Problematic due to the application of chemical insecticides on insect pests in corn cultivation

Corn has great biological diversity, which is why it is cultivated in diverse environments (^{Reséndiz et al., 2014}). Concerning its economic and cultural importance, corn is produced in large quantities, hence its great importance as a staple food in Mexico (^{Angel-Ríos et al., 2015}). However, this crop is susceptible to insect pests and diseases (^{Ramírez-Díaz et al., 2015}), despite the fact that chemical insecticides have a good effect on their control, since they greatly reduce population densities, many times another plague species is present (^{Troyo-Diéguez et al., 2006}).

Due to this, the pests considered occasional have become primary and therefore have caused significant losses (^{González-Maldonado et al., 2015}). It is estimated that for the control of the armyworm, being one of the pests with the highest incidence in the cultivation of corn, applications of chemical insecticides are made in around 4 million hectares (^{Blanco et al., 2010}). Therefore, it is also estimated that about 2 600 t of chemical insecticides are destined for S. frugiperda, which is mentioned for the state of Sinaloa, which between 2007 and 2011, 500 000 hectares per year were established, all this gives us a panorama of the number of applications made, as well as the surface to which it is intended (^{Cortez-Mondaca et al., 2012}).

This is just a panorama of the large amounts of agrochemicals used to control a proportion of different species of insect pests, so this problem has been observed with the option of giving added value when using non-conventional alternatives such as biological control, when considered as an organic crop, free of chemical products (^{Duarte, 2012}).

Factors that influence the growth of plague insect populations

Environmental conditions have an important influence on the population growth of pests (^{Reséndiz et al., 2016}). On the other hand, it is known that climate change causes alteration in the distribution, incidence and intensity of pests (^{Grageda et al., 2014}), therefore it is considered important to predict the relationship between the phenological stage of the culture and the plague (^{Méndez and González, 2014}). On the other hand, a factor that intervenes in the presence and abundance so that the plague insect has presence with the monoculture sowings (^{Cortez-Mondaca et al., 2012}).

In addition, when indiscriminate chemical applications are made, they cause resistant organisms and their reproduction is increased (^{Murguido and Elizondo, 2007}). Prediction models are used as a forecast, to then carry out an optimal control method; taking into account the relationship between the presence of the pest, crop phenology and temperature as an important factor (Valdez-Torres et al., 2012).

Main pests of corn

More than 80 species or complexes of pests species are considered in the corn crop and around 50 pests considered as occasional (Table 1) (^{Fernández, 2002}).

On the other hand, S. frugiperda (Figure 2) is considered the most important pest insect in corn cultivation (^{Rangel et al., 2014}).

Figure 2 Damage by warbler worm (a) and damage by braid worm (b).  

This insect feeds on the first vegetative stages (bud and tender leaves) until it is completely defoliated (Valdez-Torres et al., 2012). This plague is present all year round, so it additionally attacks stem and ear, competing with the elder worm Helicoverpa zea Boddie (Lepidoptera: Noctuidae) (^{González-Maldonado et al., 2015}). On the other hand, the soldier worm Spodoptera exigua Hübner (Lepidoptera: Noctuidae) is a pest that attacks the leaf and ear of corn, has a complete life cycle, develops between 15-25 days, then goes through five larval stages (^{García-Gutiérrez et al., 2012}; ^{González-Maldonado et al., 2015}).

Another plague that harms corn, especially the root zone is the blind chicken Phyllophaga spp. (Coleoptera: Melolonthidae), the damage causes it in the larval stage, causing the germination to be lost and rickets develop, its biological cycle lasts around 1 or 2 years going through different stages (^{Lugo-García et al., 2012}). Another of the rhizophagous pests of corn known as Diabrotica or braid worm Diabrotica virgifera zeae Krysan and Smith (Coleoptera: Chrysomelidae) (Figure 2), causes damage in the development of the crop by feeding on the roots, has several stages and its biological cycle is of around 45 days (^{Pérez et al., 2006}).

