Trajectories of trace element accumulation in seagrass (Posidonia oceanica) over a decade reveal the footprint of fish farming.

To evaluate the effect of trace element (TE) release from fish farms on seagrass Posidonia oceanica, we compared TE concentrations (As, Cd, Co, Cu, Mn, Mo, Ni, Pb, V, Zn) in shoots near fish cages (Station 'Cage') with those away from them (Station 'Control') in two fish farm facilities (Site 1 and Site 2, North Aegean Sea, Greece). We assessed the present (i.e., 2021, year of sampling) and past (reconstructed period 2012-2020) accumulation of TEs using the living compartments (leaf blades, sheaths, rhizomes, roots, epiphytes) and the dead sheaths, respectively. We also assessed possible seagrass degradation by reconstructing past rhizome production. P. oceanica rhizome production at the 'Cage' stations was up to 50% lower than at the 'Control' stations. Most TE concentrations were higher at 'Cage' stations, but the differences often depended on the seagrass living compartment. Significant differentiation between 'Cage' and 'Control' stations was observed based on the TE concentrations of the dead sheaths during 2012-2020. The contamination level at the 'Cage' stations was mostly moderate in Site 1 and low in Site 2, during the reconstructed period, while an increasing contamination trend was found for certain potential phytotoxic TEs (As, Cu, Cd, Mo, V). Our results emphasize the need for the aquaculture industry to work towards a more ecologically aware approach.

Decline of seagrass (Posidonia oceanica) production over two decades in the face of warming of the Eastern Mediterranean Sea.

The response of Posidonia oceanica meadows to global warming of the Eastern Mediterranean Sea, where the increase in sea surface temperature (SST) is particularly severe, is poorly investigated. Here, we reconstructed the long-term P. oceanica production in 60 meadows along the Greek Seas over two decades (1997-2018), using lepidochronology. We determined the effect of warming on production by reconstructing the annual and maximum (i.e. August) SST, considering the role of other production drivers related to water quality (i.e. Chla, suspended particulate matter, Secchi depth). Grand mean (±SE) production across all sites and the study period was 48 ± 1.1 mg DW per shoot yr-1 . Production over the last two decades followed a trajectory of decrease, which was related to the concurrent increase in annual SST and SSTaug . Annual SST > 20°C and SSTaug > 26.5°C was related to production decline (GAMM, P < 0.05), while the rest of the tested factors did not help explain the production pattern. Our results indicate a persistent and increasing threat for Eastern Mediterranean meadows, drawing attention to management authorities, highlighting the necessity of reducing local impacts to enhance the resilience of seagrass meadows to global change threats.

A Tight Interaction between the Native Seagrass Cymodocea nodosa and the Exotic Halophila stipulacea in the Aegean Sea Highlights Seagrass Holobiont Variations.

Seagrasses harbour bacterial communities with which they constitute a functional unit called holobiont that responds as a whole to environmental changes. Epiphytic bacterial communities rapidly respond to both biotic and abiotic factors, potentially contributing to the host fitness. The Lessepsian migrant Halophila stipulacea has a high phenotypical plasticity and harbours a highly diverse epiphytic bacterial community, which could support its invasiveness in the Mediterranean Sea. The current study aimed to evaluate the Halophila/Cymodocea competition in the Aegean Sea by analysing each of the two seagrasses in a meadow zone where these intermingled, as well as in their monospecific zones, at two depths. Differences in holobionts were evaluated using seagrass descriptors (morphometric, biochemical, elemental, and isotopic composition) to assess host changes, and 16S rRNA gene to identify bacterial community structure and composition. An Indicator Species Index was used to identify bacteria significantly associated with each host. In mixed meadows, native C. nodosa was shown to be affected by the presence of exotic H. stipulacea, in terms of both plant descriptors and bacterial communities, while H. stipulacea responded only to environmental factors rather than C. nodosa proximity. This study provided evidence of the competitive advantage of H. stipulacea on C. nodosa in the Aegean Sea and suggests the possible use of associated bacterial communities as an ecological seagrass descriptor.

