Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T16:53:15.510Z Has data issue: false hasContentIssue false
  • English
  • Français

Abundance and genetic variation of the coral-killing cyanobacteriosponge Terpios hoshinota in the Spermonde Archipelago, SW Sulawesi, Indonesia

Published online by Cambridge University Press:  11 May 2015

Esther van der Ent ,
Bert W. Hoeksema  and
Nicole J. de Voogd
Esther van der Ent
Affiliation:
Department of Marine Zoology, Naturalis Biodiversity Center, P.O. Box 9517, 2300RA Leiden, the Netherlands Department of Biomarine Sciences, Utrecht University, the Netherlands
Bert W. Hoeksema
Affiliation:
Department of Marine Zoology, Naturalis Biodiversity Center, P.O. Box 9517, 2300RA Leiden, the Netherlands
Nicole J. de Voogd*
Affiliation:
Department of Marine Zoology, Naturalis Biodiversity Center, P.O. Box 9517, 2300RA Leiden, the Netherlands Institute for Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, the Netherlands
*
Correspondence should be addressed to:N.J. de Voogd, Department of Marine Zoology, Naturalis Biodiversity Center, P.O. Box 9517, 2300RA Leiden, the Netherlands email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The cyanobacteriosponge Terpios hoshinota is expanding its range across the Indo-Pacific. This species can have massive outbreaks on coral reefs, actively kill corals it overgrows and affect the entire benthic community. Although it has received much attention on the post-outbreak follow-up, little is known about its ecology, habitat preferences, and the possible environmental triggers that cause its outbreaks. We present a baseline study in the Spermonde Archipelago, Indonesia, where T. hoshinota was first observed in 2012. We surveyed 27 reefs and recorded patches between 14 and 217 cm2, at four reef sites (~15% cover). The sponge was found on both mid-shelf and outer shelf reefs but not close to the coast and the city of Makassar. Differences in benthic community structure, as well as spatial variables relating to the on-to-offshore gradient in the Spermonde archipelago, neither constrained nor promoted its expansion. Patches of the sponge were mostly overgrowing branching corals, belonging to Acroporidae species. Genetic variation within T. hoshinota was studied by sequencing partitions of the mitochondrial CO1 and nuclear ribosomal 28S gene. Two haplotypes were found within the Spermonde archipelago, which differed from the CO1 sequence in GenBank. The present study provides an indication of habitat preferences of T. hoshinota in non-outbreak conditions, although it is still unclear which environmental conditions may lead to the onset of its outbreaks.

Keywords

Competitive sponge-coral interactionoutbreakbenthic communityCO128S
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. 453 - 463
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

Aerts, L.A.M. and van Soest, R.W.M. (1997) Quantification of sponge/coral interactions in a physically stressed reef community, NE Colombia. Marine Ecology Progress Series 148, 125–134.CrossRefGoogle Scholar
Becking, L.E., Cleary, D.F.R., de Voogd, N.J., Renema, W., de Beer, M., van Soest, R.W.M. and Hoeksema, B.W. (2006) Betadiversity of tropical marine assemblages in the Spermonde Archipelago, Indonesia. Marine Ecology 27, 76–88.CrossRefGoogle Scholar
Becking, L.E., Erpenbeck, D., Peijnenburg, K.T. and de Voogd, N.J. (2013) Phylogeography of the sponge Suberites diversicolor in Indonesia: insights into the evolution of marine lake populations. PLoS ONE 8, e75996.CrossRefGoogle ScholarPubMed
Bellwood, D.R., Hughes, T.P., Folke, C. and Nyström, M. (2004) Confronting the coral reef crisis. Nature 429, 827–833.CrossRefGoogle ScholarPubMed
