Resilience of Long-lived Mediterranean Gorgonians in a Changing World: Insights from Life History Theory and Quantitative Ecology

[eng] Temperate benthic communities face cumulative impacts from multiple stressors acting both at local and global scales. Understanding how local management and ocean warming affect the dynamics and resilience of dominant habitat-forming species is central to marine conservation. In this thesis, we combined long-term demographic surveys and large-scale distribution datasets with innovative population and spatial modeling approaches, and meta-analyses to unravel the causes and consequences of extreme life-histories. The final goal was to understand resilience patterns and mechanisms, and to assess the effectiveness of widely used conservation tools such as fishing regulations, marine protected areas (MPAs), and active restoration. A comparative analysis across marine sessile species revealed strong linkages between depth occurrence, longevity and demographic stability. These results demonstrated a fundamental role of environmental gradients in shaping the evolution of life-history strategies in the ocean and suggest that deep-sea benthic communities tend to be dominated by long-lived species that are very vulnerable to external sources of mortality. In addition, we demonstrate that life-history strategies play a role in important conservation issues such as recovery processes. For instance, recovery times after fishing or restoration actions for long-lived species can take several decades. Thus, accounting for the temporal dimension and life-history tradeoffs in conservation efforts is essential to avoid potential long-lasting impacts and enhance the recovery of damaged ecosystems. Focusing on the Mediterranean red coral Corallium rubrum, an overharvested precious coral emblematic of coralligenous assemblages, we revealed an extremely slow life-history strategy characterized by low reproduction success, high natural survival, and extended longevity. These traits drive a general pattern of slow population dynamics and suggest low resilience to human-driven stressors. We then show that local and global stressors such as overfishing and warming have strong impacts on different demographic processes of red coral populations. Harvesting causes dramatic decreases in total biomass and strong shifts in size-class distribution towards populations dominated by small colonies. More broadly, MPAs strongly enhance structural complexity of red coral populations but, contrary to prior expectations, have little effect on their long-term viability and associated extinction risk. Population recovery after harvesting is a very slow process that can take decades. Interestingly, recovery is not driven by sexual reproduction but by the capacity of harvested colonies to survive and regrow new branches. This recovery mechanism may explain the persistence of this historically overexploited long-lived coral. Unfortunately, novel impacts associated to climate change threat shallow red coral populations. Recurrent warming-driven mass mortality events had detrimental effects on affected populations, causing long-term declines and potential local extinction. While MPAs have been proposed to enhance the resilience of marine ecosystems to climate change, our simulations suggested that MPAs only have a weak buffering effect to climatic impacts. On the other hand, spatial analyses revealed that future climate change may cause extensive impacts on shallow populations of the red coral and the red gorgonian Paramuricea clavata (another emblematic species of coralligenous assemblages with an important structural role) across the Mediterranean Sea. Importantly, we found that the extent and severity of warming impacts is strongly dependent on depth and the global emissions scenarios. Altogether, our results demonstrate a high vulnerability and low demographic resilience of shallow red coral populations to climate change. The results presented in this thesis suggest that, only by simultaneously acting at both local and global scales, we can we ensure the persistence and enhance the structural role of the long-lived Mediterranean red coral. Finally, this thesis also shows the potential of combining long-term large-scale field data, quantitative tools, and principles of life-history theory to provide new perspectives to advance marine conservation in a changing ocean

Long-term monitoring of temperate macroalgal assemblages inside and outside a No take marine reserve

Macroalgal communities have an essential role in the shallow benthic habitats of temperate seas, where changes in their composition can resonate through entire coastal ecosystems. As all major ecosystems on Earth, algal beds have already been affected by multiple disturbances. Passive conservation tools, such as marine protected areas or No-take zones, have the potential to reduce some of the anthropogenic impacts by limiting human activity. However, without a good knowledge of the natural community dynamics, it is not easy to discern between changes fruit of the intrinsic variability of biological communities and the ones caused by human-related stressors. In this study, we evaluated the natural variability of macroalgal communities' composition inside and outside a Mediterranean No-Take marine reserve during 15 years. We described their temporal dynamics considering their main drivers and we tested the effect of protection in seaweed beds. We did not find differences either in the composition of the macroalgal assemblages or the total algal cover between protected and nonprotected locations over the fifteen years of study. Nevertheless, we observed a positive effect of the protection increasing the cover of some specific species, such as the canopy-forming Treptacantha elegans. Our results highlight the importance of obtaining long-term data in ecological studies to better understand the natural variability of marine communities. Accordingly, a robust understanding of the community dynamics would help us to avoid misinterpretations between 'impacted' or 'in-recovery' communities when recovery times are longer than the study periods

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

Re-shifting the ecological baseline for the overexploited Mediterranean red coral

