Potentiality of botanical agents for the management of post harvest insects of maize: a review

Abstract

Natural products derived from plants are emerging as potent biorational alternatives to synthetic insecticides for the integrated management of post harvest insects of maize. In this paper, effectiveness of botanicals including plant extracts, essential oils, their isolated pure compounds, plant based nano formulations and their mode of action against storage insects have been reviewed with special reference to maize. Plant based insecticides found to be the most promising means of controlling storage insects of maize in an eco friendly and sustainable manner. This article also throws light on the commercialization of botanicals, their limitations, challenges and future trends of storage insect management.

Introduction

Maize is regarded as queen of cereal crops as it has highest genetic yield potential which is used as food, feed, fodder and also serves as basic raw material in industries such as beverage, confectionery, starch, ethanol, oil, cosmetic, pharma, food processing, textile, gum and paper industries. In India, Maize is a dominant crop with production of 24.19 million tones, exported 2.7 million tones grain worth Rs 4,267 crores to West Asia (DMR 2014); contributing 36 % in global grain production. It is rich in carbohydrate, protein, oil and crude fibre contents (FAOSTAT 2014). Though production of maize has increased to meet the global demand, several biotic and abiotic factors play an important role in limiting the productivity. It is also plagued with post production storage losses. Among biotic factors contributing for storage losses, insect pests play a major role inflicting 20–30 % damage of maize grain in tropical regions (Haque et al. 2000) due to favourable conditions for their development and poor storage conditions. It has been reported that more than 37 species of arthropod insects are associated with stored maize (Abraham 1997). Rice weevil Sitophilus oryzae L., (Coleoptera: Curculionidae), Angomouis grain moth Sitotroga cerealella (Oliv.) (Lepidoptera: Gelecidae), Red Flour beetle Tribolium castaneum (Herbst.) (Coleoptera: Tenebrionidae) lesser grain borer Rhizopertha dominica (F.) (Coleoptera: Bostrichidae) and Rice moth Corcyra cephalonica Stainton (Lepidoptera: Pyralidae) are the pests that attack maize in India. Among them, S. oryzae (Lucas and Riudavets 2000) and S. cerealella are the major primary insect pests causing quantitative and qualitative losses (Lakshmi Soujanya et al. 2013a); starts infestation in the field itself and continues in stored maize. They devour the seed completely from inside make them chaffy; and eventually seed viability is lost (Hill 2002). Infestation of these insect pests further result in mold formation (Magan et al. 2003); development of Aspergillus, (a fungus producing mycotoxins) which is the most powerful carcinogen in humans and animals (Williams et al. 2012, Carrieri et al. 2013) and phytotoxicity to grain (Lee et al. 2003).

Protection of stored products from insect pests is most important to ensure food supply to all over the world. Insect pests can be managed with the use of synthetic insecticides but in storage, any intervention with insecticides leads to closest application for consumption which is totally unsafe. Further, indiscriminate use of these synthetic insecticides resulted in the development of resistance (Subramanyam and Hagstrum 1995; Arthur 1996; Mohan et al. 2010; Correa et al. 2011), residues, undesirable effects on non target organisms, human and environmental hazards (White and Leesch 1995). Moreover, methyl bromide, one of the most effective fumigants in the control of stored pests, is banned from 2015 as per Montreal Protocol, due to its ozone depleting nature (Fields and White 2002; Philips and Throne 2010; Germinara et al. 2012). As a result, managing storage insects has become more of a challenge. In view of negative fallouts of synthetic insecticides, substances of plant origin for the control of stored grain insects are quite promising as they are more biodegradable, low toxicity to human beings; and there is every possibility of maintaining environmental conditions inside the storage systems (Guzzo et al. 2006).

Botanical insect toxins are extracted or derived from plants such as azadirachtin from Azadirachta indica A. Juss (Barceloux 2008), rotenone from Derris elliptica Wall. (Sae-Yun et al. 2006), pyrethrin from Chrysanthemum cinerariifolium Trevir. (Shawkat et al. 2011). The use of locally available plants including Nicotiana, Ryania; spices-turmeric, clove, cinnamon, black pepper, ginger, garlic, star anise for the control of insect pests is an ancient practice (Thacker 2002; Kiruba et al. 2008; Paul et al. 2009). Many of these plants are widely used in traditional medicine for treatment of various ailments also (Ahalya and Mikunthan 2013). Plants are the most efficient producers of secondary metabolites, that are used in defense against different insect pests (Isman and Akhtar 2007); particularly triterpenoids, iridoid glycosides which are responsible for insecticidal activities (Sharma 1995). Many researchers have worked on plant products as they provide unique mode of action (Koul and Dhaliwal 2001; Regnault- Roger et al. 2005; Santos et al. 2011) against storage insects due to their biodegradability, broad spectrum activity and sustainability.

Plants belonging to the families of Annonaceae, Asteraceae, Apiaceae, Chenopodiaceae, Cupressaceae, Lauraceae, Lamiaceae, Meliaceae, Myrtaceae, Poaceae, Piperaceae, Rutaceae, Verbenaceae and Zingiberaceae were reported as promising sources of botanical insecticides (Isman 1995; Ukeh et al. 2010; Ebadollahi 2011; Suthisut et al. 2011; Rajashekar et al. 2014a) against storage insects. It is not necessary that all plant derivatives are non toxic, some are fast acting, potent carcinogens occur naturally such as nicotine (Park et al. 2003; Isman 2006; Rajendran and Sriranjini 2008; Regnault-Roger and Philogene 2008). In view of the above, a concise review is provided on plant derived pesticides with emphasis on plant extracts/ essential oils/ isolated compounds/ nano based formulations exhibiting insecticidal, repellent, antifeedant and fumigant activities against storage insects of maize and indicated some future directions to fill the gaps.

