Abstract
The main objective of the present study is to introduce a new and ecologically safe method for managing the rice weevil, Sitophilus oryzae. Therefore, the Agave americana leaf extract’s phytochemical profile, and its insecticidal activity against the adults of S. oryzae were evaluated. The A. americana leaf extract was screened for the following phytochemicals: total phenolics (14.70 ± 0.31 mg GAE/g FW), total flavonoids (5.15 ± 0.18 mg RE/g FW) and saponins (10.32 ± 0.20 mg OAE/g FW). The HPLC-ESI/TOF-MS analysis results revealed that flavonoid glycosides (kaempferol, quercetin, and isorhamnetin derivates) were the major phenolic compounds of the A. americana leaf extract. In addition, the GC-MS analysis identified n-alkanes (77.77%) as significant compounds of the lipophilic fraction from the leaf extract. Moreover, the insecticidal potential was assessed through contact and repellent bioassays towards the rice weevil adults. The LD50, LC50, and RC50 values were 10.55 μg/insect, 8.99 μg/cm2, and 0.055 μg/cm2 for topical application method, treated filter-paper method, and repellent bioassay, respectively. Furthermore, the A. americana leaf extract inhibited digestive enzyme activities, and median inhibition concentrations IC50 were evaluated to be 146.06 ± 1.74 and 86.18 ± 1.08 μg/mL for α-amylase and protease, respectively. Overall, our results highlighted the promising potential of the leaf extract against S. oryzae adults, allowing us to recommend the extract under investigation as an ecofriendly alternative to synthetic insecticides.
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References
Abay G, Karakoc OC, Tufekci AR, Koldas S, Demirtas I (2012) Insecticidal activity of Hypnum cupressiforme (Bryophyta) against Sitophilus granarius (Coleoptera: Curculionidae). J Stored Prod 51:6–10
Abbott WS (1925) A method for computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267
Adel MM, Sehnal F, Jurzysta M (2000) Effects of alfalfa saponins on the moth Spodoptera littoralis. J Chem Ecol 26(4):1065–1078
Ahmad E, Jaiswal JP (2018) Inheritance of resistance to rice weevil (Sitophilus oryzae L.) in bread wheat (Triticum aestivum L.). Electron J Plant Breed 9(3):1083–1093
Ahumada-Santos YP, Montes-Avila J, Uribe-Beltrán MDJ, Díaz-Camacho SP, López-Angulo G, Vega-Aviña R, López-Valenzuela JA, Heredia JB, Delgado-Vargas FD (2013) Chemical characterization, antioxidant and antibacterial activities of six Agave species from Sinaloa, Mexico. Ind Crop Prod 49:143–149
Almaraz-Abarca N, Delgado-Alvarado EA, Hernández-Vargas V, Ortega-Chávez M, Orea-Lara G, Cifuentes-Díaz De León A, Ávila-Reyes JA, Muñiz-Martínez R (2009) Profiling of phenolic compounds of somatic and reproductive tissues of Agave durangensis gentry (Agavaceae). Am J Appl Sci 6(6):1076–1085
Almaraz-Abarca N, Del Socorro González-Elizondo M, Da Graça Campos M, Eréndira Ávila-Sevilla Z, Delgado-Alvarado EA, Ávila-Reyes JA (2013) Phytochemistry variability of the foliar phenol profiles of the Agave victoriae-reginae complex (agavaceae). Bot Sci 91(3):295–306
Baker JE, Woo SM (1992) Digestion of starch granules by α-amylases from the rice weevil, Sitophilus oryzae: effect of starch type, fat extraction, granule size, mechanical damage, and detergent treatment. Insect Biochem Mol Biol 22(6):529–537
Ben Halima H, Choudhary MQ, Millis KA, Price N (2004) Phosphine resistance in stored-product insect collected from various grain storage facilities. J Stored Prod Res 40:241–249
Ben Hamissa AM, Seffena M, Aliakbarian B, Casazza AA, Perego P, Converti A (2012) Phenolics extraction from Agave americana (L.) leaves using high-temperature, high-pressure reactor. Food Bioprod Process 90(1):17–21
Benelli G, Govindarajan M, AlSalhi MS, Devanesan S, Maggi F (2017a) High toxicity of camphene and γ-elemene from Wedelia prostrata essential oil against larvae of Spodoptera litura (Lepidoptera: Noctuidae). Environ Sci Pollut Res 25(11):10383–10391
Benelli G, Canale A, Toniolo C, Higuchi A, Murugan K, Pavela R, Nicoletti M (2017b) Neem (Azadirachta indica): towards the ideal insecticide? Nat Prod Res 31:369–386
