Disentangling the ecotoxicological selectivity of clove essential oil against aphids and non-target ladybeetles
Abstract
The plant-based biopesticides have been proposed as insect pest control tools that seem to be safer for the environment and human health when compared to synthetic conventional molecules. However, such assumptions are generally made without considering the absence of detrimental effects on sublethally-exposed non-target organisms or showing the physiological basis of the selective action of such botanical products. Thus, by using in silico-based and in vivo toxicological approaches, the present investigation aimed to disentangle the ecotoxicological selectivity of clove, Syzygium aromaticum, essential oil against the aphid Rhopalosiphum maidis and the non-target ladybeetle, Coleomegilla maculata. We also investigated whether the sublethal exposure to clove essential oil would affect the locomotory and predatory abilities of C. maculata. We found that the clove essential oil concentration estimated to kill 95% (LC 95: 0.17 μL/cm 2) of the aphids was lethal to <18% of C. maculata. Indeed, our in silico results reinforced such differential susceptibility, as it predicted that eugenol and β-caryophyllene (i.e., the clove essential oil major components) bound to three potential molecular targets (i.e., transient receptor potential (TRP) channels, octopamine, and gamma-aminobutyric acid (GABA) receptors) of the aphids but only to the octopamine receptors of the ladybeetles. Additionally, the ladybeetles that were exposure to the clove essential oil exhibited unaffected abilities to locomote and to prey upon R. maidis aphids when compared to unexposed ladybeetles. Thus, by displaying lower toxicity against the ladybeetles, the clove essential oil represents a safer alternative tool to be integrated into programs aiming to manage aphid infestations.
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Toledo et al. reported that CEO had activity against aphids, but not against ladybugs; they reported an LC95 of 0.17 μL/cm2 for aphids, while the same dose only had a lethality of less than 18% for Corymbia maculata; ladybugs exposed to CEO did not exhibit impaired locomotion ability.
“Toledo et al. [104] reported that it had activity against aphids, but not against ladybugs. They reported an LC95 of 0.17 μL/cm2 for aphids, while the same dose only had a lethality of less than 18% for Corymbia maculata. The ladybugs that were exposed to CEO did not exhibit impaired locomotion ability.”
From Clove essential oil (Syzygium aromaticum L. Myrtaceae): Extraction, chemical composition, food applications, and essential bioactivity for human health (2021) · cites this paper as [104]
Cites
AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility
Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009) · Journal of Computational Chemistry · doi:10.1002/jcc.21256 · Cited by 25,745 · see citing works
SWISS-MODEL: homology modelling of protein structures and complexes
Waterhouse, A. M., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T., Rempfer, C., Bordoli, L., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky427 · Cited by 13,246 · see citing works
The Amber biomolecular simulation programs
Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Onufriev, A., Simmerling, C., Wang, B., & Woods, R. J. (2005) · Journal of Computational Chemistry · doi:10.1002/jcc.20290 · Cited by 9,535 · see citing works
Isman, M. B. (2005) · Annual Review of Entomology · doi:10.1146/annurev.ento.51.110104.151146 · Cited by 3,901 · see citing works
Plant essential oils for pest and disease management
Isman, M. B. (2000) · Crop Protection · doi:10.1016/s0261-2194(00)00079-x · Cited by 2,469 · see citing works
Repellent activity of essential oils: A review
Nerio, L. S., Olivero‐Verbel, J., & Stashenko, E. E. (2009) · Bioresource Technology · doi:10.1016/j.biortech.2009.07.048 · Cited by 1,313 · see citing works
Design and analysis of ecological experiments
Hurlbert, S. H. (1994) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(94)90324-7 · Cited by 1,308 · see citing works
Essential Oils in Insect Control: Low-Risk Products in a High-Stakes World
Régnault-Roger, C., Vincent, C., & Arnason, J. T. (2011) · Annual Review of Entomology · doi:10.1146/annurev-ento-120710-100554 · Cited by 1,288 · see citing works
Natural products in crop protection.