Effect of plant extracts and isolated pure compounds on storage pests of maize

Many previous attempts have been carried out on plant based derivatives against S. oryzae, Sitophilus zeamais, T. castaneum compared to S. cerealella, R. dominica and C. cephalonica. Plant powders, their extracts, isolated pure compounds were effective and considered eco friendly in storage insects control. Table 1 lists some of the plants tested for insecticidal activities against storage insects of maize. The bioactivity of plant extracts against storage insects of maize have been studied by numerous authors (Ogendo et al. 2004; Mihale et al. 2009; Sori 2014).

• A.Bioactivity of plant extracts on adults

Table 1.

List of plants tested for insecticidal activities against storage insects of maize

Common Name	Scientific Name	Family Name	Plant part used	Phyochemical Constituents	Target pest	References
Sweet Flag	Acorus calamus L.	Acoraceae (Araceae)	Rhizome	Asarone, choline, eugenol, ethyl ether, heptanoic acid, methylamine, saponin, tannic acid and trimethylamine	Sitophilus oryzae, Tribolium castaneum	Chander et al. (1990)
Goat Weed	Ageratum conyzoides L.	Asteraceae	Leaf and stem	α-pinene, eugenol, steroids, flavonols, glucosides and polyoxygenated flavones	T. castaneum	Jaya et al. (2014)
Dill	Anethum graveolens L.	Umbelliferae (Apiaceae)	seed	Carvone, d-limonene, phellandrene, Cis-dihydro carvone, P-cymene	T. castaneum	Chaubey (2007)
Kalmegh	Andrographis paniculata Burm.f.	Acanthaceae	Leaf	Andrographolide, phenols, tannins, alkaloids, anthraquinones and saponins	S. oryzae	Prakash et al. (1993)
Bullock’s Heart	Annona squamosa L.	Annonaceae	Leaf and stem	Anonaine, corydine, isocorydine and aporphine	S. oryzae	Ashok kumar et al. (2010)
Mugwort	Artemisia annua L.	Asteraceae	Stem and Leaf	Cineole, tauremisin, sitosterol, tetracosanol, fernenol and thujone	T. castaneum	Tripathi et al. (2000)
Chinese Worm Wood	A.capillaris	Asteraceae	Stem and Leaf	1,8-cineole, germacrene and d-camphor	Sitophilus zeamais	Liu et al. (2010)
Caraway	Carum carvi L.	Umbelliferae(Apiaceae)	Fruit	Carvone, sterols, triterpenes, myrcene, 1,8- cineole, unsaturated steroids, saponins, flavonoids, glycosides, pyrogallol, tannin and phloroglucinol	S. zeamais T. castaneum	Fang et al. (2010)
Indian Worm Seed	Chenopodium ambrosioides L.	Amaranthaceae	Fruit	Ascaridole, carene, cymene histamine, hydrocyanic acid, limonene, methyl salicylate , oxalic acid, safrole, saponin and trimethyl amine	S. zeamais	Denloye et al. (2010)
Irula	Cleome monophylla L.	Capparidaceae	Whole plant	Erpenolene, 1-α –terpeneol, pentacosane, humulene, phytol and 2-dodecanone	S. zeamais	Ndungu et al. (1995)
Red Water Tree	Erythrophleum suaveolens Guill. & Perr.	Fabaceae	Bark	Cassaidine, nor-cassaidine, cassaine, cassamine, erythrophalamine, erythrophleine and homophleine	S. zeamais	Niber et al. (1992)
Blue Gum Tree	Eucalyptus globulus Labill.	Myrtaceae	Leaf	1,8-cineole and α pinene	S. oryzae, T. castaneum	Mishra et al. (2012)
Black Sesame	Hyptis spicigera Lam.	Lamiaceae	Whole plant	Sesquiterpenes, sesquiterpene alcohol and menthol	S. zeamais	Wekesa et al. (2011)
Lavender	Lavendula angustifolia Mill.	Lamiaceae	Whole plant	Linalyl acetate, geranyl acetate, linalool, geraniol, limonene, d-pinene,coumarin, furfurol, d-borneol and cineol	S. oryzae, R. dominica, T. castaneum	Rozman et al. (2007)
Corn Mint	Mentha arvensis L.	Lamiaceae	Leaf	Menthol, menthane and menthyl acetate	S. oryzae T. castaneum	Varma and Dubey (2001)
Pepper Mint	Mentha piperita L.	Lamiaceae	Leaf powder	Acetaldehyde, amyl alcohol, caproic acid, caprylic acid, carvacrol, carvone, cineole, ethyl alcohol, formic acid, furfural, isoamyl alcohol, isovaleraldehyde, isovaleric acid, limonene, linalool, menthol, methanol, methylamine, oxalic acid, phellandrene, pulegone, salicylic acid and valeric acid	S. oryzae, T. castaneum	Lashgari et al. (2013)
Horse Mint	Mentha longifolia L.	Lamiaceae	Leaf	Menthol, menthone, piperitone, piperitenone, linalool, carvone and eucalyptol	T. castaneum	Khani and Asghari (2012)
Bitter Gourd	Momordica charantia L.	Cucurbitaceae	Leaf and seed	Charantin, momordicin, foetidin, 5-hydroxytryptamine, diosgenin and p-sitosterol	S. oryzae, T. castaneum	UshaRani and Devanand (2011)
Sweet Basil	Ocimum basilicum L.	Lamiaceae	Leaf	Anethole, camphor, carvacrol, cineole, citral, esdragole, eugenol, linalool, safrole, sapenin and thymol	S. oryzae, T. castaneum	Mishra et al. (2012)
Guava	Psidium guajava L.	Myrtaceae	Leaf	Ineol, tannins, triterpenic acids, ursolic and oleanolic acids	S. oryzae	Akhtar et al. (2013)
Fenugreek	Trigonella foenum-graecum L.	Fabaceae	Leaf	Trigonelline, steroidal sapogenin and diosgenin	S. oryzae, R. dominica	Matter et al. (2008)
Garden Thyme	Thymus vulgaris L.	Lamiaceae	Leaf and flower	Thymol, caracrol, cymol, borneol, linalool and tannin	R. dominica	Mehrabadi et al. (2011)
Nirgundi	Vitex negundo L.	Verbenaceae	Leaf	β-caryophyllene, protocatechuic acid and oleanolic acid	S. oryzae	Rana et al. (2005)

