Ecosystem service benefits and costs of deep-sea ecosystem restoration.

Deep-sea ecosystems are facing degradation which could have severe consequences for biodiversity and the livelihoods of coastal populations. Ecosystem restoration as a natural based solution has been regarded as a useful means to recover ecosystems. The study provides a social cost-benefit analysis for a proposed project to restore the Dohrn Canyon cold water corals and the deep-sea ecosystem in the Bay of Naples, Italy. By incorporating ecosystem service benefits and uncertainties related to a complex natural-technological-social system surrounding restoration activities, the study demonstrated how to evaluate large-scale ecosystem restoration activities. The results indicate that an ecosystem restoration project can be economic (in terms of welfare improvement) even if the restoration costs are high. Our study shows the uncertainty associated with restoration success rate significantly affects the probability distribution of the expected net present values. Identifying and controlling the underlying factors to improve the restoration successful rate is thus crucial.

The challenge of proving the existence of metazoan life in permanently anoxic deep-sea sediments.

The demonstration of the existence of metazoan life in absence of free oxygen is one of the most fascinating and difficult challenges in biology. Danovaro et al. (2010) discovered three new species of the Phylum Loricifera, living in the anoxic sediments of the L'Atalante, a deep-hypersaline anoxic basin of the Mediterranean Sea. Multiple and independent analyses based on staining, incorporation of radiolabeled substrates, CellTracker Green incorporation experiments and ultra-structure analyses, allowed Danovaro et al. (2010) to conclude that these animals were able to spend their entire life cycle under anoxic conditions. Bernhard et al. (2015) investigated the same basin. Due to technical difficulties in sampling operations, they could not collect samples from the permanently anoxic sediment, and sampled only the redoxcline portion of the L'Atalante basin. They found ten individuals of Loricifera and provided alternative interpretations of the results of Danovaro et al. (2010). Here we analyze these interpretations, and present additional evidence indicating that the Loricifera encountered in the anoxic basin L'Atalante were actually alive at the time of sampling. We also discuss the reliability of different methodologies and approaches in providing evidence of metazoans living in anoxic conditions, paving the way for future investigations.This paper is a response to Bernhard JM, Morrison CR, Pape E, Beaudoin DJ, Todaro MA, Pachiadaki MG, Kormas KAr, Edgcomb VG. 2015. Metazoans of redoxcline sediments in Mediterranean deep-sea hypersaline anoxic basins. BMC Biology 2015 13:105.See research article at http://bmcbiol.biomedcentral.com/articles/10.1186/s12915-015-0213-6.

Effects of seagrass (Cymodocea nodosa) restoration on nematode biodiversity.

Seagrass meadows are hot spots of biodiversity and play a key role in the provisioning of ecosystem goods and services but are often subjected to a regression due to a combination of multiple anthropogenic and climate-induced impacts. The ecological restoration of these habitat-forming species is a priority to reverse biodiversity loss and for the recovery of key ecosystem functions. Here we investigated the effects of seagrass (Cymodocea nodosa) restoration action on benthic biodiversity recovery assessed by a time-series analysis carried out for one year. We used nematode assemblages, the most widespread metazoan on global sediments, as a proxy of benthic biodiversity and compared the species richness, expected species number (ES51) and composition in donor and in restored seagrasses and in the adjacent unvegetated sediments. One year after the intervention, nematode biodiversity in restored seagrasses was more similar to that of the donor site than in unvegetated sediments, suggesting a progressive recovery. Overall, the nematode biodiversity of the restored seagrasses resulted in an intermediate level between unvegetated and pristine seagrass meadows, providing evidence that restoration intervention contributed to biodiversity recovery. Pristine and restored seagrass meadows hosted a high number of exclusive species, which resulted in an increase in the overall biodiversity in the investigated location. Our results indicate that the restoration of seagrass meadows has positive effects on benthic biodiversity and contributes to enhance the local biodiversity.

Bioaccumulation and biomagnification of heavy metals in marine micro-predators.

