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Coral Reefs

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Temporal and spatial variation in fatty acid composition in Acropora tenuis corals along water quality gradients on the Great Barrier Reef, Australia

  • Melissa M. RockerEmail author
  • David S. Francis
  • Katharina E. Fabricius
  • Bette L. Willis
  • Line K. Bay
Report

Abstract

Fatty acids (FA) play a vital role in coral physiology, metabolism and stress resistance. Optimal health requires a balance of fatty acids, and more specifically essential polyunsaturated fatty acids (PUFA), for efficient biochemical and physiological functioning. Therefore, it is necessary to fully assess and evaluate the viability of FA as biomarkers for monitoring the health of coral populations. This study explores seasonal and spatial variation in the abundance of 17 FA in the coral Acropora tenuis, along two water quality gradients on the central Great Barrier Reef. Ratios of key FA varied similarly along the two water quality gradients and were highest in corals from comparatively good water quality conditions. Strong differences in PUFA composition were found between wet and dry seasons, with high percentage n-3 PUFA defining the dry seasons (June 2013 and October 2013) and high percentage n-6 PUFA defining the wet seasons (February 2013 and 2014). Saturated FA and monounsaturated FA concentrations varied with season, positively correlated with Symbiodinium density, and had highest concentrations in corals exposed to relatively poor water quality. Overall, results demonstrate that essential FA and their derived ratios support FA as a potential indicator of coral holobiont health; however, strong seasonal variation may negate FA and their derived ratios as water quality indicators.

Keywords

PUFA Coral health indicator Scleractinia Nutrients Turbidity 

Notes

Acknowledgements

We thank Dr. Britta Schaffelke and the Australian Institute of Marine Science (AIMS) Inshore Marine Monitoring Team (MMP) for logistical and field support, Sam Noonan for field support, and Dr. Jennifer Atherton for comments to improve the manuscript. AIMS Laboratory facilities were used for this study. The Great Barrier Reef Marine Park Authority provided Research Permit No. G35406.1. AIMS, the National Environmental Research Program, the PADI Grant Foundation and the ARC Centre of Excellence for Coral Reef Studies provided funding.

Compliance with ethical standards

Conflict of interest

All authors have declare that they have no conflicts of interest.

