The cotton bollworm (Helicoverpa armigera) and Azuki bean beetle (Callosobruchus chinensis): major chickpea (Cicer arietinum L.) production challenges on smallholder farmers in Ethiopia

Abstract

Background

Chickpea (Cicer arietinum L.) is one of the most principally important legume crops in Ethiopia. Its production is mainly constrained by insect pests. Dissemination of updated information on its status and addressing alternative management options are important.

Main body

This article reviews the research status of the cotton bollworm (Helicoverpa armigera) and Azuki bean beetle (Callosobruchus chinensis) in chickpea, focusing on their distributions, host range, nature of the damage, biology, and their management practices. Helicoverpa armigera under field conditions and C. chinensis during storage are the most challenging insect pests of chickpea production in Ethiopia.

Conclusion

Managements of these two major insect pests are achieved through the use of cultural control, host plant resistance, botanical control, biological control, and chemical insecticides. Future research should focus on low-input IPM approaches that encompass all locally available and use of affordable insect pest management methods in Ethiopia.

Background

Chickpea (Cicer arietinum L.) is the most important grain legume in the world after common bean (Phaseolus vulgaris L.) and pea (Pisum sativum L.) (FAOSTAT, 2019). The seeds are a nutritious and rich source of cheap protein for the rapidly increasing population (Tejera et al., 2006). It has a dual purpose as human food and animal feeds, and also improves soil fertility through fixing the atmospheric nitrogen (Fikre et al., 2020; Werner, 2005). The crop is adapted to black soils in the cool semi-arid areas of the tropics, sub-tropics as well as temperate areas (Menale et al., 2009). It is grown all over the world in about 57 countries under varied environmental conditions including the Mediterranean basin, the Near East, Central, and South Asia, East Africa, South America, North America, and, more recently, in Australia. About 95% of chickpea cultivation and consumption is in developing countries and it contributes to around 46% of the total production of chickpea in Africa (Menale et al., 2009). African leading producers are Ethiopia, Tanzania, and Kenya (Mulwa et al., 2010; David, 2016; Mohamed et al., 2015). It ranks third in area coverage among pulses grown in Ethiopia that is preceded only by faba beans and haricot beans, generating revenue for the country and diversifying the cropping system (Fikre et al., 2020). Ethiopia is the largest producer, consumer, and exporter of chickpea in Africa and shares 4.5% of the global chickpea market and more than 60% of Africa’s chickpea market (Tebkew & Ojiewo, 2017). Furthermore, the crop was among the major export commodities (Bejiga & Daba, 2006; Shiferaw & Teklewolde, 2007). In Ethiopia, it is widely grown across the highlands and semi-arid regions of the country (Bejiga et al., 1996; Dadi et al., 2005). The largest growing regions in Ethiopia are Oromiya and Amhara regions (Tebkew & Ojiewo, 2017). The national average yield of chickpea in Ethiopia is 1913 kg/ha which remains below the potential of the crop (Keneni et al., 2011). Furthermore, disproportionally, the potential of the crop under improved management condition is more than 3 tons per hectare (Dadi et al., 2005) and also it’s below the world chickpea production average 5 tones/ha. In Ethiopia, chickpea production was limited due to both biotic and abiotic factors. Biotic factors such as diseases; root diseases (fusarium wilt, collar rot, and dry root rot), and foliar diseases (Ascochyta blight, Botrytis grey mold) (Tadesse et al., 2017; Getaneh et al., 2021), and insect pests mainly Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) and Callosobruchus chinensis (L.) (Coleoptera: Bruchidae) (Damte & Mitiku, 2021; Fite et al., 2018). The later two insect pests were among the major factors affecting chickpea production in Ethiopia (Damte & Mitiku, 2020; Fite et al., 2019). Helicoverpa armigera causes up to 33% pod damage at field (Tebkew, 2004) and C. chinensis can causes up to 50% weight losses in Ethiopia (Tebkew & Mohamed, 2006). Due to the scarcity of comprehensive published information on H. armigera and C. chinensis in chickpea and their management practices at the African level, we focused more on an Ethiopian level, since the country is one of the top African chickpea producers and consumers. In Ethiopia, H. armigera and C. chinensis are the most major insect pests of chickpea at field and storage conditions, respectively. Hence, the objective of this article is to review H. armigera and C. chinensis and their management practices in chickpea.

Cotton bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae)

Distribution and extent of damage

Helicoverpa armigera is a cosmopolitan pest of high mobility, and migratory potential (Forrester et al., 1993; Wakil et al., 2010). Helicoverpa armigera was considered the most prevalent insect pest of chickpea in Ethiopia (Fite et al., 2019; Mihretie et al., 2020) and throughout Africa, Europe, Australia, the Middle East, New Zealands, and the Pacific Islands (Sharma, 2005). It was also the most prevalent in the field on chickpea in Kenya (Kimurto et al., 2004), Tanzania (Maerere et al., 2010) and Sudan (Mansour & Mohmoud, 2014) from early seedling to maturity. Helicoverpa armigera was detected in all chickpea and other host-growing areas in Ethiopia.

The immature stages (1st, 2nd, and 3rd instar larvae) initially feed on the young shoot leaves of chickpeas. Occasionally, they enter the pod and feed upon the developing grains, and shift to developing seeds and fruits as larval instar development progresses (Reed & Pawar, 1982). The extent of pod damage on chickpea by this insect pest was found to vary with altitude; indicating that the insect was more important in mid-altitude areas than with low or high altitude chickpea growing zones (Tebkew, 2004). In chickpea, it causes up to 33% pod damage in Ethiopia (Tebkew, 2004) and 70–95% in India (Prakash et al., 2007).

Biology and seasonal abundance of H. armigera

The eggs of H. armigera were laid singly during nighttime due to the moths’ nocturnal behaviour. Freshly laid eggs are yellowish-white and glistering at first, later changed to dark brown before hatching (Ali et al., 2009). The larvae emerge after 3.37 ± 0.09 days of egg incubation. The first and second larval instars are yellowish-white to reddish-brown to blackhead capsules (Ali et al., 2009). Whereas, fully grown larvae are straw-yellow to green, pink, or light brown to reddish-brown with lateral brown strips, and the head, as well as prothoracic legs, are dark brown to black (Cunningham et al., 1999; Zalucki et al., 1994). Pupae are the obtect type with mahogany-brown colour up to 19 mm in length, smooth and rounded both anteriorly and posteriorly. They took about 10–14 days before becoming adults emerging of the adult moth depending upon the temperature (Ali et al., 2009; Nasreen & Mustafa, 2000). According to Fite et al. (2020a, 2020b), the activity of H. armigera reached the first peak being June and February the second highest peak via funnel-botrack pheromone trap at Dandi district in Ethiopia. Two population peaks were recorded in Ethiopia (Fite et al., 2020a, 2020b; Seid & Tebkew, 2002). In Egypt, up to four population peaks were reported in cotton using light traps (Al-mezayyen & Ragab, 2014).

Host plants and nature of damage

Helicoverpa armigera is a polyphagous and voracious feeder of diverse plant species. Over 200 plant species including economically important crops such as; cotton (Gossypium hirsutum), sorghum (Sorghum bicolor), pigeonpea [Cajanus cajan (L.) Millspaugh], chickpea (C. arietinum), maize (Zea mays), soybean (Glycine max), tomato (Lycopersicum esculentum), pepper (Capsicum annum), bean (Vicia faba), peas (Pisum sativum), sunflower (Helianthus annus), niger (Guizotia abyssinica) seeds and many other horticultural crops were preferred by H. armigera (Fite et al., 2018; Tebkew, 2004; Waktole, 1996). The extent of damage depends on the type of host plants they fed upon. In chickpea, the eggs are laid on leaves and young pods. The larvae initially feed on the young leaves and the larger larvae bore into the pods and consume the developing seeds inside the pods. The insect destroys various plant parts like the pods, buds, flowers, and fruits of its host plants preferring, the harvestable part of economically important crops throughout the world (Sarwar, 2013).

Management strategies for H. armigera

Cultural control

Across Africa different cultural pest management have been employed for H. armigera. The use of manures, sowing dates, and plant density was also considered as a management part of H. armigera in Ethiopia (AdARC, 2002). Higher (3.3%) chickpea (Worku variety) pod damage was recorded at a plant density of 600/4.5m² indicating that increasing plant density will result in maximum pod damage, by favouring a higher H. armigera larval population. Early planted chickpea had a relatively greater number of larvae per plant than those sown late (DZARC, 1997). In other studies, early and late sown crops received higher H. armiger pod damage than mid sown chickpea (Hossain et al., 2008). Sanitation control measures like removing grass spp. from the nearby agricultural farms since cutworm prefers to live in moist and crack soils are the most important management part and considered as the cheapest of all methods (Tekeba, 2005).

Host plant resistance (HPR)

Host plant resistance presents an ideal means of combating notorious insect pests including H. armigera (Golla et al., 2018; Xiaoyi et al., 2015). Research has been conducted by East African scientists on screening chickpea genotypes for resistance and tolerance to H. armigera (Mansour & Mohmoud, 2014; Mulwa et al., 2010). There is evidence of HPR among chickpea genotypes in Ethiopia that showed some level of resistance to H. armigera under open field conditions. From a total of 78 chickpea genotype tested under field condition, genotypes such as; ICCL-981/83-DZ/2-1, ICCL-7958/83-DZ/1-1, ICC-7881/82-DZ/4, and ICC-84204 and the improved variety Marye suffered only 1% pod damage, whereas, 22.02% from ILC-2876 chickpea genotype (AdARC, 2002). Several germplasm accessions (ICC 2580, ICC 7272, ICCV 92311, ICC 3362, ICCV 95311, ICC 506, EC 583311, and ICCVX 906183-1) (Mulwa et al., 2010) and EC58318, ICCV10, ICC14831, EC583260, EC583264, and EC583250 (Ruttoh et al., 2013) with tolerance to H. armigera have been identified in Kenya. In Sudan, genotypes Atmore and Flip03-139c recorded a higher level of resistance against H. armigera than the Mattama, Hawata, Selwa, Wad Hamed, Jebel Marra, Flip03-127c and Flip04-9c genotypes, which showed moderate resistance to H. armiger (Mansour & Mohmoud, 2014). Farmers believe that use of local landrace chickpea varieties; mainly Desi type chickpea varieties are more moderately resistant to H. armigera than the Kabuli types (Fite et al., 2019). Genotypes resistant to H. armigera accumulated more oxalic acid (in leaf exudate as an antibiotic factor) on the leaves and growth inhibition on H. armigera larvae when included in a semi-artificial diet (Mitsuru et al., 1995). Although a promising level of HPR to H. armigera has been found, the mechanism of resistance has not been adequately addressed on chickpea.

Biological control of H. armigera

Biological control by natural enemies and microbes are an important component of IPM programs against plant pests (Barratt et al., 2018; Van Lenteren et al., 2018) including H. armigera (Seid & Tebkew, 2002; Crowder et al., 2010; Fite et al., 2020a, 2020b).

Parasitoids and predators

Natural enemies, mainly the parasitoids, play a crucial role in the population regulation of H. armigera. More than 176 parasitoid species have been reported on H. armigera associated with different host plants in Africa so far (Van den Berg, 1993). In the cotton field, some egg parasitoids were recorded in Ethiopia such as; Trichogramma spp. and Telenomus spp. (IAR, 1985). Several egg and larval parasitoids H. armigera have been reported from Ethiopia (Table 1). For instance, about 12% of the H. armigera eggs were found parasitized by egg parasitoids (Trichogrammatidae, Trichogramma spp. and Scelionidae, Telenomus spp.) (Alemayehu et al., 2002) in Ethiopia. Similarly, egg parasitism by native Trichogrammatids on chickpea was reported by Gangaraddi (1987), who found 4% of H. armigera eggs parasitized by Trichogramma achaeae Nagaraja and Nagarkatti in India. Previously, larval and egg parasitoids such as; Tachinids, Ichneumonid wasps (Charops sp.), and egg parasitoids (Trichogramma sp.) have been described on H. armigera in Ethiopia (Seid & Tebkew, 2002). More recently, Fite et al. (2021) identified four tachinids; Drino sp. (Fig. 1A), Goniophthalmus halli (Fig. 1B), Linnaemya cf. longirostris (Fig. 1C), Pimelimyia sp. (Fig. 1D), and one ichneumonid (Fig. 1E) species; Charops sp. as larval parasitoids of H. armigera in chickpea from Ethiopia (Table 1). Drino sp. was the most predominant and common larval parasitoid species found in most of the surveyed districts with a parasitism rate ranging from 5.9% in Aqaqi to 13% in Tokke Kutaye districts (Fite et al., 2021). Ichneumonid wasps were recorded causing 5–10% larval mortality to H. armigera at Wello, Northern Ethiopia (Seid & Tebkew, 2002). Similarly, in cotton, Charops sp. was also detected in striga (Milner, 1967) in Tanzania. Nyambo (1990) recorded Charops sp. from H. armigera larvae collected from tomato, cleome, and chickpeas. Predators such as; bugs, ladybird beetles, and some spiders (EARO, 2000) and the wasp (Tiphia sp.) have been recorded in Ethiopia as a predatory on H. armigera larvae (Abate, 1991).

Table 1 Natural enemies of H. armigera in Ethiopia

Fig. 1

Larval parasitoid of H. armigera (Sources: Fite et al., 2019)

Microbial pesticides

Some of the microbes effective for the control of H. armigera larvae have included bacteria; Bacillus thuringiensis (Bt.) (Das et al., 2016), viruses; nuclear polyhedrosis virus (NPV) (Gómez Valderrama et al., 2018), and entomopathogenic fungi (Fite et al., 2019). Bacillus thuringiensis is available as a selective spray that only kills moth larvae and the pathogen is extensively studied on various caterpillars including H. armigera larvae (Das et al., 2016; Silva et al., 2018; Fite et al., 2019). Bacillus thuringiensis Berliner variety kurstaki were effective at the rate of 1.50 kg/ha was successfully controlled the first and second instar larvae of H. armigera up to an average of 99.58 and 90.42%, respectively (Alemayehu et al., 1993). Bacillus thuringiensis can also induce sublethal effects on the growth and reproduction of H. armigera (Fite et al., 2019). Helicoverpa armigera larvae were reported to be extremely prone to Bt δ-endotoxins (Avilla et al., 2005; Li & Bouwer, 2012). Entomopathogenic fungi/EPF; mainly strains of B. bassiana and M. anisopliae have been reported to be effective against H. armigera (Jarrahi & Safavi, 2016; Kalvnadi et al., 2018). These two EPFs are the most widely used and known for causing adverse effects on the biological parameters of H. armigera (Jarrahi & Safavi, 2016). Recently, Fite et al. (2019) tested native B. bassiana and M. anisopliae against larvae of H. armigera and found B. bassiana (Isolate; APPRC-9604) was very effective in causing high larval mortality and reduced pod damage under field conditions in Ethiopia. Similarly, Bajya et al. (2015) had reported, B. bassiana was highly effective in controlling H. armigera populations in chickpea after two sprays under field conditions.

Population monitoring

Pheromone traps are described as a good tool to monitor lepidopterous pests (Malik & Ali, 2002). Monitoring of H. armigera by using pheromone traps or light traps was successfully implemented and incorporated as basic tools used to monitor, forecast, prediction, and control decisions based upon the populations of the moth catch (Fite et al., 2020a, 2020b; Kemal & Tibebu, 1994; Yenumula & Prabhakar, 2012). Kemal and Tibebu (1994) reported that the seasonal activity, abundance, and the damages inflicted by H. armigera to pulse crops are greatly differing from place to place in Ethiopia. Using pheromone and light traps he found that the number of moth catch was low from January to April and the increment of the catch from the first week of May reaching the peak in June and July when the wind speeds were 1.94 m/s with high temperature. Fite et al. (2020a, 2020b) evaluated commercial traps and lures and found that funnel trap with botrack was most effective in couching H. armigera moths and specific at the agro-ecological area of Dandi district, Oromiya, Ethiopia during 2018/2019. Two population peaks of H. armigera were reported under the agro-ecology of Dandi district, Oromiya, Ethiopia (Fite et al., 2020a, 2020b). The economic threshold for chickpea is to treat if more than 5 moths/trap/night are capture (Reena et al., 2009).

Botanical pesticides

Botanical pesticides are now emerging as a promising insect pest management strategy on all crops due to their safety to natural enemies, the environment, and humans, and being cost-effective compared to synthetic pesticides (Junhirun et al., 2018; Begg et al., 2017; Fite et al., 2020a, 2020b). Azadirachta indica A. Juss and Milletia ferruginea have been used as a component of IPM (Habeeb, 2010; Hussain et al., 2015; Mulatu, 2007). Aqueous extracts of A. indica and M. ferruginea seed-powder at 5% concentration highly reduced larval infestations and pod damage due to H. armigera under field conditions in Ethiopia (Fite et al., 2020a, 2020b). Besides, direct larval mortality; aqueous extracts of A. indica and M. ferruginea, and 50% oil extracts of A. indica have deterrent effects against H. armigera egg lying under laboratory conditions (Fite et al., 2018). The extracts of A. indica from different parts also influenced negatively both the survival and feeding of the larvae of H. armigera under laboratory experiments (Mesfin et al., 2012). Still, exploitation of other native botanical pesticides and their active ingredients and mode of actions remained in most cases.

Synthetic chemicals

The indiscriminate and misuse of synthetic insecticides can lead to environmental pollution, health hazards to humans and other animals, resistance development, disruption of non-target insects, pest resurgence, and many other side effects (Aboua et al., 2010; Mollaei et al., 2011). However, in the IPM system, chemical pest management is considered as the last resort that should be a need-based schedule application. Synthetic insecticides such as endosulfan, profenofos and lambdacyhalothrin have been frequently used for the control of H. armigera in the cotton field (Geremew & Surachate, 2005). Under field trials, a single application of cypermethrin 20% (Ripcord 20%) or cypermethrin 25% (Cymbush 25%) at peak flowering of chickpea gave the least pod damage due to H. armigera (DZARC, 1997). Similarly, a single application of cypermethrin or endosulfan at peak flowering of chickpea was found effective in controlling H. armigera and reduced pod damage compared to the applications at peak flowering and mid-pod setting stages (Kemal & Tibebu, 1994). Conventional broad-spectrum insecticide products are not compatible with IPM programs, such as advanced generation pyrethroids and organophosphates (Deshmukh et al., 2010; DZARC, 1997; Kemal & Tibebu, 1994) have been used against H. armigera.

Insecticide resistance and integrated management for H. armigera

The indiscriminate use of synthetic insecticides has led to several adverse effects including resistance developments in H. argimera. Hence, due to its economic importance, insecticides are frequently used for the controlling of H. argimera which has been developed resistance to several conventional insecticides from the organophosphate, pyrethroid, and carbamate groups. Moreover, these insecticides are harmful to beneficial insects, thus it has become important to use insecticides that are ecologically safe for natural enemies. For instance, chemical group of insecticides such as spinosad (chemical group: Spinosyn) and indoxacarb is safe to the natural enemies (Nasreen et al., 2003; Williams et al., 2003). Spinosad was reported to be very effective against the larvae of H. argimera both on contact and by ingestion (Carneiro et al., 2014; Hamed & Khan, 2003). Recently, the application of Indoxacarb (Avaunt 150 SC) at 0.3 Lha⁻¹ or Spinosad (Tracer 480 SC) at 0.15 Lha⁻¹ three times with a week interval were reported to be effective in reducing the percentage of pod damage, mean larvae per plant and as a result increased grain yield ha⁻¹ under field condition and can be advised for the management of H.armigera (Mihretie et al., 2020). However, still investigations for very soft and effective chemical group of insecticides are remained as research outlook. Therefore, these insecticides can be used in the Integrated Pest Management (IPM) program for the control of H. armigera. Nowadays, IPM is being used to find ecologically sound, economically viable, and environmentally safe ways of pest management and received better attention. Single pest management could not provide sustainable and effective control; therefore all the available options have to be incorporated together whenever they are compatible. For instance, by integrating neem, Helicoverpa Nuclear Polyhedrosis Virus (HaNPV) and endosulfan resulted in reducing damaged pods, achieved the highest grain yield in chickpea (Visalakshmi et al., 2005). In another study conducted by Kumari et al. (2015) a combination of pheromone trap, Bt and HaNPV were significantly reduced damaged pods. Further, research should focus on IPM of all major pests emphasizing economically important crops.

Adzuki bean beetle, Callosobruchus chinensis (L.), (Coleoptera: Chysomelidae (formerly Bruchidae))

Distribution and extent of damage

Callosobruchus chinensis is considered the most important cosmopolitan species of storage insects in many food legumes (Tsedeke & Orr, 2012) including chickpea in Ethiopia (Tebkew & Mohamed, 2006; Keneni et al., 2011). This insect was native to East Asia, where its major natural hosts are Phaseoleae (Tuda et al., 2004, 2005). It is a major storage insect pest of cultivated pulses mainly in low and mid-altitude (1500–2200 m a.s.l.) areas of Ethiopia (Tebkew & Mohamed, 2006). The insect causes significant quantitative and qualitative damage and loss to chickpea in Ethiopia (Damte & Mitiku, 2020; Kemal & Tibebu, 1994). Infests legumes in the field and damage stored chickpea that can cause up to 50% weight losses in Ethiopia (Tebkew & Mohamed, 2006) and 28% in Eritrea (Adugna, 2006). As for the storage of insect pests of chickpea in Ethiopia, it is a key challenge for farmers due to the absence of well-equipped storage technologies. Therefore, future research interventions should have to focus on postharvest storage technologies.

Biology of C. chinensis

The eggs of C. chinensis are laid on chickpea seeds and the larvae and pupae complete their development inside the grain. After hatching, the larvae bore into cotyledons where it develops into adults within a month then immediately they begin mating and oviposition (Yanagi et al., 2013). A single female may lay 100 eggs depending on the environmental condition (Gwinner et al., 1996). For instance, under Ethiopian conditions a single female lays an average of 65 eggs in her lifetime and a generation is completed in about 25 days under optimum conditions (Damte et al., 2018).

Host plants and nature of damage

Callosobruchus chinensis is one of the major, polyphogous pulse beetles, causing a considerable loss to grain legumes in storage. The larvae of C. chinensis are a major pest of stored of chickpeas and cowpeas (Vigna unguiculata L.) (Pandey & Singh, 1997), soybean (Glycine max L. Merrill; Wang et al., 2010), kidney bean (Phaseolus vulgaris L.; Li & Zhu, 2009), pigeonpea (Cajanus cajan (L.) Millspaugh; Nahdy et al., 1998), peanut (Arachis hypogaea L.; Li & Zhu, 2009), lentils (Lens cultinaris Medik; Srinivasacharyulu & Yadav, 1997), adzuki bean (Vigna angular Ohwi & Ohashi; Tomooka et al., 2000), cowpea (Vigna unguiculata L.; Tomooka et al., 2000), faba bean (Vicia faba L.; Podoler & Applebaltm, 1968) and field pea (Pisum sativum L.; Bhagwat et al., 1995) across various geographical regions. In addition to the actual losses inflicted, the grain loses its germinating capacity (Ahmed & Din, 2009; Kumar et al., 2009) and nutritional quality (Sharma et al., 2007) once attacked by the beetles. It is the larvae that feed and damage the seeds. The damage and yield loss caused by C. chinensis depend upon the condition of the environments, for instance, the higher temperature and relative humidity that is conducive for the growth and development of pests (Singh, 2002). The adult and grub C. chinensis feed by making a small hole on chickpea seeds.

Management strategies for C. chinensis

Cultural control

Currently, various management options have been employed under smallholder conditions to reduce the damage caused by C. chinensis. To protect stored grains from insect pests farmers in Ethiopia uses; periodic winnowing, proper sun-drying before storage and at intervals, mixing plant materials with stored grains, mixing with inert materials (wood ash and sand), and mixing small grains with larger grains (Boxall, 1998), for instance admixing grain with teff (Eragrostis teff) are some of the most important cultural practices in IPM (Adugna, 2015; Damte & Mitiku, 2021). However, recently, the effectiveness of mixing chickpea with teff against C. chinensis was questionable (Damte & Mitiku, 2021).

Host plant resistance (HPR)

Breeding of productive genotypes with better genetic resistance to storage insect pests could be one of the stable alternatives to address problems of both developed and developing countries (Tebkew & Mohamed, 2006). The importance of host genetic improvement for resistance in chickpea for storage insect pests was also highlighted (Eker et al., 2018; Keneni et al., 2011; Swamy et al., 2020). Recently, it was evident that high protein and low starch content in maize seed were related to the resistance of maize to maize weevil (Sitophilus zeamais (Motschulsky) (Egas et al., 2017). Likely, some chickpea accessions such as Acc. Nos. 41320, 41289, 41291, 41134, 41315, 207658, 41103, 41168, 41142, 41174, 41029, 41207, 209087, 231327, 41161 and 41008 were found to have relatively better levels of resistance to C. chinensis in Ethiopia (Keneni et al., 2011). Suggesting that, resistant varieties can be used as gene sources in breeding new cultivars resistant to C. chinensis.

Biological control of C. chinensis

Natural enemies

Mainly two of the parasitoids; Anisopteromalus calandrae Howard and Dinarmus basalis Rondani (both Hymenoptera: Pteromalidae) were the major natural enemies of C. chinensis found in chickpea–teff mixture and together they caused up to 98% larval parasitism in grains of Arerti (kabuli type) and 56% in Natoli (desi type) (Damte & Mitiku, 2021). Both A. calandrae and D. basalis are dominant and cosmopolitan larval and pupal parasitoids of C. chinensis that develop concealed within the host substrate (Ghimire & Phillips, 2007; Niedermayer et al., 2016). These two parasitoids were recently reported from Ethiopia, and detailed research remained for the future. Moreover, A. calandrae and Lariophagus distinguendus (Hymenoptera: Pteromalidae) were reported to be effective at reducing the C. chinensis larval population, causing above 90% mortality rates in controlled conditions (28 ± 2 °C, 75 ± 5% relative humidity [RH]) (Iturralde-García et al., 2020). Therefore, these parasitoids can be used as effective biological control agents for the management of C. chinensis in stored chickpea as an alternative to the applications of liquid and gaseous insecticides.

Botanical pesticides

Botanical pesticides have been used as grain protectants (Park et al., 2016). Combination of ash (at 1:1 ratio, chickpea seeds to ash), insecticide (malathox 1% at 15 ppm), and oil (sesame oil at 10 mL kg⁻¹) were found effective in controlling C. chinensis for up to two months without severing grain damage to chickpea seeds (Adugna, 2015). Botanicals proved as a promising, locally available, socially acceptable, environmentally-friendly, and effective for the management of C. chinensis in chickpea and can be used as a component of IPM (Alemayehu & Getu, 2015). Mustard oil at 10 ml oil/kg of chickpea seed as a protectant was effective for up to five months against C. chinensis (Feeroza et al., 2008); botanicals such as M. ferruginea, Datura stamonium, A. indica, and Chenopodium ambrosioides, inert materials (wood ash and sand) and edible seed oils (Brassica juncea, Linum usitatissimum and Guizotia abyssinica) were very effective in controlling C. chinensis in stored chickpea grains (Tabu et al., 2012). Seed powder of A. indica at the rate of 20 g kg⁻¹ (Tebikew & Mekasha, 2002), at 2–3% w/w (Teshome, 1990) caused high mortality, and M. ferruginea at 5% w/w and fermented tobacco provided gave complete protection of chickpea for a long period (Tebikew & Mekasha, 2002). Noug (Guizotia abyssinica) oil was also reported as effective as primiphosmethyl (Alemayehu & Getu, 2015). Seed powder of A. indica at the rate of 20 g kg⁻¹ caused high adult mortality next to Malathion 5% dust at the rate of 0.5 g kg⁻¹ (Tebikew & Mekasha, 2002). As previously known, environmental conditions favour insect pest population development throughout the year in stored products such as maize, thus the stored product must be monitored regularly and appropriate interventions implemented to avoid product loss (Danso et al., 2018) which is vital for time-based insecticide application if so required. Recently, an improved storage technology; the hermetic triple-bagging technology called PICS (Purdue Improved Crop Storage) (Baoua et al., 2015; Murdock & Baoua, 2014) was introduced to Ethiopia, but with slow dissemination due to lack of a straight ward extension system to millions of farmers. PICS bags were very effective in protecting cowpea grain against bruchids (Ibrahim et al., 2018).

Synthetic chemicals

Stored product insect control mainly depended on the application of liquid and gaseous insecticides (White & Leesch, 1995). Worldwide, malathion and fumigation with methyl bromide (Subramanyam & Hangstrum, 1995) and Actellic 2% dust (Pirimiphos-methyl) (Adenekan et al., 2013) have been used for stored products as effective in controlling storage pests in various crops including pulses. The insecticide Pirimiphos-methyl at the rate of 4–5 ppm gives effective control of bruchids on stored bean grains (Abate, 1985). However, the insecticidal residuals remained on the treated crops may cause adverse side-effects on the human health and other beneficial organisms. Therefore, developing very simple, attractive, cost effective/cheap, sustainable, socially, and environmentally acceptable pest management against both H. armigera and C. chinensis in chickpea has paramount significances in boosting the productivity for small holder farmers.

Conclusions

Production and productivity of chickpea in Ethiopia were constrained mainly by H. armigera and C. chinensis. The economic losses inflicted by a single insect pest couldn’t be achieved through a single pest management method. Therefore, a comprehensive systems approach is needed to help the Ethiopian resource-poor small scale farmers whose livelihoods have been either directly or indirectly dependent upon agriculture. Various control measures such as; cultural, monitoring, botanical pesticides, the use of natural enemies, host plant resistance, synthetic chemicals, and IPM strategies have been suggested under this review. IPM encompasses all pest management techniques, that should consider farmers' economic gain/profit, environment, sustainability, effectiveness, holistic and systematic approach. Therefore, further research in Ethiopia are required to design and develop effective and sustainable H. armigera and C. chinensis management alternatives to increase the production and productivity of chickpeas for small-holder farmers.