Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-12-03T19:23:53.473Z Has data issue: false hasContentIssue false
  • English
  • Français

Asynchronous reproduction and multi-spawning in the coral-excavating sponge Cliona delitrix

Published online by Cambridge University Press:  13 August 2015

Andia Chaves-Fonnegra ,
Manuel Maldonado ,
Patricia Blackwelder  and
Jose V. Lopez
Andia Chaves-Fonnegra*
Affiliation:
NOVA Southeastern University, Oceanographic Center, 8000 North Ocean Drive. Dania Beach, FL 33004, USA
Manuel Maldonado
Affiliation:
Department of Aquatic Ecology, Center for Advanced Studies of Blanes (CEAB-CSIC), Acceso Cala St. Francesc 14, Blanes, 17300 Girona, Spain
Patricia Blackwelder
Affiliation:
NOVA Southeastern University, Oceanographic Center, 8000 North Ocean Drive. Dania Beach, FL 33004, USA
Jose V. Lopez
Affiliation:
NOVA Southeastern University, Oceanographic Center, 8000 North Ocean Drive. Dania Beach, FL 33004, USA
*
Correspondence should be addressed to: A. Chaves-Fonnegra, NOVA Southeastern University, Oceanographic Center, 8000 North Ocean Drive. Dania Beach, FL, 33004, USA email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Cliona delitrix is one of the most abundant and destructive coral-excavating sponges on Caribbean reefs. However, basic aspects of its reproductive biology, which largely determine the species propagation potential, remain unknown. A 2-year study (October 2009 to September 2011) was conducted to determine the reproductive cycle and gametogenesis of a C. delitrix population located in a shallow reef in Florida, USA. Mesohyl tissue collected from randomly chosen and tagged sponge individuals was sampled one to several times a month, and analysed by light and transmission electron microscopy (TEM). Cliona delitrix is oviparous and gonochoric, except for a few simultaneous hermaphroditic individuals. The C. delitrix reproductive cycle in Florida is from April to December, and is triggered by an increase in seawater temperature to 25°C. Oogenesis and spermatogenesis were asynchronous among individuals; with different cohorts of oocytes co-occurring in females, and spermatic cysts in males. Granulose cells acted as nurse cells, contributing to the growth and maturation of both female and male gametes. Spawning of gametes was not always synchronized with full moon phase. Unlike most other oviparous sponges, the reproductive cycle of C. delitrix is versatile and includes multiple spawning events during the summer of each year. This characteristic maximizes sponge propagation on coral reefs during the warmer months of the year, particularly when thermal stress induces coral mortality. This aspect, combined with its success on polluted areas, make C. delitrix a suitable bioindicator of coral reef health.

Keywords

Reproductive biologylife cyclegametogenesisbioindicatorFloridaCaribbean Sea
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. 515 - 528
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baldacconi, R., Nonnis-Marzano, C., Gaino, E. and Corriero, G. (2007) Sexual reproduction, larval development and release in Spongia officinalis L. (Porifera, Demospongiae) from the Apulian coast. Marine Biology 152, 969–979.CrossRefGoogle Scholar
Banks, K.E., Riegl, B.M., Richards, V.P., Walker, B.E., Helmle, K.P. and Jordan, L.K.B. (2008) The reef tract of continental Southeast Florida (Miami-Dade, Broward, and Palm Beach Counties, USA). In Riegl, B. and Dodge, R.E. (eds) Coral reefs of the USA. New York, NY: Springer-Verlag, pp. 175–220.CrossRefGoogle Scholar
