**5. Side effects on predatory spiders and mites**

ingestion of spinosad in artificial diet resulted in rapid death in *C. carnea* adults. After 7 days of ingestion, all tested adults in the three highest concentrations were dead compared to 100% of adult survival in control (Fig. 3). He mentioned also that spinosad ingestion had a profound effect on fecundity of *C. carnea*. In the three highest concentrations, almost all eggs were laid on the first two days after spinosad ingestion, and then surviving adults stopped laying eggs

**Figure 3.** Rate of *C. carnea* adult survival after feeding on spinosad treated artificial diet from the onset of oviposition,

**Figure 4.** Influence of spinosad concentration on fecundity of *C. carnea* adults when fed with treated artificial diet

from the onset of oviposition FR = field rate (*n*=8) (after Mandour 2009).

until death (Fig. 4).

18 Insecticides - Development of Safer and More Effective Technologies

FR = field rate (*n*=8) (after Mandour 2009).

There is an increasing interest in the ecology of polyphagous predators (e.g. Araneae) in agriculture. Spiders are important natural enemies of many insect pests, as they are generalist predators and comprise a large part of the beneficial arthropod community in agricultural fields (Nyffeler 1982; Riechert & Lockley 1984; Sunderland et al. 1986; Young & Lockley 1985; Everts 1990), and a number of case studies in different crops (e.g. Mansour et al. 1981; Nyffeler & Benz 1987, 1988) show that spiders can indeed be effective pest control agents in many situations. However spiders are also easily affected by pesticides (Boller et al. 1989; Everts et al. 1989; Aukema et al. 1990; Volkmar 1995, 1996; Volkmar & Wetzel 1993; Volkmar & Schier 2005; Volkmar et al. 1992, 1996 a, b, 2003, 2004).

Agricultural entomologists recorded the importance of spiders as a major factor in regulating pest and they have been considered as important predators of insect pests and serve as a buffer to limits the initial exponential growth of prey population (Volkmar 1996; Snyder & Wise 1999; Nyffeler 2000; Sigsgaard 2000; Maloney et al. 2003; Venturino et al. 2008; Chatterjee et al. 2009; Jayakumar & Sankari 2010). However researchers have exposed those spiders in rice field can play an important role as predators in reducing plant hoppers and leafhoppers (Visarto et al. 2001; Lu Zhong- Xian 2006, 2007). Several workers reported the predatory potency of spiders in rice ecosystem (Samiyyan 1996; Sahu et al. 1996; Pathak & Saha 1999; Sigsgaard 2000; Vanitha 2000; Mathirajan 2001; Sunil Jose et al. 2002; Satpathi 2004; Sudhikumar et al. 2005; Sebastian et al. 2005; Motobayashi et al. 2006). According to Peter (1988), the crop having more insects or insect visitors always had more spiders.

Many studies have demonstrated that spiders can significantly reduce prey densities. Lang et al. (1999) found that spiders in a maize crop depressed populations of leafhoppers (Cicadelli‐ dae), thrips (Thysanoptera), and aphids (Aphididae). The three most abundant spiders in win‐ ter wheat, *Pardosa agrestis* (Westring) and two species of Linyphiidae, reduced aphid populations by 34% to 58% in laboratory studies (Volkmar et al. 1992, 1996 a, b; Feber et al. 1998; Yardim & Edwards 1998; Marc et al. 1999; Nyffeler 1999; Holland et al. 2000). Both web-weav‐ ing and hunting spiders limited populations of phytophagous Homoptera, Coleoptera, and Diptera in an old field in Tennessee (Riechert & Lawrence 1997). Spiders have also proven to be effective predators of herbivorous insects in apple orchards, including the beetle *Anthonomus pomorum* Linnaeus, and Lepidoptera larvae in the family Tortricidae (Marc & Canard 1997; Buchholz & Kreuels 2009). In no-till corn, wolf spiders (Lycosidae) reduce larval densities of ar‐ myworm (Laub & Luna 1992). Wolf spiders also reduced densities of sucking herbivores (Del‐ phacidae & Cicadellidae) in tropical rice paddies (Fagan et al. 1998). Spiders are capable of reducing populations of herbivores that may not be limited by competition and food availabili‐ ty in some agroecosystems (Buchsbaum 1996; Sunderland 1999; Lemke 1999).

Among the identified species, *Lycosa pseudoannulata* (Boes & Stand) was the most prevalent fol‐ lowed by *Atypena formosana* (Oi), *Argiope catenulate* (Doleschalland) *Clubiona japonicola* (Boesen‐ berg and Strand) (Sahu et al. 1996). The population of these four species also varied at different growth stages of rice (Heong et al. 1992). In the first 35 DAT of rice, *Pardosa pseudoannulata* and *Atypena formosana* are considered as the important predators of Green leafhopper (Sahu et al. 1996; Mathirajan, 2001). Moreover *P. pseudoannulata* is the vital predator against brown plant hopper and can also effectively regulate the pest population of Leafhoppers Plant hoppers, Whorl maggot flies, leaf folders, Case worms and Stem borers (Kenmore et al. 1984; Barrion & Litsinger, 1984; Rubia et al. 1990; Ooi & Shepard 1994; Visarto et al. 2001; Drechsler & Settele 2001; Lu Zhong-xian et al. 2006).

pest insects. Spiders of several families are commonly found in agroecosystems in winter wheat and many have been documented as predators of major crop pest species and families (Roach 1987; Nyffeler & Benz 1988; Riechert & Bishop 1990; Young & Edwards 1990; Fagan & Hurd 1991; Nyffeler et al. 1992; Marc & Canard 1997; Wisniewska & Prokopy 1997; Fagan et al. 1998; Lang et al. 1999; Marc et al. 1999). Spiders may be important mortality agents of crop pests such as aphids, leafhoppers, planthoppers, fleahoppers, and Lepidoptera larvae (Rypstra

