**5. Side effects of pesticides on phytoseiid mites**

Recently, a plant protection strategy has been recommended, minimizing the use of chemical pesticides. Every crop is infested by various pests; some but not

all of them may be controlled by biological means using pathogens, predators, parasitoids, and spiders. But to achieve satisfactory control of complexes of pests, selective pesticides are also indispensable. In fact, they are a prerequisite of IPM [41]. Therefore, studying the side effect of insecticides on natural enemies is highly required to exclude the detrimental effects on the natural enemies.

Pesticide use can be modified to favor natural enemies in a variety of ways, including treating only when economic thresholds dictate, use of active ingredients and formulations that are selectively less toxic to natural enemies, use of the lowest effective rates of pesticides, and temporal and spatial separation of natural enemies and pesticides. Decisions regarding pesticide use for insect pests in IPM programs are typically based on sampling pest populations to determine if they have reached economic threshold levels, although some work has been done to incorporate natural enemy sampling into these pesticide use decisions [26]. IPM also endeavors to use chemicals that act selectively against pests but not against their enemies. However, living organisms are finely tuned systems; a chemical does not have to be lethal in order to threaten the fitness (physical as well as reproductive) of the animal, with unpredictable results on the structure of the biological community [42–44]. However, pesticides may affect the predatory and reproductive behavior of beneficial arthropods short of having direct effects on their survival, few studies investigate the sublethal effects of insecticides other than their direct toxicity (usually LD50) on nontarget animals. Thus, to show that a pesticide is relatively harmless, or indeed has no measurable effect at all, behavioral studies on the effects of sublethal concentration are necessary [41].

Several studies showed that integrating biological control with chemicals in the IPM program for spider mites is particularly attractive. In different countries, phytoseiid mites are successfully used in the management of *T. urticae* in protected environments and open fields [33–36]. Therefore, it is essential to acquire information on the toxicity of commonly used acaricides to these predators [13]. Based upon the study of the effects of two acaricides (abamectin and hexythiazox) on six phytoseiid mites, it is recommended that the frequent use of acaricides against phytophagous mites should be avoided and the feasibility of biological control programs should be promoted to protect the environment, health of living individuals, and the nontarget organisms [45]. Our studies of the effects of two acaricides (abamectin and fenpyroximate) on a phytoseiid mite revealed a similar result. Currently, great efforts are directed toward reducing the use of traditional pesticides and increasing the use of IPM techniques. Therefore, finding the pesticides that are compatible with phytoseiid mites in IPM programs is an interesting and logical approach [46].

Our studies on side effects of acaricides on phytoseiid mites illustrated that evaluating the toxicity of acaricides and insecticides to phytoseiid mites by measuring only female mortality underestimates the real effects of residual exposure, and assessment of sublethal effects is important to determine the total impacts of acaricides and insecticides on the performance of predatory mites. Our studies also demonstrated that the evaluation of pesticide effects based solely on treated mites would have incomplete endpoints. Therefore, to evaluate the total effects of the pesticides on predators, determining these effects on subsequent generations is necessary [12–14]. For example, some studies on the relative toxicity of abamectin to the treated predatory mite of Phytoseiidae family without assessing offsprings reported that the intrinsic selectivity of abamectin makes it a promising candidate for use in integrated mite management (IPM) [47–49]. In contrast, our study in 2 generations of treated predatory mites illustrated this acaricide decrease the biological performance

*Side Effects of Pesticides on Population Growth Parameters, Life Table Parameters… DOI: http://dx.doi.org/10.5772/intechopen.104229*

of *P. plumifer*; therefore, it is not a proper candidate in the IPM program [14]. Some other studies in consistence with our studies [13, 14] reported that abamectin and fenpyroximate are harmful to these species and did not recommend them in the IPM program [50, 51]. They evaluated the toxic effects of hexythiazox (Nisorun®, EC 10%), fenpyroximate (Ortus®, SC 5%), and abamectin (Vertimec®, EC 1.8%) on *Phytoseiulus persimilis*. The results showed that the total effect of all concentrations of fenpyroximate and field and one-half the field concentration of abamectin, were found to be toxic to this predatory mite and above the upper threshold. But 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 [51].

