Abstract
The whitefly Bemisia tabaci (Gennadius, 1889) (Hemiptera: Aleyrodidae) is a globally important insect pest, causing extensive damage and losses in horticultural production systems. New natural options are needed to control the whitefly. Ethanol extracts (92) of different organs from 40 plant species of the Yucatan Peninsula were evaluated against B. tabaci in a greenhouse, and an adult repellency index (RI) was determined for leaves and an oviposition deterrence index (ODI) for the extracts. Ethanol extracts at 1% (w/v) after 48 h suppressed the population density of B. tabaci. Leaves of Malpighia glabra L. had the highest repellent activity, causing a decrease in the population density of adults (RI 0.05) and eggs (ODI − 85). Three fractions differing in polarity were obtained by partitioning the ethanol extract of M. glabra, and the hexane fraction had an intermediate RI, but the ODI was not active. LC–UV–HRMS analysis of the fractions showed the presence of syringaresinol, 10-hydroxy-pheophorbide a, pheophorbide a, and lupenone, the first report of these four for this species. Eleven unknown compounds were also detected. This bioprospecting research on botanical extracts from native species of the Yucatan Peninsula enriches our knowledge of potential sources of products for pest management. M. glabra is a promising candidate for further formulation and application studies to control B. tabaci.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abubakar M, Koul B, Chandrashekar K, Raut A, Yadav D (2022) Whitefly (Bemisia tabaci) management (WFM) strategies for sustainable agriculture: a review. Agriculture 12:1317. https://doi.org/10.3390/agriculture12091317
Affandi HA, Read WR (1998) Studies on natural products of Albizia sp. Biotropia-Southeast. Asian J Trop Biol 11:1–8. https://doi.org/10.11598/btb.1998.0.11.139
Baldin LL, Crotti AEM, Wakabayashi KAL, Silva JPGF, Aguiar GP, Souza ES, Veneziani RCS, Groppo M (2013) Plant-derived essential oils affecting settlement and oviposition of Bemisia tabaci (Genn) biotype B on tomato. J Pest Sci 86(2):301–308. https://doi.org/10.1007/s10340-012-0462-x
Baldin ELL, Aguiar GP, Fanela TLM, Soares MCE, Groppo M, Crotti AEM (2014) Bioactivity of Pelargonium graveolens essential oil and related monoterpenoids against sweet potato whitefly, Bemisia tabaci biotype B. J Pest Sci 88(1):191–199. https://doi.org/10.1007/s10340-014-0580-8
Basij M, Talebi K, Ghadamyari M, Hosseininaveh V, Salmai VA (2017) Status of Resistance of Bemisia tabaci (Hemiptera: Aleyrodidae) to neonicotinoids in Iran and detoxification by cytochrome P450-dependent monooxygenases. Neotrop Entomol 46:115–124. https://doi.org/10.1007/s13744-016-0437-3
Batista LCDS, Cid YP, De Almeida AP, Prudêncio ER, Riger CJ, De Souza MAA, Coumendouros K, Chaves DS (2016) In vitro efficacy of essential oils and extracts of Schinus molle L. against Ctenocephalides felis felis. Parasitology 143(5):627–38. https://doi.org/10.1017/S0031182016000081
Bolzonella C, Lucchetta M, Teo G, Boatto V, Zanella A (2019) Is there a way to rate insecticides that is less detrimental to human and environmental health? Glob Ecol Conserv 20:e00699. https://doi.org/10.1016/j.gecco.2019.e00699
Castillo-Sánchez LE, Jiménez-Osornio JJ, Delgado-Herrera MA (2012) Actividad biológica in vitro del extracto de Capsicum chinense Jacq contra Bemisia tabaci Genn. Rev Chapingo Ser Hortic 18(3):345–356. https://doi.org/10.5154/r.rchsh.2011.04.016
Costa AM, Amorim FDO, Anjos-Duarte CS, Joachim-Bravo IS (2011) Influence of different tropical fruits on biological and behavioural aspects of the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera, Tephritidae). Rev Bras Entomol 55:355–360
