{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,26]],"date-time":"2026-10-26T14:33:40Z","timestamp":1793025220206,"version":"4.5.0"},"reference-count":82,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T00:00:00Z","timestamp":1747612800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>Attract-and-kill strategies are effective, sustainable pest control methods. Formulations combining the insecticide spinosad, at a lower dose than conventional methods, with the <jats:italic>Drosophila<\/jats:italic>-associated yeast <jats:italic>Hanseniaspora uvarum<\/jats:italic> have shown promising results<jats:italic>.<\/jats:italic> Recently, <jats:italic>Saccharomycopsis vini<\/jats:italic> was identified as the most attractive yeast for ovipositing females. In this study, the potential of <jats:italic>S. vini<\/jats:italic> for use in attract-and-kill formulations against <jats:italic>D. suzukii<\/jats:italic> was evaluated alongside <jats:italic>H. uvarum<\/jats:italic>. Behavioural assays demonstrated that <jats:italic>D. suzukii<\/jats:italic> preferred <jats:italic>S. vini<\/jats:italic> when both yeasts are simultaneously present in a close range setting but was attracted to both in long range attraction assays. In efficacy assays, <jats:italic>S. vini<\/jats:italic> and <jats:italic>H. uvarum<\/jats:italic> were equally efficient at reducing oviposition and increasing mortality in formulation with spinosad. Offering yeast formulations at the foraging sites of trained honey bees did not stimulate more feeding when compared to sugar syrup. The characterisation of the organic volatile compounds released from the cultures demonstrated that <jats:italic>S. vini<\/jats:italic> and <jats:italic>H. uvarum<\/jats:italic> were composed of overlapping as well as distinct chemicals. The antennally active compounds ethyl acetate and ethyl propanoate were abundant in the more attractive <jats:italic>S. vini<\/jats:italic> and <jats:italic>H. uvarum<\/jats:italic>, while the compounds 3-methyl-1-butanol and 2-methylthiolan-3-one were more abundant in the less attractive <jats:italic>S. cerevisiae<\/jats:italic>. These chemicals may be further studied as possible attractants or repellents for <jats:italic>D. suzukii.<\/jats:italic> We propose <jats:italic>S. vini<\/jats:italic> as a new yeast with potential for use in integrated pest management, with a distinctive volatile profile while maintaining a similar efficacy compared to <jats:italic>H. uvarum<\/jats:italic> against <jats:italic>D. suzukii.<\/jats:italic> Neither <jats:italic>H. uvarum<\/jats:italic> nor <jats:italic>S. vini<\/jats:italic> stimulated honey bee foraging behaviour, suggesting that both yeast-based attract-and-kill formulations pose a low non-target risk to honey bees.<\/jats:p>","DOI":"10.1371\/journal.pone.0323653","type":"journal-article","created":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T18:04:54Z","timestamp":1747677894000},"page":"e0323653","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["Yeast-based attract-and-kill strategies for Drosophila suzukii management without disrupting honey bee 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priorities","volume":"88","author":"MK Asplen","year":"2015","journal-title":"J Pest Sci"},{"issue":"1","key":"pone.0323653.ref003","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1111\/1365-2664.12688","article-title":"Enhanced yeast feeding following mating facilitates control of the invasive fruit pest Drosophila suzukii","volume":"54","author":"BA Mori","year":"2016","journal-title":"J Appl Ecol"},{"issue":"1","key":"pone.0323653.ref004","doi-asserted-by":"crossref","first-page":"14059","DOI":"10.1038\/srep14059","article-title":"Volatile codes: correlation of olfactory signals and reception in Drosophila-yeast chemical communication","volume":"5","author":"N Scheidler","year":"2015","journal-title":"Sci Rep"},{"issue":"7","key":"pone.0323653.ref005","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1111\/1365-2435.14054","article-title":"Yeast and fruit fly mutual niche construction and antagonism against mould","volume":"36","author":"A Chakraborty","year":"2022","journal-title":"Funct Ecol"},{"key":"pone.0323653.ref006","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1007\/BF02480367","article-title":"Odorant response of individual sensilla on the Drosophila antenna","volume":"3","author":"P Clyne","year":"1997","journal-title":"Invert Neurosci"},{"key":"pone.0323653.ref007","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1146\/annurev.neuro.20.1.595","article-title":"Mechanisms of olfactory discrimination: converging evidence for common principles across phyla","volume":"20","author":"JG Hildebrand","year":"1997","journal-title":"Annu Rev Neurosci"},{"issue":"4","key":"pone.0323653.ref008","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1016\/S0092-8674(00)81387-2","article-title":"Visualizing an olfactory sensory map","volume":"87","author":"P