Coral Reefs

, Volume 32, Issue 1, pp 1–12 | Cite as

Relationships between temperature, bleaching and white syndrome on the Great Barrier Reef

Report

Abstract

Coral bleaching and disease have often been hypothesized to be mutually reinforcing or co-occurring, but much of the research supporting this has only drawn an implicit connection through common environmental predictors. In this study, we examine whether an explicit relationship between white syndrome and bleaching exists using assemblage-level monitoring data from up to 112 sites on reef slopes spread throughout the Great Barrier Reef over 11 years of monitoring. None of the temperature metrics commonly used to predict mass bleaching performed strongly when applied to these data. Furthermore, the inclusion of bleaching as a predictor did not improve model skill over baseline models for predicting white syndrome. Similarly, the inclusion of white syndrome as a predictor did not improve models of bleaching. Evidence for spatial co-occurrence of bleaching and white syndrome at the assemblage level in this data set was also very weak. These results suggest the hypothesized relationship between bleaching and disease events may be weaker than previously thought, and more likely to be driven by common responses to environmental stressors, rather than directly facilitating one another.

Keywords

Coral reef ecology Multiple stressors Synergy Resilience Coral bleaching Coral disease 

Supplementary material

338_2012_944_MOESM1_ESM.docx (28 kb)
Supplementary material 1 (DOCX 28 kb)
338_2012_944_MOESM2_ESM.eps (2 mb)
Supplementary material 2 (EPS 2051 kb)
338_2012_944_MOESM3_ESM.eps (13.2 mb)
Supplementary material 3 (EPS 13529 kb)
338_2012_944_MOESM4_ESM.eps (15.3 mb)
Supplementary material 4 (EPS 15617 kb)