Nematodes represent >3/5 of the abundance of the world's metazoans and usually account for nearly 90% of the total benthic fauna, playing a key ecological role in the benthic ecosystem functioning on a global scale. These small metazoans include a relevant number of microscopic predators and, in turn, are the most abundant preys of macro-megafauna and fish juveniles thus playing a key role in marine food webs. Here, using two independent approaches, we test the bioaccumulation in marine nematodes of several heavy metals present in contaminated sediments. We report here that nematodes, despite their short life cycle and small size, bioaccumulate significantly heavy metals. Bioaccumulation increases from deposit feeders and microalgal grazers to predators of microbes and other tiny metazoans. These results suggest that nematodes also contribute to their biomagnification along the food webs and can contribute to increase the transfer of contaminants from the sediments to larger organisms.

Impact of resuspended mine tailings on benthic biodiversity and ecosystem processes: The case study of Portmán Bay, Western Mediterranean Sea, Spain.

Industrial seabed mining is expected to cause significant impacts on marine ecosystems, including physical disturbance and the generation of plumes of toxin-laden water. Portmán Bay (NW Mediterranean Sea), where an estimated amount of 60 Mt of mine tailings from sulphide ores were dumped from 1957 to 1990, is one of the most metal-polluted marine areas in Europe and worldwide. This bay can be used to assess the impact on marine ecosystems of particle settling from sediment plumes resulting from mine tailings resuspension. With this purpose in mind, we conducted a field experiment there to investigate subsequent effects of deposition of (artificially resuspended) contaminated sediments on (i) prokaryotic abundance and meiofaunal assemblages (in terms of abundance and diversity), (ii) the availability of trophic resources (in terms of organic matter biochemical composition), and (iii) a set of ecosystem functions including meiofaunal biomass, heterotrophic C production and C degradation rates. The results of this study show that mine tailings resuspension and plume deposition led to the decline of prokaryotic abundance and nematode's biodiversity. The later decreased because of species removal and transfer along with particle resuspension and plume deposition. Such changes were also associated to a decrease of the proteins content in the sediment organic matter, faster C degradation rates and higher prokaryotic C production. Overall, this study highlights that mine tailing resuspension and ensuing particle deposition can have deleterious effects on both prokaryotes and nematode diversity, alter biogeochemical cycles and accelerate C degradation rates. These results should be considered for the assessment of the potential effects of seabed mineral exploitation on marine ecosystems at large.

Effects of Local Acidification on Benthic Communities at Shallow Hydrothermal Vents of the Aeolian Islands (Southern Tyrrhenian, Mediterranean Sea).

The Aeolian Islands (Mediterranean Sea) host a unique hydrothermal system called the "Smoking Land" due to the presence of over 200 volcanic CO2-vents, resulting in water acidification phenomena and the creation of an acidified benthic environment. Here, we report the results of a study conducted at three sites located at ca. 16, 40, and 80 m of depth, and characterized by CO2 emissions to assess the effects of acidification on meio- and macrobenthic assemblages. Acidification caused significant changes in both meio- and macrofaunal assemblages, with a clear decrease in terms of abundance and a shift in community composition. A noticeable reduction in biomass was observed only for macrofauna. The most sensitive meiofaunal taxa were kinorhynchs and turbellarians that disappeared at the CO2 sites, while the abundance of halacarids and ostracods increased, possibly as a result of the larger food availability and the lower predatory pressures by the sensitive meiofaunal and macrofaunal taxa. Sediment acidification also causes the disappearance of more sensitive macrofaunal taxa, such as gastropods, and the increase in tolerant taxa such as oligochaetes. We conclude that the effects of shallow CO2-vents result in the progressive simplification of community structure and biodiversity loss due to the disappearance of the most sensitive meio- and macrofaunal taxa.

Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss.

BACKGROUND: Recent investigations suggest that biodiversity loss might impair the functioning and sustainability of ecosystems. Although deep-sea ecosystems are the most extensive on Earth, represent the largest reservoir of biomass, and host a large proportion of undiscovered biodiversity, the data needed to evaluate the consequences of biodiversity loss on the ocean floor are completely lacking. RESULTS: Here, we present a global-scale study based on 116 deep-sea sites that relates benthic biodiversity to several independent indicators of ecosystem functioning and efficiency. We show that deep-sea ecosystem functioning is exponentially related to deep-sea biodiversity and that ecosystem efficiency is also exponentially linked to functional biodiversity. These results suggest that a higher biodiversity supports higher rates of ecosystem processes and an increased efficiency with which these processes are performed. The exponential relationships presented here, being consistent across a wide range of deep-sea ecosystems, suggest that mutually positive functional interactions (ecological facilitation) can be common in the largest biome of our biosphere. CONCLUSIONS: Our results suggest that a biodiversity loss in deep-sea ecosystems might be associated with exponential reductions of their functions. Because the deep sea plays a key role in ecological and biogeochemical processes at a global scale, this study provides scientific evidence that the conservation of deep-sea biodiversity is a priority for a sustainable functioning of the worlds' oceans.

