Abstract
The effects of a bioinsecticide formulation based on extract of Annona squamosa L. (Annonaceae) containing 10,000 mg L−1 of acetogenin annonin as the main active ingredient were investigated against three primary pest species of stored grains in Brazil [maize weevil Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), Mexican bean weevil Zabrotes subfasciatus (Boheman) (Coleoptera: Chrysomelidae: Bruchinae), and cowpea weevil Callosobruchus maculatus (Fabricius) (Coleoptera: Chrysomelidae: Bruchinae)] by means of residual contact bioassays. In a concentration-dependent manner, the annonin-based commercial bioinsecticide caused significant adult mortality of C. maculatus (LC50 = 6890 μL kg−1), S. zeamais (LC50 = 2781 μL kg−1), and Z. subfasciatus (LC50 = 2120 μL kg−1) after 120 h of residual contact exposure. In addition to acute toxicity, the tested bioinsecticide also promoted a significant reduction of the number of eggs laid by females of C. maculatus (EC50 = 5949.7 μL kg−1) and Z. subfasciatus (EC50 = 552.7 μL kg−1). Moreover, the bioinsecticide significantly reduced the number of emerged insects (F1 generation) of C. maculatus (EC50 = 2763.0 μL kg−1), S. zeamais (EC50 = 1380.8 μL kg−1), and Z. subfasciatus (EC50 = 561.5 μL kg−1). The bioinsecticide also reduced the percentage of damaged grains for the three pest species studied, and its grain-protectant properties are comparable to or superior in efficacy in relation to a diatomaceous earth-based insecticide (Insecto® at 1000 mg kg−1) used as a positive control. Thus, this standardized formulation has promising bioactivity against stored insect species and can be a useful component for IPM of stored grains in Brazil and elsewhere.
Similar content being viewed by others
References
Agrofit (2016) Sistema de Agrotóxicos Fitossanitários-Ministério da Agricultura, Pecuária e Abastecimento, Brasil, 2016. http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Acessed 10 January 2016
Alberti G, Coons LB (1999) Acari: mites. Integument. In: Harrison FW, Foelix RF (eds) Microscopic anatomy of invertebrates. Chelicerate Arthropoda, Hardcover, New York, pp 681–714
Álvarez O, Barrachina I, Ayala I, Gonçalvez M, Moya P, Neske A, Bardón A (2008) Toxic effects of annonaceous acetogenins on Oncopeltus fasciatus. J Pest Sci 81:85–89
Ansante TF, Ribeiro LP, Bicalho KU, Fernandes JB, Silva MFGF, Vieira PC, Vendramim JD (2015) Secondary metabolites from Neotropical Annonaceae: screening, bioguided fractionation, and toxicity to Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Ind Crop Prod 74:969–976
Athanassiou CG, Kavallieratos NG, Tsaganou FC, Dimizas CB, Buchelos CT (2003) Effect of grain type on the insecticidal efficacy of Silico Sec against Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Crop Prot 22:1141–1147
Athanassiou CG, Kavallieratos NG, Vayias B, Panoussakis EC (2008) Influence of grain type on the susceptibility of different rearing media, to three diatomaceous earth formulations. J Stored Prod Res 44:279–284
Braga LS, Corrêa AS, Pereira EJG, Guedes RNC (2011) Face or flee? Fenitrothion resistance and behavioral response in populations of the maize weevil, Sitophilus zeamais. J Stored Prod Res 47:161–167
Dharmasena CM, Blaney WM, Simmonds MSJ (2001) Effect of storage on the efficacy of powdered leaves of Annona squamosa for the control of Callosobruchus maculatus on cowpeas (Vigna unguiculata). Phytoparasitica 29:191–196
González-Coloma A, Guadaño A, Inés C, Martínez-Díaz R, Cortes D (2002) Selective action of acetogenin mitochondrial complex I inhibitors. Z Natuforsch 57:1028–1034
Hinde J, Demétrio CGB (1998) Overdispersion: models and estimation. Comput Stat Data Anal 27:151–170
Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19:140–145
Isman MB, Seffrin R (2014) Natural insecticides from the Annonaceae: a unique example for developing biopesticides. In: Singh D (ed) Advances in plant biopesticides. Springer, New Delhi, pp 21–33
Johnson HA (2000) Thwarting resistance: annonaceous acetogenins as news pesticidal and antitumor agents. In: Cutler SJ, Cutler HG (eds) Biologically active natural products: pharmaceuticals. CRC Press, Boca Raton, London, New York, Washington, pp 173–184