Sharma (1999) reported that neem seed, neem kernel powder at 4 % and neem leaf powder at 5 % concentration protected maize for 5 months against S. oryzae, S. cerealella, R. dominica and T. castaneum. Also many studies have shown the effectiveness of neem against storage insects of maize (Huang and Ho 1998; Mulungu et al. 2007; Sule et al. 2012; Chebet et al. 2013). Li et al. (2000) reported that isolated fraction from leaf of Eupatorium adenophorum Spreng. showed insecticidal activity against S. oryzae (LD₅₀-15.5 mg/L). Jayasekara et al. (2005) reported that root powder of Securidaca longepedunculata Fers, its methanol extract and isolated compound methyl salycilate has repellent and toxic properties against S. zeamais adults. Additionally, fumigant effect was observed with 60 μl dose against S. zeamais and R. dominica and prolonged exposure of methylsalycilate for 6 days provided 100 % mortality of two insect pests. Saljoqi et al. (2006) observed promising results on repellency and toxicity against S. oryzae using ethanol extract of bakain fruits at 10 % concentration. According to Potenza et al. (2006), acetone extracts of Dahlia pinnata Cav., Ruta graveolens L. and Dieffenbachia brasiliensis Veiech at 5 % concentration gave 87.0, 80.0 and 75.0 % mortality for S. zeamais adults, respectively when tested for contact activity. Huang et al. (2007) reported 100 % mortality of R. dominica at 48 h post-treatment with LD₅₀ - 19.94 μg/cm² after 72 h treatment when treated with ethanol extracts of Trigonella foenum-graecum L. extract at 0.39 mg/cm².

It has been reported that chloroform extract of Aloysia polystachya Griseb. at 10 mg/mL solution was found to be feeding deterrent while hexane extract of Solanum argentinum Bitter et Lillo at 0.31 mg/cm² strongly repelled adults of S. oryzae. (Adriana et al. 2008). The work of Othira et al. (2009) mentioned fumigant, repellent and feeding deterrence activity from hexane extract of Hyptis spicigera Lam. against S. zeamais and T. castaneum in stored maize. During the investigations on the toxic properties of combination of Acorus calamus L. rhizomes and Thevetia neriifolia Juss. seed extract, the lowest LC₅₀ values (43.27 μgcm⁻¹) were found against S. oryzae at 24 h after treatment (Talukder and Khanam 2009). The contact application of methanolic root extracts of Decalepis hamiltonii Wight at 250 mg/kg seed showed significant toxicity against S. oryzae, R. dominica and T. castaneum (Rajashekar et al. 2010). Adeyemi et al. (2010) observed 50 % feeding deterrent activity of T. castaneum with 3,4,5,7, tetrahydroxy flavonol (quercetin-1) at 2 mg/ml isolated from chloroform extract of stem bark of Bobgunnia madagascariensis Desv. J.H. Kirkbr & Wiersema in stored maize; also Gressel and Ammann (2008) reported that quercetin (1) acts as an allelochemical as well as insecticidal to storage insects. Shayesteh and Ashouri (2010) observed complete mortality and reduced F1 progeny emergence of R. dominica with black pepper powder at 2.5 % concenteration. Ishii et al. (2010) found repellent activity by using methanolic extract of Cinnamomum sp at 10 mg/ml against S. zeamais. Ethyl acetate eluted fractions of Capsicum annuum Linn., Momordica charantia L., Solanum melongena L. at 10 mg/100 mL showed 100 % mortality to T. castaneum and S. oryzae within 24 h of treatment in vapour form without affecting germination in stored maize (UshaRani and Devanand 2011). Plant powder of Chenopodium ambrosioides L. at a concentration of 5 g/kg seed and seed oil of Pimpinella anisum L. at a dose of 1.50 ml cm⁻² caused 100 % mortality of T. castaneum after 14 days of exposure. Further, significant complete reduction of F1 progeny was achieved with the tested botanicals (Gomah and Sahar 2011).

