, Volume 50, Issue 5, pp 733–744 | Cite as

Synergistic effects of three sterol biosynthesis inhibiting fungicides on the toxicity of a pyrethroid and neonicotinoid insecticide to bumble bees

  • Aaron IversonEmail author
  • Casey Hale
  • Leeah Richardson
  • Olivia Miller
  • Scott McArt
Original Article


Understanding how different pesticides influence bee health is inhibited by a limited knowledge about the interactions between different compounds to which bees are simultaneously exposed. Although research has demonstrated synergistic effects of some sterol biosynthesis inhibiting (SBI) fungicides on the toxicity of certain insecticides to bees, a high degree of variability exists in the relatively few SBI fungicide-insecticide interactions tested. Furthermore, most research has been conducted on honey bees, Apis mellifera, limiting our understanding of pesticide synergisms in native wild bees. We tested the effects of the SBI fungicides difenoconazole, myclobutanil, and fenhexamid on acute contact toxicity of the insecticides thiamethoxam (neonicotinoid) and bifenthrin (pyrethroid) to the common eastern bumble bee, Bombus impatiens. Based on range-finding trials, we selected a single dosage of each pesticide, with insecticides approximating LD20 values and fungicides approximating their maximum sublethal levels. We found that the triazole SBI fungicide difenoconazole interacted synergistically with bifenthrin, with a maximum synergy ratio of 1.48, while the triazole myclobutanil interacted synergistically with both bifenthrin and thiamethoxam, with maximum synergy ratios of 11.0 and 2.38, respectively. However, the hydroxyanilide SBI fungicide fenhexamid did not exhibit a synergistic effect on either insecticide. Our results suggest that certain SBI fungicides, and potentially those from particular SBI classes, may be particularly harmful to bumble bee health when co-exposure to insecticides occurs, despite their low toxicity when experienced in isolation.


bee conservation bioassay ecotoxicology pesticide interactions wild bee 



We thank Nicolas Baert, Ashley Fersch, Nelson Milano, Kerik Cox, Greg Loeb, Marvin Pritts, and Jeff Scott for their inputs on project design and implementation. We thank Nicolas Baert for conducting the LC-MS/MS analysis. We thank Emma Williams for assistance with running the bioassays. We thank the Cornell Statistical Consulting Unit, particularly Erika Mudrak, for her advice on statistical procedures. We thank Louis Iverson and two anonymous reviewers for providing comments on the manuscript. We thank Koppert Biological Systems for providing bumble bee colonies at a discounted rate.

Authors Contribution

AI and SM conceived of the research; AI, SM, CH, and LR designed the experiments; AI, CH, LR, and OM performed experiments and analysis; all authors wrote the paper and participated in the revisions of it. All authors read and approved the final manuscript.

Funding information

Funding for this project came from the National Institute of Food and Agriculture, US Department of Agriculture, grant number 2019-67013-29561 and Multistate Hatch Grant number 1010568, and from the New York Farm Viability Institute Grant number FOC 17001, each awarded to SM.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13592_2019_681_MOESM1_ESM.docx (27 kb)
ESM 1. (DOCX 26 kb)


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Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of EntomologyCornell UniversityIthacaUSA
  2. 2.Department of Environmental StudiesSt. Lawrence UniversityCantonUSA

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