On the other hand, Helicoverpa zea Boddie (Lepidoptera: Noctuidae) is a polyphagous species that affects various crops, the damage is caused by larvae in corn and ear grains, the larval stage is 16 days, it has cannibalistic habits and it also favors the appearance of other pests (^{García-Gutiérrez et al., 2012}), such as the stigma fly Euxesta stigmatias Loew (Diptera, Otitidae= Ulidiidae), which causes decay that affects corn quality and grain yield, the damage causes it Larva status, it is estimated that around 70% are lost, in cycles with favorable conditions (^{Camacho-Báez et al., 2012}).

Biological control of insect pests

Particularly, biological control is a viable alternative, contributes to sustainability and does not affect the environment (^{Hernández-Velázquez et al., 2011}). The interest that has been observed regarding the use of biological control agents is due to the demand of these, since centers of reproduction of beneficial organisms have been created (^{Salas-Araiza and Salazar-Solis, 2003}). Therefore, insects’ parasitoids, predators and pathogenic microorganisms (^{Rios et al., 2017}), are used with the purpose of decreasing pest insect populations at a level that does not cause economic damage (Vázquez-Ramírez et al., 2015).

Parasitoids are considered insects with a wider activity, due to their diverse search capacity, which gives them the ability to reproduce and thus give continuity to the species (^{Salas-Araiza and Salazar-Solis, 2003}). On the other hand, the predators are a group of organisms that consume different plague insects and considered as generalists, of these they emphasize the catarinas in their diverse colors like those of the family Coccinellidae; they are used for the control of Lepidoptera eggs (^{Hernández-Trejo et al., 2018}). In addition, entomopathogenic microorganisms such as bacteria, viruses and fungi are widely used (Vázquez-Ramírez et al., 2015). So that they do not present a risk to the environment or harmful effects on human health; in addition, they have adequate control and strengthen the practices of integrated pest management (^{Rios et al., 2017}).

It is clear that the intention exercised by the use of biological control in the population of pests, has as its primary focus complemented not replace (^{Gallegos et al., 2003}; ^{Murguido and Elizondo, 2007}). Besides reducing risks of resistance and the amount of chemical applications in crops (^{Carreras, 2011}). So, it is evident the results that the release of egg parasitoids from pest insects has shown in the field (Figure 3), and where it has caused more than 80% mortality on the egg stage of S. frugiperda (^{Farhat et al., 2013}).

Figure 3 Parasitoid eggs on S. frugiperda (a) and depredation of flies by chiche (b).  

Entomopathogens for the control of pests in corn

The entomopathogenic fungi are microorganisms that have the particularity to parasitize different groups of insects and even some arthropods; the biological cycle of these comprises two phases: the first parasitic and the second saprophyte (^{Schapovaloff et al., 2015}). Some of these, such as M. anisopliae which is considered one of the main entomopathogenic fungi that control some pests of Lepidoptera of agricultural importance (^{Acuña et al., 2015}) and mainly feed on larval stages (^{Del Rincón-Castro et al., 2006}).

It is known that there are different groups of entomopathogenic fungi with more than 750 species, which are found in the environment (^{Motta-Delgado and Murcia-Ordoñez, 2011}), in addition to the soil that also constitutes a reservoir for different fungi and that contribute to the regulation of pest insect populations (^{Schapovaloff et al., 2015}). The genera considered to be the most important are: Metarhizium, Beauveria, Aschersonia, Entomophthora, Fusarium, Hirsutella, Paecelomyces and Verticillium, among others (^{Motta-Delgado and Murcia-Ordoñez, 2011}).

In Mexico, several studies have confirmed the presence of entomopathogenic fungi such as M. anisopliae, Beauveria bassiana (Bals.) Vuill and Paecilomyces sp., in corn crops (^{Hernández-Velázquez et al., 2011}). Regarding the biological control that is exerted on some plague insects, the entomopathogenic fungi Metarhizium and Paecilomyces have been used on larvae of S. frugiperda (^{Ángel-Ríos et al., 2015}). Also, B. bassiana is known for its wide range of hosts, develops a white mycelium that covers the insect after being infected and has been evaluated on larvae of Galleria mellonella (^{Gallegos et al., 2003}). Isaria fumosoroseus (formerly known as Paecilomyces fumosoroseus) is found to affect insect pests and has been considered as a potential control agent because it does not affect other beneficial insects (^{Flores et al., 2013}).

