Disease Problems

  • Ernesto WeilEmail author
Part of the Coral Reefs of the World book series (CORW, volume 12)


Worldwide ecological deterioration of coral reefs is mostly caused by disease-induced mass mortalities linked to thermal anomalies, and aided by local anthropogenic stressors. Mesophotic coral ecosystems (MCEs; 30–150 m) are found deeper where temperatures are cooler, in low light, and mostly offshore. These characteristics are proposed to protect MCEs (“deep reef refugia” hypothesis) from shallow-water threats (e.g., thermal stress and pollution). The most commonly reported mesophotic health problem is thermal-induced bleaching, which is now more widespread due to global climate change (GCC). The oldest deep bleaching report (90 m) is from 1989, in the Caribbean, but recent reports indicate bleached corals below 120 m in Grand Cayman. Cold-water intrusions and turbidity can also cause mesophotic coral bleaching. Not much is known about biotic diseases and potential drivers in MCEs. “White syndromes” (WS) seem to be the most common in Puerto Rico and the US Virgin Islands. Overall, 9 of the 28 common MCE scleractinian species have been observed with disease signs similar to shallow WS and white plague disease. A new disease termed “intercostal mortality syndrome” affected 19% of the colonies of Orbicella, Siderastrea, and Agaricia spp. in Hind Bank. MCE surveys showed coral community disease prevalence in Puerto Rico varied between 0% and 15%, with a mean of 6%. This chapter presents a summary of what is known about disease threats to MCEs and the disruptive potential of GCC-induced changes in seawater thermal dynamics on species susceptibility, and how this could affect the protection these deeper environments may provide.


Mesophotic coral ecosystems Thermal anomalies Biotic diseases Bleaching Climate change 



I would like to thank Kimberly Puglise and Yossi Loya for their kind invitation to be part of this important contribution. K. Puglise, E. Peters, and two anonymous reviewers provided constructive comments and corrections that helped to improve this chapter. Part of the work in Puerto Rico was supported by the National Oceanic and Atmospheric Administration’s (NOAA) National Centers for Coastal Ocean Science (NOAA/CSCOR; NA06NOS4780190 and NA10NOS42602223) through the Caribbean Coral Reef Institute (CCRI) at the Department of Marine Sciences, University of Puerto Rico, Mayagüez (DMS-UPRM). The project could not have gone through without the participation of Drs. R. Appeldoorn, C. Sherman, Nick Schizas, F. Pagan, D. Ballantine, and P. Yoshioka and our students M. Lucas, D. Soto, I. Bejarano, M. Nemeth, M. Schärer, and H. Ruiz. Mr. Milton Carlo, Diving Safety Officer of DMS-UPRM, was an integral component of the diving team and also provided extensive logistical support throughout field operations. D. Kesling, T. Dunmire, and S. Fowler, NOAA Undersea Research Center at the University of North Carolina Wilmington, and T. Cerezo, Puerto Rico Technical Diving Center, assisted with both diver training and field operations support. I would like to thank the captain and crew of the Nekton and Spree vessels for their logistical and personal support during the cruises. Photo-transects were taken by H. Ruiz and M. Nemeth. Other photos and video were provided by D. Kesling and our ROV operated by R. Appeldoorn and F. Pagan. T. Smith and GP Schmahl provided photos from the USVI and the Flower Gardens, respectively. I thank the DMS-UPR for logistical support throughout the projects.