Supplementary material

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References

  1. Ackman RG (2002) The gas chromatograph in practical analyses of common and uncommon fatty acids for the 21st century. Anal Chim Acta 465:175–192Google Scholar
  2. Al-Kandari NM, Jolliffe IT (2005) Variable selection and interpretation in correlation principal components. Environmetrics 16:659–672Google Scholar
  3. Al-Moghrabi S, Allemand D, Jaubert J (1993) Valine uptake by the scleractinian coral Galaxea fascicularis: characterization and effect of light and nutritional status. J Comp Physiol B 163:355–362Google Scholar
  4. 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 B 165:183–192Google Scholar
  5. Anderson KD, Heron SF, Pratchett MS (2015) Species-specific declines in the linear extension of branching corals at a subtropical reef, Lord Howe Island. Coral Reefs 34:479–490Google Scholar
  6. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Bio Ecol 252:221–253Google Scholar
  7. Anthony KRN, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, energetics, and coral mortality risk: Effects of temperature, light, and sediment regime. Limnol Oceanogr 52:716–726Google Scholar
  8. Armstrong SG, Wyllie SG, Leach DN (1994) Effects of season and location of catch on the fatty acid compositions of some Australian fish species. Food Chem 51:295–305Google Scholar
  9. Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554Google Scholar
  10. Baptista M, Repolho T, Maulvault AL, Lopes VM, Narciso L, Marques A, Bandarra N, Rosa R (2014) Temporal dynamics of amino and fatty acid composition in the razor clam Ensis siliqua (Mollusca: Bivalvia). Helgol Mar Res 68:465–482Google Scholar
  11. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Google Scholar
  12. Baumann J, Grottoli AG, Hughes AD, Matsui Y (2014) Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. J Exp Mar Bio Ecol 461:469–478Google Scholar
  13. Ben-David-Zaslow R, Benayahu Y (1999) Temporal variation in lipid, protein and carbohydrate content in the Red Sea soft coral Heteroxenia fuscenscens. J Mar Biol Assoc UK 79:1001–1006Google Scholar
  14. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188Google Scholar
  15. Bergé J-P, Barnathan G (2005) Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Adv Biochem Eng Biotechnol 96:49–125Google Scholar
  16. Brodie JE, Devlin MJ, Haynes D, Waterhouse J (2011) Assessment of the eutrophication status of the Great Barrier Reef lagoon (Australia). Biogeochemistry 106:281–302Google Scholar
  17. Browne NK, Tay JKL, Low J, Larson O, Todd PA (2015) Fluctuations in coral health of four common inshore reef corals in response to seasonal and anthropogenic changes in water quality. Mar Environ Res 105:39–52Google Scholar
  18. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS One 2Google Scholar
  19. Bureau DP, Kaushik SJ, Cho CY (2002) Bioenergetics. In: Halver JE, Hardy RW (eds) Fish Nutrition. Academic Press, San Diego, pp 1–59Google Scholar
  20. Clarke SD, Jump DB (1993) Regulation of gene transcription by polyunsaturated fatty acids. Prog Lipid Res 32:139–149Google Scholar
  21. Conlan JA, Humphrey CA, Severati A, Francis DS (2017) Influence of different feeding regimes on the survival, growth, and biochemical composition of Acropora coral recruits. PLoS One 12:e0188568Google Scholar
  22. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488Google Scholar
  23. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315Google Scholar
  24. Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262Google Scholar
  25. Dalsgaard J, St John M, Kattner G, Müller-Navarra DC, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340Google Scholar
  26. De’ath G, Fabricius KE (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850Google Scholar
  27. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci 109:17995–17999Google Scholar
  28. Dethier MN, Sosik E, Galloway AWE, Duggins DO, Simenstad CA (2013) Addressing assumptions: Variation in stable isotopes and fatty acids of marine macrophytes can confound conclusions of food web studies. Mar Ecol Prog Ser 478:1–14Google Scholar
  29. Dewick PM (1997) The acetate pathway: fatty acids and polyketides. Medicinal Natural Products. John Wiley & Sons Publishing, New YorkGoogle Scholar
