Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods
The comprehensive assessment of the long-term impacts of constant exposure to pollutants on wildlife populations remains a relatively unexplored area of ecological risk assessment. Empirical evidence to suggest that multigenerational exposure affects the susceptibility of organisms is scarce, and th...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-01-01
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| Series: | Environment International |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0160412023006414 |
| _version_ | 1827376950057893888 |
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| author | Jonas Jourdan Safia El Toum Abdel Fadil Jörg Oehlmann Kamil Hupało |
| author_facet | Jonas Jourdan Safia El Toum Abdel Fadil Jörg Oehlmann Kamil Hupało |
| author_sort | Jonas Jourdan |
| collection | DOAJ |
| description | The comprehensive assessment of the long-term impacts of constant exposure to pollutants on wildlife populations remains a relatively unexplored area of ecological risk assessment. Empirical evidence to suggest that multigenerational exposure affects the susceptibility of organisms is scarce, and the underlying mechanisms in the natural environment have yet to be fully understood. In this study, we first examined the arthropod candidate species, Gammarus roeselii that – unlike closely related species – commonly occurs in many contaminated river systems of Central Europe. This makes it a suitable study organism to investigate the development of tolerances and phenotypic adaptations along pollution gradients. In a 96-h acute toxicity assay with the neonicotinoid thiacloprid, we indeed observed a successive increase in tolerance in populations coming from contaminated regions. This was accompanied by a certain phenotypic change, with increased investment into reproduction. To address the question of whether these changes are plastic or emerged from longer lasting evolutionary processes, we conducted a multigeneration experiment in the second part of our study. Here, we used closely-related Hyalella azteca and pre-exposed them for multiple generations to sublethal concentrations of thiacloprid in a semi-static design (one week renewal of media containing 0.1 or 1.0 µg/L thiacloprid). The pre-exposed individuals were then used in acute toxicity assays to see how quickly such adaptive responses can develop. Over only two generations, the tolerance to the neonicotinoid almost doubled, suggesting developmental plasticity as a plausible mechanism for the rapid adaptive response to strong selection factors such as neonicotinoid insecticides. It remains to be discovered whether the plasticity of rapidly developed tolerance is species-specific and explains why closely related species – which may not have comparable adaptive response capabilities – disappear in polluted habitats. Overall, our findings highlight the neglected role of developmental plasticity during short- and long-term exposure of natural populations to pollution. Moreover, our results show that even pollutant levels seven times lower than concentrations found in the study region have a clear impact on the developmental trajectories of non-target species. |
| first_indexed | 2024-03-08T12:30:19Z |
| format | Article |
| id | doaj.art-82623e190a9e4a2885109cac04ff24d8 |
| institution | Directory Open Access Journal |
| issn | 0160-4120 |
| language | English |
| last_indexed | 2024-03-08T12:30:19Z |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Environment International |
| spelling | doaj.art-82623e190a9e4a2885109cac04ff24d82024-01-22T04:15:06ZengElsevierEnvironment International0160-41202024-01-01183108368Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipodsJonas Jourdan0Safia El Toum Abdel Fadil1Jörg Oehlmann2Kamil Hupało3Department Aquatic Ecotoxicology, Institute for Ecology, Evolution and Diversity, Goethe University, Frankfurt am Main, Germany; Kompetenzzentrum Wasser Hessen, Max-von-Laue-Straße 13 D-60438, Frankfurt am Main, Germany; Corresponding author.Department Aquatic Ecotoxicology, Institute for Ecology, Evolution and Diversity, Goethe University, Frankfurt am Main, Germany; Faculty of Life Sciences, Hamburg University of Applied Sciences, Ulmenliet 20 D-21033, Hamburg, GermanyDepartment Aquatic Ecotoxicology, Institute for Ecology, Evolution and Diversity, Goethe University, Frankfurt am Main, Germany; Kompetenzzentrum Wasser Hessen, Max-von-Laue-Straße 13 D-60438, Frankfurt am Main, GermanyDepartment of Aquatic Ecosystem Research, Faculty of Biology, University of Duisburg‐Essen, Essen, GermanyThe comprehensive assessment of the long-term impacts of constant exposure to pollutants on wildlife populations remains a relatively unexplored area of ecological risk assessment. Empirical evidence to suggest that multigenerational exposure affects the susceptibility of organisms is scarce, and the underlying mechanisms in the natural environment have yet to be fully understood. In this study, we first examined the arthropod candidate species, Gammarus roeselii that – unlike closely related species – commonly occurs in many contaminated river systems of Central Europe. This makes it a suitable study organism to investigate the development of tolerances and phenotypic adaptations along pollution gradients. In a 96-h acute toxicity assay with the neonicotinoid thiacloprid, we indeed observed a successive increase in tolerance in populations coming from contaminated regions. This was accompanied by a certain phenotypic change, with increased investment into reproduction. To address the question of whether these changes are plastic or emerged from longer lasting evolutionary processes, we conducted a multigeneration experiment in the second part of our study. Here, we used closely-related Hyalella azteca and pre-exposed them for multiple generations to sublethal concentrations of thiacloprid in a semi-static design (one week renewal of media containing 0.1 or 1.0 µg/L thiacloprid). The pre-exposed individuals were then used in acute toxicity assays to see how quickly such adaptive responses can develop. Over only two generations, the tolerance to the neonicotinoid almost doubled, suggesting developmental plasticity as a plausible mechanism for the rapid adaptive response to strong selection factors such as neonicotinoid insecticides. It remains to be discovered whether the plasticity of rapidly developed tolerance is species-specific and explains why closely related species – which may not have comparable adaptive response capabilities – disappear in polluted habitats. Overall, our findings highlight the neglected role of developmental plasticity during short- and long-term exposure of natural populations to pollution. Moreover, our results show that even pollutant levels seven times lower than concentrations found in the study region have a clear impact on the developmental trajectories of non-target species.http://www.sciencedirect.com/science/article/pii/S0160412023006414AdaptationEvolutionary ecotoxicologyMacroinvertebratesMultigenerational exposurePesticide toleranceRapid evolution |
| spellingShingle | Jonas Jourdan Safia El Toum Abdel Fadil Jörg Oehlmann Kamil Hupało Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods Environment International Adaptation Evolutionary ecotoxicology Macroinvertebrates Multigenerational exposure Pesticide tolerance Rapid evolution |
| title | Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods |
| title_full | Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods |
| title_fullStr | Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods |
| title_full_unstemmed | Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods |
| title_short | Rapid development of increased neonicotinoid tolerance in non-target freshwater amphipods |
| title_sort | rapid development of increased neonicotinoid tolerance in non target freshwater amphipods |
| topic | Adaptation Evolutionary ecotoxicology Macroinvertebrates Multigenerational exposure Pesticide tolerance Rapid evolution |
| url | http://www.sciencedirect.com/science/article/pii/S0160412023006414 |
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