  1. Andradi-Brown D, Laverick J, Bejarano I, Bridge T, Colin PL, Eyal G, Jones R, Kahng SE, Reed J, Smith TB, Spalding HL, Weil E, Wood E (2016) Threats to mesophotic coral ecosystems and management options. In: Baker EK, Puglise KA, Harris PT (eds) Mesophotic coral ecosystems—a lifeboat for coral reefs? United Nations Environment Programme and GRID-Arendal, Nairobi, pp 67–82Google Scholar
  2. Appeldoorn RS, Ballantine D, Bejarano I, Carlo M, Nemeth M, Otero E, Pagan F, Ruiz H, Schizas N, Sherman, Weil E (2015) Mesophotic coral ecosystems under anthropogenic stress: a case study at Ponce, Puerto Rico. Coral Reefs 35:63–75CrossRefGoogle Scholar
  3. Appeldoorn RS, Ballantine D, Bejarano I, Ruiz H, Schizas N, Schmidt W, Sherman C, Weil E (2016) Mesophotic coral ecosystems examined: La Parguera, Puerto Rico. In: Baker EK, Puglise KA, Harris PT (eds) Mesophotic coral ecosystems—a lifeboat for coral reefs? United Nations Environment Programme and GRID-Arendal, Nairobi, pp 45–49Google Scholar
  4. Appeldoorn RS, Alfaro M, Ballantine DL, Bejarano I, Ruíz HJ, Schizas NV, Schmidt WE, Sherman CE, Weil E (2019) Puerto Rico. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 111–129CrossRefGoogle Scholar
  5. Armstrong RA, Singh H, Torres J, Nemeth RS, Can A, Roman C, Eustice R, Riggs L, Garcia-Moliner G (2006) Characterizing the deep insular shelf coral reef habitat of the Hind Bank Marine Conservation District (US Virgin Islands) using the Seabed autonomous underwater vehicle. Cont Shelf Res 26:194–205CrossRefGoogle Scholar
  6. Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. In: Porter JW (ed) The ecology and etiology of newly emerging marine diseases, developments in hydrobiology. Kluwer, Dordrecht, pp 23–35Google Scholar
  7. Baird A, Guest J, Willis B (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Syst 40:551–575CrossRefGoogle Scholar
  8. Bak RPM, Nieuwland G, Meesters EH (2005) Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curaçao and Bonaire. Coral Reefs 24:475–479CrossRefGoogle Scholar
  9. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  10. Baker EK, Puglise KA, Colin P, Harris PT, Kahn SE, Rooney JJ, Sherman C, Slattery M, Spalding HL (2016a) What are mesophotic coral ecosystems? In: Baker EK, Puglise KA, Harris PT (eds) Mesophotic coral ecosystems—a lifeboat for coral reefs? United Nations Environment Programme and GRID-Arendal, Nairobi, pp 11–16Google Scholar
  11. Baker EK, Puglise KA, Harris PT (2016b) Mesophotic coral ecosystems—a lifeboat for coral reefs? United Nations Environment Programme and GRID-Arendal, Nairobi/Arendal, 98 pGoogle Scholar
  12. Ballantine D, Weil E, Ruiz H (2005) Coralline white band syndrome, a coralline algal affliction in the tropical Atlantic. Coral Reefs 24:117CrossRefGoogle Scholar
  13. Ballantine D, Appeldoorn R, Yoshioka P, Weil E, Armstrong R, Garcia J, Otero E, Pagan F, Sherman C, Hernandez-Delgado E (2008) Biology and ecology of Puerto Rican coral reefs. In: Riegl BM, Dodge RE (eds) Coral reefs of the USA. Springer, Dordrecht, pp 375–406CrossRefGoogle Scholar
  14. Bongaerts P, Smith TB (2019) Beyond the “Deep Reef Refuge” hypothesis: a conceptual framework to characterize persistence at depth. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 881–895Google Scholar
  15. Bongaerts P, Ridgway P, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘Deep Reef Refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29(2):309–328CrossRefGoogle Scholar
  16. Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-Guldberg O (2015a) Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. R Soc Open Sci 2(2):140297CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KRW, Bak RPM, Vermeij MJA, Hoegh-Guldberg O (2015b) Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci Rep 5:7652CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bouchon C (1981) Quantitative study of the scleractinian coral communities of a fringing reef of Reunion Island (Indian Ocean). Mar Ecol Prog Ser 4:273–288CrossRefGoogle Scholar
  19. Bridge TCL, Fabricius KE, Bongaerts P, Wallace CC, Muir PR, Done TJ, Webster JM (2012) Diversity of scleractinia and octocorallia in the mesophotic zone of the Great Barrier Reef, Australia. Coral Reefs 31:179–189CrossRefGoogle Scholar
  20. Brown BE, Dunne RW (2016) Coral bleaching: the roles of temperature and solar radiation. In: Woodley CM, Downs CA, Bruckner AW, Porter JW, Galloway SB (eds) Diseases of coral, 1st edn. Wiley, New York, pp 266–283Google Scholar
