Exploring ecosystem-based management in the North Atlantic.

The United States, the EU and Canada established a trilateral working group on the ecosystem approach to ocean health and stressors under the Atlantic Ocean Research Alliance. Recognizing the Atlantic Ocean as a shared resource and responsibility, the working group sought to advance understanding of the Atlantic Ocean and its dynamic systems to improve ocean health, enhance ocean stewardship and promote the sustainable use and management of its resources. This included consideration of multiple ocean-use sectors such as fishing, shipping, tourism and offshore energy. The working group met for 4 years and worked through eight steps that covered the development of common language as a basis for collaboration, challenges of stakeholder engagement, review of the governance mandates, exploring the links between sectors and ecosystems effects, identifying gaps in knowledge and uptake of science, identification of tools for ecosystem-based management, customary best practice for tool development and communication of key research priorities. The key findings were that ecosystem-based management enables new benefits and opportunities, and that we need to make the business case. Further findings were that adequate mandates and effective tools exist for ecosystem-based management, and that ecosystem-based management urgently requires integration of human dimensions, so we must diversify the conversation. In addition, it was found that stakeholders do not see their stake in ecosystem-based management, so greater engagement with stakeholders and targeting of ocean literacy is required and a sustainable future requires a sustained investment in ecosystem-based management, so long-term commitment is key.

Climate-induced changes in the suitable habitat of cold-water corals and commercially important deep-sea fishes in the North Atlantic.

The deep sea plays a critical role in global climate regulation through uptake and storage of heat and carbon dioxide. However, this regulating service causes warming, acidification and deoxygenation of deep waters, leading to decreased food availability at the seafloor. These changes and their projections are likely to affect productivity, biodiversity and distributions of deep-sea fauna, thereby compromising key ecosystem services. Understanding how climate change can lead to shifts in deep-sea species distributions is critically important in developing management measures. We used environmental niche modelling along with the best available species occurrence data and environmental parameters to model habitat suitability for key cold-water coral and commercially important deep-sea fish species under present-day (1951-2000) environmental conditions and to project changes under severe, high emissions future (2081-2100) climate projections (RCP8.5 scenario) for the North Atlantic Ocean. Our models projected a decrease of 28%-100% in suitable habitat for cold-water corals and a shift in suitable habitat for deep-sea fishes of 2.0°-9.9° towards higher latitudes. The largest reductions in suitable habitat were projected for the scleractinian coral Lophelia pertusa and the octocoral Paragorgia arborea, with declines of at least 79% and 99% respectively. We projected the expansion of suitable habitat by 2100 only for the fishes Helicolenus dactylopterus and Sebastes mentella (20%-30%), mostly through northern latitudinal range expansion. Our results projected limited climate refugia locations in the North Atlantic by 2100 for scleractinian corals (30%-42% of present-day suitable habitat), even smaller refugia locations for the octocorals Acanella arbuscula and Acanthogorgia armata (6%-14%), and almost no refugia for P. arborea. Our results emphasize the need to understand how anticipated climate change will affect the distribution of deep-sea species including commercially important fishes and foundation species, and highlight the importance of identifying and preserving climate refugia for a range of area-based planning and management tools.

Potential Impacts of Offshore Oil and Gas Activities on Deep-Sea Sponges and the Habitats They Form.

