Grouping groupers in the Mediterranean: Ecological baselines revealed by ancient proteins.

Marine historical ecology provides a means to establish baselines to inform current fisheries management. Groupers (Epinephelidae) are key species for fisheries in the Mediterranean, which have been heavily overfished. Species abundance and distribution prior to the 20th century in the Mediterranean remains poorly known. To reconstruct the past biogeography of Mediterranean groupers, we investigated whether Zooarchaeology by Mass Spectrometry (ZooMS) can be used for identifying intra-genus grouper bones to species level. We discovered 22 novel, species-specific ZooMS biomarkers for groupers. Applying these biomarkers to Kinet Höyük, a Mediterranean archaeological site, demonstrated 4000 years of regional Epinephelus aeneus dominance and resiliency through millennia of fishing pressures, habitat degradation and climatic changes. Combining ZooMS identifications with catch size reconstructions revealed the Epinephelus aeneus capacity for growing 30 cm larger than hitherto documented, revising the maximum Total Length from 120 to 150 cm. Our results provide ecological baselines for a key Mediterranean fishery which could be leveraged to define and assess conservation targets.

Redistribution of fisheries catch potential in Mediterranean and North European waters under climate change scenarios.

The Mediterranean Sea is a hotspot of global warming where key commercial species, such as demersal and pelagic fishes, and cephalopods, could experience abrupt distribution shifts in the near future. However, the extent to which these range shifts may impact fisheries catch potential remains poorly understood at the scale of Exclusive Economic Zones (EEZs). Here, we evaluated the projected changes in Mediterranean fisheries catches potential, by target fishing gears, under different climate scenarios throughout the 21st century. We show that the future Mediterranean maximum catch potential may decrease considerably by the end of the century under high emission scenarios in South Eastern Mediterranean countries. These projected decreases range between -20 to -75 % for catch by pelagic trawl and seine, -50 to -75 % for fixed nets and traps and exceed -75 % for benthic trawl. In contrast, fixed nets and traps, and benthic trawl fisheries may experience an increase in their catch potential in the North and Celtic seas, while future catches by pelagic trawl and seine may decrease in the same areas. We show that a high emission scenario may considerably amplify the future redistribution of fisheries catch potential across European Seas, thus highlighting the need to limit global warming. Our projections at the manageable scale of EEZ and the quantification of climate-induced impacts on a large part of the Mediterranean and European fisheries is therefore a first, and considerable step toward the development of climate mitigation and adaptations strategies for the fisheries sector.

Small-scale fisheries catch more threatened elasmobranchs inside partially protected areas than in unprotected areas.

Elasmobranchs are heavily impacted by fishing. Catch statistics are grossly underestimated due to missing data from various fishery sectors such as small-scale fisheries. Marine Protected Areas are proposed as a tool to protect elasmobranchs and counter their ongoing depletion. We assess elasmobranchs caught in 1,256 fishing operations with fixed nets carried out in partially protected areas within Marine Protected Areas and unprotected areas beyond Marine Protected Areas borders at 11 locations in 6 Mediterranean countries. Twenty-four elasmobranch species were recorded, more than one-third belonging to the IUCN threatened categories (Vulnerable, Endangered, or Critically Endangered). Catches per unit of effort of threatened and data deficient species were higher (with more immature individuals being caught) in partially protected areas than in unprotected areas. Our study suggests that despite partially protected areas having the potential to deliver ecological benefits for threatened elasmobranchs, poor small-scale fisheries management inside Marine Protected Areas could hinder them from achieving this important conservation objective.

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.

An integrated assessment of the Good Environmental Status of Mediterranean Marine Protected Areas.

Local, regional and global targets have been set to halt marine biodiversity loss. Europe has set its own policy targets to achieve Good Environmental Status (GES) of marine ecosystems by implementing the Marine Strategy Framework Directive (MSFD) across member states. We combined an extensive dataset across five Mediterranean ecoregions including 26 Marine Protected Areas (MPAs), their reference unprotected areas, and a no-trawl case study. Our aim was to assess if MPAs reach GES, if their effects are local or can be detected at ecoregion level or up to a Mediterranean scale, and which are the ecosystem components driving GES achievement. This was undertaken by using the analytical tool NEAT (Nested Environmental status Assessment Tool), which allows an integrated assessment of the status of marine systems. We adopted an ecosystem approach by integrating data from several ecosystem components: the seagrass Posidonia oceanica, macroalgae, sea urchins and fish. Thresholds to define the GES were set by dedicated workshops and literature review. In the Western Mediterranean, most MPAs are in good/high status, with P. oceanica and fish driving this result within MPAs. However, GES is achieved only at a local level, and the Mediterranean Sea, as a whole, results in a moderate environmental status. Macroalgal forests are overall in bad condition, confirming their status at risk. The results are significantly affected by the assumption that discrete observations over small spatial scales are representative of the total extension investigated. This calls for large-scale, dedicated assessments to realistically detect environmental status changes under different conditions. Understanding MPAs effectiveness in reaching GES is crucial to assess their role as sentinel observatories of marine systems. MPAs and trawling bans can locally contribute to the attainment of GES and to the fulfillment of the MSFD objectives. Building confidence in setting thresholds between GES and non-GES, investing in long-term monitoring, increasing the spatial extent of sampling areas, rethinking and broadening the scope of complementary tools of protection (e.g., Natura 2000 Sites), are indicated as solutions to ameliorate the status of the basin.

