Helicoverpa zea
(bollworm)

Helicoverpa zea is confined to the New World. It occurs throughout the Americas from Canada to Argentina (International Institute of Entomology, 1993).

Helicoverpa zea was recently added to the EPPO A1 list of quarantine pests and is also considered as a quarantine pest by APPPC. Originally, H. zea was considered as practically synonymous with Helicoverpa armigera, an A2 quarantine pest (EPPO/CABI, 1996). The addition to the EPPO list harmonizes it with EU Directive Annex I/A1.

Phytosanitary Measures

For the related H. armigera, EPPO (OEPP/EPPO, 1990) makes recommendations on phytosanitary measures which would also be suitable for H. zea. According to these, imported propagation material should derive from an area where H. armigera does not occur or from a place of production where H. armigera has not been detected during the previous 3 months.

Bibliographies are included in the monograph by Hardwick (1965) (2000 titles on H. zea), and the reviews by Fitt (1989) (194 titles), and King and Coleman (1989) (159 references). Most of the basic research on H. zea was done in the early 1900s and published under early synonyms. Many references to H. zea are made in publications relating to the cultivation/protection of specific crops, for example, Chiang (1978), Centre for Overseas Pest Research (1983) and Pitre (1985).

Helicoverpa zea is polyphagous in feeding habits but it shows a definite preference in North America for young maize cobs, and particularly for the cultivars grown as sweetcorn and popcorn, and also for sorghum. Most hosts are recorded from the Fabaceae (41% of total), Solanaceae (14%), Poaceae (9%), Asteraceae (8%) and Malvaceae (8%) (Cunningham and Zalucki, 2014); in total, more than 100 plant species are recorded as hosts. A feeding preference is shown for flowers and fruits of host plants.

For further information see Barber (1937), Neunzig (1963), Davidson and Peairs (1966) and Matthews (1991).

Eggs are laid mostly on the silks of maize plants in small numbers (one to three), stuck to the plant tissues. However, in cotton, they are mostly laid on the leaves throughout the plant, but are more common near blooms (Braswell et al., 2019a, b). Choice of oviposition site by the female seems to be governed by a combination of physical and chemical cues. Female fecundity can be dependent upon the quality and quantity of larval food, and also on the quality of adult nutrition. Up to 3000 eggs have been laid by a single female in captivity, but a few hundred to a thousand per female is more usual in the wild (Quaintance and Brues, 1905; Bilbo et al., 2018). Hatching occurs after 2-4 days and the eggs change colour from green through red to grey. The tiny grey larvae first eat the eggshell and most of the newly hatched larvae disperse from the plant or die (Zalucki et al., 2002; Braswell et al., 2019a, b). Those that remain wander actively for a while before starting to feed on the plant. In maize, they usually feed on the silks initially and then on the young tender kernels after entering the tip of the husk. By the third instar the larvae become cannibalistic and usually only one larva survives per cob. Feeding damage is typically confined to the tip of the cob. In cotton, small larvae initially feed on squares (flower buds), but they can consume small bolls. Once larvae gain a sufficient size, they begin to feed on larger sized bolls (Braswell et al., 2019a). Larval development usually takes 14-25 (mean 16) days, but under cooler conditions up to 60 days may be required. In the final instar (usually sixth) feeding ceases and the fully fed caterpillar leaves the cob and descends to the ground. It then burrows into the soil and forms an earthen cell, where it rests in a prepupal state for a day or two, before finally pupating. Two basic types of pupal diapause are recognized, one in relation to cold and the other in response to arid conditions. In the tropics, pupation takes 10-14 (mean 13) days; the male takes 1 day longer than the female. Diapausing pupae are viable as far north as 40-45°N in the USA.

Adults are nocturnal in habit and emerge in the evenings. Maize fields in the USA regularly produce 40,000 to 50,000 adult moths per hectare. Flying adults respond to light radiation at night and are attracted to light traps (Hardwick, 1968), especially the ultraviolet type, in company with many other local noctuids. Sex aggregation pheromones have been identified and synthesized for most of the Heliothis/Helicoverpa pest species, and pheromone traps can be used for population monitoring. Adult longevity is recorded as being about 17 days in captivity; they drink water and feed on nectar from both floral and extrafloral nectaries. The moths fly strongly and are regular seasonal migrants, flying hundreds of kilometres from the USA into Canada. They migrate by flying high with prevailing wind currents.

The life cycle can be completed in 28-30 days at 25°C and in the tropics there may be up to 10-11 generations per year. All stages of the insect are to be found throughout the year if food is available, but development is slowed or stopped by either drought or cold. In the northern USA there are only two generations per year, in Canada only one generation.

For more information, see Hardwick (1965), Beirne (1971), Balachowsky (1972), Allemann (1979), King and Saunders (1984) and Fitt (1989).

Kogan et al. (1989) provides a full list of natural enemy records and their relative importance in biological control is discussed in Reay-Jones (2019).

Feeding damage is usually visible and the larvae can be seen on the surface of plants but often they are hidden within plant reproductive tissue (flowers, fruits, etc). Bore holes may be visible, but otherwise it is necessary to cut open the tissue to detect the pest. Because of morphological similarity, it is impossible to distinguish the larvae of H. zea from those of Helicoverpa armigera, already present in the EPPO region. Positive identification is achieved by rearing the larvae and examining the genitalia of the adult.

