Selectivity and effects of essential oils on the egg parasitoid Telenomus remus (Nixon, 1937) (Hymenoptera: Scelionidae) reared on Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) and Corcyra cephalonica (Stainton, 1866) (Lepidoptera: Pyralidae)

Marina O. Marabesi; João P. A. Bomfim; Regiane C. Oliveira

doi:10.37486/1809-8460.ba21005

Authors

Marina O. Marabesi Universidade Estadual Paulista, Botucatu, São Paulo, Brazil https://orcid.org/0000-0001-8298-4979
João P. A. Bomfim Universidade Estadual Paulista, Botucatu, São Paulo, Brazil https://orcid.org/0000-0001-6292-2439
Regiane C. Oliveira Universidade Estadual Paulista, Botucatu, São Paulo, Brazil https://orcid.org/0000-0002-6210-8231

DOI:

https://doi.org/10.37486/1809-8460.ba21005

Keywords:

Fall armyworm, Rice moth, Biological control, Botanical extracts, Integrated Pest Management

Abstract

Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae) is a polyphagous and cosmopolitan pest that damages economically important crops. Efficient management requires integrated strategies, with emphasis on biological control. Telenomus remus (Nixon, 1937) (Hymenoptera: Scelionidae) is an egg parasitoid of Spodoptera spp., but it can also develop in other lepidopterans, such as Corcyra cephalonica (Stainton, 1866) (Lepidoptera: Pyralidae), making it a promising alternative host. The effectiveness of biological control depends on its compatibility with other tactics, such as essential oils (EOs) with insecticidal properties. This study evaluated the selectivity and effects of Syzygium aromaticum (L.) Merr. & L.M.Perry, Cymbopogon citratus DC. Stapf., Schinus terebinthifolius Raddi, Cordia verbenacea DC., Baccharis dracunculifolia DC., and Callistemon viminalis (Sol. ex Gaertn.) G. Don. EOs on T. remus reared on S. frugiperda and C. cephalonica. The longevity and parasitism of the parental and F1 generations, and the emergence rate and sex ratio of F1 and F2 generations, were assessed. Toxicity was classified according to IOBC standards. Baccharis dracunculifolia, C. citratus, and S. aromaticum showed selectivity for F1 parasitism, but not for the parental generation. Except for B. dracunculifolia, all oils were selective for F1 emergence in S. frugiperda. The longevity of parasitoids reared on C. cephalonica was lower than that observed in S. frugiperda. In the adult stage, S. terebinthifolius, C. verbenacea, C. viminalis, and C. citratus exhibited selectivity for T. remus reared on S. frugiperda, whereas in C. cephalonica, only C. viminalis was selective. No effects were observed on F2 parameters. The results indicate the potential for integrating the use of EOs with T. remus in the management of S. frugiperda.

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References

Alves, K. F.; Caetano, F. H.; Pereira Garcia, I. J.; Santos, H. L.; Silva, D. B.; Siqueira, J. M.; Tanaka, A. S.; Alves, S. N. (2018) Baccharis dracunculifolia (Asteraceae) essential oil toxicity to Culex quinquefasciatus (Culicidae). Environmental Science and Pollution Research, 25(31): 31718–31726. doi: 10.1007/s11356-018-3149-x

Angon, P. B., Mondal, S., Jahan, I., Datto, M., Antu, U. B., Ayshi, F. J., Islam, M. S. (2023) Integrated pest management (IPM) in agriculture and its role in maintaining ecological balance and biodiversity. Advances in Agriculture, 2023: 5546373. doi: 10.1155/2023/5546373

Bernardi, E. B.; Haddad, M. D. L.; Parra, J. R. P. (2000) Comparison of artificial diets for rearing Corcyra cephalonica (Stainton, 1865) (Lep., Pyralidae) for Trichogramma mass production. Revista Brasileira de Biologia, 60(1): 45-52. doi: 10.1590/s0034-71082000000100007

