New tools to evaluate plastic ingestion by northern fulmars applied to North Sea monitoring data 2002-2018.

Monitoring plastic in stomachs of beached northern fulmars for OSPAR's Ecological Quality Objectives (EcoQOs) has been incorporated into the European Marine Strategy Framework Directive (MSFD). This paper aims to provide the appropriate tools to interpret the monitoring results. MSFD requires a data-derived threshold value (Fulmar-TV) representing 'Good Environmental Status'. Such Fulmar-TV was calculated from near-pristine Canadian Arctic data where 10.06% of fulmars exceeded the level of 0.1 g ingested plastic. This Fulmar-TV is almost identical to the earlier OSPAR EcoQO, arbitrarily set at 10%. The MSFD approach was evaluated for 2661 North Sea fulmars in 2002-2018. Between 2014 and 2018, 51% of 393 fulmars exceeded 0.1 g plastic, significantly above the proposed Fulmar-TV. Linear regression of individual ingested plastic mass over the 2009-2018 period indicates a significant decrease. Over the longer term 2002-2018, logistic regression of annual EcoQ% shows a significant decline and predicts compliance with the Fulmar-TV by 2054.

Details of plastic ingestion and fibre contamination in North Sea fishes.

This study combines published datasets with unpublished data on plastic ingestion in several North Sea fish species. The combined dataset of 4389 individuals from 15 species allows the analysis of spatial distribution and temporal variability of plastic uptake in fish. Airborne fibre contamination was observed to be the main contributor to fibres encountered in the samples. The number of fibres in samples was strongly related to the time needed to process a sample, not to the number of individual fishes in the sample. Accurate correction for secondary fibre contamination was not possible, but corrections required would be similar to fibre numbers observed in the samples. Consequently, all fibres were omitted from further analysis. The frequency of occurrence and the average number of plastics in fish is generally low (1.8% and 0.022 pieces per organism respectively), with only cod having a higher prevalence (12.3%). While latitude of catch locations influences plastic uptake in fish, no correlation with the distance to the coast was found. Slightly less plastics were ingested in winter, and a decrease in plastics ingested was observed between 2009 and 2018. These factors should be considered when fish species, catch location and time are discussed as indicators for plastic pollution in the European Marine Strategy Framework Directive. We recommend considering demersal cod and pelagic sprat as two species suitable for monitoring plastic ingestion in biota, both on the seafloor and in the water column.

Piece-by-piece analysis of additives and manufacturing byproducts in plastics ingested by seabirds: Implication for risk of exposure to seabirds.

The risk of marine organisms ingesting plastics has become a growing concern due to hazard chemicals in plastics. To identify compounds to which seabirds potentially have substantial exposure, 194 plastics fragments and pellets ingested by seabirds, i.e., northern fulmars from the Faroe Islands, and laysan albatross and black-footed albatross from Mukojima Island, were analyzed piece by piece. Four kinds of UV stabilizers, 2 brominated flame retardants, and styrene oligomers were detected at detection frequencies of 4.6%, 2.1%, and 2.1%, respectively. Concentrations ranging from not detected (n.d.) - 1700 µg/g were measured for UV stabilizers, n.d. - 1100 µg/g for flame retardants, and n.d. - 3200 µg/g for styrene oligomers. We found that these chemicals could be retained in plastics during drifting and fragmentation in the ocean and transported to seabirds. This type of transport via plastics can be direct pathway that introduces hazardous compounds to marine organisms.

Marine microplastic: Preparation of relevant test materials for laboratory assessment of ecosystem impacts.

Studies investigating the effects of plastic litter on marine biota have almost exclusively utilised pristine plastic materials that are homogeneous in polymer type, size, shape and chemical composition. This is particularly the case for microplastics (<5 mm), where collecting sufficient quantities from the marine environment for use in laboratory impacts studies is simply not feasible. Weathered plastics collected from the marine environment show considerable physical and chemical differences to pristine and post-production consumer plastics. For this study, macroplastic litter was collected on a Dutch beach and cryo-milled to create a microplastic mixture for environmental impact assessments. The sample composition followed proportions of marine plastic litter types observed in an earlier large beach clean-up. Polymer composition of the sample was assessed by infrared spectroscopy (ATR-FTIR) and differential scanning calorimetry analysis (DSC). The particle size distribution of the cryo-milled microplastics showed that particles 0.5-2.0 mm represented 68% of mass, but smaller sizes (<2 mm) strongly dominated numerically. Inductively coupled plasma spectroscopy (ICP-MS and ICP-OES) analysis of the microplastic mixture revealed a broad range of metals and other elements (e.g. Al, Cd, Cr, Fe, Mg, Pb, S and Zn), representing common inorganic additives used as colorants, fillers and stabilisers. GC-MS analysis identified a broad range of organic plasticisers, stabilisers, antioxidants and flame retardants. Comparison of different analytical approaches showed that creation of a homogeneous microplastic mixture is possible, representing a first step in closing the gap between laboratory studies with pristine materials and realistic scenarios with weathered microplastic.