Effects of high temperature and marine heat waves on seagrasses: Is warming affecting the nutritional value of Posidonia oceanica?

Primary producers nutritional content affects the entire food web. Here, changes in nutritional value associated with temperature rise and the occurrence of marine heat waves (MHWs) were explored in the endemic Mediterranean seagrass Posidonia oceanica. The variability of fatty acids (FAs) composition and carbon (C) and nitrogen (N) content were examined during summer 2021 from five Mediterranean sites located at the same latitude but under different thermal environments. The results highlighted a decrease in unsaturated FAs and C/N ratio and an increase of monounsaturated FA (MUFA) and N content when a MHW occurred. By contrast, the leaf biochemical composition seems to be adapted to local water temperature since only few significant changes in MUFA were found and N and C/N had an opposite pattern compared to when a MHW occurs. The projected increase in temperature and frequency of MHW suggest future changes in the nutritional value and palatability of leaves.

Seagrass (Halophila stipulacea) invasion enhances carbon sequestration in the Mediterranean Sea.

The introduction and establishment of exotic species often result in significant changes in recipient communities and their associated ecosystem services. However, usually the magnitude and direction of the changes are difficult to quantify because there is no pre-introduction data. Specifically, little is known about the effect of marine exotic macrophytes on organic carbon sequestration and storage. Here, we combine dating sediment cores (210 Pb) with sediment eDNA fingerprinting to reconstruct the chronology of pre- and post-arrival of the Red Sea seagrass Halophila stipulacea spreading into the Eastern Mediterranean native seagrass meadows. We then compare sediment organic carbon storage and burial rates before and after the arrival of H. stipulacea and between exotic (H. stipulacea) and native (C. nodosa and P. oceanica) meadows since the time of arrival following a Before-After-Control-Impact (BACI) approach. This analysis revealed that H. stipulacea arrived at the areas of study in Limassol (Cyprus) and West Crete (Greece) in the 1930s and 1970s, respectively. Average sediment organic carbon after the arrival of H. stipulacea to the sites increased in the exotic meadows twofold, from 8.4 ± 2.5 g Corg  m-2  year-1 to 14.7 ± 3.6 g Corg  m-2  year-1 , and, since then, burial rates in the exotic seagrass meadows were higher than in native ones of Cymodocea nodosa and Posidonia oceanica. Carbon isotopic data indicated a 50% increase of the seagrass contribution to the total sediment Corg pool since the arrival of H. stipulacea. Our results demonstrate that the invasion of H. stipulacea may play an important role in maintaining the blue carbon sink capacity in the future warmer Mediterranean Sea, by developing new carbon sinks in bare sediments and colonizing areas previously occupied by the colder thermal affinity P. oceanica.

Tropical seagrass Halophila stipulacea shifts thermal tolerance during Mediterranean invasion.

Exotic species often face new environmental conditions that are different from those that they are adapted to. The tropical seagrass Halophila stipulacea is a Lessepsian migrant that colonized the Mediterranean Sea around 100 years ago, where at present the minimum seawater temperature is cooler than in its native range in the Red Sea. Here, we tested if the temperature range in which H. stipulacea can exist is conserved within the species or if the exotic populations have shifted their thermal breadth and optimum due to the cooler conditions in the Mediterranean. We did so by comparing the thermal niche (e.g. optimal temperatures, and upper and lower thermal limits) of native (Saudi Arabia in the Red Sea) and exotic (Greece and Cyprus in the Mediterranean Sea) populations of H. stipulacea. We exposed plants to 12 temperature treatments ranging from 8 to 40°C for 7 days. At the end of the incubation period, we measured survival, rhizome elongation, shoot recruitment, net population growth and metabolic rates. Upper and lower lethal thermal thresholds (indicated by 50% plant mortality) were conserved across populations, but minimum and optimal temperatures for growth and oxygen production were lower for Mediterranean populations than for the Red Sea one. The displacement of the thermal niche of exotic populations towards the colder Mediterranean Sea regime could have occurred within 175 clonal generations.

