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Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave
Abstract
Late in summer 2003, extensive mass mortality of at least 25 rocky benthic macro-invertebrate species (mainly gorgonians and sponges) was observed in the entire Northwestern (NW) Mediterranean region, affecting several thousand kilometers of coastline. We were able to characterize the mortality event by studying six areas covering the main regions of the NW Mediterranean basin. The degree of impact on each study area was quantified at 49 sites by estimating the proportion of colonies affected in populations of several gorgonian species compared with reference data obtained in years without mortality signs. According to these data, the western areas (Catalan coast and Balearic Islands) were the least affected, while the central areas (Provence coast and Corsica-Sardinia) showed a moderate impact. The northernmost and eastern areas (Gulf of Genoa and Gulf of Naples) displayed the highest impact, with almost 80% of gorgonian colonies affected. The heat wave of 2003 in Europe caused an anomalous warming of seawater, which reached the highest temperatures ever recorded in the studied regions, between 1 and 3 °C above the climatic values (mean and maximum). Because this exceptional warming was observed in the depth ranges most affected by the mortality, it seems likely that the 2003 anomalous temperature played a key role in the observed mortality event. A correlation analysis between temperature conditions and degree of impact seems to support this hypothesis. Under the present cl…
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“A variety of impacts 4 have been associated with these anomalous events, including shifts in species ranges, local 5 extinctions and economic impacts on seafood industries through declines in important fishery 6 species and impacts on aquaculture.”
From A hierarchical approach to defining marine heatwaves (2016) · cites this paper as Garrabou et al. 2009
In the citing paper
“From examples such as the 2003 MHW in the northern Mediterranean Sea (Garrabou et al. 2009), the 2011 Ningaloo Niño in Western Australia (Feng et al. 2013) and the 2012 MHW in the northwest Atlantic (Mills et al. 2013; Chen et al. 2014), it is clear that the atmosphere, land surface and ocean all may have important driving roles in how and where these prolonged heat events play out.”
From A hierarchical approach to defining marine heatwaves (2016) · cites this paper as Garrabou et al. 2009
Citations
Cites
Historical Overfishing and the Recent Collapse of Coastal Ecosystems
Jackson, J. B. C., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., Bradbury, R. H., Cooke, R., Erlandson, J., Estes, J. A., et al. (2001) · Science · doi:10.1126/science.1059199 · Cited by 6,652
Mackay, A. W. (2008) · Journal of Environmental Quality · doi:10.2134/jeq2008.0015br · Cited by 5,592
Climate Change, Human Impacts, and the Resilience of Coral Reefs
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M. A., Connolly, S. R., Folke, C., Grosberg, R. K., Hoegh‐Guldberg, O., Jackson, J. B. C., Kleypas, J. A., et al. (2003) · Science · doi:10.1126/science.1085046 · Cited by 3,935
The role of increasing temperature variability in European summer heatwaves
Schär, C., Vidale, P. L., Lüthi, D., Frei, C., Häberli, C., Liniger, M. A., & Appenzeller, C. (2004) · Nature · doi:10.1038/nature02300 · Cited by 2,787
The impacts of climate change in coastal marine systems
Harley, C. D. G., Randall Hughes, A., Hultgren, K. M., Miner, B. G., Sorte, C. J. B., Thornber, C. S., Rodriguez, L. F., Tomanek, L., & Williams, S. L. (2006) · Ecology Letters · doi:10.1111/j.1461-0248.2005.00871.x · Cited by 2,700
Emerging Marine Diseases--Climate Links and Anthropogenic Factors
