Introduction
The kidney bean, Phaseolus vulgaris L., is an annual leguminous plant (Family: Fabaceae). It is one of the most important economic vegetable crops cultivated in many countries worldwide [1]. Yield production suffers from many stresses [2-6], such as drought [7], salinity [8, 9], and biotic stress, including plant diseases [10-12] and insects [13, 14]. Kidney bean plants are liable to infestation by many phytophagous pests, such as mites. The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is a pest of more than 1100 plant species. Controlling T. urticae with acaricides is challenging because of its high reproduction rate and easy development of acaricide resistance. [15-18]. This pest lowers the quality and quantity of the host plant yield by sucking out the cell contents of the leaf, causing death in heavy infestations. The main method for mite control is chemical acaricide [19, 20]. Tetranychus urticae Koch is the most harmful pest to many plants globally [21]. Abamectin (Vertimec 1.8 EC) acaricide’s acaricidal efficacy at various concentrations, where the LC50 values were 1.02, 2.74, and 1.65 after one day, two days, and three days, respectively. Furthermore, adult fecundity, repellency, and hatchability under Vertimec varied substantially with concentration [21]. Overcoming or reducing the majority of difficulties caused by using common pesticides requires using developed, secure, unique, and selective organic compounds. Due to their clear mechanism of action on pests and lower poisonousness towards vertebrates than conventional insecticides, juvenile hormone analogs appear promising as an example of insect growth regulators [22]. The latent effects of the examined synthesized compounds on various biological parameters, including adult longevity, pupal weight, proportion of normal adult emergence, and egg hatchability, were evaluated in an additional effort to improve insecticidal compounds slightly. Seven target synthesized compounds were subjected to a molecular docking analysis against glutamate-activated chloride channels. Twelve artificial compounds with the PDB ID of 4COF were subjected to a molecular docking study against the gamma-aminobutyric acid receptor (GABA) [23]. Environmental pollutants and climate change are the major causes of abiotic stresses. Ahmad et al. 2022 [24]. Pesticides are mainly used to protect crop plants from pests and pest-transmitted diseases. However, the active ingredients of the pesticides are also a source of crop toxicity and food contamination. The persistent nature of the chemicals makes them stable against environmental degradation processes, and they continue to be in the form of pesticide residues in different plant tissues. Pesticides are mainly used to protect crop plants from pests and pest-transmitted diseases. However, the active ingredients of the pesticides are also a source of crop toxicity and food contamination. The persistent nature of the chemicals makes them stable against environmental degradation processes, and they continue to be in the form of pesticide residues in different plant tissues [25].
Abamectin (avermectin B1) belongs to the macrocyclic lactones [26]; it is one of the most commonly applied for pest control because of its broad-spectrum action [27, 28]. It is the major fermentation component of avermectins derived from a soil actinomycete (Streptomyces avermitilis) with strong insecticidal, nematicidal, and acaricidal activity [29]. Abamectin is a risk-reducing neuroactive pesticide (chloride channel activator) [30]. Fenpyroximate (pyrazole), which causes inhibition of mitochondrial electron transport at complex I, shows high efficacy with a quick knockdown effect against both tetranychid and eriophyid mites. Under the application of fenpyroximate, a significant reduction was recorded in the intrinsic rate, net reproductive rate, and finite rate of increase; however, the mean generation time in the LC10 treatment was lower than that in the other treatments [31]. Chlorfenapyr is a novel broad-spectrum insecticide derived from natural pyrrole derivatives produced by Streptomyces spp. It is a pyrrole compound, a broad-spectrum insecticide at a biochemical level, and acts as an uncoupler of oxidative phosphorylation via disruption of the proton gradient [32]. Therefore, this study aimed to evaluate the toxic effects of three new reduced-risk acaricides with different modes of action: abamectin (Vertimec 1.8% EC), chlorfenapyr (Challenger 24% SC), and fenpyroximate (Ortus 5% SC) against T. urticae under laboratory and field conditions associated with their effects on the developmental stages and life table parameters of T. urticae.
Materials and Methods
Rearing of Host Plant
Kidney bean seeds, Phaseolus vulgaris L. var Nebraska, were sown in seed trays until they reached 5-6 true leaves. Thereafter, the seedlings were transplanted into plastic pots containing peat moss and kept in a glass house at 27-30°C. Plants were irrigated whenever needed and kept pesticide-free during the rearing period.
