Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-28T12:55:56.512Z Has data issue: false hasContentIssue false

Effects of excavating-sponge removal on coral growth

Published online by Cambridge University Press:  11 August 2015

Ariel A. Halperin*
Affiliation:
Coral Reef Restoration, Assessment and Monitoring Laboratory, Nova Southeastern University Oceanographic Center, Dania Beach, Florida 33004, USA
Andia Chaves-Fonnegra
Affiliation:
Coral Reef Restoration, Assessment and Monitoring Laboratory, Nova Southeastern University Oceanographic Center, Dania Beach, Florida 33004, USA
David S. Gilliam
Affiliation:
Coral Reef Restoration, Assessment and Monitoring Laboratory, Nova Southeastern University Oceanographic Center, Dania Beach, Florida 33004, USA
*
Correspondence should be addressed to:A.A. Halperin, Coral Reef Restoration, Assessment and Monitoring Laboratory, Nova Southeastern University Oceanographic Center, Dania Beach, Florida 33004, USA email: ari.halp@gmail.com

Abstract

Some excavating sponges are strong competitors for space on coral reefs, able to kill live coral tissue and to overgrow entire coral colonies. Stony corals with excavating sponges can die or become dislodged. To date no restoration efforts to eliminate excavating sponges from live corals have been considered. In this study we examined the effect and remedial potential of removal of the excavating sponge, Cliona delitrix, by monitoring tissue loss of the stony coral Montastrea cavernosa. Thirty-three corals colonized by the sponge were used: 11 as controls, and 22 as treatments in which sponges were removed using hammer and chisel. After sponge removal, resultant cavities in the coral skeletons were filled with common cement or epoxy. Standardized photos of each coral were taken immediately after sponge removal, and at 6 and 12 months afterwards. Results were similar between fill materials and showed a reduction in coral tissue loss in colonies where the sponge was removed. This study demonstrates that eliminating the bioeroding sponge enables potential recovery in affected stony corals after a year. However, 36% of experimental corals showed renewed presence of C. delitrix on the colony surface within a year after removal, demonstrating the extraordinary ability of this sponge to colonize corals. Although the technique used in this study is applicable to enhance modern coral restoration practices by slowing tissue loss, this method is costly, elaborate, and not suitable at a reef-wide scale. Further restoration alternatives and long-term measures to prevent over-colonization of corals by excavating sponges are encouraged.

