Skip to main content

Advertisement

Log in

Disease outbreaks, bleaching and a cyclone drive changes in coral assemblages on an inshore reef of the Great Barrier Reef

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Coral disease is a major threat to the resilience of coral reefs; thus, understanding linkages between disease outbreaks and disturbances predicted to increase with climate change is becoming increasingly important. Coral disease surveys conducted twice yearly between 2008 and 2011 at a turbid inshore reef in the central Great Barrier Reef spanned two disturbance events, a coral bleaching event in 2009 and a severe cyclone (cyclone ‘Yasi’) in 2011. Surveys of coral cover, community structure and disease prevalence throughout this 4-yr study provide a unique opportunity to explore cumulative impacts of disturbance events and disease for inshore coral assemblages. The principal coral disease at the study site was atramentous necrosis (AtN), and it primarily affected the key inshore, reef-building coral Montipora aequituberculata. Other diseases detected were growth anomalies, white syndrome and brown band syndrome. Diseases affected eight coral genera, although Montipora was, by far, the genus mostly affected. The prevalence of AtN followed a clear seasonal pattern, with disease outbreaks occurring only in wet seasons. Mean prevalence of AtN on Montipora spp. (63.8 % ± 3.03) was three- to tenfold greater in the wet season of 2009, which coincided with the 2009 bleaching event, than in other years. Persistent wet season outbreaks of AtN combined with the impacts of bleaching and cyclone events resulted in a 50–80 % proportional decline in total coral cover. The greatest losses of branching and tabular acroporids occurred following the low-salinity-induced bleaching event of 2009, and the greatest losses of laminar montiporids occurred following AtN outbreaks in 2009 and in 2011 following cyclone Yasi. The shift to a less diverse coral assemblage and the concomitant loss of structural complexity are likely to have long-term consequences for associated vertebrate and invertebrate communities on Magnetic Island reefs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Aeby GS, Ross M, Williams GJ, Lewis TD, Work TM (2010) Disease dynamics of Montipora white syndrome within Kaneohe Bay, Oahu, Hawaii: distribution, seasonality, virulence, and transmissibility. Dis Aquat Org 91:1–8

    Article  PubMed  CAS  Google Scholar 

  • Ainsworth TD, Hoegh-Guldberg O (2008) Cellular processes of bleaching in the Mediterranean coral Oculina patagonica. Coral Reefs 27:593–597

    Article  Google Scholar 

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

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Anthony SL, Page CA, Bourne DG, Willis BL (2008) Newly characterized distinct phases of the coral disease ‘atramentous necrosis’ on the Great Barrier Reef. Dis Aquat Org 81:255–259

    Article  PubMed  CAS  Google Scholar 

  • 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 23:539–550

    Article  Google Scholar 

  • Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38

    Article  Google Scholar 

  • Beeden R, Willis BL, Raymundo LJ, Page CA, Weil E (2008) Underwater cards for assessing coral health on Indo-Pacific Reefs. Coral Reef Targeted Research and Capacity Building for Management Program. Currie Communications, Melbourne

    Google Scholar 

  • Bellwood DR, Hughes TP (2001) The state of coral reef science - Response. Science 293:1997

    Article  CAS  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Berumen ML, Pratchett MS (2006) Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647–653

    Article  Google Scholar 

  • Bourne DG (2005) Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24:304–312

    Article  Google Scholar 

  • Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562

    Article  PubMed  CAS  Google Scholar 

  • Brodie JE, Kroon FJ, Schaffelke B, Wolanski EC, Lewis SE, Devlin MJ, Bainbridge ZT, Waterhouse J, Davis AM (2011) Terrestrial pollutant runoff to the Great Barrier Reef: An update on issues, priorities and management responses. Mar Pollut Bull 65:81–100

    Article  Google Scholar 

  • Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2(8):e711. doi:10.1371/journal.pone.0000711

    Article  PubMed  Google Scholar 

  • 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 5:1220–1227

    Article  CAS  Google Scholar 

  • Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68:1592–1605

    Article  Google Scholar 

  • Croquer A, Weil E (2009) Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. II. Genera-level analysis. Dis Aquat Org 83:209–222

    Article  PubMed  Google Scholar 

  • De’ath G, Fabricius K (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850

    Article  PubMed  Google Scholar 

  • Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Natl Acad Sci USA 104:5483–5488

    Article  PubMed  CAS  Google Scholar 

  • Emslie MJ, Cheal AJ, Sweatman H, Delean S (2008) Recovery from disturbance of coral and reef fish communities on the Great Barrier Reef, Australia. Mar Ecol Prog Ser 371:177–190

    Article  Google Scholar 

  • English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Australia

    Google Scholar 

  • GBRMPA (2009) Great Barrier Reef Outlook Report 2009. GBRMPA, Townsville, p 211

    Google Scholar 

  • Guzman HM, Cortes J (2007) Reef recovery 20 years after the 1982–1983 El Nino massive mortality. Mar Biol 151:401–411

    Article  Google Scholar 

  • Haapkyla J, Unsworth RKF, Seymour AS, Melbourne-Thomas J, Flavell M, Willis BL, Smith DJ (2009) Spatio-temporal coral disease dynamics in the Wakatobi Marine National Park, South-East Sulawesi, Indonesia. Dis Aquat Org 87:105–115

    Article  PubMed  Google Scholar 

  • Haapkyla J, Melbourne-Thomas J, Flavell M, Willis BL (2010) Spatiotemporal patterns of coral disease prevalence on Heron Island, Great Barrier Reef, Australia. Coral Reefs 29:1035–1045

    Article  Google Scholar 

  • Haapkyla J, Unsworth RKF, Flavell M, Bourne DG, Schaffelke B, Willis BL (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS ONE 6(2):e16893