Maximum mortality of 98.8 % was achieved to adult S. zeamais with neemazal at a concentration of 12 g/kg seed after 14 days of treatment and greatly reduced F1 progeny emergence (Nukenine et al. 2011). Gandhi and Pillai (2011) mentioned the insecticidal activity and seed protective effect of leaf powders of Punica granatum L. and Murraya koenigii L. against R. dominica. Geng et al. (2011) reported that Jolkinolide B and 17 hydroxy Jolkinolide B isolated from ethanolic extracts of roots of Euphorbia fischeriana Steud. at concenteration of 30 ppm possessed strong feeding deterrent activity against S. zeamais (EC _{50 =} 342.1 and 543.9 ppm) and T. castaneum (EC _{50 =} 361.4 and 551.5 ppm). The crude leaf extracts and their chromatographic fractions eluted with ethyl acetate of Cocos nucifera L. and Terminalia catappa L. were found to be insecticidal and fumigants to adults of S. oryzae and T. castaneum (UshaRani et al. 2011).

Recent studies also proved the efficacy of plant extracts against storage insects. Thein et al. (2013) reported that crude extracts of Citronella at 20 % concentration had the strongest repellent effect on Sitophilus spp. Another plant extract from Alpinia pyramidata Blume at 7.5 % provided protection to maize grain by completely inhibiting the F1 progeny emergence. Ali and Mohammed (2013) found that methanol extracts of Zingiber officinale Roscoe caused 100 % mortality to S. oryzae. Jeon et al. (2013) studied contact and fumigant toxicity of chloroform fraction of methanolic extract of Ruta chalepensis L. and obtained 87.7 % mortality to S. oryzae at 1.02 mg/cm². Further insecticidal constituents isolated from leaves of R. chalepensis, quinoline (2) (0.057 mg/cm²), quinoline-4-carbaldehyde (3) (0.065 mg/cm²) and quinoline-3- carbaldehyde (4) (0.092 mg/cm²) were found to be most toxic to S. oryzae. Other studies have shown that T. castaneum, S. oryzae (up to 50 % after 24 h) and R. dominica (up to 60 % after 24 h) can also be repelled by plant extracts of Anagallis arvensis L., Hibiscus rosa-sinensis Linn. and Lapsana communis L. (Singh et al. 2013).

Pure compounds osajin (5), lupalbigenin (6), scandinone (7), sphaerobioside (8), genistein (9) and prenylated isoflavones (10) derived from Derris scandens Benth. caused 100 % toxicity to T. castaneum and C. cephalonica after 10th and 15th day of treatment, respectively (Usha Rani et al. 2013). Ashamo and Ogungbite (2014) reported that ethanolic extracts of seeds from Aframomum melegueta K. Schum, Eugenia aromatica (Baill.), Piper guineense Thonn et Schum and Xylopia aethiopica Dunal at 4 and 6 % concentration prevented the adult emergence of S. cerealella. Sagheer et al. (2014) reported that the acetone extract of Trachyspermum ammi L. at 10 % concentration showed notable repellent action against T. castaneum. Rajashekar and Shivanandappa (2014) reported contact toxicity of Decaleside II isolated from the edible roots of D. hamiltonii at 100 mg/kg grain against S. oryzae and T. castaneum. Sitosteryl-β-D-glucopyranoside (11) isolated from floral extracts of Peltophorum pterocarpum DC. Heyne at a dosage of 0.080 mg/30 g diet was found to be very potent in producing toxicity to adults of S. oryzae which might be due to easy penetration into insect cuticle (UshaRani et al. 2014). Rajashekar et al. (2014a) demonstrated contact and fumigant toxicity of methanolic extract from leaves of Lantana camara L. against S. oryzae (LC_{50 -} 128 μl/l, LD₅₀ - 0.158 mg/cm² ) and T. castaneum (LC_{50 -} 178.7 μl/l, LD₅₀ - 0.208 mg/cm²). A recent study by Shah et al. (2015) indicated maximum repellency with aqueous plant extracts of Mentha longifolia L. followed by Momordica charantia L. (90.0 %), Luffa aegyptiaca Mill. (80.0 %) at 25 % concentration against Rhizopertha dominica. The structures of the bioactive compounds isolated from plants tested against storage insects were shown in Table 2.

• B.Bioactivity of plant extracts on immature stages

Table 2.

Structures of bioactive compounds isolated from some of the botanicals

There have been relatively few reports in the literature concerning the control of immature stages of storage pests by the use of botanicals. It was reported that plant extracts inhibit the development of eggs and immature stages present inside the seed (Boeke et al. 2004). Acetone extract of Ipomoea palmata L. showed 57.8 % egg mortality of C. cephalonica at 100.0 % concentration (Dwivedi and Garg 2000). In other work, flower extracts of L. camara exhibited higher larval mortality, reduced fecundity and prolonged development period of R. dominica (Rao and Prakash 2002). Das et al. (2006) evaluated nimbicidine at 16 ml/kg seed against eggs of T. castaneum and observed inhibition of egg hatching, pupation and adult emergence. Rizk (2008) reported that ethanolic extract of Melia azadirachta L. at 0.1 μg/ larva caused 57.0 % larval mortality of C. cephalonica and further observed emergence of more males compared to females. Narangoda and Karunaratne (2009) reported that methanolic extracts of leaf and seed of A. indica and seed extract of Piper nigrum L. gave 100.0 % larval mortality of C. cephalonica. Further, maximum oviposition deterrency was observed with P. nigrum followed by A. indica and there is no adverse effect on the viability of maize seed.

