Biodiversity loss and turnover in alternative states in the Mediterranean Sea: a case study on meiofauna

In the Mediterranean Sea hard-bottom macroalgal meadows may switch to alternative and less-productive barrens grounds, as a result of sea urchins overgrazing. Meiofauna (and especially nematodes) represent key components of benthic ecosystems, are highly-diversified, sensitive to environmental change and anthropogenic impacts, but, so-far, have been neglected in studies on regime shifts. We report here that sedimentary organic matter contents, meiofaunal taxa richness and community composition, nematode α- and β-biodiversity vary significantly between alternative macroalgal and barren states. The observed differences are consistent in six areas spread across the Mediterranean Sea, irrespective of barren extent. Our results suggest also that the low biodiversity levels in barren states are the result of habitat loss/fragmentation, which is associated also with a lower availability of trophic resources. Furthermore, differences in meiofaunal and nematode abundance, biomass and diversity between macroalgal meadow and barren states persist when the latter is not fully formed, or consists of patches interspersed in macroalgal meadows. Since barren grounds are expanding rapidly along the Mediterranean Sea and meiofauna are a key trophic component in marine ecosystems, we suggest that the extension and persistence of barrens at the expenses of macroalgal meadows could also affect resilience of higher trophic level

Potentially combined effect of the invasive seaweed Caulerpa cylindracea (Sonder) and sediment deposition rates on organic matter and meiofaunal assemblages

The seaweed Caulerpa cylindracea (Sonder) is one of the most successful marine bioinvaders worldwide. Caulerpa cylindracea can influence the quantity and biochemical composition of sedimentary organic matter (OM). However, it is still unknown if the effects of C. cylindracea on both OM and small metazoans (i.e. meiofauna) can change according to different sediment deposition rates. To provide insights on this, we investigated the biochemical composition of sediments along with the abundance and composition of meiofaunal assemblages in sediments colonized and not-colonized by the seaweed C. cylindracea under different regimes of sediment deposition. Our results show that the presence of the invasive alga C. cylindracea could alter quantity, biochemical composition, and nutritional quality of organic detritus and influence the overall functioning of the benthic system, but also that the observed effects could be context-dependent. In particular, we show that the presence of C. cylindracea could have a positive effect on meiofaunal abundance wherever the sediment deposition rates are low, whereas the contextual presence of high to medium sedimentation rates can provoke an accumulation of sedimentary organic matter, less favourable bioavailability of food for the benthos, and consequent negative effects on meiofauna

Nematode biodiversity and benthic trophic state are simple tools for the assessment of the environmental quality in coastal marine ecosystems

A high biodiversity is essential to guarantee the stability and functioning of coastal marine ecosystems. In this perspective, the Marine Strategy Framework Directive provides prescriptions to maintain (or restore) marine biodiversity in order to achieve a Good Environmental Status (GES). Eutrophic conditions - as determined by the accumulation of sedimentary organic matter (OM) – are often associated with biodiversity loss, so that eutrophic conditions are often considered a pre-requisite or a proxy for degraded ecological conditions. The aim of this study was to investigate the feasibility of the combined use of benthic trophic status and nematode biodiversity as integrated indicators of the environmental status of marine coastal ecosystems. To achieve this objective, we investigated nematode species diversity and assemblage composition in three areas of the Adriatic Sea, characterised by different OM quantity and biochemical composition (as proxy of sedimentary trophic status) and affected by different levels of anthropogenic impact. We show that, on the basis of OM quantity and biochemical composition, the investigated sites can be classified from oligo- to meso-trophic, whereas the analysis of nematode biodiversity indicates that the ecological quality status (EQS) ranged from bad to moderately impacted. This result provides evidence that trophic status and environmental quality assessments are not interchangeable tools for the assessment of marine ecosystems EQS. Rather they should be considered as complementary proxies for the overall assessment of the (good) ecological status. Data reported here also indicate that the loss of benthic biodiversity, whatever the source of disturbance, may be associated to a decrease of the functional diversity (either as feeding and life strategies traits), which might have important consequences on ecosystems functioning. Our results suggest that the GES cannot be defined uniquely in terms of sedimentary trophic status, especially when many other multiples stressors can contribute to determine the overall environmental quality of the investigated ecosystems. Nematode biodiversity is highly sensitive to differences in ecological conditions at different spatial and temporal scales and it can provide reliable and complementary information for the assessment of the environmental status in marine coastal sediments

