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Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis

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Abstract

This study assesses the combined effect of feeding and short-term thermal stress on various physiological parameters and on the fatty acid, sterol, and alcohol composition of the scleractinian coral Turbinaria reniformis. The compound-specific carbon isotope composition of the lipids was also measured. Under control conditions (26°C), feeding with Artemia salina significantly increased the symbiont density and chlorophyll content and the growth rates of the corals. It also doubled the concentrations of almost all fatty acid (FA) compounds and increased the n-alcohol and sterol contents. δ13C results showed that the feeding enhancement of FA concentrations occurred either via a direct pathway, for one of the major polyunsaturated fatty acid (PUFA) compounds of the food (18:3n-3 FA), or via an enhancement of photosynthate transfer (indirect pathway), for the other coral FAs. Cholesterol (C27Δ5) was also directly acquired from the food. Thermal stress (31°C) affected corals, but differently according to their feeding status. Chlorophyll, protein content, and maximal photosynthetic efficiency of photosystem II (PSII) decreased to a greater extent in starved corals. In such corals, FA concentrations were reduced by 33%, (especially C16, C18 FAs, and n-3 PUFA) and the sterol content by 27% (especially the C28∆5,22 and C28∆5). The enrichment in the δ13C signature of the storage and structural FAs suggests that they were the main compounds respired during the stress to maintain the coral metabolism. Thermal stress had less effect on the lipid concentrations of fed corals, as only FA levels were reduced by 13%, with no major changes in their isotope carbon signatures. In conclusion, feeding plays an essential role in sustaining T. reniformis metabolism during the thermal stress.

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References

  • Ackman RG, Eaton CA (1966) Lipids of the fin whale (Balaenoptera physalus) from North Atlantic waters. III. Occurrence of eicosenoic and docosenoic fatty acids in the zooplankter Meganyctiphanes norvegica (M. sars) and their effect on whale oil composition. Can J Biochem 44:1561–1566

    Article  CAS  Google Scholar 

  • Alamaru A, Loya Y, Brokovich E, Yam R, Shemesh A (2009) Carbon and nitrogen utilization in two species of Red corals along a depth gradient: insights from stable isotope analysis of total organic material and lipids. Geochim Cosmochim Acta 73:5333–5342

    Article  CAS  Google Scholar 

  • Al-Moghrabi S, Allemand D, Couret JM, Jaubert J (1995) Fatty acids of the scleractinian coral Galaxea fascicularis: effect of light and feeding. J Comp Physiol 165:183–192

    Article  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetic approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550

    Article  Google Scholar 

  • Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554

    Article  Google Scholar 

  • Benson AA, Patton JS, Abraham S (1978) Energy exchange in coral reef ecosystems. Atoll Res Bull 220:33–54

    Article  Google Scholar 

  • Bernard HM (1896) The genus Turbinaria. The genus Astreopora: British Mus. (Nat. History) Cat. Madreporarian Corals 2:106 pp, 33 pls

  • Borell EM, Bishof K (2008) Feeding sustains photosynthetic quantum yield in 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 

  • Boutry JL, Saliot A, Barbier M (1979) The diversity of marine sterols and the role of algal bio-masses: from facts to hypothesis. Cell Mol Life Sci 35(12):1541–1543

    Article  CAS  Google Scholar 

  • Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the Staghorn Coral Acropora acuminata. Mar Biol 60:81–90

    Article  CAS  Google Scholar 

  • Díaz-Almeyda E, Thomé P, El Hafidi M, Iglesias-Prieto R (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30:217–225

    Article  Google Scholar 

  • Ferrier-Pagès C, Rottier C, Beraud E, Levy O (2010) Experimental assessment of the feeding effort of three scleractinian species during a thermal stress: effect on the rates of photosynthesis. J Exp Mar Biol Ecol 390:118–124

    Article  Google Scholar 

  • Grottoli AG, Wellington GM (1999) Effect of light and zooplankton on skeletal δ13C values in the eastern Pacific corals Pavona clavus and Pavona gigantea. Coral Reefs 18:29–41

