Helicoverpa armigera is a major pest affecting both agricultural and horticultural crops across the globe. With a host range of over 100 cultivated and wild plants, its status as a significant pest is largely attributed to its polyphagous nature, high mobility, diapause capability and high fertility rate. The larvae can enter diapause to survive unfavourable climatic conditions, further complicating management efforts. H. armigera is widespread across majority of Asia, southern Europe, Oceania, Africa and South America. Management of H. armigera traditionally involves the use of synthetic insecticides, microbial insecticides, biocontrol agents (including both parasitoids and predators) and genetically modified crops like Bt cotton. However, the extensive use of chemical insecticides has led to the development of resistance in H. armigera populations, reducing the effectiveness of many conventional pesticides. Increasing resistance against existing pesticides directs the urgent need for utilizing integrated pest management (IPM) strategies, which are less dependent on traditional pesticides and manage the populations of pest below the economic threshold level (ETL). This review aims to highlight the significance of continued research and the adoption of modern approaches to effectively manage H. armigera populations and reduce crop losses.

American bollworm, Polyphagous, Biology, IPM, Pesticides.

In crop cultivation, yield can be significantly reduced by various factors, with arthropod pests being a major threat. Insects that damage ovary tend to be more destructive than those that target leaves, stems, or roots (Mapuranga et al., 2015). A range of plant families, including Asteraceae, Fabaceae, Malvaceae, Poaceae, and Solanaceae, suffer yield and quality losses due to various lepidopteran pests (Murúa et al., 2014). Among these pests, Helicoverpa armigera (Lepidoptera: Noctuidae) stands out as highly polyphagous, multivoltine, and cosmopolitan pest, widely regarded as one of the most damaging pests to field crops globally (Stark & Banks, 2003; Sharma et al., 2011; Saraf et al., 2015). This pest impacts approximately 300 plant species, affecting economically significant crops such as tobacco (Nicotiana tabacum), cotton (Gossypium hirsutum L.), maize (Zea mays L.),soybean (Glycine max L.),  sorghum (Sorghum bicolor L.), pearl millet (Pennisetum glaucum), canola, tomato (Solanum lycopersicum L.), okra (Abelmoschus esculentus),sunflower (Helianthus annuus L.), pigeon pea (Cajanus cajan), chickpea (Cicer arietinum L.), and groundnut (Arachis hypogaea), and is anticipated to become a formidable pest in certain fruit crops (Sarate et al., 2012; Vinutha et al., 2013; Murúa et al., 2014; Safuraie-parizi et al., 2014; Saraf et al., 2015).

The life cycle of Helicoverpa armigera is influenced by various biotic and abiotic factors such as temperature, host availability, and environmental conditions etc. This resilience is due to its traits such as being polyphagous, highly adaptable nature, having a strong reproductive potential, and the ability to enter facultative diapause. (Yadav et al., 2022). The insect's capability to utilize a wide range of host plants is essential for its continued survival in ecosystems. Underoptimal conditions, it completes several generations within a single year. The larvae are voracious feeders and can cause significant damage to crops by consuming leaves, flowers, and fruit. Helicoverpa shows color variation in green to brown shades. Generally, the 3rd instar larvae show cannibalism. The insect has a unique feeding behaviour in which it inserts its head within the plant portion while keeping the remaining parts outside. This behaviour is mostly for respiratory requirements. Due to the extensive use of chemicals, H. armigera has developed resistance to many insecticides, including newer compounds such as fipronil, chlorfenapyr and indoxacarb (Ahmad et al., 2003; Wu 2007). Consequently, growers need to adopt new compounds with novel modes of action (MoA) (Ahmad et al., 2019) and implement rotational chemical use to effectively manage this pest (Razaq et al., 2007; Su et al., 2012). Integrated Pest Management (IPM) approaches, involving the use of biological controls, pheromone traps, and timely insecticide treatments, are widely implemented to regulate H. armigera populations and safeguard crops. However, it is old world bollworm but it is still continuing to damage different crops and difficult to manage in some cropping pattern. So, the current review is to unravelling the current status and management strategies of H. armigera.

