Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

A sponge of the Cliona viridis complex invades and excavates corals of the Gulf of Mannar, south-eastern India

Arathy Mol Ashok A C , Christine Hanna Lydia Schönberg B , Kasper Diraviya Raj A , Mahalakshmi Bhoopathi A , M. Selva Bharath A and Edward J. K. Patterson A
+ Author Affiliations
- Author Affiliations

A Suganthi Devadason Marine Research Institute, 44 Beach Road, Tuticorin, India.

B School of Earth and Environment and Oceans Institute, University of Western Australia, Crawley, WA 6009, Australia.

C Corresponding author. Email: arathyashok63@gmail.com

Marine and Freshwater Research 69(6) 874-882 https://doi.org/10.1071/MF17247
Submitted: 19 August 2017  Accepted: 8 November 2017   Published: 13 February 2018

Abstract

Sponges play an important role in biogenic coral-reef degradation, and it is acknowledged that elevated levels of sponge erosion commonly indicate poor health of coral-reef environments. An increase in the abundance of coral-excavating sponge has been reported from several locations, a development that may move coral-reef carbonate budgets increasingly towards net erosion. The role of coral-excavating sponges on Indian reefs has not been studied in as much detail as elsewhere. The present paper describes the observation of a coral-excavating sponge from the family Clionaidae. This brown, endolithic sponge formed a coherent thin layer over the surface of the substratum and had a spicule complement of tylostyles and spirasters. Therefore it belongs to the Cliona viridis species complex, which, as a group, is widely distributed and commonly displays high bioerosion rates. Accurate identification will require molecular studies and is presently deferred. The sponge was found excavating only Turbinaria mesenterina colonies of Gulf of Mannar. Within the surveyed area of 60 m2, 38.58% of T. mesenterina colonies were found to be invaded by the sponge. Targeted long-term studies across a larger spatial scale are warranted to assess the role of this sponge in more detail, and whether its abundance changes over time.

Additional keywords: bioerosion, Clionaida, coral reef health, infestation rate, Porifera, Turbinaria.


References

Abdul Wahab, M. A., de Nys, R., Webster, N., and Whalan, S. (2014). Larval behaviours and their contribution to the distribution of the intertidal coral reef sponge Carteriospongia foliascens. PloS One 9, e98181.
Larval behaviours and their contribution to the distribution of the intertidal coral reef sponge Carteriospongia foliascens.Crossref | GoogleScholarGoogle Scholar |

Aerts, L. A. (1998). Sponge/coral interactions in Caribbean reefs: analysis of overgrowth patterns in relation to species identity and cover. Marine Ecology Progress Series 175, 241–249.
Sponge/coral interactions in Caribbean reefs: analysis of overgrowth patterns in relation to species identity and cover.Crossref | GoogleScholarGoogle Scholar |

Annandale, N. (1915). Indian boring sponges of the family Clionidae. Records of the Indian Museum 11, 1–24.

Arthur, R. (2000). Coral bleaching and mortality in three Indian reef regions during an EI Nino southern oscillation event. Current Science 79, 1723–1729.

Ávila, E., and Carballo, J. L. (2009). A preliminary assessment of the invasiveness of the Indo-Pacific sponge Chalinula nematifera on coral communities from the tropical eastern Pacific. Biological Invasions 11, 257–264.
A preliminary assessment of the invasiveness of the Indo-Pacific sponge Chalinula nematifera on coral communities from the tropical eastern Pacific.Crossref | GoogleScholarGoogle Scholar |

Calcinai, B., Bavestrello, G., and Cerrano, C. (2005). Excavating sponge species from the Indo-Pacific Ocean. Zoological Studies (Taipei, Taiwan) 44, 5–18.

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 ‘Proceeding of 7th International Sponge Symposium’, 7–13 May 2006, Rio de Janeiro, Brazil. (Eds M. R. Custódio, G. Lôbo-Hajdu, E. Hajdu, and G. Muricy.) pp. 203–210. (Museu Nacional: Rio de Janeiro, Brazil.)

