Coralline barrens and benthic mega-invertebrates: An intimate connection.

Despite considerable progress in understanding the transition from algal forests to coralline barrens, knowledge of coralline barren ecosystems in terms of community composition and functioning is still sparse and important gaps remain to be filled. Using a barren/forest patch system, we tested the hypothesis that the presence of coralline barren enhances the abundance and diversity of benthic mega-invertebrates. We also analysed trophic functional diversity through isotopic analyses of δ13C and δ15N. The distribution of benthic mega-invertebrates biomass differed markedly between coralline barren and algal forest, being more abundant and diverse in the barren state. Isotopic diversity metrics of the benthic mega-invertebrates assemblage indicated comparable trophic structure between the two states, although higher isotopic uniqueness in coralline barren was determined by sea urchins, especially A. lixula, and carnivorous starfish. We showed that in a patchy coralline barren/algal forest system, a more diversified benthic mega-invertebrates assemblage in the barren caused limited trophodynamic changes. This was possibly determined by the behaviour of some trophic groups such as filter feeders, deposit feeders and omnivores. Finally, our results evidence the close association between coralline barrens and benthic mega-invertebrates, contradicting the common view of coralline barrens as depauperate habitats with low diversity and productivity.

The power of Posidonia oceanica meadows to retain microplastics and the consequences on associated macrofaunal benthic communities.

In the coastal environment, a large amount of microplastics (MPs) can accumulate in the sediments of seagrass beds. However, the potential impact these pollutants have on seagrasses and associated organisms is currently unknown. In this study, we investigated the differences in MPs abundance and composition (i.e., shape, colour and polymer type) in marine sediments collected at different depths (-5 m, -15 m, -20 m) at two sites characterized by the presence of Posidonia oceanica meadows and at one unvegetated site. In the vegetated sites, sediment samples were collected respectively above and below the upper and lower limits of the meadow (-5 m and -20 m), out of the P. oceanica meadow, and in the central portion of the meadow (-15 m). By focusing on the central part of the meadow, we investigated if the structural features (i.e. shoots density and leaf surface) can affect the amount of MPs retained within the underlying sediment and if these, in turn, can affect the associated benthic communities. Results showed that the number of MPs retained by P. oceanica meadows was higher than that found at the unvegetated site, showing also a different composition. In particular, at vegetated sites, we observed that MPs particles were more abundant within the meadow (at - 15 m), compared to the other depths, on unvegetated sediment, with a dominance of transparent fragments of polypropylene (PP). We observed that MPs entrapment by P. oceanica was accentuated by the higher shoots density, while the seagrass leaf surface did not appear to have any effect. Both the abundance and richness of macrofauna associated with P. oceanica rhizomes appear to be negatively influenced by the MPs abundance in the sediment. Overall, this study increases knowledge of the potential risks of MPs accumulation in important coastal habitats such as the Posidonia oceanica meadows.

Year-round variation in the isotopic niche of Scopoli's shearwater (Calonectris diomedea) breeding in contrasting sea regions of the Mediterranean Sea.

Top marine predators are key components of marine food webs. Among them, long-distance migratory seabirds, which travel across different marine ecosystems over the year, may experience important year-round changes in terms of oceanographic conditions and availability of trophic resources. We tested whether this was the case in the Scopoli's shearwater (Calonectris diomedea), a trans-equatorial migrant and top predator, by sampling birds breeding in three environmentally different regions of the Mediterranean Sea. The analysis of positional data and stable isotopes (δ1³C and δ15N) of target feathers revealed that birds from the three regions were spatially segregated during the breeding period while they shared non-breeding areas in the Atlantic Ocean. Isotopic baseline levels of N and C (meso-zooplankton) were significantly different among marine regions during breeding. Such variation was reflected at the higher trophic levels of pelagic and demersal fish muscles as well as in shearwater feathers grown in the Mediterranean. δ15N- and δ13C-adjusted values of shearwaters were significantly different among populations suggesting that birds from different breeding areas relied on prey species from different trophic levels. Conversely, the non-breeding spatial and isotopic niches overlapped greatly among the three populations. Shearwater trophic niches during breeding were narrower and segregated compared to the non-breeding period, revealing a high plasticity in trophic resource use. Overall, this study highlights seasonal and region-specific use of trophic resources by Scopoli's shearwater, suggesting a broad trophic plasticity and possibly a high adaptability to environmental changes.

