 18: 535–538.

    Google Scholar 

  • Matarrese, A., G. D'Onghia, M. De Florio, M. Panza & G. Costantino, 1995. Recenti acquisizioni sulla distribuzione batimetrica di Aristaeomorpha foliacea ed Aristeus antennatus (Crustacea, Decapoda) nel Mar Ionio. Biol. mar. Medit. 2: 299–300.

    Google Scholar 

  • Meusy, J. J., 1980. Vitellogenin, the extraovarian precursor of the protein yolk in Crustacea: a review. Reprod. Nutr. Dév. 20: 1–21.

    Google Scholar 

  • Mori, M., F. Biagi & S. De Ranieri, 1994. Reproductive biology of Aristaeomorpha foliacea in the southern Tuscany Archipelago (Central Tyrrhenian Sea). In Bianchini, M. L. & S. Ragonese (eds), Life Cycles and Fisheries of Deep Water Red Shrimps Aristaeomorpha foliacea and Aristeus antennatus. N.T.R.-I.T.P.P. 3: 31–32.

  • Mura, M., S. Campisi & A. Cau, 1992. Osservazioni sulla biologia riproduttiva negli aristeidi demersali del Mediterraneo centro-occidentale. Oebalia 17(Suppl. 2): 61–66.

    Google Scholar 

  • Orsi Relini, L. & M. Semeria, 1983. Oogenesis and fecundity in bathyal penaeid prawns, Aristeus antennatus and Aristaeomorpha foliacea. Rapp. Comm. int. Mer Médit. 28: 281–284.

    Google Scholar 

  • Pearse, A. G. V., 1968. In Pearse, A. G. V. (ed.), Histochemistry Theoretical and Applied. 3rd edn, Vol. 1. J. & A. Churchill Ltd, London: 607 pp.

    Google Scholar 

  • Ragonese, S., 1993. Geographical distribution of Aristaeomorpha foliacea (Crustacea, Aristeidae) in the Sicilian Channel (Mediterranean sea). ICIES Mar. Sci. Symp.: 1–12.

  • Ragonese, S. & M. L. Bianchini, 1995. Size at sexual maturity in red shrimp females, Aristaeomorpha foliacea, from the Sicilian Channel (Mediterranean Sea). Crustaceana 68: 73–82.

    Google Scholar 

  • Ragonese, S., M. L. Bianchini & V. F. Gallucci, 1994. Growth and mortality of the red shrimp Aristaeomorpha foliacea, from the Sicilian Channel (Mediterranean Sea). Crustaceana 67: 348–361.

    Google Scholar 

  • Rateau, J. G. & C. Zerbib, 1978. Étude ultrastructurale des follicules ovocytaires chez le Crustacé Amphipode Orchestia gammarellus (Pallas). C.R. Acad. Sc. Paris, Sér. D. 286: 65–68.

    Google Scholar 

  • Schade, M. L. & R. R. Shivers, 1980. Structural modulation of the surface and cytoplasm of oocytes during vitellogenesis in the lobster, Homarus americanus. An electron microscope-protein tracer study. J. Morphol. 163: 13–26.

    Google Scholar 

  • Souty, C., 1980. Electron microscopic study of follicle cell development during vitellogenesis in the marine crustacean Isopoda, Idotea balthica basteri. Reprod. Nutr. Dévelop. 20: 653–663.

    Google Scholar 

  • Souty, C., 1983. Démonstration d'une alternance des pics de synthèse des fractions, respectivement endogène et exogène, du vitellus protéique chez l'Oniscoïde Porcellio dilatatus Brandt. C.R. Acad. Sc. Paris, Sér. III 296: 221–223.

    Google Scholar 

  • Spedicato, M. T., G. Lembo, P. Carbonara & T. Silecchia, 1994. Biological parameters and dynamics of Aristaeomorpha foliacea in southern Tyrrhenian Sea. In Bianchini, M. L. & S. Ragonese (eds), Life Cycles and Fisheries of Deep Water Red Shrimps Aristaeomorpha foliacea and Aristeus antennatus. N.T.R.-I.T.P.P. Special Publication 3: 35–36.

  • Trentini, M. & F. Sabelli Scanabissi, 1978. Ultrastructural observations on the oogenesis of Triops cancriformis (Crustacea, Notostraca). I. Origin and differentiation of nurse cells. Cell Tissue Res. 194: 71–77.

    Google Scholar 

  • Wolin, E. M., H. Laufer & D. F. Albertini, 1973. Uptake of the yolk protein, lipovitellin, by developing crustacean oocytes. Dev. Biol. 35: 160–170.

    Google Scholar 

  • Zaffagnini, F., 1987. Reproduction in Daphnia. In Peters, R. H. & R. De Bernardi (eds), Daphnia. Mem. Ist. ital. Idrobiol. 45: 245–284.

  • Zeni, C. & F. Zaffagnini, 1989. Electron microscopic study on oocytes, nurse cells and yolk formation in Leptestheria dahalacensis (Crustacea, Conchrostaca). Invertebr. Reprod. Develop. 15: 119–129.

    Google Scholar 

  • Zerbib, C., 1973. Contribution à l'étude ultrastructurale de l'ovocyte chez le Crustacé Amphipode Orchestia gammarellus (Pallas). C.R. Acad. Sci 277: 1209–1212.

    Google Scholar 

  • Zerbib, C., 1975. Premières observations de granules corticaux dans l'ovocyte d'un Crustacé, l'Amphipode Orchestia gammarellus (Pallas). C.R. Acad. Sci 281: 1345–1347.

    Google Scholar 

  • Zerbib, C., 1979. Étude structurale de l'ovocyte en vitellogenèse chez les Écrevisses Astacus astacus et Astacus leptodactylus. Int. J. Invertebr. Reprod. 1: 289–295.

    Google Scholar 

  • Zerbib, C., 1980. Ultrastructural observation of oogenesis in the Crustacea Amphipoda Orchestia gammarellus (Pallas). Tissue Cell 12: 47–62.

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, University of Bari, Via E. Orabona 4, 70125, Bari, Italy

    S. Desantis

  2. Department of Zoology, University of Bari, Via E. Orabona 4, 70125, Bari, Italy

    M. Labate, P. Maiorano, A. Tursi & M. Ciccarelli

  3. Department of Zoology; Department of Animal Production, Italy

    G.M. Labate

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  1. S. Desantis
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  2. M. Labate
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  6. M. Ciccarelli
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Desantis, S., Labate, M., Maiorano, P. et al. A histochemical and ultrastructural study of oogenesis in Aristaeomorpha foliacea (Risso, 1827). Hydrobiologia 449, 253–259 (2001). https://doi.org/10.1023/A:1017519320722

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