{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T23:41:19Z","timestamp":1789688479894,"version":"4.0.1"},"reference-count":47,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T00:00:00Z","timestamp":1773619200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Sichuan Natural Science Foundation Project","award":["2023NSFSC0152"],"award-info":[{"award-number":["2023NSFSC0152"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Although Telenomus remus is an important parasitoid of Spodoptera frugiperda, the chemical basis for its host selection behavior remains unclear. To elucidate the chemical basis of this behavior, this study combined behavioral ecology and chemical ecology methods to systematically investigate the host location and recognition behaviors of this wasp, as well as the semiochemicals that regulate these behaviors. In Y-tube olfactometer assays, T. remus exhibited a significantly stronger olfactory preference for eggs of S. frugiperda over those of S. litura (p &lt; 0.05) or the non-host Ostrinia furnacalis. A total of 759 metabolites belonging to 11 categories were identified via metabolomics analysis, and principal component analysis (PCA) clearly distinguished between host eggs and non-host eggs. Analysis of differential metabolites revealed that the significantly upregulated metabolites in host eggs mainly included aldehydes, ketones and esters, followed by hydrocarbons, alcohols and amines. Subsequently, we screened and verified the effects of the significantly upregulated metabolites in host eggs compared with non-host eggs on the host-selection behavior of T. remus, including indole, 2-hexanol, and trans-1,2-dimethylcyclohexane, as well as 2-heptadecanone and n-nonadecane\u2014two alkane compounds which are specifically upregulated on the surface of S. frugiperda eggs. Behavioral validation demonstrated that 2-hexanol exerted a significant repellent effect on T. remus, whereas trans-1,2-dimethylcyclohexane exhibited a significant attractive effect on the parasitoid wasp. Among the metabolites specifically upregulated in S. frugiperda eggs, 2-heptadecanone exhibited significant attractive activity at concentrations ranging from 0.1 to 1.0 mg\/mL. This study is the first to report that the cycloalkane compound trans-1,2-dimethylcyclohexane acts as a potential broad-spectrum chemical marker for T. remus to recognize the eggs of host species belonging to the family Noctuidae, while 2-heptadecanone may further enhance its preference for the optimal host S. frugiperda. These findings provide novel candidate molecular targets for the development of behavioral regulators targeting egg parasitoids against S. frugiperda.<\/jats:p>","DOI":"10.3390\/insects17030321","type":"journal-article","created":{"date-parts":[[2026,3,17]],"date-time":"2026-03-17T09:35:57Z","timestamp":1773740157000},"page":"321","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Chemical Recognition Mechanism of Telenomus remus Preference for Spodoptera frugiperda Eggs Based on Metabolomics with GC-MS"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-1476-3996","authenticated-orcid":false,"given":"Chunyan","family":"Yi","sequence":"first","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1640-2704","authenticated-orcid":false,"given":"Wenjuan","family":"Yu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mao","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cuicui","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianqin","family":"Fan","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Yang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Song","family":"Chen","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-5947-7959","authenticated-orcid":false,"given":"Yanping","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Integrated Pest Management of Southwest Crops, Institute of Plant Protection, Sichuan Academy of Agricultural Sciences, Chengdu 610066, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,3,16]]},"reference":[{"key":"ref_1","first-page":"10","article-title":"Observation on law of diffusion damage of Spodoptera frugiperda in China in 2019","volume":"45","author":"Jiang","year":"2019","journal-title":"Plant Prot."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1016\/S2095-3119(21)63621-3","article-title":"Spread of invasive migratory pest Spodoptera frugiperda and management practices throughout China","volume":"20","author":"Yan","year":"2021","journal-title":"J. Integr. Agric."},{"key":"ref_3","first-page":"1","article-title":"Potential invasion of the crop devastating insect pest fall armyworm Spodoptera frugiperda to China","volume":"44","author":"Guo","year":"2018","journal-title":"Plant Prot."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Paredes-S\u00e1nchez, F.A., Rivera, G., Bocanegra-Garc\u00eda, V., Mart\u00ednez-Padr\u00f3n, H.Y., Berrones-Morales, M., Ni\u00f1o-Garc\u00eda, N., and Herrera-Mayorga, V. (2021). Advances in control strategies against Spodoptera frugiperda. A Review. Molecules, 26.","DOI":"10.3390\/molecules26185587"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/BF02375224","article-title":"Release of Telenomus remus (Hym.Scelionidae) against Spodoptera frugiperda (Lep.: Noctuidae) in Florida U.S.A","volume":"27","author":"Waddill","year":"1982","journal-title":"Entomophaga"},{"key":"ref_6","first-page":"15","article-title":"Research progress on predatory natural enemy insect of Spodoptera frugiperda","volume":"50","author":"Ren","year":"2022","journal-title":"Jiangsu J. Agric. Sci."