The first metazoa living in permanently anoxic conditions.

BACKGROUND: Several unicellular organisms (prokaryotes and protozoa) can live under permanently anoxic conditions. Although a few metazoans can survive temporarily in the absence of oxygen, it is believed that multi-cellular organisms cannot spend their entire life cycle without free oxygen. Deep seas include some of the most extreme ecosystems on Earth, such as the deep hypersaline anoxic basins of the Mediterranean Sea. These are permanently anoxic systems inhabited by a huge and partly unexplored microbial biodiversity. RESULTS: During the last ten years three oceanographic expeditions were conducted to search for the presence of living fauna in the sediments of the deep anoxic hypersaline L'Atalante basin (Mediterranean Sea). We report here that the sediments of the L'Atalante basin are inhabited by three species of the animal phylum Loricifera (Spinoloricus nov. sp., Rugiloricus nov. sp. and Pliciloricus nov. sp.) new to science. Using radioactive tracers, biochemical analyses, quantitative X-ray microanalysis and infrared spectroscopy, scanning and transmission electron microscopy observations on ultra-sections, we provide evidence that these organisms are metabolically active and show specific adaptations to the extreme conditions of the deep basin, such as the lack of mitochondria, and a large number of hydrogenosome-like organelles, associated with endosymbiotic prokaryotes. CONCLUSIONS: This is the first evidence of a metazoan life cycle that is spent entirely in permanently anoxic sediments. Our findings allow us also to conclude that these metazoans live under anoxic conditions through an obligate anaerobic metabolism that is similar to that demonstrated so far only for unicellular eukaryotes. The discovery of these life forms opens new perspectives for the study of metazoan life in habitats lacking molecular oxygen.

Impact of historical sulfide mine tailings discharge on meiofaunal assemblages (Portmán Bay, Mediterranean Sea).

Portmán Bay is one of the most contaminated and chronically impacted coastal marine areas of the world. Here, from the 1957 to 1990, about 60 million tons of mine tailings from the processing of sulfide ores were dumped directly at the shoreline. The resulting deposit provides a unique opportunity to assess the impact of mine tailings on coastal marine ecosystems after ca 30 years since the discharge has ceased. We investigated meiofaunal abundance, biomass and biodiversity along a gradient of metal concentration that overlaps with a bathymetric gradient from 30 to 60 m depth. Despite the localized presence of extremely high concentration of metals, the bay was not a biological desert, but, nevertheless, was characterized by evident signs of impact on benthic diversity. Meiofaunal variables increased significantly with decreasing metal contamination, eventually reaching values comparable to other uncontaminated coastal sediments. Our results show that mine tailings influenced the spatial distribution of meiofaunal taxa and nematode species composition. In particular, we report here that the bay was characterized by the dominance of nematode opportunistic species tolerant to high metal concentration. The effects of mine tailing discharge on meiofaunal biodiversity and composition were still evident ca 30 years after the end of the mining activities. Overall, this study provides new insights on the potential impact of mine tailings disposal and metal contamination in coastal sediments, and, can also contribute to predict the potential long-term consequences of ever-expanding deep-sea mining industry on benthic environments.

Ecological assessment of anthropogenic impact in marine ecosystems: The case of Bagnoli Bay.

Pollutants alter marine systems, interfering with provisioning of ecosystem services; understanding their interaction with ecological communities is therefore critical to inform environmental management. Here we propose a joint compositional- and interaction-based analysis for ecological status assessment and apply it on the benthic communities of the Bagnoli Bay. We found that contamination differentially affects the communities' composition in the bay, with prokaryotes influenced only by depth, and benthos not following the environmental gradient at all. This result is confirmed by analyses of the community structure, whose network structure suggest fast carbon flow and cycling, especially promoted by nematodes and polychaetes; the benthic prey/predator biomass ratio, adjusted for competition, successfully synthesise the status of predator taxa. We found demersal fish communities to separate into a deep, pelagic-like community, and two shallow communities where a shift from exclusive predators to omnivores occurs, moving from the most polluted to the least polluted sampling units. Finally, our study indicate that indices based on interspecific interactions are better indicators of environmental gradients than those defined based on species composition exclusively.

