Coral Reefs

, Volume 34, Issue 4, pp 1049–1061 | Cite as

Photoacclimation supports environmental tolerance of a sponge to turbid low-light conditions

  • A. Biggerstaff
  • D. J. Smith
  • J. Jompa
  • J. J. Bell


Changes to coral reefs are occurring worldwide, often resulting in declining environmental quality which can be in the form of higher sedimentation rates and increased turbidity. While environmental acclimation to turbid and low-light conditions has been extensively studied in corals, far less is known about other phototrophic reef invertebrates. The photosynthetic cyanobacteria containing sponge Lamellodysidea herbacea is one of the most abundant sponges in the Wakatobi Marine National Park (WMNP, Indonesia), and its abundance is greatest at highly disturbed, turbid sites. This study investigated photoacclimation of L. herbacea symbionts to turbid reef sites using in situ PAM fluorometry combined with shading and transplant experiments at environmental extremes of light availability for this species. We found in situ photoacclimation of L. herbacea to both shallow, clear, high-light environments and deep, turbid, low-light environments. Shading experiments provide some evidence that L. herbacea are dependent on nutrition from their photosymbionts as significant tissue loss was seen in shaded sponges. Symbionts within surviving shaded tissue showed evidence of photoacclimation. Lamellodysidea herbacea transplanted from high- to low-light conditions appeared to have photoacclimated within 5 d with no significant effect of the lowered light level on survival. This ability of L. herbacea to photoacclimate to rapid and extreme changes in light availability may be one of the factors contributing to their survival on more turbid reef sites in the WMNP. Our study highlights the ability of some sponge species to acclimate to changes in light levels as a result of increased turbidity.


Sponge Photophysiology Coral reef Phase shifts Turbidity Acclimation 



This research was facilitated by a Victoria University of Wellington doctoral scholarship awarded to Andrew Biggerstaff. A research permit for this research was issued to Professor David Smith from 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.

Supplementary material

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Supplementary material 1 (DOCX 20 kb)


