*2.1.1. Trissolcus grandis*

The scelionid egg parasitoid *Trissolcus grandis* Thompson (Hymenoptera: Scelionidae) had a very important role in reducing *Eurygaster integriceps* (Puton) population (Radjabi 1995; Critchley 1998). However, intensive use of insecticides has caused severe damage to para‐ sitoid populations (Radjabi 1995). It is estimated that egg parasitoids reduce *E. integriceps* pest population by ca. 23% yearly in Iran (Amirmaaif 2000). Presently, chemical control is the main tool used to control the *E. integriceps* populations. The chemicals currently used for controlling this pest are organophosphorous insecticides such as fenitrothion, fen‐ thion, trichlorfon, chlorpyrifos, and pirimiphos methyl (Orr et al. 1989; Kivan 1996; Saber 2002), and synthetic pyrethroids such as deltamethrin, cypermethrin, cyßuthrin, and cyha‐ lothrin (Kivan 1996). Fenitrothion and deltamethrin are the most commonly used insecti‐ cides to control the *E. integriceps* in Iran (Amirmaaif 2000; Sheikhi Garjan 2000). There are many studies on the effects of conventional insecticides on *E. integriceps* egg parasitoids (i.e. Novozhilov et al. 1973; Smilanick et al. 1996; Sheikhi Garjan 2000).

Saber et al. (2005) assessed effects of fenitrothion and deltamethrin, on adults and preimaginal stages of egg parasitoid *Trissolcus grandis*. Fenitrothion and deltamethrin reduced the emer‐ gence rates by 18,0 and 34.4%, respectively, compared with the control. However, neither insecticide significantly affected the longevity or reproductive capacity of emerged females, or the sex ratio of their progeny. This study revealed that application of these insecticides should be cautiously through season to conserve natural or released populations of *T. grandis*. Adult females of *T. grandis* usually produce the majority of offspring in the first few days after emergence. Proportion of male offspring produced by *T. grandis* in the early life span of the parasitoid is higher in the treatments than control that will result in a higher proportion of males in the insecticides treatments (Fig. 1).

**Figure 1.** Proportion of male offspring produced by *Trissolcus grandis* adults emerged from treated parasitized eggs at pupal stage and control (after Saber et al. 2005)

#### *2.1.2. Telenomus remus*

apparent when pesticides applied to control one pest cause an outbreak of other pests because of the chemical destruction of important natural enemies. There is great potential for increasing the benefits derived from naturally occurring biological controls, through the elimination or

The main objective of this book chapter studying the insecticide side effects on development, parasitism or predation efficacy and emergence capacity as well as to preserve effective biological control agents is a combination of tactics including an understanding of the biology and behaviour of arthropods (parasitoids, predators and spiders), detailed monitoring of life history and population dynamics of pests and natural enemies, employment of selective pesticides, application only when absolutely necessary, basing chemical control on established

Integrated Pest Management (IPM) programs are used worldwide for controlling different agricultural pests. The use of natural enemy agents in combination with selected insecticides, which have no effect on them, is effective in depressing the population density of the pest. Generally, egg parasitoids such as *Trichogramma* have been widely used as biological control agent as reported by Hassan (1982), Bigler (1984) and El-Wakeil & Hussein (2009); who confirmed that 65 – 93% reduction in larval infestations of *Ostrinia nubilalis* in corn fields was achieved following *Trichogramma* releases in Germany and Switzerland as well in Egypt.

The scelionid egg parasitoid *Trissolcus grandis* Thompson (Hymenoptera: Scelionidae) had a very important role in reducing *Eurygaster integriceps* (Puton) population (Radjabi 1995; Critchley 1998). However, intensive use of insecticides has caused severe damage to para‐ sitoid populations (Radjabi 1995). It is estimated that egg parasitoids reduce *E. integriceps* pest population by ca. 23% yearly in Iran (Amirmaaif 2000). Presently, chemical control is the main tool used to control the *E. integriceps* populations. The chemicals currently used for controlling this pest are organophosphorous insecticides such as fenitrothion, fen‐ thion, trichlorfon, chlorpyrifos, and pirimiphos methyl (Orr et al. 1989; Kivan 1996; Saber 2002), and synthetic pyrethroids such as deltamethrin, cypermethrin, cyßuthrin, and cyha‐ lothrin (Kivan 1996). Fenitrothion and deltamethrin are the most commonly used insecti‐ cides to control the *E. integriceps* in Iran (Amirmaaif 2000; Sheikhi Garjan 2000). There are many studies on the effects of conventional insecticides on *E. integriceps* egg parasitoids

Saber et al. (2005) assessed effects of fenitrothion and deltamethrin, on adults and preimaginal stages of egg parasitoid *Trissolcus grandis*. Fenitrothion and deltamethrin reduced the emer‐ gence rates by 18,0 and 34.4%, respectively, compared with the control. However, neither

(i.e. Novozhilov et al. 1973; Smilanick et al. 1996; Sheikhi Garjan 2000).

reduction in the use of pesticides toxic to natural enemies.

4 Insecticides - Development of Safer and More Effective Technologies

economic injury levels and application at the least injurious time.

**2. Side effects on parasitoid wasps**

**2.1. Egg parasitoids**

*2.1.1. Trissolcus grandis*

It is very important studying the insecticide side effects on egg parasitoids. The first study on side-effects of neem products on egg- parasitoids was conducted by Joshi et al. (1982) in India. These authors applied a 2% aqueous NSKE (Neem Seed Kernel Extract) on the egg masses of the noctuid *Spodopteru litura.* The egg parasitoid *Telenomus remus* was not repelled from egg laying. When the treatment was carried out before egg laying of the parasitoid, the emergence of adult parasitoids was normal but their duration of life was shorter than that of controls. On the other hand, spraying with NSKE after oviposition of *T. remus* increased the fecundity of the wasps developed in treated eggs and prolonged their life as compared with that of untreated controls; similar results were also reported by Golec (2007).

#### *2.1.3. Trichogramma species*

*Trichogramma* genus is a tiny parasitoid and some species are susceptible for chemicals. In both cases using insecticides alone or compatible with *Trichogramma*, there is a side effect on the later as studied by by Shoeb (2010), who mentioned that effect of five insecticides, Profect (w.p.), CAPL- 2 ( mineral oil), Lambda-cyhalothrin, Spinosad, and Fenitrothion (Sumithon) were studied on the immature stages of *Trichogramma evanescens* (West.). Longevity of the emerged parasitoid was affected by the tested insecticides. Eggs treatment with chemical insecticides caused death of the emerged adults within few hours post emergence. The number of parasitized eggs was varied according to timing of treatment. Adult emergence rate varied according to the used insecticide and the parasitoid stage. There was no emergence for the parasitoid treated with Lambda-cyhalothrin, spinosad, and fenitrothion (Sumithon) one, two or four days after parasitism. On the other hand, El-Wakeil et al (2006) reported that there was no serious side effect on parasitism and emergence rates of *T. pretiosum* (Riley) and *T. minu‐ tum* (Riley) when treated with neem products. Similarly, neem products achieved a good control of *H. armigera* in greenhouse. Therefore, neem products are recommended for control‐ ling *Helicoverpa* and are compatible with mass release of *Trichogramma*.

