Temperature Anomalies and Mortality Events in Marine Communities: Insights on Factors behind Differential Mortality Impacts in the NW Mediterranean

Two large-scale mass mortality events (MMEs) of unprecedented extent and severity affecting rocky benthic communities occurred during the summers of 1999 and 2003 along the coasts of the NW Mediterranean Sea. These mortality outbreaks were associated with positive thermal anomalies. In this study, we performed an analysis of inter-regional and inter-annual differences in temperature (T) conditions associated with MMEs of the red gorgonian Paramuricea clavata by analyzing high resolution T time series (hourly records for 3 to 8 years) from four regions of the NW Mediterranean with differing hydrological conditions and biological impacts. High resolution records allowed a detailed analysis using classical and new descriptors to characterize T anomalies. We were able to determine that the MMEs were triggered by two main types of positive thermal anomalies, with the first type being characterized by short periods (2 to 5 days) with high Mean T reaching more than 27°C in some regions and being associated with high intra-day and intra-period variability, while the second type of anomaly presented long duration (near one month) at warm T (24°C) with low intra-period variability. Inter-regional patterns arose; some regions displayed both types of anomalies, while others exhibited only one type. The results showed that T conditions should be considered as the main factor that explains the observed inter-regional and inter-annual differences in mortality impacts. In explaining these differences, the late timing of T anomalies, in addition to their magnitude was found to be determinant. Finally, by combining thermotolerance experimental data with the maximal T stress conditions observed in the four regions, we were able to determine the differential risk of mass mortality across regions. We conclude that expanding high resolution T series is important for the development of sound management and conservation plans to protect Mediterranean marine biodiversity in the face of climate change.

[1]  M. Harmelin-Vivien,et al.  Are the Mediterranean waters becoming warmer? Information from biological indicators , 1994 .

[2]  R. Coma,et al.  Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea , 2005 .

[3]  S. Somot,et al.  The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats , 2010, PloS one.

[4]  C. Antonaccio.  The Western Mediterranean , 2009 .

[5]  M. True.  Etude quantitative de quatre peuplements sciaphiles sur substrat rocheux dans la region marseillaise , 1970 .

[6]  Carlo Cerrano,et al.  Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. , 2010, Environmental microbiology.

[7]  J. López-Jurado,et al.  Climate change in the Western Mediterranean Sea 1900-2008 , 2010 .

[8]  O Hammer-Muntz,et al.  PAST: paleontological statistics software package for education and data analysis version 2.09 , 2001 .

[9]  J. Palutikof,et al.  Climate change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Summary for Policymakers. , 2007 .

[10]  C. Bianchi.  Biodiversity issues for the forthcoming tropical Mediterranean Sea , 2007, Hydrobiologia.

[11]  J. Garrabou,et al.  Genetic survey of shallow populations of the Mediterranean red coral [Corallium rubrum (Linnaeus, 1758)]: new insights into evolutionary processes shaping nuclear diversity and implications for conservation , 2010, Molecular ecology.

[12]  R. Ostfeld,et al.  Climate Warming and Disease Risks for Terrestrial and Marine Biota , 2002, Science.

[13]  C. Franklin,et al.  Testing the beneficial acclimation hypothesis , 2002 .

[14]  M. Bally,et al.  Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change , 2007 .

[15]  George C. Williams,et al.  Adaptation and Natural Selection , 2018 .

[16]  A. Hendry,et al.  PERSPECTIVE: THE PACE OF MODERN LIFE: MEASURING RATES OF CONTEMPORARY MICROEVOLUTION , 1999, Evolution; international journal of organic evolution.

[17]  J. Burkholder,et al.  Emerging marine diseases--climate links and anthropogenic factors. , 1999, Science.

[18]  M. Ribes,et al.  Global warming-enhanced stratification and mass mortality events in the Mediterranean , 2009, Proceedings of the National Academy of Sciences.

[19]  I. Baums.  A restoration genetics guide for coral reef conservation , 2008, Molecular ecology.

[20]  Mebrahtu Ateweberhan,et al.  EFFECTS OF CLIMATE AND SEAWATER TEMPERATURE VARIATION ON CORAL BLEACHING AND MORTALITY , 2007 .

[21]  Carlo Cerrano,et al.  Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave , 2008 .

[22]  J. Garrabou,et al.  Mass mortality event in red coral Corallium rubrum populations in the Provence region (France, NW Mediterranean) , 2001 .

