Coral Reefs

, Volume 30, Issue 3, pp 841–853 | Cite as

Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia)

  • Y. Sawall
  • M. C. Teichberg
  • J. Seemann
  • M. Litaay
  • J. Jompa
  • C. Richter
Report

Abstract

Coral responses to degrading water quality are highly variable between species and depend on their trophic plasticity, acclimatization potential, and stress resistance. To assess the nutritional status and metabolism of the common scleractinian coral, Stylophora subseriata, in situ experiments were carried along a eutrophication gradient in Spermonde Archipelago, Indonesia. Coral fragments were incubated in light and dark chambers to measure photosynthesis, respiration, and calcification in a number of shallow reefs along the gradient. Chlorophyll a (chl a), protein content, maximum quantum yield (Fv/Fm), and effective quantum yield (Φ PS II) were measured on the zooxanthellae, in addition to host tissue protein content and biomass. Photosynthetic rates were 2.5-fold higher near-shore than mid-shelf due to higher areal zooxanthellae and chl a concentrations and a higher photochemical efficiency (Φ PS II). A 2- and 3-fold increase in areal host tissue protein and biomass was found, indicating a higher nutritional supply in coastal waters. Dark respiration, however, showed no corresponding changes. There was a weak correlation between calcification and photosynthesis (Pearson r = 0.386) and a lack of metabolic stress, as indicated by constant respiration and Fv/Fm and the “clean” and healthy appearance of the colonies in spite of high turbidity in near-shore waters. The latter suggests that part of the energetic gains through increased auto- and heterotrophy were spent on metabolic expenditures, e.g., mucus production. While coastal pollution is always deleterious to the reef ecosystem as a whole, our results show that the effect on corals may not always be negative. Thus, S. subseriata may be one of the few examples of corals actually profiting from land-based sources of pollution.

Keywords

Metabolism Acclimatization Photosynthesis Nutritional status Eutrophication Stylophora subseriata 