Ecological effects of non-native species in marine ecosystems relate to co-occurring anthropogenic pressures.

Predictors for the ecological effects of non-native species are lacking, even though such knowledge is fundamental to manage non-native species and mitigate their impacts. Current theories suggest that the ecological effects of non-native species may be related to other concomitant anthropogenic stressors, but this has not been tested at a global scale. We combine an exhaustive meta-analysis of the ecological effects of marine non-native species with human footprint proxies to determine whether the ecological changes due to non-native species are modulated by co-occurring anthropogenic impacts. We found that non-native species had greater negative effects on native biodiversity where human population was high and caused reductions in individual performance where cumulative human impacts were large. On this basis we identified several marine ecoregions where non-native species may have the greatest ecological effects, including areas in the Mediterranean Sea and along the northwest coast of the United States. In conclusion, our global assessment suggests coexisting anthropogenic impacts can intensify the ecological effects of non-native species.

Author Correction: The future of Blue Carbon science.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The future of Blue Carbon science.

The term Blue Carbon (BC) was first coined a decade ago to describe the disproportionately large contribution of coastal vegetated ecosystems to global carbon sequestration. The role of BC in climate change mitigation and adaptation has now reached international prominence. To help prioritise future research, we assembled leading experts in the field to agree upon the top-ten pending questions in BC science. Understanding how climate change affects carbon accumulation in mature BC ecosystems and during their restoration was a high priority. Controversial questions included the role of carbonate and macroalgae in BC cycling, and the degree to which greenhouse gases are released following disturbance of BC ecosystems. Scientists seek improved precision of the extent of BC ecosystems; techniques to determine BC provenance; understanding of the factors that influence sequestration in BC ecosystems, with the corresponding value of BC; and the management actions that are effective in enhancing this value. Overall this overview provides a comprehensive road map for the coming decades on future research in BC science.

Publisher Correction: Global ecological impacts of marine exotic species.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Exotic Halophila stipulacea is an introduced carbon sink for the Eastern Mediterranean Sea.

Carbon and nitrogen storage in exotic Halophila stipulacea were compared to that in native Posidonia oceanica and Cymodocea nodosa meadows and adjacent unvegetated sediments of the Eastern Mediterranean Sea and to that in native H. stipulacea of the Red Sea at sites with different biogeochemical conditions and level of human pressure. Exotic H. stipulacea possessed considerable storing capacity, with 2-fold higher Corg stock (0.71 ± 0.05 kg m-2 in the top 20 cm of sediment) and burial (14.78 gCorg m-2 y-1) than unvegetated areas and C. nodosa meadows and, surprisingly, comparable to P. oceanica. N (0.07 ± 0.01 kg m-2) and Cinorg (14.06 ± 8.02 kg m-2) stocks were similar between H. stipulacea and C. nodosa or unvegetated sediments, but different to P. oceanica. Corg and N stocks were higher in exotic than native H. stipulacea populations. Based on isotopic mixing model, organic material trapped in H. stipulacea sediments was mostly allochthonous (seagrass detritus 17% vs seston 67%). Corg stock was similar between monospecific and invaded C. nodosa meadows by H. stipulacea. Higher stocks were measured in the higher human pressure site. H. stipulacea introduction may contribute in the increase of carbon sequestration in the Eastern Mediterranean.

Global ecological impacts of marine exotic species.

Exotic species are a growing global ecological threat; however, their overall effects are insufficiently understood. While some exotic species are implicated in many species extinctions, others can provide benefits to the recipient communities. Here, we performed a meta-analysis to quantify and synthesize the ecological effects of 76 exotic marine species (about 6% of the listed exotics) on ten variables in marine communities. These species caused an overall significant, but modest in magnitude (as indicated by a mean effect size of g < 0.2), decrease in ecological variables. Marine primary producers and predators were the most disruptive trophic groups of the exotic species. Approximately 10% (that is, 2 out of 19) of the exotic species assessed in at least three independent studies had significant impacts on native species. Separating the innocuous from the disruptive exotic species provides a basis for triage efforts to control the marine exotic species that have the most impact, thereby helping to meet Aichi Biodiversity Target 9 of the Convention on Biological Diversity.

