Skip to main content

Advertisement

SpringerLink
Log in

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

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

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 (F v/F m), 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 F v/F m 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • 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 2:189–194

    Google Scholar 

  • 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 142:419–426

    Article  CAS  Google Scholar 

  • 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 201:2001–2009

    CAS  PubMed  Google Scholar 

  • 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 3:453–467

    Article  Google Scholar 

  • Anthony KRN (2006) Enhanced energy status of corals on coastal, high-turbidity reefs. Mar Ecol Prog Ser 319:111–116

    Article  Google Scholar 

  • Anthony KRN, Connolly SR (2004) Environmental limits to growth: physiological niche boundaries of corals along turbidity-light gradients. Oecologia 141:373–384

    Article  PubMed  Google Scholar 

  • Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253

    Article  CAS  PubMed  Google Scholar 

  • Bell PRF (1992) Eutrophication and coral reefs - some examples in the Great Barrier Reef lagoon. Water Res 26:553–568

    Article  CAS  Google Scholar 

  • 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 253:137–144

    Article  Google Scholar 

  • Borell EM, Bischof K (2008) Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157:593–601

    Article  PubMed  Google Scholar 

  • 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 364:116–123

    Article  Google Scholar 

  • Boto KG, Bunt JS (1978) Selective excitation fluorometry for the determination of chlorophylls and pheophytins. Anal Chem 50:392–395

    Article  CAS  Google Scholar 

  • Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309

    Article  CAS  Google Scholar 

  • 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 29:899–907

    Article  Google Scholar 

  • Cortes JN, Risk MJ (1985) A reef under siltation stress: Cahuita, Costa Rica. Bull Mar Sci 36:339–356

    Google Scholar 

  • 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 25:257–270

    Article  Google Scholar 

  • 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 6:35–42

    Article  CAS  Google Scholar 

  • 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 43:86–94

    Article  Google Scholar 

  • Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

    Google Scholar 

  • 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 239:231–246

    Article  Google Scholar 

  • Dustan P (1982) Depth-dependent photoadaption by zooxanthellae of the reef coral Montastrea annularis. Mar Biol 68:253–264

    Article  CAS  Google Scholar 

  • 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 36:617–630

    Article  CAS  Google Scholar 

  • Edinger EN, Kolasa J, Risk MJ (2000) Biogeographic variation in coral species diversity on coral reefs in three regions of Indonesia. Divers Distrib 6:113–127

    Article  Google Scholar 

  • Edmunds PJ, Davies PS (1989) An energy budget for Porites porites (Scleractinia), growing in a stressed environment. Coral Reefs 8:37–43

    Article  Google Scholar 

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  PubMed  Google Scholar 

  • 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 51:384–398

    Article  CAS  PubMed  Google Scholar 

  • Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat. Nature 289:172–174

    Article  Google Scholar 

  • 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 43:1639–1648

    Article  Google Scholar 

  • 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 19:103–113

    Article  Google Scholar 

  • 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 22:229–240

    Article  Google Scholar 

  • Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457

    CAS  PubMed  Google Scholar 

  • 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 45:595–604

    Article  CAS  PubMed  Google Scholar 

  • 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 51:253–265

    Article  CAS  PubMed  Google Scholar 

  • 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 39:160–183

    Article  CAS  Google Scholar 

  • 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 117:239–250

    Article  CAS  Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie Weinheim, New York

    Google Scholar 

  • Hoogenboom MO, Connolly SR, Anthony KRN (2009) Effects of photoacclimation on the light niche of corals: a process-based approach. Mar Biol 156:2493–2503

    Article  Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2008) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

  • 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 296:145–166

    Article  Google Scholar 

  • 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 293:629–637

    Article  CAS  PubMed  Google Scholar 

  • 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 Hawaii

    Google Scholar 

  • 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 47:527–534

    Article  CAS  Google Scholar 

  • 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 18:1039–1045

    Article  Google Scholar 

  • 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 261:299–303

    Article  Google Scholar 

  • Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328

    Article  CAS  Google Scholar 

  • 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 334:93–102

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Google Scholar 

  • McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367

    Article  Google Scholar 

  • Moll H (1983) Zonation and diversity of scleractinia on reefs off S. W. Sulawesi, Indonesia. Ph.D thesis, Leiden University, p107

  • Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523

    Article  CAS  PubMed  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Article  Google Scholar 

  • Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    Article  CAS  Google Scholar 

  • 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 28:109–117

    Article  Google Scholar 

  • 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 29:649–659

    Article  Google Scholar 

  • Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413–417

    Article  PubMed  Google Scholar 

  • Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. J Exp Mar Biol Ecol 287:57–78

