Improving predictions of invasive fish ranges combining functional and ecological traits with environmental suitability under climate change scenarios.

Biological invasions represent one of the main threats to marine biodiversity. From a conservation perspective, especially in the context of increasing sea warming, it is critical to examine the suitability potential of geographical areas for the arrival of Range-Expanding Introduced and Native Species (REINS), and hence anticipate the risk of such species to become invasive in their new distribution areas. Here, we developed an empirical index, based on functional and bio-ecological traits, that estimates the Invasive Potential (IP; i.e. the potential success in transport, introduction and population establishment) for a set of 13 fishes that are expanding their distributional range into the Mediterranean Sea, the most invaded sea in the world. The IP index showed significant correlation with the observed spreading of REINS. For the six species characterized by the highest IP, we calculated contemporary and future projections of their Environmental Suitability Index (ESI). By using an ensemble modelling approach, we estimated the geographical areas that are likely to be the most impacted by REINS spreading under climate change. Our results demonstrated the importance of functional traits related to reproduction for determining high invasion potential. For most species, we found high contemporary ESI values in the South-eastern Mediterranean Sea and low to intermediate contemporary ESI values in the Adriatic Sea and North-western Mediterranean sector. Moreover, we highlighted a major potential future expansion of high ESI values, and thus REINS IP, towards the northern Mediterranean, especially in the northern Adriatic Sea. This potential future northward expansion highlights the risk associated with climate-induced impacts on ecosystem conservation and fish stock management throughout the entire Mediterranean Sea.

Exploring the relationships between marine protected areas and invasive fish in the world's most invaded sea.

Marine Protected Areas (MPAs) are an essential tool for marine biodiversity conservation. Yet, their effectiveness in protecting marine ecosystems from global stressors is debated. Biological invasions are a major driver of global change, causing biodiversity loss and altering ecosystem functioning. Here, we explored the relationships between MPAs and alien/native range-expanding fishes in the Mediterranean Sea, the world's most invaded sea. We surveyed fish and benthic communities in nine MPAs and adjacent unprotected areas across six countries. In the South and Eastern Mediterranean MPAs, the biomass of alien and native range-expanding fishes often exceeded 50% of the total fish biomass. Conversely, in the North and Western Mediterranean, alien fishes were absent. A negative relationship was found between native and alien species richness. Average and minimum sea surface temperature (SST) over six consecutive years were positively correlated with the total biomass of alien species; no alien fishes were recorded below 20.5°C average SST and 13.8°C minimum SST. We also found a negative relationship between alien fishes' biomass and the distance from the Suez Canal, which is the main pathway for the introduction of alien fish in the Mediterranean Sea. The biomass of alien and native range-expanding fishes was found to be higher in the South and Eastern Mediterranean MPAs than in adjacent unprotected areas. The association of barrens (rocky reefs deprived of vegetation) and invasive herbivores was observed at all eastern sites, regardless of protection status. Currently, the level of fishing pressure exerted on alien and native range-expanding fishes seems to be the most influential factor determining the lower biomass of invasive fishes at unprotected sites compared to MPAs. Our findings suggest that complementary management actions, such as species-targeted removals, should be taken in MPAs to effectively control invasive fish populations.

Adaptive Vertical Positioning as Anti-Predator Behavior: The Case of a Prey Fish Cohabiting with Multiple Predatory Fish within Temperate Marine Algal Forests.

Prey fish cohabit with specialized predator fish within structurally complex habitats. How the vertical stratification of the habitat affects lethal and behavioral predator-prey interactions and contributes to explaining these patterns has never been investigated within a forest-like marine habitat, i.e., a habitat containing three vertical strata (understory, canopy, open-water above). We studied this in tank experiments, with a model prey (the wrasse Symphodus ocellatus) and two model predators (the stalk-and-attack comber Serranus cabrilla and the sit-and-wait scorpionfish Scorpaena porcus), which are among the most abundant prey and predators cohabiting in Mediterranean Cystoseira forests. Wrasse anti-predator behavior was predator-specific. When exposed to the scorpionfish, the wrasse increased its vertical distance from the predator, regardless of the habitat structure. Conversely, when exposed to the comber, the wrasse sought refuge within forest structures: (1) the canopy provides more hiding opportunities due to its high complexity, and (2) the understory provides more escape/avoidance opportunities due to (a) its low complexity that allows for fast prey movements, and (b) the presence of the canopy above that limits the comber's access to the understory. Our results suggest that habitat vertical stratification mediates predator-prey interactions and potentially promotes the co-existence of prey and multiple predators within marine forests.

