Chemical Pollution Levels in a River Explain Site-Specific Sensitivities to Micropollutants within a Genetically Homogeneous Population of Freshwater Amphipods

Abstract

Anthropogenic micropollutants alter chemical and ecological conditions of freshwater ecosystems and impact aquatic species that live along the pollution gradient of a river. Species sensitivity to micropollutants depends on the site-specific exposure; however, it remains unclear to what degree this sensitivity relates to the species’ genetic structure. Here, we explored the relationship between the toxic sensitivity and genetic structure of the amphipod species Gammarus pulex (Linnaeus, 1758) along an organic micropollutant gradient in the Holtemme River in central Germany. We determined the river’s site-specific micropollutant patterns and analyzed the genetic structure of G. pulex using nuclear and mitochondrial genetic markers. Furthermore, we examined the exposure sensitivities and bioaccumulation of the commonly detected insecticide imidacloprid in G. pulex from different sites. Our results show that throughout the Holtemme River, G. pulex forms a well-connected and homogeneous population with no observable pollution-related differences in the genetic structure. However, G. pulex from polluted sites responded more sensitively to imidacloprid; survival times for half of the amphipods were up to 54% shorter, the percentage of immobile individuals increased up to 65%, and the modeled imidacloprid depuration rate was lower in comparison to amphipods from non-polluted sites. Altogether, these results suggest that the level of sensitivity of G. pulex amphipods to micropollutants in the river depends on the degree of pollution: amphipods may thrive in food-rich but polluted habitats; yet, their sensitivity is increased when chronically exposed to organic micropollutants.

Reduced genetic diversity of freshwater amphipods in rivers with increased levels of anthropogenic organic micropollutants

“…In addition to the acute toxic effects of AOM, endocrine disruptors found in Gammarus amphipods were shown to alter the male‐female ratio, influence reproductive success, and alter population size and allele frequencies in the exposed populations (Gross et al, 2001; Watts et al, 2002). In the current study, 7‐diethylamino‐4‐methylcoumarin, a driver of antiandrogenic effects in fish, was for the first time detected at high concentrations in the Eine River and confirmed for the Holtemme river (Muschket et al, 2018; Švara et al, 2021). The effects of this coumarin in amphipods remain unknown.…”

“…AOM concentrations in water and G . pulex tissue samples were analyzed by a Thermo Ultimate 3000 liquid chromatography (LC) system coupled with a quadrupole‐orbitrap high‐resolution mass spectrometer (HRMS; Thermo QExactive Plus) as described in Švara et al ( 2021 ). For details on sample preparation and LC‐HRMS measurement refer to Section S1 in the Supporting Information.…”

“…Despite multiple evidences for changes in the genetic diversity of species exposed to environmental pollutants, such as mutagenic chemicals, heavy metals, or PAHs (Bach & Dahllöf, 2012 ; Theodorakis et al, 2006 ; Ungherese et al, 2010 ; Weigand et al, 2018 ), data on genetic changes in freshwater macroinvertebrates exposed to AOM in rivers are scarce. In most cases, studies on AOM’s impact on the genetic diversity of freshwater macroinvertebrates investigated alterations at the local scale (Inostroza, Vera‐Escalona, et al, 2016 ; Inostroza, Wicht, et al, 2016 ; Švara et al, 2021 ). In a recent study investigating the frequencies of specific alleles to reveal the genetic structure of Gammarus pulex (Linnaeus, 1758) sampled along a pollution gradient in a river, the physiological condition of the amphipods was found to depend on AOM contamination at the respective sampling site, while the genetic structure of G .…”

“…In a recent study investigating the frequencies of specific alleles to reveal the genetic structure of Gammarus pulex (Linnaeus, 1758) sampled along a pollution gradient in a river, the physiological condition of the amphipods was found to depend on AOM contamination at the respective sampling site, while the genetic structure of G . pulex within the river did not show AOM‐dependent changes (Švara et al, 2021 ). However, due to the limitations of the study performed in a single river with a few sampling sites, the relationship between the genetic diversity of G .…”

“…pulex from polluted and nonpolluted sites within a river, G . pulex individuals from the different sites were found to not be genetically different (Švara et al, 2021 ). Thus, we hypothesize that (1) divergence in population genetic structure within rivers and across rivers in a region corresponds to distances between sites rather than to different levels of toxic AOM in the rivers.…”