Harvell, C. D., Kim, K., Burkholder, J. M., Colwell, R. R., Epstein, P. R., Grimes, D. J., Hofmann, E. E., Lipp, E. K., Osterhaus, A. D. M. E., Overstreet, R. M., et al. (1999) · Science · doi:10.1126/science.285.5433.1505 · Cited by 1,836
European Seasonal and Annual Temperature Variability, Trends, and Extremes Since 1500
Luterbacher, J., Dietrich, D., Xoplaki, E., Grosjean, M., & Wanner, H. (2004) · Science · doi:10.1126/science.1093877 · Cited by 1,805
Human contribution to the European heatwave of 2003
Stott, P. A., Stone, D. A., & Allen, M. R. (2004) · Nature · doi:10.1038/nature03089 · Cited by 1,735
Levitus, S., Antonov, J. I., Boyer, T. P., & Stephens, C. (2000) · Science · doi:10.1126/science.287.5461.2225 · Cited by 1,496
Temperature Biology of Animals
Cossins, A. R., & Bowler, K. (1987) · doi:10.1007/978-94-009-3127-5 · Cited by 1,184
Marine Biodiversity of the Mediterranean Sea: Situation, Problems and Prospects for Future Research
Bianchi, C. N., & Morri, C. (2000) · Marine Pollution Bulletin · doi:10.1016/s0025-326x(00)00027-8 · Cited by 931
Déqué, M. (2007) · Global and Planetary Change · doi:10.1016/j.gloplacha.2006.11.030 · Cited by 758
Southward, A., Hawkins, S., & Burrows, M. (1995) · Journal of Thermal Biology · doi:10.1016/0306-4565(94)00043-i · Cited by 598
Cerrano, C., Bavestrello, G., Bianchi, C. N., Cattaneo‐Vietti, R., Bava, S., Morganti, C., Morri, C., Picco, P., Sara, G., Schiaparelli, S., et al. (2000) · Ecology Letters · doi:10.1046/j.1461-0248.2000.00152.x · Cited by 596
Self-citationNew perspectives in sponge biology
PICTON, B. E. (1995) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(95)90017-9 · Cited by 549
Heat stress intensification in the Mediterranean climate change hotspot
Diffenbaugh, N. S., Pal, J. S., Giorgi, F., & Gao, X. (2007) · Geophysical Research Letters · doi:10.1029/2007gl030000 · Cited by 491
Ecological Effectiveness: Conservation Goals for Interactive Species
Soulé, M. E., Estes, J. A., Berger, J., & del Rio, C. M. (2003) · Conservation Biology · doi:10.1046/j.1523-1739.2003.01599.x · Cited by 448
Biodiversity issues for the forthcoming tropical Mediterranean Sea
Bianchi, C. N. (2007) · Hydrobiologia · doi:10.1007/s10750-006-0469-5 · Cited by 418
Nakamura, T., & van Woesik, R. (2001) · Marine Ecology Progress Series · doi:10.3354/meps212301 · Cited by 385
Warming trend in the western Mediterranean deep water
Béthoux, J. P., Gentili, B., Raunet, J., & Tailliez, D. (1990) · Nature · doi:10.1038/347660a0 · Cited by 382
Biodiversity issues for the forthcoming tropical Mediterranean Sea
Bianchi, C. N. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6156-1_1 · Cited by 381
Coral reef bleaching in the 1980s and possible connections with global warming
Glynn, P. W. (1991) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(91)90208-f · Cited by 378
Mediterranean Coralligenous Assemblages
Ballesteros, E. (2006) · Oceanography and Marine Biology/Oceanography and marine biology - an annual review · doi:10.1201/9781420006391.ch4 · Cited by 368
Somot, S., Sevault, F., & Déqué, M. (2006) · Climate Dynamics · doi:10.1007/s00382-006-0167-z · Cited by 355
Seasonality in coastal benthic ecosystems
Coma, R., Ribes, M., Gili, J. M., & Zabala, M. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)01970-4 · Cited by 333
Self-citationd’Alcalà, M. R., Conversano, F., Corato, F., Licandro, P., Mangoni, O., Marino, D., Mazzocchi, M. G., Modigh, M., Montresor, M., Nardella, M., et al. (2004) · Scientia Marina · doi:10.3989/scimar.2004.68s165 · Cited by 326
Long-Term Oceanographic and Ecological Research in the Western English Channel
SOUTHWARD, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I. R., Kendall, M. A., Halliday, N. C., et al. (2004) · Advances in marine biology · doi:10.1016/s0065-2881(04)47001-1 · Cited by 316
