Marine protected areas promote stability of reef fish communities under climate warming.

Protection from direct human impacts can safeguard marine life, yet ocean warming crosses marine protected area boundaries. Here, we test whether protection offers resilience to marine heatwaves from local to network scales. We examine 71,269 timeseries of population abundances for 2269 reef fish species surveyed in 357 protected versus 747 open sites worldwide. We quantify the stability of reef fish abundance from populations to metacommunities, considering responses of species and functional diversity including thermal affinity of different trophic groups. Overall, protection mitigates adverse effects of marine heatwaves on fish abundance, community stability, asynchronous fluctuations and functional richness. We find that local stability is positively related to distance from centers of high human density only in protected areas. We provide evidence that networks of protected areas have persistent reef fish communities in warming oceans by maintaining large populations and promoting stability at different levels of biological organization.

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.

Ecological traits, genetic diversity and regional distribution of the macroalga Treptacantha elegans along the Catalan coast (NW Mediterranean Sea).

The widespread decline of canopy-forming macroalgal assemblages has been documented in many regions during the last decades. This pattern is often followed by the replacement of structurally complex algal canopies by more simplified habitats (e.g., turfs or sea urchin barren grounds). Against all odds, the fucoid Treptacantha elegans, a large Mediterranean brown macroalga, broadened its depth range to deeper and exposed environments and displayed an unexpected range expansion along the northern coast of Catalonia over the last two decades. Here, we reconstruct the spread of T. elegans in time and space and unravel ecological and demographic traits such as population dynamics and genetic patterns to provide a comprehensive and integrated view of the current status and geographical expansion for this species. Fast-growing dynamics, early fertile maturity, and high turnover rate are the main competitive advantages that allow the exposed populations of T. elegans to colonize available substrata and maintain dense and patchy populations. We also provided evidence that the deeper and exposed populations of T. elegans constitute a single group across the Catalan coast, with little genetic differentiation among populations. This seems to support the hypothesis of a unique source of spread in the last decades from the Medes Islands No-Take Zone towards both southern and northern waters.

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 non-protected 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.

No-take marine reserves control the recovery of sea urchin populations after mass mortality events.

Understanding how no-take zones (NTZs) shape the population dynamics of key herbivores is crucial for the conservation and management of temperate benthic communities. Here, we examine the recovery patterns of sea urchin populations following a high-intensity storm under contrasting protection regimes in the NW Mediterranean Sea. We found significant differences in the recovery trends of Paracentrotus lividus abundance and biomass in the five years following the storm. The P. lividus populations outside the NTZ recovered faster than the populations inside the NTZ, revealing that predation was the main factor controlling the sea urchin populations inside the NTZ during the study period. Arbacia lixula reached the highest abundance and biomass values ever observed outside the NTZ in 2016. Our findings reveal that predation can control the establishment of new sea urchin populations and emphasize top-down control in NTZs, confirming the important role of fully protected areas in the structure of benthic communities.

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.

Long-term shifts in the north western Mediterranean coastal seascape: The habitat-forming seaweed Codium vermilara.

Long-term ecological studies are crucial to understand how and why natural ecosystems change over time and space. Through a revision of historical data and a comparison with current in situ field data, we contribute to the understanding of how the Mediterranean coastal seascape has changed in the last decades. Here we describe the large decrease of the main habitat-forming species Codium vermilara along the Catalan coast (NW Mediterranean). We have analyzed data on presence/absence, abundance and biomass. Since the 70s-80s, when the species reached its highest abundances, the species has totally disappeared from 45% of the revisited sites, and showed a decrease in 95% of its abundance and 97% of its biomass. Codium vermilara has also shown a reduction in its depth range, from 30 to the first 20m depth. This study highlights the importance of having historical data to detect and describe changes in ecological systems.

Effective dispersal and density-dependence in mesophotic macroalgal forests: Insights from the Mediterranean species Cystoseira zosteroides.

