Introduction

Cowpea (Vigna unguicalata (L.) Walp.) (Fabaceae) is one of the most important grain legumes for human and livestock nutrition in sub-Saharan Africa. It is relatively well adapted to various agro-ecosystems especially the semi-arid and hot regions (Coulibaly et al. 2009) and soils with variable pH levels and more than 85% sand (Obatolu 2003; Singh 2014). About 70% of the world cowpea production is from the dry Savanna and Sahel Zones of West and Central Africa (Timko et al. 2007). In West Africa particularly, cowpea is part of the traditional cropping systems and is becoming a strategic crop because of its multiple uses such as food for millions of people, fodder for livestock, soil restoration and source of income for resource-poor farmers and small scale processors (Isubikalu et al. 2000). The grain of cowpea is the major source of protein (20–32%), minerals and vitamins in the diet of majority of rural and modest city communities (Gowda et al. 2000; Sule and Bello 2006; Timko et al. 2007; Egho 2010; Boukar et al. 2013; Singh 2014). It also contains other essential micronutrients such as calcium, iron, thiamine and riboflavin (Bressani 1985; Voster et al. 2007), making cowpea an important food and nutritional security crop in sub-Saharan Africa (Nielsen et al. 1993). However, despite its importance, cowpea grain yield remains very low (100–500 kg ha−1) in famers’ field growing conditions compared to the potential yield (1.5–3.0 t ha−1) (Rachie 1985; Karungi et al. 2000; Asante et al. 2001; Asiwe et al. 2009; Boukar and Fatokun 2009; Oyewale and Bamaiyi 2013; Singh 2014). This very low yield is imputable to a complex of biotic and abiotic stress factors including insect pests, diseases, parasitic weeds, heat, low soil fertility and drought. Above all, insect pests’ infestation and damage have the most negative impact on cowpea productivity in all cropping locations worldwide (Singh and Jackai 1985). Average grain yield losses range between 50 and 80% in untreated fields (Singh and Allen 1980) and can reach 90–100% under high pest infestation conditions (Jackai and Daoust 1986; Singh 2014).

The extent of insect pests’ infestation and the severity of their attacks and damage in cowpea field vary from one location to another and depend on the plant developmental stage. Application of synthetic insecticides remains the most common measure used so far to combat insect pests in cowpea. However, because of the potential hazards caused by chemicals to humans (users and consumers), animals and the environment, and possible development of insecticide resistance by the insect pests, efforts have been made to seek eco-friendly alternative options including cultural practices, biological control, use of biopesticides and resistant varieties. Among these options, varietal resistance appears to be the most cost-effective and environmentally friendly approach to mitigate insect pests’ effects on cowpea production and value-chain (Ofuya and Lale 2001; Fatokun 2002). Indeed, plant self-defence systems including the biochemical and biophysical systems, play a major primary role in controlling pest either by killing them, affecting their physiology and behaviour, or serving as anti-feedant or repellent. Varietal resistance is the first line of defense against crops’ insect pests and should be one of the major criteria in the development and release of new cultivars to ensure cost-effective production (Sharma and Crouch 2004). Cowpea host plant resistance can be improved genetically through breeding and biotechnology applications (Boukar and Fatokun 2009) to create new lines with desired plant and grain qualities. In the past, several studies were conducted to identify cowpea genotypes with resistance against various insect pests (Woolley and Evans 1979; Chalfant 1985; Chambliss and Hunter 1997; Devereau et al. 2002). This review describes the key insect pests of cowpea, provides a non-exhaustive list of cowpea lines that were identified from past and recent studies as insect-resistant and gives an overview of the mechanisms and principles of host plant resistance to be considered as future prospects for cowpea breeding and improvement in Africa.