During the past three decades, *Trichogramma* spp. wasps have been evaluated as biological control agents for heliothine pest suppression in cotton (Knutson 1998; Suh et al. 1998, 2000; El-Wakeil 2003). Results of augmentative releases have been variable and at least some of the variability has been attributed to the use of broad spectrum insecticides in or near release plots during the time releases were made (Varma & Singh 1987; Kawamura et al. 2001; Brunner 2001; Geraldo et al. 2003). These insecticides were generally used to manage boll weevil, *Anthonomus grandis* (Boheman) and sometimes used to salvage *Trichogramma* release plots under extreme heliothine infestations. Numerous laboratory and field studies have shown that *Trichogramma* spp. wasps are highly susceptible to most broad-spectrum insecticides (Bull & Coleman 1985). Consequently, use of insecticides and *Trichogramma* has historically been

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7

Since the successful eradication of *A. grandis* in North Carolina, heliothines [predomi‐ nantly *Helicoverpa zea* (Boddie)] have emerged as the primary mid to late season insect pest in North Carolina cotton (Bacheler 1998). Thus, most of the foliar insecticide applica‐ tions (generally pyrethroids) made to cotton in North Carolina are aimed for control of the heliothine complex, *H. zea* and *Heliothis virescens* (F.). Unfortunately, these commonly used insecticides also are toxic to many non target organisms, including predators and parasitoids. Additionally, some heliothine pests (particularly *H. virescens*) have developed resistance to pyrethroids in some cotton growing areas. In an attempt to combat insecti‐ cide resistance, conserve arthropod natural enemies, and reduce health risks, several new insecticides (e.g., tebufenozide, methoxyfenozide, spinosad) have been developed and tested against lepidopteran pests in cotton (Bull & House 1983; Stapel et al. 2000; Vianna et al. 2009). Also, there is very important studies regarding the compatibility of these rel‐ atively new compounds with *Trichogramma* wasps, such as the detailed study involving *T. pretiosum* and tebufenozide (Cônsoli et al. 1998) with Neem (El-Wakeil et al. 2006) and

with other biocontrol agent *Chrysoperla carnea* (El-Wakeil & Vidal 2005).

**Example: Side effect on parasitism rates of** *T. pretiosum* **and** *T. minutum* **on** *Helicoverpa* **eggs**

El-Wakeil et al. (2006) reported that their results indicated that NeemAzal-T/S reduced the parasitism rates to 50, 48.9, 71.1 and 73.3 % at 2, 1, 0.5, 0.25% cons, respectively (Fig. 2A), compared to 96.6% on control plants. NeemAzal PC 05 reduced the parasitism rates to 70, 67.8, 70 and 80% on succeeding concentrations; 2, 1, 0.5 and 0.25%. Neem blanks achieved a less side effect on *T. pretiosum*. NeemAzal Blank reduced the parasitism rates to 81.1%. NeemAzal PC05 Blank reduced the parasitism rates to 91.3% compared to 98.7% on control plants (Fig. 2A). El-Wakeil et al. (2006) mentioned further that NeemAzal-T/S had reduced the parasitism rates, to 40, 55.4, 77.8 and 81.3 % (at 2, 1, 0.5 and 0.25% cons.), respectively, compared to 93.3% on control plants. NeemAzal PC 05 reduced the parasitism rates to 82.2, 82.2, 74.4 and 83.3% on succeeding concentrations; 2, 1, 0.5 and 0.25% (Fig. 2B). Neem blanks achieved a less side effect on *T. minutum*. Parasitism rates reached to 74.4% in neem blanks. Parasitism rates were reduced by NeemAzal PC05 Blank to 86.7% compared to 93.3% on control plants (Fig. 2B).

considered incompatible (Hassan 1983).

Assessment of the potential effects that pesticides have on the natural enemies is therefore an important part of IPM programs (Hirai 1993; Hassan 1994; Consoli et al. 1998; Takada et al. 2000). Detailed knowledge of the effects of different pesticides on the immature stages of natural enemies will help to determine the timing of sprays, thus avoiding the most susceptible stages (Campbell et al. 1991; Guifen and Hirai 1997). Mass breeding and release of parasitoids for control of various lepidopterous pests is now a commercial practice in many countries. However, the efficacy of the parasitoid is influenced a great deal by the insecticide spray schedule before and after parasitoid release. Candidate parasitoids for IPM programs should therefore be tested for susceptibility to the insecticides being used for controlling crop pests (Hassan et al. 1987). Egg parasitoids are known to be very effective against a number of crop pests. *Trichogramma dendrolimi* (Matsumura) has been described as a control agent for the pine moth, citrus swallowtail (Hirose 1986), *Spodoptera litura* (Hamada 1992), and other cruciferous insect pests (Dai et al. 1991). The cabbage moth, *Mamestra brassicae*(L.), is an important pest of ca. 20-51 species of plants (Hirata 1960). The use of broad-spectrum insecticides, however, has resulted in a decline in the natural enemies of *M. brassicae.* There are many research dealing with determining the susceptibility of *T. dendrolimi* to several insecticides, and evaluate its potential use for controlling the cabbage moth and other lepidopteran insects (Takada et al. 2000, 2001). Who tested toxicity of six insecticides, acephate, methomyl, ethofenprox, cartap, chlorfluazuron, and *Bacillus thuringiensis* (Bt) on different developmental stages of *Trichog‐ ramma dendrolimi* (Matsumura). Ethofenprox showed the highest toxicity and cartap showed relatively higher toxicity compared with the other insecticides. The development of the parasitoids treated with these two insecticides was normal, similar to that of the control group; the same trend of results was also obtained by Vianna et al. (2009) and Shoeb (2010).

Suh et al (2000) investigated effect of insecticides on emergence, adult survival, and fitness parameters of *Trichogramma exiguum*. Insecticides tested were lambda cyhalothrin, cyper‐ methrin, thiodicarb, profenophos, spinosad, methoxyfenozide, and tebufenozide. All insecti‐ cides, with the exception of methoxyfenozide and tebufenozide, adversely affected *Trichogramma* emergence from *Helicoverpa zea* (Boddie) host eggs when exposed at different preimaginal stages of development (larval, prepupal, or pupal). However, the mean life span of emerged *T. exiguum* females significantly varied among insecticides, and was significantly affected by the developmental stage when treated.

During the past three decades, *Trichogramma* spp. wasps have been evaluated as biological control agents for heliothine pest suppression in cotton (Knutson 1998; Suh et al. 1998, 2000; El-Wakeil 2003). Results of augmentative releases have been variable and at least some of the variability has been attributed to the use of broad spectrum insecticides in or near release plots during the time releases were made (Varma & Singh 1987; Kawamura et al. 2001; Brunner 2001; Geraldo et al. 2003). These insecticides were generally used to manage boll weevil, *Anthonomus grandis* (Boheman) and sometimes used to salvage *Trichogramma* release plots under extreme heliothine infestations. Numerous laboratory and field studies have shown that *Trichogramma* spp. wasps are highly susceptible to most broad-spectrum insecticides (Bull & Coleman 1985). Consequently, use of insecticides and *Trichogramma* has historically been considered incompatible (Hassan 1983).

were studied on the immature stages of *Trichogramma evanescens* (West.). Longevity of the emerged parasitoid was affected by the tested insecticides. Eggs treatment with chemical insecticides caused death of the emerged adults within few hours post emergence. The number of parasitized eggs was varied according to timing of treatment. Adult emergence rate varied according to the used insecticide and the parasitoid stage. There was no emergence for the parasitoid treated with Lambda-cyhalothrin, spinosad, and fenitrothion (Sumithon) one, two or four days after parasitism. On the other hand, El-Wakeil et al (2006) reported that there was no serious side effect on parasitism and emergence rates of *T. pretiosum* (Riley) and *T. minu‐ tum* (Riley) when treated with neem products. Similarly, neem products achieved a good control of *H. armigera* in greenhouse. Therefore, neem products are recommended for control‐