  30. Dunn SR, Thomas MC, Nette GW, Dove SG (2012) A lipidomic approach to understanding free fatty acid lipogenesis derived from dissolved inorganic carbon within cnidarian-dinoflagellate symbiosis. PLoS One 7Google Scholar
  31. Edmunds PJ, Davies PS (1986) An energy budget for Porites porites (Scleractinia). Mar Biol 92:339–347Google Scholar
  32. Fabricius KE, Cséke S, Humphrey C, De’ath G (2013a) Does trophic status enhance or reduce the thermal tolerance of scleractinian corals? A review, experiment and conceptual framework. PLoS One 8:e54399Google Scholar
  33. Fabricius KE, De’ath G, Humphrey C, Zagorskis I, Schaffelke B (2013b) Intra-annual variation in turbidity in response to terrestrial runoff on near-shore coral reefs of the Great Barrier Reef. Estuar Coast Shelf Sci 116:57–65Google Scholar
  34. Fabricius KE, Logan M, Weeks SJ, Lewis SE, Brodie J (2016) Changes in water clarity in response to river discharges on the Great Barrier Reef continental shelf: 2002–2013. Estuar Coast Shelf Sci 173:A1–A15Google Scholar
  35. 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 22:229–240Google Scholar
  36. Figueiredo J, Baird AH, Cohen MF, 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 31:613–619Google Scholar
  37. Fitt WK, Spero HJ, Halas J, White MW, Porter JW (1993) Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “Bleaching event”. Coral Reefs 12:57–64Google Scholar
  38. Flores F, Hoogenboom MO, Smith LD, Cooper TF, Abrego D, Negri AP (2012) Chronic exposure of corals to fine sediments: Lethal and sub-lethal impacts. PLoS One 7:1–12Google Scholar
  39. Funk CD (2001) Prostaglandins and leukotrienes: Advances in eicosanoid biology. Science (80-) 294:1871–1875Google Scholar
  40. Glencross BD (2009) Exploring the nutritional demand for essential fatty acids by aquaculture species. Rev Aquac 1:71–124Google Scholar
  41. 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 145:621–631Google Scholar
  42. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189Google Scholar
  43. Guil-Guerrero JL (2007) Stearidonic acid (18:4n-3): metabolism, nutritional importance, medical uses and natural sources. Eur J Lipid Sci Technol 109:1226–1236Google Scholar
  44. Harland AD, Davies PS, Fixter LM (1992) Lipid content of some Carribbean corals in relation to depth and light. Mar Biol 113:357–361Google Scholar
  45. Harland AD, Fixter LM, Davies PS, Anderson RA (1991) Distribution of lipids between the zooxanthellae and animal compartment in the symbiotic sea anemone Anemonia viridis: wax esters, triglycerides and fatty acids. Mar Biol 110:13–19Google Scholar
  46. Harland AD, Navarro JC, Davies PS, Fixter LM (1993) Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol 117:113–117Google Scholar
  47. Hazel JR, Eugene Williams E (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227Google Scholar
  48. Hinrichs S, Patten NL, Feng M, Strickland D, Waite AM (2013) Which environmental factors predict seasonal variation in the coral health of Acropora digitifera and Acropora spicifera at Ningaloo Reef? PLoS One 8:Google Scholar
  49. Hopely D, Smithers SG, Parnell KE (2007) The geomorphology of the Great Barrier Reef: Development, diversity, and changeGoogle Scholar
  50. Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17Google Scholar
  51. Hughes AD, Grottoli AG (2013) Heterotrophic compensation: A possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS One 8:1–10Google Scholar
  52. Hulbert AJ (2003) Life, death and membrane bilayers. J Exp Biol 206:2303–2311Google Scholar
  53. Imbs AB, Dang LPT, Rybin VG, Svetashev VI (2015) Fatty acid, lipid class, and phospholipid molecular species composition of the soft coral Xenia sp. (Nha Trang Bay, the South China Sea, Vietnam). Lipids 50:575–589Google Scholar
  54. Imbs AB, Yakovleva IM, Dautova TN, Bui LH, Jones P (2014) Diversity of fatty acid composition of symbiotic dinoflagellates in corals: Evidence for the transfer of host PUFAs to the symbionts. Phytochemistry 101:76–82Google Scholar
  55. Imbs AB, Yakovleva IM, Latyshev NA, Pham LQ (2010) Biosynthesis of polyunsaturated fatty acids in zooxanthellae and polyps of corals. Russ J Mar Biol 36:452–457Google Scholar
