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Currently Used Pesticides and Their Mixtures : What Are the Risks to Non-Target Aquatic Organisms? Laboratory and in Situ Approaches

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Currently Used Pesticides and Their Mixtures : What Are the Risks to Non-Target Aquatic Organisms? Laboratory and in Situ Approaches Currently used pesticides and their mixtures : what are the risks to non-target aquatic organisms? Laboratory and in situ approaches. Eliška Rozmankova To cite this version: Eliška Rozmankova. Currently used pesticides and their mixtures : what are the risks to non-target aquatic organisms? Laboratory and in situ approaches.. Ecotoxicology. Université de Bordeaux; Masarykova univerzita (Brno, République tchèque), 2020. English. NNT : 2020BORD0301. tel- 03235876 HAL Id: tel-03235876 https://tel.archives-ouvertes.fr/tel-03235876 Submitted on 26 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Currently used pesticides and their mixtures: what are the risks to non-target aquatic organisms? Laboratory and in situ approaches. Eliška Kuchovská Ph.D. Dissertation Masaryk University, Faculty of Science RECETOX & University of Bordeaux EPOC, EA – Environnements et Paléoenvironnements Océaniques et Continentaux, Ecotoxicologie aquatique Brno 2020 Supervisors: prof. RNDr. Luděk Bláha, Ph.D. prof. Patrice Gonzalez, Ph.D. Bénédicte Morin, Ph.D. THÈSE EN COTUTELLE PRÉSENTÉE POUR OBTENIR LE GRADE DE DOCTEUR DE L’UNIVERSITÉ DE BORDEAUX ET DE L’UNIVERSITÉ MASARYK ÉCOLE DOCTORALE Sciences et environnements SPÉCIALITÉ : Géochimie et Écotoxicologie Par Eliška KUCHOVSKÁ PESTICIDES LARGEMENT UTILISÉS ET LEURS MELANGES : QUELS RISQUES POUR LES ORGANISMES AQUATIQUES NON-CIBLES ? Approche en laboratoire et in situ Sous la direction de : Patrice GONZALEZ co-directeur : Luděk BLÁHA co-encadrement : Bénédicte Morin Soutenue le 17 décembre 2020 Membres du jury : M. GONZALEZ, Patrice Professeur, Université de Bordeaux Directeur M. BLAHA, Luděk Professeur, Masaryk University Directeur Mme BOLLIET, Valérie Professeure, Université de Pau et des Pays de l’Adour Présidente M. BANNI, Mohamed Professeur, ISBM Monastir Rapporteur Mme MORGANE, Danion Chargé de projets scientifiques, ANSES Examinatrice Mme LEGRADI, Jessica Assistant Professor, Vrije Universiteit Amsterdam Examinatrice Mme MORIN, Bénédicte Maître de conférences, Université de Bordeaux Encadrante M. HOFMAN, Jakub Professeur, Masaryk University Invité Title: Currently used pesticides and their mixtures: what are the risks to non-target aquatic organisms? Laboratory and in situ approaches. Abstract: Pesticides have enabled humankind to protect its crops from pests, intensifying thus the crop yields to sustain the growing population. However, pesticides often end up in aquatic water bodies, e.g. via field runoff, where they may harm non-target organisms. The environmental concentrations of pesticides are often considered safe for aquatic ecosystems although they might induce sublethal changes in exposed organisms. Moreover, the organisms are generally not dealing with only one pesticide issued from a nearby field but with a complex mixture of various chemical compounds, interacting amongst themselves, and creating a toxic cocktail with unknown and hardly predictable impacts. These compounds, each with different environmental fate, eventually degrade and form more or less toxic and persistent metabolites aggravating the complexity of the mixtures. This dissertation thesis summarizes the state-of-the-art in pesticide mixture toxicity research and is composed of five research articles dealing with sublethal effects of selected pesticides on non-target aquatic species. Vulnerable embryo-larval stages of two model organisms: freshwater zebrafish (Danio rerio) and euryhaline bivalve Pacific oyster (Magallana gigas) were used to assess the sublethal toxicity of especially environmental concentrations (detected in selected European water bodies) of commonly used herbicide S-metolachlor with its two metabolites metolachlor oxanilic acid and metolachlor ethanesulfonic acid, insecticide imidacloprid, and fungicide propiconazole, alone and in a mixture. A complementary in situ approach was carried out to evaluate a real impact on early-life stages of the Pacific oyster in Arcachon Bay in France, a final recipient of various substances including pesticides from respective watersheds. First, zebrafish embryo-larval stages were observed to be highly sensitive to environmentally relevant concentrations of propiconazole and to a lesser extent also to imidacloprid. In contrast, S-metolachlor and its metabolites had almost no effect on their development, neurobehavioral functions, or gene expression except