Costa ECC, Christofoli M, Costa GCS, Peixoto MF, Fernandes JB, Forim MR, Pereira KC, Silva FG, Cazal CM (2017) Essential oil repellent action of plants of the genus Zanthoxylum against Bemisia tabaci biotype B (Homoptera: Aleyrodidae). Sci Hortic 226:327–332. https://doi.org/10.1016/j.scienta.2017.08.041
Cruz-Cerino P, Cristóbal-Alejo J, Ruiz-Carrera V, Carnevali G, Vera-Ku M, Martín J, Reyes F, Gamboa-Angulo M (2020) Extracts from six native plants of the Yucatán Peninsula hinder mycelial growth of Fusarium equiseti and F. oxysporum. Pathogens of Capsicum chinense. Pathogens 9:827. https://doi.org/10.3390/pathogens9100827
Cruz-Estrada A, Gamboa-Angulo M, Borges-Argáez R, Ruiz-Sánchez E (2013) Insecticidal effects of plant extracts on immature whitefly Bemisia tabaci Genn. (Hemiptera: Aleyroideae). Electron J Biotechnol 16(1):1–9. https://doi.org/10.2225/vol16-issue1-fulltext-6
Cruz-Estrada A, Ruiz-Sánchez E, Cristóbal-alejo J, González-Coloma A, Andrés MF, Gamboa-Angulo M (2019) Medium-chain fatty acids from Eugenia winzerlingii leaves causing insect settling, deterrent, nematicidal, and phytotoxic effects. Molecules 24(9):1724. https://doi.org/10.3390/molecules24091724
Di Rienzo JA, Casanoves F, Gonzalez LA, Tablada EM, Diaz MP, Robledo CW, Balzarini MG (2018) InfoStat ver. 2018 Grupo InfoStat FCA Universidad Nacional de Cordoba, Argentina
Duke JA (2000) Dr Duke’s phytochemical and ethnobotanical databases Phytochemical database. USDAARS-NGRL, Beltsville Agricultural Research Centre
Dougoud J, Toepfer S, Bateman M, Jenner WH (2019) Efficacy of homemade botanical insecticides based on traditional knowledge. A review. Agron Sustain Dev 39:37. https://doi.org/10.1007/s13593-019-0583-1
El-Hawary SS, El-Fitiany RA, Mousa OM, Salama AAA, Gedaily RA (2020) Metabolic profiling and in vivo hepatoprotective activity of Malpighia glabra L. leaves. J Food Biochem 45(2):e13588. https://doi.org/10.1111/jfbc.13588
Engels G, Brinckmann J (2014) Acerola Malpighia glabra. Am Bot Council 104:64–69
Freky AM, Elsabbagh WA, Abu Bakr MS, El-Ghazaly MA, Mohamed AEI (2021) Antioxidant activity of Malpighia glabra L., leaves extract. Azhar Int J Pharm Msd Sci 1(2):88–93
Fabrick JA, Yool AJ, Spurgeon DW (2020) Insecticidal activity of marigold Tagetes patula plants and foliar extracts against the hemipteran pests, Lygus hesperus and Bemisia tabaci. PLoS ONE 15(5):1–15. https://doi.org/10.1371/journal.pone.0233511
García MD, Argüelles JC (2021) Trehalase inhibition by validamycin A may be a promising target to design new fungicides and insecticides. Pest Manag Sci 77(9):3832–3835. https://doi.org/10.1002/ps.6382
Guía-García JL, Charles-Rodríguez AV, Reyes-Valdés MH, Ramírez-Godina F, Robledo-Olivo A, García-Osuna HT, Cerqueira MA, Flores-López ML (2022) Micro and nanoencapsulation of bioactive compounds for agri-food applications: a review. Ind Crops Prod 186:115198. https://doi.org/10.1016/j.indcrop.2022.115198
Hernández-Carlos B, Gamboa-Angulo M (2019) Insecticidal and nematicidal contributions of Mexican flora in the search for safer biopesticides. Molecules 24(5):897. https://doi.org/10.3390/molecules24050897
Herrera-Gorocica A, Hernández-Núñez E, Calvo L, Sánchez-Contreras A, Ruiz-Jiménez A, Latournerie-Moreno L, Ballina-Gómez H, Ruiz-Sánchez E (2023) Effect of the essential oil of Lippia origanoides Kunth and two of its volatile organic compounds on Tetranychus urticae Koch (Acari: Tetranychidae) and Bemisia tabaci Genn (Hemiptera: Aleyrodidae) in greenhouse. Trop Subtrop Agroecosyst 26(31):14
Hikal WM, Baeshen RS, Said-Al AHAH (2017) Botanical insecticide as simple extractives for pest control. Cogent Biol 3(1):1–16. https://doi.org/10.1080/23312025.2017.1404274
Horowitz AR, Ghanim M, Roditakis E, Nauen R, Ishaaya I (2020) Insecticide resistance and its management in Bemisia tabaci species. J Pest Sci 93(3):893–910. https://doi.org/10.1007/s10340-020-01210-0
