Abstract
Links between anomalously high sea temperatures and outbreaks of coral diseases known as White Syndromes (WS) represent a threat to Indo-Pacific reefs that is expected to escalate in a changing climate. Further advances in understanding disease aetiologies, determining the relative importance of potential risk factors for outbreaks and in trialing management actions are hampered by not knowing where or when outbreaks will occur. Here, we develop a tool to target research and monitoring of WS outbreaks in the Great Barrier Reef (GBR). The tool is based on an empirical regression model and takes the form of user-friendly interactive ~1.5-km resolution maps. The maps denote locations where long-term monitoring suggests that coral cover exceeds 26% and summer temperature stress (measured by a temperature metric termed the mean positive summer anomaly) is equal to or exceeds that experienced at sites in 2002 where the only severe WS outbreaks documented on the GBR to date were observed. No WS outbreaks were subsequently documented at 45 routinely surveyed sites from 2003 to 2008, and model hindcasts for this period indicate that outbreak likelihood was never high. In 2009, the model indicated that outbreak likelihood was high at north-central GBR sites. The results of the regression model and targeted surveys in 2009 revealed that the threshold host density for an outbreak decreases as thermal stress increases, suggesting that bleaching could be a more important precursor to WS outbreaks than previously anticipated, given that bleaching was severe at outbreak sites in 2002 but not at any of the surveyed sites in 2009. The iterative approach used here has led to an improved understanding of disease causation, will facilitate management responses and can be applied to other coral diseases and/or other regions.
References
Aeby GS, Santavy DL (2006) Factors affecting susceptibility of the coral Montastrea faveolata to black-band disease. Mar Ecol Prog Ser 318:103–110
Aeby GS, Hutchinson M, MacGowan P (2008) Hawaii’s rapid response contingency plan for events of coral bleaching, disease or crown-of-thorns starfish outbreaks. The Division of Aquatic Resources, Department of Land and Natural Resources, Honolulu, HI
Anthony KRN, Hoogenboom M, Maynard JA, Middlebrook R, Grottoli A (2009) Energetics approach to predicting coral mortality risk from bleaching. Funct Ecol 23:539–550
Antolin MF (2008) Unpacking β: Within-host dynamics and evolutionary ecology of pathogen transmission. Annu Rev Ecol Evol Syst 39:415–437
Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38
Bass DK, Miller IR (1996) Crown-of-thorns starfish and coral surveys using the manta tow and scuba search techniques. Long-term Monitoring of the Great Barrier Reef Standard Operational Procedure Number 1. Australian Institute of Marine Science, Townsville
Berkelmans R, Oliver JK (1999) Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18:55–60
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 23:74–83
Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:254–262
Bruckner AW (2002) Priorities for effective management of coral diseases. NOAA, Washington, DC
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 Biology 5:1220–1227
Butterworth MH, Semenov MA, Barnes A, Moran D, West JS, Fitt BDL (2010) North-South divide: contrasting impacts of climate change on crop yields in Scotland and England. J R Soc Interface 7:123–130
Diaz M, Madin J (2010) Macroecological relationships between coral species’ traits and disease potential. Coral Reefs. doi:10.1007/s00338-010-0668-4
English S, Wilkinson CR, Baker V (eds) (2004) Survey manual for tropical marine resources, 2nd edn. Townsville, Australian Institute of Marine Science
Griffin DA, Rathbone CE, Smith GP, Suber KD, Turner PJ (2004) A decade of SST satellite data. On-line report: http://www.cmar.csiro.au/remotesensing/oceancurrents/ten_years_of_SST.doc Hobart, Australia
Harvell CD, Altizer S, Cattadori Im, Harrington L, Weil E (2009) Climate change and wildlife diseases: When does the host matter the most? Ecology 90:912–920
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warning and disease risks for terrestrial and marine biota. Science 296:2158–2162
Harvell CD, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Garriet S, Ernesto W, Willis BL (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195
Heron SF, Willis BL, Skirving WJ, Eakin MC, Page CA, Miller IR (2010) Summer hot snaps and winter conditions: modelling white syndrome outbreaks on Great Barrier Reef Corals. PloS One. doi:10.1371/journal.pone.0012210
Hijmans RJ, Forbes GA, Walker TS (2000) Estimating the global severity of potato late blight with GIS-linked disease forecast models. Plant Pathol (Oxf) 49:697–705
Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:547–1551
Lafferty KD, Holt RD (2003) How should environmental stress affect the population dynamics of disease? Ecol Lett 6:454–664
Little TJ, Kraaijeveld AR (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 19:58–60
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