Tetranychus urticae Culture
A laboratory strain of T. urticae was obtained from the Acarology Laboratory of the Plant Protection Research Institute, Egypt, and reared on P. vulgaris. var Nebraska in a growth chamber at 25±5ºC, 60±10% RH, and 12:12 L:D photoperiod for several generations before use in experiments. Bioassays were performed under the same conditions in the Virus Laboratory, Tanta Agriculture Directorate, El-Gharbia Governorate, Egypt.
Pesticides
According to IRAC [33], the Insecticide Resistance Action Committee, three reduced-risk acaricides with different modes of action were selected for the bioassay.
Abamectin: a risk-reduced neuroactive acaricide that allosterically activates glutamate-gated chloride channels (GluCls), causing paralysis.
Fenpyroximate: 21A mitochondrial complex I electron transport inhibitors inhibit electron transport complex I, preventing the utilization of energy by the cells.
Chlorfenapyr: a pyrrole compound commercialized in 1995 that, at a biochemical level, acts as an uncoupler of oxidative phosphorylation via disruption of the proton gradient. This compound is a pro-acaricide activated by N-dealkylation. Chlorfenapyr is effective against all stages of spider mites and eriophyid mites. Chlorfenapyr is included in the EPA list as an alternative to organophosphorous compounds (EPA 2011) but is not approved under Regulation 1107/2009 (EU 2011).
This study used commercial abamectin, chlorfenapyr, and fenpyroximate, which are detailed in Table 1.
Toxicity to T. urticae Adult Females under Laboratory Conditions
The standard method of the leaf disc dip technique described by Pree [34] was adopted. Leaf discs (2.5 cm diameter) of P. vulgaris L. were dipped in serial concentrations of each pesticide. Abamectin 1.8% EC (0.001, 0.01, 0.1, 1, 10) mg/mL, Fenpyroximate 5% SC (10, 20, 40, 80, 100) mg/mL, and Chlorfenapyr 24% SC (10, 20, 40, 80, 100) mg/mL for 20 seconds. Ten adult females (one day old) of T. urticae were transferred on each disc with a camel hair brush. Four replicates were done for each concentration. Control discs were dipped in distilled water. The treated discs were placed on a moist sponge, covered with a moist paper tissue, and kept in a growth chamber at 25±2ºC, 65±5% R.H., and 12:12 L:D photoperiod. Mortality of treated mites was recorded after 24, 48, and 72 h of exposure. Mites were considered dead when appendages did not move when probed with a fine camel hair brush.
The toxicity index was calculated according to the equation of Sun [35] as follows:
Toxicity to T. urticae Moving Stages under Field Conditions
The experiments were carried out on 15th February 2020 and 16th February 2021 on the newly reclaimed lands of the 11th branch, Badr region, El-Beheira Governorate, Egypt, using a complete randomized block design with three replications/treatments. The total area of the experiment (700 m2) was divided into 4 equal parts (175 m2) for 3 acaricides and control, each part divided into 3 plots (3 replications/treatment), and the plot area was 56 m2. Row spacing, plant spacing, and seasonal maintenance procedures were conducted following the recommended agronomic practices. The 3 pesticides at their recommended rates were sprayed by a motor sprayer (20-liter capacity) with 16.67 liters of water/175 m2 on 22nd March; the control was sprayed with water only. Thirty leaves were taken randomly from each replicate just before and at 3, 7, and 14 days after treatment. The leaves were placed individually in paper bags and transferred to the laboratory. The moving stages of T. urticae were counted on the lower surface of the leaf using a stereo binocular microscope (25X). The reduction percentages of the mite population were calculated according to Henderson and Tilton [36] as follows:
Where, A = Number of individuals in treatment before pesticide application, A’ = Number of individuals in treatment after pesticide application, B = Number of individuals in the control before pesticide application, B’ = Number of individuals in the control after pesticide application.
