Non-target effects of ten essential oils on the egg parasitoid Trichogramma evanescens

10.24072/pcjournal.212 - Peer Community Journal, Volume 3 (2023), article no. e2.

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Essential oils (EOs) are increasingly used as biopesticides due to their insecticidal potential. This study addresses their non-target effects on a biological control agent: the egg parasitoid Trichogramma evanescens. In particular, we tested whether EOs affected parasitoid fitness either directly, by decreasing pre-imaginal survival, or indirectly, by disrupting parasitoids' orientation abilities. The effect of Anise, Fennel, Sweet orange, Basil, Coriander, Oregano, Peppermint, Mugwort, Rosemary and Thyme EOs were studied on five strains of T. evanescens. Specific experimental setups were developed, and data obtained from image analysis were interpreted with phenomenological models fitted with Bayesian inference. Results highlight the fumigant toxicity of EOs on parasitoid development. Anise, Fennel, Basil, Coriander, Oregano, Peppermint and Thyme EOs are particularly toxic and drastically reduce the emergence rate of T. evanescens. Most EOs also affect parasitoid behavior: (i) Basil, Coriander, Oregano, Peppermint, Mugwort and Thyme EOs are highly repellent for naive female parasitoids; (ii) Anise and Fennel EOs can have repellent or attractive effects depending on strains; and (iii) Sweet orange, Oregano and Rosemary EOs have no detectable impact on orientation behavior. This study shows that EOs fumigation have non-target effects on egg parasitoids. This highlights the need to cautiously precise the deployment framework of biopesticides in an agroecological perspective.

Published online:
DOI: 10.24072/pcjournal.212
van Oudenhove, Louise 1; Cazier, Aurélie 1; Fillaud, Marine 1; Lavoir, Anne-Violette 1; Fatnassi, Hicham 1, 2; Perez, Guy 1; Calcagno, Vincent 1

1 Institut Sophia Agrobiotech, INRAE, Université Côte d'Azur, CNRS, France
2 International Center for Biosaline Agriculture, Dubai, United Arab Emirates
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {van Oudenhove, Louise and Cazier, Aur\'elie and Fillaud, Marine and Lavoir, Anne-Violette and Fatnassi, Hicham and Perez, Guy and Calcagno, Vincent},
     title = {Non-target effects of ten essential oils on the egg parasitoid {\protect\emph{Trichogramma} evanescens}},
     journal = {Peer Community Journal},
     eid = {e2},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
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%A Cazier, Aurélie
%A Fillaud, Marine
%A Lavoir, Anne-Violette
%A Fatnassi, Hicham
%A Perez, Guy
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van Oudenhove, Louise; Cazier, Aurélie; Fillaud, Marine; Lavoir, Anne-Violette; Fatnassi, Hicham; Perez, Guy; Calcagno, Vincent. Non-target effects of ten essential oils on the egg parasitoid Trichogramma evanescens. Peer Community Journal, Volume 3 (2023), article  no. e2. doi : 10.24072/pcjournal.212. https://peercommunityjournal.org/articles/10.24072/pcjournal.212/

Peer reviewed and recommended by PCI : 10.24072/pci.zool.100124

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agarwal, M.; Walia, S.; Dhingra, S.; Khambay, B. P. Insect growth inhibition, antifeedant and antifungal activity of compounds isolated/derived from Zingiber officinale Roscoe (ginger) rhizomes, Pest Management Science, Volume 57 (2001) no. 3, pp. 289-300 | DOI

[2] Akhtar, Y.; Yeoung, Y.-R.; Isman, M. B. Comparative bioactivity of selected extracts from Meliaceae and some commercial botanical insecticides against two noctuid caterpillars, Trichoplusia ni and Pseudaletia unipuncta, Phytochemistry Reviews, Volume 7 (2007) no. 1, pp. 77-88 | DOI

[3] Alcántara-de la Cruz, R.; Parreira, D. S.; Dimaté, F. A. R.; Batista, L. D.; Ribeiro, R. C.; Zanuncio, J. C. Effects of essential oils on biological attributes of Trichogramma galloi adults, Journal of Asia-Pacific Entomology, Volume 24 (2021) no. 2, pp. 64-67 | DOI

[4] Altieri, M. A.; Annamalai, S.; Katiyar, K. P.; Flath, R. A. Effects of plant extracts on the rates of parasitization ofAnagasta kuehniella [Lep.: Pyralidae] eggs by Trichogramma pretiosum [Hym.: Trichogrammatidae] under greenhouse conditions, Entomophaga, Volume 27 (1982) no. 4, pp. 431-437 | DOI

