**8. Strategies for integrated management of** *H. armigera*

#### **8.1. Chemical control**

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

*gera* [Adigozali and Fathipour, unpublished data].

by Ordinary linear and Ikemoto and Takai models.

**Stage Model Lower temperature threshold**

Egg Ordinary linear 8.61 47.85

Larva Ordinary linear 6.07 367.65

Pre-pupa Ordinary linear 11.70 42.55

Pupa Ordinary linear 14.29 132.28

Total immature stages Ordinary linear 10.39 561.78

**Table 5.** Lower temperature threshold and thermal constant of different life stages of *Helicoverpa armigera* estimated

According to results obtained by Adigozali and Fathipour [unpublished data], of the nonlin‐ ear models fitted, the Lactin-2, Lactin-2, Polynomial, Polynomial and Briere-2 models were found to be the best for modeling development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estimated values for crucial temperatures of different life stages of *H. armigera* by Adigozali and Fathipour [unpublished data] conflict with those reported by Mironidis and Savopoulou-Soultani [83] (Tables 3-6).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/equip‐ ment of the experiments. In general, the results obtained from constant temperature experi‐

C) [Adigozali and Fathipour, unpublished data].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, Pol‐ ynomial, Kontodimas-16, Analytis-1, Analytis-2 and Analytis-3) models were fitted to de‐ scribe development rate of *H. armigera* as a function of temperature. The lower temperature threshold and thermal constant of different life stages of *H. armigera* estimat‐ ed by linear models are listed in Table 5. The obtained results revealed that both models have acceptable accuracy in prediction of *Tmin* and *K* for different life stages of *H. armi‐*

(*Tmin***°C**)

Ikemoto and Takai 9.52 44.60

Ikemoto and Takai 7.18 343.00

Ikemoto and Takai 10.80 46.70

Ikemoto and Takai 13.20 150.00

Ikemoto and Takai 10.30 566.00

**Thermal constant (K DD)**

35°

244 Soybean - Pest Resistance

Historically pest management on many crops has relied largely on synthetic pesticides and in intensive cropping systems, pesticides are main components of pest management pro‐ grammes that represents a significant part of production costs [84]. However, chemical con‐ trol is still the most reliable and economic way of protecting crops from pests. Beside, over reliance on chemical pesticides without regarding to complexities of the agroecosystem is not sustainable and has resulted in many problems like environment pollution, secondary pest outbreak, pest resurgence, pest resistance to pesticides and hazardous to human health. Furthermore, over dependence on chemical pesticides has also resulted in increased plant protection, thus leading to high cost of production.

Insecticide treatments, whether or not included in IPM programmes, are currently indis‐ pensable for the control of *H. armigera* in almost all cropping systems around the world [85], so, this pest species has been subjected to heavy selection pressure. Some of the synthetic insecticides currently used for controlling this pest are indoxacarb, methoxyfe‐ nozide, emamectin benzoate, novaluron, chlorfenapyr, imidacloprid, fluvalinate, endosul‐ fan, spinosad, abamectin, deltamethrin, cypermethrin, lambda-cyhalothrin, carbaryl, methomyl, profenofos, thiodicarb and chlorpyrifos [21, 85-87]. Because of indiscriminate use of these chemicals to minimize the damage caused by *H. armigera*, however, it has developed high levels of resistance to conventional insecticides such as synthetic pyreth‐ roids, organophosphates and carbamates [88].

#### *8.1.1. Sustainable use of insecticides and obtaining maximum benefits from their application*

However, selection for resistance to pesticides will occur whenever they are used [87]. After a pest species develops resistance to a particular pesticide, how do you control it? One meth‐ od is to use a different pesticide, especially one in a different chemical class or family of pes‐ ticides that has a different mode of action against the pest. Of course, the ability to use other pesticides in order to avoid or delay the development of resistance in pest populations de‐ pends on the availability of an adequate supply of pesticides with differing modes of action. This method is perhaps not the best solution, but it allows a pest to be controlled until other management strategies can be developed and brought to bear against the pest [21]. Howev‐ er, suggestions will now be made as to how the maximum benefit can be obtained from the unique properties of the insecticides.

velopment of insecticide resistance, insecticide at low concentrations may be used in

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The most interesting component of IPM for many people is biological control. It is also the most complicated as there is a diverse range of species and types of predators, parasitoids and pathogens. The value of biological control agents in integrated pest management is be‐ coming more apparent as researches are conducted. Natural enemies clearly play an impor‐ tant role in integrated management of *Helicoverpa* spp., particularly in low value crops where they may remove the need for any chemical intervention. Likewise in high value crops (such as cotton and tomato) beneficial species provide considerable benefit but are un‐ able to provide adequate control alone, especially in situations where migratory influxes of *Helicoverpa* result in significant infestations [14]. However, although parasitoids and preda‐ tors cannot be relied upon for complete control of *H. armigera* in unsprayed area, knowledge about their role in cropping systems where *H. armigera* is an important pest is an essential

Before using a natural enemy in a biological control programme, it is essential to know about its efficiency. However, study of demographic parameters and foraging behaviors of natural enemies is the reliable criteria for assessment of their efficiency. Among the demo‐ graphic parameters, intrinsic rate of increase (*rm*) is a key parameter in the prediction of pop‐ ulation growth potential and has been widely used to evaluate efficiency of natural enemies [22, 76, 98, 99]. In addition to demographic parameters, another important aspect for assess‐ ing the efficiency of natural enemies is the study of their foraging behaviors including func‐ tional, numerical and aggregation responses, mutual interference, preference and switching [100-110]. Such information is essential to interpret how the natural enemies live, how they influence the population dynamics of their hosts/preys, and how they influence the struc‐

