Integrated Management of Helicoverpa armigera in Soybean Cropping Systems

1. Introduction

In most developing countries, agriculture is the driving force for broad-based economic growth and low agricultural productivity is a major cause of poverty, food insecurity, and malnutrition. However, food production per unit of land is limited by many factors, including fertilizer, water, genetic potential of the crop and the organisms that feed on or compete with food plants. Despite the plant-protection measures adopted to protect the principal crops, 42.1% of attainable production is lost as result of attack by pests [1]. Therefore, accelerated public investments are needed to facilitate agricultural growth through high-yielding varieties with adequate resistance to biotic and abiotic stresses, environment-friendly production technologies, availability of reasonably priced inputs in time, dissemination of information, improved infrastructure and markets, and education in basic health care.

Soybean (Glycine max (L.) Merrill) is one of the most important and widely grown oil seed crops in the world. Successful production in soybean cropping systems is hampered due to the incidence of several insect pests such as Etiella zinkienella Treitschke, Tetranychus urticae Koch, Thrips tabaci Lindeman, Spodoptera exigua (Hübner) and Helicoverpa armigera (Hübner) [2-9]. Among these pests, H. armigera represents a significant challenge to soybean production in different soybean-growing areas around the world. Helicoverpa armigera is an important pest of many crops in many parts of the world and is reported to attack more than 60 plant species belonging to more than 47 families (such as soybean, cotton, sorghum, maize, sunflower, groundnuts, cowpea, tomato and green pepper) [10-12]. This noctuid pest is distributed eastwards from southern Europe and Africa through the Indian subcontinent to Southeast Asia, and thence to China, Japan, Australia and the Pacific Islands [13]. The pest status of this species can be derived from its four life history characteristics (polyphagy, high mobility, high fecundity and a facultative diapause) that enable it to survive in unstable habitats and adapt to seasonal changes. Direct damage of the larvae of this noctuid pest to flowering and fruiting structures together with extensive insecticide spraying resulted in low crop yield and high costs of production [14].

Different methods have been applied to control H. armigera in order to improve the quality and quantity of soybean production in cropping systems of this oil seed crop. However, synthetic insecticides including organophosphates, synthetic pyrethroids and biorational compounds are the main method for H. armigera control in different parts of the world. This wide use of pesticides is of environmental concern and has repeatedly led to the development of pesticide resistance in this pest. Furthermore, the deleterious effects of insecticides on nontarget organisms including natural enemies are among the major causes of pest outbreaks. It is therefore necessary to develop a novel strategy to manage population of H. armigera and reduce the hazardous of synthetic chemicals.

The common trend towards reducing reliance on synthetic insecticides for control of insect pests in agriculture, forestry, and human health has renewed worldwide interest in integrated pest management (IPM) programmes. IPM is the component of sustainable agriculture with the most robust ecological foundation [15]. IPM not only contributes to the sustainability of agriculture, it also serves as a model for the practical application of ecological theory and provides a paradigm for the development of other agricultural system components. The concept of IPM is becoming a practicable and acceptable approach among the entomologists in recent past all over the world and focuses on the history, concepts, and the integration of available control methods into integrated programmes. However, this approach advocates an integration of all possible or at least some of the known natural means of control with or without insecticides so that the best pest management in terms of economics and maintenance of pest population below economic injury level (EIL) is achieved.

Fundamental of effective IPM programmes is the development of appropriate pest management strategies and tactics that best interface with cropping system-pest situations. Depending on the type of pest, however, some of the primary management strategies could be selected. In the case of H. armigera, several management tactics should be considered to implement a comprehensive integrated management. Potential of some of the control tactics to reduce population density of H. armigera in different cropping systems were evaluated by several researchers and attempts have been made to develop integrated management approach for H. armigera using host plant resistance [2, 4, 6, 11] including transgenic Bt crops [16], biological control (predators and parasitoids) [17], interference methods including sex pheromones [18], biopesticides (especially commercial formulations of Bacillus thuringiensis) [19], cultural practices (including appropriate crop rotations, trap crops, planting date and habitat complexity) [20] and selective insecticides [21]. Likewise there remains a need for ongoing research to develop a suite of control tactics and integrate them into IPM systems for sustainable management of H. armigera in cropping systems. Keeping this in view, integration of these methods based on the ecological data especially thermal requirements of this pest and its crucial role in forecasting programme of H. armigera could lead a successful integrated management for this pest in soybean cropping systems.

As discussed above, integrated management is typically problematic in cropping systems, especially in the case of H. armigera on soybean. However, our intent in this section is not to develop an exhaustive review of all resources that may possibly contribute to more effective pest management for the future, but to select several topic areas that will make essential contributions to sustainable soybean cropping systems. Although the past research focused on developing various pest management tactics that would be packaged into an integrated pest management strategy, we have selected several types of resources for our discussions, realizing that there are other resources can be used in developing IPM programmes. Furthermore, to generate a comprehensive management programme, we present our perspectives on future research needs and directions for sustainable management of this pest in soybean cropping systems such as tri-trophic interactions [22], importance of modeling of insect population [23], crucial role of forecasting and monitoring programmes in IPM [24], interactions among different management tactics in IPM [25] and significance of biotechnology and genetically modified plants in IPM. Therefore, considering the importance of H. armigera in successful production of soybean, this review intends to provide an appropriate document to the scientific community for sustainable management of H. armigera in soybean cropping systems.

2. History of terminology and definition of IPM

Although many IPM programmes were initiated in the late 1960s and early 1970s in several parts of the world, it was only in the late 1970s that IPM gained momentum [26]. Throughout the late 19th and early 20th centuries, in the absence of powerful pesticides, crop protection specialists relied on knowledge of pest biology and cultural practices to produce multi tactical control strategies that, in some instances, were precursors of modern IPM systems [27]. That stance changed in the early 1940s with the advent of organosynthetic insecticides when protection specialists began to focus on testing chemicals, to the detriment of studying pest biology and non-insecticidal methods of control [15]. The period from the late 1940s through the mid-1960s has been called the dark ages of pest control. By the late 1950s, however, warnings about the risks of the preponderance of insecticides in pest control began to be heard. The publication of the book “Silent Spring” by Rachael Carson in 1962 ignited widespread debate on the real and potential hazards of pesticides. This still ongoing dialogue includes scientists in many disciplines, environmentalists, and policy makers. However, “Silent Spring” contributed much to the development of alternatives to pesticides for pest management purposes, augmented global interests in developing cropping systems that limit crop pests, and added much to the environmental movement [26]. In fact, widespread concerns about the detrimental impact of pesticides on the environment and related health issues were responsible in large part for the development of the concept of IPM.