Mombaerts","year":"1996","journal-title":"Cell"},{"issue":"5","key":"pone.0323653.ref009","doi-asserted-by":"crossref","first-page":"1950","DOI":"10.1093\/jee\/toab158","article-title":"Drosophila suzukii (Diptera: Drosophilidae): a decade of research towards a sustainable integrated pest management program","volume":"114","author":"G Tait","year":"2021","journal-title":"J Econ Entomol"},{"key":"pone.0323653.ref010","first-page":"149","article-title":"A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management","volume":"65","author":"A Cini","year":"2012","journal-title":"Bull Insectol"},{"key":"pone.0323653.ref011","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.cropro.2013.08.003","article-title":"Control of spotted wing drosophila, Drosophila suzukii, by specific insecticides and by conventional and organic crop protection programs","volume":"54","author":"S Van Timmeren","year":"2013","journal-title":"Crop 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concentrations","volume":"378","author":"V Christen","year":"2019","journal-title":"J Hazard Mater"},{"key":"pone.0323653.ref015","first-page":"37","article-title":"Spinosad toxicity to pollinators and associated risk","volume":"179","author":"MA Mayes","year":"2003","journal-title":"Rev Environ Contam Toxicol"},{"issue":"1","key":"pone.0323653.ref016","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1093\/jee\/toac204","article-title":"Potential alternatives to spinosad as the killing agent mixed with two attractant products in attract-and-kill formulations used to manage the spotted-wing Drosophila, Drosophila suzukii (Diptera: Drosophilidae)","volume":"116","author":"EM Rhodes","year":"2023","journal-title":"J Econ Entomol"},{"issue":"1","key":"pone.0323653.ref017","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1093\/jisesa\/iey132","article-title":"Testing a novel attract-and-kill strategy for Drosophila suzukii (Diptera: Drosophilidae) 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attraction to yeast enhances insecticide efficacy when applied on leaves","volume":"78","author":"G Rehermann","year":"2022","journal-title":"Pest Manag Sci"},{"key":"pone.0323653.ref027","doi-asserted-by":"crossref","first-page":"106868","DOI":"10.1016\/j.cropro.2024.106868","article-title":"Canopy strip applications of Hanseniaspora uvarum combined with spinosad reduce insecticide use without compromising Drosophila suzukii control in cherry","volume":"186","author":"M Bjeljac","year":"2024","journal-title":"Crop Protection"},{"issue":"4","key":"pone.0323653.ref028","doi-asserted-by":"crossref","first-page":"1295","DOI":"10.1007\/s10340-020-01266-y","article-title":"Yeast species affects feeding and fitness of Drosophila suzukii adults","volume":"93","author":"U Spitaler","year":"2020","journal-title":"J Pest Sci"},{"issue":"11","key":"pone.0323653.ref029","doi-asserted-by":"crossref","first-page":"830","DOI":"10.1007\/s10886-024-01494-x","article-title":"Chemical and electrophysiological characterisation of headspace volatiles from yeasts attractive to Drosophila suzukii","volume":"50","author":"I Castellan","year":"2024","journal-title":"J Chem Ecol"},{"issue":"3","key":"pone.0323653.ref030","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1023\/A:1006456720416","article-title":"Varroa jacobsoni (Acari: Varroidae) is more than one species","volume":"24","author":"DL Anderson","year":"2000","journal-title":"Exp Appl Acarol"},{"issue":"18","key":"pone.0323653.ref031","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1016\/j.cub.2008.08.062","article-title":"Genetic variability and robustness of host odor preference in Drosophila melanogaster","volume":"18","author":"A Ruebenbauer","year":"2008","journal-title":"Curr Biol"},{"key":"pone.0323653.ref032","doi-asserted-by":"crossref","first-page":"821145","DOI":"10.3389\/finsc.2022.821145","article-title":"Impact of chronic exposure to two neonicotinoids on honey bee antennal responses to flower volatiles and pheromonal compounds","volume":"2","author":"R Favaro","year":"2022","journal-title":"Front Insect Sci"},{"issue":"11","key":"pone.0323653.ref033","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0143641","article-title":"Exploring the Saccharomyces cerevisiae volatile metabolome: indigenous versus commercial strains","volume":"10","author":"Z Alves","year":"2015","journal-title":"PLoS One"},{"issue":"6","key":"pone.0323653.ref034","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1038\/nmeth.3393","article-title":"MS-DIAL: data-independent MS\/MS deconvolution for comprehensive metabolome analysis","volume":"12","author":"H Tsugawa","year":"2015","journal-title":"Nat Methods"},{"issue":"2","key":"pone.0323653.ref035","doi-asserted-by":"crossref","DOI":"10.1101\/pdb.prot5565","article-title":"General approach to adoptive transfer and cell labeling for immunoimaging","volume":"2011","author":"MP Matheu","year":"2011","journal-title":"Cold Spring Harb Protoc"},{"issue":"5","key":"pone.0323653.ref036","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1016\/S0896-6273(03)00094-1","article-title":"Integrating