The active ingredients of a mitotoxic fungicide negatively affect pollen consumption and worker survival in laboratory-reared honey bees (Apis mellifera)

Authors: FISHER, A. - Arizona State University; COGLEY, T. - Arizona State Geological Survey; OZTURK, C. - Arizona State University; DeGrandi-Hoffman, Gloria; SMITH, B. - Arizona State University; KAFTANOGLU, O. - Arizona State University; FEWELL, J. - Arizona State University; HARRISON, J.F. - Arizona State University

Submitted to: Ecotoxicology and Environmental Safety
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/26/2021
Publication Date: 10/1/2021
Citation: Fisher, A., Cogley, T., Ozturk, C., Hoffman, G.D., Smith, B., Kaftanoglu, O., Fewell, J., Harrison, J. 2021. The active ingredients of a mitotoxic fungicide negatively affect pollen consumption and worker survival in laboratory-reared honey bees (Apis mellifera). Ecotoxicology and Environmental Safety. 226. Article 112841. https://doi.org/10.1016/j.ecoenv.2021.112841.
DOI: https://doi.org/10.1016/j.ecoenv.2021.112841

Interpretive Summary: The fungicide Pristine® and its active ingredients (25.2% boscalid, 12.8% pyraclostrobin) have low acute toxicity to caged honey bee workers, but many sublethal effects at field-relevant doses. In previous field tests with colonies fed Pristine® at field relevant concentrations, we found that Pristine® increased worker pollen consumption, reduced worker longevity and colony populations. To directly compare these colony-level results to more standard lab toxicology tests, we examined the effects of a range of field-relevant concentrations of Pristine® on the survival and pollen consumption of honey bee workers 0-14 days of age. Also, to separate the effects of the inert and two active ingredients, we fed bees pollen containing boscalid, pyraclostrobin, or pyraclostrobin plus boscalid, at concentrations matching those in the Pristine® treatments. Both Pyraclostrobin and Boscalid alone significantly reduced pollen consumption across the duration of the experiment in a dose-dependent manner. Boscalid alone reduced worker bee survival in a dose-dependent manner. Consumption of Pristine® or pyraclostrobin plus boscalid did not affect survival, providing evidence that the inert ingredients in Pristine® do not affect honey bees. The stronger toxic effects of Pristine® observed in field colonies compared to this lab test, and the opposite responses of pollen consumption in the lab and field to Pristine®, show that standard laboratory toxicology tests can fail to predict responses of pollinators to pesticides in field settings.

Technical Abstract: Recent observations of many sublethal effects of pesticides on pollinators have raised questions about whether standard short-term laboratory tests of pesticide effects on survival are sufficient for pollinator protection. The fungicide Pristine® and its active ingredients (25.2% boscalid, 12.8% pyraclostrobin) have been reported to have low acute toxicity to caged honey bee workers, but many sublethal effects at field-relevant doses have been reported, and we recently found in whole colony field tests that Pristine® increased worker pollen consumption, reduced worker longevity and colony populations at field relevant concentrations. To directly compare these whole-colony field results to more standard lab toxicology tests, we examined the effects of a range of field-relevant concentrations of Pristine® on the survival and pollen consumption of honey bee workers 0-14 days of age. Also, to separate the effects of the inert and two active ingredients, we fed bees pollen containing boscalid, pyraclostrobin, or pyraclostrobin plus boscalid, at concentrations matching those in the Pristine® treatments. Pyraclostrobin significantly reduced pollen consumption across the duration of the experiment, and dose-dependently reduced pollen consumption on days 12-14. Pristine® and boscalid significantly reduced pollen feeding rate on days 12-14. Boscalid reduced survival in a dose-dependent manner. Consumption of Pristine® or pyraclostrobin plus boscalid did not affect survival, providing evidence against strong negative effects of the inert ingredients in Pristine® and against negative synergistic effects of boscalid and pyraclostrobin. The stronger toxic effects of Pristine® observed in field colonies compared to this lab test, and the opposite responses of pollen consumption in the lab and field to Pristine®, show that standard laboratory toxicology tests can fail to predict responses of pollinators to pesticides and to provide protection.