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

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

21

Many farmers use chemical pesticides to help control pests. An ideal biological control agent, therefore, would be one that is tolerant to synthetic insecticides. Although spiders may be more sensitive to insecticides than insects due in part to their relatively long life spans, some spiders show tolerance, perhaps even resistance, to some pesticides. Spiders are less affected by fungicides and herbicides than by insecticides (Yardim & Edwards 1998; Maloney et al. 2003). Spiders such as the wolf spider *Pardosa pseudoannulata* are highly tolerant of botanical insecti‐ cides such as Neem-based chemicals (Theiling & Croft 1988; Markandeya & Divakar 1999). Saxena et al. (1984) reported that the wolf spider, *Lycosa* (=*Pardosa*) *pseudoannulata*, an important predator of leafhoppers in rice fields in Asia, was not harmed by neem oil (NO) and alcoholic or aqueous NSKE. In fact, NO (3%) and aqueous NSKE (5%) were quite safe for the spiders, though endosulfan induced 100 per cent mortality of the predators (Fernandez et al. 1992). NSKE, NO or NCE (10%) treated rice plots had better recolonization of spider *L. pseudoannulata* than in monocrotophos (0.07%) treated plots after seven days of treatment (Raguraman 1987; Raguraman & Rajasekaran 1996). The same neem products also spared the predatory mirid bug, *C. lividipennis* (Mohan 1989). The population of *L. pseudoannulata* and *C. lividipennis* were reported to be unaffected by different neem seed kernel extracts in paddy crop (Saxena 1987, 1989; Jayaraj et al. 1993). Similar observation on rice crop was made by Nirmala & Balasubra‐ manian (1999) who studied the effects of insecticides and neem based formulations on the pred‐

Samu & Vollrath (1992) assessed a bioassay to test (ultimately in the field) such hidden effects of agrochemicals in their application concentrations. As a paradigm we chose the web- building behaviour of the cross spider *Araneus diadematus* Clerck (Araneidea) and we selected four commonly used pesticides: Oleo Rustica 11E (mild insecticide), Fastac (pyrethroid insecticide), Bayfidan and Sportak (fungicides). Neither fungicides nor the mild insecticide seem to affect web-building behaviour significantly, whereas the pyreth‐ roid insecticide suppressed web-building frequency and severely affected web size and

There are also some studies that prove the neem's lack of toxicity against spiders and mites. Like *Cheiracanthium mildei* (predator of citrus fruit) with its prey *Tetranychus cinnabarinus* that is highly susceptible to neem (Mansour et al. 1986). *Phytoseiulus persimilis* is also not harmed by NSE, specially its fecundity while *T. cinnabarinnus* is up to 58 times more toxic than it (Mansour et al. 1987); the same trend of results was stated by Schmutterer (1997, 1999). Mansour et al. (1993, 1997) reported that the commercial products namely Margosan-O, Azatin and RD9 Repelin showed no toxicity to the spider. Serra (1992) observed that the neem products were not at all toxic to spider predators. Nandakumar & Saradamma (1996) observed

et al. 1999; Maloney et al. 2003).

atory spiders of riceecosystem.

building accuracy.

Samiyyan & Chandrasekaran (1998) reported spiders were effective against leaf folders, Cut worms and Stem borers. *Atypena formosana* has been observed to hunt the nymphs of plant hoppers and Leafhoppers small dipterans, such as whorl maggot flies (Barrion & Litsiger 1984; Sigsgaard et al. 1999). According to Mathirajan (2001) *Tetragnatha java‐ nas,* is one of the common spider found in rice ecosystem and they effectively reduce the population of Green leafhopper s and brown plant hoppers. The feeding efficiency of four spiders, namely *Lycosa pseudoannulata, Clubiona japonicola, Argiope catenulate* and *Cal‐ litrichia formosana* were also studied.

Integrated Pest Management (IPM) aims to avoid harming natural crop spiders. For this, IPM, attempts to synchronize the timing of spraying of pesticides with the life cycle of the pests, their natural enemies (predatory spiders and mites) (Bostanian et al. 1984; Volkmar 1989; Volkmar & Wetzel 1992). IPM also endeavours to use chemicals that act selectively against pests but not against their enemies. Few studies actually investigate effects of insecticides other than their direct toxicity (usually LD50) on non-target animals. However, living organisms are finely tuned systems; a chemical does not have to be le‐ thal in order to threaten the fitness (physical as well as reproductive) of the animal, with un-predictable results on the structure of the biological community (Culin & Yeargan 1983; Volkmar & Schützel 1997; Volkmar & Schier 2005). Pesticides may affect the preda‐ tory and reproductive behaviour of beneficial arthropods short of having direct effects on their survival. Thus to show that a pesticide is relatively harmless, or indeed has no measurable effect at all, behavioural studies on the effects of sublethal dosages are neces‐ sary. Such studies are not often done, presumably because of their costs in methodologi‐ cal difficulties (Vollrath et al. 1990; Volkmar et al. 1998, 2002, 2004).

#### **5.1. Side effects on predatory spiders**

Agricultural fields that are frequently sprayed with pesticides often also have lower spider populations in winter wheat (Feber et al. 1998; Yardim & Edwards 1998; Holland et al. 2000; Amalin et al. 2001). In general, spiders are more sensitive than many pests to some pesticides, such as the synthetic pyrethroids, (cypermethrin and deltamethrin); the organophosphates, (dimethoate and malathion) and the carbamate, ( carbaryl). A decrease in spider populations as a result of pesticide use can result in an outbreak of pest populations (Marc et al. 1999; Holland et al. 2000; Maloney et al. 2003).

