Effects of a heat wave event on the chemical ecology of species interactions in the potato agroecosystem

Abstract

Heat waves, brief periods of unusually high temperatures, are increasing in frequency and intensity globally. Such extreme weather events can alter plant chemistry, disrupting species interactions that contribute to pest suppression or increase their performance. Yet, most heat wave studies focus on pairwise interactions, leaving us with a poor understanding of how complex agroecosystems respond to temperature extremes. We addressed this knowledge gap by simulating an experimental heat wave in the field on potato plants (Solanum tuberosum L.) and the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), in the presence or absence of their mutualistic microbial symbionts and another pest, the potato aphid (Macrosiphum euphorbiae (Thomas)). We assessed beetle performance alongside changes in volatile organic compounds (VOCs) and glycoalkaloids from host plants. Beetle performance declined in the absence of their microbial symbionts and under aphid competition, but this effect was reversed under heat wave conditions. These results corresponded with a downregulation in glycoalkaloids, suggesting that potato prioritizes heat stress response over herbivore attack by divesting resources from the production of defensive compounds. The heat wave strongly affected VOCs composition, reducing emissions of multiple compounds while increasing others, but these changes were not directly linked with CPB performance. Overall, our results demonstrate that heat wave effects on crop–pest dynamics are dependent on the agroecological context and mediated by specialized metabolites. Importantly, under dual herbivore pressure, potato crops appear to prioritize coping with heat over defending against pests, underscoring the urgent need for pest management strategies that account for extreme climate events.