Effects on the Developmental Stages and Life Table Parameters of T. urticae Females
Thirty pre-ovipositing females of T. urticae were placed singly each on 30 leaf discs treated with LC50 of 1 tested pesticide. Control discs were dipped in distilled water in 30 replications. After 24 h of exposure, the surviving females were placed individually on untreated leaf discs. The leaf discs were checked daily, and immature stages were monitored using a stereo binocular microscope (25X). Immature mites were allowed to develop to adulthood, and females were left to deposit eggs. Leaf discs were changed every 3 to 4 days to maintain their freshness. The duration of egg incubation, larval, protonymphal, and deutonymphal developmental periods, and adult preoviposition, oviposition, and postoviposition periods were recorded. The average number of eggs/female/day and total number of eggs/female were calculated. Life table parameters of T. urticae were estimated using a specific age class (lx) and the offspring produced/female in each age class (mx), the net reproductive rate (Ro), the mean generation time (T), the intrinsic rate of increase (rm), and the finite rate of increase (λ) according to Birch [37]. The mean and standard error values of demographic parameters were determined using the computer program of Abou-Setta et al. [38].
Table 1.
Commercial abamectin, chlorfenapyr, and fenpyroximate, and their details.
Statistical Analysis
The mortality percentage of spider mites was corrected using Abbott’s [39] formula. Values of LC50 and LC90 values, along with their corresponding 95% confidence limits, were calculated by probit analysis using “Ldp line” software (http://www.ehabsoft.com/ ldpline/), Bakr [40]. The standard errors between replications and significance between means of treatments were analyzed by Anova and Duncan [41] at a 5% level (confidence interval 95%) using IBM SPSS Statistics 16.
Results and Discussion
The objective of this study was to investigate the toxic effects of 3 new reduced-risk acaricides with different modes of action: abamectin (Vertimec 1.8% EC), chlorfenapyr (Challenger 24% SC), and fenpyroximate (Ortus 5% SC) in serial concentrations against T. urticae. Under laboratory conditions, their effects on the developmental stages and life table parameters of T. urticae were studied. In addition, the efficacy of abamectin, fenpyroximate, and chlorfenapyr was evaluated at the recommended rate against the moving stage of Tetranychus urticae under field conditions.
Toxicity to Females of T. urticae under Laboratory Conditions
Based on LC50 values, abamectin was significantly the most toxic pesticide against T. urticae, followed by fenpyroximate and chlorfenapyr with LC50 values of 0.01, 19.86, and 29.66 mg/L, respectively (Table 2). Abamectin had the highest toxicity index (100), while fenpyroximate and chlorfenapyr showed toxicity indices of 0.05 and 0.03 against T. urticae, respectively. Toxicity lines of abamectin (Vertimec 1.8% EC), fenpyroximate (Ortus 5% EC), and chlorfenapyr (Challenger 24% SC) against the moving stage of Tetranychus urticae are illustrated in Fig. 1. The obtained results agree with those of Mohamed et al. [21]; they tested abamectin (Vertimec 1.8 EC) acaricide’s acaricidal efficacy at various concentrations, where the LC50 values were 1.02, 2.74, and 1.65 after 1 day, 2 days, and 3 days, respectively. Abdel Razik and Heikal [42] concluded that fenpyroximate was very toxic to T. urticae, whereas it was safer for P. persimilis for the spraying method. Rabbi et al. [43] stated that chlorfenapyr and abamectin can be used to manage T. urticae because of their high activity against T. urticae and low residual toxicity against C. septempunctata.
Toxicity to T. urticae under Field Conditions
Results presented in Table 3 indicate that abamectin, fenpyroximate, and chlorfenapyr, respectively, caused a significant difference (F = 6.06, P = 0.036) in the mean reduction percentage of T. urticae on Phaseolus vulgaris in 2020 (92.83, 86.57, and 80.43); nevertheless, in 2021 the differences were not significant (F = 1.08, P = 0.41), and the mean reduction percentages were (86.85, 80.38, and 76.13). The efficacy of abamectin, fenpyroximate, and chlorfenapyr against the moving stage of Tetranychus urticae under field conditions was illustrated in Fig. 2.
In this respect, the efficiency of the tested pesticides on T. urticae was estimated in several studies. Massoud et al. [44] showed that the order of acaricide efficacy against T. urticae was Milbemectin˃Abamectin˃Bi fenazate˃Fenpyroximate˃Hexythiazox ˃Ethoxazole after 72 h of treatment. Saleh et al. [45] found that the toxicity of acaricides could be arranged according to their potency against T. urticae as follows: abamectin 1.8% EC>buprofezin>abamectin 5%>chlorfenapyr> hexythiazox>fenpyroximate.