  21. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and sub-regional comparisons. PLoS ONE 2:e711CrossRefPubMedPubMedCentralGoogle Scholar
  22. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:e124CrossRefPubMedPubMedCentralGoogle Scholar
  23. Burge CA, Eakin CM, Friedman CS, Froelich B, Hershberger PK, Hofmann EF, Petes LE, Prager KC, Weil E, Willis BL, Ford SE, Harvell CW (2014) Climate change influences on marine infectious diseases: implications for management and society. Annu Rev Mar Sci 6:249–277CrossRefGoogle Scholar
  24. Burge CA, Friedman CS, Getchell R, House M, Lafferty KD, Mydlarz LD, Prager KC, Sutherland KP, Renault T, Kiryu I, Vega-Thurber R (2016) Complementary approaches to diagnosing marine diseases: a union of the modern and the classic. Philos Trans R Soc B 371:20150207CrossRefGoogle Scholar
  25. Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington, DCGoogle Scholar
  26. Carpenter K, Abrar M, Aeby G et al (2008) One third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563CrossRefGoogle Scholar
  27. Cassola GE, Pacheco MC, Barbosa MC, Hansen DM, Ferreira CE (2016) Decline in abundance and health state of an Atlantic subtropical gorgonian population. Mar Pollut Bull 104(1–2):329–334CrossRefGoogle Scholar
  28. Croquer A, Weil E (2009) Local and geographic variability in distribution and prevalence of coral and octocoral diseases in the Caribbean II: genera-level analysis. Dis Aqua Org Vol 83:209–223CrossRefGoogle Scholar
  29. Dubinsky Z, Stambler N (eds) (2011) Coral reefs: an ecosystem in transition. Springer, Dordrecht, 552 pGoogle Scholar
  30. Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Weil E et al (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5(11):e13969CrossRefPubMedPubMedCentralGoogle Scholar
  31. Englebert N, Bongaerts P, Muir P et al (2015) Deepest zooxanthellate corals of the great barrier reef and Coral Sea. Mar Biodivers 45(1):1–2CrossRefGoogle Scholar
  32. Enríquez S, Méndez ER, Prieto RI (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50(4):1025–1032CrossRefGoogle Scholar
  33. García-Sais JR (2010) Reef habitats and associated sessile-benthic and fish assemblages across a euphotic-mesophotic depth gradient in Isla Desecheo, Puerto Rico. Coral Reefs 29(2):277–288CrossRefGoogle Scholar
  34. García-Sais JR, Appeldoorn R, Battista T, Bauer L, Bruckner A, Caldow C, Carrubba L, Corredor J, Diaz E, Lilyestrom C, García-Moliner G, Hernández-Delgado E, Menza C, Morell J, Pait A, Sabater J, Weil E, Williams E, Williams S (2008) The state of coral reef ecosystems in Puerto Rico. In: Waddell JE, Clarke AM (eds) The state of coral reef ecosystems of the United States and Pacific freely associated states, NOAA Technical Memorandum NOS NCCOS 73. U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service, National Centers for Coastal Ocean Science, Silver Spring, pp 75–116Google Scholar
  35. García-Sais JR, Williams SM, Sabater-Clavell J, Esteves R, Carlo M (2014) Mesophotic benthic habitats and associated reef communities at Lang Bank, St. Croix, USVI. Caribbean Fishery Management Council, San Juan, 69 pGoogle Scholar
  36. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960CrossRefGoogle Scholar
  37. Ghiold J, Smith S (1990) Bleaching and recovery of deep-water, reef-dwelling invertebrates in the Cayman Islands, BWI. Caribb J Sci 26:52–61Google Scholar
  38. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2:495–509CrossRefGoogle Scholar
  39. Goreau TF, Goreau NI (1973) The ecology of Jamaican coral reefs. II. Geomorphology, zonation and sedimentary phases. Bull Mar Sci 23:399–464Google Scholar
  40. Goreau TF, Land LS (1974) Fore-reef morphology and depositional processes, North Jamaica. In: Laporte LF (ed) Reefs in time and space. Society of Economic Paleontologists and Mineralogists, Special Publication, vol 18, pp 77–89Google Scholar
  41. Goreau TF, Wells JW (1967) The shallow-water scleractinian of Jamaica: revised list of species and their vertical distribution range. Bull Mar Sci 17(2):442–453Google Scholar
  42. Grammer GM, Ginsburg RN (1992) High stand versus low stand deposition on carbonate platform margins: insights from quaternary fore-slopes in the Bahamas. Mar Geol 103:125–136CrossRefGoogle Scholar
  43. Groner M, Breyta R, Dobson A, Friedmann C, Froelich B, Garren M, Gullard F, Maynar J, Weil E, Wyllie-Echeverria S, Harvell D (2015) Emergency responses for marine diseases. Science 347(6227):1210CrossRefPubMedPubMedCentralGoogle Scholar
