Differential apicomplexan presence predicts thermal stress mortality in the Mediterranean coral Paramuricea clavata.

Paramuricea clavata is an ecosystem architect of the Mediterranean temperate reefs that is currently threatened by episodic mass mortality events related to global warming. The microbiome may play an active role in the thermal stress susceptibility of corals, potentially holding the answer as to why corals show differential sensitivity to heat stress. To investigate this, the prokaryotic and eukaryotic microbiome of P. clavata collected from around the Mediterranean was characterised before experimental heat stress to determine if its microbial composition influences the thermal response of the holobiont. We found that members of P. clavata's microeukaryotic community were significantly correlated with thermal stress sensitivity. Syndiniales from the Dino-Group I Clade 1 were significantly enriched in thermally resistant corals, while the apicomplexan corallicolids were significantly enriched in thermally susceptible corals. We hypothesise that P. clavata mortality following heat stress may be caused by a shift from apparent commensalism to parasitism in the corallicolid-coral host relationship driven by the added stress. Our results show the potential importance of corallicolids and the rest of the microeukaryotic community of corals to understanding thermal stress response in corals and provide a useful tool to guide conservation efforts and future research into coral-associated microeukaryotes.

When resilience is not enough: 2022 extreme marine heatwave threatens climatic refugia for a habitat-forming Mediterranean octocoral.

Climate change is impacting ecosystems worldwide, and the Mediterranean Sea is no exception. Extreme climatic events, such as marine heat waves (MHWs), are increasing in frequency, extent and intensity during the last decades, which has been associated with an increase in mass mortality events for multiple species. Coralligenous assemblages, where the octocoral Paramuricea clavata lives, are strongly affected by MHWs. The Medes Islands Marine Reserve (NW Mediterranean) was considered a climate refugia for P. clavata, as their populations were showing some resilience to these changing conditions. In this study, we assessed the impacts of the MHWs that occurred between 2016 and 2022 in seven shallow populations of the octocoral P. clavata from a Mediterranean Marine Protected Area. The years that the mortality rates increased significantly were associated with the ones with strong MHWs, 2022 being the one with higher mortalities. In 2022, with 50 MHW days, the proportion of total affected colonies was almost 70%, with a proportion of the injured surface of almost 40%, reaching levels never attained in our study site since the monitoring was started. We also found spatial variability between the monitored populations. Whereas few of them showed low levels of mortality, others lost around 75% of their biomass. The significant impacts documented here raise concerns about the future of shallow P. clavata populations across the Mediterranean, suggesting that the resilience of this species may not be maintained to sustain these populations face the ongoing warming trends.

El canvi climatic està impactant els ecosistemes arreu del planeta, i el Mar Mediterrani no n'és una excepció. Els esdeveniments climàtics extrems, com ara les onades de calor marines, estan augmentant en freqüència, extensió i intensitat en les darreres dècades, i estan sent associades a un increment dels esdeveniments de mortalitat massiva de múltiples espècies. El coral·ligen, on hi viu l'octocorall Paramuricea clavata, està altament afectat per les onades de calor marines. La Reserva Marina de les Illes Medes (NO del Mediterrani) es considerava un refugi climàtic per aquesta espècie, degut a que les seves poblacions mostraven certa resiliència a les condicions canviants. En aquest estudi hem avaluat els impactes de les onades de calor marines succeïdes entre els anys 2016 i 2022 a set poblacions someres de l'octocorall P. clavata, en una Àrea Marina Protegida del Mediterrani. Els anys en els quals les taxes de mortalitat van incrementar significativament s'associen amb els anys amb fortes onades de calor marines, sent el 2022 l'any amb la mortalitat més elevada. Al 2022, amb 50 dies d'onada de calor, la proporció total de colònies afectades va ser prop del 70%, amb un percentatge de superfície afectada de gairebé el 40%, arribant a valors mai observats en el lloc d'estudi des de que es va iniciar el seguiment d'aquestes poblacions. També hem observat variabilitat espacial entre les poblacions mostrejades. Mentre que algunes d'elles han mostrat poca mortalitat, altres han perdut al voltant del 75% de la seva biomassa. Els impactes documentats en aquest estudi mostren un futur preocupant de les poblacions someres de P. clavata arreu del Mediterrani, i això suggereix que la resiliència d'aquesta espècie podria no ser suficient per mantenir les seves poblacions en l'escenari d'escalfament que es preveu.

Marine Citizen Science and the Conservation of Mediterranean Corals: The Relevance of Training, Expert Validation, and Robust Sampling Protocols.

