Environmental pollutants can exert sublethal deleterious effects on animals. These include disruption of cognitive functions underlying crucial behaviours. While agrochemicals have been identified as a major threat to pollinators, metal pollutants, which are often found in complex mixtures, have so far been overlooked. Here we assessed the impact of acute exposure to field-realistic concentrations of three common metal pollutants, lead, copper, arsenic, and their combinations, on honey bee appetitive learning and memory. All treatments involving single metals slowed down learning and disrupted memory retrieval at 24 h. Combinations of these metals had additive negative effects on both processes, suggesting common pathways of toxicity. Our results highlight the need to further assess the risks of metal pollution on invertebrates.

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Environmental pollutants can exert sublethal deleterious effects on animals. These include disruption of cognitive functions underlying crucial behaviours. While agrochemicals have been identified as a major threat to pollinators, other compounds, such as heavy metals that are often found in complex mixtures, have largely been overlooked. Here, we assessed the impact of acute exposure to field-realistic concentrations of lead, copper, arsenic, and their combinations, on honey bee learning and memory. All treatments involving single metals slowed down appetitive learning and disrupted memory retrieval at 24 h. Importantly, combinations of these metals induced additive negative effects on both processes, suggesting common pathways of toxicity. Our results highlight the need to further assess the risks of heavy metal pollution on invertebrates and to their associated ecosystem services.Summary statementHoney bees displayed reduced learning and memory performances following acute exposure to arsenic, copper or lead. Exposure to combinations of these metals induced additive effects.

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Laboratory studies show detrimental effects of metal pollutants on invertebrate behaviour and cognition, even at low levels. Here, we report a field study of Western honey bees sampled from an historic mining site heavily contaminated with metal and metalloid pollution, particularly arsenic. We analysed more than 1,000 bees from five apiaries within 11 km of the world’s largest gold mine in Southern France. Bees collected close to the mine exhibited decreased olfactory learning and memory performances and developed smaller heads. Three-dimensional scans of bee brains showed that the olfactory centres of bees sampled close to the mine were also smaller, indicating impairment of brain. Our study raises serious concerns about the health of honey bee populations in metal-polluted areas and illustrates how standard cognitive tests can be used for risk assessment.