Table 2.
The activity of abamectin, fenpyroximate, and chlorfenapyr on Tetranychus urticae females under laboratory conditions.
Fig. 1.
Toxicity lines of abamectin (vertimec 1.8% EC), fenpyroximate (Ortus 5% EC), and chlorofenapyr (challenger 24% SC) against the moving stage of Tetranychus urticae under laboratory conditions.
Regarding the safety of people and the environment, abamectin has demonstrated low toxicity to non-targeted beneficial arthropods, which aids in its inclusion in integrated pest management (IPM) programs [46]. Chlorfenapyr is thought to act as an uncoupler in mitochondrial oxidative phosphorylation. It obstructs the conversion of ADP to ATP, leading to an energy metabolism disorder that ultimately causes insect death. Thus, chlorfenapyr is considered an efficient, low-toxicity, target-specific, and environmentally friendly pesticide [47]. Recommended tested rates of fenpyroximate and thiacloprid negatively influenced the biological parameters of the predator A. swirskii. However, the combined treatment of the two pesticides at reduced rates was less hazardous to A. swirskii. Our findings indicate that the combined use of these chemicals may be compatible with IPM programs utilizing A. swirskii as a biological control tool against phytophagous mites and other pests [48].
Fig. 2.
Efficacy of abamectin, fenpyroximate, and chlorofenapyr against the moving stage of Tetranychus urticae under field conditions.
Table 3.
The efficacy of abamectin, fenpyroximate, and chlorfenapyr against the moving stage of Tetranychus urticae under field conditions.
Influence on T. urticae Females’ Developmental Stages
The results obtained in Table 4 showed that fenpyroximate resulted in the highest duration of eggs (5.63±0.13 days), total immature (11.61±0.24 days), and postoviposition (2.13±0.47 days) of T. urticae. Abamectin was the most effective on deutonymph duration (2.05±0.09 days) and preoviposition duration (1.63±0.18 days). However, chlorfenapyr showed the best result on oviposition duration (3.45±0.77 days), egg/female (9.45±3.6 eggs), and female longevity duration (6.09±0.94 days). T. urticae egg incubation periods were significantly affected longer on abamectin, fenpyroximate, and chlorfenapyr excised leaf discs (F = 97.75; LSD = 0.29; P =0 .0001), recording 5.31±0.06, 5.63±0.13, and 5.53±0.11 days, respectively. The development period of mite larvae was similar in abamectin, fenpyroximate, and chlorfenapyr treatments (F = 0.001; LSD = 0.10; P = 0.10), recording 2.03±0.37; 2.03±0.38; and 2.04±0.38 days, respectively. Protonymph developmental periods in abamectin, fenpyroximate, and chlorfenapyr treatments. (F = 0.03; LSD = 0.13; P = 0.10) were 2.04±0.43, 2.05±0.52, and 2.05±0.48 days, respectively. Furthermore, the deutonymph developmental period was significantly longer (F = 4.22; LSD = 0.26; P = 0.008) in abamectin (2.05±0.09 days) than in fenpyroximate (1.72±0.11 days) and chlorfenapyr (1.60±0.13 days). Moreover, the total development time was significantly longer (F = 3.19; LSD = 0.44; P = 0.03) in fenpyroximate (11.61±0.24 days) than in chlorfenapyr (11.30±0.18 days) and abamectin (11.26±0.13 days) treatments. Wakil et al. [49] reported that the development of T. urticae on both sides of tomato leaves was meaningfully prevented by applying entomopathogenic fungi treatments or abamectin compared to the control 21 days after infestation. However, a higher number of inhabited adults, immatures, and eggs were found on the abaxial surface of the leaves compared to the adaxial surface [50, 51].