European cephalopods distribution under climate-change scenarios.

In a context of increasing anthropogenic pressure, projecting species potential distributional shifts is of major importance for the sustainable exploitation of marine species. Despite their major economical (i.e. important fisheries) and ecological (i.e. central position in food-webs) importance, cephalopods literature rarely addresses an explicit understanding of their current distribution and the potential effect that climate change may induce in the following decades. In this study, we focus on three largely harvested and common cephalopod species in Europe: Octopus vulgaris, Sepia officinalis and Loligo vulgaris. Using a recently improved species ensemble modelling framework coupled with five atmosphere-ocean general circulation models, we modelled their contemporary and potential future distributional range over the twenty-first century. Independently of global warming scenarios, we observed a decreasing in the suitability of environmental conditions in the Mediterranean Sea and the Bay of Biscay. Conversely, we projected a rapidly increasing environmental suitability in the North, Norwegian and Baltic Seas for all species. This study is a first broad scale assessment and identification of the geographical areas, fisheries and ecosystems impacted by climate-induced changes in cephalopods distributional range.

Patterns of predation on native and invasive alien fish in Mediterranean protected and unprotected areas.

Worldwide, the loss of predatory fish due to overexploitation has altered the structure of native communities and caused ecosystem shifts. Ecosystems deprived of high-level predators may be more vulnerable to invasive alien species as the latter are subject to reduced predation control. Marine protected areas (MPAs), and particularly no-take reserves where fishing is banned, can be effective tools for the restoration of predatory relationships within their boundaries. We explored whether the restoration of high-level predatory fish populations within Mediterranean MPAs can exert top-down control on alien fish. Fish tethering experiments, including native (Sardina pilchardus, Boops boops) and alien (Siganus rivulatus) dead specimens, were conducted to quantify predation within the no-take zones of three MPAs and in unprotected areas, and to assess potential differences in predation rates and prey type preferences. A subsample of experimental units was filmed to document predation events and related fish behaviour. More high-level predators interacted with the tethered fish inside the MPAs than in unprotected areas. Yet we did not find significant differences in the consumption of alien or native fishes between MPAs and unprotected areas. The native S. pilchardus was consumed more in comparison to the other tethered fishes, regardless of protection status and location. Interestingly, the alien S. rivulatus was consumed by native predators in the western Mediterranean locations where this alien fish is not established. Despite its limitations, our study provides evidence on the ability of some native predators to feed on and potentially control certain alien species without requiring 'adaptive' time-lag periods.

Management priorities for marine invasive species.

Managing invasive alien species is particularly challenging in the ocean mainly because marine ecosystems are highly connected across broad spatial scales. Eradication of marine invasive species has only been achieved when species were detected early, and management responded rapidly. Generalized approaches, transferable across marine regions, for prioritizing actions to control invasive populations are currently lacking. Here, expert knowledge was elicited to prioritize 11 management actions for controlling 12 model species, distinguished by differences in dispersion capacity, distribution in the area to be managed, and taxonomic identity. Each action was assessed using five criteria (effectiveness, feasibility, acceptability, impacts on native communities, and cost), which were combined in an 'applicability' metric. Raising public awareness and encouraging the commercial use of invasive species were highly prioritized, whereas biological control actions were considered the least applicable. Our findings can guide rapid decision-making on prioritizing management options for the control of invasive species especially at early stages of invasion, when reducing managers' response time is critical.

Capping of marine sediments with valuable industrial by-products: Evaluation of inorganic pollutants immobilization.