  44. Groner M, Maynard J, Breyta R, Carnegie B, Dobson A, Friedman CS, Froelich B, Garren M, Gulland FMD, Heron SF, Noble RT, Revie CW, Shields JD, Vanderstichel R, Weil E, Wyllie-Echeverria S, Harvell CD (2016) Managing marine disease emergencies in an era of rapid change. Philos Trans R Soc B 371:20150364CrossRefGoogle Scholar
  45. Halley RB, Garrison VE, Ciembronowicz KT, Edwards R, Jaap WC, Mead G, Earle S, Hine AC, Jarrett BD, Locker SD, Naar DF, Donahue B, Dennis GD, Twichell DC (2003) Pulley ridge—the US deepest coral reef? Joint conference on the science and restoration of the greater everglades and Florida bay ecosystem from Kissimmee to the keys, GEER program and abstracts, Palm Harbor, pp 238–240Google Scholar
  46. Halley R, Dennis GP, Weaver D, Coleman F (2005) Characterization of pulley ridge coral and fish fauna. NOAA CRCP Habitat Characterization of Pulley Ridge and the Florida Middle Grounds, 36 pGoogle Scholar
  47. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet AM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505–1510CrossRefPubMedPubMedCentralGoogle Scholar
  48. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risk for terrestrial and marine biota. Science 296:2158–2162CrossRefGoogle Scholar
  49. Harvell D, Markel S, Jordan-Dahlgren E, Raymundo L, Rosenberg E, Smith GW, Willis B, Weil E (2007) Coral disease, environmental drivers and the balance between coral and microbial associates. Oceanography 20(1):36–59CrossRefGoogle Scholar
  50. Harvell CD, Altizer S, Cattadori IM, Harrington L, Weil E (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90(4):912–920CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hernandez-Delgado E (2015) The emerging threats of climate change on tropical coastal ecosystems, public health, local economies and livelihood sustainability of small islands: cumulative impacts and synergies. Mar Pollut Bull 101:5–28CrossRefPubMedPubMedCentralGoogle Scholar
  52. Herzlieb S, Kadison E, Blondeau J, Nemeth RS (2006) Comparative assessment of coral reef systems located along the insular platform of St. Thomas, US Virgin Islands and the relative effects of natural and human impacts. In: Proceedings of the 10th International Coral Reef Symposium, Okinawa, JapanGoogle Scholar
  53. Hickerson EL, Schmahl GP, Robbart M, Precht WF, Caldow C (2008) State of coral reef ecosystems of the flower garden banks, Stetson Bank, and other banks in the Northwestern Gulf of Mexico. In: Waddell JE, Clarke AM (eds) The state of coral reef ecosystems of the United States and Pacific freely associated states: 2008, NOAA Technical Memorandum NOS NCCOS 73. U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service, National Centers for Coastal Ocean Science, Silver SpringGoogle Scholar
  54. Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on “Mesophotic coral ecosystems: characterization, ecology and management.” Coral Reefs 29:247–251CrossRefGoogle Scholar
  55. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s corals. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  56. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528CrossRefPubMedPubMedCentralGoogle Scholar
  57. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfeld P, Gomez E, Harvel CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RFH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefGoogle Scholar
  58. Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S (2017) Coral reef ecosystems under climate change and ocean acidification. Front Mar Sci 4:158CrossRefGoogle Scholar
  59. Hoeksema BH, Bongaerts P, Baldwin CC (2014) High coral cover at lower mesophotic depths: a dense Agaricia community at the leeward side of Curaçao, Dutch Caribbean. Mar Biodivers 47(1):67–70CrossRefGoogle Scholar
  60. Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407CrossRefPubMedPubMedCentralGoogle Scholar
  61. Holstein DM, Fletcher P, Groves SH, Smith TB (2019) Ecosystems services of mesophotic coral ecosystems and a call for better accounting. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 943–956CrossRefGoogle Scholar
  62. Hughes TP (1994) Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefGoogle Scholar
  63. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  64. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedPubMedCentralGoogle Scholar
