Marine Biology

, 164:220 | Cite as

Increasing benthic dominance of the phototrophic sponge Lamellodysidea herbacea on a sedimented reef within the Coral Triangle

  • A. BiggerstaffEmail author
  • J. Jompa
  • J. J. Bell
Original paper


Coral abundance on tropical reefs is declining due to climatic change and other direct anthropogenic impacts. The long-term consequences of coral ‘regime-shifts’ are not fully understood, but they are expected to impact ecosystem services (e.g., ecotourism and fisheries). Within the Wakatobi region of Indonesia a coral-to-sponge regime-shift has occurred on a sedimented reef (Sampela). The dominant sponge species, Lamellodysidea herbacea, is a phototrophic sponge that appears to be proliferating through effective sediment clearance mechanisms and rapid photoacclimation to turbid conditions. L. herbacea monitoring is required to determine whether this ecosystem is still transitioning, stable or whether the regime-shift is transient. This study (2013–2015) assessed the percentage cover and abundance of L. herbacea, along with the quantity of settled sediment, at Sampela, Pak Kasim’s (a nearby reef) and multiple reefs in the region. High growth rates for individual L. herbacea, but low recruitment rates were recorded at Sampela. Increases in the proportion of L. herbacea that decreased in areal coverage between sampling periods indicate short periods of positive growth, with this effect being greater in deeper, more sedimented zones. The percentage cover and abundance of L. herbacea, and the quantity of settled sediment, was low at all surrounding reefs and remained stable at Pak Kasim’s. However, the percentage cover of L. herbacea at Sampela was high and increased, in conjunction with a stable, comparatively high quantity of settled sediment. These results are the first to document a reef in the process of transitioning towards greater sponge dominance and indicate that efforts to reverse this regime-shift would likely require a reduced level of sedimentation.



This research was funded by a Victoria University of Wellington doctoral scholarship awarded to Andrew Biggerstaff. A research permit for this research was issued to Prof David Smith in collaboration with Prof Jamal Jompa by the Indonesian Ministry of Research and Technology (RISTEK). We also thank Operation Wallacea for providing funding for travel and accommodation associated with the data collection and the staff and volunteers of Hoga Island Marine Research Station.

Compliance with ethical standards


No funding from outside institutions, foundations or companies was received for this study other than has been mentioned in the “Acknowledgements”.

Conflict of interest

Andrew Biggerstaff declares that he has no conflict of interest. James John Bell declares that he has no conflict of interest. Jamal Jompa declares that he has no conflict of interest.

Ethical approval

This article does not contain any experimental studies with animals performed by any of the authors.

Supplementary material

227_2017_3253_MOESM1_ESM.pdf (399 kb)
Supplementary material 1 (PDF 399 kb)