These pathogenic microorganisms are effective in the control of insect pests (^{Rios et al., 2017}), however, It is important to emphasize that this requires the development of the conditions required for their reproduction, in addition to considering the management that has been given in the preparation until the application thereof (^{Motta-Delgado and Murcia-Ordoñez, 2011}; ^{Ángel-Ríos et al., 2015}). For all the above, it is important to mention that these microorganisms are the most used for the control of insect pests (^{Rios et al., 2017}).

Entomopathogenic viruses are another group of organisms that cause epizootics on insect pests and viral infection occurs orally, through the ingestion of food contaminated with viral occlusion bodies (^{Cano et al., 2004}). It is reported that at least 12 families of viruses infect insects and some arthropods, being those of the family Baculoviridae the most studied, these affect larvae of insect pests such as S. frugiperda (^{Rios et al., 2017}).

Among the microorganisms of bacteria, the most important is Bacillus thuringiensis, which has a selective toxicity because it has a broad spectrum, especially a specificity for lepidopteran insects (^{Sauka and Benintende, 2008}). It is used for the control of the Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) (^{Jojoa-Bravo and Salazar-González, 2011}). Therefore, the biological control based on entomopathogenic microorganisms in the combat of insect pests is promising, because they cause mortality in different biological stages (^{Lezama et al., 2007}).

Natural enemies for the control of pests in corn

Natural enemies are an important part of pest insect regulation and occur naturally in corn crops, both predators and parasitoids (^{Hernández-Trejo et al., 2018}). Due to the diversity of natural enemies, habits, life cycle, metabolism, among others, each one of the pests could be controlled by different predators or parasitoids, being some specific (^{Hernández-Velázquez et al., 2012}).

Within the great diversity of insects that affect corn is the stigma fly (Euxesta stigmatias) (Figure 3) and is parasitized by several species such as some wasps of the genus Spalangia (Hymenoptera: Pteromalidae) specifically in stage of pupae, this fly is introduced and deposits its eggs inside this (^{Camacho-Báez et al., 2012}). For the case of S. frugiperda, it is parasitized by several species such as Chelonus insulares Cresson and by Meteorus sp., (Nees) (^{Rios et al., 2017}) and also the Ichneumonidae family, highlighting the species Campoletis sonorensis (Cameron), also wasps such as some species of the genus Trichogramma are the parasitoids most used in the biological control of lepidoptera (^{Hernández-Trejo et al., 2018}). In addition to this, programs have been designed through the release of parasitoids, such as Telenomus remus, for the biological control of S. frugiperda, with satisfactory results (^{Farhat et al., 2013}). On the other hand, for the control of H. zea, the parasitoid Cotesia marginiventris Cresson, (Hymenoptera: Braconidae) has been reported (^{García-Gutiérrez et al., 2012}).

The predators are considered polyphagous insects, so they are less specific than the parasitoids, of these the hemimetabolos stands out, the order Hemiptera is one of the most effective, standing out the family Pentatomidae, Lygaeidae, Nabidae, Miridae, among others (^{Rios et al., 2017}). An example of these is the pirate bug (Orius insidiosus) (Say) (Hemiptera: Anthocoridae) which is a predator of the stigma fly in different biological states and so it is considered promising to be used as a biological control agent, besides that it has been observed that it feeds on lepidopteran eggs; the murine bug Sinea sp., (Hemiptera: Reduviidae) that preys on S. frugiperda larvae (^{Camacho-Báez et al., 2012}).

Likewise, holometabolos stand out in the order Diptera, Coleoptera, Neuroptera, and Hymenoptera (^{Rios et al., 2017}), as an example, this Trichogramma sp., (Hymenoptera: Trichogrammatidae) as natural enemies of lepidoptera. Therefore, predators considered generalists, continue to play an important role, since in various biological states of corn cultivation (^{García-Gutiérrez et al., 2012}).