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Some aspects of the oogenesis of three species of clathrinid sponges (Calcarea, Porifera)

Published online by Cambridge University Press:  24 August 2015

Emilio Lanna  and
Michelle Klautau
Emilio Lanna
Affiliation:
Universidade Federal da Bahia, Instituto de Biologia, Departamento de Biologia Geral, Rua Barão de Jeremoabo s/n, Campus de Ondina, Salvador, BA, Brazil Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, 21941902, Rio de Janeiro, RJ, Brazil
Michelle Klautau*
Affiliation:
Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, 21941902, Rio de Janeiro, RJ, Brazil
*
Correspondence should be addressed to:M. Klautau, Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, 21941902, Rio de Janeiro, RJ, Brazil email: mklautau@biologia.ufrj.br
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Abstract

Although oogenesis is the best-known stage of development in sponges of the subclass Calcinea (Porifera, Calcarea), several aspects of this process await further investigation. In the present study, we examined by light and electron microscopy the oogenesis of three species of the order Clathrinida (Clathrina aurea, Borojevia aspina and B. brasiliensis) from the coast of Rio de Janeiro state (Brazil). Oogenesis in these species was a rare and not synchronized event, neither in the individual nor in the population level. Oocytes grew between the choanoderm and the pinacoderm. They did not form any special structure for nourishing the egg and phagocytosis of somatic cells was not observed. The vitellogenesis of B. aspina and B. brasiliensis was performed in a mixed pathway, while in C. aurea it was not possible to observe the vitellogenesis. In the Borojevias, the surrounding choanocytes provided small clear vesicles at the same time that oocytes modified phagosomes to produce fibrous yolk inclusions. The phylogenetic character mapping analysis indicated that egg development in the mesohyl is the ancestral state for Calcinea, while the ancestral condition of the vitellogenesis is still uncertain.