Dispersal and recruitment are fundamental processes for population recovery following disturbances in sessile species. While both processes are well understood for many terrestrial species, they still remain poorly resolved for some macroalgal species. Here we experimentally investigated the effective dispersal and recruit survival of a mesophotic Mediterranean fucoid, Cystoseira zosteroides. In three isolated populations, four sets of settlement collectors were placed at increasing distances (from 0 to 10 m) and different orientations (North, South, East and West). We observed that effective dispersal was restricted to populations' vicinity, with an average of 6.43 m and not further than 13.33 m, following a Weibull distribution. During their first year of life, survival was up to 50%, but it was lower underneath the adult canopy, suggesting a negative density-dependence. To put our results in a broader context we compared the effective dispersal of other fucoid and kelp species reported in the literature, which confirmed the low dispersal ability of brown algae, in particular for fucoids, with an effective dispersal of few meters. Given the importance of recruitment for the persistence and recovery of populations after disturbances, these results underline the vulnerability of C. zosteroides and other fucoid species to escalating threats.

Thermal stratification drives movement of a coastal apex predator.

A characterization of the thermal ecology of fishes is needed to better understand changes in ecosystems and species distributions arising from global warming. The movement of wild animals during changing environmental conditions provides essential information to help predict the future thermal response of large marine predators. We used acoustic telemetry to monitor the vertical movement activity of the common dentex (Dentex dentex), a Mediterranean coastal predator, in relation to the oscillations of the seasonal thermocline during two summer periods in the Medes Islands marine reserve (NW Mediterranean Sea). During the summer stratification period, the common dentex presented a clear preference for the warm suprathermoclinal layer, and adjusted their vertical movements following the depth changes of the thermocline. The same preference was also observed during the night, when fish were less active. Due to this behaviour, we hypothesize that inter-annual thermal oscillations and the predicted lengthening of summer conditions will have a significant positive impact on the metabolic efficiency, activity levels, and population dynamics of this species, particularly in its northern limit of distribution. These changes in the dynamics of an ecosystem's keystone predator might cascade down to lower trophic levels, potentially re-defining the coastal fish communities of the future.

An ecosystem-based approach to assess the status of Mediterranean algae-dominated shallow rocky reefs.

A conceptual model was constructed for the functioning the algae-dominated rocky reef ecosystem of the Mediterranean Sea. The Ecosystem-Based Quality Index (reef-EBQI) is based upon this model. This index meets the objectives of the EU Marine Strategy Framework Directive. It is based upon (i) the weighting of each compartment, according to its importance in the functioning of the ecosystem; (ii) biological parameters assessing the state of each compartment; (iii) the aggregation of these parameters, assessing the quality of the ecosystem functioning, for each site; (iv) and a Confidence Index measuring the reliability of the index, for each site. The reef-EBQI was used at 40 sites in the northwestern Mediterranean. It constitutes an efficient tool, because it is based upon a wide set of functional compartments, rather than upon just a few species; it is easy and inexpensive to implement, robust and not redundant with regard to already existing indices.

Ordinary and Extraordinary Movement Behaviour of Small Resident Fish within a Mediterranean Marine Protected Area.

It is important to account for the movement behaviour of fishes when designing effective marine protected areas (MPAs). Fish movements occur across different spatial and temporal scales and understanding the variety of movements is essential to make correct management decisions. This study describes in detail the movement patterns of an economically and commercially important species, Diplodus sargus, within a well-enforced Mediterranean MPA. We monitored horizontal and vertical movements of 41 adult individuals using passive acoustic telemetry for up to one year. We applied novel analysis and visualization techniques to get a comprehensive view of a wide range of movements. D. sargus individuals were highly territorial, moving within small home ranges (< 1 km2), inside which they displayed repetitive diel activity patterns. Extraordinary movements beyond the ordinary home range were observed under two specific conditions. First, during stormy events D. sargus presented a sheltering behaviour, moving to more protected places to avoid the disturbance. Second, during the spawning season they made excursions to deep areas (> 50 m), where they aggregated to spawn. This study advances our understanding about the functioning of an established MPA and provides important insights into the biology and management of a small sedentary species, suggesting the relevance of rare but important fish behaviours.

