Neonicotinoid Clothianidin reduces honey bee immune response and contributes to  Varroa  mite proliferation

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Abstract

The neonicotinoid Clothianidin has a negative impact on NF-κB signaling and on immune responses controlled by this transcription factor, which can boost the proliferation of honey bee parasites and pathogens. This effect has been well documented for the replication of deformed wing virus (DWV) induced by Clothianidin in honey bees bearing an asymptomatic infection. Here, we conduct infestation experiments of treated bees to show that the immune-suppression exerted by Clothianidin is associated with an enhanced fertility of the parasitic mite Varroa destructor, as a possible consequence of a higher feeding efficiency. A conceptual model is proposed to describe the synergistic interactions among different stress agents acting on honey bees.

Abstract

Pesticides could increase bees’ susceptibility to parasites, but the nature of this interaction has been unclear. Here the authors show that the pesticide Clothianidin reduces the wound healing immune response in bees, allowing the ectoparasitic Varroa mites to consume more bee hemolymph and amplify reproduction.

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Most cited references 39

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Bee declines driven by combined stress from parasites, pesticides, and lack of flowers.

Dave Goulson, Elizabeth Nicholls, Cristina Botías … (2015)

Bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined; bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites accidentally spread by humans. Climate change is likely to exacerbate these problems in the future. Stressors do not act in isolation; for example, pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple interacting stressors is driving honey bee colony losses and declines of wild pollinators, but such interactions are not addressed by current regulatory procedures, and studying these interactions experimentally poses a major challenge. In the meantime, taking steps to reduce stress on bees would seem prudent; incorporating flower-rich habitat into farmland, reducing pesticide use through adopting more sustainable farming methods, and enforcing effective quarantine measures on bee movements are all practical measures that should be adopted. Effective monitoring of wild pollinator populations is urgently needed to inform management strategies into the future.

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The host defense of Drosophila melanogaster.

Bruno Lemaitre, Jules Hoffmann (2007)

To combat infection, the fruit fly Drosophila melanogaster relies on multiple innate defense reactions, many of which are shared with higher organisms. These reactions include the use of physical barriers together with local and systemic immune responses. First, epithelia, such as those beneath the cuticle, in the alimentary tract, and in tracheae, act both as a physical barrier and local defense against pathogens by producing antimicrobial peptides and reactive oxygen species. Second, specialized hemocytes participate in phagocytosis and encapsulation of foreign intruders in the hemolymph. Finally, the fat body, a functional equivalent of the mammalian liver, produces humoral response molecules including antimicrobial peptides. Here we review our current knowledge of the molecular mechanisms underlying Drosophila defense reactions together with strategies evolved by pathogens to evade them.

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Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