In our studies to assess the toxicity and sublethal effects of acaricides on the predatory mites, a modified leaf-dip technique was used [13, 14]. Concentrationresponse bioassay was conducted to determine the sublethal concentrations of acaricides. LC5, LC10, LC20, and LC30 values were selected for fenpyroximate [13]. For abamectin LC10, LC20, and LC30 were used [14]. The eggs laid by treated females were collected and transferred separately in a leaf disc on a petri dish. Methods were comprehensively described [13, 14]. All reproductive, survival, and voracity parameters of offspring of treated females were recorded from egg to death of the last female.

#### **5.1 Side effects of pesticides on life table and population growth parameters of the subsequent generation of treated phytoseiid mites**

Demographic toxicology has been considered as a better measure of response to toxicants than individual life-history traits [52]. Life table parameters influence the population growth rates of a mite in the current and next generations. In the female life table, the number of female progeny, the survival rate of immature and female adult stages, daily fecundity, and sex ratio were used for the estimation of different life table parameters. Some estimated parameters were the age-specific survival rate (*l*x), life expectancy (*e*x), age-specific fecundity (*m*x), gross reproductive rate (*GRR*), mean generation time (*T*), the intrinsic rate of birth (*b*), and the intrinsic rate of death (*d*) [27]. The equations and life table construction were adopted from Birch (1948) and Carey (1993) [53, 54]. In the construction of a female age-specific life table, it is necessary to calculate age-specific survival rate (*l*x) and age-specific fecundity (*m*x) based on female individuals, where *l*x shows the probability that a newborn individual will survive to age *x*, and *m*x is the mean number of female eggs laid per female adult at age *x*. *GRR* is total lifetime reproduction in the absence of mortality. This is the average lifetime reproduction of an individual that lives to senescence, useful in considering potential population growth if all ecological limits (predation, competitors, disease, and starvation) were removed for a population. *GRR* is rarely if ever attained in nature, but useful to consider how far below this a population is held by ecological limits. The jackknife method was used to estimate the pseudo-values of the above-described parameters and compare them statistically [55].

Several researchers have reported that life-table parameters of predatory mites of family Phytoseiidae were affected by sublethal concentrations of pesticides [10, 11, 56–63]. In the above-mentioned studies, the population parameters of the subsequent generation of a lot of phytoseiid mites were decreased when exposed to sublethal concentrations of pesticides. Such as offspring of *Neoseiulus longispinosus* exposed to abamectin; *P. plumifer* exposed to abamectin and fenpyroximate; *Amblyseius swirski* exposed to bifenazate and fenazaquin; *Neoseiulus californicus*

exposed to pyridaben, spirodiclofen, spiromesifen, and imidacloprid; and *P. persimilis* exposed to fenpyroximate, Propamocarb-Hydrochloride, imidaclopride, and abamectin. And they reported that the mentioned pesticides cannot be considered compatible acaricides with the exposed phytoseiid mite and should not be used with those predatory mites in integrated pest management programs.