Marine Citizen Science (MCS) has emerged as a promising tool to enhance conservation efforts. Although the quality of volunteer data has been questioned, the design of specific protocols, effective training programs, and data validation by experts have enabled us to overcome these quality concerns, thus ensuring data reliability. Here, we validated the effectiveness of volunteer training in assessing the conservation status of Mediterranean coral species. We conducted a comparative analysis of data collected by volunteers with different levels of expertise, demonstrating improvements in data precision and accuracy with only one training session, thereby achieving values equivalent to those obtained by scientists. These outcomes align with the feedback received from volunteers through a qualitative survey. Finally, we analysed the data generated by volunteers and validated by experts using the developed protocol in the Coral Alert project from the Observadores del Mar MCS initiative. Our findings highlight the importance of proper training, expert validation, robust sampling protocols, and a well-structured platform to ensure the success of long-term MCS projects. Overall, our results stress the key role MCS plays in enhancing the conservation and management strategies designed to mitigate the ongoing environmental crisis.

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.

An integrated assessment of the Good Environmental Status of Mediterranean Marine Protected Areas.

Local, regional and global targets have been set to halt marine biodiversity loss. Europe has set its own policy targets to achieve Good Environmental Status (GES) of marine ecosystems by implementing the Marine Strategy Framework Directive (MSFD) across member states. We combined an extensive dataset across five Mediterranean ecoregions including 26 Marine Protected Areas (MPAs), their reference unprotected areas, and a no-trawl case study. Our aim was to assess if MPAs reach GES, if their effects are local or can be detected at ecoregion level or up to a Mediterranean scale, and which are the ecosystem components driving GES achievement. This was undertaken by using the analytical tool NEAT (Nested Environmental status Assessment Tool), which allows an integrated assessment of the status of marine systems. We adopted an ecosystem approach by integrating data from several ecosystem components: the seagrass Posidonia oceanica, macroalgae, sea urchins and fish. Thresholds to define the GES were set by dedicated workshops and literature review. In the Western Mediterranean, most MPAs are in good/high status, with P. oceanica and fish driving this result within MPAs. However, GES is achieved only at a local level, and the Mediterranean Sea, as a whole, results in a moderate environmental status. Macroalgal forests are overall in bad condition, confirming their status at risk. The results are significantly affected by the assumption that discrete observations over small spatial scales are representative of the total extension investigated. This calls for large-scale, dedicated assessments to realistically detect environmental status changes under different conditions. Understanding MPAs effectiveness in reaching GES is crucial to assess their role as sentinel observatories of marine systems. MPAs and trawling bans can locally contribute to the attainment of GES and to the fulfillment of the MSFD objectives. Building confidence in setting thresholds between GES and non-GES, investing in long-term monitoring, increasing the spatial extent of sampling areas, rethinking and broadening the scope of complementary tools of protection (e.g., Natura 2000 Sites), are indicated as solutions to ameliorate the status of the basin.

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.

A fast-moving target: achieving marine conservation goals under shifting climate and policies.

In the Anthropocene, marine ecosystems are rapidly shifting to new ecological states. Achieving effective conservation of marine biodiversity has become a fast-moving target because of both global climate change and continuous shifts in marine policies. How prepared are we to deal with this crisis? We examined EU Member States Programs of Measures designed for the implementation of EU marine environmental policies, as well as recent European Marine Spatial Plans, and discovered that climate change is rarely considered operationally. Further, our analysis revealed that monitoring programs in marine protected areas are often insufficient to clearly distinguish between impacts of local and global stressors. Finally, we suggest that while the novel global Blue Growth approach may jeopardize previous marine conservation efforts, it can also provide new conservation opportunities. Adaptive management is the way forward (e.g., preserving ecosystem functions in climate change hotspots, and identifying and targeting climate refugia areas for protection) using Marine Spatial Planning as a framework for action, especially given the push for Blue Growth.

Climate change, biological invasions, and the shifting distribution of Mediterranean fishes: A large-scale survey based on local ecological knowledge.

Climate change and biological invasions are rapidly reshuffling species distribution, restructuring the biological communities of many ecosystems worldwide. Tracking these transformations in the marine environment is crucial, but our understanding of climate change effects and invasive species dynamics is often hampered by the practical challenge of surveying large geographical areas. Here, we focus on the Mediterranean Sea, a hot spot for climate change and biological invasions to investigate recent spatiotemporal changes in fish abundances and distribution. To this end, we accessed the local ecological knowledge (LEK) of small-scale and recreational fishers, reconstructing the dynamics of fish perceived as "new" or increasing in different fishing areas. Over 500 fishers across 95 locations and nine different countries were interviewed, and semiquantitative information on yearly changes in species abundance was collected. Overall, 75 species were mentioned by the respondents, mostly warm-adapted species of both native and exotic origin. Respondents belonging to the same biogeographic sectors described coherent spatial and temporal patterns, and gradients along latitudinal and longitudinal axes were revealed. This information provides a more complete understanding of the shifting distribution of Mediterranean fishes and it also demonstrates that adequately structured LEK methodology might be applied successfully beyond the local scale, across national borders and jurisdictions. Acknowledging this potential through macroregional coordination could pave the way for future large-scale aggregations of individual observations, increasing our potential for integrated monitoring and conservation planning at the regional or even global level. This might help local communities to better understand, manage, and adapt to the ongoing biotic transformations driven by climate change and biological invaders.