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.

Thermo-priming increases heat-stress tolerance in seedlings of the Mediterranean seagrass P. oceanica.

Seawater warming and increased incidence of marine heatwaves (MHW) are threatening the integrity of coastal marine habitats including seagrasses, which are particularly vulnerable to climate changes. Novel stress tolerance-enhancing strategies, including thermo-priming, have been extensively applied in terrestrial plants for enhancing resilience capacity under the re-occurrence of a stress event. We applied, for the first time in seedlings of the Mediterranean seagrass Posidonia oceanica, a thermo-priming treatment through the exposure to a simulated warming event. We analyzed the photo-physiological and growth performance of primed and non-primed seedlings, and the gene expression responses of selected genes (i.e. stress-, photosynthesis- and epigenetic-related genes). Results revealed that during the re-occurring stress event, primed seedlings performed better than unprimed showing unaltered photo-physiology supported by high expression levels of genes related to stress response, photosynthesis, and epigenetic modifications. These findings offer new opportunities to improve conservation and restoration efforts in a future scenario of environmental changes.

The invasive seaweed Asparagopsis taxiformis erodes the habitat structure and biodiversity of native algal forests in the Mediterranean Sea.

Invasive seaweeds are listed among the most relevant threats to marine ecosystems worldwide. Biodiversity hotspots, such as the Mediterranean Sea, are facing multiple invasions and are expected to be severely affected by the introduction of new non-native seaweeds in the near future. In this study, we evaluated the consequences of the shift from the native Ericaria brachycarpa to the invasive Asparagopsis taxiformis habitat on the shallow rocky shores of Favignana Island (Egadi Islands, MPA, Sicily, Italy). We compared algal biomass and species composition and structure of the associated epifaunal assemblages in homogenous and mixed stands of E. brachycarpa and A. taxiformis. The results showed that the biomass of primary producers is reduced by 90% in the A. taxiformis invaded habitat compared to the E. brachycarpa native habitat. The structure of the epifaunal assemblages displayed significant variations among homogenous and mixed stands. The abundance, species richness and Shannon-Wiener diversity index of the epifaunal assemblages decreased by 89%, 78% and 40%, respectively, from homogenous stands of the native E. brachycarpa to the invasive A. taxiformis. Seaweed biomass was the structural attribute better explaining the variation in epifaunal abundance, species richness and diversity. Overall, our results suggest that the shift from E. brachycarpa to A. taxiformis habitat would drastically erode the biomass of primary producers and the associated biodiversity. We hypothesize that a complete shift from native to invasive seaweeds could ultimately lead to bottom-up effects on rocky shore habitats, with negative consequences for the ecosystem structure, functioning, and the services provided.

Nest guarding behaviour of a temperate wrasse differs between sites off Mediterranean CO2 seeps.

