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A sustainable approach in the management of Callosobruchus maculatus: essential oil of Protium heptaphyllum and its major compound d-limonene as biopesticides

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Abstract

The present study aimed to investigate the bioactivity of the essential oils of Protium heptaphyllum (Aubl.) (Sapindales: Burseraceae) and its major compound d-limonene in the control of Callosobruchus maculatus (Fabr.) (Coleoptera: Chrysomelidae: Bruchinae). The compounds in the oil were identified by gas chromatography–mass spectrometry (GC–MS). Contact toxicity, fumigation, and repellency tests were conducted. The lethal concentrations for the contact and fumigation tests were determined. In the repellency tests, the lethal concentrations previously determined in the contact test were used. The results showed that d-limonene was the major compound (40.1%) in the essential oil of P. heptaphyllum. d-limonene and P. heptaphyllum oil showed toxicity to C. maculatus in the contact and fumigation tests, and the oil showed higher toxicity (14.23 μL/20 g and 191.28 μL/L air), therefore being more toxic than d-limonene (36.42 μL/20 g and 437.34 μL/L air). The number of insects that emerged in the contact and repellency tests was reduced at all concentrations, which shows that the oil and d-limonene have an ovicidal effect. Repellent effects of P. heptaphyllum and d-limonene on C. maculatus were observed. The essential oil of P. heptaphyllum, which is more toxic than its major compound, has potential as an insecticide against C. maculatus.

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References

  • Adams RP (2009) Identification of essential oil components by Gas Chromatography Quadupole Mass Spectroscopy. Allured Publishing Corporation, Carol Stream, Illinois, p 804p

    Google Scholar 

  • Ajayi OE, Appel AG, Fadamiro HY (2014) Fumigation toxicity of essential oil monoterpenes to Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Journal of Insects 2014:1–7. https://doi.org/10.1155/2014/917212

    Article  Google Scholar 

  • Alves MS, Campos IM, Brito DMC, Cardoso CM, Pontes EG, Souza MAA (2019) Efficacy of lemongrass essential oil and citral in controlling Callosobruchus maculatus (Coleoptera: Chrysomelidae), a post-harvest cowpea insect pest. Crop Prot 119. https://doi.org/10.1016/j.cropro.2019.02.007

  • Armijos C, Valarezo E, Cartuche L, Zaragoza T, Finzi PV, Mellerio GG, Vidari G (2018) Chemical composition and antimicrobial activity of Myrcianthes fragrans essential oil, a natural aromatizer of the traditional Ecuadorian beverage colada morada. J Ethnopharmacol. https://doi.org/10.1016/j.jep.2018.07.018

    Article  PubMed  Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475. https://doi.org/10.1016/j.fct.2007.09.106

    Article  CAS  PubMed  Google Scholar 

  • Barbosa DRS (2015) Associação de constituintes químicos abundantes em óleos essenciais e cultivares resistentes no manejo de Callosobruchus maculatus (FABR., 1775) em feijão-caupi. Doctorate Tesis, Federal Rural University of Pernambuco.

  • Bertoli A, Cirak C, Teixeira da Silva JA (2011) Hypericum species as sources of valuable essential oils. Med Aromat Plant Sci Biotechnol 5:29–47

    Google Scholar 

  • Cabral RSC, Alves CCF, Batista HRF, Sousa WC, Abrahão IS, Crotti AEM, Santiago MB, Martins CHG, Miranda MLD (2018) Chemical composition of essential oils from different parts of Protium heptaphyllum (Aubl.) Marchand and their in vitro antibacterial activity. Natural Product Res. https://doi.org/10.1080/14786419.2018.1536659

  • Carvalho AFU, de Sousa NM, Farias DF, da Rocha-Bezerra LCB, da Silva RMP, Viana MP, Gouveia ST, Sampaio SS, de Sousa MB, de Lima GPG, de Morais SM, Barros CC, Filho FRF (2012) Nutritional ranking of 30 Brazilian genotypes of cowpeas including determination of antioxidant capacity and vitamins. J Food Compos Anal. https://doi.org/10.1016/j.jfca.2012.01.005

    Article  Google Scholar 

  • Castelo AVM, del Menezzi CHS, Resck IS (2010) Rendimenrteo e análises espectrosćópicas (RMN (1H, 13 C; IV) da química óleos essenciais de quatro plantas do cerrado. Cerne.