Bomfim, J. P. A.; da Silva, N. N. P., da Silva, C. B.; Amaral, J. C.; das Graças Fernandes da Silva, M. F.; Bonfim, F. P. G.; de Oliveira, R. C. (2025) Compatibility of Cymbopogon citratus (DC.) Stapf (Poaceae) essential oil with egg parasitoids for the control of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). Phytoparasitica, 53(1): 2. doi: 10.1007/s12600-024-01223-w

Brügger, B. P.; Martínez, L. C.; Plata-Rueda, A.; Castro, B. M. D. C. E.; Soares, M. A.; Wilcken, C. F.; Carvalho, A. G.; Serrão, J. E.; Zanuncio, J. C. (2019) Bioactivity of the Cymbopogon citratus (Poaceae) essential oil and its terpenoid constituents on the predatory bug, Podisus nigrispinus (Heteroptera: Pentatomidae). Scientific Reports, 9(1): 8358. doi: 10.1038/s41598-019-44709-y

Carvalho, G. A.; Godoy, M. S.; Parreira, D. S.; Lasmar, O.; Souza, J. R.; Moscardini, V. F. (2010) Selectivity of growth regulators and neonicotinoids for adults of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Revista Colombiana de Entomologia, 36(2): 195-201. 10.25100/socolen.v36i2.9144

Chaaban, A.; Martins, C. E. N.; Bretanha, L. C.; Micke, G. A.; Carrer, A. R.; Rosa, N. F.; Ferreira, L.; Molento, M. B. (2018) Insecticide activity of Baccharis dracunculifolia essential oil against Cochliomyia macellaria (Diptera: Calliphoridae). Natural Product Research, 32(24): 2954-2958. doi: 10.1080/14786419.2017.1392947

Cruz, G. S.; Wanderley-Teixeira, V.; Oliveira, J. V.; Correia, A. A.; Breda, M. O.; Alves, T. J. S.; Cunha, F. M.; Teixeira, A. A. C.; Dutra, K. A.; Navarro, D. M. A. F. (2014) Bioactivity of Piper hispidinervum (Piperales: Piperaceae) and Syzygium aromaticum (Myrtales: Myrtaceae) oils, with or without formulated Bta on the biology and immunology of Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Economic Entomology, 107(1): 144-153. doi: 10.1603/ec13351

Fortes, A. D. R.; Coelho Jr, A.; Amorim, D. J.; Demetrio, C. G.; Parra, J. R. (2023) Biology and quality assessment of Telenomus remus (Hymenoptera: Scelionidae) and Trichogramma spp. (Hymenoptera: Trichogrammatidae) in eggs of Spodoptera spp. for augmentative biological control programs. Journal of Insect Science, 23(5): 5. doi: 10.1093/jisesa/iead047

Giraldi, G. T.; Zimmermann, R. C.; do Amaral, W.; Martins, C. E. N.; Schafaschek, A. M.; Maia, B. H. L. N.; dos Santos, E. F.; Mazarotto, E. J.; da Silva, M. A. N.; Foester, L. A. (2025) Toxicity of essential oils from Baccharis species on Spodoptera frugiperda and their selectivity to the parasitoid Telenomus remus. Journal of Pest Science, 98: 2247–2263. doi: 10.1007/s10340-025-01936-9

Glaudenucci, J.; Marasca, I.; Pernambuco Filho, J. C. A.; Bonfim, F. P. G.; Bueno, R. C. O. F. (2020) Selectivity and sublethal effects of botanical extracts to pupae of Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Journal of Experimental Agriculture International, 42(9): 136–146. doi: 10.9734/JEAI/2020/v42i930594

Greene, G. L.; Leppla, N. C.; Dickerson, W. A. (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. Journal of Economic Entomology, 69(4): 487-488. doi: 10.1093/jee/69.4.487

Guerra, I. C. D.; de Oliveira, P. D. L.; de Souza Pontes, A. L.; Lúcio, A. S. S. C.; Tavares, J. F.; Barbosa-Filho, J. M.; Madruga, M. S.; de Souza, E. L. (2015) Coatings comprising chitosan and Mentha piperita L. or Mentha villosa Huds essential oils to prevent common postharvest mold infections and maintain the quality of cherry tomato fruit. International Journal of Food Microbiology, 214: 168-178. doi: 10.1016/j.ijfoodmicro.2015.08.009