Bryan, P.G. (1973) Growth rate, toxicity, and distribution of the encrusting sponge Terpios sp. (Hadromerida: Suberitidae) in Guam, Mariana Islands. Micronesica 9, 237–242.Google Scholar
Chadwick, N.E. and Morrow, K.M. (2011) Competition among sessile organisms on coral reefs. In Dubinsky, Z. and Stambler, N. (eds) Coral reefs: an ecosystem in transition. Dordrecht: Springer, pp. 347–371. http://dx.doi.org/10.1007/978-94-007-0114-4_20.CrossRefGoogle 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
Cleary, D.F.R., Becking, L.E., de Voogd, N.J., Renema, W., de Beer, M., van Soest, R.W.M. and Hoeksema, B.W. (2005) Variation in the diversity and composition of benthic taxa as a function of distance offshore, depth and exposure in the Spermonde Archipelago, Indonesia. Estuarine, Coastal and Shelf Science 65, 557–570.CrossRefGoogle Scholar
Cleary, D.F.R., De Vantier, L., Vail, L., Manto, P., de Voogd, N.J., Rachello-Dolmen, P.G. and Hoeksema, B.W. (2008) Relating variation in species composition to environmental variables: a multi-taxon study in an Indonesian coral reef complex. Aquatic Sciences 70, 419–431.CrossRefGoogle Scholar
Cleary, D.F.R. and de Voogd, N.J. (2007) Environmental associations of sponges in the Spermonde Archipelago, Indonesia. Journal of the Marine Biological Association of the United Kingdom 87, 1669–1676.CrossRefGoogle Scholar
Cornils, A., Schulz, J., Schmitt, P., Lanuru, M., Richter, C. and Schnack-Schiel, S. (2011) Mesozooplankton distribution in the Spermonde Archipelago (Indonesia, Sulawesi) with special reference to the Calanoida (Copepoda). Deep-Sea Research II 57, 2076–2088.CrossRefGoogle Scholar
de Voogd, N.J., Becking, L.E., Noor, A., Hoeksema, B.W. and van Soest, R.W.M. (2004) Sponge interactions with spatial competitors in SW Sulawesi. Bollettino dei Musei e degli Istituti Biologici dell'Universita di Genova 68, 253–261.Google Scholar
de Voogd, N.J., Cleary, D.F.R., Hoeksema, B.W., Noor, A. and van Soest, R.W.M. (2006) Sponge betadiversity in the Spermonde Archipelago, Indonesia. Marine Ecology Progress Series 309, 131–142.CrossRefGoogle Scholar
de Voogd, N.J., Cleary, D.F.R. and Dekker, F. (2013) The coral-killing sponge Terpios hoshinota invades Indonesia. Coral Reefs 32, 755.CrossRefGoogle Scholar
de Voogd, N.J., Haftka, J.J.H. and Hoeksema, B.W. (2005) Evaluation of the ecological function of amphitoxin in the reef-dwelling sponge Callyspongia (Euplacella) biru (Haplosclerida: Callyspongiidae) at southwest Sulawesi, Indonesia. Contributions to Zoology 74, 53–61.CrossRefGoogle Scholar
Edinger, E., Jompa, J. and Limmon, G. (1998) Reef degradation and coral biodiversity in Indonesia: effects of land-based pollution, destructive fishing practices and changes over time. Marine Pollution Bulletin 36, 617–630.CrossRefGoogle Scholar
English, S., Wilkinson, C. and Baker, V. (1997) Survey manual for tropical marine resources, 2nd edition. Townsville: Australian Institute of Marine Science.Google Scholar
Erftemeijer, P.L.A. (1994) Differences in nutrient concentrations and resources between seagrass communities on carbonate and terrigenous sediments in South Sulawesi, Indonesia. Bulletin of Marine Science 54, 403–419.Google Scholar
Erpenbeck, D., Knowlton, A.L., Talbot, S.L., Highsmith, R.C. and Van Soest, R.W.M. (2004) A molecular comparison of Alaskan and North East Atlantic Halichondria panicea (Pallas 1766) (Porifera: Demospongiae) populations. Bollettino dei Musei e degli Istituti Biologici dell'Universita di Genova 68, 319–325.Google Scholar
Fujii, T., Keshavmurthy, S., Zhou, W., Hirose, E., Chen, C.A. and Reimer, J.D. (2011) Coral-killing cyanobacteriosponge (Terpios hoshinota) on the Great Barrier Reef. Coral Reefs 30, 483.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Hoeksema, B.W. (2004) Biodiversity and the natural resource management of coral reefs in Southeast Asia. In Visser, L.E. (ed.) Challenging coasts. Transdisciplinary excursions into integrated coastal zone development. Amsterdam: Amsterdam University Press, pp. 49–71.Google Scholar