HOST RANGE AND DISTRIBUTION

Currently, H. armigera is widely distributed throughout the world, regarded as the primary agricultural pest in the Africa, Asia, Middle East, Southern Europe (Greece, Spain, Portugal, and Turkey), New Zealand, Australia and the Pacific Islands (Karim, 2000). According to Tay et al. (2017), H. armigera is native to the old-world including Africa, Asia, Europe and Australasia (Hardwick, 1965) identifying its original range between the latitudes of 40 N and 40 S (Fig. 1) (Yücel & Hanife 2018). The species is currently present in approximately 128 nations and other dependent territories. However, it is not yet well-established in some regions like Northern America (Gonçalves et al., 2019) but, there is a strong likelihood of establishment of this pest (Kriticos et al., 2015).

One of the most polyphagous insect pest species, H. armigera infests over 200 host plant species across various families (Pratissoli et al., 2015). It affects a broad range of economically important crops, including cotton, maize, sunflower, pigeonpea, chickpea, soybean, sorghum, as well as fruits and vegetables (Cunningham et al., 1999; Khanam et al., 2003; Rahman et al., 2016). Since host plants differ in their nutritional content, H. armigera exhibits strong preference for certain host plants. The choice of the host species also affects the survival & growth of the larvae, which affects the population density of the species (Yongming & Kunjun 2001). Likewise, Sarate et al. (2012) observed that larvae reared on maize and pigeon pea experienced faster growth and bigger larval and pupal masses than those raised on vegetables and flowers. However, the leaves of tomato, okra, chickpea, and pigeonpea are considered to be favorable hosts for the oviposition of H. armigera.

Fig. 1. Worldwide distribution of Helicoverpa armigera.

BIOLOGY

Helicoverpa armigera is a holometabolous insect with a complete life cycle of egg, larval, pupal and adult stages (Fig. 2). The mature H. armigera moth has a dull black border on its hindwing and a "V"-shaped spot on its forewing. It is brown in colour. The insect lays one egg per host plant and it takes 4-7 days for the egg to hatch. When the larva reaches maturity, it is about 2 inches long, greenish with brown-gray lines and has dark and pale stripes on its dorsal side. The six larval instars occur throughout the 14-day larval stage. Then, pupates in the soil. The ideal temperature for growth and reproduction has been reported to be around 25 C (Mironidis & Savopoulou- Soultani 2014). In most cases, it complete its life cycle in 4-6 weeks during the summer and 8-12 weeks in autumn season (Ali et al., 2009).

A. Eggs

Female moths of H. armigera lay their eggs singly or in small clusters on leaves, flowers or fruit. The eggs are spherical and initially pale white, but they gradually turn yellowish or reddish-brown just before hatching. The incubation period is about 3-7 days. At higher temperatures (on average 25ºC), fertile eggs will hatch in about 3 days. In cooler conditions, hatching typically takes between 6-10 days. As eggs develop, they undergo several stages, changing colour from white to brown and eventually to a stage with a black head before hatching. Not every egg is fertile. Physical factors have a significant impact on larval establishment and egg survival. Regarding the ovipositional preference of H. armigera, it has been reported that females lay significantly more number of eggs on pigeonpea in comparison to mungbean, cotton and common sow thistle (Rajapakse and Walter 2007). According to Jallow & Matsumura (2001), H. armigera preferentially oviposits on the leaves of okra, tomato and maize. Additionally, chickpea is also thought to be excellent host for oviposition (Razmjou et al., 2014). In some regions, pigeonpea has been used as a trap crop since the 1990s because it serves as a well-known host for oviposition in H. armigera (Baker et al., 2008; Baker & Tann 2014).

Fig. 2. Lifecycle of Helicoverpa armigera a. egg, b. larvae, c. pupae, d. adult male (left) and female (right).

B. Larvae (Caterpillars)

After hatching, the larvae emerge and start feeding on plant tissues. They undergo several instars (six stages) during their larval development and number of instars varies based on environmental conditions. This stage typically lasts for 14-30 days. The larvae have a cylindrical body with a brownish or greenish coloration, and they possess a characteristic pattern of stripes and spots. Neonate larvae chew through the eggshell to create an opening for their emergence. Newly hatched larvae have brown to black coloured head with white to yellowish-white body possess 1-1.5 mm long dark spots. Initially, the larvae feed on tender and immature leaves before moving to buds, flowers, young pods, bolls and fruits.