Overview of insect pests of cowpea in sub-Saharan Africa

Insect pests represent the major limiting factor of cowpea production in SSA. A wide range of the pests causes devastating damage during the crop developmental stages and storage as well (Jackai and Daoust 1986). The high diversity of insects and their high preference for cowpea explain their regular presence in both field and store. The preponderance of insect pests in SSA cowpea fields may be the result of co-evolution since cowpea is indigenous to the sub-region. Every growth stage of the crop has at least one major insect species that can cause significant negative impact on the plants growth and subsequently substantial losses in grain yield if chemical treatment is not well applied in due course (Singh et al. 1990; Jackai and Adalla 1997; Fatokun 2002; Boukar and Fatokun 2009). Over 85 insect species attack cowpea in one way or another (Booker 1965) with about 20 of them with regular occurrence and economic importance in various cowpea production areas worldwide (Oyewale and Bamaiyi 2013). In Africa, the most widespread and damaging insect pests include the cowpea aphid Aphis craccivora Koch, Mirperus spp. and Lygus spp., the foliage beetles Ootheca spp. and Medythia spp., the hairy caterpillar Amsacta moloneyi Druce, the leafhopper Empoasca spp., the beanfly Ophiomyia phaseoli Tryon, the whitefly Bemisia tabaci Gennadius, the flower beetles Decapotoma affinis Billb, Mylabris senegalensis Voigts and Coryna agenteata F., the leaf-footed plant bug Leptoglossus australis Fabricius, the flower bud thrips Megalurothrips sjostedti Trybom and Sericothrips occipitalis Hood, the leaf thrips Hydatothrips adolfifriderici Kamy (Thysanoptera: Thripidae), the legume pod borer Maruca vitrata Fabricius, the pod sucking bugs complex Clavigralla tomentosicollis Stal, Anoplocnemis curvipes (F.), Riptortus spp., and the cowpea weevil Callosobruchus macufutus (F.). A comprehensive list of these major insect pests is presented in Table 1.

Table 1 Major insect pests of the cowpea crop and stored grains in Africa
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Among the cowpea field pests, M. vitrata, A. craccivora, C. tomentosicollis and M. sjostedti are the most economically important and most widespread within the cowpea cropping agro-ecologies worldwide (Malgwi and Onu 2004; OECD 2015). Other species like the green stink bug Nezara viridula Linnaeus, the leaffooted bug Leptoglossus phyllopus (L.) and the cowpea curculio Chalcodermus aeneus Boheman are also economically important but their occurrence is either sporadic or limited to some continents or regions. As for storage pests, Callosobruchus macufutus (F.) and C. chinensis (L.) are widely distributed, while C. rhodesianus (Pit.) and C. subinnotatus (Pit.) are restricted to southern and western Africa, respectively (Mbata 1993).

Concept of host plant resistance to insect pests

Host plant resistance (HPR) is the genetically inherited qualities in the plant that determine the ultimate degree of damage done by a pest (Painter 1951). It is associated with the ability of plants to ward off or withstand attacks and recover from injury due to a pest (Kogan 1994). Plant resistance is driven by some mechanisms or principles.

Mechanisms of plant resistance to insect pests

The host plant resistance involves very complex principles or mechanisms that were classified into 3 main categories: antibiosis, antixenosis (non-preference) and tolerance (Painter 1951; Farrar Jr and Kennedy 1991).

  • Antibiosis is the property of the host plant to affect the life of an insect when it uses the plant as food (Painter 1951; Kogan 1994). Antibiosis is essentially due to plant biochemical compounds. Plant with antibiosis effect can kill insect or disrupt some functions of its biology. Some antibiosis characteristics were detected with resistance to different biotype of cowpea aphid conferred by single dominant genes (Ombakho et al. 1987; Bata et al. 1987; Pathak 1988).

  • Antixenosis is the property of the host plant in which insect perceives the undesirability to use it for food, oviposition or shelter (Painter 1958). Plant physical and biochemical factors making the plant a refractory “guest” (xenos in Greek) for the insect are the main cause of non-preference (Kogan 1994). The repellence or/and disruption of insect behavior are the main effects of this mechanism.

  • Tolerance is the ability of host plant to withstand the pests’ infestation or recover from insects’ attack. Plant–insect friendly coexistence is the main rule of this mechanism.