Combining passive and active restoration to rehabilitate a historically polluted marine site

IntroductionPassive and active restoration approaches have been often considered as different alternatives to achieve the ecological restoration of a degraded site. This false dichotomy has been overcome in terrestrial ecosystems, for which a range of restoration approaches have often been applied within the same restoration project, creating a continuum of interventions. In the marine environment, the combined approach based on passive and active restoration is less studied.MethodsHere, we tested the possibility of actively restoring a macroalgal population in a historically polluted industrial site, subjected to decadal passive restoration (i.e., unassisted, or spontaneous recovery following cessation of industrial activity), in the Mediterranean Sea. Recently, it has been demonstrated that in the site under scrutiny, there is no longer any sign of the historical contamination or impact on benthic fauna therefore the environmental conditions are indistinguishable from surrounding non-impacted areas. We used artificial breakwater barriers already present in the site to restore a population of the brown algae Gongolaria barbata. The intervention was conducted by applying an in situ recruitment approach and a complementary action using cages to exclude the herbivores. The G. barbata recruits were transplanted on the artificial reefs and after they reached the maximum growth inside the cages, one cage was opened and another one was completely removed to also test the grazing pressure. The associated benthic assemblages were also analysed in terms of meio- and macrofaunal abundance, the richness of taxa, and taxonomic composition.Results and discussionOur results indicate that, at least over a relatively short period (i.e., 6 months), the use of the cages represents a useful tool to let the macroalgae grow enough to counterbalance the herbivory pressure. The associated fauna below the macroalgae was characterized by a different taxonomic composition when compared to controls (i.e., artificial reefs without the macroalgae), particularly when considered the rare taxa. In conclusion, the combination of passive and active restoration can be considered a useful approach to restore marine sites degraded by historical industrial activities

Fish-farm impact on metazoan meiofauna in the Mediterranean Sea: Analysis of regional vs. habitat effects.

The worldwide exponential growth of off-shore mariculture is raising severe concerns about the impacts of this industry on marine habitats and their biodiversity. We investigated the metazoan meiofaunal response to fish-farm impact in four regions of the Mediterranean Sea. Meiofaunal assemblages were investigated in two habitats (seagrass meadows of Posidonia oceanica and non-vegetated soft bottoms) comparing sites receiving faeces and uneaten food pellets from fish farms to control sites. We report here that, consistently across different regions, the meiofaunal abundance typically responded positively to fish-farm effluents. Biodeposition caused also significant changes in assemblage structure and the reduction in the richness of higher meiofaunal taxa, but the multivariate analysis of variance revealed that the effects were region- and habitat-specific. In non-vegetated systems, three of the four regions investigated displayed significant effects of the fish farms on richness of meiofaunal taxa. In vegetated habitats, meiofauna did not respond to biodeposition (except in one region), suggesting that seagrass meadows can mask the effects of fish-farm effluents on benthic biodiversity. We conclude that different indicators of fish-farm impact are needed in vegetated and non-vegetated benthic system

