Parasite and Pesticide Impacts on the Bumblebee (Bombus terrestris) Haemolymph Proteome

Author:

Askri Dalel1ORCID,Straw Edward A.23ORCID,Arafah Karim1,Voisin Sébastien N.14,Bocquet Michel5ORCID,Brown Mark J. F.2ORCID,Bulet Philippe6

Affiliation:

1. Plateforme BioPark d’Archamps, 74160 Archamps, France

2. Centre for Ecology, Evolution & Behaviour, Department of Biological Sciences, School for Life Sciences and the Environment, Royal Holloway University of London, Egham TW20 0EX, UK

3. Department of Botany, School of Natural Sciences, Trinity College Dublin, D02 PN40 Dublin, Ireland

4. Phylogene S.A. 62 RN113, 30620 Bernis, France

5. Apimedia BP22-Pringy, 74371 Annecy, France

6. CR, University Grenoble Alpes, IAB Inserm 1209, CNRS UMR5309, 38000 Grenoble, France

Abstract

Pesticides pose a potential threat to bee health, especially in combination with other stressors, such as parasites. However, pesticide risk assessment tests pesticides in isolation from other stresses, i.e., on otherwise healthy bees. Through molecular analysis, the specific impacts of a pesticide or its interaction with another stressor can be elucidated. Molecular mass profiling by MALDI BeeTyping® was used on bee haemolymph to explore the signature of pesticidal and parasitic stressor impacts. This approach was complemented by bottom-up proteomics to investigate the modulation of the haemoproteome. We tested acute oral doses of three pesticides—glyphosate, Amistar and sulfoxaflor—on the bumblebee Bombus terrestris, alongside the gut parasite Crithidia bombi. We found no impact of any pesticide on parasite intensity and no impact of sulfoxaflor or glyphosate on survival or weight change. Amistar caused weight loss and 19–41% mortality. Haemoproteome analysis showed various protein dysregulations. The major pathways dysregulated were those involved in insect defences and immune responses, with Amistar having the strongest impact on these dysregulated pathways. Our results show that even when no response can be seen at a whole organism level, MALDI BeeTyping® can detect effects. Mass spectrometry analysis of bee haemolymph provides a pertinent tool to evaluate stressor impacts on bee health, even at the level of individuals.

Funder

European Horizon 2020 research and innovation programme

Publisher

MDPI AG

Subject

Inorganic Chemistry,Organic Chemistry,Physical and Theoretical Chemistry,Computer Science Applications,Spectroscopy,Molecular Biology,General Medicine,Catalysis

Reference77 articles.

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2. European Commission, Directorate General for the Environment, and IUCN (International Union for Conservation of Nature) (2014). European Red List of Bees.

3. IPBES (2016). The Assessment Report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food Production, Zenodo.

4. Historical Decrease in Agricultural Landscape Diversity Is Associated with Shifts in Bumble Bee Species Occurrence;Hemberger;Ecol. Lett.,2021

5. Seed Coating with a Neonicotinoid Insecticide Negatively Affects Wild Bees;Andersson;Nature,2015

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