Advertisement

Marine Biology

, 166:45 | Cite as

Modes of coral disease transmission: how do diseases spread between individuals and among populations?

  • Amanda ShoreEmail author
  • Jamie M. Caldwell
Review, concept, and synthesis

Abstract

Coral disease is considered an important factor in the recent decline of coral reefs worldwide; yet transmission, a critical factor for understanding disease ecology, identifying at-risk individuals and populations, and developing management options, is understudied in coral disease research. Here, we review techniques for investigating coral disease transmission using laboratory and field experiments, and modeling analyzes, and highlight how these approaches can improve our understanding of disease ecology. We summarize current knowledge about three hypothesized modes of coral disease transmission: direct contact, water borne, and vector-borne transmission. We also discuss the key challenge in studying disease transmission, which is unknown or complex etiology. Finally, we suggest potential management strategies that may result from a better understanding of coral disease transmission.

Keywords

Transmission Coral disease Disease ecology Marine disease Vector borne Water borne 

Notes

Acknowledgements

The authors would like to acknowledge and thank Dr. Colleen Burge, Dr. Deborah Gochfeld, and two anonymous reviewers for valuable comments and suggestions, which has greatly improved the final manuscript

Funding

A. Shore was supported by a Grant from the National Institutes of Standards and Technology (0010509) and by the Rice Academy Postdoctoral Fellowship Program. J. Caldwell was supported by the Stanford University Woods Institute for the Environment, Environmental Ventures Program, and by a grant through the NASA Ecological Forecasting Program (NNX17AI21G).

Compliance with Ethical Standards

Conflict of interest

A. Shore declares no conflict of interest. J. M. Caldwell declares no conflict of interest.

Ethical approval

This article does not any contain studies with human participants or animals performed by any of the authors.

Supplementary material

227_2019_3490_MOESM1_ESM.pdf (118 kb)
Supplementary file1 (PDF 117 kb)