Hoeksema, B.W. (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. In Renema, W. (ed.) Biogeography, time and place: distributions, barriers and islands. Dordrecht: Springer, pp. 117–178.CrossRefGoogle Scholar
Hoeksema, B.W. (2012a) Distribution patterns of mushroom corals (Scleractinia: Fungiidae) across the Spermonde Shelf, Indonesia. Raffles Bulletin of Zoology 60, 183–212.Google Scholar
Hoeksema, B.W. (2012b) Evolutionary trends in onshore-offshore distribution patterns of mushroom coral species (Scleractinia: Fungiidae). Contributions to Zoology 81, 199–221.CrossRefGoogle Scholar
Hoeksema, B.W. and Crowther, A.L. (2011) Masquerade, mimicry and crypsis of the polymorphic sea anemone Phyllodiscus semoni Kwietniewski, 1897, and its aggregations in South Sulawesi. Contributions to Zoology 80, 251–268.CrossRefGoogle Scholar
Hoeksema, B.W., Dekker, F. and de Voogd, N.J. (2014a) Free-living mushroom corals strike back by overtopping a coral-killing sponge. Marine Biodiversity 44, 3–4.CrossRefGoogle Scholar
Hoeksema, B.W. and de Voogd, N.J. (2012) On the run: free-living mushroom corals avoiding interaction with sponges. Coral Reefs 31, 455–459.CrossRefGoogle Scholar
Hoeksema, B.W. and Koh, E.G.L. (2009) Depauperation of the mushroom coral fauna (Fungiidae) of Singapore (1860s–2006) in changing reef conditions. Raffles Bulletin of Zoology Supplement 22, 91–101.Google Scholar
Hoeksema, B.W., Waheed, Z. and de Voogd, N.J. (2014b) Partial mortality in corals overgrown by the sponge Terpios hoshinota at Tioman Island, Peninsular Malaysia (South China Sea). Bulletin of Marine Science 90, 989–990.CrossRefGoogle Scholar
Knittweis, L. and Wolff, M. (2010) Live coral trade impacts on the mushroom coral Heliofungia actiniformis (Scleractinia: Fungiidae) populations in the Indo-Malay Archipelago: implications for live coral trade management efforts. Conservation Genetics 10, 241–249.CrossRefGoogle Scholar
Liao, M.H., Tang, S.L., Hsu, C.M., Wen, K.C., Wu, H., Chen, W.M. and Chen, C.A. (2007) The “Black Disease” of reef-building corals at Green Island, Taiwan – outbreak of a cyanobacteriosponge, Terpios hoshinota (Suberitidae; Hadromerida). Zoological Studies 46, 520.Google Scholar
Librado, P. and Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
McCormack, G.P. and Kelly, M. (2002) New indications of the phylogenetic affinity of Spongosorites suberitoides Diaz et al. 1993 (Porifera Demospongiae) as revealed by 28 s ribosomal DNA. Journal of Natural History 36, 1009–1021.CrossRefGoogle Scholar
Meyer, C.P., Geller, J.B. and Paulay, G. (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59, 113–125.Google ScholarPubMed
Misof, B., Erpenbeck, D. and Sauer, K.P. (2000) Mitochondrial gene fragments suggest paraphyly of the genus Panorpa (Mecoptera, Panorpidae). Molecular Phylogenetics and Evolution 17, 76–84.CrossRefGoogle ScholarPubMed
Moll, H. (1983) Zonation and diversity of scleractinia on reefs off S. W. Sulawesi, Indonesia. PhD dissertation, Leiden University, the Netherlands.Google Scholar
Montano, S., Chou, W.H., Chen, C.A., Galli, P. and Reimer, J.D. (2015) First record of the coral-killing sponge Terpios hoshinota in the Maldives and Indian Ocean. Bulletin of Marine Science 91, 97–98.CrossRefGoogle Scholar
Munro, C. (2005) Diving systems. In Eleftheriou, A. and McIntyre, A. (eds) Methods for the study of marine benthos, 3rd edition. Oxford: Blackwell Science, pp. 112–159.CrossRefGoogle 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
