Systematic Underestimation of Pesticide Burden for Invertebrates Under Field Conditions: Comparing the Influence of Dietary Uptake and Aquatic Exposure Dynamics

Overview

Journal ACS Environ Au

Publisher American Chemical Society

Date 2023 Apr 27

PMID 37101586

Authors

Benedikt B Lauper

Eva Anthamatten

Johannes Raths

Maricor Arlos

Juliane Hollender

Affiliations

Soon will be listed here.

Abstract

Pesticides used in agriculture can end up in nearby streams and can have a negative impact on nontarget organisms such as aquatic invertebrates. During registration, bioaccumulation potential is often investigated using laboratory tests only. Recent studies showed that the magnitude of bioaccumulation in the field substantially differs from laboratory conditions. To investigate this discrepancy, we conducted a field bioaccumulation study in a stream known to receive pollutant loadings from agriculture. Our work incorporates measurements of stream pesticide concentrations at high temporal resolution (every 20 min), as well as sediment, leaves, and caged gammarid analyses (every 2-24 h) over several weeks. Of 49 investigated pesticides, 14 were detected in gammarids with highly variable concentrations of up to 140 ± 28 ng/g. Toxicokinetic modeling using laboratory-derived uptake and depuration rate constants for azoxystrobin, cyprodinil, and fluopyram showed that despite the highly resolved water concentrations measured, the pesticide burden on gammarids remains underestimated by a factor of 1.9 ± 0.1 to 31 ± 3.0, with the highest underestimations occurring after rain events. Including dietary uptake from polluted detritus leaves and sediment in the model explained this underestimation only to a minor proportion. However, suspended solids analyzed during rain events had high pesticide concentrations, and uptake from them could partially explain the underestimation after rain events. Additional comparison between the measured and modeled data showed that the pesticide depuration in gammarids is slower in the field. This observation suggests that several unknown mechanisms may play a role, including lowered enzyme expression and mixture effects. Thus, it is important to conduct such retrospective risk assessments based on field investigations and adapt the registration accordingly.

Citing Articles

Elimination Resistance: Characterizing Multi-compartment Toxicokinetics of the Neonicotinoid Thiacloprid in the Amphipod Using Bioconcentration and Receptor-Binding Assays.

Raths J, Schinz L, Mangold-Doring A, Hollender J Environ Sci Technol. 2023; 57(24):8890-8901.

PMID: 37283463 PMC: 10286312. DOI: 10.1021/acs.est.3c01891.

Speed it up: How temperature drives toxicokinetics of organic contaminants in freshwater amphipods.

Raths J, Svara V, Lauper B, Fu Q, Hollender J Glob Chang Biol. 2022; 29(5):1390-1406.

PMID: 36448880 PMC: 10107603. DOI: 10.1111/gcb.16542.

References

Svara V, Krauss M, Michalski S, Altenburger R, Brack W, Luckenbach T . Chemical Pollution Levels in a River Explain Site-Specific Sensitivities to Micropollutants within a Genetically Homogeneous Population of Freshwater Amphipods. Environ Sci Technol. 2021; 55(9):6087-6096. DOI: 10.1021/acs.est.0c07839. View

Miller T, McEneff G, Brown R, Owen S, Bury N, Barron L . Pharmaceuticals in the freshwater invertebrate, Gammarus pulex, determined using pulverised liquid extraction, solid phase extraction and liquid chromatography-tandem mass spectrometry. Sci Total Environ. 2014; 511:153-60. DOI: 10.1016/j.scitotenv.2014.12.034. View

Meredith-Williams M, Carter L, Fussell R, Raffaelli D, Ashauer R, Boxall A . Uptake and depuration of pharmaceuticals in aquatic invertebrates. Environ Pollut. 2012; 165:250-8. DOI: 10.1016/j.envpol.2011.11.029. View

Schwarzenbach R, Escher B, Fenner K, Hofstetter T, Johnson C, von Gunten U . The challenge of micropollutants in aquatic systems. Science. 2006; 313(5790):1072-7. DOI: 10.1126/science.1127291. View

Bjergager M, Hanson M, Lissemore L, Henriquez N, Solomon K, Cedergreen N . Synergy in microcosms with environmentally realistic concentrations of prochloraz and esfenvalerate. Aquat Toxicol. 2011; 101(2):412-22. DOI: 10.1016/j.aquatox.2010.11.004. View

