Coral Reefs

, Volume 34, Issue 1, pp 109–118 | Cite as

Mass mortality events of the coral Balanophyllia europaea (Scleractinia, Dendrophylliidae) in the Mljet National Park (eastern Adriatic Sea) caused by sea temperature anomalies

  • P. KružićEmail author
  • A. Popijač


Recurrent climate-induced mass mortalities of marine animals have been recorded in the Mediterranean Sea over the past 15 years. These mortality outbreaks have been associated with positive thermal anomalies. In this study, we assessed long-term (from 2003 to 2013) responses of the temperate coral Balanophyllia europaea to increasing seawater temperatures in the Mljet National Park in the Adriatic Sea (Northern Mediterranean Sea) and described the relationship between recurrent mortality events and sea temperature regimes in the southern Adriatic Sea. Our results indicate that polyp bleaching and tissue necrosis caused the observed mortality. The first observations of B. europaea mortality within the study area in the Mljet NP were in early September 2003. The Mediterranean area experienced high temperatures and hydrographic stability over a period of several weeks throughout that summer, which resulted in a mass mortality event. In the Mljet National Park, the highest impact of mass mortality started during the exceptionally hot summer of 2012, representing one of the most severe mass mortality events ever observed in the Adriatic Sea. In 2012, sea temperatures at a 5 m depth during the summer period (from June to September) ranged from 24.44 to 30.16 °C in the Mljet NP. The northern sites in the Mljet NP were highly impacted, with up to 80 % of B. europaea specimens affected by necrosis, while the southern sites displayed the highest impact, with 90–100 % of affected individuals. Without any coral adaptation to warming and under the present climate-warming trend, new mass mortality events may occur in the near future, possibly causing a major coral biodiversity crisis in the Mediterranean Sea.


Sea temperature anomaly Balanophyllia europaea Mass mortality Climate change Adriatic Sea 



The authors wish to thank Dr. Dušan Zavodnik from the Rovinj Research Centre and Dr. Helmut Zibrowius from Centre d’Océanologie de Marseille (France) for their helpful suggestions and support. Special thanks go to Dr. Hrvoje Mihanović from the Hydrographic Institute of the Republic of Croatia (HHI) for help with sea temperature data. We also thank the staff of Mljet National Park for fieldwork support and laboratory help.


