Skip to main content
Log in

The Use of Lipids and Fatty Acids to Measure the Trophic Plasticity of the Coral Stylophora subseriata

  • Original Article
  • Published:
Lipids

Abstract

Following up on previous investigations on the stress resistance of corals, this study assessed the trophic plasticity of the coral Stylophora subseriata in the Spermonde Archipelago (Indonesia) along an eutrophication gradient. Trophic plasticity was assessed in terms of lipid content and fatty acid composition in the holobiont relative to its plankton (50–300 μm) food as well as the zooxanthellae density, lipid, FA and chlorophyll a content. A cross-transplantation experiment was carried out for 1.5 months in order to assess the trophic potential of corals. Corals, which live in the eutrophied nearshore area showed higher zooxanthellae and chlorophyll a values and higher amounts of the dinoflagellate biomarker FA 18:4n-3. Their lipid contents were maintained at similar to levels from specimens further away from the anthropogenic impact source going up to 14.9 ± 0.9 %. A similarity percentage analysis of the groups holobiont, zooxanthellae and plankton >55 μm found that differences between the FA composition of the holobiont and zooxanthellae symbionts were more distinct in the site closer to the shore, thus heterotrophic feeding became more important. Transplanted corals attained very similar zooxanthellae, chlorophyll a and lipid values at all sites as the specimens originating from those sites, which indicates a high potential for trophic plasticity in the case of a change in food sources, which makes this species competitive and resistant to eutrophication.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ARA:

Arachidonic acid

DHA:

Docosahexaenoic acid

DM:

Dry mass

EPA:

Eicosapentaenoic acid

FA:

Fatty acid(s)

PC:

Principal component

PCA:

Principal component analysis

PUFA:

Polyunsaturated fatty acid(s)

TFA:

Total fatty acid(s)

SFA:

Saturated fatty acid(s)

SIMPER:

Similarity percentage

References

  1. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  PubMed  CAS  Google Scholar 

  2. Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:54

    Article  Google Scholar 

  3. Sawall Y, Teichberg M, Seemann J, Litaay M, Jompa J, Richter C (2011) Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia). Coral Reefs 30:841–853

    Google Scholar 

  4. Coles SL, Brown BE (2003) Coral bleaching—capacity for acclimatization and adaptation. Academic Press, San Diego

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  6. Hennige S, Smith D, Walsh S, McGinley M, Warner M, Suggett D (2010) Acclimation and adaptation of scleractinian coral communities along environmental gradients within an Indonesian reef system. J Exp Mar Biol Ecol 391:143–152

    Article  Google Scholar 

  7. Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4:e6364

    Article  PubMed  Google Scholar 

  8. Bay LK, Ulstrup KE, Nielsen HB, Jarmer H, Goffard N, Willis BL, Miller DJ, Van Oppen MJH (2009) Microarray analysis reveals transcriptional plasticity in the reef building coral Acropora millepora. Mol Ecol 18:3062–3075

    Article  PubMed  CAS  Google Scholar 

  9. 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  PubMed  Google Scholar 

  10. 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 

  11. Figueiredo J, Baird A, Cohen M, Flot JF, Kamiki T, Meziane T, Tsuchiya M, Yamasaki H (2012) Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31:613–619

    Article  Google Scholar 

  12. Szmant AM, Gassmann NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224

    Article  Google Scholar 

  13. Grimsditch G, Salm R (2006) Coral reef resilience and resistance to bleaching. IUCN, Gland

    Google Scholar 

  14. Harland AD, Navarro JC, Spencer Davies P, Fixter LM (1993) Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol 117:113–117

    Article  CAS  Google Scholar 

  15. Dalsgaard J, John MS, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Patton JS, Abraham S, Benson AA (1977) Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host. Mar Biol 44:235–247

    Article  CAS  Google Scholar 

  18. 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 

  19. 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 

  20. Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. Ecosyst World 25:75–87

    Google Scholar 

  23. Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc Biol Sci Ser B 236:311–324

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  25. 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 

  26. Goreau TF, Goreau NI, Yonge CM (1971) Reef corals: autotrophs or heterotrophs? Biol Bull 141:247–260

    Article  Google Scholar 

  27. Porter JW (1976) Autotrophy, heterotrophy, and resource partitioning in Caribbean reef-building corals. Am Nat 110:731–742

    Article  Google Scholar 

  28. Gattuso J-P, Pichon M, Jaubert J (1991) Physiology and taxonomy of scleractinian corals: a case study in the genus Stylophora. Coral Reefs 9:173–182

    Article  Google Scholar 

  29. 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 

  30. Rinkevich B, Loya Y (1979) The reproduction of the Red Sea coral Stylophora pistillata. II. Synchronization in breeding and seasonality of planulae shedding. Mar Ecol Prog Ser 1:145–152

    Article  Google Scholar 

  31. Leuzinger S, Anthony KRN, Willis B (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531

    Article  PubMed  Google Scholar 

  32. Johannes RE, Wiebe WJ (1970) Method for determination of coral tissue biomass and composition. Limnol Oceanogr 15:822–824

    Article  Google Scholar 

  33. Aminot A, Rey F (2000) Standard procedure for the determination of chlorophyll a by spectroscopic methods. ICES, Denmark

    Google Scholar 

  34. Naumann M, 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 

  35. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–501

    Google Scholar 

  36. Hagen W (2000) Lipids. Academic Press, San Diego

    Google Scholar 

  37. Kattner G, Fricke HSG (1986) Simple gas-liquid chromatographic method for the simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. J Chromatogr A 361:263–268

