Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming

Recurrent climate-induced mass-mortalities have been recorded in the Mediterranean Sea over the past 15 years. Cladocora caespitosa, the sole zooxanthellate scleractinian reef-builder in the Mediterranean, is among the organisms affected by these episodes. Extensive bioconstructions of this endemic coral are very rare at the present time and are threatened by several stressors. In this study, we assessed the long-term response of this temperate coral to warming sea-water in the Columbretes Islands (NW Mediterranean) and described, for the first time, the relationship between recurrent mortality events and local sea surface temperature (SST) regimes in the Mediterranean Sea. A water temperature series spanning more than 20 years showed a summer warming trend of 0.06°C per year and an increased frequency of positive thermal anomalies. Mortality resulted from tissue necrosis without massive zooxanthellae loss and during the 11-year study, necrosis was recorded during nine summers separated into two mortality periods (2003-2006 and 2008-2012). The highest necrosis rates were registered during the first mortality period, after the exceptionally hot summer of 2003. Although necrosis and temperature were significantly associated, the variability in necrosis rates during summers with similar thermal anomalies pointed to other acting factors. In this sense, our results showed that these differences were more closely related to the interannual temperature context and delayed thermal stress after extreme summers, rather than to acclimatisation and adaption processes

Collaborative Database to Track Mass Mortality Events in the Mediterranean Sea

Postdoctoral contract Juan de la Cierva [IJCI-2016-29329]Ministerio de Ciencia, Innovacion y Universidades PTA2015-10829-IInterreg Med Programme MPA-Adapt 1MED15_3.2_M2_337European Regional Development Fund - Foundation Albert II MonacoEuropean Union’s Horizon 2020Ministry of Education, Spain FPU15/0545

Biodiversity loss in a Mediterranean ecosystem due to an extreme warming event unveils the role of an engineering gorgonian species

Stochastic perturbations can trigger major ecosystem shifts. Marine systems have been severely affected in recent years by mass mortality events related to positive thermal anomalies. Although the immediate effects in the species demography affected by mortality events are well known, information on the mid- to long-term effects at the community level is much less documented. Here, we show how an extreme warming event replaces a structurally complex habitat, dominated by long-lived species, by a simplified habitat (lower species diversity and richness) dominated by turf-forming species. On the basis of a study involving the experimental manipulation of the presence of the gorgonian Paramuricea clavata, we observed that its presence mitigated the effects of warming by maintaining the original assemblage dominated by macroinvertebrates and delaying the proliferation and spread of the invasive alga Caulerpa cylindracea. However, due to the increase of sediment and turf-forming species after the mortality event we hypothesize a further degradation of the whole assemblage as both factors decrease the recruitment of P.clavata, decrease the survival of encrusting coralligenous-dwelling macroinvertebrates and facilitate the spreading of C. cylindracea

Climate change transforms the functional identity of Mediterranean coralligenous assemblages

We acknowledge the funding of the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019‐000928‐S). This research has also been partially funded by the HEATMED project (RTI2018‐095346‐B‐I00, MCIU/AEI/FEDER, UE), Interreg Med Programme (Projects MPA‐ENGAGE; 5216 | 5MED18_3.2_M23_007 and MPA‐Adapt, 1MED15_3.2_M2_337) 85% cofunded by the European Regional Development Fund, the MIMOSA project funded by the Foundation Prince Albert II Monaco, the Perfect project funded by the TOTAL Foundation, the Medchange project funded by the Agence Nationale pour la Recherche (ANR) and the European Union's Horizon 2020 research and innovation programme under grants agreements 689518 (MERCES) and SEP‐210597628 (FutureMARES). D.G.G. is supported by an FPU grant (FPU15/05457) from the Spanish Ministry of Education. CL gratefully acknowledges the financial support by ICREA under the ICREA Academia programme. VB is supported by the Templeton Foundation (grant #60501, ‘Putting the Extended Evolutionary Synthesis to the Test’). J‐B.L is supported by the strategic Funding UIDB/04423/2020 and UIDP/04423/2020. We thank M. Zabala, J.M Gili and A. Santín for their valuable help in trait definition. D.G.G, C.L, J‐B.L, N.B, P.L.S & J.G are part of the Marine Conservation research group (www.medrecover.org) (2017 SGR 1521) from the Generalitat de Catalunya.Quantifying changes in functional community structure driven by disturbance is critical to anticipate potential shifts in ecosystem functioning. However, how marine heatwaves (MHWs) affect the functional structure of temperate coral-dominated communities is poorly understood. Here, we used five long-term (> 10 years) records of Mediterranean coralligenous assemblages in a multi-taxa, trait-based analysis to investigate MHW-driven changes in functional structure. We show that, despite stability in functional richness (i.e. the range of species functional traits), MHW-impacted assemblages experienced long-term directional changes in functional identity (i.e. their dominant trait values). Declining traits included large sizes, long lifespans, arborescent morphologies, filter-feeding strategies or calcified skeletons. These traits, which were mostly supported by few sensitive and irreplaceable species from a single functional group (habitat-forming octocorals), disproportionally influence certain ecosystem functions (e.g. 3D-habitat provision). Hence, MHWs are leading to assemblages that are deficient in key functional traits, with likely consequences for the ecosystem functioning.Publisher PDFPeer reviewe