Bautista-Guerrero, E., Carballo, J.L. and Maldonado, M. (2014) Abundance and reproductive patterns of the excavating sponge Cliona vermifera: a threat to Pacific coral reefs? Coral Reefs 33, 259–266.CrossRefGoogle Scholar
Carballo, J.L., Bautista, E., Nava, H., Cruz-Barraza, J.A. and Chavez, J.A. (2013) Boring sponges, an increasing threat for coral reefs affected by bleaching events. Ecology and Evolution 3, 872–886.CrossRefGoogle ScholarPubMed
Carter, H.J. (1873) On two new species of Gummineae, with special and general observations. Annals and Magazine of Natural History 12, 17–30, pl. I.CrossRefGoogle Scholar
Chaves-Fonnegra, A. (2014) Increase of excavating sponges on Caribbean coral reefs: reproduction, dispersal and coral deterioration. Doctoral dissertation. Nova Southeastern University, Dania Beach, 195 pp.Google Scholar
Chaves-Fonnegra, A., Feldheim, K.A., Secord, J. and Lopez, J.V. (2015) Population structure and dispersal of the coral-excavating sponge Cliona delitrix. Molecular Ecology 24, 1447–1466.CrossRefGoogle ScholarPubMed
Chaves-Fonnegra, A. and Zea, S. (2007) Observations on reef coral undermining by the Caribbean excavating sponge Cliona delitrix (Demospongiae, Hadromerida). In Custódio, M.R., Lôbo-Hajdu, G., Hajdu, E. and Muricy, G. (eds) Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro: Museu Nacional, pp. 247–254.Google Scholar
Chaves-Fonnegra, A. and Zea, S. (2011) Coral colonization by the encrusting excavating Caribbean sponge Cliona delitrix. Marine Ecology 32, 162–173.CrossRefGoogle Scholar
Chaves-Fonnegra, A., Zea, S. and Gómez, M.L. (2007) Abundance of the excavating sponge Cliona delitrix in relation to sewage discharge at San Andrés Island, SW Caribbean, Colombia. Boletín de Investigaciones Marinas y Costeras 36, 63–78.Google Scholar
Cortés, J., Murillo, M., Guzmán, H.M. and Acuña, J. (1984) Pérdida de zooxantelas y muerte de corales y otros organismos arrecifales en el Caribe y Pacífico de Costa Rica. Revista de Biología Tropical 32, 227–231.Google Scholar
de Groot, R.A. (1977) Boring sponges (Clionidae) and their trace fossils from the coast near Rovinj (Yugoslavia). Geologie en Mijnbouw 56, 168–181.Google Scholar
Duchassaing De Fonbressin, P. and Michelotti, G. (1864) Spongiaires de la mer Caraïbe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem 21, 1–124, pls I–XXV.Google Scholar
Duckworth, A.R. and Peterson, B.J. (2013) Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells. Marine Biology 160, 27–35.CrossRefGoogle Scholar
Eakin, C.M., Morgan, J.A., Heron, S.F., et al. (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5, 1–9.CrossRefGoogle ScholarPubMed
Enochs, I.C., Manzello, D.P., Carton, R.D., Graham, D.M., Ruzicka, R. and Collela, M.A. (2015) Ocean acidification enhances the bioerosion of a common coral reef sponge: implications for the persistence of the Florida Reef Tract. Bulletin of Marine Science 91, doi: 10.5343/bms.2014.1045 2015.CrossRefGoogle Scholar
Fang, J.H.K., Athayde, M.A.M., Schönberg, C.H.L., Kline, D.I., Hoegh-Guldberg, O. and Dove, S. (2013) Sponge biomass and bioerosion rates under ocean warming and acidification. Global Change Biology 19, 3581–3591.CrossRefGoogle ScholarPubMed
Fell, P.E. (1970) The natural history of Haliclona ecbasis de Laubenfels, a siliceous sponge of California. Pacific Science Journal 24, 381–386.Google Scholar