Spiders can lower insect densities, as well as stabilize populations, by virtue of their top-down effects, microhabitat use, prey selection, polyphagy, functional responses, numerical respons‐ es, and obligate predatory feeding strategies and we aim to review the literature on these topics in the following discussion. Nevertheless, as biological control agents, spiders must be present in crop fields and prey upon specific agricultural pests. Indeed, they are present and do eat pest insects. Spiders of several families are commonly found in agroecosystems in winter wheat and many have been documented as predators of major crop pest species and families (Roach 1987; Nyffeler & Benz 1988; Riechert & Bishop 1990; Young & Edwards 1990; Fagan & Hurd 1991; Nyffeler et al. 1992; Marc & Canard 1997; Wisniewska & Prokopy 1997; Fagan et al. 1998; Lang et al. 1999; Marc et al. 1999). Spiders may be important mortality agents of crop pests such as aphids, leafhoppers, planthoppers, fleahoppers, and Lepidoptera larvae (Rypstra et al. 1999; Maloney et al. 2003).

1996; Mathirajan, 2001). Moreover *P. pseudoannulata* is the vital predator against brown plant hopper and can also effectively regulate the pest population of Leafhoppers Plant hoppers, Whorl maggot flies, leaf folders, Case worms and Stem borers (Kenmore et al. 1984; Barrion & Litsinger, 1984; Rubia et al. 1990; Ooi & Shepard 1994; Visarto et al. 2001; Drechsler & Settele

Samiyyan & Chandrasekaran (1998) reported spiders were effective against leaf folders, Cut worms and Stem borers. *Atypena formosana* has been observed to hunt the nymphs of plant hoppers and Leafhoppers small dipterans, such as whorl maggot flies (Barrion & Litsiger 1984; Sigsgaard et al. 1999). According to Mathirajan (2001) *Tetragnatha java‐ nas,* is one of the common spider found in rice ecosystem and they effectively reduce the population of Green leafhopper s and brown plant hoppers. The feeding efficiency of four spiders, namely *Lycosa pseudoannulata, Clubiona japonicola, Argiope catenulate* and *Cal‐*

Integrated Pest Management (IPM) aims to avoid harming natural crop spiders. For this, IPM, attempts to synchronize the timing of spraying of pesticides with the life cycle of the pests, their natural enemies (predatory spiders and mites) (Bostanian et al. 1984; Volkmar 1989; Volkmar & Wetzel 1992). IPM also endeavours to use chemicals that act selectively against pests but not against their enemies. Few studies actually investigate effects of insecticides other than their direct toxicity (usually LD50) on non-target animals. However, living organisms are finely tuned systems; a chemical does not have to be le‐ thal in order to threaten the fitness (physical as well as reproductive) of the animal, with un-predictable results on the structure of the biological community (Culin & Yeargan 1983; Volkmar & Schützel 1997; Volkmar & Schier 2005). Pesticides may affect the preda‐ tory and reproductive behaviour of beneficial arthropods short of having direct effects on their survival. Thus to show that a pesticide is relatively harmless, or indeed has no measurable effect at all, behavioural studies on the effects of sublethal dosages are neces‐ sary. Such studies are not often done, presumably because of their costs in methodologi‐

Agricultural fields that are frequently sprayed with pesticides often also have lower spider populations in winter wheat (Feber et al. 1998; Yardim & Edwards 1998; Holland et al. 2000; Amalin et al. 2001). In general, spiders are more sensitive than many pests to some pesticides, such as the synthetic pyrethroids, (cypermethrin and deltamethrin); the organophosphates, (dimethoate and malathion) and the carbamate, ( carbaryl). A decrease in spider populations as a result of pesticide use can result in an outbreak of pest populations (Marc et al. 1999;

Spiders can lower insect densities, as well as stabilize populations, by virtue of their top-down effects, microhabitat use, prey selection, polyphagy, functional responses, numerical respons‐ es, and obligate predatory feeding strategies and we aim to review the literature on these topics in the following discussion. Nevertheless, as biological control agents, spiders must be present in crop fields and prey upon specific agricultural pests. Indeed, they are present and do eat

cal difficulties (Vollrath et al. 1990; Volkmar et al. 1998, 2002, 2004).

2001; Lu Zhong-xian et al. 2006).

20 Insecticides - Development of Safer and More Effective Technologies

*litrichia formosana* were also studied.

**5.1. Side effects on predatory spiders**

Holland et al. 2000; Maloney et al. 2003).

Many farmers use chemical pesticides to help control pests. An ideal biological control agent, therefore, would be one that is tolerant to synthetic insecticides. Although spiders may be more sensitive to insecticides than insects due in part to their relatively long life spans, some spiders show tolerance, perhaps even resistance, to some pesticides. Spiders are less affected by fungicides and herbicides than by insecticides (Yardim & Edwards 1998; Maloney et al. 2003). Spiders such as the wolf spider *Pardosa pseudoannulata* are highly tolerant of botanical insecti‐ cides such as Neem-based chemicals (Theiling & Croft 1988; Markandeya & Divakar 1999).