Konschak M, Zubrod J, Baudy P, Fink P, Kenngott K, Luderwald S . The importance of diet-related effects of the antibiotic ciprofloxacin on the leaf-shredding invertebrate Gammarus fossarum (Crustacea; Amphipoda). Aquat Toxicol. 2020; 222:105461. DOI: 10.1016/j.aquatox.2020.105461. View

Malaj E, von der Ohe P, Grote M, Kuhne R, Mondy C, Usseglio-Polatera P . Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale. Proc Natl Acad Sci U S A. 2014; 111(26):9549-54. PMC: 4084479. DOI: 10.1073/pnas.1321082111. View

Chiaia-Hernandez A, Krauss M, Hollender J . Screening of lake sediments for emerging contaminants by liquid chromatography atmospheric pressure photoionization and electrospray ionization coupled to high resolution mass spectrometry. Environ Sci Technol. 2012; 47(2):976-86. DOI: 10.1021/es303888v. View

Dorn A, Hammel K, Dalkmann P, Faber D, Hellpointner E, Lamshoeft M . What is the actual exposure of organic compounds on Chironomus riparius? - A novel methodology enabling the depth-related analysis in sediment microcosms. Chemosphere. 2021; 279:130424. DOI: 10.1016/j.chemosphere.2021.130424. View

10.

Dalhoff K, Gottardi M, Rinnan A, Rasmussen J, Cedergreen N . Seasonal sensitivity of Gammarus pulex towards the pyrethroid cypermethrin. Chemosphere. 2018; 200:632-640. DOI: 10.1016/j.chemosphere.2018.02.153. View

11.

Camp A, Buchwalter D . Can't take the heat: Temperature-enhanced toxicity in the mayfly Isonychia bicolor exposed to the neonicotinoid insecticide imidacloprid. Aquat Toxicol. 2016; 178:49-57. DOI: 10.1016/j.aquatox.2016.07.011. View

12.

Inostroza P, Wicht A, Huber T, Nagy C, Brack W, Krauss M . Body burden of pesticides and wastewater-derived pollutants on freshwater invertebrates: Method development and application in the Danube River. Environ Pollut. 2016; 214:77-85. DOI: 10.1016/j.envpol.2016.03.064. View

13.

Richardson S . Environmental mass spectrometry: emerging contaminants and current issues. Anal Chem. 2011; 84(2):747-78. DOI: 10.1021/ac202903d. View

14.

Englert D, Zubrod J, Link M, Mertins S, Schulz R, Bundschuh M . Does Waterborne Exposure Explain Effects Caused by Neonicotinoid-Contaminated Plant Material in Aquatic Systems?. Environ Sci Technol. 2017; 51(10):5793-5802. DOI: 10.1021/acs.est.7b00827. View

15.

Xie Z, Lu G, Liu J, Yan Z, Ma B, Zhang Z . Occurrence, bioaccumulation, and trophic magnification of pharmaceutically active compounds in Taihu Lake, China. Chemosphere. 2015; 138:140-7. DOI: 10.1016/j.chemosphere.2015.05.086. View

16.

Bundschuh M, Zubrod J, Kosol S, Maltby L, Stang C, Duester L . Fungal composition on leaves explains pollutant-mediated indirect effects on amphipod feeding. Aquat Toxicol. 2011; 104(1-2):32-7. DOI: 10.1016/j.aquatox.2011.03.010. View

17.

Rosch A, Anliker S, Hollender J . How Biotransformation Influences Toxicokinetics of Azole Fungicides in the Aquatic Invertebrate Gammarus pulex. Environ Sci Technol. 2016; 50(13):7175-88. DOI: 10.1021/acs.est.6b01301. View

18.

Kleinow K, Melancon M, Lech J . Biotransformation and induction: implications for toxicity, bioaccumulation and monitoring of environmental xenobiotics in fish. Environ Health Perspect. 1987; 71:105-19. PMC: 1474347. DOI: 10.1289/ehp.8771105. View

19.

Rosch A, Gottardi M, Vignet C, Cedergreen N, Hollender J . Mechanistic Understanding of the Synergistic Potential of Azole Fungicides in the Aquatic Invertebrate Gammarus pulex. Environ Sci Technol. 2017; 51(21):12784-12795. DOI: 10.1021/acs.est.7b03088. View

20.

Burdon F, Reyes M, Alder A, Joss A, Ort C, Rasanen K . Environmental context and magnitude of disturbance influence trait-mediated community responses to wastewater in streams. Ecol Evol. 2016; 6(12):3923-39. PMC: 4972221. DOI: 10.1002/ece3.2165. View