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.

The MPA Guide: A framework to achieve global goals for the ocean.

Marine Protected Areas (MPAs) are conservation tools intended to protect biodiversity, promote healthy and resilient marine ecosystems, and provide societal benefits. Despite codification of MPAs in international agreements, MPA effectiveness is currently undermined by confusion about the many MPA types and consequent wildly differing outcomes. We present a clarifying science-driven framework­The MPA Guide­to aid design and evaluation. The guide categorizes MPAs by stage of establishment and level of protection, specifies the resulting direct and indirect outcomes for biodiversity and human well-being, and describes the key conditions necessary for positive outcomes. Use of this MPA Guide by scientists, managers, policy-makers, and communities can improve effective design, implementation, assessment, and tracking of existing and future MPAs to achieve conservation goals by using scientifically grounded practices.

Mediterranean rocky reefs in the Anthropocene: Present status and future concerns.

Global change is striking harder and faster in the Mediterranean Sea than elsewhere, where high levels of human pressure and proneness to climate change interact in modifying the structure and disrupting regulative mechanisms of marine ecosystems. Rocky reefs are particularly exposed to such environmental changes with ongoing trends of degradation being impressive. Due to the variety of habitat types and associated marine biodiversity, rocky reefs are critical for the functioning of marine ecosystems, and their decline could profoundly affect the provision of essential goods and services which human populations in coastal areas rely upon. Here, we provide an up-to-date overview of the status of rocky reefs, trends in human-driven changes undermining their integrity, and current and upcoming management and conservation strategies, attempting a projection on what could be the future of this essential component of Mediterranean marine ecosystems.

Environmental DNA effectively captures functional diversity of coastal fish communities.

Robust assessments of taxonomic and functional diversity are essential components of research programmes aimed at understanding current biodiversity patterns and forecasting trajectories of ecological changes. Yet, evaluating marine biodiversity along its dimensions is challenging and dependent on the power and accuracy of the available data collection methods. Here we combine three traditional survey methodologies (underwater visual census strip transects [UVCt], baited underwater videos [BUV] and small-scale fishery catches [SSFc]), and one novel molecular technique (environmental DNA metabarcoding [eDNA]-12S rRNA and cytochrome oxidase subunit 1 [COI]) to investigate their efficiency and complementarity in assessing fish diversity. We analysed 1,716 multimethod replicates at a basin scale to measure the taxonomic and functional diversity of Mediterranean fish assemblages. Taxonomic identities were investigated at species, genus and family levels. Functional identities were assessed using combinations of morphological, behavioural and trophic traits. We show that: (a) SSFc provided the higher taxonomic diversity estimates followed by eDNA, and then UVCt and BUV; (b) eDNA was the only method able to gather the whole spectrum of considered functional traits, showing the most functionally diversified and least redundant fish assemblages; and (c) the effectiveness of eDNA in describing functional structure reflected its lack of selectivity towards any considered functional trait. Our findings suggest that the reach of eDNA analysis stretches beyond taxon detection efficiency and provides new insights into the potential of metabarcoding in ecological studies.

Improving marine protected area governance through collaboration and co-production.

Marine protected areas (MPAs) socio-ecological effectiveness depends on a number of management and governance elements, among which stakeholder engagement and community support play key roles. Collaborative conservation initiatives that engage stakeholders in action research and knowledge co-production processes can enhance management and governance of MPAs. To design effective strategies aimed at reconciling biodiversity conservation and management of sustainable human uses, it is key to assess how local communities respond to such initiatives and identify the set of contextual factors, institutional, local and individual, potentially affecting these responses. This paper presents the approach and results of one such initiative, spanning 6 EU countries and 11 MPAs in the Mediterranean Sea, focusing on small-scale fishers as key MPA users. Through a collaborative project, managers and fishers agreed upon specific governance interventions (e.g. increasing stakeholder engagement, engaging fishers in monitoring activities, reducing fishing efforts) to be implemented in each MPA for one year. Structured surveys queried: MPA managers on the MPA context, governance structure, feasibility and effectiveness of the tested interventions; and small-scale fishers on their perceptions of the impact of the tested interventions on a set of 9 socio-ecological variables (e.g. amount of fish caught, level of participation in decision-making, support for the MPA). Results revealed that the interventions tested were relatively feasible, effective and cost-effective. Fishers reported positive perceptions of the interventions for the 9 variables considered, especially for level of support for the MPA and for those associated with aspects of governance. Proportional odds models highlighted perceived effects are maximized under certain institutional, local and individual circumstances (e.g. old MPAs, small fisher communities, and fishers with a high proportion of income from fisheries). Findings highlight that employing good governance processes involving stakeholders may rapidly generate improved local support for conservation and provide insights for potential leverage points upon which to act to maximize perceived effectiveness and enhance support toward MPAs.

