Inferring pesticide toxicity to honey bees from a field-based feeding study using a colony model and Bayesian inference

Authors: MINUCCI, JEFFREY - Us Environmental Protection Agency (EPA); CURRY, ROBERT - Crystal River Consulting Llc; DeGrandi-Hoffman, Gloria; DOUGLASS, CAMERON - Us Environmental Protection Agency (EPA); GARBER, KRIS - Us Environmental Protection Agency (EPA); PURUCKER, THOMAS - Us Environmental Protection Agency (EPA)

Submitted to: Ecological Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/16/2021
Publication Date: 8/9/2021
Citation: Minucci, J.M., Curry, R., Hoffman, G.D., Douglass, C., Garber, K., Purucker, T.S. 2021. Inferring pesticide toxicity to honey bees from a field-based feeding study using a colony model and Bayesian inference. Ecological Applications. 31(8). Article e02442. https://doi.org/10.1002/eap.2442.
DOI: https://doi.org/10.1002/eap.2442

Interpretive Summary: Honey bees are crucial pollinators for agricultural crops but are threatened by a multitude of stressors including exposure to pesticides. Linking our understanding of how pesticides affect individual bees to colony-level responses is challenging because there are complex interactions among individuals in colonies and in relation to the environment. Mathematical models that simulate honey bee colony dynamics may be a tool to link individual and colony effects of a pesticide. The U.S. Environmental Protection Agency (USEPA) and U.S. Department of Agriculture (USDA) are developing the VarroaPop+Pesticide model. The model simulates the dynamics of honey bee colonies and how they respond to multiple stressors, including weather, varroa mites and pesticides. To evaluate this model, we used Approximate Bayesian Computation to fit data from a field study where honey bee colonies were fed clothianidin in sugar syrup. We reproduced the colony feeding study data by simulating colony size and mortality from ingestion of contaminated food. The VarroaPop model, when parameterized to the feeding study data was able to predict overall trends in colony population through time as well as general caste structure. VarroaPop+Pesticide also reproduced colony declines from increasing clothianidin exposure. However, the model underestimated adverse effects at low exposure and overestimated colony recovery at the highest exposure level for adults and pupae, suggesting that mechanisms besides oral toxicity-induced mortality may play a role in colony declines. The VarroaPop+Pesticide model estimates an adult oral LD50 of 18.9 ng/bee based on the simulated feeding study data, which falls just above the 95% confidence intervals of values observed in laboratory toxicology studies on individual bees. Overall, our results demonstrate a novel method for interpreting data from individual bee and colony level studies, and for predicting how colonies might respond to hypothetical scenarios such as untested concentrations, changes in weather or additional stressors.

Technical Abstract: Honey bees are crucial pollinators for agricultural crops but are threatened by a multitude of stressors including exposure to pesticides. Linking our understanding of how pesticides affect individual bees to colony-level responses is challenging because hives show emergent properties based on complex internal processes and interactions among individual bees. Agent-based models that simulate honey bee colony dynamics may be a tool for scaling between individual and colony effects of a pesticide. The U.S. Environmental Protection Agency (USEPA) and U.S. Department of Agriculture (USDA) are developing the VarroaPop+Pesticide model which simulates the dynamics of honey bee colonies and how they respond to multiple stressors, including weather, varroa mites and pesticides. To evaluate this model, we used Approximate Bayesian Computation to fit field data from an empirical study where honey bee colonies were fed the insecticide clothianidin. This allowed us to reproduce colony feeding study data by simulating hive demography and mortality from ingestion of contaminated food. We found that VarroaPop+Pesticide was able to fit general trends in colony population size and structure and reproduce colony declines from increasing clothianidin exposure. The model underestimated adverse effects at low exposure (36 µg/kg), however, and overestimated recovery at the highest exposure level (140 µg/kg), for the adult and pupa endpoints, suggesting that mechanisms besides oral toxicity-induced mortality may have played a role in colony declines. The VarroaPop+Pesticide model estimates an adult oral LD50 of 18.9 ng/bee (95% CI: 10.1–32.6) based on the simulated feeding study data, which falls just above the 95% confidence intervals of values observed in laboratory toxicology studies on individual bees. Overall, our results demonstrate a novel method for analyzing colony-level data on pesticide effects on bees and making inferences on pesticide toxicity to individual bees.