The seed of the idea of integrated control appears in a paper by Hoskins et al. [28]. Conceivably, “integrated control” was uttered by entomologists long before formally appearing in a publication. However, it was the series of papers starting with Smith and Allen [29] that established integrated control as a new trend in economic entomology. Towards the end of the 1960s, integrated control was well entrenched both in the scientific literature and in the practice of pest control, although by then “pest management” as a sibling concept was gaining popularity [30]. However, in subsequent publications, integrated control was more narrowly defined as “applied pest control which combines and integrates biological and chemical control”, a definition that stood through much of the late 1950s and the early 1960s but began to change again in the early 1960s as the concept of pest management gained acceptance among crop protection specialists [15, 26].

The concept of “protective population management”, later shortened to “pest management”, gained considerable exposure at the twelfth International Congress of Entomology, London [31]. The Australian ecologists who coined the expression contended that “control”, as in pest control, subsumes the effect of elements that act independently of human interference. Populations are naturally controlled by biotic and abiotic factors, even if at levels intolerable to humans. Management, on the other hand, implies human interference. Although the concept of pest management rapidly captured the attention of the scientific community, in 1966 Geier seemed to minimize the semantic argument that favored “pest management” by stating that the term had no other value than that of a convenient label coined to convey the idea of intelligent manipulation of nature for humans’ lasting benefit, as in “wildlife management” [32].

Not until 1972, however, were “integrated pest management” and its acronym IPM incorporated into the English literature and accepted by the scientific community. In creating the synthesis between “integrated control” and “pest management”, no obvious attempt was made to advance a new paradigm. Much of the debate had been exhausted during the 1960s and by then there was substantial agreement that: (a) “integration” meant the harmonious use of multiple methods to control single pests as well as the impacts of multiple pests; (b) “pests” were any organism detrimental to humans, including invertebrate and vertebrate animals, pathogens, and weeds; (c) “management” referred to a set of decision rules based on ecological principles and economic/social considerations and (d) “IPM” was a multidisciplinary endeavor.

The search for a perfect definition of IPM has endured since integrated control was first defined. A survey recorded 65 definitions of integrated control, pest management, or integrated pest management [26]. Unfortunately, most of them perpetuate the perception of an entomological bias in IPM because of the emphasis on pest populations and economic injury levels, of which the former is not always applicable to plant pathogens, and the latter is usually attached to the notion of an action threshold often incompatible with pathogen epidemiology or many weed management systems [33]. Furthermore, most definitions stress the use of combination of multiple control methods, ignoring informed inaction that in some cases can be a better IPM option for arthropod pest management [15]. It was, however, in 1972 that the term ‘integrated pest management’ was accepted by the scientific community, after the publication of a report under the above title by the Council on Environmental Quality [34]. Much of the debate had already taken place during the 1960s and by then there was substantial agreement on the following issues [15]: (a) the appropriate selection of pest control methods, used singly or in combination; (b) the economic benefits to growers and to society; (c) the benefits to the environment; (d) the decision rules that guide the selection of the control action and (e) the need to consider impacts of multiple pests.

Several authors have come close to meeting the criteria for a good definition, but a consensus is yet to be reached. Accordingly, some of the IPM definitions were listed in Table 1. A broader definition was adopted by the FAO Panel of Experts [35]: “Integrated Pest Control is a pest management system that, in the context of the associated environment and the population dynamics of the pest species, utilizes all suitable techniques and methods in as compatible a manner as possible and maintains the pest population at levels below those causing economic injury.” This definition has been cited frequently and has served as a template for others. However, based on an analysis of definitions spanning the past 35 years, the following is offered in an attempt to synthesize what seems to be the current thought: “IPM is a decision support system for the selection and use of pest control tactics, singly or harmoniously coordinated into a management strategy, based on cost/benefit analyses that take into account the interests of and impacts on producers, society, and the environment” [15].

3. Systems in agriculture and the situation of IPM as a sub-system

Spedding [44] defined a system as a group of interacting components, operating together for a common purpose, capable of reaching as a whole to external stimuli. A system is unaffected by its own output and has a specified boundary based on the inclusion of all significant feedbacks. However, four types of systems are generally acknowledged in agriculture including ecosystem, agroecosystem, farming systems and cropping systems (Figure 1). In this hierarchy, a system may consist of several sub-systems. IPM is a sub-system of cropping system and considered as the operating system used by farmers to manage population of crop pests. This sub-system has a degree of independence and can be studied in isolation of the cropping system. It has its own inputs and has the same output as the main system (i. e. yield) but relates to only some of the components and therefore, to only some of the inputs [45].

IPM systems have a goal of providing the farmer with an economic and appropriate means of controlling crop pest. The aim should be to devise an IPM system which is sufficiently robust to maintain control over a prolonged period of time [46]. However, to achieve an IPM system a number of attributes will require including: (a) provide effective control of pest; (b) be economically viable; (c) simplicity and flexibility; (d) utilize compatible control measure; (e) sustainability and (f) minimum harmful effect on the environment, producer and consumer.

First and foremost the IPM system must be effective. For the farmer this means that this system should be at least as good as the conventional control methods. The system should be economic. No farmer will adopt and sustain use of uneconomic pest management practices. On the other hand, an IPM system must be designed to be as simple as possible, utilizing the minimum number of control measures compatible with maintaining pest populations at appropriate levels. The individual control measures should of course be compatible and optimize natural mortality factors. It is important during design of an IPM system to consider the level of control which is required and the best mix of control measures that will achieve this with minimal antagonism. Finally, the IPM system should be sustainable, have minimum impact on the environment and present no hazard to the farmer, their families or the consumers of the crop products [45].

4. Decision making in IPM

Following widespread concerns about the adverse effects of insecticides it became clear that calendar spraying was not the appropriate approach to pest control. In fact, determining whether an insect control measure (usually an insecticide) is “needed” is one of the basic principles of any IPM programme. “Need” can be defined in a number of ways, but most growers associate the need for an insecticide with economics. In other words, most growers ask some form of these questions: “How many insects cause how much damage?”, “Are the damage levels all significant?” and “Will the value of yield protection with an insecticide offset the cost of control?” Therefore, researchers from different agricultural disciplines came to realize that a decision rule or threshold should answer such questions and that pest control must be viewed as a decision making process (Figure 2).