Assessment of the potential effects that pesticides have on the natural enemies is therefore an important part of IPM programs (Hirai 1993; Hassan 1994; Consoli et al. 1998; Takada et al. 2000). Detailed knowledge of the effects of different pesticides on the immature stages of natural enemies will help to determine the timing of sprays, thus avoiding the most susceptible stages (Campbell et al. 1991; Guifen and Hirai 1997). Mass breeding and release of parasitoids for control of various lepidopterous pests is now a commercial practice in many countries. However, the efficacy of the parasitoid is influenced a great deal by the insecticide spray schedule before and after parasitoid release. Candidate parasitoids for IPM programs should therefore be tested for susceptibility to the insecticides being used for controlling crop pests (Hassan et al. 1987). Egg parasitoids are known to be very effective against a number of crop pests. *Trichogramma dendrolimi* (Matsumura) has been described as a control agent for the pine moth, citrus swallowtail (Hirose 1986), *Spodoptera litura* (Hamada 1992), and other cruciferous insect pests (Dai et al. 1991). The cabbage moth, *Mamestra brassicae*(L.), is an important pest of ca. 20-51 species of plants (Hirata 1960). The use of broad-spectrum insecticides, however, has resulted in a decline in the natural enemies of *M. brassicae.* There are many research dealing with determining the susceptibility of *T. dendrolimi* to several insecticides, and evaluate its potential use for controlling the cabbage moth and other lepidopteran insects (Takada et al. 2000, 2001). Who tested toxicity of six insecticides, acephate, methomyl, ethofenprox, cartap, chlorfluazuron, and *Bacillus thuringiensis* (Bt) on different developmental stages of *Trichog‐ ramma dendrolimi* (Matsumura). Ethofenprox showed the highest toxicity and cartap showed relatively higher toxicity compared with the other insecticides. The development of the parasitoids treated with these two insecticides was normal, similar to that of the control group;

the same trend of results was also obtained by Vianna et al. (2009) and Shoeb (2010).

affected by the developmental stage when treated.

Suh et al (2000) investigated effect of insecticides on emergence, adult survival, and fitness parameters of *Trichogramma exiguum*. Insecticides tested were lambda cyhalothrin, cyper‐ methrin, thiodicarb, profenophos, spinosad, methoxyfenozide, and tebufenozide. All insecti‐ cides, with the exception of methoxyfenozide and tebufenozide, adversely affected *Trichogramma* emergence from *Helicoverpa zea* (Boddie) host eggs when exposed at different preimaginal stages of development (larval, prepupal, or pupal). However, the mean life span of emerged *T. exiguum* females significantly varied among insecticides, and was significantly

ling *Helicoverpa* and are compatible with mass release of *Trichogramma*.

6 Insecticides - Development of Safer and More Effective Technologies

Since the successful eradication of *A. grandis* in North Carolina, heliothines [predomi‐ nantly *Helicoverpa zea* (Boddie)] have emerged as the primary mid to late season insect pest in North Carolina cotton (Bacheler 1998). Thus, most of the foliar insecticide applica‐ tions (generally pyrethroids) made to cotton in North Carolina are aimed for control of the heliothine complex, *H. zea* and *Heliothis virescens* (F.). Unfortunately, these commonly used insecticides also are toxic to many non target organisms, including predators and parasitoids. Additionally, some heliothine pests (particularly *H. virescens*) have developed resistance to pyrethroids in some cotton growing areas. In an attempt to combat insecti‐ cide resistance, conserve arthropod natural enemies, and reduce health risks, several new insecticides (e.g., tebufenozide, methoxyfenozide, spinosad) have been developed and tested against lepidopteran pests in cotton (Bull & House 1983; Stapel et al. 2000; Vianna et al. 2009). Also, there is very important studies regarding the compatibility of these rel‐ atively new compounds with *Trichogramma* wasps, such as the detailed study involving *T. pretiosum* and tebufenozide (Cônsoli et al. 1998) with Neem (El-Wakeil et al. 2006) and with other biocontrol agent *Chrysoperla carnea* (El-Wakeil & Vidal 2005).

#### **Example: Side effect on parasitism rates of** *T. pretiosum* **and** *T. minutum* **on** *Helicoverpa* **eggs**

El-Wakeil et al. (2006) reported that their results indicated that NeemAzal-T/S reduced the parasitism rates to 50, 48.9, 71.1 and 73.3 % at 2, 1, 0.5, 0.25% cons, respectively (Fig. 2A), compared to 96.6% on control plants. NeemAzal PC 05 reduced the parasitism rates to 70, 67.8, 70 and 80% on succeeding concentrations; 2, 1, 0.5 and 0.25%. Neem blanks achieved a less side effect on *T. pretiosum*. NeemAzal Blank reduced the parasitism rates to 81.1%. NeemAzal PC05 Blank reduced the parasitism rates to 91.3% compared to 98.7% on control plants (Fig. 2A). El-Wakeil et al. (2006) mentioned further that NeemAzal-T/S had reduced the parasitism rates, to 40, 55.4, 77.8 and 81.3 % (at 2, 1, 0.5 and 0.25% cons.), respectively, compared to 93.3% on control plants. NeemAzal PC 05 reduced the parasitism rates to 82.2, 82.2, 74.4 and 83.3% on succeeding concentrations; 2, 1, 0.5 and 0.25% (Fig. 2B). Neem blanks achieved a less side effect on *T. minutum*. Parasitism rates reached to 74.4% in neem blanks. Parasitism rates were reduced by NeemAzal PC05 Blank to 86.7% compared to 93.3% on control plants (Fig. 2B).

released at six weekly intervals 1, 2, 6 and 24h after application of NIM-20 at 2.5g/l. No negative

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Srinivasa Babu et al. (1996) studied the effects of neem-based commercial insecticides such as Repelin and Neemguard on *T. australicum* in laboratory and field conditions. They reported that both the insecticides were relatively safe at lower concentrations but higher concentrations adversely affected the parasitoids both in laboratory and in field. Effects of insecticides on the emergence of *T. japonicum* from eggs of *Corcyra cephalonica* on the third or sixth day after parasitization using chlorpyrifos, quinalphos, monocrotophos, cypermethrin, dimethoate, phosphamidon, fenvalerate, Biolep and Bioasp (both Btk products) and NeemAzal-F and Fortune Aza (both neem-based products) clearly indicate that Bt and neem products had the least effect on the emergence of parasitoids, similar results were stated by Koul & Wahab (2004). On the other hand, fenvalerate and monocrotophos had the least effect while quinal‐ phos had the most. Adult emergence was relatively less when eggs were sprayed on the sixth day after parasitization compared to third day after parasitization (Borah & Basit 1996). Similar results were obtained against *T. japonicum* using Econeem and NeemAzal-T/S (0.1-1.0 %) (Lakshmi et al. 1998). On the whole it has been assessed that neem products were fairly safe to *Trichogramma* spp. (Sreenivasa & Patil 1998; Sarode & Sonalkar 1999a; Koul & Wahab 2004).

However, some neem formulations such as Nimbecidine (0.25-4.0%), Neemgold (2.0-4.0%) and Rakshak (1.0%) are reported to possess adverse effects on parasitism (Lakshmi et al. 1998; Koul & Wahab 2004). Raguraman and Singh (1999) tested in detail the neem seed oil at concentra‐ tions of 5.0, 2.5, 1.2, 0.6 and 0.3% for oviposition deterrence, feeding deterrence, toxicity, sterili‐ ty and insect growth regulator effects against *Trichogramma chilonis*. Neem seed oil at 0.3% deterred oviposition (parasitization) by the parasitoid but the sensitivity varied considerably both under choice and no-choice conditions. Neem seed oil also deterred feeding at or above 1.2% concentration both in choice and no-choice tests. In feeding toxicity tests, neem seed oil at 5% concentration caused < 50% mortality to both males and females but in contact toxicity tests, females were affected sparing males. No sterility effect was observed when the parasitoid was fed with neem seed oil treated honey. Both pre-and post-treatment of host eggs revealed no ad‐ verse effects on the development of the parasitoid, the same trend of results was obtained by Saikia & Parameswaran (2001). Thakur & Pawar (2000) tested two neem-based insecticides (3g Achook/litre and 2 ml Neemactin/litre), two biopesticides [1 g Halt (cypermethrin)/litre] and 1 ml Dipel (Btk)/litre], and endosulfan (1.5 ml/litre) in the laboratory for their relative toxicity to newly emerged adults of *T. chilonis*. Results revealed that neem-based pesticides and biopesti‐ cides were harmless while endosulfan was slightly toxic to egg parasitoid. These observations also get support from the studies on different groups of moult inhibitors and biopesticides

against rice leaf folder, *C. medinalis* and its parasitoid *T. chilonis* (Koul & Wahab 2004).