},{"key":"ref_7","first-page":"370","article-title":"The natural enemies of the fall armyworm Spodoptera frugiperda and their application in biological control programs","volume":"56","author":"Tang","year":"2019","journal-title":"Chin. J. Appl. Entomol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Ramanujam, B., Poornesha, B., and Shylesha, A.N. (2020). Effect of entomopathogenic fungi against invasive pest Spodoptera frugiperda (J.E.Smith) (Lepidoptera: Noctuidae) in maize. Egypt. J. Biol. Pest Control, 30.","DOI":"10.1186\/s41938-020-00291-4"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"5030","DOI":"10.1007\/s11356-019-07079-6","article-title":"Biocontrol potential of methyl chavicol for managing Spodoptera frugiperda (Lepidoptera: Noctuidae), an important corn pest","volume":"27","author":"Menezes","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1007\/s10526-008-9180-y","article-title":"Activity of quinolizidine alkaloids from three Mexican lupinus against the lepidopteran crop pest Spodoptera frugiperda","volume":"54","author":"Herrera","year":"2009","journal-title":"BioControl"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Rioba, N.B., and Stevenson, P.C. (2020). Opportunities and scope for botanical extracts and products for the management of fall armyworm (Spodoptera frugiperda) for small holders in Africa. Plants, 9.","DOI":"10.3390\/plants9020207"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1653\/024.095.0225","article-title":"Insecticidal activity of Tagetes erecta extracts on Spodoptera frugiperda (Lepidoptera: Noctuidae)","volume":"95","year":"2012","journal-title":"Fla. Entomol."},{"key":"ref_13","first-page":"21","article-title":"Biology, ecology and use in pest management of Telenomus remus","volume":"21","author":"Cave","year":"2000","journal-title":"Biocontrol News Inf."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1590\/S0103-84782008000100001","article-title":"Biology and thermal requirements of Telenomus remus reared on fall armyworm Spodoptera frugiperda eggs","volume":"38","author":"Bueno","year":"2008","journal-title":"Ci\u00eanc. Rural"},{"key":"ref_15","first-page":"172","article-title":"Identification of two parasitoid wasps of Spodoptera frugiperda egg and their parasitic behavior","volume":"46","author":"Wang","year":"2020","journal-title":"Plant Prot."},{"key":"ref_16","first-page":"1146","article-title":"A Preliminary Study of Mass Rearing Telenomus remus Nixon on Spodoptera litura","volume":"37","author":"Xie","year":"2021","journal-title":"Chin. J. Biol. Control"},{"key":"ref_17","first-page":"267","article-title":"Preliminary evaluation of field competition between Trichogramma pretiosum and Telenomus remus in the control of Spodoptera frugiperda","volume":"46","author":"Zhu","year":"2020","journal-title":"Plant Prot."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/BF02372784","article-title":"Adult biology of Telenomus remus [Hymenoptera: Scelionidae] under laboratory conditions","volume":"19","author":"Schwarta","year":"1974","journal-title":"Entomophaga"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3001","DOI":"10.1016\/j.cub.2025.04.066","article-title":"An egg parasitoid assesses host egg quality from afar using oviposition-induced plant volatiles","volume":"35","author":"Tian","year":"2025","journal-title":"Curr. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Consoli, F.L., Parra, J.R.P., and Zucchi, R.A. (2010). Host searching by egg parasitoids: Exploitation of host chemical cues. Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma, Springer.","DOI":"10.1007\/978-1-4020-9110-0"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1016\/S1872-2032(08)60039-6","article-title":"Behavioral mechanisms of parasitic wasps for searching concealed insect hosts","volume":"28","author":"Wang","year":"2008","journal-title":"Acta Ecol. Sin."},{"key":"ref_22","first-page":"1250","article-title":"Evaluation of the olfactory compensation role of transient receptor potential channels in oviposition site location of Diaphorina citri","volume":"47","author":"Huang","year":"2025","journal-title":"J. Environ. Entomol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1007\/s10886-013-0373-1","article-title":"A novel fatty acyl desaturase from the pheromone glands of Ctenopseustis obliquana and C. herana with specific Z5-Desaturase activity on myristic acid","volume":"40","author":"Albre","year":"2014","journal-title":"J. Chem. Ecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e72012","DOI":"10.1002\/ece3.72012","article-title":"Attraction of Telenomus remus to egg volatiles of Spodoptera litura and oviposition-induced plant volatiles from tobacco (Nicotiana tabacum)","volume":"15","author":"Osman","year":"2025","journal-title":"Ecol. Evol."},{"key":"ref_25","unstructured":"Hu, X. (2024). Olfactory Behavior of Female Moths in Grapholita molesta (Busck) on Recognizing Yuluxiang Pear (Pyrus sinkiangensis). [Master\u2019s Thesis, Shanxi Agricultural University]."},{"key":"ref_26","unstructured":"Liang, M. (2023). A Preliminary Study on the Screening of Encarsia formosa Attractants and Their Repellent Effect on Bemisia tabaci. [Master\u2019s Thesis, Zhejiang University]."},{"key":"ref_27","unstructured":"Bi, K. (2012). Ultrastructure of Antennal Sensilla from Parasitoid Fopius arisanus and Its Responses to Semiochemicals from Bactrocera dorsalis Eggs Surface. [Master\u2019s Thesis, Fujian Agriculture and Forestry University]."