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Toxicity of Piper aduncum (Piperaceae) Essential Oil Against Euschistus heros (F.) (Hemiptera: Pentatomidae) and Non-Effect on Egg Parasitoids

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Abstract

Plant essential oils have been recognized as significant natural resources for insecticides. Herein, we have assessed the toxicity of the essential oil of Piper aduncum (Piperaceae) against Euschistus heros (F.) (Hemiptera: Pentatomidae), a key soybean pest in Neotropical America. In addition, we have assessed its effect on the performance of egg parasitoids. The essential oil was obtained from the leaves of P. aduncum via hydrodistillation. Subsequently, bioassays of the concentration response to eggs (contact and immersion methods), nymphs, and adults (topical application) were conducted, to assess the lethal effects on the stink bug. We also evaluated the performance of parasitism and adult emergence of egg parasitoids, when the host eggs were treated with essential oil. In the egg bioassay, both exposure methods were efficient for unviable eggs (immersion LC50 = 15.64 mg mL−1; contact LC50 = 21.29 mg mL−1), with the highlight on the immersion method. The bioassay with nymphs indicated a higher toxicity of essential oil, with lower concentrations (LC50 = 11.37 mg mL−1) being required to cause the death of insects. For adults, a reduction in survival of insects was observed, and consequently, there was a reduction in the number of individuals in the next generation. Although the essential oil was toxic to E. heros, it exhibited lower toxicity for egg parasitoids, as there was no effect on parasitism and the emergence of wasps. We discuss likely explanations for such selectivity. In summary, we found that the essential oil was promising for the control of E. heros, because it caused deleterious effects at all development stages of the stink bug and had no effect on parasitism and emergence of the egg parasitoids, which suggested compatibility with biological control.

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References

  • Abudulai M, Shepard BM (2003) Effects of neem Azadirachta indica A. Juss on Trissolcus basalis Wollaston (Hymenoptera: Scelionidae), a parasitoid of Nezara viridula L. Hemiptera: Pentatomidae. J Entomol Sci 38:386–397

    CAS  Google Scholar 

  • Abudulai M, Shepard BM, Mitchell PL (2003) Antifeedant and toxic effects on a neem Azadirachta indica (A. Juss) based formulation neemix against Nezara viridula (L.) (Hemiptera: Pentatomidae). J Entomol Sci 38:398–408

    CAS  Google Scholar 

  • Almeida RRP, Souto RNP, Bastos CN, Silva MHL, Maia JGS (2009) Chemical variation in Piper aduncum and biological properties of its dillapiole-rich essential oil. Chem Biodivers 6:1427–1434. doi:10.1002/cbdv.200800212

    Article  PubMed  Google Scholar 

  • Assis A, Brito V, Bittencourt M, Silva L, Oliveira F, Oliveira R (2013) Essential oils composition of four Piper species from Brazil. J Essent Oil Res 25:203–209. doi:10.1080/10412905.2013.767755

    Article  CAS  Google Scholar 

  • Austin AD, Johnson NF, Dowton M (2005) Systematics, evolution, and biology of scelionid and platygastrid wasps. Annu Rev Entomol 50:553–582. doi:10.1146/annurev.ento.50.071803.130500

    Article  CAS  PubMed  Google Scholar 

  • Bernard CB, Krishnamurty HG, Chauret D, Drust T, Philogene BJR, Sanchez-Vindas P, Hasbun C, Poveda L, San-Román L, Arnason JT (1995) Insecticidal defenses of Piperaceae from the neotropics. J Chem Ecol 21:801–814

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS One 8:e76548. doi:10.1371/journal.pone.0076548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boulogne I, Petit P, Ozier-Lafontaine H, Desfontaines L, Loranger-Merciris G (2012) Insecticidal and antifungal chemicals produced by plants: a review. Environ Chem Lett 10:325–347. doi:10.1007/s10311-012-0359-1

    Article  CAS  Google Scholar 

  • Coitinho RLBC, Oliveira JV, Gondim-Junior MGC, Câmara CAG (2011) Toxicidade por fumigação, contato e ingestão de óleos essenciais para Sitophilus zeamais Motschulsky, 1885 (Coleoptera: Curculionidae). Cienc Agrotecnol 35:172–178. doi:10.1590/S1413-70542011000100022