Gage, J.D. and Tyler, P.A. (1991) Deep-sea biology: a natural history of organisms at the deep sea floor. Cambridge: Cambridge University Press, pp. 524.CrossRefGoogle Scholar
Gardner, T.A., I.M., C., Gill, J.A., Grant, A. and Watkinson, A.R. (2003) Long-term region-wide declines in Caribbean corals. Science 301, 958–960.CrossRefGoogle ScholarPubMed
Ghiselin, M.T. (1987) Evolutionary aspects of marine invertebrate reproduction. In Giese, C.A., Pearse, J.S. and Pearse, V.B. (eds) Reproduction of marine invertebrates. Palo Alto, CA: Blackwell Scientific, pp. 609–666.Google Scholar
Gilliam, D.S. (2012) Southeast Florida coral reef evaluation and monitoring project 2011. Year 9 Final Report. Florida DEP Report #RM085. Miami Beach, FL. 49 pp.Google Scholar
González-Rivero, M., Ereskovsky, A.V., Schönberg, C.H.L., Ferrari, R., Fromont, J. and Mumby, P.J. (2013) Life-history traits of a common Caribbean coral-excavating sponge, Cliona tenuis (Porifera: Hadromerida). Journal of Natural History 47, 2815–2834.CrossRefGoogle Scholar
Grant, R.E. (1826) Notice of a new zoophyte (Cliona celata Gr.) from the Firth of Forth. Edinburgh New Philosophical Journal 1, 78–81.Google Scholar
Hancock, A. (1849) On the excavating powers of certain sponges belonging to the genus Cliona with descriptions of several new species, and an allied generic form. Annals and Magazine of Natural History 3, 321–348, pls XII–XV.CrossRefGoogle Scholar
Hancock, A. (1867) Note on the excavating sponges; with descriptions of four new species. Annals and Magazine of Natural History 19, 229–242, pls VII–VIII.CrossRefGoogle Scholar
Hoegh-Guldberg, O. (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50, 839–866.Google Scholar
Holmes, K.E. (1997) Eutrophication and its effect on bioeroding sponge communities. In Lessios H.A. and Macintyre I.G. (eds) Proceedings of the 8th International Coral Reef Symposium, Panamá, 1997. Smithsonian Tropical Research Institute, pp. 1411–1416.Google Scholar
Hoppe, W.F. and Reichert, M.J.M. (1987) Predictable annual mass release of gametes by the coral reef sponge Neofibularia nolitangere (Porifera: Demospongiae). Marine Biology 94, 277–285.CrossRefGoogle Scholar
Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J.B., Kleypas, J., Lough, J.M., Marshall, P., Nyström, M., Palumbi, S.R., Pandolfi, J.M., Rosen, B. and Roughgarden, J. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933.CrossRefGoogle ScholarPubMed
Ilan, M. and Loya, Y. (1990) Sexual reproduction and settlement of the coral reef sponge Chalinula sp. from the Red Sea. Marine Biology 105, 25–31.CrossRefGoogle Scholar
Lang, J.C. (2003) Status of coral reefs in the Western Atlantic: results of initial surveys, Atlantic and Gulf Rapid Reef Assessment (AGRRA) Program. Atoll Research Bulletin 496, 1–630.CrossRefGoogle Scholar
Leong, W. and Pawlik, J.R. (2011) Comparison of reproductive patterns among 7 Caribbean sponge species does not reveal a resource trade-off with chemical defenses. Journal of Experimental Marine Biology and Ecology 401, 80–84.CrossRefGoogle Scholar
Lévi, C. (1956) Etude des Halisarca de Roscoff. Embryologie et systématique des demosponges. Archives de Zoologie Expérimentale et Genérale 93, 1–181.Google Scholar
Liaci, L.S. and Sciscioli, M. (1967) Osservazioni sulla maturazione sessuale di un tetractinellide: Stelleta grubii O. S. (Porifera). Archivio Zoologico Italiano 52, 169–176.Google Scholar
López-Victoria, M. and Zea, S. (2005) Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Marine Ecology, 26, 33–41.CrossRefGoogle Scholar
