Efficacy of new molecule of insecticide, Emamectin benzoate against polyphagous pest, Helicoverpa armigera (Hubner): A review

Introduction

Popularly known as Gram pod borer, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is polyphagous pest and it attacks a number of economically important crops both agricultural (cotton, maize, sorghum, tobacco, pigeon pea, green gram, chickpea, black gram, red gram) and horticultural crops (tomato, chilli, okra and onion) and ornamental crops (Islam et al. 2020) [1] . The countries affected by the devastating attack of H. armigera on various crops include India, Pakistan, Turkey, Mexico, Iran, Australia and Ethiopia (Dinesh et al., 2018) [2] . It attacks 182 plants species from 68 different families (Reigada et al. 2016) [3] . Because of its polyphagy, mobility as adults, and high fecundity (Sudha Rani, et al., 2018) [4] . Now days, H. armigera management facing considerable challenges in many crops of the world (Li et al, 2018; Patil et al., 2017). It is cosmopolitan pest infesting many host plants (Fite et al., 2020) [7] . The incidence of this insect begins from early vegetative to maturity stage of the crop. At early stage, the young larvae starts feeding on leaflets, buds, flowers and finally green pods various pulses (Kassi et al. 2018) [8] . Under favorable environmental conditions it may cause average of 80-90 % damage (Javed et al. 2018) [9] . The H. armigera responsible for causing economic damage and capable of migrating over large distances Junhirun et al., 2018 [10] and its preference for flowering and fruiting parts results in heavy loss up to 60 per cent or more under subsistence agriculture in the tropics Japur et al., 2016 [11] . Helicoverpa armigera is a charismatic insect pest in agriculture accounting for the consumption of over 55 per cent of total insecticides used in India Puri et al.,1995 [12] . The problem of this pest is magnified due to its direct attack on fruiting structures, voracious feeding habits, high mobility, fecundity and multivoltine overlapping generations Sarode,1999. H. armigera caterpillars infest flowering and fruiting structures of host plants. The extensive use of insecticides and the nature of damage of H. armigera on attacked crops result in high costs of control and low productivity Thameur et al. 2020 [14] . Farmers largely follow the chemical method as it gives quick results. High frequency application is the common scenario Patil et al. 2020 [17] Chemical control the pests easy adaptability, effectiveness and immediate control. The indiscriminate and irrational use of chemical insecticide resulted in pest resurgence, resistance and residues. The cotton and pulses growers in India depend heavily on synthetic pesticides to combat pests and the crop consumes about 54 per cent of the total insecticides used in the country.

However, the indiscriminate use of organophosphates, carbamates and synthetic pyrethroids has created a number of problems such as pests developing resistance to insecticides, pest resurgence and residues in soil Ahmad et al. 2019 [16] . The existing chemicals are becoming absolute in the management of pest. Helicoverpa armigera management (IPM) approach but its management is largely based on synthetic insecticides. The adaptability of insect pests to most of conventional insecticides is leading to economic yield losses with increased negative side-effects to environment is a big challenge to the modern agriculture Bird, 2017 [17] . So newer molecules are to be evaluated for their efficacy. The indiscriminate usages increase cost of cultivation, has also led to destruction of natural enemies. For avoiding this, extra care is required in introducing newer molecules. One such new molecule, emamectin benzoate is a semi synthetic derivative of avermectin produced as fermentation metabolites of soil actinomycetes Streptomyces avermitilis Burg., Lasota and Dybas. 1990 [60] . This was discovered in 1984 and has both stomach and contact action effective against lepidopteran pests. It has been reported to possess excellent action against pests cotton and vegetables. It acts on the nerve cells to suppress muscle contraction thus inhibiting the larvae from feeding Govindan et al., 2010 and Lammers, 2018 [21] . Emamectin benzoate 5 SG with novel mode of action that is effective even at lower doses and safer to the natural enemies.

