Essential oil of Citrus aurantium var. dulcis: A new approach to control Diatraea saccharalis and Spodoptera eridania larvae
Resumo
Studies focusing on the potential use of botanical insecticides have increased significantly in recent years. Essential oils extracted from citrus fruit peels contain limonene, a monoterpene that is widely used in agricultural pest control studies. This study aimed to investigate the insecticidal properties of the essential oil of Citrus aurantium (L.) var. dulcis and analyze its effects on the midgut of Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae) and Spodoptera eridania (Stoll, 1782) (Lepidoptera: Noctuidae) neonate larvae. After essential oil dilution, five concentrations (0.06; 0.12; 0.25; 0.50 and 1.00%) were obtained and topically applied to the prothorax of larvae. Behavioral observations and larval mortality data were recorded every 24h for a duration of 120h. Midgut samples were collected 24 and 48h after the bioassays to perform histological and ultrastructural analyses. Both species exhibited low mobility, which progressed to paralysis after treatment, and mortality was only recorded in the first 48h. D. saccharalis and S. eridania larvae treated with 1.00% essential oil concentration had mortalities of 89 and 47%, respectively. The lethal concentrations (LC50) of essential oil have been estimated to be 0.50% (CI = 0.45–0.57%) for D. saccharalis and 1.06% (CI = 0.89–1.35%) for S. eridania. The histological and ultrastructural analyses revealed significant midgut damage, such as detachment of the muscle fibers from the basal region of the epithelium and spacing of columnar cells, which progressed to a complete degeneration of the epithelial cells. The negative effects of C. aurantium var. dulcis essential oil on D. saccharalis and S. eridania neonate larvae indicate its bioinsecticide potential. Our results suggest that this essential oil can be implemented in integrated pest management for sustainable crop production.
Downloads
Referências
Abdallah, M. S. I., Muhammad, I., & Warodi, F. A. (2017). Review on some plants as bio-pesticides. International Journal of Contemporary Research and Review, 8(7), 20186-20191. http://dx.doi.org/10.15520/ijcrr/2017/8/07/203
Anandakumar, P., Kamaraj, S., & Vanitha, M. K. (2021). D-limonene: a multifunctional compound with potent therapeutic effects. Journal of Food Biochemistry, 45(9), e13566. https://doi.org/10.1111/jfbc.13566
Araújo, J. R. (1987). Guia prático para a criação da broca da cana-de-açúcar e de seus parasitoides em laboratório. IAA/Planalsucar.
Arokiyaraj, C., Bhattacharyya, K., & Reddy, S. G. E. (2022). Toxicity and synergistic activity of compounds from essential oils and their effect on detoxification enzymes against Planococcus lilacinus. Frontiers in Plant Science, 13, 1-14. https://doi.org/10.3389/fpls.2022.1016737
Assadpour, E., Karaça, A. C., Fasamanesh, M., Mahdavi, S. A., Shariat-Alavi, M., Feng, J., Kharazmi, M. S., Rehman, A., & Jafari, S. M. (2023). Application of essential oils as natural biopesticides: recent advances. Critical Reviews in Food Science and Nutrition, 63(19), 6477-6497. https://doi.org/10.1080/10408398.2023.2170317
Assis, H. L. B., Paiva, P. E. B., Dinardo-Miranda, L. L., & Yamamoto, P. T. (2023). Estimating the relationship of sugarcane borer larvae and crop damage based on adult captures and climate variables. Scientia Agricola, 80, 1-8. https://doi.org/10.1590/1678-992X-2021-0274