The most common parasitoids that contribute to mortality of *Helicoverpa* spp. are shown in Table 7. Studies on the effects of parasitoids in biological control of *H. armigera* fo‐ cused on monitoring parasitism of eggs and larvae. In Botswana, parasitism of larvae collected from different crops averaged up to 50% on sorghum, 28% on sunflower, 49% on cowpeas and 76% on cotton [112]. These results showed that parasitoids had a crucial role in management of *H. armigera*. However, this level of parasitism is higher when compared to the results from East Africa where the level of parasitism was generally low (<5%) or absent [113]. Surveys made of the parasitoid of *Helicoverpa* spp. in cotton fields of Texas by Shepard and Sterling [114] showed that larval parasitoids accounted for ap‐ proximately 7% regulation of *Helicoverpa* spp. Such investigations highlight importance of parasitoids in integrated management of *H. armigera* in different cropping systems

combination with biological control.

component in the development of integrated management.

ture of the insect communities in which they exist [111].

**8.2. Biological control**

*8.2.1. Parasitoids*

around the world.


velopment of insecticide resistance, insecticide at low concentrations may be used in combination with biological control.

#### **8.2. Biological control**

*8.1.1. Sustainable use of insecticides and obtaining maximum benefits from their application*

unique properties of the insecticides.

246 Soybean - Pest Resistance

*Helicoverpa* attack [91].

However, selection for resistance to pesticides will occur whenever they are used [87]. After a pest species develops resistance to a particular pesticide, how do you control it? One meth‐ od is to use a different pesticide, especially one in a different chemical class or family of pes‐ ticides that has a different mode of action against the pest. Of course, the ability to use other pesticides in order to avoid or delay the development of resistance in pest populations de‐ pends on the availability of an adequate supply of pesticides with differing modes of action. This method is perhaps not the best solution, but it allows a pest to be controlled until other management strategies can be developed and brought to bear against the pest [21]. Howev‐ er, suggestions will now be made as to how the maximum benefit can be obtained from the

**a.** Given the decreasing susceptibility of older caterpillars than early ones, it is important to use the insecticides early. Not only young larvae of *H. armigera* are more susceptible,

**b.** To decide whether the infestation by a pest has reached the economic threshold and an insecticide is required, more attention should be devoted to monitoring programmes. On crops where *Helicoverpa* is the main target, synthetic insecticides should not be used

**c.** It is best to be used selective insecticides, a practice that will help to conserve beneficial insects. They can assist in delaying the onset and reducing the intensity of mid-season

**d.** If infestation is high and the growth of the plants rapid, spray applications should be made at short intervals to protect the new growth, which may from otherwise be at‐ tacked by larvae repelled treated older foliage. Furthermore, short interval strategy will give better spray distribution and increase the chance of obtaining direct spray im‐

**e.** For crops in which higher economic thresholds are acceptable, integration of synthetic insecticide and beneficial insects becomes a practical possibility. The integration of chemical and biological control is often critical to the success of an IPM programme for arthropod pests [92, 93]. To combine the use of natural enemies with insecticides appli‐ cation, the chemical residues must be minimally toxic to the natural enemies to prevent its population being killed and the target pests increasing again [94]. Toxicological stud‐ ies that only evaluate the lethal effects may underestimate the negative effects of insecti‐ cides on natural enemies and hence, sublethal effects should be assessed to estimate the total effect of insecticides on biological performance of natural enemies [95]. However, even though several studies showed that sublethal effects of insecticides can affect effi‐ ciency of natural enemies [96, 97], such effects on these organisms are rarely taken into account when IPM programmes are established and only mortality tests are considered when a choice between several insecticides must be made. Accordingly, to achieve max‐ imum benefit from insecticides application and to reduce the selective pressure and de‐

but first and second instars are also more exposed than later instars [89].

until these pests have reached the economic threshold [90].

pingement on adults, larvae, and eggs [90].

The most interesting component of IPM for many people is biological control. It is also the most complicated as there is a diverse range of species and types of predators, parasitoids and pathogens. The value of biological control agents in integrated pest management is be‐ coming more apparent as researches are conducted. Natural enemies clearly play an impor‐ tant role in integrated management of *Helicoverpa* spp., particularly in low value crops where they may remove the need for any chemical intervention. Likewise in high value crops (such as cotton and tomato) beneficial species provide considerable benefit but are un‐ able to provide adequate control alone, especially in situations where migratory influxes of *Helicoverpa* result in significant infestations [14]. However, although parasitoids and preda‐ tors cannot be relied upon for complete control of *H. armigera* in unsprayed area, knowledge about their role in cropping systems where *H. armigera* is an important pest is an essential component in the development of integrated management.

Before using a natural enemy in a biological control programme, it is essential to know about its efficiency. However, study of demographic parameters and foraging behaviors of natural enemies is the reliable criteria for assessment of their efficiency. Among the demo‐ graphic parameters, intrinsic rate of increase (*rm*) is a key parameter in the prediction of pop‐ ulation growth potential and has been widely used to evaluate efficiency of natural enemies [22, 76, 98, 99]. In addition to demographic parameters, another important aspect for assess‐ ing the efficiency of natural enemies is the study of their foraging behaviors including func‐ tional, numerical and aggregation responses, mutual interference, preference and switching [100-110]. Such information is essential to interpret how the natural enemies live, how they influence the population dynamics of their hosts/preys, and how they influence the struc‐ ture of the insect communities in which they exist [111].