    Article  CAS  Google Scholar 

  38. Laakmann S, Kochzius M, Auel H (2009) Ecological niches of Arctic deep-sea copepods: vertical partitioning, dietary preferences and different trophic levels minimize inter-specific competition. Deep Sea Res I 56:741–756

    Article  Google Scholar 

  39. Fay L, Richli U (1991) Location of double bonds in polyunsaturated fatty acids by gas chromatography-mass spectrometry after 4,4-dimethyloxazoline derivatization. J Chromatogr A 541:89–98

    Article  CAS  Google Scholar 

  40. Nilsson R, Liljenberg C (1991) The determination of double bond positions in polyunsaturated fatty acids–-Gas chromatography/mass spectrometry of the diethylamide derivative. Phytochem Anal 2:253–259

    Article  CAS  Google Scholar 

  41. Zhukova NV, Aizdaicher NA (1995) Fatty acid composition of 15 species of marine microalgae. Phytochemistry 39:351–356

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  43. Imbs A, Demidkova D, Latypov Y, Pham L (2007) Application of fatty acids for chemotaxonomy of reef-building corals. Lipids 42:1035–1046

    Article  PubMed  CAS  Google Scholar 

  44. 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 

  45. Hubbard DK (1986) Sedimentation as a control of reef development: St. Croix, U.S.V.I. Coral Reefs 5:117–125

    Article  Google Scholar 

  46. Wittenberg M, Hunte W (1992) Effects of eutrophication and sedimentation on juvenile corals I. Abundance, mortality and community structure. Mar Biol 112:131–138

    Article  Google Scholar 

  47. Veron JEN, Stafford-Smith M (2000) Corals of the world. Australian Institute of Marine Science, Townsville

    Google Scholar 

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

    Article  Google Scholar 

  49. Goreau TF, Goreau NI, Goreau TJ (1979) Corals and coral reefs. Sci Am 241:124–136

    Google Scholar 

  50. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    Article  PubMed  CAS  Google Scholar 

  51. 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 

  52. 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 

  53. Andrews JC, Gentien P (1982) Upwelling as a source of nutrients for the Great Barrier Reef ecosystems: a solution to Darwin’s question? Mar Ecol Prog Ser 8:257–269

    Article  Google Scholar 

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

    Article  Google Scholar 

  55. Winters G, Beer S, Zvi BB, Brickner I, Loya Y (2009) Spatial and temporal photoacclimation of Stylophora pistillata: zooxanthella size, pigmentation, location and clade. Mar Ecol Prog Ser 384:107–119

    Article  Google Scholar 

  56. Dubinsky Z, Stambler N, Ben-Zion M, McCloskey L, Muscatine L, Falkowski P (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc Biol Sci Ser B 239:231–246

    Article  Google Scholar 

  57. Mise T, Hidaka M (2003) Degradation of zooxanthellae in the coral Acropora nasuta during bleaching. Galaxea JCRS 5:33–39

    Article  Google Scholar 

  58. 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 

  59. Latyshev N, Naumenko N, Svetashev V, Latypov Y (1991) Fatty acids of reef-building corals. Mar Ecol Prog Ser Oldendorf 76:295–301

    Article  CAS  Google Scholar 

  60. Muscatine L, Pool R (1979) Regulation of numbers of intracellular algae. Proc R Soc Biol Sci Ser B 204:131–139

    Article  CAS  Google Scholar 

  61. Harland AD, Davies PS, Fixter LM (1992) Lipid content of some Caribbean corals in relation to depth and light. Mar Biol 113:357–361

    Article  CAS  Google Scholar 

  62. Ward S (1995) The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 187:193–206

    Article  CAS  Google Scholar 

  63. Van Oppen M, Gates R (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883

    Article  PubMed  Google Scholar 

  64. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543

    Article  PubMed  CAS  Google Scholar 

  65. Glynn PW (1973) Ecology of a Caribbean coral reef. The Porites reef-flat biotope: part II. Plankton community with evidence for depletion. Mar Biol 22:1–21

    Article  Google Scholar 

  66. Ayukai T (1995) Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia. Coral Reefs 14:141–147

    Article  Google Scholar 

  67. Fabricius KE, Genin A, Benayahu Y (1995) Flow-dependent herbivory and growth in zooxanthellae-free soft corals. Limnol Oceanogr 40:1290–1301

    Article  Google Scholar 

  68. Ribes M, Coma R, Gili JM (1998) Heterotrophic feeding by gorgonian corals with symbiotic zooxanthella. Limnol Oceanogr 43:1170–1179

    Google Scholar 

  69. Bak RPM, Joenje M, Jong ID, Lambrechts DYM, Nieuwland G (1998) Bacterial suspension feeding by coral reef benthic organisms. Mar Ecol Prog Ser 175:285–288

    Article  Google Scholar 

  70. Picciano M, Ferrier-Pages C (2007) Ingestion of pico- and nanoplankton by the Mediterranean red coral Corallium rubrum. Mar Biol 150:773–782

    Article  Google Scholar 

  71. Díaz-Almeyda E, Thomé PE, 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 

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 German Academic Exchange Service (DAAD). We want to thank the scientists, students, and technicians of the Center for Coral Reef Research (CCRR) 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. Special thanks to Petra Wencke, Anna Schukat, Britta Grote, and Martin Greave for help and advice within the lipid analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Seemann.

About this article

Cite this article

Seemann, J., Sawall, Y., Auel, H. et al. The Use of Lipids and Fatty Acids to Measure the Trophic Plasticity of the Coral Stylophora subseriata . Lipids 48, 275–286 (2013). https://doi.org/10.1007/s11745-012-3747-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-012-3747-1

Keywords

Navigation