Field cross-fostering and in vitro rearing demonstrate negative effects of both larval and adult exposure to a widely used fungicide in honey bees (Apis mellifera)

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

Submitted to: Ecotoxicology and Environmental Safety
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/10/2021
Publication Date: 4/24/2021
Citation: Fisher Ii, A., Hoffman, G.D., Smith, B., Ozturk, C., Kaftanoglu, O., Fewell, J., Harrison, J. 2021. Field cross-fostering and in vitro rearing demonstrate negative effects of both larval and adult exposure to a widely used fungicide in honey bees (Apis mellifera). Ecotoxicology and Environmental Safety. 217. Article 112251. https://doi.org/10.1016/j.ecoenv.2021.112251.
DOI: https://doi.org/10.1016/j.ecoenv.2021.112251

Interpretive Summary: Pollinators and other insects are experiencing an ongoing worldwide decline. While various environmental stressors are implicated, including pesticide exposure, the causes of these declines are complex and highly debated. Fungicides may constitute a particularly prevalent threat to pollinator health due to their application during bloom, and because pollinators such as bees may consume fungicide-tainted pollen or nectar. At a colony level, consumption of pollen containing the fungicide Pristine® causes worker bees to forager earlier in life, lowers worker survival, increases pollen foraging, and reduces colony population size. Because older larvae and young adult bees consume most of the pollen collected by a colony, we hypothesized that effects of feeding on pollen contaminated with Pristine® should be most pronounced in these lifestages. To test this hypothesis, we used a cross-fostering experimental design, with bees reared in colonies provided pollen patties with added Pristine®. Bee used in the study were exposed to the pollen patties only in their larval stage, only as adults, or during both larval and stages. We found that exposure to Pristine® in either the larval or adult stage reduced survival relative to control bees not exposed to Pristine® . Bees exposed to pollen patties with Pristine® during both the larval and adult stages had the lowest survival. Adult exposure caused precocious foraging, while larval exposure increased the tendency to forage for pollen. These results demonstrate that pollen containing Pristine® can affect both larvae and adults in a colony. To further test the potential negative effects of direct consumption of Pristine® on larvae, we reared them in vitro on food containing Pristine® at a range of concentrations. Consumption of Pristine® reduced survival rates of larvae at all concentrations tested, including a concentration 10% lower than those measured in pollen collected by bees foraging in a Pristine®-sprayed crop. We conclude that consumption of pollen containing Pristine® by field honey bee colonies likely impacts colony population size and foraging behavior by affecting both larvae and adult stages.

Technical Abstract: Pollinators and other insects are experiencing an ongoing worldwide decline. While various environmental stressors have been implicated, including pesticide exposure, the causes of these declines are complex and highly debated. Fungicides may constitute a particularly prevalent threat to pollinator health due to their application on many crops during bloom, and because pollinators such as bees may consume fungicide-tainted pollen or nectar. Consumption of pollen containing the fungicide Pristine® at field-relevant concentrations by honey bee colonies increases pollen foraging, causes earlier foraging, lowers worker survival, and reduces colony population size. Because most pollen is consumed by young adults, we hypothesized that Pristine® in pollen exerts its negative effects on honey bee colonies primarily by effects on the adult stage. To rigorously test this hypothesis, we used a cross-fostering experimental design, with bees reared in colonies provided Pristine® at a supra-field dose, only in the larvae, only in the adult, or both stages. In contrast to our predictions, exposure to Pristine® in either the larval or adult stage reduced survival relative to control bees not exposed to Pristine®, and exposure to the fungicide at both larval and adult stages further reduced survival. Adult exposure caused precocious foraging, while larval exposure increased the tendency to forage for pollen. These results demonstrate that pollen containing Pristine® can negatively affect both larvae and adults in a hive, though the magnitude of such effects may be smaller at field-realistic doses. To further test the potential negative effects of direct consumption of Pristine® on larvae, we reared them in vitro on food containing Pristine® at a range of concentrations. Consumption of Pristine® reduced survival rates of larvae at all concentrations tested, including a concentration 10% of the lowest Pristine® concentration measured in pollen collected by bees foraging in a Pristine®-sprayed field. Larval and adult weights were only reduced at a supra-field concentration. We conclude that consumption of pollen containing Pristine® by field honey bee colonies likely exerts impacts on colony population size and foraging behavior by affecting both larvae and adults.