Growth anomalies on the coral genera Acropora and Porites are strongly associated with host density and human population size across the Indo-Pacific

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Aeby, Greta S ^a   Williams, Gareth J ^b,c   Franklin, Erik C ^a   Haapkyla, Jessica ^d   Harvell, C Drew ^e,f   Neale, Stephen ^d   Page, Cathie A ^d   Raymundo, Laurie ^g   Vargas Ángel, Bernardo ^h   Willis, Bette L ^d   Work, Thierry M ⁱ   Davy, Simon K ^b  

^a UNIVERSITY OF HAWAII   (United States)

^b VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^c CENTER FOR MARINE BIODIVERSITY AND CONSERVATION   (United States)

^d JAMES COOK UNIVERSITY   (Australia)

^e Department of Obstetrics Gynecology   (United States)

^f AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^g UNIVERSITY OF GUAM MARINE LABORATORY   (Guam)

^h UNIVERSITY OF HAWAII   (United States)

ⁱ U S GEOLOGICAL SURVEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACROPORA; ARTICLE; CONTROLLED STUDY; CORAL; CORAL REEF; ENVIRONMENTAL DISEASE; ENVIRONMENTAL IMPACT; GEOGRAPHIC DISTRIBUTION; GEOGRAPHICAL VARIATION (SPECIES); GROWTH DISORDER; NONHUMAN; PACIFIC OCEAN; POPULATION ABUNDANCE; POPULATION DENSITY DEPENDENCE; POPULATION SIZE; PORITES; PREDICTION; SEA SURFACE TEMPERATURE; ULTRAVIOLET RADIATION; ANIMAL; ANIMAL DISEASE; ANTHOZOA; CLASSIFICATION; ECOSYSTEM; ENVIRONMENT; GROWTH, DEVELOPMENT AND AGING; HUMAN; HUMAN ACTIVITIES; INDIAN OCEAN; POPULATION DENSITY; PREVALENCE; STATISTICS;

ACROPORA; ANTHOZOA; PORITES;

ANIMAL DISEASES; ANIMALS; ANTHOZOA; ECOSYSTEM; ENVIRONMENT; GROWTH DISORDERS; HUMAN ACTIVITIES; HUMANS; INDIAN OCEAN; PACIFIC OCEAN; POPULATION DENSITY; PREVALENCE;

EID: 79951993442     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016887     Document Type: Article

References (108)

