Effects of aquaculture effluents on the slender sea pen Virgularia mirabilis.

This study aims to assess in situ the impact of effluents originating from an Atlantic salmon (Salmo salar) farm on a nearby slender sea pen (Virgularia mirabilis) field. We evidenced (1) the presence and persistence of emamectin residues (i.e. a common chemotherapeutants used for treating ectoparasites in salmons) in V. mirabilis tissue 56 days after treatment and (2) lethal and sublethal responses of V. mirabilis to effluents discharged by the salmon farm. Particularly, sea pens near the fish farm exhibited significant overproduction of mucus, contraction of polyps' tentacles, and disappearance of associated fauna. Furthermore, sea pens located directly underneath the farm showed substantial tissue necrosis and, in the most severe case, complete tissue loss and mortality. Our results suggest that lethal damages on sea pens occur directly below the farm, and that sublethal effects are visible up to 500 m from the farm. However, the presence of V. mirabilis below the studied farm, which has been active for more than twenty years, suggests that V. mirabilis population possesses the capacity to recover from the impacts of the farm, thereby preventing the complete disappearance from the area. In this context, it would be particularly interesting to run a temporal survey following the health state of V. mirabilis during an entire production cycle to have a more precise overview of fish farm impacts on this species, including during and after the post-production fallowing period.

Multi-isotopic composition of brown crab (Cancer pagurus) and seafloor sediment from a mine tailing sea disposal impacted fjord ecosystem.

Sea disposal of mine tailings in fjord ecosystems is an important coastal management issue in Norway and occurs at the land-sea interface. Here we studied accumulation of heavy metals in brown crab (Cancer pagurus) and seafloor sediment from Jøssingfjord, Norway during 2018 to evaluate long-term, legacy pollution effects of coastal mine tailing sea disposal activities. Nickel and copper sediment pollution in the mine tailing sea disposal area was classified as moderate and severe, respectively, under Norwegian environmental quality standards, and highlights the persistent hazard and legacy impacts of heavy metals in these impacted fjord ecosystems. Mercury, zinc, and arsenic had stronger affinities to brown crab muscle likely due to the presence of thiols, and availability of metal binding sites. Our multi-isotopic composition data showed that lead isotopes were the most useful source apportionment tool for this fjord. Overall, our study highlights the importance and value of measuring several different heavy metals and multiple isotopic signatures in different crab organs and seafloor sediment to comprehensively evaluate fjord pollution and kinetic uptake dynamics. Brown crabs were suitable eco-indicators of benthic ecosystem heavy metal pollution in a fjord ecosystem still experiencing short- and long-term physical and chemical impacts from coastal mining sea disposal activities.

The long-lived deep-sea bivalve Acesta excavata is sensitive to the dual stressors of sediment and warming.

Human influence in the deep-sea is increasing as mining and drilling operations expand, and waters warm because of climate change. Here, we investigate how the long-lived deep-sea bivalve, Acesta excavata responds to sediment pollution and/or acute elevated temperatures. A. excavata were exposed to suspended sediment, acute warming, and a combination of the two treatments for 40 days. We measured O2 consumption, NH4+ release, Total Organic Carbon (TOC), and lysosomal membrane stability (LMS). We found suspended sediment and warming interacted to decrease O:N ratios, while sediment as a single stressor increased the release of TOC and warming increased NH4+ release in A. excavata. Warming also increased levels of LMS. We found A. excavata used protein catabolism to meet elevated energetic demands indicating a low tolerance to stress. A. excavata has limited capacity for physiological responses to the stressors of warming and sediment which may lead to decreased fitness of A. excavata.

Effects of the sea lice chemotherapeutant, emamectin benzoate, on metabolism and behaviour of the sea-pen Pennatula phosphorea.

Chemotherapeutants used to control infestations by sea lice can be released into the marine environment surrounding aquaculture farms. Among these therapeutic agents, emamectin benzoate is extensively utilized even though its impact on non-target taxa has not been thoroughly examined. In this context, we explored the effects of emamectin benzoate on a common Norwegian habitat-forming species: the phosphorescent sea-pen Pennatula phosphorea. Specifically, we examined P. phosphorea metabolic and responses before, during and after exposure to emamectin benzoate. Results indicate that an 8-day emamectin benzoate exposure (0.8 mg/L) did not induce P. phosphorea mortality or significant behavioural or metabolic modifications. However, we highlighted the presence and persistence of emamectin benzoate in exposed P. phosphorea tissue. These results indicate that emamectin benzoate is unlikely to adversely impact P. phosphorea populations in the environment. However, persistence of emamectin benzoate in tissue constitutes a potential for bioaccumulation with repeated treatments and should be examined in further studies.

On the paradox of thriving cold-water coral reefs in the food-limited deep sea.