  56. Johns RB, Nichols PD, Perry GJ (1979) Fatty acid composition of ten marine algae from australian waters. Phytochemistry 18:799–802Google Scholar
  57. Joseph JD (1979) Lipid composition of marine and estuarine invertebrates: Porifera and Cnidaria. Prog Lipid Res 18:1–30Google Scholar
  58. Kabeya N, Fonseca MM, Ferrier DEK, Navarro JC, Bay LK, Francis DS, Tocher DR, Castro LFC, Monroig Ó (2018) Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Sci Adv 4:eaar6849Google Scholar
  59. Kellogg RB, Patton JS (1983) Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp. Mar Biol 75:137–149Google Scholar
  60. Kenkel CD, Almanza AT, Matz MV (2015) Fine-scale environmental specialization of reef-building corals might be limiting reef recovery in the Florida Keys. Ecology 96:3197–3212Google Scholar
  61. Kneeland J, Hughen K, Cervino J, Hauff B, Eglinton T (2013) Lipid biomarkers in Symbiodinium dinoflagellates: New indicators of thermal stress. Coral Reefs 32:923–934Google Scholar
  62. Latyshev NA, Naumenko NV, Svetashev VI, Latypov YY (1991) Fatty acids of reef-building corals. Mar Ecol Prog Ser 76:295–301Google Scholar
  63. Levas S, Grottoli AG, Schoepf V, Aschaffenburg M, Baumann J, Bauer JE, Warner ME (2016) Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs 35:495–506Google Scholar
  64. Levas S, Schoepf V, Warner ME, Ascha M, Baumann J, Grottoli AG (2018) Long-term recovery of Caribbean corals from bleaching. J Exp Mar Bio Ecol 506:124–134Google Scholar
  65. Meyers PA (1979) Polyunsaturated fatty acids in coral: indicators of nutritional sources. Mar Biol Lett 1:69–75Google Scholar
  66. Meyers PA, Porter JW, Chad RL (1978) Depth analysis of fatty acids in two Caribbean reef corals. Mar Biol 49:197–202Google Scholar
  67. Mika A, Gołeebiowski M, Skorkowski E, Stepnowski P (2014) Lipids of adult brown shrimp, Crangon crangon: Seasonal variations in fatty acids class composition. J Mar Biol Assoc United Kingdom 94:993–1000Google Scholar
  68. Mock T, Kroon BMA (2002) Photosynthetic energy conversion under extreme conditions - II: the significance of lipids under light limited growth in Antarctic sea ice diatoms. Phytochemistry 61:53–60Google Scholar
  69. Monroig Ó, Tocher DR, Navarro JC (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: Recent advances in molecular mechanisms. Mar Drugs 11:3998–4018Google Scholar
  70. Muscatine L, Porter JW (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460Google Scholar
  71. Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945Google Scholar
  72. Nettleton JA (1995) Introduction to fatty acids. Omega-3 Fatty Acids and Health. Chapman & Hall, pp 1–63Google Scholar
  73. Nomura M, Kamogawa H, Susanto E, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K (2013) Seasonal variations of total lipids, fatty acid composition, and fucoxanthin contents of Sargassum horneri (Turner) and Cystoseira hakodatensis (Yendo) from the northern seashore of Japan. J Appl Phycol 25:1159–1169Google Scholar
  74. Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology packageGoogle Scholar
  75. Oku H, Yamashiro H, Onaga K, Sakai K, Iwasaki H (2003) Seasonal changes in the content and composition of lipids in the coral Goniastrea aspera. Coral Reefs 22:83–85Google Scholar
  76. Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Monitpora digitata with polyunsaturated fatty acids. Comp Biochem Physiol Part B Comp Biochem 135:533–537Google Scholar
  77. Patton JS, Burris JE (1983) Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar Biol 75:131–136Google Scholar
  78. Porter JW, Fitt WK, Spero HJ, Rogers CS, White MW (1989) Bleaching in reef corals: physiological and stable isotopic responses. Proc Natl Acad Sci 86:9342–9346Google Scholar
  79. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  80. Revel J, Massi L, Mehiri M, Boutoute M, Mayzaud P, Capron L, Sabourault C (2016) Differential distribution of lipids in epidermis, gastrodermis and hosted Symbiodinium in the sea anemone Anemonia viridis. Comp Biochem Physiol -Part A Mol Integr Physiol 191:140–151Google Scholar
  81. Richier S, Sabourault C, Ferrier-Pagès C, Merle P-L, Furla P, Allemand D (2010) Cnidarian-dinoflagellate symbiosis-mediated adapation to environmental perturbations. In: Seckbach J, Grube M (eds) Symbiosis and Stress. Springer, New York, p 651Google Scholar