Schneider & Madel (1991) reported that there was no adverse effect on adults of the braconid *Diadegma semiclausum* after exposure for 3 days or during their lifetime in cages to residues of an aqueous NSKE (0.1- 5%). The longevity of the wasps exposed to neem residues was even prolonged but the difference between treated and untreated individuals was statistically not

**2.2. Larval and larval/ pupal parasitoids**

effect was observed as up to 84% of the eggs of the pest were parasitized.

Figure 2. Effect of neem products on parasitism rates of *Trichogramma pretiosum* (A) and *T. minutum* (B) on *Helicoverpa armigera* eggs in the greenhouse. Different letters indicate significant differences. **Figure 2.** Effect of neem products on parasitism rates of *Trichogrammapretiosum* (A) and *T. minutum* (B) on Helicover‐ *pa armigera* eggs in the greenhouse. Different letters indicate significant differences.

**Fig. 3 Effect of neem products on parasitism rates of** *Trichogramma* **spp.on** *Helicoverpa* **eggs in the greenhouse**

Li et al. (1986) tested 29 insecticides including Bt & Non Bt in order to study their side-effects on *Trichogramma japonicum* in the laboratory. The authors concluded from the results that Bt & Non Bt were the safest pesticides for the parasitoid. Klemm & Schmutterer (1993) applied NSKE (2.5% and 3%) against *Trichogramma* spp., egg-parasitoids of the diamondback moth, *Plutella xylostella. T. principium* accepted neem- treated eggs in the laboratory and *T. pretiosum* in the field but two treatments prevented the eclosion of adult parasitoids from treated *P. xylostella* eggs completely. Spraying of eggs with 0.2% NO reduced the number of eggs parasitized per female wasp by 13.3. As a further side-effect, Non Bt reduced the emergence of *T. principium* from treated eggs by 45.1%*.* Lyons et al. (1996, 2003) offered neem-treated eggs of *Ephestia kuehniellu* in shell vials to single females of *Trichogramma minutum* for parasitation. The eggs were fixed with adhesive to strips and held until all parasitoids had emerged from them. Azatin, Neem EC (experim. formul. 4.6% aza) and pure aza were tested at concns. of 50 g and 500 g/ha. At 50 g/ha no significant effect was observed, at 500 g/ha Azatin and Neem EC reduced the female survival by 64% and 40% respectively whereas pure aza showed no effect. Likewise, at 500 g/ha the number of parasitized eggs was reduced by 89% by Azatin, 29% by Neem EC but not reduced by aza. The parasitoid's development success was reduced by all treatments. Cano & Gladstone (1994) studied the influence of the NSK-based extract NIM-20 on parasitization of eggs of *Helicoverpa zea* in a melon field in Nicaragua. Mass-reared *T. pretiosum* were released at six weekly intervals 1, 2, 6 and 24h after application of NIM-20 at 2.5g/l. No negative effect was observed as up to 84% of the eggs of the pest were parasitized. Srinivasa Babu et al. (1996) studied the effects of neem-based commercial insecticides such as Repelin and Neemguard on *T. australicum* in laboratory and field conditions. They reported that both the insecticides were relatively safe at lower concentrations but higher concentrations adversely affected the parasitoids both in laboratory and in field. Effects of insecticides on the emergence of *T. japonicum* from eggs of *Corcyra cephalonica* on the third or sixth day after parasitization using chlorpyrifos, quinalphos, monocrotophos, cypermethrin, dimethoate, phosphamidon, fenvalerate, Biolep and Bioasp (both Btk products) and NeemAzal-F and Fortune Aza (both neem-based products) clearly indicate that Bt and neem products had the least effect on the emergence of parasitoids, similar results were stated by Koul & Wahab (2004). Of the other insecticides, fenvalerate and monocrotophos had the Li et al. (1986) tested 29 insecticides including Bt & Non Bt in order to study their side-effects on *Trichogramma japonicum* in the laboratory. The authors concluded from the results that Bt & Non Bt were the safest pesticides for the parasitoid. Klemm & Schmutterer (1993) applied NSKE (2.5% and 3%) against *Trichogramma* spp., egg-parasitoids of the diamondback moth, *Plutella xylostella. T. principium* accepted neem- treated eggs in the laboratory and *T. pretio‐ sum* in the field but two treatments prevented the eclosion of adult parasitoids from treated *P. xylostella* eggs completely. Eggs treatment with 2% neem oil (NO) reduced the number of eggs parasitized per female wasp by 13.3. As a further side-effect, Non Bt reduced the emergence of *T. principium* from treated eggs by 45.1%. Lyons et al. (1996, 2003) offered neemtreated eggs of *Ephestia kuehniellu* in shell vials to single females of *Trichogramma minutum* for parasitation. The eggs were fixed with adhesive to strips and held until all parasitoids had emerged from them. Azatin, Neem EC (experim. formul. 4.6% aza) and pure aza were tested at concns. of 50 g and 500 g/ha. At 50 g/ha no significant effect was observed, at 500 g/ha Azatin and Neem EC reduced the female survival by 64% and 40% respectively whereas pure aza showed no effect. Likewise, at 500 g/ha the number of parasitized eggs was reduced by 89% by Azatin, 29% by Neem EC but not reduced by aza. The parasitoid's development success was reduced by all treatments.

least effect while quinalphos had the most. Adult emergence was relatively less when eggs were sprayed on the sixth day after parasitization compared to third day after parasitization (Borah & Basit 1996). Similar results were obtained against *T. japonicum*  using Econeem and NeemAzal-T/S (0.1-1.0 %) (Lakshmi et al. 1998). On the whole it has been assessed that neem products were fairly safe to *Trichogramma* spp. (Sreenivasa & Patil 1998; Sarode & Sonalkar 1999a; Koul & Wahab 2004). Cano & Gladstone (1994) studied the influence of the NSK-based extract NIM-20 on parasiti‐ zation of eggs of *Helicoverpa zea* in a melon field in Nicaragua. Mass-reared *T. pretiosum* were

released at six weekly intervals 1, 2, 6 and 24h after application of NIM-20 at 2.5g/l. No negative effect was observed as up to 84% of the eggs of the pest were parasitized.

Srinivasa Babu et al. (1996) studied the effects of neem-based commercial insecticides such as Repelin and Neemguard on *T. australicum* in laboratory and field conditions. They reported that both the insecticides were relatively safe at lower concentrations but higher concentrations adversely affected the parasitoids both in laboratory and in field. Effects of insecticides on the emergence of *T. japonicum* from eggs of *Corcyra cephalonica* on the third or sixth day after parasitization using chlorpyrifos, quinalphos, monocrotophos, cypermethrin, dimethoate, phosphamidon, fenvalerate, Biolep and Bioasp (both Btk products) and NeemAzal-F and Fortune Aza (both neem-based products) clearly indicate that Bt and neem products had the least effect on the emergence of parasitoids, similar results were stated by Koul & Wahab (2004). On the other hand, fenvalerate and monocrotophos had the least effect while quinal‐ phos had the most. Adult emergence was relatively less when eggs were sprayed on the sixth day after parasitization compared to third day after parasitization (Borah & Basit 1996). Similar results were obtained against *T. japonicum* using Econeem and NeemAzal-T/S (0.1-1.0 %) (Lakshmi et al. 1998). On the whole it has been assessed that neem products were fairly safe to *Trichogramma* spp. (Sreenivasa & Patil 1998; Sarode & Sonalkar 1999a; Koul & Wahab 2004).