  1. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  2. Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Global Change Biol 13:2078–2088CrossRefGoogle Scholar
  3. Banin E, Israely T, Fine M, Loya Y, Rosenberg E (2001) Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol Lett 199:33–37CrossRefPubMedGoogle Scholar
  4. Banin E, Vassilakos D, Orr E, Martinez RJ, Rosenberg E (2003) Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi. Curr Microbiol 46:418–422CrossRefPubMedGoogle Scholar
  5. Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol Ecol 19:1705–1720CrossRefPubMedGoogle Scholar
  6. Bensoussan N, Romano JC, Harmelin JG, Garrabou J (2010) High resolution characterization of northwest Mediterranean coastal waters thermal regimes: To better understand responses of benthic communities to climate change. Estuar Coast Shelf Sci 87:431–441CrossRefGoogle Scholar
  7. Bianchi CN (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580:7–21CrossRefGoogle Scholar
  8. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:129–138CrossRefGoogle Scholar
  9. Caroselli E, Prada F, Pasquini L, Nonnis Marzano F, Zaccanti F, Falini G, Levy O, Dubinsky Z, Goffredo S (2011) Environmental implications of skeletal micro-density and porosity variation in two scleractinian corals. Zoology 114:255–264CrossRefPubMedGoogle Scholar
  10. Cebrian E, Uriz MJ, Garrabou J, Ballesteros E (2011) Sponge mass mortalities in a warming Mediterranean Sea: Are cyanobacteria-harboring species worse off? PLoS One 6:e20211CrossRefPubMedCentralPubMedGoogle Scholar
  11. Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (northwestern Mediterranean), summer 1999. Ecol Lett 3:284–293CrossRefGoogle Scholar
  12. Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215CrossRefGoogle Scholar
  13. Coma R, Ribes M, Gili JM, Zabala M (2002) Seasonality of in situ respiration rate in three temperate benthic suspension feeders. Limnol Oceanogr 47:324–331CrossRefGoogle Scholar
  14. Coma R, Pola E, Ribes M, Zabala M (2004) Long-term assessment of temperate octocoral mortality patterns, protected vs. unprotected areas. Ecol Appl 14:1466–1478CrossRefGoogle Scholar
  15. Coma R, Ribes M, Serrano E, Jiménez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc Natl Acad Sci U S A 106(15):6176–6181CrossRefPubMedCentralPubMedGoogle Scholar
  16. Crisci C, Bensoussan N, Romano JC, Garrabou J (2011) Temperature anomalies and mortality events in marine communities: insights on factors behind differential mortality impacts in the NW Mediterranean. PLoS One 6:e23814CrossRefPubMedCentralPubMedGoogle Scholar
  17. Cushman-Roisin B, Gacic M, Poulain PM, Artegiani A (2001) Physical oceanography of the Adriatic Sea: Past, present and future. Kluwer Academic Press, Norwell, pp 1–320CrossRefGoogle Scholar
  18. Garrabou J, Harmelin JG (2002) A 20-year study on life-history traits of a harvested long-lived temperate coral in the NW Mediterranean: insights into conservation and management needs. J Anim Ecol 71:966–978CrossRefGoogle Scholar
  19. Garrabou J, Perez T, Sartoretto S, Harmelin JG (2001) Mass mortality event in red coral Corallium rubrum populations in Provence region (France, NW Mediterranean). Mar Ecol Progr Ser 217:263–272CrossRefGoogle Scholar
  20. Garrabou J, Coma R, Bally M, Bensoussan N, Chevaldonné P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes M, Romano JC, Serrano E, Teixidó N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biol 15:1090–1103CrossRefGoogle Scholar
  21. Glynn PW (1991) Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol Evol 6:175–179CrossRefPubMedGoogle Scholar
  22. Goffredo S, Caroselli E, Mattioli G, Pignotti E, Zaccanti F (2007) Variation in biometry and demography of solitary corals with environmental factors in the Mediterranean Sea. Mar Biol 152:351–361CrossRefGoogle Scholar
  23. Goffredo S, Caroselli E, Mattioli G, Pignotti E, Zaccanti F (2008) Relationships between growth, population structure and sea surface temperature in the temperate solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Coral Reefs 27:623–632CrossRefGoogle Scholar
  24. Goffredo S, Caroselli E, Mattioli G, Pignotti E, Dubinsky Z, Zaccanti F (2009) Inferred level of calcification decreases along an increasing temperature gradient in a Mediterranean endemic coral. Limnol Oceanogr 54:930–937CrossRefGoogle Scholar
  25. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  26. 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 301:929–933CrossRefPubMedGoogle Scholar
  27. Kersting DK, Bensoussan N, Linares C (2013) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8(8):e70820CrossRefPubMedCentralPubMedGoogle Scholar
  28. Kružić P (2002) Marine fauna of the Mljet National Park (Adriatic Sea, Croatia). 1. Anthozoa. Nat Croat 11(3):265–292Google Scholar
  29. Kružić P (2007) Anthozoan fauna of the “Telašćica” Nature Park (Adriatic Sea, Croatia). Nat Croat 16(4):233–266Google Scholar
  30. Kružić P, Požar-Domac A (2007) Impact of tuna farming on the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs 26:665CrossRefGoogle Scholar
  31. Kružić P, Benković L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar Ecol 29:125–139CrossRefGoogle Scholar