Bowling, A. J., Sopko, M. S., Tan, S. Y., Larsen, C. M., Pence, H. E., & Zack, M. D. (2019). Insecticidal Activity of a Vip3Ab1 chimera is conferred by improved protein stability in the midgut of Spodoptera eridania. Toxins, 11(5), 1-17. https://doi.org/10.3390/toxins11050276
Braz, J. V. C., Carvalho, F. O., Meneses, D. V. C., Calixto, F. A. F., Santana, H. S. R., Almeida, I. B., Aquino, L. A. G., Araújo, A. A. S., & Serafini, M. R. (2021). Mechanism of action of limonene in tumor cells: a systematic review and meta-analysis. Current Pharmaceutical Design, 27(26), 2956-2965. https://doi.org/10.2174/1381612826666201026152902
Caballero-Gallardo, K., Scudeler, E. L., Santos, D. C., Stashenko, E. E., & Olivero-Verbel, J. (2023). Deleterious effects of Cymbopogon nardus (L.) essential oil on life cycle and midgut of the natural predator Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Insects, 14(4), 1-11. https://doi.org/10.3390/insects14040367
Caccia, S., Casartelli, M., & Tettamanti, G. (2019). The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell and Tissue Research, 377(3), 505-524. https://doi.org/10.1007/s00441-019-03076-w
Campolo, O., Giunti, G., Russo, A., Palmeri, V., & Zappalà, L. (2018). Essential oils in stored product insect pest control. Journal of Food Quality, 2018(906105), 1-18. https://doi.org/10.1155/2018/6906105
Corrêa, E. J. A., Carvalho, F. C., Oliveira, J. A. C., Bertolucci, S. K. V., Scotti, M. T., Silveira, C. H., Guedes, F. C., Melo, J. O. F., Melo-Minardi, R. C., & Lima, L. H. F. (2023). Elucidating the molecular mechanisms of essential oils’ insecticidal action using a novel cheminformatics protocol. Scientific Reports, 13(4598), 1-19. https://doi.org/10.1038/s41598-023-29981-3
Cruz, G. S., Wanderley-Teixeira, V., Oliveira, J. V., D’assunção, C. G., Cunha, F. M., Teixeira, Á. A., Guedes, C. A., Dutra, K. A., Barbosa, D. R., & Breda, M. O. (2017). Effect of trans-anethole, limonene and your combination in nutritional components and their reflection on reproductive parameters and testicular apoptosis in Spodoptera frugiperda (Lepidoptera: Noctuidae). Chemico-Biological Interactions, 263, 74-80. https://doi.org/10.1016/j.cbi.2016.12.013
Damascena, A. P., Santos, M. R., Costa, B. S., Soares, J. T., Peterle, A. B., Oliveira, C. M. R., & Pratissoli, D. (2023). D-limonene-based formulations for the management of Diaphania hyalinata, Plutella xylostella and Spodoptera eridania in a greenhouse. Revista Delos, 16(42), 219-230. https://doi.org/10.55905/rdelosv16.n42-016
Daquila, B. V., Scudeler, E. L., Dossi, F. C. A., Moreira, D. R., Pamphile, J. A., & Conte, H. (2019). Action of Bacillus thuringiensis (Bacillales: Bacillaceae) in the midgut of the sugarcane borer Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae). Ecotoxicology and Environmental Safety, 184, 109642. https://doi.org/10.1016/j.ecoenv.2019.109642
Dent, D., & Binks, R. H. (2020). Insect pest management. CABI.
Dhankhar, N., & Kumar, J. (2023). Impact of increasing pesticides and fertilizers on human health: A review. Materials Today: Proceedings, 72, 2202-2213. https://doi.org/10.1016/j.matpr.2023.03.766
Duque, J. E., Urbina, D. L., Vesga, L. C., Ortiz-Rodríguez, L. A., Vanegas, T. S., Stashenko, E. E., & Mendez-Sanchez, S. C. (2022). Insecticidal activity of essential oils from American native plants against Aedes aegypti (Diptera: Culicidae): an introduction to their possible mechanism of action. Scientific Reports, 13(2989), 1-15. https://doi.org/10.1038/s41598-023-30046-8