A larva is fully grown through six developmental stages (instars) in 2-3 weeks during summer and 4-6 weeks during spring or fall. When temperature go below 12ºC, larval activity and feeding cease. Third instar larvae, which are small to medium-sized (8-13 mm long) are responsible for 90% of the damage. The fifth and sixth instar are the most damaging stages, capable of consuming up to 80% of their total diet. Sixth instar larvae can grow up to 40 mm in length and exhibit a wide range of colors and patterns (Ali et al., 2009; Queiroz- Santos et al., 2018; Herald & Tayde  2018). 

C. Pupae

In the pre-pupal stage, larvae stop feeding and grow lethargic, wrinkled with movement (Ali et al., 2009). Individuals are typically between 22-29 mm long and 4-5 mm wide (Ali et al., 2009). Usually, the shade ranges from slightly green to yellowish, eventually becoming dark brown. Typically, the pre-pupal period lasts 1-3 days. Once the larval stage is complete, the caterpillar pupates to become an adult moth. The pupal stage occurs either in the soil or within a cocoon spun by the larva. The pupa is typically brown with a hardened outer shell that safeguards the developing moth. This pupal period lasts approximately 10 to 14 days (Ali et al., 2009; Nasreen and Mustafa 2000).

D. Adults (Moths)

After completing the pupal stage, an adult moth emerges. These medium-sized moths have a wingspan of approximately 3-4 cm and exhibit light brown or grayish-brown coloration with distinctive light and dark patches on their wings. Females have dull green to yellow or light brown forewings, while males display brownish or reddish-brown forewings. The hindwings are pale coloured with a broad black outer border and a prominent pale patch near the central black area of the border. Adult moths are primarily nocturnal and are attracted to lights. They have a lifespan of 1 to 2 weeks and feed on nectar. Females lay thousands of eggs singly on leaves, flower buds, developing fruits, and occasionally on stems and growing points throughout their lifecycle, often preferring the upper third of healthy plants and actively growing terminals (Zahid et al., 2008; Ali et al., 2009).

NATURE AND EXTENT OF DAMAGE

Starting from the second to third instar, larvae is the most destructive life stage, primarily feeding on the reproductive structures of plants. Although the first and second instars cause some damage by feeding on the leaf surface, the extent of this damage is generally minor. Polyphagy, facultative diapause, high fecundity and mobility are the four key characteristics of H. armigera (Fitt, 1989; Rahman et al., 2016). Its direct attack on plant reproductive organs, multivoltine nature, nocturnal habit and overlapping generations are further significant causes of their high infestations (Sarode, 1999). According to Sarode (1999), infestations of H. armigera in chickpea crops can lead to yield losses of up to 29% when no management practices are implemented. Similar losses have been documented in Pakistan for the tolerant and susceptible genotypes of chickpea (Sarwar et al., 2009, 2011). According to SreeLatha and Sharma (2018), the desi genotype of chickpea is observed to be more resistant to attack than the kabuli genotype. Different parameters like temperature and sowing time have a significant impact on the extent of larval damage by this pest (Akhtar et al., 2014). Thakur et al. (2017) reported that in the absence of control strategies, infestation rates of the fruit ranged from 16% to 45% in tomatoes cultivated in Himachal Pradesh, India. Selvanarayanan (2000) observed similar yield losses of up to 55% in tomatoes, with infestations often rendering the fruit unfit for human consumption (Lal et al., 1999).  According to Tripathy and Sharma (1985), the extent of plant damage varies depending on larval density and developmental stage. However, infestations commonly impact plant size, stem diameter, fruit morphology and overall fruit yield. 

ETL AND EIL FOR H. ARMIGERA ON DIFFERENT HOST CROPS

The Economic Injury Level (EIL) and Economic Threshold Level (ETL) for H. armigera on various crops have been estimated by several researchers (Table 1). However, these thresholds, particularly the EIL, are dynamic and can vary from year to year or even from field to field within a single year. Factors influencing these variations include crop variety, market conditions, plant development stages, available management options, crop value, and management costs.