  32. Kružić P, Sršen P, Benković L (2012) The impact of seawater temperature on coral growth parameters of the colonial coral Cladocora caespitosa (Anthozoa, Scleractinia) in the eastern Adriatic Sea. Facies 58(4):477–491CrossRefGoogle Scholar
  33. Kružić P, Lipej L, Mavrič B, Rodić P (2014) Impact of bleaching on the coral Cladocora caespitosa in the eastern Adriatic Sea. Mar Ecol Progr Ser 509:193–202CrossRefGoogle Scholar
  34. Kushmaro A, Rosenberg E, Fine M, Loya Y (1997) Bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol Progr Ser 147:159–165CrossRefGoogle Scholar
  35. Kushmaro A, Rosenberg E, Fine M, Ben Haim Y, Loya Y (1998) Effect of temperature on bleaching of coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 171:131–137CrossRefGoogle Scholar
  36. Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260CrossRefPubMedGoogle Scholar
  37. Linares C, Coma R, Garrabou J, Diaz D, Zabala M (2008) Size distribution, density and disturbance of two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J Appl Ecol 45:688–699CrossRefGoogle Scholar
  38. Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar Ecol Prog Ser 305:127–137CrossRefGoogle Scholar
  39. Maldonado M, Sànchez-Tocino L, Navarro C (2010) Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms. Mar Biol 157:1577–1590CrossRefGoogle Scholar
  40. McWilliams JP, Côté IM, Gill JA, Sutherland WJ, Watkinson AR (2005) Accelerating impacts of temperature-induced coral bleaching in the Caribbean. Ecology 86:2055–2060CrossRefGoogle Scholar
  41. Perez T, Garrabou J, Sartoretto S, Harmelin JG, Francour P, Vacelet J (2000) Mass mortality of marine invertebrates: an unprecedented event in the Northwestern Mediterranean. C R Acad Sci III 323:853–865CrossRefPubMedGoogle Scholar
  42. Porter JW, Fitt WK, Spero HJ, Rogers CS, White MW (1989) Bleaching in reef corals: physiological and stable isotopic responses. Proc Natl Acad Sci U S A 86:9342–9346CrossRefPubMedCentralPubMedGoogle Scholar
  43. Rodolfo-Metalpa R, Bianchi CN, Peirano A, Morri C (2000) Coral mortality in NW Mediterranean. Coral Reefs 19:24CrossRefGoogle Scholar
  44. Rodolfo-Metalpa R, Bianchi CN, Peirano A, Morri C (2005) Tissue necrosis and mortality of the temperate coral Cladocora caespitosa. Ital J Zool 72:271–276CrossRefGoogle Scholar
  45. Rodolfo-Metalpa R, Richard C, Allemand D, Bianchi CN, Morri C, Ferrier-Pagés C (2006) Response of zooxanthellae in symbiosis with the Mediterranean corals Cladocora caespitosa and Oculina patagonica to elevated temperatures. Mar Biol 150:45–55CrossRefGoogle Scholar
  46. Romano JC, Bensoussan N, Younes WAN, Arlhac D (2000) Anomalies thermiques dans les eaux du golfe de Marseille durant l’été 1999. Une explication partielle de la mortalité d’invertébrés fixés. C R Acad Sci III 323:415–427CrossRefPubMedGoogle Scholar
  47. Rosenberg E, Loya Y (1999) Vibrio shiloi is the etiological (causative) agent of Oculina patagonica bleaching: General implications. Reef Encounters 25:8–10Google Scholar
  48. Sparnocchia S, Schiano ME, Picco P, Bozzano R, Cappelletti A (2006) The anomalous warming of summer 2003 in the surface layer of the Central Ligurian Sea (Western Mediterranean). Ann Geofis 24:443–452Google Scholar
  49. Stabili L, Cardone F, Alifano P, Tredici SM, Piraino S, Corriero G, Gaino E (2012) Epidemic mortality of the sponge Ircinia variabilis (Schmidt, 1862) associated to proliferation of a Vibrio bacterium. Microb Ecol 64:802–813CrossRefPubMedGoogle Scholar
  50. Suzuki A, Gagan MK, Fabricius K, Isdale PJ, Yukino I, Kawahata H (2003) Skeletal isotope microprofiles of growth perturbations in Porites corals during the 1997-1998 mass bleaching event. Coral Reefs 22:357–369CrossRefGoogle Scholar
  51. Toren A, Landau L, Kushmaro A, Loya Y, Rosenberg E (1998) Effect of temperature on adhesion of Vibrio strain AK-1 to Oculina patagonica and on coral bleaching. Appl Environ Microbiol 64:1379–1384PubMedCentralPubMedGoogle Scholar
  52. Torrents O, Tambutte E, Caminiti N, Garrabou J (2008) Upper thermal thresholds of shallow vs. deep populations of the precious Mediterranean red coral Corallium rubrum (L.): assessing the potential effects of warming in the NW Mediterranean. J Exp Mar Biol Ecol 357:7–19CrossRefGoogle Scholar
  53. van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and loser a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76CrossRefGoogle Scholar
  54. Vilibić I, Šepić J, Proust N (2013) Observational evidence of a weakening of thermohaline circulation in the Adriatic Sea. Clim Res 55:217–225CrossRefGoogle Scholar
  55. Zabala M, Ballesteros E (1989) Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Sci Mar 53:3–17Google Scholar
  56. Zibrowius H (1980) Les Scléractiniaires de la Méditerranée et de l’Atlantique nord-oriental. Mém Inst Océanogr (Monaco) 11:1–284Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Laboratory for Marine Biology, Department of Zoology, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  2. 2.Oikon Ltd, Institute for Applied EcologyZagrebCroatia

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