Modeling the Role of Microplastics in Bioaccumulation of Organic Chemicals to Marine Aquatic Organisms. A Critical Review

Abstract It has been shown that ingestion of microplastics may increase bioaccumulation of organic chemicals by aquatic organisms. This paper critically reviews the literature on the effects of plastic ingestion on the bioaccumulation of organic chemicals, emphasizing quantitative approaches and mechanistic models. It appears that the role of microplastics can be understood from chemical partitioning to microplastics and subsequent bioaccumulation by biota, with microplastic as a component of the organisms' diet. Microplastic ingestion may either clean or contaminate the organism, depending on the chemical fugacity gradient between ingested plastic and organism tissue. To date, most laboratory studies used clean test organisms exposed to contaminated microplastic, thus favouring chemical transfer to the organism. Observed effects on bioaccumulation were either insignificant or less than a factor of two to three. In the field, where contaminants are present already, gradients can be expected to be smaller or even opposite, leading to cleaning by plastic. Furthermore, the directions of the gradients may be opposite for the different chemicals present in the chemical mixtures in microplastics and in the environment. This implies a continuous trade-off between slightly increased contamination and cleaning upon ingestion of microplastic, a trade-off that probably attenuates the overall hazard of microplastic ingestion. Simulation models have shown to be helpful in mechanistically analysing these observations and scenarios, and are discussed in detail. Still, the literature on parameterising such models is limited and further experimental work is required to better constrain the parameters in these models for the wide range of organisms and chemicals acting in the aquatic environment. Gaps in knowledge and recommendations for further research are provided.

Keywords Additives • Bioaccumulation • Chemical transfer • Microplastic • Persistent organic pollutants

Introduction

Pollution with plastic debris and microplastic fragments has been recognized as a major problem in fresh water and marine systems (Derraik 2002; Andrady 2011; Koelmans et al. 2014a). Negative effects may relate to entanglement in plastic wires or nets, or to ingestion, which has been reported for benthic invertebrates, birds, fish, mammals and turtles. Extensive overviews of the deleterious effects of litter on marine life are provided by Kühn et al. (2015) and by Lusher (2015). Furthermore, it is generally assumed that microplastic may act as a vector for transport of chemicals associated with the plastic particles, such as persistent organic pollutants (POPs) or additives, residual monomers or oligomers of the component molecules of the plastics (hereafter referred to as 'additives') (Gouin et al. 2011; Teuten et al. 2007, 2009; Hammer et al. 2012; Browne et al. 2013; Rochman 2015; Lusher 2015). Hydrophobic chemicals including polychlorobiphenyls (PCB), polycyclic aromatic hydrocarbons (PAH) or polybrominated diethyl ethers (PBDEs), are known to concentrate in polymers such as polyvinylchloride (PVC), polyethylene (PE), polystyrene (PS) or polyoxymethylene (POM), which is the basis of using the latter materials in passive sampling devices (e.g. Hale et al. 2010). Microplastic particles present in seas and oceans have been found to contain considerable quantities of these chemicals (e.g. Ogata et al. 2009; Hirai et al. 2011). Concentrations of additives such as nonylphenol (NP), bisphenol A (BPA), PBDEs and phthalates also have been reported to be high in marine plastics, rendering them a potential source to the environment and marine biota. The question whether microplastic-mediated chemical transfer poses a serious actual hazard, however, depends on several other factors. First, for transport of the chemicals from plastic to an organism, a gradient that drives the chemical from plastic to the organism is required (Gouin et al. 2011; Koelmans et al. 2013a, b). If, however, a reverse gradient existed, ingestion would lead to cleaning of the organism and ingestion would in this sense be beneficial. Second, the chemical uptake through ingestion of plastic should be substantial compared to other exposure pathways, i.e. by food ingestion or uptake from ambient water. Because POPs as well as additives are ubiquitous in many environments, a dominant role of plastic ingestion is not self-evident (Koelmans et al. 2014b). Third, the chemical hazard of microplastic ingestion should relate to all the chemicals in the plastic-organism system, that is, the chemical mixture transferred to or from the organism by ingestion and chemicals should not be considered in isolation. A plastic additive may leach from a heavily contaminated plastic particle, but clean the organism from its body burden of legacy POPs at the same time. This means that there may be a trade-off between positive and negative effects of microplastic ingestion.

To date, a few controlled experimental studies have been published confirming transfer of chemicals from microplastic to marine organisms. Besseling et al. (2013) mimicked natural conditions by exposing relatively clean worms to mixtures of a natural marine sediment and PS microplastic, which were preequilibrated with PCBs, thus providing realistic exposure conditions. The presence of microplastic caused a small (factor of three) increase in bioaccumulation. However, bioaccumulation decreased again at higher concentrations. The authors argued that PS may not have caused PCB transfer but that the increased bioaccumulation probably had a biological cause, such as a change in lipid content or feeding rates. Browne et al. (2013) did not use natural sediment but exposed clean lug worms (Arenicola marina) to sand with 5 % of PVC microplastic that was presorbed with high concentrations of nonylphenol, phenanthrene, triclosan and/or PBDE-47. Because by using clean worms, a gradient from the PVC to the organism was created, chemical transfer from the particles to the worms occurred, but uptake from sand was larger than that from the PVC microplastic. Rochman et al. (2013b) exposed fish (Japanese medaka; Oryzias latipes) to contaminated food, to contaminated food mixed with 10 % virgin low density PE (LDPE) and to contaminated food mixed with LDPE that was pre-equilibrated in seawater. They observed an increase in body burdens up to a factor of 2.4 after two months, which was statistically significant for chrysene, PCB28 and most PBDEs. Chua et al. (2014) observed that adding PBDE-spiked microplastics to seawater with amphipods (Allorchestes compressa) in closed vials resulted in PBDE uptake by the amphipods, which was however only statistically significant compared to the controls when spiked concentrations were ten times higher than environmentally relevant concentrations. Addition of clean plastic to the same closed systems yet pre-contaminated with PBDEs resulted in a decreased uptake.

Considering the complex processes involved, modelling approaches have been proven useful for the interpretation of experimental data as well as for prognostic assessments of the possible hazards caused by plastic ingestion. Model-based scenario studies have helped to define in which cases plastic ingestion may be relevant, dependent on plastic type, chemical properties and species traits. The aim of this chapter is to present and critically discuss the model approaches used to quantify the effect of plastic on bioaccumulation of POPs and additives. This includes a mathematical description of the processes at play, a review of the model-based inferences described in the literature, and an outlook to future work and recommendations.