The Paradoxical Toxicity of Microplastics under Predation Risk: The Driving Role of Gut Microbiota-Mediated Tolerance

Accurate predictions of the ecological risks of microplastics require understanding of their interplay with natural stressors. Here, we revealed that predation risk fundamentally altered the microplastics ecotoxicity on the keystone species Daphnia magna. The microplastics alone were toxic (e.g., reduced growth rate, body size, spine length, and delayed maturity) and became more toxic under predation risk. For instance, the maturation delay at high MP concentrations increased 6.67-fold. Paradoxically, microplastics also enhanced inducible defenses, with fish cues offsetting microplastics that induced reductions in spine length and somatic growth. Contrasting Daphnia genotypes revealed that the fish-adapted clone exhibited superior tolerance to combined exposure to stressors, maintaining robust growth and defensive integrity, unlike the fish-naïve clone. The gut microbiome was identified as a key mechanistic driver. The fish-adapted clone maintained a more stable microbial community structure with functions enriched in carbohydrate metabolism and immune defense. A reciprocal transplantation experiment provided causal evidence: transplanting the adapted microbiota into the predator-naïve clone reduced mortality by 39% and increased intrinsic growth by 22% under combined stress. These findings highlight that microplastics risk assessment may be flawed if they ignore the eco-evolutionary context of natural stressors.