In-situ capping of polluted sediment is considered as an inexpensive and effective treatment technology to immobilize contaminants in a short time. In this remediation technique sediments are capped by placing a layer of sand, clean sediment or other materials over sediments in order to mitigate risk. In this study, low cost industrial by products (bauxaline, steel slag, and mixture of the two products) were applied as capping agents. A bench scale laboratory experiment in aquariums was performed to evaluate their effects on Cd, Zn, As, and Cr mobility from an artificially contaminated marine sediment. Without capping, all the contaminants are constantly released with various kinetic depending of mineral oxidation or dissolution or leaching. Nevertheless, release did not exceed 31% of the initial amount of pollutant. Capping sediment with steel slag, bauxaline and their mixture totally captured Cd, Zn, and As. In the case of Cr, only steel slag actively blocked its release. A kinetic model was developed to model As and Cr release, with and without capping. The release times for Cr and As from the sediment were close to 6 days. In the presence of capping agents, the capture time for Cr was found to be 57 days for steel slag, and 7 days for bauxaline. Despite a high capture time, steel slag was the best capping agent since bauxaline matrix was a source of Cr and rapidly released it (release time = 1 day). The results indicated that steel slag and its mixture additive can be used as potential capping materials for the remediation of contaminated sites due to their significant entrapping of Cd, Zn, As, and Cr.

Seasonal assessment of biological indices, bioaccumulation, and bioavailability of heavy metals in sea urchins Paracentrotus lividus from Algerian west coast, applied to environmental monitoring.

The aim of the present work was to extend our knowledge on the variability of trace metals in sea urchin tissues, focusing on seasonal fluctuations (2010 February for "winter," May for "spring," August for "summer," November for "autumn") in the three different sampling sites of Algerian west coast (Oran Harbor (S1), Ain Defla (S2), and Hadjaj (belonging to Mostaganem City S3)). For this purpose, the bioavailability (metal indices) and bioaccumulation (metal concentrations in soft tissues) of heavy metals (Zn, Cu, Pb, and Cd), the physiological characteristics (e.g., biological indices such as condition index (CI), repletion index (RI), gonad index (GI)), and the biometric parameters (diameter (D) and the height (H)) of sea urchins Paracentrotus lividus were assessed and related to seasons and sites. To investigate the metal bioavailability to sea urchins more precisely, the metal indices were used as a reliable tool in the present work, instead of the metal concentrations only. The interest to standardize metal concentrations with the weight of the urchin test is to overcome the metal burden variations in the soft tissues of urchin related to the seasonal weight changes of the soft body of animal. We evidence that the most contaminated sites were S1 and S2. Furthermore, it should be noted that the bioavailability of metals, corresponding to the values of metal indices, is also more pronounced in S1 and S2 compared to that measured in S3. Thus, a correlation is observed between seasonal metal content in urchin tissues from the three sites and the corresponding metal indices. The high metal concentrations were obtained during the period when RI and CI were highest. So, it appears that the bioaccumulation of metals in sea urchins of the three sites studied is significantly influenced by the reproductive cycle and diet, feeding activity, and physiological state of these organisms. We noticed that the sea urchins from the sites S1 and S2 were small in size. It is probable that these animals, whose internal tissues contained high concentrations of metals, have been exposed to metal pollution, which might have affected both their growth and altered their physiological capacity. This approach is very original and might be used in the monitoring of the quality of coastal waters, and the present work provided a useful data set for Mediterranean monitoring network.

Enhancing fish Underwater Visual Census to move forward assessment of fish assemblages: An application in three Mediterranean Marine Protected Areas.

