Coral Reefs

, Volume 35, Issue 3, pp 1083–1095 | Cite as

How does the proliferation of the coral-killing sponge Terpios hoshinota affect benthic community structure on coral reefs?

  • Jennifer ElliottEmail author
  • Mark Patterson
  • Natalie Summers
  • Céline Miternique
  • Emma Montocchio
  • Eugene Vitry


Terpios hoshinota is an encrusting sponge and a fierce space competitor. It kills stony corals by overgrowing them and can impact reefs on the square kilometer scale. We investigated an outbreak of T. hoshinota in 2014 at the island of Mauritius to determine its impacts on coral community structure. Surveys were conducted at the putative outbreak center, an adjacent area, and around the island to determine the extent of spread of the sponge and which organisms it impacted. In addition, quadrats were monitored for 5 months (July–December) to measure the spreading rates of T. hoshinota and Acropora austera in areas both with and without T. hoshinota. The photosynthetic capabilities of T. hoshinota and A. austera were also measured. Terpios hoshinota was well established, covering 13% of an estimated 416 m2 of available hard coral substrate at the putative outbreak center, and 10% of an estimated 588 m2 of available hard coral substrate at the adjacent area. The sponge was observed at only one other site around Mauritius. Terpios hoshinota and A. austera increased their planar areas by 26.9 and 13.9%, respectively, over five months. No new colonies of T. hoshinota were recorded in adjacent sponge-free control areas, suggesting that sponge recruitment is very low during austral winter and spring. The sponge was observed to overgrow five stony corals; however, it showed a preference for branching corals, especially A. austera. This is the first time that a statistically significant coral substrate preference by T. hoshinota has been reported. Terpios hoshinota also had a significantly higher photosynthetic capacity than A. austera at irradiance >500 μmol photons m−2 s−1, a possible explanation for its high spreading rate. We discuss the long-term implications of the proliferation of T. hoshinota on community structure and dynamics of our study site.


Mauritius Encrusting sponges Competition Photosynthesis nMDS 



We would like to thank the Ministry of Fisheries, Government of Mauritius and Attitude Resorts for their support. Special thanks go to Tarik Gouhier for statistical assistance, Stephen Elliott, and Rishi Persand for field assistance, and all those who provided helpful discussion. Support for physiological measurements provided by US National Science Foundation Awards #1412462 and #1146056 and by Northeastern University. This is contribution number 332 from the Marine Science Center, Northeastern University.


