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RESEARCH ARTICLE
Contents Vol 58(4)

Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge

A. Riesgo A C , M. Maldonado A and M. Durfort B
+ Author Affiliations
- Author Affiliations

A Department of Aquatic Ecology, Centro de Estudios Avanzados de Blanes (CSIC), Acceso Cala St. Francesc 14, Blanes 17300, Girona, Spain.

B Department of Cell Biology, Faculty of Biology, Universidad de Barcelona, Avenida Diagonal 645, 08071 Barcelona, Spain.

C Corresponding author. Email: ariesgo@ceab.csic.es

Marine and Freshwater Research 58(4) 398-417 https://doi.org/10.1071/MF06052
Submitted: 30 March 2006  Accepted: 31 January 2007   Published: 13 April 2007

Abstract

We investigated the cycle of sexual reproduction in a Mediterranean population of Corticium candelabrum by light and electron microscopy, using non-destructive tissue sampling. Most individuals of this hermaphroditic species engaged in reproduction. The relationship between seawater temperature and gametogenesis was not straightforward. Oogenesis, characterised by a long phase of oocyte growth, was continuous, with new oocytes appearing every single month of the year. Nevertheless, maximum oocyte production coincided with declining temperatures. Likewise, spermatogenesis started in the coldest month of the year. In contrast, embryonic development and larval release were limited to a few weeks during the seasonal rise of temperature and the warmest months, respectively. Female and male gametes were located in close proximity in the mesohyl. Monociliated spermatogonia putatively derived from choanocytes, and oogonia from archaeocytes. Spermatogenesis, which strongly resembled that in higher animals, produced round spermatozoa that were provided with acrosome and anchoring system for the cilium. Mature oocytes became surrounded by a bacterial layer. Many symbiotic bacteria served for oocyte nourishment, but others were transferred to the larva. As a whole, the reproductive cycle, which also exhibited quite successful fertilisation and low mortality during embryonic development, appears finely tuned to improve the competitive ability of this sponge.

Additional keywords: cell ultrastructure, Porifera, reproductive cycle, sexual reproduction, sponge oocyte, sponge spermatozoon, symbiotic bacteria.


Acknowledgements

We thank Almudena García and Nùria Cortadellas for sample preparation for the histological study, and Carmen Carmona, Rocío Pérez, and Laura Núñez for help with fieldwork. This study was supported by two grants from the Spanish Ministry for Science and Education (MCYT-BMC2002-01228; MEC-CTM2005-05366/MAR).


References

Alberts B., Bray D., Lewis J., Raff M., Roberts K., and Watson J. D. (1993). ‘Molecular Biology of the Cell.’ (Garland Publishing: New York.)

Babcock R. C. (1986). Population biology of reef flat corals of the family Faviidae (Goniastrea, Platygyra). PhD Thesis, James Cook University of North Queensland, Townsville.

Beams H. W., and Kessel R. G. (1983). Cnidaria. In ‘Reproductive Biology of Invertebrates. Vol. I: Oogenesis, Oviposition and Oosorption’. (Eds K. G. Adiyodi and R. G. Adiyodi.) pp. 31–66. (John Wiley and Sons: Chichester.)

Bergquist P. R. (1978). ‘Sponges.’ (University of California Press: Berkeley and Los Angeles.)

Bergquist, P. R. , and Sinclair, M. E. (1968). The morphology and behaviour of larvae of some intertidal sponges. New Zealand Journal of Marine and Freshwater Research 2, 426–437.
Boury-Esnault N., and Jamieson B. G. M. (1999). Porifera. In ‘Reproductive Biology of Invertebrates. IX. Progress in Male Gamete Ultrastructure and Phylogeny’. (Eds K. G. Adiyodi and R. G. Adiyodi.) pp. 1–20. (John Wiley and Sons: Chichester.)

Brazeau, D. A. , and Lasker, H. L. (1992). Reproductive success in the Caribbean octocoral Briareum asbestinum. Marine Biology 114, 157–163.
Brien P. (1973). Les Démosponges. Morphologie et reproduction. In ‘Traité de Zoologie. Anatomie, Systématique, Biologie. Tome III. Fascicule I. Spongiaires’. (Ed. P. P. Grassé.) pp. 133–461. (Masson et Cie: Paris.)

Buss L. W. (1987). ‘The Evolution of Individuality.’ (Princeton University Press: Princeton, NJ.)

