Incidence of lesions on fungiidae corals in the eastern Red Sea is related to water temperature and coastal pollution

Marine Environmental Research

Volumn 98, Issue , 2014, Pages 29-38

  Furby, K A ^a,b   Apprill, A ^a   Cervino, J M ^a   Ossolinski, J E ^a   Hughen, K A ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Climate change; Marine ecology; Microbes; Nutrients; Saudi Arabia; Scleractinia

Indexed keywords

CLIMATE CHANGE; MARINE BIOLOGY; MARINE POLLUTION; MICROORGANISMS; SEAWATER; WATER QUALITY;

ELEVATED CONCENTRATIONS; MARINE ECOLOGY; MICROBES; MICROBIAL COMMUNITIES; SAUDI ARABIA; SCLERACTINIA; SEA SURFACE TEMPERATURE (SST); SEAWATER TEMPERATURE;

NUTRIENTS;

AMMONIA; SEA WATER; WATER POLLUTANT;

BIOGEOCHEMISTRY; CLIMATE CHANGE; CORAL; ETIOLOGY; LESION; MARINE ECOSYSTEM; MARINE POLLUTION; MICROBIAL COMMUNITY; NUTRIENT; SEAWATER; WATER QUALITY; WATER TEMPERATURE;

AQUACULTURE; ARTICLE; BIOGEOCHEMISTRY; CORAL; FUNGIIDAE; MICROBIAL COMMUNITY; NONHUMAN; NUTRIENT; SAUDI ARABIA; SEA POLLUTION; SEA SURFACE TEMPERATURE; URBAN AREA; WATER QUALITY; ANIMAL; ANTHOZOA; CHEMISTRY; INDIAN OCEAN; MICROBIOLOGY; REGRESSION ANALYSIS; TEMPERATURE; URBAN POPULATION; WATER POLLUTANT;

INDIAN OCEAN; JEDDAH; MAKKAH [SAUDI ARABIA]; RED SEA [INDIAN OCEAN]; SAUDI ARABIA;

ANIMALS; ANTHOZOA; INDIAN OCEAN; REGRESSION ANALYSIS; SAUDI ARABIA; SEAWATER; TEMPERATURE; URBAN POPULATION; WATER POLLUTANTS; WATER QUALITY;

EID: 84900399227     PISSN: 01411136     EISSN: 18790291     Source Type: Journal    
DOI: 10.1016/j.marenvres.2014.04.002     Document Type: Article

References (75)