Sponges form an important component of benthic ecosystems from shallow littoral to hadal depths. In the deep ocean, beyond the continental shelf, sponges can form high-density fields, constituting important habitats supporting rich benthic communities. Yet these habitats remain relatively unexplored. The oil and gas industry has played an important role in advancing our knowledge of deep-sea environments. Since its inception in the 1960s, offshore oil and gas industry has moved into deeper waters. However, the impacts of these activities on deep-sea sponges and other ecosystems are only starting to become the subject of active research. Throughout the development, operation and closure of an oil or gas field many activities take place, ranging from the seismic exploration of subseafloor geological features to the installation of infrastructure at the seabed to the drilling process itself. These routine activities and accidental releases of hydrocarbons during spills can significantly impact the local marine environment. Each phase of a field development or an accidental oil spill will therefore have different impacts on sponges at community, individual and cellular levels. Legacy issues regarding the future decommissioning of infrastructure and the abandonment of wells are also important environmental management considerations. This chapter reviews our understanding of impacts from hydrocarbon exploration and exploitation activities on deep-sea sponges and the habitats they form. These impacts include those (1) at community level, decreasing the diversity and density of benthic communities associated with deep-sea sponges owing to physical disturbance of the seabed; (2) at individual level, interrupting filtration owing to exposure to increased sedimentation; and (3) at cellular level, decreasing cellular membrane stability owing to exposure to drill muds. However, many potential effects not yet tested in deep-sea sponges but observed in shallow-water sponges or other model organisms should also be taken into account. Furthermore, to the best of our knowledge, no studies have shown impact of oil or dispersed oil on deep-sea sponges. To highlight these significant knowledge gaps, a summary table of potential and known impacts of hydrocarbon extraction and production activities combined with a simple "traffic light" scheme is also provided.

Marine Sponges in a Snowstorm - Extreme Sensitivity of a Sponge Holobiont to Marine Oil Snow and Chemically Dispersed Oil Pollution.

Holobionts formed by a host organism and associated symbionts are key biological units in marine ecosystems where they are responsible for fundamental ecosystem services. Therefore, understanding anthropogenic impacts on holobionts is essential. Sponges (Phylum Porifera) are ideal holobiont models. They host a complex microbial community and provide ecosystem services including nutrient cycling. At bathyal depths, sponges can accumulate forming dense sponge ground habitats supporting biodiverse associated communities. However, the impacts of spilled oil and dispersants on sponge grounds cannot be understood without considering exposures mediated through sponge filtration of marine snow particles. To examine this, we exposed the model sponge Halichondria panicea to oil, dispersant and "marine oil snow" contaminated seawater and elucidate the complex molecular response of the holobiont through metatranscriptomics. While the host response included detoxification and immune response pathways, the bacterial symbiotic response differed and was at least partially the result of a change in the host environment rather than a direct response to hydrocarbon exposure. As the sponge host reduced its pumping activity and internal tissue oxygen levels declined, the symbionts changed their metabolism from aerobic to anaerobic pathways possibly via quorum sensing. Furthermore, we found evidence of hydrocarbon degradation by sponge symbionts, but sponge mortality (even when exposed to low concentrations of hydrocarbons) implied this may not provide the holobiont with sufficient resilience against contaminants. Given the continued proposed expansion of hydrocarbon production into deep continental shelf and slope settings where sponge grounds form significant habitats it is important that dispersant use is minimised and that environmental impact assessments carefully consider the vulnerability of sponge holobionts.

Multiscale mechanical consequences of ocean acidification for cold-water corals.

Ocean acidification is a threat to deep-sea corals and could lead to dramatic and rapid loss of the reef framework habitat they build. Weakening of structurally critical parts of the coral reef framework can lead to physical habitat collapse on an ecosystem scale, reducing the potential for biodiversity support. The mechanism underpinning crumbling and collapse of corals can be described via a combination of laboratory-scale experiments and mathematical and computational models. We synthesise data from electron back-scatter diffraction, micro-computed tomography, and micromechanical experiments, supplemented by molecular dynamics and continuum micromechanics simulations to predict failure of coral structures under increasing porosity and dissolution. Results reveal remarkable mechanical properties of the building material of cold-water coral skeletons of 462 MPa compressive strength and 45-67 GPa stiffness. This is 10 times stronger than concrete, twice as strong as ultrahigh performance fibre reinforced concrete, or nacre. Contrary to what would be expected, CWCs retain the strength of their skeletal building material despite a loss of its stiffness even when synthesised under future oceanic conditions. As this is on the material length-scale, it is independent of increasing porosity from exposure to corrosive water or bioerosion. Our models then illustrate how small increases in porosity lead to significantly increased risk of crumbling coral habitat. This new understanding, combined with projections of how seawater chemistry will change over the coming decades, will help support future conservation and management efforts of these vulnerable marine ecosystems by identifying which ecosystems are at risk and when they will be at risk, allowing assessment of the impact upon associated biodiversity.