Type
Research Article
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

Acker, K.L. and Risk, M.J. (1985) Substrate destruction and sediment production by the boring sponge Cliona caribbaea on Grand Cayman Island. Journal of Sedimentary Petrology 55, 705711.Google Scholar
Antonius, A. and Ballesteros, E. (1998) Epizoism: a new threat to coral health in Caribbean reefs. Revista de Biologica Tropical 46, 145156.Google Scholar
Ateweberhan, M., Feary, D.A., Keshavmurthy, S., Chen, A., Schleyer, M.H. and Sheppard, C.R. (2013) Climate change impacts on coral reefs: synergies with local effects, possibilities for acclimation, and management implications. Marine Pollution Bulletin 74, 526539.CrossRefGoogle ScholarPubMed
Bell, J.J., Davy, S.K., Jones, T., Taylor, M.W. and Webster, N.S. (2013) Could some coral reefs become sponge reefs as our climate changes? Global Change Biology 19, 26132624.CrossRefGoogle ScholarPubMed
Calcinai, B., Azzini, F., Bavestrello, G., Gaggero, L. and Cerrano, C. (2007) Excavating rates and boring pattern of Cliona albimarginata (Porifera: Clionaidae) in different substrata. In Custódio, M.R., Hajdu, E., Lôbo-Hadju, G. and Muricy, G. (eds) Porifera research: biodiversity, innovation, and sustainability. Rio de Janeiro: Museu Nacional, pp. 203210.Google Scholar
Carballo, J.L., Bautista, E., Nava, H., Cruz-Barraza, J.A. and Chavez, J.A. (2013) Boring sponges, an increasing threat to coral reefs affected by bleaching events. Ecology and Evolution 3, 872886.CrossRefGoogle ScholarPubMed
Carballo, J.L., Bautista-Guerrero, E. and Leyte-Morales, G.E. (2008) Boring sponges and the modeling of coral reefs in the East Pacific Ocean. Marine Ecology Progress Series 356, 113122.CrossRefGoogle Scholar
Chaves-Fonnegra, A. (2014) Increase of excavating sponges on Caribbean coral reefs: reproduction, dispersal, and coral deterioration. PhD Dissertation. Nova Southeastern University, Dania Beach, Florida, USA.Google Scholar
Chaves-Fonnegra, A., Castellanos, L., Zea, S., Duque, C., Rodríguez, J. and Jiménez, C. (2008) Clionapyrrolidine A – a metabolite from the encrusting and excavating sponge Cliona tenuis that kills coral tissue upon contact. Journal of Chemical Ecology 34, 15651574.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., Hajdu, E., Lôbo-Hadju, G. and Muricy, G. (eds) Porifera research: biodiversity, innovation, and sustainability. Rio de Janeiro: Museu Nacional, pp. 247254.Google Scholar
Chaves-Fonnegra, A. and Zea, S. (2011) Coral colonization by the encrusting excavating Caribbean sponge Cliona delitrix. Marine Ecology 32, 162173.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, 6378.Google Scholar
Chiappone, M., Rutten, L.M., Miller, S.L. and Swanson, D.W. (2007) Large scale distributional patterns of the encrusting and excavating sponge Cliona delitrix (Pang) on Florida Keys coral substrates. In Custódio, M.R., Hajdu, E., Lôbo-Hadju, G. and Muricy, G. (eds) Porifera research: biodiversity, innovation, and sustainability. Rio de Janeiro: Museu Nacional, pp. 255263.Google Scholar
Collier, C., Dodge, R., Gilliam, D., Gracie, K., Gregg, L., Jaap, W., Mastry, M. and Poulos, N. (2007) Rapid response and restoration for coral reef injuries in Southeast Florida: guidelines and recommendations. Tallahassee, FL: The Southeast Florida Coral Reef Initiative (SEFCRI), Florida Department of Environmental Protection, 61 pp.Google Scholar
Forrester, G.E., O'Connell-Rodwell, C., Baily, P., Forrester, L.M., Giovannini, S., Harmon, L., Karis, R., Krumholz, J., Rodwell, T. and Jarecki, L. (2011) Evaluating methods for transplanting endangered elkhorn corals in the Virgin Islands. Restoration Ecology 19, 299306.CrossRefGoogle Scholar
Foster, N.L., Box, S.J. and Mumby, P.J. (2008) Competitive effects of macroalgae on the fecundity of the reef-building coral Montastraea annularis. Marine Ecology Progress Series 367, 143152.CrossRefGoogle Scholar
Gardner, T.A., Côté, I.M., Gill, J.A., Grant, A. and Watkinson, A.R. (2003) Long-term, region-wide declines in Caribbean corals. Science 301, 958960.CrossRefGoogle ScholarPubMed
Gilliam, D.S., Brinkhuis, V., Ruzicka, R. and Walton, C.J. (2013) Southeast Florida Coral Reef Evaluation and Monitoring Project 2012 Year 10 final report. Florida DEP Report #RM085. Miami Beach, FL, pp. 53.Google Scholar
Glynn, P.W. (1997) Bioerosion and coral-reef growth: a dynamic balance. In Birkeland, C. (ed.) Life and death of coral reefs. New York, NY: Chapman and Hall, pp. 6894.CrossRefGoogle Scholar
Halperin, A.A. (2014) Distribution, growth and impact of the coral-excavating sponge, Cliona delitrix, on the stony coral communities offshore southeast Florida. MSc thesis. Nova Southeastern University Oceanographic Center, Dania Beach, Florida.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 Eighth International Coral Reef Symposium 2. Convention Centre, Panama, 24–29 June 1996. Balboa: Smithsonian Tropical Research Institute, pp. 14111416.Google Scholar
Holmes, K.E. (2000) Effects of eutrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae). Invertebrate Biology 119, 125138.CrossRefGoogle Scholar
Hughes, T.P. (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265, 15471551.CrossRefGoogle ScholarPubMed
Jompa, J. and McCook, L.J. (2002) The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnology and Oceanography 47, 527534.CrossRefGoogle Scholar
Kennedy, E.V., Perry, C.T., Halloran, P.R., Fine, M., Carricart-Ganivet, J.P., Iglesias-Prieto, R., Form, A., Wisshak, M., Schönberg, C.H.L. and Mumby, P.J. (2013) Avoiding coral structural collapse requires local and global action. Current Biology 23, 912918.CrossRefGoogle ScholarPubMed
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, 1630.CrossRefGoogle Scholar
