Abstract
Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) causes significant losses in corn crops and necessitates the use of alternative control strategies, such as the application of bioinsecticides. We report the effect of methanolic leaf extracts of Annona dioica, Annona cacans, and Annona coriacea on the development and reproduction of S. frugiperda. A quantitative analysis was carried out to determine the total concentration of phenolics, flavonoids, and condensed tannin (CT) in leaf extracts. Corn leaves were immersed in a 1% methanolic leaf extract solution and fed to second instars of S. frugiperda. Leaf disks dipped in the synthetic insecticide Connect® (Bayer CropScience Ltda) composed of a neonicotinoid (imidacloprid) and a pyrethroid (β-cyfluthrin), which are harmful to S. frugiperda, was used as positive control. Distilled water was used as a negative control treatment. The leaf extract of A. coriacea decreased larval survivorship, arrested pupal development, and affected the weight gain of S. frugiperda. A. dioica also affected larval survivorship, but its effects were more pronounced for the adult stage, as fecundity, fertility, egg hatchability, and embryonic development were severely affected. Leaf extracts from A. cacans had no effect on S. frugiperda. The leaf extracts of A. dioica and A. coriacea showed a higher content of flavonoids and phenols, respectively. Our results indicated that both A. dioica and A. coriacea have the potential for development as botanical insecticides.
Similar content being viewed by others
References
Andrews KL (1988) Latin American research on Spodoptera frugiperda (Lepidoptera: Noctuidae). Fla Entomol 71:630–650
Blessing LT, Cólom OA, Popich S, Neske A, Bardón A (2010) Antifeedant and toxic effects of acetogenins from Annona montana on Spodoptera frugiperda. J Pest Sci 83:307–310
Boeke SJ, Kossou DK, Van Huis A, Van Loon JJA, Dicke M (2004) Field trials with plant products to protect stored cowpea against insect damage. Int J Pest Manag 50:1–9
Bogorni PC, Vendramim JD (2003) Bioatividade de extratos aquosos de Trichilia spp. sobre S. frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) em milho. Neotrop Entomol 32:665–669
Bowman DD (2006) Georgis Parasitologia Veterinária. Manole, Barueri, p 422
Breuer M, Hoste B, De Loof A, Nagvi SNH (2003) Effect of Melia azedarach extract on the activity of NADPH-cytochrome c reductase and cholinesterase in insects. Pestic Biochem Physiol 76:99–103
Carpinella MC, Ferrayoli C, Valladares G, Defago M, Palacios S (2002) Potent limonoid insect antifeedant from Melia azedarach. Biosci Biotechnol Biochem 66:1731–1736
Cavé A, Figadère B, Laurens A, Cortes D (1997) Acetogenins from Annonaceae. Fortschr Chem Org Naturst Prog Chem Org Nat Prod 70:81–288
Cechinel Filho V, Yunes RA (1998) Estratégias para a obtenção de compostos farmacologicamente ativos a partir de plantas medicinais, conceitos sobre modificação estrutural para a otimização da atividade. Quim Nova 21:99–105
Coelho MB, Marangoni S, Macedo MLR (2007) Insecticidal action of Annona coriacea lectin against the flour moth Anagasta kuehniella and the rice moth Corcyra cephalonica (Lepidoptera: Pyralidae). Comp Biochem Physiol 146:406–414
Costa ELN, Silva RFP, Fiuza LM (2004) Efeitos, aplicações e limitações de extratos de plantas inseticidas. Acta Biol Leopold 26:173–185
Cronquist A (1993) An integrated system of classification of flowering plants. Columbia University Press, New York, p 1262
Dos Santos PRD, Morais AA, Braz-Filho R (2003) Alkaloids from Annona dioica. J Braz Chem Soc 14:396–400
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec (UFLA) 35:1039–1042
Formagio ASN, Kassuya CAL et al (2013) The flavonoid content and antiproliferative, hypoglycaemic, anti-inflammatory and free radical scavenging activities of Annona dioica St. Hill. BMC Complement Altern Med 13:14
Gobbo-Neto L, Lopes NP (2007) Plantas medicinais: fatores de influência no conteúdo de metabólitos secundários. Quim Nova 30:374–381
Harborne JB, Williams CA (2000) Advances in flavonoids research since 1992. Phytochemistry 55:481–504