Pest management is a combination of processes that include obtaining the information, decision making and taking action [41]. In assessing, evaluating and choosing a particular pest control option, farmer’s perception of the problem and of potential solutions is the most important factor (Figure 2). Decision making in pest management, like other economic problems in agriculture, involves allocating scarce resources to meet food demand of a growing population. In this process, agricultural producers have to make choices regarding the use of several inputs including labor, insecticides, herbicides, fungicides, and consulting expenses related to the level and intensity of pest infestation and the timing of treatment. However, decision making process for pest control takes place in many levels at the fields. These various layers of decision making affect the whole strategy of pest control in a given cropping system, region or country as well as the set of approaches and measures that are chosen to implement pest control programmes.

5. Crucial role of economic thresholds for implementation of IPM programmes

In most situations it is not necessary, desirable, or even possible to eradicate a pest from an area. On the other hand, the presence of an acceptable level of pests in a field can help to slow or prevent development of pesticide resistance and maintain populations of natural enemies that slow or prevent pest population build-up. Therefore, the concepts of economic injury level (EIL) and economic threshold (ET [sometimes called an action threshold]) were developed (Figure 3). EIL and ET constitute two basic elements of the IPM [48]. Economic injury level was defined as the lowest population density that will cause economic damage [49]. The EIL is the most essential of the decision rules in IPM. In addition, the economic injury level provides an objective basis for decision making in pest management and the backbone for the management of pests in an agricultural system is the concept of EIL [48]. Ideally, an EIL is a scientifically determined ratio based on results of replicated research trials over a range of environments. In practice, economic injury levels tend to be less rigorously defined, but instead are nominal or empirical thresholds based on grower experience or generalized pest-crop response data from research trials. Although not truly comprehensive, such informal EILs in combination with regular monitoring efforts and knowledge of pest biology and life history provide valuable tools for planning and implementing an effective IPM programme. However, because growers will generally want to act before a population reaches EIL, IPM programmes use the economic threshold (Figure 3). The concept of economic threshold implies that if the pest population and the resulting damage are low enough, it does not pay to take control measures. In practice, the term economic threshold has been used to denote the pest population level at which economic loss begins to occur and indicate the pest population level at which pest control should be initiated [50].

6. Monitoring activity in integrated management of H. armigera

In an IPM programme, pest managers use regular inspections, called monitoring, to collect the information they need to make appropriate decisions. A central idea in IPM is that a treatment is only used when pest numbers justify it, not as a routine measure. Keeping this in view, in IPM programmes, chemical control is applied only after visual inspection or monitoring devices indicate the presence of pests in that specific area, the pest numbers have exceeded the economic threshold (ET) and adequate control cannot be achieved with non-chemical methods within a reasonable time and cost. Therefore, it was considered that monitoring could reduce spraying costs by withholding a spray until a given threshold is reached [64].

For many years, light traps have been used to monitor Helicoverpa moth populations. Hartstack et al. [65] developed a model for estimating the number of moths per hectare from these light-trap catches, to evaluate the possible use of light traps for controlling Helicoverpa spp. Walden [66] presented the first comprehensive report on seasonal occurrence and abundance of the Helicoverpa zea (Boddie), based on light trap collections. Beckham [67] used light traps to index the populations of Helicoverpa spp. and reported that a significantly lower percentage of the Helicoverpa virescens (Fabricius) populations responded to black-light lamps in traps than did H. zea.

In the last few years, pheromone traps (containing virgin females or synthetic pheromones) have replaced light traps as moth-monitoring devices. These traps provide the pest manager with a convenient and effective tool for monitoring adult moth [68]. However, pheromone traps are highly efficient, simple to construct, inexpensive, and portable (requiring no power). Furthermore, only the single species for which the trap is baited is attracted and caught, making identification and counting quick and easy. As an added bonus, pheromone traps also detect spring emergence of moths 2 or 3 weeks earlier than light traps, which should give more precision to forecasts.

Several group of researchers made the comparison of indexing populations of Helicoverpa spp. in light traps versus pheromone traps. There results revealed that light trap catches may index seasonal fluctuation of populations more accurately than pheromone traps, however, pheromone traps are more sensitive to low populations early in the season and decline in efficiency with high populations late in the season [69].

There has been a considerable improvement into synthesis of the pheromones of Helicoverpa spp. in recent years. However, preliminary studies have already revealed that the catches in pheromone traps do not correlate very well with light-trap catches and field counts of the pest in all circumstances. In fact, trap catch data do not provide a quantitative threshold for intervention because a relationship between catch number and subsequent crop damage has proved to be lacking in most cases [70].

Egg count provides a better quantitative threshold for monitoring activity of H. armigera but egg desiccation, egg infertility or egg parasitism (biasing data) together with skill needed for field scouting, too often promote weak correlations between egg number and larval damage [71]. On the other hand, fruit inspection in the field has proved to be a valuable tool when develop against a number of fruit damaging pest species including H. armigera [72]. The major advantage of thresholds based on fruit inspection is that the short time between plant scouting for larval injury and fruit damage greatly increases correlation between both of these variables. Moreover, damaged fruit-count-based decision making may also be easily learned and carried out by growers [70].

Finally, we must now determine whether these pheromone traps are going to be of practical value in Helicoverpa management. For this, there is first a need to standardize trap design, pheromone dosage and release rates from the chosen substrate, and siting of the traps. As the next step, catches in these traps should be compared with other measures of Helicoverpa populations (light traps and actual counts of Helicoverpa eggs/larvae on the host plants in the same area). However, data from pheromone traps have already been shown to be valuable in some studies in the USA, where the data have been used in prediction models and have given useful information on the timing of infestations [64].

7. Importance of thermal modeling in successful implementation of integrated management of H. armigera

For decades, models have been an integral part of IPM. For instance, the use of models has helped pest managers decide how the agroecosystem should be changed to favor economy and conservation and not to favor pests. Moreover, models have allowed scientists to conduct simulated experiments when the conduct of those experiments would not have been possible. Furthermore, models have been used whenever scientists wanted to explore as well as understand the complexities of agroecosystems [26, 73, 74]. However, among the different types of models developed for implication of IPM programmes, forecasting models (especially thermal models) have a highlighted situation. Understanding the factors governing the pest development and implementing this knowledge into forecast models enable effective timing of interventions and increases efficacy and success of control measures [74]. For a pest manager, being able to predict abundance and distribution of a pest species, and its timing and level, is crucial to both strategic planning and tactical decision making. Thermal models, based on insect physiological timescales, have been relatively successful at predicting the timing of population peaks and are useful for timing sampling and control measures.