Gradients of genetic diversity and differentiation across the distribution range of a Mediterranean coral: Patterns, processes and conservation implications

Aim: How historical and contemporary eco-evolutionary processes shape the patterns of genetic diversity and þÿdifferentiation across species distribution range remain Focusing on the orange stony coral, Astroides calycularis, we (a) characterized the pattern of neutral genetic diversity across the distribution range; (b) gave insights into the underlying processes; and (c) discussed conservation implications with emphasis on a national park located on a hotspot of genetic diversity. Location: South Mediterranean Sea and Zembra National Park. Methods: We combined new data from 12 microsatellites in 13 populations located in the Centre and in the Western Periphery of the distribution range with a published dataset including 16 populations from the Western and Eastern Peripheries. We analysed the relationship among parameters of genetic diversity (He, Ar(g)) and structure (population-specific FST) and two measures of geographic peripherality. We compared two estimators of pairwise genetic structure (GST, DEST) across the distribution range. The evolutionary and demographic history of the populations following the Last Glacial Maximum was reconstructed using approximate Bayesian computations and maximum-likelihood analyses. We inferred the contemporary connectivity among populations from Zembra National Park and with the neighbouring area of Cap Bon. Results: We demonstrate a decrease in genetic diversity and an increase in genetic differentiation from the Centre to the Eastern and Western Peripheries of the distribution range. Populations from Zembra show the highest genetic diversity reported in the species. We identified a spillover effect towards Cap Bon. Main conclusions: The patterns of genetic diversity and þÿdifferentiation are most likely explained by the postglacial range expansion hypothesis rather than the þÿ central peripheral hypothesis. Enforcement of conservatio

Regional and local environmental conditions do not shape the response to warming of a marine habitat-forming species

The differential response of marine populations to climate change remains poorly understood. Here, we combine common garden thermotolerance experiments in aquaria and population genetics to disentangle the factors driving the population response to thermal stress in a temperate habitatforming species: the octocoral Paramuricea clavata. Using eight populations separated from tens of meters to hundreds of kilometers, which were differentially impacted by recent mortality events, we identify 25 degrees C as a critical thermal threshold. After one week of exposure at this temperature, seven of the eight populations were affected by tissue necrosis and after 30 days of exposure at this temperature, the mean % of affected colonies increased gradually from 3 to 97%. We then demonstrate the weak relation between the observed differential phenotypic responses and the local temperature regimes experienced by each population. A significant correlation was observed between these responses and the extent of genetic drift impacting each population. Local adaptation may thus be hindered by genetic drift, which seems to be the main driver of the differential response. Accordingly, conservation measures should promote connectivity and control density erosion in order to limit the impact of genetic drift on marine populations facing climate change

Temporal variability in the response to thermal stress in the red gorgonian, P. clavata: Insights form common garden experiments

