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Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea)

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Abstract

Larval development and follicle structure of a representative of the Calcinea (Calcispongiae) Guancha arnesenae from the White Sea have been studied for the first time at the ultrastructural level. The follicle in G. arnesenae has an unusual structure: it consists of trapezoid cells rich in phagosomes and a surrounding dense collagen layer. Follicular cells differentiate from choanocytes. Cleavage results in formation of a hollow, equal, non-polarized coeloblastula. Larval morphogenesis occurs by means of direct hollow blastula formation without any individual cell or cell layer movements. The coeloblastula (calciblastula) larva of G. arnesenae is completely ciliated. The larva also contains rare non-ciliated cells: vacuolar cells, bottle-shaped cells and free cells in a central cavity. The basal ciliary apparatus of larval cells includes the basal body, an accessory centriole oriented perpendicularly to it, the basal foot, and two cross-striated rootlets. A bundle of microtubules emerges from the side of the basal body, opposite to the basal foot, running parallel to the outer surface. All bundles of cells are parallel to each other and oriented towards the posterior larval pole, forming a transverse cytoskeletal system. Specialized intercellular junctions in the apical regions of all ciliated cells are revealed for the first time in a Calcispongiae larva. The central larval cavity contains symbiotic bacteria, which are included inside the embryo at the blastula stage.

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References

  • Adams CL, McInerney JO, Kelly M (1999) Indications of relationships between poriferan classes using full-length 18S rRNA gene sequences. Mem Queensl Mus 44:33–43

    Google Scholar 

  • Amano S, Hori I (1992) Metamorphosis of calcareous sponges. 1. Ultrastructure of free-swimming larvae. Invertebr Reprod Dev 21:81–90

    Google Scholar 

  • Amano S, Hori I (1993) Metamorphosis of calcareous sponges. II. Cell rearrangement and differentiation in metamorphosis. Invertebr Rep Dev 24:13–26

    Google Scholar 

  • Amano S, Hori I (2001) Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa. Biol Bull 200:20–32

    Article  PubMed  CAS  Google Scholar 

  • Bergquist PR, Sinclair ME, Green CR, Silyn-Roberts H (1979) Comparative morphology and behavior of larvae of Demospongiae. In: Lévi C, Boury-Esnault N (eds) Biologie des spongiaires, vol 291. Editions du C.N.R.S, Paris, pp 103–112

    Google Scholar 

  • Bidder GP (1898) The skeleton and classification of calcareous sponge. Proc R Soc Lond 64:61–76

    Article  Google Scholar 

  • Borchiellini C, Manuel M, Boury-Esnault N, Vacelet J, Le Parco Y (2001) Sponge paraphyly and the origin of Metazoa. J Evol Biol 14:171–179

    Article  Google Scholar 

  • Borojevic R (1967) La ponte et le développement de Polymastia robusta (Démosponges). Cah Biol Mar 8:1–6

    Google Scholar 

  • Borojevic R (1969) Etude du développement et de la différenciation cellulaire d’éponges calcinéennes (genre Clathrina et Ascandra). Ann Embryol Morphol 2:15–36

    Google Scholar 

  • Borojevic R (1970) Différentiation cellulaire dans l’embryogénèse et la morphogénèse chez les Spongiaires. In: Fry WG (ed) The biology of the Porifera, vol 25. Academic Press, London, pp 467–490

    Google Scholar 

  • Boury-Esnault N, Rützler K (eds) (1997) Thesaurus of sponge morphology. Smithson Contrib Zool 596:1–55

  • Boury-Esnault N, Ereskovsky AV, Bezac C, Tokina D (2003) Larval development in Homoscleromorpha (Porifera, Demospongiae) first evidence of basal membrane in sponge larvae. Invertebr Biol 122:187–202

    Google Scholar 

  • Cavalier-Smith T, Allsopp MEP, Chao EE, Boury-Esnault N, Vacelet J (1996) Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rDNA evidence. Can J Zool 74:2031–2045

    Article  CAS  Google Scholar 

  • Collins AG (1998) Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc Natl Acad Sci USA 95:15458–15463

    Article  PubMed  CAS  Google Scholar 

  • Dendy A (1891) Studies on the comparative anatomy of Sponges. III. On the anatomy of Grantia labyrinthica, and the so-called family Teichonidae. Q J Microsc Sci 32:1–39

    Google Scholar 

  • Dendy A, Frederick LM (1924) On a collection of sponges from the Abrolhos Islands, Western Australia. J Linn Soc Lond Zool 35:477–519

    Article  Google Scholar 

  • Dohrmann M, Voigt O, Erpenbeck D, Wörheide G (2006) Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA. Mol Phylogenet Evol 40:830–843

    Article  PubMed  CAS  Google Scholar 

  • Elliott GRD, Macdonald TA, Leys SP (2004) Sponge larval phototaxis: a comparative study. Boll Mus Ist Biol Univ Genova 68:291–300

    Google Scholar 

  • Ereskovsky AV (2002) Polyaxial cleavage in sponges (Porifera): a new pattern of metazoan cleavage. Dokl Biol Sci 386:472–474

