The response of Mediterranean coralligenous assemblages to climate change: an integrated, long-term view from species and populations to the ecosystem level

Climate change has emerged as one of the greatest and most pervasive threats that our natural heritage will have to face in the coming decades. Together with other anthropogenic pressures such as pollution, overfishing or habitat degradation, climate change is causing enormous impacts on oceans, affecting all kind of marine communities and driving major losses to biodiversity. In this framework of global change, the Mediterranean Sea, which has been identified as one of the major hotspots of marine biodiversity, has also become a hotspot of climate change. Consequently, some of its most emblematic and ecologically important communities are now under threat. This is the case of the coralligenous assemblages, which are temperate benthic communities which stand out for their great structural complexity and exceptional biodiversity (they harbour approximately 10% of Mediterranean species). Most of the constituent species of these communities exhibit high longevity and slow population dynamics. Consequently, they are especially vulnerable to disturbances that increase adults mortality. In fact, thermal anomalies linked to ocean warming have impacted the coralligenous assemblages in several ways during last decades, triggering changes that go from the observed mass mortalities of benthic organisms to potential changes at the community and ecosystem levels. However, despite the increasing interest of the scientific community to conserve the coralligenous, how these benthic communities are responding to climate change at the community level is poorly understood. In this thesis, we have taken this leap by integrating responses from species to the ecosystem level, through populations and communities. In particular, we have combined field observations of ecological and environmental changes, aquaria experiments, ecological theory, and cutting-edge quantitative research to improve our understanding of the bio-ecological consequences of ocean warming for Mediterranean coralligenous assemblages. In the first three chapters, we gathered field and experimental data on sensitivity of several coralligenous species and populations to marine heatwaves (MHWs) by conducting a literature review on previous mass mortality events occurred in the Mediterranean and by carrying out scaled-up thermotolerance experiments. The results of Chapter 1 revealed contrasting patterns of sensitivity to MHWs among different coralligenous species and populations. The posterior multi-specific thermotolerance experiment (including corals, sponges and tunicates) conducted in Chapter 2 confirmed the high response diversity to warming among co-occurring species observed in the field. These results demonstrate that co-occurring species that are taxonomically and morpho- functionally similar can have contrasting thermotolerances. Moreover, the observed patterns suggest that coralligenous assemblages could have certain degree of insurance against MHWs, since the decline of sensitive species could potentially be compensated by other functionally similar species that are more resistant. The results of the multi- population thermal experiment conducted in Chapter 3 with 12 populations of the red gorgonian Paramuricea clavata (Risso, 1826) revealed that this species, which has a key habitat-forming role in coralligenous assemblages, is highly sensitive to thermal stress across its distributional range. Moreover, we found little local adaptation to average thermal regime and little acclimatization to local above-average warm temperatures prior to the experiment. These findings, which were obtained at a spatial scale never addressed before (> 2000 km) for P. clavata, question the adaptive potential of this species to climate change. In Chapter 4, we further explored the vulnerability of Mediterranean habitat- forming octocorals to climate change by exploring the long-term recovery capacity of Corallium rubrum (Linnaeus, 1758) and P. clavata from recurrent MHWs. We explored the long-term trajectories (15 years) of different populations that were firstly impacted by the 2003-MHW in terms of changes in biomass, density and size structure. We found that all impacted populations have followed collapse trajectories. These results further highlight the high vulnerability of these species to the ongoing climate change. Finally, we took the leap from species and populations to the community and ecosystem levels in Chapter 5, to explore if MHWs have driven changes in the functional community structure of coralligenous assemblages, which could imply changes for ecosystem functioning. Specifically, we conducted a multi-taxa, trait-based analysis and found that MHW are shifting the functional identity of coralligenous assemblages (i.e., dominant functional traits). Interestingly, the observed changes were driven primarily by the decline of a single functional group (habitat-forming octocorals), whose species are functionally unique. Consequently, by severely affecting habitat-forming octocorals, MHWs are leading to assemblages that are deficient in key functional traits, likely causing changes in ecosystem functioning. Overall, this thesis provides an integrated, long-term view of the interconnected responses to ocean warming found in coralligenous assemblages. The combined results of this thesis suggest that despite structural changes induced by climate change, most ecosystem functions count on certain degree of insurance against MHWs. However, some essential functions (e.g., 3D-habitat provision) could be highly compromised or even totally disappear, threatening the overall assemblage stability. Given the current climate change trends, identifying and preserving the mechanisms that maintain essential ecosystem functions and the overall ecosystem stability is critical. In this thesis, we have identified the general loss of arborescent octocorals as the greatest disruptive process for coralligenous assemblages. Therefore, the future trajectories of these emblematic Mediterranean communities will greatly depend on the design and implementation of measures that favour the conservation and adaptive management of these key habitat-forming species in the face of climate change