The results obtained are in agreement with those obtained by Bozhgani [52]. He studied the sublethal effects of LC10, LC20, and LC30 of chlorfenapyr on demographic parameters of T. urticae. He stated that the egg incubation, protonymph, and deutonymph durations of both sexes were significantly reduced due to treatment with LC20 and LC30 of chlorfenapyr. In addition, the oviposition period in LC10 lasted 9.62 days, which was closer to the control (9.73 days), while it significantly decreased with increasing the concentration from LC20 to LC30. Furthermore, LC20 and LC30 treatments decreased the fecundity of females by 55.5% and 61.6%, respectively.
Influence on T. urticae Life Table Parameters
Regarding the effect of the tested acaricides on the life table parameters of T. urticae females, data presented in Table 5 showed that the studied parameters were significantly acaricide-dependent. Mean generation time in days (T) was highly significantly different (F = 1194, P = 0.000); the shortest mean generation time (T) was 16.27 days on fenpyroximate, while the longest was 17.13 days on abamectin. Net reproductive rate (Ro) was highly significantly different (F = 5343.91, P = 0.000); the highest net reproductive rate (Ro) was 15.80 female/female in the control, and the lowest rate was 3.47 female/female in chlorfenapyr. The intrinsic rate of natural increase (rm) differed significantly (F = 14.75, P = 0.001) and was lowest, 0.07 female/ female/day in chlorfenapyr, and highest, 0.17 female/ female/day in the control. The finite rate of increase (λ) per day was significantly different (F = 14.76, P = 0.001), the lowest being 1.08 in chlorfenapyr and the highest in the control. The sex ratio (female/ total) was not significantly different (F = 3.91, P = 0.05); it was recorded as the highest at 0.77 in the control and the lowest at 0.52 in chlorfenapyr.
Table 4.
The effect of acaricides on the development of Tetranychus urticae on Phaseolus vulgaris leaf discs under laboratory conditions.
Table 5.
Life table parameters of Tetranychus urticae females reared on Phasulus vulgaris treated with different pesticides under laboratory conditions.
Bartling et al. [53] reported that exposure to lethal or sublethal concentrations of pesticides can impact various physiological parameters of insects, including development and reproduction, through the effects on exposed tissues and the modification of behaviors that contribute to insect health and reproduction.
Bozhgani [46] studied the sublethal effects of chlorfenapyr on demographic parameters of T. urticae and concluded that the sublethal concentrations of chlorfenapyr profoundly reduced the population growth rate of T. urticae. Sublethal (LC25) of Agnar 20% SC, penny 9% SC, and biomectin 5% EC significantly affected the T. urticae biological parameters such as longevity, total life span, net reproductive rate, intrinsic rate of natural increase, and finite rate of increase [54]. Our findings were in agreement with the previous results of Abu Arab et al. [55], Fadl et al. [56], and El-Shamy et al. [57]. Also, Rezaei et al. [58] found that the application of Oberon Speed® for control of T. urticae in greenhouses at low concentrations led to an increase in the developmental time of progeny; both the LC20 and LC30 treatments decreased adult longevity, but the preoviposition period was increased with the LC30 treatment. Furthermore, the LC20 and LC30 treatments significantly decreased life table parameters and increased generation time. Consequently, reducing T. urticae populations in agricultural settings after applying abamectin may enhance crop protection and yield. Finally, three new reduced-risk acaricides, abamectin (Vertimec 1.8% EC), chlorfenapyr (Challenger 24% SC), and fenpyroximate (Ortus 5% SC), against T. urticae varied significantly under laboratory conditions in their toxicity and their effects on the developmental stages and life table parameters of T. urticae. These results are due to different modes of action in Tables 2, 4, and 5. Additionally, there was a significant difference in the field conditions in 2020.
Conclusions
From the results obtained, it could be concluded that abamectin was the most toxic acaricide against T. urticae females, followed by fenpyroximate and chlorfenapyr, either under laboratory or field conditions. Biological characteristics of T. urticae include developmental time, net reproductive rate (Ro), intrinsic rate of natural increase (rm), finite rate of increase (λ), and sex ratio. Hence, the acaricides abamectin, fenpyroximate, and chlorfenapyr can effectively manage the two-spotted spider mite, T. urticae. The results of this study could be used as a guide for the rational use of abamectin, chlorfenapyr, and fenpyroximate in the field for better managing pest mites, which is done through the application of the rational and safe use of pesticides within the framework of integrated pest management to preserve the environment and beneficial insects.