the molecular and cellular basis of odor coding in the Drosophila antenna","volume":"37","author":"AA Dobritsa","year":"2003","journal-title":"Neuron"},{"issue":"3","key":"pone.0323653.ref037","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/bimj.200810425","article-title":"Simultaneous inference in general parametric models","volume":"50","author":"T Hothorn","year":"2008","journal-title":"Biom J"},{"key":"pone.0323653.ref038","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"Fitting linear mixed-effects models using lme4","volume":"67","author":"D Bates","year":"2015","journal-title":"J Stat Softw"},{"key":"pone.0323653.ref039","unstructured":"Hartig F, Hartig M. Package \u2018dharma\u2019. https:\/\/cran.r-project.org\/package=DHARMa."},{"key":"pone.0323653.ref040","volume-title":"Multcompview: visualizations of paired comparisons","author":"S Graves","year":"2019"},{"key":"pone.0323653.ref041","volume-title":"An R Companion to Applied Regression","author":"S Weisberg","year":"2019"},{"issue":"5","key":"pone.0323653.ref042","doi-asserted-by":"crossref","first-page":"3590","DOI":"10.1021\/acs.analchem.8b05592","article-title":"Systematic error removal using random forest for normalizing large-scale untargeted lipidomics data","volume":"91","author":"S Fan","year":"2019","journal-title":"Anal Chem"},{"issue":"1","key":"pone.0323653.ref043","doi-asserted-by":"crossref","first-page":"14567","DOI":"10.1038\/s41598-017-15231-w","article-title":"Chemical similarity enrichment analysis (ChemRICH) as alternative to biochemical pathway mapping for metabolomic datasets","volume":"7","author":"DK Barupal","year":"2017","journal-title":"Sci Rep"},{"key":"pone.0323653.ref044","unstructured":"R core T. 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Bruce","year":"2011","journal-title":"Phytochemistry"},{"issue":"1","key":"pone.0323653.ref048","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1038\/s41598-020-79691-3","article-title":"Separate and combined Hanseniaspora uvarum and Metschnikowia pulcherrima metabolic volatiles are attractive to Drosophila suzukii in the laboratory and field","volume":"11","author":"R Jones","year":"2021","journal-title":"Sci Rep"},{"issue":"6","key":"pone.0323653.ref049","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1111\/jen.13006","article-title":"Lure design for Drosophila suzukii based on liquid culture of fruit epiphytic yeasts: comparing the attractivity of fermentation volatiles for seasonal morphs","volume":"146","author":"AL Erdei","year":"2022","journal-title":"J Appl Entomol"},{"issue":"1","key":"pone.0323653.ref050","doi-asserted-by":"crossref","DOI":"10.1002\/ece3.9713","article-title":"Plasticity in oviposition and foraging behavior in the invasive pest Drosophila suzukii across natural and agricultural landscapes","volume":"13","author":"JE Elsensohn","year":"2023","journal-title":"Ecol Evol"},{"issue":"6","key":"pone.0323653.ref051","doi-asserted-by":"crossref","first-page":"1832","DOI":"10.1890\/06-1632.1","article-title":"Predicting the economic impact of an invasive species on an ecosystem service","volume":"17","author":"DC Cook","year":"2007","journal-title":"Ecol Appl"},{"issue":"6","key":"pone.0323653.ref052","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1016\/j.tplants.2020.01.006","article-title":"Delivering integrated pest and pollinator management (IPPM)","volume":"25","author":"PA Egan","year":"2020","journal-title":"Trends Plant Sci"},{"issue":"1","key":"pone.0323653.ref053","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1007\/s13593-021-00742-8","article-title":"Pesticide-free agriculture as a new paradigm for research","volume":"42","author":"F Jacquet","year":"2022","journal-title":"Agron Sustain Dev"},{"key":"pone.0323653.ref054","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1080\/00218839.1988.11100777","article-title":"Yeast-contaminated nectar and its effects on bee foraging","volume":"27","author":"P Kevan","year":"1988","journal-title":"J Apicult Res"},{"issue":"2","key":"pone.0323653.ref055","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.femsec.2004.06.003","article-title":"Ecology of yeasts in plant-bumblebee mutualism in Central Europe","volume":"50","author":"M Brysch-Herzberg","year":"2004","journal-title":"FEMS Microbiol Ecol"},{"issue":"1","key":"pone.0323653.ref056","article-title":"The impact of yeast presence in nectar on bumble bee behavior and fitness","volume":"90","author":"MI Pozo","year":"2020","journal-title":"Ecol Monogr"},{"issue":"8","key":"pone.0323653.ref057","doi-asserted-by":"crossref","first-page":"4141","DOI":"10.1111\/1462-2920.15528","article-title":"Pollen and yeast change nectar aroma and nutritional content alone and together, but honey bee foraging reflects only the avoidance of yeast","volume":"23","author":"CC Rering","year":"2021","journal-title":"Environ Microbiol"},{"issue":"2","key":"pone.0323653.ref058","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1002\/ps.5150","article-title":"Grower