Matsuzaki S, Rashel M, Uchiyama J, Sakurai S, Ujihara T, Kuroda M, Ikeuchi M, Tani T, Fujieda M, Wakiguchi H, Imai S (2005) Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother 11:211–219
Maynard JA, Johnson JE, Marshall PA, Goby G, Spillman C (2009) A strategic framework for responding to coral bleaching events in a changing climate. Environ Manage 44:1–11
Maynard JA, Turner PJ, Anthony KRN, Baird AH, Berkelmans R, Eakin CM, Johnson JE, 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. doi:10.1029/2007GL032175
Meehl GA, Covery C, Delworth T, Latif M, McAvaney B, Mitchell JFB, Stouffer RJ, Taylor KE (2007) The WCRP CMIP3 multimodel dataset: a new era in climate change research. Bull Am Meteorol Soc 88:1383–1394
Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following a massive bleaching in 2005 causes a 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937
Mydlarz LD, Couch CS, Weil E, Smith G, Harvell CD (2009) Immune defenses of healthy, bleached and diseases Montastrea faveolata during a natural bleaching event. Dis Aquat Org 87:67–78
Myers RL, Raymundo LJ (2009) Coral disease in Micronesian reefs: a link between disease prevalence and host abundance. Dis Aquat Org 87:97–104
Page CA, Baker DM, Harvell CD, Golbuu Y, Raymundo L, Neale SJ, Rosell KB, Rypien KL, Andras JP, Willis BL (2009) Influence of marine reserves on coral disease prevalence. Dis Aquat Org 87:135–150
Page CA, Willis BL (2008) Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation of this widespread coral disease. Coral Reefs 27:257–272
Palmer CV, Bythell JC, Willis BL (2010) Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals. FASEB J. doi:10.1096/fj.09-152447
Patterson KL, Porter JW, Ritchie KB, Polson SW, Mueller E, Peters EC, Santavy DL, Smith GW (2002) The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci USA 99:8725–8730
Raymundo LJ, Halford AR, Maypa AP, Kerr AM (2009) Functionally diverse reef-fish communities ameliorate coral disease. Proc Natl Acad Sci USA 106:17067–17070
Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:356–362
Rudolf VHW, Antonovics J (2005) Species coexistence and pathogens with frequency-dependent transmission. Am Nat 166:112–118
Savary S, Teng PS, Willocquet L, Nutter FW (2006) Quantification and modeling of crop losses: A review of purposes. Annu Rev Phytopathol 44:89–112
Sato Y, Bourne DG, Willis BL (2009) Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef, Australia). Proc R Soc Lond B Biol Sci 276:2795–2803
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman and Co, New York
Sussman M, Willis BL, Victor S, Bourne DG (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS One. doi:10.1371/journal.pone.0002393
Sussman M, Mieog JC, Doyle J, Victor S, Willis BL, Bourne DG (2009) Vibrio zinc-metalloprotease causes photoinactivation of coral endoysmbionts and coral tissue lesions. PLoS One. doi:10.1371/journal.pone.0004511
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
Williams GJ, Aeby GS, Cowie ROM, Davy SK (2010) Predictive modelling of coral disease distribution within a reef system. PLoS One. doi:10.1371/journal.pone.0009264
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 69–104
Wilkinson C, Souter D (eds) (2008) Status of Caribbean coral reefs after hurricanes and bleaching in 2005. Global Coral Reef Monitoring Network, Townsville
Wobeser GA (2006) Essentials of disease in wild animals. Blackwell Publishing, Oxford, UK
Wooldridge SA (2009) A new conceptual model for the enhanced release of mucus in symbiotic reef corals during ‘bleaching’ conditions. Mar Ecol Prog Ser 396:145–152
Work TM, Richardson LL, Reynolds TL, Willis BL (2009) Biomedical and veterinary science can increase our understanding of coral disease. J Exp Mar Biol Ecol 362:63–70
Acknowledgments
This work has been made possible by grants from the Marine and Tropical Sciences Research Facility through the Reef and Rainforest Research Centre and the Great Barrier Reef Marine Park Authority (GBRMPA) and benefited from the support of: the Coral Disease Working Group of the GEF Coral Reef Targeted Research project, the Australian Greenhouse Office, Australian Bureau of Meteorology, CSIRO Marine and Atmospheric Research and the Ocean Biology Processing Group of NASA. Field staff of the AIMS Long-Term Monitoring Program provided the disease survey data for 2002–2008, and G. Torda and Y. Sato assisted with surveys conducted in 2009. The AEDA CERF Hub and the University of Melbourne provided support to the first author and versions of the manuscript improved following insightful comments from several anonymous reviewers. This is a contribution by the ARC Centre of Excellence for Coral Reef Studies. The manuscript contents are solely the opinions of the authors and do not constitute a statement of policy, decision, or position on behalf of NOAA or the U. S. Government.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Andrew Baird
Rights and permissions
About this article
Cite this article
Maynard, J.A., Anthony, K.R.N., Harvell, C.D. et al. Predicting outbreaks of a climate-driven coral disease in the Great Barrier Reef. Coral Reefs 30, 485–495 (2011). https://doi.org/10.1007/s00338-010-0708-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-010-0708-0