  82. Rocker MM, Francis DS, Fabricius KE, Willis BL, Bay LK (2017) Variation in the health and biochemical condition of the coral Acropora tenuis along two water quality gradients on the Great Barrier Reef, Australia. Mar Pollut Bull 119:106–119Google Scholar
  83. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882Google Scholar
  84. Russo GL (2009) Dietary n-6 and n-3 polyunsaturated fatty acids: From biochemistry to clinical implications in cardiovascular prevention. Biochem Pharmacol 77:937–946Google Scholar
  85. Saunders SM, Radford B, Bourke SA, Thiele Z, Bech T, Mardon J (2005) A rapid method for determining lipid fraction ratios of hard corals under varying sediment and light regimes. Environ Chem 2:331–336Google Scholar
  86. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317Google Scholar
  87. Seemann J, Sawall Y, Auel H, Richter C (2013) The use of lipids and fatty acids to measure the trophic plasticity of the coral Stylophora subseriata. Lipids 48:275–286Google Scholar
  88. Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688Google Scholar
  89. Singmann H, Bolker B, Westfall J, Aust F (2016) afex: Analysis of factorial experimentsGoogle Scholar
  90. Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904Google Scholar
  91. Strahl J, Francis DS, Doyle J, Humphrey C, Fabricius KE (2016) Biochemical responses to ocean acidification contrast between tropical corals with high and low abundances at volcanic carbon dioxide seeps. ICES J Mar Sci 73:897–909Google Scholar
  92. Sweatman H, Delean S, Syms C (2011) Assessing loss of coral cover on Australia’s Great Barrier Reef over two decades, with implications for longer-term trends. Coral Reefs 30:521–531Google Scholar
  93. Szmant-Froelich A, Pilson MEQ (1980) The effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition of Astrangia danae Milne Edwards & Haime 1849. J Exp Mar Bio Ecol 48:85–97Google Scholar
  94. Teece MA, Estes B, Gelsleichter E, Lirman D (2011) Heterotrophic and autotrophic assimilation of fatty acids by two scleractinian corals, montastraea faveolata and porites astreoides. Limnol Oceanogr 56:1285–1296Google Scholar
  95. Thompson AA, Lonborg C, Costello P, Davidson J, Logan M, Furnas MJ, Gunn K, Liddy M, Skuza M, Uthicke S, Wright M, Zagorskis I, Schaffelke B (2014) Marine Monitoring Program. Annual Report of AIMS Activities 2013-2014 - Inshore water quality and coral reef monitoring. Report for the Great Barrier Reef Marine Park AuthorityGoogle Scholar
  96. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184Google Scholar
  97. Tolosa I, Treignier C, Grover R, Ferrier-Pagès C (2011) 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 30:763–774Google Scholar
  98. 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 53:2702–2710Google Scholar
  99. Volkman JK (1999) Australasian research on marine natural products: chemistry, bioactivity and ecology. Mar Freshw Res 50:761–779Google Scholar
  100. Ward S (1995) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. CoraL Reefs 14:87–90Google Scholar
  101. Weber M, de Beer D, Lott C, Polerecky L, Kohls K, Abed RMM, Ferdelman TG, Fabricius KE (2012) Mechanisms of damage to corals exposed to sedimentation. Proc Natl Acad Sci 109:E1558–E1567Google Scholar
  102. Wooldridge SA (2009) Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751Google Scholar
  103. Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem Physiol 122:397–407Google Scholar
  104. Yamashiro H, Oku H, Onaga K (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish Sci 71:448–453Google Scholar

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Authors and Affiliations

  1. 1.Australian Institute of Marine ScienceTownsville MCAustralia
  2. 2.AIMS@JCU, Australian Institute of Marine Science, James Cook UniversityTownsvilleAustralia
  3. 3.College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia
  4. 4.ARC Centre of Excellence for Coral Reef Studies, James Cook UniversityTownsvilleAustralia
  5. 5.Deakin University, Geelong, Australia, School of Life and Environmental Sciences, Warrnambool CampusWarrnamboolAustralia

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