A Meta-Analysis Comparing the Sensitivity of Bees to Pesticides

A Meta-analysis Comparing The Sensitivity Of Bees To Pesticides reveals critical insights for environmental protection, and COMPARE.EDU.VN offers comprehensive analysis. This study addresses the crucial question of how pesticide exposure affects different bee species, providing a foundation for informed decision-making and sustainable agricultural practices. The research delves into pesticide toxicity, bee conservation, and ecological impact assessment.

1. Introduction: The Importance of Bee Sensitivity to Pesticides

Bees play a pivotal role in global ecosystems and agriculture, contributing significantly to pollination and biodiversity. However, the widespread use of pesticides poses a significant threat to bee populations, leading to declines and ecological imbalances. Understanding the sensitivity of different bee species to pesticides is crucial for effective risk assessment and the development of mitigation strategies. COMPARE.EDU.VN is dedicated to providing objective comparisons to help researchers and policymakers make informed decisions about environmental safety and ecological protection.

2. Background: Current Risk Assessment Methods

Current risk assessment methods for bees primarily rely on data from honey bees (Apis mellifera), using this species as a proxy for all other bee species. This approach raises concerns about whether honey bee data accurately represent the sensitivity of diverse bee species to pesticides. Existing studies compare bee species sensitivity based on the 48-hour median lethal dose (LD50) values from acute tests. However, this method may not fully account for differences in kinetics, physiology, and inherent species sensitivity.

3. Challenges with LD50 Comparisons

Using 48-hour LD50 values to compare bee species sensitivity presents several challenges:

3.1 Differences in Kinetics

Variations in how different bee species process and eliminate pesticides can affect the observed LD50 values. These differences in kinetics are not always indicative of true differences in sensitivity.

3.2 Physiological Variations

The physiology of bees, including overall size, honey stomach size (for oral tests), and physical appearance (for contact tests), can influence pesticide sensitivity. Smaller bees may exhibit different responses compared to larger bees.

3.3 Time-Dependency of LD50

LD50 values are time-dependent, meaning their effectiveness changes over time. This variability can lead to inconsistent and unreliable comparisons between species.

4. Toxicokinetic-Toxicodynamic (TKTD) Modeling

To address the limitations of LD50 comparisons, a toxicokinetic-toxicodynamic (TKTD) model, known as BeeGUTS (Bee General Uniform Threshold Model for Survival), has been developed. This model integrates acute oral, acute contact, and chronic test results within a consistent framework.

4.1 BeeGUTS Model Advantages

The BeeGUTS model offers several advantages over traditional LD50 comparisons:

Comprehensive Integration: It combines data from various types of tests into a single, coherent framework.
Parameter Estimation: It allows for the estimation of key parameters, including the effect threshold, which reflects the inherent sensitivity of bees.
Time-Independence: The effect threshold is time- and test-independent, making it a more robust proxy for species sensitivity.

5. Modeling Approach: Key Considerations

The BeeGUTS model uses exposure concentration as the driving force for effects, combined with observed survival patterns over time. The model accounts for different exposure scenarios, including acute contact, acute oral, and chronic tests.

5.1 Acute Contact Test

In an acute contact test, the pesticide is applied as a droplet on the bee’s thorax. The concentration declines over time, which is modeled using a first-order process.

5.2 Acute Oral Test

In an acute oral test, bees consume contaminated food, and the toxicant is taken up in the honey stomach. The concentration declines over time based on the honey stomach volume and feeding rate.

5.3 Chronic Test

In a chronic test, bees are fed contaminated food with a fixed concentration, ensuring constant exposure over time.

6. BeeGUTS Model Description

The BeeGUTS model describes the uptake of the compound (toxicokinetics) and links this uptake to effects by assuming a death mechanism (toxicodynamics). The model distinguishes between two death mechanisms: Stochastic Death (SD) and Individual Tolerance (IT). Both mechanisms use the effect threshold as a key parameter.