    Article  Google Scholar 

  • Piniak GA, Lipschultz F (2004) Effects of nutritional history on nitrogen assimilation in congeneric temperate and tropical scleractinian corals. Mar Biol 145:1085–1096

    Article  CAS  Google Scholar 

  • Piniak GA, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136

    Article  Google Scholar 

  • 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 222:161–180

    Article  Google Scholar 

  • Ralph PJ, Larkum AWD, Kühl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28

    Article  Google Scholar 

  • 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 117–178

    Google Scholar 

  • Renema W, Troelstra SR (2001) Larger foraminifera distribution on a mesotrophic carbonate shelf in SW Sulawesi (Indonesia). Palaeogeogr Palaeoclimatol Palaeoecol 175:125–146

    Article  Google Scholar 

  • 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 186:259–275

    Article  Google Scholar 

  • Rinkevich B, Angel D, Shafir S, Bongiorni L (2003) ‘Fair is foul and foul is fair’: response to a critique. Mar Ecol Prog Ser 261:305–309

    Google Scholar 

  • Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202

    Article  Google Scholar 

  • Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293

    Article  CAS  Google Scholar 

  • Simkiss K (1964) Phosphates as crystal poison of calcification. Biol Rev 39:487–504

    Article  CAS  PubMed  Google Scholar 

  • Stafford-Smith MG (1993) Sediment-rejection efficiency of 22 species of Australian scleractinian corals. Mar Biol 115:229–243

    Article  Google Scholar 

  • Szmant A (2002) Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries 25:743–766

    Article  CAS  Google Scholar 

  • 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 29:675–682

    Article  Google Scholar 

  • Telesnicki GJ, Goldberg WM (1995) Effects of turbidity on the photosynthesis and respiration of two South Florida reef coral species. Bull Mar Sci 57:527–539

    Google Scholar 

  • 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 257:163–181

    Article  PubMed  Google Scholar 

  • Tomascik T, Sander F (1985) Effects of eutrophication on reef-building corals I. Growth rate of the reef-building coral Montastrea annularis. Mar Biol 87:143–155

    Article  Google Scholar 

  • 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 24:482–487

    Article  Google Scholar 

  • Wesseling IJ, Uychiaoco AM, Aliño PE, Vermaat J (2001) Partial mortality in Porites corals: Variation among Philippine reefs. Int Rev Hydrobiol 86:77–85

    Article  Google Scholar 

  • Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre. Townsville, Australia p26

    Google Scholar 

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  PubMed  Google Scholar 

  • Zonneveld C (1997) Modeling effects of photoadaption on the Photosynthesis-Irradiance curve. J Theor Biol 186:381–388

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the German Federal Ministry of Education and Research (BMBF) under a bilateral German-Indonesian project (SPICE). Further support was given by the Bremen International Graduate School for Marine Sciences (GLOMAR) funded by the German Research Foundation (DFG). We want to thank scientist, students, and technicians of the Center for Coral Reef Research at the Hasanuddin University for their great support in organization, field work, and space acquisition at the university as well as at the Marine Station on the island Barang Lompo. Thanks are due to Kai Bischof and Wiebke Krämer for their advice with regard to coral photosynthesis.

Author information

Author notes

  1. Y. Sawall & J. Seemann

    Present address: Museum für Naturkunde Berlin– Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Invalidenstr. 43, 10115, Berlin, Germany

Authors and Affiliations

  1. Leibniz Center for Tropical Marine Ecology, Fahrenheitstr. 6, 28359, Bremen, Germany

    Y. Sawall, M. C. Teichberg & J. Seemann

  2. Center for Coral Reef Research, Hasanuddin University, Jl. Perintis Kemerdekaan km 10, Makassar, 90245, Indonesia

    M. Litaay & J. Jompa

  3. Alfred Wegener Institute for Polar and Marine Research, Am Alten Hafen 26, 27568, Bremerhaven, Germany

    C. Richter

  4. Leibniz Institute for Marine Science, Düsternbrookerweg 20, 24105, Kiel, Germany

    Y. Sawall

Authors
  1. Y. Sawall
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. C. Teichberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Seemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Litaay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Jompa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Richter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. Sawall.

Additional information

Communicated by Biology Editor Dr. Mark Warner

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sawall, Y., Teichberg, M.C., Seemann, J. et al. Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia). Coral Reefs 30, 841–853 (2011). https://doi.org/10.1007/s00338-011-0764-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-011-0764-0

Keywords

Search

Navigation