Marine heatwaves on the rise: One of the strongest ever observed mass mortality event in temperate gorgonians.

Gorgonian population after the 2022 mass mortality event (MME) in the Calanques National Park. The year 2022 was marked by a historic gorgonian MME. This study describes the consequences for the red gorgonian (Paramuricea clavata) and red coral (Corallium rubrum) populations in the Calanques National Park (Marseille, France).

Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea.

Climate change is causing an increase in the frequency and intensity of marine heatwaves (MHWs) and mass mortality events (MMEs) of marine organisms are one of their main ecological impacts. Here, we show that during the 2015-2019 period, the Mediterranean Sea has experienced exceptional thermal conditions resulting in the onset of five consecutive years of widespread MMEs across the basin. These MMEs affected thousands of kilometers of coastline from the surface to 45 m, across a range of marine habitats and taxa (50 taxa across 8 phyla). Significant relationships were found between the incidence of MMEs and the heat exposure associated with MHWs observed both at the surface and across depths. Our findings reveal that the Mediterranean Sea is experiencing an acceleration of the ecological impacts of MHWs which poses an unprecedented threat to its ecosystems' health and functioning. Overall, we show that increasing the resolution of empirical observation is critical to enhancing our ability to more effectively understand and manage the consequences of climate change.

Climate change transforms the functional identity of Mediterranean coralligenous assemblages.

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.

Ocean weather, biological rates, and unexplained global ecological patterns.

As on land, oceans exhibit high temporal and spatial temperature variation. This "ocean weather" contributes to the physiological and ecological processes that ultimately determine the patterns of species distribution and abundance, yet is often unrecognized, especially in tropical oceans. Here, we tested the paradigm of temperature stability in shallow waters (<12.5 m) across different zones of latitude. We collated hundreds of in situ, high temporal-frequency ocean temperature time series globally to produce an intuitive measure of temperature variability, ranging in scale from quarter-diurnal to annual time spans. To estimate organismal sensitivity of ectotherms (i.e. microbes, algae, and animals whose body temperatures depend upon ocean temperature), we computed the corresponding range of biological rates (such as metabolic rate or photosynthesis) for each time span, assuming an exponential relationship. We found that subtropical regions had the broadest temperature ranges at time spans equal to or shorter than a month, while temperate and tropical systems both exhibited narrow (i.e. stable) short-term temperature range estimates. However, temperature-dependent biological rates in tropical regions displayed greater ranges than in temperate systems. Hence, our results suggest that tropical ectotherms may be relatively more sensitive to short-term thermal variability. We also highlight previously unexplained macroecological patterns that may be underpinned by short-term temperature variability.

Not out of the Mediterranean: Atlantic populations of the gorgonian Paramuricea clavata are a separate sister species under further lineage diversification.

The accurate delimitation of species boundaries in nonbilaterian marine taxa is notoriously difficult, with consequences for many studies in ecology and evolution. Anthozoans are a diverse group of key structural organisms worldwide, but the lack of reliable morphological characters and informative genetic markers hampers our ability to understand species diversification. We investigated population differentiation and species limits in Atlantic (Iberian Peninsula) and Mediterranean lineages of the octocoral genus Paramuricea previously identified as P. clavata. We used a diverse set of molecular markers (microsatellites, RNA-seq derived single-copy orthologues [SCO] and mt-mutS [mitochondrial barcode]) at 49 locations. Clear segregation of Atlantic and Mediterranean lineages was found with all markers. Species-tree estimations based on SCO strongly supported these two clades as distinct, recently diverged sister species with incomplete lineage sorting, P. cf. grayi and P. clavata, respectively. Furthermore, a second putative (or ongoing) speciation event was detected in the Atlantic between two P. cf. grayi color morphotypes (yellow and purple) using SCO and supported by microsatellites. While segregating P. cf. grayi lineages showed considerable geographic structure, dominating circalittoral communities in southern (yellow) and western (purple) Portugal, their occurrence in sympatry at some localities suggests a degree of reproductive isolation. Overall, our results show that previous molecular and morphological studies have underestimated species diversity in Paramuricea occurring in the Iberian Peninsula, which has important implications for conservation planning. Finally, our findings validate the usefulness of phylotranscriptomics for resolving evolutionary relationships in octocorals.

