Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Ingestible hydrogel microparticles improve bee health after pesticide exposure

Nature Sustainability volume 7, pages 1441–1451 (2024)Cite this article

Subjects

Abstract

Bees provide crucial pollination services for crop cultivation, contributing billions of dollars to the global agricultural economy. However, exposure to pesticides such as neonicotinoids represents a major problem for bee health, necessitating strategies that can improve agricultural sustainability and pollinator health. Here we report a simple and scalable solution, through ingestible hydrogel microparticles (IHMs), which can capture neonicotinoids in vitro and in the bee gastrointestinal tract to mitigate the harmful effects of pesticides. Using the common eastern bumblebee (Bombus impatiens) as a model species and the neonicotinoid imidacloprid, we demonstrated by means of lethal and sublethal assays the substantial benefits of IHM treatments. Under lethal exposure of imidacloprid, bumblebees that received IHM treatment exhibited a 30% increase in survival relative to groups without IHM treatment. After a sublethal exposure of 5 ng, IHM treatment resulted in improved feeding motivation and a 44% increase in the number of bees that engaged in locomotor activity. Wingbeat frequency was significantly lower after a single 5 or 10 ng imidacloprid dose; however, IHM treatment improved wingbeat frequency. Overall, the IHMs improved bumblebee health, and with further optimization have the potential to benefit apiculture and reduce risk during crop pollination by managed bees.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Schematic of pesticide detoxification strategy using IHMs and IHM characterization.
Fig. 2: Survival assays and pollen consumption.
Fig. 3: In vivo IHM tracking.
Fig. 4: Syrup consumption and locomotor activity.
Fig. 5: Wingbeat frequency.

Similar content being viewed by others

Data availability

Wingbeat frequency videos were captured using a high-speed camera, which resulted in the raw data files being exceedingly large; therefore, they are available from the corresponding author upon reasonable request. Videos acquired during locomotion studies can be found at https://github.com/julia-caserto/Bee-Locomotion-Analysis. Source data are provided with this paper.

Code availability

Code used to analyze locomotion videos can be found at https://github.com/julia-caserto/Bee-Locomotion-Analysis.

References

  1. Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. Biol. Sci. 274, 303–313 (2007).

    Google Scholar 

  2. Porto, R. G. et al. Pollination ecosystem services: a comprehensive review of economic values, research funding and policy actions. Food Secur. 12, 1425–1442 (2020).

    Google Scholar 

  3. Bruckner, S. et al. A national survey of managed honey bee colony losses in the USA: results from the Bee Informed Partnership for 2017–18, 2018–19 and 2019–20. J. Apic. Res. 62, 429–443 (2023).

    Google Scholar 

  4. Bartomeus, I. et al. Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc. Natl Acad. Sci. USA 110, 4656–4660 (2013).

    CAS  Google Scholar 

  5. LeCroy, K. A., Savoy-Burke, G., Carr, D. E., Delaney, D. A. & Roulston, T. H. Decline of six native mason bee species following the arrival of an exotic congener. Sci. Rep. 10, 18745 (2020).

    CAS  Google Scholar 

  6. Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides and lack of flowers. Science 347, 1255957 (2015).

    Google Scholar 

  7. Graham, K. K. et al. Identities, concentrations and sources of pesticide exposure in pollen collected by managed bees during blueberry pollination. Sci. Rep. 11, 16857 (2021).

    CAS  Google Scholar 

  8. Graham, K. K. et al. Pesticide risk to managed bees during blueberry pollination is primarily driven by off-farm exposures. Sci. Rep. 12, 7189 (2022).

    CAS  Google Scholar 

  9. McArt, S. H., Fersch, A. A., Milano, N. J., Truitt, L. L. & Böröczky, K. High pesticide risk to honey bees despite low focal crop pollen collection during pollination of a mass blooming crop. Sci. Rep. 7, 46554 (2017).

    CAS  Google Scholar 

  10. Krupke, C. H., Hunt, G. J., Eitzer, B. D.,Andino, G. & Given, K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7, e29268 (2012).

