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Seasonal variations in energy levels and metabolic processes of two dominant Acropora species (A. spicifera and A. digitifera) at Ningaloo Reef

Abstract

Seasonal variations in coral health indices reflecting autotrophic activity (chlorophyll a and zooxanthellae density), metabolic rates (RNA/DNA ratio and protein) and energy storage (ratio of storage: structural lipids or lipid ratios) were examined for two dominant Acropora species [Acropora digitifera (AD) and Acropora spicifera (AS)] at Ningaloo Reef (north-western Australia). Such detailed investigation of metabolic processes is important background, with regard to understanding the vulnerability of corals to environmental change. Health indices in AD and AS were measured before and after spawning in austral autumn and winter 2010, and austral summer 2011 at six stations. Health indices showed seasonal and species-specific differences but negligible spatial differences across a reef section. For AD, autotrophic indices were negatively correlated with lipid ratios and metabolic indices. Metabolic indices were significantly higher in AS than AD. No correlation was observed between RNA/DNA ratios and lipid ratios with any autotrophic indices for AS. Lipid ratios were stable throughout the year for AS while they changed significantly for AD. For both species, indices of metabolic activity were highest during autumn, while autotrophic indices were highest in winter and summer. Results suggest that the impact of the broadcast spawning event on coral health indices at Ningaloo Reef occurred only as a backdrop to massive seasonal changes in coral physiology. The La Niña summer pattern resulted in high autotrophic indices and low metabolic indices and energy stores. Our results imply different metabolic processes in A. digitifera and A. spicifera as well as a strong impact of extreme events on coral physiology.

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References

  1. 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 Biochem Syst Environ Physiol 165:183–192

    Google Scholar 

  2. Al-Sofyani AA, Niaz GR (2007) A comparative study of the components of the hard coral Seriatopora hystrix and the soft coral Xenia umbellata along the Jeddah coast, Saudi Arabia. Rev Biol Mar Oceanogr 42:207

    Article  Google Scholar 

  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  4. Anderson M, Gorley R, Clarke K (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-e, Plymouth, p 214

    Google Scholar 

  5. 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

    PubMed  Article  Google Scholar 

  6. 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 

  7. Brown BE, Dunne RP, Ambarsari I, Le Tissier MDA, Satapoomin U (1999) Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar Ecol Prog Ser 191:53–69

    Article  Google Scholar 

  8. Buckley BA, Szmant AM (2004) RNA/DNA ratios as indicators of metabolic activity in four species of Caribbean reef-building corals. Mar Ecol Prog Ser 282:143–149

    Article  CAS  Google Scholar 

  9. Cassata L, Collins LB (2008) Coral reef communities, habitats, and substrates in and near sanctuary zones of Ningaloo Marine Park. J Coast Res 24:139–151

    Article  Google Scholar 

  10. Chappell J (1980) Coral morphology, diversity and reef growth. Nature 286:249–252

    Article  Google Scholar 

  11. Chen CA, Wang JT, Fang LS, Yang YW (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121

    Article  Google Scholar 

  12. Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28:589–606

    Article  Google Scholar 

  13. Dahlhoff EP (2004) Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annu Rev Physiol 66:183–207

    PubMed  Article  CAS  Google Scholar 

  14. Davies PS (1991) Effect of daylight variations on the energy budgets of shallow-water corals. Mar Biol 108:137–144

    Article  Google Scholar 

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

    Google Scholar 

  16. 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 (Biol) 239:231–246

    Article  Google Scholar 

  17. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845

    PubMed  Article  CAS  Google Scholar 

  18. Feng M, Wild-Allen K (2009) The Leeuwin current. In: Liu K-K, Atkinson L (eds) Carbon and nutrient fluxes in continental margins. A global synthesis. Springer, Berlin Heidelberg, pp 197–210

    Google Scholar 

  19. Feng M, Meyers G, Pearce A, Wijffels S (2003) Annual and interannual variations of the Leeuwin Current at 32 S. J Geophys Res 108:3355

    Article  Google Scholar 

  20. Ferrier-Pagès C, Witting J, Tambutte 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 

  21. Ferrier-Pagès C, Hoogenboom M, Houlbrèque F (2011) The role of plankton in coral trophodynamics. In: Dubinsky Z, Stambler N (eds) Coral reefs: An ecosystem in transition. Springer, Netherlands, pp 215–229