Temperature is a critical abiotic factor influencing the dynamics of insect pests and their natural enemies [75-77]. Temperature has a direct influence on the key life processes of survivorship, development, reproduction, and movement of poikilotherms and hence their population dynamics [78]. The importance of predicting the seasonal occurrence of insects has led to the formulation of many mathematical models that describe developmental rates as a function of temperature [79]. Thermal models have been developed for insect pests to predict emergence of adults from the overwintering generation, eclosion of eggs, larval and pupal development, and generation time. These models, all based on a linear relationship between temperature and developmental rate, have been used with varying degrees of success to time pesticide application for pest control [80]. However, linear approximation enables the estimation of lower temperature thresholds (T_min) and thermal constants (K) within a limited temperature range and to describe the developmental rate more realistically and over a wider temperature range, several nonlinear models have been applied [74, 76]. These nonlinear models provide value estimates of lower and upper temperature thresholds and optimal temperature for development of a given stage.

Several studies have been conducted on the effects of temperature on developmental time of H. armigera reared on host plant materials or artificial diets [81, 82]. In a recent study by Mironidis and Savopoulou-Soultani [83], a comprehensive analysis of survivorship and development rates at all life stages of H. armigera reared under constant and corresponding alternating temperatures regimes was performed (some of the most important results are listed in Tables 3 and 4).

The results obtained by Mironidis and Savopoulou-Soultani [83] revealed that over a wide constant thermal range (15-27.5^°C) total survivorship is stable and apparently not affected by temperature. Below 15^°C, survivorship decreased rapidly, reached zero at 12.5^°C. At higher temperatures, survivorship also decreased very quickly above 28^°C and fell to zero at 40^°C. Furthermore, their results showed that H. armigera, when reared at constant temperatures, could not develop from egg to adult stage (capable of egg production) out of the temperature range of 17.5-32.5^°C. Nevertheless, alternating temperatures allowed H. armigera to complete its life cycle over a much wider range, 10-35^°C, compared with constant temperatures.

In another study, temperature-dependent development of H. armigera was studied in the laboratory conditions at eight constant temperatures (15, 17.5, 20, 22.5, 25, 30, 32.5 and 35^°C) [Adigozali and Fathipour, unpublished data]. In this study, two linear (Ordinary linear and Ikemoto and Takai) and 9 nonlinear (Briere-1, Briere-2, Lactin-1, Lactin-2, Polynomial, Kontodimas-16, Analytis-1, Analytis-2 and Analytis-3) models were fitted to describe development rate of H. armigera as a function of temperature. The lower temperature threshold and thermal constant of different life stages of H. armigera estimated by linear models are listed in Table 5. The obtained results revealed that both models have acceptable accuracy in prediction of T_min and K for different life stages of H. armigera [Adigozali and Fathipour, unpublished data].

According to results obtained by Adigozali and Fathipour [unpublished data], of the nonlinear models fitted, the Lactin-2, Lactin-2, Polynomial, Polynomial and Briere-2 models were found to be the best for modeling development rate of egg, larva, pre-pupa, pupa and total immature stages of H. armigera, respectively (Table 6). However, estimated values for crucial temperatures of different life stages of H. armigera by Adigozali and Fathipour [unpublished data] conflict with those reported by Mironidis and Savopoulou-Soultani [83] (Tables 3-6). Some possible reasons for these disagreements are: physiological difference depending on the food quality, genetic difference as a result of laboratory rearing and techniques/equipment of the experiments. In general, the results obtained from constant temperature experiments are often not applicable directly to the field where pests are subjected to diurnal variation of temperature and such information need to be validated under fluctuating temperatures before using for predictive purpose in the field. Finally, such data provide fundamental information describing development of H. armigera, when this information to be used in association with other ecological data may be valuable in integrated management of this noctuid pest in soybean cropping systems.

8. Strategies for integrated management of H. armigera

8.3. Cultural control

Cultural control is the deliberate manipulation of the cropping or soil system environment to make it less favorable for pests or making it more favorable for their natural enemies. Many procedures such as tillage, host plant resistance, planting, irrigation, fertilizer applications, destruction of crop residues, use of trap crops, crop rotation, etc. can be employed to achieve cultural control. Early workers used cultural practices as the mainstay of their insect control efforts. Newsom [145] pointed out that the rediscovery of the importance of cultural control tactics has provided highly effective components of pest management systems. Although some cultural practices have a noticeable potential in integrated management, use of some cultural controls is not universally beneficial. For example, providing nectar sources for beneficial insects may also provide nectar sources for pests.

8.3.1. Uncultivated marginal areas and abundance of natural enemies

Monoculture in modern agriculture, especially in annual crops, often discriminates against natural enemies and favors development of explosive pest populations. According to Fye [146], management of naturally occurring populations of insect predators may depend on knowledge of the succession of winter weeds and crops that provide natural hosts for food and shelter. The results obtained by Whitcomb and Bell [147] revealed that very few predators move directly from overwintering sites to field and pass one or two generations on weeds in the uncultivated marginal areas. In a 2-year study on the abundance of predators of Helicoverpa spp. in the various habitats in the Delta of Mississippi, predator populations in all the marginal areas were observed to be much higher than in the more homogeneous areas such as soybean fields.

8.3.2. Intercropping and its effect on natural enemies

Dispersal from target area often reduces the effectiveness of natural enemies especially in augmentation programmes. To minimize this shortcoming, provision of supplemental resources such as food to maintain, arrest or stimulate the released natural enemy could provide mechanisms for managing parasitoids and predators [148]. Accordingly, some environmental manipulation could affect efficiency of a natural enemy during biological control programmes of Helicoverpa spp. Roome [149] suggested that increasing plant diversity in cropping systems by intercropping crops carrying nectars could enhance effectiveness of natural enemies. When different host plants of H. armigera are interplanted, population of H. armigera and its natural enemies on a crop are influenced by neighboring crops, both directly and indirectly. Direct influences include preference for one crop over the other by ovipositing moths and the movement of larvae and natural enemies between interplanted crops. Indirect influences arise when H. armigera infestation on one crop is influenced by the population build-up or mortality level on neighboring crops [113].

