Steven J. Brooks

The environmental fate and effects of antifouling paint biocides

Antifouling (AF) biocides are the active ingredients in AF paints that prevent the settlement, adhesion and growth of organisms to a painted surface. A wide range of chemicals are used as AF biocides, which have very different physico-chemical properties and therefore differing environmental fates, behaviour and effects. Copper has been used as an antifoulant for centuries and extensive research has been performed to understand how copper speciation influences bioavailability and toxicity. For biocides that have been widely used over a number of decades, for example Irgarol 1051 and diuron, there are a large amount of environmental data in the public domain, including for their respective metabolites, that allows their environmental safety and potential risk to the environment to be assessed. For other biocides such as dichlofluanid, DCOIT (SeaNine 211) and zinc/copper pyrithione, there is a good understanding of their fate and effects. However, few monitoring studies have been performed and not so much is known about the fate and effects of their metabolites. There are also new or candidate biocides such as triphenylborane pyridine, Econea, capsaicin and medetomidine for which there is very little information in the public domain. This review provides an overview of the environmental fate and occurrence data that are in the public domain for AF biocides and provides some insight into the effects of these compounds on non-target organisms.

Seasonal variation in biomarkers in blue mussel (Mytilus edulis), Icelandic scallop (Chlamys islandica) and Atlantic cod (Gadus morhua)—Implications for environmental monitoring in the Barents Sea

In the Barents Sea, the limited data on biological relevant indicators and their responses to various anthropogenic stressors have hindered the development of a consistent scientific basis for selecting indicator species and developing practical procedures for environmental monitoring. Accordingly, the main aim of the present study was to develop a common set of baseline values for contaminants and biomarkers in three species, and to identify their strengths and limitations in monitoring of the Barents Sea. Blue mussel (Mytilus edulis), Icelandic scallop (Chlamys islandica) and Atlantic cod (Gadus morhua) were sampled from a north Norwegian fjord in March, June, September and December 2010. Digestive glands from the bivalve species and liver from Atlantic cod were analysed for biomarkers of oxidative stress (catalase [CAT], glutathione peroxidase [GPX], glutathione-S-transferase activities [GST], lipid peroxidation as thiobarbituric reactive substances [TBARS] and total oxyradical scavenging capacity [TOSC]), biotransformation (ethoxyresorufine-O-deethylase activity [EROD]) and general stress (lysosomal membrane stability [LMS]). Concentrations of polycyclic aromatic hydrocarbons (PAHs) and metals in the bivalves and PAH metabolites in fish bile were quantified. Finally, energy reserves (total lipids, proteins and carbohydrates) and electron transport system (ETS) activity in the digestive gland of the bivalves and liver of Atlantic cod provided background information for reproductive cycle and general physiological status of the organisms. Blue mussel and Icelandic scallop showed very similar trends in biological cycle, biomarker expression and seasonality. Biomarker baselines in Atlantic cod showed weaker seasonal variability. However, important biological events may have been undetected due to the large time intervals between sampling occasions. Physiological biomarkers such as energy reserves and ETS activity were recommended as complementary parameters to the commonly used stress biomarkers, as they provided valuable information on the physiological status of the studied organisms. Interpretation of the seasonality in oxidative stress biomarkers was in general difficult but TOSC and lipid peroxidation were preferred over the antioxidant enzyme activities. This study is the first reporting seasonal baseline in these three species in a sub-Arctic location. Overall, the Icelandic scallop was considered the most adequate organism for environmental monitoring in the Barents Sea due to the interpretability of the biomarker data as well as its abundance, ease to handle and wide distribution from the southern Barents Sea to Svalbard.

Water Column Monitoring of the Biological Effects of Produced Water from the Ekofisk Offshore Oil Installation from 2006 to 2009

