Aboveground herbivory elevates belowground rhizosphere volatile organic compound concentrations in ambient and polluted air, independent of volatile sampling methodology

Societal Impact Statement The effect of air pollution on plants is still underexplored, especially belowground. We used a field facility that released diesel exhaust and ozone at concentrations equivalent to those near a busy road in Reading, UK, to measure belowground gas exchange of Scots pine together with feeding by large pine weevils, a major pest of conifers. We found that blends and concentrations of belowground volatile organic compounds (VOCs) change significantly upon exposure to air pollution and aboveground insect herbivory. This impact of the rhizosphere in systemic plant‐stress responses is important, considering that VOCs can affect local pollution levels, weather and climate. Summary One of the major challenges regarding air pollution is that we do not have a clear understanding how it affects the functioning of natural systems, including the mechanisms underpinning inter‐ and intraspecific ecological interactions. Expanding our knowledge of these interactions in this area can serve as a basis upon which future nature protection policies could be built. Volatile organic compounds (VOCs) are synthesised by plants and have roles in inter‐ and intraspecific interactions and in protection against herbivores. They also have important roles in biosphere–atmosphere interactions. Rhizosphere VOCs play key roles in plant defence and soil ecology but are poorly understood due to difficulties in measurement. This study examined how aboveground herbivory by the large pine weevil ( Hylobius abietis ) influences belowground VOC concentrations in Scots pine ( Pinus sylvestris ) under ambient and polluted conditions. Experiments were conducted within a Free‐Air Diesel and Ozone Enrichment (FADOE) platform, using two field‐based VOC collection methods (a noninvasive soil collar and a VOC‐mole™ inserted into the soil). Herbivory significantly increased total belowground VOC concentrations after 38 h (by 165%), indicating a systemic plant response. In rings receiving the combined air pollution treatment, concentrations of benzenoid VOCs and oxygenated monoterpenes were also elevated (by 136% and 217%, respectively) relative to rings with ambient air. Both sampling methods produced comparable VOC profiles, supporting their interchangeable use according to experimental needs. These results suggest a role for rhizosphere VOCs in plant defence and provide robust field methods for studying plant‐stress interactions.