Coral Reefs

, Volume 31, Issue 4, pp 951–960 | Cite as

Food availability promotes rapid recovery from thermal stress in a scleractinian coral

  • S. R. ConnollyEmail author
  • M. A. Lopez-Yglesias
  • K. R. N. Anthony


Bleaching in corals due to environmental stress represents a loss of energy intake often leading to an increase in mortality risk. Successful coral recovery from severe bleaching events may depend on the rate of replenishment of algal symbiont populations following the period of thermal stress, the supply of an alternative food source, or both. Here, we explore the role of food availability in promoting the survival and recovery of a common coral (Acropora intermedia) following acute experimentally induced thermal stress. Fed corals were provided with live rotifers daily, to maintain densities of zooplankton in tanks that are typical of coral reefs. After a 6-week acclimation phase, heated corals were subjected to a +4 °C thermal anomaly for a 7-day period (bleaching phase) then temperatures were returned to normal for a further 2 weeks (recovery phase). Results demonstrated that heated corals had higher survival when they were provided with heterotrophic food. Fed corals experienced reduced loss of chlorophyll a, relative to unfed corals. During the recovery phase, both fed and unfed corals recovered within a few days; however, fed corals recovered to pre-bleaching phase levels of chlorophyll a, whereas unfed corals stabilized approximately one-third below this level. Protein levels of fed corals declined markedly during the bleaching phase, but recovered all of their losses by the end of the recovery phase. In contrast, unfed corals had low protein levels that were maintained throughout the experiment. To the extent that these results are representative of corals’ responses to thermal anomalies in nature, the findings imply that availability of particulate food matter has the potential to increase corals’ capacity to survive thermally induced bleaching and to ameliorate its sub-lethal effects. They also support the hypothesis that different rates of heterotrophy are an important determinant of variation in resilience to thermal stress among reef environments.


Coral bleaching Recovery Heterotrophy Phototrophy Nutrients 



We thank E. Graham and M. Hisano for assistance with statistical analysis and manuscript formatting, O. Hoegh-Guldberg for kindly permitting use of a MINI PAM, and G. Russ, A. Baird, J. Collins, M. Hoogenboom, and two anonymous reviewers for helpful comments on earlier drafts of this manuscript. This research was supported by the Australian Research Council and James Cook University.


