Population collapse of habitat-forming species in the Mediterranean: a long-term study of gorgonian populations affected by recurrent marine heatwaves

Understanding the resilience of temperate reefs to climate change requires exploring the recovery capacity of their habitat-forming species from recurrent marine heatwaves (MHWs). Here, we show that, in a Mediterranean highly enforced marine protected area established more than 40 years ago, habitat-forming octocoral populations that were first affected by a severe MHW in 2003 have not recovered after 15 years. Contrarily, they have followed collapse trajectories that have brought them to the brink of local ecological extinction. Since 2003, impacted populations of the red gorgonian Paramuricea clavata (Risso, 1826) and the red coral Corallium rubrum (Linnaeus, 1758) have followed different trends in terms of size structure, but a similar progressive reduction in density and biomass. Concurrently, recurrent MHWs were observed in the area during the 2003–2018 study period, which may have hindered populations recovery. The studied octocorals play a unique habitat-forming role in the coralligenous assemblages (i.e. reefs endemic to the Mediterranean Sea home to approximately 10% of its species). Therefore, our results underpin the great risk that recurrent MHWs pose for the long-term integrity and functioning of these emblematic temperate reefs.

Effects of global warming on Mediterranean coral forests

The effects of global warming have been addressed on coral reefs in tropical areas, while it is still unclear how coral forests are reacting, particularly at temperate latitudes. Here we show how mesophotic coral forests are affected by global warming in the Mediterranean Sea. We highlight how the current warming trend is causing the lowering of the thermocline and it is enhancing mucilaginous blooms. These stressors are facilitating a massive macroalgal epibiosis on living corals, here reported for the first time from different areas in the Western and Central Mediterranean Sea. We provide a focus of this phenomenon at Tremiti Islands Marine Protected Area (Adriatic Sea), were the density of the endemic red gorgonian Paramuricea clavata decreased of up to 47% in 5 years, while up to the 96% of the living corals showed signs of stress and macroalgal epibiosis. Only populations deeper than 60 m depth were not touched by this emerging phenomenon. Spot observations performed at Tuscan Archipelago and Tavolara Marine Protected Area (Tyrrhenian Sea) suggest that this this combination of stressors is likely widespread at basin scale.

The Importance of Food Pulses in Benthic-Pelagic Coupling Processes of Passive Suspension Feeders

Benthic-pelagic coupling processes and the quantity of carbon transferred from the water column to the benthic suspension feeders needs multiple intensive sampling approaches where several environmental variables and benthos performance are quantified. Here, activity, dietary composition, and capture rates of three Mediterranean gorgonians (Paramuricea clavata, Eunicella singularis, and Leptogorgia sarmentosa) were assessed in an intensive cycle considering different variables such as the seston concentration and quality (e.g., carbon, nitrogen, and zooplankton), the colony branch patterns, and the energetic input of the single species (i.e., mixotrophic and heterotrophic). The three species showed clear differences in their impact on the seston concentration. Paramuricea clavata, the most densely distributed, showed a greater impact on the near bottom water column seston. The lowest impact of E. singularis on the seston could be explained by its mixotrophy and colony branching pattern. Leptogorgia sarmentosa had a similar impact as E. singularis, having a much more complex branching pattern and more than an order of magnitude smaller number of colonies per meter square than the other two octocorals. The amount of carbon ingested in the peaks of the capture rates in the three species may cover a non-neglectable proportion of the potential carbon fluxes.