Table 1: EIL and ETL for H. armigera on various crops.

MANAGEMENT 

A. Cultural Practices

∙ To keep H. armigera populations below the economic threshold level, certain cultural practices are implemented within the crop or cropping system. Fitt and Forrester (1987) highlighted the importance of ploughing cotton stubble to reduce populations of pyrethroid-resistant H. armigera. 

∙ Clean cultivation in fields and removal of alternate weed host like Legasca, Datura ferox, Lantana camera, Nicandra physaloides grown on the bunds is beneficial in reducing pest populations(Mapuranga et al., 2015; Genç & Yücel 2017). 

∙ Deep ploughing during the summer months is an effective method to kill immature stages of H. armigera by exposing the resting pupae to predatory birds and the intense heat of the sun (Mapuranga et al., 2015).

∙ It is important to follow the recommended fertilizer dosages and practice judicious water management to prevent excessive vegetative growth, which can create harbourage for larvae (Patil et al., 2017; Mahmood, 2021).

∙ Use of trap crops like Bhendi (cotton: bhendi, 25:1), Red gram and marigold are also used to trap & kill the eggs and young larvae of boll worms in early stage (Vinutha et al., 2013; Mapuranga et al., 2015; Genç & Yücel 2017).

∙ Crop should be sown at same time or in synchrony with short duration varieties in similar ecosystem. Avoid continuous cultivation of the same host crops during both rabi and kharif seasons in the same area, as well as ratooning, to reduce the risk of H. armigera infestations(Mapuranga et al., 2015; Patil et al., 2017; Mahmood, 2021).

∙ Avoid mono-cropping and alternate host crops. Removal and destruction of old crop residues is also recommended to avoid carryover of the egg masses to the next season (Mapuranga et al., 2015).

B. Mechanical management

∙ Eggs and larvae can be handpicked and destroyed during early stage of infestation when they feed gregariously. 

∙ Installation of bird perches @ 50/hectare & setting of light traps (1 light/5 acre) for reduction of adult moth population. 

∙ Pheromone traps @ 5 traps/ ha can be installed for monitoring of adult moths and 15 traps/ ha for management of pest (Vinutha et al., 2013).

C. Biological control

Natural enemies rarely eliminate all eggs or larvae but can sometimes reduce infestations to below economic threshold levels. H. armigera is targeted by various parasitic and predatory insects, spiders, birds, bats, rodents, and diseases.

i) Predator: Many predators are opportunistic feeders, consuming Helicoverpa armigera when encountered, while some are regularly found in farms. Additionally, certain predators target specific life stages, such as eggs or larvae of particular sizes. The most common predators in field crops include predatory beetles (Exochomus flavipes, Cheilomeneslinata, C. deisha, Hippodamia variegate), bugs (Phonoctonus spp., Aphidius spp., Encarsia sub lutea, Eretrocerus spp), lacewings, spiders (Cheirancanthium lawrencei, Prucetiakunensis) and ants (Mapuranga et al., 2015).

ii) Parasitoids: Eggs, larvae, and pupae of Helicoverpa armigera are targeted by various wasps and flies. To complete their development, these parasitoids must kill their hosts. Notable parasitoids include wasp species like Telenomus, Trichogramma and Microplitis, as well as larger wasps such as Netelia, Heteropelma, and Ichneumon, along with flies like Carcelia and Chaetopthalmus. These parasitoids are particularly active in field crops against Helicoverpa (Pratissoli et al., 2015; Saraf et al., 2015).

iii) Pathogen: Insect-infecting pathogens include bacteria, fungi, and viruses, which can naturally infect and kill Helicoverpa armigera. The most common pathogens affecting larvae are fungi such as Metarhizium, Nomurea, and Beauvaria, as well as nucleopolyhedrovirus (NPV) (Haile et al., 2021; Toffa et al., 2021; Souza et al., 2020). Additionally, ascovirus, spread by wasp parasitoids, inhibits larval growth. Two commercially available pathogens for controlling Helicoverpa larvae are NPV and bacterium Bacillus thuringiensis (Bt). NPV is safe for use around people, animals, and beneficial insects, while Bt, which exclusively targets moth larvae, is widely available. Moreover, cotton plants have been genetically modified to produce the Bt toxin in their tissues (Patil et al., 2017; Mantzoukas, 2019). 