Islam W, Akutse KS, Qasim M, Khan KA, Ghramh HA, Idrees A, Latif S (2018) Bemisia tabaci -mediated facilitation in diversity of begomoviruses: evidence from recent molecular studies. Microb Pathogen 123:162–168. https://doi.org/10.1016/j.micpath.2018.07.008
Isman MB (2017) Bridging the gap: moving botanical insecticides from the laboratory to the farm. Ind Crops Prod 110:10–14. https://doi.org/10.1016/j.indcrop.2017.07.012
Lima BMFV, Moreira JOT, Aragão CA (2013) Evaluation of plant extracts in the control of whitefly Bemisia tabaci biotype B in squash. Rev Ciê Agronô 44:622–627
Liu X, Vrieling K, Klinkhamer PGL (2018) Phytochemical background mediates effects of pyrrolizidine alkaloids on western flower thrips. J Chem Ecol 45(2):116–127. https://doi.org/10.1007/s10886-018-1009-2
Lucantoni L, Magaraggia M, Lupidi G, Ouedraogo RK, Coppellotti O, Esposito F, Fabris C, Jori G, Habluetzel A (2011) Novel, meso-substituted cationic porphyrin molecule for photo-mediated larval control of the dengue vector Aedes aegypti. PLOS Negl Trop Dis 5(12):e1434. https://doi.org/10.1371/journal.pntd.0001434
Mahmood MA, Ahmed N, Hussain S, Muntaha ST, Amin I, Mansoor S (2022) Dominance of Asia II 1 species of Bemisia tabaci in Pakistan and beyond. Sci Rep 12:1528. https://doi.org/10.1038/s41598-022-05612-1
Martín J, Crespo G, González-Menéndez V, Pérez-Moreno G, Sánchez-Carrasco P, Pérez-Victoria I, Ruiz-Pérez LM, González-Pacanowska D, Vicente F, Genilloud O, Bills GF, Reyes F (2014) MDN-0104, an antiplasmodial betaine lipid from Heterospora chenopodii. J Nat Prod 77(9):2118–2123. https://doi.org/10.1021/np500577v
Maznah M, Sajap AS, Sukari MA, Omar D, Sahri MH, Rhiah R (2015) GC–MS analysis of Aglaia odoratissima B. leaves. Europ Int J Sci Technol 4(1):37–42
Miresmailli S, Isman MB (2014) Botanical insecticides inspired by plant–herbivore chemical interactions. Trends Plant Sci 19(1):29–35. https://doi.org/10.1016/j.tplants.2013.10.002
Mostafa ME (2021) Acaricidal potential and phytochemical analysis of the indigenous Centaurea aegyptiaca L. against Tetranychus urticae Koch (Acari: Tetranychidae). Int J Entomol Res 6(1):40–45
Njuguna MJ, Muriuki M, Karenga S (2022) Contact toxicity of essential oils from Tithonia diversifolia against Aphis gosypii, Thrips tabaci and Bemisia tabaci. Int J Adv Res 5(1):10–20. https://doi.org/10.37284/ijar.5.1.534
Nombela G, Muñiz M (2010) Host plant resistance for the management of Bemisia tabaci: A multicrop survey with emphasis on tomato. In: Stansly PA, Naranjo SE (eds) Bemisia: bionomics and management of a global pest. Springer, Dordrecht, pp 357–383
Oliveira MRV, Henneberry TE, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20(9):709–772. https://doi.org/10.1016/S0261-2194(01)00108-9
Ontiveros-Guerra JG, Cerna CE, Ochoa-Fuentes YM, Landeros FJ, Aguirre ULA, Hernández JA (2020) Insecticidal activity of plant extracts against whitefly nymphs Bemisia tabaci (Hemiptera: Aleyrodidae) in laboratory. J Entomol Zool Stud 8(1):595–599
Peres MC, de Souza Costa GC, dos Reis LE, da Silva LD, Peixoto MF, Alves CC, Forim MR, Quintela ED, Araújo WL, de Melo CC (2020) In natura and nanoencapsulated essential oils from Xylopia aromatica reduce oviposition of Bemisia tabaci in Phaseolus vulgaris. J Pest Sci 93:807–821. https://doi.org/10.1007/s10340-019-01186-6
Pérez-Verdugo O, Ruiz-Sánchez E, Gamboa-Angulo M, Latournerie-Moreno L, Cua-Basulto M, Chan-Cupul W (2019) Actividad biológica de productos derivados de plantas en mosquita blanca (Bemisia tabaci) y su parasitoide Encarsia formosa. Trop Subtrop Agroecosyst 22:575–583
Perring TM, Stansly PA, Liu TX, Smith HA, Andreason SA (2018) Whiteflies: biology, ecology, and management. In: Wakil W, Brust GE, Perring TM (eds) Sustainable management of arthropod pests of tomato, 1st edn. Academic Press, Cambridge, pp 73–110