1. Bellwood DR, Hughes TP, Folke C, Nystrom M, (2004) Confronting the coral reef crisis. Nature 429: 827-833.
2. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933.
3. Hoegh-Guldberg O, (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50: 839-866.
4. De'ath G, Lough JM, Fabricius KE, (2009) Declining Coral Calcification on the Great Barrier Reef. Science 323: 116-119.
5. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
6. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, et al. (2002) Ecology- Climate warming and disease risks for terrestrial and marine biota. Science 296: 2158-2162.
7. Bruno JF, Selig ER, (2007) Regional Decline of Coral Cover in the Indo-Pacific: Timing, Extent, and Subregional Comparisons. PLoS ONE 2: e711.
8. Nugues MM, (2002) Impact of a coral disease outbreak on coral communities in St. Lucia: What and how much has been lost? Marine Ecology-Progress Series 229: 61-71.
9. Richardson LL, Voss JD, (2005) Changes in a coral population on reefs of the northern Florida Keys following a coral disease epizootic. Marine Ecology-Progress Series 297: 147-156.
10. Bruckner AW, Hill RL, (2009) Ten years of change to coral communities off Mona and Desecheo Islands, Puerto Rico, from disease and bleaching. Diseases of Aquatic Organisms 87: 19-31.
11. Aronson RB, Precht WF, (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460: 25-38.
12. Kim K, Harvell CD, (2002) Aspergillosis of sea fan corals: dynamics in the Florida Keys. In: Porter JW, Porter KG, editors. The Everglades, Florida Bay, and coral reefs of the Florida Keys: an ecosystem sourcebook Boca Raton CRC pp. 813-824.
13. 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.
14. Bruno JF, Petes LE, Harvell CD, Hettinger A, (2003) Nutrient enrichment can increase the severity of coral diseases. Ecology Letters 6: 1056-1061.
15. Voss JD, Richardson LL, (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25: 569-576.
16. Baker DM, MacAvoy SE, Kim K, (2007) Relationship between water quality, delta N-15, and aspergillosis of Caribbean sea fan corals. Marine Ecology-Progress Series 343: 123-130.
17. Williams GJ, Aeby GS, Cowie ROM, Davy SK, (2010) Predictive Modeling of Coral Disease Distribution within a Reef System. PLoS ONE 5: e9264.
18. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PloS Biology 5: 1220-1227.
19. Harvell D, Kim K, Quirolo C, Weir J, Smith G, (2001) Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea). Hydrobiologia 460: 97-104.
20. 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.
21. Brandt ME, McManus JW, (2009) Disease incidence is related to bleaching extent in reef-building corals. Ecology 90: 2859-2867.
22. McClanahan TR, Weil E, Maina J, (2009) Strong relationship between coral bleaching and growth anomalies in massive Porites. Global Change Biology 15: 1804-1816.
23. Work TM, Richardson LL, Reynolds TL, Willis BL, (2008) Biomedical and veterinary science can increase our understanding of coral disease. Journal of Experimental Marine Biology and Ecology 362: 63-70.
24. Peters EC, Gassman NJ, Firman JC, Richmond RH, Power EA, (1997) Ecotoxicology of tropical marine ecosystems. Environmental Toxicology and Chemistry 16: 12-40.
25. Sutherland KP, Porter JW, Torres C, (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Marine Ecology-Progress Series 266: 273-302.
26. Cheney DP, (1975) Hard tissue tumors of scleractinian corals. Adv Exp Med Biol 64: 77-87.
27. Bak RPM, (1983) Neoplasia, regeneration and growth in the reef-building coral Acropora palmata. Marine Biology 77: 221-227.
28. Peters EC, Halas JC, McCarty HB, (1986) Calicoblastic neoplasms in Acropora palmata, with a review of reports on anomalies of growth and form in corals. Journal of the National Cancer Institute 76: 895-912.
29. Coles SL, Seapy DG, (1998) Ultraviolet absorbing compounds and tumorous growths on acroporid corals from Bandar Khayran, Gulf of Oman, Indian Ocean. Coral Reefs 17: 195-198.
30. Yamashiro H, Yamamoto M, van Woesik R, (2000) Tumor formation on the coral Montipora informis. Diseases of Aquatic Organisms 41: 211-217.
