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  • Open Access

Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera)

Authors

  • Cédric Alaux,

    Corresponding author
    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire Biologie et Protection de l'abeille, Site Agroparc, 84914 Avignon, France.
      *E-mail: cedric.alaux@avignon.inra.fr; Tel. (+33) 4 32 72 26 18; Fax (+33) 4 32 72 26 02.
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  • Jean-Luc Brunet,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire de Toxicologie Environnementale, Site Agroparc, 84914 Avignon, France.
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  • Claudia Dussaubat,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire Biologie et Protection de l'abeille, Site Agroparc, 84914 Avignon, France.
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  • Fanny Mondet,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire de Toxicologie Environnementale, Site Agroparc, 84914 Avignon, France.
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  • Sylvie Tchamitchan,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire de Toxicologie Environnementale, Site Agroparc, 84914 Avignon, France.
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  • Marianne Cousin,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire de Toxicologie Environnementale, Site Agroparc, 84914 Avignon, France.
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  • Julien Brillard,

    1. INRA, UMR 408 Sécurité et Qualité des Produits d'Origine Végétale, Site Agroparc, 84914 Avignon, France.
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  • Aurelie Baldy,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire Biologie et Protection de l'abeille, Site Agroparc, 84914 Avignon, France.
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  • Luc P. Belzunces,

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire de Toxicologie Environnementale, Site Agroparc, 84914 Avignon, France.
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  • Yves Le Conte

    1. INRA, UMR 406 Abeilles et Environnement, Laboratoire Biologie et Protection de l'abeille, Site Agroparc, 84914 Avignon, France.
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*E-mail: cedric.alaux@avignon.inra.fr; Tel. (+33) 4 32 72 26 18; Fax (+33) 4 32 72 26 02.

Summary

Global pollinators, like honeybees, are declining in abundance and diversity, which can adversely affect natural ecosystems and agriculture. Therefore, we tested the current hypotheses describing honeybee losses as a multifactorial syndrome, by investigating integrative effects of an infectious organism and an insecticide on honeybee health. We demonstrated that the interaction between the microsporidia Nosema and a neonicotinoid (imidacloprid) significantly weakened honeybees. In the short term, the combination of both agents caused the highest individual mortality rates and energetic stress. By quantifying the strength of immunity at both the individual and social levels, we showed that neither the haemocyte number nor the phenoloxidase activity of individuals was affected by the different treatments. However, the activity of glucose oxidase, enabling bees to sterilize colony and brood food, was significantly decreased only by the combination of both factors compared with control, Nosema or imidacloprid groups, suggesting a synergistic interaction and in the long term a higher susceptibility of the colony to pathogens. This provides the first evidences that interaction between an infectious organism and a chemical can also threaten pollinators, interactions that are widely used to eliminate insect pests in integrative pest management.

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