References

  1. Aeby GS (2005) Outbreak of coral disease in the Northwestern Hawaiian Islands. Coral Reefs 24:481.  https://doi.org/10.1007/s00338-005-0493-3 CrossRefGoogle Scholar
  2. Aeby GS, Santavy DL (2006) Factors affecting susceptibility of the coral Montastraea faveolata to black-band disease. Mar Ecol Prog Ser 318:103–110.  https://doi.org/10.3354/meps318103 CrossRefGoogle Scholar
  3. 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. Dis Aquat Organ 91:1–8.  https://doi.org/10.3354/dao02247 CrossRefPubMedGoogle Scholar
  4. Aeby GS, Bourne DG, Wilson B, Work TM (2011) Coral diversity and the severity of disease outbreaks: a cross-regional comparison of Acropora white syndrome in a species-rich region (American Samoa) with a species-poor region (Northwestern Hawaiian Islands). J Mar Biol 2011:490198.  https://doi.org/10.1155/2011/490198 CrossRefGoogle Scholar
  5. Aeby GS, Callahan SM, Cox EF, Runyon CM, Smith A, Stanton F, Ushijima B, Work TM (2016) Emerging coral diseases in Kaneohe Bay, Oahu, Hawaii (USA): two major disease outbreaks of acute Montipora white syndrome. Dis Aquat Organ 119:189–198.  https://doi.org/10.3354/dao02996 CrossRefPubMedGoogle Scholar
  6. Aeby GS (1998) Interactions of the digenetic trematode, Podocotyloides stenometra, with its coral intermediate host and butterflyfish definitive host: ecology and evolutionary implications. Dissertation, University of Hawaii at ManoaGoogle Scholar
  7. Aguirre-Macedo ML, Vidal-Martinez VM, Herrera-Silveira JA, Valdes-Lozano DS, Herrera-Rodriguez M, Olvera-Novoa MA (2008) Ballast water as a vector of coral pathogens in the Gulf of Mexico: the case of the Cayo Arcas coral reef. Mar Pollut Bull 56:1570–1577.  https://doi.org/10.1016/j.marpolbul.2008.05.022 CrossRefPubMedGoogle Scholar
  8. Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proc R Soc B 276:3019–3025.  https://doi.org/10.1098/rspb.2009.0339 CrossRefPubMedGoogle Scholar
  9. Antonius A, Lipscomb D (2000) First protozoan coral-killer identified in the Indo-Pacific. Atoll Res Bull.  https://doi.org/10.5479/si.00775630.481 CrossRefGoogle Scholar
  10. Antonius A, Riegl B (1997) A possible link between coral diseases and a corallivorous snail (Drupella cornus) outbreak in the Red Sea. Atoll Res Bull 447:1–9.  https://doi.org/10.5479/si.00775630.447.1 CrossRefGoogle Scholar
  11. Aronson RB, Precht WF (2001) White-Band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38.  https://doi.org/10.1023/A:1013103928980 CrossRefGoogle Scholar
  12. Atad I, Zvuloni A, Loya Y, Rosenberg E (2012) Phage therapy of the white plague-like disease of Favia favus in the Red Sea. Coral Reefs 31:665–670.  https://doi.org/10.1007/s00338-012-0900-5 CrossRefGoogle Scholar
  13. 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 40:183–189.  https://doi.org/10.3354/ame040183 CrossRefGoogle Scholar
  14. Baums IB, Paris CB, Chérubin LM (2006) A bio-oceanographic filter to larval dispersal in a reef-building coral. Limnol Oceanogr 51:1969–1981.  https://doi.org/10.4319/lo.2006.51.5.1969 CrossRefGoogle Scholar
  15. Ben-Haim Y, Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Mar Biol 141:47–55.  https://doi.org/10.1007/s00227-002-0797-6 CrossRefGoogle Scholar
  16. Beurmann S, Ushijima B, Videau P, Svoboda CM, Smith AM, Rivers OS, Aeby GS, Callahan SM (2017) Pseudoalteromonas piratica strain OCN003 is a coral pathogen that causes a switch from chronic to acute Montipora white syndrome in Montipora capitata. PLoS ONE 12:1–20.  https://doi.org/10.1371/journal.pone.0188319 CrossRefGoogle Scholar
  17. Borger J (2003) Three scleractinian coral diseases in Dominica, West Indies: distribution, infection patterns and contribution to coral tissue mortality. Rev Biol Trop 51:25–38PubMedGoogle Scholar
  18. Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340.  https://doi.org/10.1146/annurev-micro-102215-095440 CrossRefPubMedGoogle Scholar
  19. 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.  https://doi.org/10.1007/s00227-006-0603-y CrossRefGoogle Scholar
  20. Brandt ME, McManus JW (2009) Disease incidence is related to bleaching extent in reef-building corals. Ecology 90:2859–2867.  https://doi.org/10.1890/08-0445.1 CrossRefPubMedGoogle Scholar
  21. Brandt ME, Smith TB, Correa AMS, Vega-Thurber R (2013) Disturbance driven colony fragmentation as a driver of a coral disease outbreak. PLoS ONE 8:1–10.  https://doi.org/10.1371/journal.pone.0057164 CrossRefGoogle Scholar