Dayan, F., Cantrell, C., & Duke, S. (2009) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2009.01.046 · Cited by 1,187 · see citing works
Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints
Pavela, R., & Benelli, G. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.10.005 · Cited by 1,162 · see citing works
Chaieb, K., Hajlaoui, H., Zmantar, T., Kahla‐Nakbi, A. B., Rouabhia, M., Mahdouani, K., & Bakhrouf, A. (2007) · Phytotherapy Research · doi:10.1002/ptr.2124 · Cited by 934 · see citing works
Mechanism of action of insecticidal secondary metabolites of plant origin
Rattan, R. S. (2010) · Crop Protection · doi:10.1016/j.cropro.2010.05.008 · Cited by 853 · see citing works
Hance, T., Kohandani-Tafresh, F., & Munaut, F. (2007) · CABI eBooks · doi:10.1079/9780851998190.0000 · Cited by 743 · see citing works
Pesticide-Induced Stress in Arthropod Pests for Optimized Integrated Pest Management Programs
Guedes, R. N. C., Smagghe, G. J., Stark, J. D., & Desneux, N. (2015) · Annual Review of Entomology · doi:10.1146/annurev-ento-010715-023646 · Cited by 720 · see citing works
Self-citationInsecticidal activity of essential oils: octopaminergic sites of action
Enan, E. E. (2001) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/s1532-0456(01)00255-1 · Cited by 626 · see citing works
GABAA receptor signalling mechanisms revealed by structural pharmacology
Masiulis, S., Desai, R., Uchański, T., Martin, I. S., Laverty, D. C., Karia, D., Malinauskas, T., Zivanov, J., Pardon, E., Kotecha, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0832-5 · Cited by 559 · see citing works
Kostyukovsky, M., Rafaeli, A., Gileadi, C., Demchenko, N., & Shaaya, E. (2002) · Pest Management Science · doi:10.1002/ps.548 · Cited by 542 · see citing works
Botanical insecticide research: many publications, limited useful data
Isman, M. B., & Grieneisen, M. L. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.11.005 · Cited by 539 · see citing works
Priestley, C. M., Williamson, E. M., Wafford, K. A., & Sattelle, D. B. (2003) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705542 · Cited by 503 · see citing works
Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control
López, M. D., & Pascual‐Villalobos, M. J. (2009) · Industrial Crops and Products · doi:10.1016/j.indcrop.2009.11.005 · Cited by 451 · see citing works
Repeated-measures Analysis: Growth and Other Time-dependent Measures
von Ende, C. N. (2001) · doi:10.1093/oso/9780195131871.003.0008 · Cited by 417 · see citing works
Sachdev, P. S., Lipnicki, D. M., Kochan, N. A., Crawford, J. D., Thalamuthu, A., Andrews, G., Brayne, C., Matthews, F. E., Stephan, B. C. M., Lipton, R. B., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0142388 · Cited by 380 · see citing works
Harel, M., Kryger, G., Rosenberry, T. L., Mallender, W. D., Lewis, T., Fletcher, R. J., Guss, J. M., Silman, I., & Sussman, J. L. (2000) · Protein Science · doi:10.1110/ps.9.6.1063 · Cited by 299 · see citing works
Enan, E. E. (2005) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.20076 · Cited by 284 · see citing works
Cryo-electron microscopy structure of the TRPV2 ion channel
Zubcevic, L., Herzik, M. A., Chung, B. C., Liu, Z.-R., Lander, G. C., & Lee, S. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3159 · Cited by 280 · see citing works
Evolution of TRP channels inferred by their classification in diverse animal species
Peng, G., Shi, X., & Kadowaki, T. (2014) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2014.06.016 · Cited by 205 · see citing works
Opening of the human epithelial calcium channel TRPV6
McGoldrick, L. L., Singh, A. K., Saotome, K., Yelshanskaya, M. V., Twomey, E. C., Grassucci, R. A., & Sobolevsky, A. I. (2017) · Nature · doi:10.1038/nature25182 · Cited by 205 · see citing works
Comparison of antifungal activity of essential oils from different plants against three fungi