The Norwegian water column monitoring program investigates the biological effects of offshore oil and gas activities in Norwegian waters. In three separate surveys in 2006, 2008, and 2009, bioaccumulation and biomarker responses were measured in mussels (Mytilus edulis) and Atlantic cod (Gadus morhua) held in cages at known distances from the produced water (PW) discharge at the Ekofisk oil field. Identical monitoring studies performed in all three years have allowed the biological effects and bioaccumulation data to be compared, and in addition, enabled the potential environmental benefits of a PW treatment system (CTour), implemented in 2008, to be evaluated. The results of the 2009 survey showed that caged animals were exposed to low levels of PW components, with highest tissue concentrations in mussels located closest to the PW discharge. Mussels located approximately 1–2 km away demonstrated only background concentrations of target compounds. Concentrations of polycyclic aromatic hydrocarbons (PAH) and alkyl phenol (AP) metabolites in the bile of caged cod were elevated at stations 200–250 m from the discharge. There was also a signal of exposure relative to discharge for the biomarkers CYP1A in fish and micronuclei in mussels. All other fish and mussel biomarkers showed no significant exposure effects in 2009. The mussel bioaccumulation data in 2009 indicated a lower exposure to the PW effluent than seen previously in 2008 and 2006, resulting in an associated general improvement in the health of the caged mussels. This was due to the reduction in overall discharge of PW components (measured as oil in water) into the area in 2009 compared to previous years as a result of the improved PW treatment system.

Integrated biomarker assessment of the effects exerted by treated produced water from an onshore natural gas processing plant in the North Sea on the mussel Mytilus edulis

The biological impact of a treated produced water (PW) was investigated under controlled laboratory conditions in the blue mussel, Mytilus edulis. Mussel health status was assessed using an integrated biomarker approach in combination with chemical analysis of both water (with SPMDs), and mussel tissues. Acyl-CoA oxidase activity, neutral lipid accumulation, catalase activity, micronuclei formation, lysosomal membrane stability in digestive cells and haemocytes, cell-type composition in digestive gland epithelium, and the integrity of the digestive gland tissue were measured after 5 week exposure to 0%, 0.01%, 0.1%, 0.5% and 1% PW. The suite of biomarkers employed were sensitive to treated PW exposure with significant sublethal responses found at 0.01-0.5% PW, even though individual chemical compounds of PW were at extremely low concentrations in both water and mussel tissues. The study highlights the benefits of an integrated biomarker approach for determining the potential effects of exposure to complex mixtures at low concentrations. Biomarkers were integrated in the Integrative Biological Response (IBR/n) index.

Biomarker Responses in Mussels, an Integrated Approach to Biological Effects Measurements

Biological effects techniques have been used with the aim to further integrate biological effects measurements with chemical analysis and apply these methods to provide an assessment of mussel health status. Live native mussels were collected from selected coastal and estuarine sites around the British Isles, including the rivers Test, Thames, Tees, and Clyde, and Lunderston Bay. A suite of biological effects techniques was undertaken on these mussels, including whole organism responses (scope for growth), tissue responses (histopathology), and subcellular responses (lysosomal stability, multi-xenobiotic resistance [MXR], and Comet assay). In addition, whole mussel homogenates were used to measure organic (polycyclic aromatic hydrocarbons [PAH], polychlorinated biphenyls [PCB]) and metal concentrations. Overall the mussels collected from the Thames were in relatively poor health, based on histopathological markers, significantly higher DNA damage, and elevated expression of MXR detoxifying proteins. In contrast, the mussels collected from the River Test were in the best health, based on histopathological markers, respiration rate (SFG), and low frequency of DNA damage. In conclusion, the biological effects techniques were able to distinguish between relatively contaminated and clean environments, with the Thames mussels in worst health. Mussel tissue chemistry data were not able to explain the variations in biological response. Evidence indicates that the difference in the health of the mussels between the different sites was due to either effects of contaminants that were not measured, or the combined effects of mixture toxicity resulting in a threshold effect.

Field comparison of passive sampling and biological approaches for measuring exposure to PAH and alkylphenols from offshore produced water discharges.

Polycyclic aromatic hydrocarbons (PAH) and alkylphenols (AP) that are present in routine discharges of produced water (PW) from the offshore industry continue to cause concern. The suitability of biological methods and chemical based passive samplers to determine exposure to these compounds was tested by deploying them around an oil installation and at reference locations in the North Sea. PAH and AP were analysed either as parent compounds in passive samplers and mussel tissue or as metabolites in fish bile. Generally the pattern of exposure relative to proximity to the discharge was represented by mussels, SPMDs and fish for PAH. Fish and SPMDs showed good correlation for PAH accumulations, whereas some differences were apparent between mussels and SPMDs. POCIS was the only technique tested that could accurately measure the most abundant AP in PW. The advantages of biologically independent measures of exposure for inclusion in discharge monitoring studies are outlined.