Plant defense systems

Resistance is a response of plant defense system that affects the life, physiology or behaviour of the pests (Cortesero et al. 2000; Dicke and Baldwin 2010; Mahipal 2016). Many cowpea lines have good resistance systems against insect pests (OECD 2015). They are described as follows:

Physical defense factors

The plant physical defences comprise morphological and anatomical features. They are natural barriers such as trichomes, hairs, pod wall hardness, etc. (Cortesero et al. 2000) that protect plant from invasion or give the plant good strength and rigidity. In both cultivated and wild cowpea relatives, many morphological characters were found to be associated with pest-non preference proprieties. For instance, the dense and long trichomes on some cowpea cultivars were found to increase their resistance to the pod borer M. vitrata (Jackai and Oghiakhe 1989; Oghiakhe et al. 1992; Oigiangbe et al. 2006) and also to the pod sucking bugs (Oigiangbe et al. 2002, 2006). Similarly, the dense hairs found on different parts of the wild cowpea V. vexillata have been associated with resistance to pod-sucking bugs and pod borer (Oghiakhe et al. 1992; Boukar et al. 2013). Pod wall strength and hardness are considered as important traits for resistance to pods borers (Rymal and Chambliss 1981; Oigiangbe et al. 2002). Thick and compact collenchyma cells in the stems and fibrous tissues on the petal surface contributed to resistance to flower insect pests. The findings of this study (Oghiakhe et al. 1991) showed that the stem epidermis was associated with severe limitations on M. vitrata larval movement and feeding. Resistance in TVu-946 to M. vitrata was associated to its erect type and profuse flowering (Oghiakhe et al. 1992). Pods of TVu-9930 were observed to have especially harsh surface texture which may explain the inability of A. craccivora to colonize the plants (Ofuya 1993). A wild relative of cowpea, TVNu-72 showed resistance to pod sucking bugs because of the sclereids or other strengthening tissues on its pods (Jackai et al. 2001). Other wild Vigna species with resistance to M. vitrata and the pod sucking bugs include V. unguiculata ssp. dekindtiana, V. luteola, V. oblongifolia and V. recticulata (Singh et al. 1989). Finally, it was reported that cowpea varieties with pigmented calyx, petioles, pods and pod tips suffer less damage from M. vitrata (Singh et al. 2002).

Biochemical defense factors

The chemical bases of insect-plant interactions are one of the most important aspects of HPR. Direct chemical defences are due to a wide range of secondary metabolites (Allelochemicals) acting as toxins, repellents, digestibility reducers, feeding deterrents, or acting as precursors to physical defense systems (Bennett and Wallsgrove 1994; Cortesero et al. 2000). They are essentially phytochemical compounds such as non-protein amino acids, cyanogenic glycosides, alkaloids, terpenoids, tannins, lignin, flavonoids, etc. that negatively affect the physiology or behaviour of the pest (Bennett and Wallsgrove 1994; Lattanzio et al. 2000; Dicke and Baldwin 2010). The activities of the phytochemicals comprise nervous system inhibition, tissue malformation, feeding deterrence (bitterness), enzyme inhibition, growth inhibition, hemolymph coagulant, toxin, digestive or respiratory inhibition. They are involved in both antibiosis and antixenosis mechanisms (Kogan 1994). It was reported that cowpea varieties with high levels of antibiosis prevent insect pests from establishing massively on the plants (van Emden 1991). The wild cowpea line TVNu 1158 was identified as resistant to aphid (Souleymane et al. 2013) and was found to have such resistance gene (Omoigui et al. 2017). Secondary metabolites such as polyphenols, terpenoids and flavonoids can reinforce the resistance of cowpea to M. sjostedti and M. vitrata (Oigiangbe et al. 2001; Alabi et al. 2011). The ethyl-acetate content in the stems of TVu-946 showed greater feeding inhibition against M. vitrata (Otieno et al. 1985; Soundararajan et al. 2013). Many authors have reported that high plant phenols content increases resistance to insect pests (Zucker 1972; Rowell-Rahier 1984; Bennett and Wallsgrove 1994). Some cultivars that produce high level of volatile compounds are less attractive to cowpea curculio (Rymal and Chambliss 1981). Good resistance in TVu-36, TVu-408, TVu-410, TVu-801, TVu-2896 and TVu-3000 to A. craccivora was found to be due to their relatively high phenolic and or flavonoid contents (Ofuya 1997). A study done by MacFoy and Dabrowski, (1984) pointed out that an increase in total phenols and flavonoids content in the stem of TVu-310 and 408-p-2 was associated with high resistance to aphid infestation. As for the total sugars content, the same authors found more in the susceptible line Vita-1 compared to the resistant TVu-310. They argued that the basis of aphid resistance in cowpea might be antixenosis and antibiosis properties of the genotypes. Cyanogenic heterosides, flavonoids, tannins and trypsin inhibitors were identified in IT86D-716 as antibiosis compounds against the C. tomentosicollis (Dabire-Binso et al. 2010). Some biochemical compounds with potential effects on cowpea insect pests are summarized in Table 2.