  22. Bruckner AW, Bruckner RJ, Williams EH (1997) Spread of black-band disease epizootic through the coral reef system in St. Ann’s Bay, Jamaica. Bull Mar Sci 61:919–928Google Scholar
  23. Burge CA, Closek CJ, Friedman CS, Groner ML, Jenkins CM, Shore-Maggio A, Welsh JE (2016) The use of filter-feeders to manage disease in a changing world. Integr Comp Biol 56:573–587.  https://doi.org/10.1093/icb/icw048 CrossRefPubMedGoogle Scholar
  24. Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington DCGoogle Scholar
  25. Burreson EM, Ragone Calvo LM (1996) Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. J Shellfish Res 15:17–34Google Scholar
  26. Caldwell JM, Heron SF, Eakin CM, Donahue MJ (2016) Satellite SST-based coral disease outbreak predictions for the Hawaiian archipelago. Remote Sens 8:93.  https://doi.org/10.3390/rs8020093 CrossRefGoogle Scholar
  27. Caldwell JM, Donahue MJ, Harvell CD (2018) Host size and spatial proximity to diseased neighbors drive the spread of a coral disease outbreak in Hawaii. Proc R Soc B 285:20172265.  https://doi.org/10.1098/rspb.2017.2265 CrossRefPubMedGoogle Scholar
  28. Casey JM, Ainsworth TD, Choat JH, Connolly SR (2014) Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and black band disease. Proc R Soc B 281:20141032.  https://doi.org/10.1098/rspb.2014.1032 CrossRefPubMedGoogle Scholar
  29. Certner RH, Dwyer AM, Patterson MR, Vollmer S (2017) Zooplankton as a potential vector for white band disease transmission in the endangered coral Acropora cervicornis. PeerJ 5:e3502.  https://doi.org/10.7717/peerj.3502 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Chadwick NE, Morrow KM (2011) Competition among sessile organisms on coral reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 347–371CrossRefGoogle Scholar
  31. Chong-Seng KM, Cole AJ, Pratchett MS, Willis BL (2011) Selective feeding by coral reef fishes on coral lesions associated with brown band and black band disease. Coral Reefs 30:473–481.  https://doi.org/10.1007/s00338-010-0707-1 CrossRefGoogle Scholar
  32. Clemens E, Brandt ME (2015) Multiple mechanisms of transmission of the Caribbean coral disease white plague. Coral Reefs 34:1179–1188.  https://doi.org/10.1007/s00338-015-1327-6 CrossRefGoogle Scholar
  33. Cole AJ, Chong-Seng KM, Pratchett MS, Jones GP (2009) Coral-feeding fishes slow progression of black-band disease. Coral Reefs 28:965.  https://doi.org/10.1007/s00338-009-0519-3 CrossRefGoogle Scholar
  34. Dalton SJ, Godwin S (2006) Progressive coral tissue mortality following predation by a corallivorous nudibranch (Phestilla sp). Coral Reefs 25:529.  https://doi.org/10.1007/s00338-006-0139-0 CrossRefGoogle Scholar
  35. Dalton SJ, Godwin S, Smith SD, Pereg L (2010) Australian subtropical white syndrome: A transmissible, temperature-dependent coral disease. Mar Freshw Res 61:342–350.  https://doi.org/10.1071/MF09060 CrossRefGoogle Scholar
  36. Daly M, Brugler M, Cartwright P, Collins A, Dawson M, Fautin D, France S, McFadden C, Opresko D, Rodriguez E, Romano S, Stake J (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182.  https://doi.org/10.5281/zenodo.180149 CrossRefGoogle Scholar
  37. Danovaro R, Umani S, Pusceddu A (2009) Climate change and the potential spreading of marine mucilage and microbial pathogens in the Mediterranean sea. PLoS ONE 4:e7006.  https://doi.org/10.1371/journal.pone.0007006 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Davidson IC, Brown CW, Sytsma MD, Ruiz GM (2009) The role of containerships as transfer mechanisms of marine biofouling species. Biofouling 25:645–655.  https://doi.org/10.1080/08927010903046268 CrossRefPubMedGoogle Scholar
  39. Easson CG, Slattery M, Momm HG, Olson JB, Thacker RW, Gochfeld DJ (2013) Exploring individual- to population-level impacts of disease on coral reef sponges: using spatial analysis to assess the fate, dynamics, and transmission of Aplysina red band syndrome (ARBS). PLoS ONE 8:e79976.  https://doi.org/10.1371/journal.pone.0079976 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Gharaibeh DN, Biel FM, Hase CC (2013) Development of monoclonal antibody-based assays for the detection of Vibrio tubiashii zinc-metaloprotease (VtpA). J Microbiol Methods 94:125–132.  https://doi.org/10.1016/j.mimet.2013.05.009 CrossRefPubMedGoogle Scholar
  41. Gignoux-Wolfsohn SA, Marks CJ, Vollmer SV (2012) White band disease transmission in the threatened coral Acropora cervicornis. Sci Rep 2:804.  https://doi.org/10.1038/srep00804 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Goldstein MC, Carson HS, Eriksen M (2014) Relationship of diversity and habitat area in North Pacific plastic-associated rafting communities. Mar Biol 161:1441–1453.  https://doi.org/10.1007/s00227-014-2432-8 CrossRefGoogle Scholar