However, some neem formulations such as Nimbecidine (0.25-4.0%), Neemgold (2.0-4.0%) and Rakshak (1.0%) are reported to possess adverse effects on parasitism (Lakshmi et al. 1998; Koul & Wahab 2004). Raguraman and Singh (1999) tested in detail the neem seed oil at concentra‐ tions of 5.0, 2.5, 1.2, 0.6 and 0.3% for oviposition deterrence, feeding deterrence, toxicity, sterili‐ ty and insect growth regulator effects against *Trichogramma chilonis*. Neem seed oil at 0.3% deterred oviposition (parasitization) by the parasitoid but the sensitivity varied considerably both under choice and no-choice conditions. Neem seed oil also deterred feeding at or above 1.2% concentration both in choice and no-choice tests. In feeding toxicity tests, neem seed oil at 5% concentration caused < 50% mortality to both males and females but in contact toxicity tests, females were affected sparing males. No sterility effect was observed when the parasitoid was fed with neem seed oil treated honey. Both pre-and post-treatment of host eggs revealed no ad‐ verse effects on the development of the parasitoid, the same trend of results was obtained by Saikia & Parameswaran (2001). Thakur & Pawar (2000) tested two neem-based insecticides (3g Achook/litre and 2 ml Neemactin/litre), two biopesticides [1 g Halt (cypermethrin)/litre] and 1 ml Dipel (Btk)/litre], and endosulfan (1.5 ml/litre) in the laboratory for their relative toxicity to newly emerged adults of *T. chilonis*. Results revealed that neem-based pesticides and biopesti‐ cides were harmless while endosulfan was slightly toxic to egg parasitoid. These observations also get support from the studies on different groups of moult inhibitors and biopesticides against rice leaf folder, *C. medinalis* and its parasitoid *T. chilonis* (Koul & Wahab 2004).

#### **2.2. Larval and larval/ pupal parasitoids**

**Fig. 3 Effect of neem products on parasitism rates of** *Trichogramma* **spp.on** *Helicoverpa* **eggs in the greenhouse**

Figure 2. Effect of neem products on parasitism rates of *Trichogramma pretiosum* (A) and *T. minutum* (B) on *Helicoverpa armigera* eggs in the

**Figure 2.** Effect of neem products on parasitism rates of *Trichogrammapretiosum* (A) and *T. minutum* (B) on Helicover‐

Li et al. (1986) tested 29 insecticides including Bt & Non Bt in order to study their side-effects on *Trichogramma japonicum* in the laboratory. The authors concluded from the results that Bt & Non Bt were the safest pesticides for the parasitoid. Klemm & Schmutterer (1993) applied NSKE (2.5% and 3%) against *Trichogramma* spp., egg-parasitoids of the diamondback moth, *Plutella xylostella. T. principium* accepted neem- treated eggs in the laboratory and *T. pretiosum* in the field but two treatments prevented the eclosion of adult parasitoids from treated *P. xylostella* eggs completely. Spraying of eggs with 0.2% NO reduced the number of eggs parasitized per female wasp by 13.3. As a further side-effect, Non Bt reduced the emergence of *T. principium* from treated eggs by 45.1%*.* Lyons et al. (1996, 2003) offered neem-treated eggs of *Ephestia kuehniellu* in shell vials to single females of *Trichogramma minutum* for parasitation. The eggs were fixed with adhesive to strips and held until all parasitoids had emerged from them. Azatin, Neem EC (experim. formul. 4.6% aza) and pure aza were tested at concns. of 50 g and 500 g/ha. At 50 g/ha no significant effect was observed, at 500 g/ha Azatin and Neem EC reduced the female survival by 64% and 40% respectively whereas pure aza showed no effect. Likewise, at 500 g/ha the number of parasitized eggs was reduced by 89% by Azatin, 29% by Neem EC but not

Li et al. (1986) tested 29 insecticides including Bt & Non Bt in order to study their side-effects on *Trichogramma japonicum* in the laboratory. The authors concluded from the results that Bt & Non Bt were the safest pesticides for the parasitoid. Klemm & Schmutterer (1993) applied NSKE (2.5% and 3%) against *Trichogramma* spp., egg-parasitoids of the diamondback moth, *Plutella xylostella. T. principium* accepted neem- treated eggs in the laboratory and *T. pretio‐ sum* in the field but two treatments prevented the eclosion of adult parasitoids from treated *P. xylostella* eggs completely. Eggs treatment with 2% neem oil (NO) reduced the number of eggs parasitized per female wasp by 13.3. As a further side-effect, Non Bt reduced the emergence of *T. principium* from treated eggs by 45.1%. Lyons et al. (1996, 2003) offered neemtreated eggs of *Ephestia kuehniellu* in shell vials to single females of *Trichogramma minutum* for parasitation. The eggs were fixed with adhesive to strips and held until all parasitoids had emerged from them. Azatin, Neem EC (experim. formul. 4.6% aza) and pure aza were tested at concns. of 50 g and 500 g/ha. At 50 g/ha no significant effect was observed, at 500 g/ha Azatin and Neem EC reduced the female survival by 64% and 40% respectively whereas pure aza showed no effect. Likewise, at 500 g/ha the number of parasitized eggs was reduced by 89% by Azatin, 29% by Neem EC but not reduced by aza. The parasitoid's development success

Cano & Gladstone (1994) studied the influence of the NSK-based extract NIM-20 on parasitization of eggs of *Helicoverpa zea* in a melon field in Nicaragua. Mass-reared *T. pretiosum* were released at six weekly intervals 1, 2, 6 and 24h after application of NIM-20

Srinivasa Babu et al. (1996) studied the effects of neem-based commercial insecticides such as Repelin and Neemguard on *T. australicum* in laboratory and field conditions. They reported that both the insecticides were relatively safe at lower concentrations but higher concentrations adversely affected the parasitoids both in laboratory and in field. Effects of insecticides on the emergence of *T. japonicum* from eggs of *Corcyra cephalonica* on the third or sixth day after parasitization using chlorpyrifos, quinalphos, monocrotophos, cypermethrin, dimethoate, phosphamidon, fenvalerate, Biolep and Bioasp (both Btk products) and NeemAzal-F and Fortune Aza (both neem-based products) clearly indicate that Bt and neem products had the least effect on the emergence of parasitoids, similar results were stated by Koul & Wahab (2004). Of the other insecticides, fenvalerate and monocrotophos had the least effect while quinalphos had the most. Adult emergence was relatively less when eggs were sprayed on the sixth day after parasitization compared to third day after parasitization (Borah & Basit 1996). Similar results were obtained against *T. japonicum*  using Econeem and NeemAzal-T/S (0.1-1.0 %) (Lakshmi et al. 1998). On the whole it has been assessed that neem products were

Cano & Gladstone (1994) studied the influence of the NSK-based extract NIM-20 on parasiti‐ zation of eggs of *Helicoverpa zea* in a melon field in Nicaragua. Mass-reared *T. pretiosum* were

 **N.Azal T/S N.Azal Blank N.Azal PC05 N.Azal PC05 Blank Neem Products**

*pa armigera* eggs in the greenhouse. Different letters indicate significant differences.

reduced by aza. The parasitoid's development success was reduced by all treatments.

at 2.5g/l. No negative effect was observed as up to 84% of the eggs of the pest were parasitized.

fairly safe to *Trichogramma* spp. (Sreenivasa & Patil 1998; Sarode & Sonalkar 1999a; Koul & Wahab 2004).