  • Chaubey MK (2019) Essential oils as green pesticides of stored grain insects. Euro J Biol Res 9:202–244. https://doi.org/10.5281/zenodo.3528365

    Article  CAS  Google Scholar 

  • Cheng W, Lei J, Ahn JE, Wang Y, Lei C, Zhu-Salzman K (2013) CO2 enhances effects of hypoxia on mortality, development, and gene expression in cowpea bruchid, Callosobruchus maculatus. J Insect Physiol. https://doi.org/10.1016/j.jinsphys.2013.08.009

  • Citó AMGL, Costa FB, Lopes JAD, Oliveira VMM, Chaves MH (2006) Identificação de constituintes voláteis de frutos e folhas de Protium heptaphyllum Aubl (March). Revista Brasileira De Plantas Medicinais 8(4):4–7

    Google Scholar 

  • de Dutra KA, de Oliveira, JV, Navarro DMAF, Barbosa DRS, Santos JPO (2016) Control of Callosobruchus maculatus (FABR.) (Coleoptera: Chrysomelidae: Bruchinae) in Vigna unguiculata (L.) WALP. with essential oils from four Citrus spp. plants. J Stored Prod Res 68:25–32. https://doi.org/10.1016/j.jspr.2016.04.001

    Article  Google Scholar 

  • DeCarlo A, Dosoky NS, Saytal P, Sorensen A, Setzer WN (2019) The essential oils of the Burseraceae. In: Malik S (ed) Essential oil research. Springer Nature, Cham. https://doi.org/10.1007/978-3-030-16546-8_4

  • Estevam EBB, De Deus IPB, Da Silva VP, Da Silva EAJ, Alves CCF, Alves JM, Cazal CM, Magalhães LG, Pagotti MC, Esperandim VR, Souza AF, Miranda MLD (2017) In vitro antiparasitic activity and chemical composition of the essential oil from Protium ovatum leaves (Burceraceae). An Acad Bras Ciênc. https://doi.org/10.1590/0001-3765201720170310

    Article  PubMed  Google Scholar 

  • Estevam EBB, Alves CCF, Esperandim VR, Cazal CM, Souza AF, Miranda MLD (2018) Chemical composition, anti-Trypanosoma cruzi and cytotoxic activities of the essential oil from green fruits of Protium ovatum (Burseraceae). Rev Bras Frutic. https://doi.org/10.1590/0100-29452018794

    Article  Google Scholar 

  • Fang R, Jiang CH, Wang XY, Zhang HM, Liu ZL, Zhou L, Du SS, Deng ZW (2010) Insecticidal activity of essential oil of Carum Carvi fruits from china and its main components against two grain storage insects. Molecules. https://doi.org/10.3390/molecules15129391

    Article  PubMed  PubMed Central  Google Scholar 

  • Gobbo-Neto L, Lopes NP (2007) Plantas medicinais: Fatores de influência no conteúdo de metabólitos secundários. Quim Nova. https://doi.org/10.1590/S0100-40422007000200026

    Article  Google Scholar 

  • Graver JEVS (2004) Guide to fumigation under gas-proof sheets. Food and Agriculture Organization of the United Nations: Australian Centre for International Agricultural Research. Camberra, p 176

  • Hoet S, Stévigny C, Héren MF, Quetin-Leclercq J (2006) Antitrypanosomal compounds from the leaf essential oil of Strychnos spinosa. Planta Med. https://doi.org/10.1055/s-2005-916255

    Article  PubMed  Google Scholar 

  • Ibrahim MA, Kainulainen P, Aflatuni A, Tiilikkala K, Holopainen JK (2001) Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to d-limonene and its suitability for control of insect pests. Agricultural and food science in Finland https://doi.org/10.23986/afsci.5697

  • Isman MB, Machial CM (2006) Chapter 2 Pesticides based on plant essential oils: from traditional practice to commercialization. Adv Phytomed. https://doi.org/10.1016/S1572-557X(06)03002-9

  • Iturralde-García RD, Borboa-Flores J, Cinco-Moroyoqui FJ, Riudavets J, Del Toro-Sánchez CL, Rueda-Puente EO, Martínez-Cruz O, Wong-Corral FJ (2016) Effect of controlled atmospheres on the insect Callosobruchus maculatus Fab. in stored chickpea. J Stored Products Res. https://doi.org/10.1016/j.jspr.2016.06.004

  • Khani A, Rahdari T (2012) Chemical composition and insecticidal activity of essential oil from Coriandrum sativum Seeds against Tribolium confusum and Callosobruchus maculatus. ISRN Pharmaceutics. https://doi.org/10.5402/2012/263517

