Sub-lethal pesticide exposure interferes with honey bee memory of learnt colours

Authors: RÜKÜN, TUGÇE - Sabanci University; ERCAN, NESLIM - Sabanci University; CANKO, EE - Sabanci University; AVSAR, BIHTER - Sabanci University; DYER, ADRIAN - Royal Melbourne Institute Of Technology University; GARCIA, JAIR - Royal Melbourne Institute Of Technology University; ÇAKMAK, IBRAHIM - Uludag University; Mayack, Christopher

Submitted to: Science of the Total Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/8/2025
Publication Date: 1/11/2025
Citation: Rükün, T., Ercan, N., Canko, E., Avsar, B., Dyer, A.G., Garcia, J.E., Çakmak, I., Mayack, C.L. 2025. Sub-lethal pesticide exposure interferes with honey bee memory of learnt colours. Science of the Total Environment. 962. Article 178460. https://doi.org/10.1016/j.scitotenv.2025.178460.
DOI: https://doi.org/10.1016/j.scitotenv.2025.178460

Interpretive Summary: Pesticide exposure is one of many factors that are known to underlie the most recent decline in honey bee health. Despite this knowledge, for one class of pesticides, known as neonicotinoids, their use is globally still on the rise. Previous research has shown that exposure to these pesticides can lead to adverse effects on honey bee odor learning and memory, which is important for honey bee foragers to learn and remember where valuable food resources are located. Flower colour is another critical property that the foraging bee relies on to make an association between a flower and the food quality that it has to offer. We were therefore interested in what effects neonictinoid pesticides had on foraging honey bees color vision learning and memory, in a semi-natural setting. We exposed four different sub-lethal concentrations of a neonictinoid pesticide, called imidacloprid, to foraging honey bees, after they had been trained to associate a yellow flower with a food reward. We then gave a choice amongst artificial flowers with white, red, blue, green, violet, and yellow colours, to see if the foraging honey bee still retained its preference for the yellow flower. We found that for pesticide exposure higher than the lowest concentration, foraging honey bees no longer preferred the yellow flowers within the flower patch and instead were visiting flowers at random, with a complete loss of preference for the yellow flower colour. In the laboratory, we found that higher pesticide exposures also resulted in a significant decrease in gene expression of genes known to play a role in forming color vision memory, revealing that memory loss and not alteration in colour vision perception, is the most plausible explanation for the random bee foraging preferences after pesticide exposure. Across important bee pollinators, how colour vision functions is very similar and is essential for food collection and survival. Our results therefore suggest that to maintain efficient pollination services from bees it would be ideal to have environments free from neonicotinoid pesticides.

Technical Abstract: Neonicotinoid pesticide use has increased around the world despite accumulating evidence of their potential detrimental sub-lethal effects on the behaviour and physiology of bees, and its contribution to the global decline in bee health. Whilst flower colour is considered as one of the most important signals for foraging honey bees (Apis mellifera), the effects of pesticides on colour vision and memory retention in a natural setting remain unknown. We trained free flying honey bee foragers by presenting yellow flower stimuli, to an unscented artificial flower patch with 6 different flower colours to investigate if sub-lethal levels of imidacloprid would disrupt the acquired association made between flower colour and food reward. We found that for concentrations higher than 4% of LD50 value, foraging honey bees no longer preferentially visited the yellow flowers within the flower patch and instead reverted back to baseline foraging preferences, with a complete loss of preference for the yellow flower colour. Higher pesticide dosages also resulted in a significant decrease in CaMKII and CREB gene expression, revealing that memory loss and not alteration in colour vision perception, is the most plausible mechanism to explain the disruption of bee foraging preference. Across important bee pollinators, colour vision is highly conserved and essential for efficient nutrition collection and survival. We thus show that to maintain efficient pollination services bees require environments free from neonicotinoid pesticides.