Cross-basin and cross-taxa patterns of marine community tropicalization and deborealization in warming European seas.

Ocean warming and acidification, decreases in dissolved oxygen concentrations, and changes in primary production are causing an unprecedented global redistribution of marine life. The identification of underlying ecological processes underpinning marine species turnover, particularly the prevalence of increases of warm-water species or declines of cold-water species, has been recently debated in the context of ocean warming. Here, we track changes in the mean thermal affinity of marine communities across European seas by calculating the Community Temperature Index for 65 biodiversity time series collected over four decades and containing 1,817 species from different communities (zooplankton, coastal benthos, pelagic and demersal invertebrates and fish). We show that most communities and sites have clearly responded to ongoing ocean warming via abundance increases of warm-water species (tropicalization, 54%) and decreases of cold-water species (deborealization, 18%). Tropicalization dominated Atlantic sites compared to semi-enclosed basins such as the Mediterranean and Baltic Seas, probably due to physical barrier constraints to connectivity and species colonization. Semi-enclosed basins appeared to be particularly vulnerable to ocean warming, experiencing the fastest rates of warming and biodiversity loss through deborealization.

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.

Assessing the effectiveness of marine reserves on unsustainably harvested long-lived sessile invertebrates.

Although the rapid recovery of fishes after establishment of a marine reserve is well known, much less is known about the response of long-lived, sessile, benthic organisms to establishment of such reserves. Since antiquity, Mediterranean red coral (Corallium rubrum) has been harvested intensively for use in jewelry, and its distribution is currently smaller than its historical size throughout the Mediterranean Sea. To assess whether establishment of marine reserves is associated with a change in the size and number of red coral colonies that historically were not harvested sustainably, we analyzed temporal changes in mean colony diameter and density from 1992 to 2005 within red coral populations at different study sites in the Medes Islands Marine Reserve (established in 1992) and in adjacent unprotected areas. Moreover, we compared colony size in the Medes Islands Marine Reserve, where recreational diving is allowed and poaching has been observed after reserve establishment, with colony size in three other marine protected areas (Banyuls, Carry-le-Rouet, and Scandola) with the enforced prohibition of fishing and diving. At the end of the study, the size of red coral colonies at all sampling sites in the Medes Islands was significantly smaller than predicted by growth models and smaller than those in marine protected areas without fishing and diving. The annual number of recreational dives and the percent change in the basal diameter of red coral colonies were negatively correlated, which suggests that abrasion by divers may increase the mortality rates of the largest red coral colonies within this reserve . Our study is the first quantitative assessment of a poaching event, which was detected during our monitoring in 2002, inside the marine reserve. Poaching was associated with a loss of approximately 60% of the biomass of red coral colonies.

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.

Mediterranean rocky reefs in the Anthropocene: Present status and future concerns.

Global change is striking harder and faster in the Mediterranean Sea than elsewhere, where high levels of human pressure and proneness to climate change interact in modifying the structure and disrupting regulative mechanisms of marine ecosystems. Rocky reefs are particularly exposed to such environmental changes with ongoing trends of degradation being impressive. Due to the variety of habitat types and associated marine biodiversity, rocky reefs are critical for the functioning of marine ecosystems, and their decline could profoundly affect the provision of essential goods and services which human populations in coastal areas rely upon. Here, we provide an up-to-date overview of the status of rocky reefs, trends in human-driven changes undermining their integrity, and current and upcoming management and conservation strategies, attempting a projection on what could be the future of this essential component of Mediterranean marine ecosystems.

The Genome Sequence of the Octocoral Paramuricea clavata - A Key Resource To Study the Impact of Climate Change in the Mediterranean.