[5] Amichot, M.; Joly, P.; Martin-Laurent, F.; Siaussat, D.; Lavoir, A.-V. Biocontrol, new questions for Ecotoxicology?, Environmental Science and Pollution Research, Volume 25 (2018) no. 34, pp. 33895-33900 | DOI

[6] Ananthakrishnan, T. N.; Senrayan, R.; Murugesan, S.; Annadurai, R. S. Kairomones ofheliothis armigera andcorcyra cephalonica and their influence on the parasitic potential oftrichogramma chilonis (Trichogrammatidae: hymenoptera), Journal of Biosciences, Volume 16 (1991) no. 3, pp. 111-119 | DOI

[7] Araújo, C. V. M.; Laissaoui, A.; Silva, D. C. V. R.; Ramos-Rodríguez, E.; González-Ortegón, E.; Espíndola, E. L. G.; Baldó, F.; Mena, F.; Parra, G.; Blasco, J.; López-Doval, J.; Sendra, M.; Banni, M.; Islam, M. A.; Moreno-Garrido, I. Not Only Toxic but Repellent: What Can Organisms’ Responses Tell Us about Contamination and What Are the Ecological Consequences When They Flee from an Environment?, Toxics, Volume 8 (2020) no. 4 | DOI

[8] Bai, S.-X.; Wang, Z.-Y.; He, K.-L.; Im, D.-J. Olfactory Response of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) to Volatiles Emitted by Mungbean Plants, Agricultural Sciences in China, Volume 10 (2011) no. 4, pp. 560-565 | DOI

[9] Baricevic, C.; Milevoj, L.; Borstnik, J. Insecticidal effect of oregano (Origanum vulgare L. ssp. hirtum Ietswaart) on bean weevil (Acanthoscelides obtectus Say), International Journal of Horticultural Science, Volume 7 (2001) no. 2 | DOI

[10] Bedini, S.; et al. Repellency of anethole-and estragole-type fennel essential oils against stored grain pests: the different twins, Bull Insectol, Volume 69 (2016), pp. 149-157

[11] Boo, K.; Yang, J. Olfactory Response of Trichogramma chilonis to Capsicum annuum, Journal of Asia-Pacific Entomology, Volume 1 (1998) no. 2, pp. 123-129 | DOI

[12] Burte, V.; Perez, G.; Ayed, F.; Groussier, G.; Mailleret, L.; van Oudenhove, L.; Calcagno, V. Up and to the light: intra- and interspecific variability of photo- and geo-tactic oviposition preferences in genus Trichogramma, Peer Community Journal, Volume 2 (2022) | DOI

[13] Cherry, R. Attraction of the Lovebug, Plecia nearctica (Diptera: Bibionidae) to Anethole, The Florida Entomologist, Volume 81 (1998) no. 4 | DOI

[14] Cloyd, R. A.; Galle, C. L.; Keith, S. R.; Kalscheur, N. A.; Kemp, K. E. Effect of Commercially Available Plant-Derived Essential Oil Products on Arthropod Pests, Journal of Economic Entomology, Volume 102 (2009) no. 4, pp. 1567-1579 | DOI

[15] Consoli, F.; et al. Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma, Springer Netherlands, Dordrecht, 2010 | DOI

[16] Corey, D. T. The determinants of exploration and neophobia, Neuroscience & Biobehavioral Reviews, Volume 2 (1978) no. 4, pp. 235-253 | DOI

[17] Corrigan, J. E.; Laing, J. E.; Zubricky, J. S. Effects of Parasitoid to Host Ratio and Time of Day of Parasitism on Development and Emergence of Trichogramma minutum (Hymenoptera: Trichogrammatidae) Parasitizing Eggs of Ephestia kuehniella (Lepidoptera: Pyralidae), Annals of the Entomological Society of America, Volume 88 (1995) no. 6, pp. 773-780 | DOI

[18] Dunan, L.; Malanga, T.; Bearez, P.; Benhamou, S.; Monticelli, L. S.; Desneux, N.; Michel, T.; Lavoir, A.-V. Biopesticide Evaluation from Lab to Greenhouse Scale of Essential Oils Used against Macrosiphum euphorbiae, Agriculture, Volume 11 (2021) no. 9 | DOI

