Side Effects of Pesticides on Population Growth Parameters, Life Table Parameters, and Predation of the Subsequent Generation of Phytoseiid Mites

Abstract

Simply estimating pesticide effects on natural enemies of pests by measuring only lethal effects, or sublethal effects on the only treated natural enemies, may underestimate the total negative effects on them. So sublethal effects on subsequent generations should be assessed to estimate the total effects of their applications. Sublethal effects of commonly used acaricides on population growth parameters, life table parameters, and predation of the predatory mites of the family phytoseiidae were investigated. For this reason, offspring of treated females were used. Gross reproductive rate (GRR), the intrinsic rate of birth (b), the intrinsic rate of death (d), mean generation time (T), survivorship (Lx), life expectancy (ex), and prey consumption were affected in comparison with control. It could be concluded that sublethal concentrations of most applied pesticides can significantly reduce population growth and life table parameters, and this should be considered in integrated pest management (IPM) programs.

1. Introduction

Despite various control methods such as chemical, cultural, and biological control, the common control method of many insect pests is pesticide application, and chemical controls are often the dominant tactic used in integrated pest management (IPM) programs [1, 2, 3]. On the other hand, biological control has been a valuable tactic in pest management programs around the world for many years. Integration of biological control with chemical control within an IPM system could reduce pesticide applications and environmental hazards. For this reason, compatibility evaluation of pesticides with naturally existing or augmented biological control agents seems necessary. So, knowledge of the lethal and sublethal effects of pesticides on biological control agents is necessary for the successful implementation of IPM programs.

2. Importance of Tetranychus urticae

Mites of the family Tetranychidae (commonly known as spider mites) are important pests in agricultural and forestry ecosystems and can be found on many field crops, fruit trees, vegetables, and ornamental plants. Many spider mites naturally inhabit ephemeral and patchily distributed resources such as weeds. The most notorious and important tetranychid mite is the globally-distributed two-spotted spider mite, Tetranychus urticae Koch, 1836 [4]. It is one of the important pests on many crops, greenhouse, and garden products [5, 6]. It can create multiple generations (12–25 generations) and adapt to new climates quickly. It also has a broad host range, short life cycle, haploid-diploid sex-determination, and high fecundity lead to the rapid development of resistance to pesticides [7]. So, pesticide resistance, the high cost of pesticides, and loss of production time have raised interest by growers to introduce predatory phytoseiid mites to manage two-spotted spider mites and reduce their need for acaricide applications [8].

3. Chemical control of Tetranychus urticae

The rapid developmental rate of spider mites and their high fecundity allows them to attain destructive population levels very quickly. In addition, they became resistant to several extensively used acaricides. Consequently, the extensive use of pesticides led to the outbreaks of Thrips urticae during the last few decades [9]. Due to the environmental and health hazards resulting from the chemical pesticides as well as their side effects on the nontarget organisms (e.g., soil microorganisms) [10] and predators [11, 12, 13, 14], their use has been regulated firmly [15]. Many chemical-based insecticides and acaricides have been registered to control T. urticae all over the world such as in Iran, including abamectin and fenpyroximate [16].

Abamectin is a macrocyclic lactone derived from the soil microorganism, Streptomyces avermitilis, and acts on gamma-aminobutyric acid (GABA) and glutamate-gated chloride channels [17, 18, 19]. Researchers reported that abamectin potentiates the effect of neurotransmitters and increases the influx of chloride ions into nerve cells, disrupting nerve impulses and nerve functions. Abamectin as an insecticide, miticide, and nematicide is widely used in different parts of the world, including America, Europe, and Asia [20, 21, 22] and was found to be one of the most toxic chemicals to T. urticae [23].

Fenpyroximate is a pyrazole acaricide and insecticide with selective activity against important phytophagous mites in the families Tetranychidae, Eriophyiidae, and Tarsonemidae [17, 24, 25]. After spraying this acaricide, oxygen consumption and ATP production in the pest decline, causing knockdown and paralysis [24]. It is active against all stages of agriculturally important mites, showing higher efficacy against larvae than against other life stages [17].