1. Acker J.G., Leptoukh G. Online analysis enhances use of NASA earth science data. Eos, Trans. Am. Geophys. Union 2007, 88:17.
2. Acosta A. Disease in zoanthids: dynamics in space and time. Hydrobiologia 2001, 460:113-130.
3. Alker A.P., Smith G.W., Kim K. Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiologia 2001, 460:105-111.
4. Antonius A. Human impact on corals in fringing reefs near Jeddah, Red Sea. Proceedings Symposium Coral Reef. Environ. Red. Sea Jeddah 1984, 363-389.
5. Apprill A., Rappé M.S. Response of the microbial community to coral spawning in lagoon and reef flat environments of Hawaii, USA. Aquat. Microb. Ecol. 2011, 62:251-266.
6. Apprill A., Hughen K., Mincer T. Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ. Microbiol. 2013, 15:2063-2072.
7. Armstrong F.A.J., Stearns C.R., Strickland J.D.H. The measurement of upwelling and subsequent biological processes by means of the Technicon AutoAnalyzer and associated equipment. Deep-Sea Res. 1967, 14:381-389.
8. Ben-Haim Y., Thompson F.L., Thompson C.C., Cnockaert M.C., Hoste B., Swings J., Rosenberg E. Vibrio coralliilyticus sp. nov., a temperature- dependent pathogen of the coral Pocillopora damicornis. Int. J. Syst. Evol. Microbiol. 2003, 53:309-315.
9. Ben-Haim Y., Zicherman-Keren M., Rosenberg E. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol. 2003, 69:4236-4242.
10. Bernhardt H., Wilhelms A. The continuous determination of low-level iron, soluble phosphate and total phosphate with the Autoanalyzer. Technicon Symposia. Mediad Inc.: New York 1967, 385-389.
11. Berumen M.L., Hoey A.S., Bass W.H., Bouwmeester J., Catania D., Cochran J.E.M., Khalil M.T., Miyake S., Mughal M.R., et al. The status of coral reef ecology research in the Red Sea. Coral Reefs 2013, 10.1007/s00338-013-1055-8.
12. Bongaerts P., Hoeksema B.W., Hay K.B., Hoegh-Guldbery O. Mushroom corals overcome live burial through pulsed inflation. Coral Reefs 2012, 31:399.
13. Brown O.B., Minnett P.J. MODIS Infrared Sea Surface Temperature Algorithm Theoretical Basis Document, Ver 2.0 1999, http://modis.gsfc.nasa.gov/data/atbd/atbd_mod25.pdf.
14. Brugère C., Ridler N. Global Aquaculture Outlook in the Next Decades: an Analysis of National Aquaculture Production Forecasts to 2030 2004, FAO Fisheries Circular. No. 1001, Rome, FAO.
15. Bruno J.F., Petes L.E., Harvell C.D., Hettinger A. Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 2003, 6:1056-1061.
16. Bruno J.F., Selig E.R., Casey K.S., Page C.A., Willis B.L., et al. Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol. 2007, 5:e124. 10.1371/journal.pbio.0050124.
17. Central Department of Statistics, Kingdom of Saudi Arabia. (accessed 03.30.14.). http://www.citypopulation.de/SaudiArabia.html.
18. Cervino J.M., Hayes R., Polson S., Polson S.C., Goreau T.J., Martinez R.J., Smith G.W. Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Appl. Environ. Microbiol. 2004, 70:6855-6864.
19. Cervino J.M., Hayes R., Goreau T.J., Smith G.W. Zooxanthellae regulation in yellow blotch/band and other coral disease contrasted with temperature-related bleaching: in situ destruction vs expulsion. Symbiosis 2004, 37:63-85.
20. Cervino J.M., Thompson F.L., Gomez-Gil B., Lorence E.A., Goreau T.J., Hayes R.L., Winiarski-Cervino K.B., Smith G.W., Hughen K., Bartels E. The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. J. App. Microbiol. 2008, 105:1658-1671.
21. Cervino J.M., Hauff B., Haslun J.A., Winiarski-Cervino K., Cavazos M., Lawther P., Wier A.M., Hughen K., Strychar K.B. Ulcerated yellow spot syndrome: implications of aquaculture-related pathogens associated with soft coral Sarcophyton ehrenbergi tissue lesions. Dis. Aq. Org. 2012, 102:137-148.
22. Chadwick N. Competition and locomotion in free-living fungiid coral. J. Exp. Mar. Biol. Ecol. 1988, 123:189-200.
23. Chadwick-Furman N., Loya Y. Migration, habitat use, and competition among mobile corals (Scleractinia: Fungiidae) in the Gulf of Eilat, Red Sea. Mar. Biol. 1992, 114:617-623.
24. Cox E.F., Ribes M., Kinzie R.A. Temporal and spatial scaling of planktonic responses to nutrient inputs into a subtropical embayment. Mar. Ecol. Prog. Ser. 2006, 324:19-35.