Lesser, M. P., Bythell, J. C., Gates, R. D., Johnstone, R. W., & Hoegh‐Guldberg, O. (2007) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2007.02.015 · Cited by 314
Ecology of Paracentrotus lividus
Boudouresque, C., & Verlaque, M. (2001) · Developments in aquaculture and fisheries science · doi:10.1016/s0167-9309(01)80013-2 · Cited by 297
Are the Mediterranean waters becoming warmer? Information from biological indicators
Francour, P., Boudouresque, C., Harmelin, J., Harmelin‐Vivien, M., & Quignard, J. (1994) · Marine Pollution Bulletin · doi:10.1016/0025-326x(94)90071-x · Cited by 260
Self-citationACCELERATING IMPACTS OF TEMPERATURE-INDUCED CORAL BLEACHING IN THE CARIBBEAN
McWilliams, J. P., Côté, I. M., Gill, J. A., Sutherland, W. J., & Watkinson, A. R. (2005) · Ecology · doi:10.1890/04-1657 · Cited by 244
Pérez, T., Garrabou, J., Sartoretto, S., Harmelin, J., Francour, P., & Vacelet, J. (2000) · Comptes Rendus de l Académie des Sciences - Series III - Sciences de la Vie · doi:10.1016/s0764-4469(00)01237-3 · Cited by 234
Self-citationGarrabou, J., Pérez, T., Sartoretto, S., & Harmelin, J. (2001) · Marine Ecology Progress Series · doi:10.3354/meps217263 · Cited by 232
Self-citationGarrabou, J., & Harmelin, J. (2002) · Journal of Animal Ecology · doi:10.1046/j.1365-2656.2002.00661.x · Cited by 215
Self-citationBally, M., & Garrabou, J. (2007) · Global Change Biology · doi:10.1111/j.1365-2486.2007.01423.x · Cited by 205
Self-citationLinares, C., Coma, R., Díaz, D. D., Zabala, M., Hereu, B., & Dantart, L. (2005) · Marine Ecology Progress Series · doi:10.3354/meps305127 · Cited by 187
Self-citationLinares, C., Coma, R., Garrabou, J., Díaz, D., & Zabala, M. (2007) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2007.01419.x · Cited by 184
Self-citationWidespread disease in Caribbean sea fans:II. Patterns of infection and tissue loss
Nagelkerken, I., Buchan, K. C., Smith, G., Bonair, K., Bush, P., Garzón-Ferreira, J., Botero, L., Gayle, P. M. H., Harvell, C., Scherbaum-Heberer, C., et al. (1997) · Marine Ecology Progress Series · doi:10.3354/meps160255 · Cited by 166
Warming trends and decadal variability in the Western Mediterranean shelf
Vargas‐Yáñez, M., García, M. J., Salat, J., García-Martínez, M. C., Pascual, J., & Moya, F. (2007) · Global and Planetary Change · doi:10.1016/j.gloplacha.2007.09.001 · Cited by 150
Effect of Temperature on Adhesion of Vibrio Strain AK-1 to Oculina patagonica and on Coral Bleaching
Toren, A., Landau, L., Kushmaro, A., Loya, Y., & ROSENBERG, E. B. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.4.1379-1384.1998 · Cited by 148
Regional warming‐induced species shift in north‐west Mediterranean marine caves
Chevaldonné, P., & Lejeusne, C. (2003) · Ecology Letters · doi:10.1046/j.1461-0248.2003.00439.x · Cited by 142
Self-citationLIFE HISTORY AND VIABILITY OF A LONG-LIVED MARINE INVERTEBRATE: THE OCTOCORALPARAMURICEA CLAVATA
Linares, C., Doak, D. F., Coma, R., Díaz, D., & Zabala, M. (2007) · Ecology · doi:10.1890/05-1931 · Cited by 141
Self-citationLONG‐TERM ASSESSMENT OF TEMPERATE OCTOCORAL MORTALITY PATTERNS, PROTECTED VS. UNPROTECTED AREAS
Coma, R., Pola, E., Ribes, M., & Zabala, M. (2004) · Ecological Applications · doi:10.1890/03-5176 · Cited by 136
Self-citationComa, R., & Ribes, M. (2003) · Oikos · doi:10.1034/j.1600-0706.2003.12028.x · Cited by 125
Self-citationSparnocchia, S., Schiano, M. E., Picco, P., Bozzano, R., & Cappelletti, A. (2006) · Annales Geophysicae · doi:10.5194/angeo-24-443-2006 · Cited by 122
Banin, E., Israely, T., Fine, M., Loya, Y., & ROSENBERG, E. B. (2001) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(01)00162-8 · Cited by 121
Gorgonian population recovery after a mass mortality event