  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11:36–42Google Scholar
  2. Aerts LAM (1998) Sponge/coral interactions in Caribbean reefs: analysis of overgrowth patterns in relation to species identity and cover. Mar Ecol Prog Ser 175:241–249CrossRefGoogle Scholar
  3. Aerts LAM (2000) Dynamics behind standoff interactions in three reef sponge species and the coral Montastraea cavernosa. Mar Ecol 21:191–204CrossRefGoogle Scholar
  4. Aerts LAM, Van Soest RWM (1997) Quantification of sponge/coral interactions in a physically stressed reef community, NE Colombia. Mar Ecol Prog Ser 148:125–134CrossRefGoogle Scholar
  5. Ávila E, Carballo JL (2008) A preliminary assessment of the invasiveness of the Indo-Pacific sponge Chalinula nematifera on coral communities from the tropical Eastern Pacific. Biol Invasions 11:257–264CrossRefGoogle Scholar
  6. Benayahu Y, Loya Y (1981) Competition for space among coral-reef sessile organisms at Eilat, Red Sea. Bull Mar Sci 31:514–522Google Scholar
  7. Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Mar Pollut Bull 51:408–414CrossRefPubMedGoogle Scholar
  8. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York, NY, USACrossRefGoogle Scholar
  9. Brusca RC, Brusca GJ (2003) Phylum Porifera: the sponges. Invertebrates. Sinauer Press, Sunderland, MA, pp 179–208Google Scholar
  10. Bryan PG (1973) Growth rate, toxicity, and distribution of the encrusting sponge Terpios sp. (Hadromerida: Suberitidae) in Guam. Mariana Islands. Micronesica 9:238–242Google Scholar
  11. Chadwick-Furman N, Loya Y (1992) Migration, habitat use, and competition among mobile corals (Scleractinia: Fungiidae) in the Gulf of Eilat, Red Sea. Mar Biol 114:617–623CrossRefGoogle Scholar
  12. Chaves-Fonnegra A, Castellanos L, Zea S, Duque C, Rodríguez J, Jiménez C (2008) Clionapyrrolidine A—a metabolite from the encrusting and excavating sponge Cliona tenuis that kills coral tissue upon contact. J Chem Ecol 34:1565–1574CrossRefPubMedGoogle Scholar
  13. Coles SL, Bolick H (2007) Invasive introduced sponge Mycale grandis overgrows reef corals in Kāne‘ohe Bay, O‘ahu, Hawai‘i. Coral Reefs 26:911-911Google Scholar
  14. Coll JC, La Barre S, Sammarco PW, Williams WT, Bakus GJ (1982) Chemical defences in soft corals (coelenterata: octocorallia) of the Great Barrier Reef: a study of comparative toxicities. Mar Ecol Prog Ser 8:271–278CrossRefGoogle Scholar
  15. de Voogd NJ, Cleary DFR, Dekker F (2013) The coral-killing sponge Terpios hoshinota invades Indonesia. Coral Reefs 32:755-755CrossRefGoogle Scholar
  16. Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546Google Scholar
  17. Elliott J, Patterson M, Vitry E, Summers N, Miternique C (2015) Morphological plasticity allows coral to actively overgrow the aggressive sponge Terpios hoshinota (Mauritius. Mar Biodiv, Southwestern Indian Ocean). doi: 10.1007/s12526-015-0370-4 Google Scholar
  18. Ferreira C, Gonçalves J, Coutinho R (1998) Herbivory by the dusky damselfish Stegastes fuscus (Cuvier, 1830) in a tropical rocky shore: effects on the benthic community. J Exp Mar Bio Ecol 229:241–264CrossRefGoogle Scholar
  19. Finelli CM, Helmuth BS, Pentcheff ND, Wethey DS (2007) Intracolony variability in photosynthesis by corals is affected by water flow: role of oxygen flux. Mar Ecol Prog Ser 349:103–110CrossRefGoogle Scholar
  20. Fujii T, Keshavmurthy S, Zhou W, Hirose E, Chen CA, Reimer JD (2011) Coral-killing cyanobacteriosponge (Terpios hoshinota) on the Great Barrier Reef. Coral Reefs 30:483-483CrossRefGoogle Scholar
  21. Gladfelter EH, Monahan RK (1978) Growth rates of five reef-building corals in the northeastern Caribbean. Bull Mar Sci 28:728–734Google Scholar
  22. Guinan J, Grehan AJ, Dolan M, Brown C (2009) Quantifying relationships between video observations of cold-water coral cover and seafloor features in Rockall Trough, west of Ireland. Mar Ecol Prog Ser 375:125–138CrossRefGoogle Scholar