Maldonado, M. (2009) Embryonic development of verongid demosponges supports the independent acquisition of spongin skeletons as an alternative to the siliceous skeleton of sponges. Biological Journal of the Linnean Society 97, 427–447.CrossRefGoogle Scholar
Maldonado, M. and Bergquist, P. (2002) Phylum Porifera. In Young, C. (ed.) Atlas of marine invertebrate larvae. Barcelona: 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 reproducció, Volume 59. Barcelona: Societat Catalana de Biología, 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 behavior, settlement and recruitment of four tropical demosponges. Marine Ecology Progress Series 138, 169–180.CrossRefGoogle Scholar
Mangubhai, S. and Harrison, P.L. (2008) Asynchronous coral spawning patterns on equatorial reefs in Kenya. Marine Ecology Progress Series 360, 85–96.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
McCartney, M.A. (1997) Sex allocation and male fitness gain in a colonial, hermaphroditic marine invertebrate. Evolution 51, 127–140.CrossRefGoogle Scholar
Miller, A.W., Blackwelder, P.L., Al-Sayegh, H. and Richardson, L.L. (2011) Fine-structural analysis of black band disease-infected coral reveals boring cyanobacteria and novel bacteria. Diseases of Aquatic Organisms 93, 179–190.CrossRefGoogle ScholarPubMed
Nassonov, N. (1883) Zur biologie und anatomie der Clione. Zeitschrift für Wissenschaftliche Zoologie 39, 295–308.Google Scholar
Old, M.C. (1941) The taxonomy and distribution of the boring sponges (Clionidae) along the Atlantic coast of North America. Chesapeake Biological Laboratory Publications 44, 1–30.Google Scholar
Pandolfi, J.M., Bradbury, R.H., Sala, E., Hughes, T.P., Bjorndal, K.A., Cooke, R.G., McArdle, D., McClenachan, L., Newman, M.J., Paredes, G., Warner, R.R. and Jackson, J.B. (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958.CrossRefGoogle ScholarPubMed
Pang, R.K. (1973) The systematics of some Jamaican excavating sponges (Porifera). Postilla of the Peabody Museum of Natural History at Yale University 161, 1–75.Google Scholar
Piscitelli, M., Corriero, G., Gaino, E. and Uriz, M.J. (2011) Reproductive cycles of the sympatric excavating sponges Cliona celata and Cliona viridis in the Mediterranean Sea. Invertebrate Biology 130, 1–10.CrossRefGoogle Scholar
Pomponi, S.A. and Meritt, D.W. (1990) Distribution and life history of the boring sponge Cliona truitti in the Upper Chesapeake Bay. In Rützler, K. (ed.) New perspectives in sponge biology. Washington, DC: Smithsonian Institution Press, pp. 384–390.Google Scholar
Prevedelli, D., Massamba n'siala, G. and Simonini, R. (2006) Gonochorism vs. hermaphroditism: relationship between life history and fitness in three species of Ophryotrocha (Polychaeta: Dorvilleidae) with different forms of sexuality. Journal of Animal Ecology 75, 203–212.CrossRefGoogle ScholarPubMed
Queller, D.C. (2006) Sex ratios and social evolution. Current Biology 16, R664–R668.CrossRefGoogle ScholarPubMed
Renegar, D.A., Blackwelder, P.L., Miller, J.D., Gochfeld, D.J. and Moulding, A.L. (2008) Ultrastructural and histological analysis of dark spot syndrome in Siderastrea siderea and Agaricia agaricites. In Riegl, B. (ed.) Proceedings of the 11th International Coral Reef Symposium, Fort Lauderdale, pp. 185–189.Google Scholar
Richmond, R.H. and Hunter, C.L. (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Marine Ecology Progress Series 60, 185–203.CrossRefGoogle Scholar