The adults are similar in appearance to Helicoverpa armigera but differ in several details in their genitalia (Hardwick, 1965); dissection and slide-mounting are required for specific morphological determination, and some aspects are comparative so that a series of closely related species have to be available for comparison. H. armigera and H. zea can be distinguished using molecular techniques. Where H. armigera is invasive in South America, it can hybridize with H. zea (Anderson et al., 2018). In Brazil, these hybrids are more common in areas with more maize and soyabean production (Cordeiro et al., 2020).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Control

Introduction

Control of H. zea has been advocated in the USA since the middle of the 19th century, and measures fall into two broad categories: those aimed at an overall pest population reduction and others aimed at the protection of a particular crop. In most situations it is now recommended that integrated pest management be used (Bottrell, 1979).

Cultural Control

Various cultural practices can be used to kill the different instars, including deep ploughing, discing and other methods of mechanical destruction, manipulation of sowing dates and use of trap crops.

Biological Control

In many areas, natural control of this pest may be quite effective for most of the time. Insect parasitoids attack the eggs (especially Trichogramma spp.) and larvae, and some predators can be important in reducing pest populations. King and Coleman (1989) discuss the prospects for long-term biological control of Heliothis/Helicoverpa spp., and clearly this should be an important component of any regional IPM programme.

The most frequently tried method of achieving biological control has been by augmentative releases of artificially reared parasites or predators, especially using Trichogramma spp. However, releases in cotton have not been consistently effective against heliothine populations. Microplitis croceipes could be more effective because it is less affected by organophosphate pesticides and synthetic pyrethroids.

There has also been interest in exploiting entomophagous pathogens such as Bacillus thuringiensis and Heliothis NPV. NPV is commercially applied worldwide for control of Helicoverpa species, especially in Australia and Brazil, but increasingly in the USA. A number of pest and beneficial arthropod species can aid in dispersing the virus beyond where it is applied (Black et al., 2019). In cotton, maize and soyabean, transgenic crop varieties expressing the active B. thuringiensis toxin have been used commercially.

Host-Plant Resistance

The development of crop cultivars resistant or tolerant to damage by Helicoverpa spp. has major potential in their management, particularly for communities with few resources. Many crops possess some genetic potential that can be exploited by breeders to produce varieties less subject to pest damage. Resistance can take three basic forms: antixenosis, antibiosis and tolerance. Varieties of crop hosts showing resistance to Helicoverpa spp. have been identified or developed in cotton, chickpeas, soyabean, tomato, maize, sorghum, millet and tobacco.

In maize, resistant genotypes have been identified which have a high concentration of maysin (rhamnosyl-6-C-(4-ketofucosyl)-5,7,3',4'-tetrahydroxyflavone), a C-glycosyl flavone, in silk tissue. Quantitative trait loci for maysin production were identified on chromosomes one (p1) and nine (umc105a) (Byrne et al., 1996).

In cotton, gossypol glands on the calyx crowns of flower buds confers considerable resistance to H. zea (Calhoun et al., 1997).

Transgenic maize, cotton and soyabean containing genes encoding delta-endotoxins from Bacillus thuringiensis (Bt) kurstaki [Bacillus thuringiensis serovar. kurstaki] have been commercialized in various parts of the world. H. zea is targeted with Bt maize and cotton in the USA, and Bt maize, cotton, and soyabean in Brazil. Two types of Cry toxins (in the families Cry1A and Cry2A) have been used extensively, and H. zea has evolved resistance to these toxins in the USA (Dively et al., 2016; Reisig et al., 2018). Increasingly, these Cry traits are being pyramided with Vip3Aa20 in maize and Vip3Aa19 in cotton. H. zea is effectively controlled with the Vip3Aa toxin (Leite et al., 2018; Yang et al., 2020).

There is little knowledge of the interactions between natural enemies of Helicoverpa and host-plant resistance, but it cannot be assumed that resistance will always be compatible with natural control. For example, laboratory tests using resistant tomato plants containing an alkaloid (alpha-tomatine) were found to be toxic to Hyposoter exiguae, a parasite of H. zea. The parasite acquired the alkaloid from its host after the host had ingested the alkaloid (Campbell and Duffey, 1979).

Chemical Control

Chemical control of the larvae has been the most widely used and generally successful method of managing H. zea on most crops, but it is not easy because larvae feed within plant structures. The early history of chemical control of H. zea is given by Hardwick (1965). Pesticide resistance has been known for some years and is quite widespread (Fitt, 1989) especially on cotton crops.

For cotton, chlorantraniliprole is the most efficacious foliar insecticide, because it is systemic in the plant with long-lasting residual (Reisig et al., 2019; Babu et al., 2021). In soyabean, a suite of insecticides, including chlorantraniliprole, emamectin benzoate, indoxacarb, spinosad, spinetoram are effective. Foliar insecticides are not recommended in maize, as H. zea rarely limits yield (Reay-Jones and Reisig, 2014; Bibb et al., 2018; Olivi et al., 2019), however in sweetcorn, multiple sprays, with rotations and mixtures of chlorantraniliprole, pyrethroids, spinosad and spinetoram applications are generally made 3 days after silk emergence and applied on a weekly basis until silks dry down.

Sterile Backcrosses

Sterile male offspring are produced when certain species are crossed, for example, Heliothis subflexa and Heliothis virescens. This fact has been exploited and evaluated on the island of St. Croix, Virgin Islands, where after a three-year release programme, suppression was achieved.

Pheromonal Control

Mating of H. zea was reduced by 50% in a 12 ha maize field treated with hollow fibres containing (Z)-9-tetradecenyl formate (Mitchell and McLaughlin, 1982). Likewise, (Z)-11-hexadecenal, a component of the H. virescens pheromone, reduced the mating of females of H. zea by 85% (Mitchell et al., 1976).