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Reproductive cycle and larval characteristics of the sponge Haliclona indistincta (Porifera: Demospongiae)

Published online by Cambridge University Press:  31 October 2012

Kelly M.M. Stephens ,
John Galvin ,
Albert Lawless  and
Grace P. McCormack
Kelly M.M. Stephens
Affiliation:
Zoology, Ryan Institute, School of Natural Sciences, National University of Ireland, Galway, Ireland
John Galvin
Affiliation:
Zoology, Ryan Institute, School of Natural Sciences, National University of Ireland, Galway, Ireland
Albert Lawless
Affiliation:
Zoology, Ryan Institute, School of Natural Sciences, National University of Ireland, Galway, Ireland
Grace P. McCormack*
Affiliation:
Zoology, Ryan Institute, School of Natural Sciences, National University of Ireland, Galway, Ireland
*
Correspondence should be addressed to: G.P. McCormack, Zoology, Ryan Institute, School of Natural Sciences, National University of Ireland, Galway, Ireland email: [email protected]
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Abstract

Haliclona indistincta has in some respects, a typical reproductive cycle for a marine haplosclerid sponge. We suggest that oocytes originate from archaeocytes and that spermatozoa originate from choanocytes. Oocytes were first seen in November and matured as eggs by May and June. Immature spermatic cysts were identified from February and mature cysts were present in May and June only. Of the individuals surveyed that had reproductive elements present (150/200), reproductive elements from a single sex were reported in over half of the specimens (59%) but there were also many hermaphrodites (41%). Embryos were first seen in June. Larvae were distributed throughout the mesohyl and were released from the end of June to the end of July. Three mobile larval stages and fusing of sibling larvae were observed. Post-settlement stages from early settlement to the development of oscula and excurrent canals are also shown. However, some elements of the larvae (uniform ciliation and no spicules at posterior pole) are not consistent with larvae from this genus.

Keywords

Haliclona indistinctamarine spongePoriferareproductionlarval morphologyhistologymicroscopy
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 4 , June 2013 , pp. 899 - 907
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012 