Khani et al. (2012a) reported that petroleum ether extract of P. nigrum and Jatropha curcas L. at concentrations of 2 ~ 10 μl/g showed strong inhibition on egg hatchability and adult emergence of C. cephalonica with LC₅₀ values of 12.52 and 13.22 μL/mL, respectively. Zambare et al. (2012) reported that chloroform extract of Argemone mexicana L. at 4 ml concentration inhibited 60.02 % egg hatching of C. cephalonica. Fouad et al. (2014) reported that extracts of Tithonia diversifolia Hemsl. at 1 % w/w discouraged egg laying and larval mortality of S. cerealella; potentiality of this plant extract is due to the presence of sesquiterpenes, lactones (Ambrosio et al. 2008). In another recent work, Ileke (2014) reported that powders and extracts of Capsicum frutescens L., Cymbopogon citratus DC. Stapf., Moringa oleifera Lamm. and Anacardium occidentale L. at the rate of 1, 2 and 3 % concentration prevented egg hatching of S. cerealella.

• C.Application of different botanicals in storage containers

In India, maize is generally stored in traditional storage structures such as metal bins, gunny bags, earthen bins, bamboo bins and jute bags. However, there is insignificant protection of produce from storage pests when tested for natural infestation in local storage containers. It is recommended to treat maize with certain botanicals before storing in such containers which are found effective and sustainable. Plant materials can be used only for small scale storage for protection of stored grain. Leaves of botanicals are added in layers/dried and grind into powder/ burnt into ash/ and mixed with grain (Crop Protection Compendium 2013). Dried leaves protect the stored grain for 2 to 4 months against insect attack without any adverse effects. Hill farmers of Uttarakhand incorporate dried leaves (harvested and dried in shade for 2 days) of Juglans regia Linn. and Zanthoxylum alatum Roxb. trees for storing grain and the bitter smell of the leaves protect the produce from storage pests. Packing materials like jute bags are dipped in 10 % neem kernel solution for 15 min. After drying, grains can be stored in jute bags and the insects will be repelled by the action of botanical and the residual action will persist for 4 months. Small pieces of rhizomes of A. calamus were mixed with maize grains stored in bamboo baskets for the control of weevil. Grain can also be stored effectively in bamboo bins painted with a solution prepared from neem cake.

Chikukura et al. (2011) evaluated leaf powders of Lippia javanica Burm.f. and wood of Spirostachys africana Sond. at concentrations of 2 and 5 % w/w against storage insects by keeping the treated grains in polypropylene bags and then stored in improved brick and grass thatched smallholder granaries. The result of the experiment showed that L. javanica proved to be the best in reducing the grain damage caused by storage pests. Duruigbo (2010) reported that neem seed powder, pepper fruit seed powder protected the maize seed from damage by storage insects when stored in airtight plastic containers without affecting the seed viability. Iliyasu and Gabriella (2015) applied paste of repellent plant materials between the layers of double bagged grain. The result indicated that combination of Cymbopogon nardus L. and Ocimum basilicum L. at 0.5 % w/w was significantly more effective in repelling T. castaneum adults.

In our laboratory we have been working on botanicals for the integrated management of storage insects of maize from the last 5 years. The leaf powders of Vitex negundo L., Adathoda vasica L., Catharanthus roseus L. and L. camara at 5 % w/w were evaluated against S. oryzae in stored maize. All the treatments proved to be very toxic towards S. oryzae adults (Lakshmi Soujanya et al. 2012a). In our earlier research, application of acetonic extracts of V. negundo, A. vasica, C. roseus at 1 and 2 % concentration induced contact toxicity to S. cereallella resulting in suppression of adult emergence, grain damage and grain weight loss in stored maize (Lakshmi Soujanya et al. 2012b). The acetone extracts of A. vasica, L. camera and V. negundo at 1 and 2 % w/v had contact and repellent effect against S. oryzae without affecting germination. (Lakshmi Soujanya et al. 2013b). Also, the effectiveness of three medicinal plants Cissus quadrangularis L., Albizia lebbeck L. and Ageratum conyzoides L. along with three storage regimes (Aluminium foil bag, Jute bag and cloth bag) were tested against S. oryzae. The results revealed that maize treated with A. conyzoides @ 2 % w/w stored in jute bags indicated highest mortality of S. oryzae, led to minimum grain weight loss and depressed progeny development at 40 and 80 days after introduction of weevils (Lakshmi Soujanya et al. 2013c). Additionally, we evaluated the effectiveness of A. conyzoides leaf powder at 5 % w/w in combination with hermetic storage (by storing maize in high density and double layered polythene bags). The results revealed that the number of offsprings of S. oryzae and S. cerealella emerged from treated maize stored in high density polythene bags were considerably lower (Lakshmi Soujanya et al. 2014). In our current study, dichloromethane extracts of Ixora coccinea L. and its pure isolated compound, tanacetene (2,6,11-trimethyl-dodeca-2,6,10-triene) proved to be superior with regard to adult mortality against S. oryzae in stored maize (un published data). The structure of isolated compound and its toxicity was shown in Fig. 1. Many researchers have worked on different botanicals for the control of storage insect pests. In India still, there is wide range of botanicals to be exploited particularly medicinal plants for the development of potent novel molecules as they are mostly safe to non target organisms.

Fig. 1.

Structure and toxicity of pure compound tanacetene isolated from dichloro methane extract of Ixora coccinea L

Effect of plant essential oils on storage pests of maize

Essential oils are complex mixtures of 20–60 organic compounds such as monoterpenes, phenols and sesquiterpenes abundantly found in some families such as Rutaceae, Umbeliferae, Myrtaceae, Labiateae; act synergistically within the plant (Feng and Isman 1995); give characteristic odour and flavour to leaves, flowers, fruits, seed, bark and rhizomes (Bakkali et al. 2008). Especially, the monoterpenes are recently emerged as most effective compounds responsible for fumigant activity, insecticidal, antifeedant, repellents and growth regulatory activities against storage pests (Regnault-Roger and Hamroui 1995; Koul et al. 2008; Yao et al. 2008). Mint, thyme, rosemary, clove, lemon grass, cinnamon, oregano and basil are the plants containing potent essential oils. Resistance development in insects can be reduced by the use of essential oils due to synergistic action between different molecules of the oil (Varma and Dubey 1999).