  1. Anthony KRN, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, energetics, and coral mortality risk: effects of temperature, light, and sediment regime. Limnol Oceanogr 52:716–726CrossRefGoogle Scholar
  2. Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550CrossRefGoogle Scholar
  3. Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  4. Berkelmans R, De’Ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74–83CrossRefGoogle Scholar
  5. Borell EM, Bischof K (2008) Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157:593–601PubMedCrossRefGoogle Scholar
  6. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  7. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5(6):e124. doi: 10.1371/journal.pbio.0050124 PubMedCrossRefGoogle Scholar
  8. DeVantier LM, De’ath G, Turak E, Done TJ, Fabricius KE (2006) Species richness and community structure of reef-building corals on the nearshore Great Barrier Reef. Coral Reefs 25:329–340CrossRefGoogle Scholar
  9. Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324Google Scholar
  10. Edmunds PJ, Gates RD, Gleason DF (2003) The tissue composition of Montastraea franksi during a natural bleaching event in the Florida Keys. Coral Reefs 22:54–62Google Scholar
  11. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146PubMedCrossRefGoogle Scholar
  12. Ferrier-Pagès C, Rottier C, Beraud E, Levy O (2010) Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: effect on the rates of photosynthesis. J Exp Mar Biol Ecol 390:118–124CrossRefGoogle Scholar
  13. Gladfelter EH, Michel G, Sanfelici A (1989) Metabolic gradients along a branch of the reef coral Acropora palmata. Bull Mar Sci 44:1166–1173Google Scholar
  14. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189PubMedCrossRefGoogle Scholar
  15. Hoegh-Guldberg O (1994) Population dynamics of symbiotic zooxanthellae in the coral Pocillopora damicornis exposed to elevated ammonium [(NH4)2 SO4] concentrations. Pac Sci 48:263–272Google Scholar
  16. Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev Camb Philos Soc 84:1–17PubMedCrossRefGoogle Scholar
  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 296:145–166CrossRefGoogle Scholar
  18. Houlbrèque F, Tambutté E, Allemand D, Ferrier-Pagès C (2004) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469PubMedCrossRefGoogle Scholar
  19. Hueerkamp C, Glynn PW, D’Croz L, Mate JL, Colley SB (2001) Bleaching and recovery of five eastern Pacific corals in an El Nino-related temperature experiment. Bull Mar Sci 69:215–236Google Scholar
  20. Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol Prog Ser 420:91–101CrossRefGoogle Scholar
  21. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194Google Scholar
  22. Jones RJ (1997) Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Mar Ecol Prog Ser 158:51–59CrossRefGoogle Scholar
  23. Jones RJ, Ward S, Amri AY, Hoegh-Guldberg O (2000) Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event. Mar Freshw Res 51:63–71CrossRefGoogle Scholar
  24. Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531PubMedCrossRefGoogle Scholar
  25. Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  26. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163CrossRefGoogle Scholar
  27. Middlebrook R, Anthony KRN, Hoegh-Guldberg O, Dove S (2010) Heating rate and symbiont productivity are key factors determining thermal stress in the reef-building coral Acropora formosa. J Exp Biol 213:1026–1034PubMedCrossRefGoogle Scholar
  28. Muller-Parker G, McCloskey L, Hoegh-Guldberg O, McAuley P (1994) Effect of ammonium enrichment on animal and algal biomass of the coral Pocillopora damicornis. Pac Sci 48:273–283Google Scholar
  29. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Coral reefs ecosystems of the world. Elsevier, Amsterdam, pp 75–87Google Scholar
  30. Nordemar I, Nystrom M, Dizon R (2003) Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrica in the absence of particulate food. Mar Biol 142:669–677Google Scholar
  31. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422PubMedCrossRefGoogle Scholar
  32. Pinheiro JC, Bates MD, DebRoy S, Sarkar D, R Development Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version 3:1–102Google Scholar
  33. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  34. Rodrigues LJ, Grottoli AG, Pease TK (2008) Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. J Exp Mar Biol Ecol 358:136–143CrossRefGoogle Scholar
  35. Roman MR, Furnas MJ, Mullin MM (1990) Zooplankton abundance and grazing at Davies Reef, Great Barrier Reef, Australia. Mar Biol 105:73–82CrossRefGoogle Scholar
  36. Sebens KP, Grace SP, Helmuth B, Maney EJ Jr, Miles JS (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa and Porites porites, in a field enclosure. Mar Biol 131:347–360CrossRefGoogle Scholar
  37. Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224CrossRefGoogle Scholar
  38. Taguchi S, Kinzie RA III (2001) Growth of zooxanthellae in culture with two nitrogen sources. Mar Biol 138:149–155CrossRefGoogle Scholar
  39. Therneau T (2011) coxme: mixed effects cox models. R package version 2.1-3Google Scholar
  40. Therneau T, Lumley T (2011) survival: survival analysis, including penalised likelihood. R package version 2.36-5Google Scholar
  41. Tolosa I, Treignier C, Grover R, Ferrier-Pages 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 30:763–774CrossRefGoogle Scholar
  42. Veron JEN (2000) Corals of the world, vol 1–3. Australian Institute of Marine Science, Townsville, AustraliaGoogle Scholar
  43. Wallace CC (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO Publishing, CollingwoodGoogle Scholar
  44. Ward S, Harrison PJ, Hoegh-Guldberg O (2000) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. Proc 9th Int Coral Reef Symp 2:1123–1128Google Scholar
  45. Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ 19:291–299CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • S. R. Connolly
    • 1
    • 2
    Email author
  • M. A. Lopez-Yglesias
    • 1
  • K. R. N. Anthony
    • 1
    • 3
  1. 1.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  3. 3.Australian Institute of Marine ScienceTownsvilleAustralia

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