    Article  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631

    Article  CAS  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  CAS  PubMed  Google Scholar 

  • Hill R, Larkum AWD, Frankart C, Kühl M, Ralph PJ (2004) Loss of functional photosystem II Reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics. Photosynth Res 82:59–72

    Article  CAS  PubMed  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Hoegh-Guldberg O (2004) Coral reefs in a century of rapid environmental change. Symbiosis 37:1–31

    Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2009) 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 

  • Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol Prog Ser 420:91–101

    Article  CAS  Google Scholar 

  • Intriago P, Jones DA (1993) Bacteria as food for Artemia. Aquaculture 113:115–127

    Article  Google Scholar 

  • Jeffrey SW, Humphrey JF (1975) New spectrophotometric equations for determining chlorophyll a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    Article  CAS  Google Scholar 

  • Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. UNESCO, Monographs on Oceanographic Methodology, Paris, pp 529–541

    Google Scholar 

  • Jones RJ, Hoegh-Guldberg O (1999) Effects of cyanide on coral photosynthesis: implications for identifying the cause of coral bleaching and for assessing the environmental effects of cyanide fishing. Mar Ecol Prog Ser 177:83–91

    Article  CAS  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283

    Article  CAS  Google Scholar 

  • Linnæus C (1758) Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata.—pp [1-4], 1-824. Holmiæ. (Salvius)

  • Marsh JAJ (1970) Primary productivity of reef building calcareous red algae. Ecology 51:255–263

    Article  Google Scholar 

  • Meikle P, Richards GN, Yellowlees D (1988) Structural investigations on the mucus from six species of coral. Mar Biol 99:187–193

    Article  CAS  Google Scholar 

  • Muscatine L (1967) Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host. Science 156:516–518

    Article  CAS  PubMed  Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition I. 13C of zooxanthellae and animal tissue vs depth. Mar Biol 100:185–193

    Article  Google Scholar 

  • Nichols PD, Phillips K, Mooney B, Wilson G, Phleger CF (2007) Signature of lipids and fatty acid profiling in food web studies. In: Furlani DM, Lyle J (eds) Cutting-edge technologies in fish and fisheries science Australian Society for Fish Biology workshop proceedings, Hobart, 28–31 August 2006

  • Oku H, Yamashiro H, Onaga K, Iwasaki H, Takara K (2002) Lipid distribution in branching coral Montipora digitata. Fish Sci 68:517–522

    Article  CAS  Google Scholar 

  • Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Physiol 135:533–537

    Article  CAS  Google Scholar 

  • Papina M, Meziane T, van Woesik R (2007) Acclimatation effect on fatty acids of the coral Montipora digitata and its symbiotic algae. Comp Biochem Physiol Part B 147:583–589

    Article  CAS  Google Scholar 

  • Patton JS, Burris JE (1983) Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar Biol 75:131–136

    Article  CAS  Google Scholar 

  • Pernet V, Gavino V, Gavino G, Anctil M (2002) Variations of lipid and fatty acid contents during the reproductive cycle of the anthozoan Renilla koellikeri. J Comp Physiol B 172:455–465

    Article  CAS  PubMed  Google Scholar 

  • Reynaud-Vaganay S, Juillet-Leclerc A, Jaubert J, Gattuso J-P (2001) Effect of light on skeletal δ13C and δ18O, and interaction with photosynthesis, respiration and calcification in two zooxanthellate scleractinian corals. Palaeogeogr Palaeoclimateol Palaeoecol 175:393–404

    Article  Google Scholar 

  • Ritar AJ, Dunstan GA, Nelson MM, Brown MR, Nichols PD, Thomas CW, Smith EG, Crear BJ, Kolkovski S (2004) Nutritional and bacterial profiles of juvenile Artemia fed different enrichments and during starvation. Aquaculture 239:351–373

    Article  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882

    Article  Google Scholar 

  • Rodrigues LJ, Grottoli AG, Pease TK (2008a) Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. J Exp Mar Biol Ecol 358:136–143

