Toxic temperatures: Bee behaviours exhibit divergent pesticide toxicity relationships with warming

• Published in: Global change biology Vol. 29; no. 11; pp. 2981 - 2998
• Main Authors: Kenna, Daniel, Graystock, Peter, Gill, Richard J.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.06.2023
• Subjects: Animals; Bees; Behavior, Animal - physiology; Biodiversity; bumblebee; Bumblebees; Climate change; colony; Flight; Flight characteristics; Food consumption; foraging; High temperature; Imidacloprid; Insecticides; Insecticides - pharmacology; Insects; neonicotinoid; Neonicotinoids - pharmacology; Pesticide application; Pesticide toxicity; Pesticides; Plant reproduction; Pollination; pollinator; Pollinators; responsiveness; Sublethal effects; sulfoximine; Synergistic effect; Temperature; Toxicity; walking; sulfoximine; flight; neonicotinoid; colony; pollination; walking; foraging; pollinator; bumblebee; climate change; responsiveness
• ISSN: 1354-1013; 1365-2486
• DOI: 10.1111/gcb.16671

Climate change and agricultural intensification are exposing insect pollinators to temperature extremes and increasing pesticide usage. Yet, we lack good quantification of how temperature modulates the sublethal effects of pesticides on behaviours vital for fitness and pollination performance. Consequently, we are uncertain if warming decreases or increases the severity of different pesticide impacts, and whether separate behaviours vary in the direction of response. Quantifying these interactive effects is vital in forecasting pesticide risk across climate regions and informing pesticide application strategies and pollinator conservation. This multi‐stressor study investigated the responses of six functional behaviours of bumblebees when exposed to either a neonicotinoid (imidacloprid) or a sulfoximine (sulfoxaflor) across a standardised low, mid, and high temperature. We found the neonicotinoid had a significant effect on five of the six behaviours, with a greater effect at the lower temperature(s) when measuring responsiveness, the likelihood of movement, walking rate, and food consumption rate. In contrast, the neonicotinoid had a greater impact on flight distance at the higher temperature. Our findings show that different organismal functions can exhibit divergent thermal responses, with some pesticide‐affected behaviours showing greater impact as temperatures dropped, and others as temperatures rose. We must therefore account for environmental context when determining pesticide risk. Moreover, we found evidence of synergistic effects, with just a 3°C increase causing a sudden drop in flight performance, despite seeing no effect of pesticide at the two lower temperatures. Our findings highlight the importance of multi‐stressor studies to quantify threats to insects, which will help to improve dynamic evaluations of population tipping points and spatiotemporal risks to biodiversity across different climate regions. Understanding how temperature modulates the toxicity of pesticides on the behaviour of organisms is vital in developing a predictive framework to quantify the risk of pesticides under climatic variation. Focusing on an insect pollinator model system—bumblebees—this study showed that the impact of a neonicotinoid insecticide on a non‐target beneficial organism alters significantly under temperature change. The direction of this effect, however, was not uniform across the six behavioural endpoints assayed. For behaviours important for bee nest duties, toxicity decreased with warming. For flight performance important for bee foraging and pollination services, toxicity increased with warming.