    Chapter  Google Scholar 

  22. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  24. Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar Ecol Prog Ser 346:89–96

    Article  CAS  Google Scholar 

  25. Harithsa S, Raghukumar C, Dalal SG (2005) Stress response of two coral species in the Kavaratti atoll of the Lakshadweep Archipelago, India. Coral Reefs 24:463–474

    Article  Google Scholar 

  26. Harland AD, Fixter LM, Davies PS, Anderson RA (1992) Effect of light on the total lipid-content and storage lipids of the symbiotic sea-anemone Anemonia viridis. Mar Biol 112:253–258

    Article  CAS  Google Scholar 

  27. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195

    Article  Google Scholar 

  28. 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 

  29. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    PubMed  Article  CAS  Google Scholar 

  30. Hoogenboom MO, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  32. 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 

  33. Houlbrèque F, Tambutte E, Allemand D, Ferrier-Pages C (2004) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469

    PubMed  Article  Google Scholar 

  34. Howe SA, Marshall AT (2001) Thermal compensation of metabolism in the temperate coral Plesiastrea versipora (Lamarck, 1816). J Exp Mar Biol Ecol 259:231–248

    PubMed  Article  Google Scholar 

  35. Humphrey C (2009) Changes in RNA:DNA ratio of corals as an indicator of coral health. In: Fabricius K, Uthricke S, Cooper T, Humphrey C, De’ath G, Mellors J (eds) Candidate bioindicate measures to monitor exposure to changing water quality on the Great Barrier Reef. Australian Institute of Marine Science, Townsville, pp 75–92

    Google Scholar 

  36. Jeffrey S, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:1–194

    Google Scholar 

  37. Jones R, Hoegh-Guldberg O, Larkum A, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  39. Leuzinger S, Willis BL, Anthony KRN (2012) Energy allocation in a reef coral under varying resource availability. Mar Biol 159:177–186

    Article  Google Scholar 

  40. Lowe RJ, Taebi S, Symonds G, Pattiaratchi CB, Ivey GN, Brinkman R (2008) Hydrodynamics of fringing reef systems: Ningaloo Reef, Western Australia. PECS, Liverpool

    Google Scholar 

  41. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  42. Meesters EH, Nieuwland G, Duineveld GCA, Kok A, Bak RPM (2002) RNA/DNA ratios of scleractinian corals suggest acclimatisation/adaptation in relation to light gradients and turbidity regimes. Mar Ecol Prog Ser 227:233–239

    Article  CAS  Google Scholar 

  43. Mills MM, Sebens KP (2004) Ingestion and assimilation of nitrogen from benthic sediments by three species of coral. Mar Biol 145:1097–1106

    Article  CAS  Google Scholar 

  44. Muko S, Kawasaki K, Sakai K, Takasu F, Shigesada N (2000) Morphological plasticity in the coral Porites sillimaniani and its adaptive significance. Bull Mar Sci 66:225–239

    Google Scholar 

  45. Mumby PJ, Chisholm JRM, Edwards AJ, Andrefouet S, Jaubert J (2001) Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Mar Ecol Prog Ser 222:209

    Article  Google Scholar 

  46. Oku H, Yamashiro H, Onaga K (2003a) Lipid biosynthesis from [14C]-glucose in the coral Montipora digitata. Fish Sci 69:625–631

    Article  CAS  Google Scholar 

  47. Oku H, Yamashiro H, Onaga K, Sakai K, Iwasaki H (2003b) Seasonal changes in the content and composition of lipids in the coral Goniastrea aspera. Coral Reefs 22:83–85

    Google Scholar 

  48. Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 1:79–89

    Article  Google Scholar 

  49. Patten N, Wyatt ASJ, Lowe R, Waite A (2011) Uptake of picophytoplankton, bacterioplankton and virioplankton by a fringing coral reef community (Ningaloo Reef, Australia). Coral Reefs 30:555–567

    Article  Google Scholar 

  50. Pearce A, Lenanton R, Jackson G, Moore J, Feng M, Gaughan D (2011) The “marine heat wave” off Western Australia during the summer of 2010/11. Report prepared by Department of Fisheries, Government of West Australia, North Beach, WA

  51. Ribes M, Coma R, Atkinson MJ, Kinzie RA (2003) Particle removal by coral reef communities: picoplankton is a major source of nitrogen. Mar Ecol Prog Ser 257:13–23

