Simulating the Effects of Pesticides on Honey Bee (Apis mellifera L.) Colonies with BeePop+
Abstract
:1. Introduction
2. Materials and Methods
3. Results and Discussion
3.1. Phase 1: Model Objectives
3.1.1. Determining Necessary Level of Realism and Complexity
3.1.2. How Model Outputs Link to Measurement Endpoints and Protection Goals
3.1.3. Temporal and Spatial Considerations
3.1.4. Assumptions and Sources of Uncertainty
3.2. Phase 2: Data Compilation
3.3. Phase 3: Decision Steps
3.4. Phase 4: Conceptual Model
3.5. Phase 5: Model Implementation
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Protection Goal | Assessment Endpoints | Measurement Endpoints Typically Used in Risk Assessments | |
---|---|---|---|
Individual Level | Colony/Population Level | ||
Provision of pollination services | Numbers of colonies, population size, stability of native bees and commercially managed bees | Adult worker survival; larval survival; pupal survival; adult growth; adult emergence | Number each life stage present over time; presence of queen |
Production of colony products | Quantity and quality of colony products | Amount of pollen and nectar present in colony; presence of pesticide in colony products | |
Contribution to bee biodiversity | Species richness and abundance | Species richness and abundance |
Characteristic | Ecological Concept | Specification/Parameter (Simplifying Assumptions) |
---|---|---|
Stage-level energetics [17] | Different stages (adult, larvae, drones, queens) have specific energetic needs that are met by the consumption of nectar/honey and pollen. | Stage-specific energetic needs are specified directly as model parameters represented by consumption rates. |
Active season colony-level energetics [17] | Sufficient energy and pollen availabilities are required to raise brood | Nectar and pollen consumption rates for brood stages are included as parameters. |
Overwintering colony-level energetics [37,38,39] | Sufficient energy reserves and adult members (due to thermoregulation needs) are required to overwinter | Overwinter dynamics are simulated by significantly reduced foraging and egg-laying behavior, as dictated by daylength and temperature. |
Colony growth * [21,22] | Colony growth is determined by the rate of egg-laying by the queen, the mortality of each stage of bees in the colony, and the density of the colony. | Egg-laying rate is defined as queen strength parameter and is influenced by a function incorporating photoperiod, temperature, and colony size. Natural stage-based mortality rates are included directly as parameters. Mortality also occurs due to pesticide exposure and is modeled via a pesticide exposure module. Queen replacement can be simulated to represent a common beekeeping practice. Queen longevity. Colony size increase due to egg-laying rates, inverse for mortality. |
Colony population structure and stage-specific rates [22,29,39,40,41] | Stage transition rates and proportion of drones influenced by photoperiod, local climate, colony size, and resource availability. Pesticide tolerance varies by stage and across colonies. | Stage-specific populations (egg, larvae, pupae, adults (drones, workers, foragers) controlled by egg-laying rate and stage-specific development rates and division of duties. Parameter specifying proportion of eggs that become workers and drones influenced by time of year (photoperiod). Parameter specifying proportion of eligible foragers actively foraging. Parameter specifying amount of sperm influences laying of fertilized eggs (lack of sperm results in laying drones). |
Colony resource collection (by foragers) [22,29,42,43,44] | Empirical data to determine thresholds for foraging activity are limited. Forager activity influenced by temperature, wind velocity, and rainfall. Forage range varies from several hundred meters to 5500 m from colony. Foraging range and time influenced by landscape composition. | Foraging activity limited to threshold as determined by weather parameters (e.g., rainfall, temperature). No explicit spatial component of resources. Constant/unlimited resource availability is assumed. Parameter specifying number of loads and trips made by foragers for pollen and nectar. |
Seasonal pollen and nectar consumption | Sufficient pollen and nectar resources are required to rear brood, with excess resources collected during the foraging season stored in colony. A colony fails if it runs out of resources over winter. | Specified food consumption rates for different life stages and duties differ by seasons. Minimum energy reserve and adult population (for thermoregulation needs) requirements to survive overwinter are specified. Model allows for simulated supplemental feeding, a common beekeeper practice. |
Characteristic | Ecological Concept | Specification/Parameter (Simplifying Assumptions) |
---|---|---|