  1. Anthony KR, Connolly SR (2004) Environmental limits to growth: physiological niche boundaries of corals along turbidity–light gradients. Oecologia 141:373–384CrossRefGoogle Scholar
  2. Antonius A, Ballesteros E (1998) Epizoism: a new threat to coral health in Caribbean reefs. Rev Biol Trop 46:145–156Google Scholar
  3. Aronson RB, Precht WF, Toscano MA, Koltes KH (2002) The 1998 bleaching event and its aftermath on a coral reef in Belize. Mar Bio 141:435–447CrossRefGoogle Scholar
  4. Ayling AL (1980) Patterns of sexuality, asexual reproduction and recruitment in some subtidal marine Demospongiae. Biol Bull 158:271–282CrossRefGoogle Scholar
  5. Ayling AL (1983) Growth and regeneration rates in thinly encrusting demospongiae from temperate waters. Biol Bull 165:343–352CrossRefGoogle Scholar
  6. Bell JJ (2008a) The functional roles of marine sponges. Estuar Coast Shelf S 79:341–353CrossRefGoogle Scholar
  7. Bell JJ (2008b) Sponges as agents of biological disturbance. Mar Ecol Prog Ser 368:127–135CrossRefGoogle Scholar
  8. Bell JJ, Smith D (2004) Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: richness and abundance. J Mar Biol Assoc UK 84:581–591CrossRefGoogle Scholar
  9. Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Glob Change Biol 19:2613–2624CrossRefGoogle Scholar
  10. Bell JJ, Smith D, Hannan D, Haris A, Jompa J, Thomas L (2014) Resilience to disturbance despite limited dispersal and self-recruitment in tropical barrel sponges: implications for conservation and management. PLoS One 9:e91635CrossRefGoogle Scholar
  11. Biggerstaff A, Smith DJ, Jompa J, Bell JJ (2015) Photoacclimation supports environmental tolerance of a sponge to turbid low-light conditions. Coral Reefs 34:1049–1061CrossRefGoogle Scholar
  12. Biggerstaff A, Smith DJ, Jompa J, Bell JJ (2017) Metabolic responses of a phototrophic sponge to sedimentation supports transitions to sponge-dominated reefs. Sci Rep 7:2725CrossRefGoogle Scholar
  13. Browne NK (2012) Spatial and temporal variations in coral growth on an inshore turbid reef subjected to multiple disturbances. Mar Environ Res 77:71–83CrossRefGoogle Scholar
  14. Browne NK, Smithers SG, Perry CT (2012) Coral reefs of the turbid inner-shelf of the Great Barrier Reef, Australia: an environmental and geomorphic perspective on their occurrence, composition and growth. Earth Sci Rev 115:1–20CrossRefGoogle Scholar
  15. Crabbe MJC, Smith DJ (2005) Sediment impacts on growth rates of Acropora and Porites corals from fringing reefs of Sulawesi, Indonesia. Coral Reefs 24:437–441CrossRefGoogle Scholar
  16. de Cook SC, Bergquist PR (2002) Family Dysideidae Gray, 1867. In: Hooper JNA, van Soest RWM, Willenz P (eds) Systema Porifera. Springer, USA, pp 1061–1066CrossRefGoogle Scholar
  17. de Goeij JM, van den Berg H, van Oostveen MM, Epping EH, Van Duyl FC (2008) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357:139–151CrossRefGoogle Scholar
  18. de Goeij JM, van Oevelen D, Vermeij MJ, Osinga R, Middelburg JJ, de Goeij AF, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110CrossRefGoogle Scholar
  19. de Groot R, Brander L, van der Ploeg S, Costanza R, Bernard F, Braat L, Christie M, Crossman N, Ghermandi A, Hein L, Hussain S (2012) Global estimates of the value of ecosystems and their services in monetary units. Ecosyst Serv 1:50–61CrossRefGoogle Scholar
  20. De’ath G, Fabricius K (2008) Water quality of the Great Barrier Reef: distributions, effects on reef biota and trigger values for the protection of ecosystem health. Great Barrier Reef Marine Park Auth 89:11Google Scholar
  21. Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546Google Scholar
  22. Dudgeon SR, Aronson RB, Bruno JF, Precht WF (2010) Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser 413:201–216CrossRefGoogle Scholar
  23. Erftemeijer PL, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: a review. Mar Pollut Bull 64:1737–1765CrossRefGoogle Scholar