Riesgo, A. and Maldonado, M. (2009) An unexpectedly sophisticated, V-shaped spermatozoon in Demospongiae (Porifera): reproductive and evolutionary implications. Biological Journal of the Linnean Society 97, 413–426.CrossRefGoogle Scholar
Riesgo, A., Maldonado, M. and Durfort, M. (2007) Dynamics of gametogenesis, embryogenesis, and larval release in a Mediterranean homosclerophorid demosponge. Marine and Freshwater Research 58, 398–417.CrossRefGoogle Scholar
Rose, C.S. and Risk, M.J. (1985) Increase in Cliona delitrix infestation of Montastraea cavernosa heads on an organically polluted portion of the Grand Cayman. Pubblicazioni della Stazione Zoologica di Napoli Marine Ecology 6, 345–363.CrossRefGoogle Scholar
Rützler, K. (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispánica 37, 61–72.Google Scholar
Schmidt, O. (1862) Die Spongien des Adriatischen Meeres. Leipzig: Wilhelm Engelmann.Google Scholar
Schönberg, C.H.L. (2001) Small-scale distribution of Australian bioeroding sponges in shallow water. Ophelia 55, 39–54.CrossRefGoogle Scholar
Schönberg, C.H.L. and Ortiz, J.-C. (2008) Is sponge bioerosion increasing? Proceedings of the 11th International Coral Reef Symposium, Fort Lauderdale, USA. pp. 520–523.Google Scholar
Simpson, T.L. (1984) The cell biology of sponges. New York, NY: Springer-Verlag, pp. 662.CrossRefGoogle Scholar
Topsent, E. (1900) Etude monographique des spongiaires de France: III. Monaxonides Hadromerina. Archives de Zoologie Expérimentale et Genérale 8, 1–331.Google Scholar
Usher, K., Sutton, D., Toze, S., Kuo, S. and Fromont, J. (2004) Sexual reproduction in Chondrilla australiensis (Porifera: Demospongia). Marine and Freshwater Research 55, 123–134.CrossRefGoogle Scholar
Volz, P. (1939) Die Bohrschwämme (Clioniden) der Adria. Thalassia 3, 1–64.Google Scholar
Warburton, F.E. (1961) Inclusion of parental somatic cells in sponge larvae. Nature 191, 1317.CrossRefGoogle Scholar
Ward-Paige, C.A., Risk, M.J., Sherwood, O.A. and Jaap, W.C. (2005) Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. Marine Pollution Bulletin 51, 570–579.CrossRefGoogle ScholarPubMed
Weil, E. (2002) Sponge-induced coral mortality in the Caribbean. A potential new threat to Caribbean coral reefs. In Sarà, M., Arillo, A. and della Croce, N. (eds) Proceedings of the VI Internacional Sponge Conference, Genova,. Canessa, pp. 211–212.Google Scholar
Whalan, S., Battershill, C. and Nys, R.d. (2007) Sexual reproduction of the brooding sponge Rhopaloeides odorabile. Coral Reefs 26, 655–663.CrossRefGoogle Scholar
Wisshak, M., Schönberg, C.H.L., Form, A. and Freiwald, A. (2012) Ocean acidification accelerates reef bioerosion. PLoS ONE 7, 1–8.CrossRefGoogle ScholarPubMed
Wisshak, M., Schönberg, C.H.L., Form, A. and Freiwald, A. (2014) Sponge bioerosion accelerated by ocean acidification across species and latitudes? Helgoland Marine Research 68, 253–262.CrossRefGoogle Scholar
Witte, U. (1996) Seasonal reproduction in deep-sea sponges – triggered by vertical particle flux? Marine Biology 124, 571–581.CrossRefGoogle Scholar
Zea, S. and Weil, E. (2003) Taxonomy of the Caribbean excavating sponge species complex Cliona caribbaea – C. aprica – C. langae (Porifera, Hadromerida, Clionaidae). Caribbean Journal of Science 39, 348–370.Google Scholar
Zilberberg, C., Maldonado, M. and Solé-Cava, A.M. (2006) Assessment of the relative contribution of asexual propagation in a population of the coral-excavating sponge Cliona delitrix from the Bahamas. Coral Reefs 25, 297–301.CrossRefGoogle Scholar