Coral Reefs

, Volume 34, Issue 4, pp 1179–1188 | Cite as

Multiple mechanisms of transmission of the Caribbean coral disease white plague

Report

Abstract

White plague is one of the most devastating coral diseases in the Caribbean, and yet important aspects of its epidemiology, including how the disease transmits, remain unknown. This study tested potential mechanisms and rates of transmission of white plague in a laboratory setting. Transmission mechanisms including the transport of water, contact with macroalgae, and predation via corallivorous worms and snails were tested on the host species Orbicella annularis. Two of the tested mechanisms were shown to transmit disease: water transport and the corallivorous snail Coralliophilaabbreviata. Between these transmission mechanisms, transport of water between a diseased coral and a healthy coral resulted in disease incidence significantly more frequently in exposed healthy corals. Transmission via water transport also occurred more quickly and was associated with higher rates of tissue loss (up to 3.5 cm d−1) than with the corallivorous snail treatment. In addition, water that was in contact with diseased corals but was filtered with a 0.22-μm filter prior to being introduced to apparently healthy corals also resulted in the transmission of disease signs, but at a much lower rate than when water was not filtered. This study has provided important information on the transmission potential of Caribbean white plague disease and highlights the need for a greater understanding of how these processes operate in the natural environment.

Keywords

Coral white plague Coral disease Caribbean coral reefs Disease transmission 

References

  1. Aeby GS, Santavy DL (2006) Factors affecting susceptibility of the coral Montastraea faveolata to black-band disease. Mar Ecol Prog Ser 318:103–110CrossRefGoogle Scholar
  2. Ainsworth TD, Kramasky-Winter E, Loya Y, Hoegh-Guldberg O, Fine M (2007) Coral disease diagnostics: What’s between a plague and a band? J Appl Environ Microbiol 73:981–992CrossRefGoogle Scholar
  3. Bandara HMHN, Lam OLT, Jin LJ, Lakshman S (2012) Microbial chemical signaling: a current perspective. Crit Rev Microbiol 38:217–249CrossRefPubMedGoogle Scholar
  4. Barash Y, Sulam R, Loya Y, Rosenberg E (2005) Bacterial Strain BA-3 and a filterable factor cause a white plague-like disease in corals from the Eilat coral reef. Aquat Microb Ecol 40:183–189CrossRefGoogle Scholar
  5. Barott KL, Rodriguez-Mueller B, Youle M, Marhaver KL, Vermeij MJ, Smith JE, Rohwer FL (2012) Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc R Soc B Biol Sci 279:1655–1664CrossRefGoogle Scholar
  6. Bassler BL (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2:528–587CrossRefGoogle Scholar
  7. Borger JL (2003) Three scleractinian coral diseases in Dominica, West Indies: Distribution, infection patterns, and contribution to coral tissue mortality. Rev Biol Trop 51(4):25–38PubMedGoogle Scholar
  8. Borger JL (2005) Scleractinian coral diseases in south Florida: incidence, species susceptibility, and mortality. Dis Aquat Organ 67:249–258CrossRefPubMedGoogle Scholar
  9. Brandt ME, McManus JW (2009a) Disease incidence is related to bleaching extent in reef-building corals. Ecology 90:2859–2867CrossRefPubMedGoogle Scholar
  10. Brandt ME, McManus JW (2009b) Dynamics and impact of the coral disease white plague: insights from a simulation model. Dis Aquat Organ 87:117–133CrossRefPubMedGoogle Scholar
  11. Brandt ME, Smith TB, Correra AMS, Vega-Thurber R (2013) Disturbance driven colony fragmentation as a driver of a coral disease outbreak. PLoS One 8:e57164PubMedCentralCrossRefPubMedGoogle Scholar
  12. Brandt ME, Ruttenberg BI, Waara R, Miller J, Witcher B, Estep AJ, Patterson M (2012) Dynamics of an acute coral disease outbreak associated with the macroalgae Dictyota spp. in Dry Tortugas National Park, Florida, U.S.A. Bull Mar Sci 88:1035–1050CrossRefGoogle Scholar
  13. Bythell JC, Pantos O, Richardson L (2004) White plague, white band, and other “white” diseases. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 351–365CrossRefGoogle Scholar