  24. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146CrossRefGoogle Scholar
  25. Fisher R, O’Leary RA, Low-Choy S, Mengersen K, Knowlton N, Brainard RE, Caley MJ (2015) Species richness on coral reefs and the pursuit of convergent global estimates. Curr Biol 25:500–505CrossRefGoogle Scholar
  26. Golbuu Y, Van Woesik R, Richmond RH, Harrison P, Fabricius KE (2011) River discharge reduces reef coral diversity in Palau. Mar Pollut Bull 62:824–831CrossRefGoogle Scholar
  27. Graham NA, Bellwood DR, Cinner JE, Hughes TP, Norström AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Front Ecol Environ 11:541–548CrossRefGoogle Scholar
  28. Harborne AR, Rogers A, Bozec YM, Mumby PJ (2017) Multiple stressors and the functioning of coral reefs. Annu Rev Mar Sci 9:445–468CrossRefGoogle Scholar
  29. Hare SR, Mantua NJ (2000) Emperical evidence for North Pacific regime shifts in 1977 and 1989. Prog Oceanogr 47:103–145CrossRefGoogle Scholar
  30. Hill J, Wilkinson C (2004) Methods for ecological monitoring of coral reefs. Aust Inst Mar Sci Townsville 1:56–63Google Scholar
  31. Hoegh-Guldberg O (2011) Coral reef ecosystems and anthropogenic climate change. Reg Environ Change 11:215–227CrossRefGoogle Scholar
  32. Hooper JNA, Lévi C (1994) Biogeography of Indo-west Pacific sponges: Microcionidae, Raspailiidae, Axinellidae. In: van Soest RWM, van Kempen TMG, Braekman JC (eds) Sponges in time and space. Balkema, Rotterdam, pp 191–212Google Scholar
  33. Jones RJ (2011) Environmental effects of the cruise tourism boom: sediment resuspension from cruise ships and the possible effects of increased turbidity and sediment deposition on corals (Bermuda). Bull Mar Sci 87:659–679CrossRefGoogle Scholar
  34. Karlson R (1978) Predation and space utilization patterns in a marine epifaunal community. J Exp Mar Biol Ecol 31:225–239CrossRefGoogle Scholar
  35. Kelmo F (2002) Ecological consequences of the 1997–98 El Niño Southern Oscillation on the major coral reef communities from northern Bahia, Brazil. PhD thesis, University of Plymouth, PlymouthGoogle Scholar
  36. Larcombe P, Ridd PV, Prytz A, Wilson B (1995) Factors controlling suspended sediment on inner-shelf coral reefs, Townsville, Australia. Coral Reefs 14:163–171CrossRefGoogle Scholar
  37. Lopez-Victoria M, Zea S (2005) Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Mar Ecol 26:33–41CrossRefGoogle Scholar
  38. Madden RH, Wilson ME, O’Shea M (2013) Modern fringing reef carbonates from equatorial SE Asia: an integrated environmental, sediment and satellite characterisation study. Mar Geol 344:163–185CrossRefGoogle Scholar
  39. Maldonado M, Uriz MJ (1998) Microrefuge exploitation by subtidal encrusting sponges: patterns of settlement and post-settlement survival. Mar Ecol Prog Ser 174:141–150CrossRefGoogle Scholar
  40. Maldonado M, Riesgo A, Bucci A (2010) Revisiting silicon budgets at a tropical continental shelf: silica standing stocks in sponges surpass those in diatoms. Limnol Oceanogr 55:2001–2010CrossRefGoogle Scholar
  41. Maliao RJ, Turingan RG, Lin J (2008) Phase-shift in coral reef communities in the Florida Keys National Marine Sanctuary (FKNMS), USA. Mar Biol 154:841–853CrossRefGoogle Scholar
  42. Mallela J, Parkinson R, Day O (2010) An assessment of coral reefs in Tobago. Caribb J Sci 46:83–87CrossRefGoogle Scholar
  43. McMurray SE, Blum JE, Pawlik JR (2008) Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. Mar Biol 155:159–171CrossRefGoogle Scholar
  44. Muzuka AN, Dubi AM, Muhando CA, Shaghude YW (2010) Impact of hydrographic parameters and seasonal variation in sediment fluxes on coral status at Chumbe and Bawe reefs, Zanzibar, Tanzania. Estuar Coast Shelf S 89:137–144CrossRefGoogle Scholar
  45. Norström AV, Nystrom M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306CrossRefGoogle Scholar