8.3.3. Ploughing and early planting effects on Helicoverpa populations

An alternative and often complementary strategy for management of H. armigera is the control of overwintering pupae through the practice of pupae busting which has been used in several cropping areas. Ploughing in late maturing crops in winter increase the mortality of any pupae formed in cropland by exposing them to heat and predation. The other cultural control method is early planting which avoids the seasonal peaks of population thereby avoiding very heavy larval infestations and reducing the overwintering population [150].

8.3.4. Trap crops and management of H. armigera

The recent resurgence of interest in trap cropping as an IPM tool is the result of concerns about potential negative effects of pesticides. Prior to the introduction of modern synthetic insecticides, trap cropping was a common method of pest control for several cropping systems [150]. Trap crops have been defined as “plant stands that are, per se or via manipulation, deployed to attract, divert, intercept and retain targeted insects or the pathogens they vector in order to reduce damage to the main crop” [151, 152]. Trap cropping is essentially a method of concentrating a pest population into a manageable area by providing the pest with an area of a preferred host crop and when strategically planned and managed, can be utilized at different times throughout the year to help manage a range of pests. For example, spring trap crops are designed to attract H. armigera as they emerge from overwintering pupae. A trap crop, strategically timed to flower in the spring, can help to reduce the early season buildup of H. armigera in a district. Spring trap cropping, in conjunction with good Helicoverpa control in crops and pupae busting in autumn, is designed to reduce the size of the local Helicoverpa population. On the other hand, summer trap cropping has quite a different aim from that of spring trap cropping. A summer trap crop aims to draw Helicoverpa away from a main crop and concentrate them in another crop. Once concentrated into the trap crop, the Helicoverpa larvae can be controlled. Finally, in addition to diverting insect pests away from the main crop, trap crops can also reduce insect pest populations by enhancing populations of natural enemies within the field. For example, a sorghum trap crop used to manage H. armigera, also increases rates of parasitism by Trichogramma chilonis Ishii [153]. However, to avoid creating a nursery for H. armigera, the trap crop must be destroyed prior to the pupation of the first large H. armigera larvae. Furthermore, to protect the trap crop from large infestations of Helicoverpa spp. spraying may be required.

8.3.4.1. Trap crops and push-pull strategy in integrated management of H. armigera

The term push-pull was first applied as a strategy for IPM by Pyke et al. in Australia in 1987 [154]. They investigated the use of repellent and attractive stimuli, to manipulate the distribution of Helicoverpa spp. in cotton fields. Push-pull strategies involve the “behavioral manipulation of insect pests and their natural enemies via the integration of stimuli that act to make the protected resource unattractive or unsuitable to the pests (push) while luring them toward an attractive source (pull) from where the pests are subsequently removed”. The strategy is a useful tool for integrated pest management programmes reducing pesticide input [155].

In plant-based systems, naturally generated plant stimuli can be exploited using vegetation diversification, including trap cropping and these crops have a crucial role as one of the most important stimuli for pull components. The host plant stimuli responsible for making a particular plant growth stage, cultivar, or species naturally more attractive to pests than the plants to be protected can be delivered as pull components by trap crops [155]. However, the relative attractiveness of the trap crop compared with the main crop, the ratio of the main crop given to the trap crop, its spatial arrangement (i.e., planted as a perimeter or intercropped trap crop), and the colonization habits of the pest are crucial to success and require a thorough understanding of the behavior of the pest [156].

In the case of Helicoverpa spp. on cotton in Australia, the potential of combining the application of neem seed extracts to the main crop (push) with an attractive trap crop, either pigeonpea or maize (pull), to protect cotton crops from H. armigera and H. punctigera has been investigated [153]. Trap crops, particularly pigeonpea, reduced the number of eggs on cotton plants in target areas. In trials, the push-pull strategy was significantly more effective than the individual components alone. The potential of this strategy was supported by a recent study in India. Neem, combined with a pigeonpea or okra trap crop, was an effective strategy against H. armigera [157].

8.3.5. Host plant resistance

Plants that are inherently less damaged or infested by insect pests in comparable environments are considered resistant [158]. Host plant resistance (HPR) is recognized as the most effective component of IPM and has been considered to replace broad spectrum insecticides. A resistant host plant provides the basic foundation on which structures of IPM for different pests can be built [159]. The advantage that farmers gain in using cultural control with susceptible cultivars would certainly be enhanced when combined with the resistant cultivars. Adkisson and Dyck [160] stated that resistant cultivars are highly desirable in a cultural control systems designed to maintain pest numbers below the economic injury level (EIL) while preserving the natural enemies. Besides, even low level of resistance is important because of reduction of the need for other control measures in the crop production systems. Furthermore, with low value crops, where chemical control is not economical, the use of HPR may be the only economic solution to a pest problem [46]. However, the most advantageous features of HPR are the following: (a) cheapest technology; (b) easiest to introduce; (c) is specify to one or several pests; (d) cumulative effectiveness makes high level of resistance unnecessary; (e) is persistence; (f) can easily be adopted into normal farm operations; (g) is compatible with other control tactics in IPM such as chemical, biological and cultural control; (H) reducing the costs to the growers and (I) it is not detrimental to the environment [160, 161].

Generally, the phenomena of resistance are based on heritable traits. However, some traits fluctuate widely in different environmental conditions. Accordingly, plant resistance may be classified as genetic, implying the traits that are under the primary control of genetic factors; or ecological, implying the traits that are under the primary control of environmental factors. Host plants with genetic resistance to insect pest are very pleasure in IPM programmes [159]. This type of resistance is subdivided into two categories including induced and constitutive resistance. If biotic and abiotic environmental factors reduces insect fitness or negatively affects host selection processes, the effect is called induced resistance. On the other hand, constitutive resistance involves inherited characters whose expression, although influenced by the environment, is not triggered by environmental factors [41]. However, genetic resistance to insect pest could be results of three distinct mechanisms including antixenosis, antibiosis and tolerance. Antixenosis is the resistance mechanism employed by plant to deter or reduce colonization by insect. Antibiosis is the resistance mechanism that operates after the insect have colonized and started utilizing the plant. This mechanism could affect growth, development, reproduction and survivorship of insect pests and therefore, is the most important mechanism for IPM purposes. Tolerance is a characteristic of some plants that enable them to withstand or recover from insect damage [159].

