Natural enemy-derived volatiles induce non-consumptive negative effects on the pest aphid, Myzus persicae

Abstract

Biological control reduces the need for potentially hazardous insecticides and enhances sustainability of pest management but gaps in understanding of natural enemy ecology constrains its uptake and impact. Whilst direct, lethal predatory and parasitic impacts on herbivores are well-documented, non-lethal, non-consumptive effects have received very much less attention and known mechanisms of operation are confined to physical effects such as disturbance. Here we show for the first time that natural enemy-derived volatiles exert manifold negative effects on aphid biology. Myzus persicae Sulzer (Hemiptera: Aphididae) is a globally significant aphid pest for which the predatory ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) and the parasitoid wasp Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) are potentially important biological control agents. In vitro, plant-free studies showed that aphids exposed to volatiles but without direct contact with these natural enemies exhibited impaired life history traits including longevity, weight gain and fecundity. Volatiles from H. axyridis larvae were especially potent and, in olfactometer studies, caused a strong repellent effect. In whole plant studies, aphid fecundity declined and development time extended markedly when placed on leaves previously occupied by natural enemies. These findings open a new avenue in the chemical ecology of natural enemy-herbivore interactions. By highlighting the potential of volatile-mediated effects to interfere with pests such as aphids, this study offers insights that could significantly improve pest management practices, making them more effective and sustainable.