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References

REFERENCES

Amano, S. (1986) Larval release in response to a light signal by the intertidal sponge Halichondria panicea. Biological Bulletin. Marine Biological Laboratory, Woods Hole 171, 371–378.CrossRefGoogle Scholar
Ayling, A.L. (1980) Patterns of sexuality, asexual reproduction and recruitment in some subtidal marine Demospongiae. Biological Bulletin. Marine Biological Laboratory, Woods Hole 158, 271–282.CrossRefGoogle Scholar
Barthel, D. and Detmer, A. (1990) The spermatogenesis of Halichondria panicea (Porifera, Demospongiae). Zoomorphology 110, 9–15.CrossRefGoogle Scholar
Bergquist, P.R. (1978) Sponges. Los Angeles, CA: University of California Press.Google Scholar
Bergquist, P.R. (1979) Sponge chemistry: a review. In Lévi, C. and Boury-Esnault, N. (eds) Biologie de spongiaires: colloques internationaux du C.N.R.S. Paris: CNRS, pp. 382–393.Google Scholar
Bergquist, P.R., Sinclair, M.R. and Hogg, J.J. (1970) Adaptation to intertidal existence: reproductive cycles and larval behaviour in Demospongiae. Symposium of the Zoological Society of London 25, 247–271.Google Scholar
Borchiellini, C., Chombard, C., Manuel, M., Alivon, E., Vacelet, J. and Boury-Esnault, N. (2004) Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Molecular Phylogenetics and Evolution 32, 823–837.CrossRefGoogle ScholarPubMed
Bowerbank, J.S. (1866) A monograph of the British Spongiadae. Volume 2. London: The Ray Society, pp. I–XX, 1–388.Google Scholar
Brien, P. (1967) Embryogenése de Potamolepis stendelli et Spongilla moori. Polyphyletisme des éponges deau douce. Bulletin de la Académie Royale de Belgique 53, 752–757.Google Scholar
Connell, J.H. (1973) Population ecology of reef building corals. In Jones, O.A. and Endean, R. (eds) Biology and geology of coral reefs. New York: Academic Press, pp. 205–245.CrossRefGoogle Scholar
DeCaralt, S., Uriz, M.J., Ereskovsky, A.V. and Wijffels, R.H. (2007) Embryo development of Corticium candelabrum (Demospongiae: Homosclerophorida). Invertebrate Biology 126, 211–219.CrossRefGoogle Scholar
Delage, Y. (1892) Embryogenése des éponges silicieuses. Archives de Zoologie Expérimentale et Générale 10, 345–498.Google Scholar
DeWeerdt, W.H. (1986) A systematic revision of the north-eastern Atlantic shallow water Haplosclerida (Porifera, Demospongiae), Part II Chalinidae. Beaufortia 36, 49–135.Google Scholar
Diaz, J.P., Connes, R. and Paris, J. (1975) Etude ultrastructurale de l'ovogenése d'une Démosponge: Suberites massa Nardo. Journal of Microscopy 24, 105–116.Google Scholar
Efremova, S.M. and Papkovskaya, M.V. (1980) Spermatogenesis of the sponge Lubomirskia baikalensis (Pallas) ultrastructural investigation. Archives d'Anatomie, d'Histologie et d'Embryologie Normales et Expérimentales 79, 88–95.Google Scholar
Elvin, D. (1976) Seasonal growth and reproduction of an intertidal sponge, Haliclona permollis (Bowerbank). Biological Bulletin. Marine Biological Laboratory, Woods Hole 151, 108–125.CrossRefGoogle Scholar
Ereskovsky, A.V. (1999) Development of sponges of the Order Haplosclerida. Russian Journal of Marine Biology 25, 361–371.Google Scholar
Ereskovsky, A.V. (2000) Reproduction cycles and strategies of the cold-water sponges Halisarca dujardini (Demospongiae, Halisarcida), Myxilla incrustans and Iophon piceus (Demospongiae, Poecilosclerida) from the White Sea. Biological Bulletin. Marine Biological Laboratory, Woods Hole 198, 77–87.CrossRefGoogle ScholarPubMed
Ereskovsky, A.V. (2005) Comparative embryology of sponges (Porifera). St Petersburg: St Petersburg University Press.Google Scholar
Ereskovsky, A.V. (2010) The comparative embryology of sponges. Dordrecht, The Netherlands: Springer Science and Business Media B.V.CrossRefGoogle Scholar
Fell, P.E. (1974) Porifera. In Giese, A.C. and Pearse, J.S. (eds) Reproduction of marine invertebrates. New York: Academic Press, pp. 51–132.Google Scholar
Fell, P.E. (1976) The reproduction of Haliclona loosanoffi and its apparent relationship to water temperature. Biological Bulletin. Marine Biological Laboratory, Woods Hole 150, 200–210.CrossRefGoogle Scholar
Fromont, J. (1988) Aspects of the reproductive biology of Xestospongia testudinaria (Great Barrier Reef). In Choat, J.H., Barnes, D. and Borowitzka, M.A. (eds) Proceedings of the 6th International Coral Reef Symposium, James Cook University North Queensland, Townsville, Australia 2, 685–691.Google Scholar
Fromont, J. (1994) Reproductive development and timing of tropical sponges (Order Haplosclerida) from the Great Barrier Reef, Australia. Coral Reefs 13, 127–133.CrossRefGoogle Scholar
Fromont, J. (1999) Reproduction of some demosponges in a temperate Australian shallow water habitat. Memoirs of the Queensland Museum 44, 185–192.Google Scholar