**A)** *T. pretiosum*

8 Insecticides - Development of Safer and More Effective Technologies

**a a a**

**<sup>b</sup> <sup>b</sup> <sup>b</sup> <sup>b</sup> <sup>b</sup>**

**ab ab ab**

**a a**

**abab abab abab ab ab <sup>b</sup> b b b**

**a a**

**a a a a a ab ab abab ab ab ab b**

**<sup>a</sup> <sup>a</sup> ab**

**B)** *T. minutum*

**ab ababab ab abab abab ab ab**

**abab**

**a a a a**

**abab ab**

**a a**

**ab abababab**

**a a**

**ab ab**

**abab**

**c**

**c**

**bc <sup>b</sup> <sup>b</sup>**

**<sup>b</sup> <sup>b</sup> <sup>b</sup> bc**

**ab <sup>b</sup> ab b b**

**2% 1% 0.5% 0.25% Control**

 **N.Azal T/S N.Azal Blank N.Azal PC05 N.Azal PC05 Blank Neem Products**

**a a a a**

**ab ababab abababab ab**

**% Parasitism**

**Giza 86**

**Alex 4**

**Giza 89**

**c b c**

**b**

**bc <sup>c</sup> <sup>c</sup> c**

**ab**

**bc**

**bc c**

**ab ab**

**b**

greenhouse. Different letters indicate significant differences.

was reduced by all treatments.

**c**

**b**

> Schneider & Madel (1991) reported that there was no adverse effect on adults of the braconid *Diadegma semiclausum* after exposure for 3 days or during their lifetime in cages to residues of an aqueous NSKE (0.1- 5%). The longevity of the wasps exposed to neem residues was even prolonged but the difference between treated and untreated individuals was statistically not

significant. Females of the braconid, derived from larvae developed in neem-treated larvae of *P. xylostella,* showed no reduced fecundity or activity as compared with controls. Fresh extracts showed no repellent effect. The influence of aza on *Diadegma terebrans,* parasitoid of *Ostrinia nubilalis,* was investigated in the laboratory by Mccloskey et al. (1993). These authors added sublethal doses (0.1 ppm and 0.3 ppm) of aza or ethanol (carrier solvent) to diets of 2nd instar larvae of the pyralid. Both aza concns caused no significant difference of the parasitation percentage; host acceptance by the parasitoids was also not influenced. However, significantly higher mortality of parasitoids was observed in aza-treated groups compared with untreated groups, especially after emergence from the hosts. The duration of the larval instars in the hosts was prolonged and pupae weight and adults from treated groups was reduced.

Schauer (1985) reported that the aphid parasitoids *Diaeretiella rapae* and *Ephedrus cerasicola* developed normally after spraying of parasitized nymphs or mummies of *Myzus persicae,* using the neem products MeOH-NR (0.1%), AZT (0.05%) and MTB (0.01%) plus sesame oil. NO at concns of 0.5%, 1% and 2% did not reduce the rate of parasitism of *M. persicae* by *D. rapae,* but the emergence of adult wasps from aphid mummies collected from treated plants in the laboratory was reduced to 35, 24 and 0%, respectively, of the controls; similar results were obtained by Jenkins & Isaacs (2007) during their study about reducing the risk of insecticides for control of grape berry moth (Tortricidae) and conservation of its natural enemies, the same

Side Effects of Insecticides on Natural Enemies and Possibility of Their Integration in Plant Protection Strategies

http://dx.doi.org/10.5772/54199

11

In laboratory trials of Feldhege & Schmutterer (1993), using Margosan-0 as pesticide and *E. formosa,* parasitoid of *Trialeurodes vaporariorum,* as target insect, parasitized puparia of the whitefly were dipped in Margosan-0 solution containing 10 or 20 ppm aza. The lower concn showed little effect on the parasitoid emergence from the puparia and on longevity, but the higher concn caused a slight reduction of the walking activity of the wasps. Stark et al. (1992) studied under laboratory conditions the influence of aza on survival, longevity and reproduction of parasitoids of tephritid flies. The braconids *Psytallia incisi* and *Biosteres longicaudatus* developed in and eclosed from the tephritid *Bactrorera dorsalis* exposed in a diet to aza concns that inhibited adult eclosion. *Diachismomorpha tryoni* also eclosed from *Ceratitis capitata,* exposed to concns of aza that prevented eclosion of adult fruitflies. The longevity of parasitoids emerged from treated flies did not differ significantly from that of controls but reproduction of *P. incisi,* developed in flies exposed to 20 ppm aza, was reduced by 63-88%.

Stansly & Liu (1997) found that neem extract, insecticidal soap and sugar esters had little or no effect on *Encarsia pergandiella* the most abundant parasitoid of *Bemisia argentifolii* in south Florida vegetable fields and can contribute significantly to natural biological control of this and other whitefly species. Of the 10 species of leaf-mining Lepidoptera collected in apple orchards in south-western Germany in 1996, the most abundant were *Phyllonorycter blancar‐ della, Lyonetia clerkella* and *Stigmella malella* and a mining curculionid, *Rhamphus oxyacanthae*, the same trend of results was confirmed during studying effects of insecticides on two

Total parasitism by Chalcidoidea and Ichneumonoidea ranged from 10 to 29%. Use of a neem preparation for pest control had no effect on the rate of parasitism (Olivella & Vogt 1997). Sharma et al. (1999) also reported that the extracts from neem and custard apple kernels were effective against the spotted stem borer, *Chilo partellus*, Oriental army‐ worm, *Mythimna separata*, head bugs, *Calocoris angustatus*, and the yellow sugarcane aphid, *Melanaphis sacchari* in sorghum, but neem extract was non-toxic to the parasitoids and predators of the sorghum midge; as well other parasitoids as stated by Raguraman & Singh (1998, 1999). Sharma et al. (1984) reported that an active neem fraction of NSK had adverse effect on larval parasitoid, *Apanteles ruficrus* of Oriental armyworm, *M. sepa‐ rata*. Injection of 2.5 to 10µg of azadirachtin to newly ecdysed fourth and fifth instar lar‐ vae of host either partially inhibited or totally suppressed the first larval ecdysis of braconid, *Cotesia congregata* an internal larval parasitoid of tobacco hornworm, *Manduca*

The reproduction of other braconid species was not adversely affected.

parasitoids attacking *Bemisia argentifolii* by Jones et al. (1998).

vision was recorded by Desneux et al. (2007).

Schmutterer (1992, 1995, 2002) studied the side-effects of 10 ppm and 20 ppm of an azacontaining and an aza-free fraction of an aqueous NSKE, of AZT-VR-K and MTB/H,O-K-NR on *Cotesia glomerata,* a gregarious endoparasitoid of the larvae of the large cabbage white, *Pieris brassicae,* in Europe. When heavily parasitized 5th-instar larvae of the white were fed neemtreated cabbage leaves, numerous parasitoids could leave their moribund hosts, pupate and emerge as apparently normal wasps. On the other hand, high mortality was also recorded as many larvae could not spin a cocoon and adults were not able to emerge from normally looking cocoons. Intraspecific competition for food among larvae of *C. glomerata* in treated and untreated hosts could have been the main reason for high mortality, which was also observed in controls. In contrast, Osman & Bradley (1993) explained high mortality of C. *glomeraca* larvae and morphogenetic defects of adults derived troni larvae developed in neem-treated hosts mainly as effects of aza on the metamorphosis of the parasitoids. Spraying of high concns of AZT-VR-K on adult braconids and their contact with sprayed cabbage leaves for 2 days had no obvious effect on the wasps (Schmutterer 1992). Beckage et al. (1988) recorded that the development of *Cotesia congregata* was interrupted by aza in larvae of the tobacco hornworm.

