Helicoverpa zea (bollworm)

The taxonomic situation regarding H. zea is complicated and presents several problems. Hardwick (1965) reviewed the New World corn earworm species complex and the Old World African bollworms, most of which had previously been referred to as a single species (Heliothis armigera or Heliothis obsoleta), and pointed out that there was a complex of species and subspecies involved. Specifically, he proposed that the New World H. zea (first used in 1955) was distinct from the Old World H. armigera on the basis of male and female genitalia; he described the new genus Helicoverpa to include these important pest species. Some 80 or more species were formerly placed in Heliothis (sensu lato) and Hardwick referred 17 species (including 11 new species) to Helicoverpa on the basis of differences in both male and female genitalia. Within this new genus the zea group contains eight species, and the armigera group two species with three subspecies (Hardwick, 1970).

Because the old name of Heliothis for the pest species (four major pest species and three minor) is so well established in the literature, and since dissection of genitalia or genomics is required for identification, there has been resistance to the name change (for example, Heath and Emmet, 1983), but Hardwick's work is generally accepted and so the name change must also be accepted (Matthews, 1991). Later genomic studies confirmed that H. armigera and H. zea are sister species (Cho et al., 1995; Behere et al., 2007). Accepted common names for H. zea are bollworm, corn earworm and tomato fruitworm.

Egg

Eggs are subspherical, radially ribbed (n = 11 to 17), 0.51 mm high and 0.57 mm in diameter, attached individually to the plant substrate, white to yellowish-green when laid, developing a reddish band and finally turning dark grey before hatching. Egg maturity takes 2-3 days at 20-30°C (Neunzig, 1964; Hardwick, 1965). Eggs are preferentially laid on hosts during the flowering period and on many different tissue types, but primarily on leaves (Hardwick, 1965; Neunzig, 1969; Braswell et al., 2019c).

Larva

On hatching, the tiny caterpillars are translucent or yellowish-white, with a black head, but appear grey or brown to the naked eye; they grow through six instars usually, but five and seven instars are not uncommon, and the final body size is approximately 40 mm long. In the third instar, different colour phases can develop. Often, longitudinal lines of white, cream or yellow are present, and the spiracular band is the most distinct. As the larvae develop, the pattern becomes better defined, but in the final instar (sixth) the colouration can change abruptly into a bright pattern with extra striations. However, larvae can be green, reddish, or pink, without most of the brown or black pigmentation. Larval colour is determined by the interaction of environment (light, temperature and developmental host) and genetics. Larvae have five pairs of prolegs (Neunzig, 1964; Hardwick, 1965; Neunzig, 1969).

Pupa

Pupae are light to dark brown depending on maturity and approximately 20 mm long, with two distinct terminal cremaster spines. Pupae reside in earthen cells, ranging from 0.5-25 cm below the soil surface (Barber, 1941; Eger et al., 1983), but most commonly around 3-5 cm (Roach and Hopkins, 1979; Stadelbacher and Martin, 1980; Eger et al., 1983).

Adult

A stout-bodied (20-25 mm long) brown moth of wingspan 38-43 mm; forewing pale brown-yellow to brown-pink (female) to greenish (male) with darker transverse markings, underwings pale with a broad dark marginal band.

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).

Fruiting structures are consumed or damaged and feeding damage can facilitate entry by diseases and other insect pests. In cotton the square (flower bud), flowers and young bolls are attacked and larvae excavate the interior. This can cause the reproductive tissue to abscise and, in severe cases, cause total yield loss for cotton growers (Pozo-Valdivia et al., 2021). Young shoots and leaves can also be damaged, especially in the absence of fruiting structures.

Young maize plants have serial holes in the leaves following whorl feeding on the apical leaf. On larger plants the silks are grazed and eggs can be found stuck to the silks. As the ears develop, the soft milky grains in the top few centimetres of the cobs are eaten; usually only one large larva per cob can be seen because the larvae are cannibalistic. Ear damage is often localized to the tip but can increase the incidence of disease.

Sorghum heads are grazed. Legume pods are holed and the seeds eaten. Bore holes can be seen in tomato fruits, cotton bolls, cabbage and lettuce hearts, soyabean pods and flower heads.

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).

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).

In North America, it is reported that H. zea is the second most important economic pest species (preceded by codling moth, Cydia pomonella) (Hardwick, 1965). Fitt (1989) quotes the estimated annual cost of damage by H. zea and H. virescens together on all crops in the USA as more than US$ 1000 million, despite the expenditure of US$ 250 million on insecticide application.

Reasons for the success and importance of this agricultural pest include its high fecundity, polyphagous larval feeding habits, high mobility of both larvae locally and adults with their facultative seasonal migration, and a facultative pupal diapause.

Damage is usually serious and costly because of the larval feeding preference for the reproductive structures and growing points rich in nitrogen (for example, maize cobs and tassels, sorghum heads, cotton bolls and buds, etc), and they have a direct influence on yield. Many of the crops attacked are of high value (cotton, maize, tomatoes). If this pest should become established in protected cultivation economic damage could be widespread.

Infestations of maize grown for silage or for grain are not of direct economic importance; losses are typically about 5% and no control measures are taken, but they serve as a focus, or reservoir of infestation. In many areas the first generation is not regarded as a pest (often on Trifolium) and it does not become an economic pest on cultivated crops until the second, third or even fourth generation.

In North America, H. zea has long been reported as a major economic pest. During the 1960s, it was noted as being the second most important economic pest species (preceded by codling moth, Cydia pomonella) (Hardwick, 1965). Fitt (1989) quoted the estimated annual cost of damage by H. zea and Heliothis virescens together on all crops in the USA as more than US$ 1000 million, despite the expenditure of US$ 250 million on insecticide application. During 2019, H. zea and H. virescens were estimated at nearly US$ 117 million in costs of control and direct losses in cotton (Cook and Threet, 2020), and over US$ 117 million in costs of control and direct losses in soyabean (Musser et al., 2020).

Reasons for the success and importance of this agricultural pest include its high fecundity, polyphagous larval feeding habits, high mobility of both larvae locally and adults with their facultative seasonal migration and a facultative pupal diapause (Fitt, 1989).

Damage is usually serious and costly because of the larval feeding preference for the reproductive structures and growing points rich in nitrogen (for example, sorghum heads, cotton bolls and buds, soyabean seeds, etc.), and they have a direct influence on yield. Many of the crops attacked are of high value (hemp, tobacco, tomatoes). If this pest should become established in protected cultivation economic damage could be widespread.

Infestations of maize grown for silage or for grain are not of direct economic importance, and no control measures are taken, but they serve as a focus, or reservoir of infestation. In many areas the first generation is not regarded as a pest (often on Trifolium) and it does not become an economic pest on cultivated crops until the second, third or even fourth generation.

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.