Keywords

ReproductionvitellogenesisSouth-western Atlanticevolutionmixed yolk pathway
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 2: Proceedings of the 9th World Sponge Conference held in Fremantle Australia in 2013: New Frontiers in Sponge Science , March 2016 , pp. 529 - 539
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Anakina, R.P. and Drozdov, A.L. (2001) Gamete structure and fertilization in the Barents Sea sponge Leucosolenia complicata. Russian Journal of Marine Biology 27, 143–150.CrossRefGoogle Scholar
Borojevic, R. (1969) Étude du développement et de la différenciation cellulaire d'éponges calcaires calcinéennes (genres Clathrina et Ascandra). Annales d'Embryologie et de Morphogenèse 2, 15–36.Google Scholar
Dendy, A. (1913) Report on the Calcareous sponges collected by H.M.S. Sealark in the Indian Ocean. Transactions of the Linnean Society of London – Zoology 16, 1–29.CrossRefGoogle Scholar
Eckelbarger, K.J. (1994) Diversity of metazoan ovaries and vitellogenic mechanisms: implications for life history theory. Proceedings of the Biological Society of Washington 107, 193–218.Google Scholar
Eckelbarger, K.J. (2005) Oogenesis and oocytes. Hydrobiologia 535, 179–198.Google Scholar
Eckelbarger, K.J. and Larson, R. (1992) Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa. Marine Biology 114, 633–643.CrossRefGoogle Scholar
Ereskovsky, A.V. (2010) The comparative embryology of sponges. Dordrecht: Springer.CrossRefGoogle Scholar
Ereskovsky, A.V. and Willenz, P. (2008) Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127, 175–187.CrossRefGoogle Scholar
Extavour, C.G. and Akam, M. (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130, 5869–5884.CrossRefGoogle ScholarPubMed
Fernandes, L.D.d.A., Quintanilha, J., Monteiro-Ribas, W., Gonzalez-Rodriguez, E. and Coutinho, R. (2012) Seasonal and interannual coupling between sea surface temperature, phytoplankton and meroplankton in the subtropical south-western Atlantic Ocean. Journal of Plankton Research 34, 236–244.CrossRefGoogle Scholar
Franzén, W. (1988) Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea). Zoomorphology 107, 349–357.CrossRefGoogle Scholar
Gaino, E., Burlando, B. and Buffa, P. (1987) Ultrastructural study of oogenesis and fertilization in Sycon ciliatum (Porifera: Calcispongiae). International Journal of Invertebrate Reproduction and Development 11, 73–82.CrossRefGoogle Scholar
Gaino, E., Pansini, M., Pronzato, R. and Cicogna, F. (1991) Morphological and structural variations in Clathrina clathrus (Porifera, Calcispongiae). In Reitner, J. and Keupp, H. (eds) Fossil and recent sponges. Berlin: Springer-Verlag, pp. 360–371.CrossRefGoogle Scholar
Gaino, E. and Sarà, M. (1994) An ultrastructural comparative study of the eggs of two species of Tethya (Porifera, Demospongiae). Invertebrate Reproduction and Development 26, 99–106.CrossRefGoogle Scholar
Gallissian, M.F. (1981) Étude ultrastructurale de l'ovogenèse chez quelques éponges calcaires (Porifera, Calcarea). Archives de Zoologie Expérimentale et Générale 122, 329–340.Google Scholar
Gilbert, S. (2010) Developmental Biology, 9th edn.Sunderland, MA: Sinauer Associates.Google Scholar
Gilis, M., Gosselin, P., Dubois, P. and Willenz, P. (2011) Seasonal modifications and morphogenesis of the hypercalcified sponge Petrobiona massiliana (Calcarea, Calcaronea). Invertebrate Biology 130, 193–210.CrossRefGoogle Scholar
Hadzi, J. (1917) Rezultati bioloskih istrazivanja Jadranskoga mora. Porifera. Calcarea I. Clathrina blanca (Miklucho–Maclay); grada i razvoj s osobitim obzirom na opca pitanja o spuzvama. Prirod Istraziv Juguslav Akad Znaon Umjet Zagreb 9–10, 1–168.Google Scholar
Johnson, M.F. (1979) Gametogenesis and embryonic development in the calcareous sponges Clathrina coriacea and Clathrina blanca from Santa Catalina Island, California. Bulletin of the Southern California Academy of Sciences 78, 183–191.Google Scholar
Klautau, M., Azevedo, F., Cóndor–Luján, B., Rapp, H.T., Collins, A. and Russo, C.A.M. (2013) A molecular phylogeny for the order Clathrinida rekindles and refines Haeckel's taxonomic proposal for calcareous sponges. Integrative and Comparative Biology 53, 447–461.CrossRefGoogle ScholarPubMed
Klautau, M., Solé-Cava, A.M. and Borojevic, R. (1994) Biochemical systematics of sibling sympatric species of Clathrina (Porifera, Calcarea). Biochemical Systematics and Ecology 22, 367–375.CrossRefGoogle Scholar
Klautau, M. and Valentine, C. (2003) Revision of the genus Clathrina (Porifera, Calcarea). Zoological Journal of the Linnean Society 139, 1–62.CrossRefGoogle Scholar
Lanna, E. and Klautau, M. (2010) Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea). Zoomorphology 129, 249–261.CrossRefGoogle Scholar
Lanna, E. and Klautau, M. (2012) Embryogenesis and larval ultrastructure in Paraleucilla magna (Calcarea, Calcaronea), with remarks on the epilarval trophocyte epithelium (‘placental membrane’). Zoomorphology 131, 277–292.CrossRefGoogle Scholar
Lanna, E., Paranhos, R., Paiva, P.C. and Klautau, M. (2014) Environmental effects on the reproduction and fecundity of the introduced calcareous sponge Paraleucilla magna in Rio de Janeiro, Brazil. Marine Ecology. doi:10.1111/maec.12202.Google Scholar
Maddison, W.P. and Maddison, D.R. (2014) Mesquite: a modular system for evolutionary analysis. Version 3.0 http://mesquiteproject.org.Google Scholar
Maldonado, M. and Riesgo, A. (2008) Reproduction in Porifera: a synoptic overview. Treballs de la Societat Catalana de Biologia 59, 29–49.Google Scholar
Minchin, E.A. (1900) Éponges calcaires. In Boutan, L. (ed) Zoologie descriptive. Paris: Octave Doin Editeur, pp. 107–147.Google Scholar
Muricy, G., Lopes, D.A., Hajdu, E., Carvalho, M.S., Moraes, F.C., Klautau, M., Menegola, C. and Pinheiro, U. (2011) Catalogue of Brazilian porifera. Rio de Janeiro: Museu Nacional.Google Scholar
Pavans-de-Ceccatty, M. (1955) Le système nerveux des éponges calcaires et siliceuses. Annales des Sciences Naturelles, Zoologie 17, 206–288.Google Scholar
Ramirez-Llodra, E. (2002) Fecundity and life-history strategies in marine invertebrates. Advances in Marine Biology 43, 87–170.CrossRefGoogle ScholarPubMed
Riesgo, A. and Maldonado, M. (2009) Ultrastructure of oogenesis of two oviparous demosponges: Axinella damicornis and Raspaciona aculeata (Porifera). Tissue and Cell 41, 51–65.CrossRefGoogle ScholarPubMed
Rossi, A.L., Russo, C.A.M., Solé-Cava, A.M., Rapp, H.T. and Klautau, M. (2011) Phylogenetic signal in the evolution of body colour and spicule skeleton in calcareous sponges. Zoological Journal of the Linnean Society 163, 1026–1034.CrossRefGoogle Scholar
Sarà, M. (1955) La nutrizione dell'ovocita in calcispongie omoceli. Annuario dell' Instituto e Museo di Zoologia dell'Università di Napoli 7, 1–30.Google Scholar
Sciscioli, M., Lepore, E., Gherardi, M. and Scalera Liaci, L. (1994) Transfer of symbiotic bacteria in the mature oocyte of Geodia cydonium (Porifera, Demospongiae): an ultrastructural study. Cahiers de Biologie Marine 35, 471–478.Google Scholar
Sciscioli, M., Scalera Liaci, L., Lepore, E., Gherardi, M. and Simpson, T.L. (1991) Ultrastructural study of the mature egg of the marine sponge Stelletta grubii (Porifera, Demospongiae). Molecular Reproduction and Development 28, 346–350.CrossRefGoogle ScholarPubMed
Simpson, T.L. (1984) The cell biology of sponges. New York, NY: Springer-Verlag.CrossRefGoogle Scholar
Tuzet, O. (1948) Les premiers stades du développement de Leucosolenia botryoides Ellis et Sollander et de Clathrina (Leucosolenia) coriacea Mont. Annales des Sciences Naturelles, Zoologie et Biologie Animale 10, 103–114.Google Scholar
Vacelet, J. (1964) Étude monographique de l’éponge calcaire pharétronide de la Méditerranée, Petrobiona massiliana Vacelet et Lévi. Les pharétronides actuelles et fossiles. Recueil des Travaux de la Station Marine d'Endoume 34, 1–125.Google Scholar
Voigt, O., Wülfing, E. and Wörheide, G. (2012) Molecular phylogenetic evaluation of classification and scenarios of character evolution in calcareous sponges (Porifera, Class Calcarea). PloS ONE 7, 1–16.CrossRefGoogle ScholarPubMed