Fromont, J. and Bergquist, P.R. (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongiae: Petrosida) from the Great Barrier Reef. Coral Reefs 13, 119–126.CrossRefGoogle Scholar
Fry, W.G. (1971) The biology of larvae of Ophlitaspongia seriata from two North Wales populations. In Crisp, D.J. (ed.) Fourth European Marine Biology Symposium. Cambridge: Cambridge University Press, pp. 155–178.Google Scholar
Gallissian, M.F. and Vacelet, J. (1976) Ultrastructure de quelques stades de l'ovogenése de spongiaires du genre Verongia (Dictyoceratida). Annales des Sciences Naturelles Zoologie et Biologie Animale 18, 381–404.Google Scholar
Highsmith, R.C. (1982) Reproduction by fragmentation in corals. Marine Ecology Progress Series 7, 207–226.CrossRefGoogle Scholar
Ilan, M. and Loya, Y. (1990a) Sexual reproduction and settlement of the coral reef sponge Chalinula sp. from the Red Sea. Marine Biology 105, 25–31.CrossRefGoogle Scholar
Ilan, M. and Loya, Y. (1990b) Ontogenetic variation in sponge histocompatibility responses. Biological Bulletin. Marine Biological Laboratory, Woods Hole 179, 279–286.CrossRefGoogle Scholar
Ilan, M., Gugel, J. and van Soest, R.W.M. (2004) Taxonomy, reproduction and ecology of new and known Red Sea sponges. Sarsia 89, 388–410.CrossRefGoogle Scholar
Kaye, H.R. (1991) Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. Invertebrate Reproduction and Development 19, 13–24.CrossRefGoogle Scholar
Kaye, H.R. and Reiswig, H.M. (1991) Sexual reproduction in four Caribbean commercial sponges. I. Reproductive cycles and spermatogenesis. Invertebrate Reproduction and Development 19, 1–11.CrossRefGoogle Scholar
Langenbruch, P.F. and Jones, C.W. (1990) Body structure of marine sponges. VI Choanocyte chamber structure in the Haplosclerida (Porifera: Demospongiae) and its relevance to the phylogenesis of the group. Journal of Morphology 204, 1–8.CrossRefGoogle Scholar
Leveaux, M. (1941) Contribution a l'étude histologique de l'ovogenèse et de la spermatogenèse des Spongillidae. Annals de la Société Royale Zoologique de Belgique 72, 251–269.Google Scholar
Lévi, C. (1956) Etude des Halisarca de Roscoff. Embryologie et systématique des Démosponges. Travaux de la Station Biologique de Roscoff N.S 7, 3–181.Google Scholar
Leys, S.P. and Ereskovsky, A.V. (2006) Embryogenesis and larval differentiation in sponges. Canadian Journal of Zoology 84, 262–287.CrossRefGoogle Scholar
Liaci, L. and Sciscioli, M. (1967) Osservazioni sulla maturzione sessuale di un Tetractinellide: Stelletta grubii O.S. (Porifera). Archivio Zoologico Italiano 52, 169–176.Google Scholar
Maldonado, M. and Bergquist, P.R. (2002) Chapter II: Phylum Porifera. In Young, C.M., Sewel, M.A. and Rice, M.E. (eds) Atlas of marine invertebrate larvae. London: Academic Press, pp. 21–50.Google Scholar
Maldonado, M. and Riesgo, A. (2008) Reproduction in the phylum Porifera: a synoptic overview. In Durfort, M. and Vidal, F (eds) Biologia de la reproduccio. Barcelona: Societat Catalana de Biologia, pp. 29–49.Google Scholar
Maldonado, M. and Riesgo, A. (2009) Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Marine Biology 156, 2181–2197.CrossRefGoogle Scholar
Maldonado, M. and Young, C. (1996) Effects of physical factors on larval behaviour, settlement and recruitment of four tropical demosponges. Marine Ecology Progress Series 138, 169–180.CrossRefGoogle Scholar
Maldonado, M., Giraud, K. and Carmona, C. (2008) Effects of sediment on the survival of asexually produced sponge recruits. Marine Biology 154, 631–641.CrossRefGoogle Scholar
Mariani, S., Uriz, M.J. and Turon, X. (2000) Larval bloom of the oviparous sponge Cliona viridis: coupling of larval abundance and adult distribution. Marine Biology 137, 783–790.CrossRefGoogle Scholar
Mariani, S., Uriz, M.J. and Turon, X. (2005) The dynamics of sponge larvae assemblages from northwestern Mediterranean nearshore bottoms. Journal of Plankton Research 27, 249–262.CrossRefGoogle Scholar
Mariani, S., Uriz, M.J., Turon, X. and Alcoverro, T. (2006) Dispersal strategies in sponge larvae: integrating the life history of larvae and the hydrological component. Oecologia 149, 174–184.CrossRefGoogle ScholarPubMed
McGhee, K.E. (2006) The importance of life-history stage and individual variation in the allorecognition system of a marine sponge. Journal of Experimental Marine Biology and Ecology 333, 241–250.CrossRefGoogle Scholar
Meewis, H. (1936) Contribution a l'étude histologique des sponges deau douce: Spongilla lacustris, Ephydatia fluviatilis. Mémoires du Musée Royale d'Histoire Naturelle de Belgique 3, 519–537.Google Scholar
Meewis, H. (1939) Contribution a l'étude de l embryogenèse de Chalinulidae: Haliclona limbta. Annals de la Société Royale Zoologique de Belgique 70, 201–243.Google Scholar
Meewis, H. (1941) Contribution a l'étude de l'embryogenèse des éponges siliceusses—development de l'oeuf chez Adocia cinerea (Grant) et Halichondria coalita (Bowerbank). Annals de la Société Royale Zoologique de Belgique 72, 1–26.Google Scholar