#### *8.2.1. Parasitoids*

The most common parasitoids that contribute to mortality of *Helicoverpa* spp. are shown in Table 7. Studies on the effects of parasitoids in biological control of *H. armigera* fo‐ cused on monitoring parasitism of eggs and larvae. In Botswana, parasitism of larvae collected from different crops averaged up to 50% on sorghum, 28% on sunflower, 49% on cowpeas and 76% on cotton [112]. These results showed that parasitoids had a crucial role in management of *H. armigera*. However, this level of parasitism is higher when compared to the results from East Africa where the level of parasitism was generally low (<5%) or absent [113]. Surveys made of the parasitoid of *Helicoverpa* spp. in cotton fields of Texas by Shepard and Sterling [114] showed that larval parasitoids accounted for ap‐ proximately 7% regulation of *Helicoverpa* spp. Such investigations highlight importance of parasitoids in integrated management of *H. armigera* in different cropping systems around the world.


*8.2.2. Predators*

and its efficiency was evaluated in laboratory [120].

The most important predators of *Helicoverpa* spp. are listed in Table 8. In some cropping sys‐ tems these predators have considerable impact on population of *Helicoverpa* spp. These bio‐ logical control agents have been reported as major factors in mortalities of *H. armigera* in cotton agroecosystems in South Africa and in smallholder crops in Kenya. In South Africa the average daily predation rates of 37% and 30% of *H. armigera* eggs and larvae, respective‐ ly were found in absence of insecticides [128]. Regarding this considerable potential, some of these predators could be candidated for implementation of biological control programmes. Accordingly, the species of *Sycanus indagator* (Stal) was imported from India to the USA. In another programme, *Pristhesancus papuensis* Stal was introduced from Australia to the USA

**Order Family Predator species References** Coleoptera Coccinelliadae *Scymnus moreletti* Sic [118]

Hymenoptera Formicidae *Pheidole* spp. [128]

Hemiptera Miridae *Campylomma* sp. [128]

Neuroptera Chrysopidae *Chrysoperla carnea* (Stephens) [132]

**Table 8.** Important predators of *Helicoverpa* spp.

Carabidae *Calosoma* spp. [129] Staphilinidae - [128]

Anthocoridae *Orius thripoborus* (Hesse) [113]

Reduviidae *Sycanus indagator* (Stal) [130] Reduviidae *Pristhesancus papuensis* Stal [120] Pentatomidae *Podisus maculiventris* (Say) [131] Nabidae *Nabis* spp. [129] Lygaeidae *Geocoris punctipes (Say)* [131]

*Exochomus flavipes* (Thunberg) [128] *Cheilomenes propinqua* (Mulsant) [128] *Hippodamia varigata* Goeze [128] *Coccinella* sp. [118]

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*Myrmicaria* spp. [128] *Dorylus* spp. [128]

*Cardiastethus exiguous* (Poppius) [113] *Orius albidipenrzis* (Reuter), [113] *Orius tantillus* (Motschulsky) [113] *Blaptostethus* sp. [113] *Cardiastethus* sp. [113]

**Table 7.** The most common parasitoids of *Helicoverpa* spp.

#### *8.2.2. Predators*

**Order Family Parasitoid species References** Hymenoptera Trichogrammatidae *Trichogramma pretiosum* Riley [115]

248 Soybean - Pest Resistance

Braconidae *Microplitis croceipes* (Cresson) [115]

Ichneumonidae *Campoletis sonorensis* Cameron [123]

Scelionidae *Telonomus* spp. [112]

Diptera Tachinidae *Archytas marmoratus* (Townsend) [114]

**Table 7.** The most common parasitoids of *Helicoverpa* spp.

*Trichogramma exiguum* Pinto and Platner [114] *Trichogramma australicum* Girault [116] *Trichogramma pretiosum* Riley [117]

*Habrobracon brevicornis* Wesm. [118] *Habrobracon hebetor* Say [17] *Cardiochiles nigriceps* Vierick [114] *Chelonus insularis* Cresson [119] *Apanteles marginiventris* (Cresson) [114]

*Meteorus* sp. [120] *Apanteles ruficrus* Hal. [120] *Apanteles kazak* Telenga [121] *Microplitis demolitor* Wilkinson [120] *Microplitis rufiventris* Kok., [118] *Chelonus inanitus* (L.), [118] *Chelonus versalis* Wilkn [112]

*Netelia* sp. [120]

*Hyposoter didymator* (Thunb.) [123] *Heteropelma scaposum* (Morley) [120] *Barylypa humeralis* Brauns [118] *Campoletis chlorideae* Uchida [124, 125] *Pristomerus* spp. [112] *Charops* spp. [112]

*Eucelatoria bryani* Sabrosky [114] *Lespesia archippivora* (Riley) [126] *Winthemia* sp. [120]

*Chaetophthalmus dorsalis* (Malloch) [127] *Palexorista laxa* (Curran) [124] *Exorista fallax* Mg., [124] *Goriophthalmus halli* Mesnil [124] *Palexorista* sp. [112] *Paradrino halli* Curran [112] The most important predators of *Helicoverpa* spp. are listed in Table 8. In some cropping sys‐ tems these predators have considerable impact on population of *Helicoverpa* spp. These bio‐ logical control agents have been reported as major factors in mortalities of *H. armigera* in cotton agroecosystems in South Africa and in smallholder crops in Kenya. In South Africa the average daily predation rates of 37% and 30% of *H. armigera* eggs and larvae, respective‐ ly were found in absence of insecticides [128]. Regarding this considerable potential, some of these predators could be candidated for implementation of biological control programmes. Accordingly, the species of *Sycanus indagator* (Stal) was imported from India to the USA. In another programme, *Pristhesancus papuensis* Stal was introduced from Australia to the USA and its efficiency was evaluated in laboratory [120].