  43. Haapkylä J, Unsworth RK, Flavell M, Bourne DG, Schaffelke B, Willis BL (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS ONE 6:e16893.  https://doi.org/10.1371/journal.pone.0016893 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Heesterbeek JAP (2002) A brief history of R0 and a recipe for its calculation. Acta Biotheor 50:189–204.  https://doi.org/10.1023/A:1016599411804 CrossRefPubMedGoogle Scholar
  45. Heffernan JM, Smith RJ, Wahl LM (2005) Perspectives on the basic reproductive ratio. J R Soc Interface 2:281–293.  https://doi.org/10.1098/rsif.2005.0042 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hewson I, Button JB, Gudenkauf BM, Miner B, Newton AL, Gaydos JK, Wynne J, Groves CL, Hendler G, Murray M, Fradkin S, Breitbart M, Fahsbender E, Lafferty KD, Kilpatrick AM, Miner CM, Raimondi P, Lahner L, Friedman CS, Daniels S, Haulena M, Marliave J, Burge CA, Eisenlord ME, Harvell CD (2014) Densovirus associated with sea-star wasting disease and mass mortality. Proc Natl Acad Sci 111:17278–17283.  https://doi.org/10.1073/pnas.1416625111 CrossRefPubMedGoogle Scholar
  47. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226.  https://doi.org/10.3354/meps007207 CrossRefGoogle Scholar
  48. Hildemann WH, Linthicum DS, Vann DC (1975) Transplantation and immunocompatibility reactions among reef-building corals. Immunogenetics 2:269–284.  https://doi.org/10.1007/BF01572295 CrossRefGoogle Scholar
  49. Hobbs JP, Frisch AJ, Newman SJ, Wakefield CB (2015) Selective impact of disease on coral communities: outbreak of white syndrome causes significant total mortality of Acropora plate corals. PLoS ONE 10:1–15.  https://doi.org/10.1371/journal.pone.0132528 CrossRefGoogle Scholar
  50. Houlbreque F, Ferrier-Pages C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17.  https://doi.org/10.1111/j.1469-185X.2008.00058.x CrossRefPubMedGoogle Scholar
  51. Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis BL (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365.  https://doi.org/10.1016/j.cub.2006.12.049 CrossRefPubMedGoogle Scholar
  52. Israely T, Banin E, Rosenberg E (2001) Growth, differentiation and death of Vibrio shiloi in coral tissue as a function of seawater temperature. Aquat Microb Ecol 24:1–8.  https://doi.org/10.3354/ame024001 CrossRefGoogle Scholar
  53. Jolles AE, Sullivan P, Alker AP, Harvell CD (2002) Disease transmission of aspergillosis in sea fans: inferring process from spatial pattern. Ecology 83:2373–2378.  https://doi.org/10.1890/0012-9658(2002)083[2373:DTOAIS]2.0.CO;2 CrossRefGoogle Scholar
  54. Joyner JL, Sutherland KP, Kemp DW, Berry B, Griffin A, Porter JW, Amador MH, Noren HK, Lipp EK (2015) Systematic analysis of white pox disease in Acropora palmata of the Florida Keys and the role of Serratia marcescens. Appl Environ Microbiol 81:4451–4457.  https://doi.org/10.1128/AEM.00116-15 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kaczmarsky L, Richardson L (2011) Do elevated nutrients and organic carbon on Philippine reefs increase the prevalence of coral disease? Coral Reefs 30:253–257.  https://doi.org/10.1007/s00338-010-0686-2 CrossRefGoogle Scholar
  56. 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 41:124–137Google Scholar
  57. Katz SM, Pollock FJ, Bourne DG, Willis BL (2014) Crown-of-thorns starfish predation and physical injuries promote brown band disease on corals. Coral Reefs 33:705–716.  https://doi.org/10.1007/s00338-014-1153-2 CrossRefGoogle Scholar
  58. Kellogg CA, West AE, Runyon CM (2017) Predation by Acanthurus leucopareius on black-band disease in Kauai Hawaii. Bull Mar Sci.  https://doi.org/10.5343/bms.2016.1104 CrossRefGoogle Scholar
  59. Lafferty KD, Ben-Horin T (2013) Abalone farm discharges the withering syndrome pathogen into the wild. Front Microbiol 4:1–5.  https://doi.org/10.3389/fmicb.2013.00373 CrossRefGoogle Scholar
  60. Lamb JB, Willis BL, Fiorenza EA, Couch CS, Howard R, Rader DN, True JD, Kelly LA, Ahmad A, Jompa J, Harvell CD (2018) Plastic waste associated with disease on coral reefs. Science 2010:26–29.  https://doi.org/10.1126/science.aar3320 CrossRefGoogle Scholar
  61. Lamb JB, Water JA, Bourne DG, Altier C, Hein MY, Fiorenza EA, Abu N, Jompa J, Harvell CD (2017) Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355:731–733.  https://doi.org/10.1126/science.aal1956 CrossRefPubMedGoogle Scholar