  23. Harrington L, Fabricius K, De’ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437CrossRefGoogle Scholar
  24. Hidaka M (1985) Nematocyst discharge, histoincompatibility, and the formation of sweeper tentacles in the coral Galaxea fascicularis. Biol Bull 168:350–358CrossRefGoogle Scholar
  25. Hoeksema BW, Dekker F, de Voogd NJ (2014a) Free-living mushroom corals strike back by overtopping a coral-killing sponge. Mar Biodiv 44:3–4CrossRefGoogle Scholar
  26. Hoeksema BW, Waheed Z, de Voogd NJ (2014b) Partial mortality in corals overgrown by the sponge Terpios hoshinota at Tioman Island, Peninsular Malaysia (South China Sea). Bull Mar Sci 90:989–990CrossRefGoogle Scholar
  27. Hoppe WF (1988) Growth, regeneration and predation in three species of large coral reef sponges. Mar Ecol Prog Ser 50:117–125CrossRefGoogle Scholar
  28. Hsu C-M, Wang J-T, Chen CA (2013) Larval release and rapid settlement of the coral-killing sponge, Terpios hoshinota, at Green Island, Taiwan. Mar Biodiv 43:259–260CrossRefGoogle Scholar
  29. Johnson CR, Mann KH (1986) The crustose coralline alga, Phymatolithon Foslie, inhibits the overgrowth of seaweeds without relying on herbivores. J Exp Mar Bio Ecol 96:127–146CrossRefGoogle Scholar
  30. Keats DW, Knight MA, Pueschel CM (1997) Antifouling effects of epithelial shedding in three crustose coralline algae (Rhodophyta, Coralinales) on a coral reef. J Exp Mar Bio Ecol 213:281–293CrossRefGoogle Scholar
  31. Kim M-J, Choi J-S, Kang S-E, Cho J-Y, Jin H-J, Chun B-S, Hong Y-K (2004) Multiple allelopathic activity of the crustose coralline alga Lithophyllum yessoense against settlement and germination of seaweed spores. J Appl Phycol 16:175–179CrossRefGoogle Scholar
  32. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269CrossRefGoogle Scholar
  33. Lang J (1973) Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull Mar Sci 23:260–279Google Scholar
  34. Loh TL, McMurray SE, Henkel TP, Vicente J, Pawlik JR (2015) Indirect effects of overfishing on Caribbean reefs: sponges overgrow reef-building corals. PeerJ 2015:e901CrossRefGoogle Scholar
  35. López-Victoria M, Zea S, Weil E (2006) Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms. Mar Ecol Prog Ser 312:113–121CrossRefGoogle Scholar
  36. McAuliffe JR (1990) A rapid survey method for the estimation of density and cover in desert plant communities. J Veg Sci 1:653–656CrossRefGoogle Scholar
  37. McFadden CS, Reynolds AM, Janes MP (2014) DNA barcoding of xeniid soft corals (Octocorallia: Alcyonacea: Xeniidae) from Indonesia: species richness and phylogenetic relationships. System Biodivers 12:247–257CrossRefGoogle Scholar
  38. McKenna SA (1997) Interactions between the boring sponge, Cliona lampa and two hermatypic corals from Bermuda. Proc 8th Int Coral Reef Symp 2:1369–1374Google Scholar
  39. Montano S, Chou W-H, Chen CA, Galli P, Reimer JD (2015) First record of the coral-killing sponge Terpios hoshinota in the Maldives and Indian Ocean. Bull Mar Sci 91:97–98CrossRefGoogle Scholar
  40. Pawlik JR, Steindler L, Henkel TP, Beer S, Ilan M (2007) Chemical warfare on coral reefs: sponge metabolites differentially affect coral symbiosis in situ. Limnol Oceanogr 52:907–911CrossRefGoogle Scholar
  41. Pile AJ, Patterson MR, Witman JD (1996) In situ grazing on plankton <10 µm by the boreal sponge Mycale lingua. Mar Ecol Prog Ser 141:92–105CrossRefGoogle Scholar
  42. Plucer-Rosario G (1987) The effect of substratum on the growth of Terpios, an encrusting sponge which kills corals. Coral Reefs 5:197–200CrossRefGoogle Scholar
  43. Porter JW, Targett NM (1988) Allelochemical interactions between sponges and corals. Biol Bull 175:230–239CrossRefGoogle Scholar
  44. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  45. Reimer JD, Nozawa Y, Hirose E (2010) Domination and disappearance of the black sponge: a quarter century after the initial Terpios outbreak in southern Japan. Zool Stud 50:394Google Scholar
