Toxicity of the Pesticides Imidacloprid, Difenoconazole and Glyphosate Alone and in Binary and Ternary Mixtures to Winter Honey Bees: Effects on Survival and Antioxidative Defenses
Elisa Pal,
Hanine Almasri,
Laurianne Paris,
Marie Diogon,
Maryline Pioz,
Marianne Cousin,
Déborah Sené,
Sylvie Tchamitchian,
Daiana Antonia Tavares,
Frédéric Delbac,
Nicolas Blot,
Jean-Luc Brunet,
Luc P. Belzunces
Affiliations
Elisa Pal
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Hanine Almasri
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Laurianne Paris
CNRS, Laboratoire Microorganismes, Génome et Environnement, Université Clermont Auvergne, F-63000 Clermont-Ferrand, France
Marie Diogon
CNRS, Laboratoire Microorganismes, Génome et Environnement, Université Clermont Auvergne, F-63000 Clermont-Ferrand, France
Maryline Pioz
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Marianne Cousin
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Déborah Sené
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Sylvie Tchamitchian
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Daiana Antonia Tavares
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Frédéric Delbac
CNRS, Laboratoire Microorganismes, Génome et Environnement, Université Clermont Auvergne, F-63000 Clermont-Ferrand, France
Nicolas Blot
CNRS, Laboratoire Microorganismes, Génome et Environnement, Université Clermont Auvergne, F-63000 Clermont-Ferrand, France
Jean-Luc Brunet
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
Luc P. Belzunces
INRAE, UR 406 A&E, Laboratoire de Toxicologie Environnementale, F-84000 Avignon, France
To explain losses of bees that could occur after the winter season, we studied the effects of the insecticide imidacloprid, the herbicide glyphosate and the fungicide difenoconazole, alone and in binary and ternary mixtures, on winter honey bees orally exposed to food containing these pesticides at concentrations of 0, 0.01, 0.1, 1 and 10 µg/L. Attention was focused on bee survival, food consumption and oxidative stress. The effects on oxidative stress were assessed by determining the activity of enzymes involved in antioxidant defenses (superoxide dismutase, catalase, glutathione-S-transferase, glutathione reductase, glutathione peroxidase and glucose-6-phosphate dehydrogenase) in the head, abdomen and midgut; oxidative damage reflected by both lipid peroxidation and protein carbonylation was also evaluated. In general, no significant effect on food consumption was observed. Pesticide mixtures were more toxic than individual substances, and the highest mortalities were induced at intermediate doses of 0.1 and 1 µg/L. The toxicity was not always linked to the exposure level and the number of substances in the mixtures. Mixtures did not systematically induce synergistic effects, as antagonism, subadditivity and additivity were also observed. The tested pesticides, alone and in mixtures, triggered important, systemic oxidative stress that could largely explain pesticide toxicity to honey bees.