Calcinai, B., Bavestrello, G., Cerrano, C., and Gaggero, L. (2008). Substratum microtexture affects the boring pattern of Cliona albimarginata (Clionaidae, Demospongiae). In ‘Current Developments in Bioerosion’. (Eds M. Wisshak and L. Tapanila.) pp. 203–211. (Springer: Berlin, Germany)

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.
Boring sponges, an increasing threat for coral reefs affected by bleaching events.Crossref | GoogleScholarGoogle Scholar |

Carreiro-Silva, M., and McClanahan, T. R. (2012). Macrobioerosion of dead branching Porites, 4 and 6 years after coral mass mortality. Marine Ecology Progress Series 458, 103–122.
Macrobioerosion of dead branching Porites, 4 and 6 years after coral mass mortality.Crossref | GoogleScholarGoogle Scholar |

Carter, H. J. (1887). Report on the marine sponges, chiefly from King Island, in the Mergui Archipelago, collected for the trustees of the Indian Museum, Calcutta, by D. John Anderson, F.R.S., Superintendent of the museum. Zoological Journal of the Linnean Society 21, 61–84.
Report on the marine sponges, chiefly from King Island, in the Mergui Archipelago, collected for the trustees of the Indian Museum, Calcutta, by D. John Anderson, F.R.S., Superintendent of the museum.Crossref | GoogleScholarGoogle Scholar |

Dendy, A. (1916). Report on the non-calcareous sponges collected by Mr James Hornell at Okhamandal in Kattiawar in 1905–6. In ‘Report to the Government of Baroda on the Marine Zoology of Okhamandal in Kattiawar’, number 2, pp. 93–146. Available at http://www.marinespecies.org/aphia.php?p=sourcedetails&id=7404 [Verified 1 December 2017].

Díaz, M. C., and Rützler, K. (2001). Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science 69, 535–546.

English, S., Wilkinson, C., and Baker, V. (1997). ‘Survey Manual for Tropical Marine Resources 2.’ (Australian Institute of Marine Science: Townsville, Qld, Australia.)

Friday, S., Poppell, E., and Hill, M. S. (2013). Cliona tumula sp. nov., a conspicuous, massive Symbiodinium-bearing clionaid from the lower Florida Keys (USA) (Demospongiae: Hadromerida: Clionaidae). Zootaxa 3750, 375–382.
Cliona tumula sp. nov., a conspicuous, massive Symbiodinium-bearing clionaid from the lower Florida Keys (USA) (Demospongiae: Hadromerida: Clionaidae).Crossref | GoogleScholarGoogle Scholar |

George, R. M., and Jasmine, S. (2015). Scleractinian coral diversity in Indian reefs, their threats and conservation. Publication of the Central Marine Fisheries Research Institute, pp. 33–37, Cochin, India. Available at http://eprints.cmfri.org.in/10411/1/06_Rani_Mary_George.pdf [Verified 1 December 2017].

Glynn, P. (1997). Bioerosion and coral reef growth: a dynamic balance. In ‘Life and Death of Coral Reefs’. (Ed. C. Birkeland.) pp. 68–95. (Chapman & Hall: New York, NY, USA.)

González-Rivero, M., Bozec, Y. M., Chollett, I., Ferrari, R., and Schönberg, C. H. L. (2016). Asymmetric competition prevents the outbreak of an opportunistic species after coral reef degradation. Oecologia 181, 161–173.
Asymmetric competition prevents the outbreak of an opportunistic species after coral reef degradation.Crossref | GoogleScholarGoogle Scholar |

Holmes, K. E. (1997). Eutrophication and its effect on bioeroding sponge communities. In ‘Proceedings of the 8th International Coral Reef Symposium, vol. 2’, 24–29 June 1996, Panama City, Panama. (Eds H. A. Lessios and I. G. Macintyre.) pp. 1411–1415. (Smithsonian Tropical Research Institution: Balboa, Panama.)

Holmes, K. E. (2000). Effects of euthrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae). Invertebrate Biology 119, 125–138.
Effects of euthrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae).Crossref | GoogleScholarGoogle Scholar |

Holmes, K. E., Edinger, E. N., Hariyadi, , Limmon, G. V., and Risk, M. J. (2000). Bioerosion of live massive corals and branching coral rubble on Indonesian coral reefs. Marine Pollution Bulletin 40, 606–617.
Bioerosion of live massive corals and branching coral rubble on Indonesian coral reefs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFOqtL4%3D&md5=cca192f0a7fd7da891d2b05b26d0b2cfCAS |

Hughes, T. P., and Connell, J. H. (1999). Multiple stressors on coral reefs: a long-term perspective. Limnology and Oceanography 44, 932–940.
Multiple stressors on coral reefs: a long-term perspective.Crossref | GoogleScholarGoogle Scholar |

Joshi, D., Banerji, U., and Mankodi, P. C. (2015). Delayed recovery in Porites spp. following mass coral bleaching: a case study from the Gulf of Kachchh, Gujarat, India. Journal of Global Biosciences 4, 2326–2331.