Monitoring fish assemblages is needed to assess whether Marine Protected Areas (MPAs) are meeting their conservation and fisheries management goals, as it allows one to track the progress of recovery of exploited species and associated communities. Underwater Visual Census techniques (UVC) are used to monitor fish assemblages in MPAs. UVCs should be adapted to fish abundance, body-size and behaviour, which can strongly affect fish detectability. In Mediterranean subtidal habitats, however, UVC strip transects of one surface area (25x5 m2) are commonly used to survey the whole fish assemblage, from large shy fish to small crypto-benthic fish. Most high trophic level predators (HTLPs) are large shy fish which rarely swim close to divers and, consequently, their abundance may be under-estimated with commonly used transects. Here, we propose an improvement to traditional transect surveys to better account for differences in behaviour among and within species. First, we compared the effectiveness of combining two transect surface areas (large: 35x20 m2; medium: 25x5 m2) in quantifying large, shy fish within and outside Mediterranean MPAs. We identified species-specific body-size thresholds defining a smaller and a larger size class better sampled by medium and large transects respectively. Combining large and medium transects provided more accurate biomass and species richness estimates for large, shy species than using medium transects alone. We thus combined the new approach with two other transect surface areas commonly used to survey crypto-benthic (10x1 m2) and necto-benthic (25x5 m2) species in order to assess how effectively MPAs protection the whole fish assemblage. We verified that MPAs offer significant protection for HTLPs, their response in terms of biomass and density increase in MPAs was always higher in magnitude than other functional groups. Inside MPAs, the contribution of HTLP reached >25% of total fish biomass, against < 2% outside MPAs. Surveys with multiple transect surface areas allow for a more realistic assessment of the structure of the whole fish assemblage and better assessment of potential recovery of HTLPs within reserves of HTLP.

Sediment-bound trace metals in Golfe-Juan Bay, northwestern Mediterranean: Distribution, availability and toxicity.

The concentration, potential mobility, cation exchange capacity and toxicity of eight sediment-bound metals in Golfe-Juan Bay, France were examined. Results revealed significant spatial gradient of metal contamination along Golfe-Juan coast. The distribution and concentration of the metals appear to be influenced by the geochemical properties of the sediment, proximity to anthropogenic sources and general water circulation in the bay. The portion of trace metals found in the exchangeable, carbonate, oxidizable and reducible fractions of the sediment constitute 31%-58% of the total sediment-bound trace metal content, suggesting significant potential for remobilization of metals into the water column. Pb and Ni content of the sediment exceed the limits of the French marine sediment quality. Whole sediment extracts showed acute toxicity to marine rotifers. This study concludes that monitoring and management of sediment-bound trace metals in Golfe-Juan Bay are important so as not to underestimate their availability and risk to the marine ecosystems.

Juvenile fish assemblages in temperate rocky reefs are shaped by the presence of macro-algae canopy and its three-dimensional structure.

Arborescent macro-algae forests covering temperate rocky reefs are a known habitat for juvenile fishes. However, in the Mediterranean, these forests are undergoing severe transformations due to pressures from global change. In our study, juvenile fish assemblages differed between pristine arborescent forests (Cystoseira brachycarpa var. balearica) versus an alternate state: bushland (Dictyotales - Sphacelariales). Forests hosted richer and three-fold more abundant juvenile assemblages. This was consistent through space, whatever the local environmental conditions, along 40 km of NW Mediterranean subtidal rocky shores (Corsica, France). Among Cystoseira forests, juvenile assemblages varied through space (i.e. between localities, zones or sites) in terms of total abundance, composition, richness and taxa-specific patterns. More than half of this variability was explained by forest descriptors, namely small variations in canopy structure and/or depth. Our results provide essential cues for understanding and managing coastal habitats and fish populations. Further studies are needed to explain the residual part of the spatial variability of juvenile fish assemblages and to help focus conservation efforts.

Abundance and Diversity of Crypto- and Necto-Benthic Coastal Fish Are Higher in Marine Forests than in Structurally Less Complex Macroalgal Assemblages.