References

  1. Ainsworth TD, Hoegh-Guldberg O (2009) Bacterial communities closely associated with coral tissues vary under experimental and natural reef conditions and thermal stress. Aquat Biol 4:289–296CrossRefGoogle Scholar
  2. Ainsworth T, Kvennefors E, Blackall L, Fine M, Hoegh-Guldberg O (2007) Disease and cell death in white syndrome of acroporid corals on the Great Barrier Reef. Mar Biol 151:19–29CrossRefGoogle Scholar
  3. Anselin L (1995) Local indicators of spatial association - LISA. Geographical Analysis 27:93–115CrossRefGoogle Scholar
  4. 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
  5. Banin E, Vassilakos D, Orr E, Martinez RJ, Rosenberg E (2003) Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr Microbiol 46:418–422PubMedCrossRefGoogle Scholar
  6. Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242PubMedCrossRefGoogle Scholar
  7. Berkelmans R, Oliver JK (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18:55–60CrossRefGoogle Scholar
  8. Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18:219–228CrossRefGoogle Scholar
  9. 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
  10. Boyett HV, Bourne DG, Willis BL (2007) Elevated temperature and light enhance progression and spread of black band disease on staghorn corals of the Great Barrier Reef. Mar Biol 151:1711–1720CrossRefGoogle Scholar
  11. Brandt ME, McManus JW (2009) Disease incidence is related to bleaching extent in reef-building corals. Ecology 90:2859–2867PubMedCrossRefGoogle Scholar
  12. Bruckner AW, Hill RL (2009) Ten years of change to coral communities off Mona and Desecheo Islands, Puerto Rico, from disease and bleaching. Dis Aquat Org 87:19–31PubMedCrossRefGoogle Scholar
  13. 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:e124. doi:10.1371/journal.pbio.0050124 PubMedCrossRefGoogle Scholar
  14. Croquer A, Weil E (2009) Changes in Caribbean coral disease prevalence after the 2005 bleaching event. Dis Aquat Org 87:33–43PubMedCrossRefGoogle Scholar
  15. Donner SD (2011) An evaluation of the effect of recent temperature variability on the prediction of coral bleaching events. Ecol Appl 21:1718–1730PubMedCrossRefGoogle Scholar
  16. Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65CrossRefGoogle Scholar
  17. Gleeson MW, Strong AE (1995) Applying MCSST to coral reef bleaching. Adv Space Res 16:151–154CrossRefGoogle Scholar
  18. Glynn PW (1996) Coral reef bleaching: Facts, hypotheses and implications. Global Change Biol 2:495–509CrossRefGoogle Scholar
  19. Goreau TJ, Hayes RL (1994) Coral bleaching and ocean hot-spots. Ambio 23:176–180Google Scholar
  20. Harvell D, Kim K, Quirolo C, Weir J, Smith G (2001) Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea). Hydrobiologia 460:97–104CrossRefGoogle Scholar
  21. Harvell D, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B, Global Environment Facility C (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195CrossRefGoogle Scholar
  22. Hayes RL, Goreau NI (1998) The significance of emerging diseases in the tropical coral reef ecosystem. Rev Biol Trop 46:173–185Google Scholar
  23. Heron SF, Willis BL, Skirving WJ, Eakin CM, Page CA, Miller IR (2010) Summer Hot Snaps and Winter Conditions: Modelling White Syndrome outbreaks on Great Barrier Reef corals. PLoS ONE 5:e12210. doi:10.1371/journal.pone.0012210 PubMedCrossRefGoogle Scholar
  24. Jiménez C (2001) Seawater temperature measured at the surface and at two depths (7 and 12 m) in one coral reef at Culebra Bay, Gulf of Papagayo, Costa Rica. Rev Biol Trop 49:153–161PubMedGoogle Scholar
  25. Jones RJ (2008) Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Mar Biol 154:65–80CrossRefGoogle Scholar
  26. Jones RJ, Bowyer J, Hoegh-Guldberg O, Blackall LL (2004) Dynamics of a temperature-related coral disease outbreak. Mar Ecol-Prog Ser 281:63–77CrossRefGoogle Scholar
  27. Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site- and species-specificity of common bacterial associates. PLoS ONE 5:e10401. doi:10.1371/journal.pone.0010401 PubMedCrossRefGoogle Scholar
  28. Liu G, Strong AE, Skirving W (2003) Remote sensing of sea surface temperatures during 2002 Barrier Reef coral bleaching. EOS Trans Am Geophys Union 84:137–144CrossRefGoogle Scholar
  29. Lough JM (2000) 1997-98: Unprecedented thermal stress to coral reefs? Geophys Res Lett 27:3901–3904CrossRefGoogle Scholar
  30. Maina J, Venus V, McClanahan TR, Ateweberhan M (2008) Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models. Ecol Model 212:180–199CrossRefGoogle Scholar
  31. Maynard JA, Turner PJ, Anthony KRN, Baird AH, Berkelmans R, Eakin CM, Johnson J, Marshall PA, Packer GR, Rea A, Willis BL (2008) ReefTemp: An interactive monitoring system for coral bleaching using high-resolution SST and improved stress predictors. Geophys Res Lett 35, L05603, 5 pp. doi:10.1029/2007GL032175