The deep sea is amongst the most food-limited habitats on Earth, as only a small fraction (<4%) of the surface primary production is exported below 200 m water depth. Here, cold-water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep-sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food-limited deep sea, by reviewing the literature and open-access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating 'feast' conditions, interspersed with 'famine' periods during the non-productive season. Secondly, CWCs, particularly the most common reef-builder Desmophyllum pertusum (formerly known as Lophelia pertusa), are well adapted to these fluctuations in food availability. Laboratory and in situ measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium-carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future.

Recycling pathways in cold-water coral reefs: Use of dissolved organic matter and bacteria by key suspension feeding taxa.

Cold-water coral (CWC) reefs are one of the most diverse and productive ecosystems in the deep sea. Especially in periods of seasonally-reduced phytodetritus food supply, their high productivity may depend on the recycling of resources produced on the reef, such as dissolved organic matter (DOM) and bacteria. Here, we demonstrate that abundant suspension feeders Geodia barretti (high-microbial-abundance sponge), Mycale lingua (low-microbial-abundance sponge) and Acesta excavata (bivalve) are able to utilize 13C-enriched (diatom-derived) DOM and bacteria for tissue growth and respiration. While DOM was an important potential resource for all taxa, utilization of bacteria was higher for the sponges as compared to the bivalve, indicating a particle-size differentiation among the investigated suspension feeders. Interestingly, all taxa released 13C-enriched particulate organic carbon, which in turn may feed the detritus pathway on the reef. Especially A. excavata produced abundant (pseudo-)fecal droppings. A second stable-isotope tracer experiment revealed that detritivorous ophiuroids utilized these droppings. The high resource flexibility of dominant reef suspension feeders, and the efficient recycling of their waste products by the detritivore community, may provide important pathways to maintain the high productivity on cold-water coral reefs, especially in periods of low external food supply.

Broad Thermal Tolerance in the Cold-Water Coral Lophelia pertusa From Arctic and Boreal Reefs.

Along the Norwegian coasts and margins, extensive reefs of the stony coral Lophelia pertusa act as hotspots for local biodiversity. Climate models project that the temperature of Atlantic deep waters could rise by 1-3°C by 2100. In this context, understanding the effects of temperature on the physiology of cold-water species will help in evaluating their resilience to future oceanic changes. We investigated the response of L. pertusa to stepwise short-term increases in temperature. We sampled corals from four reefs, two located north of the Arctic circle and two at the mid-Norwegian shelf (boreal). In on-board experiments (one per reef), the sampled fragments were exposed to increasing temperatures from 5 to 15°C over 58 h. Respiration increased linearly by threefold for a 10°C increase. The short-term temperature increase did not induce mortality, cellular (neutral red assay for lysosome membrane stability; but one exception) or oxidative stress (lipid peroxidation assay) - to a few exceptions. However, the variability of the respiration responses depended on the experiment (i.e., reef location), possibly linked to the genetic structure of the individuals that we sampled (e.g., clones or siblings). The corals from the Arctic and boreal regions appear to have a high tolerance to the rapid temperature fluctuations they experience in the field. Over extended periods of time however, an increased metabolism could deplete the energy stored by the corals, if not met by an increased food availability and/or uptake. Empirical data on organisms' thermal performance curves, such as the one presented in this study for L. pertusa, will be useful to implement predictive models on the responses of species and populations to climate change.

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.

Impact of particulate sediment, bentonite and barite (oil-drilling waste) on net fluxes of oxygen and nitrogen in Arctic-boreal sponges.

To meet the increasing global energy demand, expanding exploration for oil and gas reserves as well as associated drilling activities are expected in the Arctic-boreal region where sponge aggregations contribute to up to 90% of benthic biomass. These deep-water sponges along with their microbial endobionts play key roles in the nitrogen cycling in Arctic-boreal ecosystems. This study aimed to investigate the effects of drilling discharges and associated sediment resuspension events on net fluxes of oxygen, ammonium, nitrate and nitrite in three common deep-water sponge species in the form of explants. Sponges were exposed to suspended bentonite and barite, the primary particulate compounds in drilling waste, as well as suspended natural sediment particles for a period of 33 days (on average 10 mg L-1 for 12 h day-1). The exposure period was followed by a pollution abatement period for a further 33 days. No sponge mortality was observed during the experiment. However, exposure to these particles, especially to barite, led to reduced oxygen consumption by up to 33% that was linearly correlated with reduced nitrite/nitrate release by the sponges. The changes in net fluxes were accompanied by decreased tissue oxygenation by up to 54% within the sponges. These findings reveal the effects of fine particles on sponge metabolic processes by reducing aerobic respiration and microbial nitrification, and possibly by favouring anaerobic processes such as microbial denitrification. Most of the sponge responses recovered to their control levels upon the pollution abatement period, but the effects caused by barite may not be reversible. Our findings provide the first insight into the ecological consequences of oil and gas drilling activities on sponge-mediated nitrogen cycling in the Arctic-boreal region.