    Article  CAS  Google Scholar 

  • Corrêa-Ferreira BS, Azevedo J (2002) Soybean seed damage by different species of stink bugs. Agric For Entomol 4:145–150. doi:10.1046/j.1461-9563.2002.00136.x

    Article  Google Scholar 

  • Costa MLM, Borges M, Vilela EF (1998) Biologia reprodutiva de Euschistus heros (F.) (Heteroptera:Pentatomidae). An Soc Entomol Bras 27:559–568. doi:10.1590/S0301-80591998000400008

  • El-Wakeil NE (2013) Botanical pesticides and their mode of action. Gesunde Pflanzen 65:125–149. doi:10.1007/s10343-013-0308-3

    Article  CAS  Google Scholar 

  • Estrela JLV, Fazolin M, Catani V, Alécio MR, Lima MS (2006) Toxicidade de óleos essenciais de Piper aduncum e Piper hispidinervum em Sitophilus zeamais. Pesq Agrop Brasileira 41:217–222. doi:10.1590/S0100-204X2006000200005

    Article  Google Scholar 

  • Fazolin M, Estrela JLV, Catani V, Lima MS, Alécio MR (2005) Toxicidade do óleo de Piper aduncum L. a adultos de Cerotoma tingomarianus Bechyné (Coleoptera: Chrysomelidae). Neotrop Entomol 34:485–489. doi:10.1590/S1519-566X2005000300018

    Article  Google Scholar 

  • Fazolin M, Estrela JLV, Catani V, Alécio MR, Lima MS (2007) Propriedade inseticida dos óleos essenciais de Piper hispidinervum C. DC.; Piper aduncum L. e Tanaecium nocturnum (Barb. Rodr.) Bur. and K. Shum sobre Tenebrio molitor L., 1758. Cienc Agrotecnol 31:113–120. doi:10.1590/S1413-70542007000100017

    Article  CAS  Google Scholar 

  • Foerster LA (2002) Seletividade de inseticidas a predadores e parasitóides.: Controle biológico no Brasil: parasitóides e predadores. In: Parra JRP, Botelho PSM, Corrêa-Ferreira BS, Bento JMS (eds) Controle biológico no Brasil: parasitóides e predadores. São Paulo, pp 95–114

  • Golin V, Loiácono M, Margaría C, Aquino D (2011) Natural incidence of egg parasitoids of Edessa meditabunda (F.) (Hemiptera: Pentatomidae) on Crotalaria spectabilis in Campo Novo do Parecis, MT, Brazil. Neotrop Entomol 40:617–618. doi:10.1590/S1519-566X2011000500015

    PubMed  Google Scholar 

  • Krinski D, Massaroli A (2014) Nymphicidal effect of vegetal extracts of Annona mucosa and Anonna crassiflora (Magnoliales, Annonaceae) against rice stalk stink bug, Tibraca limbativentris (Hemiptera, Pentatomidae). Rev Bras Frutic 36:217–224. doi:10.1590/S0100-29452014000500026

    Article  Google Scholar 

  • Laumann RA, Moraes MCB, Silva JP, Vieira AMC, Silveira S, Borges M (2010) Egg parasitoid wasps as natural enemies of the neotropical stink bug Dichelops melacanthus. Pesq Agrop Brasileira 45:442–449. doi:10.1590/S0100-204X2010000500002

    Article  Google Scholar 

  • Maia JGS, Zohhbi MGB, Andrade EHA, Santos AS, Silva MJL, Luz AIR, Bastos CN (1998) Constituents of the essential oil of Piper aduncum L. growing wild in the Amazon region. Flavour Fragance J 13:269–272. doi:10.1002/(SICI)1099-1026(1998070)13:4<269::AID-FFJ744>3.0.CO;2-A

    Article  CAS  Google Scholar 

  • Misni N, Othman H, Sulaiman S (2011) The effect of Piper aduncum Linn. (Family: Piperaceae) essential oil as aerosol spray against Aedes aegypti (L.) and Aedes albopictus Skuse. Trop Biomed 28:249–258

    PubMed  Google Scholar 

  • Mitchell PL, Gupta R, Singh AK, Kumar P (2004) Behavioral and developmental effects of neem extracts on Clavigralla scutellaris (Hemiptera: Heteroptera: Coreidae) and its egg parasitoid, Gryon fulviventre (Hymenoptera: Scelionidae). J Econ Entomol 97:916–923. doi:10.1093/jee/97.3.916