Table 2 Some biochemical compounds with adverse effects on cowpea insect pests
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Physiological patterns

Some physiological factors such as plant growth habit, recovery capacity from pest-injury, early maturity, high flower production, etc. are part of the plant tolerance traits. Some of these traits were found associated with increased tolerance of cowpea to field insect pests. For instance, it was reported that cowpea cultivars with pods independently exerted from plant canopy suffer less damage by M. vitrata (Usua and Singh 1979). Similarly, some studies conducted by Okeyo-Owuor and Ochieng, (1981) and MacFoy et al. (1983) found that TVu-946 with less dense canopy was less preferred by M. vitrata for oviposition than the cultivar Vita-1 that has denser leaf canopy because adults of the pod borer prefer dark environments. Some cowpea varieties (e.g. IT91 K-180) tolerate a high population of thrips by producing more flowers and pods to compensate the pests’ damage (Alabi et al. 2003).

Genetics of the resistance

The success in developing varieties resistant to biotic stresses depends on the availability of sources of resistance gene and the inheritance of such resistance (Rubiales et al. 2015). Factors regulating host plant resistance are carried either by several minor genes (polygenic resistance) or by single major gene (monogenic/oligogenic resistance). Polygenic resistance is suitable for controlling multiple pests. Several insect-resistance traits are found to be polygenic type but their introgression into new varieties is much more complex than that of monogenic resistance (Kogan 1994). However, the progress in biotechnology has facilitated the rapid introgression of targeted genes and traits, regardless of whether polygenic or monogenic (Sharma et al. 2002).

In past and recent times, research efforts have been made to evaluate thousands of cowpea accessions for resistance to major pests such as A. craccivora, M. vitrata, M. sjostedti, C. maculatus, Empoasca spp., etc. and for some cases the genetic basis of resistance has been established.

The monogenic nature of the aphid resistance was established in some cowpea varieties (van Emden 1991; Ofuya 1993, 1997) but in some cases the resistance was easily overcome by new biotypes of the insect pest. Also it is now known that the single dominant gene that conferred resistance to aphid in TVu-3000 and transferred to several improved cowpea varieties is no longer effective due probably to gene resistance broken down (Bata et al. 1987; Pathak 1988).

More than 8500 accessions of cowpea were evaluated for resistance to pod borer and pod-sucking bugs, and more than 4000 accessions were evaluated for resistance to flowering thrips and bruchid from 1984 to 1988 (Boukar et al. 2013). Among them, several varieties have been identified with moderate or high level of resistance to many species except M. maruca with limited resistance rather than field tolerance only. An inventory of some cowpea accessions with good level of resistance to insect pests is shown in Table 3.

Table 3 Potential sources of resistance of cowpea genotypes to major insect pests
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Progress made in cowpea breeding for resistance to insect pests in SSA