• A.Bioactivity of plant essential oils on adults

Bekele et al. (1996) tested essential oil extract of Ocimum suave Willd at higher doses against storage insects of maize and found 100.0 % mortality of S. cerealella and R. dominica. Moreover, the tested plant materials were highly repellent to S. zeamais and provided good protection. Carvacrol (12) isolated from Thujopsis dolabrata Asuhi exhibited insecticidal and fumigant action against S. oryzae (Ahn et al. 1998). In general, eggs are the most resistant ones while adults are most susceptible to fumigant toxicity (Wang et al. 2006).1,8-cineole (14), one of the components of the essential oil of Artemisia annua L. at 4 μl/ml of acetone have been reported to possess repellent and insecticidal effects against S. oryzae (Aggarwal et al. 2001).

Kim et al. (2003) screened five essential oils for their insecticidal activities and found potent insecticidal activity against adults of S. oryzae by Cinnamomum cassia Nees., Cochlearia armoracia L, and Brassica juncea L. oils at 3.5 mg/cm², within 1 day after treatment. Safrole (13) isolated from essential oil of Laurelia sempervirens (Ruiz & Pavon) Tul. exhibited insecticidal activity against S. zeamais, T. castaneum (Huang et al. 1999) and S. oryzae (Kim and Park 2008).Tripathi and Upadhyay (2009) reported repellent and insecticidal activities of leaf essential oil of Hyptis suaveolens L. against S. oryzae and T. castaneum. Zapata and Smagghe (2010) reported contact (39 to 44 μg/cm²), repellent (0.032 μl/cm²) and fumigant toxicities (1.6 to 1.7 μl/l) with different ranges of essential oils extracted from the leaves and bark of L. sempervirens against Tribolium castaneum.

Safrole, essential oil constituents isolated from stem bark of Illicium difengpi B N Chang showed pronounced contact toxicity against S. zeamais (LD₅₀ -8.54 μg/adult ) and T. castaneum (LD₅₀-4.67 μg/adult). Further it was reported that linalool (14) possessed strong fumigant toxicity against both insect pests (LC₅₀ = 10.02 mg/L for S. zeamais; 9.34 mg/L for T. castaneum) (Chu et al. 2011). In Calabar, Nigeria, monoterpenoids (R)-linalool (15) and 2-heptanol (16) isolated from essential oils of A. melegueta and Zingiber officinale Roscoe were found to be repellent against T. castaneum and R. dominica (Ukeh and Umoetok 2011). Suthisut et al. (2011) demonstrated fumigant toxicity of essential oils from rhizomes of Alpinia conchigera Griff. and pure compound Terpinen-4-ol (17) against S. zeamais and T. castaneum. Jemaa et al. (2012) noted that essential oils from leaves of Laurus nobilis L. were repellent and fumigant at 0.12 μl/cm² to adults of R. dominica and T. castaneum. Further 1,8-cineole (18), linalool and isovaleraldehyde (19) were identified as major compounds responsible for insecticidal activity in tests with essential oils against T. castaneum. Diallyl disulphide (20) and diallyl trisulphide (21), essential oil components of garlic exhibited fumigant activity, behavioural deterrent and ovipositional inhibitor against S. cerealella (Yang et al. 2012) and also highly toxic to S. zeamais and T. castaneum (Huang et al. 2000).

Similarly, UshaRani (2012) showed contact toxicity and fumigant activity at 130 μg/cm² with essential oils of Pinus longifolia L., Eucalyptus obliqua L., Coriandrum sativum L. against S. oryzae and C. cephalonica. Essential oil derieved from Eucalyptus astringens Maiden exhibited repellent action at 0.08 μl/m², (58.75 %) against R. dominica after 24 h of exposure (Khemira et al. 2012) whereas Khani et al. (2012b) observed highest toxicities of S. oryzae adults with essential oils of Mentha piperita L. and P. nigrum with LC₅₀ values of 85.0 and 287.7 μL/L air after 72 h after commencement, respectively. In the case of C. cephalonica larvae, the LC₅₀ values were 343.9 and 530.5 μL/L air for M. piperita and P. nigrum essential oils at 72 h after commencement, respectively. Nguemtchouin et al. (2013) reported that insecticidal effects of formulations based on essential oils of Ocimum gratissimum L. were persisted for about 80 days when tested against S. zeamais. A study by Benzi et al. (2014) showed that essential oils of Aloysia polystachya Griseb. exhibited contact toxicity against T. castaneum with LD₅₀-7.35 μg/insect. However, investigations specifically on mode of action of proven plant derivatives against target pest to be made for precise management of storage insects of maize. It has been observed that compounds Estragole (22) and (+)- fenchone present in the essential oil of Foeniculum vulgare Mill. were found effective against S. oryzae adults but are known to be carcinogenic (Kim and Ahn, 2001).