    Article  CAS  Google Scholar 

  • Rodrigues LJ, Grottoli AG, Lesser MP (2008b) Long-term changes in the chlorophyll fluorescence of bleached and recovering corals from Hawaii. J Exp Biol 211:2502–2509

    Article  PubMed  Google Scholar 

  • Sherwood-Lollar B, Hirschom SK, Chartrand MMG, Lacrampe-Couloume G (2007) An approach for assessing total instrumental uncertainty in compound-specific carbon isotope analysis: implications for environmental remediation studies. Anal Chem 79:3469–3475

    Article  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Sotka EE, Thacker RW (2005) Do some corals like it hot? Trends Ecol Evol 20:59–62

    Article  PubMed  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Naryan Yadav S, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tolosa I, de Mora S (2004) Isolation of neutral and acidic lipid biomarker classes for compound-specific-carbon isotope analysis by means of solvent extraction and normal-phase high-performance liquid chromatography. J Chromatogr 1045:71–84

    Article  CAS  Google Scholar 

  • Tolosa I, Lopez JF, Bentaleb I, Fontugne M, Grimalt JO (1999) Carbon isotope ratio monitoring-gas chromatography mass spectrometric measurements in the marine environment: biomarker sources and paleoclimate applications. Sci Total Environ 237(238):437–481

    Google Scholar 

  • Tolosa I, LeBlond N, Copin-Montégut C, Marty J-C, de Mora S, Prieur L (2003) Distribution of sterol and fatty alcohol biomarkers in particulate matter from the frontal structure of the Alborean Sea (S. W. Mediterranean Sea). Mar Chem 82:161–183

    Article  CAS  Google Scholar 

  • Treignier C, Grover R, Ferrier-Pagès C, Tolosa I (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr 53:2702–2710

    Article  CAS  Google Scholar 

  • Treignier C, Tolosa I, Grover R, Ferrier-Pagès C (2009) Carbon isotope composition of fatty acids and sterols in the scleractinian coral Turbinaria reniformis: Effect of light and feeding. Limnol Oceanogr 54:1933–1940

    Article  CAS  Google Scholar 

  • UNESCO (1981) Tenth report of the joint panel on oceanographic tables and standards. Unesco technical papers in marine science: 1–25

  • Veron J (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

  • Volkman JK (1986) A review of sterol markers for marine and terrigenous organic matter. Org Geochem 9:83–99

    Article  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellington GM (1982) An experimental analysis of the effects of light and zooplankton on coral zonation. Oecologia 52:311–320

    Article  PubMed  Google Scholar 

  • Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem Physio Part B 122:397–407

    Article  Google Scholar 

  • Yamashiro H, Oku H, Onaga K (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish Sci 71:448–453

    Article  CAS  Google Scholar 

  • Zhukova NV, Titlyanov EA (2003) Fatty acid variations in symbiotic dinoflagellates from Okinawan corals. Phytochemistry 62:191–195

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The IAEA is grateful for the support provided to its Marine Environment Laboratories by the Government of the Principality of Monaco.

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Authors and Affiliations

  1. Marine Environment Laboratories, International Atomic Energy Agency, 4 Quai Antoine 1er, 98000, Monaco, Principality of Monaco

    I. Tolosa

  2. Centre Scientifique de Monaco, Avenue Saint Martin, 98000, Monaco, Principality of Monaco

    C. Treignier, R. Grover & C. Ferrier-Pagès

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  1. I. Tolosa
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  2. C. Treignier
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  3. R. Grover
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  4. C. Ferrier-Pagès
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Correspondence to C. Ferrier-Pagès.

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Communicated by Biology Editor Dr. Mark Warner

R. Grover and C. Ferrier-Pagès have equally contributed to the paper.

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Tolosa, I., Treignier, C., Grover, R. et al. Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis . Coral Reefs 30, 763–774 (2011). https://doi.org/10.1007/s00338-011-0753-3

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