Large-scale assessment of Mediterranean marine protected areas effects on fish assemblages.

Marine protected areas (MPAs) were acknowledged globally as effective tools to mitigate the threats to oceans caused by fishing. Several studies assessed the effectiveness of individual MPAs in protecting fish assemblages, but regional assessments of multiple MPAs are scarce. Moreover, empirical evidence on the role of MPAs in contrasting the propagation of non-indigenous-species (NIS) and thermophilic species (ThS) is missing. We simultaneously investigated here the role of MPAs in reversing the effects of overfishing and in limiting the spread of NIS and ThS. The Mediterranean Sea was selected as study area as it is a region where 1) MPAs are numerous, 2) fishing has affected species and ecosystems, and 3) the arrival of NIS and the northward expansion of ThS took place. Fish surveys were done in well-enforced no-take MPAs (HP), partially-protected MPAs (IP) and fished areas (F) at 30 locations across the Mediterranean. Significantly higher fish biomass was found in HP compared to IP MPAs and F. Along a recovery trajectory from F to HP MPAs, IP were similar to F, showing that just well enforced MPAs triggers an effective recovery. Within HP MPAs, trophic structure of fish assemblages resembled a top-heavy biomass pyramid. Although the functional structure of fish assemblages was consistent among HP MPAs, species driving the recovery in HP MPAs differed among locations: this suggests that the recovery trajectories in HP MPAs are likely to be functionally similar (i.e., represented by predictable changes in trophic groups, especially fish predators), but the specific composition of the resulting assemblages may depend on local conditions. Our study did not show any effect of MPAs on NIS and ThS. These results may help provide more robust expectations, at proper regional scale, about the effects of new MPAs that may be established in the Mediterranean Sea and other ecoregions worldwide.

Long-term recovery patterns and limited spillover of large predatory fish in a Mediterranean MPA.

Based on 19 y of visual census data from the Medes Islands MPA (NW Mediterranean), this study analyzes the carrying capacity (K) and population recovery time of six species of fish strongly affected by harvesting pressure along the Mediterranean coast. Three of these species (Epinephelus marginatus, Diplodus cervinus and Dicentrachus labrax) have practically reached carrying capacity in the Medes Islands MPA, while others are still approaching population stabilization (Sciaena umbra) or are still increasing in biomass (Dentex dentex). The one exception to these trends is S. aurata, which tended to decrease inside the MPA, probably due to fishing just outside its borders. These results confirm that fish populations may require decadal time scales to recover from exploitation, both in terms of total abundance (21 to 29 y to exceed 95% K) as well as total biomass (25 to 35 y), and that rates of recovery differ between species (13 to 31 y). The recovery and saturation observed within the no-take zone contrasts with results obtained in the partially protected buffer area and the peripheral area open for fishing, which show much lower biomass values. In general, the spillover from the MPA is very moderate, and its effects extend only to the partially protected area.

The Mediterranean benthic herbivores show diverse responses to extreme storm disturbances.

