Chronic metal contamination shapes the size structure of Gammarus fossarum populations in French headwater rivers

Assessing the effects of multigenerational exposure of aquatic animal populations to chemical contamination is essential for ecological risk assessment. However, beyond rare examples reporting the sporadic emergence of a toxicological tolerance within populations that persist in contaminated environments, conclusive results are even more limited from field studies when it comes to the alteration of life-history traits. Here, we investigated whether long-term exposure to cadmium (Cd) influences size-related life-history traits (i.e., size at puberty, median adult size, maximum size) in Gammarus fossarum , a keystone species of European stream ecosystems. We studied 13 field populations of G. fossarum (cryptic lineage B) living in headwater rivers located in natural areas scattered at a large geographical scale and exposed to contrasted bioavailable Cd contamination levels due to different local geochemical backgrounds. We achieved a detailed description of the physical and physicochemical conditions of the river reaches investigated. Land-use parameters, hydrological characteristics (flow, slope, river width, flow structure, mosaic of substrates), and physicochemical conditions (temperature, conductivity, dissolved oxygen) were measured. Metallic bioavailable contamination was assessed using a standardized active biomonitoring procedure ( Gammarus caging). Based on the field demographic census of the 13 populations, our results demonstrated that chronic Cd contamination significantly influences life-history in the G. fossarum species, with a significant reduction in all size traits of populations (size at puberty, median adult size, maximum size). In addition, we confirmed Cd-tolerance in contaminated populations during exposure tests in the laboratory. Various hypotheses can be then put forward to explain the modification of size-related life-history traits: a direct toxic effect of Cd, a cost of Cd-tolerance, or an adaptive evolution of life-history exposed to toxic pressure. Graphical Abstract Highlights Characterization of Cd-exposure, Cd-tolerance, and size distribution of 13 Gammarus field populations. Occurrence of natural high levels of Cd exposure in headwater rivers. Reduced size at puberty, reduced mean and maximal body size in Cd-exposed populations. Cost of tolerance versus life-history adaptation as underlying evolutionary mechanisms.