[19] Fatouros, N. E.; Bukovinszkine’Kiss, G.; Kalkers, L. A.; Gamborena, R. S.; Dicke, M.; Hilker, M. Oviposition‐induced plant cues: do they arrest <i>Trichogramma</i> wasps during host location?, Entomologia Experimentalis et Applicata, Volume 115 (2005) no. 1, pp. 207-215 | DOI

[20] Fatouros, N. E.; Lucas-Barbosa, D.; Weldegergis, B. T.; Pashalidou, F. G.; van Loon, J. J. A.; Dicke, M.; Harvey, J. A.; Gols, R.; Huigens, M. E. Plant Volatiles Induced by Herbivore Egg Deposition Affect Insects of Different Trophic Levels, PLoS ONE, Volume 7 (2012) no. 8 | DOI

[21] Frenoy, C.; Durier, C.; Hawlitzky, N. Effect of kairomones from egg and female adult stages of Ostrinia nubilalis (Hübner) (Lepidoptera, Pyralidae) on Trichogramma brassicae Bezdenko (Hymenoptera, Trichogrammatidae) female kinesis, Journal of Chemical Ecology, Volume 18 (1992) no. 5, pp. 761-773 | DOI

[22] Geetha, N. Recognition of native host volatiles by laboratory reared Trichogramma chilonis Ishii, Journal of Biological Control, Volume 24 (2010), pp. 126-132 | DOI

[23] González, J. O. W.; Laumann, R. A.; da Silveira, S.; Moraes, M. C. B.; Borges, M.; Ferrero, A. A. Lethal and sublethal effects of four essential oils on the egg parasitoids Trissolcus basalis, Chemosphere, Volume 92 (2013) no. 5, pp. 608-615 | DOI

[24] Haddi, K.; Turchen, L. M.; Viteri Jumbo, L. O.; Guedes, R. N.; Pereira, E. J.; Aguiar, R. W.; Oliveira, E. E. Rethinking biorational insecticides for pest management: unintended effects and consequences, Pest Management Science, Volume 76 (2020) no. 7, pp. 2286-2293 | DOI

[25] Hassan, S. A. The mass rearing and utilization of <i>Trichogramma</i> to control lepidopterous pests: Achievements and outlook, Pesticide Science, Volume 37 (1993) no. 4, pp. 387-391 | DOI

[26] Hori, M. Repellency of rosemary oil against Myzus persicae in a laboratory and in a screen-house, Journal of Chemical Ecology, Volume 24 (1998) no. 9, pp. 1425-1432 | DOI

[27] Ikbal, C.; Pavela, R. Essential oils as active ingredients of botanical insecticides against aphids, Journal of Pest Science, Volume 92 (2019) no. 3, pp. 971-986 | DOI

[28] Ilboudo, Z. Activité Biologique de quatre huiles essentielles contre Callosobruchus maculatus Fab.(Coleoptera: Bruchidae), insecte ravageur des stocks de niébé au Burkina Faso., PhD thesis, Université de Ouagadougou, 2009

[29] Ion Scotta, M. Distributions des espèces du genre Trichogramma le long d’un gradient altitudinal et adaptations locales aux basses températures chez l’espèce Trichogramma cacoeciae, PhD thesis, Université Côte d’Azur (ComUE), 2019

[30] Isikber, A. A.; Alma, M. H.; Kanat, M.; Karci, A. Fumigant toxicity of essential oils from Laurus nobilis and Rosmarinus officinalis against all life stages of Tribolium confusum, Phytoparasitica, Volume 34 (2006) no. 2, pp. 167-177 | DOI

[31] Isman, M. B. Botanical Insecticides in the Twenty-First Century—Fulfilling Their Promise?, Annual Review of Entomology, Volume 65 (2020) no. 1, pp. 233-249 | DOI

[32] Isman, M. B.; Wilson, J. A.; Bradbury, R. Insecticidal Activities of Commercial Rosemary Oils (<i>Rosmarinus officinalis</i>) Against Larvae of <i>Pseudaletia unipuncta</i> and <i>Trichoplusia ni</i> in Relation to Their Chemical Compositions, Pharmaceutical Biology, Volume 46 (2008) no. 1-2, pp. 82-87 | DOI

[33] Jankowska, M.; Rogalska, J.; Wyszkowska, J.; Stankiewicz, M. Molecular Targets for Components of Essential Oils in the Insect Nervous System—A Review, Molecules, Volume 23 (2017) no. 1 | DOI