  1. Anthony KRN, Fabricius KFF (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253CrossRefPubMedGoogle Scholar
  2. Bañares-España E, Kromkamp JC, López-Rodas V, Costas E, Flores-Moya A (2013) Photoacclimation of cultured strains of the cyanobacterium Microcystis aeruginosa to high-light and low-light conditions. FEMS Microbiol Ecol 83:700–710CrossRefPubMedGoogle Scholar
  3. Bandaranayake WM, Bourne DJ, Sim RG (1997) Chemical Composition during Maturing and Spawning of the Sponge Dysidea herbacea (Porifera: Demospongiae). Comp Biochem Phys B 118:851–859CrossRefGoogle Scholar
  4. Beer S, Ilan M (1998) In situ measurements of photosynthetic irradiance responses of two Red Sea sponges growing under dim light conditions. Mar Biol 131:613–617CrossRefGoogle Scholar
  5. Bell JJ (2007) Contrasting patterns of species and functional composition of coral reef sponge assemblages. Mar Ecol Prog Ser 339:73–81CrossRefGoogle Scholar
  6. Bell JJ (2008) The functional roles of marine sponges. Estur Coast Shelf S 79:341–353CrossRefGoogle Scholar
  7. 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
  8. 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
  9. Bell JJ, McGrath E, Biggerstaff A, Bates T, Bennett H, Marlow J, Shaffer M (2015) Sediment impacts on marine sponges. Mar Poll Bull 94:5–13CrossRefGoogle Scholar
  10. Berthold RJ, Borowitzka MA, Mackay MA (1982) The ultrastructure of Oscillatoria spongeliae, the blue-green algal endosymbiont of the sponge Dysidea herbacea. Phycologia 21:327–335CrossRefGoogle Scholar
  11. Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington, DC, pp 3–9Google Scholar
  12. Campbell D (1996) Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142:1255–1263CrossRefGoogle Scholar
  13. Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol R 62:667–683Google Scholar
  14. Cleary DFR, de Voogd NJ (2007) Environmental associations of sponges in the Spermonde Archipelago, Indonesia. J Mar Biol Assoc UK 87:1669–1676CrossRefGoogle Scholar
  15. Clifton J, Unsworth RKF (2010) Introduction to the Wakatobi National Park, Chapter 1. In: Clifton J, Unsworth RKF, Smith DJ (eds) Marine Conservation and Research in the Coral Triangle: The Wakatobi National Park. Nova Publishers, New York, pp 1–9Google Scholar
  16. Cook SD, Bergquist PR (2002) Family Dysideidae Gray, 1867. In: Hooper JNA, van Soest RWM (eds) Systema porifera. A guide to the classification of sponges. Kluwer Academic/Plenum, New York, pp 1061–1066Google Scholar
  17. Crabbe MJC, Smith DJ (2005) Sediment impacts on growth rates of Acroporaand Porites corals from fringing reefs of Sulawesi, Indonesia. Coral Reefs 24:437–441CrossRefGoogle Scholar
  18. de Goeij JM, Van Den Burg H, Van Oostveen MM, Epping EHG, 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
  19. de Voogd NJ, Cleary DFR (2007) Relating species traits to environmental variables in Indonesian coral reef sponge assemblages. Mar Freshwater Res 58:240–249CrossRefGoogle Scholar
  20. de Voogd NJ, Cleary DFR (2008) An analysis of sponge diversity and distribution at three taxonomic levels in the Thousand Islands/Jakarta Bay reef complex, West-Java, Indonesia. Mar Ecol 29:205–215CrossRefGoogle Scholar
  21. de Voogd NJ, Beckling LE, Cleary DFR (2009) Sponge community composition in the Derawan Islands, NE Kalimantan, Indonesia. Mar Ecol Prog Ser 396:169–180CrossRefGoogle Scholar
  22. de Voogd NJ, Cleary DFR, Hoeksema BW, Noor A, van Soest RWM (2006) Sponge beta diversity in the Spermonde Archipelago, SW Sulawesi, Indonesia. Mar Ecol Prog Ser 309:131–142CrossRefGoogle Scholar
  23. Erpenbeck D, Hooper JNA, Bonnard I, Sutcliffe P, Chandra M, Perio P, Wolff C, Banaigs B, Worheide G, Debitus C, Petek S (2012) Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites. Mar Biol 159:1119–1127CrossRefGoogle Scholar
  24. Fujita Y, Murakami A, Aizawa K, Ohki K (1994) Short-term and long-term adaptation of the photosynthetic apparatus: homeostatic properties of thylakoids. In: Bryant DA (ed) The molecular biology of cyanobacteria. Springer, Netherlands, pp 677–692CrossRefGoogle Scholar
  25. Gévaert F, Créach A, Davoult D, Migné A, Levasseur G, Arzel P, Holl A-C, Lemoine Y (2003) Laminaria saccharina photosynthesis measured in situ: photoinhibition and xanthophyll cycle during a tidal cycle. Mar Ecol Prog Ser 247:43–50CrossRefGoogle Scholar
  26. Green TGA, Schroeter B, Kappen L, Seppelt RD, Maseyk K (1998) An assessment of the relationship between chlorophyll a fluorescence and CO2 gas exchange from field measurements on a moss and lichen. Planta 206:611–618CrossRefGoogle Scholar
  27. Hennige SJ, Smith DJ, Walsh SJ, McGinley MP, Warner ME, Sugget DJ (2010) Acclimation and adaptation of scleractinian coral communities along environmental gradients within an Indonesian reef system. J Exp Mar Biol Ecol 391:143–152CrossRefGoogle Scholar
  28. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatsiolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefPubMedGoogle Scholar
  29. Hoegh-Guldberg O (2011) Coral reef ecosystems and anthropogenic climate change. Reg Environ Change 11:215–227CrossRefGoogle Scholar