Hernández CR (2001) Plantas contra Plagas—potencial práctico de ajo, anona, nim, chile y tabaco. RAPAM, Estado de México, p 133
Hernández CR, Angel DN (1997) Anonáceas con propiedades insecticidas. In: São José AR, Souza IVB, Morais OM, Reboucas TNH (eds) Anonáceas: produção e mercado (pinha, graviola, atemóia e cherimólia). DFZ/UESB, Vitória da Conquista, pp 229–239
Huang RC, Tadera K, Yagi F, Minami Y, Okamura H, Iwagawa T, Nakatani M (1996) Limonoids from Melia azedarach. Phytochemistry 43:581–583
Isman MB (1995) Leads and prospects for the development of new botanical insecticides. In: Roe RM, Kuhr RJ (eds) Reviews in pesticide toxicology. Toxicology Communications Inc., Raleigh, pp 1–20
Jacobson M (1989) Botanical pesticides: past, present and future. In: Arnason JT, Philogene BJR, Morand P (eds) Inseticides of plant origin. American Chemical Society, Washington, pp 1–10
Jongsma MA, Bolter C (1997) The adaptation of insect to plant protease inhibitors. J Insect Physiol 43:885–895
Klocke JA (1987) Natural plant compounds useful in insect control. In: Waller GR (ed) Allelochemicals: role in agriculture and forestry. American Chemical Society, Washington, pp 396–415
Lage GA (2011) Isolamento, identificação química e bioprospecção de metabólitos secundários nas folhas de Annona crassiflora Mart. Dissertação, Universidade Federal de Minas Gerais, Belo Horizonte, Brasil, p 108
Leatemia JA, Isman MB (2004) Insecticidal activity of crude seed extracts of Annona spp, Lansium domesticum and Sandoricum koetjape against lepidopteran larvae. Phytoparasit 32:30–37
Lin JY, Tang CY (2007) Determination of total phenolic and flavonoid contents in selected fruits and vegetables, as well as their stimulatory effects on mouse splenocyte proliferation. Food Chem 101:140–147
Llanos CAH, Arango DL, Giraldo MC (2008) Actividad insecticida de extractos de semilla de Annona muricata (Annonaceae) sobre Sitophilus zeamais (Coleoptera: Curculionidae). Rev Colomb Entomol 34:76–82
Maroneze DM, Gallegos DMN (2009) Efeito de extrato aquoso de Melia azedarach no desenvolvimento das fases imatura e reprodutiva de Spodoptera frugiperda (J. E. Smith, 1797) (Lepidoptera: Noctuidae). Semina Ciênc Agrar 30:537–550
Martinez SS (2011) O nim, Azadiractina indica—Natureza, usos múltiplos, produção. IAPAR, Londrina, p 205
Mass PJM, Kamer MV, Junnika H, Mello-Silva R, Rainer H (2001) Annonaceae from central-eastern Brazil. Rodriguésia 52:65–98
Matos AP, Nebo L et al (2006) Atividade Biológica de Extratos Orgânicos de Trichilia spp. (Meliaceae) sobre Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) em Dieta artificial. BioAssay 1:1–6
Maxson ED, Rooney LW (1972) Evaluation of methods for tannin analysis in sorghum grain. Cereal Chem 49:719–729
Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OG (2005) Determination of the total phenolic, flavonoid and proline contents in burkina fasan honey, as well as their radical scavenging activity. Food Chem 91:571–577
Meneses Da Silva EL, Roblot F, Mahuteau J, Cavé A (1996) Coriadienin, the first annonaceous acetogenin with two double bonds isolated from Annona coriaceae. J Nat Prod 59:528–30
Menezes ELA (2005) Inseticidas botânicos: seus princípios ativos, modo de ação e uso agrícola. Embrapa Agrobiologia, Seropédica, p 58
Morimoto M, Kumeda S, Komai K (2000) Insect antifeedant flavonoids from Gnaphalium affine D. Don J Agric Food Chem 48:1888–1891
Muhammad I, Dunbar DC, Takamatsu S, Walker LA, Clark AM (2001) Antimalarial, cytotoxic, and antifungal alkaloids from Duguetia hadrantha. J Nat Prod 64:559–62
Musayimana T, Saxena RC, Kairu EW, Ogol CPKO, Khan ZR (2001) Effects of neem seed derivatives on behavioral and physiological responses of the Cosmopolites sordidus (Coleoptera: Curculionidae). J Econ Entomol 94:449–454
Oliveira AC (2009) Efeito Antialimentar do Extrato Metanólico de Annona crassiflora Mart. sobre o Percevejo Marrom Euschistus heros (Fabr. 1798) (Heteroptera: Pentatomidae). Rev Bras Agroecol 4:2633–2636
Ossipov V, Nurmi K, Loponen J, Prokopiev N, Haukioja E, Piltlaja K (1995) HPLC isolation and identification of flavonoids from white birch Betula pubescens leaves. Biochem Syst Ecol 23:213–222
