Nélia C. Mestre

Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies

Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

Ecotoxicological impact of engineered nanomaterials in bivalve molluscs: An overview

The increasing production and application of engineered nanomaterials (ENMs) in consumer products over the past decade will inevitably lead to their release into aquatic systems and thereby cause the exposure to aquatic organisms, resulting in growing environmental and human health concern. Since bivalves are widely used in the monitoring of aquatic pollution, the aim of this review was to compile and analyse data concerning the ecotoxicity of ENMs using bivalve molluscs. The state of the art regarding the experimental approach, characterization, behaviour, fate, bioaccumulation, tissue and subcellular distribution and mechanisms of toxicity of ENMs in marine and freshwater bivalve molluscs is summarized to achieve a new insight into the mode of action of these nanoparticles in invertebrate organisms. This review shows that the studies about the toxic effects of ENMs in bivalves were conducted mainly with seawater species compared to freshwater ones and that the genus Mytilus is the main taxa used as a model system. There is no standardization of experimental approaches for toxicity testing and reviewed data indicate the need to develop standard protocols for ENMs ecotoxicological testing. In general, the main organ for ENM accumulation is the digestive gland and their cellular fate differs according to nano-specific properties, experimental conditions and bivalve species. Endosomal-lysosomal system and mitochondria are the major cellular targets of ENMs. Metal based ENMs mode of action is related mainly to the dissolution and/or release of the chemical component of the particle inducing immunotoxicity, oxidative stress and cellular injury to proteins, membrane and DNA damage. This review indicates that the aquatic environment is the potential ultimate fate for ENMs and confirms that bivalve molluscs are key model species for monitoring aquatic pollution by ENMs.

Estimating dispersal distance in the deep sea: challenges and applications to marine reserves

Population connectivity refers to the exchange of individuals among populations: it affects gene flow, regulates population size and function, and mitigates recovery from natural or anthropogenic disturbances. Many populations in the deep sea are spatially fragmented, and will become more so with increasing resource exploitation. Understanding population connectivity is critical for spatial management. For most benthic species, connectivity is achieved by the planktonic larval stage, and larval dispersal is, in turn, regulated by complex interactions between biological and oceanographic processes. Coupled biophysical models, incorporating ocean circulation and biological traits, such as planktonic larval duration (PLD), have been used to estimate population connectivity and generate spatial management plans in coastal and shallow waters. In the deep sea, knowledge gaps in both the physical and biological components are delaying the effective use of this approach. Here, we review the current efforts in conservation in the deep sea and evaluate (1) the relevance of using larval dispersal in the design of marine protected areas and (2) the application of biophysical models in the study of population connectivity. Within biophysical models, PLD can be used to estimate dispersal distance. We propose that a PLD that guarantees a minimum dispersal distance for a wide range of species should be used in the planning of marine protected areas in the deep sea. Based on a review of data on species found at depths > 200 m, a PLD of 35 and 69 days ensures a minimum distance for 50% and 75%, respectively, of eurybathic and deep-sea species. We note that more data are required to enhance accuracy and address the high variability in PLD between and within taxonomic groups, limiting generalizations that are often appealing to decision-makers. Given the imminent expansion of resource exploitation in the deep sea, data relevant to spatial management are needed urgently.

Environmental Impacts of the Deep-Water Oil and Gas Industry: A Review to Guide Management Strategies