Bezazi A, Belaadi A, Bourchak M, Scarpa F (2014) Novel extraction techniques, chemical and mechanical characterization of Agave americana L. natural fibers. Compos Part B Eng 66:194–203
Castellanos I, Espinosa-García FJ (1997) Plant secondary metabolite diversity trait against insects: a test with Sitophilus granarius (Coleoptera: Curculionidae) and seed secondary metabolites. Biochem Syst Ecol 25(7):591–602
Cespedes CL, Molina SC, Muñoz E, Lamilla C, Alarcon J, Palacios SM, Maria C, Carpinella MC, Avila JG (2013) The insecticidal, molting disruption and insect growth inhibitory activity of extracts from Condalia microphylla Cav. (Rhamnaceae). Ind Crop Prod 42:78–86
Chen Y, Yu H, Wu H, Pan Y, Wang K, Jin Y, Zhang C (2015) Characterization and quantification by LC-MS/MS of the chemical components of the heating products of the flavonoids extract in Pollen typhae for transformation rule exploration. Molecules 20:18352–18366
Chernonosov AA, Karpova EA, Lyakh EM (2017) Identification of phenolic compounds in Myricaria bracteata leaves by high-performance liquid chromatography with a diode array detector and liquid chromatography with tandem mass spectrometry. Rev Bras Farmacogn 27(5):576–579
Cuyckens F, Claeys M (2004) Mass spectrometry in the structural analysis of flavonoids. J Mass Spectrom 39(1):1–15
Cuyckens F, Claeys M (2005) Determination of the glycosylation site in flavonoid mono-O-glycosides by collision-induced dissociation of electrospray-generated deprotonated and sodiated molecules. J Mass Spectrom 40(3):364–372
De Geyter E, Geelen D, Smagghe G (2007a) First results on the insecticidal action of saponins. Commun Agric Appl Biol Sci 72(3):645–648
De Geyter E, Lambert E, Geelen D, Smagghe G (2007b) Novel advances with plant saponins as natural insecticides to control pest insects. Pest Tech 1(2):96–105
De Geyter E, Swevers L, Soin T, Geelen D, Smagghe G (2012) Saponins do not affect the ecdysteroid receptor complex but cause membrane permeation in insect culture cell lines. J Insect Physiol 58(1):18–23
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Dewanto V, Wu XZ, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50(10):3010–3015
Dharmshaktu NS, Prabhakaran PK, Menon PK (1987) Laboratory study on the mosquito larvicidal properties of leaf and seed extract of the plant Agave americana. J Trop Med Hyg 90(2):79–82
Diwan RK, Saxena RC (2010) Insecticidal property of flavonoid isolated from Tephrosia purpurea. Int J Chem Sci 8(2):777–782
Domon B, Costello CE (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj J 5(4):397–409
Dorta E, González M, Gloria Lobo M, Sánchez-Moreno C, De Ancos B (2014) Screening of phenolic compounds in by-product extracts from mangoes (Mangifera indica L.) by HPLC-ESI-QTOF-MS and multivariate analysis for use as a food ingredient. Food Res Int 57:51–60
Dutra KDA, Vargas De Oliveira J, Do Amaral Ferraz Navarro DM, Rafael D, Barbosa S, Peroba Oliveira Santos J (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
Finney DJ (1971) Probit Analysis, third edn. Cambridge University Press, London
Grzywacz D, Stevenson PC, Mushobozi WL, Belmain S, Wilson K (2014) The use of indigenous ecological resources for pest control in Africa. Food Secur 6(1):1–86
Gutiérrez A, Rodríguez IM, Del Río JC (2008) Chemical composition of lipophilic extractives from sisal (Agave sisalana) fibers. Ind Crop Prod 28(1):81–87
Hanhineva K, Torronen R, Bondia-Pons I, Pekkinen J, Kolehmainen M, Mykkanan H, Poutanen K (2010) Impact of dietary polyphenols on carbohydrate metabolism. Int J Mol Sci 11(4):1365–1402
Herbert-Doctor LA, Saavedra-Aguilar M, Villarreal ML, Cardoso-Taketa A, Vite-Vallejo O (2016) Insecticidal and nematicidal effects of Agave tequilana juice against Bemisia tabaci and Panagrellus redivivus. Southwest Entomol 41(1):27–40
Hiai S, Oura H, Nakajima T (1976) Color reaction of some sapogenins and saponins with vanillin and sulfuric acid. Planta Med 29(2):116–122
Hosseininaveh V, Bandani A, Azmayeshfard P, Hosseinkhani S, Kazzazi M (2007) Digestive proteolytic and amylolytic activities in Trogoderma granarium everts (Dermestidae: Coleoptera). J Stored Prod Res 43(4):515–222
Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19(3):140–145
Jankov D, Indić D, Kljajić P, Almaši R, Andrić G, Vuković S, Grahovac M (2013) Initial and residual efficacy of insecticides on different surfaces against rice weevil Sitophilus oryzae (L.). J Pest Sci 86:211–216
Kajla M, Bhattacharya K, Gupta K, Banerjee U, Kakani P, Gupta L, Kumar S (2016) Identification of the temperature induced larvicidal efficacy of Agave angustifolia against Aedes, Culex and Anopheles larvae. Front Public Health 3:1–11
Kannaiyan S (2000) Environmental impact of pesticides in agroecosystem. In: Santharam G, Jayakumar R, Kuttalam S, Chandrasekaran S, Manoharan T (eds) Environmental impact of pesticides in agroecosystem—assessment and abatement, pp 3–9
Kareem A (1999) Biopesticides and insect pest management. In: Ignacimuthu S, Sen A (eds) Biopesticides in insect pest management. Phoenix publishing house Pvt ltd, New Delhi, pp 1–6
Kim SI, Lee DW (2014) Toxicity of basil and orange essential oils and their components against two coleopteran stored products insect pests. J Asia Pac Entomol 17(1):13–17
Kumar N, Pathera AK, Saini P, Kumar M (2012) Harmful effects of pesticides on human health. Annals Agri-Bio Res 17(2):125–127
Kumar S, Singh A, Kumar B (2017) Identification and characterization of phenolics and terpenoids from ethanolic extracts of Phyllanthus species by HPLC-ESI-QTOF-MS/MS. J Pharmaceut Anal 7(4):214–222
Maazoun MA, Ben Hlel T, Haouel HS, Belhadj F, Mediouni Ben Jemâa J, Marzouki MN (2017) Screening for insecticidal potential and acetylcholinesterase activity inhibition of Urginea maritima bulbs extract for the control of Sitophilus oryzae (L.). J Asia Pac Entomol 20(3):752–760
Mediouni Ben Jemâa J, Tersim N, Taleb Toudert K, Khouja ML (2012) Insecticidal activities of essential oils from leaves of Laurus nobilis L. from Tunisia, Algeria and Morocco, and comparative chemical composition. J Stored Prod Res 48:97–104
Mehrabadi M, Bandani AR, Mehrabadi R, Alizadeh H (2012) Inhibitory activity of proteinaceous α -amylase inhibitors from Triticale seeds against Eurygaster integriceps salivary α-amylases: interaction of the inhibitors and the insect digestive enzymes. Pestic Biochem Physiol 102:220–228
Melgar B, Dias MI, Ciric A, Sokovic M, Garcia-Castello EM, Rodriguez-Lopez AD, Barros L, Ferreira ICRF (2018) Bioactive characterization of Persea americana mill. By products: a rich source of inherent antioxidants. Ind Crop Prod 111:212–218
Miresmailli S, Isman MB (2014) Botanical insecticides inspired by plant–herbivore chemical interactions. Trends Plant Sci 19(1):29–35
Mkindi AG, Mtei KM, Njau KN, Ndakidemi PA (2015) The potential of using indigenous pesticidal plants for insect pest control to small scale farmers in Africa. Am J Appl Sci 6:3164–3174
Murdock L, Brooki-Iart G, Dtmn PED, Foard E, Kelley S, Kitch L, Shade RE, Shukle RH, Wolfson JL (1987) Cysteine digestive proteinases in Coleoptera (L.). Comp Biochem Physiol 87(4):783–787
Nenaah GE (2013) Potential of using flavonoids, latex and extracts from Calotropis procera (Ait.) as grain protectants against two coleopteran pests of stored rice. Ind Crop Prod 45:327–334
Nozzolillo C, Arnason JT, Campos F, Donskov N, Jurzysta M (1997) Alfalfa leaf saponins and insect resistance. J Chem Ecol 23(4):995–1002
Oke-Altuntas F, Ipekcioglu S, Yaglioglu AS, Behcetcan L, Demirtas I (2017) Phytochemical analysis, antiproliferative and antioxidant activities of Chrozophora tinctoria: a natural dye plant. Pharm Biol 55(1):966–973
Olvera-García V, Martín Del Campo ST, Gutiérrez-Uribe JA, Cardador-Martínez A (2015) GC–MS and HPLC–MS-TOF characterization of Agave atrovirens extracts. A preliminary study. Ind Crop Prod 78:39–47
Pavela R (2011) Insecticidal properties of phenols on Culex quinquefasciatus say and Musca domestica (L.). Parasitol Res 109(6):1547–1553
Pavela R, Benelli G (2016) Essential oils as eco-friendly biopesticides? Challenges and constraints. Tr Plant Sci 21(12):1000–1007
