loanna Gkika

Per- and polyfluoroalkyl substances (PFAS) comprise a large and diverse group of compounds with unique characteristics that have led to their extensive use and consequent release into the environment. Despite the constantly growing body of information on PFAS environmental occurrence and bioaccumulation, important knowledge gaps on these aspects still remain. The aim of this thesis was therefore to assess the environmental distribution, bioaccumulation and trophic transfer of PFAS in aquatic and terrestrial ecosystems. Employing a stepwise approach, objective 1 was to translate the general knowledge gaps concerning PFAS environmental risk assessment into specific, actionable research priorities to steer subsequent experimental work. This was achieved by consulting publicly available literature and databases and the resulting research priorities were shaped into the experimental objectives of this thesis:

2. To expand the spectrum of PFAS screened for in environmental and biotic matrices.

3. To expand the spectrum of organisms and taxa in which PFAS concentrations and bioaccumulation are measured.

4. To assess and compare the trophic transfer of a wide variety of PFAS in a terrestrial and an aquatic food web.

5. To investigate how the presence of benthic invertebrates and their bioturbation activity affect PFAS bioaccumulation.

6. To examine if PFAS molecular descriptors can describe their environmental distribution concerning a) bioaccumulation in primary producers and invertebrates, b) trophic transfer at the base of the food web, and c) redistribution in sediment-plant systems.

Chapter 2 synthesized the recent advancements in PFAS environmental research and identified the remaining knowledge gaps and the subsequent research priorities to support a more comprehensive environmental risk assessment for PFAS. This was achieved by consulting the open literature and databases on the environmental occurrence, hazard, and risk of PFAS. Results revealed that the current knowledge on the environmental fate of PFAS is based on the analysis of less than 1% of the compounds categorized as PFAS. Moreover, soils and suspended particulate matter remain largely understudied. Bioavailability, bioaccumulation, and trophic transfer studies on PFAS also focus on only a very limited number of compounds and are biased toward aquatic biota, predominantly fish, and less frequently aquatic invertebrates and macrophytes. The available ecotoxicity data cover only a small number of PFAS and are also largely biased toward aquatic organisms. Therefore, ecotoxicity studies in the terrestrial environment, as well as chronic, multigenerational, and community ecotoxicity research are needed. Finally, there is an urgent need to unravel the relationships between sorption, bioaccumulation, and ecotoxicity on the one hand and molecular descriptors of PFAS chemical structures and physicochemical properties on the other, in order to allow predictions of exposure, bioaccumulation, and toxicity.

Addressing the research priority identified in chapter 2, chapter 3 investigated the distribution and bioaccumulation of various PFAS in a contaminated terrestrial and aquatic ecosystem. Subsequently, it was examined if the calculated bioaccumulation factors, relating concentrations in the organisms to concentrations in water, sediment or soil, were related to PFAS molecular descriptors. Abiotic and biotic samples were collected from the aquatic and terrestrial compartments of a PFAS-contaminated ecosystem and screened for 44 compounds. PFAS were found in all environmental compartments with varying profiles and concentrations. Generally, higher concentrations were found in aquatic than in terrestrial organisms, as well as in animals compared to plants. Biota-to-soil and biota-to-sediment accumulation factors (BSAFs) demonstrated a strong bioaccumulation of some PFAS, reaching 96,708 kg sediment/kg biota. Similarly, a high bioconcentration of PFAS from water was observed, with bioconcentration factors (BCFs) reaching 55,597 L water/kg biota. The membrane-water partition coefficient (Kmw) explained PFAS bioaccumulation to some extent in some cases, but our limited understanding of the interplay between the various factors driving PFAS bioaccumulation calls for further mechanistic research. Nonetheless, it was concluded that many of the 44 analyzed PFAS strongly bioaccumulate in terrestrial and aquatic primary producers and animals, making these compounds of serious and long-term environmental concern.

Subsequently, chapter 4 aimed to unravel the transfer of PFAS through a terrestrial and aquatic food web, jointly ending up in predatory spiders as the top predators. To this end, predatory spiders were collected from the same PFAS-contaminated ecosystem, simultaneously with the organisms studied in chapter 3. The spiders were screened for 44 PFAS, combining the results with those of the primary producers and invertebrates from chapter 3. The trophic position of the organisms was investigated using stable isotopes. PFAS were present in organisms from all trophic levels (primary producers, herbivores, detritivores, predators), albeit with varying total concentrations and profiles. Several PFAS appeared to biomagnify in the spiders through the terrestrial food web but were biodiluted through the aquatic food web. Very high concentrations were observed for some PFAS-organism combinations, and on top of that, chapter 4 proved that some PFAS have the potential to biomagnify. The apparent arbitrariness of which substances biomagnify and which biodilute, in combination with the trophic transfer of TFA, the smallest and most polar PFAS, emphasized that we still lack insight into the drivers of PFAS distribution in the environment, their uptake and trophic transfer.

Chapter 5 examined how organisms can affect the environmental distribution of PFAS. To this end, we measured the concentrations of 40 PFAS in sediments, assessed their bioaccumulation in a rooting macrophyte (Myriophyllum spicatum) and a benthic invertebrate worm (Lumbriculus variegatus), and examined the effects of the presence and bioturbation activity of the invertebrate on PFAS bioaccumulation in the plants. The macrophytes were exposed to sediments originating from a reference and a PFAS-contaminated site. After 28 days, the worms were introduced into half of the replicates, and at the end of the experiment (56 days), PFAS were quantified in all environmental compartments. Numerous targeted PFAS were detected in both the reference and the contaminated sediment and taken up by both organisms, with summed PFAS concentrations in organisms largely exceeding concentrations in the sediments. Bioaccumulation differed between organisms and sediment type. The presence of the worms significantly reduced the PFAS concentrations in the plant tissues, but for some compounds, root bioaccumulation increased in the presence of the worms. This effect was most prominent for the degradable PFAS precursors. It is concluded that organisms can shape their environment, thereby affecting the environmental distribution of PFAS, which emphasizes that contaminant-macroinvertebrate interactions are two-sided.

This thesis addressed some of the main research priorities related to the environmental distribution and bioaccumulation of PFAS. By expanding the spectrum of targeted PFAS to include understudied structures, the widespread presence of many of these newly analyzed compounds across multiple abiotic and biotic compartments was confirmed. The inclusion of various primary producers and invertebrates from terrestrial and aquatic ecosystems showed very high bioaccumulation factors for specific PFAS-organism combinations. To the best of our knowledge, the food-web transfer study presented here is the first one to combine various low trophic level organisms from a combined terrestrial and aquatic ecosystem, while targeting a broad spectrum of PFAS. Few studies have experimentally investigated how sediment reworking processes, like bioturbation, can affect PFAS bioaccumulation and environmental distribution, even less so for such a variety of PFAS structures. Our findings showed that the arrow affecting the environmental distribution of PFAS branches into several directions, since organisms can modify their environment and adjust their behavior, thereby affecting the distribution of PFAS in ecosystems in various ways. In order to capture this multidimensional nexus, we proposed a conceptual equation, as a first step towards better describing and predicting the capricious environmental distribution of the persistent and pervasive PFAS.