  65. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cummins GS, Dalton SJ, Diaz-Pulido G, Eakin ME, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo C, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MJ, Verena Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–378CrossRefGoogle Scholar
  66. Iglesias-Prieto R, Beltran VH, Lajeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond 271:1757–1763CrossRefGoogle Scholar
  67. IPCC (2014) In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: impacts, adaptation, and vulnerability. Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge/New YorkGoogle Scholar
  68. Jackson JBC, Donovan MK, Cramer KL, Lam VV (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef Monitoring Network, IUCN, Gland, 304 pGoogle Scholar
  69. James NP, Ginsburg R (1979) The seaward margin side of Belize barrier and atoll reefs. International Association of Sedimentology, Special Publication, vol 3, 191 pGoogle Scholar
  70. Jarret BD, Hine AC, Halley RB, Naar DF, Locker SD, Newmann AC, Twichell D, Hu C, Donahue BT, Jaap WC, Palandro D, Ciembronowiccz K (2005) Strange fellows—a deep water hermatypic coral reefs superimposed on a drowned barrier island; southern pulley ridge, SW Florida platform margin. Mar Geol 214:295–307CrossRefGoogle Scholar
  71. Kahng SE (2014) Unlocking the secrets of Hawaii’s deep-water photosynthetic corals. Reef Encount 29(1):19–22Google Scholar
  72. Kahng SE, Kelley CD (2007) Vertical zonation of the megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au‘au channel, Hawaii. Coral Reefs 26:679–687Google Scholar
  73. Kahng SE, Maragos JE (2006) The deepest, zooxanthellate scleractinian corals in the world? Coral Reefs 25:254CrossRefGoogle Scholar
  74. Kahng SE, García-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275Google Scholar
  75. Kahng SE, Hochberg EJ, Apprill A, Wagner D, Luck DG, Perez D, Bidigare RR (2012) Efficient light harvesting in deep-water zooxanthellate corals. Mar Ecol Prog Ser 455:65–77CrossRefGoogle Scholar
  76. Kahng SE, Copus J, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81CrossRefGoogle Scholar
  77. Knowlton N, Caley J, Brainard R (2010) Census of Marine Life, Coral Reefs Ecosystems. Accessed 17 Mar 2018
  78. Kuhlmann DHH (1983) Composition and ecology of deep water coral associations. Helgoländer Meeresun 36:183–204CrossRefGoogle Scholar
  79. Lafferty KD, Hofmann EE (2016) Marine disease impacts, diagnosis, fore-casting, management and policy. Philos Trans R Soc B 371:20150200CrossRefGoogle Scholar
  80. Lang JC, Wicklund RI, Dill RP (1988) Depth- and habitat- related bleaching of zooxanthellate reef organisms near Lee Stocking Island, Exuma Keys, Bahamas. Proc 6th Int Coral Reef Symp Aust 3:269–274Google Scholar
  81. Leichter JJ, Genovese SJ (2006) Intermittent upwelling and subsidized growth of the scleractinian coral Madracis mirabilis on the deep fore-reef slope of Discovery Bay, Jamaica. Mar Ecol Prog Ser 316:95–103CrossRefGoogle Scholar
  82. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 405–419CrossRefGoogle Scholar
  83. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8Google Scholar
  84. Littler MM, Littler DS (1994) A pathogen of reef-building coralline algae discovered in the South Pacific. Coral Reefs 13:202CrossRefGoogle Scholar
  85. Littler M, Littler D (1995) Impact of CLOD pathogen on Pacific coral reefs. Science 267:1356–1360CrossRefPubMedPubMedCentralGoogle Scholar
  86. Locker SD, Armstrong RA, Battista TA, Rooney JJ, Sherman C, Zawada DG (2010) Geomorphology of mesophotic coral ecosystems: current perspectives on morphology, distribution, and mapping strategies. Coral Reefs 29(2):329–345CrossRefGoogle Scholar
  87. Maynard J, van Hooidonk R, Eakin MC, Puotinen M, Heron SF, Garren M, Lamb J, Williams G, Weil E, Willis B, Harvell CD (2015) Climate projections of conditions that increase coral disease susceptibility and pathogen virulence. Nat Clim 5:688–694CrossRefGoogle Scholar
  88. McClanahan TR, Weil E, Cortés J, Baird A, Ateweberhan M (2009) Consequences of coral bleaching for sessile organisms. In: van Oppen M, Lough J (eds) Coral bleaching: patterns, processes, causes and consequences. Springer-Verlag, Berlin, pp 121–138CrossRefGoogle Scholar
  89. McClanahan T, Weil E, Baird A (2018) Impact of bleaching on coral reefs. In: van Oppen M, Lough (eds) Coral bleaching: patterns, processes, causes and consequences, 2nd edn. Springer, Berlin, pp 231–264Google Scholar