Losses caused by Helicoverpa armigera various field crops

The average crop losses in India due to this polyphagous pest are estimated to be US $350 million annually Hayden and Brambila, 2015. According to Vinoth,2017 the global losses from this pest can be in excess of $2 billion annually. The gram pod borer, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) is highly polyphagous pest and yield loss caused by various agricultural crops reported by several scientist and presented. The Helicoverpa armigera is a polyphagous insect and attacks more than 200 species of almost 45 crops throughout the world Rabindra et al.,2004. The total annual yield loss of different crops by Helicoverpa armigera has been reported to be a worth of 2 billion US dollars. On an average, 2.5 to 3.0 million tonnes of pulses are lost annually due to pest problems [24] . The annual loss due to this was estimated to be US $ 400 million in pigeonpea Krishna et al., 2016 [25] . A yield loss due to pod borers in pigeonpea was estimated to a tune of 40.6 per cent. Several insects have been reported to infest pigeonpea crop at different stages during its growth period in different parts of the country Priyadarshini et al. 2013 [26] . Chickpea due to H. armigera was reported as 10-60 per cent in normal weather conditions Dinesh et al., 2018 [2] . Its preference for flowering and fruiting parts results in heavy loss up to 60 per cent or more under subsistence agriculture in the tropics. The pest feeds voraciously from seedling stage to maturity and causes about 50 to 60 per cent damage to the chickpea pods Babar et al. 2012. Saxena Saxena et al. 2012 stated that pod borer complex infesting redgram heavy yield loss (60 %) is due to H. armigera alone. The extent of losses in Chickpea caused by H. armigera varies from region to region and depends upon climate and crop intensity. Its preference for flowering and fruiting parts results in heavy monetary loss of 203 crore rupees annually Suneel Kumar and Sarada, 2015 [29] . Gram pod borer, Helicoverpa armigera caused yield losses ranging from 40-50 per cent has been reported and may cause even total loss of the crop Rai et al., 2003 [30] . Biradarpatil et al., 2018 [31] reported that capsule borer, H. armigera infested in safflower at harvesting stage, 93.8 to 100 per cent of capsules will be bored, and 57.69 to 80.11 per cent capsule will not have any grains. In cotton crop decline in 15 per cent cotton yield resulting in loss of more than Rs 2000 crore annually due to H. armigera has been estimated in India Duraimurugan and Regupathy. 2005 [32] . Cotton highly affected by H. armigera with 80 per cent loss Fakrudin et al., 2004 [33] . Helicoverpa armigera cause 25 per cent yield losses generally and in rigorous infestation 40-70 per cent yield loss in sunflower Muhammad et al., 2004 [42] .

Losses caused by Helicoverpa armigera various horticultural crops

Helicoverpa armigera is a polyphagous pest and it can infest a large number of crops and lower the market value of the vegetable crops Prasanna et al., 2013 [35] . H. armigera to cause economic harm. Around US $ 78 billion is the annual value of the crops that are exposed to this species Yengkhom et al., 2019 [36] . Islam et al., 2020 [1] who reported that responsible for 40-50 percent damage to the tomato crop and a yield loss in the range of 20 to 60 per cent Herald and Tayde. 20189. Heavy damage is inflicted by okra fruit borer inflicts direct losses in yield of marketable fruits and vitality of plant resulting in 54.04 percent net yield loss Lammers, 2018 [21] . In okra yield losses (54.04 %) and fruit damage (35-75 %) Karthikeyan and Ayysamy, 2018 [38] . Considerable economic losses due to Helicoverpa armigera reported by many workers to the extent of about 50-60 per cent in tomato fruits Reddy and Zehrm, 2004. Tomato fruit borer, Helicoverpa armigera is highly destructive pest causing serious damage and responsible for significant yield loss up to 55 per cent Talekar et al., 2006 [40] . It also caused 40 Helicoverpa armigera damage to fruit which is of up to 3.48% of economic damage level. Fruit damage results into disfiguration of surface, rotting through secondary infection by bacteria Swodesh and Bhishma, 2019 [43] . Okra fruit borer, H. armigera is the most serious pest which cause direct damage to tender fruits Thara et al., 2019 [44] . Helicoverpa armigera is reported that about 69 per cent losses in marketable yield due to attack of this insect pest Kanwar and Ameta, 2007 [45] . As reported by Baikar and Naik, 2016 [46] due to severe attack of H. armigera lead to 90 per cent flower and fruit drop in chilli. Economic yield loss in chilli may be 11-75% quantitatively and 60-80 per cent qualitatively in the event of serious infestation Ghosh et al., 2009 [47] .

Biology of pod borer Helicoverpa armigera

Life cycles of Helicoverpa armigera take about 30-34 days with an average temperature of 28 °C from egg to adult Yengkhom et al., 2019 [36] . The oviposition period lasts for 5 to 24 days, and a female may lay up to 3000 eggs (mainly at night) on leaves and flowers. Major chickpea-producing countries pods. Eggs are laid singly on leaves, flowers and young pods. The egg incubation period depends on temperature and varies between 2 and 5 days (usually 3 days). The duration of larval development depends not only on the temperature but also on the nature and quality of the host plant. It varies between 15.2 days on maize and 23.8 days on tomato. The number of larval instars varies from 5 to 7, with 6 being most common Alit et al., 2009. The larvae pupate is in the soil. The pre-pupal period lasts for 1 to 4 days. The larvae spin a loose web of silk before pupation. In non-diapausing pupae, the pupal period ranges from about 6 days at 35 °C to over 30 days at 15 °C Alit et al., 2009. The diapausing period for pupae can last several months. Pale colored adults are produced from pupae exposed to temperatures exceeding 30 °C. Female moths generally live longer than males. In the laboratory, longevity varies from 1 to 23 days for males and 5 to 28 days for females. The pod borer exhibits a facultative diapause, which allows it to survive adverse weather conditions in both winter and summer seasons. Crop Protection Compendium, 2007 Edition. © CAB International Publishing, Wallingford. The winter diapause is induced by exposure of the larvae to short photoperiods and low temperatures. In China and India, pod borer populations are composed of tropical, sub-tropical, and temperate ecotypes. In subtropical Australia, the pod borer undergoes diapauses during the winter, when temperatures are low. High temperatures can also induce diapause. It enters a true summer diapause when the larvae are exposed to very high temperatures (43 °C for 8 h daily), although the proportion of females entering diapause is nearly half compared with that of males. At these temperatures, non-diapausing males are sterile.