**Table 8.** Important predators of *Helicoverpa* spp.

#### *8.2.3. Pathogens*

Naturally occurring entomopathogens are important regulatory factors in insect popula‐ tions. The application of microorganisms for control of insect pests was proposed by notable early pioneers in invertebrate pathology such as Agostino Bassi, Louis Pasteur and Elie Metchnikoff [133]. However, it was not until the development of the bacterium *Bacillus thur‐ ingiensis* Berliner (*Bt*) that the use of microbes for the control of insects became widespread. Today a variety of entomopathogens (bacteria, viruses, fungi, protozoa, and nematodes) are used for the control of insect pests [134]. However, when environmental benefits of these pathogens including safety for humans and other nontarget organisms, reduction of pesti‐ cide residues in food and environment, increased activity of most other natural enemies and increased biodiversity in managed ecosystems are taken into account, their advantages are numerous. There are also some disadvantages, mostly linked with their persistence, speed of kill, specificity (too broad or too narrow host range) and cost relative to conventional chemical insecticides. However, their increased utilization will require (*a*) increased patho‐ gen virulence and speed of kill; (*b*) improved pathogen performance under challenging en‐ vironmental conditions; (*c*) greater efficiency in their production; (*d*) improvements in formulation that enable ease of application, increased environmental persistence, and longer shelf life; (*e*) better understanding of how they will fit into integrated systems and their in‐ teraction with the environment and other IPM components and (*f*) acceptance by growers and the general public [134].

zero. The results obtained also revealed that the sublethal effects of *B. thuringiensis* could carry over to the next generation. The intrinsic and finite rates of increase (*rm* and *λ*, respec‐ tively) were significantly lower in insects treated with sublethal concentrations compared to control. Consequent with the reduce rate of development observed for *H. armigera* treated with *B. thuringiensis*, the doubling time (*DT*) were significantly higher in insects exposed to any concentration tested compared to control (Table 10). However, according to results ob‐ tained, *B. thuringiensis* could play a critical role in integrated management of *H. armigera*.

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**Group Family Pathogen species References** Bacteria Enterobacteriaceae *Pantoea agglomerans* (Ewing and Fife) [138]

Fungi Cordycipitaceae *Beauveria bassiana* (Balsamo) [139]

Viruses Baculoviridae Nuclear Polyhedrosis Virus [142] Nematoda Heterorhabditidae *Heterorhabditis bacteriophora* Poinar [143]

> 34.81±0.24 b

> 11.69±0.48 ab

665.13±52.46 b

> 0.18±0.00 a

> 1.20±0.00 a

> 3.75±0.05 d

**Table 10.** Sublethal effects of *Bacillus thuringiensis* on biological performance of *Helicoverpa armigera* in two

Means in a row followed by the same letters are not significantly different (P <0.05) (S.N.K.)

**Table 9.** Some of the isolated microorganisms from *Helicoverpa* spp.

Parental Total immature stages

\*

Female longevity

Offspring *rm* (day-1) 0.19±0.00

In this treatment hatch rate reaching zero.

subsequent generations.

**Generation Parameter Treatments**

31.87±0.38 c

13.14±0.40 a

a

a

a

d

Total fecundity 789.52±42.68

λ (day-1) 1.21±0.00

*DT* (day) 3.59±0.05

Bacillaceae *Bacillus thuringiensis* Berliner [19]

Clavicipitaceae *Metarhizium anisopliae* (Metsch.) [140] Moniliaceae *Nomuraea rileyi* (Farlow) Samson [141]

Steinernematidae *Steinernema carpocapsae* (Weiser) [143]

**Control LC <sup>5</sup> LC <sup>10</sup> LC <sup>15</sup> LC <sup>20</sup> LC <sup>25</sup>**

35.63±0.52 b

10.28±0.86 bc

601.00±45.72 b

> 0.16±0.00 b

1.1±0.00 b

4.29±0.08 c

*Steinernema feltiae* (Filipjev) [143]

34.74±0.31 b

10.06±0.67 bc

532.53±33.70 b

> 0.14±0.00 c

> 1.16±0.01 c

> 4.78±0.08 b

36.17±0.42 ab

9.27±0.44 c

376.00±21.95 c

> 0.13±0.00 d

> 1.14±0.00 d

> 5.33±0.16 a

37.17±0.43 a

7.23±0.44 d

98.46±12.33 d

> - *\**

> > -


The critical need for safe and effective alternatives to chemical insecticides in integrated management of *H. armigera* has stimulated considerable interest in using pathogens as bio‐ logical control agents. A list of some isolated microorganisms from *Helicoverpa* spp. is pre‐ sented in Table 9. Among these microorganisms, nuclear polyhedrosis virus (NPV) and *B. thuringiensis* have a considerable effect on population of *H. armigera*. Potential of these pathogens in management programmes of *H. armigera* were evaluated by several research‐ ers. Roome [135] tested a commercial preparation of NPV against *H. armigera*. The results showed that NPV was as effective as a standard insecticide in reducing yield loss on sor‐ ghum due to damage by *H. armigera*. In addition, the long survival of NPV on sorghum (80 days) indicated that a single application of NPV was adequate to protect the crop for a growing season. In another study, Moore *et al.* [136] showed that NPV has potential in man‐ agement of *H. armigera* on citrus trees. Recent work by Jeyarani *et al.* [137] revealed that NPV has an acceptable efficiency in control of *H. armigera* on cotton and chickpea.