for altered genes implicated in the thyroid system. A mixture of these compounds exhibited a concentration addition effect on zebrafish development. These observations imply that the development of freshwater fish may be at risk with current agricultural practice. iii Second, a study with Pacific oyster embryos and larvae revealed very low toxicity of propiconazole and imidacloprid on their development and locomotion patterns. Few effects caused by these compounds were observed at the molecular level, as well as the effects caused by the mixture. The environmental concentration of the mixture induced developmental malformations in oyster larvae, however, those exposed in situ in Arcachon Bay did not show higher proportions of abnormal larvae suggesting that the water quality of Arcachon Bay is sufficient for oyster development. Nevertheless, oyster larvae exposed in the inner part of Arcachon Bay showed different gene expression levels than larvae from the reference site located near the ocean entrance, which may indicate consequences of a potential long-term impact. These results documented that embryo-larval stages of zebrafish and Pacific oysters are relevant tools for the assessment of low concentrations of pesticides and pesticides in a mixture, and that laboratory studies complemented with field research are useful for (eco)toxicity assessment and of high ecological relevance. Keywords: Ecotoxicity, Embryo-larval stages, Pacific oyster, Pesticide, Sublethal effect, Zebrafish Environnements et Paléoenvironnements Océaniques et Continentaux (EPOC- Ecotoxicologie Aquatique) UMR CNRS 5805 & RECETOX iv Titre : Pesticides largement utilisés et leurs mélanges : quels risques pour les organismes aquatiques non-cibles ? Approche en laboratoire et in situ. Résumé: Les pesticides ont pour rôle de protéger les cultures des espèces nuisibles permettant ainsi d’intensifier le rendement agricole pour nourrir une population toujours en augmentation. Néanmoins, les pesticides se retrouvent souvent dans le réseau aquatique, par exemple via le ruissellement, où ils peuvent nuire aux organismes non-cibles. Les concentrations environnementales des pesticides sont souvent considérées sans risque pour les écosystèmes aquatiques, mais elles peuvent cependant induire des effets sublétaux dans les organismes exposés. De plus, les organismes ne font généralement pas face à un seul pesticide provenant d’un champ voisin, mais à un mélange complexe de différents composés chimiques qui interagissent entre eux pour former un cocktail potentiellement toxique avec des impacts inconnus et difficilement prévisibles. Ces composés, peuvent se dégrader au fil du temps et forment des métabolites plus au moins toxiques et persistants qui aggravent encore la complexité des mélanges. Cette thèse s’intéresse à la toxicité de pesticides seuls, en mélange ou en nanoformulation sur des organismes aquatiques non-cibles. Les stades de vie précoces vulnérables de deux organismes modèles : le poisson zèbre (Danio rerio) d’eau douce et un bivalve euryhalin l’huître creuse (Magallana gigas) ont été utilisés afin d’évaluer les effets sublétauxe de concentrations environnementales (détectées dans les cours d’eau européens) de différents pesticides couramment utilisés dont l’herbicide S-métolachlore avec ses deux métabolites acides oxanilique et sulfonique du métolachlore, l’insecticide imidaclopride et le fongicide propiconazole. En complément, une approche in situ a été développée pour évaluer les effets toxiques sur les stades embryo-larvaires de l’huître creuse associés à la qualité de l’eau du Bassin d’Arcachon, réceptacle final de différentes substances provenant des bassins versants. Les résultats indiquent une grande sensibilité des embryons et larves de poisson zèbre aux concentrations environnementales de propiconazole et à un degré moindre de l’imidaclopride. Au contraire, le S-métolachlore et ses métabolites ne présentent que peu d’effet sur le développement, les fonctions neurocomportementales et l’expression des gènes à l’exception des gènes impliqués dans le système thyroïdien. Ces pesticides en mélange semblent se comporter selon un modèle d’addition des concentrations si l’on considère le développement du poisson zèbre. Ces observations sont en lien avec un risque des pratiques agricoles actuelles. v Les résultats obtenus lors de ce travail montrent une faible toxicité du propiconazole et de l’imidaclopride sur le développement et le comportement des embryons et larves de l’huître creuse. Quelques effets causés par ces composés seuls ou en mélange sont observés au niveau moléculaire. La concentration environnementale du mélange a induit les malformations
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