Nature of damage caused by Helicoverpa armigera

The 1 st , 2 nd , and 3 rd instar larvae initially feed on the foliage (young leaves) of chickpeas and a few other legumes, but mostly on the flowers and flower buds of cotton, pigeon pea, etc. Larvae shift from foliar feeders to developing seeds and fruits as larval instar development progresses Dinesh et al., 2018 [2] . The young chickpea seedlings may be destroyed completely, particularly under tropical climates in southern India. Larger larvae bore into pods/bolls and consume the developing seeds inside the pod Kailash et al., 2009 [49] . The pod borer attacks crop from seedling to maturity, damaging all parts of the plant (leaves, flowers, and pods). Initially, the larvae feed on the leaves and tender twigs of the chickpea plant, and later, when the pods areformed, the larvae bore into the pods and feed, resulting in low yield. The young pod borer larvae (1st, 2nd, and 3rd instar) occasionally enter the pod and feed upon the developing chickpea grains, but more often they feed from outside the pod with only the anterior part of its body in the pod Kailash et al., 2009 [49] .

Host ranges for Helicoverpa armigera H. armigera is a major economic pest of many agricultural and horticultural crops Torres al., 1996. It feeds on over 300 species belonging to 68 plant families around the world, including major crops such as cotton, soybean, maize and a wide range of horticultural crops Pearce et al., 2017. The most important host crops of H. armigera are tomato, cotton, pigeon pea, chickpea, sorghum, and cowpea. Other hosts include dianthus, pelargonium, chrysanthemum, groundnut, okra, peas, field beans, soybeans, lucerne, Phaseolus spp., other Leguminosae, tobacco, potatoes, maize, flax, a number of fruits (Prunus, Citrus), forest trees, and a range of vegetable and flower crops Kanwar and Ameta, 2007 [45] .

Chemical structure and properties of emamectin benzoate 1. Avermectins 1.1 Discovery

Avermectins represent a novel class of macrocyclic lactones that have nematicidal, acaricidal and insecticidal activity. They are a mixture of natural products produced by a soil actinomycete, Streptomyces avermitilis Burg., MA -4680 (NRRL 8165), which was isolated in culture at the Kitasato Institute from a soil sample collected at Kawana Ito City, Stizuoka prefecture, Japan. In screening procedure, cultures were fermented and whole broth tests were conducted for six days via diet incorporation (0.0002% of the diet) on mice infected with Nematospiroides dubius (B.), a gastrointestinal nematode. The in vivo tests demonstrated good antihelminthic activity. The isolation, characterisation and structural elucidation of the avermectins have been described by Burg and Stapley, 1989 [52] .

Structure and chemistry

The avermectins primarily consist of four major (A1a, A2a, B1a, B2a) components and four homologous minor (A1b, A2b, B1b, B2b) components (Fig 1). The "A" series has a methoxy group at the C 5 position of cyclohexane moiety, while the "B" series has a hydroxyl group. In the "2" series, the double bond is hydrated, having a hydroxyl group at C 23 while in "1" series a double bond exists between C 22 and C 23 . The "a' series has a secondary butyl group at C 25 , while the "b" series has an isopropyl group. The disaccharide substituent at C 13 contains two identical  -L -oleandrose units. The B series has more biological activity than the A series (Albers et al.,1981). Abamectin is a mixture of B1a ( 80%) and B1b ( 20%), utilized for the control of agricultural and household arthropod pests. [60]