Pathogenicity of *B. thuringiensis* for management of *H. armigera* population was investigated by several researchers [19, 144]. They showed that larvae ingest enough quantities of *B. thur‐ ingiensis* toxins to die, or at least to reduce its weight and development, depending on the toxin and conditions of the experiment. In a recent study, sublethal effects of *B. thuringiensis* on biological performance of *H. armigera* were investigated [Sedaratian and Fathipour, un‐ published data]. According to results obtained, values recorded for duration of total imma‐ ture stages increased from 31.87 days in control to 37.17 days in LC25. Furthermore, female longevity decreased from 13.14 days to 7.23 days. Fecundity was also negatively affected in female moths developed from treated neonates, with the rate of egg hatchability reaching zero. The results obtained also revealed that the sublethal effects of *B. thuringiensis* could carry over to the next generation. The intrinsic and finite rates of increase (*rm* and *λ*, respec‐ tively) were significantly lower in insects treated with sublethal concentrations compared to control. Consequent with the reduce rate of development observed for *H. armigera* treated with *B. thuringiensis*, the doubling time (*DT*) were significantly higher in insects exposed to any concentration tested compared to control (Table 10). However, according to results ob‐ tained, *B. thuringiensis* could play a critical role in integrated management of *H. armigera*.


**Table 9.** Some of the isolated microorganisms from *Helicoverpa* spp.

*8.2.3. Pathogens*

250 Soybean - Pest Resistance

and the general public [134].

Naturally occurring entomopathogens are important regulatory factors in insect popula‐ tions. The application of microorganisms for control of insect pests was proposed by notable early pioneers in invertebrate pathology such as Agostino Bassi, Louis Pasteur and Elie Metchnikoff [133]. However, it was not until the development of the bacterium *Bacillus thur‐ ingiensis* Berliner (*Bt*) that the use of microbes for the control of insects became widespread. Today a variety of entomopathogens (bacteria, viruses, fungi, protozoa, and nematodes) are used for the control of insect pests [134]. However, when environmental benefits of these pathogens including safety for humans and other nontarget organisms, reduction of pesti‐ cide residues in food and environment, increased activity of most other natural enemies and increased biodiversity in managed ecosystems are taken into account, their advantages are numerous. There are also some disadvantages, mostly linked with their persistence, speed of kill, specificity (too broad or too narrow host range) and cost relative to conventional chemical insecticides. However, their increased utilization will require (*a*) increased patho‐ gen virulence and speed of kill; (*b*) improved pathogen performance under challenging en‐ vironmental conditions; (*c*) greater efficiency in their production; (*d*) improvements in formulation that enable ease of application, increased environmental persistence, and longer shelf life; (*e*) better understanding of how they will fit into integrated systems and their in‐ teraction with the environment and other IPM components and (*f*) acceptance by growers

The critical need for safe and effective alternatives to chemical insecticides in integrated management of *H. armigera* has stimulated considerable interest in using pathogens as bio‐ logical control agents. A list of some isolated microorganisms from *Helicoverpa* spp. is pre‐ sented in Table 9. Among these microorganisms, nuclear polyhedrosis virus (NPV) and *B. thuringiensis* have a considerable effect on population of *H. armigera*. Potential of these pathogens in management programmes of *H. armigera* were evaluated by several research‐ ers. Roome [135] tested a commercial preparation of NPV against *H. armigera*. The results showed that NPV was as effective as a standard insecticide in reducing yield loss on sor‐ ghum due to damage by *H. armigera*. In addition, the long survival of NPV on sorghum (80 days) indicated that a single application of NPV was adequate to protect the crop for a growing season. In another study, Moore *et al.* [136] showed that NPV has potential in man‐ agement of *H. armigera* on citrus trees. Recent work by Jeyarani *et al.* [137] revealed that NPV

Pathogenicity of *B. thuringiensis* for management of *H. armigera* population was investigated by several researchers [19, 144]. They showed that larvae ingest enough quantities of *B. thur‐ ingiensis* toxins to die, or at least to reduce its weight and development, depending on the toxin and conditions of the experiment. In a recent study, sublethal effects of *B. thuringiensis* on biological performance of *H. armigera* were investigated [Sedaratian and Fathipour, un‐ published data]. According to results obtained, values recorded for duration of total imma‐ ture stages increased from 31.87 days in control to 37.17 days in LC25. Furthermore, female longevity decreased from 13.14 days to 7.23 days. Fecundity was also negatively affected in female moths developed from treated neonates, with the rate of egg hatchability reaching

has an acceptable efficiency in control of *H. armigera* on cotton and chickpea.


Means in a row followed by the same letters are not significantly different (P <0.05) (S.N.K.)

\* In this treatment hatch rate reaching zero.

**Table 10.** Sublethal effects of *Bacillus thuringiensis* on biological performance of *Helicoverpa armigera* in two subsequent generations.