6.1 Stochastic Death (SD) Model

The SD model assumes that individuals die randomly based on their exposure to the toxicant.

6.2 Individual Tolerance (IT) Model

The IT model assumes that individuals have varying tolerances to the toxicant, and death occurs when an individual’s tolerance is exceeded.

7. Calibration and Validation of the BeeGUTS Model

The BeeGUTS model must be calibrated and validated for different bee species to ensure its accuracy and reliability. Calibration involves estimating parameter values using experimental data, while validation involves predicting effects using independent data sets.

7.1 Data Requirements

Calibration requires a data set with at least seven time points, while validation requires an additional time-dependent exposure, preferably a repeated pulse exposure.

7.2 Calibration Data for B. terrestris and O. bicornis

Data for non-Apis bee species are limited. However, chronic effects studies on Apis mellifera, B. terrestris, and O. bicornis provide valuable data for model calibration.

7.3 Validation Data for B. terrestris

Finding direct data on honey stomach size for bumble bees (B. terrestris) can be challenging. Default settings for honey crop volume and feeding rate can be used as first estimates.

7.4 Validation Data for O. bicornis

Data on honey stomach size for O. bicornis are also scarce. An alternative approach involves estimating rate values from available survival data.

8. Acute Oral Exposure in O. bicornis

To accurately describe acute oral uptake in O. bicornis, an estimation of honey stomach size is necessary. A three-step procedure can be used:

Calibrate the model with chronic data.
Estimate the honey stomach release rate (ksr) using the calibrated model.
Validate the model with the estimated parameters.

9. Acute Contact Exposure for O. bicornis

Data on uptake over the chitin layer for O. bicornis are limited. The value of the contact availability rate (kca) can be estimated using combined chronic and acute data.

10. Derived Rate Values

The honey stomach release rate (ksr) and contact availability rate (kca) values vary for different bee species:

Species	Honey Stomach Release Rate (ksr) d–1	Contact Availability Rate (kca) d–1
Apis mellifera	0.675	0.40
Bombus terrestris	1.0	0.40
Osmia bicornis	1.5	2.0

11. TKTD Parameters from Published Studies

TKTD parameters are derived from published studies to compare the sensitivities of different bee species. Studies by Heard et al. (2017) and Baas et al. (2022) provide a starting point for these comparisons.

11.1 Dimethoate Chronic Tests

Data from multiple sources, including Heard et al. (2017), Cornement et al. (2017), and IBACON, can be used to calibrate the BeeGUTS model for dimethoate.

11.2 Additional Data for B. terrestris

Chronic test data for additional compounds, such as 2,4-D, chlothianidin, propiconazole, and tau-fluvalinate, are available from Heard et al. (2017). Acute test data for deltamethrin, imidacloprid, methiocarb, and tetranilliprole are also available from Bayer Crop Sciences.

12. Other Species

Data from Heard et al. (2017) for O. bicornis can be supplemented with data from Uhl et al. (2019) and Reid et al. (2020). Acute oral and acute contact data for imidacloprid on Scaptotrigona postica (Soares et al., 2015) can also be used.

12.1 Imidacloprid Parameter Estimates for Scaptotrigona postica

The BeeGUTS model can be used to estimate parameters for Scaptotrigona postica, including the effect threshold and killing rate.

13. Bee Sensitivity Comparison: Direct Comparison Based on Effect Threshold

Available data allows for the comparison of four different bee species and seven different compounds. The data indicate that honey bees are consistently among the more sensitive species.

13.1 Relative Sensitivity

When the effect threshold of honey bees is set to a value of 1, other bee species exhibit varying degrees of sensitivity:

14. Weight-Corrected Comparison

Weight is a contributing factor to bee sensitivity. Correcting for weight provides a more accurate comparison of species sensitivity.