  90. McClenachan L, O’Connor G, Neal BP, Pandolfi JM, Jackson JBC (2017) Ghost reefs: nautical charts document large spatial scale of coral reef loss over 240 years. Sci Adv 3:e1603155CrossRefPubMedPubMedCentralGoogle Scholar
  91. Menza C, Kendall M, Rogers C, Miller J (2007) A deep reef in deep trouble. Cont Shelf Res 27:2224–2230CrossRefGoogle Scholar
  92. Miller J, Rogers C, Waara R (2001) Monitoring the coral disease plague type II on coral reefs of St. John, US Virgin Islands. In: Proceedings of the 30th Scientific Meeting of the Association of Marine Laboratories of the Caribbean, Puerto Rico. Rev Biol Trop 51(Suppl 4):47–56Google Scholar
  93. Miller J, Muller E, Rogers CS, 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
  94. Mumby PJ (2017) Embracing a world of subtlety and nuance on coral reefs. Coral Reefs 36:1003–1011CrossRefGoogle Scholar
  95. Mumby PJ, Flower J, Chollet I et al (2014) Towards reef resilience and sustainable livelihoods. A handbook for Caribbean coral reef managers. University of Exeter, Exeter, 172 pGoogle Scholar
  96. Neal BP, Condit C, Liu G, dos Santos S, Kahru M, Mitchell BG, Kline DI (2014) When depth is no refuge: cumulative thermal stress increases with depth in Bocas del Toro, Panama. Coral Reefs 33(1):193–205CrossRefGoogle Scholar
  97. Nir O, Gruber DF, Shemesh E, Glasser E, Tchernov D (2014) Seasonal mesophotic coral bleaching of Stylophora pistillata in the Northern Red Sea. PLoS ONE 9(1):e84968CrossRefPubMedPubMedCentralGoogle Scholar
  98. Ogden JC, Wicklund RI (eds) (1988) Mass bleaching of coral reefs in the Caribbean: a research strategy. National Undersea Research Program, NOAA Research Report, 88–2, 51pGoogle Scholar
  99. Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30(2):429–440CrossRefGoogle Scholar
  100. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333(6041):418–422CrossRefPubMedPubMedCentralGoogle Scholar
  101. Peters E (2015) Diseases of coral reefs organisms. In: Birkeland C (ed) Coral reefs in the Anthropocene, 8:147–78Google Scholar
  102. Prada C, Weil E, Yoshioka P (2010) Octocoral bleaching under unusual thermal stress. Coral Reefs 29(1):41–45CrossRefGoogle Scholar
  103. Pyle RL, Boland R, Bolick H, Bowen B, Bradley CJ, Kane C, Kosaki RK, Langston R, Longenecker K, Montgomery AD, Parrish FA, Popp BN, Rooney J, Smith CM, Wagner D, Spalding HL (2016) A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago. PeerJ 4:e2475CrossRefPubMedPubMedCentralGoogle Scholar
  104. Randall CJ, Jordan-Garza AG, Muller EM, van Woesik R (2014) Relationships between the history of thermal stress and the relative risk of diseases of Caribbean corals. Ecology 95(7):1981–1994CrossRefPubMedPubMedCentralGoogle Scholar
  105. Raymundo LJ, Couch CS, Harvell CD (eds) (2008) Coral disease handbook. Guidelines for assessment, monitoring and managing. GEF-CRTR program. Currie Communications, Australia, 121 pGoogle Scholar
  106. Reaka-Kudla ML (1997) The global biodiversity of coral reefs: a comparison with rain forests. In: Reaka-Kudla ML, Wilson DE, Wilson EO (eds) Biodiversity II. Joseph Henry Press, Washington, DC, pp 83–108Google Scholar
  107. Reed JK (1985) Deepest distribution of Atlantic hermatypic corals discovered in the Bahamas. Proceedings of the 5th International Coral Reef Symposium, 6, pp 249–254Google Scholar
  108. Reed JK, Farrington S, Harter S, David A, Moe H, Horn L, Taylor G, White J, Voss J, Pomponi S, Diaz C, Hanisak D (2017) Characterization of the mesophotic coral/sponge habitats and fish assemblages in the regions of Pulley Ridge and Tortugas from ROV dives during R/V Walton Smith cruises 2012 to 2015. Harbor Branch Oceanographic Institute Technical Report 178, 76 pGoogle Scholar
  109. Reed JK, Farrington S, David A, Harter S, Pomponi S, Diaz MC, Voss JD, Spring KD, Hine AC, Kourafalou V, Smith RH, Vaz AC, Paris CB, Hanisak MD (2019) Pulley Ridge, Gulf of Mexico, U.S.A. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 57–69CrossRefGoogle Scholar
  110. Reigl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531CrossRefGoogle Scholar
  111. Richardson LL (1998) Coral diseases: what is really known? Trends Ecol Evol 13(11):438–443CrossRefPubMedPubMedCentralGoogle Scholar
  112. Richardson LL, Aronson RB (2002) Infectious diseases of reef corals. In: Proceedings of the 9th International Coral Reef Symposium, Bali, 2000, 2, pp 225–1230Google Scholar