Chen T. W. (1976). Reproduction and speciation in Halisarca. In ‘Aspects of Sponge Biology’. (Eds F. W. Harrison and R. R. Cowden.) pp. 113–139. (Academic Press: New York.)

Colussi, A. (1958). Sulla degenerazione di ovociti in Sycon raphanus (O. Schmidt) (Calcispongiae). Annuario dell'Istituto e Museo di Zoologia dell'Univeristà di Napoli 10, 1–8.
Fell P. E. (1974). Porifera. In ‘Reproduction of Marine Invertebrates: Acoelomate and Pseudocoelomate Metazoans’. (Eds A. C. Giese and J. S. Pearse.) pp. 51–132. (Academic Press: New York.)

Fell, P. E. (1976). The reproduction of Haliclona loosanoffi and its apparent relationship to water temperature. The Biological Bulletin 150, 200–210.
| Crossref | GoogleScholarGoogle Scholar | Fell P. E. (1983). Porifera. In ‘Reproductive Biology of Invertebrates I: Oogenesis, Oviposition and Oosorption’. (Eds K. G. Adiyodi and R. G. Adiyodi.) pp. 1–29. (John Wiley and Sons: Chichester.)

Franzén, A. (1996). Ultrastructure of spermatozoa and spermiogenesis in the hydrozoan Cordylophora caspia with comments on structure and evolution of the sperm in the Cnidaria and the Porifera. Invertebrate Reproduction & Development 29, 19–26.
Fromont J. (1994). The reproductive biology of tropical species of Haplosclerida and Petrosida on the Great Barrier Reef. In ‘Sponges in Time and Space’. (Eds R. W. M. van Soest, J. C. Braekman and T. M. G. van Kempen.) pp. 307–311. (Balkema: Rotterdam.)

Fromont, J. (1999). Reproduction of some demosponges in a temperate Australian shallow water habitat. Memoirs of the Queensland Museum 44, 185–192.
Harrison P. L., and Wallace C. C. (1978). Reproduction, dispersal and recruitment of scleractinian corals. In ‘Coral Reef Ecosystems, Ecosystems of the World’. (Ed. Z. Dubinsky.) pp. 133–207. (Elsevier Science Publishers: Amsterdam.)

Hooper J. A. N., and van Soest R. W. M. (2002). ‘Systema Porifera: A Guide to the Classification of Sponges.’ (Kluwer Academic/Plenum Publishers: New York.)

Hoppe, W. F. (1988). Reproductive patterns in three species of large coral reef sponges. Coral Reefs 7, 45–50.
| Crossref | GoogleScholarGoogle Scholar | Kinne O. (1970). Temperature invertebrates. In ‘Marine Ecology: A Comprehensive Integrated Treatise of Life in Oceans and Coastal Waters’. (Ed. O. Kinne.) pp. 407–514. (Wiley-Interscience: London.)

Lepore, E. , Sciscioli, M. , Scalera-Liaci, L. , Santarelli, G. , and Gaino, E. (2000). Sexual reproduction of Cinachyra tarentina (Porifera, Demospongiae). The Italian Journal of Zoology 67, 153–158.
Levitan D. R. (1995). The ecology of fertilisation in free-spawning invertebrates. In ‘Ecology of Marine Invertebrate Larvae’. (Ed. L. R. McEdward.) pp. 124–52. (CRC Press: Boca Ratón, FL.)

Leys S. (2004). Gastrulation in sponges. In ‘Gastrulation. From Cells to Embryo’. (Ed. C. Stern.) pp. 23–31. (CSHL Press: Cold Spring Harbor, NY.)

Maldonado, M. (2004). Choanoflagellates, choanocytes, and animal multicellularity. Invertebrate Biology 123, 1–22.
Maldonado M., and Bergquist P. R. (2002). Phylum Porifera. In ‘Atlas of Marine Invertebrate Larvae’. (Ed. C. M. Young.) pp. 21–50. (Academic Press: New York.)

Maldonado, M. , and Uriz, M. J. (1998). Microrefuge exploitation by subtidal encrusting sponges: patterns of settlement and post-settlement survival. Marine Ecology Progress Series 138, 169–180.
Muricy G., and Díaz M. C. (2002). Order Homosclerophorida Dendy, 1905. Family Plakinidae Schulze, 1880. In ‘Systema Porifera. A Guide to the Classification of Sponges. Vol. I’. (Eds J. A. N. Hooper and R. W. M. van Soest.) pp. 71–82. (Kluwer Academic/Plenun Publishers: NY.)