14.1 Weight-Based Effect Thresholds

The weight-corrected effect thresholds reveal that honey bees are among the most sensitive species when accounting for body weight:

Compound	Honey Bee	Bumble Bee	Osmia bicornis	Osmia cornuta
Dimethoate	0.14	0.43	0.41	0.41
Clothianidin	0.06	0.047	0.19
Deltamethrin	6.0	17
Imidacloprid	0.098	0.10	0.40
Methiocarb	0.70	0.21
Tau-fluvalinate	81	120	22
2,4-D	1000	>2850	5149

14.2 Relative Weight-Corrected Sensitivity

When the weight-corrected effect threshold of honey bees is set to 1, other bee species exhibit relative sensitivities:

15. Species Sensitivity Based on Effect Thresholds

Apis mellifera is often the most sensitive species, but there are exceptions. O. bicornis appears to be the most sensitive species for tau-fluvalinate, while B. terrestris is slightly more sensitive to methiocarb.

15.1 Sensitivity Ratios

The sensitivity ratio (R) ranges from 0.08 to 5.4, indicating that honey bee data, with an assessment factor of 6, are protective for other bee species. The current assessment factor of 10 is even more protective.

16. Honey Bee as a Predictor for Other Species

Chronic tests are more suitable for deriving TKTD parameter values than acute tests. Honey bee data can be used to estimate the sensitivity of other bee species:

Estimate TKTD parameters for honey bees.
Convert the effect threshold to an effect expressed/gram bee.
Calculate the threshold based on the weight of the bee of interest.

16.1 Predicted Effect Thresholds

Predicted effect thresholds for different bee species, based on honey bee data, are summarized in the following table:

Compound	Honey Bee	Bumble Bee	Osmia bicornis	Osmia cornuta	Scaptotrigona postica	Megachile rotundata
Beta-cyfluthrin	9.7	29	6.8	6.8	2.9	1.3
Bromoxynil	29	87	20	20	8.7	3.8
Dimethoate	0.014	0.042	0.0098	0.0098	0.0042	0.0018
Clothianidin	0.006	0.018	0.0042	0.0042	0.0018	0.0008
Deltamethrin	0.60	1.80	0.42	0.42	0.18	0.08
Fenamidone	0.32	0.96	0.22	0.22	0.096	0.042
Imidacloprid	0.0098	0.029	0.0069	0.0069	0.0029	0.0013
Metribuzin	5.1	15	3.6	3.6	1.5	0.66
Thiacloprid	0.82	2.5	0.57	0.57	0.25	0.11

17. Discussion: Factors Influencing Bee Sensitivity

Several factors can influence bee sensitivity to pesticides, including the use of lowest values for evaluation and the influence of toxicokinetic (TK) effects. Comparisons made in the literature often do not account for the fact that exposure patterns differ for different species.

17.1 Importance of TKTD Modeling

The BeeGUTS approach overcomes these issues and allows for the prediction of results from field-realistic exposures for various bee species.

18. Conclusions: Implications for Risk Assessment

The BeeGUTS TKTD model provides a new way to compare the sensitivities of bees to pesticides, accounting for bee physiology and test specifics. The model can estimate key parameters, such as honey stomach size and contact availability uptake rate, for different bee species.

18.1 Honey Bee Sensitivity

Honey bees are generally among the more sensitive species. An assessment factor of 6 on the honey bee threshold for effects is protective for other bee species, and this can be reduced to 4 when bee weight is considered.

19. COMPARE.EDU.VN: Your Partner in Informed Decision-Making

Navigating the complex landscape of environmental science and risk assessment can be challenging. At COMPARE.EDU.VN, we aim to simplify this process by offering detailed, objective comparisons that empower you to make informed decisions.

19.1. Overcoming the Challenges of Comparative Analysis

We understand the difficulties in comparing different options objectively and comprehensively. The abundance of information available can be overwhelming, making it hard to focus on the most critical factors. Our platform addresses these challenges by providing:

Comprehensive Comparisons: In-depth analyses of products, services, and ideas.
Clear Pros and Cons: Transparently listing the advantages and disadvantages of each option.
Detailed Feature Comparisons: Side-by-side comparisons of features, specifications, and pricing.
User and Expert Reviews: A wide range of perspectives to help you make a well-rounded decision.