Human impacts on deep-sea sponge grounds: Applying environmental omics to monitoring.

Sponges (Phylum Porifera) are the oldest extant Metazoans. In the deep sea, sponges can occur at high densities forming habitats known as sponge grounds. Sponge grounds can extend over large areas of up to hundreds of km2 and are biodiversity hotspots. However, as human activities, including deep-water hydrocarbon extraction, continue to expand into areas harbouring sponge grounds, understanding how anthropogenic impacts affect sponges and the ecosystem services they provide at multiple biological scales (community, individual and (sub)cellular levels) is key for achieving sustainable management. This chapter (1) provides an update to the chapter of Advances in Marine Biology Volume 79 entitled "Potential Impacts of Offshore Oil and Gas Activities on Deep-Sea Sponges and the Habitats They Form" and (2) discusses the use of omics as a future tool for deep-sea ecosystem monitoring. While metagenomics and (meta)transcriptomics studies have contributed to improve our understanding of sponge biology in recent years, metabolomics analysis has mostly been used to identify natural products. The sponge metabolome, therefore, remains vastly unknown despite the fact that the metabolome is a key link between the genotype and phenotype, giving us a unique new insight to how key components of an ecosystem are functioning. As the fraction of the metabolome released into the seawater, the sponge exometabolome has only just started to be characterised in comparative environmental metabolomic studies. Yet, the sponge exometabolome constitute a unique opportunity for the identification of biomarkers of sponge health as compounds can be measured in seawater, bypassing the need for physical samples which can still be difficult to collect in the deep sea. Within sponge grounds, the characterisation of a shared sponge exometabolome could lead to the identification of biomarkers of ecosystem functioning and overall health. Challenges remain in establishing omics approaches in environmental monitoring but constant technological advances and reduction in costs means these techniques will become widely available in the future.

Larval behaviour, dispersal and population connectivity in the deep sea.

Ecosystem connectivity is an essential consideration for marine spatial planning of competing interests in the deep sea. Immobile, adult communities are connected through freely floating larvae, depending on new recruits for their health and to adapt to external pressures. We hypothesize that the vertical swimming ability of deep-sea larvae, before they permanently settle at the bottom, is one way larvae can control dispersal. We test this hypothesis with more than [Formula: see text] simulated particles with a range of active swimming behaviours embedded within the currents of a high-resolution ocean model. Despite much stronger horizontal ocean currents, vertical swimming of simulated larvae can have an order of magnitude impact on dispersal. These strong relationships between larval dispersal, pathways, and active swimming demonstrate that lack of data on larval behaviour traits is a serious impediment to modelling deep-sea ecosystem connectivity; this uncertainty greatly limits our ability to develop ecologically coherent marine protected area networks.

Ocean sprawl facilitates dispersal and connectivity of protected species.

Highly connected networks generally improve resilience in complex systems. We present a novel application of this paradigm and investigated the potential for anthropogenic structures in the ocean to enhance connectivity of a protected species threatened by human pressures and climate change. Biophysical dispersal models of a protected coral species simulated potential connectivity between oil and gas installations across the North Sea but also metapopulation outcomes for naturally occurring corals downstream. Network analyses illustrated how just a single generation of virtual larvae released from these installations could create a highly connected anthropogenic system, with larvae becoming competent to settle over a range of natural deep-sea, shelf and fjord coral ecosystems including a marine protected area. These results provide the first study showing that a system of anthropogenic structures can have international conservation significance by creating ecologically connected networks and by acting as stepping stones for cross-border interconnection to natural populations.

Historic scale and persistence of drill cuttings impacts on North Sea benthos.