Hu, F., Tu, X.-F., Thakur, K., Hu, F., Li, X., Zhang, Y.-S., Zhang, J., & Wei, Z. (2019) · Food and Chemical Toxicology · doi:10.1016/j.fct.2019.110821 · Cited by 198 · see citing works
Tembo, Y. L. B., Mkindi, A. G., Mkenda, P. A., Mpumi, N., Mwanauta, R. W., Stevenson, P. C., Ndakidemi, P. A., & Belmain, S. R. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.01425 · Cited by 187 · see citing works
He, Y., Zhao, J., Zheng, Y., et al. (2012) · Ecotoxicology · doi:10.1007/s10646-012-0883-6 · Cited by 185 · see citing works
Segala, E., Guo, D. M., Cheng, R. K. Y., Bortolato, A., Deflorian, F., Dore, A. S., Errey, J. C., Heitman, L. H., IJzerman, A. P., Marshall, F. H., et al. (2016) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b00653 · Cited by 181 · see citing works
Miller, J. L., Nehmé, R., Warne, T., Edwards, P. C., Schertler, G. F. X., Leslie, A. G. W., & Tate, C. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092727 · Cited by 169 · see citing works
Evolutionary conservation and changes in insect TRP channels
Matsuura, H., Sokabe, T., Kohno, K., et al. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-228 · Cited by 164 · see citing works
Plata-Rueda, A., Campos, J. M., da Silva Rolim, G., Martínez, L. C., Dos Santos, M. H., Fernandes, F. L., Serrão, J. E., & Zanuncio, J. C. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.03.033 · Cited by 148 · see citing works
Price, D. N., & Berry, M. S. (2006) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2005.11.010 · Cited by 130 · see citing works
Blenau, W., & Thamm, M. (2011) · Arthropod Structure & Development · doi:10.1016/j.asd.2011.01.004 · Cited by 129 · see citing works
Paine, M. D. (1996) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620150901 · Cited by 122 · see citing works
AHRENS, D. C., & Ribera, I. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-234 · Cited by 117 · see citing works
Pavela, R. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-018-1398-3 · Cited by 114 · see citing works
Brügger, B. P., Martínez, L. C., Plata‐Rueda, A., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-44709-y · Cited by 114 · see citing works
Tu, X.-F., Hu, F., Thakur, K., et al. (2018) · Industrial Crops and Products · doi:10.1016/j.indcrop.2018.07.065 · Cited by 106 · see citing works
Structural insight into TRPV5 channel function and modulation
Dang, S., van Goor, M. K. C., Asarnow, D. E., Wang, Y., Julius, D. J., Cheng, Y., & van der Wijst, J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820323116 · Cited by 106 · see citing works
Effects of Systemic Imidacloprid onColeomegilla maculata(Coleoptera: Coccinellidae)
Smith, S. F., & Krischik, V. (1999) · Environmental Entomology · doi:10.1093/ee/28.6.1189 · Cited by 102 · see citing works
Jumbo, L. O. V., Faroni, L. R. D., de Oliveira, E. E., et al. (2014) · Industrial Crops and Products · doi:10.1016/j.indcrop.2014.02.038 · Cited by 93 · see citing works
Self-citationKohno, K., Sokabe, T., Tominaga, M., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2001-10.2010 · Cited by 92 · see citing works
Pesticides Based on Plant Essential Oils: Phytochemical and Practical Considerations
Isman, M. B. (2016) · ACS symposium series · doi:10.1021/bk-2016-1218.ch002 · Cited by 89 · see citing works
Xiao, D., Zhao, J., Guo, X., et al. (2016) · Ecotoxicology · doi:10.1007/s10646-016-1721-z · Cited by 86 · see citing works
Haddi, K., de Oliveira, E. E., Faroni, L. R. D., et al. (2015) · Journal of Economic Entomology · doi:10.1093/jee/tov255 · Cited by 84 · see citing works
Self-citationCorrea, Y. D. C. G., Faroni, L. R. D., Haddi, K., et al. (2015) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2015.06.005 · Cited by 82 · see citing works
Self-citationKrischik, V., Rogers, M., Gupta, G., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119133 · Cited by 78 · see citing works