D. Host Plant Resistance

Using resistant crop cultivars is one of the most effective and reliable methods for managing H. armigera. These cultivars are often a key component of integrated pest management (IPM) strategies, significantly reducing crop losses (Rahoo et al., 2017; Shahzaman et al., 2015; Thia et al., 2021). The primary aim of this approach is to minimize the use of broad-spectrum synthetic pesticides, which helps mitigate the negative environmental impacts of pesticide use, lowers production costs, and protects natural enemies of H. armigera, such as ichneumonid and braconid wasps (Kambrekar, 2016; Kassi et al., 2018).

E. Biotechnological control

(i) RNA interference (RNAi) technology: The H. armigera, is well known for its resistance to various common insect poisons. Thus, a biotechnological approach, such as RNA interference (RNAi) mediated by dsRNA is started. It involves the silencing of specific deadly genes. The dsRNA is delivered either by ingestion, infusion or by ingesting specially engineered microbial forms expressing dsRNA (Jing & Zhao-jun 2014). 

Another biotechnological strategy for pest control is nanotechnology. This involves pest management using formulations of pesticides, insecticides, bio-forms, anti-agents and pheromone based on nanoparticles. This improves the survivability and efficacy of these substances. In order to protect host plants from lepidopteran pests, it is also utilized to deliver DNA and other desirable synthetic materials into plant tissues (Vinutha et al., 2013).

(ii) Sterile insect technology: This technique is crucial for reducing pest populations in the field. It involves releasing radiation-sterilized male insects to limit population growth. Mating with these sterile males produces abnormal progeny, effectively controlling the pest population. This sterility method is advantageous as it does not interfere with other pest control strategies (Yadav et al., 2022; Yadav et al., 2022).

F. Botanicals

Azadirachtin: Applied at a concentration of 0.03% or in quantities ranging from 2.50 to 5 kg, azadirachtin functions both as an antifeedant, which reduces feeding activity and as a growth regulator, which impedes the development of H. armigera larvae (Mehta et al., 2010; Vinutha et al., 2013; Salman Ahmad et al., 2015).

Neem and Garlic Extracts: These botanicals exhibit multiple effects against H. armigera. Neem extracts can be utilized for their larvicidal and ovicidal properties for effective killing of larvae and eggs. They also act as toxic repellents, deterring the pests from feeding and have anti-ovipositional effects, reducing the likelihood of egg laying. Garlic extracts similarly contribute to pest management through their repellent and toxic properties, impacting both feeding behaviour and reproduction (Prakash & Srivastava 2008; Mehta et al., 2010; Vinutha et al., 2013).

G. Chemical control

Insecticides are continuing to be a crucial aspect of pest management, especially in short- and medium-term scenarios, allowing farmers to cultivate crops of sufficient quality at affordable prices (Bueno et al., 2017). In comparison to biopesticides, synthetic pesticides are often more effective at controlling H. armigera (Rizvi & Jaffar 2015). Ambule et al. (2015) reported successful control of H. armigera on tomato crop in India after the introduction of novel insecticides like flubendiamide and chlorantraniliprole. Spinosad, a mixture of various substances derived from the bacteria Saccharopolyspora spinosa (Mertz & Yao), is also very efficient in controlling this pest (Ambule et al., 2015; Hakeem et al., 2017). High pesticide doses can completely eradicate the target pest, although sublethal effects can also reduce the pest species' fitness and reproductive rates without actually killing them. According to Carneiro et al. (2016), sublethal pesticide doses in H. armigera produce physiological abnormalities and have a negative impact on the fertility, development and longevity of the pupal stage, pupal weight and the oviposition phase. Novaluron, indoxacarb, chlorantraniliprole, cyantraniliprole, imidacloprid, diazinon and flubendiamide, as well as the bacterium-derived substances spinosad and emamectin, are a few examples of synthetic chemical insecticides that have been successfully utilised against H. armigera in different crops (Table 2).

Table 2: List of Insecticides and Biopesticides approved by CIB & RC against Helicoverpa armigera in different crops.