[34] Kaiser, L. Plasticité comportementale et rôle des médiateurs chimiques dans la sélection de l’hôte par Trichogramma Maidis Pint. Et Voeg.: (hym. Trichogrammatidae), PhD thesis, Paris 11, 1988

[35] Kaiser, L.; Pham-Delegue, M. H.; Bakchine, E.; Masson, C. Olfactory responses of Trichogramma maidis Pint, et Voeg.: Effects of chemical cues and behavioral plasticity, Journal of Insect Behavior, Volume 2 (1989) no. 5, pp. 701-712 | DOI

[36] Karolkowski, A.; Guichard, E.; Briand, L.; Salles, C. Volatile Compounds in Pulses: A Review, Foods, Volume 10 (2021) no. 12 | DOI

[37] Khan, Z.; Hassanali, A.; Pickett, J. Managing Polycropping to Enhance Soil System, Biological Approaches to Sustainable Soil Systems, CRC Press, 2006, pp. 575-586 | DOI

[38] Khedr, M.; El-Kawas, H. Control of Spodoptera littoralis (Boisd.) (Lepidoptera:Noctuidae) and Tetranychus urticae Koch (Acari:Tetranychidae) by Coriander Essential Oil, Journal of Entomology, Volume 10 (2013) no. 4, pp. 170-181 | DOI

[39] Kumar, P.; Mishra, S.; Malik, A.; Satya, S. Repellent, larvicidal and pupicidal properties of essential oils and their formulations against the housefly, Musca domestica, Medical and Veterinary Entomology, Volume 25 (2011) no. 3, pp. 302-310 | DOI

[40] Köhler, H.-R.; Triebskorn, R. Wildlife Ecotoxicology of Pesticides: Can We Track Effects to the Population Level and Beyond?, Science, Volume 341 (2013) no. 6147, pp. 759-765 | DOI

[41] Lewis, W. J.; Jones, R. L.; Nordlund, D. A.; Sparks, A. N. Kairomones and their use for management of entomophagous insects: I. Evaluation for increasing rates of parasitization by Trichogramma spp. in the field, Journal of Chemical Ecology, Volume 1 (1975) no. 3, pp. 343-347 | DOI

[42] Mills, C.; Cleary, B. V.; Walsh, J. J.; Gilmer, J. F. Inhibition of acetylcholinesterase by Tea Tree oil, Journal of Pharmacy and Pharmacology, Volume 56 (2004) no. 3, pp. 375-379 | DOI

[43] Milonas, P. G.; Martinou, A. F.; Kontodimas, D. C.; Karamaouna, F.; Konstantopoulou, M. A. Attraction of Different <i>Trichogramma</i> Species to <i>Prays oleae</i> Sex Pheromone, Annals of the Entomological Society of America, Volume 102 (2009) no. 6, pp. 1145-1150 | DOI

[44] Morey, R. A.; Khandagle, A. J. Bioefficacy of essential oils of medicinal plants against housefly, Musca domestica L., Parasitology Research, Volume 111 (2012) no. 4, pp. 1799-1805 | DOI

[45] Mossa, A.-T. H. Green Pesticides: Essential Oils as Biopesticides in Insect-pest Management, Journal of Environmental Science and Technology, Volume 9 (2016) no. 5, pp. 354-378 | DOI

[46] Nerio, L. S.; Olivero-Verbel, J.; Stashenko, E. Repellent activity of essential oils: A review, Bioresource Technology, Volume 101 (2010) no. 1, pp. 372-378 | DOI

[47] Noldus, L. P. J. J.; Lewis, W. J.; Tumlinson, J. H. Beneficial arthropod behavior mediated by airborne semiochemicals. IX. Differential response of Trichogramma pretiosum, an egg parasitoid of Heliothis zea, to various olfactory cues, Journal of Chemical Ecology, Volume 16 (1990) no. 12, pp. 3531-3544 | DOI

[48] Parreira, D. S.; Alcántara-de la Cruz, R.; Leite, G. L. D.; Ramalho, F. d. S.; Zanuncio, J. C.; Serrão, J. E. Quantifying the harmful potential of ten essential oils on immature Trichogramma pretiosum stages, Chemosphere, Volume 199 (2018), pp. 670-675 | DOI