Effects of dissolved organic carbon on the toxicity of copper to the developing embryos of the pacific oyster (Crassostrea gigas)

The effects of humic acid (HA) on copper speciation and its subsequent toxicity to the sensitive early life stages of the Pacific oyster (Crassostrea gigas) are presented. Differential pulse anodic stripping voltammetry with a hanging mercury drop electrode was used to measure the copper species as labile copper (LCu; free ion and inorganic copper complexes) and total copper (TCu) with respect to increasing HA concentration. The TCu and LCu 50% effect concentrations (EC50s) in the absence of HA were 20.77 microg/L (95% confidence interval [CI], 24.02-19.97 microg/L) and 8.05 microg/L (95% CI, 9.6-5.92 microg/L) respectively. A corrected dissolved organic carbon (DOC) concentration (HA only) of 1.02 mg/L was required to significantly increase the TCu EC50 to approximately 41.09 microg/L (95% CI, 44.27-37.52 microg/L; p < 0.05), almost doubling that recorded when DOC (as HA) was absent from the test media. In contrast, the LCu EC50 was unaffected by changes in DOC concentration and was stable throughout the corrected DOC concentration range. The absence of change in the LCu EC50, despite increased HA concentration, suggests that the LCu fraction, not TCu, was responsible for the observed toxicity to the oyster embryo. This corresponds with the current understanding of copper toxicity and supports the free-ion activity model for copper toxicity.

Blue mussels (Mytilus edulis spp.) as sentinel organisms in coastal pollution monitoring: A review

The blue mussel (Mytilus spp.) is widely used as a bioindicator for monitoring of coastal water pollution (mussel watch programs). Herein we provide a review of this study field with emphasis on: the suitability of Mytilus spp. as environmental sentinels; uptake and bioaccumulation patterns of key pollutant classes; the use of Mytilus spp. in mussel watch programs; recent trends in Norwegian mussel monitoring; environmental quality standards and background concentrations of key contaminants; pollutant effect biomarkers; confounding factors; particulate contaminants (microplastics, engineered nanomaterials); climate change; harmonization of monitoring procedures; and the use of deployed mussels (transplant caging) in pollution monitoring. Lastly, the overall state of the art of blue mussel pollution monitoring is discussed and some important issues for future research and development are highlighted.

Integrated coastal monitoring of a gas processing plant using native and caged mussels

The biological effects of a coastal process water (PW) discharge on native and caged mussels (Mytilus edulis) were assessed. Chemical analyses of mussel tissues and semi permeable membrane devices, along with a suite of biomarkers of different levels of biological complexity were measured. These were lysosomal membrane stability in haemocytes and digestive cells; micronuclei formation in haemocytes; changes in cell-type composition in the digestive gland epithelium; integrity of digestive gland tissue; peroxisome proliferation; and oxidative stress. Additionally the Integrative Biological Response (IBR/n) index was calculated. This integrative biomarker approach distinguished mussels, both native and caged, exhibiting different stress conditions not identified from the contaminant exposure. Mussels exhibiting higher stress responses were found with increased proximity to the PW discharge outlet. However, the biological effects reported could not be entirely attributed to the PW discharge based on the chemicals measured, but were likely due to either other chemicals in the discharge that were not measured, the general impact of the processing plant and or other activities in the local vicinity.

Integrated biomarker assessment of the effects of tailing discharges from an iron ore mine using blue mussels (Mytilus spp.).

The blue mussel (Mytilus spp.) has been used to assess the potential biological effects of the discharge effluent from the Sydvaranger mine, which releases its tailings into Bøk fjord at Kirkenes in the north of Norway. Metal bioaccumulation and a suite of biomarkers were measured in mussels positioned for 6 weeks at varying distances from the discharge outlet. The biomarkers used included: stress on stress (SS); condition index (CI); cellular energy allocation (CEA); micronuclei formation (MN); lysosomal membrane stability (LMS), basophilic cell volume (VvBAS); and neutral lipid (NL) accumulation. The individual biomarkers were integrated using the integrated biological response (IBR/n) index. The accumulation of Fe was significantly higher in mussels located closer to the discharge outlet, indicating that these mussels had been exposed to the suspended mine effluent. The IBR/n results were in good agreement with the location of the mussels in relation to the distance from the discharge outlet and expected exposure to the mine effluent. Several biomarkers showed responses resulting in higher IBR/n values of analysed mussels within a 3 km distance from the tailing discharge.