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The encapsular developmental sequence of the mesogastropod Turritella communis (Gastropoda: Turritellidae)

Published online by Cambridge University Press:  11 May 2009

J. J. Kennedy  and
B. F. Keegan
J. J. Kennedy
Affiliation:
Department of Zoology, Martin Ryan Marine Institute, University College Galway, Galway City, Ireland
B. F. Keegan
Affiliation:
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Extract

The development of the lecithotrophic encapsulated larva of the internally-fertilizing, sublittoral gastropod Turritella communis Risso 1826 was documented using scanning electron microscopy and light microscopy. Encapsulated development was completed in 12 days at 15°C in the laboratory. Spawning occurred above ~10°C. Spawn masses consisted of numerous gelatinous egg capsules, each of which contained ~28 eggs, encased in albumen and fertilizing sperm. The eggs had an average diameter of 139 μm. Fertilization was accomplished by unpaired eupyrene sperm and occurred at the germinal vesicle stage. The developmental sequence followed the typical gastropod pattern, but was unique in a number of respects. Polar lobes were produced during meiotic maturation and early cleavage, with an especially large lobe occurring in association with the first cleavage, which was unequal. The blastula developed into a dorso-ventrally flattened placula at the 70-cell stage. Gastrulation occurred through invagination and epiboly acting together, and was uniquely accompanied by the development of ectodermal microvilli measuring ~ 1 μm in length. Extra-embryonic albumen began to be depleted after the development of the microvilli. It is proposed that the ciliated telotrochal cells gave rise to the pair of statocysts. Torsion was additionally observed to be facilitated by the growth of pre-mantle tissue on the right side and retardation of growth on the left side.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 72 , Issue 4 , November 1992 , pp. 783 - 805
Copyright
Copyright © Marine Biological Association of the United Kingdom 1992