Microbiome analysis of a disease affecting the deep-sea sponge Geodia barretti.

Reports of sponge disease are becoming increasingly frequent, although almost all instances involve shallow-water, tropical species. Here, we describe the first disease affecting the deep-water sponge, Geodia barretti. The disease is characterised by brown/black discolouration of the sponge tissue, extensive levels of tissue disintegration and increased levels of fouling. Disease prevalence was quantified using video survey transects conducted between 100 and 220 m in Korsfjorden, Norway, and the microbial communities of healthy and diseased sponges were compared using 16S rRNA gene sequencing. Highly divergent community profiles were evident between the different health states, with distinct community shifts involving higher relative abundances of Bacteroidetes, Firmicutes and Deltaproteobacteria in diseased individuals. In addition, three operational taxonomic units were exclusively present in diseased individuals and were shared between the disease lesions and the apparently healthy tissue of diseased individuals, suggesting a non-localised infection or dysbiosis. Genomic analysis of the G. barretti microbiome combined with experimental work to assess the mechanisms of infection will further elucidate the role of microorganisms in the disease.

Consumption of aquaculture waste affects the fatty acid metabolism of a benthic invertebrate.

Trophic subsidies can drive widespread ecological change, thus knowledge of how keystone species respond to subsidies is important. Aquaculture of large carnivorous fish generates substantial waste as faeces and lost feed, providing a food source to mobile benthic invertebrates. We used a controlled feeding study combined with a field survey to better understand the interaction between salmon aquaculture and the sea urchin, Echinus acutus, a dominant mobile invertebrate in Norwegian fjords. We tested if diets affected urchin fatty acid composition by feeding them one of three diet treatments ("aquafeed", "composite" and "natural") for 10weeks. To test if proximity to fish farms altered E. acutus fatty acid composition, populations were sampled at 10 locations in Hardangerfjord and Masfjord (Western Norway) from directly adjacent and up to 12km from farms. Fatty acids were measured in gonads and eggs in the diet experiment and in gonads and gut contents from wild animals. Urchins directly assimilated aquaculture waste at farm sites, as evidenced by elevated linoleic acid (LA), oleic acid (OA) and ∑LA, OA in their tissues. The diet experiment highlighted the biosynthetic and selective dietary sparing capacity of E. acutus in both gonads and eggs, with evidence for the elongation and desaturation of eicosapentaenoic acid (EPA) and arachidonic acid (ARA) from C18 fatty acid precursors. Elevated biosynthesis of non-methylene interrupted (NMI) fatty acids, in particular 20:3Δ7,11,14 and 20:2 Δ5,11, were also linked to a high C18 fatty acid, low ≥C20 long-chain polyunsaturated fatty acid (LC-PUFA) diet. Fatty acid composition of gonads of wild urchins indicated a highly variable diet. The study indicates that the generalist feeding ecology of E. acutus, coupled with extensive biosynthetic capacity, enables it to exploit aquaculture waste as an energy-rich trophic subsidy.

Sub-lethal effects of water-based drilling muds on the deep-water sponge Geodia barretti.

Offshore oil and gas activities can result in the discharge of large amounts of drilling muds. While these materials have generally been regarded as non-toxic to marine organisms, recent studies have demonstrated negative impacts to suspension feeding organisms. We exposed the arctic-boreal sponge Geodia barretti to the primary particulate components of two water-based drilling muds; barite and bentonite. Sponges were exposed to barite, bentonite and a natural reference sediment at a range of total suspended solid concentrations (TSS = 0, 10, 50 or 100 mg/L) for 12 h after which we measured a suite of biomarker responses (lysosomal membrane stability, lipid peroxidation and glutathione). In addition, we compared biomarker responses, organic energy content and metal accumulation in sponges, which had been continuously or intermittently exposed to suspended barite and natural sediment for 14 d at relevant concentrations (10 and 30 mg TSS/L). Lysosomal membrane stability was reduced in the sponges exposed to barite at 50 and 100 mg TSS/L after just 12 h and at 30 mg TSS/L for both continuous and intermittent exposures over 14 d. Evidence of compromised cellular viability was accompanied by barite analysis revealing concentrations of Cu and Pb well above reference sediments and Norwegian sediment quality guidelines. Metal bioaccumulation in sponge tissues was low and the total organic energy content (determined by the elemental composition of organic tissue) was not affected. Intermittent exposures to barite resulted in less toxicity than continuous exposure to barite. Short term exposures to bentonite did not alter any biomarker responses. This is the first time that these biomarkers have been used to indicate contaminant exposure in an arctic-boreal sponge. Our results illustrate the potential toxicity of barite and the importance of assessments that reflect the ways in which these contaminants are delivered under environmentally realistic conditions.