    CAS  Google Scholar 

  11. Pettis, J. S. et al. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8, e70182 (2013).

    CAS  Google Scholar 

  12. Stanley, D. A. et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548–550 (2015).

    CAS  Google Scholar 

  13. Whitehorn, P. R., O’Connor, S., Wackers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012).

    CAS  Google Scholar 

  14. Deguine, J.-P. et al. Integrated pest management: good intentions, hard realities. A review. Agron. Sustain. Dev. 41, 38 (2021).

    Google Scholar 

  15. Chen, J. et al. Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators. Nat. Food 2, 339–347 (2021).

    CAS  Google Scholar 

  16. Camp, A. A. & Lehmann, D. M. Impacts of neonicotinoids on the bumble bees Bombus terrestris and Bombus impatiens examined through the lens of an adverse outcome pathway framework. Environ. Toxicol. Chem. 40, 309–322 (2021).

    CAS  Google Scholar 

  17. Liu, G. Y., Ju, X. L. & Cheng, J. Selectivity of Imidacloprid for fruit fly versus rat nicotinic acetylcholine receptors by molecular modeling. J. Mol. Model. 16, 993–1002 (2010).

    CAS  Google Scholar 

  18. Grünewald, B. & Siefert, P. Acetylcholine and its receptors in honeybees: involvement in development and impairments by neonicotinoids. Insects 10, 420 (2019).

  19. Alkassab, A. T. & Kirchner, W. H. Sublethal exposure to neonicotinoids and related side effects on insect pollinators: honeybees, bumblebees and solitary bees. J. Plant Dis. Prot. 124, 1–30 (2017).

    Google Scholar 

  20. Gregorc, A. et al. Effects of coumaphos and imidacloprid on honey bee (Hymenoptera: Apidae) lifespan and antioxidant gene regulations in laboratory experiments. Sci. Rep. 8, 15003 (2018).

    Google Scholar 

  21. Wu, Y.-Y. et al. Sublethal effects of imidacloprid on targeting muscle and ribosomal protein related genes in the honey bee Apis mellifera L. Sci. Rep. 7, 15943 (2017).

    Google Scholar 

  22. Yao, J., Zhu, Y. C. & Adamczyk, J. Responses of honey bees to lethal and sublethal doses of formulated clothianidin alone and mixtures. J. Econ. Entomol. 111, 1517–1525 (2018).

    CAS  Google Scholar 

  23. Tasman, K., Hidalgo, S., Zhu, B., Rands, S. A. & Hodge, J. J. L. Neonicotinoids disrupt memory, circadian behaviour and sleep. Sci. Rep. 11, 2061 (2021).

    CAS  Google Scholar 

  24. He, B. et al. Imidacloprid activates ROS and causes mortality in honey bees (Apis mellifera) by inducing iron overload. Ecotoxicol. Environ. Saf. 3, 112709 (2021).

    Google Scholar 

  25. Xu, X. et al. Neonicotinoids: mechanisms of systemic toxicity based on oxidative stress-mitochondrial damage. Arch. Toxicol. 96, 1493–1520 (2022).

    CAS  Google Scholar 

  26. Imidacloprid: Proposed Interim Registration Review Decision. Case Number 7605 (EPA, 2020); www.epa.gov/sites/default/files/2020-01/documents/imidacloprid_pid_signed_1.22.2020.pdf

  27. Klingelhöfer, D., Braun, M., Brüggmann, D. & Groneberg, D. A. Neonicotinoids: a critical assessment of the global research landscape of the most extensively used insecticide. Environ. Res. 213, 113727 (2022).

    Google Scholar 

  28. Hirata, K., Jouraku, A., Kuwazaki, S., Kanazawa, J. & Iwasa, T. The R81T mutation in the nicotinic acetylcholine receptor of Aphis gossypii is associated with neonicotinoid insecticide resistance with differential effects for cyano- and nitro-substituted neonicotinoids. Pestic. Biochem. Physiol. 143, 57–65 (2017).

    CAS  Google Scholar 

  29. Sahoo, T. R. & Prelot, B. in Nanomaterials for the Detection and Removal of Wastewater Pollutants (eds Bonelli, B. et al.) 161–222 (Elsevier, 2020).

