Skip to main content
SpringerLink
Log in

Micromorphology and ultrastructure of Caribbean sclerosponges

I. Ceratoporella nicholsoni and Stromatospongia norae (Ceratoporellidae: Porifera)

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Fine structural analysis of living tissue of the sclerosponges Ceratoporella nicholsoni (Hickson) and Stromatospongia norae Hartman, collected near Discovery Bay, Jamaica, between 1984 and 1986, was carried out using transmission and scanning electron microscopy (TEM and SEM). The thick dermal membrane of these sponges is covered by exopinacocytes having a “T” shape in sections perpendicular to the surface. A dense, complex glycocalyx is produced at the surface of these cells. Choanocyte chambers are diplodal and unusually small. The inhalant and exhalant canals of both species are characterized by the presence of valvules, made by transverse lamellipodial processes of the endopinacocytes lining them. An abundant and diversified bacterial community occupies almost 20% of the mesohyl. A single layer of active basopinacocytes lines the mesohyl at the interface between the living tissue and the aragonitic skeleton. Basopinacocytes are presumed to be precursors of the irregular fibrillar organic matrix found in the aragonitic skeleton. Sclerocytes and spongocytes are abundant in the vicinity of the siliceous spicules. Typical lophocytes releasing smooth collagen fibrils are common in the dermal membrane as well as in the choanosome where they can be grouped in bundles. Uniquely, C. nicholsoni elaborates rough intercellular fibrils characterized by periodically spaced thickenings. The endolithic algae Ostreobium sp. is present in the most apical zones of the aragonitic skeleton, but does not seem to interfere with its development. The striking micromorphological resemblances between both species are discussed and compared to demosponges.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Anderson, H. C. (1980). Calcification processes. Path. An. 2: 45–75

    Google Scholar 

  • Bagby, R. M. (1970). The fine structure of pinacocytes in the marine sponge Microciona prolifera (Ellis and Solander). Z. Zellforsch. 105: 579–594

    Google Scholar 

  • Bertrand, J.-C., Vacelet, J. (1971). L'Association entre éponges cornées et bactéries. C. r. hebd. Séanc. Acad. Sci., Paris (Sér. D) 273: 638–641

    Google Scholar 

  • Bevelander, G., Nakahara, H. (1969). An electron microscopic study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calcif. Tissue Res. 3: 84–92

    Google Scholar 

  • Boury-Esnault, N. (1973). L'exopinacoderme des spongiaires. Bull. Mus. natn. Hist. nat., Paris (Sér. 3) No. 178 (Zool. 117): 1193–1206

  • Boury-Esnault, N., De Vos, L., Donadey, C., Vacelet, J. (1984). Comparative study of the choanosome of Porifera: 1. The Homoscleromorpha. J. Morph. 180: 3–17

    Google Scholar 

  • Boury-Esnault, N., De Vos, L., Donadey, C., Vacelet, J. (in press). Ultrastructure of choanosomes and sponge classification. Proc. 3rd int. Conf. Biol. Sponges, Woods Hole, Massachusetts, November 1985

  • Brien, P. (1973). Les Démosponges. In: Grassé, P.-P. (ed.) Traité zool., Vol. III. Masson et Cie, Paris, Fasc. 1: 133–461

    Google Scholar 

  • Bubel, A. (1975). An ultrastructural study of the mantle of the barnacle, Elminius modestus Darwin in relation to the shell formation. J. exp. mar. Biol. Ecol. 20: 287–324

    Google Scholar 

  • Crenshaw, M. A. (1980). Mechanisms of shell formation and dissolution. In: Rhoads, D. C., Lutz, R. A. (eds.) Skeletal growth of aquatic orgaisms. Biological records of environmental change. Plenum Press, New York, p. 115–132

    Google Scholar 

  • Donadey, C. (1979). Contribution à l'étude cytologique de deux démosponges Homosclerophorides: Oscarella lobularis (Schmidt) et Plakina trilopha Schulze. In: Lévi, C., Boury-Esnault N. (eds.) Biologie des spongiares. Coll. int. C. N. R. S. 291: 165–172

  • Donadey, C. (1982). Les cellules pigmentaires et les cellules à inclusions de l'éponge Cacospongia scalaris (Démosponge Dictyoceratide). Vie mar. 4: 67–74

    Google Scholar 

  • Duboscq, O., Tuzet, O. (1939). Les amebocytes et les cellules germinales des éponges calcaires. Mém. Mus. r. Hist. nat. Belg. 3: 209–226

    Google Scholar 

  • Dunkelberger, D. G., Watabe, N. (1974). An ultrastructural study on spicule formation in the pennatulid colony Renilla reniformis. Tissue Cell 6: 573–586

    Google Scholar 

  • Eisenman, E. A., Alfert, M. (1981). A new fixation procedure for preserving the ultrastructure of marine invertebrate tissues. J. Microscopy 125: 117–120