Lincoln, R.J., Boxshall, G.A. and Clark, P.F. (1998) A dictionary of ecology, evolution and systematics. Cambridge: Cambridge University Press.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, 3341.CrossRefGoogle Scholar
López-Victoria, M., Zea, S. and Weil, E. (2006) Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms. Marine Ecology Progress Series 312, 113121.CrossRefGoogle Scholar
MacGeachy, J.K. and Stearn, C.W. (1976) Boring by macro-organisms in the coral Montastrea annularis on Barbados Reefs. Internationale Revue der gesamten Hydrobiologie 61, 715745.CrossRefGoogle Scholar
Mallela, J. and Perry, C.T. (2007) Calcium carbonate budgets for two coral reefs affected by different terrestrial runoff regimes, Rio Bueno, Jamaica. Coral Reefs 26, 129145.CrossRefGoogle Scholar
McKenna, S.A. (1997) Interactions between the boring sponge, Cliona lampa and two hermatypic corals from Bermuda. In Lessios, H.A. and MacIntyre, I.G. (eds) Proceedings of the Eighth International Coral Reef Symposium 2. Convention Centre, Panama, 24–29 June 1996. Balboa: Smithsonian Tropical Research Institute, pp. 13691374.Google Scholar
Nava, H. and Carballo, J.L. (2008) Chemical and mechanical bioerosion of boring sponges from Mexican Pacific coral reefs. Journal of Experimental Biology 211, 28272831.CrossRefGoogle ScholarPubMed
Perry, C.T., Spencer, T. and Kench, P. S. (2008) Carbonate budgets and reef production states: a geomorphic perspective on the ecological phase-shift concept. Coral Reefs 27, 853866.CrossRefGoogle Scholar
Pomponi, S.A. (1979) Cytochemical studies of acid phosphatase in etching cells of boring sponges. Journal of the Marine Biological Association of the United Kingdom 59, 785789.CrossRefGoogle Scholar
Rose, C.S. and Risk, M.J. (1985) Increase in Cliona delitrix infestation of Montastrea cavernosa heads on an organically polluted portion of the Grand Cayman fringing reef. Marine Ecology 6, 345363.CrossRefGoogle Scholar
Rützler, K. (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispanica 37, 6172.Google Scholar
Schönberg, C.H.L. (2002) Substrate effects on the bioeroding demosponge Cliona orientalis. 1. Bioerosion rates. Pubblicazioni della Stazione Zoologica di Napoli, Italy, Marine Ecology 23, 313326.CrossRefGoogle Scholar
Schönberg, C.H.L. (2008) A history of sponge erosion: from past myths and hypotheses to recent approaches. In Wisshak, M. and Tapanila, L. (eds) Current developments in bioerosion. Berlin, Germany: Springer, pp. 165202.CrossRefGoogle Scholar
Schönberg, C.H.L. and Ortiz, J.C. (2009) Is sponge bioerosion increasing? In Riegl, B. (ed.) Proceedings of the Eleventh International Coral Reef Symposium, Reefs for the future. Convention Centre, Fort Lauderdale, 7–11 July 2008. Fort Lauderdale, FL: International Coral Reef Society, pp. 520523.Google Scholar
Schönberg, C.H.L. and Suwa, R. (2007) Why bioeroding sponges may be better hosts for symbiotic dinoflagellates than many corals. In Custódio, M.R., Lôbo-Hajdu, G., Hajdu, E. and Muricy, G. (eds) Porifera research. Biodiversity, innovation and sustainability. Rio de Janeiro: National Museum, pp. 569580.Google Scholar
Schönberg, C.H.L., Suwa, R. and Hidaka, M. (2008) Sponge and coral zooxanthellae in heat and light: preliminary results of photochemical efficiency monitored with pulse amplitude modulated fluorometry. Marine Ecology 29, 247258.CrossRefGoogle Scholar
Schönberg, C.H.L. and Wilkinson, C.R. (2001) Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20, 6976.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn.New York, NY: W.H. Freeman and Co.Google Scholar
Sullivan, B.W. and Faulkner, D.J. (1990) Chemical studies of the burrowing sponge Siphonodictyon coralliphagum. In Rützler, K. (eds) New perspectives in sponge biology. Washington, DC: Smithsonian Institution Press, pp. 4550.Google Scholar
Sullivan, B.W., Faulkner, D.J. and Webb, L. (1983) Siphonodictidine, a metabolite of the burrowing sponge Siphonodictyon sp. that inhibits coral growth. Science 221, 11751176.CrossRefGoogle ScholarPubMed
Tanner, J.E. (1995) Competition between scleractinian corals and macroalgae: an experimental investigation of coral growth, survival and reproduction. Journal of Experimental Marine Biology and Ecology 190, 151168.CrossRefGoogle Scholar
Van Soest, R.W.M., Boury-Esnault, N., Hooper, J.N.A., Rützler, K., de Voogd, N.J., Alvarez de Glasby, B., Hajdu, E., Pisera, A.B., Manconi, R., Schönberg, C., Janussen, D., Tabachnick, K.R., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M.C. and Cárdenas, P. (2014) World Porifera database at http://www.marinespecies.org/porifera.Google Scholar
Vicente, V.P. (1978) An ecological evaluation of the West Indian demosponge Anthosigmella varians (Hadromerida: Spirastrellidae). Bulletin of Marine Science 28, 771779.Google 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, 570579.CrossRefGoogle ScholarPubMed
Wisshak, M., Schönberg, C.H.L., Form, A. and Friewald, A. (2014) Sponge bioerosion accelerated by ocean acidification across species and latitudes? Helgoland Marine Research 68, 253262.CrossRefGoogle Scholar
Young, C.N., Schopmeyer, S.A. and Lirman, D. (2012) A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and Western Atlantic. Bulletin of Marine Science 88, 10751098.CrossRefGoogle Scholar
Zardus, J.D., Nedved, B.T., Huang, Y., Tran, C. and Hadfield, M.G. (2008) Microbial biofilms facilitate adhesion in biofouling invertebrates. Biological Bulletin 214, 9198.CrossRefGoogle ScholarPubMed
Zundelevich, A., Lazar, B. and Ilan, M. (2007) Chemical versus mechanical bioerosion of coral reefs by boring sponges – lessons from Pione cf. vastifica. Journal of Experimental Biology 210, 9196.CrossRefGoogle ScholarPubMed