Despite its long history of hydrocarbon exploitation, the United Kingdom lacks scientific protocols to monitor ecological impacts of drill cuttings (mixtures between rocky material excavated from wells and drilling mud). The present study used the UK Benthos industry database to apply standardised variance partitioning and measure the scale and persistence of these effects at 19 sites across the UK sector of the North Sea. Generally, effects were limited to within 1 km from the platform, but two platforms historically drilled with oil-based mud were impacted up to 1.2 km away. Impacts persisted for at least 6-8 years in the northern and central North Sea, but were undetectable in the south where cuttings piles do not accumulate. This study underpins new recommendations to implement regional, phase-based approaches to drill cuttings monitoring, and to apply a precautionary approach in considering decommissioning options that will minimise disturbance to cuttings piles.

Assessing the living and dead proportions of cold-water coral colonies: implications for deep-water Marine Protected Area monitoring in a changing ocean.

Coral growth patterns result from an interplay of coral biology and environmental conditions. In this study colony size and proportion of live and dead skeletons in the cold-water coral (CWC) Lophelia pertusa (Linnaeus, 1758) were measured using video footage from Remotely Operated Vehicle (ROV) transects conducted at the inshore Mingulay Reef Complex (MRC) and at the offshore PISCES site (Rockall Bank) in the NE Atlantic. The main goal of this paper was to explore the development of a simple method to quantify coral growth and its potential application as an assessment tool of the health of these remote habitats. Eighteen colonies were selected and whole colony and dead/living layer size were measured. Live to dead layer ratios for each colony were then determined and analysed. The age of each colony was estimated using previously published data. Our paper shows that: (1) two distinct morphotypes can be described: at the MRC, colonies displayed a 'cauliflower-shaped' morphotype whereas at the PISCES site, colonies presented a more flattened 'bush-shaped' morphotype; (2) living layer size was positively correlated with whole colony size; (3) live to dead layer ratio was negatively correlated to whole colony size; (4) live to dead layer ratio never exceeded 0.27. These results suggest that as a colony develops and its growth rate slows down, the proportion of living polyps in the colony decreases. Furthermore, at least 73% of L. pertusa colonies are composed of exposed dead coral skeleton, vulnerable to ocean acidification and the associated shallowing of the aragonite saturation horizon, with significant implications for future deep-sea reef framework integrity. The clear visual contrast between white/pale living and grey/dark dead portions of the colonies also gives a new way by which they can be visually monitored over time. The increased use of marine autonomous survey vehicles offers an important new platform from which such a surveying technique could be applied to monitor deep-water marine protected areas in the future.

The occurrence of the cold-water coral Lophelia pertusa (Scleractinia) on oil and gas platforms in the North Sea: colony growth, recruitment and environmental controls on distribution.

This study reports a newly established sub-population of Lophelia pertusa, the dominant reef-framework forming coral species in the north-east Atlantic, on oil and gas platforms in the northern North Sea. L. pertusa was positively identified on 13 of 14 platforms examined using existing oil and gas industry visual inspections. Two platforms were inspected in more detail to examine depth and colony size distributions. We recorded 947 colonies occurring between 59 and 132 m depth that coincides with cold Atlantic water at depths below the summer thermocline in the northern North Sea. We suggest that these colonies provide evidence for a planktonic larval stage of L. pertusa with recruits initially originating from populations in the north-east Atlantic and now self recruiting to the platforms. Size class distribution showed a continuous range of size classes, but with few outlying large colonies. The break between the largest colonies and the rest of the population is considered as the point when colonies began self recruiting to the platforms, resulting in greater colonization success. We present the first documented in situ colony growth rate estimate (26 +/- 5 mm yr(-1)) for L. pertusa based on 15 colonies from the Tern Alpha platform with evidence for yearly recruitment events starting the year the platform was installed. Evidence of contamination from drill muds and cuttings was observed on the Heather platform but appeared limited to regions close to drilling discharge points, where colonies experience partial as well as whole colony mortality.

Sensitivity of marine protected area network connectivity to atmospheric variability.

