Coral Reefs

, Volume 32, Issue 3, pp 815–824 | Cite as

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

  • J. Haapkylä
  • J. Melbourne-Thomas
  • M. Flavell
  • B. L. Willis
Report

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.

Keywords

Coral disease dynamics Disturbance Atramentous necrosis Coral bleaching Cyclone ‘Yasi’ Disease susceptibility 

Notes

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.

References

  1. 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 91:1–8PubMedCrossRefGoogle Scholar
  2. Ainsworth TD, Hoegh-Guldberg O (2008) Cellular processes of bleaching in the Mediterranean coral Oculina patagonica. Coral Reefs 27:593–597CrossRefGoogle Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UKGoogle Scholar
  5. 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 81:255–259PubMedCrossRefGoogle Scholar
  6. 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
  7. Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38CrossRefGoogle Scholar
  8. 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, MelbourneGoogle Scholar
  9. Bellwood DR, Hughes TP (2001) The state of coral reef science - Response. Science 293:1997CrossRefGoogle Scholar
  10. Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833PubMedCrossRefGoogle Scholar
  11. 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
  12. 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 25:647–653CrossRefGoogle Scholar
  13. Bourne DG (2005) Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24:304–312CrossRefGoogle Scholar
  14. Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562PubMedCrossRefGoogle Scholar
  15. 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 65:81–100CrossRefGoogle Scholar
  16. 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 PubMedCrossRefGoogle Scholar
  17. 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 5:1220–1227CrossRefGoogle Scholar
  18. Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68:1592–1605CrossRefGoogle Scholar
  19. 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 83:209–222PubMedCrossRefGoogle Scholar
  20. De’ath G, Fabricius K (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850PubMedCrossRefGoogle Scholar
  21. 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 104:5483–5488PubMedCrossRefGoogle Scholar
  22. 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 371:177–190CrossRefGoogle Scholar
  23. English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, AustraliaGoogle Scholar
  24. GBRMPA (2009) Great Barrier Reef Outlook Report 2009. GBRMPA, Townsville, p 211Google Scholar
  25. Guzman HM, Cortes J (2007) Reef recovery 20 years after the 1982–1983 El Nino massive mortality. Mar Biol 151:401–411CrossRefGoogle Scholar
  26. 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 87:105–115PubMedCrossRefGoogle Scholar
  27. 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 29:1035–1045CrossRefGoogle Scholar
  28. 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):e16893PubMedCrossRefGoogle Scholar
  29. 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 296:2158–2162PubMedCrossRefGoogle Scholar
  30. 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 20:172–195CrossRefGoogle Scholar
  31. 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):e12210PubMedCrossRefGoogle Scholar
  32. 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 318:1737–1742PubMedCrossRefGoogle Scholar
  33. Intergovernmental Panel on Climate Change (IPCC) (2007) Working group 1 report: the physical science basis., Cambridge, UKGoogle Scholar
  34. 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 293:629–638PubMedCrossRefGoogle Scholar
  35. 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
  36. Kaczmarsky LT (2006) Coral disease dynamics in the central Philippines. Dis Aquat Org 69:9–21PubMedCrossRefGoogle Scholar
  37. Larcombe P, Ridd PV, Prytz A, Wilson B (1995) Factors controlling suspended sediment on inner-shelf coral reefs, Townsville, Australia. Coral Reefs 14:163–171CrossRefGoogle Scholar
  38. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  39. 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 77:503–525CrossRefGoogle Scholar
  40. Miller I (1996) Black band disease on the Great Barrier Reef. Coral Reefs 15:58Google Scholar
  41. 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 28:925–937CrossRefGoogle Scholar
  42. 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
  43. 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 PubMedCrossRefGoogle Scholar
  44. Page CA (2009) Ecology and biology of coral disease on the Great Barrier Reef. Ph.D. thesis, James Cook University, Townsville, Australia, p 201Google Scholar
  45. 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 27:257–272CrossRefGoogle Scholar
  46. 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 302:1502–1503Google Scholar
  47. 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 460:1–24CrossRefGoogle Scholar
  48. Raymundo LJ, Rosell KB, Reboton CT, Kaczmarsky L (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis Aquat Org 64:181–191PubMedCrossRefGoogle Scholar
  49. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  50. Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326PubMedCrossRefGoogle Scholar
  51. 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 276:2795–2803CrossRefGoogle Scholar
  52. 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 111–128CrossRefGoogle Scholar
  53. 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
  54. Thompson AA, Dolman AM (2010) Coral bleaching: one disturbance too many for near-shore reefs of the Great Barrier Reef. Coral Reefs 29:637–648CrossRefGoogle Scholar
  55. Trenberth KE (1998) Atmospheric moisture residence times and cycling: Implications for rainfall rates and climate change. Clim Change 39:667–694CrossRefGoogle Scholar
  56. Vargas-Angel B (2009) Coral health and disease assessment in the US Pacific remote island areas. Bull Mar Sci 84:211–227Google Scholar
  57. 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 58:1428–1436PubMedCrossRefGoogle Scholar
  58. Weil E (2004) Coral reef diseases in the wider Caribbean. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, pp 35–68CrossRefGoogle Scholar
  59. 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 26:689–693CrossRefGoogle Scholar
  60. 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 30:621CrossRefGoogle Scholar
  61. 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
  62. Wobeser GA (2006) Essentials of disease in wild animals. Wiley-Blackwell, Oxford, UKGoogle Scholar
  63. 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 58:745–751PubMedCrossRefGoogle Scholar
  64. Work TM, Aeby GS (2006) Systematically describing gross lesions in corals. Dis Aquat Org 70:155–160PubMedCrossRefGoogle Scholar
  65. 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 362:63–70CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • J. Haapkylä
    • 1
    • 2
  • J. Melbourne-Thomas
    • 3
  • M. Flavell
    • 1
  • B. L. Willis
    • 1
  1. 1.School of Marine and Tropical Biology, and ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.AIMS@JCUTownsvilleAustralia
  3. 3.Antarctic Climate and Ecosystems Cooperative Research CentreUniversity of TasmaniaHobartAustralia

Personalised recommendations