  113. Richardson LL, Goldberg WM, Carlton RG, Halas JC (1998a) Coral disease outbreak in the Florida Keys: plague type II. Rev Biol Trop 46:187–198Google Scholar
  114. Richardson LL, Goldberg WM, Kuta KG, Aronson RB, Smith GW, Ritchie KB, Halas JC, Feingold JS, Miller M (1998b) Florida’s mystery coral killer identified. Nature 392:557–558CrossRefGoogle Scholar
  115. Richmond RH (1993) Coral reefs: present problems and future concerns resulting from anthropogenic disturbance. Integr Comp Biol 33(6):524–536Google Scholar
  116. Ritchie KB (2006) Regulation of microbial populations by mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  117. Rivero-Calle S, Armstrong RA, Soto-Santiago FJ (2009). Biological and physical characteristics of a mesophotic coral reef: Black Jack Reef, Vieques, Puerto Rico. In: Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, Florida, pp 574–578Google Scholar
  118. Rogers CS, Miller J, Muller EM, Edmunds P, Nemeth RS, Beets J, Friedlander AM, Smith TB, Boulon R, Jeffrey CFG, Menza C, Caldow C, Idrisi N, Kojis B, Monaco ME, Spitzack A, Gladfelter EH, Ogden JC, Hillis-Starr Z, Lundgren I, Schill WB, Kuffner IB, Richardson LL, Devine BE, Voss JD (2008a) Ecology of coral reefs in the US Virgin Islands. In: Riegl BM, Dodge RE (eds) Coral reefs of the USA. Springer, Dordrecht, pp 303–373CrossRefGoogle Scholar
  119. Rogers CS, Miller J, Muller EM (2008b) Coral diseases following massive bleaching in 2005 cause 60 percent decline in coral cover and mortality of the threatened species, Acropora palmata, on reefs in the U.S. Virgin Islands. USGS Fact Sheet 2008–3058Google Scholar
  120. Rogers AD, Kemp KM, Davies AJ, Taylor ML (2016) The diseases of deep-water corals. In: Woodley CM, Downs CA, Bruckner AW, Porter JW, Galloway SB (eds) Diseases of coral, 1st edn. Wiley, Hoboken, pp 416–443Google Scholar
  121. Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326CrossRefPubMedPubMedCentralGoogle Scholar
  122. Rosenberg E, Loya Y (eds) (2004) Coral reef health and diseases. Springer, BerlinGoogle Scholar
  123. Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408(6814):850–853CrossRefGoogle Scholar
  124. Selig ER, Harvell CD, Bruno JF, Willis BL, Page CA et al (2006) Analyzing the relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney J, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. American Geophysical Union, Washington, DC, pp 111–128CrossRefGoogle Scholar
  125. Sherman C, Nemeth M, Ruiz H, Bejarano I, Appeldoorn R, Pagán F, Schärer M, Weil E (2010) Geomorphology and mesophotic coral ecosystems of the upper insular slope of Southwest Puerto Rico. Coral Reefs 29:347–360CrossRefGoogle Scholar
  126. Sherman C, Appeldoorn R, Ballantine D, Bejarano I, Carlo M, Kesling D, Nemeth M, Pagan F, Ruiz H, Schizas N, Weil E (2013) Exploring the mesophotic zone: diving operations and scientific highlights of three research cruises (2010–2012) across Puerto Rico and US Virgin Islands. In: Proceedings of the AAUS Symposium, Curaçao. American Academy of Underwater Sciences, Dauphin Island, pp 297–312Google Scholar
  127. Sinniger F, Morita M, Harii S (2013) “Locally extinct” coral species Seriatopora hystrix found at upper mesophotic depths in Okinawa. Coral Reefs 32:153CrossRefGoogle Scholar
  128. Sinniger F, Ballantine D, Bejarano I, Colin P, Pochon X, Pomponi SA, Puglise KA, Pyle RL, Reaka M, Spalding HL, Weil E (2016) Biodiversity of mesophotic coral ecosystems. In: Baker EK, Puglise KA, Harris PT (eds) Mesophotic coral ecosystems—a lifeboat for coral reefs? United Nations Environment Programme and GRID-Arendal, Nairobi, pp 50–62Google Scholar
  129. Sinniger F, Prasetia R, Yorifuji M, Bongaerts P, Harii S (2017) Seriatopora diversity preserved in upper mesophotic coral ecosystems in southern Japan. Front Mar Sci 4:155CrossRefGoogle Scholar
  130. Smith TB, Nemeth RS, Blondeau J, Calnan JM, Kadison E, Herzlieb S (2008) Assessing coral reef health across onshore to offshore stress gradients in the US Virgin Islands. Mar Pollut Bull 56:1983–1991CrossRefGoogle Scholar
  131. Smith TB, Blondeau J, Nemeth RS, Pittman SJ, Calnan JM, Kadison E, Gass J (2010) Benthic structure and cryptic mortality in a Caribbean mesophotic coral reef bank system, the Hind Bank Marine Conservation District, U.S. Virgin Islands. Coral Reefs 29:289–308CrossRefGoogle Scholar
  132. Smith TB, Gyory J, Brandt ME, Miller WJ, Jossart J, Nemeth RS (2016) Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Glob Chang Biol 8:2756–2765CrossRefGoogle Scholar