Hassan, E.; Obaidoon, Y.; Mostafiz, M. M.; Senior, L. (2023) Effect of plant essential oil formulations on Bemisia Tabaci MEAM1 (Gennadius) and its parasitoid Eretmocerus hayati (Zolnerowich and Rose). Plants, 12(24): 4137. doi: 10.3390/plants12244137

Hassan, S. A.; Halsall, N.; Gray, A. P.; Kuehner, C.; Moll, M.; Bakker, F. M.; Roembke, J.; Yousef, A.; Nasr, F.; Abdelgader, H. A. (2000) A laboratory method to evaluate the side effects of plant protection products on Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae). In: Candolfi, M. P.; Blümel, S.; Forster, R.; Bakker, F. M.; Grimm, C.; Hassan, S. A.; Heimbach, U.; Mead-Briggs, M.A.; Reber, B.; Schmuck, R.; Vogt, H. (Eds), Guidelines to evaluate side-effects of plant protection products to non-target arthropods, pp. 107-119. Reinheim: IOBC/WPRS.

Knaak, N.; Wiest, S. L.; Andreis, T. F.; Fiuza, L. M. (2013) Toxicity of essential oils to the larvae of Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Biopesticides, 6(1): 49.

Li, T. H.; de Freitas Bueno, A.; Desneux, N.; Zhang, L.; Wang, Z.; Dong, H.; Wang, S.; Zang, L. S. (2023) Current status of the biological control of the fall armyworm Spodoptera frugiperda by egg parasitoids. Journal of Pest Science, 96(4): 1345-1363. doi: 10.1007/s10340-023-01639-z

Lisi, F.; Siscaro, G.; Biondi, A.; Zappalà, L.; Ricupero, M. (2025) Non-target effects of bioinsecticides on natural enemies of arthropod pests. Current Opinion in Environmental Science & Health, 45: 100624. doi: 10.1016/j.coesh.2025.100624

Parra, J. R. P. (2019) Controle biológico na agricultura brasileira. Entomological Communications, 1: ec01002. doi: 10.37486/2675-1305.ec01002

Parreira, D. S.; Alcántara-de la Cruz, R.; Leite, G. L. D.; de Souza Ramalho, F.; Zanuncio, J. C.; Serrão, J. E. (2018b) Quantifying the harmful potential of ten essential oils on immature Trichogramma pretiosum stages. Chemosphere, 199: 670-675. doi: 10.1016/j.chemosphere.2018.02.083

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. (2018a) Essential oils cause detrimental effects on biological parameters of Trichogramma galloi immatures. Journal of Pest Science, 91(2): 887-895. doi: 10.1007/s10340-017-0945-x

Parreira, D. S.; Dimaté, F. A. R.; Batista, L. D.; Ribeiro, H. C. B.; Guanabens, R. E.; da Cunha, A. F.; Ribeiro, R. C. (2017) Efeito de óleos essenciais sobre estágios imaturos de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Ensaios e Ciência: Ciências Biológicas, Agrárias e da Saúde, 21(2): 80-85. doi: 10.17921/1415-6938.2017v21n2p80-85

Pomari-Fernandes, A.; Bueno, A. F.; Queiroz, A. P.; De Bortoli, S. A. (2015) Biological parameters and parasitism capacity of Telenomus remus Nixon (Hymenoptera: Platygastridae) reared on natural and factitious hosts for successive generations. African Journal of Agricultural Research, 10(33): 3225-3233. doi: 10.5897/AJAR2015.10154

Pratissoli, D.; Bueno, R. C. O. F.; Carvalho, J. R. (2019) O controle biológico. In: Pratissoli, D.; Bueno, R. C. O. F.; Carvalho, J.R. (Eds.), Trichogramma: da coleta à pesquisa aplicada, pp. 15-17. Alegre: Unicopy.