  30. Hooper JNA, Levi C (1994) Biogeography of Indo-west Pacific sponges: Microcionidae, Raspailiidae, Axinellidae. In: Braekman JC, van Kampen TMG, van Soest RWG (eds) Sponges in time and space. Balkema, Rotterdam, pp 265–271Google Scholar
  31. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  32. Kromkamp JC, Domin A, Dubinsky Z, Lehmann C, Schanz F (2001) Changes in photosynthetic properties measured by oxygen evolution and variable chlorophyll fluorescence in a simulated entrainment experiment with the cyanobacterium Planktothrix rubescens. Aquat Sci 63:363–382CrossRefGoogle Scholar
  33. Lemloh ML, Fromont J, Brümmer F, Usher KM (2009) Diversity and abundance of photosynthetic sponges in temperate Western Australia. BMC Ecol 9:4PubMedCentralCrossRefPubMedGoogle Scholar
  34. Lopez-Victoria M, Zea S (2004) Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Mar Ecol 26:33–41CrossRefGoogle Scholar
  35. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38CrossRefGoogle Scholar
  36. Maldonado M, Riesgo A, Bucci A, Rutzler K (2010) Revisiting silicon budgets at a tropical continental shelf: Silica standing stocks in sponges surpass those in diatoms. Limnol Oceanogr 55:2001–2010CrossRefGoogle Scholar
  37. Masojídek J, Grobbelaar JU, Pechar L, KoblíŽek M (2001) Photosystem II electron transport rates and oxygen production in natural waterblooms of freshwater cyanobacteria during a diel cycle. J Plankton Res 23:57–66CrossRefGoogle Scholar
  38. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659–688CrossRefPubMedGoogle Scholar
  39. McMinn A, Ryan K, Gademann R (2003) Diurnal changes in photosynthesis of Antarctic fast ice algal communities determined by pulse amplitude modulation fluorometry. Mar Biol 143:359–367CrossRefGoogle Scholar
  40. 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
  41. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems. Science 301:955–958CrossRefPubMedGoogle Scholar
  42. 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:e29569PubMedCentralCrossRefPubMedGoogle Scholar
  43. Powell AL (2013) The impacts of fish predation and habitat degradation on Indo-Pacific sponge assemblages. PhD thesis, Victoria University of Wellington, New ZealandGoogle Scholar
  44. 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. The Open Marine Biology Journal 4:31–38CrossRefGoogle Scholar
  45. 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:e85253PubMedCentralCrossRefPubMedGoogle Scholar
  46. Putchakarn S (2007) Species diversity of marine sponges dwelling in coral reefs in Had Khanom—Mo Ko Thale Tai National Park, Nakhon Si Thammarat Province, Thailand. J Mar Biol Assoc UK 87:1635–1642CrossRefGoogle Scholar
  47. Ralph PJ, Gademann R, Larkum AWD, Schreiber U (1999) In situ underwater measurements of photosynthetic activity of coral zooxanthellae and other reef-dwelling dinoflagellate endosymbionts. Mar Ecol Prog Ser 180:139–147CrossRefGoogle Scholar
  48. Ryan KG, Cowie ROM, Liggins E, McNaughtan D, Martin A, Davy SK (2009) The Short-term Effect of Irradiance on the Photosynthetic Properties of Antarctic Fast-Ice Microalgal Communties. J Phycol 45:1290–1298CrossRefGoogle Scholar
  49. Schils T (2012) Episodic eruptions of volcanic ash trigger a reversible cascade of nuisance species outbreaks in pristine coral habitats. PLOS ONE. 7:e46639PubMedCentralCrossRefPubMedGoogle Scholar
  50. Steindler L, Beer S, Pretzman-Shemer A, Nyberg C, Ilan M (2001) Photoadaptation of zooxanthellae in the sponge Cliona vastifica from the Red Sea, as measured in situ. Mar Biol 138:511–515CrossRefGoogle Scholar
  51. Thacker RW (2005) Impacts of Shading on Sponge-Cyanobacteria Symbioses: A Comparison between Host-Specific and Generalist Associations. Integr Comp Biol 45:369–376CrossRefPubMedGoogle Scholar
  52. Usher KM (2008) The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar Ecol 29:178–192CrossRefGoogle Scholar
  53. van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. PNAS 112:2307–2313PubMedCentralCrossRefPubMedGoogle Scholar
  54. 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 51:570–579CrossRefPubMedGoogle Scholar
  55. Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346CrossRefPubMedGoogle Scholar
  56. Wilkinson CR (1987a) Interocean differences in size and nutrition of coral reef sponge populations. Science 236:1654–1667CrossRefPubMedGoogle Scholar
  57. Wilkinson CR (1987b) Productivity and abundance of large sponge populations on Flinders Reef flats, Coral Sea. Coral Reefs 5:183–188CrossRefGoogle Scholar
  58. Wilkinson CR (1999) Global and local threats to coral reef functioning and existence: review and predictions. Mar Freshwater Res 50:867–878CrossRefGoogle Scholar
  59. Wulff JL (2006) Ecological interactions of marine sponges. Can J Zool 84:146–166CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • A. Biggerstaff
    • 1
  • D. J. Smith
    • 2
  • J. Jompa
    • 3
  • J. J. Bell
    • 1
  1. 1.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  2. 2.Coral Reef Research Unit, Department of Biological SciencesUniversity of EssexColchesterUK
  3. 3.Research and Development Centre on Marine, Coastal and Small IslandsHasanuddin UniversityMakassarIndonesia

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