Protection reveals density-dependent dynamics in fish populations: A case study in the central Mediterranean.

Casting light on how the interaction between protection and density dependence affects fish population dynamics is critical for understanding the effectiveness of marine protected areas (MPAs). We developed a framework based on nonparametric statistics, model selection and multi-model inference to contrast alternative hypotheses about the effect of density dependence on demographic dynamics under protected and unprotected conditions. We trialed it using a 12-year long time series of white seabream (Diplodus sargus sargus) population density within the no-take zone of Torre Guaceto MPA (Italy) and at two nearby unprotected locations. Then, we showed how the demographic models obtained can be used to assess the consequences of protection on population viability. Population dynamics were significantly influenced by fish density within the MPA and at one of the unprotected locations, where demography is possibly driven by directional recruitment subsidy from the MPA. The comparison of population growth rates within and outside the MPA suggests that in unprotected conditions the fishery may remove a fraction between 40 and 70% of the population each year. The population viability analysis pointed out that, while the probability that the population becomes depleted (i.e. undergoes a local, temporary quasi-extinction) is high in unprotected locations, it is negligible within the no-take zone of the MPA.

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.

European spiny lobster recovery from overfishing enhanced through active restocking in Fully Protected Areas.

Fully protected areas (FPAs) help preserving biodiversity and reversing the global decline of fishery resources. Stocks of the European spiny lobster Palinurus elephas (Fabr. 1787), among the most precious gourmet seafood worldwide, are currently facing a dramatic decline. Previous attempts of recovery based on fishery restrictions or active post-larval restocking in marine reserves provided unsuccessful outcomes. Here we present results of a 5-year restocking program carried through a Collaborative Fishery Research (CFR) project, in three ad-hoc established FPAs replenished using below-legal size wild juveniles. Results showed that Catch per Unit Effort (CPUE) in terms of both density and biomass burst (by ca. 300-700%) just 2 years since FPAs establishment, regardless of location. We also report tangible spillover effects (ca. 30-50% increase in density and biomass CPUE outside the FPAs) by the end of the program. Data from a 15-years lasting monitoring of a pilot FPA established in 1998, where the restocking protocol was conducted and protection kept in force once restocking ceased, demonstrated the persistence in time of restocking' benefits. We foster that creation of FPAs assisted with local restocking under oriented CFR programs can represent an option for the recovery of European spiny lobster stocks from overfishing.

Organization Science improves management effectiveness of Marine Protected Areas.

The ecological management effectiveness (EME) of Marine Protected Areas (MPAs) is the degree to which MPAs reach their ecological goals. The significant variability of EME among MPAs has been partly explained by MPA design, management and implementation features (e.g. surface area, enforcement, age of protection). We investigated EME variability by employing, for the first time, Organization Science. Eight Mediterranean MPAs were taken into account as case studies to explore the relationships between EME and MPA features, such as: 1) organizational size (i.e. the ratio between the number of full-time employees and the total MPA surface area), 2) management performance (i.e. the level of effort exerted to enhance and sustain the MPA management, including enforcement), 3) total surface area, and 4) MPA age. The log-response ratios of fish biomass and density in protected vs unprotected (control) areas were used as a proxy of EME. Management performance, organizational size and, to a lesser extent, MPA age were positively correlated with the log-response ratio of fish biomass, whereas total surface area did not display a significant role. None of the four features considered was significantly correlated with the log-response ratio of fish density. Based on our findings, we argue that the employment of Organization Science in the management effectiveness assessment can assist MPA managers to reach MPAs goals more effectively, with a more efficient use of available resources.

Ocean acidification affects somatic and otolith growth relationship in fish: evidence from an in situ study.

Ocean acidification (OA) may have varied effects on fish eco-physiological responses. Most OA studies have been carried out in laboratory conditions without considering the in situ pCO2/pH variability documented for many marine coastal ecosystems. Using a standard otolith ageing technique, we assessed how in situ ocean acidification (ambient, versus end-of-century CO2 levels) can affect somatic and otolith growth, and their relationship in a coastal fish. Somatic and otolith growth rates of juveniles of the ocellated wrasse Symphodus ocellatus living off a Mediterranean CO2 seep increased at the high- pCO2 site. Also, we detected that slower-growing individuals living at ambient pCO2 levels tend to have larger otoliths at the same somatic length (i.e. higher relative size of otoliths to fish body length) than faster-growing conspecifics living under high pCO2 conditions, with this being attributable to the so-called 'growth effect'. Our findings suggest the possibility of contrasting OA effects on fish fitness, with higher somatic growth rate and possibly higher survival associated with smaller relative size of otoliths that could impair fish auditory and vestibular sensitivity.