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References

Bayne, C.J., 1968. Histochemical studies on the egg capsules of eight gastropod molluscs. Proceedings of the Malacological Society of London, 38, 199–212.Google Scholar
Brown, D., Noonan, E. & Kensler, C.B., 1975. Algal culture: development of a working system. Fish Farming International, 2(4), 28–31.Google Scholar
Buddenbrock, W. von, 1915. Die statocysten von Pecten, ihre histologie und physiologic Zoologische Jahrbücher, Allgemeine Zoologie und Physiologie der Tiere, 35, 301–356.Google Scholar
Cather, J.N. & Verdonk, N.H., 1974. The development of Bithynia tentaculata (Prosobranchia: Gastropoda) after removal of the polar lobe. Journal of Embryology and Experimental Morphology, 31, 415–422.Google ScholarPubMed
Charin, N., 1926. Uber die Nahrung des Embryo von Paludina vivipara. Bulletin de la Société Naturalistes de Voronèje, 1, 60–66.Google Scholar
Clement, A.C., 1952. Experimental studies on germinal localization in Ilyanassa. I. The role of the polar lobe in determination of the cleavage pattern and its influence in later development. Journal of Experimental Zoology, 121, 593–625.CrossRefGoogle Scholar
Clement, A.C., 1971. Ilyanassa. In Experimental embryology of marine and freshwater invertebrates (ed. G., Reverberi), pp. 188–214. Amsterdam: North-Holland.Google Scholar
Costello, D.P. & Henley, C., 1971. Methods for obtaining and handling marine eggs and embryos, 2nd ed. Marine Biological Laboratory, Woods Hole, Massachusetts.CrossRefGoogle Scholar
Dohmen, M.R. & Verdonk, N.H., 1979. The ultrastructure and role of the polar lobe in development of molluscs. In Determinants of spatial organization (ed. S., Subtelny and I.R., Konigsberg), pp. 3–27. New York: Academic Press.CrossRefGoogle Scholar
Dongen, C.A.M. van & Geilenkirchen, W.L.M., 1974. The development of Dentalium with special reference to the significance of the polar lobe. I. Division chronology and development of the cell pattern in Dentalium dentale (Scaphopoda). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, series C, 77, 57–70.Google Scholar
Dongen, C.A.M. van & Geilenkirchen, W.L.M., 1975. The development of Dentalium with special reference to the significance of the polar lobe. IV. Division chronology and development of the cell pattern in Dentalium dentate after removal of the polar lobe at first cleavage. Proceedings of the Koninklijke Nederlandse Akademie Wetenschappen, series C, 78, 358–375.Google Scholar
Franc, A., 1940. Recherches sur le dévelopment d'Ocinebra aciculata, Lamarck (Mollusque: Gastéropode). Bulletin Biologiaue de la France et de la Belgiaue, 74, 327–345.Google Scholar
Fretter, V. & Graham, A., 1962. British prosobranch molluscs: their functional anatomy and ecology. London: Ray Society.Google Scholar
Fretter, V. & Graham, A., 1981. The prosobranch molluscs of Britain and Denmark. Part 6. Cerithiacea, Strombacea, Hipponicacea, Calyptraeacea, Lamellariacea, Cypraeacea, Naticacea, Tonnacea, Heteropoda. Journal of Molluscan Studies, supplement 9, 285–363.Google Scholar
Fretter, V. & Manly, R., 1979. Observations on the biology of some sublittoral prosobranchs. Journal of Molluscan Studies, 45, 209–218.CrossRefGoogle Scholar
Fretter, V. & Montgomery, M.C., 1968. The treatment of food by prosobranch veligers. Journal of the Marine Biological Association of the United Kingdom, 48, 499–520.CrossRefGoogle Scholar
Fretter, V. & Pilkington, M.C., 1970. Prosobranchia. Veliger larvae of Taenioglossa and Stenoglossa. Conseil International pour l‘Exploration de la Mer. Zooplankton, sheets 129–132, 1–26.Google Scholar
Fretter, V. & Shale, D., 1973. Seasonal changes in population density and vertical distribution of prosobranch veligers in offshore plankton at Plymouth. Journal of the Marine Biological Association of the United Kingdom, 53, 471–492.CrossRefGoogle Scholar
Gallardo, C.S., 1979. Developmental pattern and adaptations for reproduction in Nucella crassilabrum and other muricacean gastropods. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 157, 453–463.CrossRefGoogle ScholarPubMed
Guerrier, P., Biggelaar, J.A.M. van den, Dongen, C.A.M. van & Verdonk, N.H., 1978. Significance of the polar lobe for the determination of dorsoventral polarity in Dentalium vulgare (da Costa). Developmental Biology, 63, 233–242.CrossRefGoogle ScholarPubMed
Gustafson, R.G. & Reid, R.G.B., 1986. Development of the pericalymma larva of Solemya reidi (Bivalvia: Cryptodonta: Solemyidae) as revealed by light and electron microscopy. Marine Biology, 93, 411–427.CrossRefGoogle Scholar
Hertling, H., 1928. Beobachtungen und Versuche an den Eiern von Littorina und Lacuna. Bedeutung der Eihüllen. Entwicklung im natürlichen und abgeänderten Medium. Wissenschaftliche Meeresuntersuchungen. Neue Folge. Abteilung Helgoland, 17, 1–49.Google Scholar
Hyman, L.H., 1967. The invertebrates, vol. VI. Mollusca I. New York: McGraw-Hill.Google Scholar
Kantor, Y.I., 1986. Egg capsules and intracapsular development of young in the sub-family Volutopsinae (Gastropoda: Bucciniidae). Zhurnal Obshchei Biologii, 47(3), 411–416. [In Russian with English Abstract.]Google Scholar
Lebour, M.V., 1933. The eggs and larvae of Turritella communis Lamarck and Aporrhais pes-pelicani (L.). Journal of the Marine Biological Association of the United Kingdom, 18, 499–506.CrossRefGoogle Scholar
Lebour, M.V., 1937. The eggs and larvae of the British prosobranchs with special reference to those living in the plankton. Journal of the Marine Biological Association of the United Kingdom, 22, 105–166.CrossRefGoogle Scholar
Mahieu, G.C. de, Penchaszadeh, P.E. & Casal, A.B., 1974. Algunos aspectos de las variaciones de proteinas y aminoacidos libres totales del liquido intracapsular en relacion al desarrollo embrionario en Adelomelon brasiliana (Lamarck, 1811) (Gastropoda, Prosobranchia, Volutidae). Cahiers de Biologie Marine, 15, 215–227.Google Scholar
Manahan, D.T. & Crisp, D.J., 1982. The role of dissolved organic material in the nutrition of pelagic larvae: amino acid uptake by bivalve veligers. American Zoologist, 22, 635–646.CrossRefGoogle Scholar
Pechenik, J.A., 1979. Role of encapsulation in invertebrate life histories. American Naturalist, 114, 859–870.CrossRefGoogle Scholar
Pechenik, J.A., 1983. Egg capsules of Nucella lapillus (L.) protect against low-salinity stress. Journal of Experimental Marine Biology and Ecology, 71, 165–179.CrossRefGoogle Scholar
Pechenik, J.A., 1986. The encapsulation of eggs and embryos by mollusca: an overview. American Malacological Bulletin, 42, 165–172.Google Scholar
Pechenik, J. A., Chang, S.C. & Lord, A., 1984. Encapsulated development of the marine prosobranch gastropod Nucella lapillus. Marine Biology, 78, 223–229.CrossRefGoogle Scholar
Richter, G. & Thorson, G., 1975. Pelagishe prosobranchier-larven des Golfes von Neapel. Ophelia, 13, 109–185.CrossRefGoogle Scholar
Smith, F.G.W., 1935. The development of Patella vulgata. Philosophical Transactions of the Royal Society of London, series B, 225, 95–125.Google Scholar
Sullivan, C.H. & Bonar, D.B., 1984. Biochemical characterization of the hatching process inllyanassa obsoleta. Journal of Experimental Zoology, 229, 223–234.CrossRefGoogle Scholar
Thiriot-Quiévreux, C., 1969. Caractéristiques morphologiques des véligères planctoniques de gasteropodes de la région de Banyuls-sur-Mer. Vie et Milieu, B, 20, 333–366.Google Scholar
Thorson, G., 1946. Reproduction and larval development of Danish marine bottom invertebrates with special reference to the planktonic larvae in the Sound (Øresund). Meddelelser fra Kommissionen for Danmarks Fiskeri-og Havundersøgelser. Serie: Plankton, 4, 1–523.Google Scholar
Thorson, G., 1950. Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews, 25, 1–45.CrossRefGoogle ScholarPubMed
Verdonk, N.H. & Cather, J.N., 1983. Morphogenetic determination and differentiation. In The Mollusca, vol. III. Development (ed. A.S., Tompaet al.), pp. 215–252. London: Academic Press.Google Scholar
Verdonk, N.H. & Biggelaar, J.A.M. van den, 1983. Early development and the formation of the germ layers. In The Mollusca, vol. III. Development (ed. A.S., Tompaet al.), pp. 91–122. London: Academic Press.Google Scholar
Verduin, A., 1977. On a remarkable dimorphism of the apices in many groups of sympatric, closely related marine gastropod species. Basteria, 41, 91–95.Google Scholar