    Article  CAS  PubMed  Google Scholar 

  • Mithofer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450. doi:10.1146/annurev-arplant-042110-103854

    Article  PubMed  Google Scholar 

  • Morais SM, Facundo VA, Bertini LM, Cavalcanti ESB, Anjos JF, Ferreira SA, Brito ES, Souza-Neto MA (2007) Chemical composition and larvicidal activity of essential oils from Piper species. Biochem Syst Ecol 35:670–675. doi:10.1016/j.bse.2007.05.002

    Article  Google Scholar 

  • Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378. doi:10.1016/j.biortech.2009.07.048

    Article  CAS  PubMed  Google Scholar 

  • Orr DB (1988) Scelionid wasps as biological control agents: a review. Fla Entomol 71:506–528

    Article  Google Scholar 

  • Peres WAA, Corrêa-Ferreira BS (2004) Methodology of mass multiplication of Telenomus podisi Ash. and Trissolcus basalis (Woll.) (Hymenoptera: Scelionidae) on eggs of Euschistus heros (Fab.) (Hemiptera: Pentatomidae). Neotrop Entomol 33:457–462. doi:10.1590/S1519-566X2004000400010

    Article  Google Scholar 

  • Pinheiro PV, Quintela ED (2010) Efeito inseticida e deterrente do óleo de nim em machos e fêmeas de Oebalus Poecilus (Hemiptera: Pentatomidae). Pesqui Agrop Trop 40:394–400. doi:10.1590/S1983-40632010000400018

    Article  Google Scholar 

  • Piton LP, Turchen LM, Butnariu AR, Pereira MJB (2014) Natural insecticide based-leaves extract of Piper aduncum (Piperaceae) in the control of stink bug brown soybean. Ciênc Rural 44:1915–1920. doi:10.1590/0103-8478cr20131277

    Article  Google Scholar 

  • Potzernheim MCL, Bizzo HR, Silva JP, Vieira RF (2012) Chemical characterization of essential oil constituents of four populations of Piper aduncum L. from Distrito Federal, Brazil. Biochem Syst Ecol 42:25–31. doi:10.1016/j.bse.2011.12.025

    Article  CAS  Google Scholar 

  • Prista LN, Alves AC, Morgado RMR (1981) Técnica farmacêutica e farmácia galênica. Calouste Gulbenkian, Lisboa, p 147

    Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. URL http://www.R-project.org/

  • Riba MJ, Martí J, Sans A (2003) Influence of azadirachtin on development and reproduction of Nezara viridula L. (Het., Pentatomidae). J Appl Entomol 127:37–41. doi:10.1046/j.1439-0418.2003.00684.x

    Article  CAS  Google Scholar 

  • Sahayaraj K, Kalidas S (2011) Evaluation of nymphicidal and ovicidal effect of a seaweed, Padina pavonica (Linn.) (Phaeophyceae) on cotton pest, Dysdercus cingulatus (Fab.). Indian J Geo-Mar Sci 40:125–129

    CAS  Google Scholar 

  • Scott IM, Jensen HR, Philogène BJR, Arnason JT (2007) A review of Piper spp. (Piperaceae) phytochemistry, insecticidal activity and mode of action. Phytochem Rev 7:65–75. doi:10.1007/s11101-006-9058-5

    Article  Google Scholar 

  • Silva CC, Laumann RA, Blassioli MC, Pareja M, Borges M (2008) Euschistus heros mass rearing technique for the multiplication of Telenomus podisi. Pesq Agrop Brasileira 43:575–580. doi:10.1590/S0100-204X2008000500004

    Google Scholar 

  • Silva FA, Calizotti GS, Panizzi AR (2011) Survivorship and egg production of phytophagous pentatomids in laboratory rearing. Neotrop Entomol 40:35–38. doi:10.1590/S1519-566X2011000100005

    Article  CAS  PubMed  Google Scholar 

  • Silva FAC, Silva JJ, Depieri RA, Panizzi A (2012) Feeding activity, salivary amylase activity, and superficial damage to soybean seed by adult Edessa meditabunda (F.) and Euschistus heros (F.) (Hemiptera: Pentatomidae). Neotrop Entomol 41:386–390. doi:10.1007/s13744-012-0061-9