[49] Parreira, D. S.; Alcántara-de la Cruz, R.; Rodrigues Dimaté, F. A.; Batista, L. D.; Ribeiro, R. C.; Rigueira Ferreira, G. A.; Zanuncio, J. C. Bioactivity of ten essential oils on the biological parameters of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) adults, Industrial Crops and Products, Volume 127 (2019), pp. 11-15 | DOI

[50] Parreira, D. S.; Alcántara-de la Cruz, R.; Zanuncio, J. C.; Lemes, P. G.; da Silva Rolim, G.; Barbosa, L. R.; Leite, G. L. D.; Serrão, J. E. Essential oils cause detrimental effects on biological parameters of Trichogramma galloi immatures, Journal of Pest Science, Volume 91 (2017) no. 2, pp. 887-895 | DOI

[51] Pavela, R.; Benelli, G. Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints, Trends in Plant Science, Volume 21 (2016) no. 12, pp. 1000-1007 | DOI

[52] Perez, G.; Burte, V.; Baron, O.; Calcagno, V. Une méthode d’analyse d’image automatique pour quantifier rapidement les nombres d’œufs et les taux de parasitisme chez Trichogramma sp., Cahiers techniques de l’INRA. Innovations entomologiques: du laboratoire au champ, 2017, pp. 135-142

[53] Pettersson, J. An Aphid Sex Attractant, Insect Systematics & Evolution, Volume 1 (1970) no. 1, pp. 63-73 | DOI

[54] Peñaflor, M. F. G. V.; Erb, M.; Miranda, L. A.; Werneburg, A. G.; Bento, J. M. S. Herbivore-Induced Plant Volatiles Can Serve as Host Location Cues for a Generalist and a Specialist Egg Parasitoid, Journal of Chemical Ecology, Volume 37 (2011) no. 12, pp. 1304-1313 | DOI

[55] Pintureau, B. La lutte biologique et les Trichogrammes: Application au contrôle de la pyrale du maïs, Editions Le Manuscrit, 2009

[56] Plummer, M. rjags: Bayesian graphical models using mcmc, R package version 1.0.3-12, 2009 (http://CRAN.R-project.org/package=rjags)

[57] Poorjavad, N.; Goldansaz, S. H.; Dadpour, H.; khajehali, J. Effect of Ferula assafoetida essential oil on some biological and behavioral traits of Trichogramma embryophagum and T. evanescens, BioControl, Volume 59 (2014) no. 4, pp. 403-413 | DOI

[58] Price, P. W. Evolutionary Strategies of Parasitic Insects and Mites, Springer US, Boston, MA, 1975 | DOI

[59] R Core Team R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2020

[60] Rani, P. U.; Kumari, S. I.; Sriramakrishna, T.; Sudhakar, T. R. Kairomones Extracted from Rice Yellow Stem Borer and their Influence on Egg Parasitization by Trichogramma Japonicum Ashmead, Journal of Chemical Ecology, Volume 33 (2007) no. 6, p. 1297-1297 | DOI

[61] Rani, P. U.; Sandhyarani, K. Specificity of systemically released rice stem volatiles on egg parasitoid, <i>Trichogramma japonicum</i> Ashmead behaviour, Journal of Applied Entomology, Volume 136 (2012) no. 10, pp. 749-760 | DOI

[62] Regnault-Roger, C. The potential of botanical essential oils for insect pest control, Integrated Pest Management Reviews, Volume 2 (1997) no. 1, pp. 25-34 | DOI

[63] Regnault-Roger, C.; Vincent, C.; Arnason, J. T. Essential Oils in Insect Control: Low-Risk Products in a High-Stakes World, Annual Review of Entomology, Volume 57 (2012) no. 1, pp. 405-424 | DOI

[64] Renou, M.; Nagnan, P.; Berthier, A.; Durier, C. Identification of compounds from the eggs of Ostrinia nubilalis and Mamestra brassicae having kairomone activity on Trichogramma brassicae, Entomologia Experimentalis et Applicata, Volume 63 (1992) no. 3, pp. 291-303 | DOI

[65] Ris, N.; Groussier, G.; Sellier, N.; Marchand, A.; Warot, S. Brc “egg parasitoids collection"(epcoll), Portail Data INRAE, 2018

[66] Rodrigues, V. M.; Rosa, P. T. V.; Marques, M. O. M.; Petenate, A. J.; Meireles, M. A. A. Supercritical Extraction of Essential Oil from Aniseed (<i>Pimpinella anisum</i> L) Using CO<sub>2</sub>:  Solubility, Kinetics, and Composition Data, Journal of Agricultural and Food Chemistry, Volume 51 (2003) no. 6, pp. 1518-1523 | DOI