    Article  PubMed  CAS  Google Scholar 

  • Ereskovsky AV (2004) Comparative embryology of sponges and its application for poriferan phylogeny. Boll Mus Ist Biol Univ Genova 68:301–318

    Google Scholar 

  • Ereskovsky AV (2005) Comparative embryology of sponges (Porifera). Saint-Petersburg University Press, Saint-Petersburg

    Google Scholar 

  • Ereskovsky AV, Tokina DB (2004) Morphology and fine structure of the swimming larvae of Ircinia oros (Porifera, Demospongiae, Dictyoceratida). Invertebr Reprod Dev 45:137–150

    Google Scholar 

  • Gallissian MF, Vacelet J (1992) Ultrastructure of the oocyte and embryo of the calcified sponge, Petrobiona massiliana (Porifera, Calcarea). Zoomorphology 112:133–141

    Article  Google Scholar 

  • Gonobobleva EL, Ereskovsky AV (2004a) Polymorphism in free swimming larvae of Halisarca dujardini (Demospongiae, Halisarcida). Boll Mus Ist Biol Univ Genova 68:349–356

    Google Scholar 

  • Gonobobleva EL, Ereskovsky AV (2004b) Metamorphosis of the larva of Halisarca dujardini (Demospongiae, Halisarcida). Bull Inst r Sci nat Belgique Biol 74:101–115

    Google Scholar 

  • Green CR, Bergquist PR (1979) Cell membrane specializations in the Porifera. In: Lévi C, Boury-Esnault N (eds) Biologie des spongiaires, vol 291. Editions du C.N.R.S, Paris, pp 153–158

    Google Scholar 

  • Hartman WD (1958) A re-examination of Bidder’s classification of the Calcarea. Syst Zool 7:55–109

    Article  Google Scholar 

  • Johnson MF (1978) Studies on the reproductive cycles of the calcareous sponges Clathrina coriacea and C. blanca. Mar Biol 50:73–79

    Article  Google Scholar 

  • Johnson MF (1979) Gametogenesis and embryonic development in the calcareous sponges Clathrina coriacea and C. blanca from Santa Catalina Island, California. Bull South Calif Acad Sci 78:183–191

    Google Scholar 

  • Klautau M, Valentine C (2003) Revision of the genus Clathrina (Porifera, Calcarea). Zool J Linn Soc 139:1–62

    Article  Google Scholar 

  • Kruse M, Leys SP, Müller IM, Müller WEG (1998) Phylogenetic position of the Hexactinellida within the phylum Porifera based on the amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. J Mol Evol 46:721–728

    Article  PubMed  CAS  Google Scholar 

  • Ledger PW (1975) Septate junctions in the Calcareous sponge Sycon ciliatum. Tissue Cell 7:13–18

    Article  PubMed  CAS  Google Scholar 

  • Lévi C (1956) Étude des Halisarca de Roscoff. Embryologie et systématique des Démosponges. Trav Stat Biol Roscoff NS 7:3–181

    Google Scholar 

  • Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Can J Zool 84:262–287

    Article  Google Scholar 

  • Maldonado M (2004) Choanoflagellates, choanocytes, and animal multicellularity. Invert Biol 123:1–22

    Google Scholar 

  • Maldonado M, Bergquist PR (2002) Phylum Porifera. In: Young CM, Sewel MA, Rice ME (eds) Atlas of marine invertebrate larvae. Academic Press, Barcelona, pp 21–50

    Google Scholar 

  • Manuel M (2006) Phylogeny and evolution of calcareous sponges. Can J Zool 84:225–241

    Article  Google Scholar 

  • Manuel M, Borojevic R, Boury-Esnault N, Vacelet J (2002) Class Calcarea. In: Hooper JNA, van Soest RWM (eds) Systema Porifera: a guide to the supraspecific classification of the phylum Porifera, vol 2. Kluwer /Plenum, New York, pp 1103–1110

    Google Scholar 

  • Manuel M, Borchiellini C, Alivon E, Le Parco Y, Vacelet J, Boury-Esnault N (2003) Phylogeny and evolution of calcareous sponges: monophyly of Calcinea and Calcaronea, high level of morphological homoplasy, and the primitive nature of axial symmetry. Syst Biol 52:311–333

    Article  PubMed  Google Scholar 

  • Manuel M, Borchiellini C, Alivon E, Boury-Esnault N (2004) Molecular phylogeny of calcareous sponges using 18S rRNA and 28S rRNA sequences. Boll Mus Ist Biol Univ Genova 68:449–461

    Google Scholar 

  • Medina M, Collins AG, Silberman JD, Sogin ML (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci USA 98:9707–9712

    Article  PubMed  CAS  Google Scholar 

  • Metschnikoff E (1879) Spongiologische Studien. Z Wiss Zool 32:349–387

    Google Scholar 

  • Minchin EA (1896) Note on the larva and the postlarval development of Leucosolenia variabilis n. sp., with remarks on the development of other Asconidae. Proc R Soc Lond 60:43–52

    Google Scholar 

  • Minchin EA (1900) The Porifera and Coelenterata. Adam and Charles Black, London