Plant and sediment properties in seagrass meadows from two Mediterranean CO2 vents: Implications for carbon storage capacity of acidified oceans.

Assessing the status of important carbon sinks such as seagrass meadows is of primary importance when dealing with potential climate change mitigation strategies. This study examined plant and sediment properties in seagrass meadows (Cymodocea nodosa (Ucria) Asch.) from two high pCO2-low pH Mediterranean vent systems, located at Milos (Greece) and Vulcano (Italy) Islands, providing insights on carbon storage potential in future acidified oceans. Contrary to what has been suggested, carbon content (both inorganic and organic) and its surficial accumulation decreased at high pCO2-low pH in comparison with controls. The decrease in inorganic carbon may result from the higher solubility of carbonates due to the more acidic conditions. At Vulcano, the seagrass properties (e.g., leaf area, biomass) appeared negatively affected by environmental conditions at high pCO2-low pH conditions and this may have had a detrimental effect on the organic carbon content and accumulation. At Milos, organic carbon decreased at high pCO2-low pH conditions, despite the increase in seagrass aboveground biomass, leaf length and area, probably as a consequence of site-specific features, which need further investigation and may include both biotic and abiotic factors (e.g., oligotrophic conditions, decreased sedimentation rate and input of allochthonous material). Results suggest that, in contrast to previous predictions based exclusively on the expected positive response of seagrasses to ocean acidification, carbon storage capacity of the seagrass C. nodosa may not increase at high pCO2-low pH conditions. This study emphasizes the need to investigate further the potential alteration in the climate mitigation service delivered by seagrass meadows in acidified oceans.

Seagrass sedimentary deposits as security vaults and time capsules of the human past.

Seagrass meadows form valuable ecosystems, but are considered to have low cultural value due to limited research efforts in this field. We provide evidence that seagrass deposits play a hitherto unrealized central role in preserving valuable submerged archaeological and historical heritage across the world, while also providing an historical archive of human cultural development over time. We highlight three case studies showing the significance of seagrass in protecting underwater cultural heritage in Denmark, the Mediterranean and Australia. Moreover, we present an overview of additional evidence compiled from the literature. We emphasize that this important role of seagrasses is linked to their capacity to form thick sedimentary deposits, accumulating over time, thereby covering and sealing submerged archaeological heritage. Seagrass conservation and restoration are key to protecting this buried heritage while also supporting the role of seagrass deposits as carbon sinks as well as the many other important ecosystem functions of seagrasses.

Species-specific response to sulfide intrusion in native and exotic Mediterranean seagrasses under stress.

We explored the sulfur dynamics and the relationships between sediment sulfur and nutrient pools, seagrass structural and physiological variables and sulfide intrusion in native (Posidonia oceanica, Cymodocea nodosa) and exotic (Halophila stipulacea) Mediterranean seagrasses at six sites affected by cumulative anthropogenic pressures to understand the factors controlling sulfide intrusion in seagrass. Sensitive indicators of seagrass stress (leaf TN, δ15N, TS, Fsulfide) were increased at several sites, implying that seagrasses are under pressure. Sulfide intrusion was not related to sediment TOC but it was negatively related to shoot size and below-ground biomass. Sulfide intrusion in seagrass tissue was high in P. oceanica (12-17%) and considerably higher in C. nodosa (27-35%). Intrusion was particularly high in H. stipulacea (30-50%), suggesting that its possible biogeographical expansion due to warming of the Mediterranean may result in accumulation of sulfides in the sediments and hypoxia/anoxia with further implications in ecosystem function.