The reliance on the entomopathogens for management of *H. armigera*, however, is risky since the different factors that govern epizootics. Accordingly, in most cases no single micro‐ bial control agent will provide sustainable control of this pest. Nevertheless, as components of an integrated management programme, entomopathogens can provide significant and se‐ lective control [134]. In the not too distant future we envision a broader appreciation for the attributes of entomopathogens and expect to see synergistic combinations of microbial con‐ trol agents with other technologies that will enhance the effectiveness and sustainability of integrated management of *H. armigera*.

*H. armigera* and its natural enemies on a crop are influenced by neighboring crops, both di‐ rectly and indirectly. Direct influences include preference for one crop over the other by ovi‐ positing 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

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An alternative and often complementary strategy for management of *H. armigera* is the con‐ trol 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].

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 sys‐ tems [150]. Trap crops have been defined as "plant stands that are, per se or via manipula‐ tion, 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 pu‐ pae. A trap crop, strategically timed to flower in the spring, can help to reduce the early sea‐ son 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 dif‐ ferent 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 en‐ hancing 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

population build-up or mortality level on neighboring crops [113].

*8.3.3. Ploughing and early planting effects on Helicoverpa populations*

*8.3.4. Trap crops and 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 applica‐ tions, 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. Al‐ though 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 preda‐ tors 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 re‐ sources such as food to maintain, arrest or stimulate the released natural enemy could pro‐ vide 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 diversi‐ ty 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 di‐ rectly and indirectly. Direct influences include preference for one crop over the other by ovi‐ positing 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 con‐ trol 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 reliance on the entomopathogens for management of *H. armigera*, however, is risky since the different factors that govern epizootics. Accordingly, in most cases no single micro‐ bial control agent will provide sustainable control of this pest. Nevertheless, as components of an integrated management programme, entomopathogens can provide significant and se‐ lective control [134]. In the not too distant future we envision a broader appreciation for the attributes of entomopathogens and expect to see synergistic combinations of microbial con‐ trol agents with other technologies that will enhance the effectiveness and sustainability of

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 applica‐ tions, 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. Al‐ though some cultural practices have a noticeable potential in integrated management, use of some cultural controls is not universally beneficial. For example, providing nectar sources

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 preda‐ tors 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

Dispersal from target area often reduces the effectiveness of natural enemies especially in augmentation programmes. To minimize this shortcoming, provision of supplemental re‐ sources such as food to maintain, arrest or stimulate the released natural enemy could pro‐ vide 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 diversi‐ ty 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

integrated management of *H. armigera*.

for beneficial insects may also provide nectar sources for pests.

*8.3.1. Uncultivated marginal areas and abundance of natural enemies*

**8.3. Cultural control**

252 Soybean - Pest Resistance

areas such as soybean fields.

*8.3.2. Intercropping and its effect on natural enemies*

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 sys‐ tems [150]. Trap crops have been defined as "plant stands that are, per se or via manipula‐ tion, 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 pu‐ pae. A trap crop, strategically timed to flower in the spring, can help to reduce the early sea‐ son 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 dif‐ ferent 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 en‐ hancing 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 "be‐ havioral 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].

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 fac‐ tors. 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 con‐ stitutive resistance. If biotic and abiotic environmental factors reduces insect fitness or nega‐ tively affects host selection processes, the effect is called induced resistance. On the other hand, constitutive resistance involves inherited characters whose expression, although influ‐ enced 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 de‐ ter or reduce colonization by insect. Antibiosis is the resistance mechanism that operates af‐ ter 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

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Plant resistance to insect pests can be inherited in two distinct ways including vertical (mon‐ ogenic) 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 resist‐ ance to only one insect pest and thus, depending on the pest species in specific area a culti‐ var 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 infec‐ tion 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

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 differ‐ ent host plants could reveal the suitability of one crop for this noctuid pest than other host

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 re‐ searchers 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

that enable them to withstand or recover from insect damage [159].

with horizontal resistance to insect pests [162].

*8.3.5.1. Plant resistance to H. armigera*

plants.

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 in‐ tercropped trap crop), and the colonization habits of the pest are crucial to success and re‐ quire 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 applica‐ tion of neem seed extracts to the main crop (push) with an attractive trap crop, either pi‐ geonpea 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 cot‐ ton 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 re‐ cent 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 environ‐ ments 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 sus‐ ceptible 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 con‐ trol 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. Further‐ more, 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 fea‐ tures 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 unneces‐ sary; (*e*) is persistence; (*f*) can easily be adopted into normal farm operations; (*g*) is compati‐ ble 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 fac‐ tors. 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 con‐ stitutive resistance. If biotic and abiotic environmental factors reduces insect fitness or nega‐ tively affects host selection processes, the effect is called induced resistance. On the other hand, constitutive resistance involves inherited characters whose expression, although influ‐ enced 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 de‐ ter or reduce colonization by insect. Antibiosis is the resistance mechanism that operates af‐ ter 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 (mon‐ ogenic) 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 resist‐ ance to only one insect pest and thus, depending on the pest species in specific area a culti‐ var 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 infec‐ tion 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*

the distribution of *Helicoverpa* spp. in cotton fields. Push-pull strategies involve the "be‐ havioral 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

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 in‐ tercropped trap crop), and the colonization habits of the pest are crucial to success and re‐

In the case of *Helicoverpa* spp. on cotton in Australia, the potential of combining the applica‐ tion of neem seed extracts to the main crop (push) with an attractive trap crop, either pi‐ geonpea 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 cot‐ ton 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 re‐ cent study in India. Neem, combined with a pigeonpea or okra trap crop, was an effective

Plants that are inherently less damaged or infested by insect pests in comparable environ‐ ments 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 sus‐ ceptible 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 con‐ trol 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. Further‐ more, 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 fea‐ tures 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 unneces‐ sary; (*e*) is persistence; (*f*) can easily be adopted into normal farm operations; (*g*) is compati‐ ble 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].

programmes reducing pesticide input [155].