[67] Romeis, J.; Shanower, T. G.; Zebitz, C. P. W. Volatile Plant Infochemicals Mediate Plant Preference of Trichogramma chilonis, Journal of Chemical Ecology, Volume 23 (1997) no. 11, pp. 2455-2465 | DOI

[68] Ryan, M. F.; Byrne, O. Plant-insect coevolution and inhibition of acetylcholinesterase, Journal of Chemical Ecology, Volume 14 (1988) no. 10, pp. 1965-1975 | DOI

[69] Saeidi, M.; et al. Insecticidal and repellent activities of Citrus reticulata, Citrus limon and Citrus aurantium essential oils on Callosobruchus maculatus, IOBC/WPRS Bulletin, Volume 69 (2011), pp. 289-293

[70] Sampson, B. J.; Tabanca, N.; Kirimer, N.; Demirci, B.; Baser, K. H. C.; Khan, I. A.; Spiers, J. M.; Wedge, D. E. Insecticidal activity of 23 essential oils and their major compounds against adultLipaphis pseudobrassicae (Davis) (Aphididae: Homoptera), Pest Management Science, Volume 61 (2005) no. 11, pp. 1122-1128 | DOI

[71] Sanei-Dehkordi, A.; et al. Chemical compositions of the peel essential oil of Citrus aurantium and its natural larvicidal activity against the malaria vector Anopheles stephensi (Diptera: Culicidae) in comparison with Citrus paradisi, Journal of arthropod-borne diseases, Volume 10 (2016), p. 577

[72] Saroukolai, A. T.; Nouri-Ganbalani, G.; Hadian, J.; Rafiee-Dastjerdi, H. Antifeedant activity and toxicity of some plant essential oils to Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), Plant Protection Science, Volume 50 (2014) no. No. 4, pp. 207-216 | DOI

[73] Saxena, K. N.; Basit, A. Inhibition of oviposition by volatiles of certain plants and chemicals in the leafhopper Amrasca devastons (distant), Journal of Chemical Ecology, Volume 8 (1982) no. 2, pp. 329-338 | DOI

[74] Schindelin, J.; Arganda-Carreras, I.; Frise, E.; Kaynig, V.; Longair, M.; Pietzsch, T.; Preibisch, S.; Rueden, C.; Saalfeld, S.; Schmid, B.; Tinevez, J.-Y.; White, D. J.; Hartenstein, V.; Eliceiri, K.; Tomancak, P.; Cardona, A. Fiji: an open-source platform for biological-image analysis, Nature Methods, Volume 9 (2012) no. 7, pp. 676-682 | DOI

[75] Schneider, C. A.; Rasband, W. S.; Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis, Nature Methods, Volume 9 (2012) no. 7, pp. 671-675 | DOI

[76] Schöller, M.; Prozell, S. Response of Trichogramma evanescens to the main sex pheromone component of Ephestia spp. and Plodia interpunctella, (Z,E)-9,12-tetra-decadenyl acetate (ZETA), Journal of Stored Products Research, Volume 38 (2002) no. 2, pp. 177-184 | DOI

[77] Sehari, N. H.; Hellal, B.; Sehari, M.; Maatoug, M. Insecticide effect of pennyroyal and rosemary essential oils on the rice weevil, Ukrainian Journal of Ecology, Volume 8 (2018) no. 1, pp. 696-702 | DOI

[78] Siviter, H.; Muth, F. Do novel insecticides pose a threat to beneficial insects?, Proceedings of the Royal Society B: Biological Sciences, Volume 287 (2020) no. 1935 | DOI

[79] Sousa, R. M. O.; Cunha, A. C.; Fernandes-Ferreira, M. The potential of Apiaceae species as sources of singular phytochemicals and plant-based pesticides, Phytochemistry, Volume 187 (2021) | DOI

[80] Spiegelhalter, D. J.; Best, N. G.; Carlin, B. P.; van der Linde, A. Bayesian measures of model complexity and fit, Journal of the Royal Statistical Society: Series B (Statistical Methodology), Volume 64 (2002) no. 4, pp. 583-639 | DOI

[81] Su, Y.-S.; Yajima, M. R2jags: Using R to Run ‘JAGS’, R package version 0.5-7, 2015