Cerrano, C., Arillo, A., Azzini, F., Calcinai, B., Castellano, L., Muti, C., Valisano, L., Zega, G., & Bavestrello, G. (2004) · Aquatic Conservation Marine and Freshwater Ecosystems · doi:10.1002/aqc.661 · Cited by 117
Self-citationSuperoxide Dismutase Is a Virulence Factor Produced by the Coral Bleaching Pathogen Vibrio shiloi
Banin, E., Vassilakos, D., Orr, E., Martinez, R. J., & ROSENBERG, E. B. (2003) · Current Microbiology · doi:10.1007/s00284-002-3912-5 · Cited by 110
Zabala, M., & Ballesteros, E. (1989) · Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) · Cited by 108
Self-citationTorrents, O., Tambutté, É., Caminiti-Segonds, N., & Garrabou, J. (2008) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2007.12.006 · Cited by 104
Self-citationComa, R., Linares, C., Ribes, M., Díaz, D. D., Garrabou, J., & Ballesteros, E. (2006) · Marine Ecology Progress Series · doi:10.3354/meps327051 · Cited by 102
Self-citationThe Past and Present Topology and Structure of Mediterranean Subtidal Rocky-shore Food Webs
Sala, E. (2004) · Ecosystems · doi:10.1007/s10021-003-0241-x · Cited by 98
Sponges in Time and Space, Biology, Chemistry, Paleontology
Simpson, T. L. (1995) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(95)90012-8 · Cited by 91
Seasonality of in situ respiration rate in three temperate benthic suspension feeders
Coma, R. (2002) · Limnology and Oceanography · doi:10.4319/lo.2002.47.1.0324 · Cited by 89
Self-citationSchiaparelli, S., Castellano, M., Povero, P., Sartoni, G., & Cattaneo‐Vietti, R. (2007) · Marine Ecology · doi:10.1111/j.1439-0485.2007.00155.x · Cited by 87
Romano, J., Bensoussan, N., Younes, W. A. N., & Arlhac, D. (2000) · Comptes Rendus de l Académie des Sciences - Series III - Sciences de la Vie · doi:10.1016/s0764-4469(00)00141-4 · Cited by 81
Self-citationMartin, Y., Bonnefont, J.-L., & Chancerelle, L. (2002) · Water Research · doi:10.1016/s0043-1354(01)00251-2 · Cited by 77
Coral mortality in NW Mediterranean
Metalpa, R. R., Bianchi, C. N., Peirano, A., & Morri, C. (2000) · Coral Reefs · doi:10.1007/s003380050221 · Cited by 54
Attrill, M. J., Kelmo, F., & Jones, M. B. (2004) · Climate Research · doi:10.3354/cr026151 · Cited by 43
Mistri, M., & Ceccherelli, V. U. (1996) · The European Zoological Journal · doi:10.1080/11250009609356137 · Cited by 30
Scinto, A., Benvenuto, C., Cerrano, C., & Mori, M. (2007) · Journal of Crustacean Biology · doi:10.1651/s-2693.1 · Cited by 19
Self-citationIs global change a real threat for conservation of the NW Mediterranean marine biodiversity
Garrabou, J., & Dimar Team (2003) · EAEJA · Cited by 11
Self-citationBavestrello, G., Bertone, S., Vietti, R. C., Cerrano, C., Gaino, E., & ZANZI, D. (1994) · CINECA IRIS Institutial Research Information System (University of Genoa) · Cited by 5
Self-citationA comparison of well velocity methods in South Texas
Wood, A. B. (1959) · Geophysics · doi:10.1190/1.1438607 · Cited by 3
Research works printed but not linked: 12
- 10.1111/j.1574-6968.2001.tb10647.x · DOI
- Cigliano M, 2007, The long hot summer. A further mortality event of gorgonians along the Phlaegrean Islands (Tyrrhenian Sea), Biologia Marina Mediterranea, 14, 292
- Gambi MC, 2006, Segnalazione di un evento di mortalità di gorgonacei lungo le coste delle isole di Ischia e Procida (Golfo di Napoli, Mar Tirreno), Biologia Marina Mediterranea, 13, 583
- Harmelin JG, 1994, Population structure and partial mortality of the gorgonian Paramuricea clavata in the north‐western Mediterranean, Marine Life, 4, 5
- IPCC(2007) Climate change 2007: the physical science basis. Contribution of working group I to the Fourth Assesment Report of the intergovernmental panel on climate change (edsSolomonSD QinM ManningZet al. )Cambridge University Press Cambridge UKand New York NY USA 996p.