Priyanka, S. L.; Jeyarani, S.; Sathiah, N.; Mohankumar, S.; Nakkeeran, S. (2023) Influence of host egg age on parasitic potential of the entomophagous, Telenomus remus Nixon (Hymenoptera: Scelionidae) against the Fall armyworm, Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae) and investigations on the developmental biology and ultrastructure of egg parasitoid immature stages. Egyptian Journal of Biological Pest Control, 33(1): 26. doi: 10.1186/s41938-023-00676-1

Queiroz, A. P.; de Freitas Bueno, A.; Pomari-Fernandes, A.; Grande, M. L. M.; Bortolotto, O. C.; da Silva, D. M. (2017a) Quality control of Telenomus remus (Hymenoptera: Platygastridae) reared on the factitious host Corcyra cephalonica (Lepidoptera: Pyralidae) for successive generations. Bulletin of Entomological Research, 107(6): 791-798. doi: 10.1017/S000748531700030X

Queiroz, A. P.; Bueno, A. D. F.; Pomari-Fernandes, A.; Grande, M. L. M.; Bortolotto, O. C.; Silva, D. M. (2017b) Low temperature storage of Telenomus remus (Nixon) (Hymenoptera: Platygastridae) and its factitious host Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). Neotropical Entomology, 46(2): 182-192. doi: 10.1007/s13744-016-0442-6

Sampaio, I. B. M. (2002) Estatística aplicada à experimentação animal. 2ª. ed. Belo Horizonte: Fundação de Estudo e Pesquisa em Medicina Veterinária e Zootecnia.

Santana, E. D. R.; Thiesen, L. V.; Ribeiro, L. D. P.; Takahashi, T. A.; Parra, J. R. P.; Yamamoto, P. T. (2025) Harmful to Parents, Harmless to Offspring: Lethal and Transgenerational Effects of Botanical and Synthetic Insecticides on the Egg Parasitoid Trichogramma atopovirilia. Insects, 16(5): 493. doi: 10.3390/insects16050493

Şen, E.; Gençer, N. (2023) Effects of five essential oils on three generalist predators and two important whitefly parasitoids. Zemdirbyste, 110(3): 279-286. doi: 10.13080/z-a.2023.110.032

Sterk, G.; Hassan, S. A.; Baillod, M.; Bakker, F.; Bigler, F.; Blümel, S.; Bogenschütz, H.; Boller, E.; Bromand, B.; Brun, J., et al. (1999) Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group ‘Pesticides and Beneficial Organisms’. BioControl, 44(1): 99-117. doi: 10.1023/A:1009959009802

Tagliari, M. S.; Knaak, N.; Fiuza, L. M. (2010) Efeito de extratos de plantas na mortalidade de lagartas de Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae). Arquivos do Instituto Biológico, 77(2): 259-264. doi: 10.1590/1808-1657v77p2592010

Tang, Y.; Zou, Q.; Yu, G.; Liu, F.; Wu, Y.; Zhao, X.; Wang, W.; Liu, X.; Hu, F.; Wang, Z. (2025) Immunotranscriptomic profiling of Spodoptera frugiperda challenged by different pathogenic microorganisms. Insects, 16(4): 360. doi: 10.3390/insects16040360

Tirelli, A. A.; Alves, D. S.; Carvalho, G. A.; Sâmia, R. R.; Brum, S. S.; Guerreiro, M. C. (2010) Efeito de frações tânicas sobre parâmetros biológicos e nutricionais de Spodoptera frugiperda (Lepidoptera: Noctuidae). Ciência e Agrotecnologia, 34(6): 1417-1424. doi: 10.1590/s1413-70542010000600009

Zanuncio, J. C.; Mourão, S. A.; Martínez, L. C.; Wilcken, C. F.; Ramalho, F. S.; Plata-Rueda, A.; Soares, M. A.; Serrão, J. E. (2016) Toxic effects of the neem oil (Azadirachta indica) formulation on the stink bug predator, Podisus nigrispinus (Heteroptera: Pentatomidae). Scientific Reports, 6(1): 30261. doi: 10.1038/srep30261