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.

From sea monsters to charismatic megafauna: Changes in perception and use of large marine animals.

Marine megafauna has always elicited contrasting feelings. In the past, large marine animals were often depicted as fantastic mythological creatures and dangerous monsters, while also arousing human curiosity. Marine megafauna has been a valuable resource to exploit, leading to the collapse of populations and local extinctions. In addition, some species have been perceived as competitors of fishers for marine resources and were often actively culled. Since the 1970s, there has been a change in the perception and use of megafauna. The growth of marine tourism, increasingly oriented towards the observation of wildlife, has driven a shift from extractive to non-extractive use, supporting the conservation of at least some species of marine megafauna. In this paper, we review and compare the changes in the perception and use of three megafaunal groups, cetaceans, elasmobranchs and groupers, with a special focus on European cultures. We highlight the main drivers and the timing of these changes, compare different taxonomic groups and species, and highlight the implications for management and conservation. One of the main drivers of the shift in perception, shared by all the three groups of megafauna, has been a general increase in curiosity towards wildlife, stimulated inter alia by documentaries (from the early 1970s onwards), and also promoted by easy access to scuba diving. At the same time, environmental campaigns have been developed to raise public awareness regarding marine wildlife, especially cetaceans, a process greatly facilitated by the rise of Internet and the World Wide Web. Currently, all the three groups (cetaceans, elasmobranchs and groupers) may represent valuable resources for ecotourism. Strikingly, the economic value of live specimens may exceed their value for human consumption. A further change in perception involving all the three groups is related to a growing understanding and appreciation of their key ecological role. The shift from extractive to non-extractive use has the potential for promoting species conservation and local economic growth. However, the change in use may not benefit the original stakeholders (e.g. fishers or whalers) and there may therefore be a case for providing compensation for disadvantaged stakeholders. Moreover, it is increasingly clear that even non-extractive use may have a negative impact on marine megafauna, therefore regulations are needed.

Author Correction: Ecological effects of full and partial protection in the crowded Mediterranean Sea: a regional meta-analysis.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Applying organization science to assess the management performance of Marine Protected Areas: An exploratory study.

Marine Protected Areas (MPAs) are important tools to achieve marine conservation and resources management goals. The management effectiveness of MPAs (the degree to which MPAs achieve their goals) is highly variable and can be affected by many MPA attributes, for example their design, enforcement and age. Another key factor possibly affecting MPA management effectiveness is the management performance, here conceived according to Horigue et al. definition (2014) as the "level of effort exerted to enhance and sustain management of MPAs". Organization Science (OS), the discipline that studies organizations, can offer a useful framework to assess and interpret MPA management performance. Using an exploratory multiple case study approach, we applied OS principles to 11 Mediterranean MPAs in order to: i) characterize several MPA organizational features; ii) assess MPA management performance (evaluated as the effort deployed in, for example, planning the future, formalizing measurable goals, and implementing specific strategies). Results show that a number of organizational features and networking attributes are highly variable among the MPAs we have studied. For instance, goals are seldom measurable and the strategy to achieve goals is not systematically pursued. Two relevant outcomes emerge from this exploratory study: i) the management performance of the MPAs considered needs considerable improvements; ii) the methods and the approach proposed could help MPAs' managers and policy makers to understand how to improve their management performance and, consequently, their effectiveness.

Fish mitigate trophic depletion in marine cave ecosystems.

Dark marine habitats are often characterized by a food-limited condition. Peculiar dark habitats include marine caves, characterized by the absence of light and limited water flow, which lead to reduced fluxes of organic matter for cave-dwelling organisms. We investigated whether the most abundant and common cave-dwelling fish Apogon imberbis has the potential to play the role of trophic vector in Mediterranean marine caves. We first analysed stomach contents to check whether repletion changes according to a nycthemeral cycle. We then identified the prey items, to see whether they belong to species associated with cave habitats or not. Finally, we assessed whether A. imberbis moves outside marine caves at night to feed, by collecting visual census data on A. imberbis density both inside and outside caves, by day and by night. The stomach repletion of individuals sampled early in the morning was significantly higher than later in the day. Most prey were typical of habitats other than caves. A. imberbis was on average more abundant within caves during the day and outside during the night. Our study supports the hypothesis regarding the crucial trophic role of A. imberbis in connecting Mediterranean marine caves with external habitats.