  62. Lang J (1973) Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull Mar Sci 23:260–279Google Scholar
  63. Lang J, Chornesky E (1990) Competition between scleractinian reef corals-a review of mechanisms and effects. In: Dubinsky Z (ed) Ecosystems of the world-coral reefs. Elsevier, Amsterdam, pp 209–252Google Scholar
  64. Lentz JA, Blackburn JK, Curtis AJ (2011) Evaluating patterns of a white-band disease (WBD) outbreak in Acropora palmata using spatial analysis: a comparison of transect and colony clustering. PLoS ONE 6:e21830.  https://doi.org/10.1371/journal.pone.0021830 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Lesser MP, Jarett JK (2014) Culture-dependent and culture-independent analyses reveal no prokaryotic community shifts or recovery of Serratia marcescens in Acropora palmata with white pox. FEMS Microbiol Ecol 88:457–467.  https://doi.org/10.1111/1574-6941.12311 CrossRefPubMedGoogle Scholar
  66. 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 346:36–44.  https://doi.org/10.1016/j.jembe.2007.02.015 CrossRefGoogle Scholar
  67. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359.  https://doi.org/10.1038/nature04153 CrossRefPubMedGoogle Scholar
  68. Lobban CS, Raymundo LM, Montagnes DJS (2011) Porpostoma guamensis n. sp., a Philasterine scuticociliate associated with brown-band disease of corals. J Eukaryot Microbiol 58:103–113.  https://doi.org/10.1111/j.1550-7408.2010.00526.x CrossRefPubMedGoogle Scholar
  69. Lozada-Misa P, Kerr A, Raymundo L (2015) Contrasting lesion dynamics of white syndrome among the scleractinian corals Porites spp. PLoS ONE 10:1–14.  https://doi.org/10.1371/journal.pone.0129841 CrossRefGoogle Scholar
  70. Lynch SA, Armitage DV, Coughlan J, Mulachy MF, Culloty SC (2007) Investigating the possible role of benthic macroinvertebrates and zooplankton in the life cycle of the haplosporidian Bonamia ostreae. Exp Parasitoloogy 115:359–368.  https://doi.org/10.1016/j.exppara.2006.09.021 CrossRefGoogle Scholar
  71. Maynard J, van Hooidonk R, Eakin CM, Puotinen CM, Garren M, Williams GJ, Heron S, Lamb J, Weil E, Willis BL, Harvell CD (2015) Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat Clim Chang 5:688–694.  https://doi.org/10.1038/NCLIMATE2625 CrossRefGoogle Scholar
  72. McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modeled? Trends Ecol Evol 16:295–300.  https://doi.org/10.1016/S0169-5347(01)02144-9 CrossRefPubMedGoogle Scholar
  73. Mera H, Bourne DG (2018) Disentangling causation: complex roles of coral-associated microorganisms in disease. Environ Microbiol 20:431–449.  https://doi.org/10.1111/1462-2920.13958 CrossRefPubMedGoogle Scholar
  74. Miller MW, Williams DE (2007) Coral disease outbreak at Navassa, a remote Caribbean island. Coral Reefs 26:97–101.  https://doi.org/10.1007/s00338-006-0165-y CrossRefGoogle Scholar
  75. Miller J, Muller E, 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 28:925–937.  https://doi.org/10.1007/s00338-009-0531-7 CrossRefGoogle Scholar
  76. Miller MW, Marmet C, Cameron CM, Williams DE (2014) Prevalence, consequences, and mitigation of fireworm predation on endangered staghorn coral. Mar Ecol Prog Ser 516:187–194.  https://doi.org/10.3354/meps10996 CrossRefGoogle Scholar
  77. Moreira APB, Chimenno Tonon LA, Pereira VP, Alves N, Amado-Filho GM, Francini-Filho RB, Paranhos R, Thompson FL (2014) Culturable heterotrophic bacteria associated with healthy and bleached scleractinian Madracis decactis and the fireworm Hermodice carunculata from the remote St. Peter and St. Paul Archipelago, Brazil. Curr Microbiol 68:38–46.  https://doi.org/10.1007/s00284-013-0435-1 CrossRefPubMedGoogle Scholar
  78. Morrow KM, Ritson-Williams R, Ross C, Liles MR, Paul VJ (2012) Macroalgal extracts induce bacterial assemblage shifts and sublethal tissue stress in Caribbean corals. PLoS ONE 7:1–12.  https://doi.org/10.1371/journal.pone.0044859 CrossRefGoogle Scholar
  79. Muller EM, van Woesik R (2012) Caribbean coral diseases: primary transmission or secondary infection? Glob Chang Biol 18:3529–3535.  https://doi.org/10.1111/gcb.12019 CrossRefGoogle Scholar
  80. Newsom S (2006) Pioneers in infection control: John Snow, Henry Whitehead, the Broad Street pump, and the beginnings of geographical epidemiology. J Hosp Infect 64:210–216.  https://doi.org/10.1016/j.jhin.2006.05.020 CrossRefPubMedGoogle Scholar
  81. Nicolet KJ, Hoogenboom MO (2013) The corallivorous invertebrate Drupella aids in transmission of brown band disease on the Great Barrier Reef. Coral Reefs 32:585–595.  https://doi.org/10.1007/s00338-013-1010-8 CrossRefGoogle Scholar