[82] Szczepanik, M.; et al. Insecticidal activities of Thymus vulgaris essential oil and its components (thymol and carvacrol) against larvae of lesser mealworm, Alphitobius diaperinus Panzer (Coleoptera: Tenebrionidae), Allelopathy Journal, Volume 30 (2012), pp. 129-142

[83] Tamò, C.; Held, M.; Davison, A.; Ricard, I.; Turlings, T. A comparison of naïve and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours, Animal Biology, Volume 56 (2006) no. 2, pp. 205-220 | DOI

[84] Tsuneya, T.; Ishihara, M.; Shiota, H.; Shiga, M. Volatile components of quince fruit (Cydonia oblonga Mill.), Agricultural and Biological Chemistry, Volume 47 (1983) no. 11, pp. 2495-2502 | DOI

[85] Turek, C.; Stintzing, F. C. Stability of Essential Oils: A Review, Comprehensive Reviews in Food Science and Food Safety, Volume 12 (2013) no. 1, pp. 40-53 | DOI

[86] Tóth, M.; Klein, M. G.; Imrei, Z. Field Screening for Attractants of Scarab (Coleoptera: Scarabaeidae) Pests in Hungary, Acta Phytopathologica et Entomologica Hungarica, Volume 38 (2003) no. 3-4, pp. 323-331 | DOI

[87] Van Oudenhove, L.; Cazier, A.; et al. Non-target effects of ten essential oils on the egg-parasitoid Trichogramma evanescens, bioRxiv (2022) | DOI

[88] Van Oudenhove, L. Non-target effects of ten essential oils on the egg-parasitoid Trichogramma evanescens [dataset], 2022 | DOI

[89] Vet, L. E. M.; Dicke, M. Ecology of Infochemical Use by Natural Enemies in a Tritrophic Context, Annual Review of Entomology, Volume 37 (1992) no. 1, pp. 141-172 | DOI

[90] Vet, L. E. M.; Lenteren, J. C. V.; Heymans, M.; Meelis, E. An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects, Physiological Entomology, Volume 8 (1983) no. 1, pp. 97-106 | DOI

[91] Vital, R.; et al. Evaluation de l’intérêt de l’utilisation d’huiles essentielles dans des stratégies de protection des cultures, Innovations Agronomiques, Volume 63 (2018), pp. 1-20 | DOI

[92] Volkoff, A.-N.; Daumal, J.; Barry, P.; François, M.-C.; Hawlitzky, N.; Rossi, M. M. Development of Trichogramma cacoeciae Marchal (Hymenoptera : Trichogrammatidae): time table and evidence for a single larval instar, International Journal of Insect Morphology and Embryology, Volume 24 (1995) no. 4, pp. 459-466 | DOI

[93] Vos, M. Linking foraging behavior to lifetime reproductive success for an insect parasitoid: adaptation to host distributions, Behavioral Ecology, Volume 14 (2003) no. 2, pp. 236-245 | DOI

[94] Wajnberg, E.; Colazza, S. Chemical ecology of insect parasitoids, John Wiley & Sons, 2013

[95] Wang, J.; Zhu, F.; Zhou, X.; Niu, C.; Lei, C. Repellent and fumigant activity of essential oil from Artemisia vulgaris to Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), Journal of Stored Products Research, Volume 42 (2006) no. 3, pp. 339-347 | DOI

[96] Werrie, P.-Y.; Durenne, B.; Delaplace, P.; Fauconnier, M.-L. Phytotoxicity of Essential Oils: Opportunities and Constraints for the Development of Biopesticides. A Review, Foods, Volume 9 (2020) no. 9 | DOI

[97] Wickham, H. ggplot2, Use R!, Springer International Publishing, Cham, 2016 | DOI

[98] Wilson, J. K.; Woods, H. A. Innate and Learned Olfactory Responses in a Wild Population of the Egg Parasitoid <i>Trichogramma</i> (Hymenoptera: Trichogrammatidae), Journal of Insect Science, Volume 16 (2016) no. 1 | DOI

[99] van Lenteren, J. C. The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake, BioControl, Volume 57 (2011) no. 1, pp. 1-20 | DOI

[100] van Oudenhove, L.; Mailleret, L.; Fauvergue, X. Infochemical use and dietary specialization in parasitoids: a meta-analysis, Ecology and Evolution, Volume 7 (2017) no. 13, pp. 4804-4811 | DOI

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