Animal Forest Mortality: Following the Consequences of a Gorgonian Coral Loss on a Mediterranean Coralligenous Assemblage

In this work, the consequences of a local gorgonian coral mortality on the whole coralligenous assemblage were studied. A Before/After-Control/Impact sampling design was used: the structure of the coralligenous assemblage was compared before and after the gorgonian mortality event at the mortality site and two control sites. At the mortality site, a relevant decrease in alpha and beta diversity occurred, with a shift from a stratified assemblage characterized by gorgonians and other invertebrates to an assemblage dominated by algal turfs; conversely, neither significant variations of the structure nor decrease in biodiversity were observed at the control sites. The assemblage shift involved the main taxa in different times: in autumn 2018, a large proportion of the plexaurid coral Paramuricea clavata died, but no significant changes were observed in the structure of the remaining assemblage. Then, in autumn 2019, algal turfs increased significantly and, one year later, the abundance of the gorgonian Eunicella cavolini and bryozoans collapsed. Although the mechanisms of the assemblage shift following gorgonian loss will remain uncertain and a cause-effect relationship cannot be derived, results suggest the need for detecting signs of gorgonian forests stress in monitoring programs, which should be considered early indicators of their condition. in the coralligenous monitoring programs for detecting any sign of gorgonian forests stress which should be considered an early indicator of the assemblage condition.

Updating the current knowledge on the relationships between Haplosyllis chamaeleon Laubier, 1960 (Annelida, Syllidae) and Paramuricea clavata (Risso, 1826) (Cnidaria, Plexauridae) in the Mediterranean Sea

In the Mediterranean Sea, the symbiosis between the gorgonian Paramuricea clavata (Risso, 1826) and the polychaete Haplosyllis chamaeleon Laubier, 1960 (Annelida, Syllidae, Syllinae) has only been documented from the western basin. Our findings extend its geographic distribution to the north-central basin and represent the first record of H. chamaeleon in Italy and Croatia. Periodic observations from the Ligurian Sea allowed establishing that the symbiont occurs on P. clavata almost throughout the year, showing a reproductive period longer than previously reported. Morphometric comparisons of three Mediterranean populations, from Portofino Promontory (Ligurian Sea), Cape of Creus (Catalan Sea) and Chafarinas Archipelago (Alboran Sea) proved that there were no significant differences in body measurements, whilst the observed differences in dorsal cirri length pattern could be consider intra-specific. Our behavioural observations confirm that the species had (i) a kleptoparasitic behaviour, (ii) did not cause injuries to the host and (iii) did not induce the host to generate any malformation.

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.

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 and 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 hybrid assembly accounting for 712.4 Mb and 107,682 scaffolds. The contig and scaffold N50 are 15.85 Kb and 17.01 Kb, respectively. Despite of the low contiguity of the assembly, the gene completeness was relatively high, including 86% of the 978 metazoan genes contained in the metazoa_odb9 database. A total of 76,508 protein-coding genes and 85,763 transcripts 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, the genome of P. clavata will help to understand various aspects of its evolutionary ecology and to elaborate effective conservation plans such as active restoration actions to overcome the threats of global change.

The importance of coastal gorgonians in the blue carbon budget

Terrestrial (trees, shrubs) and marine (seaweeds and seagrasses) organisms act as carbon (C) sinks, but the role of benthic suspension feeders in this regard has been largely neglected so far. Gorgonians are one of the most conspicuous inhabitants of marine animal forests (mainly composed of sessile filter feeders); their seston capture rates influence benthic-pelagic coupling processes and they act as C sinks immobilizing carbon in their long-living structures. Three gorgonian species (Paramuricea clavata, Eunicella singularis and Leptogorgia sarmentosa) were studied coupling data of population size structure, biomass and spatial distribution in a NW Mediterranean area (Cap de Creus, Spain) with feeding, respiration and growth rates. In the study area, we calculated that P. clavata sequestered 0.73 ± 0.71 g C m−2 year−1, E. singularis 0.73 ± 0.89 g C m−2 year−1 and L. sarmentosa 0.03 ± 0.02 g C m−2 year−1. To our knowledge, this is the first attempt to calculate the importance as C sinks of gorgonian species that we consider as a starting point to estimate the importance of marine animal forests in C sequestration, and to ensure appropriate management and protection especially in areas and at depths where they are concentrated.