Mechanism of action

The experimental findings by Lasota and Dybas, 1990 [60] and Wright,1985 highlighted the avermectins are likely to act on GABAergic (Gamma -aminobutyric acid) neurons. Turner and Schaeffer, 1989 [55] reported that avermectins increase the muscle permeability to chloride ions, thereby reducing excitatory potentials and input resistance and reduction in membrane permeability. It causes the action of picrotoxin (Chloride ion channel blocker) and bicuculline (GABA receptor antagonist). Thus, avermectins act as a chloride channel agonist (Albrecht and Sherman, 1987). Demonstrated that avermectins are functioning as a GABA agonist in roundworm (Humans) as a model system Kass et al., 1984 [57] . In addition, physiological evidence suggests an increase in membrane permeability to chloride ions Scott and Dwe, 1985 [58] . Sami and Vaid, 1988 [59] proposed that the affinity of avermectins for retinol binding proteins would also have a possible mechanism of action of avermectins. Abamectin which belongs to the avermectins group, has potent pesticidal activities. It is a broad spectrum pesticide and highly toxic to many arthropods including spidermites, agromyzid leafminers, ants, cockroaches and selected lepidopteran pest species Dybas, 1989 [60] and Pearce et al., 2017. Abamectin is ecologically a selective compound with short residual, low -contact activity rather than physiological selectivity Strong and Brown,1987. Abamectin is toxic to 84 species of insects in 10 orders, most of which are of economic importance and abamectin is also a promising and effective acaricide Strong and Brown, 1987.

Bio efficacy of emamectin benzoate against Helicoverpa armigera in field crops

Several scientists evaluated the efficacy of emamectin benzoate against Helicoverpa armigera and presented below. [62] Very effective in reducing the boll damage 2 Cotton American boll worm H. armigera EB 5 SG 11 g a.i. ha -1 Lammers, 2018 [21] Effective in reducing the larval population 3 Cotton Bollworm complex EB 5 SG 11 g a.i. ha -1 Karthik and Thiruveni, 2017 [63] Effectively reduced the boll damage 4 Sorghum Ear head worm, H. armigera EB 5 SG 11 g a.i. ha -1 Nagare et al., 2018 [64] High mortality of 96 to 100 per cent [65] Effectively reduced the pod damage 7.

Gram pod borer, H. armigera EB 5 SG 11 g a.i. ha -1 Yadav et al., 2018 [66] Effectively reduced the pod damage and larval population 8 Sun flower Capitulum borer, H.armigera EB 1.9 EC 200 ml / acre Muhammad et al., 2020 [34] Effective in reducing the larval population

Bioefficacy of emamectin benzoate against

Helicoverpa armigera in horticultural crops: Several scientist evaluated the efficacy of emamectin benzoate against Helicoverpa armigera and presented below. Effectively reduced the fruit damage Fruit borer, H. armigera 5% WDG 3 g/10 Liter Sarkar and Rai, 2015 [70] Effectively reduced the fruit damage 2 Okra

Fruit borer, H. armigera 5SG 3 g/10 Liter Thara et al., 2019 [44] Effectively reduced the fruit damage Fruit borer, H. armigera 1.9 EC 3 g/10 Liter Karthikeyan and Ayysamy, 2018 [38] Effectively reduced the fruit damage

Tomato

Fruit borer, H. armigera 5SG 4 g/10 Liter Taimur et al., 2018 [65] Effectively reduced the fruit damage Fruit borer, H. armigera 1.9 EC 4 ml /10 Liter Khan et al., 2019 [68] Effectively reduced the fruit damage Fruit borer, H. armigera 5SG 4 g/10 Liter Islam et al., 2020 [1] Very effective in reducing the fruit damage and larval population

Fruit borer, H. armigera 5SG 4 g/10 Liter Patil et al. 2020 [15] Very effective in reducing the fruit damage and larval population 4. Grapes Fruit borer, H. armigera 5SG 4 g/10 Liter Muthukrishnan et al., 2012 [69] Very effective in reducing the fruit damage and larval population

Conclusion

After reviewing findings of several researchers it can be concluded that gram pod borer, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is polyphagous pest and it attacks a number of economically important crops both agricultural, horticultural crops and ornamental crop. It feeds on over 300 species belonging to 68 plant families around the world, including major crops. Now days, H. armigera management facing considerable challenges in many crops of the world. A critical review on various groups of chemical insecticides indicates that for the last five decades conventional insecticides, all neuroactive chemicals have played major role in management of insect pests in pulses, their indiscriminate uses led to several problems like resistance, residue, resurgence and safety to environment. The focus therefore shifted to search for and development of new green chemistries having novel biochemical targets in the context of pest control and resistance management. The novel groups of insecticides like emamectin benzoate is very effective at lower doses and have low risk to non-target organisms and environment, and their versatility in application methods. These important classes of new insecticides will certainly play a greater role in the present context of environmental safety and their consequent uses in integrated pest management and insect resistance management programmes. The main advantages of emamectin benzoate are ecofriendly, easily biodegradable, nontoxic to non target organisms and could be exploited for sustainable insect pest management of H. armigera in field and horticultural crops.

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