  14. Cook GM, Rothenberger JP, Sikaroodi M, Gillevet PM, Peters EC, Jonas RB (2013) A comparison of culture-dependent and culture-independent techniques used to characterize bacterial communities on healthy and white plague-diseased corals of the Montastraea annularis species complex. Coral Reefs 32:375–388CrossRefGoogle Scholar
  15. Croquer A, Weil E, Zubillaga AL, Pauls SM (2005) Impact of a white plague-II outbreak on a coral reef in the Archipelago Los Roques National Park. Venezuela. Caribb J Sci 41:815Google Scholar
  16. Denner EBM, Smith GW, Busse HJ, Schumann P (2003) Aurantimonas coralicida gen. Nov., sp. Nov., the causative agent of white plague type ii on caribbean scleractinian corals. Int J Syst Evol Microbiol 53:1115–1122CrossRefPubMedGoogle Scholar
  17. Diggle PJ (1983) Statistical Analysis of Spatial Point Patterns. Academic Press, New YorkGoogle Scholar
  18. Dustan P (1977) Vitality of reef coral populations off Key Largo Florida: recruitmant and mortality. Environ Geol 2:51–58CrossRefGoogle Scholar
  19. Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Buchoun C, Brandt ME, Bruckner AW, Bunkley-Williams L, Cameron A, Causey BD, Chiappone M, Christensen TRL, Crabbe MJC, Day O, de la Guardia E, Diaz-Pulido G, Diresta D, Gil-Agudelo DL, Gilliam DS, Ginsburg RN, Gore S, Guzman CM, Hendee JC, Hernandez-Delgado EA, Husain E, Jeffery CFG, Jones RJ, Jordan-Dahlgren E, Kaufman LS, Kline DI, Kramer PA, Lang JC, Lirman D, Mallela J, Manfrino C, Marachal JP, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Orozco Toro CA, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodriquez SN, Ramierz AR, Romano S, Samhouri F, Sanches JA, Schmahl GP, Shank BV, Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Wlater C, Weil E, Williams EH, Roberson KW, Yusuf Y (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS One 5:e313969CrossRefGoogle Scholar
  20. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-Luxl family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275PubMedCentralPubMedGoogle Scholar
  21. Goldberg K, Eltzov E, Shnit-Orland M, Marks RS, Kushmaro A (2011) Characterization of quorum sensing signals in coral-associated bacteria. Microb Ecol 61:783–792CrossRefGoogle Scholar
  22. Gray MA, Pratte ZA, Kellogg CA (2013) Comparison of DNA preservation methods for environmental bacterial community samples. FEMS Micro Ecol 82:468–477CrossRefGoogle Scholar
  23. Green EP, Bruckner AW (2000) The significance of coral disease epizootiology for coral reef conservation. Biol Conserv 96:347–361CrossRefGoogle Scholar
  24. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162CrossRefPubMedGoogle Scholar
  25. 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
  26. Lesser MP, Bythell JC, Gates RD, Johnstone RW, Hoegh-Guldberg O (2007) Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J Exp Mar Bio Ecol 346:36–44CrossRefGoogle Scholar
  27. McCallum H, Harvell D, Dobson D (2003) Rates of spread of marine pathogens. Ecol Lett 6:1062–1067CrossRefGoogle Scholar
  28. Miller J, Muller EM, 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
  29. Miller MW, Williams DE (2007) Coral disease outbreak at Navassa, a remote Caribbean island. Coral Reefs 26:97–101CrossRefGoogle Scholar
  30. Morrow KM, Moss AG, Chadwick NE, Liles MR (2012) Bacterial associates of two Caribbean coral species reveal species-specific distribution and geographic variability. Appl Environ Microbiol 78:6438–6449Google Scholar
  31. Muller E, van Woesik R (2012) Caribbean coral diseases: primary transmission or secondary infection? Glob Chang Biol 18:3529–3535CrossRefGoogle Scholar
  32. 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
  33. Nugues MM (2002) Impact of a coral disease outbreak on coral communities in St. Lucia: What and how much has been lost? Mar Ecol Prog Ser 229:61–71CrossRefGoogle Scholar
  34. Nugues MM, Smith GW, van Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923CrossRefGoogle Scholar
