Abstract
Coral disease is a growing problem for reef corals and a primary driver of reef degradation. Incidences of coral disease on the Great Barrier Reef (GBR) are increasing; however, our understanding of differences among species in their potential for contracting disease is poor. In this study, we integrate observations of coral disease on the GBR from the primary literature as well as morphological, ecological and biogeographical traits of coral species that have been hypothesised to influence “disease potential.” Most of the examined traits influence species’ disease potential when considered alone. However, when all traits are analysed together, diversity of predators, geographical range size and characteristic local abundance are the primary predictors of disease potential. Biases associated with species’ local abundance and phylogeny are tested but do not overpower relationships. This large-scale macroecological evaluation of coral disease provides insights into species-level traits that drive disease susceptibility.
References
Aeby G, Santavy D (2006) Factors affecting susceptibility of the coral Montastraea faveolata to black-band disease. Mar Ecol Prog Ser 318:103–110
Antonius A, Lipscomb D (2001) First protozoan coral-killer identified in the Indo-Pacific. Atoll Res Bull 481:1–21
Antonius A, Riegl B (1997) A possible link between coral disease and a corallivorous snail (Drupella cornus) outbreak in the Red Sea. Atoll Res Bull 447:2–9
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141
Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Syst 40:551–571
Broström G (2009) glmmML: generalized linear models with clustering: a maximum likelihood and bootstrap approach to mixed models. R Development Core Team
Bruno J, Selig E (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 8:e711, 1–8
Bruno J, Petes L, Harvell D, Hettinger A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–1061
Bruno J, Selig E, Casey K, Page C, Willis B, Harvell D, Sweatman H, Melendy A (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology 5:e124, 1220–1227
Carpenter KE, Abrar M, Aeby G, Aronson R, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek C, DeVantier L, Edgar G, Edwards A, Fenner D, Guzmán H, Hoeksema B, Hodgson G, Johan O, Licuanan W, Livingstone S, Lovell E, Moore J, Obura D, Ochavillo D, Polidoro B, Precht W, Quibilan M, Reboton C, Richards Z, Rogers A, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron J, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevate extinction risk from climate change and local impacts. Science 321:560–563
Chamberlain JA (1978) Mechanical properties of coral skeleton: compressive strength and its adaptive significance. Paleobiology 4:419–435
Cole AJ, Chong Seng KM, Pratchett MS, Jones GP (2009) Coral-feeding fishes slow progression of black band disease. Coral Reefs 28:965
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: reviews and synthesis. Mar Pollut Bull 50:125–146
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Francini-Filho R, Moura R, Thompson F, Reis R, Kaufman L, Kikuchi R, Leão Z (2008) Diseases leading to accelerated decline of reef corals in the largest South Atlantic reef complex (Albrolhos Bank, eastern Brazil). Mar Pollut Bull 56:1008–1014
Frias-Lopez J, Bonheyo G, Fouke B (2003) Cyanobacteria associated with coral black band disease in Caribbean and Indo-Pacific reefs. Appl Environ Microbiol 69:2409–2413
Gardner T, Coté I, Gill J, Grant A, Watkinson A (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Glynn PW, Colley NJ (2008) Survival of brooding and broadcasting reef corals following large scale disturbances: is there any hope for broadcasting species during global warming. Proc 11th Int Coral Reef Symp: 361–365
Hughes T, Baird A, Bellwood D, Card M, Connolly S, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson BC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933
Jackson JBC (1979) Morphological strategies of sessile animals. In: Larwood G, Rosen BR (eds) Biology and systematics of colonial organisms. Academic Press, New York, pp 499–555
Jones R, Bowyer J, Hoegh-Guldberg O, Blackall L (2004) Dynamics of a temperature-related coral disease outbreak. Mar Ecol Prog Ser 281:63–77
Jovani R, Serrano D (2001) Feather mites (Astigmata) avoid moulting wing feathers of passerine birds. Anim Behav 62:723–727
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics (in press)
Kerr AM (2005) Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biol Rev 80:543–558