  46. Reimer JD, Mizuyama M, Nakano M, Fujii T, Hirose E (2011) Current status of the distribution of the coral-encrusting cyanobacteriosponge Terpios hoshinota in southern Japan. Galaxea 13:35–44CrossRefGoogle Scholar
  47. Richardson CA, Dustan P, Lang JC (1979) Maintenance of living space by sweeper tentacles of Montastrea cavernosa, a Caribbean reef coral. Mar Biol 55:181–186CrossRefGoogle Scholar
  48. Rose CS, Risk MJ (1985) Increase in Cliona delitrix infestation of Montastrea cavernosa heads on an organically polluted portion of the Grand Cayman fringing reef. Mar Ecol 6:345–363CrossRefGoogle Scholar
  49. Rossi G, Montori S, Cerrano C, Calcinai B (2015) The coral killing sponge Chalinula nematifera (Porifera: Haplosclerida) along the eastern coast of Sulawesi Island (Indonesia). Ital J Zool 82:143–148CrossRefGoogle Scholar
  50. Rützler K (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geologica Hispanica 37:61–72Google Scholar
  51. Rützler K, Muzik K (1993) Terpios hoshinota, a new cyanobacteriosponge threatening Pacific reefs. Sci Mar 57:395–403Google Scholar
  52. Sammarco PW, Coll JC, La Barre S, Willis B (1983) Competitive strategies of soft corals (Coelenterata: Octocorallia): allelopathic effects on selected scleractinian corals. Coral Reefs 1:173–178CrossRefGoogle Scholar
  53. Schils T (2012) Episodic eruptions of volcanic ash trigger a reversible cascade of nuisance species outbreaks in pristine coral habitats. PLoS One 7:e46639CrossRefPubMedPubMedCentralGoogle Scholar
  54. Schonberg C, Wilkinson C (2001) Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20:69–76CrossRefGoogle Scholar
  55. Shi Q, Liu GH, Yan HQ, Zhang HL (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 41:446–455CrossRefPubMedPubMedCentralGoogle Scholar
  56. Suzuki Y, Takabayashi T, Kawaguchi T, Matsunaga K (1998) Isolation of an allelopathic substance from the crustose coralline algae, Lithophyllum spp., and its effect on the brown alga, Laminaria religiosa Miyabe (Phaeophyta). J Exp Mar Bio Ecol 225:69–77CrossRefGoogle Scholar
  57. Tang S-L, Hong M-J, Liao M-H, Jane W-N, Chiang P-W, Chen C-B, Chen CA (2011) Bacteria associated with an encrusting sponge (Terpios hoshinota) and the corals partially covered by the sponge. Environ Microbiol 13:1179–1191CrossRefPubMedGoogle Scholar
  58. Teruya T, Nakagawa S, Koyama T, Arimoto H, Kita M, Uemura D (2004) Nakiterpiosin and nakiterpiosinone, novel cytotoxic C-nor-D-homosteroids from the Okinawan sponge Terpios hoshinota. Tetrahedron 60:6989–6993CrossRefGoogle Scholar
  59. Turner J, Klaus R (2005) Coral reefs of the Mascarenes, western Indian Ocean. Philos Trans R Soc Lond A 363:229–250CrossRefGoogle Scholar
  60. Van der Ent E, Hoeksema BW, de Voogd NJ (2015) Abundance and genetic variation of the coral-killing cyanobacteriosponge Terpios hoshinota in the Spermonde Archipelago, SW Sulawesi, Indonesia. J Mar Biol Assoc UK 96:453–463Google Scholar
  61. Vermeij MJA, van Moorselaar I, Engelhard S, Hörnlein C, Vonk SM, Visser PM (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS One 5:e14312–e14318CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wang JT, Chen YY, Meng PJ, Sune YH, Hsu CM, Wei KY, Chen CA (2012) Diverse interactions between corals and the coral-killing sponge, Terpios hoshinota (Suberitidae: Hadromerida). Zool Stud 51:150–159Google Scholar
  63. Wilkinson CR (1983) Net primary productivity in coral reef sponges. Science 219:410–412CrossRefPubMedGoogle Scholar
  64. Yahel G, Sharp JH, Marie D, Häse C, Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: bulk DOC is the major source for carbon. Limnol Oceanogr 48:141–149CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Northeastern UniversityNahantUSA
  2. 2.Reef ConservationPéreybèreMauritius

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