    Google Scholar 

  • Erben, H. K. (1972). Über die Bildung und das Wachstum von Perlmutt. ForschBer. Biomineralis. Akad. Wiss. Lit., Mainz (Biomineraliz. Res. Rep.) 4: 15–46

    Google Scholar 

  • Erben, H. K. (1974). On the structure and growth of the nacreous tablets in gastropods. ForschBer. Biomineralis. Akad. Wiss. Lit., Mainz (Biomineraliz. Res. Rep.) 7: 14–27

    Google Scholar 

  • Erben, H. K., Watabe, N. (1974) Crystal formation and growth in bivalve nacre. Nature, Lond. 248: 128–130

    Google Scholar 

  • Evans, C. W. (1977). The ultrastructure of larvae from the marine sponge Halichondria moorei Bergquist (Porifera, Demospongiae). Cah. Biol. mar. 18: 427–433

    Google Scholar 

  • Fullmer, H. M., (1966). Histochemical studies of mineralized tissues. Annls Histochim 11: 369–374

    Google Scholar 

  • Garrone, R. (1969). Collagene, spongine et squelette minéral chez l'éponge Haliclona rosea (O.S.) (Démosponge, Haploscléride). J. Microscopie 8: 581–598

    Google Scholar 

  • Garrone, R. (1978). Phylogenesis of connective tissue. In: Robert, L. (ed.) Frontiers of matrix biology. S. Karger, Basel, p. 1–250

    Google Scholar 

  • Grégoire, Ch. (1967). Sur la structure des matrices organiques des coquilles de mollusques. Biol. Rev. 42: 653–687

    Google Scholar 

  • Hartman, W. D. (1969). New genera and species of coralline sponges (Porifera) from Jamaica. Postilla 13: 1–39

    Google Scholar 

  • Hartman, W. D., Goreau, T. F. (1970). Jamaican coralline sponges: Their morphology, ecology and fossil relatives. Symp. zool. Soc. Lond. 25: 205–243

    Google Scholar 

  • Hartman, W. D., Goreau, T. F. (1972). Ceratoporella (Porifera: Sclerospongiae) and the chaetetid “corals”. Trans. Conn. Acad. Arts Sci. 44: 133–148

    Google Scholar 

  • Hartman, W. D., Goreau, T. F. (1975). A Pacific tabulate sponge, living representative of a new order of sclerosponges. Postilla 167: 1–21

    Google Scholar 

  • Johnston, I. S. (1977). Aspects of the structure of a skeletal organic matrix, and the process of skeletogenesis in the reef-coral Pocillopora damicornis. Proc. 3rd int. Symp. coral Reefs 2: 447–453 [Taylor, D. L. (ed.) School of marine and Atmospheric Sciences, University of Miami]

    Google Scholar 

  • Johnston, I. S. (1979). The organization of a structural organic matrix within the skeleton of a reef-building coral. S. E. Microsc. 2: 421–431

    Google Scholar 

  • Johnston, I. S. (1980). The ultrastructure of skeletogenesis in hermatypic corals. Int. Rev. Cytol. 67: 171–214

    Google Scholar 

  • Laubenfels, M. W. de (1948). The order Keratosa of the phylym Porifera: a monographic study. Occ. Pap. Allan Hancock Fdn., 3: 1–217

    Google Scholar 

  • Ledger, P. (1976). Aspects of the secretion and structure of calcareous sponge spicules. Thesis, University College North Wales

  • Lévi, C. (1956). Etudes des Halisarca de Roscoff. Embryologie et systématique des Démosponges. Archs Zool. exp. gén. 93: 1–184

    Google Scholar 

  • Lévi, C., Porte, A. (1962). Etude au microscope électronique de l;éponge Oscarella lobularis Schmidt et de sa larve amphiblastula. Cah. Biol. mar. 3: 307–315

    Google Scholar 

  • Luft, J. H. (1971a). Ruthenium red and voilet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat. Rec. 171: 347–368

    Google Scholar 

  • Luft, J. H. (1971b) Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat. Rec. 171: 369–416

    Google Scholar 

  • Lukas, K. J. (1973). Taxonomy and ecology of the endolithic microflora of reef corals with a review of the literature on endolithic microphytes. Ph. D. thesis, University Rhode Island

  • Lukas, K. J. (1974). Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J. Phycol. 10: 331–335

    Google Scholar 

  • Pavans de Ceccaty, M. (1966). Ultrastructures et rapports des cellules mesenchymateuses de type nerveux de l'éponge Tethya lyncurium Lmk. Ann. Sci. Nat. Zool. Biol. Anim. 8: 577–614

    Google Scholar 

  • Pottu-Boumendil, J. (1975). Ultrastructure, cytochimie, et comportements morphogénétiques des cellules de l'éponge Ephydatia mülleri (Lieb.). Thèse, Université Claude Bernard, Lyon

  • Rasmont, R., Rozenfeld, F. (1981). Etude microcinématographique de la formation des chambers choanocytaires chez une éponge d'eau douce. Annls Soc. r. zool. Belg. 111: 33–44

