Positive micro- and macro-organism interactions: the way forward for nature-based restoration of Mediterranean octocorals.

Restoring marine ecosystems is urgent to stop marine biodiversity loss caused by mounting anthropogenic and climate change pressures, and the subsequent impact on human well-being. Corals are priority targets of restoration efforts because they are ecosystem engineers that support high biodiversity and provide many ecosystem services. Diverse methods exist to favour coral recovery (e.g., direct adults’ transplantation, coral gardening, artificial reefs), and their strengths and limitations are well documented. The main concerns related to these approaches are that they are rarely adapted to the biology of the organism being restored and are not based on the ecological processes fundamental to the reproduction and survival of the species. Nature-based approaches that take advantage of ecological processes (i.e. - relying on sexually derived propagules and improved larval settlement to support coral reproductive, recruitment, and growth successes), are more promising for corals’ long-term recovery and for improving their resilience to climate change.

Mortality events of the Mediterranean white gorgonian (Eunicella singularis), mainly caused by climate change, have been observed at shallow depths over the last two decades, and exacerbated environmental pressures are expected to further impact this species in the future. The settlement of E. singularis larvae is promoted by selected crustose coralline algae (CCAs), but the exact mechanism involved in this facilitative process is unknown. A better understanding of the dynamics driving the early life stages of this species is needed to inform its conservation and restoration.

We present the knowledge gained through an experimental study that aimed at understanding 1) whether the microbiome and/or metabolites of specific CCAs may be drivers of higher settlement rate of E. singularis larvae, and 2) how the related mechanisms can be affected by ocean acidification and warming. First, we collected two phylogenetically identified CCA morphotypes, predominant and closely associated with E. singularis forests in Banyuls-sur-Mer (France, Western Mediterranean Sea). Prior to larvae arrival, CCA holobionts were exposed for eight weeks to projected 2100 temperature and pH conditions for the area (+2.5ºC and pH 7.78), and to a heatwave (26ºC for three weeks). Then we used these CCAs as substrates in experimental aquaria in the presence of E. singularis larvae. The bacterial community composition of these holobionts and the production of metabolites were analyzed before and after the treatments, and at the end of the settlement experiment to disentangle their effects on E. singularis larvae. We also assessed the potential transfer of bacteria from CCAs to gorgonian settlers.

Our results suggest that the production of chemical cues by CCAs in synergy with their associated bacterial communities promote a higher settlement success of E. singularis larvae. The unique sharing of bacterial sequences between CCAs and settlers hints at a potential influence of CCAs on the bacteria community composition of E. singularis microbiome, at least in its early life stages.

The study provides ecological knowledge on E. singularis settlement capacity under different climate change scenarios, and inform nature-based restoration strategies.