Catastrophic storms have been observed to be one of the major elements in shaping the standing structure of marine benthic ecosystems. Yet, little is known about the effect of catastrophic storms on ecosystem processes. Specifically, herbivory is the main control mechanism of macrophyte communities in the Mediterranean, with two main key herbivores: the sea urchin Paracentrotus lividus and the fish Sarpa salpa. Consequently, the effects of extreme storm events on these two herbivores (at the population level and on their behaviour) may be critical for the functioning of the ecosystem. With the aim of filling this gap, we took advantage of two parallel studies that were conducted before, during and after an unexpected catastrophic storm event. Specifically, fish and sea urchin abundance were assessed before and after the storm in monitored fixed areas (one site for sea urchin assessment and 3 sites for fish visual transects). Additionally, we investigated the behavioural response to the disturbance of S. salpa fishes that had been tagged with acoustic transmitters. Given their low mobility, sea urchins were severely affected by the storm (ca. 50% losses) with higher losses in those patches with a higher density of sea urchins. This may be due to a limited availability of refuges within each patch. In contrast, fish abundance was not affected, as fish were able to move to protected areas (i.e. deeper) as a result of the high mobility of this species. Our results highlight that catastrophic storms differentially affect the two dominant macroherbivores of rocky macroalgal and seagrass systems due to differences in mobility and escaping strategies. This study emphasises that under catastrophic disturbances, the presence of different responses among the key herbivores of the system may be critical for the maintenance of the herbivory function.

Multiple processes regulate long-term population dynamics of sea urchins on Mediterranean rocky reefs.

We annually monitored the abundance and size structure of herbivorous sea urchin populations (Paracentrotus lividus and Arbacia lixula) inside and outside a marine reserve in the Northwestern Mediterranean on two distinct habitats (boulders and vertical walls) over a period of 20 years, with the aim of analyzing changes at different temporal scales in relation to biotic and abiotic drivers. P. lividus exhibited significant variability in density over time on boulder bottoms but not on vertical walls, and temporal trends were not significantly different between the protection levels. Differences in densities were caused primarily by variance in recruitment, which was less pronounced inside the MPA and was correlated with adult density, indicating density-dependent recruitment under high predation pressure, as well as some positive feedback mechanisms that may facilitate higher urchin abundances despite higher predator abundance. Populations within the reserve were less variable in abundance and did not exhibit the hyper-abundances observed outside the reserve, suggesting that predation effects maybe more subtle than simply lowering the numbers of urchins in reserves. A. lixula densities were an order of magnitude lower than P. lividus densities and varied within sites and over time on boulder bottoms but did not differ between protection levels. In December 2008, an exceptionally violent storm reduced sea urchin densities drastically (by 50% to 80%) on boulder substrates, resulting in the lowest values observed over the entire study period, which remained at that level for at least two years (up to the present). Our results also showed great variability in the biological and physical processes acting at different temporal scales. This study highlights the need for appropriate temporal scales for studies to fully understand ecosystem functioning, the concepts of which are fundamental to successful conservation and management.

The structure of Mediterranean rocky reef ecosystems across environmental and human gradients, and conservation implications.

Historical exploitation of the Mediterranean Sea and the absence of rigorous baselines makes it difficult to evaluate the current health of the marine ecosystems and the efficacy of conservation actions at the ecosystem level. Here we establish the first current baseline and gradient of ecosystem structure of nearshore rocky reefs at the Mediterranean scale. We conducted underwater surveys in 14 marine protected areas and 18 open access sites across the Mediterranean, and across a 31-fold range of fish biomass (from 3.8 to 118 g m(-2)). Our data showed remarkable variation in the structure of rocky reef ecosystems. Multivariate analysis showed three alternative community states: (1) large fish biomass and reefs dominated by non-canopy algae, (2) lower fish biomass but abundant native algal canopies and suspension feeders, and (3) low fish biomass and extensive barrens, with areas covered by turf algae. Our results suggest that the healthiest shallow rocky reef ecosystems in the Mediterranean have both large fish and algal biomass. Protection level and primary production were the only variables significantly correlated to community biomass structure. Fish biomass was significantly larger in well-enforced no-take marine reserves, but there were no significant differences between multi-use marine protected areas (which allow some fishing) and open access areas at the regional scale. The gradients reported here represent a trajectory of degradation that can be used to assess the health of any similar habitat in the Mediterranean, and to evaluate the efficacy of marine protected areas.

Impacts on the deep-sea ecosystem by a severe coastal storm.

