The driving factors of per- and polyfluorinated alkyl substance (PFAS) accumulation in selected fish species: The influence of position in river continuum, fish feed composition, and pollutant properties

Highlights

• Geographical trends of PFAS contamination were found in the Czech largest rivers.

• Bioaccumulation of PFAS in fish and isotopic ratios were studied.

• PFAS concentrations increased downstream and were positively correlated with δ¹⁵N.

• Relationship between accumulations and species with different diets was revealed.

• Molecular mass and fluorine number play crucial roles in PFAS bioaccumulation.

Abstract

Per- and polyfluorinated alkyl substances (PFASs) represent a group of highly recalcitrant micropollutants, that continuously endanger the environment. The present work describes the geographical trends of fish contamination by individual PFASs (including new compounds, e.g., Gen-X) assessed by analyzing the muscle tissues of 5 separate freshwater fish species from 10 locations on the Czech section of the Elbe River and its largest tributary, the Vltava River. The data of this study also showed that the majority of the detected PFASs consisted of long-chain representatives (perfluorooctane sulfonate (PFOS), perfluorononanoic acid, perfluorodecanoic acid, and perfluoroundecanoic acid), whereas short-chain PFASs as well as other compounds such as Gen-X were detected in relatively small quantities. The maximum concentrations of the targeted 32 PFASs in fish were detected in the lower stretches of the Vltava and Elbe Rivers, reaching 289.9 ng/g dw, 140.5 ng/g dw, and 162.7 ng/g dw for chub, roach, and nase, respectively. Moreover, the relationships between the PFAS (PFOS) concentrations in fish muscle tissue and isotopic ratios (δ¹⁵N and δ¹³C) were studied to understand the effect of feed composition and position in the river continuum as a proxy for anthropogenic activity. Redundancy analysis and variation partitioning showed that the largest part of the data variability was explained by the interaction of position in the river continuum and δ¹⁵N (δ¹³C) of the fish. The PFAS concentrations increased downstream and were positively correlated with δ¹⁵N and negatively correlated with δ¹³C. A detailed study at one location also demonstrated the significant relationship between δ¹⁵N (estimated trophic position) and PFASs (PFOS) concentrations. From the tested physicochemical properties, the molecular mass and number of fluorine substituents seem to play crucial roles in PFAS bioaccumulation.

Introduction

Per- and polyfluorinated alkyl substances (PFASs) are a group of global pollutants of main concern (Nakayama et al., 2019). The structure of PFASs is composed of a partially or fully fluorinated alkyl chain and a polar functional group. Due to its unique molecular architecture, a broad range of PFASs display often hydrophobic and lipophobic properties and are in high demand in many industrial sectors (Prevedouros et al., 2006; Rayne and Forest, 2009). On the other hand, the strong carbon–fluorine bonds in the fluorinated alkyl chain create a high resistance to abiotic degradation and even greater resistance to biodegradation (Merino et al., 2016). The most common and environmentally relevant representatives of PFASs, which differ only in their alkyl chain lengths and polar nonfluorinated functional groups, are sulfonates (PFSAs), carboxylates (PFCAs), sulfonamides (FASAs), and fluorotelomer acrylates and sulfonates (e.g., FTCAs and FTSAs) (Buck et al., 2011). Two representatives of PFASs, perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS), are already included in the Stockholm Convention and are restricted and regulated as persistent organic pollutants (POPs) (Sznajder-Katarzyńska et al., 2019). In spite of regulations, both of these compounds are still widely detected across the environment in large quantities. The detection of PFASs in environmental matrices such as ground and surface water, soil, biota, and sediments demonstrates a global level of contamination by these anthropogenic compounds (Ahrens et al., 2010).

There are many potential sources of PFASs in surface water; however, wastewater treatment plant effluents, surface runoff, and industrial activity play a crucial role in the contamination of water bodies by PFASs and in the exposure of aquatic biota (Ahrens and Bundschuh, 2014; Kunacheva et al., 2011; Xiao et al., 2012). Moreover, rivers consist of connected but constantly changing habitats, which are known as river continuums. The position in the river continuum, which can be described by the distance from the sea, exerts effects on many environmental properties, such as the proportions of allochthonous and autochthonous resources at the bottom of the food web, sediment quality, oxygen levels, and transport and accumulation of pollutants. For example, the geographical position of fish in rivers could influence the total accumulated mercury concentrations (Cyr et al., 2017).

In the last two decades, many authors have studied the adverse effects of PFASs on fish and have found PFAS-induced endocrine disruption of the thyroid system, developmental and reproductive toxicity, and metabolism disturbances (Lee et al., 2020). Because of their high bioaccumulation potential, even low concentrations of long-chain PFASs in water could present a risk for aquatic organisms, and through the food chain, the top predators could be more severely affected (Loi et al., 2011; Ng and Hungerbühler, 2014). Therefore, PFAS accumulation in fish can directly pose a risk to human health (Mazzoni et al., 2019; Zhao et al., 2011). Even in the most remote areas that are far from the production and use of PFASs (e.g., mountain lakes and the Qinghai–Tibet Plateau), these compounds have been detected in fish tissue (Shi et al., 2010). Many authors have already documented PFAS contamination in various freshwater fish species in Asia, South and North America, Africa, and Australia. This contamination has also been documented in Europe, including the Czech Republic (Cerveny et al., 2018, Cerveny et al., 2016; Hlouskova et al., 2013; Svihlikova et al., 2015). The accumulation of common PFAS representatives (e.g., PFSAs, PFCAs, FASAs) in fish has already been demonstrated; however, the differences in the concentrations among different species/trophic levels/positions in the river remain unclear, even though this parameter could be crucial in risk assessments of fish used for human consumption. Some current studies have found no significant magnification of PFAS levels in the aquatic food web, including fish (Lescord et al., 2015; Verhaert et al., 2017; Zhou et al., 2012). On the other hand, the higher PFAS concentrations in piscivorous fish and recent studies combining stable isotope analysis (used to determine the trophic position) and diet residue determinations suggest the opposite (Babut et al., 2017; Groffen et al., 2018; Ye et al., 2008).

The Vltava River and the lower part of the Elbe River, the two largest rivers in the Czech Republic, have been selected to monitor the current PFAS contamination of surface waters in this area. Despite the spread of contamination and bioaccumulative potential of PFOS and PFOA in aquatic biota, only limited information is available about other PFASs, including new compounds such as short-chain PFASs (short-chain PFASs having the number of perfluorinated carbons < 7; long-chain PFASs > 7) and GenX. Incorporating the analysis of these compounds in this study helped to determine their environmental fates. By using freshwater fish as a bioindicator, geographical contamination trends were discovered, and a potential source was suggested. Moreover, the spatial distribution of PFASs within one sampled locality is also discussed. Finally, the relationships among fish species and size, distance from the sea, isotopic abundance (δ¹⁵N and δ¹³C), and PFAS concentrations in muscle tissues were studied to determine the leading factors for bioaccumulation. We expect that the trophic position of fish in the food chain and the distance of fish habitats from the sea would be major factors that would influence PFAS contamination.