Saxena et al. (1984) reported that the wolf spider, *Lycosa* (=*Pardosa*) *pseudoannulata*, an important predator of leafhoppers in rice fields in Asia, was not harmed by neem oil (NO) and alcoholic or aqueous NSKE. In fact, NO (3%) and aqueous NSKE (5%) were quite safe for the spiders, though endosulfan induced 100 per cent mortality of the predators (Fernandez et al. 1992). NSKE, NO or NCE (10%) treated rice plots had better recolonization of spider *L. pseudoannulata* than in monocrotophos (0.07%) treated plots after seven days of treatment (Raguraman 1987; Raguraman & Rajasekaran 1996). The same neem products also spared the predatory mirid bug, *C. lividipennis* (Mohan 1989). The population of *L. pseudoannulata* and *C. lividipennis* were reported to be unaffected by different neem seed kernel extracts in paddy crop (Saxena 1987, 1989; Jayaraj et al. 1993). Similar observation on rice crop was made by Nirmala & Balasubra‐ manian (1999) who studied the effects of insecticides and neem based formulations on the pred‐ atory spiders of riceecosystem.

Samu & Vollrath (1992) assessed a bioassay to test (ultimately in the field) such hidden effects of agrochemicals in their application concentrations. As a paradigm we chose the web- building behaviour of the cross spider *Araneus diadematus* Clerck (Araneidea) and we selected four commonly used pesticides: Oleo Rustica 11E (mild insecticide), Fastac (pyrethroid insecticide), Bayfidan and Sportak (fungicides). Neither fungicides nor the mild insecticide seem to affect web-building behaviour significantly, whereas the pyreth‐ roid insecticide suppressed web-building frequency and severely affected web size and building accuracy.

There are also some studies that prove the neem's lack of toxicity against spiders and mites. Like *Cheiracanthium mildei* (predator of citrus fruit) with its prey *Tetranychus cinnabarinus* that is highly susceptible to neem (Mansour et al. 1986). *Phytoseiulus persimilis* is also not harmed by NSE, specially its fecundity while *T. cinnabarinnus* is up to 58 times more toxic than it (Mansour et al. 1987); the same trend of results was stated by Schmutterer (1997, 1999). Mansour et al. (1993, 1997) reported that the commercial products namely Margosan-O, Azatin and RD9 Repelin showed no toxicity to the spider. Serra (1992) observed that the neem products were not at all toxic to spider predators. Nandakumar & Saradamma (1996) observed the activity of natural enemies in cucurbit fields, where neem-based pesticides were applied for the control of *Henosepilachna vigintioctopunctata*. Natural enemies observed in considerable numbers were *Tetrastichus* sp., *Chrysocoris johnsoni*, *Tetragnatha* sp., *Oxyopes* sp. and orb-web spiders, and neem product did not inflict any harm to them. Lynx spider, *Oxyopes javanus* was less sensitive To neem oil (NO) (50% EC) than *L. pseudoannulata* (LC50 values = 9.73 and 1.18%, respectively) (Kareem et al. 1988; Karim et al. 1992), thereby confirming that NO was the safest pesticide for spiders. In cornfields (Breithaupt et al. 1999) and cabbage fields (Saucke 1995) in Papua New Guinea no significant effect was observed against *Oxyopes papuanus* from aqueous NSKEs (2%) or NeemAzal-S treatments. Serra (1992) did not observe adverse effects from NSKE 4 per cent applied on unidentified spiders in tomato fields in the Caribbean.

successful utilization of biological control could depend on the compatibility of the natu‐ ral predators with pesticides. Studies on the side effects of pesticides on phytoseiid mites in Portugal have begun in 1995 (Rodrigues et al. 2002; Cavaco et al. 2003). Further re‐ search to evaluate these side effects of pesticides on all sensitive stages of the phytoseiid mites were conducted (Blümel et al. 2000; Broufas et al. 2008; Olszak & Sekrecka 2008).

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

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

23

The predatory mite *Phytoseiulus persimilis* (Athias-Henriot) is an economically important species in integrated mite pest management and biological control of spider mites in many countries throughout the world. Mass rearing and releasing natural enemies mainly phytoseiid mites are one of the goals of biological control of these pests in indoor and outdoor conditions (McMurtry & Croft 1997); additional food should be found for predatory mites (Pozzebon et al. 2005; Pozzebon & Duso (2008) in case of rareness of preys. For optimal biological mite management, it is important to know if acaricides have adverse undesirable effects on the predatory mites (Arbabi 2007). Nadimi et al. (2008) evaluated the toxic effects of hexythiazox (Nisorun®, EC 10%), fenpyroximate (Ortus®, SC 5%) and abamectin (Vertimec®, EC 1.8%) on *P. persimilis*. The results showed that the total effect values of all concentrations of hexythiazox were below the lower threshold thus it could be considered a harmless acaricide to this predatory mite. In contrast, the total effect of all concentrations of fenpyroximate, and field, as well as, one half the field concentration of abamectin were found toxic to predatory mite and above upper threshold. The overall results confirmed that *P. persimilis* is promise and crucial to develop IPM programs in agricultural crops; similar results were obtained by (Cloyd

There are many spider mites such as *Tetranycus urticae* (Koch), which is considered one of the most important mite pest species with a wide range of host plants (Herron & Rophail 1993; Bolland et al. 1998). Many efforts have been undertaken to manage *T. urticae* problems in agricultural crops such as the application of new acaricides with the lower concentrations and release of predacious mites such as *Phytoseiulus persimlis* in glasshouses on cucumbers (Arbabi 2007) and in fields of beans, cotton as well as soybeans (Daneshvar & Abaii 1994). It has gained increasing attention by research scientists in many parts of the world. Selective pesticides that can be used to control pests without adversely affecting important natural enemies are urgently needed. Testing programme represented by IOBC (International Organization for Biological Control), is not only meant to provide valuable information on the side effects of pesticides on beneficial organisms but it also gives the testing members an opportunity to improve testing techniques, compare results and exchange experience with colleagues in the

Biological control of these pests is increasing because of the pressure on growers to find alternatives to chemical pesticides (van Lenteren 2000). In the presence of chemical applica‐ tions, biological control of spider mites may be achieved by the selective use of pesticides that are less toxic to natural enemies than to pest species (Zhang & Sanderson 1990). Ruberson et al. (1998) suggested that selective pesticide were the most useful tool of integration of biological control agents into pest control programs. A strain of *P. persimilis* was introduced into Iran from the Netherlands (Department of Entomology, Wageningen Agricultural University) in 1988 (Daneshvar 1989) and it was effective in controlling spider mites under greenhouses and

et al. 2006, Pozzebon & Duso 2010).