31. Gateno D, Leon A, Barki Y, Cortes J, Rinkevich B, (2003) Skeletal tumor formations in the massive coral Pavona clavus. Marine Ecology-Progress Series 258: 97-108.
32. Domart-Coulon IJ, Traylor-Knowles N, Peters E, Elbert D, Downs CA, et al. (2006) Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa. Coral Reefs 25: 531-543.
33. Work TM, Aeby GS, Coles SL, (2008) Distribution and morphology of growth anomalies in Acropora from the Indo-Pacific. Diseases of Aquatic Organisms 78: 255-264.
34. Williams GJ, Work TM, Aeby GS, Knapp IS, Davy SK, (2010) Gross and microscopic morphology of lesions in Cnidaria from Palmyra Atoll, Central Pacific. Journal of Invertebrate Pathology 106 (2): 165-173.
35. Kaczmarsky L, Richardson LL, (2007) Transmission of growth anomalies between Indo-Pacific Porites corals. Journal of Invertebrate Pathology 94: 218-221.
36. Friedlander AM, DeMartini EE, (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Marine Ecology-Progress Series 230: 253-264.
37. Raymundo LJ, Rosell KB, Reboton CT, Kaczmarsky L, (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Diseases of Aquatic Organisms 64: 181-191.
38. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, et al. (2008) Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 3: e1548.
39. Williams GJ, Knapp IS, Maragos JE, Davy SK, (2010) Modeling patterns of coral bleaching at a remote Central Pacific atoll. Marine Pollution Bulletin 60: 1467-1476.
40. CIESIN (2005) Center for International Earth Science Information Network Gridded Population of the World Version 3 (GPWv3): Population Grids (accessed 2008) http://sedac.ciesin.columbia.edu/gpw.
41. Selig ER, Casey KS, Bruno JF, (2010) New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management. Global Ecology and Biogeography 19: 397-411.
42. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, et al. (2008) A global map of human impact on marine ecosystems. Science 319: 948-952.
43. McPeters R, Barthia PA, Krueger AJ, Herman JR, Wellemeyer CG, et al. (1998) Earth Probe Total Ozone Mapping Spectrometer (TOMS) Data Products User's Guide, NASA/TP-1998-206895.
44. McArdle BH, Anderson MJ, (2001) Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82: 290-297.
45. Anderson MJ, Gorley RN, Clarke KR, (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. Plymouth, UK PRIMER-E.
46. Schwarz G, (1978) Estimating the dimension of a model. Annals of Statistics 6: 461-464.
47. Clarke KR, Somerfield PJ, Chapman MG, (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology 330: 55-80.
48. Clarke KR, Gorley RN, (2006) PRIMER v6: User manual/Tutorial. Plymouth, UK PRIMER-E.
49. Porter JW, Dustan P, Jaap WC, Patterson KL, Kosmynin V, et al. (2001) Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 460: 1-24.
50. Garzon-Ferreira J, Gil-Agudelo DL, Barrios LM, Zea S, (2001) Stony coral diseases observed in southwestern Caribbean reefs. Hydrobiologia 460: 65-69.
51. Jordan-Dahlgren E, Rodriguez-Martinez E, (2004) Coral diseases in Gulf of Mexico reefs. In: Rosenberg E, Loya Y, editors. Coral Health and Disease Berlin Springer-Verlag pp. 105-118.
52. Page C, Willis B, (2006) Distribution, host range and large-scale spatial variability in black band disease prevalence on the Great Barrier Reef, Australia. Diseases of Aquatic Organisms 69: 41-51.
53. Haapkyla J, Seymour AS, Trebilco J, Smith D, (2007) Coral disease prevalence and coral health in the Wakatobi Marine Park, south-east Sulawesi, Indonesia. Journal of the Marine Biological Association of the United Kingdom 87: 403-414.
54. Myers RL, Raymundo LJ, (2009) Coral disease in Micronesian reefs: a link between disease prevalence and host abundance. Diseases of Aquatic Organisms 87: 97-104.
55. Aeby GS, Work TM, Fenner D, Didonato E, (2008) Coral and crustose coralline algae disease on the reefs of American Samoa. Ft. Lauderdale, Florida Proceedings of the 11th International Coral Reef Symposium pp. 197-201.
56. Williams GJ, Aeby GS, Davy SK, (2008) Coral disease at Palmyra Atoll, a remote reef system in the Central Pacific. Coral Reefs 27: 207.
57. Winkler R, Antonius A, Renegar DA, (2004) The skeleton eroding band disease on coral reefs of Aqaba, Red Sea. Marine Ecology 25 (2): 129-144.