Nakamura Y., Okada K., and Watanabe Y. (1998) The ultrastructure of spermatozoa and its structural change in the choanocytes of Sycon calcaravis Hozawa. In ‘Sponge Sciences’. (Eds Y. Watanabe and N. Fusetani.) pp. 179–193. (Springer-Verlag: Tokyo.)

Nielsen C. (2001). ‘Animal Evolution: Interrelationships of the Living Phyla.’ (Oxford University Press: Oxford.)

Reiswig, H. M. (1970). Porifera: Sudden sperm release by tropical Demospongiae. Science 170, 538–539.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Reiswig H. M. (1983). Porifera. In ‘Reproductive Biology of Invertebrates. II. Spermatogenesis and Sperm Function’. (Eds K. G. Adiyodi and R. G. Adiyodi.) pp. 1–21. (John Wiley and Sons: Chichester.)

Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17, 208–212.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Sarà M., and Vacelet J. (1973). Ecologie des Démosponges. In ‘Traité de Zoologie. Vol. 3: Spongiaires’. (Ed. P. P. Grassé.) pp. 462–576. (Masson et Cie: Paris.)

Sarà, A. , Cerrano, C. , and Sarà, M. (2002). Viviparous development in the Antarctic sponge Stylocordyla borealis Loven, 1868. Polar Biology 25, 425–431.
Simpson T. L. (1984). Gamete, embryo, larval development. In ‘The Cell Biology of Sponges’. (Ed. T. L. Simpson.) pp. 341–413. (Springer-Verlag: Berlin.)

Storr J. F. (1964). ‘Ecology of the Gulf of Mexico Commercial Sponges and its Relation to the Fishery.’ Special Scientific Report of Fisheries No. 466. (US Fish Wildlife Service: Washington, DC.)

Tanaka-Ichiara K., and Watanabe Y. (1990). Gametogenic cycle of Halichondria okadai. In ‘New Perspectives in Sponge Biology’. (Ed. K. Rützler.) pp. 170–174. (Smithsonian Institution Press: Washington, DC.)

Tsurumi, M. , and Reiswig, H. M. (1997). Sexual versus asexual reproduction in an oviparous rope-form sponge, Aplysina cauliformis (Porifera: Verongida). Invertebrate Reproduction & Development 32, 1–9.
Tuzet O. (1964). L’origine de la ligneé germinale et la gametogénèse chez les spongiaires. In ‘L’Origine de la Ligneé Germinale.’ (Ed. E. Wolff.) pp. 79–111. (Hermann: Paris.)

Tuzet, O. , and Paris, J. (1964). La spermatogenèse, l’ovogenèse, la fécondation et les premiers stades du développement chez Octavella galangaui. Vie et Milieu 15, 309–327.
Wapstra M., and van Soest R. W. M. (1987). Sexual reproduction, larval morphology and behaviour in demosponges from the southwest of the Netherlands. In ‘Taxonomy of Porifera’. (Eds J. Vacelet and N. Boury-Esnault.) pp. 281–307. (Springer Verlag: Berlin.)

Watanabe Y., and Masuda Y. (1990). Structure of fiber bundles in the egg of Tetilla japonica and their possible function in development. In ‘New Perspectives in Sponge Biology’. (Ed. K. Rützler.) pp. 193–199. (Smithsonian Institution Press: Washington, DC.)

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.
| Crossref | GoogleScholarGoogle Scholar |

Zea, S. (1993). Recruitment of demosponges (Porifera, Demospongiae) in rocky and coral reef habitats of Santa Marta, Colombian Caribbean. Marine Ecology 14, 1–21.


Zihler, J. (1972). Zur Gametogenese and Befruchtungsbiologie von Hydra. Wilhelm Roux's Archives 169, 239–267.
| Crossref | GoogleScholarGoogle Scholar |




1 We use the term cilia to refer to eukaryotic organelles whose structure is characterised by an essentially identical arrangement of microtubules. Following Nielsen (2001) and Maldonado (2004), this definition covers a spectrum from the undulating cilium of many protists and the undulating-rotating cilium of sperm cells to the planar cilium of vertebrate multiciliated cells. In agreement with other zoologists, we reserve the term flagellum for simpler structures found in bacteria, which lack microtubules.