[23]  Steven D. Gaines,et al.  Marine community ecology , 2001 .

[24]  O. Dupont,et al.  An analysis of the July 2006 heatwave extent in Europe compared to the record year of 2003 , 2009 .

[25]  X. Turon,et al.  Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediterranean Sea , 2004, Molecular ecology.

[26]  D. Bellwood,et al.  New paradigms for supporting the resilience of marine ecosystems. , 2005, Trends in ecology & evolution.

[27]  J. Hay,et al.  Coastal systems and low-lying areas , 2007 .

[28]  Robert J. Hofman,et al.  Environmental effects of marine fishing , 1995 .

[29]  Ø. Hammer,et al.  PAST: PALEONTOLOGICAL STATISTICAL SOFTWARE PACKAGE FOR EDUCATION AND DATA ANALYSIS , 2001 .

[30]  K. Bjorndal,et al.  Historical Overfishing and the Recent Collapse of Coastal Ecosystems , 2001, Science.

[31]  D. Allemand,et al.  Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures , 2006, Journal of Experimental Biology.

[32]  M. Palma,et al.  Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event , 2011 .

[33]  E. Ballesteros,et al.  Structure of cnidarian populations in mediterranean sublittoral benthic communities as a result of adaptation to different environmental con ditions , 1991 .

[34]  S. Coles.  A Comparison of Effects of Elevated Temperature versus Temperature Fluctuations on Reef Corals at Kahe Point, Oahu , 1975 .

[35]  J. Romano,et al.  Série du marégraphe de Marseille : mesures de températures de surface de la mer de 1885 à 1967 , 2007 .

[36]  P. Picco,et al.  A catastrophic mass‐mortality episode of gorgonians and other organisms in the Ligurian Sea (North‐western Mediterranean), summer 1999 , 2000 .

[37]  D. Allemand,et al.  Physiological response of the symbiotic gorgonian Eunicella singularis to a long-term temperature increase , 2009, Journal of Experimental Biology.

[38]  J. Vacelet,et al.  Mortalité massive d'invertébrés marins : un événement sans précédent en Méditerranée nord-occidentale , 2000 .

[39]  T. Oliver,et al.  Do fluctuating temperature environments elevate coral thermal tolerance? , 2011, Coral Reefs.

[40]  M. Ribes,et al.  Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization , 2003 .

[41]  R. Grosberg,et al.  Climate Change, Human Impacts, and the Resilience of Coral Reefs , 2003, Science.

[42]  M. Oppen,et al.  Genetic structure of a reef-building coral from thermally distinct environments on the Great Barrier Reef , 2006, Coral Reefs.

[43]  T. Kawecki,et al.  Conceptual issues in local adaptation , 2004 .

[44]  Michel Crépon,et al.  21st century climate change scenario for the Mediterranean using a coupled atmosphere–ocean regional climate model , 2008 .

[45]  A. Winter,et al.  Coefficient of variation of sea surface temperature (SST) as an indicator of coral bleaching , 2006 .

[46]  E. Ballesteros,et al.  Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean , 1989 .

[47]  Christopher D G Harley,et al.  The impacts of climate change in coastal marine systems. , 2006, Ecology letters.

[48]  C. Millot.  Wind induced upwellings in the Gulf of Lions , 1979 .

[49]  S. Gorshkov,et al.  World ocean atlas , 1976 .

[50]  C. Kappel.  Losing pieces of the puzzle: threats to marine, estuarine, and diadromous species , 2005 .

[51]  J. Garrabou,et al.  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 , 2008 .

[52]  G. Daniel,et al.  The western Mediterranean , 1967 .

[53]  Joaquim Garrabou,et al.  High resolution characterization of northwest Mediterranean coastal waters thermal regimes: To better understand responses of benthic communities to climate change , 2010 .

[54]  D. Lüthi,et al.  The role of increasing temperature variability in European summer heatwaves , 2004, Nature.

[55]  E. Ballesteros,et al.  Structure and Dynamics of North-western Mediterranean Rocky Benthic Communities along a Depth Gradient , 2002 .

[56]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[57]  C. Cerrano,et al.  Oxygen consumption in Mediterranean octocorals under different temperatures , 2010 .

[58]  James T. Carlton,et al.  Human alterations of marine communities: students beware! , 2001 .