  30. Azpiazu, C. et al. Chronic oral exposure to field-realistic pesticide combinations via pollen and nectar: effects on feeding and thermal performance in a solitary bee. Sci. Rep. 9, 13770 (2019).

    Google Scholar 

  31. Muth, F., Gaxiola, R. L. & Leonard, A. S. No evidence for neonicotinoid preferences in the bumblebee Bombus impatiens. R. Soc. Open Sci. 7, 191883 (2020).

    CAS  Google Scholar 

  32. Parmezan, A. R. S., Souza, V. M. A., Žliobaitė, I. & Batista, G. E. A. P. A. Changes in the wing-beat frequency of bees and wasps depending on environmental conditions: a study with optical sensors. Apidologie 52, 731–748 (2021).

    Google Scholar 

  33. Santoyo, J., Azarcoya, W., Valencia, M., Torres, A. & Salas, J. J. P. A. Frequency analysis of a bumblebee (Bombus impatiens) wingbeat. Pattern Anal. Applic. 19, 487–493 (2016).

    Google Scholar 

  34. Panziera, D., Requier, F., Chantawannakul, P., Pirk, C. W. W. & Blacquière, T. The diversity decline in wild and managed honey bee populations urges for an integrated conservation approach. Front. Ecol. Evol. 10, 767950 (2022).

  35. Ward, L. T. et al. Pesticide exposure of wild bees and honey bees foraging from field border flowers in intensively managed agriculture areas. Sci. Total Environ. 831, 154697 (2022).

    CAS  Google Scholar 

  36. Peng, Y.-S. & Marston, J. M. Filtering mechanism of the honey bee proventriculus. Physiol. Entomol. 11, 433–439 (1986).

    Google Scholar 

  37. Sambe, H., Hoshina, K., Moaddel, R., Wainer, I. W. & Haginaka, J. Uniformly-sized, molecularly imprinted polymers for nicotine by precipitation polymerization. J. Chromatogr. A 1134, 88–94 (2006).

    CAS  Google Scholar 

  38. Chen, J. et al. Dummy template surface molecularly imprinted polymers based on silica gel for removing imidacloprid and acetamiprid in tea polyphenols. J. Sep. Sci. 43, 2467–2476 (2020).

    CAS  Google Scholar 

  39. Kumar, N., Narayanan, N. & Gupta, S. Application of magnetic molecularly imprinted polymers for extraction of imidacloprid from eggplant and honey. Food Chem. 255, 81–88 (2018).

    CAS  Google Scholar 

  40. Wang, X., Mu, Z., Liu, R., Pu, Y. & Yin, L. Molecular imprinted photonic crystal hydrogels for the rapid and label-free detection of imidacloprid. Food Chem. 141, 3947–3953 (2013).

    CAS  Google Scholar 

  41. Russell, A. L., Morrison, S. J., Moschonas, E. H. & Papaj, D. R. Patterns of pollen and nectar foraging specialization by bumblebees over multiple timescales using RFID. Sci. Rep. 7, 42448 (2017).

    Google Scholar 

  42. Marletto, F., Patetta, A. & Manino, A. Laboratory assessment of pesticide toxicity to bumblebees. Bull. Insectol. 56, 159–164 (2003).

  43. Chen, Y. R., Tzeng, D. T. W. & Yang, E. C. Chronic effects of imidacloprid on honey bee worker development—molecular pathway perspectives. Int. J. Mol. Sci. 22, 11835 (2021).

    CAS  Google Scholar 

  44. Démares, F. J. et al. Honey bee (Apis mellifera) exposure to pesticide residues in nectar and pollen in urban and suburban environments from four regions of the United States. Environ. Toxicol. Chem. 41, 991–1003 (2022).

    Google Scholar 

  45. Kim, S. et al. Chronic exposure to field-realistic doses of imidacloprid resulted in biphasic negative effects on honey bee physiology. Insect Biochem. Mol. Biol. 144, 103759 (2022).