Plastic ingestion by harbour porpoises Phocoena phocoena in the Netherlands: Establishing a standardised method.

Stomach contents of harbour porpoises (Phocoena phocoena) collected in the Netherlands between 2003 and 2013 were inspected for the presence of plastic and other man-made litter. In 654 stomach samples the frequency of occurrence of plastic litter was 7% with less than 0.5% additional presence of non-synthetic man-made litter. However, we show that when a dedicated standard protocol for the detection of litter is followed, a considerably higher percentage (15% of 81 harbour porpoise stomachs from the period 2010-2013) contained plastic litter. Results thus strongly depended on methods used and time period considered. Occurrence of litter in the stomach was correlated to the presence of other non-food remains like stones, shells, bog-wood, etc., suggesting that litter was often ingested accidentally when the animals foraged close to the bottom. Most items were small and were not considered to have had a major health impact. No evident differences in ingestion were found between sexes or age groups, with the exception that neonates contained no litter. Polyethylene and polypropylene were the most common plastic types encountered. Compared to earlier literature on the harbour porpoise and related species, our results suggest higher levels of ingestion of litter. This is largely due to the lack of dedicated protocols to investigate marine litter ingestion in previous studies. Still, the low frequency of ingestion, and minor number and mass of litter items found in harbour porpoises in the relatively polluted southern North Sea indicates that the species is not a strong candidate for annual monitoring of marine litter trends under the EU marine strategy framework directive. However, for longer-term comparisons and regional differences, with proper dedicated protocols applied, the harbour porpoise has specific use in quantifying litter presence in the, for that specific objective, poorly studied benthic marine habitat.

Plastic ingestion by juvenile polar cod (Boreogadus saida) in the Arctic Ocean.

One of the recently recognised stressors in Arctic ecosystems concerns plastic litter. In this study, juvenile polar cod (Boreogadus saida) were investigated for the presence of plastics in their stomachs. Polar cod is considered a key species in the Arctic ecosystem. The fish were collected both directly from underneath the sea ice in the Eurasian Basin and in open waters around Svalbard. We analysed the stomachs of 72 individuals under a stereo microscope. Two stomachs contained non-fibrous microplastic particles. According to µFTIR analysis, the particles consisted of epoxy resin and a mix of Kaolin with polymethylmethacrylate (PMMA). Fibrous objects were excluded from this analysis to avoid bias due to contamination with airborne micro-fibres. A systematic investigation of the risk for secondary micro-fibre contamination during analytical procedures showed that precautionary measures in all procedural steps are critical. Based on the two non-fibrous objects found in polar cod stomachs, our results show that ingestion of microplastic particles by this ecologically important fish species is possible. With increasing human activity, plastic ingestion may act as an increasing stressor on polar cod in combination with ocean warming and sea-ice decline in peripheral regions of the Arctic Ocean. To fully assess the significance of this stressor and its spatial and temporal variability, future studies must apply a rigorous approach to avoid secondary pollution.

Comment on "Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds" by Savoca et al.

In their recent paper, Savoca and collaborators (2016) showed that plastic debris in the ocean may acquire a dimethyl sulfide (DMS) signature from biofouling developing on their surface. According to them, DMS emission may represent an olfactory trap for foraging seabirds, which explains patterns of plastic ingestion among procellariiform seabirds. This hypothesis is appealing, but some of the data that Savoca et al. used to support their claim are questionable, resulting in a misclassification of species, as well as other decisions regarding the variables to include in their models. Furthermore, with their focus on a single lifestyle trait (nesting habit) of dubious relevance for explaining plastic ingestion, Savoca et al. neglect the opportunity to explore other factors that might provide better ecological insight. Finally, we are deeply concerned by the conservation policy recommendation proposed by Savoca et al.-to increase antifouling properties of consumer plastics-which constitutes a substantial environmental risk and delivers the wrong message to decision-makers. The reduction of plastic consumption, waste prevention, and proactive reuse through a circular economy should be at the heart of policy recommendations for future mitigation efforts.