• B.Bioactivity of plant essential oils on immature stages

It was reported earlier by Dwivedi and Garg (2000) that mixture of plant oils of Citronella, pine, lemon grass and marigold commonly known as citrus clean exhibited 66.6 % egg mortality of C. cephalonica. In tests with pupae of S. oryzae, Waterford et al. (2004) observed enhanced toxicity of the (95:5 % v/v) mixture containing carvone (23) or thujone (24) at 24 h exposure. DaCosta et al. (2006) studied the fumigant toxicity of mustard essential oil against first, third-instar larvae and pupa of S. zeamais. The LC₅₀and LC₉₅ against first and third-instar larvae and pupa were found to be 4.63 and 10.32; 5.17 and 13.29; and 6.17 and 15.78 ml/L jar volume, respectively. Further, it was reported first instar larvae of S. zeamais were more susceptible than third-instar while pupal stage was most resistant to the vapors of mustard essential oil. Islam et al. (2009) demonstrated fumigant toxicity at dosage of 12.0 μg/mL, contact toxicity at 20 μg/mL and repellent activities at 12 μg/mL with essential oil of Coriandrum sativum L. against eggs, larvae and adults of T. castaneum. Inspite of advantages from essential oils, much research should be focussed on affect of seed germination, nutritional quality of treated seed, tainting and residues in essential oil treated produce before going for recommendation.

Effect of Nano based botanical derivatives on storage pests

Nano technology is the most promising recent approach and can be used as an innovative tool for the control of storage insects. In nano formulations active compound concentrates near the center core, lined by the matrix polymer and is slowly but efficiently released to a particular host which can overcome the constraints of plant essential oils. Nano formulations increase the solubility of active ingredient and protect it from premature degradation which leads to more effective interaction with target insect. Further, it was reported that micro encapsulation reduces the loss of active principles leading to high loaded micro particles that offers the possibility of controlled drug release and phytotoxicity of essential oils can be reduced. Nanospheres, nanocapsules and nanogels are the most popular shape of nano materials used in controlled release formulations. For example in the preparation of nano material in capsule form, garlic essential oil is an active compound and polyethylene glycol acted as polymer. However, very little research has been done on the application of nano materials specifically on storage insect pests.

Yang et al. (2009) reported that nanoparticles loaded with garlic essential oil is most effective against Tribolium castaneum Herbst. Stadler et al. (2010) showed that nano alumina has potential to control stored grain insects. Nano ingredients of nanotube have the ability to stick to the surface hair of insect pests and ultimately enters the body and influences certain physiological functions (Patil 2009). Negahban et al. (2012) studied the effect of nano-capsules of essential oil from Cuminum cyminum L. which was prepared by in situ polymerization (O/W) emulation using poly urea-formaldehyde and reported that the fumigant toxicity from nanocapsules (LC₅₀ = 16.25 ppm) were highly effective compared to pure essential oil (LC₅₀ = 32.12 ppm) after 7 days of exposure. Zahir et al. (2012) synthesized silver nano particles by using extracts of Euphorbia prostrata L. and determined its insecticidal activity against S. oryzae. Complete mortality (100 %) of S. oryzae adults was observed on 7th day at 250 mg/kg seed and indicated the potentiality for development as botanical based nano particles. Vani and Brindhaa (2013) reported that amorphous silica nano particles were found to be highly effective against C. cephalonica causing 100 % mortality. Gonzalez et al. (2014) reported that nano particles increased the residual contact toxicity of T. castaneum and R. dominica due to slow and persistent release of active terpenes isolated from Geranium and Bergamot. A recent investigation by Ziaee et al. (2014) demonstrated fumigant toxicity of C. cyminium oil loaded nano gels (OLNs) against S. granarius and T. castaneum and revealed OLNs were most toxic and encapsulation improved the persistence of the oil. Detailed investigation should be focused on the development of new formulations based on products derieved from plants as well as the use of nanotechnology which will improve the stability and potentiality of natural products. Besides, detailed studies are also essential on the biosafety of nano particles to other non target organisms.

Mode of action

Understanding the mode of action of botanicals is important to delay the development of insecticide resistance in target insect pests. Several authors have worked on mode of action of botanicals against storage insect pests (Talukder et al. 2004; Copping and Duke 2007; Rattan 2010). The bioactivity, mammalian toxicity Oral (rat) LD 50 (mg/kg) and mechanisms of action of different botanicals effective against storage pests were shown in Tables 3 and 4. Plant extracts and essential oils are highly lipophilic and have the ability to penetrate through insect cuticle (Tripathi et al. 2009). In particular to neem, azadirachtin (active ingredient) causes sterilization of insect pests, disrupting moulting of larvae, nymphs, mating and sexual communication, inhibiting the formation of chitin, impaired fitness and reproductive activity, modifies insect development by inhibiting the release of prothoracicotropic hormones and allatotropins (Banken and Stark 1997) however, it lacks contact toxicity (Islam and Talukder 2005; Morgan 2009); rotenone is powerful inhibitor of cellular respiration, exerts its toxic effect on nerve and muscle cells; pyrethrins block voltage gated sodium channels in nerve axon; essential oils monoterpenes are inhibitors of choline esterase (Miyazawa et al. 1997; Owokotomo et al. 2015) while some plant derivatives inhibit moulting processes resulting in considerable reduction of insect population (Mohal et al. 2006); interfere with normal growth processes (Dwivedi and Garg 2003; Morya et al. 2010).

Table 3.