In Mediterranean subtidal rocky reefs, Cystoseira spp. (Phaeophyceae) form dense canopies up to 1 m high. Such habitats, called 'Cystoseira forests', are regressing across the entire Mediterranean Sea due to multiple anthropogenic stressors, as are other large brown algae forests worldwide. Cystoseira forests are being replaced by structurally less complex habitats, but little information is available regarding the potential difference in the structure and composition of fish assemblages between these habitats. To fill this void, we compared necto-benthic (NB) and crypto-benthic (CB) fish assemblage structures between Cystoseira forests and two habitats usually replacing the forests (turf and barren), in two sampling regions (Corsica and Menorca). We sampled NB fish using Underwater Visual Census (UVC) and CB fish using Enclosed Anaesthetic Station Vacuuming (EASV), since UVC is known to underestimate the diversity and density of the 'hard to spot' CB fish. We found that both taxonomic diversity and total density of NB and CB fish were highest in Cystoseira forests and lowest in barrens, while turfs, that could be sampled only at Menorca, showed intermediate values. Conversely, total biomass of NB and CB fish did not differ between habitats because the larger average size of fish in barrens (and turfs) compensated for their lower densities. The NB families Labridae and Serranidae, and the CB families Blenniidae, Cliniidae, Gobiidae, Trypterigiidae and Scorpaenidae, were more abundant in forests. The NB taxa Diplodus spp. and Thalassoma pavo were more abundant in barrens. Our study highlights the importance of using EASV for sampling CB fish, and shows that Cystoseira forests support rich and diversified fish assemblages. This evidence suggests that the ongoing loss of Cystoseira forests may impair coastal fish assemblages and related goods and services to humans, and stresses the need to implement strategies for the successful conservation and/or recovery of marine forests.

Five key attributes can increase marine protected areas performance for small-scale fisheries management.

Marine protected areas (MPAs) have largely proven to be effective tools for conserving marine ecosystem, while socio-economic benefits generated by MPAs to fisheries are still under debate. Many MPAs embed a no-take zone, aiming to preserve natural populations and ecosystems, within a buffer zone where potentially sustainable activities are allowed. Small-scale fisheries (SSF) within buffer zones can be highly beneficial by promoting local socio-economies. However, guidelines to successfully manage SSFs within MPAs, ensuring both conservation and fisheries goals, and reaching a win-win scenario, are largely unavailable. From the peer-reviewed literature, grey-literature and interviews, we assembled a unique database of ecological, social and economic attributes of SSF in 25 Mediterranean MPAs. Using random forest with Boruta algorithm we identified a set of attributes determining successful SSFs management within MPAs. We show that fish stocks are healthier, fishermen incomes are higher and the social acceptance of management practices is fostered if five attributes are present (i.e. high MPA enforcement, presence of a management plan, fishermen engagement in MPA management, fishermen representative in the MPA board, and promotion of sustainable fishing). These findings are pivotal to Mediterranean coastal communities so they can achieve conservation goals while allowing for profitable exploitation of fisheries resources.

Fish assemblages of Mediterranean marine caves.

Fish assemblages associated with 14 marine caves and adjacent external rocky reefs were investigated at four Marine Protected Areas (MPAs) along the coasts of Italy. Within the caves sampling was carried out in different sub-habitats: walls, ceilings, bottoms and ends of caves. On the whole, 38 species were recorded inside the 14 caves investigated. Eighteen species were exclusively found inside the caves: they were mainly represented by speleophilic (i.e. species preferentially or exclusively inhabiting caves) gobids (e.g. Didogobius splechtnai) and nocturnal species (e.g. Conger conger). Forty-one species were censused outside, 20 of which were shared with cave habitats. Apogon imberbis was the most common fish found in all 14 caves investigated, followed by Thorogobius ephippiatus (recorded in 13 caves), and Diplodus vulgaris and Scorpaena notata (both censused in 12 caves). Distinct fish assemblages were found between external rocky reefs and the different cave sub-habitats. New data on the distribution of some speleophilic gobids were collected, showing the existence of a pool of species shared by marine caves on a large scale (i.e. hundreds of km). Considering the uniqueness of cave fishes (18 exclusive species and different assemblage structures), the inclusion of marine caves among the habitats routinely investigated for fish biodiversity monitoring could facilitate the achievement of more comprehensive inventories. Due to their contribution to local species diversity and the shelter they provide to species valuable for conservation, marine caves should be prioritized for their inclusion not only within future MPAs through the Mediterranean Sea, but also into larger management spatial planning.