    CAS  Google Scholar 

  46. Sampson, B. et al. Sensitivity to imidacloprid insecticide varies among some social and solitary bee species of agricultural value. PLoS ONE 18, e0285167 (2023).

    CAS  Google Scholar 

  47. Gradish, A. E. et al. Comparison of pesticide exposure in honey bees (Hymenoptera: Apidae) and bumble bees (Hymenoptera: Apidae): implications for risk assessments. Environ. Entomol. 48, 12–21 (2018).

    Google Scholar 

  48. Paus-Knudsen, J. S., Sveinsson, H. A., Grung, M., Borgå, K. & Nielsen, A. The neonicotinoid imidacloprid impairs learning, locomotor activity levels and sucrose solution consumption in bumblebees (Bombus terrestris). Environ. Toxicol. Chem. 42, 1337–1345 (2023).

    CAS  Google Scholar 

  49. Lambin, M., Armengaud, C., Raymond, S. & Gauthier, M. Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch. Insect Biochem. Physiol. 48, 129–134 (2001).

    CAS  Google Scholar 

  50. Lin, Y. C., Lu, Y. H., Tang, C. K., Yang, E. C. & Wu, Y. L. Honey bee foraging ability suppressed by imidacloprid can be ameliorated by adding adenosine. Environ. Pollut. 332, 121920 (2023).

    CAS  Google Scholar 

  51. Switzer, C. M. & Combes, S. A. The neonicotinoid pesticide, imidacloprid, affects Bombus impatiens (bumblebee) sonication behavior when consumed at doses below the LD50. Ecotoxicology 25, 1150–1159 (2016).

    CAS  Google Scholar 

  52. Combes, S. A., Gagliardi, S. F., Switzer, C. M. & Dillon, M. E. Kinematic flexibility allows bumblebees to increase energetic efficiency when carrying heavy loads. Sci. Adv. 6, eaay3115 (2020).

    CAS  Google Scholar 

  53. David, A. et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ. Int. 88, 169–178 (2016).

    CAS  Google Scholar 

  54. Schuhmann, A. & Scheiner, R. A combination of the frequent fungicides boscalid and dimoxystrobin with the neonicotinoid acetamiprid in field-realistic concentrations does not affect sucrose responsiveness and learning behavior of honeybees. Ecotoxicol. Environ. Saf. 256, 114850 (2023).

    CAS  Google Scholar 

  55. Kenna, D. et al. Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees. Ecol. Evol. 9, 5637–5650 (2019).

    Google Scholar 

  56. El Khoury, S., Giovenazzo, P. & Derome, N. Endogenous honeybee gut microbiota metabolize the pesticide clothianidin. Microorganisms 10, 493 (2022).

    CAS  Google Scholar 

  57. Zhou, T., Jørgensen, L., Mattebjerg, M. A., Chronakis, I. S. & Ye, L. Molecularly imprinted polymer beads for nicotine recognition prepared by RAFT precipitation polymerization: a step forward towards multi-functionalities. RSC Adv. 4, 30292–30299 (2014).

    CAS  Google Scholar 

  58. Rademacher, E., Harz, M. & Schneider, S. Effects of oxalic acid on Apis mellifera (Hymenoptera: Apidae). Insects 8, 84 (2017).

    Google Scholar 

  59. Lagergren, S. About the theory of so-called adsorption of sobule substances. Kungl. Svenska Vetenskapsakad. Handl. 24, 1–39 (1898).

    Google Scholar 

  60. Ho, Y. S. & McKay, G. A comparison of chemisorption kinetic models applied to pollutant removal on various sorbents. Process Saf. Environ. Prot. 76, 332–340 (1998).

    CAS  Google Scholar 

  61. Wang, M., Yang, C., Cao, J., Yan, H. & Qiao, F. Dual-template hydrophilic imprinted resin as an adsorbent for highly selective simultaneous extraction and determination of multiple trace plant growth regulators in red wine samples. Food Chem. 411, 135471 (2023).

    CAS  Google Scholar 

  62. Blanchard, G., Maunaye, M. & Martin, G. Removal of heavy metals from waters by means of natural zeolites. Water Res. 18, 1501–1507 (1984).