The industrialization of the deep sea is expanding worldwide. Expanding oil and gas exploration activities in the absence of sufficient baseline data in these ecosystems has made environmental management challenging. Here, we review the types of activities that are associated with global offshore oil and gas development in water depths over 200 m, the typical impacts of these activities, some of the more extreme impacts of accidental oil and gas releases, and the current state of management in the major regions of offshore industrial activity including 18 exclusive economic zones. Direct impacts of infrastructure installation, including sediment resuspension and burial by seafloor anchors and pipelines, are typically restricted to a radius of approximately 100 m on from the installation on the seafloor. Discharges of water-based and low-toxicity oil-based drilling muds and produced water can extend over 2 km, while the ecological impacts at the population and community levels on the seafloor are most commonly on the order of 200-300 m from their source. These impacts may persist in the deep sea for many years and likely longer for its more fragile ecosystems, such as cold-water corals. This synthesis of information provides the basis for a series of recommendations for the management of offshore oil and gas development. An effective management strategy, aimed at minimizing risk of significant environmental harm, will typically encompass regulations of the activity itself (e.g. discharge practices, materials used), combined with spatial (e.g. avoidance rules and marine protected areas) and temporal measures (e.g. restricted activities during peak reproductive periods). Spatial management measures that encompass representatives of all of the regional deep-sea community types is important in this context. Implementation of these management strategies should consider minimum buffer zones to displace industrial activity beyond the range of typical impacts: at least 2 km from any discharge points and surface infrastructure and 200 m from seafloor infrastructure with no expected discharges. Although managing natural resources is, arguably, more challenging in deep-water environments, inclusion of these proven conservation tools contributes to robust environmental management strategies for oil and gas extraction in the deep sea.

The ocean is not deep enough: pressure tolerances during early ontogeny of the blue mussel Mytilus edulis

Early ontogenetic adaptations reflect the evolutionary history of a species. To understand the evolution of the deep-sea fauna and its adaptation to high pressure, it is important to know the effects of pressure on their shallow-water relatives. In this study we analyse the temperature and pressure tolerances of early life-history stages of the shallow-water species Mytilus edulis. This species expresses a close phylogenetic relationship with hydrothermal-vent mussels of the subfamily Bathymodiolinae. Tolerances to pressure and temperature are defined in terms of fertilization success and embryo developmental rates in laboratory-based experiments. In M. edulis, successful fertilization under pressure is possible up to 500u200aatm (50.66u200aMPa), at 10, 15 and 20°C. A slower embryonic development is observed with decreasing temperature and with increasing pressure; principally, pressure narrows the physiological tolerance window in different ontogenetic stages of M. edulis, and slows down metabolism. This study provides important clues on possible evolutionary pathways of hydrothermal vent and cold-seep bivalve species and their shallow-water relatives. Evolution and speciation patterns of species derive mostly from their ability to adapt to variable environmental conditions, within environmental constraints, which promote morphological and genetic variability, often differently for each life-history stage. The present results support the view that a direct colonization of deep-water hydrothermal vent environments by a cold eurythermal shallow-water ancestor is indeed a possible scenario for the Mytilinae, challenging previous hypothesis of a wood/bone to seep/vent colonization pathway.

Resilience of benthic deep-sea fauna to mining activities

With increasing demand for mineral resources, extraction of polymetallic sulphides at hydrothermal vents, cobalt-rich ferromanganese crusts at seamounts, and polymetallic nodules on abyssal plains may be imminent. Here, we shortly introduce ecosystem characteristics of mining areas, report on recent mining developments, and identify potential stress and disturbances created by mining. We analyze species potential resistance to future mining and perform meta-analyses on population density and diversity recovery after disturbances most similar to mining: volcanic eruptions at vents, fisheries on seamounts, and experiments that mimic nodule mining on abyssal plains. We report wide variation in recovery rates among taxa, size, and mobility of fauna. While densities and diversities of some taxa can recover to or even exceed pre-disturbance levels, community composition remains affected after decades. The loss of hard substrata or alteration of substrata composition may cause substantial community shifts that persist over geological timescales at mined sites.

Microplastics effects in Scrobicularia plana

One of the most common plastics in the marine environment is polystyrene (PS) that can be broken down to micro sized particles. Marine organisms are vulnerable to the exposure to microplastics. This study assesses the effects of PS microplastics in tissues of the clam Scrobicularia plana. Clams were exposed to 1mgL-1 (20μm) for 14days, followed by 7days of depuration. A qualitative analysis by infrared spectroscopy in diffuse reflectance mode period detected the presence of microplastics in clam tissues upon exposure, which were not eliminated after depuration. The effects of microplastics were assessed by a battery of biomarkers and results revealed that microplastics induce effects on antioxidant capacity, DNA damage, neurotoxicity and oxidative damage. S. plana is a significant target to assess the environmental risk of PS microplastics.

