Association of Beauveria bassiana with maize alters volatile organic compounds and enhances attraction of the egg parasitoid Telenomus podisi

Abstract

Entomopathogenic fungi can associate with plants and influence plant defence mechanisms, promoting growth and affecting interactions among crops, herbivores and natural enemies. This study evaluated the effects of maize plant colonisation by Beauveria bassiana on direct and indirect plant defences. For this, we evaluated (i) the survival and reproductive biology of the stink bug Diceraeus melacanthus on seed-inoculated, foliar-inoculated and non-inoculated maize plants, (ii) the influence of fungal inoculation on maize volatile organic compound emissions and (iii) the subsequent influence of maize volatiles in the searching behaviour of the egg parasitoid Telenomus podisi. Fungal colonisation was confirmed in more than 75% of foliar-treated plants. Fungus-treated plants (foliar spray or seed-treated) showed no significant effects on D. melacanthus survival or on female fecundity and fertility. Behavioural bioassays using a Y-olfactometer showed that T. podisi female parasitoids exhibited no preference for fungus-treated plants 24 h after inoculation, compared to untreated plants or clean air. However, 120 h post-inoculation, parasitoids were significantly attracted to foliar-inoculated plants over untreated plants or clean air controls. At this time point, foliar-inoculated plants emitted higher levels of methyl salicylate and lower levels of (E)-β-farnesene and (E,E)-α-farnesene compared to the other treatments. These results indicate that association with B. bassiana can modify maize volatile signalling and enhance attraction of a key egg parasitoid. Such fungus-mediated modulation of plant indirect defences may contribute to the compatibility between entomopathogenic fungi and natural enemies in integrated pest management programmes.