Plant resistance to insect pests can be inherited in two distinct ways including vertical (monogenic) and horizontal (polygenic) resistance. Vertical resistance is generally controlled by a single gene, referred as R-gene. These R-genes can be remarkably effective in suppression of pest populations and can confer complete resistance. However, each R-gene confers resistance to only one insect pest and thus, depending on the pest species in specific area a cultivar may appear strongly resistant or completely susceptible. Horizontal resistance is also known as polygenic resistance due to this type of resistance is controlled by many genes. Unlike vertical resistance, horizontal resistance generally does not completely prevent a plant from becoming damaged. For insect pests, this type of resistance may slow the infection process so much that the pest does not grow well or spread to other plants. However, because of the large number of genes involved, it is much more difficult to breed cultivars with horizontal resistance to insect pests [162].

8.3.5.1. Plant resistance to H. armigera

To evaluate plant resistance to H. armigera several researchers evaluate population growth parameters of this pest on different host plants. Table 11 presents the main finding of several studies regarding to population growth parameters of this noctuid pest on different crop plants. However, information about population growth parameters of H. armigera on different host plants could reveal the suitability of one crop for this noctuid pest than other host plants.

In the case of H. armigera on different soybean cultivars, resistance of some cultivars to this noctuid pest was evaluated under laboratory conditions [6]. Results obtained by these researchers showed that various soybean cultivars differed greatly in suitability as diets for H. armigera when measured in terms of development, survivorship, life table parameters and nutritional indices. Fathipour and Naseri [11] presented detailed information regarding evaluation of soybean resistance to H. armigera in a book chapter entitled “ Soybean cultivars affecting performance of Helicoverpa armigera (Lepidoptera: Noctuidae) ”. This chapter is now freely available on the INTECH website at http://www.intechopen.com/articles/show/title/soybean-cultivars-affecting-performance-of-helicoverpa-armigera-lepidoptera-noctuidae-. However, a review of literature showed that a little information regarding resistance evaluation in field conditions is available and hence, for sustainable management of H. armigera in soybean cropping systems more attention should be devoted to fill this gap.

Crop	Experimental conditions		R 0 (female offspring)	rm (day -1 )	T (day)	DT (day)	References
	Temperature °C	Diet type
Canola (10) a	25	artificial b	157.4 - 331.5	0.153 - 0.179	31.10 - 36.10	3.80 - 4.50	[12]
Chickpea	25	artificial	359.67	0.161	33.28	4.27	[c]
Chickpea (4)	25	artificial	59.49 - 195.00	0.140 - 0.205	24.11 - 30.36	3.40 - 4.88	[d]
Common bean	27	leaf and fruit	19.50	-	-	-	[163]
Corn	25	artificial	203.14	0.130	40.56	5.29	[84]
Corn	25	artificial	147.40	0.126	37.90	5.62	[c]
Corn	27	leaf and fruit	44.50	-	-	-	[163]
Corn		cob	50.1	0.0853	46.6	-	[164]
Cotton	27	leaf and fruit	117.60	-	-	-	[163]
Cowpea	25	artificial	228.5	0.131	34.88	5.28	[e]
Cowpea	25	artificial	365.66	0.180	31.62	3.92	[c]
Cowpea	25	artificial	250.60	0.178	30.38	3.85	[d]
Hot pepper	27	leaf and fruit	5.10	-	-	-	[163]
Navy bean	25	artificial	294.28	0.164	32.31	4.14	[c]
Pearl millet	-	-	374.01	0.142	-	-	[165]
Soybean	25	artificial	239.69	0.161	33.28	4.23	[c]
Soybean (10)	25	artificial	16.00 - 270.00	0.084 - 0.114	36.72 - 45.28	6.08 - 8.10	[6]
Soybean (13)	25	leaf and pod	89.35 - 354.92	0.132 - 0.185	28.85 - 36.61	3.75 - 5.23	[166]
Sunflower	-	-	143.77	0.113	-	6.11	[167]
Tobacco	27	leaf	11.70	-	-	-	[163]
Tomato	27	leaf and fruit	9.5	-	-	-	[163]
Tomato (10)	25	leaf and fruit	1.36 - 62.32	0.008 - 0.137	30.26 - 37.34	5.06 - 27.41	[f]

Table 11.

Effects of different host plants on some population growth parameters of Helicoverpa armigera

a Digits in parentheses show number of tested cultivars.

b Artificial diet based on the seed of host plant.

[c] Baghery and Fathipour, unpublished data; [d] Fallahnejad-Mojarrad and Fathipour, unpublished data; [e] Adigozali and Fathipour, unpublished data; [f] Safuraie and Fathipour, unpublished data.

8.3.5.2. Integration of HPR with other control measures and possible interactions

Several studies have been performed to investigate the possible interactions of host plant resistance to insect with other control measures. Results obtained revealed both incompatibility and compatibility of HPR in an integrated programme. However, in IPM programmes there can be three types of interactions between different control measures including additive, synergistic, and antagonistic. Additive interaction means the combined effect of two control measures is equal to the sum of the effect of the two measures taken separately. In synergistic interaction, the effect of two control measures taken together is greater than the sum of their separate effect. Finally, antagonistic interaction means that the effect of two control measures is actually less than the sum of their effects taken independently of each other. However, despite importance of such information in IPM, a little knowledge in this field is available.

8.3.5.2.1. HPR and biological control

Plant resistance and biological control are the key components of IPM for field crops and generally considered to be compatible. Insects feeding on HPR commonly experience retarded growth and an extended developmental period. Under field conditions, such poorly developed insect herbivores are more vulnerable to natural enemies for a longer period and the probability of their mortality is higher. Insect herbivores that develop slowly on resistant cultivars are more effectively regulated by the predators than those developed robustly on the susceptible cultivars. This is because the predator has to consume more small-sized prey to become satiated [168]. Wiseman et al. [169] found that populations of Orius insidiosus (Say), a predator on H. zea larvae, were higher on the resistant corn hybrids than on the susceptible ones, an indication of the compatibility of HPR and the predator.

van Emden and Wearing [170] developed a simple model on the interaction of HPR with natural enemies. On the basis of this model, the reduced rate of multiplication of aphids on moderator resistant cultivars should magnify the plant resistance in the presence of natural enemies (Figure 4). Danks et al. [123] stated that a number of predators and parasitoids attack early instars of Helicoverpa sp. on soybean and tobacco but generally do not attack bigger larvae. But because of moderately resistance of host plants, the larvae remain in early instars for longer period and are more likely to be parasitized. However, such interactions are valuable phenomenon in the development of practical IPM.