References

  1. Abdel-Salam H, Porter JW, Hatcher BG (1988) Physiological effects of sediment rejection on photosynthesis and respiration in three Caribbean reef corals. Proc 6th Int Coral Reef Symp 2:189–194Google Scholar
  2. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426CrossRefGoogle Scholar
  3. Allemand D, Tambutté E, Girard JP, Jaubert J (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin. J Exp Biol 201:2001–2009PubMedGoogle Scholar
  4. Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté E, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3:453–467CrossRefGoogle Scholar
  5. Anthony KRN (2006) Enhanced energy status of corals on coastal, high-turbidity reefs. Mar Ecol Prog Ser 319:111–116CrossRefGoogle Scholar
  6. Anthony KRN, Connolly SR (2004) Environmental limits to growth: physiological niche boundaries of corals along turbidity-light gradients. Oecologia 141:373–384CrossRefPubMedGoogle Scholar
  7. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253CrossRefPubMedGoogle Scholar
  8. Bell PRF (1992) Eutrophication and coral reefs - some examples in the Great Barrier Reef lagoon. Water Res 26:553–568CrossRefGoogle Scholar
  9. Bongiorni L, Shafir S, Angel D, Rinkevich B (2003) Survival, growth and gonad development of two hermatypic corals subjected to in situ fish-farm nutrient enrichment. Mar Ecol Prog Ser 253:137–144CrossRefGoogle Scholar
  10. Borell EM, Bischof K (2008) Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157:593–601CrossRefPubMedGoogle Scholar
  11. Borell EM, Yuliantri AR, Bischof K, Richter C (2008) The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. J Exp Mar Biol Ecol 364:116–123CrossRefGoogle Scholar
  12. Boto KG, Bunt JS (1978) Selective excitation fluorometry for the determination of chlorophylls and pheophytins. Anal Chem 50:392–395CrossRefGoogle Scholar
  13. Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309CrossRefGoogle Scholar
  14. Colombo-Pallotta M, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907CrossRefGoogle Scholar
  15. Cortes JN, Risk MJ (1985) A reef under siltation stress: Cahuita, Costa Rica. Bull Mar Sci 36:339–356Google Scholar
  16. Costa OS Jr, Nimmo M, Attrill MJ (2008) Coastal nutrification in Brazil: a review of the role of nutrient excess on coral reef demise. J South Am Earth Sci 25:257–270CrossRefGoogle Scholar
  17. Crossland CJ (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–42CrossRefGoogle Scholar
  18. Dennison WC, Orth RJ, Moore KA, Stevenson JC, Carter V, Kollar S, Bergstrom PW, Batiuk RA (1993) Assessing water quality with submersed aquatic vegetation. Bioscience 43:86–94CrossRefGoogle Scholar
  19. Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324Google Scholar
  20. Dubinsky Z, Stambler N, Ben-Zion M, McCloskey LR, Muscatine L, Falkowski PG (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc Lond B 239:231–246CrossRefGoogle Scholar
  21. Dustan P (1982) Depth-dependent photoadaption by zooxanthellae of the reef coral Montastrea annularis. Mar Biol 68:253–264CrossRefGoogle Scholar
  22. Edinger EN, Jompa J, Limmon GV, Widjatmoko W, Risk MJ (1998) Reef degradation and coral biodiversity in Indonesia: effects of land-based pollution, destructive fishing practices and changes over time. Mar Pollut Bull 36:617–630CrossRefGoogle Scholar
  23. Edinger EN, Kolasa J, Risk MJ (2000) Biogeographic variation in coral species diversity on coral reefs in three regions of Indonesia. Divers Distrib 6:113–127CrossRefGoogle Scholar
  24. Edmunds PJ, Davies PS (1989) An energy budget for Porites porites (Scleractinia), growing in a stressed environment. Coral Reefs 8:37–43CrossRefGoogle Scholar
  25. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146CrossRefPubMedGoogle Scholar
  26. Fabricius K, De’ath G, McCook L, Turak E, Williams DM (2005) Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Mar Pollut Bull 51:384–398CrossRefPubMedGoogle Scholar
  27. Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174CrossRefGoogle Scholar
  28. Ferrier-Pagès C, Allemand D, Gattuso JP, Jaubert J, Rassoulzadegan F (1998) Microheterotrophy in the zooxanthellate coral Stylophora pistillata: effects of light and ciliate density. Limnol Oceanogr 43:1639–1648CrossRefGoogle Scholar
  29. Ferrier-Pagès C, Gattuso JP, Dallot S, Jaubert J (2000) Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19:103–113CrossRefGoogle Scholar
  30. Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240CrossRefGoogle Scholar
  31. Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457PubMedGoogle Scholar
  32. Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S (2005) The symbiotic anthozoan: a physiological chimera between alga and animal. Integr Comp Biol 45:595–604CrossRefPubMedGoogle Scholar
  33. Furnas M, Mitchell A, Skuza M, Brodie J (2005) In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar Pollut Bull 51:253–265CrossRefPubMedGoogle Scholar
  34. Gattuso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool 39:160–183CrossRefGoogle Scholar
  35. Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. 2. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250CrossRefGoogle Scholar
  36. Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie Weinheim, New YorkGoogle Scholar
  37. Hoogenboom MO, Connolly SR, Anthony KRN (2009) Effects of photoacclimation on the light niche of corals: a process-based approach. Mar Biol 156:2493–2503CrossRefGoogle Scholar
  38. Houlbrèque F, Ferrier-Pagès C (2008) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17CrossRefPubMedGoogle Scholar
  39. Houlbrèque F, Tambutté E, Ferrier-Pagès C (2003) Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166CrossRefGoogle Scholar
  40. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637CrossRefPubMedGoogle Scholar
  41. Jameson SC, Kelty RA (2004) A review of indicators of land-based pollution stress on coral reefs. Joint EPA/NOAA/USGA/DOI Workshop on Assessing Pollution Stress on Coral Reefs, Honolulu HawaiiGoogle Scholar