    CAS  Google Scholar 

  63. Skorupski, P. & Chittka, L. Photoreceptor spectral sensitivity in the bumblebee, Bombus impatiens (Hymenoptera: Apidae). PLoS ONE 5, e12049 (2010).

    Google Scholar 

  64. Kántor, I. et al. Biocatalytic synthesis of poly[ε-caprolactone-co-(12-hydroxystearate)] copolymer for sorafenib nanoformulation useful in drug delivery. Catal. Today 366, 195–201 (2021).

  65. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    CAS  Google Scholar 

  66. Therneau, T. M. coxme: Mixed effects Cox models. R package version 2.2-18.1 (2022).

  67. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2023).

  68. Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

Download references

Acknowledgements

Cornell University Department of Human Ecology for the use of HPLC. Fluorescence microscopy was carried out at the Cornell Institute of Biotechnology’s BRC Imaging Facility. We acknowledge the use of field emission scanning electron microscopy supported by NSF through the Cornell University Materials Research Science and Engineering Center DMR-1719875. This work was supported by the New York State Environmental Protection Fund. We acknowledge the following USDA NIFA grants: 2021-22-127 (M.M.) and 2021-08373 (M.K.S.). We thank A. Rios Tascon for helping design locomotion chambers and providing code to analyze locomotion videos. Schematics in Fig. 1a and 4a were created with BioRender.com.

Author information

Authors and Affiliations

  1. Robert Frederick Smith School of Chemical and Biomolecular Engineering, Cornell University, Ithaca, NY, USA

    Julia S. Caserto

  2. Department of Biological and Environmental Engineering, Cornell University, Ithaca, NY, USA

    Lyndsey Wright, Mary K. Salcedo, Stephanie Fuchs, Sunghwan Jung & Minglin Ma

  3. Department of Entomology, Cornell University, Ithaca, NY, USA

    Corey Reese & Scott H. McArt

  4. Department of Biological Sciences, Cornell University, Ithaca, NY, USA

    Matthew Huang

Authors
  1. Julia S. Caserto
    View author publications

    Search author on:PubMed Google Scholar

  2. Lyndsey Wright
    View author publications

    Search author on:PubMed Google Scholar

  3. Corey Reese
    View author publications

    Search author on:PubMed Google Scholar

  4. Matthew Huang
    View author publications

    Search author on:PubMed Google Scholar

  5. Mary K. Salcedo
    View author publications

    Search author on:PubMed Google Scholar

  6. Stephanie Fuchs
    View author publications

    Search author on:PubMed Google Scholar

  7. Sunghwan Jung
    View author publications

    Search author on:PubMed Google Scholar

  8. Scott H. McArt
    View author publications

    Search author on:PubMed Google Scholar

  9. Minglin Ma
    View author publications

    Search author on:PubMed Google Scholar

Contributions

J.S.C. and M.M. conceived the study. J.S.C., M.M. and S.H.M. designed experiments. J.S.C. conducted and supervised all experiments and data collection. L.W. prepared materials, performed colony maintenance and assisted with bee transfers and experiments. S.F. assisted with bee transfers and experiments. C.R., M.H., S.J. and M.K.S. collected WBF data and calculated WBF. J.S.C. analyzed all data collected. J.S.C., S.H.M. and M.M. reviewed and interpreted the results. J.S.C. wrote the paper; M.M. provided substantial edits. All authors reviewed and commented on the paper.

Corresponding author

Correspondence to Minglin Ma.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Sustainability thanks Rachel Parkinson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–8.

Reporting Summary

Supplementary Data

Source data for Supplementary Figs. 3, 4 and 7.

Source data

Source Data

Statistical source data for Figs 1c,d, 2a–d, 4b,d and 5b,c.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Caserto, J.S., Wright, L., Reese, C. et al. Ingestible hydrogel microparticles improve bee health after pesticide exposure. Nat Sustain 7, 1441–1451 (2024). https://doi.org/10.1038/s41893-024-01432-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41893-024-01432-5

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene