Insect Pests of Chickpea and Lentil Pod Borers: Helicoverpa armigera and Helicoverpa punctigera

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Insect Pests of Chickpea and Lentil

Pod Borers: Helicoverpa armigera and Helicoverpa punctigera
Nearly 60 insect species are known to feed on chickpea, of which the pod borers Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae) are the major pests. The former is a major pest of chickpea in Asia, Africa, and Australia, while the latter is confined to Australia. Helicoverpa-inflicted losses to chickpea crops in the semi-arid tropics are estimated at over US $328 million annually. Pod borers rarely become a serious pest on lentil. Worldwide, losses due to Heliothis/Helicoverpa in cotton, legumes, vegetables, cereals, etc., exceed $2 billion, and the cost of insecticides used to control these pests is over $1 billion annually. There are several common names for pod-borers, namely cotton bollworm, corn earworm, African cotton bollworm, native budworm, old world bollworm, legume pod borers, gram pod borer, and tomato fruit worm.
Geographic distribution

Helicoverpa armigera is widely distributed in Asia, Africa, Australia, and the Mediterranean Europe, while H. punctigera is restricted to southern regions of Australia. Additionally, there are reports of H. armigera outbreaks in Hungary, Italy, Romania, Slovakia, Spain, Sweden, Switzerland, and the United Kingdom.
Host range

Helicoverpa armigera and H. punctigera are major pests of cotton, pigeonpea, chickpea, sunflower, tomato, maize, sorghum, pearl millet, okra, Phaseolus spp., vegetables, tobacco, linseed, a number of fruits (Prunus, Citrus, etc.), and forest trees. In recent years, H. armigera damage has been reported in carnation, grapevine, apple, strawberries, finger millet, etc. Helicoverpa punctigera is a major pest of cotton, corn, sorghum, tomato, chickpea and other grain legumes.
Nature of damage

Helicoverpa females lay eggs singly on leaves, flowers, and young pods. The larvae initially feed on the foliage (young leaves) in chickpea and a few other legumes (Fig. 1), but mostly on flowers and flower buds in cotton, pigeonpea, etc. The young seedlings of chickpea 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 (Fig. 2). In Australia where the climate is cooler, the Helicoverpa populations build up in spring, attacking chickpea in late spring before moving on to summer crops growing in the sub-tropical regions.
Life cycle

The oviposition period lasts for 5 to 24 days, and a female may lay up to 3,000 eggs, mainly at night on leaves, flowers, and pods (Fig. 3). The egg incubation period depends on temperature, and varies between 2 to 5 days (usually 3 days). Duration of larval development depends not only on the temperature, but also on the nature and quality of the host plant, and varies between 15.2 days on maize to 23.8 days on tomato (Fig. 4). The number of larval instars varies from 5 to 7, with six being most common. The larvae pupate in the soil (Fig. 5). 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. The diapausing period for pupae may last several months. Pale colored adults are produced from pupae exposed to temperatures exceeding 30°C. In captivity, longevity varies from 1 to 23 days for males and 5 to 28 days for females (Fig. 6).

Helicoverpa armigera exhibits a facultative diapause, which enables it to survive adverse weather conditions in both winter and summer. The winter diapause is induced by exposure of the larvae to short photoperiods and low temperatures. In China and India, H. armigera populations are comprised of tropical, sub-tropical, and temperate ecotypes. In subtropical Australia, H. armigera undergoes diapause during winters when the 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 to that of males. At these temperatures, non-diapausing males are sterile. In Australia, H. punctigera has been observed to enter a diapause in spring when temperatures are quite high and plant hosts are scarce.

Economic thresholds. Monitoring of Helicoverpa populations is necessary to determine if threshold has been exceeded and control measures are required. Action thresholds based on egg numbers have been used to make control decisions. One larva per meter row in chickpea causes economic loss. A simple rule of thumb based on monsoon rains and November rainfall has been developed to forecast H. armigera populations in India. Models for long-range forecasts of H. armigera and H. punctigera populations in Australia have also been developed. These population-forecasting models may be incorporated into crop production models for pest management. In Australia, three crops, cotton, tomato and maize, have high levels of Helicoverpa attack and require multiple sprays of pesticides. Of the legume crops, field peas and chickpeas are spring flowering crops grown in the southern regions of Australia, and usually suffer sporadic damage from H. punctigera, requiring a single pesticide application only.
Host plant resistance. The development of crop cultivars resistant or tolerant to H. armigera and H. punctigera has considerable potential for use in integrated pest management, particularly under subsistence farming conditions in developing countries. Several chickpea germplasm accessions (ICC 506EB, ICC 10667, ICC 10619, ICC 4935, ICC 10243, ICCV 95992, and ICC 10817) with resistance to H. armigera have been identified, and varieties such as ICCV 7, ICCV 10, and ICCL 86103 with moderate levels of resistance have been released for cultivation (Fig. 1). However, most of these lines are highly susceptible to Fusarium wilt. Therefore, concerted efforts have been made to break the linkage by raising a large population of crosses between Helicoverpa- and wilt-resistant parents. Several wild relatives of chickpea have shown high levels of resistance to H. armigera, and efforts are underway to transfer resistance from the wild relatives into high yielding varieties of chickpea
Genetically modified crops. In recent years, genetic engineering has enabled the introgression of genes from distantly related organisms (i.e., Bacillus thuringiensis) into crops such as cotton, corn, pigeonpea, and chickpea. Chickpea cultivars ICCV 1 and ICCV 6 have been transformed with cry IAc gene. Insect feeding assays indicated that the expression level of the cry IAc gene was inhibitory to the development and feeding by H. armigera. Efforts are underway at ICRISAT to develop transgenic chickpeas for resistance to pod borer. A resistance management strategy has been developed for transgenic cotton growing in Australia to prevent undesirable side effects, including the development of resistance to Bt, which will also be applicable to chickpea in case transgenic chickpeas are released for cultivation.
Cultural manipulation of the crop and its environment. A number of cultural practices such as time of sowing, spacing, fertilizer application, deep ploughing, interculture, and flooding have been reported to reduce the survival and damage by Helicoverpa species. Inter-cropping or strip-cropping with marigold, sunflower, linseed, mustard, or coriander can minimize the extent of damage to the main crop. Strip-cropping also increases the efficiency of chemical control. Hand-picking of large larvae can reduce Helicoverpa damage. However, the adoption of cultural practices depends on the crop husbandry practices in a particular agro-ecosystem. An area-wide management strategy has been implemented in regions of Queensland and New South Wales, Australia, to suppress local population densities of H. armigera, with chickpea trap crops playing an important role in this strategy. The chickpea trap crop is planted after the commercial crops to attract H. armigera emerging from winter diapause. The trap crops are destroyed before larvae commence pupation. As a result, the overall H. armigera pressure on summer crops is reduced, resulting in greater opportunity for adoption of soft control options, reduced insecticide use, and greater activity of the natural enemies.
Natural enemies. The importance of biotic and abiotic factors on the seasonal abundance of H. armigera and H. punctigera is poorly understood. Some parasitic wasps avoid chickpea due to dense layers of trichomes and their acidic exudates. Trichogramma egg parasitoids are seldom present in high numbers in chickpea crops in India. The ichneumonid wasp, Campoletis chlorideae is an important larval parasitoid of H. armigera on chickpea in India. The dipteran parasitoids Carcelia illota, Goniophthalmus halli, and Palexorista laxa have been reported to parasitize up to 54% of the larvae on chickpea. Predators such as Chrysopa spp., Chrysoperla spp., Nabis spp., Geocoris spp., Orius spp., and Polistes spp. are common in India. Provision of bird perches or planting of tall crops that serve as resting sites for insectivorous birds such as Myna (Acridotheris tritis) and Drongo (Dicrurus macrocercus) helps to reduce the numbers of H. armigera larvae.
Biopesticides and natural plant products. The use of microbial pathogens such as H. armigera nuclear polyhedrosis virus (HaNPV), entomopathogenic fungi, Bacillus thuringiensis (Bt), nematodes, and natural plant products such as neem, custard apple, and karanj (Pongamia pinnata) kernel extracts have shown some potential to control H. armigera. HaNPV has been reported to be a viable option to control H. armigera in chickpea in India. Jaggery (locally made brown sugar from sugarcane juice) (0.5%), sucrose (0.5%), egg white (3%), and chickpea flour (1%) increase the activity of HaNPV. In Australia, the efficacy of HaNPV in chickpea has been increased by the addition of milk powder, and more recently the additive Aminofeed® (Farma-Chem, Australia). The entomopathogenic fungus Nomuraea rileyi (106 spores per ml) resulted in 90 to 100% mortality of the larvae. Another entomopathogenic fungus, Beauveria bassiana (2.68 x 107 spores per ml) resulted in 10% reduction in damage by H. armigera over the control plants. Bt formulations are also used as sprays to control Helicoverpa. Spraying Bt formulations in the evening results in better control than spraying at other times of the day.
Chemical control. Management of Helicoverpa in India and Australia in chickpea and other high-value crops relies heavily on insecticides. There is substantial literature on the comparative efficacy of different insecticides against Helicoverpa. Endosulfan, cypermethrin, fenvalerate, methomyl, thiodicarb, profenophos, spinosad, and indoxacarb have been found to be effective for controlling H. armigera. Spray initiation at 50% flowering has been found to be most effective. Development of resistance to insecticides is a major problem in H. armigera, but not in H. punctigera because of its high mobility. Helicoverpa armigera populations in several regions have developed resistance to pyrethroids, carbamates, and organophosphates. Introduction of new compounds such as thiodicarb, indoxacarb, and spinosad has helped in overcoming development of resistance in H. armigera to conventional insecticides.
Integrated pest management (IPM). Several management tactics have been investigated, which provide a framework for improved management of pod borers in chickpea and lentil cropping systems worldwide. For example, crop cultivars with resistance to Helicoverpa (derived through conventional plant breeding or biotechnological approaches) can play an important role. Cultural practices such as deep ploughing, interculture, flooding, and intercropping could potentially reduce the intensity of Helicoverpa. Although the role of natural enemies as biological control agents is unclear, their impact could be improved by reducing pesticide applications, and adopting cropping practices that encourage their activity. Most studies have shown that insecticide applications are more effective than neem kernel extracts, Bt, HaNPV, or augmentative releases of natural enemies. However, biopesticides and synthetic insecticides, applied alone, together, or in rotation, are effective for Helicoverpa control in chickpea. Moreover, scouting for eggs and young larvae is critical for initiating timely control measures. Insecticides with ovicidal action, and/or systemic action are effective against Helicoverpa during the flowering stage. Finally, the development of transgenic plants with different insecticidal genes, molecular marker assisted selection, and exploitation of the wild relatives of Cicer and Lens species should be pursued to develop comprehensive programs for Helicoverpa management on chickpeas and lentils.
Selected References

Commonwealth Agricultural Bureau International (CABI). 1993. Distribution Maps of Plant Pests, No. 15. Commonwealth Agricultural Bureau International, Wallingford, UK.

Fitt, G. P. 1989. The ecology of Heliothis species in relation to agro-ecosystems. Annu. Rev. Entomol. 34:17-52.

Fitt, G. P., and Cotter, S. C. 2005. The Helicoverpa problem in Australia: Biology and Management. In: Heliothis/Helicoverpa Management: Emerging Trends and Strategies for Future Research (Sharma, H.C., ed.). Oxford and IBH Publishing, New Delhi, India. pp. 45-61.

King, A. B. S. 1994. Heliothis/Helicoverpa (Lepidoptera: Noctuidae). In: Insect Pests of Cotton (Matthews, G.A., and Tunstall, J.P., eds.). CAB International, Wallingford, UK. pp. 39-106.

Maelzer, D.A., and Zalucki, M.P. 2000. Long range forecasts of the numbers of Helicoverpa punctigera and H. armigera (Lepidoptera: Noctuidae) in Australia using the Southern Oscillation Index and the sea surface temperature. Bull. Entomol. Res. 90:133-146.

Matthews, M. 1999. Heliothine Moths of Australia. A Guide to Pest Bollworms and Related Noctuid Groups. Monograph on Australian Lepidoptera, Volume 7. CSIRO Publishing, P O Box 1139, 150 Oxford Street, Callingford, Victoria, 3066, Australia, 320 pp.

Romeis, J., and Shanower, T.G. 1996. Arthropod natural enemies of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in India. Biocontr. Sci. Tech. 6:481-508.

Sharma, H. C. (ed.). 2005. Heliothis/Helicoverpa Management: Emerging Trends and Strategies for Future Research. Oxford and IBH Publishers, New Delhi, India, 469 pp.

(Prepared by H. C. Sharma, T. J .Ridsdill-Smith and S. L. Clement)

Fig. 1. Leaf damage by Helicoverpa armigera in chickpea (Left – Resistant line ICC 506EB, and Right - Susceptible line ICC 3137). (Courtesy ICRISAT)

Fig. 2. Pod damage by Helicoverpa armigera. (Courtesy ICRISAT)

Fig. 3. Eggs of Helicoverpa armigera on chickpea. (Courtesy ICRISAT)

Fig. 4. A) Larva of Helicoverpa armigera (Photo: ICRISAT), and B) H. punctigera. (Courtesy Richard Lloyd)

Fig. 5. Pupa of Helicoverpa armigera. (Courtesy ICRISAT)

Fig. 6. Adult of Helicoverpa armigera. (Courtesy ICRISAT)

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