254 Soybean - Pest Resistance

strategy against *H. armigera* [157].

*8.3.5. Host plant resistance*

quire a thorough understanding of the behavior of the pest [156].

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 differ‐ ent 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 re‐ searchers 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-noctui‐ dae-. 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. armi‐ gera* in soybean cropping systems more attention should be devoted to fill this gap.

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

importance of such information in IPM, a little knowledge in this field is available.

ceptible ones, an indication of the compatibility of HPR and the predator.

*8.3.5.2.1. HPR and biological control*

resistance (B) (after van Emden and Wearing [170]).

Several studies have been performed to investigate the possible interactions of host plant re‐ sistance 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, syn‐ ergistic, and antagonistic. Additive interaction means the combined effect of two control meas‐ ures 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

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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 retard‐ ed growth and an extended developmental period. Under field conditions, such poorly de‐ veloped 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 sus‐

**Figure 4.** Influence of a low level of plant resistance to pest attack on the effectiveness of natural enemies. ○, without predator; ●, with predator. Predator activity fails to exert economic control of insect pests on susceptible plants (A), whereas the same degree of predator activity exert economic control of the insect pest on plants with some degree of


*a* Digits in parentheses show number of tested cultivars.

*<sup>b</sup>* 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.

**Table 11.** Effects of different host plants on some population growth parameters of *Helicoverpa armigera*

#### *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 re‐ sistance 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, syn‐ ergistic, and antagonistic. Additive interaction means the combined effect of two control meas‐ ures 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*

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-noctui‐ dae-. 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. armi‐*

*gera* in soybean cropping systems more attention should be devoted to fill this gap.

**offspring)**

Canola (10) *<sup>a</sup>* 25 artificial *<sup>b</sup>* 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]

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

**Table 11.** Effects of different host plants on some population growth parameters of *Helicoverpa armigera*

*rm* (**day-1**)

*T* **(day)**

*DT* **(day)** **References**

**Crop Experimental conditions** *R <sup>0</sup>* **(female**

Digits in parentheses show number of tested cultivars.

and Fathipour, unpublished data; [f] Safuraie and Fathipour, unpublished data.

*<sup>b</sup>* Artificial diet based on the seed of host plant.

**Diet type**

**Temperature °C**

256 Soybean - Pest Resistance

*a*

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 retard‐ ed growth and an extended developmental period. Under field conditions, such poorly de‐ veloped 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 sus‐ ceptible ones, an indication of the compatibility of HPR and the predator.

**Figure 4.** Influence of a low level of plant resistance to pest attack on the effectiveness of natural enemies. ○, without predator; ●, with predator. Predator activity fails to exert economic control of insect pests on susceptible plants (A), whereas the same degree of predator activity exert economic control of the insect pest on plants with some degree of resistance (B) (after van Emden and Wearing [170]).

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 at‐ tack early instars of *Helicoverpa* sp. on soybean and tobacco but generally do not attack big‐ ger 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.

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. integri‐ ceps* 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

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**Figure 5.** Effect of plant resistance on the selectivity of an insecticide. A: susceptible cultivar; B: resistant cultivar where dose for the herbivore can be reduced by one third; C: dose mortality curve for carnivore; H: dose mortality curve for

However, in addition to negative effects on insect bodyweight, repellent chemicals or mor‐ phological traits of resistant cultivars may be effective in reduction of insecticide spray. Re‐ pellency 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 fe‐ cundity. Furthermore, repellency is equivalent to using low doses of insecticides along with

**8.4. Semiochemicals and their possible use in suppression of** *H. armigera* **populations**

Many insects and other arthropods rely on chemical messages to communicate with each other or to find suitable hosts. Chemical messages that trigger various behavioral responses

herbivore; DC: dose scale for carnivore; DH: dose scale for herbivore (after van Emden, [178]).

the repellent properties of the host plant [159].

and 114.01 and for new adults was 303.35 and 227.88 ppm, respectively.

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 geno‐ types of tobacco with glandular trichomes have been shown to severely limit the parasitiza‐ tion 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 anti‐ biotic 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 cu‐ cumber leaves significantly increase effectiveness of *Encarsia formosa* Gahan on the green‐ house whitefly [173].

#### *8.3.5.2.2. HPR and insect pathogens*

Schultz [174] hypothesized that the effectiveness of insect pathogens may be reduced or im‐ proved, 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 af‐ fected 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 feed‐ ing 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. integri‐ ceps* 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.

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 at‐ tack early instars of *Helicoverpa* sp. on soybean and tobacco but generally do not attack big‐ ger 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

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 geno‐ types of tobacco with glandular trichomes have been shown to severely limit the parasitiza‐ tion 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 anti‐ biotic 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 cu‐ cumber leaves significantly increase effectiveness of *Encarsia formosa* Gahan on the green‐

Schultz [174] hypothesized that the effectiveness of insect pathogens may be reduced or im‐ proved, 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 af‐ fected 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

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 feed‐ ing 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

are valuable phenomenon in the development of practical IPM.

house whitefly [173].