  42. Jompa J, McCook LJ (2002) The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol Oceanogr 47:527–534CrossRefGoogle Scholar
  43. Lampert-Karako S, Stambler N, Katcoff DJ, Achituv Y, Dubinsky Z, Simon-Blecher N (2008) Effects of depth and eutrophication on the zooxanthella clades of Stylophora pistillata from the Gulf of Eilat (Red Sea). Aquatic Conserv: Mar Freshw Ecosyst 18:1039–1045CrossRefGoogle Scholar
  44. Loya Y, Kramarsky-Winter E (2003) In situ eutrophication caused by fish farms in the northern Gulf of Eilat (Aqaba) is beneficial for its coral reefs: a critique. Mar Ecol Prog Ser 261:299–303CrossRefGoogle Scholar
  45. Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328CrossRefGoogle Scholar
  46. Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J, Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar Ecol Prog Ser 334:93–102CrossRefGoogle Scholar
  47. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659–668PubMedGoogle Scholar
  48. McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367CrossRefGoogle Scholar
  49. Moll H (1983) Zonation and diversity of scleractinia on reefs off S. W. Sulawesi, Indonesia. Ph.D thesis, Leiden University, p107Google Scholar
  50. Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523CrossRefPubMedGoogle Scholar
  51. Muscatine L, Porter JW (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  52. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611CrossRefGoogle Scholar
  53. Naumann MS, Niggl W, Laforsch C, Glaser C, Wild C (2009) Coral surface area quantification-evaluation of established techniques by comparison with computer tomography. Coral Reefs 28:109–117CrossRefGoogle Scholar
  54. Naumann M, Haas A, Struck U, Mayr C, el-Zibdah M, Wild C (2010) Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29:649–659CrossRefGoogle Scholar
  55. Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417CrossRefPubMedGoogle Scholar
  56. Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. J Exp Mar Biol Ecol 287:57–78CrossRefGoogle Scholar
  57. Piniak GA, Lipschultz F (2004) Effects of nutritional history on nitrogen assimilation in congeneric temperate and tropical scleractinian corals. Mar Biol 145:1085–1096CrossRefGoogle Scholar
  58. Piniak GA, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136CrossRefGoogle Scholar
  59. Porter JW, Muscatine L, Dubinsky Z, Falkowski PG (1984) Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proc R Soc Lond B 222:161–180CrossRefGoogle Scholar
  60. Ralph PJ, Larkum AWD, Kühl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28CrossRefGoogle Scholar
  61. Renema W, Hoeksema B (2007) Delineation of the Indo-Malayan Centre of Maximum Marine Biodiversity: The Coral Triangle. In: Landman NH, Jones DS (eds) Biogeography, time, and place: Distributions, Barriers, and Islands, vol 29. Springer, Netherlands, pp 117–178Google Scholar
  62. Renema W, Troelstra SR (2001) Larger foraminifera distribution on a mesotrophic carbonate shelf in SW Sulawesi (Indonesia). Palaeogeogr Palaeoclimatol Palaeoecol 175:125–146CrossRefGoogle Scholar
  63. Riegl B, Branch GM (1995) Effects of sediment on the energy budgets of four scleractinian (Bourne 1900) and five alcyonacean (Lamouroux 1816) corals. J Exp Mar Biol Ecol 186:259–275CrossRefGoogle Scholar
  64. Rinkevich B, Angel D, Shafir S, Bongiorni L (2003) ‘Fair is foul and foul is fair’: response to a critique. Mar Ecol Prog Ser 261:305–309Google Scholar
  65. Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202CrossRefGoogle Scholar
  66. Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293CrossRefGoogle Scholar
  67. Simkiss K (1964) Phosphates as crystal poison of calcification. Biol Rev 39:487–504CrossRefPubMedGoogle Scholar
  68. Stafford-Smith MG (1993) Sediment-rejection efficiency of 22 species of Australian scleractinian corals. Mar Biol 115:229–243CrossRefGoogle Scholar
  69. Szmant A (2002) Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries 25:743–766CrossRefGoogle Scholar
  70. Tanaka Y, Ogawa H, Miyajima T (2010) Effects of nutrient enrichment on the release of dissolved organic carbon and nitrogen by the scleractinian coral Montipora digitata. Coral Reefs 29:675–682CrossRefGoogle Scholar
  71. Telesnicki GJ, Goldberg WM (1995) Effects of turbidity on the photosynthesis and respiration of two South Florida reef coral species. Bull Mar Sci 57:527–539Google Scholar
  72. Titlyanov EA, Titlyanova TV, Yamazato K, van Woesik R (2001) Photo-acclimation of the hermatypic coral Stylophora pistillata while subjected to either starvation or food provisioning. J Exp Mar Biol Ecol 257:163–181CrossRefPubMedGoogle Scholar
  73. Tomascik T, Sander F (1985) Effects of eutrophication on reef-building corals I. Growth rate of the reef-building coral Montastrea annularis. Mar Biol 87:143–155CrossRefGoogle Scholar
  74. van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487CrossRefGoogle Scholar
  75. Wesseling IJ, Uychiaoco AM, Aliño PE, Vermaat J (2001) Partial mortality in Porites corals: Variation among Philippine reefs. Int Rev Hydrobiol 86:77–85CrossRefGoogle Scholar
  76. Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre. Townsville, Australia p26Google Scholar
  77. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694CrossRefPubMedGoogle Scholar
  78. Zonneveld C (1997) Modeling effects of photoadaption on the Photosynthesis-Irradiance curve. J Theor Biol 186:381–388CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Y. Sawall
    • 1
    • 5
  • M. C. Teichberg
    • 1
  • J. Seemann
    • 1
    • 2
  • M. Litaay
    • 3
  • J. Jompa
    • 3
  • C. Richter
    • 4
  1. 1.Leibniz Center for Tropical Marine EcologyBremenGermany
  2. 2.Museum für Naturkunde Berlin– Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University BerlinBerlinGermany
  3. 3.Center for Coral Reef ResearchHasanuddin UniversityMakassarIndonesia
  4. 4.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany
  5. 5.Leibniz Institute for Marine ScienceKielGermany

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