Tschoeke, P. H., de Oliveira, E. E., Dalcin, M. S., Silveira-Tschoeke, M. C. A. C., Sarmento, R. A., & dos Santos, G. R. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.04.133 · Cited by 78 · see citing works
Self-citationInsect TRP channels as targets for insecticides and repellents
Salgado, V. L. (2017) · Journal of Pesticide Science · doi:10.1584/jpestics.d16-104 · Cited by 77 · see citing works
Nawaz, M., Cai, W., Jing, Z., et al. (2017) · Chemosphere · doi:10.1016/j.chemosphere.2017.03.082 · Cited by 77 · see citing works
Jumbo, L. O. V., Haddi, K., Faroni, L. R. D., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0207618 · Cited by 67 · see citing works
Self-citationThomas, A., Mazigo, H. D., Manjurano, A. M., Morona, D., & Kweka, E. J. (2017) · Parasites & Vectors · doi:10.1186/s13071-017-2355-6 · Cited by 63 · see citing works
Thomas, E., Chiquet, M., Sander, B., et al. (2017) · Parasites & Vectors · doi:10.1186/s13071-017-2390-3 · Cited by 63 · see citing works
Tian, B., Liu, Q.-Z., Liu, Z.-L., Li, P., & Wang, J.-W. (2015) · Journal of Economic Entomology · doi:10.1093/jee/tov075 · Cited by 62 · see citing works
Moscardini, V. F., Gontijo, P. D. C., Michaud, J. P., et al. (2015) · Ecotoxicology · doi:10.1007/s10646-015-1462-4 · Cited by 61 · see citing works
Swapping of transmembrane domains in the epithelial calcium channel TRPV6
Singh, A. K., Saotome, K., & Sobolevsky, A. I. (2017) · Scientific Reports · doi:10.1038/s41598-017-10993-9 · Cited by 56 · see citing works
Toledo, P. F. S., Ferreira, T. P., Bastos, I. M. A. D. S., et al. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.113153 · Cited by 54 · see citing works
Self-citationXiao, M., Brugler, M. R., Broe, M. B., Gusmão, L. C., Daly, M., & Rodríguez, E. (2019) · Scientific Reports · doi:10.1038/s41598-019-54637-6 · Cited by 53 · see citing works
Fogel, M. N., Schneider, M. I., Rimoldi, F., et al. (2016) · Environmental Science and Pollution Research · doi:10.1007/s11356-016-6654-9 · Cited by 49 · see citing works
Castilhos, R. V., Grützmacher, A. D., & Coats, J. R. (2017) · Neotropical Entomology · doi:10.1007/s13744-017-0547-6 · Cited by 49 · see citing works
Ferreira, T. P., de Oliveira, E. E., Tschoeke, P. H., et al. (2017) · Industrial Crops and Products · doi:10.1016/j.indcrop.2017.08.023 · Cited by 44 · see citing works
Self-citationSilva, S. M., Haddi, K., Jumbo, L. O. V., et al. (2017) · Entomologia Experimentalis et Applicata · doi:10.1111/eea.12559 · Cited by 43 · see citing works
Self-citationHe, F., Sun, S., Tan, H., et al. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.03.025 · Cited by 42 · see citing works
Razmjou, J., & Golizadeh, A. (2010) · Applied Entomology and Zoology · doi:10.1303/aez.2010.267 · Cited by 40 · see citing works
Xie, H., Zhao, L., Wang, W., Wang, Z., Ni, X., Cai, W., & He, K. (2014) · Journal of Economic Entomology · doi:10.1603/ec13302 · Cited by 35 · see citing works
Effects of Botanical Insecticides on Hymenopteran Parasitoids: a Meta-analysis Approach
Monsreal-Ceballos, R. J., Ruíz-Sánchez, E., Ballina−Gómez, H. S., Reyes-Ramírez, A., & González‐Moreno, A. (2018) · Neotropical Entomology · doi:10.1007/s13744-017-0580-5 · Cited by 35 · see citing works
Miyazawa, M., Nakahashi, H., Usami, A., & Matsuda, N. (2016) · Journal of Natural Medicines · doi:10.1007/s11418-015-0961-1 · Cited by 34 · see citing works
Bergougnoux, M., Treilhou, M., & Armengaud, C. (2012) · Apidologie · doi:10.1007/s13592-012-0158-5 · Cited by 30 · see citing works
Bing, J., Novak, M. G., Obrycki, J. J., et al. (1991) · Annals of the Entomological Society of America · doi:10.1093/aesa/84.5.549 · Cited by 30 · see citing works
Pesticides, pollution and the UK's silent spring, 1963–1964: Poison in the Garden of England
Clark, J. F. M. (2017) · Notes and Records the Royal Society Journal of the History of Science · doi:10.1098/rsnr.2016.0040 · Cited by 30 · see citing works
Plant essential oils: the way forward for aphid control?
Atanasova, Д., & Leather, S. R. (2018) · Annals of Applied Biology · doi:10.1111/aab.12451 · Cited by 29 · see citing works
Armijos, M. J. G., Jumbo, L. O. V., Faroni, L. R. D., et al. (2019) · Revista de Ciencias Agrícolas · doi:10.22267/rcia.193601.94 · Cited by 24 · see citing works
Silva, R. B., Cruz, I., Figueiredo, M. D. L. C., et al. (2010) · Revista Brasileira de Milho e Sorgo · doi:10.18512/1980-6477/rbms.v9n1p13-26 · Cited by 19 · see citing works
Haddi, K., Jumbo, L. O. V., Costa, M. S., et al. (2017) · Journal of Pest Science · doi:10.1007/s10340-017-0860-1 · Cited by 18 · see citing works
Self-citationMixed effects of landscape complexity and insecticide use on ladybeetle abundance in wheat fields
Yang, L., Zhang, Q., Liu, B., Zeng, Y., Pan, Y., Li, M., & Lu, Y. (2018) · Pest Management Science · doi:10.1002/ps.5281 · Cited by 18 · see citing works
Pointeau, S., Jaguenet, E., Couty, A., Dubois, F., Rambaud, C., & Ameline, A. (2014) · Industrial Crops and Products · doi:10.1016/j.indcrop.2014.01.018 · Cited by 14 · see citing works
Cabrera, P., Cormier, D., & Lucas, É. (2018) · Journal of Pest Science · doi:10.1007/s10340-018-0978-9 · Cited by 13 · see citing works
Allen, M. L. (2015) · Florida Entomologist · doi:10.1653/024.098.0247 · Cited by 8 · see citing works
Lady Beetle (Coleoptera: Coccinellidae) Communities in Soybean and Maize
Prescott, K., & Andow, D. A. (2015) · Environmental Entomology · doi:10.1093/ee/nvv154 · Cited by 8 · see citing works
de Campos, A. P., Júnior, A. L. B., & Ribeiro, Z. A. (2014) · Revista CERES · doi:10.1590/0034-737x201461050008 · Cited by 4 · see citing works
A review of imidacloprid toxicity in coccinellids
Amjad, A., Azam, I., & Sarwar, E. A. M. K. (2018) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 3 · see citing works
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Haro-González, J. N., Castillo-Herrera, G. A., Martínez-Velázquez, M., & Espinosa-Andrews, H. (2021) · Molecules · doi:10.3390/molecules26216387 · Cited by 463 · see citing works
- Authors
- Toledo, P. F. S., Viteri Jumbo, L. O., Rezende, S. M., Haddi, K., Silva, B. A., Mello, T. S., Della Lucia, T. M. C., Aguiar, R. W. S., Smagghe, G., & Oliveira, E. E.
- Affiliations
- Universidade Federal de Viçosa (BR)
- Universidade Federal de Lavras (BR)
- Southwest Bahia State University (BR)
- Ghent University (BE)
- Corresponding author
- Oliveira, Eugenio E.
- ORCID
- Venue
- Science of The Total Environment
- Publisher
- Elsevier BV
- Published
- 2020-05
- Volume
- 718
- Pages
- 137328
- ISSN
- 0048-9697 (ISSN-L)
- OpenAlex
- W3005664549
- Cited by
- 52
- References
- 85
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 7 · 2023: 11 · 2022: 11 · 2021: 6 · 2020: 2
- FWCI
- 4.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Science of The Total Environment (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Funders
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Fundação de Amparo à Pesquisa do Estado de Minas Gerais
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Insect Pest Control Strategies
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
- Keywords
- clove oil, Syzygium aromaticum, Rhopalosiphum maidis, Coleomegilla maculata, non-target effects, sublethal exposure, biopesticides, eugenol, β-caryophyllene, octopamine receptor, GABA receptors, TRP channels, predatory behavior, aphid control
- MeSH terms
- Animals, Aphids, Insect Control, Oils, Volatile, Syzygium, Clove Oil
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