Working Group (Hassan et al. 1991).

Babu et al. (1998) reported that a combination of seedling root dip in 1 percent neem oil emulsion for 12h + soil application of neem cake at 500 kg/ha + 1 per cent neem oil spray emulsion at weekly intervals gave an effective level of control of green leafhopper (*Nephotettix virescens*) infesting rice (var. Swarna). A combination of neem oil+urea at a ratio of 1:10 when applied three times at the basal, tillering and panicle initiation stages gave a superior level of control of brown planthopper (*Nilaparvata lugens*). The treatments, urea+nimin [neem seed extract] and a seedling root dip with 1 per cent neem oil emulsion+neem cake at 500 kg/ha+1 per cent neem oil spray emulsion at weekly intervals was equally effective against *N. lugens*. All neem products had little effect on predators, *C. lividipennis* and *L. pseudoannulata* (Sontakke 1993; Babu et al. 1998). NSKE sprays at 5, 10 and 20 per cent were also substantially safe for spiders and ants in cowpea ecosystems (Sithanantham et al. 1997).

Nanda et al. (1996) tested the bioefficacy of neem derivatives against the predatory spi‐ ders, wolf spiders (*L. pseudoannulata*), jumping spider (*Phidippus* sp), lynx spider (*Oxyopes* sp.), dwarf spider (*Callitrichia formosana*), orb spider (*Argiope* sp.), damselflies (*Agriocnemis* sp.) and mirid bug (*C. lividipennis*). It was observed that the neem kernel extract and oil were relatively safer than the insecticides to *L. pseudoannulata*, *Phidippus* sp. and *C. lividi‐ pennis* in field conditions. Markandeya & Divakar (1999) evaluated the effect of a com‐ mercial neem formulation (Margosan 1500 ppm) in the laboratory against two parasitoids and two predators. The formulation was tested at the field recommended dose of 10 ml/l. The neem formulation Margosan 1500 ppm was safe to all the four bio‐ agents studied viz., *T. chilonis, B. brevicornis, L. pseudoannulata* and *C. sexmaculata*. Spider population in rice ecosystem was the lowest in carbofuran treatment and highest in neem cake treatments. The mean predator population of *Ophionea indica, Paederus fuscipes, Lycosa* sp. and coccinellid beetles was significantly higher in plots with *Azolla* at 5 t/ha, with or without neem cake at 1.5 t/ha, in field trials conducted in southern Tamil Nadu, India under lowland rice irrigated conditions (Baitha et al. 2000).

#### **5.2. Side effects on predatory mites**

Members of the family Phytoseiidae show a remarkable ability to reduce red spider mite infestations. There are many behavioural aspects that need to be considered in the phy‐ tophagous and predacious mites. Recognizing these behaviours and the side effects of pesticides on predatory mites can increase the success of biological control. Therefore, successful utilization of biological control could depend on the compatibility of the natu‐ ral predators with pesticides. Studies on the side effects of pesticides on phytoseiid mites in Portugal have begun in 1995 (Rodrigues et al. 2002; Cavaco et al. 2003). Further re‐ search to evaluate these side effects of pesticides on all sensitive stages of the phytoseiid mites were conducted (Blümel et al. 2000; Broufas et al. 2008; Olszak & Sekrecka 2008).

the activity of natural enemies in cucurbit fields, where neem-based pesticides were applied for the control of *Henosepilachna vigintioctopunctata*. Natural enemies observed in considerable numbers were *Tetrastichus* sp., *Chrysocoris johnsoni*, *Tetragnatha* sp., *Oxyopes* sp. and orb-web spiders, and neem product did not inflict any harm to them. Lynx spider, *Oxyopes javanus* was less sensitive To neem oil (NO) (50% EC) than *L. pseudoannulata* (LC50 values = 9.73 and 1.18%, respectively) (Kareem et al. 1988; Karim et al. 1992), thereby confirming that NO was the safest pesticide for spiders. In cornfields (Breithaupt et al. 1999) and cabbage fields (Saucke 1995) in Papua New Guinea no significant effect was observed against *Oxyopes papuanus* from aqueous NSKEs (2%) or NeemAzal-S treatments. Serra (1992) did not observe adverse effects from

NSKE 4 per cent applied on unidentified spiders in tomato fields in the Caribbean.

spiders and ants in cowpea ecosystems (Sithanantham et al. 1997).

22 Insecticides - Development of Safer and More Effective Technologies

India under lowland rice irrigated conditions (Baitha et al. 2000).