    Article  CAS  PubMed  Google Scholar 

  • Silva VP, Pereira MJB, Turchen LM (2013) Efeito de extratos vegetais no controle de Euschistus heros (F.) (Hemiptera: Pentatomidae) em lavoura de soja na região sudoeste do Estado de Mato Grosso. Rev Agric 88:185–190

    Google Scholar 

  • Singha A, Thareja V, Singh AK (2007) Application of neem seed kernel extracts result in mouthpart deformities and subsequent mortality in Nezara viridula (L.) (Hem: Pentatomidae). J Appl Entomol 131:197–201. doi:10.1111/j.1439-0418.2006.01134.x

    Article  Google Scholar 

  • Smaniotto LF, Gouvea A, Potrich M, Silva ERL, Silva J, Pegorini CS (2013) Selectivity of alternative products to Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Semina Cienc Agrar 34:3295–3306

    Google Scholar 

  • Sosa-Gomez DR, Silva JJ (2010) Neotropical brown stink bug (Euschistus heros) resistance to methamidophos in Paraná, Brazil. Pesq Agrop Brasileira 45:767–769. doi:10.1590/S0100-204X2010000700019

    Article  Google Scholar 

  • Souto RNP, Harada AY, Andrade EHA, Maia JGS (2012) Insecticidal activity of Piper essential oils from the amazon against the fire ant Solenopsis saevissima (Smith) (Hymenoptera: Formicidae). Neotrop Entomol 41:510–517. doi:10.1007/s13744-012-0080-6

    Article  CAS  PubMed  Google Scholar 

  • Souza EM, Cordeiro JR, Pereira MJB (2007) Avaliação da atividade inseticida dos diferentes extratos das sementes de Annona coriacea sobre Dichelops melacanthus (Dallas, 1851). Rev Bras Agroecologia 2:1107–1110

    Google Scholar 

  • Turchen LM, Golin V, Butnariu AR, Pereira MJB (2014) Selectivity of Annona (Annonaceae) extract on egg parasitoid Trissolcus urichi Crawford, 1913 (Hymenoptera: Platygastridae). Rev Colomb Entomol 40:176–180

    Google Scholar 

  • Turchen LM, Golin V, Butnariu AR, Guedes RNC, Pereira MJB (2016) Lethal and sublethal effects of insecticides on the egg parasitoid Telenomus podisi (Hymenoptera: Platygastridae). J Econ Entomol 109:84–92. doi:10.1093/jee/tov273

    Article  CAS  PubMed  Google Scholar 

  • Volpe XLH, Fazolin M, Garcia RB, Magnani RF, Barbosa JC, Miranda MP (2015) Efficacy of essential oil of Piper aduncum against nymphs and adults of Diaphorina citri. Pest Manag Sci. doi:10.1002/ps.4143

    PubMed  Google Scholar 

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Acknowledgments

The authors thanks the Fundação de Amparo a Pesquisa do Estado de Mato Grosso (FAPEMAT) for financial assistance (process number: 163079/2014), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for providing Masters scholarship (process number: 134392/2015-9), and Dr. Norman Johnson for confirmation of species of Telenomus podisi and Trissolcus urichi.

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Authors and Affiliations

  1. Dept of Entomology, Univ Federal de Viçosa, Viçosa, MG, Brasil

    L M Turchen

  2. Dept of Agronomy, Univ do Estado de Mato Grosso, Tangará da Serra, MT, Brasil

    L P Piton, A R Butnariu & M J B Pereira

  3. Dept of Chemistry, Univ Federal do Mato Grosso, Cuiabá, MT, Brasil

    E L Dall’Oglio

  4. Depto de Entomologia, Programa de Pós Graduação em Entomologia, Univ Federal de Viçosa, Viçosa, MG, 36570-000, Brasil

    L M Turchen

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  1. L M Turchen
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  4. A R Butnariu
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Correspondence to L M Turchen.

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Turchen, L.M., Piton, L.P., Dall’Oglio, E.L. et al. Toxicity of Piper aduncum (Piperaceae) Essential Oil Against Euschistus heros (F.) (Hemiptera: Pentatomidae) and Non-Effect on Egg Parasitoids. Neotrop Entomol 45, 604–611 (2016). https://doi.org/10.1007/s13744-016-0409-7

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