Blueberries infected with the fungal pathogen Colletotrichum fioriniae release odors that repel Drosophila suzukii

Authors: Rering, Caitlin; QUADREL, AMANDA - Rutgers University; URBANEJA-BERNAT, PABLO - Rutgers University; Beck, John; BEN-ZVI, YAHEL - Virginia Polytechnic Institution & State University; KHODADADI, FATEMAH - Virginia Polytechnic Institution & State University; RODRIGUEZ-SAONA, CESAR - Rutgers University

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/11/2023
Publication Date: 8/7/2023
Citation: Rering, C.C., Quadrel, A., Urbaneja-Bernat, P., Beck, J.J., Ben-Zvi, Y., Khodadadi, F., Rodriguez-Saona, C.R. 2023. Blueberries infected with the fungal pathogen Colletotrichum fioriniae release odors that repel Drosophila suzukii. Pest Management Science. 79(12):4906-4920. https://doi.org/10.1002/ps.7692.
DOI: https://doi.org/10.1002/ps.7692

Interpretive Summary: Drosophila suzukii is among the most destructive pests of small fruits like strawberries, raspberries, cherries, and blueberries in the USA, causing over $300 million in losses annually. D. suzukii females lay their eggs in ripening fruit. The developing larvae make the food unmarketable, and the wounds left by the female cause microbial infection. Because the eggs and larvae of D. suzukii are enclosed within the fruit, they are shielded from contact with insecticide sprays, making control of this pest very difficult. As an alternative to pesticide application, odors can be used to manipulate pest behavior in the field. For example, attractive odors can be mixed with toxins to kill the pest, or repellent odors can be used to divert the pest away from a crop. Only a few repellents have been identified for D. suzukii to date and more options are needed. Scientists previously identified that D. suzukii were repelled by odors emanating from blueberries infected with the fungal pathogen Colletotrichum fioriniae, but the exact changes in chemical composition responsible for their avoidance was unknown. ARS Scientists at the Center for Medical, Agricultural, and Veterinary Entomology, in Gainesville, FL in collaboration with scientists from Rutgers University infected blueberry fruits with the pathogen and studied the odors which were produced. We found that infected fruit produced higher amounts of 14 chemicals. We then tested how D. suzukii responded to each chemical individually. Of the 14 chemicals tested, nine were repellent, two were attractive, and three had no impact on D. suzukii behavior. All nine repellent chemicals were not previously known to elicit avoidance in D. suzukii adults. Additionally, one novel chemical attractant was identified. Results from this study present promising new tools that are needed for effective management of this destructive agricultural pest.

Technical Abstract: Spotted-wing drosophila, Drosophila suzukii, is a serious pest of soft, thin-skinned fruits. Alternative methods to control this pest are needed, including new repellents which can be deployed in push-pull systems. Previous research demonstrated that D. suzukii adults use odor cues to avoid blueberries infected with the fungal pathogen Colletotrichum fioriniae, which causes the disease anthracnose. To identify novel repellent volatiles, we investigated the volatile emission of infected blueberry and tested the differentially induced volatiles by infection on D. suzukii adult behavior. Two sample types were compared: experimentally-infected fruit which were inoculated with five C. fioriniae isolates in the laboratory, and field-collected fruit, which were naturally infected and harvested from a field. Volatile emission was similar between all five C. fioriniae strains and good agreement was found between experimentally-infected and field-collected berries. In total, 14 volatiles were found to be more abundant in the headspace of infected fruit versus uninfected. In multiple-choice bioassays nine of the 14 volatiles elicited repellency responses from adult D. suzukii. These nine volatiles were further evaluated in dual choice assays where all nine reduced fly capture by 43–96% compared to the control. The most repellent compounds tested were the esters ethyl butanoate and ethyl (E)-but-2-enoate. Additionally, a novel D. suzukii attractant, styrene, was identified. In total, we report nine volatiles which may be useful semiochemicals for the behavioral manipulation of D. suzukii in the field.