How are bees impacted by pesticide mixtures?

In recent decades, pollinating insects have experienced alarming declines with potential consequences for global food production (1). Crucial for crop pollination, bees are of particular concern as they have experienced regional losses in both wild and managed populations across Europe (2, 3, 4). Pesticide use has been identified as one of the major threats facing bees, but there is little understanding of the impacts of multiple compounds (1). Therefore the goal of my PhD project is to better understand how mixtures of pesticides affect the longevity and physiology of bees.

Why mixtures?

The effects of single pesticides and binary mixtures on bees have been extensively studied (5). However, the reality is much more complex – bees are exposed to mixtures of insecticides, herbicides, and fungicides in the environment with differing modes of action (6). These pesticides can have interactive effects. For example, certain fungicides are not highly toxic on their own, but they hinder the metabolism of insecticides, potentially through the suppression of cytochrome P450 detoxification enzymes (7, 8). Such synergistic effects underpin the importance of studying the effects of multiple pesticides.

Studying the toxicity of mixtures

My research is a part of the SPRINT project (Horizon 2020), which aims to evaluate the presence, risks, and impacts of plant protection products on the health of the environment. To achieve this, case study sites were established across Europe, where pesticide residues were measured in the soil, crops, water, and dust (9). Together with colleagues from this project, we have chosen mixtures of 5 pesticides representative of each site, based on their concentration and frequency in each field and potential threat to wildlife including honey bees (Apis mellifera) and bumble bees (Bombus terrestris).

To assess the toxic effects of these mixtures on bees, we will measure the median lethal dose – the dose at which a group of bees reaches 50% mortality. We can then identify any potential interactive effects by observing if the measured toxicity of a mixture deviates from the expected toxicity based on the single components. For instance, if the measured LD50 is much greater than expected, we can infer that certain pesticides in the mixture are working synergistically.

Sublethal effects

Bees are eusocial insects, so although low levels of pesticides may not kill them outright, they could have sublethal effects that make them less efficient, potentially leading to the loss of the colony. To better understand such effects, we will assess how sublethal doses of mixtures impact several important functions.

Like humans, bees host a community of specialized microbes in their gut important for the breakdown of plant-derived compounds, pathogen resistance, and detoxification (10). We plan to test how exposure to pesticide mixtures may perturb this community, which has been observed with exposure to single pesticides (11). Additionally, microbes characteristic of the bee gut can be isolated and cultured in the lab, providing the opportunity to evaluate the sensitivity of these isolates to both the mixtures and single component pesticides.

One of the most fascinating traits of honey bees is their division of labor within the colony. For instance, nurse bees are responsible for feeding larvae with royal jelly while foragers are indispensable for the food stores of the colony. However, pesticides may impact a bee’s ability to carry out its duties. Another goal of this research will be to investigate how mixtures affect important functions in the colony, including the structure and development of the hypopharyngeal gland of nurse bees, which is important for producing royal jelly to feed the bee larvae, and the flight ability of foragers which is essential for efficient foraging.

Overall, I’m looking forward to this project and working with honey bees and bumble bees. Hopefully in the next few years we will gain new insights on how bees respond to multiple stressors (and not get stung too much!)

References

1. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol [Internet]. 2010;25(6):345–53. Available from: http://dx.doi.org/10.1016/j.tree.2010.01.007

2. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science. 2006;313(5785):351–4.

3. Jaffé R, Dietemann V, Allsopp MH, Costa C, Crewe RM, Dall’Olio R, et al. Estimating the density of honeybee colonies across their naturalrange to fill the gap in pollinator decline censuses. Conserv Biol. 2010;24(2):583–93.

4. Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, Jones R, et al. Declines of managed honey bees and beekeepers in Europe. J Apic Res. 2010;49(1):15–22.

5. Benuszak J, Laurent M, Chauzat M-P. The exposure of honey bees (Apis mellifera; Hymenoptera: Apidae) to pesticides: Room for improvement in research. Sci Total Environ [Internet]. 2017;587–588:423–38. Available from: http://dx.doi.org/10.1016/j.scitotenv.2017.02.062

6. David A, Botías C, Abdul-Sada A, Nicholls E, Rotheray EL, Hill EM, et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ Int [Internet]. 2016;88:169–78. Available from: http://dx.doi.org/10.1016/j.envint.2015.12.011

7. Zhu YC, Yao J, Adamczyk J, Luttrell R. Synergistic toxicity and physiological impact of imidacloprid alone and binary mixtures with seven representative pesticides on honey bee (Apis mellifera). PLoS One. 2017;12(5):e0176837.

8. Sanchez-Bayo F, Goka K. Pesticide residues and bees - A risk assessment. PLoS One. 2014;9(4):e94482.

9. Silva V, Alaoui A, Schlünssen V, Vested A, Graumans M, van Dael M, et al. Collection of human and environmental data on pesticide use in Europe and Argentina: Field study protocol for the SPRINT project. PLoS One. 2021;16(11):e0259748.

10. Kwong WK, Moran NA. Gut microbial communities of social bees. Nat Rev Microbiol. 2016;14(6):374–84.

11. Daisley BA, Chmiel JA, Pitek AP, Thompson GJ, Reid G. Missing microbes in bees: How systematic depletion of key symbionts erodes immunity. Trends Microbiol [Internet]. 2020;28(12):1010–21. Available from: https://doi.org/10.1016/j.tim.2020.06.006