**5.2. Side effects on predatory mites**

Babu et al. (1998) reported that a combination of seedling root dip in 1 percent neem oil emulsion for 12h + soil application of neem cake at 500 kg/ha + 1 per cent neem oil spray emulsion at weekly intervals gave an effective level of control of green leafhopper (*Nephotettix virescens*) infesting rice (var. Swarna). A combination of neem oil+urea at a ratio of 1:10 when applied three times at the basal, tillering and panicle initiation stages gave a superior level of control of brown planthopper (*Nilaparvata lugens*). The treatments, urea+nimin [neem seed extract] and a seedling root dip with 1 per cent neem oil emulsion+neem cake at 500 kg/ha+1 per cent neem oil spray emulsion at weekly intervals was equally effective against *N. lugens*. All neem products had little effect on predators, *C. lividipennis* and *L. pseudoannulata* (Sontakke 1993; Babu et al. 1998). NSKE sprays at 5, 10 and 20 per cent were also substantially safe for

Nanda et al. (1996) tested the bioefficacy of neem derivatives against the predatory spi‐ ders, wolf spiders (*L. pseudoannulata*), jumping spider (*Phidippus* sp), lynx spider (*Oxyopes* sp.), dwarf spider (*Callitrichia formosana*), orb spider (*Argiope* sp.), damselflies (*Agriocnemis* sp.) and mirid bug (*C. lividipennis*). It was observed that the neem kernel extract and oil were relatively safer than the insecticides to *L. pseudoannulata*, *Phidippus* sp. and *C. lividi‐ pennis* in field conditions. Markandeya & Divakar (1999) evaluated the effect of a com‐ mercial neem formulation (Margosan 1500 ppm) in the laboratory against two parasitoids and two predators. The formulation was tested at the field recommended dose of 10 ml/l. The neem formulation Margosan 1500 ppm was safe to all the four bio‐ agents studied viz., *T. chilonis, B. brevicornis, L. pseudoannulata* and *C. sexmaculata*. Spider population in rice ecosystem was the lowest in carbofuran treatment and highest in neem cake treatments. The mean predator population of *Ophionea indica, Paederus fuscipes, Lycosa* sp. and coccinellid beetles was significantly higher in plots with *Azolla* at 5 t/ha, with or without neem cake at 1.5 t/ha, in field trials conducted in southern Tamil Nadu,

Members of the family Phytoseiidae show a remarkable ability to reduce red spider mite infestations. There are many behavioural aspects that need to be considered in the phy‐ tophagous and predacious mites. Recognizing these behaviours and the side effects of pesticides on predatory mites can increase the success of biological control. Therefore,

The predatory mite *Phytoseiulus persimilis* (Athias-Henriot) is an economically important species in integrated mite pest management and biological control of spider mites in many countries throughout the world. Mass rearing and releasing natural enemies mainly phytoseiid mites are one of the goals of biological control of these pests in indoor and outdoor conditions (McMurtry & Croft 1997); additional food should be found for predatory mites (Pozzebon et al. 2005; Pozzebon & Duso (2008) in case of rareness of preys. For optimal biological mite management, it is important to know if acaricides have adverse undesirable effects on the predatory mites (Arbabi 2007). Nadimi et al. (2008) evaluated the toxic effects of hexythiazox (Nisorun®, EC 10%), fenpyroximate (Ortus®, SC 5%) and abamectin (Vertimec®, EC 1.8%) on *P. persimilis*. The results showed that the total effect values of all concentrations of hexythiazox were below the lower threshold thus it could be considered a harmless acaricide to this predatory mite. In contrast, the total effect of all concentrations of fenpyroximate, and field, as well as, one half the field concentration of abamectin were found toxic to predatory mite and above upper threshold. The overall results confirmed that *P. persimilis* is promise and crucial to develop IPM programs in agricultural crops; similar results were obtained by (Cloyd et al. 2006, Pozzebon & Duso 2010).

There are many spider mites such as *Tetranycus urticae* (Koch), which is considered one of the most important mite pest species with a wide range of host plants (Herron & Rophail 1993; Bolland et al. 1998). Many efforts have been undertaken to manage *T. urticae* problems in agricultural crops such as the application of new acaricides with the lower concentrations and release of predacious mites such as *Phytoseiulus persimlis* in glasshouses on cucumbers (Arbabi 2007) and in fields of beans, cotton as well as soybeans (Daneshvar & Abaii 1994). It has gained increasing attention by research scientists in many parts of the world. Selective pesticides that can be used to control pests without adversely affecting important natural enemies are urgently needed. Testing programme represented by IOBC (International Organization for Biological Control), is not only meant to provide valuable information on the side effects of pesticides on beneficial organisms but it also gives the testing members an opportunity to improve testing techniques, compare results and exchange experience with colleagues in the Working Group (Hassan et al. 1991).

Biological control of these pests is increasing because of the pressure on growers to find alternatives to chemical pesticides (van Lenteren 2000). In the presence of chemical applica‐ tions, biological control of spider mites may be achieved by the selective use of pesticides that are less toxic to natural enemies than to pest species (Zhang & Sanderson 1990). Ruberson et al. (1998) suggested that selective pesticide were the most useful tool of integration of biological control agents into pest control programs. A strain of *P. persimilis* was introduced into Iran from the Netherlands (Department of Entomology, Wageningen Agricultural University) in 1988 (Daneshvar 1989) and it was effective in controlling spider mites under greenhouses and outdoor conditions (Daneshvar & Abaii 1994). However, Biological control of spider mites using this predaceous mite is effective only against low population densities of the pest (Pralavorio et al. 1985). When the population densities are high an acaricide treatment is needed to reduce the pest population before release of beneficial mites (Malezieux et al. 1992; Bakker et al. 1992; Hassan et al. 1994). Although various aspect of pesticide effects on *P. persimilis* have been studied by many workers in the past (Samsøe-Petersen 1983; Zhang & Sanderson 1990; Oomen et al. 1991; Blümel et al. 1993, 2000; Blümel & Gross 2001; Blümel & Hausdorf 2002; Cloyd et al. 2006). Only Kavousi & Talebi (2003) investigated side-effects of heptenophos, malathion and pirimiphosmethyl on *P. persimilis*. Moreover, there is no adequate information on the susceptibility of many strains and species to other pesticides, especially acaricides (Zhang 2003).