Eddin, L. B., Jha, N. K., Meeran, M. F. N., Kesari, K. K., Beiram, R., & Ojha, S. (2021). Neuroprotective potential of limonene and limonene containing natural products. Molecules, 26(15), 1-26. https://doi.org/10.3390/molecules26154535
Gadelhaq, S. M., Aboelhadid, S. M., Abdel-Baki, A.-A. S., Hassan, K. M., Arafa, W. M., Ibrahium, S. M., Al-Quraishy, S., Hassan, A. O., & El-Kareem, S. G. A. (2023). D-limonene nanoemulsion: lousicidal activity, stability, and effect on the cuticle of Columbicola columbae. Medical and Veterinary Entomology, 37(1), 63-75. https://doi.org/10.1111/mve.12607
González-Mas, M. C., Rambla, J. L., López-Gresa, M. P., Blázquez, M. A., & Granell, A. (2019). Volatile compounds in Citrus essential oils: A comprehensive review. Frontiers in Plant Science, 10(12), 1-18. https://doi.org/10.3389/fpls.2019.00012
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. https://doi.org/10.1093/jee/69.4.487
Hensley, S. D., & Hammond, A. H. (1968). Laboratory techniques for rearing the sugarcane borer on an artificial diet. Journal of Economic Entomology, 61(6), 1742-1743. https://doi.org/10.1093/jee/61.6.1742
IBM Corporation. (2017). IBM SPSS Statistics for Windows (Version 25.0). IBM. http://www.ibm.com
Inkscape. (1991). Inkscape Free Software Foundation Inc. Version 1.2.2. http://www.inkscape.org
Jain, P., Satapathy, T., & Pandey, R. K. (2021). Acaricidal activity and biochemical analysis of Citrus limetta seed oil for controlling ixodid tick Rhipicephalus microplus infesting cattle. Systematic and Applied Acarology, 26(7), 1307-1320. https://doi.org/10.11158/saa.26.7.13
Junqueira, L. C. U., & Junqueira, L. M. M. S. (1983). Técnicas básicas de citologia e histologia. Santos.
Lehane, M. J., & Billingsley, P. F. (1996). Biology of the Insect Midgut. Chapman and Hall.
Leite-Andrade, M. C., Neto, L. N. A., Buonafina-Paz, M. D. S., Santos, F. A. G., Alvez, A. I. S., Castro, M. C. A. B., Mori, E., Lacerda, B. C. G. V., Araújo, I. M., Coutinho, H. D. M., Kowalska, G., Kowalski, R., Baj, T., & Neves, R. P. (2022). Antifungal effect and inhibition of the virulence mechanism of D-Limonene against Candida parapsilosis. Molecules, 27(24), 1-12. https://doi.org/10.3390/molecules27248884
Lin, H., Li, Z., Sun, Y., Zhang, Y., Wang, S., Zhang, Q., Cai, T., Xiang, W., Zeng, C., & Tang, J. (2024). D-Limonene: Promising and sustainable natural bioactive compound. Applied Sciences, 14(11), 1-27. https://doi.org/10.3390/app14114605
Lima, V. O., Braghini, A., Paula, F. C., Souza, J. M. R., Figueiredo, G. P., & Vacari, A. M. (2024). Toxicity of botanical insecticides at different developmental stages of the coffee leaf miner, Leucoptera coffeella (Lepidoptera: Lynetiidae), and their side effects on predator Chrysoperla externa (Neuroptera: Chrysopidae). Crop Protection, 155, 106678. https://doi.org/10.1016/j.cropro.2024.106678
Moungthipmalai, T., Puwanard, C., Aungtikun, J., Sittichok, S., & Soonwera, M. (2023). Ovicidal toxicity of plant essentials oils and their major constituents against two mosquito vectors and their non-target aquatic predators. Scientific Reports, 13(2119), 1-13. https://doi.org/10.1038/s41598-023-29421-2
Mursiti, S., Lestari, N. A., Febriana, Z., Rosanti, Y. M., & Ningsih, T. W. (2019). The activity of D-limonene from sweet orange peel (Citrus sinensis L.) extract as a natural insecticide controller of bedbugs (Cimex Cimicidae). Oriental Journal of Chemistry, 35(4), 1420-1425. http://dx.doi.org/10.13005/ojc/350424
Muthukrishnan, S., Merzendorfer, H., Arakane, Y., & Kramer, K. J. (2012). Chitin metabolism in insects. In L. I. Gilbert (Ed.), Insect molecular biology and biochemistry. Academic Press.