    Google Scholar 

  • Nielsen C (2008) Six major steps in animal evolution: are we derived sponge larvae? Evol Dev 10:241–257

    PubMed  Google Scholar 

  • Rapp HT (2006) Calcareous sponges of the genera Clathrina and Guancha (Calcinea, Calcarea, Porifera) of Norway (north-east Atlantic) with the description of five new species. Zool J Linn Soc 147:331–365

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rieger RM (1994) Evolution of the “lower” Metazoa. In: Bengston S (ed) Early life on Earth, Nobel Symp, vol 84. Columbia University Press, New York, pp 475–488

  • Sanderson MJ (1984) Cilia. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. Springer, Berlin, pp 17–42

    Google Scholar 

  • Sarà M (1955) La nutrizione dell’ovocita in Calcispongie Omoceli. Ann Ist Mus Zool Univ Napoli 7:1–30

    Google Scholar 

  • Schmidt O (1877) Das Larvenstadium von Ascetta primordialis und Ascetta clathrus. Arch Mikrobiol Anat 14:249–263

    Article  Google Scholar 

  • Schreiber A, Wörheide G, Thiel V (2006) The fatty acids of calcareous sponges (Calcarea, Porifera). Chem Phys Lipids 143:29–37

    Article  PubMed  CAS  Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer, New York

    Google Scholar 

  • Tuzet O (1948) Les premiers stades du développement de Leucosolenia botryoides Ellis et Solander et de Clathrina (Leucosolenia) coriacea Mont. Ann Sci Nat 10:103–113

    Google Scholar 

  • Usher K, Ereskovsky AV (2005) Larval development, ultrastructure and metamorphosis in Chondrilla australiensis Carter, 1873 (Demospongiae, Chondrosida, Chondrillidae). Invertebr Reprod Dev 47:51–62

    Google Scholar 

  • Vacelet J (1967) Descriptions d’éponges Pharétronides actuelles des tunnels obscurs sous- récifaux de Tuléar (Madagascar). Rec Trav Stat Mar d’Endoume Suppl 6:37–62

    Google Scholar 

  • Vacelet J (1977) Eponges Pharétronides actuelles et Sclérosponges de Polynésie Française, Madagascar et de La Réunion. Bull Mus Nat Hist Nat Paris 444:345–366

    Google Scholar 

  • Wapstra M, van Soest RWM (1897) Sexual reproduction, larval morphology and behaviour in Demosponges from the southwest of the Netherlands. In: Boury-Esnault N, Vacelet J (eds) Taxonomy of Porifera. NATO ASI Ser 13, pp 281–307

  • Woollacott RM, Pinto RL (1995) Flagellar basal apparatus and its utility in phylogenetic analyses of the Porifera. J Morphol 226:247–265

    Article  Google Scholar 

  • Wörheide G, Hooper JNA (1999) Calcarea from the Great Barrier Reef, 1: cryptic Calcinea from Heron Island and Wistari Reef (Capricorn-Bunker Group). Mem Queensl Mus 43:859–891

    Google Scholar 

  • Wörheide G, Hooper JNA (2003) New species of Calcaronea (Porifera: Calcarea) from cryptic habitats of the southern Great Barrier Reef (Heron Island and Wistari Reef, Capricorn-Bunker Group, Australia). J Nat Hist 37:1–47

    Article  Google Scholar 

  • Zrzavý J, Mihulka S, Kepka P, Bezdĕk A, Tietz D (1998) Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249–285

    Google Scholar 

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Acknowledgments

The authors are warmly grateful to Dr. Jean Vacelet and Dr. Nicole Boury-Esnault Centre d’Océanologie de Marseille, for helpful discussions, to Dr. Patrick Flammang, Marine Biology Laboratory, University of Mons-Hainaut, Belgium, for permitting use of the TEM in his laboratory, to J. Cillis and L. Despontin, Royal Belgian Institute of Natural Sciences, for assistance with semi-thin sections and SEM preparations, and to Natalia Lentsman for improving the English. The work of A. Ereskovsky at the Royal Belgian Institute of Natural Sciences was made possible by a grant from the Belgian Federal Science Policy Office. This work was also financially supported partially by the Russian Foundation for Basic Research (grant no. 06–04-48660) and by grant of Marie Curie IIF MIF1-CT-2006-040065.

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  1. Centre d’Océanologie de Marseille, Station marine d’Endoume, Aix-Marseille Université, CNRS UMR 6540-DIMAR, rue de la Batterie des Lions, 13007, Marseille, France

    Alexander V. Ereskovsky

  2. Department of Embryology, Faculty of Biology and Soils, Saint-Petersburg State University, Universitetskaja nab. 7/9, St. Petersburg, 199034, Russia

    Alexander V. Ereskovsky

  3. Department of Invertebrates, Royal Belgian Institute of Natural Sciences, 29 rue Vautier, 1000, Brussels, Belgium

    Philippe Willenz

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Correspondence to Alexander V. Ereskovsky.

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Ereskovsky, A.V., Willenz, P. Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127, 175–187 (2008). https://doi.org/10.1007/s00435-008-0061-9

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  • DOI: https://doi.org/10.1007/s00435-008-0061-9

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