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.

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 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.

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.

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.

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.

Stable symbionts across the HMA-LMA dichotomy: low seasonal and interannual variation in sponge-associated bacteria from taxonomically diverse hosts.

Marine sponges host bacterial communities with important ecological and economic roles in nature and society, yet these benefits depend largely on the stability of host-symbiont interactions and their susceptibility to changing environmental conditions. Here, we investigated the temporal stability of complex host-microbe symbioses in a temperate, seasonal environment over three years, targeting sponges across a range of symbiont density (high and low microbial abundance, HMA and LMA) and host taxonomy (six orders). Symbiont profiling by terminal restriction fragment length polymorphism analysis of 16S rRNA gene sequences revealed that bacterial communities in all sponges exhibited a high degree of host specificity, low seasonal dynamics and low interannual variability: results that represent an emerging trend in the field of sponge microbiology and contrast sharply with the seasonal dynamics of free-living bacterioplankton. Further, HMA sponges hosted more diverse, even and similar symbiont communities than LMA sponges and these differences in community structure extended to core members of the microbiome. Together, these findings show clear distinctions in symbiont structure between HMA and LMA sponges while resolving notable similarities in their stability over seasonal and inter-annual scales, thus providing insight into the ecological consequences of the HMA-LMA dichotomy and the temporal stability of complex host-microbe symbioses.