adoption of insecticide resistance management practices increase with extension-based program","volume":"75","author":"AB Leach","year":"2019","journal-title":"Pest Manag Sci"},{"key":"pone.0323653.ref059","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.biosystems.2017.10.010","article-title":"Fundamental principles of the olfactory code","volume":"164","author":"V Grabe","year":"2018","journal-title":"Biosystems"},{"issue":"3","key":"pone.0323653.ref060","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1007\/s10886-016-0681-3","article-title":"Pheromonal cues deposited by mated females convey social information about egg-laying sites in Drosophila melanogaster","volume":"42","author":"C Dum\u00e9nil","year":"2016","journal-title":"J Chem Ecol"},{"issue":"1","key":"pone.0323653.ref061","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1111\/phen.12088","article-title":"Olfactory responses of Drosophila suzukii females to host plant volatiles","volume":"40","author":"S Revadi","year":"2015","journal-title":"Physiol Entomol"},{"issue":"2","key":"pone.0323653.ref062","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1007\/s10886-015-0544-3","article-title":"Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit","volume":"41","author":"IW Keesey","year":"2015","journal-title":"J Chem Ecol"},{"issue":"4","key":"pone.0323653.ref063","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1007\/s10340-018-1006-9","article-title":"Identification of attractive blend for spotted wing drosophila, Drosophila suzukii, from apple juice","volume":"91","author":"Y Feng","year":"2018","journal-title":"J Pest Sci (2004)"},{"issue":"10","key":"pone.0323653.ref064","doi-asserted-by":"crossref","first-page":"922","DOI":"10.1007\/s10886-018-1000-y","article-title":"Advances in the chemical ecology of the spotted wing drosophila (Drosophila suzukii) and its applications","volume":"44","author":"KR Cloonan","year":"2018","journal-title":"J Chem Ecol"},{"issue":"2","key":"pone.0323653.ref065","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1093\/jee\/toab006","article-title":"Assessment of attractant lures and monitoring traps for Drosophila suzukii (Diptera: Drosophidae) using electrophysiology, laboratory choice assays, and field trials","volume":"114","author":"CM Little","year":"2021","journal-title":"J Econ Entomol"},{"issue":"8","key":"pone.0323653.ref066","doi-asserted-by":"crossref","first-page":"3698","DOI":"10.1002\/ps.6282","article-title":"Behavioral and physiological responses of Drosophila melanogaster and D. suzukii to volatiles from plant essential oils","volume":"77","author":"Q Wang","year":"2021","journal-title":"Pest Manag Sci"},{"issue":"2","key":"pone.0323653.ref067","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1093\/ee\/nvv013","article-title":"Behavioral and antennal responses of Drosophila suzukii (Diptera: Drosophilidae) to volatiles from fruit extracts","volume":"44","author":"J Abraham","year":"2015","journal-title":"Environ Entomol"},{"issue":"3","key":"pone.0323653.ref068","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1093\/ee\/nvy046","article-title":"Comparative antennal and behavioral responses of summer and winter morph Drosophila suzukii (Diptera: Drosophilidae) to ecologically relevant volatiles","volume":"47","author":"DM Kirkpatrick","year":"2018","journal-title":"Environ 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Roelofs","year":"1984"},{"issue":"3","key":"pone.0323653.ref080","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1152\/jn.1991.65.3.702","article-title":"Characterization of the electroantennogram in Drosophila melanogaster and its use for identifying olfactory capture and transduction mutants","volume":"65","author":"E Alcorta","year":"1991","journal-title":"J Neurophysiol"},{"issue":"1","key":"pone.0323653.ref081","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1002\/ps.4666","article-title":"Evaluating a push-pull strategy for management of Drosophila suzukii Matsumura in red raspberry","volume":"74","author":"AK Wallingford","year":"2018","journal-title":"Pest Manag Sci"},{"issue":"3","key":"pone.0323653.ref082","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1002\/etc.4008","article-title":"Forensic source attribution for toluene in environmental samples","volume":"37","author":"PI Richards","year":"2018","journal-title":"Environ Toxicol Chem"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0323653","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,19]],"date-time":"2025-05-19T18:05:07Z","timestamp":1747677907000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0323653"}},"subtitle":[],"editor":[{"given":"Nikos T.","family":"Papadopoulos","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,5,19]]},"references-count":82,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5,19]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0323653","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,19]]}}}