International efforts are underway to establish well-connected systems of marine protected areas (MPAs) covering at least 10% of the ocean by 2020. But the nature and dynamics of ocean ecosystem connectivity are poorly understood, with unresolved effects of climate variability. We used 40-year runs of a particle tracking model to examine the sensitivity of an MPA network for habitat-forming cold-water corals in the northeast Atlantic to changes in larval dispersal driven by atmospheric cycles and larval behaviour. Trajectories of Lophelia pertusa larvae were strongly correlated to the North Atlantic Oscillation (NAO), the dominant pattern of interannual atmospheric circulation variability over the northeast Atlantic. Variability in trajectories significantly altered network connectivity and source-sink dynamics, with positive phase NAO conditions producing a well-connected but asymmetrical network connected from west to east. Negative phase NAO produced reduced connectivity, but notably some larvae tracked westward-flowing currents towards coral populations on the mid-Atlantic ridge. Graph theoretical metrics demonstrate critical roles played by seamounts and offshore banks in larval supply and maintaining connectivity across the network. Larval longevity and behaviour mediated dispersal and connectivity, with shorter lived and passive larvae associated with reduced connectivity. We conclude that the existing MPA network is vulnerable to atmospheric-driven changes in ocean circulation.

Physiological response of the cold-water coral Desmophyllum dianthus to thermal stress and ocean acidification.

Rising temperatures and ocean acidification driven by anthropogenic carbon emissions threaten both tropical and temperate corals. However, the synergistic effect of these stressors on coral physiology is still poorly understood, in particular for cold-water corals. This study assessed changes in key physiological parameters (calcification, respiration and ammonium excretion) of the widespread cold-water coral Desmophyllum dianthus maintained for ∼8 months at two temperatures (ambient 12 °C and elevated 15 °C) and two pCO2 conditions (ambient 390 ppm and elevated 750 ppm). At ambient temperatures no change in instantaneous calcification, respiration or ammonium excretion rates was observed at either pCO2 levels. Conversely, elevated temperature (15 °C) significantly reduced calcification rates, and combined elevated temperature and pCO2 significantly reduced respiration rates. Changes in the ratio of respired oxygen to excreted nitrogen (O:N), which provides information on the main sources of energy being metabolized, indicated a shift from mixed use of protein and carbohydrate/lipid as metabolic substrates under control conditions, to less efficient protein-dominated catabolism under both stressors. Overall, this study shows that the physiology of D. dianthus is more sensitive to thermal than pCO2 stress, and that the predicted combination of rising temperatures and ocean acidification in the coming decades may severely impact this cold-water coral species.

Environmental variability and biodiversity of megabenthos on the Hebrides Terrace Seamount (Northeast Atlantic).

We present the first remotely operated vehicle investigation of megabenthic communities (1004-1695 m water depth) on the Hebrides Terrace Seamount (Northeast Atlantic). Conductivity-temperature-depth casts showed rapid light attenuation below the summit and an oceanographic regime on the flanks consistent with an internal tide, and high short-term variability in water temperature, salinity, light attenuation, aragonite and oxygen down to 1500 m deep. Minor changes in species composition (3-14%) were explained by changes in depth, substratum and oceanographic stability, whereas environmental variability explained substantially more variation in species richness (40-56%). Two peaks in species richness occurred, the first at 1300-1400 m where cooler Wyville Thomson Overflow Water (WTOW) mixes with subtropical gyre waters and the second at 1500-1600 m where WTOW mixes with subpolar mode waters. Our results suggest that internal tides, substrate heterogeneity and oceanographic interfaces may enhance biological diversity on this and adjacent seamounts in the Rockall Trough.

Ecohydrodynamics of cold-water coral reefs: a case study of the Mingulay Reef Complex (western Scotland).