Effects of ocean acidification and diet on thickness and carbonate elemental composition of the test of juvenile sea urchins.

Continuous anthropogenic CO2 emissions to the atmosphere and uptake by the oceans will cause a reduction of seawater pH and saturation state (Ω) of CaCO3 minerals from which marine calcifiers build their shells and skeletons. Sea urchins use the most soluble form of calcium carbonate, high-magnesium calcite, to build their skeleton, spines and grazing apparatus. In order to highlight the effects of increased pCO2 on the test thickness and carbonate elemental composition of juvenile sea urchins and potential differences in their responses linked to the diet, we performed a laboratory experiment on juvenile Paracentrotus lividus, grazing on calcifying (Corallina elongata) and non-calcifying (Cystoseira amentacea, Dictyota dichotoma) macroalgae, under different pH (corresponding to pCO2 values of 390, 550, 750 and 1000 µatm). Results highlighted the importance of the diet in determining sea urchin size irrespectively of the pCO2 level, and the relevance of macroalgal diet in modulating urchin Mg/Ca ratio. The present study provides relevant clues both in terms of the mechanism of mineral incorporation and in terms of bottom-up processes (algal diet) affecting top-down ones (fish predation) in rocky subtidal communities.

Cascading effects of ocean acidification in a rocky subtidal community.

Temperate marine rocky habitats may be alternatively characterized by well vegetated macroalgal assemblages or barren grounds, as a consequence of direct and indirect human impacts (e.g. overfishing) and grazing pressure by herbivorous organisms. In future scenarios of ocean acidification, calcifying organisms are expected to be less competitive: among these two key elements of the rocky subtidal food web, coralline algae and sea urchins. In order to highlight how the effects of increased pCO2 on individual calcifying species will be exacerbated by interactions with other trophic levels, we performed an experiment simultaneously testing ocean acidification effects on primary producers (calcifying and non-calcifying algae) and their grazers (sea urchins). Artificial communities, composed by juveniles of the sea urchin Paracentrotus lividus and calcifying (Corallina elongata) and non-calcifying (Cystoseira amentacea var stricta, Dictyota dichotoma) macroalgae, were subjected to pCO2 levels of 390, 550, 750 and 1000 µatm in the laboratory. Our study highlighted a direct pCO2 effect on coralline algae and on sea urchin defense from predation (test robustness). There was no direct effect on the non-calcifying macroalgae. More interestingly, we highlighted diet-mediated effects on test robustness and on the Aristotle's lantern size. In a future scenario of ocean acidification a decrease of sea urchins' density is expected, due to lower defense from predation, as a direct consequence of pH decrease, and to a reduced availability of calcifying macroalgae, important component of urchins' diet. The effects of ocean acidification may therefore be contrasting on well vegetated macroalgal assemblages and barren grounds: in the absence of other human impacts, a decrease of biodiversity can be predicted in vegetated macroalgal assemblages, whereas a lower density of sea urchin could help the recovery of shallow subtidal rocky areas affected by overfishing from barren grounds to assemblages dominated by fleshy macroalgae.

An ecotoxicological approach with transplanted mussels (Mytilus galloprovincialis) for assessing the impact of tyre reefs immersed along the NW Mediterranean Sea.

Tyre artificial reefs were deposited in a marine protected area (Vallauris-Golfe Juan Bay, France) located along the NW Mediterranean coast, during the early 80's. The potential toxic effects of the tyre artificial reefs were investigated using transplantation of marine mussels, Mytilus galloprovincialis, to stations located above tyre blocks (St1, St2) or reference site (StR). Mussels transplanted to different stations presented the following sequence of mortality: St1 > St2 > StR. Principal Component Analysis, taking into account metal accumulation (cadmium, copper and zinc) and biomarker (SOD, CAT, GST and AChE activities, TBARS and MT levels, Condition Index) responses in mussel tissues indicated a clear separation between the three stations. St1 organisms were significantly more affected by tyre reefs than those from other stations. Such an integrated monitoring study represents a key approach to assess in situ the biological impact of >25 year-old tyre artificial reefs.