4th Mediterranean Symposium on the Conservation of Coralligenous & other Calcareous Bio-Concretions, 20-21 September 2022, Genoa, Italy.-- 6 pages, 2 figuresRecurrent mass mortality events (MMEs) linked to marine heatwaves (MHWs) have been observed in the Mediterranean Sea affecting thousands of kilometers of coastline. Coralligenous habitats were among the most impacted during these events. Information on how the exposure to recurrent MHWs is affecting the coralligenous is critical to anticipate the consequences of climate change and implement actions to enhance their resilience. Combining field surveys with experiments in controlled conditions allowed to dilucidate the differential responses to thermal stress among species, populations and individuals and to explore the spatial and taxonomic variability response to thermal stress linked to MHWs. Yet, the temporal variability in the response to thermal stress remains to be characterized. Thus, we aim to fill this gap focusing on the temporal variability in the response to thermal stress of the coralligenous key habitat-forming species Paramuricea clavata (Plexauridae). We replicated thermal stress experiments during 3 consecutive years following a common garden setup (control vs. thermal stress) involving the same individuals from the same three populations. Considering different phenotypic responses including the level of tissue necrosis during the time of the experiment and the survival of the individuals, we found that the average percentage of tissue necrosis per population variated greatly across years while the probability of survival was considerably reduced in 2017. During the experiments, several individuals from the 3 populations systematically showed reduced level of tissue necrosis suggesting resistance to thermal stress. Overall our data will contribute to help better inform further conservation strategies of habitat-forming coral species in the Mediterranean SeaPeer reviewe

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

Collaborative Database to Track Mass Mortality Events in the Mediterranean Sea

Anthropogenic climate change, and global warming in particular, has strong and increasing impacts on marine ecosystems (Poloczanska et al., 2013; Halpern et al., 2015; Smale et al., 2019). The Mediterranean Sea is considered a marine biodiversity hot-spot contributing to more than 7% of world's marine biodiversity including a high percentage of endemic species (Coll et al., 2010). The Mediterranean region is a climate change hotspot, where the respective impacts of warming are very pronounced and relatively well documented (Cramer et al., 2018). One of the major impacts of sea surface temperature rise in the marine coastal ecosystems is the occurrence of mass mortality events (MMEs). The first evidences of this phenomenon dated from the first half of'80 years affecting the Western Mediterranean and the Aegean Sea (Harmelin, 1984; Bavestrello and Boero, 1986; Gaino and Pronzato, 1989; Voultsiadou et al., 2011). The most impressive phenomenon happened in 1999 when an unprecedented large scale MME impacted populations of more than 30 species from different phyla along the French and Italian coasts (Cerrano et al., 2000; Perez et al., 2000). Following this event, several other large scale MMEs have been reported, along with numerous other minor ones, which are usually more restricted in geographic extend and/or number of affected species (Garrabou et al., 2009; Rivetti et al., 2014; Marbà et al., 2015; Rubio-Portillo et al., 2016, authors' personal observations). These events have generally been associated with strong and recurrent marine heat waves (Crisci et al., 2011; Kersting et al., 2013; Turicchia et al., 2018; Bensoussan et al., 2019) which are becoming more frequent globally (Smale et al., 2019). Both field observations and future projections using Regional Coupled Models (Adloff et al., 2015; Darmaraki et al., 2019) show the increase in Mediterranean sea surface temperature, with more frequent occurrence of extreme ocean warming events. As a result, new MMEs are expected during the coming years. To date, despite the efforts, neither updated nor comprehensive information can support scientific analysis of mortality events at a Mediterranean regional scale. Such information is vital to guide management and conservation strategies that can then inform adaptive management schemes that aim to face the impacts of climate change.MV-L was supported by a postdoctoral contract Juan de la Cierva-Incorporación (IJCI-2016-29329) of Ministerio de Ciencia, Innovación y Universidades. AI was supported by a Technical staff contract (PTA2015-10829-I) Ayudas Personal Técnico de Apoyo of Ministerio de Economía y Competitividad (2015). Interreg Med Programme (grant number Project MPA-Adapt 1MED15_3.2_M2_337) 85% cofunded by the European Regional Development Fund, the MIMOSA project funded by the Foundation Prince Albert II Monaco and the European Union's Horizon 2020 research and innovation programme under grant agreement no 689518 (MERCES). DG-G was supported by an FPU grant (FPU15/05457) from the Spanish Ministry of Education. J-BL was partially supported by the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT - Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020