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SIL, Lee DW (2014) Toxicity of basil and orange essential oils and their components against two coleopteran stored products insect pests. J Asia-Pacific Entomol. https://doi.org/10.1016/j.aspen.2013.09.002

    Article  Google Scholar 

  • Knaak N, Fiuza L (2010) Potencial dos óleos essenciais de plantas no controle de insetos e microrganismos. Neotropical Biol Conserv 5:120–132. https://doi.org/10.4013/nbc.2010.52.08

    Article  Google Scholar 

  • Krzyżowski M, Francikowski J, Baran B, Babczyńska A (2020) The short-chain fatty acids as potential protective agents against Callosobruchus maculatus infestation. J Stored Prod Res. https://doi.org/10.1016/j.jspr.2020.101570

    Article  Google Scholar 

  • Lee BH, Annis PC, Tumaalii F, Choi WS (2004) Fumigant toxicity of essential oils from the Myrtaceae family and 1,8-cineole against 3 major stored-grain insects. J Stored Prod Res. https://doi.org/10.1016/j.jspr.2003.09.001

    Article  Google Scholar 

  • Liang JY, Xu J, Yang YY, Shao YZ, Zhou F, Wang JL (2020) Toxicity and synergistic effect of Elsholtzia ciliata essential oil and its main components against the adult and larval stages of Tribolium castaneum. Foods. https://doi.org/10.3390/foods9030345

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang JY, Guo SS, Zhang WJ, Geng ZF, Deng ZW, Du SS, Zhang J (2018) Fumigant and repellent activities of essential oil extracted from Artemisia dubia and its main compounds against two stored product pests. Natural Product Res. https://doi.org/10.1080/14786419.2017.1331227

  • Lopes LM, Sousa AH, Santos VB, Silva GN, Abreu AO (2018) Development rates of Callosobruchus maculatus (Coleoptera: Chrysomelidae) in landrace cowpea varieties occurring in southwestern Amazonia. J Stored Prod Res. https://doi.org/10.1016/j.jspr.2018.01.008

    Article  Google Scholar 

  • Mahfuz I, Khalequzzaman M (2007) Contact and fumigant toxicity of essential oils against Callosobruchus maculatus. Univ J Zool Rajshahi Univ 26:63–66

    Article  Google Scholar 

  • Malaikozhundan B, Vinodhini J (2018) Nanopesticidal effects of Pongamia pinnata leaf extract coated zinc oxide nanoparticle against the pulse beetle, Callosobruchus maculatus. Mater Today Commun. https://doi.org/10.1016/j.mtcomm.2017.12.015

  • Marques DD, Sartori RA, Lemos TLG, Machado LL, de Souza JSN, Monte FJQ (2010) Chemical composition of the essential oils from two subspecies of Protium heptaphyllum. Acta Amazon. https://doi.org/10.1590/s0044-59672010000100029

    Article  Google Scholar 

  • Matos LF, Barbosa DRS, Lima EC, Dutra KA, Navarro DMAF, Alves JLR, Silva GN (2020) Chemical composition and insecticidal effect of essential oils from Illicium verum and Eugenia caryophyllus on Callosobruchus maculatus in cowpea. Ind Crops Prod 145:112088. https://doi.org/10.1016/j.indcrop.2020.112088

    Article  CAS  Google Scholar 

  • Mendes JL, De Araújo TF, Geraldo De Carvalho M, Júnior ACFE, Albuquerque Costa R (2019) Chemical composition and mechanism of vibriocidal action of essential oil from resin of Protium heptaphyllum. Science World Journal. https://doi.org/10.1155/2019/9563213

    Article  Google Scholar 

  • Mobin M, De Lima SG, Almeida LTG, Takahashi JP, Teles JB, Szeszs MW, Martins MA, Carvalho AA, Melhem MSC (2016) MDGC-MS analysis of essential oils from Protium heptaphyllum (Aubl.) and their antifungal activity against Candida specie. Revista Brasileira de Plantas Medicinais. https://doi.org/10.1590/1983-084x/15_110

  • Moreira-Araújo RSDR, Sampaio GR, Soares RAM, Da Silva CP, Araújo MADM, Arêas JAG (2018) Identificação e quantificação de compostos fenólicos e da atividade antioxidante no feijão-caupi em grãos da cultivar BRS Xique-xique. Revista Caatinga. https://doi.org/10.1590/1983-21252018v31n124rc