Macroalgal forest restoration: the effect of the foundation species

IntroductionActive restoration is the strategy needed to trigger or accelerate the recovery of degraded marine habitats, which provide the goods and services essential for preserving biodiversity and human wellbeing. Ecosystem engineers are generally the target species in the ecological restoration of marine ecosystems, and large-sized brown macroalgae (e.g., the Cystoseira complex) are a priority due to their crucial ecological importance and vulnerability in many regions of the Mediterranean Sea. MethodsHere, we present the results of a successful intervention of ecological restoration of Gongolaria barbata. Results and DiscussionOne year after the restoration intervention, we observed the recovery of the canopy in terms of ca. 15m2 with a significant increase in faunal abundance and biodiversity compared with reference areas. However, despite the high restored macroalgal growth rates, the assemblage structure was still significantly different from that of reference pristine areas. Despite the fast faunal colonization of a new 3D habitat linked to the successful re-introduction of the ecosystem engineers (i.e., macroalgae), the complete restoration of the properties of a habitat can be a much longer process. We conclude that, after 1 year, active restoration of macroalgal forests still results in a partial recovery of ecosystem functions (i.e., rehabilitation) rather than a full ecosystem restoration, thus stressing the need for long-term monitoring of restoration interventions

Denitrification, Nitrogen Uptake, and Organic Matter Quality Undergo Different Seasonality in Sandy and Muddy Sediments of a Turbid Estuary

The interaction between microbial communities and benthic algae as nitrogen (N) regulators in poorly illuminated sediments is scarcely investigated in the literature. The role of sediments as sources or sinks of N was analyzed in spring and summer in sandy and muddy sediments in a turbid freshwater estuary, the Curonian Lagoon, Lithuania. Seasonality in this ecosystem is strongly marked by phytoplankton community succession with diatoms dominating in spring and cyanobacteria dominating in summer. Fluxes of dissolved gas and inorganic N and rates of denitrification of water column nitrate (Dw) and of nitrate produced by nitrification (Dn) and sedimentary features, including the macromolecular quality of organic matter (OM), were measured. Shallow/sandy sites had benthic diatoms, while at deep/muddy sites, settled pelagic microalgae were found. The OM in surface sediments was always higher at muddy than at sandy sites, and biochemical analyses revealed that at muddy sites the OM nutritional value changed seasonally. In spring, sandy sediments were net autotrophic and retained N, while muddy sediments were net heterotrophic and displayed higher rates of denitrification, mostly sustained by Dw. In summer, benthic oxygen demand increased dramatically, whereas denitrification, mostly sustained by Dn, decreased in muddy and remained unchanged in sandy sediments. The ratio between denitrification and oxygen demand was significantly lower in sandy compared with muddy sediments and in summer compared with spring. Muddy sediments displayed seasonally distinct biochemical composition with a larger fraction of lipids coinciding with cyanobacteria blooms and a seasonal switch from inorganic N sink to source. Sandy sediments had similar composition in both seasons and retained inorganic N also in summer. Nitrogen uptake by microphytobenthos at sandy sites always exceeded the amount loss via denitrification, and benthic diatoms appeared to inhibit denitrification, even in the dark and under conditions of elevated N availability. In spring, denitrification attenuated N delivery from the estuary to the coastal area by nearly 35%. In summer, denitrification was comparable (~100%) with the much lower N export from the watershed, but N loss was probably offset by large rates of N-fixation

Microbiome-assisted restoration of degraded marine habitats: a new nature-based solution?

Microorganisms interact with all biological components in a variety of ways. They contribute to increase the efficiency of marine food webs and facilitate the adaptation of multicellular organisms to climate change and other human-induced impacts. Increasing evidence suggests that microbiomes are essential for the health of marine species, for maintaining productive marine ecosystems, and thus for the sustainable functioning of the global biosphere. Marine microbiomes are typically species- or habitat-specific and are susceptible to environmental and human-driven changes. The microbiota of seagrasses, macroalgae, mangroves or tropical corals benefits their hosts by increasing their fitness, contributing to the removal of toxic compounds, conferring protection against pathogens, and/or supporting nutrient requirements. Alterations of the microbiomes might have negative consequences on species’ health, survival, and overall ecosystem functioning. Despite the key ecological role of microbiomes in all ecosystems, their potential for the restoration of degraded habitats is still largely unexplored. Here we present a literature survey of the existing information on the microbiota associated with habitat-forming species and suggest that the resilience/recovery of damaged marine habitats can depend largely on the changes in the microbiota. Nature-based solutions relying on microbiome analyses (also through omics approaches) enable health monitoring of transplanted organisms/metacommunities and potential identification/production of probiotics/bio-promoters to stabilize unhealthy conditions of transplants. In the context of international strategies concerning ecological restoration, the use of the scientific knowledge acquired on the marine microbiome deserves to be exploited to assist both traditional and innovative restoration approaches. The success of habitat restoration may depend on our ability to maintain, along with the restored species and habitats, a functional microbiota

