Parasites are ubiquitous in natural systems and integral components of biodiversity (Wood and Johnson, 2015). They often play significant roles in regulating host populations, influencing food web dynamics, and maintaining ecosystem stability (Anderson, 1978, Collinge and Ray, 2006, Peacock et al., 2015). Parasites exert a potent selective force on their hosts, contributing to shaping the evolution of species (Duffy and Forde, 2009, Heil, 2016, Papkou et al., 2016). Many parasite species are threatened by environmental stressors, such as pollution and climate change, directly or indirectly via effects on their host (Altizer et al., 2013, Caminade et al., 2019, Lafferty and Kuris, 1999). Indeed, environmental stressors may influence parasites’ development, survival, and reproductive outputs (Gleichsner et al., 2016). Recent studies have highlighted a decade-long decline in parasite populations, attributed to climate-associated stressors (Welicky et al., 2021, Wood et al., 2023). This decline poses major issues for ecosystem stability and resilience, which often rely on the regulatory roles of these organisms.

Anthropogenic pollution poses a major threat to freshwater ecosystems (Schäfer et al., 2016, Schmutz and Sendzimir, 2018). While the impacts of pollutants on hosts are well-documented (Amoatey and Baawain, 2019, Relyea, 2009), evaluating their effects on parasites remain equally critical (Šebelová et al., 2002). These effects are still difficult to assess, as most studies focus on the free-living stages of parasites (Pietrock and Marcogliese, 2003). Moreover, disentangling the direct effects of pollutants on parasites from the indirect effects mediated through their hosts remains challenging. For example, environmental pollutants can increase host susceptibility and infection rates (Buss and Hua, 2023, Koprivnikar et al., 2007), through immunotoxicity and lower host resistance (Morley et al., 2006, Regala et al., 2001, Sures and Knopf, 2004). In contrast, pollutants can reduce host susceptibility to parasites by impairing transmission and decreasing infection levels (Koprivnikar et al., 2007, Pietrock and Goater, 2005), and by jeopardizing parasite survival (Rohr et al., 2008). Overall, the potential impacts of pollution on parasite populations are difficult to evaluate and predict. They may be context-dependent and may vary according to factors such as the parasite’s development stage (Dhakal et al., 2020), the timing of infection (Dhakal et al., 2020) but also the timing and dose of pollutant exposure (Koprivnikar et al., 2006, Rohr et al., 2008).

An additional layer of complexity is that parasites, traditionally viewed as harmful, can also conditionally benefit their host. For instance, some parasite species accumulate pollutants from their hosts (Rosa Leite et al., 2021, Sures et al., 1994), potentially reducing the hosts’ toxic burden. The enormous sequestration of pollutants by certain taxa (e.g., Trematoda, Cestoda, Acanthocephala) can affect pollutant bioavailability to their hosts and potentially mitigate ecotoxicological effects (Goutte and Molbert, 2022, Morley et al., 2006, Sures et al., 2017, Sures and Siddall, 1999, Turcekova and Hanzelova, 1999). This also implies that parasites face high pollutant loads, with largely unknown consequences for their survival, growth, and reproduction.

Parasite responses to pollutants are also shaped by ecological and biological factors beyond pollutant exposure itself. Environmental factors and host-related traits can profoundly influence parasite dynamics (Fleury et al., 2009, Patz et al., 2000). Temperature, for instance, determines the growth and transmission rates of many parasites, as well as their ability to complete life cycles (Schoebel et al., 2011, Studer et al., 2010). Seasonal variation and water quality parameters further impact parasite survival and infectivity (Altizer et al., 2006, Erkano, 2021). Survival and infectivity can also be influenced by host diet, affecting the availability of nutrients essential for parasite development (Pulkkinen and Ebert, 2004). These intricate interactions highlight the complexity of parasitic relationships. They are shaped by an interplay between environmental conditions and host-specific characteristics, often resulting in context-dependent outcomes for parasite populations and their ecosystems (Marcogliese and Pietrock, 2011). Understanding how pollutants, habitat and host-related parameters impact parasites is crucial for fully assessing the consequences of pollution on freshwater ecosystems.

In this study, we tested whether experimental exposure to pesticide and pharmaceutical residues, along with environmental and host-related factors, may influence parasite infection and fitness, using acanthocephalan parasites (Pomphorhynchus sp.) of chub (Squalius cephalus), as a freshwater model system. These intestinal thorny-headed worms accumulate many organic pollutants (Molbert et al., 2020), and are particularly resistant to pollutants (Fanton et al., 2022). Therefore, they provide an ideal framework for studying both direct and indirect effects of contamination (Perrot-Minnot et al., 2023). First of all, given the impact of the environment in which fish develop on parasites (Altizer et al., 2006, Erkano, 2021, Pulkkinen and Ebert, 2004), we investigated how host traits (size, body condition) and environmental factor (site of capture, seasonality) influence parasite infection intensity, size, and reproductive outputs (production of eggs). We also expected that parasite infection intensity would reduce individual parasites size, due to intra-individual competition (Dianne et al., 2012, Lagrue and Poulin, 2008), and that parasite-related traits (intensity and size) would influence eggs production of parasites (Poulin et al., 2003). Then, we experimentally exposed chub to pollutants at environmentally relevant doses, including the pesticide imidacloprid, the pharmaceutical compounds acetaminophen, diclofenac, and the herbicide S-metolachlor, all found in high concentrations in Seine river tributaries (Lorrain-Soligon et al., 2025b, Marchand et al., 2024), to evaluate their impacts on parasite infection intensity, size, and reproductive traits. Given the heightened sensitivity of invertebrates, including parasites, to certain toxicants (Blanar et al., 2009), we hypothesize that exposure to these pollutants will negatively impact key components of parasite fitness.