    Article  Google Scholar 

  • Murdock LL, Margam V, Baoua I, Balfe S, Shade RE (2012) Death by desiccation: Effects of hermetic storage on cowpea bruchids. J Stored Prod Res. https://doi.org/10.1016/j.jspr.2012.01.002

    Article  Google Scholar 

  • Murthy KSR, Reddy MC, Rani SS, Pullaiah T (2016) Bioactive principles and biological properties of essential oils of Burseraceae: a review. J Pharmacognosy Phytochem 5(2):247–258

    CAS  Google Scholar 

  • Mutlu Ç, Öğreten A, Kaya C, Mamay M (2019) Influence of different grain storage types on Khapra beetle, Trogoderma granarium Everts, 1898 (Coleoptera: Dermestidae), infestation in southeastern Anatolia (Turkey) and its resistance to malathion and deltamethrin. Turkish J Entomol 43(2):131–142. https://doi.org/10.16970/entoted.528623

    Article  Google Scholar 

  • Negahban M, Moharramipour S, Sefidkon F (2006) Chemical composition and insecticidal activity of Artemisia scoparia essential oil against three coleopteran stored-product insects. J Asia-Pacific Entomol. https://doi.org/10.1016/S1226-8615(08)60318-0

    Article  Google Scholar 

  • Oboh G, Ademosun AO, Olumuyiwa TA, Olasehinde TA, Ademiluyi AO, Adeyemo AC (2017) Insecticidal activity of essential oil from orange peels (Citrus sinensis) against Tribolium confusum, Callosobruchus maculatus and Sitophilus oryzae and its inhibitory effects on acetylcholinesterase and Na+/K+-ATPase activities. Phytoparasitica. https://doi.org/10.1007/s12600-017-0620-z

    Article  Google Scholar 

  • Oliveira JV, de França SM, Barbosa DRS, Dutra KA, Araujo AMN, Navarro DMAF (2017) Fumigation and repellency of essential oils against Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae) in cowpea. Pesquisa Agropecuaria Brasileira 52:10–17. https://doi.org/10.1590/S0100-204X2017000100002

    Article  Google Scholar 

  • Oliveira PV, Ferreira JC, Moura FS, Lima GS, De Oliveira FM, Oliveira PES, Conserva LM, Giulietti AM, Lemos RPL (2010) Larvicidal activity of 94 extracts from ten plant species of northeastern of Brazil against Aedes aegypti L. (Diptera: Culicidae). Parasitol Res. https://doi.org/10.1007/s00436-010-1880-4

  • Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and Constraints. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2016.10.005

  • Pontes WJT, De Oliveira JCG, Da Câmara CAG, Lopes ACHR, Gondim MGC, De Oliveira JV, Barros R, Schwartz MOE (2007) Chemical composition and acaricidal activity of the leaf and fruit essential oils of Protium heptaphyllum (Aubl.) Marchand (Burseraceae). Acta Amazonica. https://doi.org/10.1590/S0044-59672007000100012

  • Pourya M, Sadeghi A, Ghobari H, Taning CNT, Smagghe G (2018) Bioactivity of Pistacia atlantica desf. Subsp. Kurdica (Zohary) Rech. F. and Pistacia khinjuk stocks essential oils against Callosobruchus maculatus (F, 1775) (Coloeptera: Bruchidae) under laboratory conditions. J Stored Products Res. https://doi.org/10.1016/j.jspr.2018.03.007

  • Rajendran S, Sriranjini V (2008) Plant products as fumigants for stored-product insect control. J Stored Prod Res. https://doi.org/10.1016/j.jspr.2007.08.003

    Article  Google Scholar 

  • Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol. https://doi.org/10.1146/annurev-ento-120710-100554

    Article  PubMed  Google Scholar 

  • Reis SL, Mantello AG, Macedo JM, Gelfuso EA, Da Silva CP, Fachin AL, Cardoso AM, Beleboni RO (2016) Typical monoterpenes as insecticides and repellents against stored grain pests. Molecules. https://doi.org/10.3390/molecules21030258

    Article  PubMed  PubMed Central  Google Scholar 

  • Saad MMG, Abou-Taleb HK, Abdelgaleil SAM (2018) Insecticidal activities of monoterpenes and phenylpropenes against sitophilus oryzae and their inhibitory effects on acetylcholinesterase and adenosine triphosphatases. Appl Entomol Zool. https://doi.org/10.1007/s13355-017-0532-x

    Article  Google Scholar 

  • SAS Institute (2001) User’s Guide, Version 8.02, TS Level 2MO. SAS Institute Inc., Cary, NC.