Miles & Dutton (2003) conducted extended laboratory experiments, semi-field and field tests to examine effects of spinosad on predatory mites. Under extended laboratory conditions (exposure on natural substrates) no effects were seen on *Amblyseius cucumeris*, *Hypoaspis aculeifer* or *Hypoaspis miles* at rates up to 540 g a.i./ha. When *Phytoseiulus persimilis* was tested under semi-field conditions, spinosad was harmless at rates of 9.6, 19.2 and 36 g a.i./hL. No effects were noted to *Amblyseius californicus* at 19.2 g a.i./hL under semi-field conditions. In the field, single applications of spinosad at 48 or 96 g a.i./ha in vines caused no unacceptable effects to populations of *T. pyri* or *Kampimodromus aberrans*. It was concluded that spinosad was highly selective to most predatory mite species and that effects noted in tier I laboratory studies did not translate to higher tiers of testing or use in the field. The reason for this is not clear but could be due to agronomic practice, difference in species sensitivity, sublethal or behavioural effects or even effects on prey. However use patterns safe to predatory mites and compatible

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

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

25

Papaioannou et al. (2000) studied the effects of a NSKE (Neemark) and Bioryl(R) vegetable oils against phytophagous and predatory mites using bean leaves treated with different concen‐ trations. Neemark (3 and 5%) was moderately toxic to *T. urticae*, and highly toxic to *P. persimilis*. Other studies investigated the toxicological tests (acute and sublethal effects) of fungicides on predatory mites (Blümel et al. 2000; Auger et al. 2004; Bernard et al. 2004).

Conservation of predators in the field can be accomplished by reducing both chemical and physical disturbance of the habitat. Natural enemy densities and diversities are significantly higher in orchards and fields where no pesticides have been sprayed (Yardim and Edwards 1998; Marc et al. 1999; Holland et al. 2000; Amalin et al. 2001). Restricting insecticide treatment to crucial periods in the pest life cycle or limiting spraying to midday when many wandering natural enemies are inactive and in sheltered locations can help conserve spider numbers (Riechert & Lockley 1984). Natural enemies can recolonize if the interval between chemical applications is long enough, but several applications per season can destroy natural enemy communities. Some pesticides are also retained in the natural enemies and can be detrimental

Besides pesticides, other human practices that can disrupt natural enemy populations are mowing, plowing, harvesting, and crop rotation (Nyffeler et al 1994; Marc et al. 1999). Soil disturbance by plowing destroys overwintering sites and can kill any agent already present in the soil (Marshall & Rypstra 1999; Maloney et al. 2003). The movement of farm equipment through a crop field damages spider webs and may destroy web attach‐ ment sites (Young & Edwards 1990). Consequently, density and diversity of natural ene‐ mies are higher in organic fields than in conventional ones. For example, in cereal fields, Lycosidae made up only 2% of the community in conventional fields, but 11% in organic fields. Most lycosids were found in field edges (Marc et al. 1999). Clearly, human input is harmful to natural enemies, and the best spider conservation strategy may be non-in‐

**6. Conservation and enhancement of natural enemy assemblages**

with IPM have been developed for a wide range of crops.

to those spiders that ingest their webs daily (Marc et al. 1999).

tervention (Young & Edwards 1990; Maloney et al. 2003).

Bostanian et al. (2004) studied the toxicity of Indoxacarb to two predacious mites: *Amblyseius fallacis* (Garman) (Phytoseiidae) and *Agistemus fleschneri* (Summers) (Stigmaeidae). They reported that Indoxacarb had no adverse effects on *A. fallacis* and *A. fleschneri* adults, number of eggs laid by treated adults of both species and percent hatch of treated eggs of these two species, as stated also by Kim et al. (2000, 2005).

Rodrigues et al (2004) evaluated the toxicity of five insecticides (*Bacillus thuringiensis,* tebufe‐ nozide, flufenoxuron, phosalon and deltamethrin) on predatory mites (Acari: Phytoseiidae). The results were similar in both trials: phosalon and deltamethrin had a poor selectivity (harmful) on the phytoseiid mites, *Bacillus thuringiensis,* tebufenozide and flufenoxuron showed a good selectivity to these predators. The most abundant Phytoseiid species identified were *Phytoseius plumifer* (Canest & Fanzag) (91.8%) in Minho region and *Typhlodromus phialatus* Athias-Henriot (96.7%) in Castelo Branco region.

Cavaco et al (2003) studied evaluating the field toxicity of five insecticides on predatory mites (Acari: Phytoseiidae). The dominant species of phytoseiid in the region of Guarda was *Typhlodromus pyri* Scheuten (99.9%) and the dominant species in the region of Castelo Branco was *Typhlodromus phialatus* Athias-Henriot (96.4%). The results of imidacloprid showed good selectivity for phytoseiids while dimethoate was harmful. It was found that *T. pyri* was more tolerant to the other insecticides tested than *T. phialatus*. These results are of interest for the enhancement of integrated pest management programs. They suggest differences in suscept‐ ibility of *T. pyri* and *T. phialatus* to the tested insecticides, mainly to vamidothion.