According to Jakob & Dickler (1996) adults of the ectoparasitic, gregarious eulophid *Colporljp‐ cus floriis,* an important parasitoid of the tortricid *Adoxophyes orana,* were not adversely affected by application of NeemAzal-S (25 ppm and 100 ppm) in the laboratory and in the field, but 100% of the larvae died, apparently due to lack of appropriate food on the neem-treated decaying larvae of the host.

Hoelmer et al. (1990) evaluated the side effects of Margosan-O on parasitoids of the whitefly *Bemisia tabaci* and the aphid *Aphis gossypii* in the laboratory. The survival of the aphelinid *Eretmocerus calijornicus* was identical on treated and untreated hibiscus leaves, whereas the aphid parasitoids *Lysiphlebus testaceipes* (Aphidiidae) and *Aphelinus asychis* (Aphelinidae) showed more sensitivity to neem-treated leaf surfaces. *E. californicus* pairs in sealed Petri dishes with treated and untreated leaves survived for 5 days. Dipping of aphid mummies parasitized by *L. testaceipes* in Margosan-0 solution did not prevent the eclosion of the wasps. The same applied to the emergence of *Encarsia formosa* and *E. transversa* after dipping of parasitized puparia of *B. tabaci.* Only in the case of *E. calfornicus* was the emergence from treated whitefly puparia reduced by 50% as compared with untreated. Other researches had studied the toxicity of abamectin and spinosad on the parasitic wasp *Encarsia formosa* (van de Veire & Tirry 2003; van de Veire et al. 2004).

Schauer (1985) reported that the aphid parasitoids *Diaeretiella rapae* and *Ephedrus cerasicola* developed normally after spraying of parasitized nymphs or mummies of *Myzus persicae,* using the neem products MeOH-NR (0.1%), AZT (0.05%) and MTB (0.01%) plus sesame oil. NO at concns of 0.5%, 1% and 2% did not reduce the rate of parasitism of *M. persicae* by *D. rapae,* but the emergence of adult wasps from aphid mummies collected from treated plants in the laboratory was reduced to 35, 24 and 0%, respectively, of the controls; similar results were obtained by Jenkins & Isaacs (2007) during their study about reducing the risk of insecticides for control of grape berry moth (Tortricidae) and conservation of its natural enemies, the same vision was recorded by Desneux et al. (2007).

significant. Females of the braconid, derived from larvae developed in neem-treated larvae of *P. xylostella,* showed no reduced fecundity or activity as compared with controls. Fresh extracts showed no repellent effect. The influence of aza on *Diadegma terebrans,* parasitoid of *Ostrinia nubilalis,* was investigated in the laboratory by Mccloskey et al. (1993). These authors added sublethal doses (0.1 ppm and 0.3 ppm) of aza or ethanol (carrier solvent) to diets of 2nd instar larvae of the pyralid. Both aza concns caused no significant difference of the parasitation percentage; host acceptance by the parasitoids was also not influenced. However, significantly higher mortality of parasitoids was observed in aza-treated groups compared with untreated groups, especially after emergence from the hosts. The duration of the larval instars in the

10 Insecticides - Development of Safer and More Effective Technologies

hosts was prolonged and pupae weight and adults from treated groups was reduced.

Schmutterer (1992, 1995, 2002) studied the side-effects of 10 ppm and 20 ppm of an azacontaining and an aza-free fraction of an aqueous NSKE, of AZT-VR-K and MTB/H,O-K-NR on *Cotesia glomerata,* a gregarious endoparasitoid of the larvae of the large cabbage white, *Pieris brassicae,* in Europe. When heavily parasitized 5th-instar larvae of the white were fed neemtreated cabbage leaves, numerous parasitoids could leave their moribund hosts, pupate and emerge as apparently normal wasps. On the other hand, high mortality was also recorded as many larvae could not spin a cocoon and adults were not able to emerge from normally looking cocoons. Intraspecific competition for food among larvae of *C. glomerata* in treated and untreated hosts could have been the main reason for high mortality, which was also observed in controls. In contrast, Osman & Bradley (1993) explained high mortality of C. *glomeraca* larvae and morphogenetic defects of adults derived troni larvae developed in neem-treated hosts mainly as effects of aza on the metamorphosis of the parasitoids. Spraying of high concns of AZT-VR-K on adult braconids and their contact with sprayed cabbage leaves for 2 days had no obvious effect on the wasps (Schmutterer 1992). Beckage et al. (1988) recorded that the development of *Cotesia congregata* was interrupted by aza in larvae of the tobacco hornworm.

According to Jakob & Dickler (1996) adults of the ectoparasitic, gregarious eulophid *Colporljp‐ cus floriis,* an important parasitoid of the tortricid *Adoxophyes orana,* were not adversely affected by application of NeemAzal-S (25 ppm and 100 ppm) in the laboratory and in the field, but 100% of the larvae died, apparently due to lack of appropriate food on the neem-treated

Hoelmer et al. (1990) evaluated the side effects of Margosan-O on parasitoids of the whitefly *Bemisia tabaci* and the aphid *Aphis gossypii* in the laboratory. The survival of the aphelinid *Eretmocerus calijornicus* was identical on treated and untreated hibiscus leaves, whereas the aphid parasitoids *Lysiphlebus testaceipes* (Aphidiidae) and *Aphelinus asychis* (Aphelinidae) showed more sensitivity to neem-treated leaf surfaces. *E. californicus* pairs in sealed Petri dishes with treated and untreated leaves survived for 5 days. Dipping of aphid mummies parasitized by *L. testaceipes* in Margosan-0 solution did not prevent the eclosion of the wasps. The same applied to the emergence of *Encarsia formosa* and *E. transversa* after dipping of parasitized puparia of *B. tabaci.* Only in the case of *E. calfornicus* was the emergence from treated whitefly puparia reduced by 50% as compared with untreated. Other researches had studied the toxicity of abamectin and spinosad on the parasitic wasp *Encarsia formosa* (van de Veire & Tirry 2003;

decaying larvae of the host.

van de Veire et al. 2004).

In laboratory trials of Feldhege & Schmutterer (1993), using Margosan-0 as pesticide and *E. formosa,* parasitoid of *Trialeurodes vaporariorum,* as target insect, parasitized puparia of the whitefly were dipped in Margosan-0 solution containing 10 or 20 ppm aza. The lower concn showed little effect on the parasitoid emergence from the puparia and on longevity, but the higher concn caused a slight reduction of the walking activity of the wasps. Stark et al. (1992) studied under laboratory conditions the influence of aza on survival, longevity and reproduction of parasitoids of tephritid flies. The braconids *Psytallia incisi* and *Biosteres longicaudatus* developed in and eclosed from the tephritid *Bactrorera dorsalis* exposed in a diet to aza concns that inhibited adult eclosion. *Diachismomorpha tryoni* also eclosed from *Ceratitis capitata,* exposed to concns of aza that prevented eclosion of adult fruitflies. The longevity of parasitoids emerged from treated flies did not differ significantly from that of controls but reproduction of *P. incisi,* developed in flies exposed to 20 ppm aza, was reduced by 63-88%. The reproduction of other braconid species was not adversely affected.