  133. Smith TB, Brandt ME, Brandtneris VW, Ennis RS, Groves SH, Habtes S, Holstein DM, Kadison E, Nemeth RS (2019) The United States Virgin Islands. In: Loya Y, Puglise KA, Bridge TCL (eds) Mesophotic coral ecosystems. Springer, New York, pp 131–147CrossRefGoogle Scholar
  134. Sunagawa S, DeSantis TZ, Piceno YM, Brodie EL, DeSalvo MK, Voolstra CR, Weil E, Andersen GL, Medina M (2009) Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata assessed by 16S rRNA microarray analysis and clone library sequencing. ISME J 3:1–10CrossRefGoogle Scholar
  135. 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
  136. Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastraea annularis. Coral Reefs 8:217–224CrossRefGoogle Scholar
  137. Tyler EHM, Speight MR, Henderson P, Manica A (2009) Evidence for a depth refuge effect in artisanal coral reef fisheries. Biol Conserv 142:652–667CrossRefGoogle Scholar
  138. van Oppen M, Lough J (eds) (2009) Coral bleaching: patterns, processes, causes and consequences. Ecological studies. Springer, BerlinGoogle Scholar
  139. van Oppen MJH, Lough JM (eds) (2018) Coral bleaching: patterns, processes, causes and consequences. Ecological Studies, vol 233, 2nd edn. Springer, Berlin, p 355Google Scholar
  140. Vargas B (2010) Crustose coralline algal diseases in the US-Affiliated Pacific islands. Coral Reefs 29:943–956CrossRefGoogle Scholar
  141. Ward JR, Lafferty K (2004) The elusive base- line of marine disease: are marine diseases in ocean ecosystems increasing? PLoS Biol 2:542–547Google Scholar
  142. Weil E (2004) Coral reef diseases in the wider Caribbean. In: Rosenberg E, Loya Y (eds) Coral reef health and diseases. Springer, Berlin, pp 35–68Google Scholar
  143. Weil E, Croquer A (2009) Local and geographic variability in distribution and prevalence of coral and octocoral diseases in the Caribbean I: community-level analysis. Dis Aquat Org 83:195–208CrossRefPubMedPubMedCentralGoogle Scholar
  144. Weil E, Hooten AJ (2008) Underwater cards for assessing coral health on Caribbean reefs. GEF-CRTR Program, Center for Marine Sciences, University of Queensland, Brisbane, 24 pGoogle Scholar
  145. Weil E, Rogers CS (2011) Coral reef disease in the Atlantic-Caribbean. In: Dubinski Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer-Verlag, New York, pp 465–492CrossRefGoogle Scholar
  146. Weil E, Smith GW, Gil-Agudelo D (2006) Status and progress in coral reef disease research. Dis Aquat Org 69:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  147. Weil E, Croquer A, Urreiztieta I (2009a) Temporal variability and consequences of coral diseases and bleaching in La Parguera, Puerto Rico from 2003–2007. Caribb J Sci 45(2–3):221–246CrossRefGoogle Scholar
  148. Weil E, Cróquer A, Urreiztieta I (2009b) Yellow band disease compromises the reproductive output of the reef-building coral Montastraea faveolata (Anthozoa, Scleractinia). Dis Aquat Org 87:45–55CrossRefPubMedPubMedCentralGoogle Scholar
  149. Weil E, Rogers CS, Croquer A (2017) Octocoral diseases in a changing sea. In: Rossi S, Gori A, Orejas Seco del Valle C (eds) Marine animal forests: the ecology of benthic biodiversity hotspots. Springer, SwitzerlandGoogle Scholar
  150. Wilkinson C (2004) Status of coral reefs of the world: 2004, vol I, II. Global Coral Monitoring Network and Australian Institute of Marine Sciences, Townsville, 553 pGoogle Scholar
  151. Wilkinson C, Souter D (2008) Status of Caribbean coral reefs after bleaching and hurricanes in 2005. Global Coral Reef Monitoring Network, and Reef and Rainforest Research Centre, Townsville, 152 pGoogle Scholar
  152. Williams EH, Bunkley-Williams L (1988) Bleaching of Caribbean coral reef symbionts in 1987–88. In: Proceedings of the 6th International Coral Reef Symposium, Australia, vol 3, pp 313–318Google Scholar
  153. Williams EH, Bunkley-Williams L (1990) The worldwide coral bleaching cycle and related sources of coral mortality. Atoll Res Bull 335:1–71CrossRefGoogle Scholar
  154. Willis BL, Page CA, Dinsdale EA (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 69–104CrossRefGoogle Scholar
  155. Woodley CM, Downs CA, Bruckner AW, Porter JW, Galloway SB (eds) (2016) Diseases of coral, 1st edn. Wiley, HobokenGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of Puerto RicoMayagüezUSA

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