25. Dinsdale E.A., Pantos O., Smriga S., Edwards R.A., Angly F., Wegley L., Hatay M., Hall D., Brown E., Haynes M., Krause L., Sala E., Sandin S.A., Thurber R.V., Willis B.L., Azam F., Knowlton N., Rohwer F. Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 2008, 3:e1584. 10.1371/journal.pone.001584.
26. Duedall I.W., Bowman M.J., O'Connors H.B. Sewage sludge and ammonium concentrations in the New York Bight apex. Estuar. Coast. Mar. Sci. 1975, 3:457-463.
27. Edmunds P.J., Bruno J.F. The importance of sampling scale in ecology: kilometer-wide variation in coral communities. Mar. Ecol. Prog. Ser. 1996, 143:165-171.
28. Edmunds P.J. Long-term dynamics of coral reefs in St. John, US Virgin Islands. Coral Reefs 2002, 21:357-367.
29. Erftemeijer P.L.A., Riegl B., Hoeksema B.W., Todd P.A. Environmental impacts of dredging and other sediment disturbances on corals: a review. Mar. Pollut. Bull. 2012, 64:1737-1765.
30. Fabricius K.E. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar. Pollut. Bull. 2005, 50:125-146.
31. Furby K.A., Bouwmeester J., Berumen M.L. Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 2013, 32:505-513.
32. Garcia-Fernandez J.M., de Marsac N.T., Diez J. Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol. Mol. Rev. 2004, 68:630-638.
33. Garren M., Smriga S., Azam F. Gradients of coastal fish farm effluents and their effect on coral reef microbes. Environ. Microbiol. 2008, 10:2299-2312.
34. Gilmour J.P. Asexual budding in fungiid corals. Coral Reefs 2004, 23:595.
35. Goffredo S., Chadwick-Furman N. Abundance and distribution of mushroom corals (Scleractinia: Fungiidae) on a coral reef at Eilat, Northern Red Sea. Bull. Mar. Sci. 2000, 66:241-254.
36. Goreau T.J., Cervino J., Goreau M., Hayes R., Hayes M., Richardson L., Smith G., DeMeyer K., Nagelkerken I., Garzon-Ferrera J., Gil D., Garrison G., Williams E.H., Bunkley-Williams L., Quirolo C., Patternson K., Porter J.W., Porter K. Rapid spread of diseases in Caribbean coral reefs. Rev. Biol. Trop. 1998, 46:157-171.
37. Green E.P., Bruckner A.W. The significance of coral disease epizootiology for coral real conservation. Biol. Conserv. 2000, 96:347-361.
38. Harvell C.D., Kim K., Burkholder J.M., Colwell R.R., Epstein P.R., et al. Emerging marine diseases - climate links and anthropogenic factors. Science 1999, 285:1505.
39. Harvell C.D., Mitchell C.E., Ward J.R., Altizer S., Dobson A.P., et al. Climate warming and disease risks for terrestrial and marine biota. Science 2002, 296:2158-2162.
40. Harvell C.D., Jordan-Dahlgren E., Merkel S., Rosenberg E., Raymundo L., Smith G., Weil E., Willis B. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 2007, 20:172-195.
41. Hayes M.L., Bonaventura J., Mitchell T.P., Prospero J.M., Shinn E.A., Van Dolah F., Barber R.T. How are climate and marine biological outbreaks functionally linked?. Hydrobiologia 2001, 460:213-220.
42. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 1999, 50:839-866.
43. Hoekesema B.W. Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fungiidae). Zool. Verh. 1989, 254:3-295.
44. Hoeksema B.W. Control of bleaching in mushroom coral populations (Scleractinia: Fungiidae) in the Java Sea: stress tolerance and interference by life history strategy. Mar. Ecol. Prog. Ser. 1991, 74:225-237.
45. Hoeksema B.W., Matthews J.L. Contrasting bleaching patterns in mushroom coral assemblages at Koh Tao, Gulf of Thailand. Coral Reefs 2011, 30:95.
46. Hoeksema B.W. Distribution patterns of mushroom corals (Scleractinia: fungiidae) across the Spermonde shelf, south Sulawesi. Raffles Bull. Zool. 2012, 60:183-212.
47. Hoeksema B.W. Evolutionary trends in onshore-offshore distribution patterns of mushroom coral species (Scleractinia: Fungiidae). Contrib. Zool. 2012, 81:199-221.
48. Holmes R.M., Aminot A., Kerouel R., Hooker B.A., Peterson B.J. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aq. Sci. 1999, 1801-1808.
49. Kushmaro A., Rosenberg E., Fine M., Ben Haim Y., Loya Y. Effects of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar. Ecol. Prog. Ser. 1998, 171:131-137.