The paradox of an unpolluted coastal site facing a chronically contaminated industrial area

Present and past industrial activities in coastal areas have left us a legacy of contamination and habitat degradation with potential implications for human health. Here, we investigated a coastal marine area enclosed in a Site of National Interest (SNI) of the central-western Adriatic (Mediterranean Sea), where priority actions of environmental remediation are required by governmental laws due the high environmental and human risk, and that is off-limits to any human activity since 2002. In particular, our investigation was focused on an area located in front of a chemical industry dismissed more than 3 decades ago. We report that the concentrations of heavy-metal and organic contaminants in the investigated sediments were generally lower than those expected to induce detrimental biological effects. Meiofaunal abundance, biomass and community structure changed among stations, but regardless of the distance from the abandoned industrial plant. Taxa richness within the SNI did not change significantly compared to the controls and the lack of some taxa in the SNI transects was not due to the contamination of the SNI area. The results of this study suggest a natural recovery of the marine area over 2 decades of restrictions on human activities, including fishing and shipping bans. If the hypothesis of the natural recovery of this SNI will be further confirmed by other studies, the plans forthe identification and monitoring of the most polluted areas in Italy should necessarily be redefined also in the light of the Water Framework, the Marine Strategy Framework and the Environmental Quality Standard Directives

Identifying priorities for the protection of deep Mediterranean Sea ecosystems through an integrated approach

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fanelli, E., Bianchelli, S., Foglini, F., Canals, M., Castellan, G., Guell-Bujons, Q., Galil, B., Goren, M., Evans, J., Fabri, M.-C., Vaz, S., Ciuffardi, T., Schembri, P. J., Angeletti, L., Taviani, M., & Danovaro, R. Identifying priorities for the protection of deep Mediterranean Sea ecosystems through an integrated approach. Frontiers in Marine Science, 8, (2021): 698890, https://doi.org/10.3389/fmars.2021.698890.Benthic habitats of the deep Mediterranean Sea and the biodiversity they host are increasingly jeopardized by increasing human pressures, both direct and indirect, which encompass fisheries, chemical and acoustic pollution, littering, oil and gas exploration and production and marine infrastructures (i.e., cable and pipeline laying), and bioprospecting. To this, is added the pervasive and growing effects of human-induced perturbations of the climate system. International frameworks provide foundations for the protection of deep-sea ecosystems, but the lack of standardized criteria for the identification of areas deserving protection, insufficient legislative instruments and poor implementation hinder an efficient set up in practical terms. Here, we discuss the international legal frameworks and management measures in relation to the status of habitats and key species in the deep Mediterranean Basin. By comparing the results of a multi-criteria decision analysis (MCDA) and of expert evaluation (EE), we identify priority deep-sea areas for conservation and select five criteria for the designation of future protected areas in the deep Mediterranean Sea. Our results indicate that areas (1) with high ecological relevance (e.g., hosting endemic and locally endangered species and rare habitats),(2) ensuring shelf-slope connectivity (e.g., submarine canyons), and (3) subject to current and foreseeable intense anthropogenic impacts, should be prioritized for conservation. The results presented here provide an ecosystem-based conservation strategy for designating priority areas for protection in the deep Mediterranean Sea.This study was supported by the DG ENV project IDEM (Implementation of the MSFD to the Deep Mediterranean Sea; contract EU No. 11.0661/2017/750680/SUB/EN V.C2). MC and QG-B acknowledge support from Generalitat de Catalunya autonomous government through its funding scheme to excellence research groups (Grant 2017 SGR 315)