Exposure pathway [45] | Consumption of nectar and pollen contaminated with pesticide(s). Contact exposure for foraging bees. | In colony, bees (larvae and adults) have age and stage-specific food consumption rates. Their pesticide dose is a function of food intake rate and pesticide concentration in pollen and nectar. Does not account for in-colony transfer and transformation of pesticide residues. Pollen and nectar (honey) stores are assumed to be well mixed, but they are actually stored in individual cells with variable pesticide concentrations. Does not account for exposure via plant guttation water. |
Timing of exposures [46] | Contact exposure occurs during application. Dietary exposure happens while crops are blooming. | Migratory bee colonies (for pollination services) may have repeated exposures. Exposure may occur past the growing season when stored nectar and pollen are contaminated with persistent pesticide. |
Exposure pattern within habitat | Approach assumes that colonies are only feeding on treated crops. | Available information indicates that bees forage on a variety of plants, not just crops. Model can be adjusted to calculate percent of foraging on treated crop needed to impact a colony. |
Exposure profile by stage [18] | Stage-specific food consumption rates account for different exposure levels among life stages. | BeeREX includes information on stage and age-specific food consumption rates. Food consumption rates can be varied in Monte Carlo simulation. |
Representation of toxic effects | Standard laboratory-based toxicity information for adult and larval bees used to calculate magnitude of mortality resulting from specific doses. Accounts for exposures and effects of a pesticide active ingredient. | Magnitude of mortality in a cohort corresponds to magnitude of exposure and dose-response curve from standard LD50 study. Does not account for sublethal effects; however, user can adjust adult longevity or decrease foraging activity if toxicity data are available. Does not incorporate queen mortality resulting from pesticide exposure, user can adjust queen longevity/replacement. Queen exposure assumed to be lower than workers because workers consume pollen and nectar and queen consumes jelly. Does not account for effects of multiple pesticide active ingredient exposures. |
Characteristic | Ecological Concept | Specification/Parameter (Simplifying Assumptions) |
---|---|---|
Biological stressors [47,48,49] | Varroa mites impose stress on colony dynamics through the spread of viruses, including deformed wing virus (DWV). Other stressors include bacteria, fungal diseases, and pest insects. | Biological stressors associated with Varroa mites, including viral infection, are accounted for directly by Varroa infestation in pupal cells and indirectly by manipulating adult worker longevity rates. Other stressors are not considered. |
Beekeeper management practices [50] | The model simulates impacts of miticide treatments on reducing Varroa impacts. Supplemental feeding can be considered. | Interactions between in-colony medications/miticides and pesticides. |
Environmental stressors [22] | Egg laying rates influenced by temperature and photoperiod Foraging influenced by temperature, wind speed, and rainfall | Weather parameters chosen to represent geographic location of interest. Some days may be partial foraging days. |
Landscape composition [29] | Assemblage of natural and cultivated plants determine nectar and pollen resource availability, which influences foraging success and distance of foraging. Availability of pollen and nectar varies over time based on phenology of plants. | Landscape composition and corresponding resource availability is temporo-spatially determined. Model assumes that bees forage 100% on treated crop; however, user can evaluate impact of this assumption by calculating % foraging on crop needed to impact colonies. Effect of landscape on forager lifespan and mortality is not considered. |
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Garber, K.; DeGrandi-Hoffman, G.; Curry, R.; Minucci, J.M.; Dawson, D.E.; Douglass, C.; Milone, J.P.; Purucker, S.T. Simulating the Effects of Pesticides on Honey Bee (Apis mellifera L.) Colonies with BeePop+. Ecologies 2022, 3, 275-291. https://doi.org/10.3390/ecologies3030022
Garber K, DeGrandi-Hoffman G, Curry R, Minucci JM, Dawson DE, Douglass C, Milone JP, Purucker ST. Simulating the Effects of Pesticides on Honey Bee (Apis mellifera L.) Colonies with BeePop+. Ecologies. 2022; 3(3):275-291. https://doi.org/10.3390/ecologies3030022
Chicago/Turabian StyleGarber, Kristina, Gloria DeGrandi-Hoffman, Robert Curry, Jeffrey M. Minucci, Daniel E. Dawson, Cameron Douglass, Joseph P. Milone, and S. Thomas Purucker. 2022. "Simulating the Effects of Pesticides on Honey Bee (Apis mellifera L.) Colonies with BeePop+" Ecologies 3, no. 3: 275-291. https://doi.org/10.3390/ecologies3030022