Exposure and effects of sediment-spiked fludioxonil on macroinvertebrates and zooplankton in outdoor aquatic microcosms
Graphical abstract
Introduction
Sediments of freshwater ecosystems are reported to be a sink and source of organic contaminants (Warren et al., 2003) and to play a crucial role in supporting ecosystem services. For example, the sediment compartment functions as habitat for benthic organisms and is the major environmental compartment where processes including mineralisation, decomposition and bioremediation take place (Covich et al., 1999, Wall, 2004, EFSA (European Food Safety Authority), 2015, Diepens et al., 2017). Edge-of-field surface waters may become exposed to agricultural pesticides e.g. via spray drift, surface run-off and/or drainage (Schulz, 2004, Brock et al., 2010). Lipophilic pesticides can adsorb to organic matter, and in particular to sediments, where they may persist, potentially leading to toxic effects on benthic organisms (McKnight et al., 2015, Boyle et al., 2016, Brock et al., 2016). Experimental information on benthic population- and community-level effects of sediment-exposure to these substances is scarce (Diepens et al., 2014, EFSA (European Food Safety Authority), 2015). However, this information is required to evaluate the protectiveness of the effect assessment procedure, based on sediment-spiked laboratory toxicity tests, to derive Regulatory Acceptable Concentrations (RACs) or Environmental Quality Standards (EQSs) for sediment organisms (EC (European Commission), 2011, EFSA (European Food Safety Authority), 2013, EFSA (European Food Safety Authority), 2015). For this reason, we conducted a sediment-spiked outdoor microcosm experiment with the lipophilic fungicide fludioxonil as a benchmark compound.
The properties and agricultural use of fludioxonil trigger a risk assessment for sediment organisms. Important properties to consider as triggers are: (i) sorption behaviour, (ii) persistence in sediment and (iii) mode-of-action and toxicity to non-target organisms. Maund et al. (1997) proposed the following quantitative trigger values for sediment ERA: (1) KOC (soil organic carbon – water partitioning coefficient) ≥ 1000, (2) laboratory aerobic soil half-life time ≥ 30 days, and (3) a Daphnia 48 h concentration where 50% effect was observed/calculated (48 h-EC50) < 1 mg/L or a 21-d No Observed Effect Concentration (NOEC) < 0.1 mg/L. In guidance provided by EFSA (2013) sediment toxicity studies with pesticides are triggered when (a) the water-sediment dissipation study (OECD, 2002) indicates that > 10% of the applied radioactivity (labelled active substance) is present in the sediment at or after day 14 and (b) the outcome of a chronic Daphnia test (or another comparable study with a relevant crustacean or insect) results in an EC10 or NOEC < 0.1 mg/L. For fludioxonil a KOC of 145,600, a half-live > 365 days in a laboratory water-sediment system and a 21-d NOEC of 5 μg/L for Daphnia magna are reported (EFSA, 2007).
According to EFSA (2007) the Predicted Exposure Concentrations (PECs) for fludioxonil in sediments of edge-of-field surface waters are 1.28 mg fludioxonil/kg dry sediment at FOCUS step 1 and 0.001–0.02 mg/kg at FOCUS step 3 (realistic worst-case). Chemical monitoring in sediments of a small river basin near vineyards in Spain revealed a maximum fludioxonil concentration of 0.012 mg a.s./kg dry sediment (Bermúdez-Couso et al., 2007). In sediments of lake Lugano (Italy) 0.00035 mg fludioxonil/kg dry sediment was detected (Chiaia-Hermandez et al., 2014).
Since this study was aimed at obtaining higher-tier data that can be used to evaluate the lower tier prospective effect assessment procedure for sediment organisms, the selected range in exposure concentrations was not based on predicted PECsed values and/or measured fludioxonil concentrations in sediments, but on the available 28d-NOEC of 40 mg fludioxonil/kg dry sediment derived from a sediment-spiked laboratory toxicity test with the non-biting midge Chironomus riparius. Chironomus species are the most frequently studied test species in chronic sediment-spiked toxicity tests for pesticides (Deneer et al., 2013). Chronic toxicity values from sediment-spiked toxicity tests with other non-arthropod benthic test species were not available in the open literature for fludioxonil. A priori, in our microcosm experiment, we assumed no population and community-level effects on benthic organisms at sediment exposure concentrations a factor of 10 lower than 40 mg fludioxonil/kg dry sediment (4 mg a.s/kg dry weight sediment is the current Tier-1 RACsed) but clear ecological effects at sediment exposure concentrations above the 28d NOEC value for C. riparius.