Overexploitation leads to the ecological extinction of many oceanic species. The depletion of historical abundances of large animals, such as whales and sea turtles, is well known. However, the magnitude of the historical overfishing of exploited invertebrates is unclear. The lack of rigorous baseline data limits the implementation of efficient management and conservation plans in the marine realm. The precious Mediterranean red coral Corallium rubrum has been intensively exploited since antiquity for its use in jewellery. It shows dramatic signs of overexploitation, with no untouched populations known in shallow waters. Here, we report the discovery of an exceptional red coral population from a previously unexplored shallow underwater cave in Corsica (France) harbouring the largest biomass (by more than 100-fold) reported to date in the Mediterranean. Our findings challenge current assumptions on the pristine state of this emblematic species. Our results suggest that, before intense exploitation, red coral lived in relatively high-density populations with a large proportion of centuries-old colonies, even at very shallow depths. We call for the re-evaluation of the baseline for red coral and question the sustainability of the exploitation of a species that is still common but ecologically (functionally) extinct and in a trajectory of further decline

Estudi de la dinàmica de la població de l'espècie de briozou Pentapora fascialis de la Reserva Marina de les Illes Medes. Informe tècnic per al Parc Natural del Montgrí, les Illes Medes i el Baix Ter.

Estudi realitzat per la Universitat de Barcelona per encàrrec del Parc Natural del Montgrí, les Illes Medes i el Baix TerAquesta memòria presenta els resultats del grup de treball del Departament d’Ecologia de la UB respecte a l’estudi de les comunitats de briozous de la Reserva Marina de les Illes Medes amb l’objectiu d’estudiar i caracteritzar la dinàmica del briozou Pentapora fascialis i establir les bases per a utilitzar aquesta espècie com a indicadora de l’efecte dels submarinistes sobre les comunitats bentòniques

Harvesting effects, recovery mechanisms, and management strategies for a long-lived and structural precious coral

Overexploitation is a major threat for the integrity of marine ecosystems. Understanding the ecological consequences of different extractive practices and the mechanisms underlying the recovery of populations is essential to ensure sustainable management plans. Precious corals are long-lived structural invertebrates, historically overfished, and their conservation is currently a worldwide concern. However, the processes underlying their recovery are poorly known. Here, we examined harvesting effects and recovery mechanisms of red coral Corallium rubrum by analyzing long-term photographic series taken on two populations that were harvested. We compared the relative importance of reproduction and re-growth as drivers of resilience. Harvesting heavily impacted coral populations causing large de- creases in biomass and strong size-class distribution shifts towards populations dominated by small colonies. At the end of the study (after 4 and 7 years) only partial recovery was ob- served. The observed general pattern of low recruitment and high mortality of new recruits demonstrated limited effects of reproduction on population recovery. Adversely, low mortali- ty of partially harvested adults and a large proportion of colonies showing new branches highlighted the importance of re-growth in the recovery process. The demographic projec- tions obtained through stochastic models confirmed that the recovery rates of C. rubrum can be strongly modulated depending on harvesting procedures. Thus, leaving the basal section of the colonies when harvesting to avoid total mortality largely enhances the resil- ience of C. rubrum populations and quickens their recovery. On the other hand, the high survival of harvested colonies and the significant biomass reduction indicated that abun- dance may not be an adequate metric to assess the conservation status of clonal organisms because it can underestimate harvesting effects. This study highlights the unsustainability of current harvesting practices of C. rubrum and provides urgently needed data to improve management practices that are still largely based on untested assumptions

Seguiment de la biodiversitat marina al Parc Natural de Cap de Creus i al Parc Natural del Montgrí, les Illes Medes i el Baix Ter. Informe 2014

Informe 2014. Contracte nº AG-2014-654 amb la Generalitat de Catalunya. Departament d‘Agricultura, Ramaderia, Pesca, Alimentació i Medi Natural. Servei d'Espais Naturals Protegits.Aquesta memòria presenta els resultats del grup de treball del Departament d’Ecologia de la UB respecte el seguiment de l’any 2014, tal i com consta al plec prescripcions expedient AG-2014-654, en compliment de la llei 19/1990 de 10 de desembre del Parlament de Catalunya, i amb les millores proposades a l’oferta tècnica Seguiment del medi marí als Parcs Naturals marins de Catalunya. Aquests resultats tenen l’objectiu d’avaluar les poblacions i hàbitats marins en relació tant amb les activitats humanes que hi tenen lloc com amb els factors ambientals; analitzar l’estat de les espècies i les comunitats, la seva evolució temporal i l’efecte que hi produeix la protecció, així com detectar altres situacions de risc pel patrimoni natural com podrien ser les espècies introduïdes o invasores o bé els possibles efectes del canvi climàtic

Seguiment anual de Briozous, Gorgònia vermella i Coves a la Reserva Natural Parcial Marina de les Medes del Parc Natural del Montgrí, les illes Medes i el Baix Ter. Memòria 2017

