Behavioral evidence for contextual olfactory‐mediated avoidance of the ubiquitous phytopathogen Botrytis cinerea by Drosophila suzukii

Abstract

Herbivorous insects may benefit from avoiding the smell produced by phytopathogens infecting plant host tissue if the infected tissue reduces insect fitness. However, in many cases the same species of phytopathogen can also infect host plant tissues that do not directly affect herbivore fitness. Thus, insects may benefit from differentiating between pathogen odors emanating from food and nonfood tissues. This is based on the hypothesis that unnecessarily staying attentive to pathogen odor from nonfood tissue may incur opportunity costs associated with not responding to other important survival functions. In this study adults of Drosophila suzukii Matsumura, an invasive larval frugivore, showed reduced attraction to the odor of raspberry fruit, a food tissue, when infected with Botrytis cinerea Pers., a ubiquitous phytopathogen, in favor of odors of uninfected raspberry fruit. Moreover, D. suzukii oviposited fewer eggs on infected raspberry fruit relative to uninfected raspberry fruit. Larval survival and adult size after eclosion were significantly reduced when reared on B. cinerea-infected raspberry relative to uninfected fruit. Interestingly, when the behavioral choice experiment was repeated using Botrytis-infected vs.-uninfected strawberry leaves, a nonfood tissue, in combination with fresh raspberry fruit, odor from B. cinerea-infected leaves did not reduce D. suzukii attraction to raspberries relative to raspberries with uninfected leaves. These behavioral results illustrate the important role context can play in odor-mediated interactions between insects, plants and microbes. We discuss implications of our findings for developing a repellent that can be useful for the management of D. suzukii.

Repellent, oviposition-deterrent, and insecticidal activity of the fungal pathogen Colletotrichum fioriniae on Drosophila suzukii (Diptera: Drosophilidae) in highbush blueberries

“…Previously, Graziosi and Rieske 36 had also shown that infection by Colletotrichum acutatum increases the mortality of the Asian chestnut gall wasp D. kuriphilus. Raspberries infected by the fungus B. cinerea also repelled D. suzukii and reduced larval survival and adult oviposition and size 11 . Interestingly, our results showed that both anthracnose solutions ('field' and 'colony'), but not the 'filtered' solution, have repellent and insecticidal effects on D. suzukii, indicating that removing C. fioriniae conidia eliminates these negative effects.…”

“…However, fruit infection by fungal pathogens can also negatively affect Drosophila spp. For example, D. suzukii larval survival and adult size were significantly reduced when they were reared on raspberries infected by Botrytis cinerea Pers., and fruit infection by this fungus also reduced fly attraction and oviposition 11 . Therefore, odors from microbes associated with D. suzukii could serve as sources of attractive and repellent compounds to manipulate the fly's behavior in agroecosystems 17,18 .…”

“…Because plant–insect and plant-pathogen interactions share many features including adaptations and counter-adaptions and negative effects of invasive species on humans 8 , understanding complex plant-pathogen-insect interactions could help in the discovery of novel pest management strategies in agroecosystems. Drosophila spp., including D. suzukii , have associations with microbes (i.e., fungi and bacteria) that can be mutualistic (where both species benefit) 9 , commensal (where only one of the species benefits) 10 , or antagonistic (where one species has a negative effect on the other) 11 . For example, D. suzukii has a strong relationship with mutualistic yeasts that improve larval survival and development and increase oviposition on fruits 12 .…”

“…including D. suzukii, have associations with microbes (i.e., fungi and bacteria) that can be mutualistic (where both species benefit) 9 , commensal (where only one of the species benefits) 10 , or antagonistic (where one species has a negative effect on the other) 11 . For example, D. suzukii has a strong relationship with mutualistic yeasts that improve larval survival and development and increase oviposition on fruits 12 .…”

Automated aerosol puffers effectively deliver 1‐OCTEN‐3‐OL, an oviposition antagonist useful against spotted‐wing drosophila

“…16,21,22 While octenol is a common mushroom alcohol emitted by fungal fruiting bodies, geosmin is an earthy odor associated with soil dwelling fungi and bacteria, 21 and both are presumably deterrent due to the close association of these odors with potential pathogen infection. 23,24 Previous studies on these repellents have focused on product efficacy aimed at establishing the degree of deterrent action and relative dose responses. In the lab, octenol reduces oviposition in raspberries at concentrations as low as 0.1%, increasing in effect in preparations up to 10% v/v preparation in mineral oil.…”