  82. Nicolet KJ, Chong-Seng KM, Pratchett MS, Willis BL, Hoogenboom MO (2018) Predation scars may influence host susceptibility to pathogens: evaluating the role of corallivores as vectors of coral disease. Sci Rep 8:1–10.  https://doi.org/10.1038/s41598-018-23361-y CrossRefGoogle Scholar
  83. Nugues MM, Bak RPM (2009) Brown-band syndrome on feeding scars of the crown-of-thorn starfish Acanthaster planci. Coral Reefs 28:507–510.  https://doi.org/10.1007/s00338-009-0468-x CrossRefGoogle Scholar
  84. Nugues MM, Smith GW, van Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923.  https://doi.org/10.1111/j.1461-0248.2004.00651.x CrossRefGoogle Scholar
  85. Page CA, Willis BL (2008) Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation of this widespread coral disease. Coral Reefs 27:257–272.  https://doi.org/10.1007/s00338-007-0317-8 CrossRefGoogle Scholar
  86. Patterson KL, Porter JW, Ritchie KB, Polson SW, Mueller E, Peters EC, Santavy DL, Smith GW (2002) The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata. Proc Natl Acad Sci 99:8725–8730.  https://doi.org/10.1073/pnas.092260099 CrossRefPubMedGoogle Scholar
  87. Paull SH, Song S, McClure KM, Sackett LC, Marm Kilpatrick A, Johnson PTJ (2012) From superspreaders to disease hotspots: linking transmission across hosts and space. Front Ecol Environ 10:75–82.  https://doi.org/10.1890/110111 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Pollock FJ, Morris PJ, Willis BL, Bourne DG (2011) The urgent need for robust coral disease diagnostics. PLoS Pathog 7:e1002183.  https://doi.org/10.1371/journal.ppat.1002183 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Pollock FJ, Katz SM, Bourne DG, Willis BL (2013) Cymo melanodactylus crabs slow progression of white syndrome lesions on corals. Coral Reefs 32:43–48.  https://doi.org/10.1007/s00338-012-0978-9 CrossRefGoogle Scholar
  90. Pollock FJ, Krediet CJ, Garren M, Stocker R, Winn K, Wilson B, Huete-Stauffer C, Willis BL, Bourne DG (2015) Visualization of coral host–pathogen interactions using a stable GFP-labeled Vibrio coralliilyticus strain. Coral Reefs 34:655–662.  https://doi.org/10.1007/s00338-015-1273-3 CrossRefGoogle Scholar
  91. Pratchett MS, Graham NA, Sheppard CR, Mayes B (2010) Are infestations of Cymo melanodactylus killing Acropora cytherea in the Chagos archipelago? Coral Reefs 29:941.  https://doi.org/10.1007/s00338-010-0654-x CrossRefGoogle Scholar
  92. Pratte ZA, Richardson LL (2016) Possible links between white plague-like disease, scleractinian corals, and a cryptochirid gall crab. Dis Aquat Organ 122:153–161.  https://doi.org/10.3354/dao03074 CrossRefPubMedGoogle Scholar
  93. Randall CJ, van Woesik R (2015) Contemporary white-band disease in Caribbean corals driven by climate change. Nat Clim Chang 5:375–379.  https://doi.org/10.1038/nclimate2530 CrossRefGoogle Scholar
  94. Randall CJ, Jordan-Garza AG, Muller EM, van Woesik R (2016) Does dark-spot syndrome experimentally transmit among caribbean corals? PLoS ONE 11:1–16.  https://doi.org/10.1371/journal.pone.0147493 CrossRefGoogle Scholar
  95. Rath J, Ying WuK, Herndl GJ, DeLong EF (1998) High phylogenetic diversity in a marine-snow-associated bacterial assemblage. Aquat Microb Ecol 14:261–269.  https://doi.org/10.3354/ame014261 CrossRefGoogle Scholar
  96. Raymundo LJ, Harvell CD, Reynolds TL (2003) Porites ulcerative white spot disease: description, prevalence, and host range of a new coral disease affecting Indo-Pacific reefs. Dis Aquat Organ 56:95–104.  https://doi.org/10.3354/dao056095 CrossRefPubMedGoogle Scholar
  97. Raymundo LJ, Halford AR, Maypa AP, Kerr AM (2009) Functionally diverse reef-fish communities ameliorate coral disease. PNAS 106:17067–17070.  https://doi.org/10.1073/pnas.0900365106 CrossRefPubMedGoogle Scholar
  98. Raymundo LJ, Work TM, Miller RL, Lozada-Misa PL (2016) Effects of Coralliophila violacea on tissue loss in the scleractinian corals Porites spp. depend on host response. Dis Aquat Organ 119:75–83.  https://doi.org/10.3354/dao02982 CrossRefPubMedGoogle Scholar
  99. Richardson LL, Goldberg WM, Carlton R, Halas JC (1998) Coral disease outbreak in the Florida Keys: plague type II. Rev Biol Trop 46:187–198Google Scholar
  100. Riegl B (2002) Effects of the 1996 and 1998 positive sea-surface temperature anomalies on corals, coral diseases and fish in the Arabian Gulf (Dubai, UAE). Mar Biol 140:29–40.  https://doi.org/10.1007/s002270100676 CrossRefGoogle Scholar