Pet-Soede, C., Cesar, H.S.J. and Pet, J.S. (1999) An economic analysis of blast fishing on Indonesian coral reefs. Environmental Conservation 26, 83–93.CrossRefGoogle Scholar
Plucer-Rosario, G. (1987) The effect of substratum on the growth of Terpios, an encrusting sponge which kills corals. Coral Reefs 5, 197–200.CrossRefGoogle Scholar
Reimer, J.D., Mizuyama, M., Nakano, M., Fujii, T. and Hirose, E. (2011a) Current status of the distribution of the coral-encrusting cyanobacteriosponge Terpios hoshinota in southern Japan. Galaxea, Journal of Coral Reef Studies 13, 35–44.CrossRefGoogle Scholar
Reimer, J.D., Nozawa, Y. and Hirose, E. (2011b) Domination and disappearance of the black sponge: a quarter century after the initial Terpios outbreak in southern Japan. Zoological Studies 50, 394.Google Scholar
Renema, W., Hoeksema, B.W. and Van Hinte, J.E. (2001) Larger benthic foraminifera and their distribution patterns on the Spermonde shelf, South Sulawesi. Zoologische Verhandelingen 344, 115–150.Google Scholar
Renema, W. and Troelstra, S.R. (2001). Larger foraminifera distribution on a mesotrophic carbonate shelf in SW Sulawesi (Indonesia). Palaeogeography, Palaeoclimatology, Palaeoecology 175, 125–146.CrossRefGoogle Scholar
Reveillaud, J., Remerie, T., van Soest, R., Erpenbeck, D., Cárdenas, P., Derycke, S. and Vanreusel, A. (2010) Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae). Molecular Phylogenetics and Evolution 56, 104–114.CrossRefGoogle ScholarPubMed
Rützler, K. (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispanica 37, 61–72.Google Scholar
Rützler, K. and Muzik, K. (1993) Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. Scientia Marina 57, 395–403.Google Scholar
Sawall, Y., Teichberg, M., Seemann, J., Litaay, M., Jompa, J. and Richter, C. (2011) Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia). Coral Reefs 30, 841–853.CrossRefGoogle Scholar
Schils, T. (2012) Episodic eruptions of volcanic ash trigger a reversible cascade of nuisance species outbreaks in pristine coral habitats. PLoS ONE 7, e46639.CrossRefGoogle ScholarPubMed
Shi, Q., Liu, G.H., Yan, H.Q. and Zhang, H.L. (2012) Black disease (Terpios hoshinota): a probable cause for the rapid coral mortality at the northern reef of Yongxing Island in the South China Sea. Ambio 41, 446–455.CrossRefGoogle ScholarPubMed
Soong, K., Yang, S. and Chen, C.A. (2009) A novel dispersal mechanism of a coral-threatening sponge, Terpios hoshinota (Suberitidae, Porifera). Zoological Studies 48, 596–596.Google Scholar
Sterrenburg, F.A.S., Erftemeijer, P.L.A. and Nienhuis, P.H. (1995) Diatoms as epiphytes on seagrasses in South Sulawesi (Indonesia) comparison with growth on inert substrata. Botanica Marina 38, 1–8.CrossRefGoogle Scholar
Tang, S.L., Hong, M.J., Liao, M.H., Jane, W.N., Chiang, P.W., Chen, C.B. and Chen, C.A. (2011) Bacteria associated with an encrusting sponge (Terpios hoshinota) and the corals partially covered by the sponge. Environmental Microbiology 13, 1179–1191.CrossRefGoogle ScholarPubMed
Verheij, E. and Erftemeijer, P.L.A. (1993) Distribution of seagrasses and associated macroalgae in South Sulawesi, Indonesia. Blumea 38, 45–64.Google Scholar
Verheij, E. and Prud'homme van Reine, W.F. (1993) Seaweeds of the Spermonde Archipelago, SW Sulawesi, Indonesia. Blumea 37, 385–510.Google Scholar
Veron, J.E.N. (2000) Corals of the World, Volumes 1–3. Townsville: Australian Institute of Marine Science.Google Scholar
Wang, J.T., Chen, Y.Y., Meng, P.J., Sune, Y.H., Hsu, C.M., Wei, K.Y. and Chen, C.A. (2012) Diverse interactions between corals and the coral-killing sponge, Terpios hoshinota (Suberitidae: Hadromerida). Zoologial Studies 51, 150–159.Google Scholar
Wulff, J. (2012) Ecological interactions and the distribution, abundance, and diversity of sponges. Advances in Marine Biology 61, 146–166.Google ScholarPubMed