Organisms may respond to changing environmental conditions by adjusting their behaviour (i.e., behavioural plasticity). Ocean acidification (OA), resulting from anthropogenic emissions of carbon dioxide (CO2), is predicted to impair sensory function and behaviour of fish. However, reproductive behaviours, and parental care in particular, and their role in mediating responses to OA are presently overlooked. Here, we assessed whether the nesting male ocellated wrasse Symphodus ocellatus from sites with different CO2 concentrations showed different behaviours during their breeding season. We also investigated potential re-allocation of the time-budget towards different behavioural activities between sites. We measured the time period that the nesting male spent carrying out parental care, mating and exploring activities, as well as changes in the time allocation between sites at ambient (~400 µatm) and high CO2 concentrations (~1000 µatm). Whilst the behavioural connectance (i.e., the number of linkages among different behaviours relative to the total amount of linkages) was unaffected, we observed a significant reduction in the time spent on parental care behaviour, and a significant decrease in the guarding activity of fish at the high CO2 sites, with a proportional re-allocation of the time budget in favour of courting and wandering around, which however did not change between sites. This study shows behavioural differences in wild fish living off volcanic CO2 seeps that could be linked to different OA levels, suggesting that behavioural plasticity may potentially act as a mechanism for buffering the effects of ongoing environmental change. A reallocation of the time budget between key behaviours may play a fundamental role in determining which marine organisms are thriving under projected OA.

Boosted fish abundance associated with Posidonia oceanica meadows in temperate shallow CO2 vents.

Ocean acidification (OA) may induce major shifts in the structure and function of coastal marine ecosystems. Studies in volcanic CO2 vents, where seawater is naturally acidified, have reported an overall simplification of fish assemblages structure, while some primary producers are likely to increase their biomass under elevated concentration of CO2. Here we used temperate shallow CO2 vents located around the coast of Ischia island (Italy) to assess the effects of OA on necto-benthic fish assemblages associated with the foundation seagrass species Posidonia oceanica in the Mediterranean Sea. We compared P. oceanica meadow structure, its epiphytic community and the associated fish assemblage structure and diversity at vents with low pH sites and reference sites with ambient pH using underwater visual census strip transects, in two seasons (fall 2018 and summer 2019). Data were analysed using both univariate and multivariate statistical techniques. Results showed greater P. oceanica habitat complexity (i.e. shoot density) and lower abundance of epiphytic calcareous species (e.g. coralline algae) at the vents than reference sites. Total abundance of adult and juvenile fish was higher at vents than reference sites, while no differences were found for species richness and composition. Overall, the herbivore Sarpa salpa stands out among the species contributing the most to dissimilarity between vents and reference sites, showing higher abundances under OA conditions. This pattern could be explained by the combined effect of a positive response to the higher structural meadows complexity and the greater seagrasses palatability/nutritional value occurring at the vents, which may help herbivores to withstand the higher energetic cost to live under high pCO2/low pH conditions. Our results indicate that necto-benthic fish assemblages associated with the Mediterranean P. oceanica ecosystem may cope with OA under the CO2 emission scenarios forecasted for the end of this century.

Reply to "Letter to the editor regarding the article 'Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods' by Alagna et al., published in Marine Pollution Bulletin, 149: 2019 (110578)" by Calvo et al. Marine Pollution Bulletin, 158:2020 (111395).

Calvo et al. (2020) criticize a new seagrass rehabilitation method proposed by Alagna et al. (2019) and inspired by the Posidonia oceanica spontaneous recovery observed at Capo Feto (Sicily), were recolonization was detected almost exclusively on rubbles deployed to fill a pipeline trench. Calvo et al. (2020) claim that natural recovery occurred consistently also on dead matte along the eastern side of the trench, weakening the assumption on which the method is based. Here we show that the P. oceanica patches reported by these authors as new establishments were already documented in 2003 (Vega Fernandez et al., 2005) and are attributable to the fragmentation of the pristine meadow caused by altered sedimentation rate after an extensive dredging operation. Moreover, we outline the area of applicability of the method tested in Alagna et al. (2019) and provide a point-by-point rebuttal to the complaints of imprecise and misleading contents of the paper.

The perfect microsite: How to maximize Posidonia oceanica seedling settlement success for restoration purposes using ecological knowledge.