In our studies, population growth and life table parameters of offspring of treated predatory mite *P. plumifer* were significantly and in some parameters severely affected by sublethal concentrations of two acaricides abamectin and fenpyroximate [10, 11]. The gross reproductive rate (*GRR*) was 35.66 females per female in the subsequent generation of untreated predators. It was significantly decreased in offspring of the treated female with all sublethal concentrations of fenpyroximate. It was reached to 5.4 females in offspring of LC30 treatment. In offspring of treated females with the sublethal concentration of abamectin, *GRR* was decreased significantly too. It was 10.30 in offspring of treated females with LC20 (treated females with LC30 of abamectin laid no egg, so it was not subsequent generation in this concentration) (**Figure 1**). However, abamectin affected the reproductive of treated females more than fenpyroximate, *GRR* was decreased less in the subsequent generation. It was because of the severe effect of fenpyroximate on the sex ratio of treated females. The sex ratio was 16:8 (female: male) in the subsequent generation of untreated females that changed to 10:26 (female: male) in the subsequent generation of treated females with LC30 of fenpyroximate. So, decreasing the number of females in the subsequent generation of the treated female with fenpyroximate can be the reason for lower GRR in offspring of treated females with fenpyroximate in comparison with offspring of treated females with abamectin [10, 11]. Other studies have investigated the sublethal effects of fenpyroximate and pyridaben on two predatory mites from family Phytoseiidae, *Neoseiulus womersleyi* and *P. persimilis*, and reported similar data [59, 61]. The other studies reported a similar decrease in this parameter due to abamectin application on phytoseiid mites, *Notoplites longispinosus* and *P. persimilis* [56, 64]. *GRR* was decreased by other insecticides in the subsequent generation of treated phytoseiid mites [60–62, 65]. In contrast, in the other study spirodiclofen did not affect the *GRR* of the

#### *Side Effects of Pesticides on Population Growth Parameters, Life Table Parameters… DOI: http://dx.doi.org/10.5772/intechopen.104229*

subsequent generation of treated predatory mite, *A. swirskii* [65]. But fenazaquin was affected on *GRR* of the subsequent generation of this species [60].

The intrinsic rate of birth (*b*) was significantly decreased and the intrinsic rate of death (*d*) was significantly increased in offspring of treated females of *P. plumifer* with fenpyroximate and abamectin. The ratio of birth to death (*b*/*d*), which is the number of births per death, was 6.55 in control, which decreased to 0.56 in offspring of treated females with LC30 of fenpyroximate. It was 4.11 in offspring of treated females with LC20 of abamectin (as mentioned earlier, treated females with LC30 of abamectin laid no egg, so it was not subsequent generation in this concentration). Mean generation time (*T*) in offspring of treated females with fenpyroximate was decreased from 17.07 days in control to 13.55 days in LC30 treatment [13]. This parameter does not change significantly in offspring of treated females with abamectin [14]. This is in consistence the other study of the effect of spirodiclofen, spiromesifen on predatory mite, *A. swirskii*, *N. colifornicus*, respectively [62, 65]. *T* was decreased in the subsequent generation of *N. longispinosus* treated females with abamectin [56]. The age-specific survival rate of the subsequent generation of the treated and untreated females of *P. plumifer* are given in **Figure 2**. Life expectancy (*ex*) on the first day of adult emergence showed a noticeable reduction in offspring of treated individuals in comparison with control (**Figure 3**).

In contrast to our findings, the other study suggests that sublethal concentrations of spirodiclofen may not affect the population parameters of offspring from treated females of *A. swirskii* [65]. This difference may be due to different predatory mite species or acaricides mode of action. Indeed, fenpyroximate functions as mitochondrial electron transport inhibitors (METI) at Complex I [66], and abamectin acts on gamma-aminobutyric acid (GABA) and glutamate-gated chloride channels [19] while spirodiclofen inhibits the acetyl-CoA carboxylase [67]. In another study, however, reproductive and total fecundity of the subsequent generation of *A. swirskii* were affected by sublethal concentrations of propargite, researchers suggested that the usage of spirodiclofen and propargite as a selective acaricide and at sublethal dosage against spider mites may not affect the life table parameters. However, it is necessary to pay attention to the direct toxicity of spirodiclofen on *A. swirskii* for considering this acaricide in IPM programs [65, 68]. In contrast, fenazaquin and bifenazate are not compatible acaricide with *A. swirskii* and should not be used with this predatory mite in the integrated management of *T. urticae* [60, 69].

