Importance of Dietary Uptake for in Situ Bioaccumulation of Systemic Fungicides Using Gammarus pulex as a Model Organism

Abstract

Bioaccumulation of organic contaminants from contaminated food sources might pose an underestimated risk toward shredding invertebrates. This assumption is substantiated by monitoring studies observing discrepancies of predicted tissue concentrations determined from laboratory‐based experiments compared with measured concentrations of systemic pesticides in gammarids. To elucidate the role of dietary uptake in bioaccumulation, gammarids were exposed to leaf material from trees treated with a systemic fungicide mixture (azoxystrobin, cyprodinil, fluopyram, and tebuconazole), simulating leaves entering surface waters in autumn. Leaf concentrations, spatial distribution, and leaching behavior of fungicides were characterized using liquid chromatography coupled with high‐resolution tandem mass spectrometry (LC‐HRMS/MS) and matrix‐assisted laser desorption ionization‐mass spectrometric imaging. The contribution of leached fungicides and fungicides taken up from feeding was assessed by assembling caged (no access) and uncaged (access to leaves) gammarids. The fungicide dynamics in the test system were analyzed using LC‐HRMS/MS and toxicokinetic modeling. In addition, a summer scenario was simulated where water was the initial source of contamination and leaves contaminated by sorption. The uptake, translocation, and biotransformation of systemic fungicides by trees were compound‐dependent. Internal fungicide concentrations of gammarids with access to leaves were much higher than in caged gammarids of the autumn scenario, but the difference was minimal in the summer scenario. In food choice and dissectioning experiments gammarids did not avoid contaminated leaves and efficiently assimilated contaminants from leaves, indicating the relevance of this exposure pathway in the field. The present study demonstrates the potential impact of dietary uptake on in situ bioaccumulation for shredders in autumn, outside the main application period. The toxicokinetic parameters obtained facilitate modeling of environmental exposure scenarios. The uncovered significance of dietary uptake for detritivores warrants further consideration from scientific as well as regulatory perspectives. Environ Toxicol Chem 2023;00:1–14. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Ecological Theory and Concepts in Ecotoxicology

“…Stevenson et al (2023) link adverse outcome pathways to the dynamic energy budget theory, with the aim of forming quantitative predictions of chemical exposures to individuals. Raths et al (2023) explore the role of dietary exposure in the bioaccumulation of systemic fungicides in leaf-shredding amphipods. These authors use ecological concepts to explain a mismatch between predicted tissue concentrations determined from laboratory-based experiments compared with measured concentrations of systemic pesticides in gammarids during monitoring studies.…”

Dietborne Toxicity of Tebuconazole to a Benthic Crustacean, Heterocypris incongruens and Its Relative Contribution to the Overall Effects under Food–Water Equilibrium Partitioning

“…Recent accumulation studies using G. pulex have revealed the importance of the dietary route, with approximately 30% of the body burden of TEB attributed to diet. 14 However, a gap persists between the bioaccumulation results and the observed toxicity effects of TEB. Notably, the detected toxicants found in organisms' bodies could originate from stored compounds within specific lipid-rich cells or tissues 15 and may not necessarily exert immediate toxicity effects.…”

“…Recent accumulation studies using G. pulex have revealed the importance of the dietary route, with approximately 30% of the body burden of TEB attributed to diet . However, a gap persists between the bioaccumulation results and the observed toxicity effects of TEB.…”