Importance of exposure route in determining nanosilver impacts on a stream detrital processing chain

The commercial use and spread of silver nanoparticles (AgNPs) in freshwaters have greatly increased over the last decade. Both AgNPs and ionic silver (Ag⁺) released from nanoparticles are toxic to organisms and compromise ecosystem processes such as leaf litter decomposition. Yet little is known about how AgNPs affect multitrophic systems of interacting species. Furthermore, past work has focused on waterborne exposure with scarce attention given to effects mediated by the consumption of contaminated food. We assessed the importance of direct (via water) and indirect (via diet) AgNP exposure to a processing chain comprising leaf litter, fungi, a shredder (Gammarus pulex) and a collector (Habroleptoides confusa) in microcosms. Direct exposure to contaminated water for 15 days impaired microbial leaf decomposition by ∼50% and leaf-associated fungal biomass by ∼10%. Leaf consumption was reduced by ∼20% but only when G. pulex was exposed to silver via contaminated leaves. There was no effect on FPOM production. Ag ⁺ could impose oxidative stress on the shredders and collectors independent of exposure route, as indicated by increased catalase and glutathione S-transferase activities and decreased superoxide dismutase activity. The activity of a neuronal enzyme (cholinesterase) in collectors, but not shredders, also decreased by almost 50% when the animals were indirectly exposed to AgNP. Our results show that AgNPs and Ag⁺ may disrupt detrital processing chains through direct and indirect exposure routes, even at low concentrations. This highlights the importance of AgNP exposure pathways to interconnected stream biota and ecosystem processes for realistic assessments of risks to freshwater ecosystems.