Paulus, W. (1989) Ultrastructural investigation of spermatogenesis in Spongilla lacustris and Ephydatia fluviatilis (Porifera, Spongillidae). Zoomorphology 109, 123–130.CrossRefGoogle Scholar
Paulus, W. and Weissenfels, N. (1986) The spermatogenesis of Ephydatia fluviatilis (Porifera). Zoomorphology 106, 155–162.CrossRefGoogle Scholar
Raleigh, J., Redmond, N.E., Delahan, E., Torpey, S., van Soest, R.W.M., Kelly, M., and McCormack, G.P. (2007) Mitochondrial cytochrome oxidase 1 phylogeny supports alternative taxonomic scheme for the marine Haplosclerida. Journal of the Marine Biological Association of the United Kingdom 87, 1577–1584.CrossRefGoogle Scholar
Redmond, N.E., van Soest, R.W.M., Kelly, M., Raleigh, J., Travers, S.A.A. and McCormack, G.P. (2007) Reassessment of the classification of the Order Haplosclerida (Class Demospongiae, Phylum Porifera) using 18S rRNA gene sequence data. Molecular Phylogenetics and Evolution 43, 344–352.CrossRefGoogle ScholarPubMed
Redmond, N.E., Raleigh, J., van Soest, R.W.M., Kelly, M., Travers, S.A.A., Bradshaw, B., Vartia, S., Stephens, K.M. and McCormack, G.P. (2011) Phylogenetic relationships of the marine Haplosclerida (Phylum Porifera) employing ribosomal (28S rRNA) and mitochondrial (cox1, nad1) gene sequence data. PLoS 1 6, e24344.Google ScholarPubMed
Reiswig, H.M. (1983) Porifera, reproductive biology of invertebrates: spermatogenesis. Chichester: John Wiley & Sons.Google Scholar
Saller, U. (1988) Oogenesis and larval development of Enhydra fluviatilis (Porifera, Spongillidae). Zoomorphology 108, 23–28.CrossRefGoogle Scholar
Saller, U. and Weissenfels, N. (1985) The development of Spongilla lacustris from the oocyte to the free larva (Porifera, Spongillidae). Zoomorphology 105, 367–374.CrossRefGoogle Scholar
Sarà, M. (1993) Porifera. In Adiyodi, K.G. and Adiyodi, R.G. (eds) Reproductive biology of invertebrates, Volume 5. Sexual differentiation and behaviour. Chichester: John Wiley & Sons, pp. 1–29.Google Scholar
Simpson, T.L. (1980) Reproductive processes in sponges: a critical evaluation of current data and views. Invertebrate Reproduction and Development 2, 251–269.CrossRefGoogle Scholar
Simpson, T.L. (1984) The cell biology of sponges. New York: Springer, I–XX, 1–388 pp.CrossRefGoogle Scholar
Sperling, E., Petersen, K. and Pisani, D. (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of eumetazoa. Molecular Biology and Evolution 26, 2261–2274.CrossRefGoogle ScholarPubMed
Sukhodolskaya, A.N. and Papkovskaya, M.V. (1985) Electron microscopical study of spermatogenesis in the fresh-water sponges, Ephydatia fluviatilis and Spongilla lacustris. Tsitologiya 27, 297–302.Google Scholar
Tarin, J.J. and Cano, A. (2000) Fertilization in protozoa and metazoan animals. Berlin: Springer.CrossRefGoogle Scholar
Tuzet, O. (1932) Recherches sur l'histologie des éponges. Archives de Zoologie Expérimentale et Générale 74, 169–192.Google Scholar
Tuzet, O. (1947) L'ovogenése et la fécondation de l'éponge calcaire Leucosolenia (Clathrina) coriacea et de l'éponge siliceuse Reniera elegans. Archives de Zoologie Expérimentale et Générale 85, 127–148.Google Scholar
Van deVyver, G. (1970) La non confluence intraspecifique chez les spongiaires et la notion d'individu. Annales d'Embryologie et de Morphologenèse 3, 251–262.Google Scholar
Wapstra, M. and Van Soest, R.W.M. (1987) Sexual reproduction, larval morphology and behavior in Demosponges from the southwest of the Netherlands. In Boury-Esnault, N. and Vacelet, J. (eds) Taxonomy of Porifera. NATO ASI Series, Vol 13. Berlin: Springer, pp. 281–307.CrossRefGoogle Scholar
Weissenfels, N. (1989) Biologie und microscopishe Anayomie der Süßswassershwämme (Spongillidae). Stuttgart and New York: Fisher.Google Scholar
Whalan, S., Battershill, C. and de Nys, R. (2007) Sexual reproduction of the brooding sponge Rhopaloeides odorabile. Coral Reefs 26, 655–663.CrossRefGoogle Scholar
Whalan, S., de Nys, R., Smith-Keune, C., Evans, B., Battershill, C. and Jerry, D. (2008) Low genetic variability within and among populations of the brooding sponge Rhopaloeides odorabile on the central Great Barrier Reef. Aquatic Biology 3, 111–119.CrossRefGoogle Scholar
Wilson, H.V. (1935) Some critical points in the metamorphosis of the halichondrine sponge larva. Journal of Morphology 58, 285–353.CrossRefGoogle Scholar
Witte, U., Barthel, D. and Tendal, O. (1994) The reproductive cycle of the sponge Halichondria panicea Pallas (1766) and its relationship to temperature and salinity. Journal of Experimental Marine Biology and Ecology 183, 41–52.CrossRefGoogle Scholar
Woollacott, R.W. (1993) Structure and swimming behaviour of the larva of Haliclona tubifera (Porifera: Demospongiae). Journal of Morphology 218, 301–321.CrossRefGoogle ScholarPubMed
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