Environmental variability and heavy metal concentrations from five lagoons in the Ionian Sea (Amvrakikos Gulf, W Greece).

BACKGROUND: Coastal lagoons are ecosystems of major importance as they host a number of species tolerant to disturbances and they are highly productive. Therefore, these ecosystems should be protected to ensure stability and resilience. The lagoons of Amvrakikos Gulf form one of the most important lagoonal complexes in Greece. The optimal ecological status of these lagoons is crucial for the well-being of the biodiversity and the economic prosperity of the local communities. Thus, monitoring of the area is necessary to detect possible sources of disturbance and restore stability. NEW INFORMATION: The environmental variables and heavy metals concentrations, from five lagoons of Amvrakikos Gulf were measured from seasonal samplings and compared to the findings of previous studies in the area, in order to check for possible sources of disturbance. The analysis, showed that i) the values of the abiotic parameters vary with time (season), space (lagoon) and with space over time; ii) the variability of the environmental factors and enrichment in certain elements is naturally induced and no source of contamination is detected in the lagoons.

Mussel farming in Maliakos Gulf and quality indicators of the marine environment: Good benthic below poor pelagic ecological status.

Biological and geochemical variables in the water column and sediments were monitored along a transect of a mussel farm located in a transitional environment in Maliakos Gulf, a semi-enclosed gulf in eastern Mediterranean. Analyses of water, sediment and macrofauna samples were used to calculate ecological status indicators in the context of the European Water Framework Directive. The water column ecological status was "Poor" or "Bad" showing little change with distance from the farm, but the ecological status of the benthic communities was found to be "Good," although there were quantitative changes in macrofaunal indices with distance from the farm.

Seagrass meadows (Posidonia oceanica) distribution and trajectories of change.

Posidonia oceanica meadows are declining at alarming rates due to climate change and human activities. Although P. oceanica is considered the most important and well-studied seagrass species of the Mediterranean Sea, to date there has been a limited effort to combine all the spatial information available and provide a complete distribution of meadows across the basin. The aim of this work is to provide a fine-scale assessment of (i) the current and historical known distribution of P. oceanica, (ii) the total area of meadows and (iii) the magnitude of regressive phenomena in the last decades. The outcomes showed the current spatial distribution of P. oceanica, covering a known area of 1,224,707 ha, and highlighted the lack of relevant data in part of the basin (21,471 linear km of coastline). The estimated regression of meadows amounted to 34% in the last 50 years, showing that this generalised phenomenon had to be mainly ascribed to cumulative effects of multiple local stressors. Our results highlighted the importance of enforcing surveys to assess the status and prioritize areas where cost-effective schemes for threats reduction, capable of reversing present patterns of change and ensuring P. oceanica persistence at Mediterranean scale, could be implemented.

Seagrass ecosystem response to long-term high CO2 in a Mediterranean volcanic vent.

We examined the long-term effect of naturally acidified water on a Cymodocea nodosa meadow growing at a shallow volcanic CO2 vent in Vulcano Island (Italy). Seagrass and adjacent unvegetated habitats growing at a low pH station (pH = 7.65 ± 0.02) were compared with corresponding habitats at a control station (pH = 8.01 ± 0.01). Density and biomass showed a clear decreasing trend at the low pH station and the below- to above-ground biomass ratio was more than 10 times lower compared to the control. C content and δ(13)C of leaves and epiphytes were significantly lower at the low pH station. Photosynthetic activity of C. nodosa was stimulated by low pH as seen by the significant increase in Chla content of leaves, maximum electron transport rate and compensation irradiance. Seagrass community metabolism was intense at the low pH station, with significantly higher net community production, respiration and gross primary production than the control community, whereas metabolism of the unvegetated community did not differ between stations. Productivity was promoted by the low pH, but this was not translated into biomass, probably due to nutrient limitation, grazing or poor environmental conditions. The results indicate that seagrass response in naturally acidified conditions is dependable upon species and geochemical characteristics of the site and highlight the need for a better understanding of complex interactions in these environments.