Abstract
Understanding environmental drivers of black band disease (BBD), a virulent disease affecting corals worldwide, is critical to managing coral populations. Field monitoring studies have implicated seasonally elevated temperature and light as drivers of annual BBD outbreaks on the Great Barrier Reef, but do not distinguish their relative impacts. Here, we compare progression of BBD lesions on Montipora hispida among three controlled temperature (28.0, 29.0, 30.5°C) and two controlled light treatments (170, 440 μmol m−2 s−1) within normal seasonal ranges at the site. BBD progression rates were greatest (5.2 mm d−1) in the 30.5°C/high-light treatment and least (3.2 mm d−1) in the 28°C/low-light treatment. High light significantly enhanced BBD progression, whereas increases in disease progression under high temperatures were not statistically significant, identifying the greater role of light in driving BBD dynamics within the temperature range examined. Greater BBD progression during daytime compared with nighttime (by 2.2–3.6-fold across temperature and light treatments) corroborates our conclusion that light is the pre-eminent factor driving BBD progression at typical summer temperatures. Decreased photochemical efficiency of algal endosymbionts in the high-temperature/high-light treatments suggests that compromised health of the coral holobiont contributes to enhanced disease progression, highlighting the complexity of disease dynamics in host–pathogen systems responding to environmental changes.
References
Al-Moghrabi SM (2001) Unusual black band disease (BBD) outbreak in the northern tip of the Gulf of Aqaba (Jordan). Coral Reefs 19:330–331
Antonius A (1981) The ‘band’ diseases in coral reefs. Proc 4th Int Coral Reef Symp 2:7-14
Arotsker L, Siboni N, Ben-Dov E, Kramarsky-Winter E, Loya Y, Kushmaro A (2009) Vibrio sp. as a potentially important member of the Black Band Disease (BBD) consortium in Favia sp. corals. FEMS Microbiol Ecol 70:183–192
Barneah O, Ben-Dov E, Kramarsky-Winter E, Kushmaro A (2007) Characterization of black band disease in Red Sea stony corals. Environ Microbiol 9:1995–2006
Borger JL (2005) Scleractinian coral diseases in south Florida: incidence, species susceptibility, and mortality. Dis Aquat Org 67:249–258
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 151:1711–1720
Bruckner AW, Bruckner RJ (1997) The persistence of black-band disease in Jamaica: impact on community structure. Proc 8th Int Coral Reef Symp 1:601-606
Bruckner AW, Bruckner RJ, Williams EH (1997) Spread of a black-band disease epizootic through the coral reef system in St Ann’s Bay, Jamaica. Bull Mar Sci 61:919–928
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
Carlton RG, Richardson LL (1995) Oxygen and sulfide dynamics in a horizontally migrating cyanobacterial mat - Black band disease of corals. FEMS Microbiol Ecol 18:155–162
Cooney RP, Pantos O, Tissier MDAL, Barer MR, O’Donnell AG, Bythell JC (2002) Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques. Environ Microbiol 4:401–413
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
Edmunds PJ (1991) Extent and effect of black band disease on a Caribbean reef. Coral Reefs 10:161–165
Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65
Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68:2214–2228
Frias-Lopez J, Klaus JS, Bonheyo GT, Fouke BW (2004) Bacterial community associated with black band disease in corals. Appl Environ Microbiol 70:5955–5962
Gantar M, Sekar R, Richardson L (2009) Cyanotoxins from black band disease of corals and from other coral reef environments. Microb Ecol 58:856–864
Glas M, Motti CA, Negri A, Sato Y, Froscio S, Humpage AR, Krock B, Cembella A, Bourne DG (2010) Cyanotoxins are not implicated in the etiology of coral black band disease outbreaks on Pelorus Island, Great Barrier Reef. FEMS Microbiol Ecol 73:43–54
Gochfeld DJ, Aeby GS (2008) Antibacterial chemical defenses in Hawaiian corals provide possible protection from disease. Mar Ecol Prog Ser 362:119–128
Gochfeld DJ, Olson JB, Slattery M (2006) Colony versus population variation in susceptibility and resistance to dark spot syndrome in the Caribbean coral Siderastrea siderea. Dis Aquat Org 69:53–65
Green EP, Bruckner AW (2000) The significance of coral disease epizootiology for coral reef conservation. Biol Conserv 96:347–361
Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus A, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Review: Marine ecology - Emerging marine diseases - Climate links and anthropogenic factors. Science 285:1505–1510
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
Hildemann WH, Raison RL, Cheung G, Hull CJ, Akaka L, Okamoto J (1977) Immunological specificity and memory in a scleractinian coral. Nature 270:219–223
Jones RJ (2004) Testing the ‘photoinhibition’ model of coral bleaching using chemical inhibitors. Mar Ecol Prog Ser 284:133–145
Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: Photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Env 24:89–99
Jones RJ, Kerswell AP (2003) Phytotoxicity of Photosystem II (PSII) herbicides to coral. Mar Ecol Prog Ser 261:149–159
Kaczmarsky LT (2006) Coral disease dynamics in the central Philippines. Dis Aquat Org 69:9–21
Kaczmarsky LT, Draud M, Williams EH (2005) Is there a relationship between proximity to sewage effluent and the prevalence of coral disease? Caribb J Sci 41:124–137
Koh EGL (1997) Do scleractinian corals engage in chemical warfare against microbes? J Chem Ecol 23:379–398
Kuta KG, Richardson LL (1996) Abundance and distribution of black band disease on coral reefs in the northern Florida Keys. Coral Reefs 15:219–223
Kuta KG, Richardson LL (1997) Black band disease and the fate of diseased coral colonies in the Florida Keys. Proc 8th Int Coral Reef Symp 1:575-578