  46. Pandolfi JM (2015) Incorporating uncertainty in predicting the future response of coral reefs to climate change. Annu Rev Ecol Evol Syst 46:281–303CrossRefGoogle Scholar
  47. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422CrossRefGoogle Scholar
  48. Perea-Blazquez A, Davy SK, Bell JJ (2012) Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PLoS One 7:e29569CrossRefGoogle Scholar
  49. Petersen JK, Hansen JW, Laursen MB, Clausen P, Carstensen J, Conley DJ (2008) Regime shift in a coastal marine ecosystem. Ecol Appl 18:497–510CrossRefGoogle Scholar
  50. Pineda MC, Duckworth A, Webster N (2016) Appearance matters: sedimentation effects on different sponge morphologies. J Mar Biol Assoc UK 96:481–492CrossRefGoogle Scholar
  51. 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
  52. Pollock FJ, Lamb JB, Field SN, Heron SF, Schaffelke B, Shedrawi G, Bourne DG, Willis BL (2014) Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS One 9:e102498CrossRefGoogle Scholar
  53. Powell AL, Hepburn LJ, Smith DJ, Bell JJ (2010) Patterns of sponge abundance across a gradient of habitat quality in the Wakatobi Marine National Park, Indonesia. Open Mar Biol J 4:31–38CrossRefGoogle Scholar
  54. Powell AL, Smith DJ, Hepburn LJ, Jones T, Berman J, Jompa J, Bell JJ (2014) Reduced diversity and high sponge Abundance on a sedimented Indo-Pacific reef system: implications for future changes in environmental quality. PLoS One 9:e85253CrossRefGoogle Scholar
  55. Roberts DE, Davis AR (1996) Patterns in sponge (Porifera) assemblages on temperate coastal reefs off Sydney, Australia. Mar Freshw Res 47:897–906CrossRefGoogle Scholar
  56. Rützler K (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geol Hisp 37:61–72Google Scholar
  57. Sale PF, Hixon MA (2014) Addressing the global decline in coral reefs and forthcoming impacts on fishery yields. Interrelationships between coral reefs and fisheries. CRC Press, Boca Raton, pp 7–18Google Scholar
  58. Salinas-de-León P, Dryden C, Smith DJ, Bell JJ (2013) Temporal and spatial variability in coral recruitment on two Indonesian coral reefs: consistently lower recruitment to a degraded reef. Mar Biol 160:97–105CrossRefGoogle Scholar
  59. Schils T (2012) Episodic eruptions of volcanic ash trigger a reversible cascade of nuisance species outbreaks in pristine coral habitats. PLOS One. 7:e46639CrossRefGoogle Scholar
  60. Slattery M, Kamel HN, Ankisetty S, Gochfeld DJ, Hoover CA, Thacker RW (2008) Hybrid vigor in a tropical pacific soft-coral community. Ecol Monogr 78:423–443CrossRefGoogle Scholar
  61. Unsworth RK, Clifton J, Smith DJ (2010) Marine research and conservation in the Coral Triangle: the Wakatobi National Park. Nova Science, pp. 17–32Google Scholar
  62. Ward-Paige CA, Risk MJ, Sherwood OA, Jaap WC (2005) Clionid sponge surveys on the Florida reef tract suggest land-based nutrient inputs. Mar Pollut Bull 51:570–579CrossRefGoogle Scholar
  63. Wilkinson CR (1987) Interocean differences in size and nutrition of coral reef sponge populations. Science 236:1654–1667CrossRefGoogle Scholar
  64. Wilkinson CR, Cheshire AC (1990) Comparisons of sponge populations across the Barrier Reefs of Australia and Belize: evidence for higher productivity in the Caribbean. Mar Ecol Prog Ser 67:285–294CrossRefGoogle Scholar
  65. Wilkinson CR, Evans E (1989) Sponge distribution across Davies Reef, great barrier reef, relative to location, depth, and water movement. Coral Reefs 8:1–7CrossRefGoogle Scholar
  66. Williams EH, Bartels PJ, Bunkley-Williams L (1999) Predicted disappearance of coral-reef ramparts: a direct result of major ecological disturbances. Glob Change Biol 5:839–845CrossRefGoogle Scholar
  67. Wulff JL (2006) Ecological interactions of marine sponges. Can J Zoolog 84:146–166CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  2. 2.Research and Development Centre on Marine, Coastal and Small IslandsHasanuddin UniversityMakassarIndonesia

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