The octocoral, Paramuricea clavata, is a habitat-forming anthozoan with a key ecological role in rocky benthic and biodiversity-rich communities in the Mediterranean and Eastern Atlantic. Shallow populations of P. clavata in the North-Western Mediterranean are severely affected by warming-induced mass mortality events (MMEs). These MMEs have differentially impacted individuals and populations of P. clavata (i.e., varied levels of tissue necrosis and mortality rates) over thousands of kilometers of coastal areas. The eco-evolutionary processes, including genetic factors, contributing to these differential responses remain to be characterized. Here, we sequenced a P. clavata individual with short and long read technologies, producing 169.98 Gb of Illumina paired-end and 3.55 Gb of Oxford Nanopore Technologies (ONT) reads. We obtained a de novo genome assembly accounting for 607 Mb in 64,145 scaffolds. The contig and scaffold N50s are 19.15 Kb and 23.92 Kb, respectively. Despite of the low contiguity of the assembly, its gene completeness is relatively high, including 75.8% complete and 9.4% fragmented genes out of the 978 metazoan genes contained in the metazoa_odb9 database. A total of 62,652 protein-coding genes have been annotated. This assembly is one of the few octocoral genomes currently available. This is undoubtedly a valuable resource for characterizing the genetic bases of the differential responses to thermal stress and for the identification of thermo-resistant individuals and populations. Overall, having the genome of P. clavata will facilitate studies of various aspects of its evolutionary ecology and elaboration of effective conservation plans such as active restoration to overcome the threats of global change.

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.

Response diversity in Mediterranean coralligenous assemblages facing climate change: Insights from a multispecific thermotolerance experiment.

Climate change threatens coastal benthic communities on a global scale. However, the potential effects of ongoing warming on mesophotic temperate reefs at the community level remain poorly understood. Investigating how different members of these communities will respond to the future expected environmental conditions is, therefore, key to anticipating their future trajectories and developing specific management and conservation strategies. Here, we examined the responses of some of the main components of the highly diverse Mediterranean coralligenous assemblages to thermal stress. We performed thermotolerance experiments with different temperature treatments (from 26 to 29°C) with 10 species from different phyla (three anthozoans, six sponges and one ascidian) and different structural roles. Overall, we observed species-specific contrasting responses to warming regardless of phyla or growth form. Moreover, the responses ranged from highly resistant species to sensitive species and were mostly in agreement with previous field observations from mass mortality events (MMEs) linked to Mediterranean marine heat waves. Our results unravel the diversity of responses to warming in coralligenous outcrops and suggest the presence of potential winners and losers in the face of climate change. Finally, this study highlights the importance of accounting for species-specific vulnerabilities and response diversity when forecasting the future trajectories of temperate benthic communities in a warming ocean.

Divergent responses to warming of two common co-occurring Mediterranean bryozoans.

Climate change threatens the structure and function of marine ecosystems, highlighting the importance of understanding the response of species to changing environmental conditions. However, thermal tolerance determining the vulnerability to warming of many abundant marine species is still poorly understood. In this study, we quantified in the field the effects of a temperature anomaly recorded in the Mediterranean Sea during the summer of 2015 on populations of two common sympatric bryozoans, Myriapora truncata and Pentapora fascialis. Then, we experimentally assessed their thermal tolerances in aquaria as well as different sublethal responses to warming. Differences between species were found in survival patterns in natural populations, P. fascialis showing significantly lower survival rates than M. truncata. The thermotolerance experiments supported field observations: P. fascialis started to show signs of necrosis when the temperature was raised to 25-26 °C and completely died between 28-29 °C, coinciding with the temperature when we observed first signs of necrosis in M. truncata. The results from this study reflect different responses to warming between these two co-occurring species, highlighting the importance of combining multiple approaches to assess the vulnerability of benthic species in a changing climate world.

Thermal stratification drives movement of a coastal apex predator.

A characterization of the thermal ecology of fishes is needed to better understand changes in ecosystems and species distributions arising from global warming. The movement of wild animals during changing environmental conditions provides essential information to help predict the future thermal response of large marine predators. We used acoustic telemetry to monitor the vertical movement activity of the common dentex (Dentex dentex), a Mediterranean coastal predator, in relation to the oscillations of the seasonal thermocline during two summer periods in the Medes Islands marine reserve (NW Mediterranean Sea). During the summer stratification period, the common dentex presented a clear preference for the warm suprathermoclinal layer, and adjusted their vertical movements following the depth changes of the thermocline. The same preference was also observed during the night, when fish were less active. Due to this behaviour, we hypothesize that inter-annual thermal oscillations and the predicted lengthening of summer conditions will have a significant positive impact on the metabolic efficiency, activity levels, and population dynamics of this species, particularly in its northern limit of distribution. These changes in the dynamics of an ecosystem's keystone predator might cascade down to lower trophic levels, potentially re-defining the coastal fish communities of the future.