Stansly & Liu (1997) found that neem extract, insecticidal soap and sugar esters had little or no effect on *Encarsia pergandiella* the most abundant parasitoid of *Bemisia argentifolii* in south Florida vegetable fields and can contribute significantly to natural biological control of this and other whitefly species. Of the 10 species of leaf-mining Lepidoptera collected in apple orchards in south-western Germany in 1996, the most abundant were *Phyllonorycter blancar‐ della, Lyonetia clerkella* and *Stigmella malella* and a mining curculionid, *Rhamphus oxyacanthae*, the same trend of results was confirmed during studying effects of insecticides on two parasitoids attacking *Bemisia argentifolii* by Jones et al. (1998).

Total parasitism by Chalcidoidea and Ichneumonoidea ranged from 10 to 29%. Use of a neem preparation for pest control had no effect on the rate of parasitism (Olivella & Vogt 1997). Sharma et al. (1999) also reported that the extracts from neem and custard apple kernels were effective against the spotted stem borer, *Chilo partellus*, Oriental army‐ worm, *Mythimna separata*, head bugs, *Calocoris angustatus*, and the yellow sugarcane aphid, *Melanaphis sacchari* in sorghum, but neem extract was non-toxic to the parasitoids and predators of the sorghum midge; as well other parasitoids as stated by Raguraman & Singh (1998, 1999). Sharma et al. (1984) reported that an active neem fraction of NSK had adverse effect on larval parasitoid, *Apanteles ruficrus* of Oriental armyworm, *M. sepa‐ rata*. Injection of 2.5 to 10µg of azadirachtin to newly ecdysed fourth and fifth instar lar‐ vae of host either partially inhibited or totally suppressed the first larval ecdysis of braconid, *Cotesia congregata* an internal larval parasitoid of tobacco hornworm, *Manduca* *sexta* (Feng & Wang 1984; Mani & Krishnamoorthy 1984; Peter & David 1988; Beckage et al. 1988). They also reported that the parasitoid growth was arrested, while the host lar‐ vae survived for two weeks or longer, following injection of azadirachtin but their para‐ sitoids never recovered and died encased within exuvial cuticle.

Augmentative releases of several coccinellid species are well documented and effective; how‐ ever, ineffective species continue to be used because of ease of collect ion (Obrycki & Kring 1998). About 90% of approximately 4,200 coccinellid species are considered beneficial because

Side Effects of Insecticides on Natural Enemies and Possibility of Their Integration in Plant Protection Strategies

http://dx.doi.org/10.5772/54199

13

Pesticides are highly effective, rapid in action, convenient to apply, usually economical and most powerful tools in pest management. However, indiscriminate, inadequate and improper use of pesticides has led to severe problems such as development of pest re‐ sistance, resurgence of target species, outbreak of secondary pests, destruction of benefi‐ cial insects, as well as health hazards and environmental pollution. It is therefore, a high time to evaluate the suitable products to be used in plant protection strategy. In an inte‐ grated control programme, it was necessary to utilize some insecticides with minimal toxicity to natural enemies of pests. Such practice might help to alleviate the problems of pest resurgence, which is frequently associated with insecticide up use in plant protec‐

*Coccinella undecimpunctata* L. (Coleoptera: Coccinellidae) is a euryphagous predator that feeds especially on aphids (Hodek & Honěk 1996). Given its voracity toward these pests, *C. undecimpunctata* offers interesting potential as a control agent in the context of Integrat‐ ed Pest Management (IPM) (ElHag 1992; Zaki et al. 1999a; Moura et al. 2006; Cabral et al. 2006, 2008, 2009). The success of IPM programs depends, in part, on the optimal use of selective insecticides that are less harmful to natural enemies (Tillman & Mulrooney 2000; Stark et al. 2007), which requires knowledge of their side-effects on the biological and be‐ havioural traits of these organisms (Tillman & Mulrooney 2000; Sechser et al. 2003; Youn et al. 2003; Bozski 2006; Stark et al. 2007). Some studies have been done to assess the sus‐ ceptibility of *C. undecimpunctata* to different insecticides but all, in some way, adversely affected this species (Salman & Abd-el-Raof 1979; Lowery & Isman 1995; Omar et al. 2002). Recent studies showed that, in general, pirimicarb and pymetrozine had no ad‐ verse effects on the biological traits (i.e. developmental time, fecundity, fertility, percent‐ age of egg hatch) of immature or adult stages of *C. undecimpunctata* when sprayed on the insects, which makes these chemicals potentially suitable to use in combination with *C.*

*undecimpunctata* for integrated control of sucking pests (Cabral et al. 2008, 2011).

The coccinellids predatory activity usually starts at medium high level of pest density, so the natural control is not quick, but is often effective. Untreated areas (such as edge rows) close to the orchards serve as refugia and play a strategic role in increasing biolog‐ ical control by coccinellids. The side effects (short term/ microscale) of several organo‐ phosphate and carbamate derived insecticides (commonly used to control tortricids, leafminers or scale pests in differnt orchards) against aphid-feeding coccinellid species were evaluated in fields tests in apple, pear and peach orchards according to the method described by Stäubli et al. (1985). The main species of aphid feeding coccinellids found were *Adalia bipunctata*, *C. septempunctata* & *Oenopia conglobata*, in order of population den‐

The influence of 7 pesticides (6 insecticides & 1 acaricide) on different stages (adults, larvae, eggs) of *C. septempunctata* and adults of *A. bipunctata* was evaluated under laboratory condi‐

of their predatory activity, mainly against homopterous insects and mites.

tion (Yadav, 1989; Meena et al. 2002).

sity observed (Pasqualini 1980; Brown 1989).

Stark et al. (1992) studied the survival, longevity and reproduction of the three braconid parasitoids namely *Psystallia incisi* and *Diachasmimorpha longicaudata* from *Bactrocera dorsalis* and *Diachasmimorpha tryoni* from *Ceratitis capitata*. They also studied the effect of azadirachtin concentration on these three parasitoids. Results of the first test were in conformity with Stark et al. (1990). All larvae that were exposed to sand treated with azadirachtin, pupated. Adult eclosion was concentration-dependent in both fly species, with little or no fly eclosion at 10 ppm. However, *P. incisi* and *D. longicaudata* successfully eclosed from pupae treated with < 10ppm azadirachtin. In all the cases after the exposure of azadirachtin, the adult eclosion was inhibited.

Facknath (1999) and Reddy & Guerrero (2000) evaluated biorational and regular insecti‐ cide applications for management of the diamondback moth *P. xylostella* in cabbage and side effects on aphid parasitoids and other beneficial insects; they reported that the these biocontrol agents were not affected by neem treatments, whereas Pirimor R treatments re‐ duced beneficial insect numbers. Although Pirimor R would be the preferred choice for immediate aphid control through contact action in commercial crop production, neem still has a place in the control of aphids in situations such as organic crop production, or in crops where resistance to other chemicals by aphids or their natural enemies has re‐ sulted (Stark & Wennergren 1995; Holmes et al. 1999; Hoelmer et al 1999).

Perera et al. (2000) studied the effect of three feeding deterrents: denatonium benzoate, azadirachtin and Pestistat on 4th instar larvae of *Chrysodeixis eriosoma* and *P. xylostella* and on the parasitoid, *Cotesia plutellae*. Their results suggested that the three antifeedants were effective in managing cabbage pests, *C. eriosoma* and *P. xylostella* and could be used in integrated pest management programmes. Denatonium benzoate was comparatively safer to the parasitoids *C. plutellae*.

Bruhnke et al. (2003) evaluated effects of pesticides on the wasp *Aphidius rhopalosiphi*. They emphasize that whole-plant test designs seemed to be more attractive to the wasps than single leaves and there were no harmful side effects. Similar results were mentioned by Mead-Briggs (2008) and Dantinne & Jansen (2008).