50. McClanahan T., Polunin N., Done T. Ecological states and the resilience of coral reefs. Conserv. Ecol. 2002, 6:18.
51. Moore L.R., Goericke R., Chisholm S.W. Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar. Ecol. Prog. Ser. 1995, 116:259-275.
52. Partensky F., Blanchot J., Vaulot D. Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters : a review. Bull. l'Institut océanogr. 1999, NS19:457-475.
53. Pastorok R., Bilyard G. Effects of sewage pollution on coral-reef communities. Mar. Ecol. Prog. Ser. 1985, 21:175-189.
54. Peters E.C. A survey of cellular reactions to environmental stress and disease in Caribbean scleractinian corals. Helgol. Meeresunters 1984, 37:113-137.
55. Porter J.W., Dustan P., Jaap W.C., Patterson K.L., Kosmynin V., Meier O.W., Patterson M.E., Parsons M. Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 2001, 460:1.
56. Quadfasel D. Red sea circulation. Encyclopedia of Ocean Sciences 2001, 666-676. Academic Press, Oxford. J.H. Steele, S.A. Thorpe, K.K. Turekian (Eds.).
57. Risk M.J., Lapointe B.E., Sherwood O.A., Bedford B.J. The use of [delta]15N in assessing sewage stress on coral reefs. Mar. Pollut. Bull. 2009, 58:793-802.
58. Rosenberg E., Ben-Haim Y. Minireview: microbial diseases of corals and global warming. Environ. Microbiol. 2002, 4:318-326.
59. Ruangpan L., Kitao T. Vibrio bacteria isolated from black tiger shrimp, Penaeus monodon Fabricius. J. Fish. Dis. 1991, 14:383-388.
60. Sato Y., Bourne D.G., Willis B.L. Dynamics of seasonal outbreaks of black band disease in an assemblage of Montipora species at Pelorus Island (Great Barrier Reef, Australia). Proc. Royal Soc. B 2009, 276:2795-2803.
61. Schumacher H. Ability of fungiid corals to overcome sedimentation. Proceedings of the 3rd International Coral Reef Symposium 1977, Rosentiel School of Marine and Atmospheric Science, University of Miami.
62. Selig E.R., Harvell C.D., Bruno J.F., Willis B.L., Page C.A., Casey K.S., Sweatman H. Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. Coastal and Estuarine Series 2006, vol. 61:111-128. American Geophysical Union Press, Washington, D.C. J.T. Phinney, A. Strong, W. Skrving, J. West, J. Kleypas, O. Hough-Guldberg (Eds.).
63. Sheppard C.R.C. Interspecific aggression between reef corals with reference to their distribution. Mar. Ecol. Prog. Ser. 1979, 1:237-247.
64. Smith S.V., Kimmerer W.J., Laws E.A., Brock R.E., Walsh T.W. Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. Pac. Sci. 1981, 35:279-395.
65. Szmant A. Nutrient enrichment on coral reefs: is it a major cause of coral reef decline?. Estuaries 2002, 25:743-766.
66. Toren A., Landau L., Kushmaro A., Loya Y., Rosenberg E. Effects of temperature on adhesion of Vibrio strain AK-1 to Oculina patagonica and on coral bleaching. Appl. Environ. Microbiol. 1998, 64:1379-1384.
67. Nitrogen, Ammonia. Method 350.1 (Colorimetric, Automated, Phenate). Methods for Chemical Analysis of Water and Wastes: Cincinnati 1983, 350-1.1-350-1.4. U.S. Environmental Protection Agency.
68. Vincent P. Jeddah's environmental problems. Geogr. Rev. 2003, 93:394-412.
69. Veron J.E.N. Corals of the World 2000, Australian Institute of Marine Science, Townsville. M. Stafford-Smith (Ed.).
70. Walker D.I., Ormond R.F.G. Coral death from sewage and phosphate pollution at Aqaba, Red Sea. Mar. Pollut. Bull. 1982, 13:21-25.
71. Walton C.C., Pichel W.G., Sapper J.F. The development and operational application of nonlinear algorithms for the measurement of sea surface temperatures with the NOAA polar-orbiting environmental satellites. J. Geophys. Res. 1998, 103:27999-28012.
72. Weisse T. The microbial loop in the Red Sea: dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar. Ecol. Prog. Ser. 1989, 55:241-250.
73. Status of Caribbean Coral Reefs After Bleaching and Hurricanes in 2005. Global Coral Reef Monitoring Network 2008, 1-148. C.R. Wilkinson, D. Souter (Eds.).
74. Willis B.L., Page C.A., Dinsdale E.A. Coral disease on the Great Barrier Reef. Coral Health and Disease 2004, 69-104. Springer, New York. E. Rosenberg, Y. Loya (Eds.).
75. Work T.M., Aeby G.S. Systematically describing gross lesions in corals. Dis. Aq. Org. 2006, 70:155-160.