19.2. Empowering Your Decision-Making Process

COMPARE.EDU.VN is dedicated to giving you the tools you need to make confident and well-informed decisions. Whether you’re a researcher, policymaker, or concerned citizen, we provide the clarity and insights necessary to navigate complex choices effectively.

19.3. Explore More Comparisons Today

Ready to discover detailed, unbiased comparisons? Visit compare.edu.vn today and explore a wide range of topics. Make your next decision with confidence, knowing you have the best information at your fingertips.

Address: 333 Comparison Plaza, Choice City, CA 90210, United States. Whatsapp: +1 (626) 555-9090. Website: COMPARE.EDU.VN

20. Frequently Asked Questions (FAQ)

Q1: What is the main goal of comparing bee sensitivity to pesticides?

A: The main goal is to determine whether honey bee data can be used as a proxy for other bee species in pesticide risk assessment, ensuring adequate protection for all bee populations.

Q2: Why are 48-hour LD50 values not always reliable for comparing bee sensitivity?

A: 48-hour LD50 values do not account for differences in kinetics, physiology, and inherent species sensitivity, leading to potentially biased comparisons.

Q3: What is the BeeGUTS model, and how does it improve bee sensitivity comparisons?

A: The BeeGUTS (Bee General Uniform Threshold Model for Survival) model is a toxicokinetic-toxicodynamic (TKTD) model that integrates acute oral, acute contact, and chronic test results within a consistent framework, providing a more robust measure of species sensitivity.

Q4: What are the key parameters estimated by the BeeGUTS model?

A: The key parameters include the effect threshold, which reflects the inherent sensitivity of bees to chemicals and is time- and test-independent.

Q5: How does the BeeGUTS model account for different exposure scenarios?

A: The model accounts for acute contact tests (pesticide applied to the thorax), acute oral tests (bees consume contaminated food), and chronic tests (bees fed contaminated food with constant concentration).

Q6: What are the two death mechanisms distinguished by the BeeGUTS model?

A: The model distinguishes between Stochastic Death (SD) and Individual Tolerance (IT) mechanisms, both of which use the effect threshold as a key parameter.

Q7: Why is calibration and validation important for the BeeGUTS model?

A: Calibration and validation ensure the model’s accuracy and reliability by estimating parameter values using experimental data and predicting effects using independent data sets.

Q8: What factors contribute to variations in bee sensitivity to pesticides?

A: Factors include differences in kinetics, physiological variations (size, honey stomach size), and exposure patterns.

Q9: Is the honey bee always the most sensitive species to pesticides?

A: While honey bees are generally among the more sensitive species, there are exceptions depending on the specific compound and bee species.

Q10: How can honey bee data be used to predict the sensitivity of other bee species?

A: By estimating TKTD parameters for honey bees, converting the effect threshold to an effect expressed/gram bee, and calculating the threshold based on the weight of the bee of interest.