    Google Scholar 

  • Reiswig, H. W. (1975). The aquiferous systems of three marine demospongiae. J. Morph. 145: 493–502

    Google Scholar 

  • Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17: 208–212

    Google Scholar 

  • Simpson, T. L. (1984). The cell biology of sponges. Springer-Verlag, New York

    Google Scholar 

  • Simpson, T. L. (1985). Cortical and endosomal structure of the marine sponge Stelletta grubti. Mar. Biol. 86: 37–45

    Google Scholar 

  • Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26: 31–43

    Google Scholar 

  • Thiney, Y. (1972). Morphologie et cytochimie ultrastructurale de l'oscule d'Hippospongia communis Lmk et de sa régénération. Thèse, Université Calude Bernard, Lyon

  • Tuzet, O. (1973). Eponges calcaires. In: Grassé P.-P. (ed.) Traité de zoologie, Vol. III. Masson et Cie, Paris, Fasc 1: 27–132

    Google Scholar 

  • Vacelet, J. (1964). Etude monographique de l'éponge calcaire pharétronide de Méditerranée, Petrobiona massiliana Vacelet et Lévi. Les Pharétronides actuelles et fossiles. Thèse, Université d'Aix-Marseille

  • Vacelet, J. (1970). Description de cellules à bactéries intranucléaires chez des éponges Verongia. J. Microscopie 9: 333–346

    Google Scholar 

  • Vacelet J. (1971). L'ultrastructure de la cuticule d'éponges cornées du genre Verongia. J. Microscopie 10: 113–116

    Google Scholar 

  • Vacelet, J. (1975). Etude en microscopie électronique de l'association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J. Microscopie Biol. cell. 23: 271–288

    Google Scholar 

  • Vacelet, J. (1979). Description et affinités d'une éponge sphinctozoaire actuelle. In: Lévi, C., Boury-Esnault, N. (eds.) Biologie des spongiaires. Coll. int. C. N. R. S. 291: 483–493

  • Vacelet, J. (1980). Squelette calcaire facultatif et corps de régénération dans le genre Merlia, éponges apparentées aux chaetétidés fossiles. C.r. hebd. Séanc. Acad. Sci., Paris, (Sér. D) 290: 227–230

    Google Scholar 

  • Vacelet, J. (1985). Coralline sponges and the evolution of Porifera. In: Morris, S. C., George, J. D., Gibson, R., Platt, H. M. (eds.) The origins and relationships of lower invertebrates. The Systematics Association, Vol. 28, p. 1–13

  • Vacelet, J., Boury-Esnault, N., De Vos, L., Donadey, C. (1989). Comparative study of the choanosome of Porifera: II. The Keratose sponges. J. Morph. 201: 119–129

    Google Scholar 

  • Vacelet, J., Donadey, C. (1977). Electron microscope study of the association between some sponges and bacteria. J. exp. mar. Biol. Ecol. 30: 301–314

    Google Scholar 

  • Vacelet, J., Garrone, R. (1985). Two distinct populations of collagen fibrils in a “sclerosponge” (Porifera). In: Bairati, A., Garrone, R. (eds.) Biology of invertebrate and lower vertebrate collagens. NATO ASI series. Series A, Life sciences Plenum Press, New York, 93: 183–189

    Google Scholar 

  • Wilbur, K. M., Saleuddin, A. S. M. (1983). Shell formation. In: Saleuddin, A. S. M., Wilbur, K. M. (eds.) The mollusca. Vol. 4 Physiology, Part 1. Academic Press, New York, p. 235–287

    Google Scholar 

  • Wilkinson, C. R. (1978). Microbial associations in sponges. II Numerical analysis of sponge and water bacterial populations. Mar. Biol. 49: 169–176

    Google Scholar 

  • Willenz, Ph. (1983). Aspects cinétiques, quantitatifs et ultrastructuraux de l'endocytose, la digestion et l'exocytose chez les éponges. Thèse, Université Libre de Bruxelles

  • Willenz, Ph., Van de Vyver, G. (1982). Endocytosis of latex beads by the exopinacoderm in the freshwater sponge Ephydatia fluviatilis: an in vitro and in situ study in SEM and TEM. J. Ultrastruct. Res. 79: 294–306

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biologie Animale et Cellulaire, Université Libre de Bruxelles, 50 Avenue F. Roosevelt, B-1050, Bruxelles, Belgium

    Ph. Willenz

  2. Peabody Museum of Natural History, Yale University, 170 Whitney Avenue, P.O. Box 6666, 06511, New Haven, Connecticut, USA

    W. D. Hartman

Authors
  1. Ph. Willenz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. D. Hartman
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Contribution no. 472 from the Discovery Bay Marine Laboratory, University of the West Indies, Discovery Bay, Jamaica, West Indies

Rights and permissions

Reprints and permissions

About this article

Cite this article

Willenz, P., Hartman, W.D. Micromorphology and ultrastructure of Caribbean sclerosponges. Mar. Biol. 103, 387–401 (1989). https://doi.org/10.1007/BF00397274

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00397274

Keywords

Search

Navigation