Parra JRP (2001) Técnicas de criação de insetos para programas de controle biológico. Fealq, Piracicaba, p 134
Pontes WJT, De Oliveira JCS, Da Câmara CAG, Gondim Júnior MGC, De Oliveira JV, Schwartz MOE (2007) Atividade acaricida dos óleos essencias de folhas e frutos de Xylopia sericea sobre o ácaro rajado (Tetranychus urticae Koch). Quim Nova 30:838–841
Pratissoli D, Thuler RT, Pereira FF, Dos Reis EF, Ferreira AT (2004) Ação transovariana de lufenuron (50 g/l) sobre adultos de Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) e seu efeito sobre o parasitóide de ovos Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Ciênc Agrotec 28:9–14
Reyes-Chilpa R, Viveros-Rodriguez N, Gomez-Garibay F, Alavez-Solano D (1995) Antitermitic activity of Lonchocarpus castilloi flavonoids and heartwood extracts. J Chem Ecol 21:455–463
Ribeiro JF, De Brito MA, Scaloppi Junior EJ, Da Fonseca CEL (2000) Araticum (Annona crassiflora MART). FUNEP, Jaboticabal, 52 p
Roel AR, Vendramin JD (1999) Desenvolvimento de S. frugiperda (J. E. Smith) em genótipos de milho tratados com extrato acetato de etila de Trichilia pallida (Swartz). Sci Agric 56:581–586
Rossi GD, Santos CD, Carvalho GA, Alves DS, Pereira LLS, Carvalho GA (2012) Biochemical analysis of a castor bean leaf extract and its insecticidal effects against Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). Neotrop Entomol 41:503–509
Santos SC, Mello JCP (2003) Taninos. In: Simões CMO, Schenkel EP, Gosmann G, Mello JCP, Mentz LA, Petrovick JCP (eds) Farmacognosia: da planta ao medicamento. Editora da UFRGS, Porto Alegre, pp 615–655
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
Silva APT, Pereira MJB, Bento LF (2007) Extrato metanólico da semente de araticum (Annona coriacea) (Mart.) sobre a mortalidade da traça-do-tomateiro (Tuta absoluta). Rev Bras Agroecol 2:1150–1153
Simmonds MSJ (2001) Importance of flavonoids in insect–plant interactions: feeding and oviposition. Phytochemistry 56:245–252
Soetan KO (2008) Pharmacological and other beneficial effects of anti-nutritional factors in plants—a review. Afr J Biotechnol 7:4713–4721
Terra WR, Ferreira C (2005) Biochemistry of digestion. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier, Oxford, pp 171–224
Tiangda CH, Gritsanapan W et al (2000) Anti headlice activity of a preparation of Annona squamosa seed extract. Southeast Asian J Trop Med Public Health 31:174–7
Torrecillas SM, Vendramim JD (2001) Extrato aquoso de ramos de Trichilia pallida e o desenvolvimento de Spodoptera frugiperda em genótipos de milho. Sci Agric 58:27–31
Torres AL, Barros R, Oliveira JV (2001) Efeito de extratos aquosos de plantas no desenvolvimento de Plutella xylostella (L.) (Lepidoptera: Plutellidae). Neotrop Entomol 30:151–156
Trindade RCP, Luna JS, Lima MRF, Silva PP, Sant’ana AEG (2011) Larvicidal activity and seasonal variation of Annona muricata (Annonaceae) extract on Plutella xylostella (Lepidoptera: Plutellidae). Rev Colomb Entomol 37:223–227
Vega MRG, Esteves-Souza A, Vieira IJC, Mathias L, Braz-Filho R, Echevarria A (2007) Flavonoids from Annona dioica leaves and their effects in Ehrlich carcinoma cells DNA-topoisomerase I and II. J Braz Chem Soc 18:1554–1559
Yang H, Li X, Tang Y, Zhang N, Chen J, Cai B (2009) Supercritical fluid CO2 extraction and simultaneous determination of eight annonaceous acetogenins in Annona genus plant seeds by HPLC-DAD method. J Pharm Biomed Anal 49:140–144
Acknowledgments
The author would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship and the company, Semeali, for providing the seeds of corn.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Raul NC Guedes – UFV
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 1945 kb)
Rights and permissions
About this article
Cite this article
Freitas, A.F., Pereira, F.F., Formagio, A.S.N. et al. Effects of Methanolic Extracts of Annona Species on the Development and Reproduction of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Neotrop Entomol 43, 446–452 (2014). https://doi.org/10.1007/s13744-014-0225-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-014-0225-x