Infection with acanthocephalans increases tolerance of Gammarus roeselii (Crustacea: Amphipoda) to pyrethroid insecticide deltamethrin

Abstract

Crustacean amphipods serve as intermediate hosts for parasites and are at the same time sensitive indicators of environmental pollution in aquatic ecosystems. The extent to which interaction with the parasite influences their persistence in polluted ecosystems is poorly understood. Here, we compared infections of Gammarus roeselii with two species of Acanthocephala, Pomphorhynchus laevis, and Polymorphus minutus, along a pollution gradient in the Rhine-Main metropolitan region of Frankfurt am Main, Germany. Prevalence of P. laevis was very low at the unpolluted upstream reaches (P ≤ 3%), while higher prevalence (P ≤ 73%) and intensities of up to 9 individuals were found further downstream—close to an effluent of a large wastewater treatment plant (WWTP). Co-infections of P. minutus and P. laevis occurred in 11 individuals. Highest prevalence of P. minutus was P ≤ 9% and one parasite per amphipod host was the maximum intensity recorded. In order to assess whether the infection affects survival in the polluted habitats, we tested the sensitivity of infected and uninfected amphipods towards the pyrethroide insecticide deltamethrin. We found an infection-dependent difference in sensitivity within the first 72 h, with an effect concentration (24 h EC50) of 49.8 ng/l and 26.6 ng/l for infected and uninfected G. roeselii, respectively. Whereas final host abundance might partially explain the high prevalence of P. laevis in G. roeselii, the results of the acute toxicity test suggest a beneficial effect of acanthocephalan infection for G. roeselii at polluted sites. A strong accumulation of pollutants in the parasite could serve as a sink for pesticide exposure of the host. Due to the lack of a co-evolutionary history between parasite and host and a lack of behavioral manipulation (unlike in co-evolved gammarids), the predation risk by fish remains the same, explaining high local prevalence. Thus, our study exemplifies how organismic interaction can favor the persistence of a species under chemical pollution.

Evidence of predation pressure on sensitive species by raccoons based on parasitological studies

“…laevis is a typical fish parasite. Both parasite species utilize amphipods and fish as intermediate hosts ( Romanovski, 1964 ; Itämies et al, 1980 ; Gaillard et al, 2004 ; Kochmann et al, 2023 ). The presence of both parasite species in the examined raccoons suggests that they must have preyed on infected amphipods, waterfowl, or fish in the study areas, even if no direct evidence of such species was found in the stomach or intestine, except for the rainbow trout Oncorhynchus mykiss in Hesse ( Table 3 ) ( Itämies et al, 1980 ; Piróg et al, 2018 ).…”

Much effort, little success: causes for the low ecological efficacy of restoration measures in German surface waters

“…Ref. [140] collected water grab samples between July 2015 and July 2016 in eight sampling campaigns at 13 sites of the river Horloff which are identical with sites 3-5, 14-21, 23 and 25 in our study. These samples were analyzed by liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) for 161 medium polar emerging pollutants (54 pharmaceuticals, 18 biocides and pesticides, 10 industrial compounds, 4 X-ray contrast media, 3 artificial sweeteners, 2 corrosion inhibitors, 1 repellent, 1 aversive agent and 1 stimulant), including 67 transformation products.…”

“…As an integrative measure for the potential toxicity caused by these compounds, the authors calculated in a first step toxic units (TUs, dimensionless) for those 57 of the 161 analyzed compounds with available toxicity data by dividing the arithmetic mean concentration from all sampling campaigns at a given site for the respective compound by its 50% effect concentration (EC 50 ) for immobilization in acute tests with daphnids. According to the concentration addition concept of [141] the authors calculated in the second step the potential mixture toxicity as the sum of the individual TUs at a given station (see [140] for details).…”

“…Mixture toxicity based on the sum of toxic units (TU) in Daphnia spec. for 57 analyzed chemicals (a, data from[140]) and mean and standard error of the mean of EC 50 values for baseline toxicity, determined with the Microtox assay (b), and of dioxin-like activity, determined with the yeast dioxin screen (c), in water samples from the river Horloff. Dashed arrows mark the outflow of the last of the four small wastewater treatment plants (WWTPs) downstream of site 4 in the upper reach of the Horloff and of the WWTP Wölfersheim downstream of site 19.…”

Uncovering the Grinnellian niche space of the cryptic species complex Gammarus roeselii

“…Like many other amphipods, G. roeselii sensu lato is expected to play a key role as a leaf shredder in the nutrient circle ( Jourdan et al, 2016 ) and can occur in high densities ( Karaman & Pinkster, 1977 ). Both in Central Europe and in the Balkans, G. roeselii sensu lato colonize different habitat types ( e.g ., lakes, mountain streams, rivers) and can also occur in habitats that are heavily anthropogenically stressed ( Jourdan et al, 2019 ; Kochmann et al, 2023 ). So far, G. roeselii sensu lato is considered to have a high tolerance to many environmental conditions and pollution ( Gergs, Schlag & Rothhaupt, 2013 ; Jourdan et al, 2019 ).…”