Host-parasites transfert of micropollutants and eco-physiological consequences on a freshwater fish: Case study of chub-acanthocephalan model

Exposure to complex mixtures of environmental contaminants may have severe consequences in free-living animals through the disruption of physiological mechanisms, reduced reproductive outputs and survival, thereby leading to population collapse. Contaminant analyses in fish have been used as a routine approach in studies of aquatic pollution. Located at the upper levels of the food webs, fish are indeed particularly exposed to chronic contamination. Under natural conditions, organisms are also exposed to a vast array of stressors, including parasites. Both chemical exposure and parasite infection have been well studied and documented, but have in many cases been investigated independently from one another. However, it is crucial to simultaneously assess their combined effect on wild organisms given that parasites may interfere with the fate of environmental contaminants within their host through their bioaccumulation capacity. This thesis focuses on six families of organic contaminants, and some of their metabolites, including persistent pollutants still reported at sublethal levels in freshwater fish despite their ban from use and production, (Polychlorinated biphenyl: PCBs, organochlorine pesticides: OCPs and Polybrominated diphenyl ethers: PBDEs) as well as substances broadly use in industrial processes, agriculture and in residential areas (Polycyclic aromatic hydrocarbons: PAHs, phthalates, insecticides).
Based on a field study, completed by an experimental approach, I investigated the fate and consequences of these organic contaminants in a host-parasite system composed of a freshwater fish, the European chub, Squalius cephalus, and its intestinal parasite, Pomphorhynchus sp. from the Marne River, France. Specifically, I investigated whether intestinal parasites were able to accumulate toxicants and how their presence affected the stress response of their definitive host exposed to environmental contaminants. This was examined at different biological levels with the use of general biomarkers providing information on their immune and oxidative physiological state (lysozyme, peroxidase, antioxidants, oxidative damage), the diversity and composition of gut bacterial communities (microbiota), their body condition (Fulton’s index and hepatosomatic index) and life expectancy (telomere length). This PhD work underlines the toxicity of metabolites of organic contaminants, which were associated with increased oxidative damage, reduced antioxidant defenses and shorter telomeres. Importantly, we demonstrated that intestinal worms were able to accumulate organic contaminants, detoxify their hosts and that their effects on the oxidative balance shifted from negative to positive as chemical exposure increased. Evidence from both our field and laboratory studies therefore suggests that natural infection by intestinal worms can modulate the host’s stress response to toxicants through physiological changes, which might benefit the host under polluted condition.