4. Biological control of Tetranychus urticae with emphasis on family Phytoseiidae

Natural enemies have been utilized in the management of agricultural pests for centuries. However, the last 100 years have seen a dramatic increase in their use [26]. Biological control, or biocontrol, is the use of an organism to reduce the population density of another organism and it is the core component of IPM that is growing in popularity, especially among organic growers [27]. It is one of the most economical and environmentally harmless methods of pest control for farmers [28]. Two types of biocontrol, natural biocontrol and applied biocontrol, are often distinguished. Natural biocontrol is the reduction of native pest organisms by their indigenous natural enemies. In contrast, applied biocontrol is achieved through human efforts or intervention and consists of three main approaches: conservation, inoculative (classical), and augmentative biocontrol [27]. In some agricultural systems, the natural enemies can suppress the spider mite populations below levels of economic damage [29]. Mite predators play an important role in the IPM of phytophagous mites, particularly in complex cropping systems where they may remove the need for any chemical intervention. Further information on IPM definitions and history can be found [27].

Predatory mites from families Phytoseiidae, Ameroseiidae, Parasitidae, Stigmaeidae, Anystidae, and Bdellidae as natural enemies of Tetranychidae were founded during sampling from Northwestern Iran and Varamin province (2007–2008). Among predator insects, Stethorus gilvifrons Mulsant (Coleoptera: Coccinellidae), Oenopia conglobata (Linnaeus) (Coleoptera: Coccinellidae), Exochomus quadripustulatus (Linnaeus) (Coleoptera: Coccinellidae), Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae), Scolothrips sp. (Thysanoptera: Thripidae), and Orius horvathi Reuter (Heteroptera: Anthocoridae) were found [30]. Among the predatory mites that have been found, we worked on family Phytoseiidae. Because predaceous mites of the family Phytoseiidae are considered one of the most important groups of natural enemies used in biological control [31]. Indeed, they are considered the most effective natural enemies of tetranychid mites and other microarthropods of economic importance such as thrips [6, 32]. In different countries, phytoseiid mites are successfully used in the management of T. urticae in protected environments and open fields [33, 34, 35, 36]. Certain phytoseiids consume large numbers of prey and maintain plant-feeding mites at low densities. They have a high reproductive rate, a rapid developmental rate comparable to their prey, a female-biased sex ratio equivalent to their prey allowing them to respond numerically to increased prey density, and can easily be mass-reared [6, 32]. Furthermore, several species within the family may utilize pollen as a food source and can develop and reproduce on pollen as well. Phytoseiids may persist or even maintain themselves at relatively high densities in the crop at times when their main prey is scarce or absent. Therefore, phytoseiids can prevent prey resurgence, without the normal time lag usually associated with a numerical response [37]. Among the predatory mites of the family Phytoseiidae, we worked on Phytoseius plumifer (Canestrini and Fanzago) (Acari: Phytoseiidae) because it is an effective predator of phytophagous mites distributed in several countries such as Iran, Egypt, France, Italy, and Israel [38, 39, 40], but there is a little available data about acaricides side effects on this predator’s performance [13]. One of the projects was the assessment of lethal and sublethal effects of two commonly used acaricides on Plumozetes plumifer [12, 13, 14].

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, 43, 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, 34, 35, 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, 13, 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, 48, 49]. In contrast, our study in 2 generations of treated predatory mites illustrated this acaricide decrease the biological performance 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]. Concentration-response 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, 57, 58, 59, 60, 61, 62, 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 californicusexposed 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, 61, 62, 65]. In contrast, in the other study spirodiclofen did not affect the GRR of the subsequent generation of treated predatory mite, A. swirskii [65]. But fenazaquin was affected on GRR of the subsequent generation of this species [60].

Figure 1.

The gross reproductive rate (GRR) of offspring of the treated and untreated females of Phytoseius plumifer.

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).

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.

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].

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 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.

Treatment	μg a.i./ml		Total prey consumption (Protonymph)	Total prey consumption (Deutonymph)	Total prey consumption (nymph stage)
Control	0	0	6.28 ± 0.14^a	9.24 ± 0.59^a	14.40 ± 0.63^a
Fenpyroximate	3.899	LC5	5.80 ± 0.44^a	7.00 ± 0.37^b	12.95 ± 0.62^a
	5.607	LC10	5.46 ± 0.58^Aa	6.74 ± 0.56^Ab	12.60 ± 0.56^Aa
	10.290	LC20	5.46 ± 0.45^Aa	6.41 ± 0.73^Ab	12.07 ± 0.7^Aa
	11.956	LC30	2.65 ± 0.31^b	3.19 ± 0.48^c	5.96 ± 0.57^b
Abamectin	0.021	LC10	7.00 ± 1.06^Aa	6.00 ± 0.93^Aa	13.00 ± 0.89^Aab
	0.033	LC20	5.12 ± 0.66^Ab	7.75 ± 1.82^Aa	10.71 ± 1.47^Ab
	0.046	LC30	—	—	—

Table 1.

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

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).

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.