The use of sexual propagules to restore seagrass meadows has raised increasing attention in the last years as seed-based strategies avoid impacts on donor beds while preserving genetic diversity in restored populations. However, the availability of suitable microsites for seedling establishment at transplantation locations is crucial in order to achieve positive outcome of restoration actions. In this study we develop ad-hoc holders that act as optimal microsites for Posidonia oceanica seedling establishment. Holders are intended to be transferred in the field for restoration purposes after few months of indoor seedling culture. Seedling ability to self-anchor to rocky substrates via adhesive root hairs was exploited. We tested rocky holders with different designs in order to maximize seedling survival and settlement. The effect of the holder design on seedling anchorage performances was evaluated. Holders were provided with different topographical complexity and substrate slope. Topographical complexity significantly influenced settlement success, as seedlings did not attach to flat holders, while anchorage reached 100% on holders provided with complexity at seed and the root scales. Substrate slope did not affect the percentage of anchored seedlings, conversely it influenced root growth pattern and thus anchorage stability. This study shows how ecological knowledge of species' life history strategies and associated critical traits provides valuable hints to develop alternative approaches to seagrass restoration tailored to the biology of the system under study.

Microplastics impair the feeding performance of a Mediterranean habitat-forming coral.

The impact of plastic debris, and in particular of microplastics (here referred as particles smaller than 5 mm) on aquatic environments has now become a topic of raising concern. Microplastics are particularly abundant in the Mediterranean Sea, potentially exerting substantial pressures on marine organisms at different levels of organization. Ingestion of microplastics has been observed in a large number of marine species. The aim of this work is to test if microplastics produce a feeding impairment in Astroides calycularis, a shallow water, habitat-forming coral endemic to the Mediterranean Sea. Our findings suggest a lack of any avoidance mechanism allowing the polyps to discern between food items and microplastics when occurring simultaneously. Moreover, polyps spend a considerable amount of time on handling microplastic particles. As a consequence, microplastics impair the feeding efficiency in A. calycularis, since polyps may not be fully able to profit from the drifting plankton aggregations. Therefore, we suggest that microplastics can cause a reduction of fitness in A. calycularis, and presumably also in other species characterized by suspension feeding strategy.

A fast-moving target: achieving marine conservation goals under shifting climate and policies.

In the Anthropocene, marine ecosystems are rapidly shifting to new ecological states. Achieving effective conservation of marine biodiversity has become a fast-moving target because of both global climate change and continuous shifts in marine policies. How prepared are we to deal with this crisis? We examined EU Member States Programs of Measures designed for the implementation of EU marine environmental policies, as well as recent European Marine Spatial Plans, and discovered that climate change is rarely considered operationally. Further, our analysis revealed that monitoring programs in marine protected areas are often insufficient to clearly distinguish between impacts of local and global stressors. Finally, we suggest that while the novel global Blue Growth approach may jeopardize previous marine conservation efforts, it can also provide new conservation opportunities. Adaptive management is the way forward (e.g., preserving ecosystem functions in climate change hotspots, and identifying and targeting climate refugia areas for protection) using Marine Spatial Planning as a framework for action, especially given the push for Blue Growth.

Anthropogenic impact is negatively related to coral health in Sicily (Mediterranean Sea).

Shallow-water marine organisms are among the first to suffer from combined effects of natural and anthropogenic drivers. The orange coral Astroides calycularis is a shallow-water bioconstructor species endemic to the Mediterranean Sea. Although raising conservation interest, also given its special position within the Dendrophylliidae, information about the threats to its health is scant. We investigated the health status of A. calycularis at five locations in northwestern Sicily along a gradient of cumulative human impact and the most probable origin of the threats to this species, including anthropogenic land-based and sea-based threats. Cumulative human impact appeared inversely related to the performance of A. calycularis at population, colony, and polyp levels. Sea-based human impacts appeared among the most likely causes of the variation observed. The reduction in polyp length can limit the reproductive performance of A. calycularis, while the decrease of percent cover and colony area is expected to impair its peculiar feeding behaviour by limiting the exploitable dimensional range of prey and, ultimately, reef functioning. This endangered habitat-forming species appeared susceptible to anthropogenic pressures, suggesting the need to re-assess its vulnerability status. Creating microprotected areas with specific restrictions to sea-based human impacts could be the best practice preserve these bioconstructions.

Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods.

Seagrasses are among the most threatened biomes worldwide. Until now, seagrass rehabilitation success has reached about 38% overall and more effective approaches to restoration are urgently needed. Here we report a novel method to rehabilitate Posidonia oceanica meadows based on observation of the species' natural recovery after disturbance. Posidonia oceanica rhizomes were transplanted on gabions filled with rocks of selected sizes in order to build a firm substrate with topographic complexity in the relevant scale range to propagules. Five techniques were tested, each involving a different anchoring device. The "slot" technique, which uses a wire-net pocket to retain the cuttings, was the most successful, with survival exceeding 85% after thirty months. Branching allowed final shoot survival to reach 422% of initial planting density. This study shows how an in-depth knowledge of species life history processes provides a suitable foundation for developing effective restoration methods that benefit from species recovery ability.

Threats to marine biodiversity in European protected areas.

Marine protected areas (MPAs) represent the main tool for halting the loss of marine biodiversity. However, there is increasing evidence concerning their limited capacity to reduce or eliminate some threats even within their own boundaries. Here, we analysed a Europe-wide dataset comprising 31,579 threats recorded in 1692 sites of the European Union's Natura 2000 conservation network. Focusing specifically on threats related to marine species and habitats, we found that fishing and outdoor activities were the most widespread threats reported within MPA boundaries, although some spatial heterogeneity in the distribution of threats was apparent. Our results clearly demonstrate the need to reconsider current management plans, standardise monitoring approaches and reporting, refine present threat assessments and improve knowledge of their spatial patterns within and outside MPAs in order to improve conservation capacity and outcomes.

Application of Hyperspectral Imaging to Underwater Habitat Mapping, Southern Adriatic Sea.

Hyperspectral imagers enable the collection of high-resolution spectral images exploitable for the supervised classification of habitats and objects of interest (OOI). Although this is a well-established technology for the study of subaerial environments, Ecotone AS has developed an underwater hyperspectral imager (UHI) system to explore the properties of the seafloor. The aim of the project is to evaluate the potential of this instrument for mapping and monitoring benthic habitats in shallow and deep-water environments. For the first time, we tested this system at two sites in the Southern Adriatic Sea (Mediterranean Sea): the cold-water coral (CWC) habitat in the Bari Canyon and the Coralligenous habitat off Brindisi. We created a spectral library for each site, considering the different substrates and the main OOI reaching, where possible, the lower taxonomic rank. We applied the spectral angle mapper (SAM) supervised classification to map the areal extent of the Coralligenous and to recognize the major CWC habitat-formers. Despite some technical problems, the first results demonstrate the suitability of the UHI camera for habitat mapping and seabed monitoring, through the achievement of quantifiable and repeatable classifications.

Synergistic reduction of a native key herbivore performance by two non-indigenous invasive algae.

Native generalist grazers can control the populations of non-indigenous invasive algae (NIIA). Here, it was found that the simultaneous consumption of two co-occurring NIIA, Caulerpa cylindracea and C. taxifolia var. distichophylla, hinders the grazing ability of the main Mediterranean herbivorous, the native sea urchin Paracentrotus lividus. The ingestion of any of the two NIIA alone did not produce any difference in sea urchin righting time with respect to usual algal diet. In contrast, the simultaneous consumption of both NIIA, which grow intermingled in nature and are consumed by P. lividus, retarded its righting behavior. Such result reveals substantial physiological stress in the sea urchin, which resulted in reduced motility and coordination. The reported findings reveal the potential of NIIA co-occurrence to escape the supposed control exerted by the main native generalist grazer in Mediterranean sublittoral communities, which in turn can be locked in an "invaded" state.

Benthic-pelagic coupling mediates interactions in Mediterranean mixed fisheries: An ecosystem modeling approach.