    Article  Google Scholar 

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

    Article  Google Scholar 

  53. Rossi S, Tsounis G (2007) Temporal and spatial variation in protein, carbohydrate, and lipid levels in Corallium rubrum (Anthozoa, Octocorallia). Mar Biol 152:429–439

    Article  CAS  Google Scholar 

  54. Rossi S, Gili JM, Coma R, Linares C, Gori A, Vert N (2006) Temporal variation in protein, carbohydrate, and lipid concentrations in Paramuricea clavata (Anthozoa, Octocorallia): evidence for summer–autumn feeding constraints. Mar Biol 149:643–651

    Article  CAS  Google Scholar 

  55. Rousseaux CSG, Lowe R, Feng M, Waite AM, Thompson PA (2011) The role of the Leeuwin Current and mixed layer depth on the autumn phytoplankton bloom off Ningaloo Reef, Western Australia. Cont Shelf Res 32:22–35

    Article  Google Scholar 

  56. Rowan R (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265

    PubMed  Article  CAS  Google Scholar 

  57. 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 2:331–336

    Article  CAS  Google Scholar 

  58. Sheppard CRC (2009) The biology of coral reefs. Oxford University Press, Oxford

    Book  Google Scholar 

  59. Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460

    Article  Google Scholar 

  60. Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904

    Google Scholar 

  61. Stimson J (1997) The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 214:35–48

    Article  Google Scholar 

  62. Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74

    Article  Google Scholar 

  63. Taebi S, Lowe RJ, Pattiaratchi CB, Ivey GN, Symonds G, Brinkman R (2011) Nearshore circulation in a tropical fringing reef system. J Geophys Res 116:1–15

    Article  Google Scholar 

  64. Titlyanov E, Titlyanova T (2002) Reef-building corals—symbiotic autotrophic organisms: 2. Pathways and mechanisms of adaptation to light. Russ J Mar Biol 28:16–31

    Article  Google Scholar 

  65. Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337

    PubMed  Article  Google Scholar 

  66. 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 

  67. Ulstrup KE, Hill R, Van Oppen MJH, Larkum AWD, Ralph PJ (2008) Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Mar Ecol Prog Ser 361:139–150

    Article  Google Scholar 

  68. Wallace C (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO Publishing, Australia

    Google Scholar 

  69. Ward S (1995) Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14:87–90

    Article  Google Scholar 

  70. Wyatt ASJ, Lowe RJ, Humphries S, Waite AM (2010) Particulate nutrient fluxes over a fringing coral reef: relevant scales of phytoplankton production and mechanisms of supply. Mar Ecol Prog Ser 405:113–130

    Article  CAS  Google Scholar 

  71. Yamaguchi M (1974) Effect of elevated temperature on the metabolic activity of the coral reef asteroid Acanthaster planci (L.). Pac Sci 28:139–146

    Google Scholar 

  72. Yamashiro H, Oku H, Onaga K, Iwasaki H, Takara K (2001) Coral tumors store reduced level of lipids. J Exp Mar Biol Ecol 265:171–179

    Article  CAS  Google Scholar 

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Acknowledgments

We thank M. Mohl, M. Saunders, H. Shortland-Jones, A. Metaxas, R. Scheibling, A. Turco, T. Hill, B. Copson, S. Bickford, T. Stokes, J. Gustav Engelstad and N. Kresoje for assistance in the field and the laboratory; D. Krikke, A. Wyatt, C. Rousseaux, T. Cooper and R. Jones for providing information about methods; and N. Rosser for identifying coral species. Funding was provided by a Discovery Grant to AMW from the Australian Research Council. Funding was provided by the Endeavour International Postgraduate Research (IPRS) Scholarship from the Australian Government and a top-up scholarship from the Western Australian Marine Science Institute (Node 2) to S. Hinrichs.

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Communicated by Biology Editor Dr. Anastazia Banaszak

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Hinrichs, S., Patten, N.L., Allcock, R.J.N. et al. Seasonal variations in energy levels and metabolic processes of two dominant Acropora species (A. spicifera and A. digitifera) at Ningaloo Reef. Coral Reefs 32, 623–635 (2013). https://doi.org/10.1007/s00338-013-1027-z

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Keywords

  • Coral
  • Metabolism
  • Energy
  • Health
  • Seasonality
  • Ningaloo Reef