Ecohydrodynamics investigates the hydrodynamic constraints on ecosystems across different temporal and spatial scales. Ecohydrodynamics play a pivotal role in the structure and functioning of marine ecosystems, however the lack of integrated complex flow models for deep-water ecosystems beyond the coastal zone prevents further synthesis in these settings. We present a hydrodynamic model for one of Earth's most biologically diverse deep-water ecosystems, cold-water coral reefs. The Mingulay Reef Complex (western Scotland) is an inshore seascape of cold-water coral reefs formed by the scleractinian coral Lophelia pertusa. We applied single-image edge detection and composite front maps using satellite remote sensing, to detect oceanographic fronts and peaks of chlorophyll a values that likely affect food supply to corals and other suspension-feeding fauna. We also present a high resolution 3D ocean model to incorporate salient aspects of the regional and local oceanography. Model validation using in situ current speed, direction and sea elevation data confirmed the model's realistic representation of spatial and temporal aspects of circulation at the reef complex including a tidally driven current regime, eddies, and downwelling phenomena. This novel combination of 3D hydrodynamic modelling and remote sensing in deep-water ecosystems improves our understanding of the temporal and spatial scales of ecological processes occurring in marine systems. The modelled information has been integrated into a 3D GIS, providing a user interface for visualization and interrogation of results that allows wider ecological application of the model and that can provide valuable input for marine biodiversity and conservation applications.

Fine-scale nutrient and carbonate system dynamics around cold-water coral reefs in the northeast Atlantic.

Ocean acidification has been suggested as a serious threat to the future existence of cold-water corals (CWC). However, there are few fine-scale temporal and spatial datasets of carbonate and nutrients conditions available for these reefs, which can provide a baseline definition of extant conditions. Here we provide observational data from four different sites in the northeast Atlantic that are known habitats for CWC. These habitats differ by depth and by the nature of the coral habitat. At depths where CWC are known to occur across these sites the dissolved inorganic carbon ranged from 2088 to 2186 µmol kg(-1), alkalinity ranged from 2299 to 2346 µmol kg(-1), and aragonite Ω ranged from 1.35 to 2.44. At two sites fine-scale hydrodynamics caused increased variability in the carbonate and nutrient conditions over daily time-scales. The observed high level of variability must be taken into account when assessing CWC sensitivities to future environmental change.

Tidal downwelling and implications for the carbon biogeochemistry of cold-water corals in relation to future ocean acidification and warming.

Cold-water coral (CWC) reefs are recognized as ecologically and biologically significant areas that generate habitats and diversity. The interaction between hydrodynamics and CWCs has been well studied at the Mingulay Reef Complex, a relatively shallow area of reefs found on the continental shelf off Scotland, UK. Within 'Mingulay Area 01' a rapid tidal downwelling of surface waters, brought about as an internal wave, is known to supply warmer, phytoplankton-rich waters to corals growing on the northern flank of an east-west trending seabed ridge. This study shows that this tidal downwelling also causes short-term perturbations in the inorganic carbon (CT ) and nutrient dynamics through the water column and immediately above the reef. Over a 14 h period, corresponding to one semi-diurnal tidal cycle, seawater pH overlying the reef varied by ca. 0.1 pH unit, while pCO2 shifted by >60 µatm, a shift equivalent to a ca. 25 year jump into the future, with respect to atmospheric pCO2 . During the summer stratified period, these downwelling events result in the reef being washed over with surface water that has higher pH, is warmer, nutrient depleted, but rich in phytoplankton-derived particles compared to the deeper waters in which the corals sit. Empirical observations, together with outputs from the European Regional Shelf Sea Ecosystem Model, demonstrate that the variability that the CWC reefs experience changes through the seasons and into the future. Hence, as ocean acidification and warming increase into the future, the downwelling event specific to this site could provide short-term amelioration of corrosive conditions at certain times of the year; however, it could additionally result in enhanced detrimental impacts of warming on CWCs. Natural variability in the CT and nutrient conditions, as well as local hydrodynamic regimes, must be accounted for in any future predictions concerning the responses of marine ecosystems to climate change.

Reefs of the deep: the biology and geology of cold-water coral ecosystems.

Coral reefs are generally associated with shallow tropical seas; however, recent deep-ocean exploration using advanced acoustics and submersibles has revealed unexpectedly widespread and diverse coral ecosystems in deep waters on continental shelves, slopes, seamounts, and ridge systems around the world. Advances reviewed here include the use of corals as paleoclimatic archives and their biogeological functioning, biodiversity, and biogeography. Threats to these fragile, long-lived, and rich ecosystems are mounting: The impacts of deep-water trawling are already widespread, and effects of ocean acidification are potentially devastating.