  101. Rinkevich B (2004) Allorecognition and xenorecognition in reef corals: a decade of interactions. Hydrobiologia 530–531:443–450.  https://doi.org/10.1007/s10750-004-2686-0 CrossRefGoogle Scholar
  102. Rodriguez S, Croquer A, Guzman HM, Bastidas C (2009) A mechanism of transmission and factors affecting coral susceptibility to Halofolliculina sp. infection. Coral Reefs 28:67–77.  https://doi.org/10.1007/s00338-008-0419-y CrossRefGoogle Scholar
  103. Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91.  https://doi.org/10.3354/meps07531 CrossRefGoogle Scholar
  104. Ruiz GM, Rawlnigs TK, Dobbs FC, Drake LA, Mullady T, Huq A, Colwell RR (2000) Global spread of microorganisms by ships. Nature 408:49.  https://doi.org/10.1038/35040695 CrossRefPubMedGoogle Scholar
  105. Rutzler K, Santavy DL, Antonius A (1983) The black band disease of Atlantic reef corals. III. Distribution, ecology, and development. Mar Ecol 4:329–358.  https://doi.org/10.1111/j.1439-0485.1983.tb00118.x CrossRefGoogle Scholar
  106. Rypien KL, Baker DM (2009) Isotopic labeling and antifungal resistance as tracers of gut passage of the sea fan pathogen Aspergillus sydowii. Dis Aquat Organ 86:1–7.  https://doi.org/10.3354/dao02106 CrossRefPubMedGoogle Scholar
  107. 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 276:2795–2803.  https://doi.org/10.1098/rspb.2009.0481 CrossRefPubMedGoogle Scholar
  108. Sebens KP, Grace SP, Helmuth B, Maney EJ, Miles JS (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa and Porites porites, in a field enclosure. Mar Biol 131:347–360.  https://doi.org/10.1007/s002270050328 CrossRefGoogle Scholar
  109. Shapiro OH, Fernandez VI, Garren M, Guasto JS, Debaillon-Vesque FP, Kramarsky-Winter E, Vardi A, Stocker R (2014) Vortical ciliary flows actively enhance mass transport in reef corals. Proc Natl Acad Sci 111:13391–13396.  https://doi.org/10.1073/pnas.1323094111 CrossRefPubMedGoogle Scholar
  110. Sheridan C, Baele J, Kushmaro A, Frejaville Y, Eeckhaut I (2014) Terrestrial runoff influences white syndrome prevalence in SW Madagascar. Mar Environ Res 101:44–51.  https://doi.org/10.1016/j.marenvres.2014.08.003 CrossRefPubMedGoogle Scholar
  111. Shore A (2016) Ecology and epidemiology of Montipora white syndrome, a tissue loss disease of the Hawaiian coral, Montipora capitata. Dissertation, University of Hawaii at ManoaGoogle Scholar
  112. Shore-Maggio A, Callahan SM, Aeby GS (2018) Trade-offs in disease and bleaching susceptibility among two color morphs of the Hawaiian reef coral Montipora capitata. Coral Reefs.  https://doi.org/10.1007/s00338-018-1675-0 CrossRefGoogle Scholar
  113. Smith GW, Ives LD, Nagelkerken I, Ritchie K (1996) Caribbean sea-fan mortalities. Nature 383:487.  https://doi.org/10.1038/383487a0 CrossRefGoogle Scholar
  114. Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Organ 87:5–18.  https://doi.org/10.3354/dao02099 CrossRefPubMedGoogle Scholar
  115. Sokolow SH, Foley P, Foley JE, Hastings A, Richardson LL (2009) Disease dynamics in marine metapopulations: modelling infectious diseases on coral reefs. J Appl Ecol 46:621–631.  https://doi.org/10.1111/j.1365-2664.2009.01649.x CrossRefGoogle Scholar
  116. Stedman TL (2000) Stedman’s medical dictionary, 27th edn. Lippincott Williams and Wilkins, PhilidelphiaGoogle Scholar
  117. Sudek M, Williams GJ, Runyon C, Aeby GS, Davy SK (2015) Disease dynamics of Porites bleaching with tissue loss: prevalence, virulence, transmission, and environmental drivers. Dis Aquat Organ 113:59–68.  https://doi.org/10.3354/dao02828 CrossRefPubMedGoogle Scholar
  118. 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 5:250–255.  https://doi.org/10.1046/j.1462-2920.2003.00424.x CrossRefPubMedGoogle Scholar
  119. Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302.  https://doi.org/10.3354/meps266273 CrossRefGoogle Scholar
  120. Sutherland KP, Porter JW, Turner JW, Thomas BJ, Looney EE, Luna TP, Meyers MK, Futch JC, Lipp EK (2010) Human sewage identified as likely source of white pox disease of the threatened Caribbean elkhorn coral, Acropora palmata. Environ Microbiol 12:1122–1131.  https://doi.org/10.1111/j.1462-2920.2010.02152.x CrossRefPubMedGoogle Scholar
  121. Sutherland KP, Shaban S, Joyner JL, Porter JW, Lipp EK (2011) Human pathogen shown to cause disease in the threatened eklhorn coral Acropora palmata. PLoS ONE 6:e23468.  https://doi.org/10.1371/journal.pone.0023468 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Sutherland KP, Berry B, Park A, Kemp DW, Kemp KM, Lipp EK, Porter JW (2016) Shifting white pox aetiologies affecting Acropora palmata in the Florida Keys, 1994–2014. Philisophical Trans R Soc B 371:20150205.  https://doi.org/10.1098/rstb.2015.0205 CrossRefGoogle Scholar