Major coastal storms, associated with strong winds, high waves and intensified currents, and occasionally with heavy rains and flash floods, are mostly known because of the serious damage they can cause along the shoreline and the threats they pose to navigation. However, there is a profound lack of knowledge on the deep-sea impacts of severe coastal storms. Concurrent measurements of key parameters along the coast and in the deep-sea are extremely rare. Here we present a unique data set showing how one of the most extreme coastal storms of the last decades lashing the Western Mediterranean Sea rapidly impacted the deep-sea ecosystem. The storm peaked the 26(th) of December 2008 leading to the remobilization of a shallow-water reservoir of marine organic carbon associated with fine particles and resulting in its redistribution across the deep basin. The storm also initiated the movement of large amounts of coarse shelf sediment, which abraded and buried benthic communities. Our findings demonstrate, first, that severe coastal storms are highly efficient in transporting organic carbon from shallow water to deep water, thus contributing to its sequestration and, second, that natural, intermittent atmospheric drivers sensitive to global climate change have the potential to tremendously impact the largest and least known ecosystem on Earth, the deep-sea ecosystem.

Assessing the effectiveness of marine reserves on unsustainably harvested long-lived sessile invertebrates.

Although the rapid recovery of fishes after establishment of a marine reserve is well known, much less is known about the response of long-lived, sessile, benthic organisms to establishment of such reserves. Since antiquity, Mediterranean red coral (Corallium rubrum) has been harvested intensively for use in jewelry, and its distribution is currently smaller than its historical size throughout the Mediterranean Sea. To assess whether establishment of marine reserves is associated with a change in the size and number of red coral colonies that historically were not harvested sustainably, we analyzed temporal changes in mean colony diameter and density from 1992 to 2005 within red coral populations at different study sites in the Medes Islands Marine Reserve (established in 1992) and in adjacent unprotected areas. Moreover, we compared colony size in the Medes Islands Marine Reserve, where recreational diving is allowed and poaching has been observed after reserve establishment, with colony size in three other marine protected areas (Banyuls, Carry-le-Rouet, and Scandola) with the enforced prohibition of fishing and diving. At the end of the study, the size of red coral colonies at all sampling sites in the Medes Islands was significantly smaller than predicted by growth models and smaller than those in marine protected areas without fishing and diving. The annual number of recreational dives and the percent change in the basal diameter of red coral colonies were negatively correlated, which suggests that abrasion by divers may increase the mortality rates of the largest red coral colonies within this reserve . Our study is the first quantitative assessment of a poaching event, which was detected during our monitoring in 2002, inside the marine reserve. Poaching was associated with a loss of approximately 60% of the biomass of red coral colonies.

Multiple controls of community structure and dynamics in a sublittoral marine environment.

The structure and dynamics of ecological communities can be determined by both top-down (e.g., predation) and bottom-up (e.g., energy inputs) processes, which can act synergistically and across spatial and temporal scales. Here we aimed at understanding the role of multiple controls in a Mediterranean rocky sublittoral marine community that harbors a diverse algal community and strongly interacting herbivores, and which is subject to marked seasonality in energy inputs. We conducted an experiment by manipulating densities of the major consumers of benthic algae (fishes and sea urchins) in approximately 100-m2 enclosures in a marine reserve, and monitored algal assemblages over two and a half years. Most algae showed a marked annual cycle, with a biomass peak in late spring/summer and low biomass in winter, following seasonal fluctuations in resource availability, indicating the existence of bottom-up processes. Sea urchins reduced the abundance of most algal species, indicating the existence of top-down processes. The effect of fish grazing on algal abundances was significantly weaker. Sea urchin grazing was inhibited when predatory fish were present. Multivariate analysis showed that the interaction between seasonal resource inputs and herbivory induced the formation of algal assemblages characterized by different species abundances. The organization of algal assemblages was determined by the synergistic interaction between top-down and bottom-up processes: top-down control regulated total algal abundance, while bottom-up control determined seasonal fluctuations.