258 Soybean - Pest Resistance

against *H. zea*.

*8.3.5.2.2. HPR and insect pathogens*

*8.3.5.2.3. HPR and chemical control*

**Figure 5.** Effect of plant resistance on the selectivity of an insecticide. A: susceptible cultivar; B: resistant cultivar where dose for the herbivore can be reduced by one third; C: dose mortality curve for carnivore; H: dose mortality curve for herbivore; DC: dose scale for carnivore; DH: dose scale for herbivore (after van Emden, [178]).

However, in addition to negative effects on insect bodyweight, repellent chemicals or mor‐ phological traits of resistant cultivars may be effective in reduction of insecticide spray. Re‐ pellency 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 fe‐ cundity. Furthermore, repellency is equivalent to using low doses of insecticides along with the repellent properties of the host plant [159].

#### **8.4. Semiochemicals and their possible use in suppression of** *H. armigera* **populations**

Many insects and other arthropods rely on chemical messages to communicate with each other or to find suitable hosts. Chemical messages that trigger various behavioral responses are collectively referred to as semiochemicals. Generally, semiochemicals is subdivided into two distinct groups including pheromones and allelochemicals (Table 12). The term phero‐ mone is used to describe compounds that operate intraspecifically, while allelochemical is the general term for an interspecific effector [26]. However, the realization that behaviors critical to insect survival were strongly influenced by semiochemicals rapidly led to propos‐ als for using these agents as practical tools for pest suppression [180].

As discussed in previous section (see section 6) and in addition to using the pheromones of *Helicoverpa* spp. for essential monitoring of infested areas, these compounds have been shown to be useful for suppression of *Helicoverpa* infestation. Attractant-baited lures form the basis for three direct control measures: (1) mass trapping of male, (2) attract-and-kill strategy and (3) mating disruption via permeating the atmosphere of crop environments with sex pheromones. Potential of synthesized pheromones for mass trapping of *H. armi‐ gera* was investigated by several researchers. According to Pawar *et al.* [181], *H. armigera* will readily respond to synthesized pheromones and traps are capable of capturing hun‐ dreds of male moths per trap per night. The same results were reported by Reddy and Manjunath [18]. Attract-and-kill is a promising new strategy that involves an attractant such as a pheromone and a toxicant. Unlike mating disruption, which functions by con‐ fusing the insect, this strategy attracts the insect to a pesticide laden gel matrix and kills them. This strategy has been successfully used on several lepidopteran species [18] but no information is available in the case of *Helicoverpa* spp. However, the most developed tactic is mating disruption. This approach entails releasing large amounts of synthetic sex pheromone into the atmosphere of a crop to interfere with mate-finding, thereby control‐ ling the pest by curtailing the reproductive phase of its life cycle. Mating disruption through the use of some synthesized pheromone such as (Z)-9-tetradecen-1-ol for air per‐ meation is a potentially valuable development in integrated management of *Helicoverpa* spp. It has been shown to be very effective with *H.* zea and *H. virescens* and should cer‐

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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 em‐ ployed to study the species composition of the pest population and to identify strains, races

Another important application of molecular diagnostic techniques is for monitoring both the presence and frequency of genes of particular interest. For example, genes for resist‐ ance to a specific class of pesticides and their frequency in particular region can be as‐ sessed. Such information is very useful for designing and implementing rational pest

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 man‐ agement option, but cultivated germplasm has only low to moderate resistance levels to some key pests. Furthermore, some sources of resistance have poor agronomic characteris‐ tics. On the other hand, development of cultivars with enhanced resistance will strengthen

tainly be pursued for the same purpose with *H. armigera* [182].

**9. Biotechnology in IPM**

or biotypes of the same species.

management strategies [159].


a classified according to function

b classified according to the advantage to receiver or sender

**Table 12.** Classification of behavior-modifying chemicals (semiochemicals)

As discussed in previous section (see section 6) and in addition to using the pheromones of *Helicoverpa* spp. for essential monitoring of infested areas, these compounds have been shown to be useful for suppression of *Helicoverpa* infestation. Attractant-baited lures form the basis for three direct control measures: (1) mass trapping of male, (2) attract-and-kill strategy and (3) mating disruption via permeating the atmosphere of crop environments with sex pheromones. Potential of synthesized pheromones for mass trapping of *H. armi‐ gera* was investigated by several researchers. According to Pawar *et al.* [181], *H. armigera* will readily respond to synthesized pheromones and traps are capable of capturing hun‐ dreds of male moths per trap per night. The same results were reported by Reddy and Manjunath [18]. Attract-and-kill is a promising new strategy that involves an attractant such as a pheromone and a toxicant. Unlike mating disruption, which functions by con‐ fusing the insect, this strategy attracts the insect to a pesticide laden gel matrix and kills them. This strategy has been successfully used on several lepidopteran species [18] but no information is available in the case of *Helicoverpa* spp. However, the most developed tactic is mating disruption. This approach entails releasing large amounts of synthetic sex pheromone into the atmosphere of a crop to interfere with mate-finding, thereby control‐ ling the pest by curtailing the reproductive phase of its life cycle. Mating disruption through the use of some synthesized pheromone such as (Z)-9-tetradecen-1-ol for air per‐ meation is a potentially valuable development in integrated management of *Helicoverpa* spp. It has been shown to be very effective with *H.* zea and *H. virescens* and should cer‐ tainly be pursued for the same purpose with *H. armigera* [182].