Environmental hazard assessment of a marine mine tailings deposit site and potential implications for deep-sea mining.

Portmán Bay is a heavily contaminated area resulting from decades of metal mine tailings disposal, and is considered a suitable shallow-water analogue to investigate the potential ecotoxicological impact of deep-sea mining. Resuspension plumes were artificially created by removing the top layer of the mine tailings deposit by bottom trawling. Mussels were deployed at three sites: i) off the mine tailings deposit area; ii) on the mine tailings deposit beyond the influence from the resuspension plumes; iii) under the influence of the artificially generated resuspension plumes. Surface sediment samples were collected at the same sites for metal analysis and ecotoxicity assessment. Metal concentrations and a battery of biomarkers (oxidative stress, metal exposure, biotransformation and oxidative damage) were measured in different mussel tissues. The environmental hazard posed by the resuspension plumes was investigated by a quantitative weight of evidence (WOE) model that integrated all the data. The resuspension of sediments loaded with metal mine tails demonstrated that chemical contaminants were released by trawling subsequently inducing ecotoxicological impact in mussels' health. Considering as sediment quality guidelines (SQGs) those indicated in Spanish action level B for the disposal of dredged material at sea, the WOE model indicates that the hazard is slight off the mine tailings deposit, moderate on the mine tailings deposit without the influence from the resuspension plumes, and major under the influence of the resuspension plumes. Portmán Bay mine tailings deposit is a by-product of sulphide mining, and despite differences in environmental setting, it can reflect the potential ecotoxic effects to marine fauna from the impact of resuspension of plumes created by deep-sea mining of polymetallic sulphides. A similar approach as in this study could be applied in other areas affected by sediment resuspension and for testing future deep-sea mining sites in order to assess the associated environmental hazards.

A submarine volcanic eruption leads to a novel microbial habitat.

Submarine volcanic eruptions are major catastrophic events that allow investigation of the colonization mechanisms of newly formed seabed. We explored the seafloor after the eruption of the Tagoro submarine volcano off El Hierro Island, Canary Archipelago. Near the summit of the volcanic cone, at about 130 m depth, we found massive mats of long, white filaments that we named Venus's hair. Microscopic and molecular analyses revealed that these filaments are made of bacterial trichomes enveloped within a sheath and colonized by epibiotic bacteria. Metagenomic analyses of the filaments identified a new genus and species of the order Thiotrichales, Thiolava veneris. Venus's hair shows an unprecedented array of metabolic pathways, spanning from the exploitation of organic and inorganic carbon released by volcanic degassing to the uptake of sulfur and nitrogen compounds. This unique metabolic plasticity provides key competitive advantages for the colonization of the new habitat created by the submarine eruption. A specialized and highly diverse food web thrives on the complex three-dimensional habitat formed by these microorganisms, providing evidence that Venus's hair can drive the restart of biological systems after submarine volcanic eruptions.

Corrigendum: A submarine volcanic eruption leads to a novel microbial habitat.

This corrects the article DOI: 10.1038/s41559-017-0144.

Effects of antifouling booster biocide Irgarol 1051 on the structure of free living nematodes: a laboratory experiment.

A mesocosm experiment was conducted to evaluate the effects of Irgarol on nematode diversity, composition and trophic structure. Sediment samples were experimentally contaminated using four increasing Irgarol concentrations [I1 (11.5 ng g(-1)), I2 (35 ng g(-1)), I3 (105 ng g(-1)) and I4 (315 ng g(-1))] and compared to non-contaminated sediments (controls). Nematode diversity as the number of nematodes species (S) and species richness (d) was significantly lower in all Irgarol treatments than in the controls while the evenness (J') increased significantly in I4 treated mesocosms. The nematode species composition significantly changed following Irgarol concentrations. Paracomesoma dubiun and Terschellingia longicaudata appeared as "tolerant" species to the highest Irgarol concentration. Additionally, Chromadorina germanica and Microlaimus cyatholaimoides appeared as "opportunistic" species. In contrast, Daptonema normandicum seemed to be a "sensitive" species to Irgarol contamination. Irgarol modified also the nematode trophic structure where the relative abundance of deposit feeders decreased significantly in all the treatments compared to control mesocosms and optional predators decreased only in treated mesocosms with I3. Epigrowth feeders increased significantly in treated mesocosms with I3 and I4 and the microvores increased with I1 and decreased with I4. The relative abundance of ciliate consumers appeared unaffected by the presence of Irgarol contamination. Our results open new perspectives on the potential impact of antifouling booster biocide Irgarol 1051 on nematode biodiversity and functional diversity as trophic structures.