Kuta KG, Richardson LL (2002) Ecological aspects of black band disease of corals: relationships between disease incidence and environmental factors. Coral Reefs 21:393–398
Lesser MP, Gorbunov MY (2001) Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Mar Ecol Prog Ser 212:69–77
Manzello D, Warner M, Stabenau E, Hendee J, Lesser M, Jankulak M (2009) Remote monitoring of chlorophyll fluorescence in two reef corals during the 2005 bleaching event at Lee Stocking Island, Bahamas. Coral Reefs 28:209–214
McClanahan TR, Weil E, Maina J (2009) Strong relationship between coral bleaching and growth anomalies in massive Porites. Global Change Biol 15:1804–1816
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 87:67–78
Mydlarz LD, McGinty ES, Drew Harvell C (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945
Myers JL, Richardson LL (2009) Adaptation of cyanobacteria to the sulfide-rich microenvironment of black band disease of coral. FEMS Microbiol Ecol 67:242–251
Myers JL, Sekar R, Richardson LL (2007) Molecular detection and ecological significance of the cyanobacterial genera Geitlerinema and Leptolyngbya in black band disease of corals. Appl Environ Microbiol 73:5173–5182
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
Palmer CV, Mydlarz LD, Willis BL (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc R Soc B Biol Sci 275:2687–2693
Palmer CV, Roth MS, Gates RD (2009) Red fluorescent protein responsible for pigmentation in trematode-infected Porites compressa tissues. Biol Bull 216:68–74
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) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958
Porter JW, Meier OW (1992) Quantification of loss and change in Floridian reef coral populations. Am Zool 32:625–640
Reed KC, Muller EM, Van Woesik R (2010) Coral immunology and resistance to disease. Dis Aquat Org 90:85–92
Richardson LL (1996) Horizontal and vertical migration patterns of Phormidium corallyticum and Beggiatoa spp. associated with black-band disease of corals. Microb Ecol 32:323–335
Richardson LL (2004) Black band disease. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Heidelberg, pp 325–336
Richardson LL, Kuta KG (2003) Ecological physiology of the black band disease cyanobacterium Phormidium corallyticum. FEMS Microbiol Ecol 43:287–298
Richardson LL, Kuta KG, Schnell S, Carlton RG (1997) Ecology of the black band disease microbial consortium. Proc 8th Int Coral Reef Symp 1:597-600
Richardson LL, Sekar R, Myers JL, Gantar M, Voss JD, Kaczmarsky L, Remily ER, Boyer GL, Zimba PV (2007) The presence of the cyanobacterial toxin microcystin in black band disease of corals. FEMS Microbiol Lett 272:182–187
Richardson LL, Miller AW, Broderick E, Kaczmarsky L, Gantar M, Stanic D, Sekar R (2009) Sulfide, microcystin, and the etiology of black band disease. Dis Aquat Org 87:79–90
Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Rodriguez S, Croquer A (2008) Dynamics of black band disease in a Diploria strigosa population subjected to annual upwelling on the northeastern coast of Venezuela. Coral Reefs 27:381–388
Roff G, Ulstrup KE, Fine M, Ralph PJ, Hoegh-Guldberg O (2008) Spatial heterogeneity of photosynthetic activity within diseased corals from the Great Barrier Reef. J Phycol 44:526–538
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 B Biol Sci 276:2795–2803
Sato Y, Willis BL, Bourne DG (2010) Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME J 4:203–214
Sekar R, Kaczmarsky LT, Richardson LL (2008) Microbial community composition of black band disease on the coral host Siderastrea siderea from three regions of the wider Caribbean. Mar Ecol Prog Ser 362:85–98
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
Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302
Viehman TS, Richardson LL (2002) Motility patterns of Beggiatoa and Phormidium corallyticum in black band disease. Proc 9th Int Coral Reef Symp 2:1251-1255
Voss JD, Richardson LL (2006) Coral diseases near Lee Stocking Island, Bahamas: Patterns and potential drivers. Dis Aquat Org 69:33–40
Voss JD, Mills DK, Myers JL, Remily ER, Richardson LL (2007) Black band disease microbial community variation on corals in three regions of the wider Caribbean. Microb Ecol 54:730–739
Weil E, Croquer A (2009) Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. I. Community-level analysis. Dis Aquat Org 83:195–208
Williams GJ, Aeby GS, Cowie ROM, Davy SK (2010) Predictive modeling of coral disease distribution within a reef system. PLoS ONE 5:e9264
Winters G, Loya Y, Beer S (2006) In situ measured seasonal variations in Fv/Fm of two common Red Sea corals. Coral Reefs 25:593–598
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
Zvuloni A, Artzy-Randrup Y, Stone L, Kramarsky-Winter E, Barkan R, Loya Y (2009) Spatio-temporal transmission patterns of black-band disease in a coral community. PLoS ONE 4
Acknowledgments
This study was funded by an Australian Research Council grant to B. Willis administered through the Australian Research Council Centre of Excellence for Coral Reef Studies and by the Disease Working Group in the Coral Reef Targeted Research and Capacity Building for Management Program, and was supported logistically by AIMS@JCU. Authors thank staff of James Cook University’s Orpheus Island Research Station for their logistic support, D. Abrego, E. Puill-Stephan, Y. Zhang, E. Graham, J. Plass-Johnson, and D. Bayley for their support in experimental and field work.
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Sato, Y., Bourne, D.G. & Willis, B.L. Effects of temperature and light on the progression of black band disease on the reef coral, Montipora hispida . Coral Reefs 30, 753–761 (2011). https://doi.org/10.1007/s00338-011-0751-5
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DOI: https://doi.org/10.1007/s00338-011-0751-5