58. Raymundo LJH, Harvell CD, Reynolds TL, (2003) Porites ulcerative white spot disease: description, prevalence, and host range of a new coral disease affecting Indo-Pacific reefs. Diseases of Aquatic Organisms 56: 95-104.
59. Aeby GS, (2006) Baseline levels of coral disease in the Northwestern Hawaiian Islands. Atoll Research Bulletin pp. 471-488.
60. Vargas-Angel B, (2009) Coral health and disease assessment in the US Pacific Remote Island Areas. Bulletin of Marine Science 84: 211-227.
61. Santavy DL, Mueller E, Peters EC, MacLaughlin L, Porter JW, et al. (2001) Quantitative assessment of coral diseases in the Florida Keys: strategy and methodology. Hydrobiologia 460: 39-52.
62. Veron J, (2000) Corals of the world (Vol 1-3). Townsville, Australia Australian Institute of Marine Science and CPR Qld Pyt Ltd.
63. Lloyd-Smith JO, Cross PC, Briggs CJ, Daugherty M, Getz WM, et al. (2005) Should we expect population thresholds for wildlife disease? Trends in Ecology & Evolution 20: 511-519.
64. Altizer SM, Augustine DJ, (1997) Interactions between frequency-dependent and vertical transmission in host-parasite systems. Proceedings of the Royal Society of London Series B-Biological Sciences 264: 807-814.
65. McCallum H, Barlow N, Hone J, (2001) How should pathogen transmission be modelled? Trends in Ecology & Evolution 16: 295-300.
66. Brown CR, Brown MB, (2004) Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85: 1619-1626.
67. Ramsey D, Spencer N, Caley P, Efford M, Hansen K, et al. (2002) The effects of reducing population density on contact rates between brushtail possums: implications for transmission of bovine tuberculosis. Journal of Applied Ecology 39: 806-818.
68. Berthier K, Langlais M, Auger P, Pontier D, (2000) Dynamics of a feline virus with two transmission modes within exponentially growing host populations. Proceedings of the Royal Society of London Series B-Biological Sciences 267: 2049-2056.
69. Bjornstad ON, Finkenstadt BF, Grenfell BT, (2002) Dynamics of measles epidemics: Estimating scaling of transmission rates using a Time series SIR model. Ecological Monographs 72: 169-184.
70. Begon M, Feore SM, Brown K, Chantrey J, Jones T, et al. (1998) Population and transmission dynamics of cowpox in bank voles: testing fundamental assumptions. Ecology Letters 1: 82-86.
71. Begon M, Hazel SM, Baxby D, Bown K, Cavanagh R, et al. (1999) Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proceedings of the Royal Society of London Series B-Biological Sciences 266: 1939-1945.
72. Aeby GS, (2007) Spatial and temporal patterns of Porites trematodiasis on the reefs of Kaneohe Bay, Oahu, Hawaii. Bulletin of Marine Science 80: 209-218.
73. 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. Diseases of Aquatic Organisms 91: 1-8.
74. Daszak P, Cunningham AA, Hyatt AD, (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78: 103-116.
75. Dobson A, Foufopoulos J, (2001) Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 356: 1001-1012.
76. Coyner DF, Spalding MG, Forrester DJ, (2002) Epizootiology of Eustrongylides ignotus in Florida: Distribution, density, and natural infections in intermediate hosts. Journal of Wildlife Diseases 38: 483-499.
77. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, et al. (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution 19: 535-544.
78. Bradley CA, Altizer S, (2007) Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution 22: 95-102.
79. Aguirre AA, Tabor GM, (2008) Global Factors Driving Emerging Infectious Diseases Impact on Wildlife Populations. Animal Biodiversity and Emerging Diseases: Prediction and Prevention 1149: 1-3.
80. Van Houtan KS, Hargrove SK, Balazs GH, (2010) Land Use, Macroalgae, and a Tumor-Forming Disease in Marine Turtles. PLoS ONE 5: e12900.
81. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, et al. (1999) Review: Marine ecology- Emerging marine diseases- Climate links and anthropogenic factors. Science 285: 1505-1510.
82. Richardson LL, Miller AW, Broderick E, Kaczmarsky L, Gantar M, et al. (2009) Sulfide, microcystin, and the etiology of black band disease. Diseases of Aquatic Organisms 87: 79-90.