  • Siani AC, Ramos MFS, Menezes-De-Lima O, Ribeiro-Dos-Santos R, Fernadez-Ferreira E, Soares ROA, Rosas EC, Susunaga GS, Guimarães AC, Zoghbi MGB, Henriques MGMO (1999) Evaluation of anti-inflammatory-related activity of essential oils from the leaves and resin of species of Protium. J Ethnopharmacol. https://doi.org/10.1016/S0378-8741(98)00148-2

    Article  PubMed  Google Scholar 

  • Siani AC, Garrido IS, Monteiro SS, Carvalho ES, Ramos MFS (2004) Protium icicariba as a source of volatile essences. Biochem Syst Ecol. https://doi.org/10.1016/j.bse.2003.11.003

    Article  Google Scholar 

  • Teke MA, Mutlu Ç (2021) Insecticidal and behavioral effects of some plant essential oils against Sitophilus granarius L. and Tribolium castaneum (Herbst). J Plant Dis Prot 128:109–119. https://doi.org/10.1007/s41348-020-00377-z

  • Toudert-Taleb K, Hedjal-Chebheb M, Hami H, Debras J-F, Kellouche A (2014) Composition of essential oils extracted from six aromatic plants of Kabylian Origin (Algeria) and evaluation of their bioactivity on Callosobruchus maculatus (Fabricius, 1775) (Coleoptera: Bruchidae). African Entomol. https://doi.org/10.4001/003.022.0220

    Article  Google Scholar 

  • Tripathi AK, Prajapati V, Khanuja SPS, Kumar S (2003) Effect of d-limonene on three stored-product beetles. J Econ Entomol. https://doi.org/10.1093/jee/96.3.990

    Article  PubMed  Google Scholar 

  • Vasantharaja R, Abraham LS, Inbakandan D, Thirugnanasambandam R, Senthilvelan T, Jabeen SKA, Prakash P (2019) Influence of seaweed extracts on growth, phytochemical contents and antioxidant capacity of cowpea (Vigna unguiculata L. Walp). Biocatal Agric Biotechnol. https://doi.org/10.1016/j.bcab.2019.01.021

  • Violante IMP, Hamerski L, Silva Garcez W, Lucia Batista A, Rodrigues Chang M, Joana Pott V, Rodrigues Garcez F (2012) Antimicrobial activity of some medicinal plants from the Cerrado of the central-western region of Brazil. Braz J Microbiol. https://doi.org/10.1590/S1517-83822012000400009

    Article  PubMed  PubMed Central  Google Scholar 

  • Wakil W, Riasat T, Lord JC (2013) Effects of combined thiamethoxam and diatomaceous earth on mortality and progeny production of four Pakistani populations of Rhyzopertha dominica (Coleoptera: Bostrichidae) on wheat, rice and maize. J Stored Prod Res. https://doi.org/10.1016/j.jspr.2012.09.002

    Article  Google Scholar 

  • Yang K, Wang CF, You CX, Geng ZF, Sun RQ, Guo SS, Du SS, Liu ZL, Deng ZW (2014) Bioactivity of essential oil of Litsea cubeba from China and its main compounds against two stored product insects. J Asia-Pacific Entomol. https://doi.org/10.1016/j.aspen.2014.03.011

    Article  Google Scholar 

  • You CX, Wang Y, Zhang WJ, Yang K, Wu Y, Geng ZF, Chen HP, Jiang HY, Du SS, Deng ZW, Liu ZL (2014) Chemical compounds and biological activities of the purple perilla essential oil against Lasioderma serricorne. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2014.07.021

    Article  Google Scholar 

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RMBAR; Fontes, LS participated in all stages of manuscript production; AMGLC and ISC contributed to the chromatographic analysis; RCB and EMJS participated in the execution of the experiments; DRSB and GNS contributed with statistical analysis and helped to write the manuscript.

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Correspondence to Douglas Rafael e Silva Barbosa.

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de Andrade Rodrigues, R.M.B., da Silva Fontes, L., de Carvalho Brito, R. et al. A sustainable approach in the management of Callosobruchus maculatus: essential oil of Protium heptaphyllum and its major compound d-limonene as biopesticides. J Plant Dis Prot 129, 831–841 (2022). https://doi.org/10.1007/s41348-022-00617-4

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