Breeding for improved insect pests resistant varieties is a sustainable strategy for crop production especially in SSA where accessibility and affordability synthetic insecticides are an issue. In addition to being eco-friendly, it can particularly enhance the crops’ productivity and value chain. This will therefore insure the regular availability of pest-resistant varieties that will be more attractive to farmers by decreasing their input costs and enhancing their profits (Fatokun 2002; Hall et al. 2003). According to Painter 1951, the cultivation of pests’ resistant varieties must occupy the first line of defense against insect pests although this can be reinforced by other controlled measures. The value of plant defense systems rests on the development and use of pest-resistant crop varieties (Smith 1989; Cortesero et al. 2000). Breeding for resistance to insect pests has occupied an important place in cowpea improvement program in SSA with the objective of finding genetic sources of resistance to major pests (Semple 1992; Boukar and Fatokun 2009). Through conventional breeding, many improved cowpea lines with highly desirable plant and grain traits have been developed (Boukar and Fatokun 2009; Boukar et al. 2015). Some of these varieties that have moderate to good levels of resistance to various insect pests (e.g. A. craccivora M. sjostedti and M. vitrata), diseases and parasitic weeds, have been released to farmers (OECD 2015; Boukar et al. 2015). Since 1990’s, advances in biotechnology such as marker assisted selection have accelerated the research in host plant resistance to cowpea insect pests (Jackai and Adalla 1997). The cowpea breeding programs in SSA are applying these tools in order to introgress desirable traits into improved varieties (Boukar and Fatokun 2009; Boukar et al. 2015). A non-exhaustive list of some used markers is shown in Table 4.

Table 4 Some available markers and QTLs for biotic and abiotic stresses in cowpea
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Also, recurrent selection had been pursued to increase the level of cowpea resistance to multiple insect pests (Ehlers and Hall 1997).

Some accessions of wild Vigna species were found to have high levels of resistance to many insect pests of cowpea (Singh et al. 1990; Fatokun et al. 1997; Jackai et al. 2001). Concerted but unsuccessful attempts were made to cross pests’ resistant wild Vigna species (e.g. Vigna vexillata and V. oblongifolia) with cultivated V. unguiculata (Murdock 1992; Fatokun 2002).

On the other hand, genetically modified (GM) cowpea is being developed in some research stations in SSA (ACB 2015). The GM cowpea was modified to carry an insecticidal Cry1Ab gene that encodes a Bt (Bacillus turrigiensis) toxin. It was developed by the Australian Commonwealth Scientific and Industrial Research Organization (CSIRO) with Monsanto donating the Cry1Ab and nptII (neomycin antibiotic resistance) genes (Sirinathsinghji 2015). Ghana, Malawi, Burkina Faso and Nigeria are the countries where field evaluations were performed. Field trials were conducted in Nigeria and Burkina Faso from 2014 and in Ghana from 2012. In recent times genetic engineering option had been undertaken for the development of Maruca resistant cowpea. A transgenic cowpea was obtained by inserting the Cry1Ab Bt gene (Popelka et al. 2006). The Bt gene has been transferred through backcrossing to some improved and released cowpea varieties in different countries. These Bt containing varieties have shown resistance to Maruca under confined field trials carried out in some West African countries (Mohammed et al. 2015).

One limitation of the native Bt genes is their poor expression in higher eukaryotes (Bett et al. 2017). Indeed, insecticidal proteins need to be expressed at high levels in their plant hosts in order to be effective against targeted insects (Gatehouse 2008). Another limitation is the selectivity properties of the Bt genes that target mostly Lepidopteran species than other group of insects.

Conclusion

This review article provides a summary of recent and past research findings on host plant resistance to insect pests. More specifically, it describes the main insect pests and their occurrence and damages on cowpea, provides a useful list of genetic material constituting potential sources of resistance to cowpea insects that can be exploited in the breeding program to develop new improved varieties with very limited need of insecticide application. Moreover the review has highlighted the need of using molecular markers in breeding process to complement the conventional breeding in order to reduce the time and effort required to develop new cultivars and avoid tedious inoculations and screenings process.

For future prospect, research efforts should be maintained to overcome the crossing barriers between the wild and cultivated cowpea so as to take advantage of genes present in some wild relatives. Investigations on the mechanisms and genetic basis of resistance to major insect pests in cowpea cultivars should be carried out. Pyramiding of genes for resistance to multiple abiotic stresses which is one of the objectives of the International Institute of Tropical Agriculture’s (IITA) cowpea improvement program in collaboration with national agricultural research systems (NARS) and advanced research institutes’ (ARIs) programs should be vigorously pursued as a priority mission in order to develop high desired cultivar combining resistance genes to different insect pests that would be a more welcome option for farmers in SSA.