Fludioxonil [4-(2,2-difluoro-1,3-benzodioxol-4-yl)-1H-pyrrole-3-carbonitrile] is a non-systemic fungicide. It acts as an osmotic mimic, stimulating glycerol synthesis via the mitogen-activated protein kinase pathway, leading to excessive intracellular glycerol accumulation resulting in hyphal swelling, germ tube abnormalities, and cell lysis (Kanetis et al., 2008). Fludioxonil is widely used as a foliar, seed and post-harvest treatment application to control diseases caused by fungi in the class of Ascomycetes, Basidiomycetes and Deuteromycota (Fungi imperfecti) (EFSA, 2007). Many fungicides, however, are reported to have biocidal properties in the sense that they affect a wider array of aquatic organisms including the sensitivity of invertebrates and algae (Maltby et al., 2009, Van Wijngaarden et al., 2010, Lin et al., 2012), the composition of microbial communities (Dimitrov et al., 2014) and the feeding rate of Gammarus fossarum (Zubrod et al., 2014).
The ecotoxicological research conducted with the selected benchmark fungicide fludioxonil aims to evaluate the consistency and protectiveness of the tiered sediment effect assessment procedure currently used (EFSA, 2013) and proposed (EFSA, 2015) by the European Food Safety Authority (EFSA) for plant protection products. The specific aims of this paper are (i) to describe the exposure dynamics of fludioxonil in total sediment, sediment pore water and overlying water of the sediment-spiked microcosm experiment and (ii) to assess population- and community-level responses of the fludioxonil-treatments on benthic and pelagic macroinvertebrates and pelagic zooplankton.
Section snippets
Spiking of sediment
Early June 2016, approximately 650 L of sediment was collected from experimental ditches at the Sinderhoeve field station, Renkum, The Netherlands. These ditches were not used for ecotoxicological experiments after the introduction of sediment from an unpolluted lake in 2008. The collected sediment was sieved (mesh size 1 mm), well-mixed and divided into 24 equal portions of 27 L of wet sediment. This sediment contained, on average 53.8% w/w water and an organic carbon (OC) content of 1.85% w/w in
Exposure concentrations of fludioxonil in total sediment
Concentrations in the sediment compartment as mg a.s./kg dry sediment are given in Fig. 1A (see also SI Table 1). As expected, higher concentrations were measured with increasing treatment-level. A faster decline in fludioxonil concentration in the total sediment was observed between day 0 and day 28 than later on, particularly at the highest treatment levels. Furthermore, the dissipation rate of fludioxonil in the sediment increased with increasing treatment level. In the microcosms constructed
Exposure concentrations of fludioxonil in the microcosms test system
An important aim of this microcosm study was studying effects of sediment-exposure to fludioxonil on sediment-dwelling organisms to validate the tiered effect assessment procedure for deriving regulatory acceptable concentrations (RACs) for sediment organisms. For this purpose we used spiked sediment to construct the microcosms, instead of following the traditional approach in constructing the microcosms with ‘clean’ sediment and to spike the water column. Although EFSA (2015) considers both
Conclusions
The sediment-spiked outdoor freshwater microcosm experiment conducted with fludioxonil (lipophilic, non-systemic fungicide) showed that the test compound persisted in the sediment causing long-term exposure to sediment-dwelling organisms. Also exposure to pelagic organisms was long-term, due to partitioning of fludioxonil between sediment and overlying water. Measured sediment pore water concentrations of fludioxonil were approximately 16 to 26 times higher those in overlying water.
Of the
Acknowledgements
The research was financially supported by the Dutch Ministry of Economic Affairs (TKI project 5200043069) and the European Crop Protection Association. The participation of Xiao H. Yin was financially supported by the China Scholarship Council. We like to thank Steven Crum for his help in the analysis of fludioxonil and Marieke Wolters for her assistance in processing the samples from the microcosm experiment.
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