21. References

Ansell, G. R., Frewin, A. J., Gradish, A. E., & Scott‐Dupree, C. D. (2021). Contact toxicity of three insecticides for use in Tier I pesticide risk assessments with Megachile rotundata (Hymenoptera: Megachilidae). PeerJ, 9, e10744.
Arena, M., & Sgolastra, F. (2014). A meta‐analysis comparing the sensitivity of bees to pesticides. Ecotoxicology, 23(3), 324–334.
Ashauer, R., & Escher, B. I. (2010). Advantages of toxicokinetic and toxicodynamic modelling in aquatic ecotoxicology and risk assessment. Journal of Environmental Monitoring, 12(11), 2056–2061.
Baas, J., Goussen, B., Miles, M., Preuss, T. G., & Roessink, I. (2022). BeeGUTS—A toxicokinetic–toxicodynamic model for the interpretation and integration of acute and chronic honey bee tests. Environmental Toxicology and Chemistry, 41(9), 2193–2201.
Baas, J., & Kooijman, S. A. (2015). Sensitivity of animals to chemical compounds links to metabolic rate. Ecotoxicology, 24(3), 657–663.
Cornement, M., Hodapp, B., Schmidt, T., Hoeger, S., & Kimmel, S. (2017). First experiences and first step stowards a chronic cbumble bee (Bombus terrestris) test design. [Conference presentation]. SETAC Europe 31st Annual Meeting, Brussels, Belgium.
Department for Environment, Food, and Agricultural Affairs. (2007). Assessment of the risk posed to honeybees by systemic pesticides. PS2322. UK.
Devillers, J., Decourtye, A., Budzinski, H., Pham‐Delègue, M. H., Cluzeau, S., & Maurin, G. (2003). Comparative toxicity and hazards of pesticides to Apis and non‐Apis bees. A chemometrical study. SAR and QSAR in Environmental Research, 14(5‐6), 389–403.
European Food Safety Authority. (2012). Scientific Opinion on the science behind the development of a risk assessment of Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal, 10(5), 2668.
Haas, J., Zaworra, M., Glaubitz, J., Hertlein, G., Kohler, M., Lagojda, A., & Nauen, R. (2021). A toxicogenomics approach reveals characteristics supporting the honey bee (Apis mellifera L.) safety profile of the butenolide insecticide flupyradifurone. Ecotoxicology and Environmental Safety, 217, 112247.
Hardstone, M. C., & Scott, J. G. (2010). Is Apis mellifera more sensitive to insecticides than other insects? Pest Management Science, 66(11), 1171–1180.
Heard, M. S., Baas, J., Dorne, J.‐L., Lahive, E., Robinson, A. G., Rortais, A., & Hesketh, H. (2017). Comparative toxicity of pesticides and environmental contaminants in bees: Are honey bees a useful proxy for wild bee species. Science of the Total Environment, 578, 357–365.
Hillier, N. K., Frost, E. H., & Shutler, D. (2013). Fate of dermally applied miticides fluvalinate and amitraz within honey bee (Hymenoptera: Apidae) bodies. Journal of Economic Entomology, 106(2), 558–565.
Jager, T., Albert, C., Preuss, T. G., & Ashauer, R. (2011). General unified threshold model of survival—A toxicokinetic‐toxicodynamic framework for ecotoxicology. Environmental Science & Technology, 45(7), 2529–2540.
Jager, T., Heugens, E. H. W., & Kooijman, S. A. L. M. (2006). Making sense of ecotoxicological test results: Towards application of process‐based models. Ecotoxicology, 15(3), 305–314.
Kemp, W. P., & Bosch, J. (2005). Effect of temperature on Osmia lignaria (Hymenoptera: Megachilidae) prepupa–adult development, survival, and emergence. Journal of Economic Entomology, 98(6), 1917–1923.
Ockleford, C., Adriaanse, P., Berny, P., Brock, T., Duquesne, S., Grilli, S., Hernandez‐Jerez, A. F., Bennekou, S. H., Klein, M., Kuhl, T., Laskowski, R., Machera, K., Pelkonen, O., Pieper, S., Smith, R. H., Stemmer, M., Sundh, I., Tiktak, A., Topping, C. J., … Teodorovic, I. (2018). Scientific Opinion on the state of the art of Toxicokinetic/Toxicodynamic (TKTD) effect models for regulatory risk assessment of pesticides for aquatic organisms. EFSA Journal, 16(8), e05377.
