Citation:

Minucci, J., R. Curry, G. DeGrandi-Hoffman, C. Douglass, K. Garber, AND S. Purucker. Inferring pesticide toxicity to honey bees from a field-based feeding study using a colony model and Bayesian inference. ECOLOGICAL APPLICATIONS. Ecological Society of America, Ithaca, NY, 31(8):e02442, (2021). https://doi.org/10.1002/eap.2442

Impact/Purpose:

The EPA Office of Pesticide Programs (OPP) registers pesticides under the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA). This research is an active collaboration with OPP to improve the Agency’s method for evaluating the effects of pesticides on bee colonies. Honey bees provide essential pollination for many agricultural crops, but these services are threatened by increased colony losses in North America and Europe in recent decades. While multiple stressors are implicated (i.e., disease, habitat change, genetic issues linked to breeding), pesticides have been identified as an important contributor to these declines because they can cause direct mortality to individual bees, as well as a wide range of sublethal effects. We present a method for inferring individual-level pesticide toxicity from colony-level field data using the VarroaPop+Pesticide agent-based colony model. We used data from a registrant-submitted feeding study on clothianidin, a neonicotinoid insecticide, where hives were dosed with spiked nectar of varying concentrations over a five-week period. We implemented a Bayesian hierarchical model based on VarroaPop to explain the dynamics of single colonies in the feeding study. We then applied Approximate Bayesian Computation (ABC) to fit our model to the empirical data and inferred parameters describing individual toxicity in VarroaPop. This method was done in a repeatable way so that it can be used by the program office for other pesticides of concern for honeybees.

Description:

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 colonies 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 colony 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.

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