Khalequzzaman M, Sultana S (2006) Insecticidal activity of Annona squamosa L. seed extracts against the red flour beetle, Tribolium castaneum (Herbst). J Bio-Science 14:107–112
Kirti S, Sambasiva RN, Islam SN, Mala S (2013) Joint action between fraction IX of ethyl acetate extract of custard apple and azadirachtin in controlling rice moth, Corcyra cephalonica and khapra beetle, Trogoderma granarium in storage. Pestic Res J 106:106–111
Nelder JA, Wedderburn RWM (1972) Generalized linear models. J Royal Stat Soc 135:370–384
Ocampo D, Ocampo R (2006) Bioactividad de la família Annonaceae. Rev Univ Caldas 1:135–155
Parvin S, Islam E, Rahman M, Haque E (2003) Pesticidal activity of pure compound annotemoyin-1 isolated from chloroform extract of the plant Annona squamosa Linn. against Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Pakistan J Biol Sci 6:1088–1091
Pereira CJ, Pereira EJG, Cordeiro EMG, Della Lucia TMC, Tótola MR, Guedes RNC (2009) Organophosphate resistance in the maize weevil Sitophilus zeamais: magnitude and behavior. Crop Prot 28:168–173
Pimentel MAG, Faroni LRD’S, Guedes RNC, Sousa AH, Tótola MR (2009) Phosphine resistance in Brazilian populations of Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). J Stored Prod Res 45:71–74
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rao NS, Sharma K, Sharma RK (2005) Anti-feedant and growth inhibitory effects of seed extracts of custard apple Annona squamosa against khapra beetle, Trogoderma granarium. J Agric Technol 1:43–54
Ribeiro LP, Vendramim JD, Andrade MS, Bicalho KU, Fernandes MFGF, Vieira PC, Fernandes JB (2014) Tropical plants extracts as sources of grain protectant compounds against Sitophilus zeamais. Neotrop Entomol 43:470–482
Ribeiro LP, Vendramim JD, Bicalho KU, Andrade MS, Fernandes JB, Moral RA, Demétrio CGB (2013) Annona mucosa Jacq. (Annonaceae): a promising source of bioactive compounds against Sitophilus zeamais Mots. (Coleoptera: Curculionidae). J Stored Prod Res 55:6–14
Ribeiro LP, Vendramim JD, Gonçalves GLP, Ansante TF, Gloria EM, Lopes JC, Mello-Silva R, Fernandes JB (2016) Searching for promising sources of grain protectors in extracts from Neotropical Annonaceae. Blacpma 15:215–232
Sas Institute (2011) Statistical analysis system: getting started with the SAS learning. Version 9.2. SAS Institute, Cary
Seffrin RC, Shikano I, Akhtar Y, Isman MB (2010) Effects of crude seed extracts of Annona atemoya and Annona squamosa L. against the cabbage looper, Trichoplusia ni in the laboratory and greenhouse. Crop Prot 29:20–24
Sims SR, Greenplate JT, Stone B, Caprio MA, Gould F (1996) Monitoring strategies for early detection of Lepidoptera resistance to Bacillus thuringiensis insecticidal proteins. In: Brown TM (ed) Molecular genetics and evolution of pesticide resistance. American Chemical Society, Washington, DC, pp 229–242
Vassilakos TN, Athanassiou CG, Tsiropoulos NG (2015) Influence of grain type on the efficacy of spinotoram for the control of Rhyzopertha dominica, Sitophilus granarius and Sitophilus oryzae. J Stored Prod Res 64:1–7
Viegas Júnior C (2003) Terpenos com atividade inseticida: uma alternativa para o controle químico de insetos. Quim Nov. 26:390–400
Willer H, Kilcher L (2009) The world of organic agriculture. Statistics and emerging trends. Bonn (Germany): IFOAM
Zanardi OZ, Ribeiro LP, Ansante TF, Santos MS, Bordini GP, Yamamoto PT, Vendramim JD (2015) Bioactivity of a matrine-based biopesticide against four pest species of agricultural importance. Crop Prot 67:160–167
Acknowledgments
The authors thank the São Paulo State Research Foundation (FAPESP-grant number 2010/52638-0) and the National Council for Scientific and Technological Development (CNPq-grant number 140651/2013-6) for the financial support and scholarships granted.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Lessando Moreira Gontijo – UFV
Rights and permissions
About this article
Cite this article
Ribeiro, L.P., Zanardi, O.Z., Gonçalves, G.L.P. et al. Toxicity of an Annonin-Based Commercial Bioinsecticide Against Three Primary Pest Species of Stored Products. Neotrop Entomol 47, 145–151 (2018). https://doi.org/10.1007/s13744-017-0510-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-017-0510-6