Feeding behavior and species interactions increase the bioavailability of microplastics to benthic food webs

Abstract

Plastics are pervasive in aquatic ecosystems, in which they circulate in the water column, accumulate in sediments, and are taken up, retained, and exchanged with their biotic environment via trophic and non-trophic activities. Identifying and comparing organismal interactions are a necessary step to improve monitoring and risk assessments of microplastics. We use a community module to test how abiotic and biotic interactions determine the fate of microplastics in a benthic food web. Using single-exposure trials on a trio of interacting freshwater animals (the quagga mussel Dreissena bugensis, a filter feeder; the gammarid amphipod Gammarus fasciatus, a deposit feeder; and the round goby Neogobius melanostomus, a benthivorous fish), we quantify the (1) uptake of microplastics from environmental routes (water, sediment) under six exposure concentrations, (2) the depuration capacities over 72 h, and (3) the transfer of microbeads via trophic (predator-prey) and behavioral interactions (commensalism, intraspecific facilitation). Under 24 h exposures, each animal of our module acquired beads from both environmental routes. The body burden of filter-feeders was higher when they were exposed to particles in suspension, whereas detritivores had similar uptake from either route. Mussels transferred microbeads to amphipods, and both invertebrates transferred beads to their mutual predator, the round goby. Round gobies generally displayed low contamination from all routes (suspension, sedimented, trophic transfer) with a higher microbead load from preying on contaminated mussels. Higher mussel abundance (10-15 mussel per aquaria, i.e., ~200-300 mussels·m²) did not increase individual mussel burdens during exposure, and neither did it increase the transfer of beads from mussels to gammarids via biodeposition. Our community module approach revealed that the feeding behavior of animals allows microplastic uptake from multiple environmental routes, whereas trophic and non-trophic species interactions increased their burden within their food web community.

Keywords: Depuration; Food web; Microplastic; Species interactions; Trophic transfer; Uptake.