Modulation of carbendazim toxicity by enhanced acanthocephalan infection in a freshwater fish.

Abstract

Interactions between parasites and their hosts are shaped by ecological context, yet how anthropogenic pollution modifies these coevolved relationships remains poorly understood. Freshwater ecosystems are particularly exposed to chronic contamination by pesticides, which can affect host physiology, immunity, and behavior, as well as parasite development and transmission. Disentangling the independent and interactive effects of these stressors requires controlled experimental approaches. Here, 109 individuals of the freshwater fish Squalius cephalus were experimentally infected, each with 15 acanthocephalan parasites Pomphorhynchus laevis. These infections were followed by 6 exposures to carbendazim, a widely used fungicide, at a dose of 0.75 μg per gram of fish across a 1 month period. Carbendazim exposure alone altered immune profiles and body coloration. Experimental infections successfully enhanced parasites number in hosts, which in turn modified fish behavior and pigmentation. Importantly, we also detected interactive effects between enhanced parasitism and pollutant exposure: pollutant-induced alterations were reduced in European chubs with enhanced acanthocephalan load compared to fish with natural parasite load. These results suggest that parasites can modulate host responses to chemical stress, potentially by reducing pollutant bioavailability or host metabolic and immune pathways. Parasite fitness, however, appeared largely unaffected by pollutant exposure. Our findings support the hypothesis that pollutants can mediate a shift from parasitism to mutualism and highlight the need to explicitly incorporate host-parasite dynamics into predictions of ecological and evolutionary responses to pollution.