- Marullo S, 2003, L'anomalia termica del 2003 nel Mar Mediterraneao ossevata da satellite, Energia, Ambiente e Innovazione, 6, 48
- Meinesz A, 1983, Sur les fortes mortalities de Spondylus gaederopus Linné observées sur les côtes de Méditerranée, Travaux Scientifiques du Parc National de Port-Cros, 9, 89
- Pascual J, 1995, Evolución de la temperatura del mar entre 1974 y 1994, cerca de la costa catalana, Internationale Colloque Okeanos, 95, 23
- PrieurL(2002) Physical historical data on the Ligurian Sea from the Villefranche‐sur‐mer Observatory. In:Tracking Long‐Term Hydrological Change in the Mediterranean Sea. CIESM Workshop Series no. 16 pp. 37–40.
- Ribes M, 2005, The role of engineer species in the benthic–pelagic coupling, Limnology and Oceanography
- Sbrescia L, 2008, Analisi delle popolazioni di gorgonie dell'AMP di Punta Campanella dopo eventi di moria di massa. Proceedings Associazione Italiana di Oceanologia e Limnologia, Atti Associazione Italiana di Oceanologia e Limnologia, 19, 449
- Siccardi A, 1998, Atti del 12° Congresso dell'Associazione Italiana di Oceanologia e Limnologia, 263
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Metadata
- Authors
- GARRABOU, J., COMA, R., BENSOUSSAN, N., BALLY, M., CHEVALDONNÉ, P., CIGLIANO, M., DIAZ, D., HARMELIN, J. G., GAMBI, M. C., KERSTING, D. K., LEDOUX, J. B., LEJEUSNE, C., LINARES, C., MARSCHAL, C., PÉREZ, T., RIBES, M., ROMANO, J. C., SERRANO, E., TEIXIDO, N., TORRENTS, O., ZABALA, M., ZUBERER, F., & CERRANO, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Consejo Superior de Investigaciones Científicas (ES)
- Stazione Zoologica Anton Dohrn (IT)
- Universitat de Barcelona (ES)
- Station Marine d'Endoume (FR)
- University of Genoa (IT)
- Corresponding author
- GARRABOU, J.
- ORCID
- Venue
- Global Change Biology
- Publisher
- Wiley
- Published
- 2009-04-07
- Volume
- 15
- Issue
- 5
- Pages
- 1090-1103
- ISSN
- 1354-1013 (ISSN-L)
- 1365-2486
- OpenAlex
- W2108313195
- Cited by
- 1,049
- References
- 65
- Citations by year
- 2026: 38 · 2025: 83 · 2024: 89 · 2023: 124 · 2022: 96 · 2021: 87 · 2020: 70 · 2019: 74 · 2018: 62 · 2017: 64 · 2016: 51 · 2015: 44 · 2014: 31 · 2013: 48 · 2012: 27
- FWCI
- 17.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Global Change Biology (publishedVersion)
- HAL AMU (submittedVersion)
- HAL (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-05-BDIV-0005)
- Topics
- Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Biology and Ecology Research
- Physical Sciences › Environmental Science › Global and Planetary Change › Marine Ecology and Invasive Species
- Keywords
- mass mortality, 2003 European heatwave, gorgonian corals, sponges, macroinvertebrates, ocean warming, NW Mediterranean, Gulf of Genoa, Gulf of Naples, biodiversity crisis, global warming
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