  32. Maynard JA, Anthony KRN, Harvell CD, Burgman MA, Beeden R, Sweatman H, Heron SF, Lamb JB, Willis BL (2011) Predicting outbreaks of a climate-driven coral disease in the Great Barrier Reef. Coral Reefs 30:485–495CrossRefGoogle Scholar
  33. McClanahan TR, Ateweberhan M, Sebastian CR, Graham NAJ, Wilson SK, Bruggemann JH, Guillaume MMM (2007) Predictability of coral bleaching from synoptic satellite and in situ temperature observations. Coral Reefs 26:695–701CrossRefGoogle Scholar
  34. Menard S (1995) Applied Logistic regression analysis: Sage University Series on Quantitative Applications in the Social Sciences. Sage, Thousand Oaks, CAGoogle Scholar
  35. Miller J, Waara R, Muller E, Rogers C (2006) Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands. Coral Reefs 25:418–419CrossRefGoogle Scholar
  36. Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23PubMedGoogle Scholar
  37. Muller EM, van Woesik R (2009) Shading reduces coral-disease progression. Coral Reefs 28:757–760CrossRefGoogle Scholar
  38. Muller EM, Rogers CS, Spitzack AS, van Woesik R (2008) Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27:191–195CrossRefGoogle Scholar
  39. Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD (2009) Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event. Dis Aquat Org 87:67–78PubMedCrossRefGoogle Scholar
  40. Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945PubMedCrossRefGoogle Scholar
  41. Nicholls RJ, Wong PP, Burkett VR, Codignotto JO, Hay JE, McLean RF, Ragoonaden S, Woodroffe CD (2007) Coastal systems and low-lying areas. In: Parry ML, Canziani OF, Palutikof JP, Linden PJvd, Hanson CE (eds) Climate change 2007: Impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, pp 315–356Google Scholar
  42. Ord JK, Getis A (1995) Local spatial autocorrelation statistics: distributional issues and an application. Geogr Anal 27:286–306CrossRefGoogle Scholar
  43. Peirce CS (1884) The numerical measure of the success of predictions. Science 4:453–454PubMedCrossRefGoogle Scholar
  44. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073PubMedCrossRefGoogle Scholar
  45. Richier S, Cottalorda JM, Guillaume MMM, Fernandez C, Allemand D, Furla P (2008) Depth-dependant response to light of the reef building coral, Pocillopora verrucosa: Implication of oxidative stress. J Exp Mar Biol Ecol 357:48–56CrossRefGoogle Scholar
  46. Ripley BD (1976) The second-order analysis of stationary point processes. J Appl Prob 13:255–266CrossRefGoogle Scholar
  47. Ripley BD (1977) Modelling spatial patterns. JR Stat Soc B 39:172–212Google Scholar
  48. Roff G, Kvennefors ECE, Fine M, Ortiz J, Davy JE, Hoegh-Guldberg O (2011) The ecology of ‘Acroporid White Syndrome’, a coral disease from the Southern Great Barrier Reef. PLoS ONE 6:e26829. doi:10.1371/journal.pone.0026829 PubMedCrossRefGoogle Scholar
  49. Rosenberg E, Kushmaro A, Kramarsky-Winter E, Banin E, Yossi L (2009) The role of microorganisms in coral bleaching. ISME J 3:139–146PubMedCrossRefGoogle Scholar
  50. Selig ER, Casey KS, Bruno JF (2010) New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management. Glob Ecol Biogeogr 19:397–411CrossRefGoogle Scholar
  51. Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Org 87:5–18PubMedCrossRefGoogle Scholar
  52. Stephenson DB (2000) Use of the “odds ratio” for diagnosing forecast skill. Weather Forecast 15:221–232CrossRefGoogle Scholar
  53. Sweatman H, Cheal A, Coleman G, Emslie M, Johns K, Jonker M, Miller I, Osborne K (2008) Long-term monitoring of the Great Barrier Reef, Status Report No. 8. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  54. van Hooidonk R, Huber M (2009) Quantifying the quality of coral bleaching predictions. Coral Reefs 28:579–587CrossRefGoogle Scholar
  55. Vinebrooke RD, Cottingham KL, Norberg J, Scheffer M, Dodson SI, Maberly SC, Sommer U (2004) Impacts of multiple stressors on biodiversity and ecosystem functioning: The role of species co-tolerance. Oikos 104:451–457CrossRefGoogle Scholar
  56. Willis BL, Page CA, Dinsdale EA (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, pp 69–104CrossRefGoogle Scholar
  57. Wolanski E, Hamner W (1988) Topographically controlled fronts in the ocean and their biological influence. Science 241:177–181PubMedCrossRefGoogle Scholar
  58. Wooldridge S (2007) Quantifying the synergistic interaction between thermal stress and water quality in determining the bleaching sensitivity of inshore reefs in the Great Barrier Reef Marine Park. Marine and Tropical Sciences Research Facility, Townsville, p 21Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • S. S. Ban
    • 1
  • N. A. J. Graham
    • 1
  • S. R. Connolly
    • 1
    • 2
  1. 1.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia

Personalised recommendations