Environmental behaviour and ecotoxicity of quantum dots at various trophic levels: A review

Despite the wide application of quantum dots (QDs) in electronics, pharmacy and nanomedicine, limited data is available on their environmental health risk. To advance our current understanding of the environmental impact of these engineered nanomaterials, the aim of this review is to give a detailed insight on the existing information concerning the behaviour, transformation and fate of QDs in the aquatic environment, as well as on its mode of action (MoA), ecotoxicity, trophic transfer and biomagnification at various trophic levels (micro-organisms, aquatic invertebrates and vertebrates). Data show that several types of Cd-based QDs, even at low concentrations (<mgCdL-1), induce different toxic effects compared to their dissolved counterpart, indicating nano-specific ecotoxicity. QD ecotoxicity at different trophic levels is highly dependent on its physico-chemical properties, environmental conditions, concentration and exposure time, as well as, species, while UV irradiation increases its toxicity. The state of the art regarding the MoA of QDs according to taxonomic groups is summarised and illustrated. Accumulation and trophic transfer of QDs was observed in freshwater and seawater species, while limited biomagnification and detoxification processes were detected. Finally, current knowledge gaps are discussed and recommendations for future research identified. Overall, the knowledge available indicates that in order to develop sustainable nanotechnologies there is an urgent need to develop Cd-free QDs and new core-shell-conjugate QD structures.

Tissue specific responses to cadmium-based quantum dots in the marine mussel Mytilus galloprovincialis.

In recent years, Cd-based quantum dots (QDs) have generated interest from the life sciences community due to their potential applications in nanomedicine, biology and electronics. However, these engineered nanomaterials can be released into the marine environment, where their environmental health hazards remain unclear. This study investigated the tissue-specific responses related to alterations in the antioxidant defense system induced by CdTe QDs, in comparison with its dissolved counterpart, using the marine mussel Mytilus galloprovincialis. Mussels were exposed to CdTe QDs and dissolved Cd for 14 days at 10 μgCd L(-1) and biomarkers of oxidative stress [superoxide dismutase (SOD), catalase (CAT), glutathione peroxidases (total, Se-independent and Se-dependent GPx) and glutathione-S-transferase (GST) activities] were analyzed along with Cd accumulation in the gills and digestive gland of mussels. Results show that both Cd forms changed mussels antioxidant responses with distinct modes of action (MoA). There were tissue- and time-dependent differences in the biochemical responses to each Cd form, wherein QDs are more pro-oxidant when compared to dissolved Cd. The gills are the main tissue affected by QDs, with effects related to the increase of SOD, GST and GPx activities, while those of dissolved Cd was associated to the increase of CAT activity, Cd accumulation and exposure time. Digestive gland is a main tissue for accumulation of both Cd forms, but changes in antioxidant enzyme activities are smaller than in gills. A multivariate analysis revealed that the antioxidant patterns are tissue dependent, indicating nano-specific effects possibly associated to oxidative stress and changes in redox homeostasis.

Sustained hydrostatic pressure tolerance of the shallow water shrimp Palaemonetes varians at different temperatures: insights into the colonisation of the deep sea.

We investigated the tolerance of adult specimens of the shallow-water shrimp Palaemonetes varians to sustained high hydrostatic pressure (10 MPa) across its thermal tolerance window (from 5 to 27 °C) using both behavioural (survival and activity) and molecular (hsp70 gene expression) approaches. To our knowledge, this paper reports the longest elevated hydrostatic pressure exposures ever performed on a shallow-water marine organism. Behavioural analysis showed a 100% survival rate of P. varians after 7 days at 10 MPa and 5 or 10 °C, whilst cannibalism was observed at elevated temperature (27 °C), suggesting no impairment of specific dynamic action. A significant interaction of pressure and temperature was observed for both behavioural and molecular responses. Elevated pressure was found to exacerbate the effect of temperature on the behaviour of the animals by reducing activity at low temperature and by increasing activity at high temperature. In contrast, only high pressure combined with low temperature increased the expression of hsp70 genes. We suggest that the impressive tolerance of P. varians to sustained elevated pressure may reflect the physiological capability of an ancestral species to colonise the deep sea. Our results also support the hypothesis that deep-sea colonisation may have occurred during geological periods of time when the oceanic water column was warm and vertically homogenous.