From avoidance to ingestion: Microplastic-induced behavioral and physiological adaptations elevate microplastic ingestion and chronic toxicological risks in marine medaka (Oryzias melastigma)

Owing to their particulate nature, microplastics (MPs) in aquatic ecosystems can elicit behavioral and physiological adaptations that reshape exposure pathways compared with dissolved pollutants. Using marine medaka (Oryzias melastigma) as a model, we investigated how foraging decisions and physiological adjustments jointly drive a transition from initial avoidance of MPs to their intentional ingestion, and how this shift modulates chronic toxicological risks. In short-term experiments, medaka clearly avoided MPs under favorable feeding conditions, including abundant food (detrital fish feed, live zooplankton, algae) and distinct spatial segregation of MPs from food. However, reduced food availability, diffuse spatial overlap between MPs and food, and lower food attractiveness all increased MP ingestion, either intentionally or unintentionally. Notably, initial intake of palatable zooplankton strongly stimulated prolonged, wide-ranging foraging, which led to significantly higher intentional MP uptake after the first feeding. This intensive MP intake resulted in compact MP clustering in the intestinal lumen that may aggravate inflammation and oxidative stress. Chronic incubation experiments further revealed that occasional exposure to MP-food mixtures gradually altered feeding patterns: initial avoidance of MPs diminished, and fish increasingly ingested MPs intentionally even when alternative food was available, resulting in approximately 50-fold higher daily MP ingestion on day 28 than at the start of incubation. Although most ingested MPs were eliminated within 24 h, their repeated passage through the gut under chronic exposure induced persistent sublethal effects, including suppressed antioxidant defenses (CAT and GSH), altered muscle energy metabolism, and gut microbiota dysbiosis, which may substantially exacerbate ecological risks of MPs, particularly under food-limited conditions.