N. Simon-Delso, V. Amaral-Rogers, L P Belzunces … (2014)

Since their discovery in the late 1980s, neonicotinoid pesticides have become the most widely used class of insecticides worldwide, with large-scale applications ranging from plant protection (crops, vegetables, fruits), veterinary products, and biocides to invertebrate pest control in fish farming. In this review, we address the phenyl-pyrazole fipronil together with neonicotinoids because of similarities in their toxicity, physicochemical profiles, and presence in the environment. Neonicotinoids and fipronil currently account for approximately one third of the world insecticide market; the annual world production of the archetype neonicotinoid, imidacloprid, was estimated to be ca. 20,000 tonnes active substance in 2010. There were several reasons for the initial success of neonicotinoids and fipronil: (1) there was no known pesticide resistance in target pests, mainly because of their recent development, (2) their physicochemical properties included many advantages over previous generations of insecticides (i.e., organophosphates, carbamates, pyrethroids, etc.), and (3) they shared an assumed reduced operator and consumer risk. Due to their systemic nature, they are taken up by the roots or leaves and translocated to all parts of the plant, which, in turn, makes them effectively toxic to herbivorous insects. The toxicity persists for a variable period of time—depending on the plant, its growth stage, and the amount of pesticide applied. A wide variety of applications are available, including the most common prophylactic non-Good Agricultural Practices (GAP) application by seed coating. As a result of their extensive use and physicochemical properties, these substances can be found in all environmental compartments including soil, water, and air. Neonicotinoids and fipronil operate by disrupting neural transmission in the central nervous system of invertebrates. Neonicotinoids mimic the action of neurotransmitters, while fipronil inhibits neuronal receptors. In doing so, they continuously stimulate neurons leading ultimately to death of target invertebrates. Like virtually all insecticides, they can also have lethal and sublethal impacts on non-target organisms, including insect predators and vertebrates. Furthermore, a range of synergistic effects with other stressors have been documented. Here, we review extensively their metabolic pathways, showing how they form both compound-specific and common metabolites which can themselves be toxic. These may result in prolonged toxicity. Considering their wide commercial expansion, mode of action, the systemic properties in plants, persistence and environmental fate, coupled with limited information about the toxicity profiles of these compounds and their metabolites, neonicotinoids and fipronil may entail significant risks to the environment. A global evaluation of the potential collateral effects of their use is therefore timely. The present paper and subsequent chapters in this review of the global literature explore these risks and show a growing body of evidence that persistent, low concentrations of these insecticides pose serious risks of undesirable environmental impacts.

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Author and article information

Contributors

Francesco Nazzi:

ORCID: http://orcid.org/0000-0002-2085-7621

francesco.nazzi@uniud.it

Francesco Pennacchio:

ORCID: http://orcid.org/0000-0002-8794-9328

f.pennacchio@unina.it

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 18 November 2020

Publication date PMC-release: 18 November 2020

Publication date Collection: 2020

Volume: 11

Electronic Location Identifier: 5887

Affiliations

[1 ]GRID grid.5390.f, ISNI 0000 0001 2113 062X, Dipartimento di Scienze AgroAlimentari, Ambientali e Animali, Università degli Studi di Udine, ; Udine, Italy

[2 ]GRID grid.4691.a, ISNI 0000 0001 0790 385X, Dipartimento di Agraria, Laboratorio di Entomologia “E. Tremblay”, Università degli Studi di Napoli “Federico II”, ; Portici, Napoli Italy

[3 ]GRID grid.423616.4, ISNI 0000 0001 2293 6756, Present Address: CREA, Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria, Centro di Ricerca Agricoltura e Ambiente, ; Bologna, Italy

[4 ]GRID grid.83440.3b, ISNI 0000000121901201, Present Address: Department of Biological Sciences, Royal Holloway, University of London, ; London, UK

Author information

Desiderato Annoscia http://orcid.org/0000-0002-2405-4914

Davide Frizzera http://orcid.org/0000-0002-8809-2768

Francesco Nazzi http://orcid.org/0000-0002-2085-7621

Francesco Pennacchio http://orcid.org/0000-0002-8794-9328

Article

Publisher ID: 19715

DOI: 10.1038/s41467-020-19715-8

PMC ID: 7675992

PubMed ID: 33208729

SO-VID: 9ad862bc-b1cf-43d3-a736-8c814bec2367

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 10 April 2020

Date accepted : 23 October 2020

Funding

Funded by: FundRef https://doi.org/10.13039/100010661, EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020);

Award ID: 773921

Award Recipient : Francesco Nazzi

Funded by: Italian Ministry of University, PRIN 2017 - UNICO (2017954WNT)

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ScienceOpen disciplines: Uncategorized

Keywords: ecology,parasitology,virology,entomology

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ScienceOpen disciplines: Uncategorized

Keywords: ecology, parasitology, virology, entomology

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Neonicotinoid Clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation

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Most cited references 39

Bee declines driven by combined stress from parasites, pesticides, and lack of flowers.

The host defense of Drosophila melanogaster.

Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites

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