Spinosad controls many caterpillar pests in vines, pome fruit and vegetables (including tomatoes and peppers), thrips in tomatoes, peppers and ornamental cultivation and dipterous leafminers in vegetables and ornamentals (Bylemans & Schoonejans 2000). Spinosad can be used to control pests in crops where the conservation of predatory mites is an important component of Integrated Pest Management (IPM) (Thompson et al. 1997). Additionally, there are governmental and environmental pressures to develop and use products safely with minimum impact on non-target arthropods. Predatory mite species are recognised as both important antagonists of pest species and sensitive indicators of ecologically significant effects (Overmeer 1988; Sterk & Vanwetswinkel 1988).

Miles & Dutton (2003) conducted extended laboratory experiments, semi-field and field tests to examine effects of spinosad on predatory mites. Under extended laboratory conditions (exposure on natural substrates) no effects were seen on *Amblyseius cucumeris*, *Hypoaspis aculeifer* or *Hypoaspis miles* at rates up to 540 g a.i./ha. When *Phytoseiulus persimilis* was tested under semi-field conditions, spinosad was harmless at rates of 9.6, 19.2 and 36 g a.i./hL. No effects were noted to *Amblyseius californicus* at 19.2 g a.i./hL under semi-field conditions. In the field, single applications of spinosad at 48 or 96 g a.i./ha in vines caused no unacceptable effects to populations of *T. pyri* or *Kampimodromus aberrans*. It was concluded that spinosad was highly selective to most predatory mite species and that effects noted in tier I laboratory studies did not translate to higher tiers of testing or use in the field. The reason for this is not clear but could be due to agronomic practice, difference in species sensitivity, sublethal or behavioural effects or even effects on prey. However use patterns safe to predatory mites and compatible with IPM have been developed for a wide range of crops.

outdoor conditions (Daneshvar & Abaii 1994). However, Biological control of spider mites using this predaceous mite is effective only against low population densities of the pest (Pralavorio et al. 1985). When the population densities are high an acaricide treatment is needed to reduce the pest population before release of beneficial mites (Malezieux et al. 1992; Bakker et al. 1992; Hassan et al. 1994). Although various aspect of pesticide effects on *P. persimilis* have been studied by many workers in the past (Samsøe-Petersen 1983; Zhang & Sanderson 1990; Oomen et al. 1991; Blümel et al. 1993, 2000; Blümel & Gross 2001; Blümel & Hausdorf 2002; Cloyd et al. 2006). Only Kavousi & Talebi (2003) investigated side-effects of heptenophos, malathion and pirimiphosmethyl on *P. persimilis*. Moreover, there is no adequate information on the susceptibility of many strains and species to other pesticides, especially

Bostanian et al. (2004) studied the toxicity of Indoxacarb to two predacious mites: *Amblyseius fallacis* (Garman) (Phytoseiidae) and *Agistemus fleschneri* (Summers) (Stigmaeidae). They reported that Indoxacarb had no adverse effects on *A. fallacis* and *A. fleschneri* adults, number of eggs laid by treated adults of both species and percent hatch of treated eggs of these two

Rodrigues et al (2004) evaluated the toxicity of five insecticides (*Bacillus thuringiensis,* tebufe‐ nozide, flufenoxuron, phosalon and deltamethrin) on predatory mites (Acari: Phytoseiidae). The results were similar in both trials: phosalon and deltamethrin had a poor selectivity (harmful) on the phytoseiid mites, *Bacillus thuringiensis,* tebufenozide and flufenoxuron showed a good selectivity to these predators. The most abundant Phytoseiid species identified were *Phytoseius plumifer* (Canest & Fanzag) (91.8%) in Minho region and *Typhlodromus*

Cavaco et al (2003) studied evaluating the field toxicity of five insecticides on predatory mites (Acari: Phytoseiidae). The dominant species of phytoseiid in the region of Guarda was *Typhlodromus pyri* Scheuten (99.9%) and the dominant species in the region of Castelo Branco was *Typhlodromus phialatus* Athias-Henriot (96.4%). The results of imidacloprid showed good selectivity for phytoseiids while dimethoate was harmful. It was found that *T. pyri* was more tolerant to the other insecticides tested than *T. phialatus*. These results are of interest for the enhancement of integrated pest management programs. They suggest differences in suscept‐

Spinosad controls many caterpillar pests in vines, pome fruit and vegetables (including tomatoes and peppers), thrips in tomatoes, peppers and ornamental cultivation and dipterous leafminers in vegetables and ornamentals (Bylemans & Schoonejans 2000). Spinosad can be used to control pests in crops where the conservation of predatory mites is an important component of Integrated Pest Management (IPM) (Thompson et al. 1997). Additionally, there are governmental and environmental pressures to develop and use products safely with minimum impact on non-target arthropods. Predatory mite species are recognised as both important antagonists of pest species and sensitive indicators of ecologically significant effects

ibility of *T. pyri* and *T. phialatus* to the tested insecticides, mainly to vamidothion.

acaricides (Zhang 2003).

species, as stated also by Kim et al. (2000, 2005).

24 Insecticides - Development of Safer and More Effective Technologies

(Overmeer 1988; Sterk & Vanwetswinkel 1988).

*phialatus* Athias-Henriot (96.7%) in Castelo Branco region.

Papaioannou et al. (2000) studied the effects of a NSKE (Neemark) and Bioryl(R) vegetable oils against phytophagous and predatory mites using bean leaves treated with different concen‐ trations. Neemark (3 and 5%) was moderately toxic to *T. urticae*, and highly toxic to *P. persimilis*. Other studies investigated the toxicological tests (acute and sublethal effects) of fungicides on predatory mites (Blümel et al. 2000; Auger et al. 2004; Bernard et al. 2004).