Ngegba, P. M., Cui, G., Khalid, M. Z., & Zhong, G. (2022). Use of botanical pesticides in agriculture as an alternative to synthetic pesticides. Agriculture, 12(600), 1-24. https://doi.org/10.3390/agriculture12050600
Oliveira, F. M., Wanderley-Teixeira, V., Cruz, G. S., Silva, C. T. S., Dutra, K. A., Costa, H. N., Braga, V. A. A., Silva, E. J., Guedes, C. A., Alves, T. J. S., & Teixeira, A. A. C. (2021). Histological, histochemical and energy disorders caused by R-limonene on Aedes aegypti L. larvae (Diptera: Culicidae). Acta Tropica, 221, 105987. https://doi.org/10.1016/j.actatropica.2021.105987
Oliveira, J. A. C., Fernandes, L. A., Figueiredo, K. G., Corrêa, E. J. A., Lima, L. H. F., Alves, D. S., Bertolucci, S. K. V., & Carvalho, G. A. (2024a). Effects of essential oils on biological characteristics and potential molecular targets in Spodoptera frugiperda. Plants, 13(13), 1-21. https://doi.org/10.3390/plants13131801
Oliveira, J. J., Passos, E. M., Alves, S. M., Sarmento, V. H. V., Bjerk, T. R., Cardoso, J. C., Blanco-Llamero, C., Souto, E. B., Severino, P., & Mendonça, M. C. (2024b). Microemulsion of essential oil of Citrus aurantium var. dulcis for control of Aleurocanthus woglumi and evaluation of selectivity against Aschersonia aleyrodis and Ceraeochrysa cornuta. Crop Protection, 155, 1-9. https://doi.org/10.1016/j.cropro.2024.106586
Oyedeji, A. O., Okunowo, W. O., Osuntoki, A. A., Olabode, T. B., & Ayo-Folorunso, F. (2020). Insecticidal and biochemical activity of essential oil from Citrus sinensis peel and constituents on Callosobrunchus maculatus and Sitophilus zeamais. Pesticide Biochemistry and Physiology, 168, 104643. https://doi.org/10.1016/j.pestbp.2020.104643
Parra, J. R. P., Coelho Jr., A., Cuervo-Rugno, J. B., Garcia, A. G., Moral, R. A., Specht, A., & Dourado-Neto, D. (2021). Important pest species of the Spodoptera complex: biology, thermal requirements and ecological zoning. Journal of Pest Science, 95, 169-186. https://doi.org/10.1007/s10340-021-01365-4
Pathak, V. M., Verma, V. K., Rawat, B. S., Kaur, B., Babu, N., Sharma, A., Dewali, S., Yadav, M., Kumari, R., Singh, S., Mohapatra, A., Pandey, V., Rana, N., & Cunill, J. M. (2022). Current status of pesticide effects on environment, human health and it’s eco-friendly management as bioremediation: A comprehensive review. Frontiers in Microbiology, 13, 1-29. https://doi.org/10.3389/fmicb.2022.962619
Pavela, R., & Benelli, G. (2016). Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends in Plant Science, 21(12), 1000-1007. https://doi.org/10.1016/j.tplants.2016.10.005
Pinheiro, D. O., & Gregório, E. A. (2003). Ultrastructure of the columnar epithelial cell along the midgut of the Diatraea saccharalis (Lepidoptera: Pyralidae) larvae. Acta Microscopica, 12(1), 27-30.
Puentes-Cala, E., Atehortúa-Bueno, M., Tapia-Perdomo, V., Navarro-Escalante, L., Hernández-Torres, J., & Castillo-Villamizar, G. (2023). First insights into the gut microbiome of Diatraea saccharalis: from a sugarcane pest to a reservoir of new bacteria with biotechnological potential. Frontiers in Ecology and Evolution, 11, 1-8. https://doi.org/10.3389/fevo.2023.1027527
Rahayu, S. E., Leksono, A. S., Gama, Z. P., & Tarno, H. (2024). Histological and physiological responses of Spodoptera litura F. larvae after exposure to papaya leaf extract (Carica papaya L.). BIO Web of Conferences, 117, 1-8. https://doi.org/10.1051/bioconf/202411701028
Rosca, M., Cozma, P., & Hlihor, R.-M. (2023). Environmental and human impacts of the toxic pesticides use in agriculture: a review. Proceedings of the Romanian Academy, Series B, 25(2), 185-191.