Pavela R, Maggi F, Ngahang Kate SL, Rakotosaona R, Rasoanaivo P, Nicoletti M, Canale A, Benelli G (2017) Chemical composition of Cinnamosma madagascariensis (Cannelaceae) essential oil and its larvicidal potential against the filariasis vector Culex quinquefasciatus Say. S Afr J Bot 108:359–363
Pelah D, Abramovich Z, Markus A, Wiesman Z (2002) The use of commercial saponin from Quilla jasaponaria bark as a natural larvicidal agent against Aedes aegypti and Culex pipiens. J Ethnopharmacol 81(3):407–409
Poonsri W, Pluempanupat W, Chitchirachan P, Bullangpoti V, Koul O (2015) Insecticidal alkanes from Bauhinia scandens var. horsfieldii against Plutella xylostella L. (Lepidoptera: Plutellidae). Ind Crop Prod 65:170–174
Pritsos CA, Pastore J, Pardini RS (1991) Role of superoxide-dismutase in the protection and tolerance to the pro oxidant allelochemical quercetin in Papilio polyxenes, Spodoptera eridania and Trichoplusia ni. Arch Insect Biochem Physiol 16(4):273–282
Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29(9):913–920
Rekha MR, Sasikiran K, Padmaja G (2004) Inhibitor potential of protease and α-amylase inhibitors of sweet potato and taro on the digestive enzymes of root crop storage pests. J Stored Prod Res 40(4):461–470
Salunke BK, Kotkar HM, Mendki PS, Upasani SM, Maheshwari VL (2005) Efficacy of flavonoids in controlling Callosobruchus chinensis (L.) (Coleoptera: Bruchidae), a post-harvest pest of grain legumes. Crop Prot 24(10):888–893
Sami AJ, Shakoor AR (2014) Potential of azadirachtin and neem (Azadirachta indica) based saponins as biopesticides for in vitro insect pests cellulase (Beta-1,4-endoglucanase) enzyme inhibition and in vivo repellency on Tribolium castaneum. Br Biotechnol J 4(8):904–917
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic–phosphotungtic acid reagents. Am J Enol Vitic 16:144–158
Soulé S, Guntner C, Vazquez A, Argandona V, Moina P, Ferreira F (2000) An aphid repellent glycoside from Solanum laxum. Phytochemistry. 55(3):217–222
Sparg SG, Light ME, Staden JV (2004) Biological activities and distribution of plant saponins. J Ethnopharmacol 94(2–3):219–243
Stintzing FC, Kammerer D, Schieber A, Adama H, Nacoulma OG, Carle R (2004) Betacyanins and phenolic compounds from Amaranthus spinosus L. and Boerhavia erecta L. Z National 59(1–2):1–8
Szczepanik M, Krystkowiak K, Jurzysta M, Bialy Z (2001) Biological activity of saponins from alfalfa tops and roots against Colorado potato beetle larvae. Acta Agro Botanica 54(2):235–245
Szczepanik M, Bialy Z, Jurzysta M (2004) The insecticidal activity of saponins from various Medicago spp. against Colorado potato beetle, Leptinotarsa decem lineata say. Allelopath J 14(2):177–185
Tapondjou AL, Adler C, Fontem DA, Bouda H, Reichmuth C (2005) Bioactivities of cymol and essential oils of Cupressus sempervirens and Eucalyptus saligna against Sitophilus zeamais Motschulsky and Tribolium confusum du Val. J Stored Prod Res 41(1):91–102
Taylor WG, Fields PG, Sutherland DH (2004) Insecticidal components from field pea extracts: Soyasaponins and lysolecithins. J Agric Food Chem 52(25):7484–7490
Walia S, Saha S, Tripathi V, Sharma KK (2017) Phytochemical biopesticides: some recent developments. Phytochem Rev 16:989–1007
Yankanchi SR, Gadache AH (2010) Grain protectant efficacy of certain plant extracts against rice weevil, Sitophilus oryzae L. (Coleoptera: Curculionidae). J Biopesticides 3(2):511–513
Zoubiri S, Baaliouamer A (2014) Potentiality of plants as source of insecticide principles. J Saudi Chem Soc 18(6):925–938
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This work was supported by the Ministry of Higher Education and Scientific Research, Tunisia.
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Maazoun, A.M., Hamdi, S.H., Belhadj, F. et al. Phytochemical profile and insecticidal activity of Agave americana leaf extract towards Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Environ Sci Pollut Res 26, 19468–19480 (2019). https://doi.org/10.1007/s11356-019-05316-6
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DOI: https://doi.org/10.1007/s11356-019-05316-6