    Article  PubMed  CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Ecology - Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  PubMed  CAS  Google Scholar 

  • Harvell CD, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis BL (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195

    Article  Google Scholar 

  • 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(8):e12210

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2007) Working group 1 report: the physical science basis., Cambridge, UK

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  PubMed  CAS  Google Scholar 

  • Jones RJ, Bowyer J, Hoegh-Guldberg O, Blackall LL (2004) Dynamics of a temperature-related coral disease outbreak. Mar Ecol Prog Ser 281:63–77

    Article  Google Scholar 

  • Kaczmarsky LT (2006) Coral disease dynamics in the central Philippines. Dis Aquat Org 69:9–21

    Article  PubMed  Google Scholar 

  • Larcombe P, Ridd PV, Prytz A, Wilson B (1995) Factors controlling suspended sediment on inner-shelf coral reefs, Townsville, Australia. Coral Reefs 14:163–171

    Article  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McClanahan TR, Ateweberhan M, Muhando CA, Maina J, Mohammed MS (2007) Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecol Monogr 77:503–525

    Article  Google Scholar 

  • Miller I (1996) Black band disease on the Great Barrier Reef. Coral Reefs 15:58

    Google Scholar 

  • Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B (2009) Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28:925–937

    Article  Google Scholar 

  • 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 27:191–195

    Article  Google Scholar 

  • Osborne K, Dolman AM, Burgess SC, Johns KA (2011) Disturbance and the dynamics of coral cover on the Great Barrier Reef (1995–2009). PLoS ONE 6(3):e17516. doi:10.1371/journal.pone.0017516

    Article  PubMed  CAS  Google Scholar 

  • Page CA (2009) Ecology and biology of coral disease on the Great Barrier Reef. Ph.D. thesis, James Cook University, Townsville, Australia, p 201

  • 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

    Article  Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Causes of coral reef degradation - Response. Science 302:1502–1503

    CAS  Google Scholar 

  • Porter JW, Dustan P, Jaap WC, Patterson KL, Kosmynin V, Meier OW, Patterson ME, Parsons M (2001) Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 460:1–24

    Article  Google Scholar 

  • Raymundo LJ, Rosell KB, Reboton CT, Kaczmarsky L (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis Aquat Org 64:181–191

    Article  PubMed  Google Scholar 

  • Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14

    Article  CAS  Google Scholar 

  • Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326

    Article  PubMed  Google Scholar 

  • 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 Biol Sci Ser B 276:2795–2803

    Article  Google Scholar 

  • Selig ER, Harvell CD, Bruno JF, Willis B, Page CA, Casey KS, Sweatman H (2006) Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney JT, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. American Geophysical Union, Washington, DC, pp 111–128

    Chapter  Google Scholar 

  • Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Org 87:5–18

    Article  PubMed  Google Scholar 

  • Thompson AA, Dolman AM (2010) Coral bleaching: one disturbance too many for near-shore reefs of the Great Barrier Reef. Coral Reefs 29:637–648

    Article  Google Scholar 

  • Trenberth KE (1998) Atmospheric moisture residence times and cycling: Implications for rainfall rates and climate change. Clim Change 39:667–694

    Article  Google Scholar 

  • Vargas-Angel B (2009) Coral health and disease assessment in the US Pacific remote island areas. Bull Mar Sci 84:211–227

    Google Scholar 

  • Veron JEN, Hoegh-Guldberg O, Lenton TM, Lough JM, Obura DO, Pearce-Kelly P, Sheppard CRC, Spalding M, Stafford-Smith MG, Rogers AD (2009) The coral reef crisis: The critical importance of < 350 ppm CO2. Mar Pollut Bull 58:1428–1436

    Article  PubMed  CAS  Google Scholar 

  • Weil E (2004) Coral reef diseases in the wider Caribbean. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, pp 35–68

    Chapter  Google Scholar 

  • Whelan KRT, Miller J, Sanchez O, Patterson M (2007) Impact of the 2005 coral bleaching event on Porites porites and Colpophyllia natans at Tektite Reef, US Virgin Islands. Coral Reefs 26:689–693

    Article  Google Scholar 

  • Williams GJ, Knapp IS, Work TM, Conklin EJ (2011) Outbreak of Acropora white syndrome following a mild bleaching event at Palmyra Atoll, Northern Line Islands, Central Pacific. Coral Reefs 30:621

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Wobeser GA (2006) Essentials of disease in wild animals. Wiley-Blackwell, Oxford, UK

    Google Scholar 

  • Wooldridge SA (2009) Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751

    Article  PubMed  CAS  Google Scholar 

  • Work TM, Aeby GS (2006) Systematically describing gross lesions in corals. Dis Aquat Org 70:155–160

    Article  PubMed  Google Scholar 

  • Work TM, Richardson LL, Reynolds TL, Willis BL (2008) Biomedical and veterinary science can increase our understanding of coral disease. J Exp Mar Biol Ecol 362:63–70

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank the James Cook University, AIMS@JCU and the Australian Research Council (ARC) for providing funding for this study. We are very grateful to numerous volunteers that helped with fieldwork and to the X-Base Backpackers on Magnetic Island for logistical support during our surveys.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Haapkylä.

Additional information

Communicated by Biology Editor Dr. Hugh Sweatman

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haapkylä, J., Melbourne-Thomas, J., Flavell, M. et al. Disease outbreaks, bleaching and a cyclone drive changes in coral assemblages on an inshore reef of the Great Barrier Reef. Coral Reefs 32, 815–824 (2013). https://doi.org/10.1007/s00338-013-1029-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-013-1029-x

Keywords

Navigation