Pollen foraging mediates exposure to dichotomous stressor syndromes in honey bee

Authors: WIZENBERG, SYDENY - York University; FRENCH, SARAH - York University; NEWBURN, LAURA - York University; PEPINELLI, MATEUS - York University; CONFLITTI, IDA - York University; MOUBONEY, MASHABA - York University; RITCHIE, CAROLINE - York University; JAMIESON, AIDAN - York University; ACHKANIAN, ANAHID - York University; TRAVAS, ANTHEA - York University; IMRIT, MOHAMMED - York University; KHUSI, DAVE - York University; CHIHATA, MATTHEW - York University; HIGO, HEATHER - University Of British Columbia; COMMON, JULIA - University Of British Columbia; Walsh, Elizabeth; BIXBY, MIRIAM - University Of British Columbia; GUARNA, MARTA - Agriculture And Agri-Food Canada; PERNAL, STEPHEN - Agriculture And Agri-Food Canada; HOOVER, SHELLEY - University Of Lethbridge; CURRIE, ROBERT - University Of Manitoba; GIOVENAZZO, P - Laval University; GUZMAN-NOVOA, ERNESTO - University Of Guelph; BORGES, DANIEL - Ontario Beekeepers Association; FOSTER, LEONARD - University Of British Columbia; ZAYED, ZAMRO - York University

Submitted to: Proceedings of the National Academy of Sciences-Nexus
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/7/2024
Publication Date: 10/18/2024
Citation: Wizenberg, S.M., French, S.K., Newburn, L.R., Pepinelli, M., Conflitti, I.M., Mouboney, M., Ritchie, C., Jamieson, A., Achkanian, A., Travas, A., Imrit, M., Khusi, D., Chihata, M., Higo, H., Common, J., Walsh, E.M., Bixby, M., Guarna, M.M., Pernal, S.F., Hoover, S.E., Currie, R., Giovenazzo, P., Guzman-Novoa, E., Borges, D., Foster, L.J., Zayed, Z. 2024. Pollen foraging mediates exposure to dichotomous stressor syndromes in honey bee. Proceedings of the National Academy of Sciences-Nexus. https://doi.org/10.1093/pnasnexus/pgae440.
DOI: https://doi.org/10.1093/pnasnexus/pgae440

Interpretive Summary: Insect-mediated pollination is an important ecological process that is crucial to the successful cultivation of many crops. As native insect populations have declined, managed honey bee colonies have become a key player in food production systems, but their role has been threatened by on-going health issues that contribute to colony decline. Crop pollination is likely a route of exposure to these stressors nested within agroecosystems, and understanding the foraging behaviour of managed honey bee colonies in this context could provide pivotal information to improve management efforts. Here, we studied how honey bee colonies across Canada become exposed to stressors and characterized their foraging behaviour in relation to major Canadian crops. We found that honey bees have distinct, measurable foraging preferences and that the breadth of plant interactions is a strong predictor of the abundance and diversity of stressors any given colony is exposed to.

Technical Abstract: Recent declines in the health of honey bee colonies used for crop pollination pose a considerable threat to global food security. Foraging by honey bee workers represents the primary route of exposure to a plethora of toxins and pathogens known to affect bee health, but it remains unclear how foraging preferences impact colony-level stressor exposure. Resolving this knowledge gap is crucial for enhancing the health of honey bees and the agricultural systems that rely on them for pollination. To address this, we carried out a continental-scale experiment encompassing 456 Canadian honey bee colonies to first characterize pollen foraging preferences in relation to major crops, then explore how foraging behaviour influences patterns of stressor exposure. We used a metagenomic approach to quantify honey bee dietary breadth and found that bees display distinct foraging preferences that vary substantially relative to crop type and proximity, and the breadth of foraging interactions can be used to predict the abundance and diversity of stressors a colony is exposed to. High dietary diversity was associated with increased exposure to pathogens, while low dietary diversity was associated with increased exposure to agrochemicals, bolstered by landscape-level effects. Our work provides the first large-scale empirical evidence that pollen foraging behaviour plays an influential role in determining exposure to dichotomous stressor syndromes in honey bees.