Kennedy, E. V., Perry, C. T., Halloran, P. R., Iglesias-Prieto, R., Schönberg, C. H. L., Wisshak, M., Carricart-Ganivet, J. P., Fine, M., Eakin, C. M., and Mumby, P. J. (2013). Avoiding coral reef functional collapse requires local and global action. Current Biology 23, 912–918.
Avoiding coral reef functional collapse requires local and global action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVGitL8%3D&md5=7e894bcc1049421560ed5a9027f01b68CAS |

Kumaraguru, A. K., Jayakumar, K., and Ramakritinan, C. M. (2003). Coral bleaching 2002 in the Palk Bay, southeast coast of India. Current Science 85, 1787–1792.
| 1:CAS:528:DC%2BD2cXht1Sgtbs%3D&md5=35177cd534cfd911106c4611a50fed94CAS |

Leal, C. V., De Paula, T. S., Lôbo-Hajdu, G., Schönberg, C. H. L., and Esteves, E. L. (2016). Morphological and molecular systematics of the ‘Cliona viridis complex’ from south-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 96, 313–322.
Morphological and molecular systematics of the ‘Cliona viridis complex’ from south-eastern Brazil.Crossref | GoogleScholarGoogle Scholar |

López-Victoria, M., and Zea, S. (2005). Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Marine Ecology (Berlin) 26, 33–41.
Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs.Crossref | GoogleScholarGoogle 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, 113–121.
Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms.Crossref | GoogleScholarGoogle Scholar |

Machendiranathan, M., Senthilnathan, L., and Ranith, R. (2016). Trend in coral-algal phase shift in the Mandapam group of Islands, Gulf of Mannar Marine Biosphere Reserve, India. Journal of Ocean University of China 15, 1080–1086.
Trend in coral-algal phase shift in the Mandapam group of Islands, Gulf of Mannar Marine Biosphere Reserve, India.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVygsrfL&md5=929cf4fad62b88cfb639e6a73b5b837aCAS |

Mahadevan, S., and Nayar, K. N. (1972). Distribution of coral reefs in Gulf of Mannar and Palk Bay and their exploitation and utilization. In ‘Proceedings of the Symposium on Corals and Coral Reefs’, 12–16 January 1969, Mandapam. (Eds C. Mukundan and C. S. Gopindha Pillai.) pp. 181–190. (Marine Biological Association of India: Mandapam Camp, India.)

Moberg, F., and Folke, C. (1999). Ecological goods and services of coral reef ecosystems. Ecological Economics 29, 215–233.
Ecological goods and services of coral reef ecosystems.Crossref | GoogleScholarGoogle Scholar |

Old, M. C. (1941). The taxonomy and distribution of the boring sponges (Clionidae) along the Atlantic coast of North America. Publications of Chesapeake Biological Laboratory 44, 1–30.

Pandolfi, J. M., Bradbury, R. H., Sala, E., Hughes, T. P., Bjorndal, K. A., Cooke, R. G., McArdle, D., McClenachan, L., Newman, M. J. H., Paredes, G., Warner, R. R., and Jackson, J. B. C. (2003). Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958.
Global trajectories of the long-term decline of coral reef ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1elsLw%3D&md5=f22521b2e69d3dfeb099943d160086cfCAS |

Pang, R. K. (1973). The systematics of some Jamaican excavating sponges (Porifera). Postilla of the Peabody Museum at the Yale University 161, 1–75.

Patterson, E. J. K. (2009). Annual coral bleaching in Gulf of Mannar. South Indian Coastal and Marine Bulletin 1, 18.

Patterson, E. J. K., Gilbert, M., Patterson, J., Dan, W., Jerker, T., and Olof, L. (2007). ‘Coral reefs of the Gulf of Mannar, South East Coast of India. Distribution, Diversity and Status.’ Special Research Publication 12. (Sdmri: Thoothukudi, India.)

Patterson, E. J. K., Gilbert, M., Raj, K. D., Thinesh, T., Patterson, J., Tamelander, J., and Wilhelmsson, D. (2012). Coral reefs of Gulf of Mannar, India: signs of resilience. In ‘Proceedings of the 12th International Coral Reef Symposium’, 7–11 July 2008, Cairns, Qld, Australia. (Eds D. Yellowlees and T. Hughes.) p. 18F. (James Cook University: Townsville, Qld, Australia.) Available at https://researchonline.jcu.edu.au/23802/ [Verified 1 December 2017].

Patterson, E. J. K., Mathews, G., Diraviya Raj, K., Laju, R. L., Selva Bharath, M., Arasamuthu, A., Dinesh Kumar, P., Deepak S. Bilgi, Malleshappa H., Coral mortality in Gulf of Mannar, Southeastern India, due to bleaching caused by elevated sea temperature in 2016. Current Science, in press.

Peyrot-Clausade, M., Chazottes, V., and Pari, N. (1999). Bioerosion in the carbonate budget of two Indo-Pacific reefs: La Reunion (Indian Ocean) and Moorea (Pacific Ocean). Bulletin of the Geological Society of Denmark 45, 151–155.

Raj, K. D., Gilbert, M., and Patterson, E. J. K. (2006). Macro algal assemblage structure on the reefs of Tuticorin groups of islands in the Gulf of Mannar. Journal of the Marine Biological Association of India 48, 166–172.

Raj, K. D., Gilbert, M., Selva-Bharath, M., and Patterson, E. J. K. (2016). Mass mortality of Montipora digitata (Scleractinia) in Vaan Island, Gulf of Mannar, southeast India. Current Science 110, 1407–1408.

Rajan, R., Satyanarayana, C., Raghunathan, C., Koya, S. S., Ravindran, J., Manikandan, B., and Venkataraman, K. (2015). Status and review of health of Indian coral reefs. Journal of Aquatic Biology & Fisheries 3, 1–4.

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, 345–363.
Increase in Cliona delitrix infestation of Montastrea cavernosa heads on an organically polluted portion of the Grand Cayman fringing reef.Crossref | GoogleScholarGoogle Scholar |

Rossi, G., Montori, S., Cerrano, C., and Calcinai, B. (2015). Marine sponges are an integral part of coral reef ecosystems and are considered strong space-competitors with corals. Italian Journal of Zoology 82, 143–148.
Marine sponges are an integral part of coral reef ecosystems and are considered strong space-competitors with corals.Crossref | GoogleScholarGoogle Scholar |

Rützler, K. (1971). Bredin–Archbold–Smithsonian biological survey of Dominica: burrowing sponges, genus Siphonodictyon Bergquist, from the Caribbean. Smithsonian Contributions to Zoology 77, 1–37.
Bredin–Archbold–Smithsonian biological survey of Dominica: burrowing sponges, genus Siphonodictyon Bergquist, from the Caribbean.Crossref | GoogleScholarGoogle Scholar |

Rützler, K. (2002). Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispanica 37, 61–72.

Rützler, K., and Muzik, K. (1993). Terpios hoshinota, a new cyanobacterio sponge threatening Pacific reefs. Scientia Marina 57, 395–403.

Rützler, K., and Rieger, G. (1973). Sponge burrowing: fine structure of Cliona lampa penetrating calcareous substrata. Marine Biology 21, 144–162.
Sponge burrowing: fine structure of Cliona lampa penetrating calcareous substrata.Crossref | GoogleScholarGoogle Scholar |

Schönberg, C. H. L. (2000). Bioeroding sponges common to the central Australian Great Barrier Reef: description of three new species, two new records, and additions to two previously described species. Senckenbergiana Maritima 30, 161–221.
Bioeroding sponges common to the central Australian Great Barrier Reef: description of three new species, two new records, and additions to two previously described species.Crossref | GoogleScholarGoogle Scholar |

Schönberg, C. H. L. (2001). Small-scale distribution of Great Barrier Reef bioeroding sponges in shallow water. Ophelia 55, 39–54.
Small-scale distribution of Great Barrier Reef bioeroding sponges in shallow water.Crossref | GoogleScholarGoogle Scholar |

Schönberg, C. H. L. (2002). Sponges of the ‘Cliona viridis complex’: a key for species identification. In ‘Proceedings of 9th International Coral Reef Symposium, vol. 1’, 23–27 October 2000, Bali, Indonesia. (Eds M. K. Moosa, S. Soemodihardjo, A. Soegiarto, K. Romimohtarto, A. Nontji, Soekarno, and Suharsono.) pp. 295–299. (International Socierty of Coral Reef Studies: Bali, Indonesia.)

Schönberg, C. H. L. (2015). Monitoring bioeroding sponges: using rubble, quadrat, or intercept surveys? The Biological Bulletin 228, 137–155.
Monitoring bioeroding sponges: using rubble, quadrat, or intercept surveys?Crossref | GoogleScholarGoogle Scholar |

Schönberg, C. H. L., and Ortiz, J. C. (2009). Is sponge bioerosion increasing? In ‘Proceedings of the 11th International Coral Reef Symposium, vol. 8’, 7–11 July 2008, Fort Lauderdale, FL, USA. (Eds B. Riegl and R. E. Dodge.) pp. 520–523. (Nova Southeastern University National Coral Reef Institute: Davie, FL, USA.)

Schönberg, C. H. L., and Suwa, R. (2007). Why bioeroding sponges may be better hosts for symbiotic dinoflagellates than many corals. In ‘Porifera Research. Biodiversity, Innovation and Sustainability’. (Eds M. R. Custódio, G. Lôbo-Hajdu, E. Hajdu, and G. Muricy.) pp. 569–580. (National Museum: Rio de Janeiro, Brazil.)

Schönberg, C. H. L., and Wilkinson, C. R. (2001). Induced colonization of corals by a clinoid bioeroding sponge. Coral Reefs 20, 69–76.
Induced colonization of corals by a clinoid bioeroding sponge.Crossref | GoogleScholarGoogle Scholar |

Schönberg, C. H. L., Fang, J. K. H., Carreiro-Silva, M., Tribollet, A., and Wisshak, M. (2017a). Bioerosion: the other ocean acidification problem. ICES Journal of Marine Science 74, 895–925.

Schönberg, C. H. L., Fang, J. K. H., and Carballo, J. L. (2017b). Bioeroding sponges and the future of coral reefs. In ‘Climate Change, Ocean Acidification and Sponges’. (Eds J. J. Bell and J. L. Carballo.) pp. 179–372. (Springer International: Cham, Switzerland.)

Scott, P. J. B. (1987). Associations between corals and macro-infaunal invertebrates in Jamaica, with a list of Caribbean and Atlantic coral associates. Bulletin of Marine Science 40, 271–286.

Sollas, W. J. (1878). On two new and remarkable species of Cliona. Annals & Magazine of Natural History 1, 54–67.
On two new and remarkable species of Cliona.Crossref | GoogleScholarGoogle Scholar |

Thinesh, T., Raj, K. D., Gilbert, M., and Patterson, E. J. K. (2013). Coral diseases are major contributors to coral mortality in Shingle Island, Gulf of Mannar, southeastern India. Diseases of Aquatic Organisms 106, 69–77.
Coral diseases are major contributors to coral mortality in Shingle Island, Gulf of Mannar, southeastern India.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c%2Fgs1Kmug%3D%3D&md5=5f7d4b1cb2b5ff5549056c0d31481e8eCAS |

Thinesh, T., Gilbert, M., Raj, K. D., and Patterson, E. J. K. (2014). Coral diseases are major contributors to coral mortality in Shingle Island, Gulf of Mannar, southeastern India. Diseases of Aquatic Organisms 110, 227–234.
Coral diseases are major contributors to coral mortality in Shingle Island, Gulf of Mannar, southeastern India.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M%2FhtVSjsw%3D%3D&md5=7dffa28997caaa6d057c8536d53e9d01CAS |

Thomas, P. A. (1972). Boring sponges on the reefs of Gulf of Mannar and Palk Bay. In ‘Symposium of Corals and Coral Reefs’, 12–16 January 1969, Mandapam Camp, India. (Eds C. Mukundan and C. S. Gopindha Pillai.) pp. 333–362. (Marine Biological Association of India: Mandapam Camp, India.)

Thomas, P. A. (1979). Boring sponges destructive to economically important molluscan beds and coral reefs in Indian seas. Indian Journal of Fisheries 26, 163–200.

Thomas, P. A. (1989). Sponge fauna of Lakshadweep. Central Marine Fisheries Research Institute Bulletin 43, 150–161.

Van Soest, R. W. M., Boury-Esnault, N., Hooper, J. N. A., Rützler, K., de Voogd, N. J., Alvarez, B., Hajdu, E., Pisera, A. B., Manconi, R., Schönberg, C., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M.-C., Cárdenas, P., Carballo, J. L., Rios, P., and Downey, R. (2017). World Porifera database. Available at http://www.marinespecies.org/porifera/index.php [Verified 11 August 2017].

Zahir, H. (2002). Assessing bioerosion and its effect on reef structure following a bleaching event in the Maldives. In ‘Coral Reef Degradation in the Indian Ocean’. (Eds O. Lindén, D. Souter, D. Wilhelmsson, and D. Obura.) Status Report 2002, pp. 135–138. CORDIO, Kalmar, Sweden.