Behavioral manipulation of Drosophila suzukii for pest control: high attraction to yeast enhances insecticide efficacy when applied on leaves

Abstract

BACKGROUND The invasive pest, Drosophila suzukii attacks fresh soft‐skinned fruit. Broad‐spectrum insecticides are implemented for control but there is a need to reduce environmental risks and insecticide residues on fruits. Hanseniaspora uvarum is a yeast frequently found on ripe fruits and associated with D. suzukii. We aim to exploit the ecological association and attraction of D. suzukii to H. uvarum by developing an attract‐and‐kill strategy, with spray‐application on canopy but not fruit. We therefore investigated D. suzukii attraction, egg‐laying and mortality when exposed to insecticidal yeast‐based formulations. RESULTS Hanseniaspora uvarum strongly attracted D. suzukii when applied on leaves of grapevine, Vitis vinifera. Notably, this attractiveness was competitive to ripe grape berries that were susceptible to D. suzukii infestation. Moreover, adding H. uvarum enhanced the efficacy of insecticidal formulations against D. suzukii. Flies exposed to leaves treated with yeast‐insecticide formulations showed higher mortality and laid a lower number of eggs compared to flies exposed to insecticide alone. In a wind tunnel, all treatments containing H. uvarum alone or in combination with insecticides, caused similar upwind flight and landing at the odor source, which provides evidence that the addition of insecticide did not reduce D. suzukii attraction to yeast. CONCLUSION Hanseniaspora uvarum can be used to manipulate the behavior of D. suzukii by attracting flies to insecticide formulations. Yeast attraction is competitive to grape berries and improves insecticide effectiveness, suggesting that sprays covering canopy only, could reduce residues on fruit without compromising management efficacy.

Field and greenhouse application of an attract‐and‐kill formulation based on the yeast Hanseniaspora uvarum and the insecticide spinosad to control Drosophila suzukii in grapes

“…Control of adult D. suzukii is important because flies immigrating into vineyards from noncrop hosts cause initial infestations 32–34 . Since D. suzukii females are more attracted to the fruit than to the grapevine leaves, a promising strategy is the application of the bait evenly on the foliage, thus creating a multitude of attractive points to reduce the attraction to the fruit and increase the attraction to H. uvarum ‐treated leaves 19,35 . After attraction, the flies readily come into contact with the insecticide as they stay on the leaves to feed.…”

“…For practical uses in agriculture, an issue could be the difficulty in obtaining a stable H. uvarum ‐based formulation 19,20 . For commercial use, a stable and dry product would simplify marketing and use by farmers.…”

“…16,17 Control methods based on H. uvarum and insecticides were previously tested in the laboratory and greenhouse, and led to reduced oviposition and higher mortality of D. suzukii adults. 5,6,8,18,19 Attraction to yeast is strain-specific, 20 therefore an H. uvarum strain that has been extensively studied and is attractive to D. suzukii was used in the present study. The H. uvarum strain LB-NB-2.2 was isolated from feeding galleries of D. suzukii larvae in infested grape berries of the variety Vernatsch in South Tyrol in 2012.…”

“…Furthermore, H. uvarum is naturally present on grapes, therefore its presence likely would not interfere with winemaking 16,17 . Control methods based on H. uvarum and insecticides were previously tested in the laboratory and greenhouse, and led to reduced oviposition and higher mortality of D. suzukii adults 5,6,8,18,19 …”

“… 16 , 17 Control methods based on H. uvarum and insecticides were previously tested in the laboratory and greenhouse, and led to reduced oviposition and higher mortality of D. suzukii adults. 5 , 6 , 8 , 18 , 19 …”