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Sublethal doses of glyphosate impair olfactory memory retention, but not learning in the honey bee (Apis mellifera scutellata)

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Abstract

Learning and memory are important biological processes that allow for optimized honey bee behavior. Factors negatively affecting bee cognition are important contributors to declines in pollination and food security. Agrochemical use, including herbicides, is one of the primary stressors linked to bee decline. Predicted agricultural expansion and associated increased use of glyphosate combined with scarcity of honey bees further highlights the need to understand the relationship between glyphosate and honey bee cognition and health. Here we investigated the effect of field-realistic doses of glyphosate on honey bee olfactory learning and memory. We used the conditioning of the Proboscis Extension Reflex (PER) to evaluate olfactory absolute conditioning. We found no differences in olfactory PER performance between glyphosate-exposed and control bees. We also did not find differences in olfactory memory retrieval at 15 min or 24 h after conditioning between exposed and non-exposed bees. However, we found that sublethal doses of glyphosate impaired memory retention; bees exposed to sublethal doses of glyphosate showed a decay trajectory of learned information, while in non-exposed bees the trajectory had a positive increment with time. This trend in memory retention was significantly different between bees exposed to 1500 ng and controls. Implications for insect conservation: Field-realistic doses of glyphosate had negative effect on memory dynamics in the honey bee. These results suggest glyphosate affects time-dependent neural mechanisms underlying information processing. This negative effect contributes to declines in pollination function and food security. We highlight the need to critically evaluate the cost-benefit analysis of indiscriminate glyphosate use.

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Acknowledgements

To the Instituto de Ciencias Naturales, Universidad Nacional de Colombia for supporting the development of the Cognitive Ecology Laboratory, and Colciencias for funding this research. To Rodulfo Ospina for support with the use of the LABUN’s Apiary. To the anonym reviewers whose observations and generous suggestions greatly help to improve the quality of the manuscript.

Funding

Universidad Nacional de Colombia, Colciencias granted to JH a Young Researcher Funding (Code number: M301PR03F17), Hermes code: 38989. Grant IV-FGD003 (DIeI, Universidad del Rosario to AJR).

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Correspondence to Marisol Amaya-Márquez.

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Hernández, J., Riveros, A.J. & Amaya-Márquez, M. Sublethal doses of glyphosate impair olfactory memory retention, but not learning in the honey bee (Apis mellifera scutellata). J Insect Conserv 25, 683–694 (2021). https://doi.org/10.1007/s10841-021-00335-6

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  • DOI: https://doi.org/10.1007/s10841-021-00335-6

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