Prakash A, Baskaran R (2018) Acerola, an untapped functional superfruit: a review on latest frontiers. J Food Sci Technol 55(9):3373–3384. https://doi.org/10.1007/s13197-018-3309-5
Rosen R, Kanakala S, Kliot A, Cathrin Pakkianathan B, Farich BA, Santana-Magal N, Elimelech M, Kontsedalov S, Lebedev G, Cilia M, Ghanim M (2015) Persistent, circulative transmission of begomoviruses by whitefly vectors. Curr Opin Virol 15:1–8. https://doi.org/10.1016/j.coviro.2015.06.008
Ruiz-Jiménez AL, González-Coloma A, Andrés-Yeves MF, Ruiz-Sánchez E, Heredia G, Peraza-Sánchez SR, Medina-Baizabal IL, Reyes-Estebanez M, Canto-Canché B, Gamboa-Angulo M (2017) Insect deterrent and nematicidal screening of microfungi from Mexico and anti-aphid compounds from Gliomastix masseei. Rev Argent Microbiol 49(1):83–92. https://doi.org/10.1016/j.ram.2016.08.009
Sani I, Ismail SI, Abdullah S, Jalinas J, Jamian S, Saad N (2020) A review of the biology and control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to biological control using entomopathogenic fungi. Insects 11(9):619. https://doi.org/10.3390/insects11090619
Teixeira Pinto Z, Ferreira Carneiro J, Carriço C, Leal Caetano R, Baia Ferreira V, Martins Mendoça P, Rangel Berenger AL, Figueiredo MR (2018) Efecto acaricida de siete extractos de plantas brasileñas. Rev Colomb Entomol 44(1):44–47. https://doi.org/10.25100/socolen.v44il.6541
Villaseñor JL (2016) Checklist of the native vascular plants of México. Rev Mex Biodivers 87:559–902. https://doi.org/10.1016/j.rmb.2016.06.017
Wang R, Fang Y, Che W, Zhang Q, Wang J, Luo C (2022) Metabolic resistance in abamectin-resistant Bemisia tabaci mediterranean from Northern China. Toxins 14(7):424. https://doi.org/10.3390/toxins14070424
Wohllebe S, Richter R, Richter P, Häder DP (2009) Photodynamic control of human pathogenic parasites in aquatic ecosystems using chlorophyllin and pheophorbid as photodynamic substances. Parasitol Res 104(3):593–600. https://doi.org/10.1007/s00436-008-1235-6
Yang L, Wen KS, Ruan X, Zhao YX, Wei F, Wang Q (2018) Response of plant secondary metabolites to environmental factors. Molecules 23(4):762. https://doi.org/10.3390/molecules23040762
Zharkov D, Nizamutdinov T, Dubovikoff D, Abakumov E, Pospelova A (2023) Navigating agricultural expansion in Harsh conditions in Rusia: balancing development with insect protection in the era of pesticides. Insects 14(6):557. https://doi.org/10.3390/insects14060557
Acknowledgements
The authors thank Irma L. Medina-Baizabal for her technical support with the plant extracts. MEC thanks CONACYT for a postgraduate student scholarship (No. 997980).
Funding
This research was financially supported by CONACYT project PDCPN-2015-266, Mexico.
Author information
Authors and Affiliations
Contributions
MCE-C helped in conceptualization, experimental data, analysis, and writing original draft; ER-S was involved in conceptualization, supervision, analysis, data curation, and manuscript revision; HSB-G contributed to analysis, manuscript revision; JM; FR helped in LC–UV–HRMS acquisition and analysis, manuscript revision; GM; JLT-M helped in plant material collects and taxonomical identification, manuscript revision; MG-A contributed to conceptualization, formal analysis, supervision, funding acquisition, project administration, manuscript revision.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Esquivel-Chi, M.C., Ruiz-Sánchez, E., Ballina-Gómez, H.S. et al. Repellent screening of ethanol extracts from plants of the Yucatan Peninsula against Bemisia tabaci (Gennadius, 1889) and chemical profile of Malpighia glabra L. leaves. J Plant Dis Prot 131, 811–821 (2024). https://doi.org/10.1007/s41348-024-00901-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-024-00901-5