Microplastics alter behavioural responses of an insect herbivore to a plant-soil system

Pollution by microplastics in natural and cultivated soils is an emerging issue of global interest. Microplastics may interfere with the soil structure, microorganism and invertebrate biodiversity, and related biological processes. Surprisingly, there is a poor understanding of how microplastics influence the interactions between members of different trophic levels. We investigated whether a high level of contamination (5% w/w concentration) with high-density polyethylene (HDPE) microplastics (<0.25 mm size) in soil interferes with the attraction of an insect herbivore towards a plant-soil system under short-term laboratory conditions. As a model system, we used the black fungus gnat Bradysia difformis (Diptera: Sciaridae), which is an important crop pest, and lentil (Lens culinaris), a host plant. Through one-way olfactometer bioassays, we recorded the female responses to plant-soil systems subjected to different combinations of HDPE exposures and watering regimes. Female residence time (i.e., the time spent in the olfactometer sector close to the stimulus) was higher when testing high-watered (75.3% ± 2.99) than low-watered, microplastic-free plant-soil systems (58.6% ± 3.88). However, residence time was lower towards systems maintained 7 days with 5% HDPE (53.9% ± 4.79) compared to HDPE-free (76.5% ± 2.64) systems. Notably, the attraction of females towards HDPE-free systems compared to 5% HDPE was higher only under high watering regime. Attractiveness of 5% HDPE plant-soil system was restored when cues from fungal colonies were added (66.1% ± 4.33). Here we demonstrated for the first time that microplastics alter the attraction of female fungus gnats towards a plant-soil system. Our results depict an extreme scenario with high HDPE (5%), which is occasionally found in soils close to industrial areas. Therefore it is still too early to derive strong conclusions for typical agricultural settings. However, if microplastic pollution increases in agricultural soils, possible interferences in the established soil-plant-herbivore communication mechanisms should be carefully considered.