Complete mitochondrial genome of the branching octocoral Paramuricea grayi (Johnson, 1861), phylogenetic relationships and divergence analysis.

The Gray's sea fan, Paramuricea grayi (Johnson, 1861), typically inhabits deep littoral and circalittoral habitats of the eastern temperate and tropical Atlantic Ocean. Along the Iberian Peninsula, where P. grayi is a dominant constituent of circalittoral coral gardens, two segregating lineages (yellow and purple morphotypes) were recently identified using single-copy nuclear orthologues. The mitochondrial genomes of 9 P. grayi individuals covering both color morphotypes were assembled from RNA-seq data, using samples collected at three sites in southern (Sagres and Tavira) and western (Cape Espichel) Portugal. The complete circular mitogenome is 18,668 bp in length, has an A + T-rich base composition (62.5%) and contains the 17 genes typically found in Octocorallia: 14 protein-coding genes (atp6, atp8, cob, cox1-3, mt-mutS, nad1-6, and nad4L), the small and large subunit rRNAs (rns and rnl), and one transfer RNA (trnM). The mitogenomes were nearly identical for all specimens, though we identified a noteworthy polymorphism (two SNPs 9 bp apart) in the mt-mutS of one purple individual that is shared with the sister species P. clavata. The mitogenomes of the two species have a pairwise sequence identity of 99.0%, with nad6 and mt-mutS having the highest rates of non-synonymous substitutions.

Physiological response of the symbiotic gorgonian Eunicella singularis to a long-term temperature increase.

Increase in seawater temperature is one of the major effects of global climate change that affects marine organisms, including Cnidaria. Among them, gorgonians from the NW Mediterranean Sea, such as the species Eunicella singularis, have suffered spectacular and extensive damage. We thus investigated in a controlled laboratory experiment the response of E. singularis to a long-term increase in temperature and we took a special interest in its photosynthetic and calcification response to the stress. Two populations collected at 15 and 35 m depths were studied in order to determine whether there was a difference in sensitivity to thermal stress between living depths. Our results show: (a) that calcification and photosynthesis were impacted only when gorgonians were maintained for more than two weeks at 26 degrees C, and (b) that colonies of E. singularis living in shallow waters were less tolerant than those living in deep waters. Because E. singularis is a symbiotic species, we have also discussed the potential role of symbiosis in the thermotolerance response.

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.

Potential for adaptive evolution at species range margins: contrasting interactions between red coral populations and their environment in a changing ocean.

Studying population-by-environment interactions (PEIs) at species range margins offers the opportunity to characterize the responses of populations facing an extreme regime of selection, as expected due to global change. Nevertheless, the importance of these marginal populations as putative reservoirs of adaptive genetic variation has scarcely been considered in conservation biology. This is particularly true in marine ecosystems for which the deep refugia hypothesis proposes that disturbed shallow and marginal populations of a given species can be replenished by mesophotic ones. This hypothesis therefore assumes that identical PEIs exist between populations, neglecting the potential for adaptation at species range margins. Here, we combine reciprocal transplant and common garden experiments with population genetics analyses to decipher the PEIs in the red coral, Corallium rubrum. Our analyses reveal partially contrasting PEIs between shallow and mesophotic populations separated by approximately one hundred meters, suggesting that red coral populations may potentially be locally adapted to their environment. Based on the effective population size and connectivity analyses, we posit that genetic drift may be more important than gene flow in the adaptation of the red coral. We further investigate how adaptive divergence could impact population viability in the context of warming and demonstrate differential phenotypic buffering capacities against thermal stress. Our study questions the relevance of the deep refugia hypothesis and highlights the conservation value of marginal populations as a putative reservoir of adaptive genetic polymorphism.

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.

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.