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.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00338-013-1027-z/MediaObjects/338_2013_1027_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00338-013-1027-z/MediaObjects/338_2013_1027_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00338-013-1027-z/MediaObjects/338_2013_1027_Fig3_HTML.gif)
References
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
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
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson M, Gorley R, Clarke K (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-e, Plymouth, p 214
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
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
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
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
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
Chappell J (1980) Coral morphology, diversity and reef growth. Nature 286:249–252
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
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
Dahlhoff EP (2004) Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annu Rev Physiol 66:183–207
Davies PS (1991) Effect of daylight variations on the energy budgets of shallow-water corals. Mar Biol 108:137–144
Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324
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
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
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
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
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
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
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
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
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
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
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
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
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
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
Hoogenboom MO, Connolly SR, Anthony KRN (2008) Interactions between morphological and physiological plasticity optimize energy acquisition in corals. Ecology 89:1144–1154
Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17
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
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
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
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
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
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
Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531
Leuzinger S, Willis BL, Anthony KRN (2012) Energy allocation in a reef coral under varying resource availability. Mar Biol 159:177–186
Lowe RJ, Taebi S, Symonds G, Pattiaratchi CB, Ivey GN, Brinkman R (2008) Hydrodynamics of fringing reef systems: Ningaloo Reef, Western Australia. PECS, Liverpool
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
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
Mills MM, Sebens KP (2004) Ingestion and assimilation of nitrogen from benthic sediments by three species of coral. Mar Biol 145:1097–1106
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
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
Oku H, Yamashiro H, Onaga K (2003a) Lipid biosynthesis from [14C]-glucose in the coral Montipora digitata. Fish Sci 69:625–631
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
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
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
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
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
Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882
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
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
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
Rowan R (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265
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
Sheppard CRC (2009) The biology of coral reefs. Oxford University Press, Oxford
Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460
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
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
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
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
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
Todd PA (2008) Morphological plasticity in scleractinian corals. Biol Rev 83:315–337
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
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
Wallace C (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO Publishing, Australia
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
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
Yamaguchi M (1974) Effect of elevated temperature on the metabolic activity of the coral reef asteroid Acanthaster planci (L.). Pac Sci 28:139–146
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Anastazia Banaszak
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-013-1027-z