The use of potassium hydroxide (KOH) solution as a suitable approach to isolate plastics ingested by marine organisms.

In studies of plastic ingestion by marine wildlife, visual separation of plastic particles from gastrointestinal tracts or their dietary content can be challenging. Earlier studies have used solutions to dissolve organic materials leaving synthetic particles unaffected. However, insufficient tests have been conducted to ensure that different categories of consumer products partly degraded in the environment and/or in gastrointestinal tracts were not affected. In this study 63 synthetic materials and 11 other dietary items and non-plastic marine debris were tested. Irrespective of shape or preceding environmental history, most polymers resisted potassium hydroxide (KOH) solution, with the exceptions of cellulose acetate from cigarette filters, some biodegradable plastics and a single polyethylene sheet. Exposure of hard diet components and other marine debris showed variable results. In conclusion, the results confirm that usage of KOH solutions can be a useful approach in general quantitative studies of plastic ingestion by marine wildlife.

The ecological impacts of marine debris: unraveling the demonstrated evidence from what is perceived.

Anthropogenic debris contaminates marine habitats globally, leading to several perceived ecological impacts. Here, we critically and systematically review the literature regarding impacts of debris from several scientific fields to understand the weight of evidence regarding the ecological impacts of marine debris. We quantified perceived and demonstrated impacts across several levels of biological organization that make up the ecosystem and found 366 perceived threats of debris across all levels. Two hundred and ninety-six of these perceived threats were tested, 83% of which were demonstrated. The majority (82%) of demonstrated impacts were due to plastic, relative to other materials (e.g., metals, glass) and largely (89%) at suborganismal levels (e.g., molecular, cellular, tissue). The remaining impacts, demonstrated at higher levels of organization (i.e., death to individual organisms, changes in assemblages), were largely due to plastic marine debris (> 1 mm; e.g., rope, straws, and fragments). Thus, we show evidence of ecological impacts from marine debris, but conclude that the quantity and quality of research requires improvement to allow the risk of ecological impacts of marine debris to be determined with precision. Still, our systematic review suggests that sufficient evidence exists for decision makers to begin to mitigate problematic plastic debris now, to avoid risk of irreversible harm.

Validating the use of intrinsic markers in body feathers to identify inter-individual differences in non-breeding areas of northern fulmars.

Many wildlife studies use chemical analyses to explore spatio-temporal variation in diet, migratory patterns and contaminant exposure. Intrinsic markers are particularly valuable for studying non-breeding marine predators, when direct methods of investigation are rarely feasible. However, any inferences regarding foraging ecology are dependent upon the time scale over which tissues such as feathers are formed. In this study, we validate the use of body feathers for studying non-breeding foraging patterns in a pelagic seabird, the northern fulmar. Analysis of carcasses of successfully breeding adult fulmars indicated that body feathers moulted between September and March, whereas analyses of carcasses and activity patterns suggested that wing feather and tail feather moult occurred during more restricted periods (September to October and September to January, respectively). By randomly sampling relevant body feathers, average values for individual birds were shown to be consistent. We also integrated chemical analyses of body feather with geolocation tracking data to demonstrate that analyses of δ13C and δ15N values successfully assigned 88 % of birds to one of two broad wintering regions used by breeding adult fulmars from a Scottish study colony. These data provide strong support for the use of body feathers as a tool for exploring non-breeding foraging patterns and diet in wide-ranging, pelagic seabirds.

Linking effects of anthropogenic debris to ecological impacts.

Accelerated contamination of habitats with debris has caused increased effort to determine ecological impacts. Strikingly, most work on organisms focuses on sublethal responses to plastic debris. This is controversial because (i) researchers have ignored medical insights about the mechanisms that link effects of debris across lower levels of biological organization to disease and mortality, and (ii) debris is considered non-hazardous by policy-makers, possibly because individuals can be injured or removed from populations and assemblages without ecological impacts. We reviewed the mechanisms that link effects of debris across lower levels of biological organization to assemblages and populations. Using plastic, we show microplastics reduce the 'health', feeding, growth and survival of ecosystem engineers. Larger debris alters assemblages because fishing-gear and tyres kill animals and damage habitat-forming plants, and because floating bottles facilitate recruitment and survival of novel taxa. Where ecological linkages are not known, we show how to establish hypothetical links by synthesizing studies to assess the likelihood of impacts. We also consider how population models examine ecological linkages and guide management of ecological impacts. We show that by focusing on linkages to ecological impacts rather than the presence of debris and its sublethal impacts, we could reduce threats posed by debris.