  123. Sweet MJ, Bythell JC, Nugues MM (2013) Algae as reservoirs for coral pathogens. PLoS ONE 8:e69717.  https://doi.org/10.1371/journal.pone.0069717 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Ushijima B, Videau P, Burger AH, Shore-Maggio A, Runyon CM, Sudek M, Aeby GS, Callahan SM (2014) Vibrio coralliilyticus strain OCN008 is an etiological agent of acute Montipora white syndrome. Appl Environ Microbiol 80:2102–2109.  https://doi.org/10.1128/AEM.03463-13 CrossRefPubMedPubMedCentralGoogle Scholar
  125. Velthuis AGJ, Bouma A, Katsma WEA, Nodelijk G, De Jong MCM (2007) Design and analysis of small-scale transmission experiments with animals. Epidemiol Infect 135:202–217.  https://doi.org/10.1017/S095026880600673X CrossRefPubMedGoogle Scholar
  126. Vollmer SV, Kline DI (2008) Natural disease resistance in threatened staghorn corals. PLoS ONE 3:e3718.  https://doi.org/10.1371/journal.pone.0003718 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Adv Mar Biol 63:67–132.  https://doi.org/10.1016/B978-0-12-394282-1.00002-8 CrossRefPubMedGoogle Scholar
  128. Ward JR, Lafferty KD (2004) The elusive baseline of marine disease: Are diseases in ocean ecosystems increasing? PLoS Biol 2:542–547.  https://doi.org/10.1371/journal.pbio.0020120 CrossRefGoogle Scholar
  129. Williams DE, Miller MW (2005) Coral disease outbreak: pattern, prevalence and transmission in Acropora cervicornis. Mar Ecol Prog Ser 301:119–128.  https://doi.org/10.3354/meps301119 CrossRefGoogle Scholar
  130. Williams GJ, Knapp IS, Work TM, Conklin EJ (2011) Outbreak of Acropora white syndrome following a mild bleaching event at Palmyra Atoll, Northern Line Islands Central Pacific. Coral Reefs 30:621.  https://doi.org/10.1007/s00338-011-0762-2 CrossRefGoogle Scholar
  131. Wilson B, Muirhead A, Bazanella M, Huete-Stauffer C, Vezzulli L, Bourne DG (2013) An improved detection and quantification method for the coral pathogen Vibrio coralliilyticus. PLoS ONE 8:e81800.  https://doi.org/10.1371/journal.pone.0081800 CrossRefPubMedPubMedCentralGoogle Scholar
  132. Wolf AT, Nugues MM (2013) Synergistic effects of algal overgrowth and corallivory on Caribbean reef-building corals. Ecology 94:1667–1674.  https://doi.org/10.1890/12-0680.1 CrossRefPubMedGoogle Scholar
  133. Wolf AT, Nugues MM, Wild C (2014) Distribution, food preference, and trophic position of the corallivorous fireworm Hermodice carunculata in a Caribbean coral reef. Coral Reefs 33:1153–1163.  https://doi.org/10.1007/s00338-014-1184-8 CrossRefGoogle Scholar
  134. Work TM, Aeby GS (2006) Systematically describing gross lesions in corals. Dis Aquat Organ 70:155–160.  https://doi.org/10.3354/dao070155 CrossRefPubMedGoogle Scholar
  135. Work TM, Russell R, Aeby GS (2012) Tissue loss (white syndrome) in the coral Montipora capitata is a dynamic disease with multiple host responses and potential causes. Proc R Soc B 279:4334–4341.  https://doi.org/10.1098/rspb.2012.1827 CrossRefPubMedGoogle Scholar
  136. Zettler ER, Mincer TJ, Amaral-Zettler LA (2013) Life in the “plastisphere”: microbial communities on plastic marine debris. Environ Sci Technol 47:7137–7146.  https://doi.org/10.1021/es401288x CrossRefPubMedGoogle Scholar
  137. Zhenyu X, Shaowen K, Chaoqun H, Zhixiong Z, Shifeng W, Yongcan Z (2013) First characterization of bacterial pathogen, Vibrio alginolyticus, for Porites andrewsi white syndrome in the South China Sea. PLoS ONE 8:e75425.  https://doi.org/10.1371/journal.pone.0075425 CrossRefPubMedPubMedCentralGoogle Scholar
  138. 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:e4993.  https://doi.org/10.1371/journal.pone.0004993 CrossRefPubMedPubMedCentralGoogle Scholar
  139. Zvuloni A, Artzy-Randrup Y, Katriel G, Loya Y, Stone L (2015) Modeling the impact of white-plague coral disease in climate change scenarios. PLoS Comput Biol 11:e1004151.  https://doi.org/10.1371/journal.pcbi.1004151 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiosciencesRice UniversityHoustonUSA
  2. 2.Department of Marine Biotechnology, Institute of Marine and Environmental TechnologyUniversity of Maryland Baltimore CountyBaltimoreUSA
  3. 3.Hawaii Institute of Marine Biology, School of Ocean and Earth Science and TechnologyUniversity of Hawaii At ManoaKaneoheUSA
  4. 4.Department of BiologyStanford UniversityStanfordUSA

Personalised recommendations