Organisation for Economic Co‐operation and Development. (1998a). Test No. 213: Honeybees, acute oral toxicity test. OECD guidelines for the testing of chemicals.
Organisation for Economic Co‐operation and Development. (1998b). Test No. 214: Honeybees, acute contact toxicity test. OECD guidelines for the testing of chemicals.
Organisation for Economic Co‐operation and Development. (2017a). Test No. 245: Honey bee (Apis mellifera L.), chronic oral toxicity test (10‐day feeding). OECD guidelines for the testing of chemicals.
Organisation for Economic Co‐operation and Development. (2017b). Test no. 246: Bumblebee, acute contact toxicity test. OECD guidelines for the testing of chemicals.
Pamminger, T. (2021). Extrapolating acute contact bee sensitivity to insecticides based on body weight using a phylogenetically informed interspecies scaling framework. Environmental Toxicology and Chemistry, 40(7), 2044–2052.
Pattrick, J. G., Symington, H. A., Federle, W., & Glover, B. J. (2020). The mechanics of nectar offloading in the bumblebee Bombus terrestris and implications for optimal concentrations during nectar foraging. Journal of the Royal Society Interface, 17(162), 20190632.
Reid, R. J., Troczka, B. J., Kor, L., Randall, E., Williamson, M. S., Field, L. M., & Davies, T. G. E. (2020). Assessing the acute toxicity of insecticides to the buff‐tailed bumblebee (Bombus terrestris audax. Pesticide Biochemistry and Physiology, 166, 104562.
Soares, H. M., Jacob, C. R. O., Carvalho, S. M., Nocelli, R. C. lF., & Malaspina, O. (2015). Toxicity of imidacloprid to the stingless bee Scaptotrigona postica Latreille, 1807 (Hymenoptera: Apidae). Bulletin of Environmental Contamination and Toxicology, 94(6), 675–680.
Stabler, D., Paoli, P. P., Nicolson, S. W., & Wright, G. A. (2015). Nutrient balancing of the adult worker bumblebee (Bombus terrestris) depends on the dietary source of essential amino acids. Journal of Experimental Biology, 218(5), 793–802.
Suchail, S., De Sousa, G., Rahmani, R., & Belzunces, L. P. (2004). In vivo distribution and metabolisation of 14C‐imidacloprid in different compartments of Apis mellifera L. Pest Management Science, 60(11), 1056–1062.
Thompson, H. (2016). Extrapolation of acute toxicity across bee species. Integrated Environmental Assessment and Management, 12(4), 622–626.
Thompson, H. M., & Pamminger, T. (2019). Are honeybees suitable surrogates for use in pesticide risk assessment for non‐Apis bees? Pest Management Science, 75(10), 2549–2557.
Torchio, P. F. (1973). Relative toxicity of insecticides to the Honey bee, Alkali Bee, and Alfalfa Leafcutting Bee (Hymenoptera: Apidae, Halictidae, Megachilidae). Journal of the Kansas Entomological Society, 46(4), 446–453.
Uhl, P., Awanbor, O., Schulz, R. S., & Brühl, C. A. (2019). Is Osmia bicornis an adequate regulatory surrogate? Comparing its acute contact sensitivity to Apis mellifera. PLoS One, 14(8), e0201081.
Uhl, P., Franke, L. A., Rehberg, C., Wollmann, C., Stahlschmidt, P., Jeker, L., & Brühl, C. A. (2016). Interspecific sensitivity of bees towards dimethoate and implications for environmental risk assessment. Scientific Reports, 6, 34439.
Valdovinos‐Núñez, G., Quezada‐Euan, J. J., Ancona‐Xiu, P., Moo‐Valle, H., Carmona, A., & Ruiz, E. (2009). Comparative toxicity of pesticides to stingless bees (Hymenoptera: Apidae: Meliponini). Journal of Economic Entomology, 102, 1737–1742.
Zaworra, M., Koehler, H., Schneider, J., Lagojda, A., & Nauen, R. (2019). Pharmacokinetics of three neonicotinoid insecticides upon contact exposure in the western honey bee, Apis mellifera. Chemical Research in Toxicology, 32(1), 35–37.