However, there are instances of deleterious interactions between HPR and biological control which could be more important in the IPM. Sometimes, plant morphological traits and plant defense chemicals had adverse effects on the natural enemies. For example, certain genotypes of tobacco with glandular trichomes have been shown to severely limit the parasitization of the eggs of Manduca sexta (Linnaeus) by Trichogramma minutum Riley [171]. Resistant eggplant cultivars to Tetranychus urticae Koch adversely affected biological performance of Typhlodromus bagdasarjani Wainstein and Arutunjan [22]. These researchers stated that antibiotic compounds in resistant cultivars are also toxic for T. bagdasarjani and concentrated compounds in the T. urticae reduced effectiveness of this predator. Barbour et al. [172] found that methylketone adversely affected the egg predators of H. zea that fed on the foliage of wild tomato. However, plant breeders can sometimes manipulate plant traits to promote the effectiveness of natural enemies [159]. For example, a reduction in trichomes density of cucumber leaves significantly increase effectiveness of Encarsia formosa Gahan on the greenhouse whitefly [173].

8.3.5.2.2. HPR and insect pathogens

Schultz [174] hypothesized that the effectiveness of insect pathogens may be reduced or improved, depending upon plant chemistry and variability of plant resistance. Interactions among HPR, herbivores and their pathogens can alter pathogenicity of B. thuringiensis on M. sexta [175]. Furthermore, insect susceptibility to the entomopathogenic fungus can also be affected by HPR. Felton and Duffey [176] reported the possible incompatibility of resistant cultivars of tomato with NPV control of H. zea. These researchers revealed that chlorogenic acid in resistant cultivars of tomato is oxidized by foliar phenol oxidases and generated components binds to the occlusion bodies of NPV, thereby decreasing its pathogenicity against H. zea.

8.3.5.2.3. HPR and chemical control

There is usually a beneficial interaction between HPR and chemical control. Because the toxicity of an insecticide is a function of insect bodyweight, it is expected that a lower concentration is needed to control insect feeding on a resistant cultivar than those feeding on a susceptible ones [177]. van Emden [178] pointed out that there is a potentially useful interaction in the possibility of using reduced dosses of insecticide on resistant cultivar, when spray is needed. This theory relies on the selectivity of the insecticide in favor of natural enemies as dose rate is reduced (Figure 5). However, it appears that even in the presence of small levels of plant resistance, insecticide concentration can be reduced to one-third of that required on a susceptible cultivar [178]. This reduced use of pesticide not only benefits the agroecosystems and natural enemies but also results in lower pesticide residues in the human food chain. Accordingly, Wiseman et al. [179] showed that even one low-dose application of insecticide to the resistant hybrid of corn gave an H. zea control equal to that achieved with seven applications to the susceptible hybrid. Fathipour et al. [25] compared the chemical control of Eurygaster integriceps Put. on resistant and susceptible cultivars of wheat. The results obtained by these researchers revealed that the sensitivity of 4th and 5th instar nymphs and new adults of E. integriceps to insecticide Fenitrothion was enhanced on resistant cultivar compared with those on susceptible cultivar. Accordingly, the LC₅₀ of insecticide on susceptible and resistant cultivars for 4th instar nymphs was 42.16 and 33.48, for 5th instar nymphs was 147.03 and 114.01 and for new adults was 303.35 and 227.88 ppm, respectively.

However, in addition to negative effects on insect bodyweight, repellent chemicals or morphological traits of resistant cultivars may be effective in reduction of insecticide spray. Repellency is to be effective in limiting pest damage to treated crops and it may also keep the pests away from their suitable resources and therefore cause indirect mortality or lower fecundity. Furthermore, repellency is equivalent to using low doses of insecticides along with the repellent properties of the host plant [159].

9. Biotechnology in IPM

Recent advantage in biotechnology, particularly cellular and molecular biology have opened new avenues for developing resistant cultivars. From this diagnostic perspective, molecular techniques are likely to play an important role in identification, quantification and genetic monitoring of pest populations [183]. The diagnostic information is a necessary prerequisite for implementing rational control strategy. Appropriate molecular techniques can be employed to study the species composition of the pest population and to identify strains, races or biotypes of the same species.

Another important application of molecular diagnostic techniques is for monitoring both the presence and frequency of genes of particular interest. For example, genes for resistance to a specific class of pesticides and their frequency in particular region can be assessed. Such information is very useful for designing and implementing rational pest management strategies [159].

The most important application of biotechnology in IPM is the introduction of novel genes for resistance into crop cultivars through genetic engineering. HPR is a highly effective management option, but cultivated germplasm has only low to moderate resistance levels to some key pests. Furthermore, some sources of resistance have poor agronomic characteristics. On the other hand, development of cultivars with enhanced resistance will strengthen the control of H. armigera in different cropping systems. Therefore, we need to make a concerted effort to transfer pest resistance into genotypes with desirable agronomic and grain characteristics. Recent achievements of genetics and molecular biology have been widely implemented into breeding new crop cultivars and brought in many various traits absent from parent species and cultivars. Furthermore, new progress in biotechnology makes it feasible to transfer genes from totally unrelated organisms, breaking species barriers not possible by conventional genetic enhancement. Today, transgenic plants expressing insecticidal proteins from the bacterium B. thuringiensis, are revolutionizing agriculture. Bacillus thuringiensis has become a major insecticide because genes that produce B. thuringiensis toxins have been engineered into major crops grown on 11.4 million ha worldwide (including soybean, cotton, peanut, tomato, tobacco, corn and canola). These crops have shown positive economic benefits to growers and reduced the use of other insecticides. Genetically engineered cottons expressing delta-endotoxin genes from B. thuringiensis offer great potential to dramatically reduce pesticide dependence for control of Helicoverpa spp. and consequently offer real opportunities as a component of sustainable and environmentally acceptable IPM systems [16]. Certainly, for sustainable management of H. armigera in soybean cropping systems, such soybean resistant cultivars could play pivotal role. Therefore, to achieve this goal, much works should be conducted in breeding new soybean cultivars expressing Bt toxins against H. armigera.

The potential ecological and human health consequences of Bt crops, including effects on nontarget organisms, food safety, and the development of resistant insect populations, are being compared for Bt plants and alternative insect management strategies. However, Bt plants were deployed with the expectation that the risks would be lower than current or alternative technologies and that the benefits would be greater. Based on the data to date, these expectations seem valid [16]. The major challenge to sustainable use of transgenic Bt crops is the risk that target pests may evolve resistance to the B. thuringiensis toxins. Helicoverpa armigera is a particular resistance risk having consistently developed resistance to synthetic pesticides in the past [21]. For this reason a pre-emptive resistance management strategy was implemented to accompany the commercial release of transgenic cultivars. The strategy, based on the use of structured refuges to maintain susceptible individuals in the population, seeks to take advantage of the polyphagy and local mobility of H. armigera to achieve resistance management by utilizing gene flow to counter selection in transgenic crops. However, refuge crops cannot be treated with Bt sprays, and must be in close proximity to the transgenic crops (within 2 km) to maximize the chance of random mating among sub-populations [184].

10. Tritrophic interactions and its manipulation for IPM

Plant quality can affect herbivore fitness directly (as food of herbivores) and indirectly (by affecting foraging cues for natural enemies) [12, 23]. Until recently, there has been a tendency by those involved in IPM to be principally concerned with effects on herbivores or interactions between just two trophic levels [185]. However, interest in the importance of interactions among the three or four trophic levels (Figure 6) that characterize most natural systems and agroecosystems has been increased rapidly during the last two decades [26].

It is interesting that many traditional cultural practices exert their effects through complex multitrophic interactions, but it is exactly this complexity that makes such systems difficult to assess experimentally or validate conclusively across a broad range of environments. For example, it has been demonstrated that toxic secondary compounds in an herbivore diet may affect development, survivorship, morphology and size of its natural enemies. This effect of poor-quality plants can thus indirectly lead to poor-quality natural enemies [186].

As knowledge of interactions across multitrophic systems both in nature and in agroecosystems expands, researchers and pest management practitioners are beginning to find ways of manipulating interactions across different trophic levels in order to develop more sustainable approaches to pest management. Accordingly, population ecologists are actively debating the relative importance of bottom-up (resource-driven) and top-down (natural enemy-driven) processes in the regulation of herbivores populations [22, 187, 188]. However, there are a number of key areas where manipulation of host plant-pest-natural enemy interactions could provide substantial benefits in pest management systems (manipulation of host plant quality, allelochemicals and crop diversification and genetic manipulation of insect) [26].

For many years, there was a widely held view that HPR should be seen as an integral component of IPM programmes, but it has been demonstrated that HPR is by no means always compatible with biological control [178]. The significant and growing evidence from fundamental research in allelochemically mediated interactions hold substantial promise with regard to the development of novel IPM techniques. Allelochemicals mediated interactions in insect-host plant relationship have been recognized as the most important factors in the successful establishment of an insect species on a crop [189]. Furthermore, allelochemicals produced by plants also have considerable influence on the prey/host selection behavior of natural enemies, so that plants, herbivores, and natural enemies are interconnected through the well-knit array of chemicals. The host plant volatiles play a key role in attracting/repelling or retaining the natural enemies, thereby causing considerable changes in pest populations on different plant cultivars [190]. Hare [191] cited 16 studies where interactions between resistant cultivars and natural enemies (parasitoids) were studied and the outcomes show a spectrum of interactions, ranging from synergistic, to additive, to none apparent through to disruptive or antagonistic. Negative interactions can occur due to the presence of secondary chemicals that are ingested or sequestered by natural enemies feeding on hosts present on resistant or partially resistant plants [192]. For example, specific toxic components in partially resistant soybean plants can be particularly problematic in this regard [193]. In addition to allelochemicals, morphological traits of host plants such as trichome density and color complexion can affect insect fitness and effectiveness of its natural enemies. It was observed that plant cultivars were sufficiently differing in their trichome density and color complexion which were considered as main resource of variations in rate of parasitism on different plant cultivars. Cotton cultivars with low density of hairs on the upper leaf surface and high hair density on the lower leaf surface help in reduction of pest incidence [194]. The rates of parasitism were negatively associated with trichome density as revealed by Mohite and Uthamasamy [195]. In another study, Asifulla et al. [196] noticed higher parasitism by T. chilonis on H. armigera eggs in glabrous cotton species compared to hairy types.

In conclusion, as a novel strategy for IPM programmes, well understanding of multitrophic interactions is critical to develop the sustainable, less pesticide-dependent or pesticide-free pest management programmes [197]. In the interest of agricultural sustainability, tritrophic manipulation, as a distinct approach to biological or cultural control, is probably to be prioritized increasingly by both researchers and those responsible for the development and practical implementation of pest management programmes. This process will be facilitated if improvements in the understanding of crop-pest-natural enemy evolution and their interactions are achieved [26, 197]. Information in this regard are essential in finding out what role the plant play in supporting the action of natural enemies and how this role could be manipulated reserving the natural enemies.

11. Conclusion

Helicoverpa armigera represents a significant challenge to soybean cropping systems in many parts of the world and remain the target for concentrated management with synthetic insecticides. However, the extensive use of insecticides for combating H. armigera populations is of environmental concern and has repeatedly led to the development of resistance in this pest as well as the deleterious effects on nontarget organisms and environment. The common trend towards reducing reliance on chemicals for control of insect pests in agriculture renewed worldwide interest in integrated pest management (IPM) programmes and it seems that in most areas the aim must be integrated management, particularly on crops such as soybean where H. armigera is part of a diverse pest complex. Accordingly, in this chapter we attempt to introduce basic elements for implementation of sustainable management of H. armigera. For this, we reviewed the main findings of different researchers and in some cases present our data. However, our findings revealed that for successful management of H. armigera, more attention should be devoted to some basic information such as monitoring efforts, forecasting activities and economic thresholds. In addition, more studies are needed to evaluate potential of novel control measures including selective insecticides and sublethal doses, HPR and genetically modified soybean cultivars and microbial pathogens (especially commercial formulations of B. thuringiensis and NPV) for control of this noctuid pest. However, for future outlook of integrated management of H. armigera in soybean cropping systems, the development and use of resistant cultivars will play a crucial role. In other words, more works should be conducted to evaluate resistance of soybean cultivars to H. armigera in field conditions. Moreover, a further need is to evaluate tritrophic interactions among the soybean cultivars, H. armigera and its natural enemies and new studies should be included to evaluate such interactions. However, the information gathered in the current chapter could be valuable for integrated management of H. armigera in soybean cropping systems.