Bioactivity and mammalian toxicity of botanicals effective against storage insects

Name of the plant	Bioactivity	Mammalian toxicity Oral (rat) LD 50 (mg/kg)
Acorus calamus L.	Antigonadial activity	200–500
Allium sativum L.	Insecticidal	4800
Annona squamosa Linn.	Insecticidal	300
Azadirachta indica A. Juss.	Antifeedant, insect growth regulator, repellent	>5000
Aloe vera L.	Repellent	>200
Carum carvi L.	Fumigant	1640
Chrysanthemum cinerariifolium Trevir.	Insecticidal	350–500
Derris elliptica Wall.	Insecticidal	132
Euphorbia fischeriana Steud.	Feeding deterrent	>1500
Eucalyptus globulus Labill.	Repellent	12,302
Eucalyptus saligna Sm.	Insecticidal and repellent	2290
Nicotiana tobaccum L	Insecticidal	50–60
Ocimum gratissimum L.	Insecticidal, repellent	>12,882
Pongamia pinnata L.	Repellent, antifeedant	2000
Ricinus communis L.	Insecticidal	2000
Schoenocaulon officinale Schltdl. & Cham.	Neurotoxic	4000
Tagetus erecta L.	Repellent	3700
Vitex negundo L.	Repellent, fumigant	2000

Table 4.

Mechanism of action of different botanical insecticides against storage insects

Botanical pesticides	Mechanism of action	References
Azadirachtin	Hormonal balance disruption	Copping and Menn (2000)
Nicotine	Mimics acetyl choline	Kukel and Jennings (1994)
Rotenone	Mitochondrial poison	Khambay et al. (2003)
Sabadilla	Affect nerve cell membrane action	Bloomquist (2003)
Thymol	GABA gated chloride channel	Enan (2005)
Essential oils	Octopaminergic system	Keane and Ryan (1999)

N-β-glucopyranosyl-p-hydroxy phenyl acetamide, p-hydroxy phenyl acetic acid and p-hydroxyphenyl acetonitrile isolated from Drypetus gossweileri Exell. inhibit the activity of acetylcholinesterase (Fournier 2005; Dohi et al. 2009) of insect pests where as terpenoid limonene (25) increases the spontaneous activity of sensory nerves. Chaubey (2011) reported that inhibiton of AChE activity occurred by fumigation of S. oryzae adults with sublethal concentrations of α-pinene, β- caryophyllene isolated from essential oils of C. cyminum and P. nigrum whereas Miyazawa et al. (2001) and Houghton et al. (2006) observed inhibiton of acetylcholine esterase activity by terpenes. Methyl isothiocyanate isolated from Boscia senegalensis Lam Ex. Poir. exhibited insecticidal activity against S. zeamais and T. castaneum by enzymatical degradation of glucocapparin (Gueye et al. 2011, 2013). In recent work, Rajashekar et al. (2014b) reported coumarin, a biofumigant isolated from L. camara as acetylcholine esterase inhibitor of S. oryzae.

Constraints in the development and use of plant derieved insecticides

Plant based insecticides face number of challenges in their development, manufacture and application. In India so far, only Azadirachtin (neem based), Pyrethrum sp, Cymbopogon sp are registered as botanical pesticides under Insecticides act, 1968 and among them, only neem based products hold potential ( Kandpal 2014). Production of plant materials on large scale, inadequate field based data, slow action, lack of residual action, improper standardization of formulation procedures for regulatory approval, difficulty in commercialization due to high cost of meeting the registration protocols including toxicological testing and inadequate shelf life are the major problems hindering the development of plant based products.

How to overcome the constraints of botanicals

Policy makers should emphasize on propagation of plants having insecticidal properties locally on large scale so that raw materials may be available freely for production of botanical pesticides. Scientific community must produce adequate data on field based application of botanicals compared to laboratory bioassays. The shelf life of plant based pesticides can be increased by the use of nano particles like nano silica and nano alumina against storage insects. The efficacy of botanicals can also be improved by blending with fixed seed oils; for example, natural pyrethrum extract can be enhanced by blending with seed oil of Gossypium hirsutum (Wanyika et al. 2009). Residual action can be enhanced by nano encapsulated formulations as they have the ability of control release of molecules at the site of action (Jhones et al. 2014). Formulations of botanicals can be standardized by the use of nanotechnology for isolation, purification and compounding of natural products. The cost of testing the botanical pesticides for human toxicity should be reduced so that commercialization can become easier. Use of high end technologies such as chemoinformatics, bioinformatics helps in identification of genes and pathways that are associated with secondary plant metabolites of botanicals.

Future trends

The use of plant based insecticides as synergists to synthetic insecticides have broader use in future by nano formulated bioproducts. Studies on mode of action of pure isolated compounds targeted against specific storage pests are essential. Using of biomass i.e., extraction and isolation of compounds from maize husk, silk, shank can be advantageous such as d- limonene from citrus peel (Isman 2010). Further, more biodegradable and target selective compounds are needed for integrated storage insect pest management. Investigations on mammalian toxicity and or toxicity to non target organisms, organoleptic characteristics of treated grain should be carried out apart from testing of botanicals for insecticidal, repellant and fumigant properties. As a result of nano formulations (particularly encapsulated forms) from natural plant extracts, new ways for control of storage insect pests will emerge in stored ecosystem for a secure future.

Conclusions

This review paper provides current perspective of the potentiality of botanicals for the management of storage insects of maize. Top priority must be given to insecticidal bio molecules for the control of storage insects as they are biodegradable and reduce the problem of increasing pest resistance. It is high time to focus research on use of plant derived compounds with nano particles for the development of potential stored grain protectant.

Compliance with ethical standards

Conflicts of Interest

There is no potential conflict of interest reported from the authors.