Relationships between meiofaunal biodiversity and prokaryotic heterotrophic production in different tropical habitats and oceanic regions.

Tropical marine ecosystems are among the most diverse of the world oceans, so that assessing the linkages between biodiversity and ecosystem functions (BEF) is a crucial step to predict consequences of biodiversity loss. Most BEF studies in marine ecosystems have been carried out on macrobenthic diversity, whereas the influence of the meiofauna on ecosystem functioning has received much less attention. We compared meiofaunal and nematode biodiversity and prokaryotic heterotrophic production across seagrass, mangrove and reef sediments in the Caribbean, Celebes and Red Seas. For all variables we report the presence of differences among habitats within the same region, and among regions within the same habitat. In all regions, the richness of meiofaunal taxa in reef and seagrass sediments is higher than in mangrove sediments. The sediments of the Celebes Sea show the highest meiofaunal biodiversity. The composition of meiofaunal assemblages varies significantly among habitats in the same region. The nematode beta diversity among habitats within the same region is higher than the beta diversity among regions. Although one site per habitat was considered in each region, these results suggest that the composition of meiofaunal assemblages varies primarily among biogeographic regions, whereas the composition of nematode assemblages varies more considerably among habitats. Meiofauna and nematode biodiversity and prokaryotic heterotrophic production, even after the removal of covariate effects linked with longitude and the quantity and nutritional quality of organic matter, are positively and linearly linked both across regions and within each habitat type. Our results confirm that meiofauna and nematode biodiversity may influence benthic prokaryotic activity, which, in turn, implies that diversity loss could have negative impacts on ecosystem functioning in these systems.

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 systems.

Deep-sea biodiversity in the Mediterranean Sea: the known, the unknown, and the unknowable.

Deep-sea ecosystems represent the largest biome of the global biosphere, but knowledge of their biodiversity is still scant. The Mediterranean basin has been proposed as a hot spot of terrestrial and coastal marine biodiversity but has been supposed to be impoverished of deep-sea species richness. We summarized all available information on benthic biodiversity (Prokaryotes, Foraminifera, Meiofauna, Macrofauna, and Megafauna) in different deep-sea ecosystems of the Mediterranean Sea (200 to more than 4,000 m depth), including open slopes, deep basins, canyons, cold seeps, seamounts, deep-water corals and deep-hypersaline anoxic basins and analyzed overall longitudinal and bathymetric patterns. We show that in contrast to what was expected from the sharp decrease in organic carbon fluxes and reduced faunal abundance, the deep-sea biodiversity of both the eastern and the western basins of the Mediterranean Sea is similarly high. All of the biodiversity components, except Bacteria and Archaea, displayed a decreasing pattern with increasing water depth, but to a different extent for each component. Unlike patterns observed for faunal abundance, highest negative values of the slopes of the biodiversity patterns were observed for Meiofauna, followed by Macrofauna and Megafauna. Comparison of the biodiversity associated with open slopes, deep basins, canyons, and deep-water corals showed that the deep basins were the least diverse. Rarefaction curves allowed us to estimate the expected number of species for each benthic component in different bathymetric ranges. A large fraction of exclusive species was associated with each specific habitat or ecosystem. Thus, each deep-sea ecosystem contributes significantly to overall biodiversity. From theoretical extrapolations we estimate that the overall deep-sea Mediterranean biodiversity (excluding prokaryotes) reaches approximately 2805 species of which about 66% is still undiscovered. Among the biotic components investigated (Prokaryotes excluded), most of the unknown species are within the phylum Nematoda, followed by Foraminifera, but an important fraction of macrofaunal and megafaunal species also remains unknown. Data reported here provide new insights into the patterns of biodiversity in the deep-sea Mediterranean and new clues for future investigations aimed at identifying the factors controlling and threatening deep-sea biodiversity.