  35. Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O’Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environ Microbiol 5:370–382CrossRefPubMedGoogle Scholar
  36. Remily ER, Richardson LL (2006) Ecological physiology of a coral pathogen and the coral reef environment. Micro Ecol 51:345–354CrossRefGoogle Scholar
  37. Richardson LL (1988) Coral diseases: what is really known? TREE 13:438–443Google Scholar
  38. Richardson LL, Voss JD (2005) Changes in a coral population on reefs of the northern Florida Keys following a coral disease epizootic. Mar Ecol Prog Ser 297:147–157CrossRefGoogle Scholar
  39. Richardson LL, Smith GW, Ritchie KB, Carlton RG (2001) Integrating microbiological, microsensor, molecular, and physiologic techniques in the study of coral disease pathogenesis. Hydrobiologia 460:71–89CrossRefGoogle Scholar
  40. Richardson LL, Goldberg WM, Kuta KG, Aronson RB, Smith GW, Ritchie KB, Halas JC, Feingold JS, Miller SL (1998) Florida’s mystery coral-killer identified. Nature 392:557–558CrossRefGoogle Scholar
  41. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  42. Rosenberg E, Koren O, Resef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362CrossRefPubMedGoogle Scholar
  43. Rutzler K, Santavy D, Antonius A (1983) The black band disease of Atlantic reef corals. III. Distribution, ecology and development. Mar Ecol 4:329–358CrossRefGoogle Scholar
  44. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral morality. Ecol Lett 9:835–845CrossRefPubMedGoogle Scholar
  45. Smith TB, Nemeth RS, Blondeau J, Calnan JM, Kadison E, Herzlieb S (2008) Assessing coral reef health across onshore and offshore stress gradients in the US Virgin Islands. Mar Pollut Bull 56:1983–1991CrossRefPubMedGoogle Scholar
  46. Smith TB, Brandt MN, Calnan JM, Nemeth RS, Blondeau J, Kadison E, Taylor M, Rothenberger P (2013) Convergent mortality responses of Caribbean coral species to seawater warming. Ecosphere 4:87–98Google Scholar
  47. Soffer N, Brandt ME, Correa AMS, Smith TB, Vega-Thurber R (2013) Potential role of viruses in white plague coral disease. ISME J 8:271–283PubMedCentralCrossRefPubMedGoogle Scholar
  48. Sussman M, Loya Y, Fine M, Rosenberg E (2003) The marine fireworm Hermodice carunculata is a winter reservoir and spring-summer vector for the coral-bleaching pathogen Vibrio shiloi. Environ Microbiol 5:250–255CrossRefPubMedGoogle Scholar
  49. Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302CrossRefGoogle Scholar
  50. Teplitski M, Ritchie KB (2009) How feasible is the biological control of coral disease? Trends Ecol Evol 24:378–385CrossRefPubMedGoogle Scholar
  51. Weil E (2004) Coral reef diseases in the wider Caribbean. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 35–68CrossRefGoogle Scholar
  52. Weil E, Smith G, Gil-Agudelo DL (2006) Status and progress in coral reef disease research. Dis Aquat Organ 69:1–7CrossRefPubMedGoogle Scholar
  53. Weil E, Hernandez-Delgado EA, Bruckner AW, Ortiz A, Nemeth M, Ruiz H (2003) Distribution and status of acroporid (scleractinia) populations in Puerto Rico. In Acropora spp. Caribbean Workshop Potential application of the US Endangered Species Act (ESA) as a Conservation Strategy, NOAA-NMFS, NCORE, RSMAS, U of Miami pp 71–90Google Scholar
  54. Williams DE, Miller MW (2005) Coral disease outbreak: Pattern, prevalence and transmission in acropora cervicornis. Mar Ecol Prog Ser 301:119–128CrossRefGoogle Scholar
  55. Vega-Thurber R, Burkepile DE, Correa AMS, Thurber AR, Shantz AA, Welsh R, Pritchard C, Rosales S (2012) Macroalgae decrease growth and alter microbial community structure of the reef-building coral. Porites astreoides. PLoS One 7:e44246CrossRefPubMedGoogle Scholar
  56. Voss JD, Richardson LL (2006) Coral diseases near Lee Stocking Island, Bahamas: patterns and potential drivers. Dis Aquat Organ 69:33–40CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Center for Marine and Environmental StudiesUniversity of the Virgin IslandsSaint ThomasUSA

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