Krackow S, Tkadlec E (2001) Analysis of brood sex ratios: implications of offspring clustering. Behav Ecol Sociobiol 50:293–301
Kuta KG, Richardson L (1996) Abundance and distribution of black band disease on coral reefs in the northern Florida Keys. Coral Reefs 15:219–223
Lesser M (2004) Experimental biology of coral reef ecosystems. J Exp Mar Biol Ecol 300:217–252
Lesser M, Bythell J, Gates R, Johnstone R, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Biol Ecol 346:36–44
Lirman D, Manzello D (2009) Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. J Exp Mar Biol Ecol 369:72–77
Mumby P, Steneck R (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563
Nakamura T, van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304
Nugues MM, Bak RP (2009) Brown-band syndrome on feeding scars of the crown-of-thorn starfish Acanthaster planci. Coral Reefs 28:507–510
Page C, Willis B (2006) Distribution, host range and large-scale spatial variability in black band disease prevalence on the Great Barrier Reef, Australia. Dis Aquat Org 69:41–51
Page C, Willis B (2008) Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation if this widespread coral disease. Coral Reefs 27:257–272
Palmer CV, Mydlarz LD, Willis B (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc R Soc Lond B Biol Sci 275:2687–2693
Pandolfi J, Bradbury R, Sala E, Hughes T, Bjorndal K, Cooke R, McArdle D, McClenachan L, Newman M, Paredes G, Warner R, Jackson J (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer, New York
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
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
Richardson L (1998) Coral diseases: what is really known? Trends Ecol Evol 13:438–443
Rotjan R, Lewis S (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91
Selig E, Harvell D, Bruno J, Willis B, Page C, Casey K, Sweatman H (2006) Analyzing the relationships between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney J, 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
Sofonia J, Anthony K (2008) High- sediment tolerance in reef coral Turbinaria mesenterina from the inner Great Barrier Reef lagoon (Australia). Estuar Coast Shelf Sci 78:748–752
Soong K, Lang JC (1992) Reproductive integration in reef corals. Biol Bull 183:418–431
Sutherland K, Porter J, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302
Ulstrup K, Kühl M, Bourne D (2007) Zooxanthellae harvested by ciliates associated with brown band syndrome of corals remain photosynthetically competent. Appl Environ Microbiol 73:1968–1975
Venables WN, Ripley BD (2002) Modern applied statistics with S. Fourth Edition. Springer, New York
Veron JEN (1986) Corals of Australia and the Indo-Pacific. University of Hawaii Press, Honolulu
Veron JEN, Pichon M (1976) Scleractinia of eastern Australia. Part I. Families Thamnasteriidae, Astrocoeniidae, Pocilloporidae. Australian Government Publishing Service, Canberra
Veron JEN, Pichon M (1980) Scleractinia of eastern Australia. Part III. Families Agariciidae,Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophyllidae, Dendrophyliidae. Australian Institute of Marine Science in association with Australian National University Press, Canberra
Veron JEN, Stafford-Smith M (2002) Coral ID. Australian Institute of Marine Science and CCR Qld Pty Ltd
Veron JEN, Pichon M, Wijsman-Best M (1977) Scleractinia of eastern Australia. Part II. Families Faviidae, Trachyphylliidae. Australian Government Publishing Service, Canberra
Wallace C (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO Publishing, Collingwood
Willis B, Page C, Dinsdale E (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 69–104
Work T, Richardson L, Reynolds T, Willis B (2008) Biomedical and veterinary science can increase our understanding of coral disease. J Exp Mar Biol Ecol 362:63–70
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgments
We thank the Juan Armando Sánchez for helpful input about conducting the phylogenetic analysis. We thank the Andrew Allen and Melanie Bishop for analytical advice, and Andrew Baird, Simon Davy, and three anonymous reviewers for insightful manuscript reviews. The study was supported by an Australian Research Council Discovery Project grant to JSM (DP0987892).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Andrew Baird
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Díaz, M., Madin, J. Macroecological relationships between coral species’ traits and disease potential. Coral Reefs 30, 73–84 (2011). https://doi.org/10.1007/s00338-010-0668-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-010-0668-4