Benthic-pelagic coupling plays a pivotal role in aquatic ecosystems but the effects of fishery driven interactions on its functioning has been largely overlooked. Disentangling the benthic-pelagic links including effects of mixed fisheries, however, needs sketching a whole description of ecosystem interactions using quantitative tools. A holistic food web model has been here developed in order to understand the interplay between the benthic-pelagic coupling and mixed fisheries in a Mediterranean system such as the Strait of Sicily. The reconstruction of the food web required review and integration of a vast set of local and regional biological information from bacteria to large pelagic species that were aggregated into 72 functional groups. Fisheries were described by 18 fleet segments resulting from combination of fishing gears and fishing vessel size. The input-output analysis on the food web of energy pathways allowed identifying effects of biological and fishery components. Results showed that the structure of the Strait of Sicily food web is complex. Similarly to other Mediterranean areas, the food web of the Strait of Sicily encompasses 4.5 trophic levels (TLs) with the highest TLs reached by bluefin tuna, swordfish and large hake and largely impacted by bottom trawling and large longline. Importantly, benthic-pelagic coupling is affected by direct and indirect impacts among groups of species, fleets and fleets-species through the whole trophic spectrum of the food web. Moreover, functional groups able to move on large spatial scales or life history of which is spent between shelf and slope domains play a key role in linking subsystems together and mediate interactions in the Mediterranean mixed fisheries.

Adaptive responses along a depth and a latitudinal gradient in the endemic seagrass Posidonia oceanica.

Seagrass meadows provide important ecosystem services and are critical for the survival of the associated invertebrate community. However, they are threatened worldwide by human-driven environmental change. Understanding the seagrasses' potential for adaptation is critical to assess not only their ability to persist under future global change scenarios, but also to assess the persistence of the associated communities. Here we screened a wild population of Posidonia oceanica, an endemic long-lived seagrass in the Mediterranean Sea, for genes that may be target of environmental selection, using an outlier and a genome-wide transcriptome analysis. We identified loci where polymorphism or differential expression was associated with either a latitudinal or a bathymetric gradient, as well as with both gradients in an effort to identify loci associated with temperature and light. We found the candidate genes underlying growth and immunity to be divergent between populations adapted to different latitudes and/or depths, providing evidence for local adaptation. Furthermore, we found evidence of reduced gene flow among populations including adjacent populations. Reduced gene flow, combined with low sexual recombination, small effective population size, and long generation time of P. oceanica raises concerns for the long-term persistence of this species, especially in the face of rapid environmental change driven by human activities.

Mediterranean Bioconstructions Along the Italian Coast.

Marine bioconstructions are biodiversity-rich, three-dimensional biogenic structures, regulating key ecological functions of benthic ecosystems worldwide. Tropical coral reefs are outstanding for their beauty, diversity and complexity, but analogous types of bioconstructions are also present in temperate seas. The main bioconstructions in the Mediterranean Sea are represented by coralligenous formations, vermetid reefs, deep-sea cold-water corals, Lithophyllum byssoides trottoirs, coral banks formed by the shallow-water corals Cladocora caespitosa or Astroides calycularis, and sabellariid or serpulid worm reefs. Bioconstructions change the morphological and chemicophysical features of primary substrates and create new habitats for a large variety of organisms, playing pivotal roles in ecosystem functioning. In spite of their importance, Mediterranean bioconstructions have not received the same attention that tropical coral reefs have, and the knowledge of their biology, ecology and distribution is still fragmentary. All existing data about the spatial distribution of Italian bioconstructions have been collected, together with information about their growth patterns, dynamics and connectivity. The degradation of these habitats as a consequence of anthropogenic pressures (pollution, organic enrichment, fishery, coastal development, direct physical disturbance), climate change and the spread of invasive species was also investigated. The study of bioconstructions requires a holistic approach leading to a better understanding of their ecology and the application of more insightful management and conservation measures at basin scale, within ecologically coherent units based on connectivity: the cells of ecosystem functioning.