Seabirds, gyres and global trends in plastic pollution.

Fulmars are effective biological indicators of the abundance of floating plastic marine debris. Long-term data reveal high plastic abundance in the southern North Sea, gradually decreasing to the north at increasing distance from population centres, with lowest levels in high-arctic waters. Since the 1980s, pre-production plastic pellets in North Sea fulmars have decreased by ∼75%, while user plastics varied without a strong overall change. Similar trends were found in net-collected floating plastic debris in the North Atlantic subtropical gyre, with a ∼75% decrease in plastic pellets and no obvious trend in user plastic. The decreases in pellets suggest that changes in litter input are rapidly visible in the environment not only close to presumed sources, but also far from land. Floating plastic debris is rapidly "lost" from the ocean surface to other as-yet undetermined sinks in the marine environment.

Plastic ingestion by harbour seals (Phoca vitulina) in The Netherlands.

Abundance of ingested debris by seals has been mentioned as a potential indicator of marine litter in the European Marine Strategy Framework Directive (MSFD). A sample of 107 stomachs, 100 intestines and 125 scats of harbour seals from the Netherlands was analysed for the presence of plastics. Incidence of plastic was 11% for stomachs, 1% for intestines, and 0% for scats. Younger animals, up to 3 years of age, were most affected. This is the first quantitative study of plastic ingestion by phocid seals. The observed level of incidence is of environmental concern, but is low in the sense of suitability of seals for MSFD monitoring purposes.

Plastic ingestion by the northern fulmar (Fulmarus glacialis) in Iceland.

In 2011, northern fulmars (Fulmarus glacialis) from Iceland were used to test the hypothesis that plastic debris decreases at northern latitudes in the Atlantic when moving away from major human centres of coastal and marine activities. Stomach analyses of Icelandic fulmars confirm that plastic pollution levels in the North Atlantic tend to decrease towards higher latitudes. Levels of pollution thus appear to link to regions of intense human coastal and marine activities, suggesting substantial current inputs in those areas.

Monitoring plastic ingestion by the northern fulmar Fulmarus glacialis in the North Sea.

The abundance of plastics in stomachs of northern fulmars from the North Sea is used in the OSPAR Ecological Quality Objective (EcoQO) for marine litter. The preliminary EcoQO defines acceptable ecological quality as the situation where no more than 10% of fulmars exceed a critical level of 0.1 g of plastic in the stomach. During 2003-2007, 95% of 1295 fulmars sampled in the North Sea had plastic in the stomach (on average 35 pieces weighing 0.31 g) and the critical level of 0.1 g of plastic was exceeded by 58% of birds, with regional variations ranging from 48 to 78%. Long term data for the Netherlands since the 1980s show a decrease of industrial, but an increase of user plastics, with shipping and fisheries as the main sources. The EcoQO is now also used as an indicator for Good Environmental Status in the European Marine Strategy Framework Directive.

Monitoring the abundance of plastic debris in the marine environment.

Plastic debris has significant environmental and economic impacts in marine systems. Monitoring is crucial to assess the efficacy of measures implemented to reduce the abundance of plastic debris, but it is complicated by large spatial and temporal heterogeneity in the amounts of plastic debris and by our limited understanding of the pathways followed by plastic debris and its long-term fate. To date, most monitoring has focused on beach surveys of stranded plastics and other litter. Infrequent surveys of the standing stock of litter on beaches provide crude estimates of debris types and abundance, but are biased by differential removal of litter items by beachcombing, cleanups and beach dynamics. Monitoring the accumulation of stranded debris provides an index of debris trends in adjacent waters, but is costly to undertake. At-sea sampling requires large sample sizes for statistical power to detect changes in abundance, given the high spatial and temporal heterogeneity. Another approach is to monitor the impacts of plastics. Seabirds and other marine organisms that accumulate plastics in their stomachs offer a cost-effective way to monitor the abundance and composition of small plastic litter. Changes in entanglement rates are harder to interpret, as they are sensitive to changes in population sizes of affected species. Monitoring waste disposal on ships and plastic debris levels in rivers and storm-water runoff is useful because it identifies the main sources of plastic debris entering the sea and can direct mitigation efforts. Different monitoring approaches are required to answer different questions, but attempts should be made to standardize approaches internationally.