Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge
A. Riesgo A C , M. Maldonado A and M. Durfort BA 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).
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.
Brazeau, D. A. , and Lasker, H. L. (1992). Reproductive success in the Caribbean octocoral Briareum asbestinum. Marine Biology 114, 157–163.
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. (1976). The reproduction of Haliclona loosanoffi and its apparent relationship to water temperature. The Biological Bulletin 150, 200–210.
| Crossref | GoogleScholarGoogle Scholar |
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. (1999). Reproduction of some demosponges in a temperate Australian shallow water habitat. Memoirs of the Queensland Museum 44, 185–192.
Hoppe, W. F. (1988). Reproductive patterns in three species of large coral reef sponges. Coral Reefs 7, 45–50.
| Crossref | GoogleScholarGoogle Scholar |
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.
Maldonado, M. (2004). Choanoflagellates, choanocytes, and animal multicellularity. Invertebrate Biology 123, 1–22.
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.
Reiswig, H. M. (1970). Porifera: Sudden sperm release by tropical Demospongiae. Science 170, 538–539.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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, A. , Cerrano, C. , and Sarà, M. (2002). Viviparous development in the Antarctic sponge Stylocordyla borealis Loven, 1868. Polar Biology 25, 425–431.
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. , 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.
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.