Ryan, M. F., & Byrne, O. (1988). Plant-insect coevolution and inhibition of acetylcholinesterase. Journal of Chemical Ecology, 14(10), 1965-1975. https://doi.org/10.1007/BF01013489
Sampaio, F., Batista, M. M., & Machioro, C. A. (2024). Temperature-dependent reproduction of Spodoptera eridania: developing an oviposition model for a novel invasive species. Pest Management Science, 80(3), 1118-1125. https://doi.org/10.1002/ps.7842
Scudeler, E. L., & Santos, D. C. (2013). Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navas, 1911) (Neuroptera: Chrysopidae). Micron, 44(1), 125-132. https://doi.org/10.1016/j.micron.2012.05.009
Sena-Filho, J. G., Almeida, A. S., Pinto-Zevallos, D., Barreto, I. C., Cavalcanti, S. C. H., Nunes, R., Teodoro, A. V., Xavier, H. S., Barbosa Filho, J. M., Guan, L., Neves, A. L. A., & Duringer, J. M. (2023). From plant scent defense to biopesticide discovery: evaluation of toxicity and acetylcholinesterase docking properties for Lamiaceae monoterpenes. Crop Protection, 163, 106126. https://doi.org/10.1016/j.cropro.2022.106126
Sharma, A., Kumar, V., & Zheng, B. (2023). Pesticides in the environment. Elsevier.
Silva, C. T. S., Wanderley-Teixeira, V., Cunha, F. M., Oliveira, J. V., Dutra, K. A., Ferraz-Navarro, D. M. A., & Teixeira, A. A. C. (2017). Effects of citronella oil (Cymbopogon winterianus Jowitt ex Bor) on Spodoptera frugiperda (J. E. Smith) midgut and fat body. Biotechnic & Histochemistry, 93(1), 36-48. https://doi.org/10.1080/10520295.2017.1379612
Silva, M. F., Funichello, M., & Souza, D. M. (2020). Desempenho de inseticidas no controle de Diatraea saccharalis (Lepidoptera: Crambidae) em cana-de-açúcar. Arquivos do Instituto Biológico, 87, 1-6. https://doi.org/10.1590/1808-1657000782018
Souza, L., Cardoso, M. G., Konig, I. F. M., Ferreira, V. R. F., Caetano, A. R. S., Campolina, G. A., & Haddi, K. (2022). Toxicity, histopathological alterations and acetylcholinesterase inhibition of Illicium verum essential oil in Drosophila suzukii. Agriculture, 12(10), 1-17. https://doi.org/10.3390/agriculture12101667
Souza, C. O., Teixeira, V. W., Cruz, G. S., Guedes, C. A., Nascimento, J. C. S., Lapa-Neto, C. J. C., & Teixeira, A. A. C. (2023). Toxicology, histophysiological and nutritional changes in Apis mellifera (Hymenoptera: Apidae) submitted to limonene and natural pesticides in comparison to synthetic pesticides. Journal of Apicultural Research, 62(2), 912-923. https://doi.org/10.1080/00218839.2023.2166229
Turek, C., & Stintzing, F. C. (2013). Stability of essential oils: A review. Comprehensive Reviews in Food Science and Food Safety, 12(1), 40-53. https://doi.org/10.1111/1541-4337.12006
Copyright (c) 2026 Richard Henrique Siebra Bergamo, Bruno Vinicius Daquila, Ricardo Antonio Polanczyk, Elton Luiz Scudeler, Helio Conte (Autor)
This work is licensed under a Creative Commons Attribution 4.0 International License.
DECLARAÇÃO DE ORIGINALIDADE E DIREITOS AUTORAIS
Declaro que o presente artigo é original, não tendo sido submetido à publicação em qualquer outro periódico nacional ou internacional, quer seja em parte ou em sua totalidade.
Os direitos autorais pertencem exclusivamente aos autores. Os direitos de licenciamento utilizados pelo periódico é a licença Creative Commons Attribution 4.0 (CC BY 4.0): são permitidos o compartilhamento (cópia e distribuição do material em qualqer meio ou formato) e adaptação (remix, transformação e criação de material a partir do conteúdo assim licenciado para quaisquer fins, inclusive comerciais.
Recomenda-se a leitura desse link para maiores informações sobre o tema: fornecimento de créditos e referências de forma correta, entre outros detalhes cruciais para uso adequado do material licenciado.
