Juveniles at risk: behaviour and colour changes in sole juveniles (Solea solea) after exposure to estuarine ragworms (Hediste diversicolor) contaminated with microplastics.

Due to strong anthropogenic pressures and their location at the interface between continental and oceanic environments, estuarine areas are affected by significant diverse pollution and species that live in these areas are particularly exposed. Microplastic (MPs) pollution is a worldwide issue and causes substantiated trouble in estuaries where sometimes the number of MPs equal or exceed the number of fish larvae which suggest a high risk of contamination of biota especially in benthic organisms and demersal fish. There are growing evidence that, beyond intrinsic toxicity, MPs can transfer chemicals (additives or pollutants). In order to get closer to environmental situations, in this study we tackled an issue that is rarely dealt with, namely the trophic transfer of MPs and chemicals through the food chain between a sediment- and a benthic-feeder. To take into account these specificities, we used an emblematic and common species of the European coastlines, the common sole (Solea solea) and its annelid prey. Sole juveniles were fed with estuarine ragworms (Hediste diversicolor) previously exposed to MPs via enriched MPs sediment. The MPs used were either a mixture of micronized plastics collected from the Seine Estuary (eMPs, two environmental concentrations at 1 or 100 mg/kg of sediment, median size range 52-77 μm) or model MPs of PVC particles (at 1 g/kg of sediment, size range 125-250 μm), either uncontaminated or contaminated with Benzo(a)Pyrene (BaP, 11.5 μg/g MPs) or benzophenone-3 (BP3, 66 ng/g MPs). Several indicators of health status such as survival, growth, behaviour, energy metabolism, and histopathology were studied. Sole individuals fed ragworms exposed to eMPs or PVC MPs displayed a change in behaviour (place preference between black/white background). Seine Estuary eMPs lead to an increase in body colour chroma for the highest concentration and behaviour was modified with an increase in time spent on white bottom and transition number for the highest concentration when distance moved increased only at the lowest concentration. Sole exposed to BaP-PVC-MPs displayed the lowest time spent on white background compared to control and BP3-PVC-MPs group. Soles exposed to BP3-PVC MPs displayed a significant skin colour increase in chroma and a wider combination of value/chroma reflecting more diverse skin colours. Finally, lipid content in muscle and DNA damage were significantly higher in BP3-MPs. Although the exact mechanisms underpinning such changes are largely unknown, these observations are indicative of physiological stress which may have a significant impact on survival by increasing predation risks for fish juveniles, hence the ecosystem health and calls for further trophic transfer experimental research.