83. Smith GW, Ives LD, Nagelkerken IA, Ritchie KB, (1996) Caribbean sea-fan mortalities. Nature 383: 487-487.
84. Geiser DM, Taylor JW, Ritchie KB, Smith GW, (1998) Cause of sea fan death in the West Indies. Nature 394: 137-138.
85. Patterson KL, Porter JW, Ritchie KE, Polson SW, Mueller E, et al. (2002) The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proceedings of the National Academy of Sciences of the United States of America 99: 8725-8730.
86. Davy SK, Burchett SG, Dale AL, Davies P, Davy JE, et al. (2006) Viruses: agents of coral disease? Diseases of Aquatic Organisms 69: 101-110.
87. Wetz JJ, Lipp EK, Griffin DW, Lukasik J, Wait D, et al. (2004) Presence, infectivity, and stability of enteric viruses in seawater: relationship to marine water quality in the Florida Keys. Marine Pollution Bulletin 48: 698-704.
88. Aeby GS, (1998) A digenean metacercaria from the reef coral, Porites compressa, experimentally identified as Podocotyloides stenometra. Journal of Parasitology 84: 1259-1261.
89. Rosenberg E, Ben-Haim Y, Toren A, Banin E, Kushmaro A, et al. (1999) Effect of temperature on bacterial bleaching of corals. In: Rosenberg E, editors. Microbial ecology and infectious disease Washington DC American Society for Microbiology pp. 242-254.
90. Denner EBM, Smith GW, Busse HJ, Schumann P, Narzt T, et al. (2003) Aurantimonas coralicida gen. nov., sp nov., the causative agent of white plague type II on Caribbean scleractinian corals. International Journal of Systematic and Evolutionary Microbiology 53: 1115-1122.
91. Richardson LL, (2004) Black band disease. In: Rosenberg E, Loya Y, editors. Coral Health and Disease Berlin Springer-Verlag pp. 325-336.
92. Cervino JM, Thompson FL, Gomez-Gil B, Lorence EA, Goreau TJ, et al. (2008) The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. Journal of Applied Microbiology 105: 1658-1671.
93. Sussman M, Willis BL, Victor S, Bourne DG, (2008) Coral pathogens identified for white syndrome (WS) epizootics in the Indo-Pacific. PLoS ONE 3: e2393.
94. Stimson J, Ecological characterization of coral growth anomalies on Porites compressa in Hawai'i. Coral Reefs In Press.
95. Work TM, Balazs GH, Rameyer RA, Morris RA, (2004) Retrospective pathology survey of green turtles Chelonia mydas with fibropapillomatosis in the Hawaiian Islands, 1993-2003. Diseases of Aquatic Organisms 62: 163-176.
96. Work TM, Rameyer RA, Balazs GH, Cray C, Chang SP, (2001) Immune status of free-ranging green turtles with fibropapillomatosis from Hawaii. Journal of Wildlife Diseases 37: 574-581.
97. Anders K, Yoshimizu M, (1994) Role of viruses in the induction of skin tumors and tumor-like proliferations of fish. Diseases of Aquatic Organisms 19: 215-232.
98. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, et al. (2008) Microbial Ecology of Four Coral Atolls in the Northern Line Islands. PLoS ONE 3: e1584.
99. Vega Thurber RL, Barott KL, Hall D, Liu H, Rodriguez-Mueller B, et al. (2008) Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proceedings of the National Academy of Sciences of the United States of America 105: 18413-18418.
100. Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, et al. (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11: 2148-2163.
101. 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.
102. Ward JR, Kim K, Harvell CD, (2007) Temperature affects coral disease resistance and pathogen growth. Marine Ecology-Progress Series 329: 115-121.
103. Blanford S, Thomas MB, Pugh C, Pell JK, (2003) Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters 6: 2-5.
104. Edmunds PJ, (1991) Extent and effect of Black Band Disease on a Caribbean reef. Coral Reefs 10: 161-165.
105. Bruckner AW, Bruckner RJ, (1997) The persistence of black band disease in Jamaica: impact on community structure. Proceedings of the 8th International Coral Reef Symposium, Smithsonian Tropical Research Institute, Panama 1: 601-606.
106. 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.
107. 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. Marine Biology 151: 1711-1720.
108. Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, et al. (2009) Microbial disease and the coral holobiont. Trends in Microbiology 17: 554-562.