**Figure 2.**

*Survival rate (lx) of offspring of the treated and untreated females of Phytoseius plumifer with fenpyroximate and abamectin.*

**Figure 3.** *Life expectancy (ex) of offspring of the treated and untreated females of Phytoseius plumifer with fenpyroximate and abamectin.*

Different small letters above each bar indicate a statistically significant difference between concentrations. Different capital letters above each bar indicate a statistically significant difference between acaricides (*P* < 0.05) (LSD).

#### **5.2 Side effects of pesticides on predation of the subsequent generation of treated phytoseiid mites**

Besides demographic and life table parameters, the predation rate is an important factor in the biological performance of predatory mites. A direct effect of predation rate on biological performance is suppressing the pest population. The indirect effect of predation rate in biological control success is maintaining egg production and developmental success of predator. Predation rate is potentially affected by sublethal concentrations of pesticides and ignoring this effect may lead to underestimating the negative effect of pesticides on the population of predators [12]. A few studies have evaluated the sublethal effect of pesticides on predation of treated phytoseiid mites [70], but to date, apart from our study [12], no data is available on the side effects of acaricides on prey consumption of subsequent generations of treated phytoseiid mites. For example, a study evaluated the effects of four selective pesticides on predation of treated females of a phytoseiid mite, *Neoseiulus cucumeris*. They reported that flubendiamide, spirotetramat, and metaflumizone had significant impacts on the predation of immature stages; spirotetramat had the greatest effect. The four selective pesticides significantly reduced prey consumption of treated females [71]. In the other study, evaluation of the sublethal effect of abamectin on the functional response of *P. persimilis*, a significant decrease in attack rate and an increase in the handling time (Th) observed and indicating a negative effect of abamectin on the predation. Therefore, they reported that the predator requires more time to identify, persecute, consume, and digest the prey when it is under the influence of acaricide compared to control [70]. About it and as a result of predator biological behavior, Reddy (2013) mentions that the decrease in feeding is reflected by the exposure of thin layer residuals abamectin, when it enters in contact with the mite, it affects the capacity of the neurotransmitters GABA and glutamate stimulating the flow of chlorine ions into the nerve cells resulting in the loss of the function, these ions that flow inside the channel to an opening result in the loss of the cellular function and

*Side Effects of Pesticides on Population Growth Parameters, Life Table Parameters… DOI: http://dx.doi.org/10.5772/intechopen.104229*


*Means followed by different small letters in each column are significantly different in each acaricide. Means followed by different capital letters in each column are significantly different between acaricides in each concentration (P < 0.05) (LSD).*

#### **Table 1.**

*Effect of sublethal concentrations on prey consumption (mean ± SE) of immature stages of the subsequent generation of exposed females of Phytoseius plumifer.*

interruption of the nervous impulses and consequently, the mites stop their feeding, concluding a negative affect for the predatory mites [72]. The other study reported that the effect of pesticides on predation may be due to a repellent effect of the pesticide. Their findings after evaluating four selective pesticides on development, fecundity, and predation of phytoseiid mite, *N. cucumeris*, showed that chlorantraniliprole could be used in fields with *N. cucumeris*, whereas flubendiamide and metaflumizone had poor compatibility with this predatory mite. It would be counterproductive to combine the use of this biological control agent with spirotetramat [71].

Prey consumption of nymphs in subsequent generation of treated females with abamectin and fenpyroximate was significantly decreased in comparison with control. Total prey consumption of nymph was 14.40 in control and decreased to 5.96 in the subsequent generation of treated females with LC30 (**Table 1**). Daily prey consumption of females of the subsequent generation of exposed females was not significantly decreased. But total prey consumption of them was decreased. That was because of the decrease in longevity.

### **6. Conclusion**

Due to the considerable effects of abamectin and fenpyroximate, in lower than the recommended field rate for *T. urticae* control, on population growth and life table parameters and predation of *P. plumifer* resulted in our studies and a lot of phytoseiid mites resulted in other studies quoted in this chapter, they are not compatible with a lot of species of phytoseiid mites so could not be recommended to use in two-spotted spider mites IPM programs.