Les mesures de protecció a les illes Medes van entrar en vigor el 1983, amb una Ordre de la Generalitat de Catalunya que establia la Reserva Marina de les illes Medes i que comportava restringir l’activitat en aquest indret de gran interès per a la biodiversitat marina. Al 1985 una resolució establia normes de compliment obligatori a la zona vedada i el 1990 i la Llei 19/1990 va convertir-se en el marc jurídic de la protecció i conservació de la flora i fauna del fons marí de les illes Medes i del tros de costa del Montgrí, entre la roca del Molinet i la Punta Salines. Finalment, El Parc Natural del Montgrí, les illes Medes i el Baix Ter es va crear per la llei 15/2010, de 21 de maig de 2010, amb l’objectiu principal d’unificar la normativa de protecció dels tres espais que conformen el Parc Natural (massís del Montgrí, les illes Medes i el Baix Ter). En aquest espai protegit podem trobar diferents zones amb diferents nivells de protecció: 1) la zona de Parc Natural (PN) a la costa del Montgrí entre la punta del Milà i la punta Salines, on la pesca, inclosa la pesca submarina és permesa; 2) la Zona Perifèrica de Protecció (ZPP) que correspon al tram de costa entre punta Milà i punta del Molinet, on la pesca submarina és prohibida; i 3) la Reserva Natural Parcial (RNP), que comprèn les illes Medes, on no es permet cap tipus d’activitat pesquera. La normativa específica dels usos i activitats de la zona estan regulats pel Pla Rector d’Usos i Gestió recollit aprovat el 2008 (en el Decret 222/2008, d'11 de novembre, pel qual s'aprova el Pla rector d'ús i gestió de l'Àrea Protegida de les illes Medes), i que recentment ha estat modificat en els seus annexes 1 i 6 (ORDRE AAM/112/2015, de 30 d'abril)..

Seguiment anual de Briozous, Gorgònia vermella i Coves a la Reserva Natural Parcial Marina de les Medes del Parc Natural del Montgrí, les illes Medes i el Baix Ter. Memòria 2018

Comanda: Direcció General de Polítiques Ambientals i Medi Natural / Departament de Territori i Sostenibilitat, Generalitat de Catalunya. Número d’expedient: PTOP_2017_130Les mesures de protecció a les illes Medes van entrar en vigor el 1983, amb una Ordre de la Generalitat de Catalunya que establia la Reserva Marina de les illes Medes i que comportava restringir l’activitat en aquest indret de gran interès per a la biodiversitat marina. Al 1985 una resolució establia normes de compliment obligatori a la zona vedada i el 1990 i la Llei 19/1990 va convertir-se en el marc jurídic de la protecció i conservació de la flora i fauna del fons marí de les illes Medes i del tros de costa del Montgrí, entre la roca del Molinet i la Punta Salines. Finalment, El Parc Natural del Montgrí, les illes Medes i el Baix Ter es va crear per la llei 15/2010, de 21 de maig de 2010, amb l’objectiu principal d’unificar la normativa de protecció dels tres espais que conformen el Parc Natural (massís del Montgrí, les illes Medes i el Baix Ter). En aquest espai protegit podem trobar diferents zones amb diferents nivells de protecció: 1) la zona de Parc Natural (PN) a la costa del Montgrí entre la punta del Milà i la punta Salines, on la pesca, inclosa la pesca submarina és permesa; 2) la Zona Perifèrica de Protecció (ZPP) que correspon al tram de costa entre punta Milà i punta del Molinet, on la pesca submarina és prohibida; i 3) la Reserva Natural Parcial (RNP), que comprèn les illes Medes, on no es permet cap tipus d’activitat pesquera. La normativa específica dels usos i activitats de la zona estan regulats pel Pla Rector d’Usos i Gestió recollit aprovat el 2008 (en el Decret 222/2008, d'11 de novembre, pel qual s'aprova el Pla rector d'ús i gestió de l'Àrea Protegida de les illes Medes), i que recentment ha estat modificat en els seus annexes 1 i 6 (ORDRE AAM/112/2015, de 30 d'abril

Temporal variability in the response to thermal stress in the red gorgonian, P. clavata: Insights form common garden experiments

4th Mediterranean Symposium on the Conservation of Coralligenous & other Calcareous Bio-Concretions, 20-21 September 2022, Genoa, Italy.-- 6 pages, 2 figuresRecurrent mass mortality events (MMEs) linked to marine heatwaves (MHWs) have been observed in the Mediterranean Sea affecting thousands of kilometers of coastline. Coralligenous habitats were among the most impacted during these events. Information on how the exposure to recurrent MHWs is affecting the coralligenous is critical to anticipate the consequences of climate change and implement actions to enhance their resilience. Combining field surveys with experiments in controlled conditions allowed to dilucidate the differential responses to thermal stress among species, populations and individuals and to explore the spatial and taxonomic variability response to thermal stress linked to MHWs. Yet, the temporal variability in the response to thermal stress remains to be characterized. Thus, we aim to fill this gap focusing on the temporal variability in the response to thermal stress of the coralligenous key habitat-forming species Paramuricea clavata (Plexauridae). We replicated thermal stress experiments during 3 consecutive years following a common garden setup (control vs. thermal stress) involving the same individuals from the same three populations. Considering different phenotypic responses including the level of tissue necrosis during the time of the experiment and the survival of the individuals, we found that the average percentage of tissue necrosis per population variated greatly across years while the probability of survival was considerably reduced in 2017. During the experiments, several individuals from the 3 populations systematically showed reduced level of tissue necrosis suggesting resistance to thermal stress. Overall our data will contribute to help better inform further conservation strategies of habitat-forming coral species in the Mediterranean SeaPeer reviewe