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1111\/j.1570-7458.1992.tb01586.x","article-title":"Identification of compounds from the eggs of Ostinia nubilalis and Mamestra brassicae having kairomone activity on Trichogramma brassicae","volume":"63","author":"Renou","year":"1992","journal-title":"Entomol. Exp. Appl."},{"key":"ref_29","unstructured":"Wang, H. (2024). Screening of Active Odors on Searching and Locating Spodoptera frugiperda by Parasitoid Telenomus remus and the Binding Properties of TremOBP1 and TremOBP11. [Master\u2019s Thesis, Shanxi Agricultural University]."},{"key":"ref_30","first-page":"1399","article-title":"Population growth potential of Telenomus remus Nixon (Hymenoptera: Scelionidae) on eggs of three noctuid moths","volume":"45","author":"Lin","year":"2023","journal-title":"J. Environ. Entomol."},{"key":"ref_31","first-page":"1140","article-title":"Screening of host species for the mass rearing of Telenomus remus Nixon (Hymenoptera: Platygastridae)","volume":"37","author":"Wu","year":"2021","journal-title":"Chin. J. Biol. Control"},{"key":"ref_32","first-page":"89","article-title":"Effects of egg-surface chemicals on the oviposition behaviors of Bactrocera dorsalis Hendel","volume":"36","author":"Zhao","year":"2014","journal-title":"J. Environ. Entomol."},{"key":"ref_33","first-page":"535","article-title":"Contact response of Trichogramma confusum to 13 saturated hydrocarbons from host egg shells and abdominal scales of Plutella xylostella","volume":"37","author":"Lv","year":"2010","journal-title":"J. Plant Prot."},{"key":"ref_34","unstructured":"Wang, W. (2024). Study on the Olfactory Response Mechanism of Cotesia ruficrus to Spodoptera frugiperda. [Doctoral Dissertation, Fujian Agriculture and Forestry University]."},{"key":"ref_35","first-page":"244","article-title":"Extraction and identification of maize volatiles and cuticular volatiles of larval Helicoverpa armigera (Lepidoptera: Noctuidae) related to host-habitat location and host location of parasitic wasp Microplitis mediator (Hymenoptera: Braconidae)","volume":"58","author":"Shi","year":"2015","journal-title":"Acta Entomol. Sin."},{"key":"ref_36","unstructured":"Dong, Z. (2021). Behavior and Mechanism on Oviposition Selection of Glenea cantor Fabricius. [Doctoral Dissertation, Guangxi University]."},{"key":"ref_37","unstructured":"Li, Q. (2024). The Mechanism of Nitrogen-Mediated Indoleemission and Antiherbivore Defense Against Spodoptera frugiperda in Maize. [Master\u2019s Thesis, Fujian Agriculture and Forestry University]."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.phytochem.2011.08.029","article-title":"Biosynthesis and emission of insect herbivory-induced volatile indole in rice","volume":"73","author":"Zhuang","year":"2012","journal-title":"Phytochemistry"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1016\/j.phytochem.2003.11.021","article-title":"Transcriptional activation of Igl, the gene for indole formation in Zea mays: A structure-activity study with elicitor-active N-acyl glutamines from insects","volume":"65","author":"Frey","year":"2004","journal-title":"Phytochemistry"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"14801","DOI":"10.1073\/pnas.260499897","article-title":"An herbivore elicitor activates the gene for indole emission in maize","volume":"97","author":"Frey","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"eaar4767","DOI":"10.1126\/sciadv.aar4767","article-title":"An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars","volume":"4","author":"Ye","year":"2018","journal-title":"Sci. Adv."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"6273","DOI":"10.1038\/ncomms7273","article-title":"Indole is an essential herbivore-induced volatile priming signal in maize","volume":"6","author":"Erb","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2733","DOI":"10.1007\/s10886-006-9196-7","article-title":"The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps","volume":"32","author":"Held","year":"2006","journal-title":"J. Chem. Ecol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1007\/BF00989557","article-title":"Defensive secretions of New Zealand tenebrionids V. Presence of methyl ketones in Uloma tenebrionoides (Coleoptera: Tenebrionidae)","volume":"11","author":"Gnanasunderam","year":"1985","journal-title":"J. Chem. Ecol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e2215442119","DOI":"10.1073\/pnas.2215442119","article-title":"Sex pheromone communication in an insect parasitoid, Campoletis chlorideae Uchida","volume":"119","author":"Guo","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1007\/s10886-007-9300-7","article-title":"The Egg Parasitoid Trissolcus basalis uses n-nonadecane, a Cuticular Hydrocarbon from its Stink Bug Host Nezara viridula, to Discriminate Between Female and Male Hosts","volume":"33","author":"Colazza","year":"2007","journal-title":"J. Chem. Ecol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1007\/s10886-009-9692-7","article-title":"Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize","volume":"35","author":"Brunner","year":"2009","journal-title":"J. Chem. Ecol."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/3\/321\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,17]],"date-time":"2026-03-17T11:21:41Z","timestamp":1773746501000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/3\/321"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,3,16]]},"references-count":47,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2026,3]]}},"alternative-id":["insects17030321"],"URL":"https:\/\/doi.org\/10.3390\/insects17030321","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,3,16]]}}}